REALIZING LIVELIHOOD AND ENVIRONMENTAL BENEFITS OF FORAGES IN TROPICAL CROP- TREE-LIVESTOCK SYSTEMS EDITED BY : Michael Peters, Ngonidzashe Chirinda, Stefan Burkart, An Notenbaert and Rein Van Der Hoek PUBLISHED IN : Frontiers in Sustainable Food Systems Frontiers eBook Copyright Statement About Frontiers The copyright in the text of individual articles in this eBook is the Frontiers is more than just an open-access publisher of scholarly articles: it is a property of their respective authors or their respective institutions or pioneering approach to the world of academia, radically improving the way scholarly funders. The copyright in graphics research is managed. The grand vision of Frontiers is a world where all people have and images within each article may be subject to copyright of other an equal opportunity to seek, share and generate knowledge. Frontiers provides parties. In both cases this is subject immediate and permanent online open access to all its publications, but this alone to a license granted to Frontiers. is not enough to realize our grand goals. The compilation of articles constituting this eBook is the property of Frontiers. Frontiers Journal Series Each article within this eBook, and the eBook itself, are published under The Frontiers Journal Series is a multi-tier and interdisciplinary set of open-access, the most recent version of the Creative Commons CC-BY licence. online journals, promising a paradigm shift from the current review, selection and The version current at the date of dissemination processes in academic publishing. All Frontiers journals are driven publication of this eBook is CC-BY 4.0. If the CC-BY licence is by researchers for researchers; therefore, they constitute a service to the scholarly updated, the licence granted by community. At the same time, the Frontiers Journal Series operates on a revolutionary Frontiers is automatically updated to the new version. invention, the tiered publishing system, initially addressing specific communities of When exercising any right under the scholars, and gradually climbing up to broader public understanding, thus serving CC-BY licence, Frontiers must be the interests of the lay society, too. attributed as the original publisher of the article or eBook, as applicable. Dedication to Quality Authors have the responsibility of ensuring that any graphics or other Each Frontiers article is a landmark of the highest quality, thanks to genuinely materials which are the property of collaborative interactions between authors and review editors, who include some others may be included in the CC-BY licence, but this should be of the world’s best academicians. Research must be certified by peers before entering checked before relying on the a stream of knowledge that may eventually reach the public - and shape society; CC-BY licence to reproduce those materials. Any copyright notices therefore, Frontiers only applies the most rigorous and unbiased reviews. relating to those materials must be complied with. Frontiers revolutionizes research publishing by freely delivering the most outstanding Copyright and source research, evaluated with no bias from both the academic and social point of view. acknowledgement notices may not By applying the most advanced information technologies, Frontiers is catapulting be removed and must be displayed in any copy, derivative work or scholarly publishing into a new generation. partial copy which includes the elements in question. What are Frontiers Research Topics? All copyright, and all rights therein, are protected by national and Frontiers Research Topics are very popular trademarks of the Frontiers Journals international copyright laws. The above represents a summary only. Series: they are collections of at least ten articles, all centered on a particular subject. For further information please read With their unique mix of varied contributions from Original Research to Review Frontiers’ Conditions for Website Use and Copyright Statement, and Articles, Frontiers Research Topics unify the most influential researchers, the latest the applicable CC-BY licence. key findings and historical advances in a hot research area! Find out more on how ISSN 1664-8714 to host your own Frontiers Research Topic or contribute to one as an author by ISBN 978-2-83250-709-4 DOI 10.3389/978-2-83250-709-4 contacting the Frontiers Editorial Office: frontiersin.org/about/contact Frontiers in Sustainable Food Systems 1 November 2022 | Realizing Livelihood and Environmental Benefits REALIZING LIVELIHOOD AND ENVIRONMENTAL BENEFITS OF FORAGES IN TROPICAL CROP- TREE-LIVESTOCK SYSTEMS Topic Editors: Michael Peters, Alliance Bioversity International and CIAT, France Ngonidzashe Chirinda, Mohammed VI Polytechnic University, Morocco Stefan Burkart, Alliance of Bioversity International and CIAT, Colombia An Notenbaert, Alliance Bioversity International and CIAT, France Rein Van Der Hoek, Alliance Bioversity International and CIAT, France Citation: Peters, M. Chirinda, N., Burkart, S., Notenbaert, A., Van Der Hoek, R., eds. (2022). Realizing Livelihood and Environmental Benefits of Forages in Tropical Crop-Tree-Livestock Systems. Lausanne: Frontiers Media SA. doi: 10.3389/978-2-83250-709-4 Frontiers in Sustainable Food Systems 2 November 2022 | Realizing Livelihood and Environmental Benefits Table of Contents 05 Editorial: Realizing Livelihood and Environmental Benefits of Forages in Tropical Crop-Tree-Livestock Systems Ngonidzashe Chirinda, Michael Peters, Stefan Burkart, An Notenbaert and Rein Van Der Hoek 08 Nutritional Evaluation of Tropical Forage Grass Alone and Grass-Legume Diets to Reduce in vitro Methane Production Stiven Quintero-Anzueta, Isabel Cristina Molina-Botero, Juan Sebastian Ramirez-Navas, Idupulapati Rao, Ngonidzashe Chirinda, Rolando Barahona-Rosales, Jon Moorby and Jacobo Arango 21 Ex-Ante Evaluation of Economic Impacts of Adopting Improved Forages in the Colombian Orinoquía Karen Enciso, Andres Charry, Álvaro Rincón Castillo and Stefan Burkart 38 Promoting Forage Legume–Pollinator Interactions: Integrating Crop Pollination Management, Native Beekeeping and Silvopastoral Systems in Tropical Latin America Manuel Ernesto Narjes Sanchez, Juan Andrés Cardoso Arango and Stefan Burkart 48 Risk Reduction and Productivity Increase Through Integrating Arachis pintoi in Cattle Production Systems in the Colombian Orinoquía Karen Johanna Enciso Valencia, Álvaro Rincón Castillo, Daniel Alejandro Ruden and Stefan Burkart 69 Classification of Megathyrsus Maximus Accessions Grown in the Colombian Dry Tropical Forest by Nutritional Assessment During Contrasting Seasons Juliana Isabel Carvajal-Tapia, Johanna Mazabel and Nelson Jose Vivas-Quila 81 Avena sativa AV25-T (Altoandina) Supplementation as Alternative for Colombia’s High-Altitude Dairy Systems: An Economic Analysis Karen Enciso, Javier Castillo, Luis Orlando Albarracín, Luis Fernando Campuzano, Mauricio Sotelo and Stefan Burkart 95 Forage-Fed Insects as Food and Feed Source: Opportunities and Constraints of Edible Insects in the Tropics Paula Andrea Espitia Buitrago, Luis Miguel Hernández, Stefan Burkart, Neil Palmer and Juan Andrés Cardoso Arango 102 Tapping Into the Environmental Co-benefits of Improved Tropical Forages for an Agroecological Transformation of Livestock Production Systems An M. O. Notenbaert, Sabine Douxchamps, Daniel M. Villegas, Jacobo Arango, Birthe K. Paul, Stefan Burkart, Idupulapati Rao, Chris J. Kettle, Thomas Rudel, Eduardo Vázquez, Nikola Teutscherova, Ngonidzashe Chirinda, Jeroen C. J. Groot, Michael Wironen, Mirjam Pulleman, Mounir Louhaichi, Sawsan Hassan, Astrid Oberson, Sylvia S. Nyawira, Cesar S. Pinares-Patino and Michael Peters Frontiers in Sustainable Food Systems 3 November 2022 | Realizing Livelihood and Environmental Benefits 120 Geographic Distribution of Colombian Spittlebugs (Hemiptera: Cercopidae) via Ecological Niche Modeling: A Prediction for the Main Tropical Forages’ Pest in the Neotropics Luis M. Hernández, Paula Espitia, David Florian, Valheria Castiblanco, Juan Andrés Cardoso and María I. Gómez-Jiménez 137 In vitro Fermentation Profile and Methane Production of Kikuyu Grass Harvested at Different Sward Heights Alejandra Marín, Jérôme Bindelle, Ángel S. Zubieta, Guillermo Correa, Jacobo Arango, Ngonidzashe Chirinda and Paulo César de Faccio Carvalho 149 Perspectives on Reducing the National Milk Deficit and Accelerating the Transition to a Sustainable Dairy Value Chain in Zimbabwe Ngonidzashe Chirinda, Chrispen Murungweni, Addmore Waniwa, Justice Nyamangara, Aziza Tangi, Michael Peters, An Notenbaert and Stefan Burkart 158 Performance of Urochloa and Megathyrsus Forage Grasses in Smallholder Farms in Western Kenya Solomon Waweru Mwendia, Ruth Odhiambo, Alfred Juma, David Mwangi and An Notenbaert 169 On (Dis)Connections and Transformations: The Role of the Agricultural Innovation System in the Adoption of Improved Forages in Colombia Karen Enciso, Natalia Triana, Manuel Díaz and Stefan Burkart 189 Public Policies for the Development of a Sustainable Cattle Sector in Colombia, Argentina, and Costa Rica: A Comparative Analysis (2010–2020) Leonardo Moreno Lerma, Manuel Francisco Díaz Baca and Stefan Burkart 207 A Transcriptomic Analysis of Stylo [Stylosanthes guianensis (Aubl.) Sw.] Provides Novel Insights Into the Basis of Salinity Tolerance Yiming Liu, Danyu Kong, Hubiao Yang, Sabine Douxchamps, Mary Atieno, Bin Xu, Wenqiang Wang and Guodao Liu Frontiers in Sustainable Food Systems 4 November 2022 | Realizing Livelihood and Environmental Benefits TYPE Editorial PUBLISHED 21 October 2022 DOI 10.3389/fsufs.2022.1056522 Editorial: Realizing livelihood OPEN ACCESS and environmental benefits of EDITED AND REVIEWED BY Andrew Juan Challinor, forages in tropical University of Leeds, United Kingdom *CORRESPONDENCE crop-tree-livestock systems Ngonidzashe Chirinda Ngonidzashe.Chirinda@um6p.ma SPECIALTY SECTION Ngonidzashe Chirinda1*, Michael Peters2, Stefan Burkart3, This article was submitted to Climate-Smart Food Systems, An Notenbaert2 and Rein Van Der Hoek4 a section of the journal Frontiers in Sustainable Food Systems 1Mohammed VI Polytechnic University (UM6P), AgroBioSciences (AgBS), Agricultural Innovations and Technology Transfer Centre (AITTC), Ben Guerir, Morocco, 2Alliance of Bioversity International RECEIVED 28 September 2022 and International Center for Tropical Agriculture, Africa Hub, Nairobi, Kenya, 3Tropical Forages ACCEPTED 07 October 2022 Program, Alliance of Bioversity International-CIAT, Crops for Nutrition and Health, Cali, Colombia, PUBLISHED 21 October 2022 4Tropical Forages Program, Alliance of Bioversity International-CIAT, Dakar, Senegal CITATION Chirinda N, Peters M, Burkart S, Notenbaert A and Van Der Hoek R KEYWORDS (2022) Editorial: Realizing livelihood and environmental benefits of forages sustainable livestock intensification, enteric methane emissions, livestock feed in tropical crop-tree-livestock systems. resources, genetic innovations, management innovations Front. Sustain. Food Syst. 6:1056522. doi: 10.3389/fsufs.2022.1056522 COPYRIGHT © 2022 Chirinda, Peters, Burkart, Notenbaert and Van Der Hoek. This is Editorial on the Research Topic an open-access article distributed Realizing livelihood and environmental benefits of forages in tropical under the terms of the Creative Commons Attribution License (CC BY). crop-tree-livestock systems The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the Ruminant livestock, such as cattle, can convert biomass into high-quality, nutrient- original publication in this journal is dense foods (Broderick, 2018). This ability enables livestock to play a critical role in cited, in accordance with accepted academic practice. No use, distribution increasing the productive utilization not only of fertile but also of marginal lands or reproduction is permitted which unsuitable for crop production (Wang et al., 2021). In the tropics, the sustainable does not comply with these terms. intensification of livestock production systems plays a critical role in supporting rural livelihoods and meeting food security and environmental goals (Herrero et al., 2013; Rao et al., 2015). Despite its importance, less is known about the productivity and environmental impacts of tropical livestock systems compared to livestock production systems under other climatic regimes (i.e., temperate climate). This knowledge gap limits our ability to inform actions that lead to sustainable intensification in the tropics. However, it is unambiguous that the intensification of livestock systems in the tropics heavily depends on availability and access to quality feed since the limited previous studies have generally reported higher levels of animal production when feed supplements are included in livestock diets. Specifically, feed options such as cultivated forage legumes, crop residues and improved grasslands represent necessary feed resources, which can be accessible to tropical farmers with limited investments and better organization. The papers in this collection, which explored livestock production systems in Latin America, Africa and Asia, all suggest the possibility of increasing livestock productivity by adopting innovative policies, technologies, and management practices. Frontiers in Sustainable FoodSystems frontiersin.org 5 Chirinda et al. 10.3389/fsufs.2022.1056522 The presented evidence suggests that the inclusion of legumes as a disconnect between institutions and other actors along in grazed pastures has the potential to increase cattle production livestock value chains resulting in insufficient synchrony of (Valencia et al.), reduce methane emissions (Quintero-Anzueta efforts to support the adoption of critical innovations (Enciso, et al.) and increase the persistence of forage grasses (Valencia Triana et al.). While the need to sustainability intensify et al.). Including feed supplements such as Altoandina oat silage livestock production systems at the national and global levels was reported to be an economically viable option for increasing is frequently well articulated, connections between policies the productivity of Colombia’s High-Altitude Dairy Systems and investments and, thus, actions on the ground largely (Enciso, Castillo et al.). Management options that optimize remain weak (Lerma et al.). Chirinda et al. emphasize the rotational pasture grazing based on simple metrics such as need to create inclusive and creatively organized livestock value sward height may increase livestock productivity and reduce chains that improve stakeholder linkages, information flows enteric methane emissions from grazing cattle (Marín et al.). and equity. Besides the adoption of better pasture management systems, genetic innovations can be used to overcome challenges such as droughts (Carvajal-Tapia et al.), soil salinity (Liu et al.) and low Author contributions biomass accumulation (Mwendia et al.). An additional emerging use of tropical forages is their NC made the first draft of the Editorial. MP, SB, AN, potential as a food source for edible insects (Bawa et al., 2020; and RV made edits and suggestions to improve the draft Oonincx et al., 2020). Buitrago et al. share their perspectives version. All authors contributed to the article and approved the on this aspect and suggest that integrating tropical forage- submitted version. based diets in edible insect production systems represents low- cost feed sources for insects and supports transiting to circular economies. On the other hand, as Hernández et al. highlight, Acknowledgments tropical forage production systems must be protected from harmful insects such as Spittlebugs. Narjes Sanchez et al. also This work was undertaken as part of the CGIAR Research provide critical insights into the possible role of tropical forage Program (CRP) on Livestock. In addition, it was supported by legumes in pollinator conservation efforts, income generation, the OneCGIAR Initiatives on Livestock, Climate and System and closing the forage legume seed bottleneck that still limits Resilience (LCSR) and Sustainable Animal Productivity for further advances in sustainable intensification efforts of the Livelihoods, Nutrition and Gender Inclusion (SAPLING). We cattle sector as of today. thank all donors that globally support our work through their In addition to providing food, the livestock sector can contributions to the CGIAR system. generate ecosystem benefits such as increased on-farm agro- biodiversity, soil restoration, mitigation of GHG emissions and more efficient use of nutrients and water resources. Conflict of interest Narjes Sanchez et al. showed that silvopastoral systems have the potential to support the provision of ecosystem services The authors declare that the research was conducted in the such as pollination. In a separate study, Notenbaert et al. absence of any commercial or financial relationships that could used previous studies to demonstrate the multiple potential be construed as a potential conflict of interest. benefits of managed livestock production systems. They further demonstrate linkages between managed livestock production systems and agroecology and how the sustainable intensification Publisher’s note of livestock production systems can contribute to the 13 principles of agroecology. All claims expressed in this article are solely those of the From this paper collection, it appears there is clarity on authors and do not necessarily represent those of their affiliated what needs to be done to sustainably intensify tropical livestock organizations, or those of the publisher, the editors and the production systems to meet livelihood, food security and reviewers. Any product that may be evaluated in this article, or environmental goals. Nevertheless, the slow progress appears claim that may be made by its manufacturer, is not guaranteed disproportionately attributable to non-technical aspects such or endorsed by the publisher. Frontiers in Sustainable FoodSystems frontiersin.org 6 Chirinda et al. 10.3389/fsufs.2022.1056522 References Bawa, M., Songsermpong, S., Kaewtapee, C., and Chanput, W. (2020). Effect of omega 3 fatty acids. Insect Sci. 27, 500–509. doi: 10.1111/1744-7917. diet on the growth performance, feed conversion, and nutrient content of the house 12669 cricket. J. Insect Sci. 20, 1–10. doi: 10.1093/jisesa/ieaa014 Rao, I, Peters, M., Castro, A., Schultz-Kraft, R.,White, D., Fisher, M., et al. (2015). Broderick, G.A. (2018). Review: Optimizing ruminant conversion of feed protein LivestockPlus—the sustainable intensification of forage-based agricultural systems to human food protein. Animal 12, 1722–1734. doi: 10.1017/S1751731117002592 to improve livelihoods and ecosystem services in the tropics. Trop. Grasslands Herrero, M., Grace, D., Njuki, J., Johnson, N., Enahoro, D., Silvestri, S., 3, 59–82. doi: 10.17138/tgft(3)59-82 et al. (2013). The roles of livestock in developing countries. Animal 7, Wang, T., Jin, H., Kreuter, U., and Teague, R. (2021). Expanding 3–18. doi: 10.1017/S1751731112001954 grass-based agriculture on marginal land in the U.S. Great plains: the Oonincx, D. G. A. B., Laurent, S., Veenenbos, M. E., and van role of management intensive grazing. Land Use Policy 104, 105155. Loon, J. J. A. (2020). Dietary enrichment of edible insects with doi: 10.1016/j.landusepol.2020.105155 Frontiers in Sustainable FoodSystems frontiersin.org 7 ORIGINAL RESEARCH published: 14 June 2021 doi: 10.3389/fsufs.2021.663003 Nutritional Evaluation of Tropical Forage Grass Alone and Grass-Legume Diets to Reduce in vitro Methane Production Stiven Quintero-Anzueta 1,2†, Isabel Cristina Molina-Botero 2,3†, Juan Sebastian Ramirez-Navas 1,4, Idupulapati Rao 2, Ngonidzashe Chirinda 2,5, Rolando Barahona-Rosales 6, Jon Moorby 7 and Jacobo Arango 2* Edited by: 1 School of Basic Sciences, University of Santiago de Cali, Cali, Colombia, 2 International Center for Tropical Agriculture Bruno José Rodrigues Alves, (CIAT), Palmira, Colombia, 3Department of Nutrition, Faculty of Animal Science, Universidad Nacional Agraria La Molina, Brazilian Agricultural Research Lima, Peru, 4 Faculty of Natural and Exact Sciences, Universidad del Valle, Cali, Colombia, 5Mohammed VI Polytechnic Corporation (EMBRAPA), Brazil University (UM6P), AgroBioSciences (AgBS), Agricultural Innovations and Technology Transfer Centre (AITTC), Ben Guerir, Reviewed by: Morocco, 6Department of Animal Production, Faculty of Agricultural Sciences, Universidad Nacional de Colombia, Medellin, Luis Alonso Villalobos Villalobos, Colombia, 7 Institute of Biological, Environmental and Rural Sciences, Aberystwyth, United Kingdom University of Costa Rica, Costa Rica Siriwan Martens, Saxon State Office for Environment, Forage grass nutritional quality directly affects animal feed intake, productivity, and Agriculture and Geology, Germany enteric methane (CH4) emissions. This study evaluated the nutritional quality, in vitro Daniel Casagrande, Universidade Federal de Lavras, Brazil enteric CH4 emission potential, and optimization of diets based on two widely grown *Correspondence: tropical forage grasses either alone or mixed with legumes. The grasses Urochloa Jacobo Arango hybrid cv. Cayman (UHC) and U. brizantha cv. Toledo (UBT), which typically have low j.arango@cgiar.org concentrations of crude protein (CP), were incubated in vitro either alone or mixed with †These authors have contributed the legumesCanavalia brasiliensis (CB) and Leucaena diversifolia (LD), which have higher equally to this work CP concentrations. Substitution of 30% of the grass dry matter (DM) with CB or LD did not affect gas production or DM degradability. After 96 h of incubation, accumulated CH Specialty section: 4 This article was submitted to was 87.3mg CH4 g−1 DM and 107.7mg CH4 g−1 DM for the grasses alone (UHC and Climate-Smart Food Systems, UBT, respectively), and 100.7mg CH4 g −1 DM and 113.2mg CH4 g −1 DM for combined a section of the journal Frontiers in Sustainable Food Systems diets (70% grass, 15% CB, and 15% LD). Diets that combined legumes (CB or LC) Received: 02 February 2021 and grass (UHC or UBT) had higher CP contents, gross, and metabolizable energy (GE, Accepted: 10 May 2021 ME, respectively) densities, as well as lower concentrations of neutral detergent fiber Published: 14 June 2021 (NDF) and acid detergent lignin (ADL). The ME and nutritional variables such as NFD, Citation: tannins (T), and CP showed a positive correlation with in vitro net gas production, while Quintero-Anzueta S, Molina-Botero IC, Ramirez-Navas JS, Rao I, Chirinda N, ruminal digestibility was affected by CP, ADL, T, and GE. Optimal ratios of components Barahona-Rosales R, Moorby J and for ruminant diets to reduce rumen net gas production and increase protein content were Arango J (2021) Nutritional Evaluation of Tropical Forage Grass Alone and found with mixtures consisting of 60% grass (either UHC or UBT), 30% CB, and 10% Grass-Legume Diets to Reduce LD. However, this ratio did not result in a decrease in CH4 production. in vitro Methane Production. Front. Sustain. Food Syst. 5:663003. Keywords: Canavalia brasiliensis, in-vitro fermentation, Leucaena sp., nutritional quality, Urochloa brizantha cv. doi: 10.3389/fsufs.2021.663003 Toledo, Urochloa hybrid cv. Cayman Frontiers in Sustainable Food Systems | www.frontiersin.org 18 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages INTRODUCTION concentrations of protein and high digestibility. However, the relationships between CH4 emissions (in vitro) and nutritional Cattle and other ruminant livestock are a significant food source quality of the legumes Leucaena diversifolia (more information for the global human population and are good at converting is available on Leucaena leucocephala) and Canavalia brasiliensis fibrous species indigestible by humans into highly nutritious have been little studied despite their potentials when associated food (Wilkinson, 2011). This metabolic conversion is possible with tropical grasses such as Urochloa, which is an important due to rumen-dwelling microorganisms that can break down forage grass genus that is widely used in Latin America, Australia low-quality fibrous plant material, with the formation of gases and parts of Asia (Low, 2011). (methane [CH4] and CO2) that are expelled into the atmosphere, This work aimed to evaluate the effect of mixing different plus energy-rich compounds that are required to perform vital ratios of relevant tropical grasses (Urochloa sp. cv. Cayman functions for both the population of rumen organisms and and Toledo) and legumes (Canavalia brasiliensis and Leucaena the host animal (Hyland et al., 2016; Cammack et al., 2018). diversifolia) on diet nutritional quality, rumen degradability, and However, this symbiosis betweenmicroorganisms and ruminants net in vitro total gas and CH4 production. In addition, using is negatively affected by the consumption of diets that are low in optimization analysis, we aimed to find out the ideal proportions protein and high in insoluble fiber (Figueiras et al., 2010). of grass and legume(s) to not only reduce net gas production (as a Therefore, in the search for suitable diets based on tropical possible indicator of CH4) at the rumen level but also to increase forages that simultaneously meet the nutritional needs of crude protein (CP) content in the diet. livestock and decrease their impact on the environment, mixed production (i.e., agro-pastoral, silvopastoral, and agro- MATERIALS AND METHODS silvopastoral) systems are proposed as a viable option (Arango et al., 2020). In these systems, forage grasses and legumes are Location combined toward a process of sustainable intensification of Forage samples were collected in the rainy season between April livestock production, aiming at not only improving available feed and May of 2016 from a silvopastoral experiment established for ruminants but also to restore degraded lands and increase at the International Center for Tropical Agriculture (CIAT), system resilience to more frequent droughts and floods that are Palmira, Valle del Cauca, Colombia (3◦ 30′ 17′′ N and 76◦ 21′ associated with climate change (Rao et al., 2015; Ku-Vera et al., 24′′ E) at an altitude of 965 meters above sea level. Soils are 2020a). Furthermore, if properly managed, grass-legume tropical mollisols, with a pH of 7.2. During sample collection, average pastures can potentially accumulate large amounts of soil organic temperature was 25.4◦C, average relative humidity was 65%, carbon; improve chemical, physical, and biological soil health and total precipitation was 231mm (5.5mm day−1) and these characteristics; fix atmospheric nitrogen; inhibit soil nitrification; conditions allowed good regrowth of forage for 56 days. improve animal productivity and animal welfare; and reduce CH4 emissions per unit of livestock product (Peters et al., 2012; Forage Samples and Mixed Diets Rao et al., 2015; Aynekulu et al., 2020; Ku-Vera et al., 2020a; The tropical forage species evaluated were the two grasses Vazquez et al., 2020). Urochloa hybrid (CIAT BR02/1752) cv. Cayman (UHC) and Despite the multiple benefits of silvopastoral systems (SPS), Urochloa brizantha (CIAT 26110) cv. Toledo (UBT), the the use of grass-legume associations is limited in tropical herbaceous legume Canavalia brasiliensis (CIAT 17009) (CB), agricultural systems by several factors. These include reduced and the shrub legume Leucaena diversifolia (ILRI 15551) (LD). plant growth associated with interspecies competition and Forage materials were planted 2 years before the start of shading, the potentially low palatability of legumes, the the experiment (2014). The forage crops did not receive any reluctance of farmers to adopt new species due to a general lack fertilizers, pesticides or irrigation. One kilogram of each of of awareness of the benefits of these systems, and the limited UHC, UBT, and CB were collected at the vegetative stage of availability of legume seeds (Karsten and Carlassare, 2002). development before the beginning of flowering (after 6 weeks However, the specific effects of each association depend on the of regrowth), by cutting at 10 cm above soil level. Young leaf plant species involved. and stem samples (2:1 ratio) of LD were also manually collected. A widely studied species in the tropics is the shrub legume Two gas production experiments were conducted at two different Leucaena sp., which when planted in SPS provides multiple times: one with UHC, CB, and LD forages, and the other with benefits to grazing livestock, including the provision of high UBT, CB, and LD. In each experiment the individual forages quality protein throughout the year without the need for nitrogen were evaluated alone (100% UHC or 100% UBT, 100% CB, and inputs from synthetic fertilizers (Shelton and Dalzell, 2007; Cook 100% LD) and in mixtures with different proportions of DM of et al., 2020), increased forage biomass (Naranjo et al., 2012; grasses and legumes. We used the order (UHC or UBT) - CB Gaviria et al., 2015), improved voluntary forage intake (Cuartas - LD, on a DM basis, with the treatment proportions of 0-50- Cardona et al., 2015; Gaviria-Uribe et al., 2015), increased 50; 50-50-0 and 50-0-50 which correspond to a mixture in equal animal productivity (Cuartas Cardona et al., 2014), and reduced proportions (50%) between two species, either a grass with one CH4 emissions (Molina et al., 2015; Montoya-Flores et al., of the two legumes or with both legumes without UHB or UBT. 2020). Canavalia sp. is a herbaceous legume that can grow The treatment denoted 70-30-0 corresponds to the incubated in various Latin America locations by direct seeding, alone mixture of 70% grass DM plus 30% CB DM, while 70-15-15 or in combination with tropical grasses, characterized by high refers to the DM proportions 70% UHC or UBT plus 15% CB Frontiers in Sustainable Food Systems | www.frontiersin.org 29 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages and 15% LD. Finally, the treatment: 33.3-33.3-33.3, indicates a test, the contents of the bottles were filtered and dried in a forced- mixture in equal DM proportions of 33% of the forages (UHC air oven at 105◦C for 24 h to determine DM loss. Dry matter or UBT): CB: LB. A total of nine different treatments were degradability (DMD, g kg−1) was calculated for each sample as evaluated in each of the two experiments. The proportions of the change in sample DM weight following incubation, divided the forages incubated were determined in order to perform a by the starting sample DM weight, multiplied by 1,000. simplex-centroid mixture design. Accumulated gas production (AGP) curves were fitted to the Gompertz model, as proposed by Lavrenčič et al. (1997), using Nutritional Quality the CurveExpert Professional©R software, version 2.4.0 (Hyams, Samples were evaluated at the Forage Quality and Animal 2016). This model was used to evaluate the gas production points Nutrition Laboratory of CIAT. Samples were dried in a using the following equation: Memmert©R UF 750 forced air oven at 60◦C for 72 h and until constant weight was achieved. Samples were ground using a AGP(mL g−1OM) = ae−eb−ct (1) cutting mill (Retsch©R SM 100, Haan, Germany) with a 1mm sieve. The content of acid detergent fiber (ADF) and neutral Where a, b, and c are the equation parameters [a, maximum detergent fiber (NDF) was determined using an Ankom 2000 gas production; b, the difference between initial and final gas at fiber analyzer (Ankom Technology Corp., Macedon, NY, USA) time x; c, specific gas accumulation rate; and t, time (hours; h)], following the method of Van Soest et al. (1991). The ash the accumulated gas production results were expressed on an content was determined using the AOAC method (Association organic matter (OM) basis. Other biologically significant values of Official Analytical Chemists, 1990); organic matter (OM) were calculated based on parameters a, b, and c. These included content was calculated as 1,000—ash concentration in g kg−1 the time at inflection point (TIP, h), gas volume at inflection point DM. Gross energy (GE) density was determined using a Parr (GIP, mL), maximum gas production rate (MGPR, mL h−1), and 6400 (Parr Instrument Company, Illinois, USA) isoperibol lag phase (LP or microbial settlement, h). These values were calorimeter in accordance with International Standardization estimated using the following formulas: Organization, 1998: ISO 9831:1998 specifications. Acid detergent lignin (ADL) content was determined using the method of TIP = b× c−1 (2) ANKOM (2016). Total nitrogen content was determined using GIP = a× e−1 (3) an autoanalyzer (Skalar Analytical B.V. Breda, Holland) after MGPR = (axc) xe−1 (4) digestion with sulfuric acid and selenium (Krom, 1980; Searle, (( ) ( )) LP = bxc−1 − 1xc−1 1984). Crude protein (CP) content was estimated as 6.25 × (5) total nitrogen content. Total phenol and tannin contents were determined using Folin-Ciocalteu’s method (Makkar, 2003). The where “e” is Euler’s number, ca. 2.72. metabolizable energy (ME) was calculated according to Lindgren Methane Measurements (1983) from the in vitro digestibility value obtained at 96 h. Methane concentration was quantified in all gas samples In vitro Gas Production and Dry Matter collected at the Greenhouse Gas Laboratory of CIAT using a gas chromatograph (Shimadzu, Kyoto, Japan) equipped with a flame Degradation ionization detector. A three-meter long HayeSep N column was The methodology of Theodorou et al. (1994) was employed for in used and the mobile phase was high purity nitrogen at a flow rate vitro gas production. Rumen fluid was drawn and mixed from of 35mL min−1. The oven, injector, and detector temperatures two rumen-fistulated Brahman steers, grazing on a star grass were 250, 100, and 325◦C, respectively. (Cynodon plectostachyus)-dominated pasture with ad libitum access tomineralized salt. Briefly,∼1.0 g of dried/ground samples Experimental Design and Data Analysis were placed in individual Wheaton bottles and inoculated with a The nutritional quality, DMD, and CH4 production data were rumen fluid/buffer solution mixture. After inoculation, all bottles analyzed using a randomized complete block design, where were depressurized (at time 0) and placed in a water bath set each treatment had three replicates at each time the readings at 39◦C. Thereafter, pressure and volume measurements were were taken and three inoculums, the latter being the blocking taken at 3, 6, 9, 12, 24, 36, 48, 60, 72, and 96 h of incubation. factor. Mean comparisons were made using Tukey’s test when a After each reading, the bottles were gently shaken and placed significant treatment effect (P < 0.05) was identified. To check back in the water bath. Pressure measurements were taken using for the normality of data distribution, the Shapiro-Wilk test an 8,40,065 wide-range pressure gauge (Sper Scientific, Arizona, was conducted on the original residuals using PROC GLM. To USA) and a PS100 2-bar pressure transducer (Lutron Electronic determine the correlations among the above variables, type II Enterprise Co. Ltd., Taipei, Taiwan) connected to a three-way linear regressions were carried out using the bisectormodel linear valve. The first output was connected to a 1′′ 22G needle (25mm functional relationship procedure of Genstat 18th Edition (VSN × 0.7mm), the second output to the transducer, the third to International Ltd., Hemel Hempstead, UK). All analyses were a 60mL syringe, making it possible to record the gas volume conducted using SAS©R 9.4 Software (SAS Institute, 2012). removed at each time point required to reduce the bottle internal The completely randomized model was: pressure to atmospheric pressure and to save gas samples for subsequent chromatographic analysis. Upon completion of the Yij = µi+ eij (6) Frontiers in Sustainable Food Systems | www.frontiersin.org 130 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages Where:Yij: observation of the j-th repetition of the i-th treatment; and UBT, respectively). The diet combinations from both systems µi: mean value of the i-th treatment, eij: experimental error of had a very fast fermentation rate, as evidenced by the low TIP and unit ij LP values. The lowest total accumulated gas production values The linear regression model employed was: at 96 h occurred with the LD-only treatment in both systems, a value that was almost 0.6 of that from the diet comprising UHC, Yi = β0 + β1∗xi+ ei (7) LD, and CB in a ratio of 70:15:15 and UBT-only diet, respectively (Figures 1, 2). Where: Yi: observation of the i-th variable response, The highest (inverse) correlation was observed between the corresponding with the i-th value xi of the x predictive content of CP and the AGP values (R2 = 0.919; Table 5). In variable (dependent variable); β0 and β1 are the regression contrast, ME content and gas production were positively related, parameters; xi is the independent variable; and e: experimental i.e., the higher the ME content, the higher the gas production error of unit i. (R2 = 0.907). Other strong inverse relationships were observed Regression analysis of nutritional quality data (NDF, CP, ADL, between the concentration of ADL and DMD g kg−1, GE density GE, and ME) against AGP and DMD parameters was carried and DMD g kg−1, and between T and AGP, and T and DMD. out to identify an optimal mixed-diet in which the nutritional The correlation analysis results provided the basis for carrying quality could be improved (specifically CP) while at the same out the optimization objective of selecting the best forage time reducing gas production. A simplex-centroid mix design combination for increasing the CP concentration of a dietary mix was run, using the special cubic model as a response adjustment while decreasing AGP. In the case of the UHC-based treatments, model using the StatPoint Technologies Inc., 2010: Statgraphics©R the percentage variance accounted for by these two parameters software (Centurion XVI, version 16.1.18). was 87.9% for CP and 84.3% for AGP. In the UBT-based The complete simplified special cubic model was: treatments, the percentage variance accounted for CP and AGP y = x1G+ x2C + x3L+ x was 87.8 and 87.9%, respectively. Table 6 shows the restrictions 1, 2GC + x1, 3GL used for obtaining a suitable inclusion of grasses and legumes, as +x2, 3CL+ x1, 2, 3GCL (8) well as the ratio of the best mix found (optimized) and the CP Where (y) is the crude protein (CP g kg−1) response variable and AGP obtained with the specific mix. or accumulated gas production (mL g−1 OM), x1, x1,2, x1,2,3 are the regression coefficients for individual ingredients and Methane Production mix interactions; G, C, and L are the relative ratios of forage When incubated alone, CH4 production from CB started components (grass, CB, and LD). declining rapidly after 60 h in measurements of both grasses (Tables 7, 8 for UHC and UBT, respectively). The same CH4 RESULTS accumulation trend was observed with the other diets for 96 h. It is worth noting that the largest production of CH4 in the Nutritional Quality UHC diets came from the 70% UHC: 15% CB: 15% LD diet. The The CP content of LD was 3.5 times greater than that of both incorporation of legumes into the UBT system contributed to grasses (Tables 1, 2 for UHC and UBT, respectively) and it was decreased CH4 production compared to the 100% of UBT diet. also greater than that of CB (P≤ 0.05). The NDF contents ranged from 492 (CB) to 700 g kg−1 DM (100% UBT) (P < 0.0001) DISCUSSION while the concentrations of ADF were less variable, ranging between 344 and 399 g kg−1 DM. For the treatments where Feeds intended for livestock are typically evaluated individually different proportions of legumes and grasses were mixed, in both to determine their nutritional values and not integrated with experiments it was observed that the CP content decreased as the a diet (Tang et al., 2008). Evaluations of individual forages proportion of grasses increased, however, the opposite occurred does not allow us to determine interactions with other dietary with the NDF content. The lignin content of CB was similar to components in the digestion process (Moss et al., 1992). that of UBT, whereas the lignin content of LD was similar to that Although the values of some nutritional parameters of diet of UHC. Legumes, especially LD, have higher GE contents than components are additive (e.g., CP concentrations), there are that reported for 100% grasses treatments or when grasses are possible interactions and synergies between different feeds in replaced up to 30% by legumes (P = 0.001), however, this trend a diet and their nutritional values (e.g., energy yield and CP is reversed when ME is calculated, since LD treatments or the concentrations) that could not be evaluated independently (Tang combination of legumes in equal proportions (50% LD + 50% et al., 2008). This situation can be explained at the rumen CB) obtain the lowest values of ME. Much higher concentrations level, because depending on the type of diet, some synergy or of phenols and tannins were measured in LD compared to both antagonism may develop due to co-existence of nutrients and grasses and CB, and the concentrations of both of secondary their interactions with different microorganisms (i.e., bacteria, metabolites were also higher in CB than in both grasses. protozoa, fungi, and methanogenic archaea) in the rumen (Cammack et al., 2018). Gas Production and Dry Matter In this investigation, great variability in nutritional Degradation composition was found among the different forage diets. The total volume of gas produced during the fermentation For example, the legumes contained twice as much CP as the process ranged from 150 to 255mL g−1 OM (Tables 3, 4 for UHC two grasses evaluated, and the grasses had higher concentrations Frontiers in Sustainable Food Systems | www.frontiersin.org 141 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages TABLE 1 | Mean chemical composition of Urochloa hybrid grass cv. Cayman (UHC) and the two forage legumes, C. brasiliensis (CB) and L. diversifolia (LD), and their mixed proportions used in the study. Mix UHC-CB-LD DM Ash NDF ADF ADL CP GE, MJ kg–1 DM ME, MJ kg–1 DO TP T 100-0-0 199de 122a 642a 365 157ab 68i 17.29c 8.09ab 24.6 1.07 0-100-0 189e 117a 492e 346 98c 195c 17.90bc 7.10d 46.2 15.24 0-0-100 292a 51e 530d 344 176a 256a 19.82a 5.94e 101.1 47.47 0-50-50 240bc 84d 529d 330 132bc 214b 19.32a 6.95d – – 50-50-0 194de 117a 565c 368 99c 125f 17.66c 8.02ab – – 50-0-50 245b 85d 598b 320 166a 154e 18.49b 7.48cd – – 1/3-1/3-1/3 224bcd 96c 566c 317 108c 164d 18.55b 7.66cb – – 70-30-0 192de 119a 608b 354 96c 101h 17.76c 8.22a – – 70-15-15 206cde 109b 603b 320 91c 110g 17.75c 8.25a – – p-value 0.001 0.001 0.001 0.062 0.001 0.0001 0.001 0.001 – – EMS 23.435 1.85 4.68 20.58 15.01 33.8 5.789 0.18 – – Data presented as g kg−1 DM unless otherwise indicated. a,b,c,d,e,f ,g,h,iMean values in a column with a different letter are statistically different (P < 0.05). UHC, Cayman grass; CB, Canavalia brasiliensis; LD, Leucaena diversifolia; DM, dry matter; NDF, neutral detergent fiber; ADF, acid detergent fiber; ADL, acid detergent lignin; CP, crude protein; GE, gross energy; ME, metabolizable energy; TP, total phenols; T, tannins; EMS, error mean square. TABLE 2 | Mean chemical composition of Urochloa brizantha cv. Toledo (UBT) and the two forage legumes, C. brasiliensis (CB) and L. diversifolia (LD), and their mixed proportions used in the study. Mix UBT-CB-LD DM Ash NDF ADF ADL CP GE, MJ kg–1 DM ME, MJ kg–1 DO TP T 100-0-0 248.5a 97.2d 700a 399a 83cde 77i 17.69e 8.57a 21.2 0.68 0-100-0 188.7f 117.0a 492f 346ab 98cde 195c 17.78de 7.42c 46.2 15.24 0-0-100 292.0bc 51.4i 530e 344ab 176a 256a 20.06a 6.17e 101.1 47.47 0-50-50 240.3cd 84.4g 529e 330b 132b 214b 19.32bc 6.85d – – 50-50-0 218.6de 107.5b 595d 363ab 91cde 129f 17.76de 8.30ab – – 50-0-50 270.2ab 73.5h 623c 335b 113bc 158e 18.80c 7.58c – – 1/3-1/3-1/3 240.6cd 87.4f 583d 338b 105bcd 167d 18.26cd 7.86bc – – 70-30-0 206.6ef 102.2c 655b 383ab 79de 107h 17.74de 8.53a – – 70-15-15 213.2ef 92.5e 654b 368ab 67e 116g 18.13de 8.19ab – – p-value 0.001 0.001 0.001 0.0045 0.001 0.001 0.001 0.001 – – EMS 6.77 4.3 4.79 19.49 11.01 10.76 3.588 0.16 – – Values in g kg−1 DM unless otherwise indicated. a,b,c,d,e,f ,g,h,iMean values in a column with a different letter are statistically different (P < 0.05). UBT, Toledo grass; CB, Canavalia brasiliensis; LD, Leucaena diversifolia; DM, dry matter; NDF, neutral detergent fiber; ADF, acid detergent fiber; ADL, acid detergent lignin; CP, crude protein; GE, gross energy; ME, metabolizable energy; TP, total phenols; T, tannins; EMS, error mean square. of NDF than the legumes. Similarly, concentrations of phenolic et al., 2020) and the time of the year (Demarchi et al., 2016; compounds were lower in the grasses than the legumes. These Abdalla et al., 2019). The ADL content of Urochloa grasses findings concur with data reported in the literature for these was 86 and 157 g/kg DM, both values were between the ranges tropical species (Lee, 2018; Cook et al., 2020; Gaviria-Uribe reported by Wassie et al. (2018), according to these authors et al., 2020), where CP values for grasses can range between 40 ADL content can vary between 91.2 and 186.9 g/kg depending and 140 g kg−1 DM, and for both legumes studied here, shrub on ecotype, regrowth age (60, 90 and 120 d) and altitude of the and herbaceous, ranged between 190 and 250 g CP kg−1 DM. sowing site (1,230, 1,774, and 2,650 masl). It is noteworthy that However, the CP content obtained in the present study was little information is available on the ADL content of Urochloa slightly lower than that reported by Peters et al. (2002) for U. hybrid cv. Cayman. The ME values found for the legume L. brizantha cv. Toledo who stated that under optimal conditions diversifolia are slightly lower (8.6 MJ ME kg−1 DM) than the CP content ranges between 90 and 120 g kg−1 DM. Likewise, the results reported by Geleti et al. (2013), while the ME for grasses NDF content was within the range of 600 and 800 g kg−1 DM are above those obtained by Nguku (2015) for 9 grasses of the reported for U. brizantha sp. (Cook et al., 2020; Gaviria-Uribe genus Urochloa, whose values ranged between 6.6 and 5.9 MJ et al., 2020). However, forage quality has been shown to be closely ME kg−1 DM. However, this variable, as well as the rest of the related to pasture age (Vendramini et al., 2014; Gaviria-Uribe nutritional components of the diet, can vary according to the Frontiers in Sustainable Food Systems | www.frontiersin.org 152 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages TABLE 3 | Accumulated gas production (AGP; mL g−1 OM), dry matter degradability (DMD), and profiles of the adjustment made using the Gompertz model for UHC, CB, LD, and their mixes. Mix UHC-CB-LD AGP (mL g–1 OM) DMD (g kg–1) Gompertz model a b c TIP (h) GIP (mL) MGPR (mL h–1) LP (h) 100-0-0 231.5a 712a 215.05a 1.11a 0.06c 17.09a 79.09a 5.12cd 1.63a 0-100-0 180.3cd 638bc 168.63bcd 0.98ab 0.11a 8.66f 62.02bcd 7.05a −0.15b 0-0-100 150.0de 517d 146.91d 0.88b 0.06c 14.95abc 54.04d 3.18e −2.06h 0-50-50 167.5d 608c 159.35cd 0.88b 0.08bc 11.07e 58.61cd 4.64cd −1.56g 50-50-0 210.0ab 703a 200.73ab 0.96ab 0.09b 11.19ab 73.83ab 6.31ab −0.52c 50-0-50 199.6bc 641bc 196.84ab 0.95ab 0.06c 16.38e 72.40ab 4.21de −0.83e 33.3-33.3-33.3 193.4bc 662b 185.91abc 0.90b 0.07bc 12.32de 68.38abc 5.00cd −1.36f 70-30-0 213.5ab 718a 205.75a 0.95ab 0.07bc 12.87cde 75.68a 5.59bc −0.65cd 70-15-15 234.8a 713a 218.88a 0.95ab 0.07bc 14.02bcd 80.51a 5.45bc −0.75de p-value 0.001 0.001 0.001 0.015 0.001 0.001 0.001 0.001 0.001 EMS 8.824 12.01 12.575 0.066 0.007 0.839 4.626 0.402 0.600 a,b,c,d,e,f ,gMean values in a column with a different letter are statistically different (P < 0.05). UHC, Cayman grass; CB, Canavalia brasiliensis; LD, Leucaena diversifolia; AGP, accumulated gas production; OM, organic matter; DMD, dry matter degradability; a, maximum gas production (mL); b, difference between initial gas and final gas at an × time; c, specific gas accumulation rate; TIP, time to the inflection point, h; GIP, gas at the inflection point, mL; MRGP, maximum rate of gas production, mL/h; LP, lag phase, h; EMS, error mean square. TABLE 4 | Accumulated gas production (AGP; mL g−1 OM), dry matter degradability (DMD), and profiles of the adjustment made using the Gompertz model for UBT, CB, LD, and their mixes. Mix UBT-CB-LD AGP (mL g–1 OM) DMD (g Kg–1) Gompertz model a b c TIP (h) GIP (mL) MGPR (mL h–1) LP (h) 100-0-0 252.9a 726ab 249.84a 1.13a 0.05cd 20.93a 91.89a 4.96ab 2.41a 0-100-0 182.0de 661d 171.64cd 0.98ab 0.09a 10.38e 63.13cd 5.96a −0.20c 0-0-100 155.6f 532f 153.65d 0.92b 0.05cd 16.87bc 56.51d 3.09d −1.39g 0-50-50 175.7def 598e 167.20cd 0.94ab 0.07ab 12.34de 61.5bc 4.68bc −0.79d 50-50-0 225.7bc 715ab 214.91ab 0.92b 0.07bc 13.17de 79.04ab 5.56ab −1.04ef 50-0-50 202.4e 640d 200.69bc 0.99ab 0.05d 18.71ab 73.81cd 3.91cd −0.17bc 33.3-33.3-33.3 207.1cde 669cd 199.47bc 0.92b 0.06bcd 14.59cd 73.36bc 4.67bc −1.11f 70-30-0 230.6ab 727a 230.76ab 0.94ab 0.06bcd 15.16cd 84.87ab 5.28ab −0.90de 70-15-15 233.7ab 695bc 228.05ab 1.00ab 0.05bcd 17.07bc 83.88ab 4.92bc 0.03b P 0.001 0.001 0.001 0.028 0.001 0.001 0.001 0.001 0.001 EMS 7.119 1.098 14.784 0.066 0.006 1.045 5.437 0.355 0.076 a,b,c,d,e,f ,gMean values in a column with a different letter are statistically different (P < 0.05). UBT, Toledo grass; CB, Canavalia brasiliensis; LD, Leucaena diversifolia; AGP, accumulated gas production; OM, organic matter; DMD, dry matter degradability; a, maximum gas production (mL); b, difference between initial gas and final gas at an × time; c, specific gas accumulation rate; TIP, time to the inflection point, h; GIP, gas at the inflection point, mL; MRGP, maximum rate of gas production, mL/h; LP, lag phase, h; EMS, error mean square. age of the species and time of year (Givens et al., 1993, Nguku, to these grasses. Despite this, there was a clear pattern and as 2015). In the present investigation, there were differences in the level of inclusion of legumes increased, gas production and ME content between legumes and grasses, contrary to what was degradability decreased. Blümmel et al. (1997) suggested that a reported by Evitayani et al. (2004), who found average values feed consisting of a mix of different kinds of ingredients can of 7.6 ± 0.14 and 7.3 ± 0.12 MJ ME kg−1 DM for grasses and result in asynchrony in releasing nutrients, thus changing both legumes, respectively. Likewise, the highest ME concentrations the biomass of microorganisms produced and gas produced by were for the treatments: 100-0-0, 70-30-0 or 70-15-15, this may them. In addition, one factor that can affect the fermentation favor the synthesis of microbial proteins at the rumen level and gas production of feeds is the configuration of their cell wall (Krizsan et al., 2020). polysaccharides (Molina-Botero et al., 2020, Valencia-Salazar For the in vitro analysis, the highest gas production and et al., 2021). Therefore, the digestibility values depend upon degradability rates were obtained for samples of both grasses that their composition of structural carbohydrates, including the were individually incubated and when 30% legumes were added concentration of lignin (Barahona and Sánchez, 2005) and Frontiers in Sustainable Food Systems | www.frontiersin.org 163 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages FIGURE 1 | Modeled mean accumulated gas production (mL g−1 OM) for UHC, CB, LD, and 6 dietary mixtures. UHC, Cayman 100%; CB, Canavalia 100%; LD, Leucaena 100%; CB50LD50, Canavalia 50% + Leucaena 50%; UHC50CB50, Cayman 50% + Canavalia 50%; UHC50LD50, Cayman 50% + Leucaena 50%; UHC33.3CB33.3LD33.3, Cayman 33.3% + Canavalia 33.3% + Leucaena 33.3%; UHC70CB30, Cayman 70% + Canavalia 30%; UHC70CB15LD15, Cayman 70% + Canavalia 15% + Leucaena 15%. the protein included in the diet or treatment evaluated. This and their effect depends on their concentration or ratio with postulate agrees with the high correlation values obtained in this the substrate with which they interact. High concentrations of study between nutritional compounds such as CP or ADL and tannins, such as the ones found in diets containing legumes variables such as DMD or AGP. Similar results were reported (CB and LD) can delay the digestion of forages by reducing the by Lee (2018) where 136 forage plant species or hybrid cultivars activity of fibrolytic enzymes (Archimède et al., 2016; Henke grown in 30 countries were evaluated, finding that parameters et al., 2017; Ku-Vera et al., 2020b). This phenomenon is related such as ADF, NDF, ADL content had a correlation >0.7 with to the microbial degradation of structural polysaccharides, and DMD or OMD. Although Lee (2018) affirmed that there is a the rate and extent of forage degradation (Archimède et al., 2016; positive correlation (0.62, respectively) between CP and DMD, Henke et al., 2017). Likewise, a negative effect has been shown on in the current study there was an inverse correlation between protein degradation when tannins encapsulate it at low rumen both parameters, perhaps due to the concomitant increase of pH (Hess et al., 2003; Archimède et al., 2016). The described the content of anti-nutritional compounds associated with the tannin effect could explain our results obtained in this study, as inclusion of CB and/or LD, which could potentially mask the full in the treatments with an inclusion between 50 and/or 100% of expression of a diet rich in CP and GE, as was also reported by some of these two containing-tannin- legumes (15.2 and 47.5 g Jayanegara et al. (2011). kg−1 DM for Canavalia and Leucaena, respectively) and total It is clear that to increase our understanding of the nutritive phenols (46.2 and 101.1 g kg−1 DM) a reduction in digestibility value of forage mixtures composed of tropical forages, the action variables and therefore in gas production was observed. These of the various secondary metabolites (i.e., tannins, saponins) that results are in contrast to the 100% grass treatments where the are present in some legumes must be taken into consideration values of tannins and total phenols did not exceed 1.07 g T kg−1 (Tiemann et al., 2008a,b; Lascano and Cárdenas, 2010). The DM and 24.2 g TP kg−1 DM. This observation is consistent effect of secondary metabolites depends on their concentration with the study of Seresinhe et al. (2012), where a strong inverse or proportion to the substrate with which they interact. For relationship was found between tannin concentration and gas example, tannins can be found both in the cell wall and inside production. Tolera et al. (1998) reported condensed tannins the cytoplasmic vacuoles of some legumes, primarily in the form content ranging from 7.1 to 13.5% in LD. This concentration of of condensed tannins (McAllister et al., 1994; Patra et al., 2017) tannins could have bacteriostatic effects on some populations, Frontiers in Sustainable Food Systems | www.frontiersin.org 174 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages FIGURE 2 | Accumulated gas production (AGP; mL g−1 OM) for UBT, CB, LD, mixed diets. UBT, Toledo 100%; CB, Canavalia 100%; LD, Leucaena 100%; CB50LD50, Canavalia 50% + Leucaena 50%; UBT50CB50, Toledo 50% + Canavalia 50%; UBT50LD50, Toledo 50% + Leucaena 50%; UBT33.3CB33.3LD33.3, Toledo 33.3% + Canavalia 33.3% + Leucaena 33.3%; UBT70CB30, Toledo 70% + Canavalia 30%; UBT70CB15LD15, Toledo 70% + Canavalia 15% + Leucaena 15%. TABLE 5 | Correlations obtained by type II linear regression analysis. Correlation Equation R2 SE slope SE constant NDF g kg−1 (x) on AGP mL g−1 OM (y) y = 0.46x – 63.8 0.743 0.064 37.55 NDF g kg−1 (x) on DMD g kg−1 (y) y = 1.12x + 7.47 0.434 0.247 148.7 CP g kg−1 (x) on AGP mL g−1 OM (y) y = −0.51x + 281.6 0.919 0.037 6.145 CP g kg−1 (x) on DMD g kg−1 (y) y = −1.12x + 834.9 0.876 0.102 16.86 ADL g kg−1 (x) on AGP mL g−1 OM (y) y = −0.70x + 280.0 0.622 0.142 16.55 ADL g kg−1 (x) on DMD g kg−1 (y) y = −1.70x + 847.3 0.769 0.240 28.07 GE MJ kg−1 (x) on AGP mL g−1 OM (y) y = −44.9x + 1,025 0.654 16.56 303.7 GE MJ kg−1 (x) on DMD g kg−1 (y) y = −83.9x + 2,198 0.864 26.93 494.1 ME MJ kg−1 (x) on AGP mL g−1 OM (y) y = −36.8x + 77.7 0.907 2.936 22.94 T g kg−1 (x) on AGP mL g−1 OM (y) y = −2.20x + 243.2 0.791 0.279 6.185 T g kg−1 (x) on DMD g kg−1 (y) y = −4.56x + 742.5 0.948 0.266 6.019 NDF, neutral detergent fiber; CP, crude protein; ADL, acid detergent lignin; GE, gross energy; ME, metabolizable energy; T, tannins; AGP, accumulated gas production; OM, organic matter; DMD, dry matter degradation; R2, determination coefficient; SE, standard error. leading to lower digestibility of the fermented material and emission, it was never intended to be zero. This expectation (Tavendale et al., 2005). is because gas production is of great importance to maintain Evaluation of the AGP and CP content in a mix of the three ideal conditions inside the rumen. For example, in the case dietary components (grass, CB, and LD) yielded an optimal of cattle it is important that the formation and utilization of diet ratio of 60% grass (UHC or UBT), 30% CB, and 10% metabolic hydrogen is synchronized (Calsamiglia et al., 2005) in LD. It should be clarified that although a reduction in gas the metabolic pathway that is responsible for glucose oxidation production was pursued as a measure to reduce CH4 production (glycolysis). This is required to regenerate the reducing power Frontiers in Sustainable Food Systems | www.frontiersin.org 185 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages TABLE 6 | Optimization of the crude protein (CP; maximize) and accumulated gas production (AGP; minimize) response variables in the UHC and UBT forage systems. Systems Factor Restrictions Calculated Optimal value Optimized CP Optimized AGP optimal value (desirability) (g kg–1 DM) (mL g–1 OM) Minimum Maximum UHC UHC (%) 60 100 60.0 0.398 147 200 CB (%) 0 40 30.0 LD (%) 10 40 10.0 UBT UBT (%) 60 100 60.0 0.420 151 215 CB (%) 0 40 30.0 LD (%) 10 40 10.0 UHC, Cayman 100%; UBT, Toledo 100%; CB, Canavalia 100%; LD, Leucaena 100%; AGP, accumulated gas production; CP, crude protein; DM, dry matter; OM, organic matter. TABLE 7 | Methane yield from UHC, CB, LD, and their mixed diets. Treatment Methane yield (g CH4 kg–1 DM) at different post-incubation times g CH4 kg–1 DMD 3 h 6 h 9 h 12 h 24 h 36 h 48 h 60 h 72 h 96 h 96 h UHC 0.07c 0.98b 1.99c 3.05c 8.98a 11.11ab 13.19a 14.27a 15.55a 18.08a 24.36ab CB 0.50a 1.99a 4.43a 6.85a 10.42a 13.72a 14.99a 16.34a 11.72b 11.44b 18.52b LD 0.25b 0.93b 1.77c 2.87c 7.68a 8.90b 9.72b 10.77b 11.16b 12.68b 23.28ab UHC70CB30 0.49a 1.55a 3.01b 4.65b 10.31a 12.58a 14.68a 15.19a 15.76a 17.84a 23.62ab UHC70CB15LD15 0.56a 1.66a 3.02b 4.68b 10.68a 12.65a 14.81a 15.97a 17.00a 19.66a 26.29a p-vale 0.001 0.001 0.001 0.001 0.001 0.0072 0.0013 0.001 0.001 0.001 0.012 EMS 0.054 0.163 0.356 0.546 1.431 1.255 1.184 1.260 0.979 1.232 1.817 a,b,cMean values in a column with a different letter are statistically different (P < 0.05). DM, dry matter; CH4, methane; DMD, dry matter degradation; UHC, Cayman 100%; CB, Canavalia 100%; LD, Leucaena 100%; UHC70CB30: Cayman 70% + Canavalia 30%; UHC70CB15LD15: Cayman 70% + Canavalia 15% + Leucaena 15%. TABLE 8 | Methane yield from UBT, CB, LD, and their mixes. Treatment Methane yield (g CH4 kg–1 DM) at different post-incubation times g CH4 kg–1 DMD 3 h 6 h 9 h 12 h 24 h 36 h 48 h 60 h 72 h 96 h 96 h UBT 0.07b 0.46c 1.41d 3.27b 10.71a 14.64a 16.65ab 18.18ab 19.84ab 22.44a 31.57a CB 0.14ab 0.85a 2.90bc 6.18a 11.85a 13.87a 16.03b 17.13b 16.26b 11.29c 17.69c LD 0.08ab 0.55bc 1.87cd 3.30b 7.07b 8.93b 10.55c 11.42c 11.32c 12.71b 25.22b UBT70CB30 0.14a 0.83a 4.00a 5.69a 13.28a 15.71a 18.16a 19.70a 20.81a 21.85a 30.83a UBT70CB15LD15 0.12ab 0.74ab 3.17ab 5.25a 12.43a 15.04a 17.24ab 18.54ab 19.24ab 21.42a 31.69a p-vale 0.016 0.0015 0.001 0.001 0.0008 0.001 0.001 0.001 0.001 0.001 0.001 EMS 0.027 0.092 0.405 0.709 1.207 0.741 0.703 0.847 1.350 0.953 1.714 a,b,c,dMean values in a column with a different letter are statistically different (P < 0.05). DM, dry matter; CH4, methane; DMD, dry matter degradation; UBT, Toledo 100%; CB, Canavalia 100%; LD, Leucaena 100%; UBT70CB30, Toledo 70% + Canavalia 30%; UBT70CB15LC15, Toledo 70% + Canavalia 15% + Leucaena 15%. of cofactors such as NAD+ and FAD+, while increasing the mixtures of grasses and legumes to improve the quality of the synthesis the synthesis of adenosine triphosphate, promoting diet and have an optimal protein:energy balance at the rumen the growth of other microbial species (e.g., fibrolytic) and helps level. Moreover, these proportions coincide with those found to regulate the osmotic pressure inside the rumen (Yokoyama in experiments with ruminants fed with tropical legumes that and Johnson, 1993; Calsamiglia et al., 2005). Regarding the are rich in tannins and whose results affirm that DM intake proportions established in the evaluated diets, this is consistent was reduced when the amount of CT exceeds 50 g kg−1 DM with the observations of Rojas et al. (2005), who suggested that (Patra and Saxena, 2011). Likewise, cattle systems where the diet the percentage of legumes should range from 30 to 40% in is composed of 100% low quality grasses, have low productive Frontiers in Sustainable Food Systems | www.frontiersin.org 196 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages indexes due to the low CP concentration, required by ruminal CONCLUSIONS microorganisms for the breakdown of carbohydrates, in addition to a reduction in DM intake due to the high content of structural Diets that combined legumes (CB or LC) with grass (UHC or carbohydrates (Krizsan et al., 2010). UBT) had higher protein contents and gross and metabolizable Enteric CH4 emission rates are associated with the energy densities, as well as decreased concentrations of NDF and physicochemical characteristics of the diet (e.g., CP and lignin. Metabolizable energy and nutritional compounds such as NDF contents), which have a direct impact on diet intake NDF, T, and CP had a high correlation with net gas production, (Gaviria-Uribe et al., 2020) and eating frequency (Grant et al., while ruminal digestibility was affected by CP, ADL, GE, T, and 2015). Several studies have evaluated the effect of adding a other unidentified compounds provided by CB and/or LD. legume to a grass on CH4 production both in vitro (Tope et al., Optimal ratios of dietary components in both systems were 2013; Molina-Botero et al., 2020) and in vivo (Molina-Botero found with mixtures consisting of 60% grass (either UHC or et al., 2019a,b; Gaviria-Uribe et al., 2020; Montoya-Flores et al., UBT), 30%CB, and 10% LD. The system containing UHC yielded 2020). Nevertheless, the conclusions drawn from these studies the best combination in terms of an increase in CP and a decrease are unclear, as in some cases the addition of a legume increased in AGP. However, this ratio did not result in a decrease in in vitro CH4 production (Carulla et al., 2005; Molina-Botero methane production. Therefore, further characterization of the et al., 2020), but in others, it had the opposite effect (Lee et al., content and activity of other secondary metabolites, perhaps 2004). In our case, net CH4 production per kg of DM did present in both legumes, is required to better explain the behavior not differ between treatments containing legumes (up to 30% response resulting from grass-legume interactions. inclusion) and grasses alone, but less gas was produced when 100% legumes were incubated. A similar trend was observed DATA AVAILABILITY STATEMENT for CH4 production per unit DMD, being most noticeable for the treatment of 100% CB. When comparing both legumes, we The raw data supporting the conclusions of this article will be observed that CB was characterized by containing less NDF made available by the authors, without undue reservation. and ADL than LD, contributing to improved digestibility and therefore higher gas production. This finding coincides with the ETHICS STATEMENT conclusion reached by Hess et al. (2003), who stated that the difference in in vitro CH4 production among various kinds of The animal study was reviewed and approved by Colombian forages could be accounted for by the differences between the law No. 84/1989 and the Ethics Committee of the International ratios of digestible carbohydrates and cellulose. Likewise, Patra Center for Tropical Agriculture. and Saxena (2010) proposed that the presence of secondary metabolites can affect methanogenesis. However, this was not AUTHOR CONTRIBUTIONS observed in the present study, because the inclusion of up to 30% of legumes did not reduce in vitro CH4 production. In SQ-A, IM-B, JR-N, and RB-R: conceptualization. SQ-A and addition, a greater reduction would be expected with the LD IM-B: methodology. SQ-A, IM-B, and JM: formal analysis. SQ-A: treatment alone, since it contained a greater amount of total writing—original draft preparation. SQ-A, IM-B, IR, RB-R, phenols and tannins compared to CB alone. These results can NC, JA, and JM: writing—review and editing. RB-R and JA: be explained by indirect effects of other secondary compounds supervision. JA: project administration. NC, JM, and JA: funding present in these species, such as mimosine, alkaloids, saponins, acquisition. All authors contributed to the article and approved steroids, among others that were not evaluated (Hu et al., the submitted version. 2005; Oseni et al., 2011). With our results, it should not be ignored that the in vitro technique, despite being an artificial FUNDING system, is a viable option to initially simulate possible dietary combinations of forages (Danielsson et al., 2017) that can then This work was implemented as part of the CGIAR Research be validated using ruminants. This is why we highlight the Program (CRP) on Climate Change, Agriculture and Food importance of including legumes in cattle diets as a strategy to Security (CCAFS), and the Livestock CRP which are carried reduce CH4 emissions. out with support from CGIAR Fund Donors and through Although it was not the primary aim of this study, the use bilateral funding agreements. For details, please visit https://ccafs. of herbaceous and shrub legumes was shown to have potential cgiar.org/donors. We also acknowledge the financial assistance positive environmental benefits besides improving nutritive of BBSRC grants: UK—CIAT Joint Centre on Forage Grasses values of diets for ruminants. Vazquez et al. (2020) showed how for Africa (BBS/OS/NW/000009); RCUK-CIAT Newton Fund— combining the three types of forages tested here clearly improved Toward climate-smart forage-based diets for Colombian livestock chemical, physical and biological soil health characteristics. In (BB/R021856/1); Advancing sustainable forage-based livestock addition, the use of shrubs and trees in silvopastoral systems have production systems in Colombia (CoForLife) (BB/S01893X/1) and shown the capacity to sequester greater amounts of carbon at a GROW Colombia from the UK Research and Innovation (UKRI) system level (Aynekulu et al., 2020). Global Challenges Research Fund (GCRF) (BB/P028098/1). Frontiers in Sustainable Food Systems | www.frontiersin.org 170 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages REFERENCES Gaviria, X., Rivera, J. E., and Barahona, R. (2015). Calidad nutricional y fraccionamiento de carbohidratos y proteína en los componentes forrajeros de Abdalla, A., Abdalla Filho, A., Natel, A., Louvandini, H., Piccolo, M., Nechet, un sistema silvopastoril intensivo. Pastos y Forrajes 38, 194–201. K. L., et al. (2019). Nutritive value and enteric methane production of Gaviria-Uribe, X., Bolivar, D., Rosenstock, T., Molina-Botero, I. C., Chirinda, Brachiaria spp. under elevated [CO2]. Int. J. Plant Product. 14, 119–126. N., Barahona, R., et al. (2020). Nutritional quality, voluntary intake and doi: 10.1007/s42106-019-00072-6 enteric methane emissions of diets based on novel Cayman grass and its ANKOM (2016). Acid Detergent Lignin Method (in Beakers). Retrieved associations with two Leucaena shrub legumes. Vet. Sci. Front. 7:579189. from: https://www.ankom.com/sites/default/files/document-files/Method_8_ doi: 10.3389/fvets.2020.579189 Lignin_in_beakers.pdf (accessed January 15, 2021). Gaviria-Uribe, X., Naranjo-Ramírez, J. F., Bolívar-Vergara, D. M., and Arango, J., Ruden, A., Martinez-Baron, D., Loboguerrero, A. M., Berndt, A., Barahona-Rosales, R. (2015). Consumo y digestibilidad en novillos Chacón, M., et al. (2020). Ambition meets reality: achieving GHG emission cebuínos en un sistema silvopastoril intensivo. Arch. De Zootec. 64, 21–27. reduction targets in the livestock sector of Latin America. Front. Sustain. Food doi: 10.21071/az.v64i245.370 Syst. 4:65. doi: 10.3389/fsufs.2020.00065 Geleti, D., Hailemariam, M., Mengistu, A., and Tolera, A. (2013). Nutritive Archimède, H., Rira, M., Barde, D. J., Labirin, F., Marie-Magdeleine, C., Calif, B., value of selected browse and herbaceous forage legumes adapted to medium et al. (2016). Potential of tannin-rich plants, Leucaena leucocephala, Glyricidia altitude subhumid areas of western Oromia, Ethiopia. Glob. Vet. 11, 809–816. sepium and Manihot esculenta, to reduce enteric methane emissions in sheep. doi: 10.5829/idosi.gv.2013.11.6.8216 J. Anim. Physiol. Anim. Nutr. 100, 1149–1158. doi: 10.1111/jpn.12423 Givens, D. I., Moss, A. R., and Adamson, A. H. (1993). Influence of Association of Official Analytical Chemists (1990). Ash of Animal Feed. 942.05 growth stage and season on the energy value of fresh herbage. 1. Official Methods of Analysis, 15th Edn. Rockville, MD: A.O.A.C. Changes in metabolizable energy content. Grass For. Sci. 48, 166–174. Aynekulu, E., Suber, M., van Noordwijk, M., Arango, J.;, Roshetko, J. M., and doi: 10.1111/j.1365-2494.1993.tb01849.x Rosenstock, T. S. (2020). Carbon storage potential of silvopastoral systems of Grant, R. J., Dann, H. M., and Woolpert, M. E. (2015). Time required for Colombia. Land 9:309. doi: 10.3390/land9090309 adaptation of behavior, feed intake, and dietary digestibility in cattle. J. Dairy Barahona, R., and Sánchez, M. (2005). Limitaciones físicas y químicas de la Sci. 98(Suppl. 2):312. digestibilidad de pastos tropicales y estrategias para aumentarla. Ciencia y Henke, A., Dickhoefer, U., Westreicher-Kristen, E., Knappstein, K., Molkentin, Tecnología Agropecuaria 6, 69–62. doi: 10.21930/rcta.vol6_num1_art:39 J., Hasler, M., et al. (2017). Effect of dietary Quebracho tannin extract Blümmel, M., Makkar, H. P. S., and Becker, K. (1997). In vitro gas on feed intake, digestibility, excretion of urinary purine derivatives production: a technique revisited. J. Anim. Physiol. Anim. Nutr. 77, 24–34. and milk production in dairy cows. Arch. Anim. Nutr. 71, 37–53. doi: 10.1111/j.1439-0396.1997.tb00734.x doi: 10.1080/1745039X.2016.1250541 Calsamiglia, S., Castillejos, L., and Busquet, M. (2005). “Estrategias nutricionales Hess, H. D., Monsalve, L. M., Lascano, C. E., Carulla, J. E., Diaz, T. E., and Kreuzer, para modificar la fermentación ruminal en vacuno lechero,” in XXI Curso de M. (2003). Supplementation of a tropical grass diet with forage legumes and Especialización, eds P. G. Rebollar, C. de Blass, and G. G. Mateos (Barcelona: Sapindus saponaria fruits: effects on in vitro ruminal nitrogen turnover and Sitio Argentino de Producción Animal), 161–185. methanogenesis. Crop Pasture Sci. 54, 703–713. doi: 10.1071/AR02241 Cammack, K. M., Austin, K. J., Lamberson, W. R., Conant, G. C., and Hu, W. L., Liu, J. X., Ye, J. A., Wu, Y. M., and Guo, Y. Q. (2005). Effect of tea Cunningham, H. C. (2018). RUMINANTNUTRITION SYMPOSIUM: tiny but saponin on rumen fermentation in vitro.Anim. Feed Sci. Technol. 120, 333–339. mighty: the role of the rumenmicrobes in livestock production.Anim. Sci. J. 96, doi: 10.1016/j.anifeedsci.2005.02.029 752–770 doi: 10.1093/jas/skx053 Hyams, D. G. (2016). CurveExpert Professional (Release 2.4.0) [Computer Carulla, J. E., Kreuzer, M., Machmuller, A., and Hess, H. D. (2005). Software]. Chattanooga, TN: Hyams Development. Available online at: http:// Supplementation of Acacia mearnsii tannins decreases methanogenesis and www.curveexpert.net (accessed January 15, 2021). urinary nitrogen in forage-fed sheep. Aust. J. Agric. Res. 56, 961–970. Hyland, J. J., Styles, D., Jones, D. J., and Williams, A. P. (2016). Improving doi: 10.1071/AR05022 livestock production efficiencies presents a major opportunity to Cook, B. G., Pengelly, B. C., Schultze-Kraft, R., Taylor, M., Burkart, S., Cardoso reduce sectoral greenhouse gas emissions. Agric. Syst. 147, 123–131 Arango, J. A., et al. (2020). Tropical Forages: An Interactive Selection Tool, 2nd doi: 10.1016/j.agsy.2016.06.006 and Revised Edn. Cali; Nairobi: International Center for Tropical Agriculture International Standardization Organization (1998). ISO 9831:1998: Animal (CIAT); Colombia and International Livestock Research Institute (ILRI). Feeding Stuffs Animal Products, and Faeces or Urine - Determination of Gross Available online at: www.tropicalforages.info (accessed January 15, 2021). Calorific Value - Bomb Calorimeter Method. Switzerland: ISO. Cuartas Cardona, C. A., Naranjo Ramírez, J. F., Tarazona Morales, A. M., Jayanegara, A., Wina, E., Soliva, C. R., Marquardt, S., Kreuzer, M., and Correa Londoño, G. A., and Barahona Rosales, R. (2015). Dry matter and Leiber, F. (2011). Dependence of forage quality and methanogenic nutrient intake and diet composition in Leucaena leucocephala-based intensive potential of tropical plants on their phenolic fractions as determined by silvopastoral systems. Trop. Subtrop. Agroecosyst. 18, 303–311. principal component analysis. Anim. Feed Sci. Technol. 163, 231–243. Cuartas Cardona, C. A., Naranjo Ramírez, J. F., Tarazona Morales, A. M., doi: 10.1016/j.anifeedsci.2010.11.009 Murgueitio Restrepo, E., Chará Orozco, J. D., Ku Vera, J., et al. (2014). Karsten, H. D., and Carlassare, M. (2002). Describing the botanical composition of Contribution of intensive silvopastoral systems to animal performance and to a mixed species northeastern US pasture rotationally grazed by cattle. Crop Sci. adaptation and mitigation of climate change. Revista Colombiana de Ciencias 42, 882–889. doi: 10.2135/cropsci2002.0882 Pecuarias 27, 76–94. Krizsan, S. J., Ahvenjärvi, S., and Huhtanen, P. (2010). A meta-analysis of Danielsson, R., Ramin, M., Bertilsson, J., Lund, P., and Huhtanen, P. (2017). passage rate estimated by rumen evacuation with cattle and evaluation of Evaluation of a gas in vitro system for predicting methane production in vivo. passage rate prediction models. J. Dairy Sci. 93, 5890–5901. doi: 10.3168/jds.20 J. Dairy Sci. 100, 8881–8894. doi: 10.3168/jds.2017-12675 10-3457 Demarchi, J., Manella, M., Primavesi, O., Frighetto, R., Romero, L., Berndt, A., Krizsan, S. J., Pang, D., Fatehi, F., Rinne, M., and Huhtanen, P. (2020). et al. (2016). Effect of seasons on enteric methane emissions from cattle grazing Metabolisable energy of grass and red clover silages fed to sheep at maintenance Urochloa brizantha. J. Agric. Sci. 8, 106–115. doi: 10.5539/jas.v8n4p106 level. Animal 14, 753–762 doi: 10.1017/S1751731119002556 Evitayani, E., Warly, L., Fariani, A., Ichinohe, T., and Fujihara, T. (2004). Study on Krom, M. D. (1980). Spectrophotometric determination of ammonia: a study of a nutritive value of tropical forages in North Sumatra, Indonesia. Asian Austr. J. modified Berthelot reaction using salicylate and dichloroisocyanurate. Analyst Anim. Sci. 17, 1518–1152. doi: 10.5713/ajas.2004.1518 105, 305–316. doi: 10.1039/an9800500305 Figueiras, J. F., Detmann, E., Paulino, M. F., Valente, T. N. P., de Campos Valadares Ku-Vera, J. C., Castelán-Ortega, O. A., Galindo-Maldonado, F. A., Arango, Filho, S., and Lazzarin, I. (2010). Intake and digestibility in cattle under grazing J., Chirinda, N., Jiménez-Ocampo, R., et al. (2020a). Review: strategies for supplemented with nitrogenous compounds during dry season. R. Bras. Zootec. enteric methane mitigation in cattle fed tropical forages. Animal 4, s453–s463. 39, 1303–1312. doi: 10.1590/S1516-35982010000600020 doi: 10.1017/S1751731120001780 Frontiers in Sustainable Food Systems | www.frontiersin.org 181 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages Ku-Vera, J. C., Jiménez-Ocampo, R., Valencia-Salazar, S., Flores-Santiago, E. J., Oseni, O. A., Ibeto, A. U., and Aruna, M. O. (2011). Effects of dehusking on Montoya-Flores, M. D., Molia-Botero, I. C., et al. (2020b). Role of secondary the composition of phytochemicals nutrients, antinutrients, minerals and in- plant metabolites on enteric methane mitigation in ruminants. Front. Vet. Sci. vitro multi enzyme digestibility of the seed of Brazilian Jack beans (Canavalia 7:584. doi: 10.3389/fvets.2020.00584 braziliensis). Int. Res. J. Biotechnol. 2, 192–197. Lascano, C. E., and Cárdenas, E. (2010). Alternatives for methane Patra, A. K., Park, T., Kim, M., and Yu, Z. (2017). Rumen methanogens emission mitigation in livestock systems. R. Bras. Zootec. 39, 175–182. and mitigation of methane emissions by anti-methanogenic compounds doi: 10.1590/S1516-35982010001300020 and substances. J. Anim. Sci. Biotechnol. 8:13. doi: 10.1186/s40104-017- Lavrenčič, A., Stefanon, B., and Susmel, P. (1997). An evaluation of the Gompertz 0145-9 model in degradability studies of forage chemical components. Anim. Sci. J. 64, Patra, A. K., and Saxena, J. (2010). A new perspective on the use of plant 423–431. doi: 10.1017/S1357729800016027 secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry Lee, J. M., Woodward, S. L., Waghorn, G. C., and Clark, D. A. (2004). 71, 1198–1222. doi: 10.1016/j.phytochem.2010.05.010 Methane emissions by dairy cows fed increasing proportions of white clover Patra, A. K., and Saxena, J. (2011). Exploitation of dietary tannins to improve (Trifolium repens) in pasture. Proc. N. Zeal. Grass. Assoc. 66, 151–155. rumen metabolism and ruminant nutrition. J. Sci. Food Agric. 91, 24–37. doi: 10.33584/jnzg.2004.66.2552 doi: 10.1002/jsfa.4152 Lee, M. A. (2018). A global comparison of the nutritive values of forage Peters, M., Franco, L., Schmidt, A., and Hincapié, B. (2002). Especies plants grown in contrasting environments. J. Plant Res. 131, 641–654. Forrajeras Multipropósito: Opciones para productores de Centroamérica. Cali: doi: 10.1007/s10265-018-1024-y Centro Internacional de Agricultura Tropical (CIAT); Bundesministerium Lindgren, E. (1983). Recalibration of the VOS Method for Determination of für Wirtschaftliche Zusammenarbeit und Entwicklung (BMZ); Deutsche Energy Content in Forages (Nykalibrering av VOS-metoden för bestämning av Gesellschaft für Technische Zusammenarbeit (GTZ), 113. energivärde hos vallfoder). Working Paper. Uppsala: Swedish University of Peters, M., Rao, I. M., Fisher, M. J., Subbarao, G., Martens, S., Herrero, G., et al. Agricultural Sciences (In Swedish). (2012). “Tropical forage-based systems to mitigate greenhouse gas emissions,” Low, S. G. (2011). Signal grass (Urochloa decumbens) toxicity in grazing ruminants. in Eco-Efficiency: From Vision to Reality, ed C. H. Hershey, (Cali: Centro Agriculture 5, 971–990. doi: 10.3390/agriculture5040971 Internacional de Agricultura Tropical (CIAT)), 20. Makkar, H. P. (2003). “Measurement of total phenolics and tannins using Folin- Rao, I., Peters, M., Castro, A., Schultze-Kraft, R., White, D., Fisher, M., et al. (2015). Ciocalteu method,” in Quantification of Tannins in Tree and Shrub Foliage: A LivestockPlus - the sustainable intensification of forage-based agricultural Laboratory Manual, ed H. Makkar (Dordrecht: Kluwer Academic Publisher), systems to improve livelihoods and ecosystem services in the tropics. Trop. 49–50. doi: 10.1007/978-94-017-0273-7_3 Grass. For. Trop. 3:59. doi: 10.17138/TGFT(3)59-82 McAllister, T. A., Bae, H. D., Jones, G. A., and Cheng, K. J. (1994). Microbial Rojas, S., Olivares, J., Jimenez, R., and Hernández, E. (2005). Manejo de praderas attachment and feed digestion in the rumen. Anim. Sci. J. 72, 3004–3018. asociadas de gramíneas y leguminosas para pastoreo en el trópico. Revista doi: 10.2527/1994.72113004x Electronica de Veterinaria 6, 103–122. Molina, I. C., Donney‘s, G., Montoya, S., Rivera, J. E., Villegas, G., Chará, J., SAS Institute (2012). User’s Guide: Statistics (Version 9.4) [Computer Software]. et al. (2015). La inclusión de Leucaena leucocephala reduce la producción de Cary, NC: SAS Institute Inc. metano de terneras Lucerna alimentadas a base de Cynodon plectostachyus Searle, P. L. (1984). The Berthelot or indophenol reaction and its use in y Megathyrsus maximus. Livestock Research for Rural Development, 27. the analytical chemistry of nitrogen. A review. Analyst 109, 549–568. Available online at: http://www.lrrd.org/lrrd27/5/moli27096.html doi: 10.1039/an9840900549 Molina-Botero, I. C., Arroyave-Jaramillo, J., Valencia-Salazar, S., Barahona- Seresinhe, T., Madushika, S. A. C., Seresinhe, Y., Lal, P. K., and Orskov, Rosales, R., Aguilar-Pérez, C. F., Ayala Burgos, A., et al. (2019b). Effects of E. R. (2012). Effects of tropical high tannin non legume and low tannin tannins and saponins contained in foliage of Gliricidia sepium and pods of legume browse mixtures on fermentation parameters and methanogenesis Enterolobium cyclocarpum on fermentation, methane emissions and rumen using gas production technique. Asian Austral. J. Anim. 25, 1404–1410. microbial population in crossbred heifers. Anim. Feed Sci. Technol. 251:1–11. doi: 10.5713/ajas.2012.12219 doi: 10.1016/j.anifeedsci.2019.01.011 Shelton, H.M., and Dalzell, S. A. (2007). Production, economic and environmental Molina-Botero, I. C., Mazabel, J., Arceo-Castillo, J., Urrea-Benitez, J. L., benefits of leucaena pastures. Trop. Grass. For. Trop. 41, 174–190. Olivera-Castillo, L., Barahona-Rosales, R., et al. (2020). Effect of the StatPoint Technologies Inc. (2010). STATGRAPHICS©R Centurion XVI (Version addition of Enterolobium cyclocarpum pods and Gliricidia sepium forage 16.1.18, 32 Bits) [Computer Software]. The Plains, VA: Available online on dry matter degradation, volatile fatty acid con-centration, and in at: http://www.statgraphics.net/ (accessed January 15, 2021). vitro methane production. Trop. Anim. Health Prod. 52, 2787–2798. Tang, S. X., Tayo, G. O., Tan, Z. L., Sun, Z. H., Wang, M., Ren, G. P., et al. (2008). doi: 10.1007/s11250-020-02324-4 Use of in vitro gas production technique to investigate interactions between rice Molina-Botero, I. C., Montoya, D., Zavala, L., Barahona, R., Arango, J., straw, wheat straw, maize stover and alfalfa or clover.Asian Austral. J. Anim. 21, and Ku, J. (2019a). Effects of long-term diet supplementation with 1278–1285. doi: 10.5713/ajas.2008.70447 Gliricidia sepium foliage mixed with Enterolobium cyclocarpum pods on Tavendale, M. H., Meagher, L. P., Pacheco, D., Walker, N., Attwood, G. T., and enteric methane, apparent digestibility, and rumen microbial population Sivakumaran, S. (2005). Methane production from in vitro rumen incubations in crossbred heifers. J. Anim. Sci. 97, 1619–1633. doi: 10.1093/jas/ with Lotus pedunculatus and Medicago sativa, and effects of extractable skz067 condensed tannin fractions on methanogenesis. Anim. Feed Sci. Technol. 123, Montoya-Flores, M. D., Molina-Botero, I. C., Arango, J., Romano-Muñoz, J. 403–419. doi: 10.1016/j.anifeedsci.2005.04.037 L., Solorio-Sánchez, F. J., Aguilar-Pérez, C. F., et al. (2020). Effect of dried Theodorou, M. K., Williams, B. A., Dhanoa, M. S., McAllan, A. B., and France, leaves of Leucaena leucocephala on rumen fermentation, rumen microbial J. (1994). A simple gas production method using a pressure transducer to population, and enteric methane production in crossbred heifers. Animals determine the fermentation kinetics of ruminant feeds.Anim. Feed Sci. Technol. 10:300. doi: 10.3390/ani10020300 48, 185–197. doi: 10.1016/0377-8401(94)90171-6 Moss, A. R., Givens, D. I., and Phipps, R. H. (1992). Digestibility and energy Tiemann, T. T., Lascano, C. E., Kreuzer, M., and Hess, H. D. (2008a). The ruminal value of combinations of forage mixtures.Anim. Feed Sci. Technol. 39, 151–172. degradability of fibre explains part of the low nutritional value and reduced doi: 10.1016/0377-8401(92)90038-8 methanogenesis in highly tanniniferous tropical legumes. J. Sci. Food Agric. 88, Naranjo, J. F., Cuartas, C. A., Murgueitio, E., Char,á, J., and Barahona, R. (2012). 1794–1803. doi: 10.1002/jsfa.3282 Balance de gases de efecto invernadero en sistemas silvopastoriles intensivos Tiemann, T. T., Lascano, C. E., Wettstein, H.-R., Mayer, A. C., Kreuzer, M., con Leucaena leucocephala en Colombia. LRRD 24:150. and Hess, H. D. (2008b). Effect of the tropical tannin-rich shrub legumes Nguku, S. A. (2015). An evaluation of brachiaria grass cultivars productivity in semi Calliandra calothyrsus and Flemingia macrophylla on methane emission arid Kenya (Doctoral dissertation). Available online at: http://repository.seku. and nitrogen and energy balance in growing lambs. Animal 2, 790–799. ac.ke/handle/123456789/1380 (accessed January 15, 2021). doi: 10.1017/S1751731108001791 Frontiers in Sustainable Food Systems | www.frontiersin.org 192 June 2021 | Volume 5 | Article 663003 Quintero-Anzueta et al. In-vitro Methane From Tropical Forages Tolera, A., Seyoum, M., and Sundstol, F. (1998). “Nutritive evaluation of Leucaena Wassie, W. A., Tsegay, B. A., Wolde, A. T., and Limeneh, B. A. (2018). leucocephala, L. diversifolia and L. pallida in Awassa, Southern Ethiopia,” Evaluation of morphological characteristics, yield and nutritive value of in Proceedings of a Workshop held in Hanoi, Vietnam 9-14 February 1998: brachiaria grass ecotypes in northwestern Ethiopia. Agric. Food Secur. 7, 1–10. Leucaena - Adaptation, Quality and Farming Systems eds H. M. Shelton, R. C. doi: 10.1186/s40066-018-0239-4 Gutteridge, B. F. Mullen, and R. A. Bray (ACIAR Proceedings), 261–264. Wilkinson, J. M. (2011). Re-defining efficiency of feed use by Tope, A. F., Oluwafemi, O. J., Oladunni, O. F., and Aderemi, A. D. (2013). Feeding livestock. Animal 5, 1014–1022. doi: 10.1017/S1751731111 values of seven browse tree foliages mixed in varying proportions with Panicum 00005X maximum for feeding ruminants. Am. J. Sci. 9, 64–71. Yokoyama, M. T., and Johnson, K. A. (1993). “Microbiología del rumen e Valencia-Salazar, S. S., Jiménez-Ferrer, G., Arango, J., Molina-Botero, I., Chirinda, intestino,” in El rumiante: fisiología digestiva y nutrición, ed D. C. Church N., Piñeiro-Vázquez, A., et al. (2021). Enteric methane mitigation and (Zaragoza: Acribia S.A.), 137–156. fermentation kinetics of forage species from Southern Mexico: in vitro screening. Agrofor. Syst. 95, 293–305. doi: 10.1007/s10457-020-00585-4 Conflict of Interest: The authors declare that the research was conducted in the Van Soest, P., Robertson, J., and Lewis, B. (1991). Methods for dietary fiber, neutral absence of any commercial or financial relationships that could be construed as a detergent fiber and non-starch polysaccharides in relation to animal nutrition. potential conflict of interest. J. Dairy Sci. 74, 3583–3597. doi: 10.3168/jds.S0022-0302(91)78551-2 Vazquez, E., Teutscherova, N., Lojka, B., Arango, J., and Pulleman, M. (2020). Copyright © 2021 Quintero-Anzueta, Molina-Botero, Ramirez-Navas, Rao, Pasture diversification affects soil macrofauna and soil biophysical properties Chirinda, Barahona-Rosales, Moorby and Arango. This is an open-access article in tropical (silvo)pastoral systems. Agric. Ecosyst. Environ. 302:107083. distributed under the terms of the Creative Commons Attribution License (CC BY). doi: 10.1016/j.agee.2020.107083 The use, distribution or reproduction in other forums is permitted, provided the Vendramini, J. M., Sollenberger, L. E., Soares, A. B., da Silva, W. L., Sanchez, J. M., original author(s) and the copyright owner(s) are credited and that the original Valente, A. L., et al. (2014). Harvest frequency affects herbage accumulation and publication in this journal is cited, in accordance with accepted academic practice. nutritive value of brachiaria grass hybrids in Florida. Trop. Grass. For. Trop. 2, No use, distribution or reproduction is permitted which does not comply with these 197–206. doi: 10.17138/TGFT(2)197-206 terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1203 June 2021 | Volume 5 | Article 663003 ORIGINAL RESEARCH published: 20 September 2021 doi: 10.3389/fenvs.2021.673481 Ex-Ante Evaluation of Economic Impacts of Adopting Improved Forages in the Colombian Orinoquía Karen Enciso1, Andres Charry1, Álvaro Rincón Castillo2 and Stefan Burkart 1* 1The Alliance of Bioversity International-CIAT, Crops for Nutrition and Health, Tropical Forages Program, Cali, Colombia, 2The Colombian Agricultural Research Corporation (AGROSAVIA), Villavicencio, Colombia Forage-based cattle systems play a key role in rural economies of developing countries in terms of food security and poverty alleviation. However, they can generate negative environmental impacts by contributing to increased greenhouse gas emissions, land degradation, and reduction of biodiversity. As a result of that, large amounts of resources have been allocated to research and development (R&D) in forage material improvement and a broad range of improved materials were released showing superior characteristics in terms of productivity and environmental impacts compared to native or naturalized materials. However, data are still scarce on both the economic and environmental “yields” of investments in R&D activities around improved forage Edited by: materials. Through an ex-ante evaluation, this study aims at estimating the potential Glenn Hyman, Independent Researcher, Dapa, “yields” of the investment in R&D and diffusion activities of the improved forage variety Colombia Brachiaria brizantha 26,124 cv. Agrosavia Caporal in the Colombian Orinoquía region. The Reviewed by: analysis used two evaluation methodologies: 1) a combined discounted free cash flow Jeffrey Alwang, model and Monte Carlo simulation using the simulation software @Risk to determine the Virginia Tech, United States Muntasir Murshed, impact on individual welfare, and 2) an economic surplus model an risk analysis to North South University, Bangladesh determine the potential social benefits of the technologies and their distribution among *Correspondence: producers and consumers, considering changes in adoption rates, productivity levels and Stefan Burkart probability of success. The results suggest that the evaluated material presents important s.burkart@cgiar.org economic benefits for the study region and results in a positive return on the investments Specialty section: made in R&D activities. The results are a key input for decision making processes among This article was submitted to public and private institutions involved in funding and executing the development of Environmental Economics and improved forage materials and will help to set research priorities and resource allocation. Management, a section of the journal Keywords: agricultural research and development, priority setting, technological change, economic surplus Frontiers in Environmental Science analysis, decision making, funding allocation for research, sustainable intensification (SI), conservation Received: 01 March 2021 Accepted: 06 September 2021 Published: 20 September 2021 INTRODUCTION Citation: Enciso K, Charry A, Castillo ÁR and The Cattle Sector in the Colombian Orinoquía Burkart S (2021) Ex-Ante Evaluation of Cattle production is one of the main agricultural activity in Colombia and plays a major role in the Economic Impacts of Adopting achievement of the Sustainable Development Goals in the region, as it holds a large potential for Improved Forages in the Colombian Orinoquía. economic, social and environmental improvements. The Colombian cattle sector contributes with Front. Environ. Sci. 9:673481. 21.8% of the agricultural Gross Domestic Product of the country and generates approximately 6% of doi: 10.3389/fenvs.2021.673481 the national and 19% of agricultural employment, respectively (FEDEGAN, 2018). Its importance Frontiers in Environmental Science | www.frontiersin.org 211 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía also lies in its impact on a social level. Cattle farming is mainly humidicola CIAT 679 cv. Humidicola, Brachiaria brizantha carried out by small-scale farmers (81% of the cattle farms in CIAT 26110 cv. Toledo and, more recently, Brachiaria Colombia possess less than 50 animals, with an average of 18 brizantha CIAT 26124 cv. Agrosavia Caporal stand out as animals per farm) (ICA, 2020). Additionally, it is estimated that superior alternatives to the traditional Brachiaria decumbens 44% of the cattle producer households live in conditions of cultivars mainly used in the Orinoquía (Miles et al., 1996). poverty (DANE-CNA, 2014; UPRA, 2019, 2020). According to Processes of identification and release of new forage materials the Food and Agriculture Organization of the United Nations represent the first step towards sustainable intensification (FAO, 2018), the sector has the potential to contribute to the goals (improving efficiency without the need to further expand of income and poverty reduction, reducing the environmental pasture areas), increasing food security and decreasing footprint, enhancing the provision of ecosystem services and environmental trade-offs (including greenhouse gas emission promoting peace and social stability, among others. Over 20% intensities of the cattle sector). Under the right enabling of the total agricultural production from developing countries conditions (e.g., subsidized credit, technical assistance, comes from this sector, and the increasing demand for animal protective tariffs and land tenure security), sustainable source foods, coupled with changing diets and decreased intensification can help in achieving the objective of liberating availability of suitable land, pose major pressures on increasing areas with potential for crop cultivation, reforestation, the efficiency of the sector in ways that are inclusive, conservation or landscape recovery. environmentally responsible and improve food security. In Research on new varieties for the agricultural sector is Colombia, its environmental relevance is primary, as cattle recognized as a powerful instrument to accelerate economic production generates 16% of the greenhouse gas emissions of growth and development (The World Bank, 2008; Stads and the Colombian Agriculture, Forestry and Other Land Use sector Beintema, 2009), but this process requires steady financing to (AFOLU), and is also one of the principal activities associated maintain and enhance the necessary scientific, technical and with deforestation and the expansion of the agricultural Frontier technological capacities and infrastructure. In particular, most (IDEAM and MADS, 2016). resources for agricultural research come from public funds, The Orinoquía region is of special importance for the making it of special importance that the technologies derived country’s cattle sector, as it holds approximately 20% of the from R&D processes are profitable and viable. Ex-ante impact total national cattle inventory (ICA, 2020), with nearly 55% of its evaluations allow estimating the possible benefits of R&D agricultural land destined to cattle grazing (UPRA, 2015a; UPRA, investments, providing information for prioritization and more 2015b; UPRA, 2015c). Although the average farm size in the strategic decision-making (Maredia et al., 2014). region is rather large (534 ha), this is biased by a small number of Studies on the evaluation of impacts generated by the large-scale farmers while the region is dominated by small-scale development of new forage materials in Colombia are scarce cattle farms with an inventory of less than 50 animals (ICA, and date back to the 1990s and early 2000s. They focus on new 2020). The sector faces important challenges, as the expansion of Brachiaria hybrids and accessions adapted to different regions of cattle production threatens biodiversity and strategic ecosystems the country (e.g., Vera et al., 1989; Seré et al., 1993; Rivas and in the region, such as natural savannas, gallery forests, foothills or Holmann, 2004a, 2004b), providing consistent results on the flooded forests. Additionally, forage supply is highly dependent positive economic impacts derived from the adoption in cattle on the marked water seasonality of the region (excessive rainfall systems. No recent studies, however, evaluate the potential and drought), directly affecting cattle production and making the benefits of new forage materials. New grasses and legumes -- sector more vulnerable to climate change. Investments in more including cv. Agrosavia Caporal, the most recent technology to be intensive cattle production systems, considering the specific delivered to Colombia’s cattle producers–lack economic environmental conditions, water dynamics and presence of evaluation. B. brizantha cv. Agrosavia Caporal will be the strategic ecosystems in the region, therefore, have been the third Brachiaria brizantha material released in the country, main approach for achieving a sustainable development of the after the La Libertad (CIAT 26646) and the Toledo varieties regional cattle sector (CIAT and CORMACARENA, 2018). released in 1987 and 2002, respectively. This material has been To advance towards sustainable intensification of cattle evaluated since 1986 and was identified as a promising alternative farming in the Orinoquía, institutions such as the Colombian to improve cattle production in well-drained soils of the Agricultural Research Corporation (AGROSAVIA, before Orinoquía. In this sense, the objective of this study is to Corpoica) and the International Center for Tropical evaluate the impact of R&D and adoption of the new variety Agriculture (CIAT) have been commissioned to carry out Brachiaria brizantha 26,124 cv. Agrosavia Caporal (Agrosavia research on new forage materials. Government and research Caporal from here on) in the Colombian Orinoquía region, with institutions consider the region as strategic for forage research emphasis on the beef raising and fattening production system. and development (R&D), due to high soil acidity and low fertility For this purpose, we applied models at two aggregation scales - - both key for carrying out adaptation and productivity trials with the micro and macro level. At the micro or farm level, a cost- new and promising materials (Peters et al., 2013; Rao et al., 2015). benefit analysis was performed using a discounted free cash flow Research has been aimed at identifying new forage materials with model and a Monte Carlo simulation analysis. This model was better productive characteristics, a greater range of adaptation to used to evaluate and analyze potential impacts on the primary extreme conditions and higher resistance to local pests and producer and to determine if the adoption of the technology is diseases. Among the released materials, the grasses Brachiaria economically feasible. At the macro level or the regional scale, an Frontiers in Environmental Science | www.frontiersin.org 222 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía economic surplus model was used in order to estimate and approximately US$11.8 million, which represents an internal analyze the potential added benefit for the society and its social rate of return on investments of 38% over a 20-year distribution among two different social groups: producers and period. Schiek et al. (2018) evaluated the potential economic consumers. The economic surplus model is the most widely used impact of the development and release of improved Brachiaria model for measuring ex-ante impacts of technological varieties in six East African countries, using an economic surplus innovations, providing a consistent theoretical basis with model. According to their results, investment in a forage research minimum data requirements. Although there are other more program is a low risk endeavor with a high probability of precise models (e.g., the IMPACT model), we aimed at obtaining positive results at a minimum adoption rate of 10%. maximizing the precision of our estimates, considering budget Most of the described studies used the economic surplus limitations, time constraints and access to available data. method as main approach for impact evaluation. In general, Agrosavia Caporal has already been developed, but it is not yet across all reviewed studies, positive results were found available to producers (planned year of release: 2022). One of the regarding the benefits of research on forage alternatives with aims of this study is, therefore, to not only guide the decision- better productive characteristics as strategy for intensifying cattle making process of investing in the development of future production. Although some of the past studies focused on the varieties, but to also provide evidence on the potential benefits impacts of improved forages in different regions of Colombia, of other endeavors with similar contexts. This study also attempts neither more recent ex-ante evaluations were found, nor to highlight some of the minimal conditions in terms of adoption particular studies regarding the species Brachiaria brizantha or levels and expected benefits, necessary to make such investments micro-level studies that include quantitative risk assessments, profitable both at the individual and social levels. The article is which give more robust results and improve decision-making at structured as follows: First, we present the theoretical framework the primary producer level. This document is intended to be a on adoption processes at the micro and macro level, a literature contribution to the literature in that sense, and provides useful review on previous studies on the subject and the empirical information to donors and decision-makers regarding the methodology we applied. In Section Results, we present our potential yields of investing in forage research for the results. Section Discussion discusses these results considering Colombian Orinoquía. previous studies on the subject and on-going adoption processes in the region. The final section presents the conclusions of the article. MATERIALS AND METHODS Data Sources Review on Economic Evaluations of Productivity data for the Agrosavia Caporal variety were obtained Brachiaria in Latin America from field trials carried out by AGROSAVIA and CIAT in the In the context of adopting improved forages, impact evaluation Colombian Orinoquía region. Evaluations were carried out at the studies were conducted mainly at the end of last century, and Taluma experimental station and the Carimagua Research Center especially regarding Brachiaria hybrids and accessions in under well-drained soil conditions. The average temperature at different regions of Latin America (e.g., Seré and Estrada, the site is 26°C and the average annual rainfall 2,500 mm. 1982; Rivas and Holmann, 2004a; Rivas and Holmann, 2004b). Productivity was calculated as the average of the accumulated Seré and Estrada (1982) evaluated the profitability of cattle live weight gain over a year in a cattle raising and fattening fattening under different feeding scenarios (with improved system. These measurements were carried out on a monthly basis forages) in various locations of the Orinoquía, finding Internal between 2011 and 2015, with six groups of young crossbred bulls Rates of Return (IRR) of between 10.7 and 30.4% (Vera et al., in a rotational grazing design, with 14 days of occupation and 1989). calculated that the use of Antropogon gayanus (Carimagua 28 days of recuperation. Information on the traditional I) is 33% more profitable than traditional (naturalized) forages in technology (reference technology) used in the region was the Orinoquía region and 78% the northern Caribbean of obtained through interviews with AGROSAVIA researchers Colombia, respectively. Seré et al. (1993) examined the and from past field evaluations conducted in the region. The profitability of tropical forages released by CIAT and its local ex-ante impact analysis seeks to compare a novel technology with partners in Latin America, identifying an IRR of between 20 and a technology traditionally used in the study region. In our case, 100%. Rivas and Holmann (2004a) evaluated the potential impact Brachiaria decumbens as monoculture is the technology with the of new Brachiaria hybrids resistant to spittlebug in the eastern largest area in the Colombian Orinoquía, with important Orinoquía region and the Caribbean coast of Colombia, and characteristics in terms of productivity and adaptability to estimated benefits for 2004 of US$960 million, which was well-drained soils in the region (Rincón et al., 2010). The equivalent to 43% of the country’s meat and milk production grass Brachiaria decumbens, was introduced and used value in 2003 (direct impact on the livestock sector). More recent massively in the country in the 1970s. The scenario assumes studies on the subject were found for the African continent, where adequate management practices in terms of fertilization and the impact of higher-yielding Brachiaria varieties was estimated. rotation, to avoid overestimating the benefits associated with Elbasha et al. (1999), for example, evaluated the impact of the adoption of the new variety. different planted forages in West Africa during the period Information related to economic and technological from 1977 to 1997 and estimated economic benefits of assumptions, as well as the R&D costs used in the economic Frontiers in Environmental Science | www.frontiersin.org 233 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía surplus model, was obtained through expert consultation and animal feeding trials carried out at two locations in the literature review. Section 2.6.1 shows the data sources Orinoquía (Taluma experimental station and Carimagua corresponding to each parameter used. The establishment and Research Center), where it was compared with Brachiaria management costs of the evaluated technologies were calculated decumbens - the control material predominant in the region. based on the economic information collected during the trials, The main characteristics that made Agrosavia Caporal an which was adjusted with the help of forage and livestock experts outstanding alternative for animal feeding, and especially according to the conditions of a typical beef cattle raising and compared to other evaluated accessions such as Toledo fattening farm in the Orinoquía region. Prices were updated to (Brachiaria brizantha CIAT 26110), are its high forage 2018 according to the price bulletins of the Colombian Price productivity and quality, drought resistance (i.e., avoiding Information System of the Agricultural Sector SIPSA/DANE cattle weight losses during dry season) and grazing persistence (2020) and databases of the Colombian Cattle Farmer (Rincón et al., 2021). B. brizantha cv. Agrosavia Caporal also Federation, FEDEGAN, (2019a). shows good tolerance to water stress during the rainy season, as well as to different spittlebug species (Aeneolamia varia and Zulia Characteristics of the New Technology pubescens) present in the region (Rincón et al., 2021). B. brizantha cv. Agrosavia Caporal is a new forage alternative Table 1 provides a summary of the main productive indicators coming directly from the species Brachiaria brizantha, which was of cv. Orinoquía, as well as the reference technology (Brachiaria collected in Karuzi (Burundi, Africa) in 1985. CIAT researchers decumbens) for comparison. The adoption of Agrosavia Caporal collected this material in collaboration with the Burundian increases the total available forage biomass by 23% and the national agricultural research institution (ISABU) (Rincón protein content by 28% compared to the reference technology, et al., 2021). Agrosavia Caporal is a perennial grass that grows reflected also in the animal response, with average annual live in clumps, with decumbent stems of a height of 60–150 cm, weight gains per hectare of 226 kg for Agrosavia Caporal versus capable of rooting in the ground and favoring soil coverage, 198 kg for Brachiaria decumbens. According to the daily live persistence and lateral displacement of the grass. Its leaves are weight gain data, the raising and fattening cycle until reaching the lanceolate with little pubescence, reaching up to 60 cm in length final sales weight (from 200 kg to 450 kg) is 19 months for and 2.5 cm in width. It grows well in tropical conditions up to Agrosavia Caporal and 24 months for Brachiaria decumbens. altitudes of 1,800 m above sea level. It develops best at temperatures between 20 and 35°C, with the highest forage production occurring during rainy season and in conditions Methodological Approach: Cost-Benefit with annual rainfall between 1,600 and 3,500 mm (Rincón Analysis et al., 2021). Although the variety was targeted to the Through a cost-benefit analysis, we estimated the impact of Orinoquía region, it holds the potential for broader adoption investing in the establishment of Agrosavia Caporal in a cattle in other regions of Colombia, given its adaptation potential to raising and fattening system at the micro level (from a primary different climates (humid and sub-humid tropics) and soils producer’s point of view) in the Colombian Orinoquía. This (medium to good fertility) (M. Sotelo, personal methodology was used as it allows to analyze the market viability communication, May 17, 2020). of an investment project in a reliable way, considering all the The first evaluation records of B. brizantha cv. Agrosavia relevant costs and benefits in a process of technology adoption at Caporal in Colombia date back to 1986, when antibiotic the farm level, the lifespan of the technology, productivity flows resistance to spittlebug was evaluated among 400 accessions of and relevant market prices. Such analysis is being applied when a Brachiaria. Accession 26,124 was part of a group of 27 materials comparison has to be made between a traditional technology and which were selected for presenting greater resistance compared to a new one, in order to determine the changes in costs and income the commercial material Brachiaria brizantha cv. Marandú associated with the new technology. In our case, the comparison (CIAT, 1991). In 1997, it was one of the materials selected for is made with the reference technology–a monoculture pasture of presenting better drought resistance in trials established at the Brachiaria decumbens (A. Rincón, personal communication, Carimagua research station in the Colombian Orinoquía (CIAT, February 12, 2021). 1997). In 1999, it was introduced for agronomic evaluation in The cost-benefit analysis is based on a discounted free cash different locations across Colombia (CIAT, 1999), and in 2000, in flow model to estimate financial profitability indicators and to the Orinoquía (CIAT, 2001). In a participatory evaluation determine the viability of the different investment options. exercise, Agrosavia Caporal was selected by producers as a Profitability indicators include the Internal Rate of Return promising material for cattle production in the Orinoquían (IRR), Net Present Value (NPV), Benefit/Cost ratio (B/C) and savannas, due to its good stem-leaf ratio, soft leaves, rooting investment payback period (PRI). The model includes a behavior and rapid recovery after grazing (CIAT, 2001). systematic categorization of the variable costs and benefits In 2011, in an inter-institutional agreement between associated with the two evaluated options. Specifically, the AGROSAVIA and CIAT, forage germplasm evaluations under following per hectare cost categories have been considered: well-drained soils were started in the Orinoquía with the establishment costs, renovation and maintenance costs, establishment of 58 materials and the aim of selecting the five opportunity costs of capital during the establishment period most promising ones. The Agrosavia Caporal accession was (3 months, from establishment until first grazing), and identified as one of these materials, and was included in operating costs (e.g., purchase of animals, animal health, Frontiers in Environmental Science | www.frontiersin.org 244 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía TABLE 1 | Dry matter production, nutritional quality and animal response of the evaluated grasses. Parameter Variable Brachiaria brizantha 26,124 Brachiaria decumbens cv. Agrosavia caporal (reference technology) Biomass production DM (ton ha−1 y−1) 7.1 5.8 Nutritional quality Crude protein (% DM) 9.6 7–8 IVDMD (%) 65 62 Animal response Animal carrying capacity (AU) 1.4 1.2 Live weight gain (g AU−1 d−1) 418 345 Animal productivity (kg ha−1 y−1) 226 198 Raising and fattening period (months)1 19 24 IVDMD  In Vitro Dry Matter Digestibility; 1 AU (Animal Unit)  400 kg/animal; DM  Dry Matter; 1 Period of time required to bring an animal of 200 kg average weight to a sales weight of 450 kg. TABLE 2 | Variables simulated with the Monte Carlo model. # Variable Distribution Most likely Minimum value Maximum value value 1 Meat price (US$ kg−1) Triangular1 1.26 1.21 1.31 2 Live weight gain Agrosavia Caporal (g AU−1 d−1) PERT2 226 199 262 3 Live weight gain References technology (g AU−1 d−1) PERT2 198 128 227 4 Establishment costs Agrosavia Caporal (US$ ha−1) Triangular 341 273 409 5 Establishment costs References technology (US$ ha−1) Triangular 306 245 368 aPrices in US$–/US$/COP XRT: Average 2020; 1This triangular distribution is an average of the three values and is recommended to specify situations that involve costs and investments; 2A PERT distribution is a weighted average of the three values with greater emphasis on the center of the distribution and was selected by judgment of the researchers according to data availability. supplementation, permanent and occasional labor). On the other identified as critical (meat price, live weight gain, hand, the benefits are derived from beef production in a cattle establishment costs) are randomly assigned, according to their raising and fattening system, according to the obtained animal probability distribution functions, to later calculate the response indicators (Table 1). For the construction of the cash determined profitability indicators (model outputs). This flow we assumed constant prices and an evaluation horizon of process is repeated numerous times to obtain the probability 10 years according to the estimated lifespan of pastures (Riesco distributions of said outputs (Park, 2007). In our study, 5,000 and Seré, 1985). The cost of financing is chosen as the discount simulations or iterations were carried out, where the variables live rate according to the rural credit lines of the Colombian Fund for weight gain (per animal and day), investment costs, and sales the Financing of the Agricultural Sector (FINAGRO), and price (per kg live weight) were randomly combined. The considered as the opportunity cost of capital, associated with a simulation used a 95% confidence interval. The probability risk factor present in the activities of the rural sector. The distributions for the input variables are presented in Table 2. following discount rate was, therefore, established: Fixed-term The decision criteria are the mean values and the variations of deposit rate (DTF) + 5% effective annual interest rate. The the profitability indicators resulting from the simulation, as well investment is assumed to happen in year 0, and from year one as the probability of success (NPV>0). The use of the mean value to year 10, the income and expenses associated with each criterion is based on the law of large numbers, which states that if technology are generated. It is important to mention that, many repetitions of an experiment are carried out, the average although data were obtained at an experimental level, we result will tend towards the expected value (Park, 2007). expect the differences to the real conditions of the region to Additionally, a sensitivity analysis was performed using a be insignificant, if the producers follow the technical tornado diagram, which displays each variable according to its recommendations for pasture management (e.g., fertilization impact on the variance of the model result. The diagram identifies plans, periods of pasture occupation and recovery) and if the the variables defined as critical and those with greater effects on material is established under agroecological conditions similar to the profitability indicators. those recommended (e.g., altitude, soil type, precipitation regime). In addition, at a methodological level, different scenarios are applied for the returns of each of the evaluated Methodological Approach: Economic technologies (Table 2). Surplus Model To include risk and uncertainty levels and consider different The equation system for the economic surplus model is based on scenarios, a quantitative risk analysis was performed using a Alston et al. (1995) (Figure 1). It proposes to model and measure Monte Carlo simulation with the software @Risk (Paladise the economic effects of technological changes induced by Corporation). In this simulation, values of the variables research in market environments, through parallel and linear Frontiers in Environmental Science | www.frontiersin.org 255 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía shifts of the supply and demand curves. In this case, the product 1995): 1) There are no policy distortions such as subsidies, in question (beef) is a perishable good that is not closely linked to production quotas, or others; 2) markets are competitive; 3) international markets and therefore, equations for a closed the supply equals the demand for the good, since prices are economy are used. adjusted to reach equilibrium quantities, 4) the change in total The annual change in total surplus is defined as: surplus is a measure of the change in social welfare; and 5) the shift in the supply curve is only the result of technological change. ΔET  KtP0Q0(1 + 1 Ztn) (1) 2 Model Parameters whereP0 andQ0 are the equilibriumprices and quantities, respectively; To estimate the social benefits of forage varieties by means of the Z t is the proportional price decrease in year t, defined as: surplus model, it is necessary to consider different technical and economic parameters. Technical parameters allow identifying the Zt  Ktε ε + (2) magnitude of the shift in the supply function and the behavior of n the adoption curve over time and are related to: 1) changes in and Kt is the supply displacement factor associated with productivity levels, 2) year of technology launch and duration of technological change, and its value is variable over time, the diffusion period, 3) speed and intensity of the adoption depending on the dynamics of the adoption process; n is the process, and 4) R&D levels. The economic parameters define absolute value of demand elasticity and ε the supply elasticity: the markets under analysis in terms of: 1) type of economy, 2) initial equilibrium quantities and prices, and 3) price elasticities of K supply and demand. t  [E(Y) − E(C) ε 1 + E(Y)]pAtδt (3) Table 3 presents a summary of the parameters related to both where E(Y) is the average proportional yield increase per hectare, the market and the technology used to estimate the model in the with ε being the supply elasticity used to convert the gross output basic scenario, as well as the respective data sources. The impact effect of R&D-induced performance changes into a gross unit calculations at the national level were made assuming values of production cost effect; E(C) is the average proportional change in productivity increases and a potential area determined by the variable costs per hectare required to achieve the increased yield; current rate of adoption of the Brachiaria brizantha species at the national level, given its high adaptation potential. Technology p is the probability of success in the technology adoption process; δt is the depreciation factor of the technology; At is the adoption adoption behavior and the estimation of R&D costs are further rate in year t, and is determined by a logistic curve: explained in the subsequent sections. R&D costs occur from the initial year of research until the release of the new technology (2011–2022). After its release, the technology is acquired by the At  AMAX 1 + e−(α+βt) (4) private sector (in this case a seed production and marketing company from Brazil) who assumes the subsequent costs Amax is the maximum adoption rate, and the parameters α associated with seed production, marketing and distribution. and β control displacement and slope, respectively and are As these costs do not correspond to public research determined by both the duration of research and adoption. institutions or governmental institutions, they are excluded The annual change in consumer surplus is defined as: from the calculations in our study. In order to examine the sensitivity of the model results, three ΔECt  ZtP0Q0(1 + 1 Ztn) (5) 2 analysis scenarios have been considered: basic (B), optimistic (O) and pessimistic (P). The parameters that vary between scenarios The change in producer surplus is defined as: are productivity, maximum expected adoption rate, and ΔEPt  ΔET probability of success (Table 4). The probability of success is t − ΔECt (6) defined as the success of developing a technology for commercial The economic benefits associated with the change in surpluses use, as well as the annual adoption rate being met at a defined are expressed as annual flows of net benefits and the NPV is percentage. Although Agrosavia Caporal has already been estimated. The NPV of the new R&D technology is calculated as: developed, it is not yet commercially available to producers. According to preliminary agreements with seed producing ΔET NPV  ∑T t − kt companies, it will be commercialized in 2022. Additionally, (1 + r)t (7) t heat maps were elaborated to analyze the effect of the variation simultaneal of the first two variables on the IRR The aggregate IRR was calculated as the discount rate that indicator. equates the aggregate NPV to zero as follows: Cost of Research and Development ∑T ΔETt − kt The R&D costs for the evaluation and selection of the new (1 + TIR)t  0 (8) t Agrosavia Caporal variety were estimated according to the requirements of scientific personnel in a process of Additionally, for the estimation of the ex-ante evaluation improvement by selection, and the annual budgets approved model, the following assumptions are considered (Alston et al., under the macroproject Evaluación y desarrollo de materiales Frontiers in Environmental Science | www.frontiersin.org 266 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía TABLE 3 | Description of the key parameters and data sources for the analysis of economic surpluses in the basic scenario. Parameter Value Description Source Economic assumptions Economy type Closed Beef from the Orinoquía region is destined for the local and Own estimate based on data from DANE (2021) extra-regional market (mainly Bogotá, Cúcuta and Bucaramanga). At the national level, 93% of the beef produced is destined for internal consumption Supply elasticity 0.7 The offered quantities vary less than proportionally to price Rivas and Holmann (2004a) changes Demand elasticity −1.17 According to Ramirez (2012), the long-term elasticity of the Ramirez (2012) beef demand is relatively elastic (>1). The estimates of cross elasticity with the other types of meat (chicken, pork) show a high substitution effect regarding price changes Regional initial production 200,560 Own estimate based on data from FEDEGAN (2019a) and (tons) ICA (2020) National initial production 932,813 FEDEGAN (2019a) (tons) Initial price (US$/ton) 2,376 Own calculations based on data from FEDEGAN and Bogota (2019b) R&D costs (US$) 563,243 Expert estimation based on R&D budgets involved in the selection process of a new forage variety Technical assumptions R&D period (years) 5 (2011–2015) Evaluations for the selection of promising materials under the agreement AGROSAVIA-CIAT. Diffusion period (years) 27 The diffusion period can vary between 25 and 30 years, Rivas and Holmann (2004b) depending on the agro-ecosystem and the production system Year of release 2022 The initial year of introducing Brachiaria brizantha 26,124 (A. Rincón, personal communication, February 12, 2021) cv. Agrosavia Caporal has been set for 2022, since AGROSAVIA is currently in the process of producing basic seed and in negotiations with seed companies in Brazil for seed production at a commercial level Effects on productivity (%) +14 Better animal response associated with the best Estimates according to agronomic and animal response trial characteristics in terms of nutritional quality and biomass data production of the new variety compared to traditional technologies in the region Changes in costs (%) 0 There are no changes in production costs associated with Information provided by livestock and forages experts the new material Probability of success of 80 As a basic scenario, the assumptions used in the model are Judgment of the researchers according to expert opinion research (%) expected to be fulfilled by 80% regarding the success of other research programs in other countries and regions Discount rate (%) 12 Social rate recommended by the National Planning DNP (2013) Department for public investment projects in Colombia Adoption profile Logistic adoption Behavior of the adoption-diffusion process of agricultural Alston et al. (1995) curve technologies Initial adoption rate (%) 0.001 A logistical distribution is assumed Alston et al. (1995) Maximum expected 2.22 Percentage of area grown with Brachiaria brizantha in the Labarta et al. (2017) adoption rate (%) - Regional Colombian Orinoquía region Maximum expected 2.8 Percentage of area grown with Brachiaria brizantha in Labarta et al. (2017) adoption rate (%) - National Colombia forrajeros para integrarlos a los sistemas de producción ganaderos TABLE 4 | Scenarios for the sensitivity analysis of the economic surplus model for de la Orinoquía, financed by the Colombian Ministry of Brachiaria brizantha 26,124 cv. Agrosavia Caporal. Agriculture and Rural Development (MADR), and executed by Scenario Regional National AGROSAVIA and the International Center for Tropical P B O P B O Agriculture (CIAT). In this project, 58 forage accessions were evaluated in the Orinoquía region in order to identify five Changes in productivity (%) 10 14 20 10 14 20 Probability of success (%) 70 80 100 70 80 100 promising varieties adapted to the local edaphoclimatic Expected final adoption rate (%) 1.11 2.22 3.33 1.4 2.8 4.2 conditions. The R&D period was 5 years, from 2011 to 2015. The project had an annual budget of US$65,000, where 30% was P: pessimistic scenario; B: basic scenario; O: optimistic scenario. allocated for the evaluation of Agrosavia Caporal. This included Frontiers in Environmental Science | www.frontiersin.org 277 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía FIGURE 1 | Effects of technological change at different scales: a) Production function (micro level); b) Producer and consumer surplus (macro level). Source: Adapted from Alston et al. (1995, 206). operational expenses for the establishment, maintenance and technological innovations, the individual decision-making evaluation of the trials, such as agricultural inputs, agricultural process about the acceptance of a previously unknown services (e.g., labor for field work), equipment and machinery, innovation, which implies learning through the acquisition of transportation, travel expenses, and laboratory analysis. information and its incorporation into the production function. Personnel requirements were estimated from the percentages of On the other hand, diffusion refers to the process of acceptance of time devoted by scientists, researchers, technicians and workers in a a technology by a set of individuals in time and for a given region process of improvement by selection. This process consists of five (Rogers, 2003). main stages: 1) evaluation of the visual characteristics of the materials Empirical evidence on adoption/diffusion processes of new (height, coverage, dynamometer, vigor, pests and diseases); 2) agricultural technologies shows that it normally follows a logistic evaluation of visual characteristics, dry matter production (DM) or sigmoid pattern (Mansfield, 1961; Mahajan and Peterson, and nutritional quality (e.g., protein content, digestibility, neutral 1985). On the subject of pastures, although literature is scarce, detergent fiber) of the pre-selected materials in (i); 3) evaluation of the studies of Jarvis (1981) confirm that adoption adjusts to a plant-animal interaction of the materials identified in (ii), which are logistic model, meaning that the adoption curve is characterized established on a larger scale to determine palatability, material by three stages: 1) early adoption, 2) exponential growth, and 3) persistence and animal productivity (meat or milk); 4) evaluation the transition phase. In the first stage, the technology has a low of the plant-animal interaction of the materials identified in (iii); and adoption rate since only the least risk averse producers, or in 5) establishment of the selected materials in different locations other words, those who are more innovative, decide to invest in a depending on whether they are for release at the regional or new technology (in our case a new forage variety). After that, the national level. Prior to these stages, the costs associated with benefits of the new technology begin to be known and a stage of processes of application, reception, and field establishment of the rapid growth starts, characterized in turn by two sub-stages (2a) seed for multiplication, as well as institutional costs and equipment an early majority and (2b) a late majority. In the latter stage, depreciation were also included. The total duration of the evaluation adoption continues to grow, but each time at lower rates, as the process was five consecutive years (2011–2015). Since 2016, some process approaches its upper limit. evaluations have continued, mainly at the Taluma experimental To estimate the adoption curve, we make use of ex-post data on station, with an approximate annual budget of US$2,708. This the adoption of varieties similar to the new Agrosavia Caporal. Data includes the costs associated with the maintenance of the trials were obtained froma nationally representative adoption study carried and administrative expenses. In the years 2014–2016, out by Labarta et al. (2017) inColombia. Their results indicate that 2.2 multiplication of basic seed was carried out CIAT’s facilities in and 2.8% of the total area, respectively at regional and national levels, Palmira, Colombia, and the associated costs were also included. are planted with the variety Brachiaria brizantha cv. La Libertad. The total estimated R&D cost for the variety was estimated with Considering that this grass was introduced to the country 50 years US$563,243. ago, it is plausible to assume that the adoption-diffusion process is already in amaturation stage. This rate is considered, therefore, as the Technology Adoption and Diffusion maximum level of adoption for the basic scenario. For the pessimistic Before any economic impact associated with technical change can and optimistic scenarios, we expect the adoption rate to be 50% occur, a process of adoption and diffusion of the new technology below/above the maximum adoption rate expected for the basic needs to happen. By adoption we mean, in the context of scenario, indicating aminimum rate of 1.11% and amaximum rate of Frontiers in Environmental Science | www.frontiersin.org 288 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía FIGURE 2 | Adoption curves at the regional level for the basic, optimistic and pessimistic scenarios of the economic surplus model. TABLE 5 | Costs and income for cattle raising and fattening under both evaluated technologies. Parameter Brachiaria brizantha 26,124 Brachiaria decumbens cv. Agrosavia caporal (reference technology) Investment costs Establishment (US$ ha−1) 341 306 purchase of animals (US$ ha−1 cycle−1) 284 244 Operational costs Maintenance costs (US$ ha−1)1 182 182 Permanent labor (US$ ha−1 yr−1)2 89 84 Animal health (US$ ha−1 yr−1) 6.51 5.56 Supplementation (US$ ha−1 yr−1)3 14.1 12.03 Other costs 8.60 7.93 Gross income (average US$ ha−1 yr−1) 583 456 Unit cost of production (average US$ kg−1)4 1.027 1.029 Net income (average US$ ha−1 yr−1)5 112 94 1Maintenance is carried out every 2 years and includes weed control, fertilizing with half the dose used for establishment; 2Estimated: 2.5 permanent jobs required for every 100 animals in a cattle raising and fattening system (FEDEGAN, 2003), and a legal minimum wage in force plus benefits in 2020 of US$375. 3Supplementation with mineralized salt at a rate of 50 g ha−1 d−1. 4Unit cost of production: dividing total cost of the product by total production. 5Net income: total income (sales price x yield) minus total costs. TABLE 6 | Profitability indicators of the simulation model. Decision criterion Indicator Brachiaria brizantha 26,124 Brachiaria decumbens cv. Agrosavia caporal (reference technology) NPV (US$) Meana 328 182 SDb 95 134 IC (95%)c (30)-622 (223)-509 IRR (%) Mean 21% 18% Payback period (years) Mean 5 5 aMean value of the NPV obtained in the simulation (5,000 iterations). bSD: Standard deviation of the NPV with respect to the mean value. cIC: Minimum and maximum values with a 95% confidence interval. Frontiers in Environmental Science | www.frontiersin.org 299 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía FIGURE 3 | Probability and accumulative density distributions of the NPV. FIGURE 4 | Tornado diagram showing contributions of random input variables to the variance of the NPV. 3.3% at the regional level, and a minimum rate of 1.4% and a The total period of diffusion and adoption is 27 years (2022–2048), maximum rate of 4.2% at the national level, respectively (Figure 2). In the maximum adoption rate will be reached in year 20 (2041), and both cases, the aim is to examine the changes in the net social benefits from there on, a constant behavior is assumed. when a successful dissemination process is assumed or when a process with serious difficulties is considered. However, much higher rates could be expected in an optimistic scenario, given RESULTS adoption rates for other Brachiaria species, such as Brachiaria dictyoneura cv. Llanero and Brachiaria decumbens, which register Cost-Benefit Analysis adoption levels of 10.7 and 12.87%, respectively (Labarta et al., 2017). Table 5 provides an overview on the per hectare costs and income Nevertheless, in order to avoid, as far as possible, the overestimation for both the Agrosavia Caporal and the reference technology. of potential benefits coming along with adopting the new Agrosavia Regarding the direct production costs, the purchase of animals, Caporal variety, we preferred to make more conservative estimates. pasture establishment and labor make up the highest shares. Frontiers in Environmental Science | www.frontiersin.org 130 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía TABLE 7 | Economic surplus model results (values in thousand US$). Level Scenario Change CS Change PS Change TS NPV IRR (%) B/C Regional B 1,184 1,979 3,165 903 19 8 O 2,540 4,246 6,786 1,573 20 18 P 444 742 1,186 -36 11 3 National B 7,115 11,893 19,008 5,087 26 50.3 O 15,261 25,508 40,768 11,342 30 108 P 1,905 3,184 5,089 1,085 19 13.5 CS: Consumer Surplus, PS: Producer Surplus, TS: Total Surplus. These three items participate with more than 80% of the total the results are similar to the ones at regional level, except that value. The unit cost per kilogram of beef produced was US$1.027 their magnitude is greater as a result of the increase in the for the Agrosavia Caporal variety and US$1.029 for the reference expected adoption rate and affected production volume. The technology. As a result of the better animal response indicators of distribution of benefits is concentrated on the producers, who the Agrosavia Caporal, the average gross income per year would receive 62.5% of the surplus. In the absence of increased by 28% and the net profit by 19%. international trade, the surplus production generated by the The summary of the main financial results of the simulation is use of the new variety must be absorbed by the domestic presented in Table 6. Under the assumptions used in this model, market. Given that the demand curve is elastic (ED 1.17), the Agrosavia Caporal proves to be financially profitable and allows new equilibrium point is reached through small price variations, the improvement of all risk and performance indicators when increasing beef sales and producer incomes significantly while compared to the reference technology. For Agrosavia Caporal, the reducing consumer prices. The increase in production and model estimates an average NPV of US$328 and an IRR to equity reduction in consumer prices, in particular, favor low-income of 21% per hectare. Regarding the probability of not obtaining consumers who are more sensitive to price changes and thus financial feasibility of the evaluated technologies, Figure 3 shows contribute to improving food and nutritional security of the the NPV indicator distributions, which reflect the amplitude of its population. variation. For the reference technology, the indicator could range Under the optimistic scenario, the new variety could achieve between US$-90 and US$540, with a probability of obtaining productivity increases of 16%, and cover 3.33% of the total negative values of 13%. For Agrosavia Caporal, the improvement Orinoquía region, respectively 4.2% of the national territory, in productivity allows a shift to the right of the distribution curve, leading to expected benefits of US$6,786,000 and US$40, 768, reducing the probability of losses to 0%, with values ranging from 000, respectively. Under this scenario, the investments in the US$52 to 708. development of Agrosavia Caporal would be very profitable, since The contribution of the input variables to the NPV variance is the IRR would be >30% and the benefit/cost ratio would indicate shown in the tornado diagram in Figure 4. The correlation that around US$108 are generated from every US$ invested. coefficients calculated between the input values and the NPV Under the pessimistic scenario, changes in yields of 12%, a variance show that profitability is affected mainly by two regional adoption rate of 1.11% and a probability of success of variables: liveweight gain and beef sales price. Increases in 70% were considered, which would yield total benefits of these variables have a positive effect on the variability of the US$1,186,000 for the Orinoquía region. Likewise, the indicator as follows: changes in the animal productivity variable estimated profitability would be 11% and thus lower than the modify the variance of the indicator by 89 and 90% for the new social discount rate of 12%, meaning that the total surpluses variety and the reference technology, respectively. Similarly, generated at the regional level would not be sufficient to changes in the beef sales price lead to changes in the variance compensate the spent R&D costs. These results show a latent of 9 and 6%, respectively. Under the reference price of risk that the R&D investment spent for developing the material US$1.24 kg−1, animal productivity below 0.174 tons ha−1 year−1 might not exceed the additional benefits and, therefore, in such (equivalent to a live weight gain of 126 kg AU−1 year−1) are not scenario, an investment would not be recommended. For an profitable for Agrosavia Caporal. Under the same reference price, investment to become socially and economically profitable, a the threshold for the base technology is a productivity level of series of requirements must be met that go beyond the R&D 0.155 tons ha−1 year−1 (equivalent to a live weight gain of 129 kg phase and the release of a material with outstanding AU−1 year−1). characteristics, such as the development of efficient technology promotion and dissemination strategies (including the Economic Surplus Model availability of commercial seed, distribution networks, The results of the economic surplus model are presented in communication strategies and competitive costs) that lead to Table 7. At both the regional and national levels, the potential both higher adoption levels than the projected 1.11% and benefits of Agrosavia Caporal are positive in the three analyzed productivity changes superior than 12%. In addition, since a scenarios. Under the basic scenario, at the regional level, a total probability of success of >70% is necessary, it is important that benefit of US$3,165,000 is estimated, which represents an internal the developed technologies, in addition to their differentiating social rate of return on investments of 19%. At the national level, technical characteristics, are cost efficient and provide sufficient Frontiers in Environmental Science | www.frontiersin.org 131 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía TABLE 8 | Heat map for the sensitivity of the IRR (total surplus basis) with respect to changes in the adoption rate and productivity level. Adoption rate (regional level) Change in productivity 18.8% 1% 2% 3% 4% 5% 6% 7% 8% 9% 10% 5% 8.9% 12.5% 14.7% 16.3% 17.5% 18.6% 19.5% 20.3% 21.0% 21.7% 10% 12.5% 16.3% 18.6% 20.3% 21.7% 22.8% 23.8% 24.7% 25.5% 26.2% 15% 14.7% 18.6% 21.0% 22.8% 24.3% 25.5% 26.5% 27.4% 28.2% 28.9% 20% 16.3% 20.3% 22.8% 24.7% 26.2% 27.4% 28.5% 29.4% 30.2% 31.0% Adoption rate (National level) Change in productivity 26% 1% 2% 3% 4% 5% 6% 7% 8% 9% 10% 5% 14.9% 18.3% 20.4% 22.0% 23.2% 24.2% 25.1% 25.8% 26.5% 27.1% 10% 18.3% 22.0% 24.2% 25.8% 27.1% 28.2% 29.1% 29.9% 30.7% 31.3% 15% 20.4% 24.2% 26.5% 28.2% 29.5% 30.7% 31.6% 32.5% 33.2% 33.9% 20% 22.0% 25.8% 28.2% 29.9% 31.3% 32.5% 33.4% 34.3% 35.1% 35.8% seed for multiplication. At the national level however, the IRR 79% increase of the NPV and a 16% increase of the IRR, would be 19% given the higher overall adoption and total respectively. With an average NPV of approximately US$328 production affected by potential yield increases, suggesting and an IRR of 21%, the technology appears as a viable alternative that the R&D investment would be profitable at the national to improve both efficiency and profitability of the region’s level–even under the pessimistic scenario. cattle farms. To verify the robustness of the estimates for impacts and Agrosavia Caporal also presents a reduction in the probability return on investment estimates, a sensitivity analysis was carried of obtaining economic losses (0 versus 13% for the reference out with respect to the reference scenario. In particular, the technology), resulting from its higher productivity and lower variables of maximum expected adoption rate and productivity yield variability (between 199 and 262 kg ha−1 year−1). This is level were examined. Table 8 shows heat maps corresponding to essential for regions such as the Orinoquía, where high water the changes of these variables and their effects on the IRR under seasonality affects cattle production and the general availability of basic scenario assumptions (probability of success of 80%, 2.8% food. The region is projected to experience important difficulties adoption rate at regional and 2.2% at national level, respectively). due to climate change, with reductions in annual precipitation as The results suggest that, at the regional level, the technology is well as increases in maximum temperatures (IDEAM et al., 2015). profitable when productivity increases greater than 5% occur and These increasing risks, coupled with changes in market with an adoption rate of 1%. Although the results of the analysis conditions (e.g., sales and input price variations), substantially are clearly sensitive to these two variables, investing in this affect long-term investment decisions at the producer level, such alternative is highly profitable under most of the assigned values. as the adoption of new technologies. In this sense, forages that can guarantee a lower risk–such as Agrosavia Caporal–provide additional incentives for adoption (Marra et al., 2003). It is DISCUSSION important to note that for both evaluated technologies, the productivity parameters used assume adequate pasture The material Brachiaria brizantha 26,124 cv. Agrosavia Caporal management. Inadequate management will inevitably translate was identified as a promising variety for release, given its good into pasture degradation and affect the feasibility of the system, characteristics in terms of nutritional quality, biomass production undermining the technology’s potential as a promising material and persistence during dry season. Planting the variety leads to and affecting the environment by increasing carbon dioxide beef yield increases of around 14% when compared to Brachiaria (CO2) emissions. According to Rincón (2006), degraded decumbens (reference technology). This is consistent with the pastures in the region cause a reduction in beef and dairy findings of Pardo and Pérez (2010), and Lascano et al. (2002), production of more than 50%, directly associated with a loss who have shown the potential of integrating new Brachiaria of biomass production, soil compaction, weed invasion and brizantha accessions in different areas of the Colombian erosion, among others, making it essential to provide training Orinoquía to increase cattle productivity. These studies to the primary producer through specific extension and conclude that, compared to traditional technologies, the new technology transfer programs, focusing i.e., on establishing and accessions allow increasing meat production per hectare between maintaining the pasture. 9 and 100%. According to our results, the higher productivity can Despite the previously mentioned benefits, pastures under improve the net returns of beef cattle production at a farm level by monoculture remain significantly exposed to changes in an average of 19%, as consequence of higher daily live weight production and quality throughout the year (Tedonkeng et al., gains, which reduce the length of the fattening cycle and generate 2007). The association of improved grass varieties with trees and faster and more frequent income flows. This translates into better legumes should be promoted as a technological package, since financial indicators compared to the reference technology, with a they can reduce heat stress in animals, contribute to increasing Frontiers in Environmental Science | www.frontiersin.org 132 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía pasture persistence (due to nitrogen fixation) and improve the access to resources (e.g., credit, labor, level of wealth), making provision of ecosystem services (e.g., contribution of organic resource-rich producers the main group of potential adopters. Yet matter to pastures, improvement of soil quality and soil at the same time, when it comes to actual adoption, large producers carbon accumulation, temperature regulation) (Harrison et al., are described as less likely to adopt, presumably due to scale 2015; Reckling et al., 2016; Dubeux et al., 2017). Cohn et al. (2014) limitations, security concerns, and lack of infrastructure. To the found that policy instruments, such as taxes on cattle from above-mentioned considerations, a series of structural factors can be conventional systems or subsidies for production in diversified, added, such as land prices or local wage levels, that may or may not more sustainable systems, might be effective methods to promote encourage the adoption of improved forages in the region. such technological and cultural changes among farmers and Regarding environmental aspects, greenhouse gas emissions strengthen the long-term sustainability, while reducing and deforestation are the main concerns for the Orinoquía greenhouse gas emissions. cattle sector, with widespread adoption of improved forages At a macro level, the results from the economic surplus model potentially contributing to generating positive outcomes. But show that, on average, investing in the development of more these improved forages also pose additional challenges and productive forages, such as Agrosavia Caporal, can be highly risks. Cattle production is one of the main sources of profitable from a social point of view, given the significant greenhouse gas emissions, resulting from the ruminant digestion performance gains and the particular conditions of the cattle process that generates methane (CH4) and nitrous oxide emissions sector in both the Orinoquía and Colombia. We found that, if (CIAT and CORMACARENA, 2018). Higher quality forages allow adopted, the forecasted productivity increases obtained with increasing animal productivity and feeding efficiency (conversion Agrosavia Caporal could generate a shift in beef supply, of forage to animal protein), reducing CH4 emissions per unit of associated with significant economic benefits. The estimated NPV product (Knapp et al., 2014; Zubieta et al., 2021). Cardoso et al. of the social benefits for the period from 2022 to 2048 would be (2016) estimate that increased quality and quantity of forage can approximately US$903,000 and US$11.3 million at the regional and potentially decrease greenhouse gas emissions per kg carcass national levels, respectively. These results are consistent with other weight by 50%, principally resulting from a reduction of CH4 studies that evaluated the impact of improved forage varieties in the emissions. The expansion of areas for cattle production is one of country and identified internal social rates of return on investments the main drivers of deforestation, a process that also generates high of up to 100% (Vera et al., 1989; Rivas and Holmann, 2004a, 2004b). amounts of greenhouse gas emissions and is particularly The results of the economic surplus model depend mainly on the problematic in the Orinoquía region, which holds various key variables maximum expected adoption rate and productivity. Under ecosystems, such as natural savannas, flooded forests, humid the pessimistic scenario, with an adoption rate of <1.11% (equivalent forests or foothills (CIAT and CORMACARENA, 2018). In this to 144,000 ha in the Orinoquía) and yield increases of <10%, the regard, the effects of increasing productivity of agricultural systems R&D investment would become unfeasible at a regional level. This on forest conservation can be ambiguous: it can incentivize the has important implications both the R&D and dissemination expansion of production in the agricultural Frontier through the processes. The use of new forage varieties that do not provide clearing of forest areas, but it can also be used as an indirect tool to sufficient benefits at a social level may be economically feasible at reduce the pressure of expanding the agricultural Frontier, an idea a farm level but not justify a new R&D process. Even if reasonably known as the Borlaug effect. larger productivity and risk reduction gains were to be expected, a In the Orinoquía, the introduction of Brachiaria grasses since strong dissemination process should be ensured so that the expected the end of the 1960s (Brachiaria decumbens, Rincón et al., 2010) adoption levels can be reached. This includes a strong seed system has been a subject of debate, mainly in environmental terms. The that also focuses on communication, information and training. adoption of these varieties occurred spontaneously and massively Success in that regard will depend entirely on the capacity of and by the producers and was associated with several desirable traits coordination among institutions, which include actors from the that increased productivity, such as a high biomass production public, private andmixed sectors. To ensure adoption, other barriers and nutritional quality, adaptation to marginal lands and low that need to be addressed include the access to credit and inputs, land fertility soils (Rao et al., 1998). Different studies for the region tenure insecurity, market instability and inadequate infrastructure have reported that the adoption of Brachiaria varieties resulted in (e.g., Lapar and Ehui, 2004; Wunscher et al., 2004; Dill et al., 2015). productivity increases from 18 to 37 kg ha−1 year−1 (no adoption) Regarding the social distribution of potential benefits, our study to 294–402 kg ha−1 year−1 (with Brachiaria), resulting in shows that they are mostly concentrated in the primary sector important impacts at the productive, economic, environmental (supply side). Within the primary sector, it is not clear, however, and social levels (Pérez and Vargas, 2001; Rincón et al., 2010). how these benefits will be distributed among or concentrated within Positive impacts include the reduction of land degradation and different segments (e.g., small, medium or large producers). Given pressure on the native savanna, methane emissions reductions that the micro level analysis reveals that the investment can be due to increased feeding efficiency, greenhouse gas emissions feasible even at minimum scales (1 ha), and considering the reductions associated with native savanna burning (Smith et al., producer typology in the Orinoquía (53.4% of the producers have 1997), better soil cover and improved soil quality parameters <50 animals (ICA, 2020)), we assume a large share of the potential (better water infiltration and reduced soil erosion), and higher beneficiaries will be small producers. These results, however, may be nitrogen and carbon fixation to the soil (Boddey et al., 1998). ambiguous: Labarta et al. (2017) describe a direct relationship These positive impacts are, however, often conditioned to the between the adoption of improved forages in the region and the (proper) management of the pastures. Negative impacts are Frontiers in Environmental Science | www.frontiersin.org 133 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía mainly associated with the degradation of native savannas, threats in technological terms. Transaction costs that occur once the to biodiversity, soil erosion, deforestation for expanding grazing variety is released, i.e., related to its adoption, dissemination and areas and increased greenhouse gas emissions (Peñuela et al., promotion, and that are assumed by the private seed sector were 2011; Peñuela et al., 2014; CIAT and CORMACARENA, 2018). ignored in our study, since they are not part of the publicly- Various studies evaluated the conditions in which both scenarios funded R&D process. These simplifications can lead to an are more likely to occur. In Brazil (Cohn et al., 2014), and De overestimation of the estimated net benefits. To mitigate such Oliveira Silva et al. (2016) have estimated a large greenhouse gas limitations, we made conservative estimations based on expert mitigation potential through cattle ranching intensification when consultations. Our model does not consider additional benefits coupled with no deforestation scenarios, taxes on conventional that could derive from, e.g., an increase in milk production (since pastures and subsidies for semi-intensive systems. Some studies we evaluated the technologies in a dual-purpose system) and have found that land use changes derived from agricultural other technical parameters in the region (e.g., interval between intensification are strongly linked to the characteristics of a births, birth rates). Nevertheless, these could substantially particular area and the land tenure conditions. Decreasing increase the benefits of the new variety for the region. Hence, deforestation patterns were found when intensification occurs research should be conducted to quantify such additional in consolidated agricultural regions, and increasing deforestation benefits. when it occurs on marginal lands (Maertens et al., 2006; Barretto As mentioned before, the variety Agrosavia Caporal is the third et al., 2013) and land with unclear land tenure (Kubitza et al., Brachiaria brizantha variety released in the area after Toledo and La 2018). A meta-study of 60 cases conducted by Rasmussen et al. Libertad. These cultivars, together with the new variety, are materials (2018) found that there are scant cases where agricultural with characteristics superior to the traditional technology intensification has had simultaneously a positive effect on predominantly used in the area (Brachiaria decumbens). There well-being and ecosystem services. These studies suggest that are, however, differences between them in both desirable forage holding the sustainability claims of cattle ranching intensification characteristics and limitations. Toledo, for example, has shown to would likely require a combination of various policy and market present better dry matter yields compared to Agrosavia Caporal mechanisms, such as effective monitoring and control, law (Lascano et al., 2002), and better characteristics in terms of tolerance enforcement, taxes, subsidies and land tenure rights, among to humidity, recovery after grazing, and vigor of the plant compared others. In areas where land is not a constraining factor, as is to La Libertad (Lascano et al., 2002). Agrosavia Caporal, on the other the case of the Colombian Orinoquía, there is a greater pressure to hand, has shown resistance to different species of spittlebug, while expand, making this a major threat and topic to consider. While Toledo and La Libertad are more susceptible (Lascano et al., 2002), there are initiatives in the country seeking to prevent and has better palatability and drought tolerance in the dry season (A. deforestation derived from the cattle sector (such as the Rincón, personal communication, August 06, 2021). In this sense, National Zero Deforestation Agreements), it is still too early to they are materials with differentiating characteristics that could also provide evidence that can support their effectiveness, and further have different economic impacts associated with their adoption. It is research is advised. recommended, therefore, to evaluate each of these technologies to As mentioned in the methodology section, our evaluation is determine their viability in terms of R&D and to identify the forage based on a partial equilibrium model and does therefore neither attributes that could have the greatest economic impact. include potential impacts on other economic sectors nor on natural resources. Our study demonstrates, however, the importance of new pasture technologies, their high potential to CONCLUSION produce social benefits, and the need to develop mechanisms to take advantage of this potential. Both our study and other Our study shows the economic feasibility both at the primary previously conducted ex-ante studies (reviewed at the producer level and at the social level of adopting a new forage beginning of this document), were carried out after the technology with superior productive characteristics. The new investments in R&D have already happened and just before Agrosavia Caporal variety, which will be released in 2022, the release of the particular technology. It is recommended, shows very good animal response parameters that increase the however, to conduct such studies before making decisions on economic viability of cattle raising and fattening systems in the R&D investments, so that the results can serve in the decision- Colombian Orinoquía region. At the social level, technology making process and for the allocation of ever scarce funds. adoption could generate an outward shift in the supply of Despite this, our results still provide insights into the potential meat, which would be associated with important benefits at benefits at the regional level and serve for justifying future R&D both the regional and national levels. However, the potential processes of new forage varieties for other regions of the country. success of Agrosavia Caporal, as well as of other potential new When interpreting our results, it is important to bear in mind that varieties with superior characteristics, is highly conditioned to the the economic surplus model used is a minimum data approach adoption level and to proper technology management that allows that simplifies reality. Given data limitations, production maintaining expected productivity levels. Therefore, it is essential estimates affected by technical change are based on average to develop adequate support mechanisms during the release and yields at the regional and national levels. Likewise, the model adoption process, in order to provide farmers with solid extension assumes that yield increases are the same for all producers, strategies and training programs that focus, for example, on without considering existing heterogeneities among them, e.g., planting and cultivar management. Likewise, it is crucial that Frontiers in Environmental Science | www.frontiersin.org 134 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía commercial seed availability of the material is guaranteed in the restricted. Requests to access these datasets should be directed to release, adoption and diffusion processes. SB, s.burkart@cgiar.org The cattle sector in the Colombian Orinoquía region is not only important at an economic or social level but also plays a significant role at an environmental level. It is recognized for being one of the AUTHOR CONTRIBUTIONS main contributors to the country’s greenhouse gas emissions, and one of the main drivers of deforestation, affecting the different SB, KE, AC, and ARC: Conceptualization. KE, AC, ARC, and SB: strategic ecosystems present in the Orinoquía. The sector is also Methodology. KE, AC, and ARC: Formal analysis. KE, AC, ARC, highly dependent on and affected by water seasonality, a situation and SB:Writing the original draft and review and editing. AC, KE, that could further aggravate under the forecasted climate change ARC, and SB: Resources. SB: Supervision and funding scenarios for the region. Sustainable intensification of the cattle acquisition. SB: Project administration. All authors contributed sector is considered to be the route to reducing negative to the article and approved the submitted version. environmental impacts while improving per area productivity, and forages with superior characteristics play an important role in this sense. The inclusion of trees and legumes in cattle systems, FUNDING which improve the provision of ecosystem services and animal welfare, however, should be considered as add-on in order to This work was funded by the CGIAR Research Program on move towards more sustainability and away from grass Livestock and by the Colombian Ministry of Agriculture and monocultures. The superior nutritional characteristics of Rural Development (MADR). The funders had no role in the Agrosavia Caporal can have positive effects on the environmental design of the study; in the collection, analyses, or interpretation of impacts of the local cattle systems. Reduced CH4 emissions and the data; in the writing of the manuscript, or in the decision to release of areas can be expected, given the higher intensification and publish the results. better digestibility. In order to achieve the economic, social and, above all, the environmental benefits of this new technology, coordinated efforts of the involved actors will be required. ACKNOWLEDGMENTS Extension campaigns need to provide information on the importance of sustainable intensification (focused on liberating This workwas carried out as part of theCGIARResearch Programon areas for conservation) and conserving strategic ecosystems Livestock. We thank all donors who globally support our work present in the region. Public policies and monitoring systems are through their contributions to the CGIAR System. The views needed in order to prevent an unwanted spread of the new expressed in this document may not be taken as the official views technology (and any other new technology in the future) to of these organizations. CGIAR is a global research partnership for a protected areas or ecosystems of the region. food-secure future. Its science is carried out by 15 Research Centers in close collaboration with hundreds of partners across the globe. This work was conducted as part of the project Evaluación y desarrollo de DATA AVAILABILITY STATEMENT materiales forrajeros para integrarlos a los sistemas de producción ganaderos de la Orinoquía, conducted under the cooperation The data analyzed in this study is subject to the following licenses/ agreement between AGROSAVIA (before CORPOICA) and restrictions: Data is from another project/institution and still CIAT, and funded by MADR. REFERENCES CIAT (1991). Annual Report Tropical Pastures Program 1987-1991. Cali, Colombia: Centro Internacional de Agricultura Tropical (CIAT). Available at: https://hdl.handle.net/10568/69061. Alston, J. M., Norton, G., and Pardey, P. (1995). Science under Scarcity: Principles CIAT and CORMACARENA (2018). Plan regional integral de cambio climático and Practice for Agricultural Research Evaluation and Priority Setting. New para la Orinoquía. CIAT publicación No. 438. Cali, Colombia. Centro York: Cornell University Press. Internacional de Agricultura Tropical (CIAT). Barretto, A. G. O. P., Berndes, G., Sparovek, G., and Wirsenius, S. (2013). CIAT (1997). Gramíneas y leguminosas tropicales: Optimización de la diversidad Agricultural Intensification in Brazil and its Effects on Land-Use Patterns: genética para usos múltiples (Proyecto IP-5). Informe Anual 1997. Cali, an Analysis of the 1975-2006 Period. Glob. Change Biol. 19 (6), 1804–1815. Colombia: Centro Internacional de Agricultura Tropical (CIAT). Available doi:10.1111/gcb.12174 at: https://hdl.handle.net/10568/69061. Boddey, R. M., Rao, I., and Thomas, R. J. (1998). “Reciclaje de nutrimentos e CIAT (1999). Gramíneas y leguminosas tropicales: Optimización de la diversidad impacto ambiental de las pasturas de Brachiaria,” in Brachiaria: Biología, genética para usos múltiples (Proyecto IP-5). Informe Anual 1999. Cali, Agronomía Y Mejoramiento. Colombia: Centro Internacional de Agricultura Colombia: Centro Internacional de Agricultura Tropical (CIAT). Available Tropical (CIAT); Campo Grande, Brazil: Empresa Brasileira de Pesquisa at: https://hdl.handle.net/10568/69061. Agropecuaria (EMBRAPA). Editors J. W. Miles, B. L. Maass, and CIAT (2001). Tropical Grasses and Legumes: Optimizing Genetic Diversity for C. B. do. Valle. Cali. Available at: https://hdl.handle.net/10568/54362. Multipurpose Use (Project IP-5). Annual Report 2001. Cali, Colombia: Centro Cardoso, A. S., Berndt, A., Leytem, A., Alves, B. J. R., de Carvalho, I. d. N. O., de Internacional de Agricultura Tropical (CIAT). Available at: https://hdl.handle. Barros Soares, L. H., et al. (2016). Impact of the Intensification of Beef net/10568/69061. Production in Brazil on Greenhouse Gas Emissions and Land Use. Agric. Cohn, A. S., Mosnier, A., Havlík, P., Valin, H., Herrero, M., Schmid, E., et al. (2014). Syst. 143, 86–96. doi:10.1016/j.agsy.2015.12.007 Cattle Ranching Intensification in Brazil Can Reduce Global Greenhouse Gas Frontiers in Environmental Science | www.frontiersin.org 135 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía Emissions by Sparing Land from Deforestation. Proc. Natl. Acad. Sci. 111 (20), Labarta, R., Martinez, J. M., Yaccelga, A., Reyes, B., Gomez, L., Maredia, M., et al. 7236–7241. doi:10.1073/pnas.1307163111 (2017). Assessing the Adoption and Economic & Environmental Impacts of DANE (2021). Censo sacrificio de Ganado total y departamental -vacunos, porcinos Brachiaria Grass Forage Cultivars in Latin America Focusing in the Experience y otras especies enero -diciembre 2020. Bogotá DC, Colombia: Departamento of Colombia SPIA Technical Report. Rome, Italy: Standing Panel for Impact Nacional de Estadística. Available at: https://www.dane.gov.co/index.php/ Assessment (SPIA). estadisticas-por-tema/agropecuario/encuesta-de-sacrificio-de-ganado. Lapar, M. L. A., and Ehui, S. K. (2004). Factors Affecting Adoption of Dual- Dane-Cna (2014). Censo Nacional Agropecuario 2014, Bogotá D.C., Colombia. Purpose Forages in the Philippine Uplands. Agric. Syst. 81 (2), 95–114. Available at: https://www.dane.gov.co/index.php/estadisticas-por-tema/ doi:10.1016/j.agsy.2003.09.003 agropecuario/censo-nacional-agropecuario-2014. Lascano, C., Pérez, R., Plazas, C., Medrano, J., Pérez, O., and Argel, P. J. (2002). de Oliveira Silva, R., Barioni, L. G., Hall, J. A. J., Folegatti Matsuura, M., Zanett Pasto Toledo (Brachiaria brizatha, CIAT 26110). Gramínea de crecimiento Albertini, T., Fernandes, F. A., et al. (2016). Increasing Beef Production Could vigoroso para intensificar la ganadería colombiana. Villavicencio, Meta. Lower Greenhouse Gas Emissions in Brazil if Decoupled from Deforestation. Colombia: Corporación Colombiana de Investigación Agropecuaria Nat. Clim Change 6 (5), 493–497. doi:10.1038/nclimate2916 (CORPOICA); Cali, Colombia: Centro Internacional de Agricultura Tropical Dill, M. D., Emvalomatis, G., Saatkamp, H., Rossi, J. A., Pereira, G. R., and (CIAT). Available at: https://hdl.handle.net/10568/54199. Barcellos, J. O. J. (2015). Factors Affecting Adoption of Economic Management Maertens, M., Zeller, M., and Birner, R. (2006). Sustainable Agricultural Practices in Beef Cattle Production in Rio Grande Do Sul State, Brazil. J. Rural Intensification in forest Frontier Areas. Agric. Econ. 34 (2), 197–206. Stud. 42, 21–28. doi:10.1016/j.jrurstud.2015.09.004 doi:10.1111/j.1574-0864.2006.00118.x DNP (2013). Manual de soporte conceptual metodología general para la Mahajan, V., and Peterson, R. (1985). Models for Innovation Diffusion. California: formulación y evaluación de proyectos. (Departamento Nacional de SAGE Publications, Inc. doi:10.4135/9781412985093 Planeación). Colombia: Bogotá. Mansfield, E. (1961). Technical Change and the Rate of Imitation. Econometrica 29 Dubeux, J. C. B., Jr, Blount, A. R. S., Mackowiak, C., Santos, E. R. S., Pereira Neto, (4), 741–766. doi:10.2307/1911817 J. D., Riveros, U., et al. (2017). Biological N2 Fixation, Belowground Responses, Maredia, M. K., Shankar, B., Kelley, T. G., and Stevenson, J. R. (2014). Impact and Forage Potential of Rhizoma Peanut Cultivars. Crop Sci. 57 (2), 1027–1038. Assessment of Agricultural Research, Institutional Innovation, and Technology doi:10.2135/cropsci2016.09.0810 Adoption: Introduction to the Special Section. Food Policy 44, 214–217. Elbasha, E., Thornton, P. K., and Tarawali, G. (1999). An Ex-post Economic doi:10.1016/j.foodpol.2013.10.001 Assessment of Planted Forages in West Africanet/10568/502. ILRI Impact Marra, M., Pannell, D. J., and Abadi Ghadim, A. (2003). The Economics of Risk, Assessment Series. No. 2. Nairobi (Kenya): International Livestock Research Uncertainty and Learning in the Adoption of New Agricultural Technologies: Institute. where Are We on the Learning Curve? Agric. Syst. 75 (2–3), 215–234. FAO (2018). World Livestock: Transforming the Livestock Sector through the doi:10.1016/S0308-521X(02)00066-5 Sustainable Development Goals. Rome: FAO. Available at: http://www.fao. Miles, J. W., Maass, B. L., and do Valle, C. B. (1996). Brachiaria: Biology, Agronomy org/3/CA1201EN/ca1201en.pdf. and Improvement. Cali, Colombia. Centro Internacional de Agricultura Fedegan (2018). Ganadería Colombiana Hoja De Ruta 2018 – 2022. Editor Tropical. (CIAT); Campo Grande, Brazil: Empresa Brasileira de Pesquisa D. C. Bogotá (Colombia. Available at: https://www.fedegan.org.co/noticias/ Agropecuaria (EMBRAPA) Available at: https://hdl.handle.net/10568/54362. ganaderia-colombiana-hoja-de-ruta-2018-2022. Pamo, E. T., Boukila, B., Fonteh, F. A., Tendonkeng, F., Kana, J. R., and Nanda, A. S. FEDEGAN (2003). Índice de costos ganaderos diciembre 2002 – marzo 2003. Carta (2007). Nutritive Value of Some Grasses and Leguminous Tree Leaves of the Fedegán Magazine No. 79. Bogotá, Colombia: Federación Colombiana de Central Region of Africa. Anim. Feed Sci. Technology 135 (3–4), 273–282. Ganaderos, 17–32. doi:10.1016/j.anifeedsci.2006.07.001 Fedegan (2019a). Producción de carne- Colombia. Editor D. C. Bogotá (Colombia. Pardo, O., and Pérez, O. (2010). “Alternativas forrajeras para los Llanos Orientales Available at: http://www.fedegan.org.co/estadisticas/produccion-0. de Colombia,” in Establecimiento. manejo y utilización de recursos forrajeros en FEDEGAN (2019b). Precio promedio de ganado gordo en pie Colombia: Precio de sistemas ganaderos de suelos ácidos. Colombia: Corporación Colombiana de referencia. Editor D. C. Bogotá (Colombia. Available at: http://www.fedegan. Investigación Agropecuaria (CORPOICA). Editors A. Rincón and org.co/estadisticas/precios. C. A. Jaramillo. Villavicencio. Harrison, M. T., Mcsweeney, C., Tomkins, N. W., and Eckard, R. J. (2015). Park, C. S. (2007). Contemporary Engineering Economics. 4th Edn. New Jersey: Improving Greenhouse Gas Emissions Intensities of Subtropical and Prentice-Hall. Tropical Beef Farming Systems Using Leucaena Leucocephala. Agric. Syst. Peñuela, L., Fernández, A. P., Castro, F., and Ocampo, A. (2011). Uso y manejo de 136, 138–146. doi:10.1016/j.agsy.2015.03.003 forrajes nativos en la sabana inundable de la Orinoquía. Convenio de ICA (2020). Censo Pecuario Año 2019. Bogotá D.C., Colombia. Instituto Colombiano cooperación interinstitucional entre The Nature Conservancy (TNC) y la Agropecuario. Available at: https://www.ica.gov.co/areas/pecuaria/servicios/ Fundación Horizonte Verde (FHV) con el apoyo de la Fundación epidemiologia-veterinaria/censos-2016/censo-2020/bovinos-censo-2020.aspx. Biodiversidad de España y la Corporación Autónoma Regional de la IDEAM, PNUD, MADS, DNP, CANCILLERÍA (2015). Nuevos escenarios de Orinoquía (CorpOrinoquía). cambio climático para Colombia 2011– 2100 Herramientas Científicas para Peñuela, L., Solano, C., Ardila, V., and Galán, S. (Eds.) (2014). “Fortalecimiento la Toma de Decisiones – Enfoque Nacional – Departamental: Tercera institucional y de politica para incrementar la conservación de la biodiversidad Comunicación Nacional de Cambio Climático. Bogotá, Colombia. Instituto en predios privados en Colombia”, in Grupo Colombiano Interinstitucional de de Hidrología, Meteorología y Estudios Ambientales de Colombia (IDEAM). Herramientas de Conservación Privada (G5): Asociación Red Colombiana de Ideam, P. N. U. D., Mads, D. N. P., and Cancillería (2016). Inventario nacional y Reservas Naturales de la Sociedad Civil (RESNATUR), Fundación Natura (FN), departamental de Gases Efecto Invernadero –Colombia. Tercera Comunicación World Wildlife Fund (WWF). Serie: Conservación de la biodiversidad en Nacional de Cambio Climático. Bogotá, Colombia: Instituto de Hidrología, predios productivos (Bogotá, Colombia: The Nature Conservancy (TNC), y Meteorología y Estudios Ambientales de Colombia (IDEAM). Parques Nacionales Naturales de Colombia (PNN)), 230. Jarvis, L. S. (1981). Predicting the Diffusion of Improved Pastures in Uruguay. Am. Peters, M., Herrero, M., Fisher, M., Erb, K.-H., Rao, I., Subbarao, G. V., et al. (2013). J. Agric. Econ. 63 (3), 495–502. doi:10.2307/1240540 Challenges and Opportunities for Improving Eco-Efficiency of Tropical Forage- Knapp, J. R., Laur, G. L., Vadas, P. A., Weiss, W. P., and Tricarico, J. M. (2014). Based Systems to Mitigate Greenhouse Gas Emissions. Trop. Grass - Forr Trop. Invited Review: Enteric Methane in Dairy Cattle Production: Quantifying the 1 (2), 156–167. doi:10.17138/TGFT(1)156-167 Opportunities and Impact of Reducing Emissions. J. Dairy Sci. 97 (6), Ramirez Hassan, A. (2012). A Multi-Stage Almost Ideal Demand System: The Case 3231–3261. doi:10.3168/jds.2013-7234 of Beef Demand in Colombia. SSRN Journal. doi:10.2139/ssrn.2193822 Kubitza, C., Krishna, V. V., Urban, K., Alamsyah, Z., and Qaim, M. (2018). Land Rao, I., Kerridge, P. C., and Macedo, M. C. M. (1998). “Requerimientos Property Rights, Agricultural Intensification, and Deforestation in Indonesia. nutricionales y adaptación a los suelos ácidos de especies de Brachiaria,” in Ecol. Econ. 147, 312–321. doi:10.22004/ag.econ.26116610.1016/ Brachiaria: Biología, Agronomía Y Mejoramiento. Colombia: Centro j.ecolecon.2018.01.021 Internacional de Agricultura Tropical (CIAT); Campo Grande, Brazil: Frontiers in Environmental Science | www.frontiersin.org 136 September 2021 | Volume 9 | Article 673481 Enciso et al. Forage Impact in the Orinoquía Empresa Brasileira de Pesquisa Agropecuaria (EMBRAPA). Editors J. W. Miles, Stads, G.-J., and Beintema, N. M. (2009). Investigación agrícola pública en América B. L. Maass, and C. B. do. Valle. Cali. Available at: https://hdl.handle.net/10568/ Latina y el Caribe: tendencias de capacidad e inversión. Washington: 54362. International Food Policy Research Institute. Available at: https://www.ifpri. Rao, I., Peters, M., Castro, A., Schultze-Kraft, R., White, D., Fisher, M., et al. (2015). org/node/2395. LivestockPlus - the Sustainable Intensification of Forage-Based Agricultural The World Bank (2008). World Development Report 2008Agriculture for Systems to Improve Livelihoods and Ecosystem Services in the Tropics. Trop. Development. Washington, DC: The World Bank. Grasslands - Forrajes Tropicales 3 (2), 59–82. doi:10.17138/TGFT(3)59-82 UPRA (2020). Análisis Situacional Cadena Cárnica V3. Bogotá D.C., Colombia. Rasmussen, L. V., Coolsaet, B., Martin, A., Mertz, O., Pascual, U., Corbera, E., Available at: http://www.andi.com.co/Uploads/20200914_PPT_Analisis_ Dawson, N., Fisher, J. A., Franks, P., and Ryan, C. M. (2018). Social-ecological Situacional_Carne_GrupoBase.pdf. Outcomes of Agricultural Intensification. Nat. Sustain. 1 (6), 275–282. UPRA (2019). Cadena productiva de ganadería bovina Línea Base de Indicadores de la doi:10.1038/s41893-018-0070-8 Cadena Láctea. Colombia: Bogotá D.C. Available at: https://www.upra.gov.co/ Reckling, M., Bergkvist, G., Watson, C. A., Stoddard, F. L., Zander, P. M., Walker, documents/10184/124468/LINEA+BASE+LECHE+PRUEBA.pdf/c5d3ec3f-4d8d- R. L., et al. (2016). Trade-offs between Economic and Environmental Impacts of 423e-82af-a0fdd0b15aeb?version1.0. Introducing Legumes into Cropping Systems. Front. Plant Sci. 7, 1–15. UPRA (2015a). Departamento de Arauca: Vocación de uso del suelo, cobertura de doi:10.3389/fpls.2016.00669 la tierra, zonificación para plantaciones forestales comerciales, tamaño de la Riesco, A., and Seré, C. (1985). ““Análisis económico de resultados de las pruebas propiedad, producción agrícola. Available at: https://sites.google.com/a/upra. de pastoreo” in Evaluación de pasturas con animales,” in Alternativas gov.co/presentaciones-upra/departamental/arauca. (Accessed January 25, metodológicas. Memorias de una reunión celebrada en Perú 1–5 de octubre, 2020). 1984. Editors C. Lascano and E. Pizarro (Cali, Colombia: Red Internacional de UPRA (2015b). Departamento de Vichada: vocación de uso del suelo, cobertura de Evaluación de Pastos Tropicales), 201–232. https://hdl.handle.net/10568/55923 las tierras, conflictos de uso, zonificación para plantaciones forestales Rincón, A., Bueno, G. A., Álvarez, M., Pardo, Ó., Pérez, O., and Caicedo, S. (2010). comerciales, suelos potenciales para adecuación de tierras, producción Establecimiento, manejo y utilización de recursos forrajeros en sistemas agrícola. Available at: https://sites.google.com/a/upra.gov.co/presentaciones- ganaderos de suelos ácidos. Villavicencio, Meta, Colombia: Corporación upra/departamental/vichada. (Accessed January 25, 2020). Colombiana de Investigación Agropecuaria (CORPOICA). Available at: UPRA (2015c). Departamento del Meta: Vocación de uso del suelo, Cobertura de las http://hdl.handle.net/20.500.12324/12703. tierras, Zonificación para plantaciones forestales comerciales, Suelos potenciales Rincón, A., Peters, M., Otoniel, P., Sotelo, M., Burkart, S., and Enciso, K. (2021). para adecuación de tierras, Producción agrícola. Available at: https://sites.google. Brachiaria brizanthaCIAT 26124: Gramínea forrajera para los sistemas ganaderos de com/a/upra.gov.co/presentaciones-upra/departamental/meta. (Accessed January la Orinoquia colombiana [Unpublished]. Corporación Colombiana de Investigación 25, 2020). Agropecuaria (AGROSAVIA),Ministerio de Agricultura yDesarrollo Rural (MADR), Vera, R. R., Seré, R. C., Toledo, J. M., Vera, R. R., Lascano, C. E., and Lenné, J. M. Centro Internacional de Agricultura Tropical (CIAT). (1989). Resultados obtenidos con Andropogon gayanus en las fincas de los Rivas, L., and Holmann, F. (2004b). Impacto de la adopción de híbridos de productores de ganado. Andropogon gayanus Kunth: Un pasto para los Brachiarias resistentes al salivazo: Colombia, México, y Centroamérica. Cali, suelos ácidos del trópico. Colombia: Centro Internacional de Agricultura Colombia. Centro Internacional de Agricultura Tropical (CIAT). Available at: Tropical), 323–355. https://hdl.handle.net/10568/1747. Wünscher, T., Schultze-Kraft, R., Peters, M., and Rivas, L. (2004). Early Adoption Rivas, L., and Holmann, F. (2004a). Impacto económico potencial de la adopción of the Tropical Forage Legume Arachis Pintoi in Huetar Norte, Costa Rica. Ex. de nuevas Brachiarias resistentes a cercópidos. Pasturas Tropicales 26 (3), Agric. 40 (2), 257–268. doi:10.1017/S0014479703001583 39–55. Available at: https://www.tropicalgrasslands.info/index.php/tgft/pages/ Zubieta, Á. S., Savian, J. V., de Souza Filho, W., Wallau, M. O., Gómez, A. M., view/Pasturas. Bindelle, J., et al. (2021). Does Grazing Management Provide Rogers, E. M. (2003). Diffusion of Innovations. New York: Free Press. Opportunities to Mitigate Methane Emissions by Ruminants in Pastoral Schiek, B., González, C., Mwendia, S., and Prager, S. D. (2018). Got Forages? Ecosystems? Sci. Total Environ. 754, 142029. doi:10.1016/ Understanding Potential Returns on Investment in Brachiaria Spp. For Dairy j.scitotenv.2020.142029 Producers in Eastern Africa. Trop. grassl.-Forrajes Trop. 6 (3), 117–133. doi:10.17138/TGFT(6)117-133 Conflict of Interest: The authors declare that the research was conducted in the Seré, C., Estrada, R., and Ferguson, J. (1993). Estudios de adopción e impacto en absence of any commercial or financial relationships that could be construed as a pasturas tropicales, investigación con pasturas en fincasCentro Internacional de potential conflict of interest. Agricultura Tropical (CIAT). Cali, Colombia. Available at: https://hdl.handle. net/10568/55753. Publisher’s Note: All claims expressed in this article are solely those of the authors Seré, C., and Estrada, R. (1982). “Análisis económico de sistemas de ceba en pastos and do not necessarily represent those of their affiliated organizations, or those of mejorados en los Llanos Orientales de Colombia,” in Referencias y ayudas the publisher, the editors and the reviewers. Any product that may be evaluated in utilizadas en el programa de capacitación científica en investigación para la this article, or claim that may be made by its manufacturer, is not guaranteed or producción y utilización de pastos tropicales. Cali, Colombia: Centro endorsed by the publisher. Internacional de Agricultura Tropical). Editor J. M. Spain, 1063–1075. Available at: https://hdl.handle.net/10568/54901. Copyright © 2021 Enciso, Charry, Castillo and Burkart. This is an open-access article SIPSA/DANE (2020). Data from: Series Históricas Componente Insumos. distributed under the terms of the Creative Commons Attribution License (CC BY). Available at: https://www.dane.gov.co/index.php/servicios-al-ciudadano/ The use, distribution or reproduction in other forums is permitted, provided the servicios-informacion/sipsa. original author(s) and the copyright owner(s) are credited and that the original Smith, J., Cadavid, J., Rincón, A., and Vera, R. (1997). Land Speculation and publication in this journal is cited, in accordance with accepted academic practice. Intensification at the Frontier: A Seeming Paradox in the Colombian savanna. No use, distribution or reproduction is permitted which does not comply with Agric. Syst. 54 (4), 501–520. doi:10.1016/S0308-521X(96)00088-1 these terms. Frontiers in Environmental Science | www.frontiersin.org 137 September 2021 | Volume 9 | Article 673481 PERSPECTIVE published: 22 September 2021 doi: 10.3389/fsufs.2021.725981 Promoting Forage Legume–Pollinator Interactions: Integrating Crop Pollination Management, Native Beekeeping and Silvopastoral Systems in Tropical Latin America Manuel Ernesto Narjes Sanchez 1,2, Juan Andrés Cardoso Arango 3 and Stefan Burkart 3* 1 The Alliance of Bioversity International-CIAT, Multifunctional Landscapes, Cali, Colombia, 2University of Hohenheim, Department of Production Theory and Resource Economics, Stuttgart, Germany, 3 The Alliance of Bioversity International-CIAT, Crops for Nutrition and Health, Tropical Forages Program, Cali, Colombia Major declines of insect pollinators are a worldwide concern. Such losses threaten human food supplies and ecosystem functions. Monocultures of pastures used to feed cattle are among the drivers of insect pollinator declines in Tropical Latin America. Plants of the legume family (fabaceae) are mostly pollinated by insects, in particular by bees. The inclusion of legumes in pastures (grass-legume system), as forage banks or the development of silvo-pastoral systems (SPS) with tree legumes, has been widely Edited by: promoted to improve livestock production and soil fertility, but not to enhance ecosystem Eduardo Vázquez, University of Bayreuth, Germany services from pollinators. Shortages of seed for the establishment of legumes as Reviewed by: forage banks or within pastures or SPS remain a bottleneck for the improvement of Marta Cecilia Telesnicki, ecosystem services brought about by pollinators within these systems and beyond. University of Buenos Aires, Argentina Bruce Ferguson, In this perspective paper, we provide an overview of forage legumes, their interplay El Colegio de la Frontera Sur, Mexico with pollinators, and the ecological and socio-economic benefits of pollinator–forage *Correspondence: legume interactions, at different scales (farm and landscape level). We further discuss Stefan Burkart the challenges and opportunities of scaling sustainably intensified cattle production s.burkart@cgiar.org systems that integrate legume forage-seed production with principles of pollinator Specialty section: ecology and native beekeeping. Finally, we provide interested stakeholders, policy-and This article was submitted to decision-makers with a perspective on how such agroecosystems may be designed and Climate-Smart Food Systems, a section of the journal scaled into multifunctional landscapes. Frontiers in Sustainable Food Systems Keywords: sustainable intensification, silvo-pastoral systems, cattle, forage legumes, meliponiculture, ecosystem Received: 16 June 2021 services, pollinators, nature-based solutions Accepted: 27 August 2021 Published: 22 September 2021 Citation: INTRODUCTION Narjes Sanchez ME, Cardoso Arango JA and Burkart S (2021) There is a growing demand for livestock products (Bernabucci, 2019). Intensification of cattle Promoting Forage Legume–Pollinator production systems (i.e., increase in production per unit of available resource) is proposed Interactions: Integrating Crop to meet market requirements (Sakamoto et al., 2020), increase economic returns and reduce Pollination Management, Native environmental impacts (Cassman and Grassini, 2020) including land use (Martha et al., 2012) and Beekeeping and Silvopastoral Systems in Tropical Latin America. greenhouse gas (GHG) emissions (Eckard et al., 2010; Herrero et al., 2013; Ruviaro et al., 2015; Front. Sustain. Food Syst. 5:725981. Cardoso et al., 2016). Traditionally, cattle production systems in Tropical Latin America rely on doi: 10.3389/fsufs.2021.725981 grazing animals that feed upon planted or naturalized pastures. For intensification in this region, Frontiers in Sustainable Food Systems | www.frontiersin.org 318 September 2021 | Volume 5 | Article 725981 Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions pastures tend to be dominated by a single species of a high governments, research institutions and academia to coordinate yielding grass (da Silva et al., 2020), and subject to practices the global implementation of the International Pollinator aimed to improve their productivity and nutritional quality. This Initiative (IPI) (FAO, 2021). The IPI’s plan of action offers includes aspects such as grazing management and the application guidelines for the improvement and development of practices of fertilizers, herbicides and pesticides (Gerssen-Gondelach et al., that promote the conservation and sustainable use of pollinator 2017). However, evidence indicates an association between diversity, restoring pollinator habitats in agriculture and related intensified pastures and biodiversity loss (Bobbink et al., 2010; ecosystems (Byrne and Fitzpatrick, 2009; CBD, 2018). Since Fontana et al., 2016), including the decline of insect pollinators its launch at the 5th COP of the Convention on Biological (Potts et al., 2010). Diversity in 2000, the IPI has catalyzed the development Insect pollinator decline is a major concern. Overcoming this and implementation of several other initiatives both at the declination is essential for global food security and ecosystem regional (e.g., the African Pollinator Initiative) and national (e.g., functioning (Van der Sluijs and Vaage, 2016; Van der Sluijs, the Brazilian and Colombian Pollinator Initiatives) levels. For 2020). The inclusion of legumes (fabacea) is a nature positive instance, the Colombian Pollinator Initiative (CPI) recognizes action to increase plant diversity within a pasture. Most legumes the contribution of pollination services to food security through are pollinated by insects (Suso et al., 2016), suggesting that the role pollinators play in the production of both crops and legume inclusion in pastures might provide ecosystem services livestock, also identifying the expansion of cattle ranching coming from pollination. Orford et al. (2016) showed thatmodest as a major threat to pollinator habitats (Nates-Parra, 2016), enhancements to pasture diversity can improve the provision building on a national strategy for the conservation and of pollination services to surrounding habitats. Furthermore, sustainable use of pollinators. Currently, Colombia’s National the inclusion of legumes brings other benefits to improve the Congress is considering a bill that establishes mechanisms for the efficiency and sustainability of cattle production systems (see conservation of pollinators and fosters the husbandry of native sustainable intensification of livestock production systems, Rao bee species. Although not explicitly stated in the CPI, its roadmap et al., 2015). Benefits of legumes introduction include: (1) presents an opportunity for pursuing synergies with Colombia’s increases in quantity and quality of livestock feed and (2) soil COP21 Nationally Appropriate Mitigation Actions (NAMA) for improvement as a result of biological nitrogen fixation, soil the cattle sector. stabilization and nutrient recycling (Schultze-Kraft et al., 2018). Aligning national and/or regional pollinator initiatives with There is a wide variety of legumes available for cattle production national efforts to reduce GHG emissions from cattle production (i.e., forage legumes). Forage legumes can be annual or perennial may contribute to the 2030 Agenda for Sustainable Development. plants with different growth habits and various forms (i.e., Pollinators can indeed be protected (i.e., UN-SDG 15: Life on herbaceous, shrub and tree legumes). The use of legumes in cattle land), by taking climate protection and adaptation concepts into production systems is not restricted to their inclusion in pastures account (i.e., UN-SDG 13: Climate action), while generating as a grass-legume system. They are also used as forage banks opportunities for employment and additional income in rural (i.e., plant material used to supplement animal diets) or within areas (i.e., UN-SDG 8: Decent work and economic growth) silvopastoral systems (SPS). and pursuing other sustainable development goals. Costa Rica’s SPS consist of diverse agroforestry arrangements that combine Cattle NAMA, for example, seeks to achieve an eco-competitive herbaceous plants, shrubs and trees for animal nutrition and sector that reconciles the goals of employment generation, complementary uses like timber or fruit production (Murgueitio biodiversity conservation and gender equality (UN-SDG 5) et al., 2011). In particular, SPS with tree legumes are a promising through the implementation of SPS (Ministerio de Agricultura nature-based solution to reduce the environmental impact of y Ganadería, 2019). It recently completed its pilot phase, cattle production, while increasing its productivity, especially which preceded a first scaling effort aimed at reaching 5% in Latin America (Dubeux et al., 2017; Chará et al., 2018; of Costa Rica’s cattle farms. By 2030, Costa Rica expects up- Landholm et al., 2019; Arango et al., 2020; Lira Junior et al., 2020). scaling to 27% of its farms (Climate Clean Air Coalition, SPS arrangements might be in the form of scattered trees in 2020). NAMAs are one of several public policies that have pastures, pastures within tree alleys, living fences and windbreaks seen advances promoting SPS as a silver-bullet solution for surrounding a pasture, to name a few (Murgueitio and Ibrahim, the sustainable intensification of the cattle sector, such as 2001; Murgueitio et al., 2011; Chará et al., 2018). SPS promote has been the case of Colombia (Ministerio de Agricultura biodiversity by creating complex habitats that support a diverse y Desarrollo Rural, 2019, 2020), Argentina (Presidencia de above-ground flora and fauna, harbor a richer soil biota and la Nación Argentina, 2018) and Costa Rica (Ministerio de improve connectivity between forest fragments (Ibrahim et al., Agricultura y Ganadería, 2011). A limited availability of 2006; Cubillos et al., 2016). At a landscape level, they provide legume seed, which depends on animal-mediated pollination more ecosystem services than open pastures (Calle et al., 2009; for its production, may nevertheless hamper scaling efforts Murgueitio et al., 2011). In Brazil, the conversion from pasture for sustainably intensified cattle systems and thus limit their monocultures to SPS has increased the abundance, richness and potential to deliver ecological, environmental and socioeconomic diversity of insects, including pollinators (Auad et al., 2015; Paiva benefits at larger scales (Rao et al., 2015; Rubyogo et al., 2019; et al., 2020). Arango et al., 2020). Through its Global Action on Pollination Services for This perspective paper provides an overview of forage Sustainable Agriculture, the FAO has joined efforts with legumes and agroecosystem management tools, available to Frontiers in Sustainable Food Systems | www.frontiersin.org 329 September 2021 | Volume 5 | Article 725981 Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions cattle systems for the conservation of insect pollinators, BENEFITS OF BEE POLLINATION ON optimization of crop-pollination services and tackling legume LEGUME SEED PRODUCTION forage-seed bottlenecks. We discuss the opportunities and challenges of integrating principles of pollinator ecology The role of pollination in legume seed formation and yield and native beekeeping into SPS and artisanal and large- depends on these plants’ species-specific reproductive systems. scale propagation of legume forage-seeds. Finally, we provide While many forage legumes require insects (i.e., bees) for their interested stakeholders, policy- and decision-makers with a pollination (i.e., out-crossing plants), others, including most perspective on how such agroecosystems may be designed tropical forage legumes, are self-pollinating (Kumar et al., 2020). as mosaics or scaled into multifunctional landscapes. This Many self-pollinating legumes, however, exhibit an increased article is structured as follows: The Forage Legume Seed seed formation when their flowers are visited by bees (Palmer Bottleneck section provides an overview on the limitation et al., 2009). that a forage seed bottleneck currently imposes on the With the exceptions of trees in SPS, both forage banks widespread adoption of SPS and grass-legume systems, and and grass-legume systems are intensively managed to minimize the role that pollinators can play in tackling this challenge. flowering of plants (i.e., no pollination service). In contrast, In Benefits of Bee Pollination on Legume Seed Production the set-up of legume seed production sites allows the creation section, we present a list of interventions that can be of gardens for wild and managed bees (i.e., both introduced, implemented at the farm and landscape levels. We continue such as Apis mellifera, and native). Tropical forage legumes in the Proposed Interventions Section discussing macro-level are numerous and highly diverse (see www.tropicalforages.info; conditions required to enable the implementation and guarantee Cook et al., 2020). The large diversity of tropical forage legumes the sustainability of the proposed interventions. Finally, the allows the design of diverse garden blends that can provide a Required Enabling (Macro) Conditions Section offers concluding rich source of nectar and pollen for bees. The inclusion of several remarks and recommendations. forage legumes for seed production can also support differences in flowering times, thereby offering foraging sites throughout the year for a higher bee diversity. Pollination gardens are a THE FORAGE LEGUME SEED doublee win, since they (i) enhance the abundance, diversity, BOTTLENECK and community composition of bees and other pollinators, whose populations are threatened to decline due to agricultural The benefits of introducing forage legumes into cattle production intensification (Kovács-Hostyánszki et al., 2017) and climate systems have been highlighted in numerous occasions (Schultze- change, especially in the tropics (Forrest, 2017); and (ii) increase Kraft et al., 2018 and references therein). However, widespread pollinator visitation rates of bees to legume flowers, resulting adoption of forage legumes in Tropical Latin America is in higher seed yields (Suso et al., 2016). Table 1 offers a list of very low (see Muir et al., 2017). Seed scarcity is one of the herbaceous and tree legumes known to be self-pollinated but with reasons limiting a wider use of forage legumes into cattle increased out-crossing when visited by different bee species. production systems in Tropical Latin America. This hinders the implementation of more sustainable, yet intensified, cattle PROPOSED INTERVENTIONS production systems in the region. Several projects, such as the Sustainable Colombian Cattle Project, support and promote the Table 2 presents various potential interventions at different use of SPS through establishing pilot/reference farms for scaling, levels (farm to landscape) and sectors (private and public) and although these projects have made significant advances, with the aim to promote the use of legumes as a nature- e.g., the establishment of 35,500 hectares of SPS in Colombia based solution that facilitate pollination services from insects, (Ganadería Colombiana Sostenible, 2018), once they end, a whilst allowing sustainable intensification of cattle production widespread adoption of these systems may be limited by legume systems. Furthermore, these interventions allow the creation seed scarcity. of seed production enterprises and different revenue avenues Even though there is a strong private tropical forage seed (e.g. meliponiculture). sector in Brazil and Mexico, its focus is set on Gramineae seed production, which leaves legume seeds largely neglected. This bottleneck could thus be tackled by having these companies add REQUIRED ENABLING (MACRO) legume seeds to their portfolio. Alternatively, artisanal on-farm CONDITIONS legume seed production could be integrated into the overall design of sustainably intensified systems (Peters et al., 2003; National Development Plans and other policies, e.g., in Chakoma and Chummun, 2019; Philp et al., 2019; Rubyogo et al., Colombia, Argentina or Costa Rica, increasingly outline the 2019), taking advantage of the numerous possible interactions need for establishing SPS and other legume-based options between legume cultivars and local plant-pollinator networks as strategies for sustainable intensification of cattle farming, (Palmer et al., 2009; Boelt et al., 2015; Suso et al., 2016; creating a demand for forage legume seed production (Ministerio Cong et al., 2020). This approach offers the potential added de Agricultura y Ganadería, 2011; Presidencia de la Nación benefit of income diversification and employment creation Argentina, 2018; Ministerio de Agricultura y Desarrollo Rural, among smallholders. 2019, 2020). Such demand is crucial for establishing large- Frontiers in Sustainable Food Systems | www.frontiersin.org 430 September 2021 | Volume 5 | Article 725981 Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions TABLE 1 | List of herbaceous and tree legumes known to be self-pollinated but with increased out-crossing when visited by different bee species. Species Plant growth References for out-crossing legumes Pollinating bee species; bee Interaction type habit species relevant for meliponiculture? (Yes/No) Cajanus cajan Herbaceous Saxena et al. (1994) Pollinating bee spp. unknown to the authors Centrosema spp. Herbaceous Spears (1987), Miles et al. (1990), Maass and Centris (Centris) aenea, Centris Flower visitations with no Torres (1992, 1998) (Hemisiella) trigonoides, Centris reference to specific floral (Centris) flavifrons, Centris resource (Trachina) sp. (No) Chamaecrista rotundifolia Herbaceous Maass and Torres (1998) Xylocopa frontalis; (N) Foraging for pollen Desmodium spp. Herbaceous Hutton (1960), Rotar and Urata (1967), Centris (Hemisiella) tarsata, Flower visitations with no Quesenberry et al. (1989) Thygater aethiops;(No) reference to specific floral resource Gliricidia sepium Tree Dawson et al. (1997), Srinivasa Rao et al. Xylocopa frontalis; (No) Foraging for pollen (2011) Bombus pullatus; (No) Melipona favosa, Tetragonisca angustula; (Yes) Codariocalix gyroides Herbaceous Maass and Torres (1998) Pollinating bee spp. unknown to the authors Dicorynia guianensis Tree Latouche-Hallé et al. (2004) Dinizia excelsa Tree Dick et al. (2003) Galactia striata Herbaceous Nogueira Couto et al. (1997), Maass and Torres (1998) Indigofera spacitata Herbaceous Hutton (1960) Lablab purpureus Herbaceous Kukade and Tidke (2014) Leucaena leucocephala Tree Hutton (1981) Neonotonia wightii Herbaceous Hutton (1970) Platypodium elegans Tree Murawski and Hamrick (1991) Platypodium elegans Tree Hufford and Hamrick (2003) African Trifolium spp. Herbaceous Pritchard and t’ Mannetje (1967) Senna multijuga Tree Ribeiro and Lovato (2004) Stylosanthes spp. Herbaceous Miles (1985), Santos-Garcia et al. (2011) Tachigalia versicolor Tree Loveless et al. (1998) Tachigalia versicolor Tree Murawski and Hamrick (1991) Vouacapoua americana Tree Dutech et al. (2002) The names of the bee species and the corresponding interaction types that are listed on this table were obtained from Nates-Parra (2016). or small-scale seed production systems that integrate local lands (White et al., 2001) or where land tenure is unclear (Kubitza plant-pollinator networks. These policies, however, lack the et al., 2018). To counteract such developments, public policies inclusion of pollinators and the ecosystem services they provide. (e.g., the Zero-Deforestation Agreements in Colombia and Brazil Likewise, payment schemes for ecosystem services, such as for or the Brazilian Forest Code) (Presidência da República, 2012; the establishment of SPS (e.g., Diaz et al., 2019a,b), do not Gibbs et al., 2015; FAO, 2016; Alianza Colombia TFA, 2021), include forage legume seed production models and pollinator safeguards and comprehensive monitoring/control mechanisms ecosystem services. are required. Other instruments such as taxes, subsidies and land Sustainable intensification strategies are a subject of algid tenure rights are also needed (Cohn et al., 2014; de Oliveira Silva debate. Despite the positive impacts of incorporation of forage et al., 2016). legumes on cattle production systems (e.g., GHG emission Investing in sustainable intensification strategies, smallholder reductions, animal welfare, biodiversity or land sparing) (Jansen legume seed production systems and meliponiculture require et al., 1997; Rivas and Holmann, 2000; Peters et al., 2001; access to credit and inputs. Some advances stand out, such as Valentim and Andrade, 2005; Enciso et al., 2019), an increased credit lines destined to the establishment of SPS in Colombia profitability of the system could be a driver for further expansion (Ministerio de Agricultura y Desarrollo Rural, 2020). However, of the agricultural frontier at the expense of forests or protected more access to credit is still missing for the establishment of seed ecosystems (Kaimowitz and Angelsen, 2008; Peñuela et al., 2011, multiplication plots and integrated meliponiculture. Resolving 2014; CIAT and Cormacarena, 2017). This is likely to happen on this bottleneck is crucial for assuring continuous seed supply, marginal lands (Maertens et al., 2006; Barretto et al., 2013), cheap ecosystem services and the scaling up of SPS. Supporting the Frontiers in Sustainable Food Systems | www.frontiersin.org 441 September 2021 | Volume 5 | Article 725981 Flower visitations with no reference to specific floral resource Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions TABLE 2 | List of potential interventions considering legume-pollinator interactions. Intervention Description Potential benefits Farm-level interventions Smallholder on-farm legume seed For own intensification purposes or as a business model to Income diversification and additional income (seed sales), production supply other producers who are intensifying or renewing their support of sustainable intensification (scaling), provision of systems. Small-holder on-farm legume seed production should habitats for pollinators (ecosystem services), employment take account of local knowledge (i.e., the use of already present creation and opportunities for women and rural youth legumes in a particular area combined with local knowledge of (preventing migration to cities) the given species). Seed production systems should also consider the processes of selection, conservation and exchanging of locally adapted legumes by local farmers Integrated crop pollination (ICP) Organizing framework that structures the development and Maximization of economic returns from pollinator-dependent evaluation of efficient and flexible crop pollination strategies crops, resilience to crop-pollination threats, additional income around the use of managed pollinator species in combination from hive product revenues, benefits from other enhanced with farm management practices. It focuses on integrating and farmland ecosystem services, reduced health risks from diversifying pollinators, after balancing the pros and cons of occupational and dietary exposure to pesticides using a single managed bee species, or mixtures of managed bee species and/or wild pollinators. In addition to the use of wild and managed bee species, ICP encompasses various strategies that enhance the farm environment for pollinators, including directed habitat management and pesticide stewardship. These strategies can be combined and adapted to the economic constraints of each specific farm by using decision support tools that consider crop value, yield benefits and the costs of adopting each alternative ICP component and practice Garibaldi et al., 2017; Isaacs et al., 2017 Meliponiculture and other forms of In addition to the introduced European honeybee (A. mellifera), Income diversification and additional income (hive products, traditional beekeeping other bees that can be managed for their hive products and legume seed sales and increased yields of other pollinator crop pollination include many stingless bee species dependent crops), home production and consumption of honey (Hymenoptera: Apidae: Meliponini), which constitute the most and propolis with characteristic physicochemical properties diverse group of eusocial tropical bees, the Asian honeybee (A. linked to traditional medicine, preservation of traditional cerana) and a few Bombus species that are only reared for their knowledge and practices, employment creation (including the crop pollination services. The integration of meliponiculture (i.e., establishment of a local industry of handcrafted wooden keeping and managing native stingless bee species) in legume beehives and the commercialization of other beekeeping seed production systems can benefit farmers directly, through supplies), benefits from other enhanced farmland ecosystem revenues from selling hive products, and indirectly due to an services and opportunities for women and youth in rural improved crop pollination, including that of legume forages. communities, which can help preventing rural exodus Beekeeping may also help raise the awareness of farmers with regard to the importance of adopting pollinator-friendly farm practices (e.g., sowing annual flowering plant strips to offer floral resources for pollinators throughout the year, integrated pest management, reduced insecticide application and minimizing pollinator poisoning by limiting insecticide applications to periods of low pollinator activity) Silvo-pastoral systems The versatility of SPS allows matching plant functional Promote biodiversity and enhance ecosystem services beyond groups–including multiple leguminous herb, shrub and tree carbon sequestration Phelan et al., 2015; Suso et al., 2016; Wu species–with pollinator functional groups Fontaine et al., 2006; et al., 2017; Otieno et al., 2020 Woodcock et al., 2014 Public and private sector interventions Landscape restoration approach The interventions presented above can be implemented at the Biodiversity conservation, supply of multiple ecosystem services farm level, yet pollinators are mobile organisms with foraging that include improved local climate regulation and protection, behaviors that cover distances between a few hundred meters water availability and a diverse cultural landscape with potential to several kilometers. They are thus affected by the availability of touristic attractiveness. resources and nesting sites at the landscape scale Pufal et al., 2017. The ecological effectiveness of the proposed interventions can therefore be maximized by integrating them into SPS that are planned, co-designed, coordinated and implemented at the landscape scale with the participation of local communities, local administrations, ecological restoration experts and environmental authorities. The versatility of legume-based SPS systems (e.g., with a high densities of tree legumes in combination with herbaceous legumes and with improved grasses) makes them especially suitable to restore the connectivity of fragmented landscapes, as their components (e.g., live fences, scattered trees and riparian buffers) can be arranged to provide ecologically important structural elements, such as connectivity corridors and hedgerows, thereby creating complex habitats for other wild animals and plants Murgueitio et al., 2011; Chará et al., 2019 Large scale legume seed As a company business model or through the integration of Support of sustainable intensification (scaling), standardization of production through the private smallholder seed producers seed quality, provision of habitats for pollinators (ecosystem seed sector services), employment creation, opportunities for women and rural youth (preventing migration to cities) Frontiers in Sustainable Food Systems | www.frontiersin.org 452 September 2021 | Volume 5 | Article 725981 Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions organization of both cattle and seed producers could help in Compared to grass monoculture pastures, which when facilitating credit access and coordination of investment efforts. largely expanded are associated with a homogenized Likewise, the development of payment schemes for ecosystem vegetation and the application of insecticides and services, incentives or new value chains with differentiated herbicides, silvo-pastoral systems improve biodiversity products (e.g., sustainable beef, honey) (Charry et al., 2019) and offer promising results regarding the restoration of could contribute to financing such investments at the farm level. habitats and pollinator populations in agroecosystems, Another financing model could be a cooperation amongst seed especially if combined with integrated crop pollination producers/beekeepers and companies who wish to green their and native beekeeping. Nevertheless, research and adaptive image and are willing to finance the establishment of local seed farm management efforts should be considered for each production plots with integrated meliponiculture. agroecological context in order to leverage the potential The establishment of seedmultiplication plots, seedmarketing pollinator conservation synergies from the interaction and beekeeping also require access to different knowledge sets, between traditional management practices and the natural such as legume seed production, treatment and marketing, regeneration processes of legume populations in legume-based beekeeping, and honey production, or product differentiation. silvo-pastoral systems. Already existing knowledge should be integrated into the rural extension system, which also needs to be strengthened in reach and content (i.e., harmonization of different approaches to CONCLUDING REMARKS AND LOOK assure homogeneity of concepts and avoid confusion among FORWARD producers) (Bravo et al., 2018; Charry et al., 2018; Enciso et al., 2018). Knowledge that helps to put the innovations The development of pollinator friendly environments, based into practice and facilitates scaling processes should be on forage-legumes and SPS and their introduction into cattle generated through research, i.e., regarding the adaptation to systems, brings several benefits, including the (i) provision and selection of legumes for specific agro-ecological conditions of habitats for pollinators on decline, and (ii) promotion of and seed production, bee species for integrated meliponiculture, legume seed yield considered as barrier to the wider adoption the ecology of plant-pollinator interactions, or pollinator of grass-legume, forage banks, or tree legume systems such diseases and invasiveness. Likewise, research should focus as SPS. Higher seed yield makes it easier for seed producers on the additional environmental and productive benefits of to establish a business model to supply others to intensify legume seed production with integrated meliponiculture, e.g., or renew their forage-based cattle systems. It also allows the regarding GHG emissions, biodiversity, soil health, profitability creation of different revenues such as those coming from or risk. bee farming (i.e., meliponiculture). The benefits from the There is a vast diversity of forage legumes, of which interplay of pollinators and forage legumes can be further a sample is safeguarded in the CGIAR gene banks (i.e., extended to the landscape level, affecting positively the yield over 22,000 accessions of 72 species). Although the CGIAR of nearby pollinator-dependent crops. Furthermore, benefits of gene banks hold the world’s largest collection of tropical pollinators from cattle production systems can extend upon forage species (Alliance of Bioversity International-CIAT, nearby ecosystems that might be fragmented or under decline 2020), this remains as a largely unexplored source of due to several factors. For these pollination-based benefits to genetic material, key for the evaluation of legumes for occur, enabling conditions, including policies, payment schemes sustainable intensification scenarios, seed production and for ecosystem services, incentives or new value chains, must be integrated meliponiculture. in place. Regarding meliponiculture, legislation and codes of practice, Seed availability is a bottleneck for the inclusion of legumes such as those established by Colombia’s Corporation for in cattle production systems at scale. It is noteworthy, the Sustainable Development of the Southern Amazon however, that small scale cattle producers in Tropical Latin (Corpoamazonia, 2016), must be set in place and enforced America often use and conserve native legumes in their in order to avoid the overexploitation of native stingless bees, production systems. These small-scale producers can be while promoting their sustainable use and propagation by considered guardians of legume diversity and related knowledge smallholders and beekeepers. This is important considering (e.g., management and synergies/antagonism between grasses the threat that the extraction and relocation of stingless bee and legumes). Sadly, this knowledge is often neglected by top- colonies from their habitats imposes to their wild populations, down approaches driven by researchers or business interests. not least because of the spatiotemporal dynamics of the To counteract this shortcoming, approaches are needed that parasites and diseases they carry. Additionally, research recognize small cattle producers’ knowledge, and that foster efforts need to be directed at harmonizing quality standards their strategies for integrating legumes into their local farming and export requirement specifications for the diversity of systems in a sustainable and profitable manner. Likewise, stingless bee honeys, in order to meet their increasing global increasing the forage legume seed availability might not result demand as food and/or medicine, which could be seen in impacts at scale unless measures are introduced and as an additional opportunity for improved and diversified disseminated among farmers to ensure pasture management rural livelihoods. that favors the inclusion of legumes. In this sense, research Frontiers in Sustainable Food Systems | www.frontiersin.org 463 September 2021 | Volume 5 | Article 725981 Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions and incentives are needed regarding, for example, rotational FUNDING grazing and grazing pressure, weeding, burning, the use of agrochemicals, and the selection of Gramineae compatible with This work was funded by the CGIAR Research Program on legume species. Livestock. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. We DATA AVAILABILITY STATEMENT also acknowledge the financial assistance of GROW Colombia from the UK Research and Innovation (UKRI) Global Challenges The original contributions presented in the study are included Research Fund (GCRF) (BB/P028098/1). in the article/supplementary material, further inquiries can be directed to the corresponding author. ACKNOWLEDGMENTS AUTHOR CONTRIBUTIONS This work was carried out as part of the CGIAR Research Program on Livestock. We thank all donors who globally support MN, JC, and SB: conceptualization, methodology, our work through their contributions to the CGIAR System. formal analysis, writing the original draft and review CGIAR is a global research partnership for a food-secure future. and editing, and resources. SB and JC: supervision Its science is carried out by 15 Research Centers in close and funding acquisition and project administration. collaboration with hundreds of partners across the globe.We also All authors contributed to the article and approved the thank the reviewers for their constructive comments that helped submitted version. to improve the manuscript. REFERENCES Cardoso, A. S., Berndt, A., Leytem, A., Alves, B. J. R., Carvalho, I. N. O., Barros Soares, L. H., et al. (2016). Impact of the intensification of beef production Alianza Colombia TFA (2021). Cero deforestación en Colombia: ABC de las in Brazil on greenhouse gas emissions and land use. Agric. Syst. 143, 86–96. cadenas cero deforestación de palma, cacao, carne y leche en Colombia. Bogotá, doi: 10.1016/j.agsy.2015.12.007 Colombia. Available online at: https://bit.ly/3g6dW8J (accessed September 03, Cassman, K. G., and Grassini, P. (2020). A global perspective 2021). on sustainable intensification research. Nat Sustain 3, 262–268. Alliance of Bioversity International-CIAT (2020). Tropical Forage Diversity. doi: 10.1038/s41893-020-0507-8 Available online at: https://ciat.cgiar.org/what-we-do/crop-conservation-and- CBD (2018). Convention on Biological Diversity, Subsidiary Body on Scientific, use/tropical-forage-diversity/ (accessed September 03, 2021). Technical and Technological Advice 22nd meeting of SBSTTA “Conservation Arango, J., Ruden, A., Martinez-Baron, D., Loboguerrero, A. M., Berndt, A., and Sustainable use of Pollinators”, Montreal, Canada 2018. Chacón, M., et al. (2020). Ambition meets reality: achieving ghg emission Chakoma, I., and Chummun, B. Z. (2019). Forage seed value chain analysis in a reduction targets in the livestock sector of Latin America. Front. Sustain. Food subhumid region of Zimbabwe: perspectives of smallholder producers. Afric. J. Syst. 4:65. doi: 10.3389/fsufs.2020.00065 Range Forage Sci. 36, 95–104. doi: 10.2989/10220119.2018.1546229 Auad, A. M., Braga, A. F. L., Fonseca, M. G., Resende, T. T., Toledo, A. M. O., Chará, J., Reyes, E., Peri, P., Otte, J., Arce, E., and Schneider, F. (2018). Silvopastoral Lucindo, T. S., et al. (2015). Does the silvopastoral system alter hymenopteran Systems and their Contribution to Improved Resource Use and Sustainable fauna (insecta: hymenoptera) in brachiaria decumbens monocultures? Ann. Development Goals (SDG): Evidence from Latin America. Geneva: Food and Entomol. Soc. Am. 108, 468–473. doi: 10.1093/aesa/sav035 Agriculture Organization of the United Nations (FAO), Centre for Research on Barretto, A. G. O. P., Berndes, G., Sparovek, G., and Wirsenius, S. (2013). Sustainable Agriculture (CIPAV), Agri Benchmark. Available online at: http:// Agricultural intensification in Brazil and its effects on land-use patterns: www.fao.org/3/ca2792en/ca2792en.pdf (accessed September 03, 2021). an analysis of the 1975–2006 period. Glob. Change Biol. 19, 1804–1815. Chará, J., Reyes, E., Peri, P., Otte, J., Arce, E., and Schneider, F. (2019). Silvopastoral doi: 10.1111/gcb.12174 Systems and their Contribution to Improved Resource Use and Sustainable Bernabucci, U. (2019). Climate change: impact on livestock and how can we adapt. Development Goals: Evidence from Latin America. Cali: FAO, CIPAV and Agri Anim. Front. 9, 3–5. doi: 10.1093/af/vfy039 Benchmark, 60. Available online at: http://www.fao.org/3/ca2792en/ca2792en. Bobbink, R., Hicks, K., Galloway, J., Spranger, T., Alkemade, R., Ashmore, M., et al. pdf (accessed September 03, 2021). (2010). Global assessment of nitrogen deposition effects on terrestrial plant Charry, A., Jäger, M., Enciso, K., Romero, M., Sierra L., Quintero, M., et al. diversity: a synthesis. Ecol. Appl. 20, 30–59. doi: 10.1890/08-1140.1 (2018). Cadenas de valor con enfoque ambiental y cero deforestación en Boelt, B., Julier, B., Karagić, D., and Hampton, J. (2015). Legume seed production la Amazonía colombiana – Oportunidades y retos para el mejoramiento meeting market requirements and economic impacts. Crit. Rev. Plant Sci. 34, sostenible de la competitividad regional. CIAT Políticas en Síntesis No. 41. 412–427. doi: 10.1080/07352689.2014.898477 Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. 10 Bravo, A., Enciso, K., Hurtado. J. J., del Cairo, J. R., Jäger, M., Charry, A., p. https://hdl.handle.net/10568/97203 (accessed September 03, 2021). et al. (2018). Estrategia sectorial de la cadena de ganadería doble propósito en Charry, A., Narjes, M., Enciso, K., Peters, M., and Burkart, S. (2019). Guaviare, con enfoque agroambiental y cero deforestación. Publicación CIAT Sustainable intensification of beef production in Colombia—chances for No. 453. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. product differentiation and price premiums. Agric. Food Econ. 7:22. Available online at: https://hdl.handle.net/10568/91289 (accessed September doi: 10.1186/s40100-019-0143-7 03, 2021). CIAT and Cormacarena (2017). Plan regional integral de cambio climático para la Byrne, A., and Fitzpatrick, Ú. (2009). Bee conservation policy at the global, regional Orinoquía. CIAT publicación No. 438. Cali, Colombia: Centro Internacional and national levels. Apidologie 40, 194–210. doi: 10.1051/apido/2009017 de Agricultura Tropical (CIAT). Available online at: https://issuu.com/ Calle, A., Montagnini, F., and Zuluaga, A. F. (2009). Farmers’ perceptions juanpablomaringarcia/docs/evidencia_5.compressed (accessed September 03, of silvopastoral system promotion in Quindío, Colombia. Bois For. Trop. 2021). 300, 79–94. Available online at: http://bft.cirad.fr/cd/BFT_300_79-94.pdf. Climate and Clean Air Coalition (2020). Enhancing climate ambition and action doi: 10.19182/bft2009.300.a20417 in Costa Rica. Available online at: https://www.ccacoalition.org/en/activity/ Frontiers in Sustainable Food Systems | www.frontiersin.org 474 September 2021 | Volume 5 | Article 725981 Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions enhancing-climate-ambition-and-action-costa-rica (accessed September 03, an economic perspective. Trop. Grasslands Forrajes Trop. 7, 359–369. 2021). doi: 10.17138/tgft(7)359-369 Cohn, A. S., Mosnier, A., Havlík, P., Valin, H., Herrero, M., Schmid, FAO (2021). The International Pollinator Initiative. Plan of action 2018–2030. E., et al. (2014). Cattle ranching intensification in Brazil can reduce Rome: FAO. Available online at: https://www.cbd.int/sbstta/sbstta-22-sbi-2/ global greenhouse gas emissions by sparing land from deforestation. sbstta-22-ipi-draft.pdf (accessed September 03, 2021). Proc. Natl. Acad. Sci. 111, 7236–7241. doi: 10.1073/pnas.13071 FAO (2016). El Estado de los bosques del mundo 2016. Los bosques y la agricultura: 63111 desafíos y oportunidades en relación con el uso de la tierra. Rome, Italy: Cong, W., Dupont, Y. L., Søegaard, K., and Eriksen, J. (2020). Optimizing yield FAO. Availble online at: http://www.fao.org/documents/card/en/c/6547e46e- and flower resources for pollinators in intensively managed multi-species 3e6f-4c47-8dcb-8c5c19a18e00/ (accessed September 03, 2021). grasslands. Agric. Ecosyst. Environ. 302:107062. doi: 10.1016/j.agee.2020.1 Fontaine, C., Dajoz, I., Meriguet, J., and Loreau, M. (2006). Functional 07062 diversity of plant-pollinator interaction webs enhances the persistence of plant Cook, B. G., Pengelly, B. C., Schultze-Kraft, M., Taylor, M., Burkart, S., Cardoso communities. PLoS Biol. 4:e1. doi: 10.1371/journal.pbio.0040001 Arango, J. A., et al. (2020). Tropical Forages: An Interactive Selection Tool. 2nd Fontana, C. S., Dotta, G., Marques, C. K., Repenning, M., Agne, C. and Revised Edn. CIAT (International Center for Tropical Agriculture) and E., and dos Santos, R. J. (2016). Conservation of grassland birds in ILRI (International Livestock Research Institute). Available online at: www. South Brazil: a land management perspective. Nat. Conser. 14, 83–87. tropicalforages.info doi: 10.1016/j.ncon.2016.09.005 Corpoamazonia (2016). Aprobada la Gestión de CORPOAMAZONIA en el Marco Forrest, J. R. K. (2017). “Chapter 5. Insect Pollinators and Climate Change,” in del Plan de Acción 2016-2019 “Ambiente para la Paz”. Mocoa, Colombia. Global Climate Change and Terrestrial Invertebrates, eds. S.T. Johnson and T. Accessed on August 10 2021. Available online at: https://www.corpoamazonia. Hefin Jones. New York, NY: Wiley. doi: 10.1002/9781119070894.ch5 gov.co/index.php/noticias/1060-aprobada-gestion-corpoamazonia-2016- Ganadería Colombiana Sostenible (2018). ‘En qué consiste el proyecto Ganadería 2019-ambiente-para-la-paz. Colombiana Sostenible? Colombia. Available online at: https://bit.ly/32IkHat Cubillos, A. M., Vallejo, V. E., Arbeli, Z., Terán, W., Dick, R. P., Molina, C. H., (accessed September 03, 2021). et al. (2016). Effect of the conversion of conventional pasture to intensive Garibaldi, L. A., Requier, F., Rollin, O., and Andersson, G. K. S. (2017). Towards silvopastoral systems on edaphic bacterial and ammonia oxidizer communities an integrated species and habitat management of crop pollination. Curr. Opin. in Colombia. Eur. J. Soil Biol. 72, 42–50. doi: 10.1016/j.ejsobi.2015.12.003 Insect Sci. 21, 105–114. doi: 10.1016/j.cois.2017.05.016 da Silva, F. S., Domiciano, L. F., Gomes, F. J., Sollenberger, L. E., Pedreira, C. Gerssen-Gondelach, S. J., Lauwerijssen, R. B. G., Havlík, P., Herrero, M., Valin, H., G. S., Pereira, D. H., et al. (2020). Herbage accumulation, nutritive value and Faaij, A. P. C., et al. (2017). Intensification pathways for beef and dairy cattle beef cattle production onmarandu palisadegrass pastures in integrated systems. production systems: Impacts on GHG emissions, land occupation and land use Agrofor. Syst. 94, 1891–1902. doi: 10.1007/s10457-020-00508-3 change. Agric. Ecosyst. Environ. 240, 135–147. doi: 10.1016/j.agee.2017.02.012 Dawson, I. K., Waugh, R., Simons, A. J., and Powell, W. (1997). Simple Gibbs, H. K., Munger, J., L’Roe, J., Barreto, P., Pereira, R., Christie, M., et al. (2015). sequence repeats provide a direct estimate of pollen-mediated gene Did ranchers and slaughterhouses respond to zero deforestation agreements in dispersal in tropical tree Gliricidia sepium. Mol. Ecol. 6, 179–183. the Brazilian Amazon? Conserv. Lett. 9, 1–10. doi: 10.1111/conl.12175 doi: 10.1046/j.1365-294X.1997.00163.x Herrero, M., Havlík, P., Valin, H., Notenbaert, A., Rufino, M. C., and Thornton, de Oliveira Silva, R., Barioni, L. G., Hall, J. A. J., Matsuura, M. F., Albertini, P. K. (2013). Biomass use, production, feed efficiencies, and greenhouse gas T. Z., Fernandes, F. A., et al. (2016). Increasing beef production could lower emissions from global livestock systems. Proc. Natl. Acad. Sci. U. S. A. 110, greenhouse gas emissions in Brazil if decoupled from deforestation. Nat. Clim. 20888–20893. doi: 10.1073/pnas.1308149110 Change 6, 493–497. doi: 10.1038/nclimate2916 Hufford, K. M., and Hamrick, J. L. (2003). Viability selection at three early life Diaz, M. F., Enciso, K., Triana, N., and Burkart, S. (2019b). Protocolo para stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). la entrada en operación de esquemas de Pagos por Servicios Ambientales Evolution 57, 518–526. doi: 10.1111/j.0014-3820.2003.tb01543.x para sistemas silvopastoriles. Publicación CIAT No. 488. Cali, CO: Centro Hutton, E.M. (1970). Tropical pastures. Adv. Agron. 22, 1–73. Internacional de Agricultura Tropical (CIAT).Available online at: https://hdl. doi: 10.1016/S0065-2113(08)60265-5 handle.net/10568/106846 (accessed September 03, 2021). Hutton, E. M. (1960). Flowering and pollination in Indigoferaspicata, Phaseolus Diaz, M. F., Enciso, K., Triana, N., Muriel, J., and Burkart, S. (2019a). Pagos lathyroides, Desmodium uncinatum, andsome other tropical pasture legumes. por Servicios Ambientales para sistemas silvopastoriles en Colombia. Cali, J. Exp. Agric. 28, 235–243. Available online at: https://www.cabdirect.org/ CO: Centro Internacional de Agricultura Tropical (CIAT). Available online cabdirect/abstract/19611600570 (accessed September 03, 2021). at: https://hdl.handle.net/10568/106849 (accessed September 03, 2021). Hutton, E. M. (1981). Natural crossing and acid tolerance in some Leucaena Dick, C. W., Etchelecu, G., and Austerlitz, F. (2003). Pollen dispersal of tropical species. Leucaena Res. Rep. 2, 2–4. Available online at: https://www.cabi.org/ trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees isc/abstract/19860610173 (accessed September 03, 2021). in pristine and fragmented Amazonian rainforest. Mol Ecol 12, 753–764. Ibrahim, M., Villanueva, C., Casasola, F., and Rojas, J. (2006). Sistemas doi: 10.1046/j.1365-294X.2003.01760.x silvopastoriles como una herramienta para el mejoramiento de la productividad Dubeux, J. C. B., Jr., Muir, J. P., Apolinário, V. X. O., Ramachandran Nair, P. K., y restauración de la integridad ecológica de paisajes ganaderos. Past. Lira, M. A. and Sollenberger, L. E. (2017). Tree legumes: an underexploited Forrajes 29, 383–419. Available online at: https://www.redalyc.org/pdf/2691/ resource in warm-climate silvopastures. Braz. J. Anim. Sci. 46, 689–703. 269121676004.pdf (accessed September 03, 2021). doi: 10.1590/S1806-92902017000800010 Isaacs, R., Williams, N., Ellis, J., Pitts-Singer, T. L., Bommarco, R., and Vaughan, M. Dutech, C., Seiter, J., Petronelli, P., Joly, H. I., and Jarne, P. (2002). Evidence of (2017). Integrated crop pollination: combining strategies to ensure stable and low gene flow in a neotropical clustered tree species in two rainforest stands sustainable yields of pollination-dependent crops. Basic Appl. Ecol. 22, 44–60. of French Guiana. Mol. Ecol. 11, 725–738. doi: 10.1046/j.1365-294X.2002.0 doi: 10.1016/j.baae.2017.07.003 1475.x Jansen, H. G. P., Ibrahim, M. A., Nieuwenhuyse, A., ’t Mannetje, L., Joenje, M., Eckard, R. J., Grainger, C., and de Klein, C. A.M. (2010). Options for the abatement and Abarca, S. (1997). The economics of improved pasture and silvopastoral of methane and nitrous oxide from ruminant production: a review. Livestock technologies in the Atlantic zone of Costa Rica. Trop. Grassl. 31, 588–598. Sci. 130, 47–56. doi: 10.1016/j.livsci.2010.02.010 Available online at: https://www.tropicalgrasslands.info/public/journals/4/ Enciso, K., Bravo, A., Charry, A., Rosas, G., Jäger, M., Hurtado, J. J., et al. (2018). Historic/Tropical%20Grasslands%20Journal%20archive/Abstracts/Vol_31_ Estrategia sectorial de la cadena de ganadería doble propósito en Caquetá, con 1997/Abs_31_06_97_pp588_598.html (accessed September 03, 2021). enfoque agroambiental y cero deforestación. Publicación CIAT No. 454. Cali, Kaimowitz, D., and Angelsen, A. (2008). Will livestock intensification Colombia: Centro Internacional de Agricultura Tropical (CIAT). Available help save latin America’s tropical forests? J. Sustain. For. 27, 6–24. online at: https://hdl.handle.net/10568/91981 (accessed September 03, 2021). doi: 10.1080/10549810802225168 Enciso, K., Sotelo, M., Peters, M., and Burkart, S. (2019). The inclusion Kovács-Hostyánszki, A., Espíndola, A., Vanbergen, A. J., Settele, J., Kremen, C., of Leucaena diversifolia in a Colombian beef cattle production system: and Dicks, L. V. (2017). Ecological intensification to mitigate impacts of Frontiers in Sustainable Food Systems | www.frontiersin.org 485 September 2021 | Volume 5 | Article 725981 Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions conventional intensive land use on pollinators and pollination. Ecol. Lett. 20, Murgueitio, E., Calle, Z., Uribe, F., Calle, A., and Solorio, B. (2011). 673–689. doi: 10.1111/ele.12762 Native trees and shrubs for the productive rehabilitation of tropical cattle Kubitza, C., Krishna, V. V., Urban, K., Alamsyah, Z., and Qaim, M. (2018). Land ranching lands. For. Ecol. Manag. 261, 1654–1663. doi: 10.1016/j.foreco.2010. property rights, agricultural intensification, and deforestation in Indonesia. 09.027 Ecol. Econ. 147, 312–321. doi: 10.1016/j.ecolecon.2018.01.021 Murgueitio, E., and Ibrahim, M. (2001). “Agroforestería pecuaria para la Kukade, S. A., and Tidke, J. A. (2014). Reproductive biology of Dolichos lablab L. reconversión de la ganadería en Latinoamérica,” in Livestock Research for Rural (Fabaceae). Indian J. Plant Sci. 3, 22–25. Development 13. Available online at: http://www.lrrd.org/lrrd13/3/murg133. Kumar, A., Hanson, J., and Abdena, A. (2020). “Production of high-quality tropical htm (accessed December 5, 2021). forage legume seeds,” in Advances in Seed Production and Management, eds. A. Nates-Parra, G. (2016). Iniciativa Colombiana de Polinizadores—Abejas— K. Tiwari. Singapore: Springer. doi: 10.1007/978-981-15-4198-8_6 icpa. Bogotá, D. C.: Departamento de Biología, Universidad Nacional de Landholm, D. M., Pradhan, P., Wegmann, P., Sánchez Romero, M. A., Colombia. ISBN 978-958-775-866-5 (digital). Available online at: https://www. Salazar Suárez, J. C., and Kropp, J. P. (2019). Reducing deforestation and uneditorial.com/pageflip/acceso-abierto/pdf/abejas-polinizadoras-ebook- improving livestock productivity: greenhouse gas mitigation potential 40217.pdf (accessed September 03, 2021). of silvopastoral systems in Caquetá. Environ. Res. Lett. 14:114007. Nogueira Couto, R. H., Favoretto, V., Almeida, L. F., de Prandi, D. M., and de doi: 10.1088/1748-9326/ab3db6 Andrade Rodriguez, L. R. (1997). Insect pollination and plant guiding in Latouche-Hallé, C., Ramboer, A., Bandou, E., Caron, H., and Kremer, A. (2004). Galactia striata (Jacq.) Urb. (Leguminosae). Pasturas Trop. 19, 51–54. Available Long-distance pollen flow and tolerance to selfing in a neotropical tree species. online at: https://www.tropicalgrasslands.info/public/journals/4/Elements/ Mol. Ecol. 13, 1055–1064. doi: 10.1111/j.1365-294X.2004.02127.x DOCUMENTS/1997-vol19-rev1-2-3/Vol19_rev1_97_art10.pdf (accessed Lira Junior, M. A., Fracetto Cury, F. J., Da Ferreira, J. S., Silva, M. B., Fracetto, M., September 03, 2021). and Gomes Monteiro, G. (2020). Legume silvopastoral systems enhance soil Orford, K. A., Murray, P. J., Vaughan, I. P., and Memmott, J. (2016). Modest organic matter quality in a subhumid tropical environment. Soil Sci. Soc. Am. enhancements to conventional grassland diversity improve the provision of J. 84, 1209–1218. doi: 10.1002/saj2.20106 pollination services. J. Appl. Ecol. 53, 906–915. doi: 10.1111/1365-2664.12608 Loveless, M. D., Hamrick, J. L., and Foster, R. B. (1998). Population structure and Otieno, M., Steffan-Dewenter, I., Potts, S. G., Kinuthia, W., Kasina, M. J., and mating system in Tachigali versicolor, a monocarpic neotropical tree. Heredity Garratt, M. P. D. (2020). Enhancing legume crop pollination and natural pest 81, 134–143. doi: 10.1046/j.1365-2540.1998.00353.x regulation for improved food security in changing African landscapes. Glob. Maass, B. L., and Torres, A. M. (1998). Off-types indicate natural outcrossing in Food Secur. 26:100394. doi: 10.1016/j.gfs.2020.100394 five tropical forage legumes in Colombia. Trop. Grassl. 32, 124–130. Available Paiva, I. G., Auad, A. M., Veríssimo, B. A., and Silveira, L. C. P. (2020). Differences online at: https://www.tropicalgrasslands.info/public/journals/4/Historic/ in the insect fauna associated to a monocultural pasture and a silvopasture in Tropical%20Grasslands%20Journal%20archive/Abstracts/Vol_32_1998/Abs_ Southeastern Brazil. Sci. Rep. 10:12112. doi: 10.1038/s41598-020-68973-5 32_02_98_pp124_130.html (accessed September 03, 2021). Palmer, R. G., Perez, P. T., Ortiz-Perez, E., Maalouf, F., and Suso, M. J. Maass, B. L., and Torres, A. M. (1992). “Outcrossing in the tropical forage (2009). The role of crop-pollinator relationships in breeding for pollinator- legume Centrosema brasilianum (L.) Benth,” Abstracts of the XIII EUCARPIA friendly legumes: from a breeding perspective. Euphytica 170, 35–52. Congress, Angers, France,1992, 465–466. Available online at: https://hdl.handle. doi: 10.1007/s10681-009-9953-0 net/10568/89580 (accessed September 03, 2021). Peñuela, L., Fernández, A. P., Castro, F., and Ocampo, A. (2011). Uso y manejo Maertens, M., Zeller, M., and Birner, R. (2006). Sustainable agricultural de forrajes nativos en la sabana inundable de la Orinoquía. Convenio intensification in forest frontier areas. Agric. Econ. 34, 197–206. de cooperación interinstitucional entre The Nature Conservancy (TNC) doi: 10.1111/j.1574-0864.2006.00118.x y la Fundación Horizonte Verde (FHV) con el apoyo de la Fundación Martha, G. B., Alves, E., and Contini, E. (2012). Land-saving approaches Biodiversidad de España y la Corporación Autónoma Regional de la Orinoquía and beef production growth in Brazil. Agric. Syst. 110, 173–177. (CorpOrinoquía). Available online at: https://infopastosyforrajes.com/libros- doi: 10.1016/j.agsy.2012.03.001 y-manuales-pdf/uso-y-manejo-de-forrajes-nativos-en-la-sabana-inundable- Miles, J. W. (1985). Evaluation of potential genetic marker traits and estimation de-la-orinoquia/ (accessed September 03, 2021). of outcrossing rate in Stylosanthes guianensis. Aust. J. Agric. Res. 36, 259–265. Peñuela, L., Solano, C., Ardila, V., and Galán, S. (2014). Sabana inundable doi: 10.1071/AR9850259 y ganadería, opción productiva de conservación en la Orinoquia. Bogotá, Miles, J. W., Clements, R. J., Grof,. B., and Serpa, A. (1990). “Genetics and Colombia: Asociación Red Colombiana de Reservas Naturales de la breeding of Centrosema,” in Centrosema: Biology, Agronomy, and Utilization, Sociedad Civil, Fundación Natura, World Wildlife Fund, The Nature eds. R. Schultze-Kraft, R. J. Clements. CIAT publication no. 92. Colombia: Cali, Conservancy, y Parques Nacionales Naturales de Colombia. Available 245–270. Available online at: https://library.ciat.cgiar.org/cgi-bin/koha/opac- online at: https://horizonteverde.org.co/wp-content/uploads/2020/02/LIBRO- detail.pl?biblionumber=23425 (accessed September 03, 2021). GANADERO-G5-FINAL.pdf (accessed September 03, 2021). Ministerio de Agricultura y Desarrollo Rural (2019). Política agropecuaria y de Peters, M., Horne, P., Schmidt, A., Holmann, F., Kerridge, P. C., Tarawali, S. desarrollo rural 2018-2022: un campo para la equidad. Bogotá. Available online A., et al. (2001). The Role of Forages in Reducing Poverty and Degradation of at: https://n9.cl/yjgle (accessed September 03, 2021). Natural Resources in Tropical Production Systems. Agricultural Research and Ministerio de Agricultura y Desarrollo Rural (2020). MinAgricultura Rodolfo Extension Network. Network Paper No. 117. Available online at: https://cdn. Zea lanza nueva línea para financiar los sistemas silvopastoriles. Colombia. odi.org/media/documents/5218.pdf (accessed September 03, 2021). Available online at: https://bit.ly/3sNo6ze (accessed September 03, 2021). Peters, M., Lascano, C. E., Roothaert, R., and de Haan, N. C. (2003). Ministerio de Agricultura y Ganadería (2011). Política de Estado para el Sector Linking research on forage germplasm to farmers: the pathway to increased Agroalimentario y el Desarrollo Rural Costarricense 2010–2021. Costa Rica. adoption—a CIAT, ILRI and IITA perspective. Field Crops Res. 84, 179–188. Available online at: https://bit.ly/2QlzRjr (accessed September 03, 2021). doi: 10.1016/S0378-4290(03)00149-7 Ministerio de Agricultura y Ganadería (2019). Costa Rica, en ruta hacia la Phelan, P., Moloney, A. P., McGeough, E. J., Humphreys, J., Bertilsson, descarbonización de la ganadería 2013–2018. San José: Costa Rica. Available J., O’Riordan, E. G., et al. (2015). Forage legumes for grazing and online at: https://bit.ly/3najylF (accessed September 03, 2021). conserving in ruminant production systems. Crit. Rev. Plant Sci. 34, 281–326. Muir, J. P., Tedeschi, L. O., Dubeux, J. C. B., Peters, M., and Burkart, S. (2017). doi: 10.1080/07352689.2014.898455 Enhancing food security in Latin America with forage legumes, Aumentar a Philp, J. N.M., Vance,W., Bell, R.W., Chhay, T., Boyd, D., Phimphachanhvongsod, segurança alimentar na América Latina com leguminosas forrageiras. Arch. V., and et al. (2019). Forage options to sustainably intensify smallholder Latinoamerican. Prod. Anim. 25, 113–131. Available online at: https://hdl. farming systems on tropical sandy soils. A review. Agron. Sustain. Dev. 39:30. handle.net/10568/96233 (accessed September 03, 2021). doi: 10.1007/s13593-019-0576-0 Murawski, D. A., and Hamrick, J. L. (1991). The effect of the density of flowering Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., and Kunin, individuals on the mating systems of nine tropical tree species. Heredity 67, W. E. (2010). Global pollinator declines: trends, impacts and drivers. Trends 167–174. doi: 10.1038/hdy.1991.76 Ecol. Evol. 25, 345–353. doi: 10.1016/j.tree.2010.01.007 Frontiers in Sustainable Food Systems | www.frontiersin.org 496 September 2021 | Volume 5 | Article 725981 Narjes Sanchez et al. Promoting Forage Legume–Pollinator Interactions Presidência da República (2012). Lei N◦ 12.651, de 25 de maio de 2012. Dispõe Srinivasa Rao, C., Venkateswarlu, B., Dinesh Babu, M., Wani, S. P., Dixit, S., sobre a proteção da vegetação nativa e dá outras providências. Presidência da Sahrawat, K. L., et al. (2011). Soil Health Improvement with Gliricidia Green Leaf República. Available online at: http://www.planalto.gov.br/ccivil_03/_ato2011- Manuring in Rainfed Agriculture, on Farm Experiences. Santoshnagar: Central 2014/2012/lei/L12651compilado.htm (accessed September 03, 2021). Research Institute for Dryland Agriculture, p. 16. Available online at: http://oar. Presidencia de la Nación Argentina (2018). Objetivos de desarrollo sostenible. icrisat.org/5534/ (accessed September 03, 2021). Argentina. Available online at: https://bit.ly/3tlDzbb (accessed September 03, Suso, M. J., Bebeli, P. J., Christmann, S., Mateus, C., Negri, 2021). V., and Pinheiro de Carvalho, M. A. A. (2016). Enhancing Pritchard, A. J., and t’ Mannetje, L. (1967). The breeding systems and some legume ecosystem services through an understanding of plant- interspecific relations of a number of African Trifolium spp. Euphytica 16, pollinator interplay. Front. Plant Sci. 7:333. doi: 10.3389/fpls.2016. 324–329. doi: 10.1007/BF00028938 00333 Pufal, G., Steffan-Dewenter, I., and Klein, A.-M. (2017). Crop pollination Valentim, J. F., and Andrade, C. M. S. (2005). Forage peanut (Arachis pintoi): a services at the landscape scale. Curr. Opin Insect Sci. 21, 91–97. high yielding and high-quality tropical legume for sustainable cattle production doi: 10.1016/j.cois.2017.05.021 systems in the western Brazilian Amazon. Trop. Grassl. 39:222. Available online Quesenberry, K. H., McKellar, M. A., and Moon, D. E. (1989). “Evaluation and at: https://www.tropicalgrasslands.info/public/journals/4/Historic/Tropical hybridization of germplasm in the Desmodium heterocarpon-D. ovalifolium %20Grasslands%20Journal%20archive/PDFs/Vol_39_2005/Vol_39_04_2005_ species complex,” in Proceedings of the XVI International Grassland Congress, pp222_222.pdf (accessed September 03, 2021). Nice, France, 1989, pp. 251–252. Association Francaise pour la Production Van der Sluijs, J. P. (2020). Insect decline, an emerging global environmental risk. Fourragere, Versailles (France): AFPF, 1989. ISBN 2-9504110-0-2, 251-252. Curr. Opin. Environ. Sustain. 46, 39–42. doi: 10.1016/j.cosust.2020.08.012 Rao, I., Peters, M., Castro, A., Schultze-Kraft, R.,White, D., Fisher, M., et al. (2015). Van der Sluijs, J. P., and Vaage, N. S. (2016). Pollinators and global food LivestockPlus—the sustainable intensification of forage-based agricultural security: the need for holistic global stewardship. Food Ethics 1, 75–91. systems to improve livelihoods and ecosystem services in the tropics. Trop. doi: 10.1007/s41055-016-0003-z Grass Forr. Trop. 3:59. doi: 10.17138/TGFT(3)59-82 White, D., Holmann, F., Fujisaki, S., Reategui, K., and Lascano, C. (2001). Will Ribeiro, R. A., and Lovato, M. B. (2004). Mating system in a neotropical intensifying pasture management in Latin America protect forests—Or is it the tree species, Senna multijuga (Fabaceae). Genet. Mol. Biol. 27, 418–424. other way around? Agricultural Technologies and Tropical Deforestation, eds. doi: 10.1590/S1415-47572004000300018 A. Angelsen, and D. Kaimowitz (Wallingford, UK: CABI Publishing), 91–113. Rivas, L., and Holmann, F. (2000). Early adoption of Arachis pintoi in the humid doi: 10.1079/9780851994512.0091 tropics: the case of dual-purpose livestock systems in Caquetá, Colombia. Woodcock, B. A., Savage, J., Bullock, J. M., Nowakowski, M., Orr, R., Tallowin, Livestock Research for Rural Development, 12:Article#23. Available online J. R. B., et al. (2014). Enhancing floral resources for pollinators in productive at: http://www.lrrd.org/lrrd12/3/riva123.htm (accessed September 03, 2021). agricultural grasslands. Biol. Conserv. 171, 44–51. doi: 10.1016/j.biocon.2014. Rotar, P. P., and Urata, U. (1967). Cytological studies in the genus Desmodium; 01.023 some chromosome counts. Am. J. Bot. 54, 1–4. doi: 10.2307/2440881 Wu, G. L., Liu, Y., Tian, F. P., and Shi, Z. H. (2017). Legumes functional Rubyogo, J. C., Akpo, E., Omoigui, L., Pooran, G., Chaturvedi, S. K., and Fikre, A. group promotes soil organic carbon and nitrogen storage by increasing (2019). Market-led options to scale up legume seeds in developing countries: plant diversity. Land Degrad. Develop. 28, 1336–1344. doi: 10.1002/ldr. experiences from the Tropical Legumes Project. Plant Breed. 138, 474–486. 2570 doi: 10.1111/pbr.12732 Ruviaro, C. F., de Léis, C. M., Lampert, V., do, N., Barcellos, J. O. J., and Author Disclaimer: The views expressed in this document may not be taken as the Dewes, H. (2015). Carbon footprint in different beef production systems official views of these organizations. on a southern Brazilian farm: a case study. J. Clean. Prod. 96, 435–443. doi: 10.1016/j.jclepro.2014.01.037 Conflict of Interest: The authors declare that the research was conducted in the Sakamoto, L. S., Berndt, A. P., André de, F., Lemes, A. P., Azenha, M. absence of any commercial or financial relationships that could be construed as a V., Alves, T. C., et al. (2020). Pasture intensification in beef cattle potential conflict of interest. production can affect methane emission intensity. In J. Anim. Sci. 98:skaa309. doi: 10.1093/jas/skaa309 Publisher’s Note: All claims expressed in this article are solely those of the authors Santos-Garcia, M. O., Resende, R. M. S., Chiari, L., Imaculada Zucchi, M., and and do not necessarily represent those of their affiliated organizations, or those of Pereira de Souza, A. (2011). Mating systems in tropical forages: Stylosanthes the publisher, the editors and the reviewers. Any product that may be evaluated in capitata Vog. and Stylosanthes guianensis (Aubl.) Sw. Euphytica 178, 185–193. this article, or claim that may be made by its manufacturer, is not guaranteed or doi: 10.1007/s10681-010-0293-x Saxena, K. B., Jayasekera, S. J. B. A., Ariyaratne, H. P., Ariyanayagam, R. P., endorsed by the publisher. and Fonseka, H. H. D. (1994). Frequency of natural out-crossing in partially cleistogamous pigeon pea lines in diverse environments. Crop Sci. 34, 660–662. Copyright © 2021 Narjes Sanchez, Cardoso Arango and Burkart. This is an open- doi: 10.2135/cropsci1994.0011183X003400030011x access article distributed under the terms of the Creative Commons Attribution Schultze-Kraft, R., Rao, I. M., Peters, M., Clements, R. J., Bai, C., and Liu, G. (2018). License (CC BY). The use, distribution or reproduction in other forums is permitted, Tropical forage legumes for environmental benefits: an overview. Trop. Grassl. provided the original author(s) and the copyright owner(s) are credited and that the Forr. Trop. 6, 1–14. doi: 10.17138/TGFT(6)1-14 original publication in this journal is cited, in accordance with accepted academic Spears, Jr., E.E. (1987). Island and mainland pollination ecology of Centrosema practice. No use, distribution or reproduction is permitted which does not comply virginianum and Opuntia stricta. J. Ecol. 75, 351–362. doi: 10.2307/2260423 with these terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1470 September 2021 | Volume 5 | Article 725981 ORIGINAL RESEARCH published: 04 October 2021 doi: 10.3389/fsufs.2021.666604 Risk Reduction and Productivity Increase Through Integrating Arachis pintoi in Cattle Production Systems in the Colombian Orinoquía Karen Johanna Enciso Valencia 1, Álvaro Rincón Castillo 2, Daniel Alejandro Ruden 1 and Stefan Burkart 1* 1 The Alliance of Bioversity International-CIAT, Crops for Nutrition and Health, Tropical Forages Program, Cali, Colombia, 2 The Colombian Agricultural Research Corporation, Villavicencio, Colombia In many parts of the foothills of the Orinoquía region of Colombia, cattle production takes place on poorly drained soils. The region is dominated by extensive grazing systems of Brachiaira humidicola cv. Humidicola, a grass with high adaptation potential under temporal waterlogging conditions. Inadequate management practices and low soil fertility result in degradation, however, with important negative effects on pasture Edited by: Glenn Hyman, productivity and the quality and provision of (soil) ecosystem services–a situation Independent Researcher, Colombia that is likely to worsen in the near future due to climate change. Against this Reviewed by: background, AGROSAVIA (Corporación Colombiana de Investigación Agropecuaria) Alisher Mirzabaev, Center for Development Research selected Arachis pintoi CIAT 22160 cv. Centauro (Centauro) as a promising alternative (ZEF), Germany for the sustainable intensification of livestock production and rehabilitation of degraded Ajit Singh, areas. This study assesses dual-purpose milk production in the foothills of the Colombian University of Nottingham Malaysia Campus, Malaysia Orinoquía from an economic perspective. We compare two production systems: the *Correspondence: Centauro–Brachiaira humidicola cv. Humidicola association (new system) and Brachiaira Stefan Burkart humidicola cv. Humidicola as a monoculture (traditional system). We used cashflow and s.burkart@cgiar.org risk assessment models to estimate economic indicators. The projections for economic Specialty section: returns consider changes in forage characteristics under regional climate change This article was submitted to scenarios RCP (2.6, 8.5). The LIFE-SIM model was used to simulate dairy production. Land, Livelihoods and Food Security, a section of the journal Results show that the inclusion of Centauro has the potential to increase animal Frontiers in Sustainable Food Systems productivity and profitability under different market scenarios. The impact of climatic Received: 15 February 2021 variables on forage production is considerable in both climate change scenarios. Both Accepted: 06 September 2021 total area and potential distribution of Centauro could change, and biomass production Published: 04 October 2021 could decline. Brachiaira humidicola cv. Humidicola showed better persistence due to Citation: Enciso Valencia KJ, Rincón Castillo Á, higher nitrogen levels in soil when grown in association with Centauro. The legume Ruden DA and Burkart S (2021) Risk also provides a number of ecosystem services, such as improving soil structure and Reduction and Productivity Increase composition, and also contributes to reducing greenhouse gas emissions. This helps to Through Integrating Arachis pintoi in Cattle Production Systems in the improve the adaptation and mitigation capacity of the system. Colombian Orinoquía. Front. Sustain. Food Syst. 5:666604. Keywords: climate change, forage legumes, adoption, economic evaluation, risk analysis (RA), land-use change doi: 10.3389/fsufs.2021.666604 (LUC) Frontiers in Sustainable Food Systems | www.frontiersin.org 418 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems INTRODUCTION reproduction (CIAT CORMACARENA, 2018). Furthermore, not only projected mean changes can have an impact, but also Context of Improved Forages in the changes in the variability and strength of extreme weather events, Orinoquía leading to significant consequences for livestock production (e.g., In many parts of the foothills of the Orinoquía region of increased frequency of heat stress, drought events and floods; Colombia, cattle production takes place on poorly drained Thornton et al., 2009). The effect of these climatic phenomena soils. Consequently, extensive grazing systems characterize the is also reflected at the macroeconomic level via prices, because region and Brachiaira humidicola cv. Humidicola is the most when faced with climatic events, food prices tend to vary, common feed option to be found. It was introduced in the generating transitory inflationary pressures (Melo et al., 2017). As 1970s in order to improve the production of the region, due a result of reductions in precipitation levels caused by the El Niño to its high adaptation potential under temporal waterlogging phenomenon, for example, a reduction in agricultural supply is conditions and good forage production (ICA, 1987). As a result generated, which in turn leads to temporary price increases (Melo of inappropriate management practices and low soil fertility in et al., 2017). the region, however, most of these pastures are, today, in some Apart from the climatic impacts on local production systems, state of degradation (Rincón et al., 2018). This has led to a the increasing demand for animal source food (OECD/FAO, significant reduction in pasture productivity, as well as negative 2020) creates pressure on livestock producers to extend effects on the quality and provision of soil ecosystem services production areas. In the case of the Orinoquía, this can cause (Fonte et al., 2014; Galdino et al., 2015), generating important increasing rates of deforestation and a penetration of important economic and ecological implications for the region. Cattle and local ecosystems (such as native savannas), leading to irreversible dairy production are considered to be one of the main sources changes within, and losses of, local ecosystems, biodiversity and of greenhouse gas emissions, derived from the digestion process cultural heritage, aggravating climate change even further. of the animals (methane and nitrous oxide emissions), the use In this sense, there is an increasingly pressing need to of nitrogen fertilizers, as well as the expansion of productive implement sustainable production systems with greater capacity areas through deforestation or the invasion of protected areas for adaptation and mitigation to climate change, systems that (CIAT CORMACARENA, 2018). The cattle sector is therefore contribute to maintaining, improving and protecting local considered one of the key sectors for interventions with great ecosystems. One of themost promising alternatives to achieve the potential for climate change mitigation. In this sense, achieving previous objectives, as well as to restore degraded areas, is the use intensive livestock farming in a sustainable way has become one of forage legumes in livestock systems (Fisher et al., 1994; Shelton of the main approaches for sector development in the Orinoquía. et al., 2005; Murgueitio et al., 2011; Schultze-Kraft et al., 2018). In short, this meansmore efficient cattle farms which consider, Their high protein content improves nutritional values and the protect and sustainably use existing water and environmental efficiency of animal feed, which in turn reduces enteric methane resources, allowing for a reduction of greenhouse gas emissions emissions (Dickie et al., 2014). Legumes also contribute Nitrogen and deforestation levels. This focus is particularly important (N) to the soil through symbiotic N fixation that improves both for the Orinoquía, which is recognized for its strategic soil fertility and forage persistence (Rao et al., 2014; Villegas et al., environmental importance with ecosystems of high conversation 2020). According to Fisher et al. (1994), the association of deep- value, such as natural savannas, flooded forests, humid forests, rooted grasses with nitrogen-fixing legumes has three important foothills, estuaries and wetlands. The need to achieve more effects, namely (i) increased nutrient cycling, (ii) improved efficient cattle farming without affecting natural ecosystems is animal production, and (iii) increased soil biological activity, and enshrined in the most recent Regional Climate Change Plan for thus play a key role in restoration, stabilizing the global carbon the Orinoquía (CIAT CORMACARENA, 2018), which is aligned cycle and reducing greenhouse gas emissions. In addition to that, with the national approaches defined in the Strategic Plan for the they provide many other ecosystem services, such as improved Colombian Cattle Sector from 2019 (FEDEGAN, 2018)1. soil structure, water infiltration, increased carbon accumulation, This context is likely to aggravate under a climate change favored biological activity, and contributions to weed control and scenario that would accelerate soil degradation processes (Olsson soil conservation (Jensen et al., 2012; Schultze-Kraft et al., 2018). et al., 2019), especially when combined with unsustainable As part of the research efforts to identify forage legumes land use or poor management practices (Sattler et al., 2018). adapted to the specific conditions of temporary water saturation According to the climate projections for the Orinoquía to 2100, in the Orinoquía foothills, AGROSAVIA started evaluating annual precipitation will decrease and maximum temperatures 22 promising legumes in 2013. After 3 years of agronomic will increase, leading to periods of more extreme heat and heat evaluations, Arachis pintoi CIAT 22160 cv. Centauro (Centauro) stress (IDEAM, 2015). These forecasts would affect livestock was selected as the most promising material for release. It production mainly through (i) changes in biomass production presents desirable characteristics in both productive terms (e.g., and quality of forages, which translates into a decrease in milk good nutritional quality, less weed presence, greater foliar and meat production, and (ii) heat stress in animals, which leads area, absence of pests and diseases) and environmental terms to significant losses in production, growth, development and (e.g., better soil coverage and, consequently, less susceptibility to soil erosion) and has high potential for integration in 1FEDEGAN: Federación Colombiana de Ganaderos, Colombian Cattle silvo-pastoral systems (shade tolerance) (Rincón et al., 2020). Federation. These characteristics make Centauro a good alternative for Frontiers in Sustainable Food Systems | www.frontiersin.org 429 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems the purposes of sustainable intensification and restoration of projection of economic returns is carried out considering degraded pastures in the region. When it comes to new changes in forage characteristics (drymatter production) for both technologies, however, land-use and adoption decisions by production systems as a response to changes in projected climatic the livestock producer are mainly based on the profitability variables, according to the climate change scenarios for the promises that the technology can generate (Pannell et al., 2006). Representative Concentration Pathways of the region (RCP 2.6 Profitability is a fundamental attribute to incentivize or generate and 8.5; IDEAM, 2015). It also includes potential effects on price adoption, information which, in many cases, is not available variations as a consequence of recurring climatic events (El Niño to the livestock producer or the extension agents supporting and La Niña). With this information, profitability indicators for decision-making processes. Profitability is not, however, the only each system (e.g., Net Present Value, Internal Rate of Return) are measure since other factors exist that contribute to incentivizing calculated and help in the identification of the treatment with or discouraging the adoption of new technologies, such as better adaptability under climate change scenarios. cultural, behavioral or environmental factors. Regarding economic studies on the inclusion of Arachis pintoi in livestock systems, limited advances have been made so far. Research on Arachis pintoi in the Most of them were carried out by the International Center Neotropics for Tropical Agriculture (CIAT) in Latin America more than Historical Review: Technical Evaluation Processes of two decades ago. These studies mainly dealt with measuring Arachis pintoi in Colombia the effects on different economic indicators of the inclusion The evaluation of Arachis genotypes in Colombia began in of Arachis pintoi CIAT 17434 in grazing systems. Rivas and 1978 with the introduction of 45 accessions from germplasm Holmann (2000) evaluated changes that occurred between 1986 collections in the U.S. [i.e., from the University of Florida and the and 1997 in productive and economic indicators in farms in the United States Department of Agriculture (USDA)] by CIAT to Colombian Caquetá Department that were early adopters of the its Carimagua Research Center in the Orinoquía region (Rincón Arachis pintoi CIAT 17434 variety. According to their results, et al., 1992). These accessions have been wild-collected since production levels of both meat and milk more than doubled 1981 by USDA, EMBRAPA (Empresa Brasileira de Pesquisa with the inclusion of the legume, reflected in higher gross yields Agropecuária) and CIAT (Valls and Pizarro, 1995). Arachis per hectare (6%) and animal (20%). Based on these results, species are present in countries such as Brazil (more than 60 wild the same authors carried out an ex-ante evaluation estimating species), Bolivia (15), Paraguay (14), Argentina (6), and Uruguay an Internal Rate of Return (IRR) of between 19.3 and 21.1% (2) (Valls and Pizarro, 1995). resulting from the inclusion of the legume—which equates to From 1987 to 1990, CIAT (in collaboration with other an increase compared to the traditional production system (IRR institutions) worked on the selection ofArachis pintoi germplasm = 12%). Evaluations in Costa Rica estimated a 30% reduction with potential for adaptation to acid soils and to restore in production costs per kilogram of milk associated with the large areas of degraded pastures in the Colombian Caquetá inclusion of Arachis pintoi and Cratylia (Peters et al., 2001). Also Department. The grass-legume association of Arachis pintoi in Costa Rica, Jansen et al. (1997) estimated an IRR of 122% in with various species of Brachiaria was identified as the most a well-managed grass-legume association of Brachiaria brizantha promising solution (Lascano et al., 2005), and after several years and Arachis pintoi. For the Amazon region of Brazil, Valentim of research, the variety Arachis pintoi CIAT 17434 (perennial and Andrade (2005) estimated a gross profit per year of US$ forage peanut) was released in 1992. The variety is characterized 4,000 generated by the adoption of Arachis pintoi by ∼1,000 by its good adaptation to climate and soil conditions in the cattle producers. According to our literature review, neither more Colombia Orinoquía but also has some important limitations recent economic analyses nor any quantitative risk assessments such as slow establishment, low forage production during the or climate change impact estimates were found forArachis pintoi, first 2 years and high defoliation rate in the dry season (Rincón, nor the new CIAT 22160 Centauro variety. Our study therefore 2001). In an attempt to solve these problems, the evaluation of contributes to closing an important knowledge gap and provides new Arachis pintoi accessions was taken up in 1994 in various updated information on the new Centauro variety, released in South American countries (Colombia, Brazil, Ecuador, Peru and 2020, in order to facilitate dissemination and adoption processes Bolivia). The accession CIAT 22160 was among the evaluated for the actors involved (e.g., cattle producers, extension agents, materials. This accession is native to Brazil, was found in the development agencies or donors). eastern Andes, between the Amazon and La Plata rivers, and In this sense, the objective of our study is to evaluate the was collected in 1992 by the researcher Wantuil Werneck and economic viability of milk production in a dual-purpose cattle delivered to the CIAT gene bank by EMBRAPA (Brazil). system in the foothills region of the Colombian Orinoquía The first evaluations of this material were made in Brazil in under a grass-legume association with Brachiaria humidicola cv. 1994 together with another 49 Arachis pintoi accessions. CIAT Humidicola and Arachis pintoi CIAT 22160 cv. Centauro (grass- 22160 stood out for presenting high persistence during the dry legume association). We compare these results with a traditional season (CIAT, 1994). In Colombia, the earliest evaluation records production system under a Brachiaria humidicola cv. Humidicola of CIAT 22160 were documented by Moreno et al. (1999), monoculture (grass monoculture). In order to estimate economic Cárdenas et al. (1999), and Peters et al. (2000) as part of a indicators, we used a cashflow model and conducted a multilocational trial with several Arachis pintoi accessions. The risk assessment using a Monte Carlo simulation model. The objective was to find alternatives to Arachis pintoi CIAT 17434 Frontiers in Sustainable Food Systems | www.frontiersin.org 530 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems (perennial forage peanut) with higher adaptability. The evaluated TABLE 1 | Animal response data for the grass-legume association and grass accessions were acquired by CIAT between 1993 and 1994 from monoculture. EMBRAPA-CENARGEN (Brazil) and the National Institute of Variable Grass-legume association Grass monoculture Agricultural Technology (INTA, Argentina) (CIAT, 1994). The (Mean ± SD) (Mean ± SD) experiments were established between 1994 and 1995 in different locations: (i) 39 accessions in a tropical dry forest (Moreno et al., Biomass production (kg 919 808 DM−1 ha−1 y−1 1999), (ii) 41 accessions in a very humid premontane forest ) (Cárdenas et al., 1999), and (iii) 61 accessions in a very humid Crude protein (%) 9.2 6.6 forest ecosystem (Peters et al., 2000). Accession CIAT 22160 was Neutral Detergent Fiber 65 75 identified as promising material for very humid tropical forests, (NDF, %) with superior characteristics to the control variety (Arachis Acid Detergent Fiber 30 38 (ADF, %) pintoi CIAT 17434), such as greater rooting, faster growth, Degradability (%) 67 64 higher dry matter production and a more efficient use of Stocking rate (AU2 ha−1) 2 1.5 Phosphorus (CIAT, 2002). The first evaluation of CIAT 22160 in the Colombian Orinoquía was conducted by Rincón (2001) Milk production (l AU−1 6.5 ± 1.34 5.7 ± 1.28 d−1) with 11 Arachis pintoi accessions (Arachis pintoi CIAT 17434 as Milk production (l ha−1 13 ± 2.68 8.5 ± 1.92 control variety). Rincón (2001) established two experiments at d−1) the CORPOICA (now AGROSAVIA) research center La Libertad in the Meta Department on poorly drained soils, leading to a DM, Dry Matter; AU, Animal Unit. Source: Own elaboration based on the study carried out by Rincón et al. from 2016 to preselection of the three best performing accessions according to 2020 (Rincón et al., 2020). The technical parameters obtained by Rincón et al. were used their agronomic performance: Arachis pintoi 22160, 18748, and for the economic evaluation presented in this article. 18744. All three accessions stood out for their high dry matter production (>1 ton/ha) and level of soil cover (>70%) (Rincón, 2001). daily milking time at an amount of 2 kg/animal/d for ∼180 days a year. In order to maintain pasture productivity levels, Evaluation of Arachis pintoi CIAT 22160 Under maintenance fertilization and weed control were performed once Temporary Flooding Conditions a year for both treatments. Diammonium Phosphate (DAP) In 2013, CORPOICA (now AGROSAVIA) started the evaluation (100 kg ha−1) and Sulgamac (100 kg ha−1) were applied for of Arachis pintoi under temporary flooding conditions in the the grass-legume association. For the grass monoculture urea Orinoquía (Rincón and Pesca, 2017). Trials were established (100 kg ha−1) was added to DAP and Sulgamac. The results at the research center La Libertad in the Meta Department of these measurements (biomass production, nutritional quality under medium drainage conditions and included 22 Arachis and animal response) for each treatment are presented in pintoi accessions. Each accession was established in plots with Table 1, since our economic analysis is based on these technical an area of 6 m2, in a complete random block design with three parameters obtained in the study by Rincón et al. (2020), repetitions. From 2013 to 2014, a series of agronomic evaluations previously described. were carried out that led to the preselection of four accessions (22160, 18748, 18744, and 17434) which were then evaluated General Characteristics of Arachis pintoi CIAT 22160 at the agronomic level during both the dry and rainy seasons. cv. Centauro After another year of evaluation, the Arachis pintoi CIAT 22160 Arachis pintoi CIAT 22160 was identified by AGROSAVIA as was selected for grazing trials as a result of its outstanding a promising material to improve the quality of cattle feed in attributes of soil cover, persistence, competition with weeds, the Colombian Orinoquía, especially under poorly drained soil forage production and nutritional quality. conditions (Rincón et al., 2020). It was released in 2020 under The grazing trials were carried out from February 2016 to the common name Centauro (Arachis pintoi CIAT 22160 cv. April 2017 at the farm Los Arrayanes, and from October 2019 Centauro), but its commercialization will only begin in 2022 to February 2020 at the farm El Recreo, both located in the in accordance with private sector seed production schedules. Orinoquía region and presenting temporary flooding conditions. Centauro is a perennial herbaceous forage legume with prostrate The accession CIAT 22160was established in August 2015 in both growth. It has an average height of 20 cm and a leaf-stem ratio locations with vegetative material, in an area of 2000 m2 and in of 1.4 (60% leaves and 40% stems) (Rincón et al., 2020). Its association with the grass Brachiaria humidicola cv. Humidicola flower is generally self-pollinated but can also be cross-pollinated (grass-legume association). Productivity results were compared by bees. The first flowers appear at a plant age of 14–55 days with data obtained from a monoculture grazing trial with the (Simpson et al., 1995). Centauro has a wide range of adaptation, grass Brachiaria humidicola cv. Humidicola (grass monoculture). from low acid soils to high fertility soils, with a soil texture Animal productivity was measured in lactating cows under a ranging from sandy loam to clay loam and with good or poor dual-purpose system. The animals were supplemented, in both drainage. In addition, it grows well in tropical regions from 0 treatments (grass monoculture and grass-legume association) to 1,800m elevation and with an annual rainfall between 1,200 with 8% mineralized salt at an amount of 80 g AU−1 d−1 and 4,000mm. It is characterized by a high biomass production throughout the year. Cut grass silage was supplied during the and forage quality (Table 1), and its leaf crude protein levels vary Frontiers in Sustainable Food Systems | www.frontiersin.org 541 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems between 15 and 18%. It adapts well in association with invasive with ruminal fermentation processes (higher nutritional quality Gramineae or in silvo-pastoral systems (good shade tolerance), of the forage) and the application of nitrogen fertilizers, while has strong persistence, competes with weeds, and is tolerant contributing to the intensification of cattle systems through to several pests and diseases. Its prostrate and invasive growth productivity and increases in animal carrying capacity (Rincón results in soil cover levels of >90%, favoring the reduction of soil et al., 2020). compaction and erosion (Rincón et al., 2020). MATERIALS AND METHODS Potential Ecosystem Services of Arachis pintoi CIAT 22160 cv. Centauro Discounted Cash Flow Model The inclusion of Centauro in forage-based livestock systems has The present study’s economic analysis is based on a discounted high potential regarding the provision of ecosystem services. In cash flow model and the estimation of profitability indicators, grazing systems, different studies have shown a high persistence such as Net Present Value (NPV) and Internal Rate of Return of Arachis pintoi with positive effects on soil conservation (IRR). These indicators are obtained assuming the most probable and improving soil conditions (Rincón, 1999; CIAT, 2004; values of the model variables (associated with benefits and Castillo-Gallegos et al., 2005; Robertson, 2005; Valentim and costs). The analysis is carried out by comparing the profitability Andrade, 2005). These positive effects are mainly associated indicators for the grass-legume association and the grass with high production of seed below ground, a prostrate growth monoculture. The cash flow allows ordering and synthesizing habit that invades bare soil, as well as tolerance to trampling the sequence of income, costs and investments associated with and defoliation, protecting the arable soil layer and, therefore, the evaluated technologies. The following cost categories were avoiding degradation and erosion processes (Rincón, 1999; considered: total costs of establishment and maintenance of Rincón et al., 2020). Under animal grazing trials, grass-legume each treatment, opportunity costs of capital and operating costs associations with Arachis pintoi have not shown signs of (animal health, supplementation, permanent and occasional degradation after several years of grazing (e.g., Lascano, 1994; labor). The benefits are derived from milk production in a dual- Rincón, 1999; Valentim and Andrade, 2005). Arachis pintoi has purpose system, according to the animal response indicators positive effects on the soil organic matter content and soil obtained for each treatment (Table 1). biodiversity (Rincón, 2001), improving the physical, chemical and biological soil conditions and avoiding erosion associated Model Assumptions with overgrazing, but may reduce above ground biodiversity. For the construction of the cash flow it is necessary to Arachis pintoi can also improve the persistence of the associated establish different economic and technical assumptions. The grasses resulting from a symbiotic nitrogen fixation to the following sections provide detailed explanations for each soil, which is then used by the grass (Villegas et al., 2020). of them. For example, Dubeux et al. (2017) estimated a range of 123 to 280 kg ha−1 yr−1 Technical Assumptions of fixed nitrogen in six Arachis pintoi Given that productivity was measured only for daily milk accessions, and Pereira et al. (2019) evaluated beef production in production (see section Research on Arachis pintoi in the an associated system of Brachiaria brizhanta and Arachis pintoi Neotropics), the other technical indicators are assumed to be (cv. Belomonte), estimating a minimum nitrogen fixation of the same for both treatments and were described by consulting 120 kg ha−1 yr−1. The higher contribution of nitrogen not only average values reported for the study region: (i) 550 days calving represents a strategy for the restoration of degraded pastures, interval; (ii) calf age of 9 months and weight of 150 kg at weaning; but also contributes to reducing the use of nitrogen fertilizers and (iii) lactation time of 8.5 months. AGROSAVIA researchers and, therefore, to reducing nitrous oxide emissions. Other studies verified these indicators for the region. focused on estimating the effect of Arachis pintoi accessions on carbon levels and other elements in the soil. Nutrient uptake Evaluation Horizon in Brachiaria humidicola monoculture pastures and in grass- The evaluation horizon is established according to the expected legume associations of Brachiaria humidicola and Arachis pintoi lifespan of a technology under evaluation. For the evaluation of in acid soils with low fertility was, for example, measured in the grass-legume association and the grass monoculture, a period the Orinoquía, showing that the inclusion of Arachis pintoi of 10 years (2020–2029) was defined, which is in accordance increased the nitrogen, calcium, potassium and phosphorus with the productive lifespan for improved pastures (Riesco and availability in the soil by 130, 133, 19, and 13%, respectively Seré, 1985). It is, however, worthwhile mentioning that improved (CIAT, 1994). In evaluations in the Atlantic coast of Costa pastures can have a much longer productive lifespan if managed Rica and the humid forest of the Colombian Amazon, different adequately (e.g., in terms of grazing and fertilization). grass-legume associations with Arachis pintoi showed statistically higher levels of carbon reserves in the soil than in the native Discount Rate forest (Amézquita et al., 2004). In the Orinoquía, the inclusion The cost of financing is chosen as the discount rate according of Arachis pintoi in a Brachiaria humidicola pasture notably to the rural credit lines of FINAGRO (the Colombian Fund for increased the amount of carbon in the soil (CIAT, 1994). Arachis the Financing of the Agricultural Sector). This financing cost pintoi also helps in reducing greenhouse gas emissions associated is considered the opportunity cost of capital and is associated Frontiers in Sustainable Food Systems | www.frontiersin.org 552 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems with a risk factor present in the activities of the rural sector. The Quantitative Risk Analysis following discount rate was therefore established: DTF (fixed- Risk is defined as the possibility that the real return on term deposit rate) + 5% effective annual interest rate. The an investment is less than the expected return (Park, 2007). projection of the discount rate in the corresponding periods was Profitability is therefore associated with the variability of made following the DTF projections according to the Annual revenue and cost streams, and these in turn depend on the Report on Economic Projections Colombia 2020 (Bancolombia– randomness of the main variables of the investment project Dirección de Investigaciones Económicas, 2020). (e.g., yields, market prices). Rural investment projects involve particular risks, and their results depend on a broad set Permanent Labor of variables which, in many cases, cannot be controlled by The required permanent labor is defined according to the the investor/producer (e.g., climatic factors). In this sense, weighting factors for labor established by FEDEGAN (2003). In it is necessary to incorporate risk levels associated with the a dual-purpose cattle system, 4.8 permanent jobs are needed profitability indicators for each of the evaluated investment for every 100 animals. The minimum salary for 2019 was alternatives. For this purpose, we apply aMonte Carlo simulation used, including transportation assistance, contributions to social model. The accuracy of simulation models depends on the security, and social and parafiscal benefits, adding up to US$ quality of the input data. In this study, for example, the milk 422 per month. For salary projections during the period of production data under each treatment was derived from on- analysis (2020–2029), the following was assumed: Variation of the farm measurements carried out during representative periods minimum salary (in %) = expected inflation (in %) + observed (i.e., rainy and dry seasons; section Evaluation of Arachis variation of workforce productivity (WP, in %). A WP of 1% is pintoi CIAT 22160 Under Temporary Flooding Conditions). We assumed, according to historical estimates from national statistics consider this data reliable, reflecting the distribution and real (DANE, 2020a). behavior of the variable observed by the technical team. Cost data and possible variations of its values were constructed with Currency at Current Prices experts from AGROSAVIA according to the real conditions Inflation is considered for estimating revenue and cost streams of cattle producers in the region in terms of prices and during the evaluation period. For revenues, the projection of quantities used. the Consumer Price Index (CPI) estimated by Bancolombia– Dirección de Investigaciones Económicas (2020) for the period 2020-2023 was considered. For production costs, the Producer Monte Carlo Simulation Model Price Index (PPI) estimated by DANE (2020b) was used. Monte Carlo simulation is a method in which a random Milk Price. Price information was obtained from the Milk sample of results is generated for a specific probability Price Monitoring Unit (USP) for the predefined Region 2, where distribution (Park, 2007). This method allows potential investors dual-purpose production systems predominate (MADR/USP, or decision makers to see all the possible results and to 2020). The prices were projected according to the CPI evaluate the impact of risk on profitability indicators in projections. Additionally, we included projections for the effect investment projects. To perform the simulation, it is necessary of extreme climatic events (El Niño and La Niña phenomena) to determine the random input variables (those that can on milk price variations. Abril et al. (2017) quantified climate have more than one possible value) and the possible range impacts on food inflation in Colombia. According to their results, values for each. These variables are assigned a probability after the occurrence of an El Niño or La Niña phenomenon, distribution, to later calculate the determined profitability food inflation increases significantly between four and 5 months indicators. Monte Carlo simulation was performed with the later (increasingly when the intensity of the phenomenon is software @Risk (Paladise Corporation). For the evaluated strong), and its response is asymmetric depending on the impacts treatments, 5,000 iterations were performed with a confidence and size of the shock. This directly affects the income received level of 95%. by producers and household purchasing power in Colombia. Regarding milk prices, variations have been >7% in the years with such climatic events, compared to variations of<1% in years Decision Criteria without (DANE, 2020a,b). The variation margin of the CPI was As decision criteria, the mean values and the variance assumed for the occurrence climatic phenomena as follows: (i) of the profitability indicators resulting from the simulation the spread of the CPI vs. the CPI of milk in 2018 was assumed as are used: Net Present Value (NPV) and Internal Rate of the spread that the price of milk would have against the national Return (IRR) [Equations (1, 2)]. The use of the mean CPI for a scenario where no climatic phenomenon occurs; (ii) the value criterion is based on the law of large numbers, which spread of the CPI vs. the milk CPI of 2015–2016 was assumed as establishes that, if many repetitions of an experiment are the spread that the price of milk would have against the national carried out, the average result will tend toward the expected CPI for a scenario where a climatic phenomenon occurs; (iii) value (Park, 2007). The variance of the indicators determines variations in the CPI of 7% with a climatic phenomenon and the degree of spread or dispersion on both sides of the <1% without are considered (Figure 1); and (iv) both the CPI mean value (Park, 2007). That is, the lower the variance, and CPI for milk were obtained from DANE (DANE, 2020b,c). the lower the variability (loss potential) associated with Frontiers in Sustainable Food Systems | www.frontiersin.org 563 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems FIGURE 1 | Consumer Price Index (CPI) and Producer Price Index (PPI) behavior of milk in the face of climatic events. Source: Own elaboration based on DANE (2020b,c). the indicators. Simulated Variables n The study considers how sensitive the economic results are to ∑ E(FCt) NPV(Mean) = (1) changes in the main variables of the model. Table 1 shows the (1+ r)t t=0 variables identified as risk variables and the distributions and n parameters used for modeling them. For modeling the milk ∑ E(FCt) IRR(Mean) = (1+ r∗)t = 0 (2) production variable for the grass-legume association and the t=0 grass monoculture, a distribution adjustment of the data was performed with @Risk. Where, E (FCt): Expected value of the net profit flow for period t Var (FCt): Net profit flow variance for period t. Economic Evaluation Under Climate r: Real discount rate Change Scenarios RCP 2.6 and 8.5 r∗: Internal rate of return Forage Production Under Climate Change Scenarios t: Evaluation horizon of the project The effect of climate change on livestock productivity was The NPV at risk indicator (VaR) is also estimated and the determined by comparing forage biomass production under a probability of success of the evaluated investments is estimated baseline (current) scenario with estimated levels under climate (Prob NPV (mean) > 0). The VaR is defined as the maximum change scenarios. We used two climate change scenarios for the expected loss that the project could suffer from investment in region: RCP 2.6 and RCP 8.5 (Armenta et al., 2015). To identify a time interval and with a certain level of confidence (Park, the main environmental factors that affect the productivity of 2007). The probability of success is defined as the proportion the evaluated treatments, as well as the magnitude of the effect, of positive results of all interactions (NPV > 0, the project an analysis of variance (ANOVA) was performed. The delta is economically viable). A sensitivity analysis was performed identified in both climate change scenarios was applied to each using a tornado graph, which sensitizes each variable in order to of these environmental factors, to estimate the monthly biomass measure its impact on the profitability indicators and to identify production per hectare. This delta refers to the change in climatic within the critical variables those with the greatest effects on the variables between one scenario and another. It is important to profitability indicators. note that the model is only considering changes in the climatic Frontiers in Sustainable Food Systems | www.frontiersin.org 574 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems TABLE 2 | Variables simulated with the Monte Carlo model. # Variable Distribution Most likely value Lower limit Upper limit 1 Milk price (US$ l−1 ) Triangular 0.35 0.33 0.36 2 Productivity milk GLAa (l d−1) Pert 6.5 5.16 7.84 3 Productivity milk GMb (l d−1) Pert 5.7 4.42 6.98 4 Establishment costs GLA (US$‘ha−1) Triangular 642 578 706 5 Establishment costs GM (US$ ha−1) Triangular 450 405 495 6 Periodicity of El Niño phenomenon (y) Discrete uniform n/a 2 7 7 Variation of the discount rate (%) Triangular 0 1 2 8 Variation IPC (%) Triangular −0.5 0 0.5 aGLA, grass-legume association; bGM, grass monoculture. variables of the RCP, keeping constant the assumptions of pasture TABLE 3 | LIFE-SIM model inputs for the animal component. and soil management, level of technology, investment in labor and animal characteristics. Variable Value In addition to possible changes at the productive level of the forage species, the change in environmental conditions under (A) Existing information climate change scenarios can alter the potential distribution of Calving interval (days) 550 plant species. In other words, the species would tend to modify Calf weaning age (months) 9 their distribution toward latitudes and altitudes different to those Calf weaning weight (kg) 150 where they are currently found (Walther et al., 2005). To identify Lactation time (months) 8.5 this possible effect, themaximum entropymodelMaxent (version Number of lactations 9–10 3.4.1; Phillips et al., 2021) was used. The model makes it possible Weight (kg AU−1) 400 to estimate the extent of future environments and to determine, (B) Estimated information in the case of the legume Arachis, if and where conditions similar Age of animals (years) 3 to the current environments exist. Weight after delivery (kg) 380 The Maxent model requires two input streams: (i) points Duration of gestation (days) 282 of presence (distribution) of the species throughout the world Birth weight (kg) 28 and, (ii) bioclimatic variables. The current distribution points of Weight loss during lactation (%) 8 Arachis were downloaded from Global Biodiversity Information Expected weight at next delivery (kg) 412.2 Facility (GBIF.org, 2020) with more than 600 points of presence Fat content of milk (%) 3 which, after cleaning outliers and anomalous data, reached Protein content of (%) 3.1 just over 300 total points. The second input of the Maxent Non-fat solids content of milk (%) 8.7 model were the bioclimatic variables for RCP 2.6 and 8.5 Animal fur thickness (mm) 2 obtained from Navarro-Racines et al. (2020). These variables represent annual trends (e.g., mean annual temperature and precipitation), seasonality (e.g., annual ranges of temperature and precipitation) and extreme or limiting environmental Economic Evaluation Under Climate Change factors (e.g., temperature of the coldest and warmest month, Scenarios precipitation of humidity). Based on the results of milk production under the climate change scenarios (Table 7) and according to the methodology presented Milk Production Under Climate Change Scenarios in sections Evaluation of Arachis pintoi CIAT 22160 Under Based on the forage production estimates under climate change Temporary Flooding Conditions and General Characteristics scenarios (section Potential Ecosystem Services of Arachis of Arachis pintoi CIAT 22160 cv. Centauro, the profitability pintoi CIAT 22160 cv. Centauro), milk production estimations indicators were estimated for both treatments. Figure 2 shows were performed in the LIFE-SIM model (version Dairy 15.1), how the different models used in this study are interlinked developed by the International Potato Center (CIP; León- (Maxent, LIFE-SIM and economic models). Velarde et al., 2006). In this model, milk production estimations are based on the characteristics of the animals, forages and RESULTS climatic conditions (temperature, humidity and wind speed) (León-Velarde et al., 2006). Tables 2, 3 and 4 present the Discounted Cash Flow Model information used in the model. The analysis did not consider Table 5 shows the average costs and revenues for the grass- episodes of heat stress in the animals, which could also affect legume association and the grass monoculture, respectively. The milk production. models include the variable costs and revenues associated with Frontiers in Sustainable Food Systems | www.frontiersin.org 585 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems TABLE 4 | LIFE-SIM model inputs–climatic variables. Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Average temperature (◦C) C.S.a 26.1 26.6 26.7 25.7 25.4 24.8 24.6 25 25.5 25.5 25.7 25.6 RCP 2.6 28.3 28.7 28.6 27.6 27.3 26.5 26.4 27 27.3 27.6 27.7 27.5 RCP 8.5 28.6 29.2 29 27.9 27.6 26.9 26.7 27.3 27.7 27.9 28 27.9 Wind speed (km/h) C.S. 6 6.3 5.6 5 4.6 4.8 4.9 4.5 4.9 4.5 4.5 5.4 RCP 2.6 6.4 6.8 6.0 5.4 4.9 5.2 5.3 4.8 5.3 4.8 4.8 5.8 RCP 8.5 6.5 6.9 6.1 5.4 5.0 5.2 5.3 4.9 5.3 4.9 4.9 5.9 Humidity (%) C.S. 68.5 62.3 74.7 81.5 84.1 85.5 81.9 82.8 78.5 79.6 80.5 78.6 RCP 2.6 74.0 67.3 80.7 88.1 90.8 92.3 88.5 89.4 84.7 86.0 86.9 84.9 RCP 8.5 74.8 68.1 81.6 89.1 91.9 93.4 89.4 90.4 85.7 87.0 87.9 85.9 aC.S., Current Scenario. FIGURE 2 | Interdependence of the models used in this study (Maxent, Life-Sim, and economic models). the establishment of each technology under a dual-purpose of milk is US$ 0.23 for the grass-legume association and US$ production system. The revenue results from the sale of raw 0.31 for the grass monoculture, respectively, representing 35% milk and the sale of weaned calves (150 kg) every 550 days lower costs for the grass-legume association. The average net (calving interval). According to average daily milk production, profit for the year is US$ 212 for the grass-legume association and the inclusion of Centauro in the system (grass-legume) allowed US$ −6.95 for the grass monoculture. Under these assumptions, an increase in milk production per hectare by, on average, 52% production under the grass monoculture is unprofitable, a when compared to grass in monoculture. Particularly during the consequence of the low productive indicators associated with months of minimal rainfall (dry season from January to March), this alternative. It is important, however, to highlight the social grass-legume showed greater persistence and, consequently, a connotation of dual-purpose systems in the country: given the more stable milk production. The average production was cash flow provided by the sale of raw milk, its high nutritional 2,373 l ha−1 yr−1 for the grass-legume association and 1,560 l value and the relatively low barriers for getting involved in the ha−1 yr−1 for the grass monoculture, respectively. This is business, it is still an attractive alternative for many producers, equivalent to a gross income from raw milk sales of US$ 822 from which they derive the subsistence for their family. This and US$ 518, respectively, representing a 58% increase for the exercise includes the required labor costs (permanent and grass-legume association. occasional), valued at the minimum salary (plus benefits). These Regarding production costs, labor (63%) makes up the largest costs could, however, reflect the opportunity cost of family share, followed by inputs for pastures (21%), supplements (8.5%), labor that, in many cases, is not accounted for within the cost drugs (1.2%), and other costs (5%). The unit production cost structures, but rather represents part of the household income. Frontiers in Sustainable Food Systems | www.frontiersin.org 596 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems TABLE 5 | Summary of main costs and revenues for the grass-legume association and the grass monoculture. Economic indicators Grass-legume association Grass monoculture Milk production (l ha−1 y−1) 2,373 1,560 Gross income from milk sales (US$ ha−1 y−1) 834.2 548.6 Gross income from weaned calf sales (US$ ha−1 y−1) 489.5 257.0 Pasture establishment costs (US$ ha−1)a 642 450 Production costs (US$ ha−1 y−1) 787.9 699.7 Net income system (US$ ha−1 y−1) 212.0 −7.0 Unit cost of milk production (US$ l−1) 0.2 0.3 Milk income (US$ l−1) 0.3 0.3 Milk profit margin (US$ l−1) 0.1 0.0 Unit cost of calf production (US$ kg−1) 1.2 1.5 a Includes the costs associated with soil analysis, machinery rental, inputs and labor required for soil preparation, fertilization, weed control, and planting of the material for both treatments. Vegetative material and labor costs for planting the legume are added to the items required for the establishment of a grass in monoculture. TABLE 6 | Profitability indicators of the simulation model for the grass-legume TABLE 7 | Changes in milk production under climate change scenarios. association and the grass monoculture. Treatment Scenario Milk production, Milk production, Decision criterion Indicator Grass-legume Grass dry season rainy season association monoculture (average liters per (average liters per AU−1 d−1) AU−1 d−1) NPV (US$)* Meana 121 (941) SDb 391 276 Grass-legume C.S.a 5.49 5.59 association CV 3.24 0.29 2050 RCP 2.6 4.2 5.4 VaR (902) (1,637) 2050 RCP 8.5 3.66 4.53 Prob < 0 (%) 60.9 100 Grass C.S. 4.97 5.1 IRR (%) Mean 12.2 – monoculture aMean value of the NPV obtained in the simulation (5,000 iterations). 2050 RCP 2.6 1.83 2.93 bSD, Standard deviation of the NPV with respect to the mean value. *Prices in US$- 2050 RCP 8.5 1.63 2.35 US$/COP XRT: Average 2019. aC.S., Current Scenario. Profitability Indicators and Risk Analysis The summary of the main financial indicators obtained from has with the NPV profitability indicator. As can be seen, the the Monte Carlo simulation is presented in Table 6 Under the profitability of the treatments measured by the NPV indicator assumptions used in the model and according to the indicator is highly sensitive to changes in the milk production variable coefficient of variation (CV) and VaR, the inclusion of Centauro for both treatments. The correlation between the NPV indicator in the grass-legume association allows better economic and lower and the milk production variable is positive, which means that risk indicators to be obtained when compared with Brachiaria changes in daily production affect the indicator bymore than 90% humidicola cv. Humidicola as amonoculture. The results indicate for both treatments. This results from the high dependence on that the investment in the establishment of the grass-legume the income generated frommilk production and the productivity association is profitable, with an average NPV of US$ 121 and levels in this system. an IRR of 12.2%. Regarding the probability of not obtaining financial feasibility, Economic Evaluation Under Climate the results of the NPV probability distribution are presented in Figure 3 and reflect the amplitude of the variation for the Change Scenarios RCP 2.6 and 8.5 NPV indicator. For the grass-legume association, in 60.9% of Forage Production Under Climate Change Scenarios the scenarios generated during the simulation, an NPV > 0 was The estimates for dry matter production for the evaluated climate obtained, whereas for the grass monoculture, the investment was change scenarios are presented in Figure 5. According to the not profitable under any of the generated scenarios. results, changes in the climatic variables in the RCP scenarios have notable impacts on the productivity of both treatments. For Sensitivity Analysis the grass-legume association, biomass production was reduced, Figure 4 shows the contribution of different input variables to the on average, by 7.74 and 16.62% under RCP 2.5 and 8.5, NPV variance as result of the simulation. These graphs represent respectively. For the grass monoculture, the reductions were the correlation that each input variable simulated in the model 14.95 and 35.27% under RCP 2.5 and 8.5, respectively. The most Frontiers in Sustainable Food Systems | www.frontiersin.org 1570 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems FIGURE 3 | Probability density distributions for NPV for the grass-legume association and the grass monoculture. GLA, Grass-legume association; GM, Grass monoculture. influential environmental factors on productivity were average In the case of the grass monoculture, the change in climatic temperature and bio32 for the grass-legume association and variables would cause a reduction of milk production during dry precipitation73 and bio3 for the grass monoculture. season of 63 and 67% for RCP 2.6 and RCP 8.5, respectively. In addition to the possible changes at the productive level of During rainy season, the effect on productivity would be above Arachis, projected changes in environmental conditions under 40% for both RCP scenarios. climate change scenarios can alter its potential distribution. According to the results of the Maxent model, under RCP 2.6 Profitability Indicators Under Climate Change (until 2050) a shift of suitable areas for Arachis toward higher Scenarios altitudes would occur (Figure 6), meaning a decrease in their The reduced milk production under both climate change suitability for lower altitudes like the foothills or savannas. Under scenarios leads to a leftward shift of the distribution curves for RCP 8.5, in addition to the described shift of suitable areas, a the NPV indicator in both treatments, when compared to the total reduction of the potential area for Arachis would occur current scenario (Figure 7). The net income is reduced by 60 (Figure 6). and 90% for the grass-legume association, and 113 and 131% for the grass monoculture under the scenarios RCP 2.6 and RCP Milk Production Under Climate Change Scenarios 8.5, respectively. Although including Centauro in the system has The effects of the climate change scenarios on forage biomass highly positive effects at the productive level and therefore on production translate into a strongly marked decrease in milk the economic performance, both climate change scenarios would production for both treatments (Table 6). For the grass-legume affect the system in such a strong way that the investment in any association, during the first 3 months of the year (dry season) of the treatments would not be profitable. and compared to the current scenario, a decrease of close to 23% would occur under RCP 2.6 and 33% under RCP 8.5, respectively. DISCUSSION These reductions are less marked during the rainy season but are still relevant for the low production volumes under this system. The inclusion of the legume Arachis pintoi CIAT 22160 cv. Centauro in a monoculture of Brachiaria humidicola cv. 2bio3 is a percentage indicator that shows the variability of the diurnal temperature Humidicola allows an improvement in the technical parameters range with respect to the annual temperature range. Bio3 = (Bio2/Bio7)∗100; of the production system and results in better economic Where: Bio2 = Mean Diurnal Range [Mean of monthly (max temp – min temp)] indicators. At the productive level, this association increased and Bio7 = Temperature Annual Range (Max Temperature of Warmest Month – daily milk production by 14% on average and the animal stocking Min Temperature of Coldest Month). 3precipitation 7 is a continuous variable representing the amount of rainfall per rate by 33% compared to the monoculture. This results from m2 at a geographic point during the seventh month of the year (July). the higher crude protein content of the diet (39%), the higher Frontiers in Sustainable Food Systems | www.frontiersin.org 1581 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems FIGURE 4 | Contribution to the NPV variance for the grass-legume association and the grass monoculture. GLA, Grass-legume association; GM, Grass monoculture. dry matter production (14%) and the lower proportion of Acid (mainly CIAT 17434) in integrated grass-legume systems for Detergent Fiber that favors digestibility and, therefore, a better livestock production in the tropics. These studies highlight, use of the available forage (Rincón et al., 2020). The higher milk in comparison with monoculture pastures, improvements in production level in turn helps to improve the financial indicators both forage quantity and quality, a strong compatibility with of the association compared to the monoculture base scenario. aggressive Brachiaria species, as well as higher meat and milk These results (i.e., the increased milk productivity by 52% production levels and stocking rate (Peters et al., 2011; Crestani and the related increased income from milk sales by 58%) are et al., 2013; Pereira et al., 2019; Boddey et al., 2020; Villegas et al., consistent with (and even surpass the results of) different studies 2020). Other studies show average increases in milk production that have evaluated the potential of Arachis pintoi accessions of 31% in Colombia (Rivas and Holmann, 2000), 7 and 11.4% Frontiers in Sustainable Food Systems | www.frontiersin.org 1592 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems FIGURE 5 | Dry Matter (DM) production under climate change scenarios (RCP 2.6 y 8.5) and Current Scenario (C.S). GLA, Grass-legume association; GM, Grass monoculture. in Costa Rica (Peters et al., 2001; Romero and González, 2004), analysis shows that the daily milk production variable has the and 20% in Peru (Lara and Reategui, 2004). In addition to milk highest impact on the economic performance indicators. The yield increases, Romero and González (2004) found differences monoculture is more sensitive to small reductions in milk regarding the milk composition: both the milk protein (3.66 production as when associated with Centauro. Changes of just vs. 3.54%) and total solid contents (13.89 vs. 13.73%) were 1% in milk production lead, however, to changes in profitability higher in a grass-legume association with Arachis pintoi than indicators of more than 90% in both systems. Since different in a grass monoculture with Brachiaria. Regarding the animal empirical studies have shown that risk factors (perception of risk stocking rate, the reported increases are between 33 and 50% in about future returns from implementing a new technology, and Colombia (1.5-2AU ha−1 vs. 1 AU ha−1; Holmann, 2004), 29% level of risk aversion of the producer) are determining factors in in Brazil (2.26 vs. 1.6; Vasques et al., 2019), 50% in the Peruvian technology adoption (e.g., Marra et al., 2003; van Winsen et al., Amazon (4.13 vs. 2.07; Lara and Reategui, 2004), and 25% in 2014; Trujillo-Barrera et al., 2016), there is reason to believe that Costa Rica (4.6 vs. 3.7; Romero and González, 2004). Other the lower risk levels resulting from the inclusion of Centauro in studies highlight successful cases of early adoption of Arachis the cattle production system will enhance technology adoption. accessions in livestock systems, e.g., in western Brazil (Valentim The inclusion of different climate change scenarios (RCP 2.6 and Andrade, 2005), in the Colombian Caquetá Department and RCP 8.5) in our models revealed the substantial impact (Lascano et al., 2005) and in northern Costa Rica (Wunscher that climatic variables have on forage production, both in terms et al., 2004), suggesting the relevance of, and the potential of geographic distribution and available forage biomass. Until for dissemination, across different regions, for the technology 2050, the available forage biomass would reduce in both systems, evaluated in our study. the grass monoculture and the grass-legume association. For The improvements in the economic indicators resulting from the latter, however, reductions would be of a lower magnitude the inclusion of Centauro are also associated with improvements (maximum reduction of 16.6 vs. 35.3% for the monoculture). in the risk indicators. The probability of obtaining economic loss The highest losses are to be expected during dry season from was reduced from 100 to 39.1%, for example. The sensitivity January to March. These effects on forage productivity are the Frontiers in Sustainable Food Systems | www.frontiersin.org 1603 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems FIGURE 6 | Estimated change in suitable areas for Centauro by 2050 under RCP 2.6 (left) and RCP 8.5 (right). result of a combination of increased temperatures, variations estimates provided by CIAT CORMACARENA (2018), putting in precipitation levels and atmospheric CO2 concentrations livestock production in a difficult position. caused by climate change (Thornton et al., 2009; Rojas-Downing Although the modeled impacts from the climate change et al., 2017). Not only would forage productivity be affected if scenarios were relevant for both alternatives, the grass the favorable environmental conditions changed but also the monoculture and the grass-legume association, the latter potential distribution of Centauro and other Arachis varieties. shows a better adaptation capacity. This can be attributed to the Centauro would migrate to higher altitudes more favorable for its symbiotic effect between the legume and the grass associated development and the overall potential area for distribution would with the contribution of nitrogen-fixing (Dubeux et al., 2017; decrease. This could pave the way for the arrival of new (invasive) Pereira et al., 2019; Villegas et al., 2020). The higher availability species or native grasses with a better adaptation capacity to the of N improves both the yields and persistence of the grass, conditions projected for 2050. Although in our model we only and comes with the co-benefit of mitigating GHG emissions made projections for Centauro, the impacts of climate change through reducing (i) methane emissions (as a result of an in the Orinoquía would also affect the distribution, quantity improved diet), and (ii) synthetic fertilizer use (resulting in and quality of other forage species by up to 60% according to lower N2O emissions). Simultaneously, Arachis has positive Frontiers in Sustainable Food Systems | www.frontiersin.org 1614 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems FIGURE 7 | NPV probability distribution for the grass-legume association and the grass monoculture under climate change scenarios. GLA, Grass-legume association; GM, Grass monoculture. impacts on the physical and chemical properties of the soil, could also be affected, however, by other possible effects not and contributes to increasing both soil microfauna and organic considered in our study, such as effects on health, growth and matter (Schultze-Kraft et al., 2018). Arachis accessions in reproduction, water availability, and the distribution of pests and particular, offer dense soil cover and, therefore, prevent soil diseases (Garnett, 2009; Thornton et al., 2009; Rojas-Downing erosion problems (Schultze-Kraft et al., 2018). et al., 2017). In particular, periods of heat stress could become The effects of climate change on forage biomass production the main source of loss at the productive level in the livestock would lead to a strong decrease in milk production in both sector (Garnett, 2009; Nardone et al., 2010). This scenario does systems. The grass-legume would, however, be less affected not, however, consider potential technological changes nor the (-19%) than the grass monoculture (−56%). This in turn inclusion of other (new) species better adapted to the predicted would lead to significant economic losses in the dual-purpose regional climate change scenarios. Likewise, our study does not production systems in the region. Given the low productivity include any potential benefits that might be derived from culled levels and values of technical indicators in dual-purpose livestock cows on the beef market. systems, profitability margins are inherently sensitive to small Despite the benefits of including Arachis pintoi and other changes in production levels. The effects of climatic variations legumes in cattle systems, adoption levels remain low. Several on livestock production have been identified in the literature as studies have identified some of the factors that limit the one of the main impacts (e.g., Garnett, 2009; Thornton et al., adoption of Arachis accessions in countries such as Colombia 2009; Nardone et al., 2010; Henry et al., 2012). The severity or and Costa Rica, including a lack of commercial seed availability, level of the impact varies significantly between regions, however high establishment costs of planting material, limited technical (Rojas-Downing et al., 2017). For the Orinoquía region, CIAT information on the establishment and management of the CORMACARENA, 2018 predict that the impact of climate material in pastures, a lack of promotion and little knowledge change would lead to significant losses in cattle live weight about its benefits (CIAT, 2004; Wunscher et al., 2004; Lascano gains and dairy production, and lower birth and increased et al., 2005). A particularly important issue is seed supply, mortality rates. As mentioned in the methodology, our study which also continues to be a restriction in the dissemination only considers changes in dairy production as a result of the and adoption processes for the new Centauro accession. In this impacts of climate change on pasture productivity. Production sense, it is necessary to develop focused strategies, for example, Frontiers in Sustainable Food Systems | www.frontiersin.org 1625 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems artisanal seed production by cattle producers, as this could not availability in the long-term (Peñuela et al., 2014); and (iii) only contribute to generating higher technology adoption levels. reduction of nitrous oxide emissions, associated with Biological Focused strategies could also play an important role in providing Nitrification Inhibition (BNI) in Brachiaria humidicola pastures additional income, assuring income diversification, and opening (Subbarao et al., 2009, 2017; Moreta et al., 2014). On the other new business alternatives for young people and women. In the hand, however, negative effects have also been reported and long run, this would strongly contribute to supporting both include (i) the loss and degradation of native savannas and threats the rural economy and sustainable intensification processes in to biodiversity (decrease in bird, animal and fish species), with the region. In addition, the increased demand and adoption of gallery forests being the ecosystems under the greatest threat the legume could generate interest from the private sector for in the most intensified areas (Smith et al., 1997); (ii) increases seed production. in deforestation levels to expand grazing areas with introduced In addition to the above-mentioned limiting factors, there forages and, therefore, compromising ecosystem stability and are structural conditions that could slow down or discourage functions (e.g., altering microclimates and shifting the rates of sustainable intensification. The prevailing tradition of extensive consumption and supply of light, water and mineral nutrients), production systems and low land prices, for example, make it and increasing greenhouse gas emissions due to land-use changes more efficient to acquire more (new) land than to intensify (Williams and Baruch, 2000; Reid et al., 2010; Peñuela et al., 2014; existing land (White et al., 2001). In particular, in regions such as CIAT CORMACARENA, 2018); (iii) a displacement of native the Orinoquía, where land is relatively abundant and are prices species given the aggressive growth characteristics, invasive low, producers continue to favor more extensive systems at the behavior and fire resistance of Brachiaria species, particularly cost of deforestation processes. Even if the costs of implementing Brachiaria humidicola in savannas and highlands (Peñuela et al., new technologies are below land prices, cattle producers may 2014); (iv) increased soil erosion processes (Peñuela et al., not reduce the area, since one of the main reasons for land 2011); and (v) increased frequency and intensity of fires due to expansion is to secure land ownership rights (Kaimowitz and establishment and management processes and the large standing Angelsen, 2008). This may be favored by speculation processes necro mass left by grasses of African origin (such as Brachiaria) in land prices, where a high price generates additional incentives at the end of the dry season that facilitate the combustion for extension, given the increase in the value of capital gains (Williams and Baruch, 2000). In the case of the new Centauro (Smith et al., 1997). These speculation processes could also, variety, although its introduction into livestock systems provides however, promote intensification if the amount of land that a strategy to restore degraded areas, improve productivity and can be acquired is reduced, for example by regulations (Smith provide ecosystem services, it could also be a technology that et al., 1997). Unfortunately, in most cases producers may not promotes deforestation processes and has negative impacts on be willing to intensify until land is scarce and most forests are protected ecosystems. The higher profitability associated with gone (Kaimowitz and Angelsen, 2008). Similarly, if producers new technologies, such as Centauro, could, for example, lead have few alternatives to invest their savings other than cattle producers to increase their herd size and hence their pasture area. production, this can contribute to the expansion of pasture areas. Likewise, profitable technologies can also provide farmers with This situation is further aggravated by the precarious controls the additional capital they need to finance livestock expansion on land tenure and the lack of monitoring and control regarding (Kaimowitz and Angelsen, 2008). the expansion of the agricultural frontier. Positive advances have In this sense, diffusion and adoption processes of new been documented in Costa Rica, where the agricultural frontier technologies like Centauro must be accompanied by land use cannot be expanded any further as a result of the little remaining governance and management policies. These policies require forest area and high land prices, forcing cattle producers to use a multidimensional approach that includes the development their land more efficiently, e.g., through incorporating Arachis of coordinated land tenure security policies, specific economic pintoi in their pastures and adopting Cratylia protein banks incentives aimed at promoting sustainable intensification (e.g., (White et al., 2001). The opposite was documented in Peru, where special credit lines, conservation requirements to access benefits land is still abundant and cheap, and market access is limited. or credits), integrated planning and zoning of land use, Producers failed to adopt legumes such as Arachis in Peru, given protection of forests and ecosystems, and tracking and the higher level of investment required (White et al., 2001). monitoring of land use change, particularly at the agricultural Intensification strategies in the Orinoquía have been a subject frontier. This also implies greater institutional coordination and of debate, mainly in environmental terms, since the introduction coordination between national policies (e.g., related to land improved forages (Brachiaira species) in the 1970s. On the one use, agriculture, rural development), partnerships between the hand, different studies have reported positive impacts associated public and private sectors, and local communities that increase with intensification processes with improved forages, such as (i) the effectiveness of policies and other instruments. Brazil for lower incidence of degradation of native savannas in intensified example, has reported a notable reduction in deforestation areas with improved forages, since they reduce the pressure rates in the Amazon region, which has been the result of a to produce animal feed in the native savannas (Smith et al., combination of multiple public and private mechanisms for 1997); (ii) reduction of greenhouse gas emissions associated with the protection of forests (FAO, 2016). For example, the new burning native savannas (Smith et al., 1997), carried out to Brazilian Forest Code (Federal Law No. 12,651/2012; Presidência increase grassland and savanna productivity in the short term da República, 2012) obliges rural land owners to submit data at the expense of eliminating vegetation cover and nutrient with geographic coordinates for the registration of private Frontiers in Sustainable Food Systems | www.frontiersin.org 1636 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems rural properties, certify their intention to comply environmental approaches need to be applied (which include extension and regulations, and in cases where this does not occur, land owners training programs), involving institutions relevant to the region are subject to administrative, civil or criminal processes and within a context that helps to close information and monitoring charges. Commercial banks are required (in accordance with gaps. In the case of Centauro, the focus of such information the Forest Code) to request rural land owners and holders to efforts should be on the correct establishment and management provide a registration certificate from the Rural Environmental of the legume, highlighting both potential economic benefits and Registry before granting loans for agricultural purposes. Zero environmental threats. This needs to go hand in hand with strong deforestation agreements for livestock signed by major beef inter- and intra-institutional coordination, and the development companies have helped in reducing deforestation in certain parts of public policies and comprehensive monitoring and control of Brazil (Gibbs et al., 2015) and the Brazil Green Bag Initiative mechanisms. National and regional multi-stakeholder platforms, (Presidência da República, 2012) is a conditional cash transfer such as the Colombian Roundtable for Sustainable Beef and program with a commitment to responsibly manage resources Dairy (MGS) and its regional sub-roundtables, can fill some and conserve ecosystems (FAO, 2016). of the gaps—at least in short- to medium-term, e.g., through providing targeted information campaigns and trainings CONCLUSIONS or developing indicators and frameworks for sustainable intensification of the sector. In the long term, however, and based The results of this study suggest that integrating the legume on the abovementioned efforts of multi-stakeholder platforms, Arachis pintoi CIAT 22160 cv. Centauro in a Brachiaria comprehensive public policies need to be developed, applied humidicola cv. Humidicola monoculture has great potential and monitored. to improve both productive and economic indicators in the Accelerating climate change will also affect the Orinoquía dual-purpose cattle production system of the Orinoquía region. region. Our study suggests that variations in the local climatic Not only that, Centauro also helps in generating important conditions would have significant impacts on the economic ecosystem services with positive effects on, for example, the viability of the dual-purpose cattle systems of the region. quality and persistence of the associated grass (restoration of It is necessary, therefore, to implement regional climate degraded pastures), the soil system and biodiversity. Centauro change adaptation and mitigation measures that include improves the system’s resilience to climatic variations, which is specific strategies for the local context. Among others, especially important considering the rather pessimistic climate animal breeding strategies that improve cattle by crossing projections for the region. These attributes make the inclusion with rustic breeds, silvo-pastoral systems or scattered trees of Centauro in the production system a key alternative for in pastures for heat stress reduction, and water harvesting sustainable intensification in the region, and thus also contributes for animal consumption, can significantly increase the to achieving other environmental objectives such as the liberation adaptation potential of dual-purpose systems, particularly of areas for reforestation purposes or the protection of during dry seasons. local ecosystems. It is important to mention, however, that, despite their numerous environmental benefits (see section Potential DATA AVAILABILITY STATEMENT Ecosystem Services of Arachis pintoi CIAT 22160 cv. Centauro) and because of their economic and social benefits, forage The data analyzed in this study is subject to the following technologies that are selected for intensification purposes (even licenses/restrictions: Data was retrieved from another research if sustainable such as Centauro), bear a risk of misuse in regions project and is not publicly available. Requests to access these and contexts where neither grasses nor legumes should be datasets should be directed to s.burkart@cgiar.org. planted. This could lead to results contrary to the objectives of sustainable intensification and could therefore negatively affect AUTHOR CONTRIBUTIONS local landscapes with significant ecological consequences. In the case of the Orinoquía region, this includes for example the SB, KE, and DR: conceptualization and methodology. KE, DR, promotion of deforestation or the penetration of important local and ÁR: formal analysis. KE, DR, ÁR, and SB: writing the original ecosystems (such as native flooded savannas). The Orinoquía has draft, review, editing, and resources. SB: supervision, funding a high degree of vulnerability to changes generated by human acquisition, and project administration. All authors contributed actions, which include transformations of productive models to the article and approved the submitted version. that are ignorant of the natural cycles threatening the ecosystem balance. The continuous search for productivity increases has led to significant changes in the productive models of the region, FUNDING including, for example, the introduction of improved pastures in floodable savannas (Peñuela et al., 2011). This situation is likely This work was funded by the CGIAR Research Program on to worsen considering the imminent effects of climate change, Livestock and by the Colombian Ministry of Agriculture and and threatens the savanna ecosystem as it could become subject Rural Development (MADR). The funders had no role in the to desertification processes as a consequence of inadequate design of the study; in the collection, analyses, or interpretation natural resource management (Peñuela et al., 2011). To avoid of data; in the writing of the manuscript, or in the decision to such unwanted consequences, effective technology diffusion publish the results. Frontiers in Sustainable Food Systems | www.frontiersin.org 1647 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems ACKNOWLEDGMENTS de Carne y leche en los sistemas ganaderos de la Orinoquía Colombiana, conducted under the cooperation agreement This work was carried out as part of the CGIAR Research between MADR, AGROSAVIA (previously CORPOICA) and Program on Livestock. We thank all donors who globally support CIAT and funded by MADR. Additionally, this work was part our work through their contributions to the CGIAR System. of the project Evaluación multilocacional de nuevo germoplasma CGIAR is a global research partnership for a food-secure future. forrajero, conducted under the cooperation agreement between Its science is carried out by 15 Research Centers in close AGROSAVIA and CIAT under the macroproject Incremento de collaboration with hundreds of partners across the globe. This la oferta forrajera a través de la liberación de nuevos materiales y work was conducted as part of the project Materiales forrajeros el desarrollo de estrategias integrales de manejo para aumentar la y estrategias de utilización y manejo, para mejorar la producción competitividad de la ganadería en Colombia, funded by MADR. REFERENCES DANE (2020a). Data from: Productividad Total de los Factores (PTF). Available online at: https://www.dane.gov.co/index.php/estadisticas-por-tema/cuentas- Abril, D. S., Melo, L. F., and Parra, D. (2017). “Impactos de los fenómenos nacionales/productividad (accessed September 14, 2021). climáticos sobre el precio de los alimentos en Colombia,” in El desarrollo DANE (2020b). Data from: Índice de precios al Productor (IPP). Available equitativo, competitivo y sostenible del sector agropecuario en Colombia, eds C. online at: https://www.dane.gov.co/index.php/estadisticas-por-tema/precios- G. Cano, A. M. Iregui, M. T. Ramirez, and A. M. Tribin (Caracas: Banco de y-costos/indice-de-precios-del-productor-ipp (accessed September 14, 2021). Desarrollo de América Latina), 315–347. DANE (2020c). Data from: Índice de precios al consumidor (IPC). Available Amézquita, M. C., Ibrahim, M., Llanderal, T., Buurman, P., and Amézquita, E. online at: https://www.dane.gov.co/index.php/estadisticas-por-tema/precios- (2004). Carbon sequestration in pastures, silvo-pastoral systems and forests y-costos/indice-de-precios-al-consumidor-ipc/ipc-historico (accessed in four regions of the latin American tropics. J. Sustain. For. 21, 31–49. September 14, 2021). doi: 10.1300/J091v21n01_02 Dickie, A., Streck, C., Roe, S., Zurek, M., Haupt, F., and Dolginow, A. Armenta, G., Dorado, J., Rodríguez, A., and Ruiz, J. (2015). Escenarios (2014). Strategies for Mitigating Climate Change in Agriculture: Abridged de cambio climático para precipitación y temperaturas en Colombia. Report. Climate Focus and California environmental Associates, Prepared Instituto de Hidrología, Meteorología y Estudios Ambientales de Colombia With the Support of the Climate and Land Use Alliance. Available IDEAM. Available online at: http://documentacion.ideam.gov.co/cgi- online at: https://www.climateandlandusealliance.org/reports/strategies-for- bin/koha/opac-detail.pl?biblionumber=37489 (accessed January 15, mitigating-climate-change-in-agriculture/ (accessed December 20, 2020). 2021). Dubeux, J. C. B., Blount, A. R. S., Mackowiak, C., Santos, E. R. S., Pereira-Neto, J. Bancolombia–Dirección de Investigaciones Económicas, Sectoriales y de D., Riveros, U., et al. (2017). Biological N2 fixation, belowground responses, Mercados (2020). Actualización de proyecciones económicas para Colombia– and forage potential of rhizoma peanut cultivars. Crop Sci. 57, 1027–1038. segundo trimestre de 2020. Available online at: https://www.shorturl.at doi: 10.2135/cropsci2016.09.0810 (accessed February 05, 2020). FAO (2016). El Estado de los bosques del mundo 2016. Roma: Los bosques y la Boddey, R. M., Casagrande, D. R., Homem, B. G. C., and Alves, B. J. R. agricultura: desafíos y oportunidades en relación con el uso de la tierra. (2020). Forage legumes in grass pastures in tropical Brazil and likely FEDEGAN (2003). Índice de costos ganaderos diciembre 2002–marzo 2003. impacts on greenhouse gas emissions: a review. Grass Forage Sci. 75, 1–15. Carta Fedegán Magazine No. 79. Bogotá: Federación Colombiana de doi: 10.1111/gfs.12498 Ganaderos, 17–32. Cárdenas, E. A., Maass, B. L., Peters, M., and Franco, L. H. (1999). FEDEGAN (2018). Ganadería Colombiana Hoja De Ruta 2018–2022. Evaluación de germoplasma nuevo de Arachis pintoi en Colombia. 2. Bogotá: FEDEGAN. Bosque muy húmedo–Premontano (Zona cafetera), Caldas. Past. Trop. 21, Fisher, M. J., Rao, I. M., Ayarza, M. A., Lascano, C. E., Sanz, J. I., Thomas, R. J., 42–59. et al. (1994). Carbon storage by introduced deep-rooted grasses in the South Castillo-Gallegos, E., Mannetje, L., and Aluja-Schunemann, A. (2005). Production American savannas. Nature 371, 236–238. doi: 10.1038/371236a0 and persistence of a native pasture-Arachis pintoi association in the humid Fonte, S. J., Nesper, M., Hegglin, D., Velásquez, J. E., Ramirez, B., Rao, I. M., et al. tropics of Mexico. Trop. Grassl. 39. Available online at: https://www. (2014). Pasture degradation impacts soil phosphorus storage via changes to tropicalgrasslands.info/index.php/tgft/pages/view/tropicalGrasslands aggregate-associated soil organic matter in highly weathered tropical soils. Soil CIAT (1994). Programa de Forrajes Tropicales-Informe Anual 1994. Cali: Biol. Biochem. 68, 150–157. doi: 10.1016/j.soilbio.2013.09.025 Centro Internacional de Agricultura Tropical (CIAT). Available online Galdino, S., Sano, E. E., Andrade, R. G., Grego, C. R., Nogueira, S. F., Bragantini, C., at: https://cgspace.cgiar.org/handle/10568/69061?show=full (accessed April et al. (2015). Large-scale modeling of soil erosion with rusle for conservationist 21, 2021). planning of degraded cultivated Brazilian pastures. Land Degrad. Dev. 27, CIAT (2002). Tropical Grasses and Legumes: Optimizing genetic Diversity for 773–784. doi: 10.1002/ldr.2414 Multipurpose Use (Project IP5). Cali: Centro Internacional de Agricultura Garnett, T. (2009). Livestock-related Greenhouse Gas Emissions: impacts Tropical (CIAT). Available online at: hdl.handle.net/10568/69061 (accessed and options for policy makers. Environ. Sci. Policy 12, 491–503. September 14, 2021). doi: 10.1016/j.envsci.2009.01.006 CIAT (2004). Tropical Grasses and Legumes: Optimizing genetic Diversity for GBIF.org (2020). GBIF Occurrence. Available online at: https://doi.org/10.15468/ Multipurpose Use (Project IP5). Annual Report 2004. Cali: Centro Internacional dl.wvj4tj (accessed June 02, 2020). de Agricultura Tropical. Available online at: hdl.handle.net/10568/69061 Gibbs, H. K., Munger, J., L’Roe, J., Barreto, P., Pereira, R., Christie, M., et al. (2015). (accessed September 14, 2021). Did ranchers and slaughterhouses respond to zero deforestation agreements in CIAT and CORMACARENA (2018). Plan regional integral de cambio climático the Brazilian Amazon? Conserv. Lett. 9, 32–42. doi: 10.1111/conl.12175 para la Orinoquía. CIAT publicación No. 438. Cali: Centro Internacional de Henry, B., Charmley, E., Eckard, R., Gaughan, J. B., and Hegarty, R. (2012). Agricultura Tropical (CIAT). Livestock production in a changing climate: adaptation andmitigation research Crestani, S., Mendonça, H., Ribeiro, F. N., Frederico, M. M., Almeida, E. X., in Australia. Crop Past. Sci. 63, 191–202. doi: 10.1071/CP11169 and Portela, F. A. (2013). Steers performance in dwarf elephant grass pastures Holmann, F. (2004). “Potential benefits of new forage germplasm in dual-purpose alone or mixed with Arachis pintoi. Trop. Anim. Health Prod. 45, 1369–1374. cattle systems in the dry tropics,” in Feeding Systems With Forage Legumes doi: 10.1007/s11250-013-0371-x to Intensify dairy Production in Latin America and the Caribbean-A Project Frontiers in Sustainable Food Systems | www.frontiersin.org 1658 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems Executed by the Tropileche Consortium, eds F. Holmann and C. Lascano (h Nardone, A., Ronchi, B., Lacetera, N., Ranieri, M. S., and Bernabucci, U. (2010). ttps://www.google.com/search?sxsrf=AOaemvIjDC_c2FIZ_-CAz1wW7vh Effects of climate changes on animal production and sustainability of livestock QfNP8DA:1631316354048&q=Cali,+Colombia&stick=H4sIAAAAAAAAA systems. Livest. Sci. 130, 57–69. doi: 10.1016/j.livsci.2010.02.011 OPgE-LUz9U3MDFPtyxWAjMNC4qL07SMMsqt9JPzc3JSk0sy8_P084vSE Navarro-Racines, C., Tarapues, J., Thornton, P., Jarvis, A., and Ramirez-Villegas, _MyqxJBnGKrjNTElMLSxKKS1KJihZz8ZLDwIlY-58ScTB0F5_yc_NykzM J. (2020). High-resolution and bias-corrected CMIP5 projections for climate QdrIwA8gbAbWAAAAA&sa=X&ved=2ahUKEwir_bH-xvXyAhUbOisKH change impact assessments. Sci. Data 7:7. doi: 10.1038/s41597-019-0343-8 faTDKsQmxMoAXoECC4QAw Cali: Centro Internacional de Agricultura OECD/FAO (2020). OECD-FAO Agricultural Outlook 2020-2029. Paris: FAO, Tropical-CIAT), 114–131. Rome/OECD Publishing. ICA (1987). Pasto Llanero Brachiaria dictyoneura. Boletín técnico No. 151. Olsson, L., Barbosa, H., Bhadwal, S., Cowie, A., Delusca, K., Flores-Renteria, Villavicencio: ICA. Available online at: http://ciat-library.ciat.cgiar. D., et al. (2019). “Land degradation,” in Climate Change and Land: An org/forrajes_tropicales/Released/Materiales/PastoLlaneroC.pdf (accessed IPCC Special Report on Climate Change, Desertification, Land Degradation, December 15, 2020). Sustainable Land Management, Food Security, and Greenhouse Gas Fluxes IDEAM, PNUD,MADS, DNP, and Cancillería (2015).Nuevos escenarios de cambio in Terrestrial Ecosystems, eds P. R. Shukla, J. Skea, E. Calvo Buendia, V. climático para Colombia 2011–2100 Herramientas Científicas para la Toma de Masson-Delmotte, H.-O. Pörtner, D. C. Roberts, P. Zhai, R. Slade, S. Connors, Decisiones–Enfoque Nacional–Departamental: Tercera Comunicación Nacional R. van Diemen, M. Ferrat, E. Haughey, S. Luz, S. Neogi, M. Pathak, J. de Cambio Climático. Bogotá: Instituto de Hidrología, Meteorología y Estudios Petzold, J. Portugal Pereira, P. Vyas, E. Huntley, K. Kissick, M. Belkacemi, Ambientales de Colombia (IDEAM). J. Malley (Geneva: Intergovernmental Panel on Climate Change), 345–436. Jansen, H. G. P., Ibrahim, M. A., Nieuwenhuyse, A., ’t Mannetje, L., Joenje, M., Available online at: https://www.ipcc.ch/site/assets/uploads/sites/4/2019/11/ and Abarca, S. (1997). The economics of improved pasture and silvopastoral 07_Chapter-4.pdf (accessed September 14, 2021). technologies in the Atlantic zone of Costa Rica. Trop. Grassl. 31, 588–598. Pannell, D. J., Marshall, G. R., Barr, N., Curtis, A., and Vanclay,. F. W. R. Jensen, E. S., Peoples, M. B., Boddey, R. M., Gresshoff,., P. M., Hauggard-Nielsen, (2006). Understanding and promoting adoption of conservation practices H., et al. (2012). Legumes for mitigation of climate change and the provision by rural landholders. Aust. J. Exp. Agric. 43, 1407–1424. doi: 10.1071/EA0 of feedstock for biofuels and biorefineries. a review. Agron. Sustain. Dev. 32, 5037 329–364. doi: 10.1007/s13593-011-0056-7 Park, C. S. (2007). Contemporary Engineering Economics, 4th Edn. Upper Saddle Kaimowitz, D., and Angelsen, A. (2008). Will livestock intensification River, NJ: Prentice Hall. help save latin America’s tropical forests? J. Sustain. For. 27, 6–24. Peñuela, L., Fernández, A. P., Castro, F., and Ocampo, A. (2011). Uso doi: 10.1080/10549810802225168 y manejo de forrajes nativos en la sabana inundable de la Orinoquía. Lara, D., and Reategui, K. (2004). “Effect of associating Brachiaria brizantha Convenio de cooperación interinstitucional entre The Nature Conservancy with Arachis pintoi on milk yield,” in Feeding Systems With Forage Legumes (TNC) y la Fundación Horizonte Verde (FHV) con el apoyo de la Fundación to Intensify Dairy Production in Latin America and the Caribbean: A Project Biodiversidad de España y la Corporación Autónoma Regional de la Orinoquía Executed by the Tropileche Consortium, eds. F. Holmann and C.E. Lascano (CorpOrinoquía) (Bogota, DC). 66. (Cali: Centro Internacional de Agricultura Tropical, Tropileche Consortium; Peñuela, L., Solano, C., Ardila, V., and Galán, S. (2014). Sabana inundable Addis Ababa: System-wide Livestock Programme; Nairobi: International y ganadería, opción productiva de conservación en la Orinoquia. Bogotá: Livestock Research Institute), 67–68. Asociación Red Colombiana de Reservas Naturales de la Sociedad Civil, Lascano, C. (1994). “Nutritive value and animal production of forage Arachis,” in Fundación Natura, World Wildlife Fund, The Nature Conservancy, y Parques Biology and Agronomy of Forage Arachis, eds P. C. Kerridge and B. Hardy (Cali: Nacionales Naturales de Colombia. Centro Internacional de Agricultura Tropical (CIAT)), 109–121. Pereira, J. M., Rezende, C. P., Ferreira, A. M., Homem, B. G. C., Casagrande, Lascano, C. E., Peters, M., and Holmann, F. (2005). Arachis pintoi in the humid D. R., Macedo, T. M., et al. (2019). Production of beef cattle grazing tropics of Colombia: a forage legume success story. Trop. Grassl. 39:220. on Brachiaria brizantha (Marandu grass)—Arachis pintoi (forage Available online at: https://www.tropicalgrasslands.info/index.php/tgft/pages/ peanut cv. Belomonte) mixtures exceeded that on grass monocultures view/tropicalGrasslands (accessed April 17, 2021). fertilized with 120 kg N/ha. Grass Forage Sci. 75, 28–36. doi: 10.1111/gfs. León-Velarde, C., Cañas, R., Quiroz, R., Osorio, J., Guerrero, J., and 12463 Pezo, D. (2006). LIFE-SIM: Livestock Feeding Strategies Simulation Models. Peters, M., Franco, L., Schmidt, A., and Hincapié, B. (2011). Especies Forrajeras Lima: International Potato Center (CIP). https://bit.ly/3nBVWVD (Accessed Multipropósito: Opciones para productores del trópico americano. Cali: December, 12, 2020). Centro Internacional de Agricultura Tropical (CIAT); Bundesministerium MADR/USP (2020). Precio pagado al productor Res 0017 de 2002. Available online für Wirtschaftliche Zusammenarbeit und Entwicklung (BMZ); Deutsche at: http://uspleche.minagricultura.gov.co/ (accessed June 12, 2020). Gesellschaft für Technische Zusammenarbeit (GIZ). Marra, M., Pannell, D. J., and Abadi Ghadim, A. (2003). The economics Peters, M., Horne, P., Schmidt, A., Holmann, F., Kerridge, P. C., Tarawali, S. of risk, uncertainty and learning in the adoption of new agricultural A., et al. (2001). The Role of Forages in Reducing Poverty and Degradation of technologies: where are we on the learning curve? Agric. Syst.75, 215–234. Natural Resources in Tropical Production Systems. Agricultural Research and doi: 10.1016/S0308-521X(02)00066-5 Extension Network. Network Paper No. 117. Available online at: https://cdn.odi. Melo, S., Riveros, L., Romero, G., Álvarez, A., and Diaz, C., Calderón, S. org/media/documents/5218.pdf (accessed September 14, 2021). (2017). Efectos económicos de futuras sequías en Colombia: Estimación Peters, M., Maass, B. L., Franco, L. H., and Cárdenas, E. A. (2000). Evaluación a partir del Fenómeno El Niño 2015. Arch. Econ. 466, 1–34. Available de germoplasma nuevo de Arachis pintoi en Colombia. 3. Bosque muy online at: https://colaboracion.dnp.gov.co/CDT/Estudios%20Econmicos/466. húmedo tropical–Piedemonte amazónico, Caquetá. Past. Trop. 22, 2–28. pdf (accessed September 14, 2021). Available online at: http://ciat-library.ciat.cgiar.org/Articulos_Ciat/PAST2221. Moreno, I. R., Maass, B. L., Peters, M., and Cárdenas, E. A. (1999). Evaluación pdf (accessed September 14, 2021). de germoplasma nuevo de Arachis pintoi en Colombia. 1. Bosque seco Phillips, S.J., Dudík, M., Schapire, R.E. (2021). Maxent software for modeling tropical, Valle del Cauca. Past. Trop. 21:18–32. Available online at: https://www. species niches and distributions (Version 3.4.1). Available online at: http:// tropicalgrasslands.info/index.php/tgft/pages/view/Pasturas biodiversityinformatics.amnh.org/open_source/maxent/ (accessed October 02, Moreta, D. E., Arango, J., Sotelo, M., Vergara, D., Rincón, A., Ishitani, M., et al. 2020). (2014). Biological nitrification inhibition (BNI) in Brachiaria pastures: a novel Presidência da República (2012). Lei N◦ 12.651, de 25 de maio de 2012. Dispõe strategy to improve eco-efficiency of crop-livestock systems and to mitigate sobre a proteção da vegetação nativa e dá outras providências. Presidência da climate change. Trop. Grassl. 2, 88–91. doi: 10.17138/TGFT(2)88-91 República. Available online at: http://www.planalto.gov.br/ccivil_03/_ato2011- Murgueitio, E., Calle, Z., Uribe, F., Calle, A., and Solorio, B. (2011). Native trees 2014/2012/lei/L12651compilado.htm (accessed April 24, 2021). and shrubs for the productive rehabilitation of tropical cattle ranching lands. Rao, I., Van der Hoek, R., Peters, M., and Castro, A. (2014). Tropical forage- For. Ecol. Manage. 261, 1654–1663. doi: 10.1016/j.foreco.2010.09.027 based systems for climate-smart livestock production in Latin America. Frontiers in Sustainable Food Systems | www.frontiersin.org 1669 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems Rural 21, 12–15. Available online at: https://www.biopasos.com/biblioteca/74v Simpson, C. E., Valls, J. F. M., and Miles, J. W. (1995). “Biología reproductiva y %20rural2014_04-S12-15.pdf (accessed September 14, 2021). potencial para la recombinación genética de Arachis,” in Biología y Agronomía Reid, R. S., Bedelian, C., Said, M. Y., Kruska, R. L., Mauricio, R. M., Castel, de Especies Forrajeras de Arachis, ed P.C. Kerridge (Cali: Centro Internacional V., et al. (2010). “Global livestock impacts on biodiversity,” in Livestock in de Agricultura Tropical), 46–55. Available online at: https://hdl.handle.net/ a Changing Landscape, Volume 1. Drivers, Consequences, and Responses, eds 10568/54798 H. Steinfeld, H. A. Mooney, F. Schneider, L. E. Neville (Washington, DC: Smith, J., Cadavid, J. V., Rincón, A., and Vera, R. (1997). Land speculation Island Press), 111–137. Available online at: https://hdl.handle.net/10568/2532 and intensification at the frontier: a seeming paradox in the Colombian (accessed September 14, 2021). Savanna. Agric. Syst. 54, 501–520. doi: 10.1016/S0308-521X(96)00 Riesco, A., and Seré, C. (1985). “Análisis económico de resultados de las pruebas de 088-1 pastoreo,” in Evaluación de pasturas con animales. Alternativas metodológicas. Subbarao, G., Nakahara, K., Hurtado, M., Ono, H., Moreta, D., Salcedo, Memorias de una reunión celebrada en Perú 1-5 de octubre, 1984, eds C. A. F., et al. (2009). Evidence for biological nitrification inhibition in Lascano and E. Pizarro (Lima: Red Internacional de Evaluación de Pastos Brachiaria pastures. PNAS 106, 17302–17307. doi: 10.1073/pnas.090369 Tropicales), 201–232. 4106 Rincón, A. (1999). Maní forrajero (Arachis pintoi), la leguminosa para sistemas Subbarao, G. V., Arango, J., Masahiro, K., Hooper, A. M., Yoshihashi, sostenibles de producción agropecuaria. Bogotá: Corporación Colombiana de T., Ando, Y., et al. (2017). Genetic mitigation strategies to tackle Investigación Agropecuaria–Agrosavia. Available online at: http://hdl.handle. agricultural GHG emissions: The case for biological nitrification net/11348/4114 (accessed September 14, 2021). inhibition technology. Plant Sci. 262, 165–168. doi: 10.1016/j.plantsci.2017. Rincón, A. (2001). Potencial productivo de ecotipos de Arachis pintoi en el 05.004 Piedemonte de los Llanos Orientales de Colombia. Past. Trop. 23, 19–24. Thornton, P. K., Van de Steeg, J., Notenbaert, A., and Herrrero, M. Available online at: https://www.tropicalgrasslands.info/index.php/tgft/pages/ (2009). The impacts of climate change on livestock and livestock view/Pasturas (accessed September 14, 2021). systems in developing countries: a review of what we know and what Rincón, A., Bueno, G., Diaz, R. A., Burkart, S., and Enciso, K. (2020). Cultivar we need to know. Agric. Syst. 101, 113–127. doi: 10.1016/j.agsy.2009. Centauro (Arachis pintoi CIAT 22160): leguminosa forrajera para sistemas 05.002 de ganadería sostenible. Bogotá: Corporación Colombiana de Investigación Trujillo-Barrera, A., Pennings, J. M. E., and Hofenk, D. (2016). Agropecuaria (Agrosavia). Understanding producers’ motives for adopting sustainable Rincón, A., Cuesta, P. A., Pérez, R., Lascano, C. E., and Ferguson, J. (1992). practices: the role of expected rewards, risk perception and risk Maní Forrajero Perenne (Arachis pintoi Krapovickas y Gregory) Una Alternativa tolerance. Eur. Rev. Agric. Econ. 43, 359–382. doi: 10.1093/erae/ para Ganaderos y Productores. Cali: Centro Internacional de Agricultura jbv038 Tropical (CIAT). Available online at: http://ciat-library.ciat.cgiar.org/forrajes_ Valentim, J. F., and Andrade, C. M. S. (2005). Forage peanut (Arachis pintoi): tropicales/pdf/Leaflets/arachis_colombia.pdf (accessed September 14, 2021). a high yielding and high-quality tropical legume for sustainable cattle Rincón, A., Flórez, H., Ballesteros, H., and León, L. M. (2018). Efectos de la production systems in the western Brazilian Amazon. Trop. Grassl. 39:222. fertilización en la productividad de una pastura de Brachiaria humidicola cv. Available online at: https://www.tropicalgrasslands.info/index.php/tgft/pages/ Llanero en el Piedemonte de los Llanos Orientales de Colombia. Trop. Grassl. view/tropicalGrasslands (accessed September 14, 2021). 6, 158–168. doi: 10.17138/tgft(6)158-168 Valls, J. F. M., and Pizarro, E. A. (1995). “Recolección de germoplasma de Rincón, A., and Pesca, A. (2017). Productividad animal de una leguminosa forrajera Arachis silvestre,” in Biología y Agronomía de Especies Forrajeras de Arachis, seleccionada para pastoreo en suelos con drenaje deficiente (Unpublished report). ed P. C. Kerridge (Cali: Centro Internacional de Agricultura Tropical), 21–30. Bogotá: Corporación colombiana de investigación agropecuaria (Agrosavia). Available online at: https://hdl.handle.net/10568/54796 (accessed September Rivas, L., and Holmann, F. (2000). Early adoption of Arachis pintoi in the humid 14, 2021). tropics: the case of dual-purpose livestock systems in Caquetá, Colombia. van Winsen, F., de Mey, Y., Lauwers, L., Van Passel, S., Vancauteren, Livest. Res. Rural Dev. 12:23. Available online at: http://www.lrrd.org/lrrd12/ M., and Wauters, E. (2014). Determinants of risk behaviour: effects 3/riva123.htm (accessed September 14, 2021). of perceived risks and risk attitude on farmer’s adoption of risk Robertson, A. D. (2005). “Forage Arachis in Nepal: a simple success,” in management strategies. J. Risk Res. 19, 56–78. doi: 10.1080/13669877.2014.94 Proceedings of the XX International Grassland Congress: Offered papers 0597 (Dublin), 214. Available online at: https://www.tropicalgrasslands.info/public/ Vasques, I. C. F., Souza, A. A., Morais, E. G., Benevenute, P. A. N., journals/4/Historic/Tropical%20Grasslands%20Journal%20archive/PDFs/ da Silva, L. C. M., Homem, B. G. C., et al. (2019). Improved Vol_39_2005/Vol_39_04_2005_pp214_214.pdf (accessed September 14, 2021). management increases carrying capacity of Brazilian pastures. Rojas-Downing, M., Pouyan, A., Harrigan, T., andWoznicki, S. A. (2017). Climate Agric. Ecosyst. Environ. 282, 30–39. doi: 10.1016/j.agee.2019.05. change and livestock: impacts, adaptation, and mitigation. Clim. Risk Manag. 017 16, 145–163. doi: 10.1016/j.crm.2017.02.001 Villegas, D. M., Velasquez, J., Arango, J., Obregon, K., Rao, I. M., Rosas, G., Romero, F., and González, J. (2004). “Effects of Brachiaria decumbens alone and et al. (2020). Urochloa grasses swap nitrogen source when grown in association associated with Arachis pintoi on milk production and milk components,” with legumes in tropical pastures. Diversity 12:419. doi: 10.3390/d1211 in Feeding systems with forage legumes to intensify dairy production in Latin 0419 America and the Caribbean-A project executed by the Tropileche Consortium, Walther, G., Beibner, S., and Burga, A. (2005). Trends in the upward shift of eds Holmann and Lascano (Cali: Centro Internacional de Agricultura alpine plants. J. Veg. Sci. 16, 541–548. doi: 10.1111/j.1654-1103.2005.tb02 Tropical), 5–11. Available online at: http://hdl.handle.net/10568/830 (accessed 394.x September 14, 2021). White, D., Holmann, F., Fujisaki, S., Reategui, K., and Lascano, C. (2001). “Will Sattler, D., Seliger, R., Nehren, U., Naegeli, F., Soares da Silva, A., Raedig, C., et al. intensifying pasture management in Latin America protect forests–or is it the (2018). “Pasture degradation in south east brazil: status, drivers and options for other way around?” inAgricultural Technologies and Tropical Deforestation, eds sustainable land use under climate change,” in Climate Change Adaptation in A. Angelsen and D. Kaimowitz (Wallingford: CABI Publishing), 91–113. Latin America, eds W. L. Filho and L. E. de Freitas (Cham: Springer), 3–17. Williams, D. G., and Baruch, Z. (2000). African grass invasion Schultze-Kraft, R., Rao, I. M., Peters, M., Clements, R. J., Bai, C., and Liu, G. (2018). in the Americas: ecosystem consequences and the role of Tropical forage legumes for environmental benefits: an overview. Trop. Grassl. ecophysiology. Biol. Invasions 2, 123–140. doi: 10.1023/A:101004052 6, 1–14. doi: 10.17138/TGFT(6)1-14 4588 Shelton, H. M., Franzel, S., and Peters, M. (2005). Adoption of tropical legume Wunscher, T., Schultze-Kraft, R., Peters, M., and Rivas, L. (2004). Early technology around the world: analysis of success. Trop. Grassl. 39, 198–209. adoption of the tropical forage legume Arachis Pintoi in Huetar norte, Available online at: https://www.tropicalgrasslands.info/index.php/tgft/pages/ Costa Rica. Exp. Agric. 40, 257–268. doi: 10.1017/S001447970300 view/tropicalGrasslands (accessed September 14, 2021). 1583 Frontiers in Sustainable Food Systems | www.frontiersin.org 2670 October 2021 | Volume 5 | Article 666604 Enciso Valencia et al. Arachis pintoi in Cattle Systems Author Disclaimer: The views expressed in this document may not be taken as the this article, or claim that may be made by its manufacturer, is not guaranteed or official views of these organizations. endorsed by the publisher. Conflict of Interest: The authors declare that the research was conducted in the Copyright © 2021 Enciso Valencia, Rincón Castillo, Ruden and Burkart. This is an absence of any commercial or financial relationships that could be construed as a open-access article distributed under the terms of the Creative Commons Attribution potential conflict of interest. License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the Publisher’s Note: All claims expressed in this article are solely those of the authors original publication in this journal is cited, in accordance with accepted academic and do not necessarily represent those of their affiliated organizations, or those of practice. No use, distribution or reproduction is permitted which does not comply the publisher, the editors and the reviewers. Any product that may be evaluated in with these terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 2681 October 2021 | Volume 5 | Article 666604 ORIGINAL RESEARCH published: 21 October 2021 doi: 10.3389/fsufs.2021.684747 Classification of Megathyrsus Maximus Accessions Grown in the Colombian Dry Tropical Forest by Nutritional Assessment During Contrasting Seasons Juliana Isabel Carvajal-Tapia 1*, Johanna Mazabel 2 and Nelson Jose Vivas-Quila 3 1National Open and Distance University, CEAD, Popayán, Colombia, 2 Alliance Bioversity International and CIAT, Cali, Colombia, 3 Agricultural Nutrition Research Group, NUTRIFACA, School of Agricultural Sciences, University of Cauca, Popayán, Colombia The diversity and use of tropical forages for cattle feeding are the protagonists in Edited by: livestock systems. The production and nutritional quality of forages represent a strategy Stefan Burkart, Alliance Bioversity International and of continuous research in animal feeding to help mitigate the environmental impact CIAT, France generated by tropical livestock. The objective of this study was to classify the nutritional Reviewed by: behavior in contrasting seasons and the relationship with agronomic traits of a collection Aníbal Coutinho do Rêgo, Federal Rural University of the of 129 CIAT (Centro Internacional de Agricultura Tropical) accessions of Megathyrsus Amazon, Brazil Maximus established in the Colombian dry tropics. By means of the near-infrared Jaime Rosero, reflectance spectroscopy (NIRS) technique, crude protein (CP), neutral detergent fiber University of Antioquia, Colombia Julián Botero, (NDF), acid detergent fiber (ADF), and in vitro dry matter digestibility (IVDMD) were Industrial University of determined under rainy and dry seasons as fixed effects. We measured plant height, Santander, Colombia dry matter biomass (DMB) and flowering in field. Aspects such as plant height and DMB *Correspondence: Juliana Isabel Carvajal-Tapia did not show correlation with nutritional aspects, whereas flowering was correlated with jicarvajal@unicauca.edu.co; the content of structural carbohydrates. Despite genotype and precipitation affecting juliana.carvajal@unad.edu.co nutritional value, there is relative nutritional steadiness in NDF, ADF, and IVDMD between seasons for some accessions. According to the cluster analysis carried out for each Specialty section: This article was submitted to season, it was evidenced that from the total collection, 51.2% of the accessions Climate-Smart Food Systems, during the dry season and 19.4% of the accessions during the rainy season were a section of the journal Frontiers in Sustainable Food Systems classified with a better nutritional profile, thus, showing a higher number of materials Received: 04 May 2021 with better nutritional behavior in the dry season. Both the genotypic characteristics Accepted: 10 September 2021 of M. maximus and environmental conditions during contrasting seasons are factors Published: 21 October 2021 that might influence the variability of the nutritional content, productive parameters, and Citation: flowering. Additionally, fodder material classification under Hotelling’s T-squared test and Carvajal-Tapia JI, Mazabel J and Vivas-Quila NJ (2021) Classification of Nutritional Classification Index suggests accessions that might be promising for resilient Megathyrsus Maximus Accessions nutritional quality and adequate DMB, which proves that M. maximus could become Grown in the Colombian Dry Tropical Forest by Nutritional Assessment an alternative for animal feeding and sustainable livestock production during critical dry During Contrasting Seasons. periods in tropical agroecosystems. Front. Sustain. Food Syst. 5:684747. doi: 10.3389/fsufs.2021.684747 Keywords: forages, grassland, Guinea grass, livestock, Panicum Frontiers in Sustainable Food Systems | www.frontiersin.org 619 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons INTRODUCTION the establishment and development of eco-efficient livestock production or to select material with improved fodder quality The expansion of the agricultural frontier with crops and pastures (Ramakrishnan et al., 2014). in tropical regions of developing countries for food production The nutritional quality and association with the productive requires implementing production strategies with an eco-efficient parameters of a broad range of accessions of M. maximus in focus to sustainably meet the increasing demand for food Colombian tropical regions have not been described in detail (Rao, 2013). or correlated with climatic factors. This is a relevant aspect in The major part of livestock activity in intertropical regions the identification of resilient forage species, particularly for the is carried out under grazing systems and mixed model systems agricultural sector that faces the consequences of climate change. (concentrated pastures), (Gerber et al., 2015). Food for these Therefore, we propose the hypothesis that the rainfall pattern that livestock systems based on pastures is developed through the determines two contrasting seasons (rainy and dry) in tropical production of forages, which depends on the rainfall pattern regions influences not only the agronomic behavior of the (Castañeda et al., 2015; Gándara et al., 2017; Marcillo et al., collection of M. maximus but also the nutritional composition 2021), which is influenced by the consequences of climate change. and at the same time can be related to the productive variables The instability in forage production brings along with it an of forages. increase in production costs because of the use of supplements NIRS (near-infrared reflectance spectroscopy) is a fast (concentrates), (Morales-Vallecilla and Ortiz-Grisales, 2018) and and accurate technique with an eco-friendly technology to nutritional variables that influence productivity (Cooke et al., diagnose the nutritional quality of tropical forages (International 2020), thus, compromising both cattle feeding efficiency and the Organization for Standardization ISO 12099:2017., 2017; Parrini sustainable management of herds (Paul et al., 2020). et al., 2018; Mazabel et al., 2020). Since 2015, the CIAT The diversity and use of tropical forages for livestock feeding forages and animal nutrition quality laboratory has worked on are protagonists in tropical livestock systems. Characteristics the development of NIRS predictive models, in particular, for such as biomass yield and nutritional quality depend on neutral detergent fiber (NDF), acid detergent fiber (ADF), crude genetics, environment, and some other factors (Paul et al., protein (CP), and in vitro dry matter digestibility (IVDMD) for 2020). Investigating and evaluating these characteristics will tropical forages. contribute to the development of forages adapted to the With the purpose of helping to identify promising forage specific edaphoclimatic conditions of the tropics and identifying crops for tropical areas and to classify potential germplasm for genotypes capable of producing “more with less,” which, smallholder farmers or plant breeding programs, the object of according to Rao (2013), is important for advancing toward an this study was to classify the vegetative material of M. maximus eco-efficient livestock system. established in the Colombian dry tropics according to nutritional Megathyrsus maximus–Panicum maximum (Cook and behavior using NIRS methodology during contrasting seasons Schultze-Kraft, 2015) is an African species that has been and the relationship with plant height, forage production, and widely distributed in the warm areas of Colombia. Under flowering with nutritional quality. edaphoclimatic conditions of the Colombian dry tropical forest, the response in terms of production is adequate during MATERIALS AND METHODS low-precipitation periods. Also, this grass has short recovery periods, tolerance of shade and moderate drought periods, Location tolerance of short flooding periods (Morales-Velasco et al., The experiment was conducted in a tropical dry forest 2016; Matínez-Mamian et al., 2020), and an adequate response agroecosystem in the Patía Valley, which is located in the in association with forage legumes (Matínez-Mamian et al., department of Cauca in southwestern Colombia, with an average 2020) and with silvopastoral systems (Barragán-Hernández and temperature of 27.9◦C and bimodal cycle with average annual Cajas-Girón, 2019). This grass is promising for environmental precipitation of 1,414mm (Figure 1). To guarantee the process management of cattle because of its potential for biological of establishing experimental plots, we used water irrigation and nitrification inhibition (IBN), (Carvajal-Tapia et al., 2021) and mechanical weed control. is outstanding for its nutritive value, perenniality, and adaptive The local soil is a medium-fertility Mollisol. Chemical potential, and for showing diversity among cultivars in terms analysis in the 0-to 20-cm layer showed pH of 6.26, organic of yield, forage quality, and response to nutrient fertilization matter content of 4.50%, phosphorus content of 6.3 ppm, and (Benabderrahim and Elfalleh, 2021). calcium, magnesium, and potassium content of 14.58, 6.91, and The nutritional quality of M. maximus in terms of 0.59 cmol/kg, respectively. 1 year after establishment of the protein and fiber content, and digestibility, has a wide range experimental plots, we applied fertilizer only once at a rate of of values generated by different edaphoclimatic, genotypic, 150 kg N/ha and 95 kg P/ha. and management conditions. The attributes of adaptation to edaphoclimatic limitations, forage quality, and seed production Experimental Design in Fields facilitate the development of superior cultivars in current For the agronomic and nutritional evaluation in December of grass breeding activities (Rao, 2013). However, identifying the 2015, 129 accessions of M. maximus, including commercial nutritional behavior of the species in a potential livestock varieties provided by the germplasm bank of the International area can help to find a versatile feeding alternative for Center for Tropical Agriculture (CIAT) and two improved Frontiers in Sustainable Food Systems | www.frontiersin.org 720 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons present in the experimental plot in a range of 0–100% at the time of evaluation. For dry matter biomass (DMB), we estimated the availability of green forage (GF) after cutting at the height of 30 cm from the ground and measuring the weight per plot in the field. Out of all the GF, we weighed subsamples of ∼200 g. These were dried in an oven with controlled ventilation at a temperature of 60◦C (140◦F) until reaching constant weight (48 to 72 h). With the final weight of the subsamples, we estimated dry matter. Near-Infrared Reflectance Spectroscopy Testing in the Laboratory The subsamples obtained in the field to determine DMB were analyzed in the CIAT forages and animal nutrition quality FIGURE 1 | Average temperature values and rainfall accumulation during laboratory, where they were pulverized using a Retsch SM ′ experiments in field trials. Coordinates: N: 1◦ ′′ ′ ′′ 59 13 ; W: 77◦5 57’ , Patía 100 (Retsch GmbH, Haan, Germany) with a 1-mm bottom Valley. Source: NUTRIFACA Weather Station, 2016–2018. screen. For NIRS processing, we used a Foss 6,500 model and ISIS software (IS-2,250) version 2.71 (FOSS and Infrasoft International, USA, 2005). For each sample, duplicates of the TABLE 1 | Centro internacional de agricultura tropical (CIAT) accession numbers spectra were taken in separate quartz cells of 3.5-cm internal and origin of evaluated Megathyrsus maximus and commercial cultivars. diameter and 1-cm thick. The wavelength range was from 400 Origin CIAT accessions to 2,500 nm. The values obtained through wet chemistry were used to Kenya 622, 688, 691, 692, 693, 6,526, 6,536, 6,571, 6,890, build chemo metric models (Mazabel et al., 2020) and generate 6,891, 6,893, 6,897, 6,898, 6,900, 6,901, 6,903, 6,906, 6,912, 6,915, 6,918, 6,923, 6,981, 6,982, 6,983, 6,984, predictive equations in NIRS. Chemical analyses were performed 6,986, 6,990, 6,996, 16,003, 16,004 y 16,005 in duplicate for each accession in both seasons (rainy and Tanzania 6,927, 6,928, 6,929, 6,944, 6,945, 6,948, 6,949, 6,951, dry) under the guidelines of the 21st edition of the Official 6,954, 6,955, 6,960, 6,963, 6,967, 6,968, 6,969, 6,975, Methods of Analysis of (AOAC International, 2002). Crude 16,011, 16,017, 16,018, 16,019, 16,021, 16,023, protein content was determined using the FOSS KjeltecTM 8,100 16,025, 16,027, 16,028, 16,034, 16,035, 16,036, (Foss Company, HillerØed, Denmark). An ANKOM 2,000 fiber 16,038, 16,039, 16,041, 16,044, 16,046, 16,048, 16,049, 16,051, 16,054, 16,055, 16,057, 16,058, analyzer (ANKOM Technology Corporation, Macedon, NY, 16,059, 16,060, 16,061, 16,062, 16,064, 16,065, USA) was used for NDF and ADF (Van Soest et al., 1991) and 16,068, 16,069 y 16,071 for IVDMD (Tilley and Terry, 1963). Unknown 673, 685, 6,094, 6,095, 6,171, 6,175, 6,461, 6,497, The results of the reference chemical analysis and the spectral 6,500, 6,501, 6,525, 6,658, 6,784, 6,787, 6,796, 6,799, signals of each sample were processed using Win ISI software 6,805, 6,831, 6,836, 6,837, 6,839, 6,840, 6,842, 6,843, version 4.0. Then, the results were incorporated in equations 6,855, 6,857, 6,864, 6,866, 6,868, 26,723, 26,906, 26,911, 26,917, 26,923, 26,924, 26,925, 26,936, generated at the CIAT forages and animal nutrition quality 26,937, 26,939, 26,942, 26,944 y 26,947 laboratory, as follows: R2 of 0.93, 0.98, 0.85, and 0.98 and Ivory Coast 6,872 standard error for cross validation (SECV) of 2.11, 1.22, 2.78, and Rwanda 26,360 0.61 for NDF, ADF, IVDMD, and CP, respectively (Molano et al., Commercial 6,962 Mombasa, 6,826 Coloniao, 16,031 Tanzania, 2016). This increases the action range and accuracy of the model. 6,299 Tobiatá, 26,900 Vencedor y Massai Data Analysis Descriptive statistics and Pearson correlation coefficient for every Urochloa species (U. brizantha cv. Toledo and hybrid cv. season were obtained with SAS Statistical Software (Statistical Cayman) as controls (Table 1), were established in plots using a Analysis System) version 9.4 (2018) (SAS, 2016). Figure of randomized complete block design with three replications. The correlation was obtained with package corrplot in R (Wei experimental units (plots) measured 4m2, and the plants had 10– and Simko, 2017). Cluster analysis was used, and principal 12 tillers. The distance between plots was 1m, and the distance components were calculated using the library “FactoMineR” and between blocks was 2m (Figure 2). package “Factoextra” (Kassambara and Mundt, 2020) with the To determine the number of regrowing days and provide variables NDF, ADF, CP, and IVDMD for every season. Figures homogeneous conditions for all accessions, a standardization cut were created in R using the package “ggplot2” (Wickham, 2016). was applied. It was a mechanical cutting of plots at a residual Wilcoxon sum rank test was used to compare differences between height of 30 cm above the soil. Seasonal conditions in the field means in terms of the season for each of the variables in R area and harvesting age are shown in Table 2. version 4.0.3 (R Core Team, 2020). We measured (a) plant height according to the methodology To find a classification index for the fodder material of Toledo and Schultze-Kraft (1982) and (b) flowering (FW). according to nutritional content, multicriteria weighted indices We used observations and calculated the percentage of flowering were adapted (Contreras et al., 2004). To obtain a level Frontiers in Sustainable Food Systems | www.frontiersin.org 731 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons FIGURE 2 | Aerial view of the field experimental design. R, replications. TABLE 2 | Seasonal conditions and plant harvesting parameters for agronomy and nutritional evaluation in the Patía Valley, Cauca, Colombia. Season Plant harvesting parameter Period of evaluation Temperature (◦C) Humidity Total from average % precipitation (mm) Regrowing Average height (cm) Minimum Maximum Average Average Rainy 6 weeks or 41 days 130.7 March 24 to May 4, 2017 21.5 31.8 26.7 77 172.1 Dry 8 weeks or 55 days 55.2 June 30 to August 24, 2017 19.6 36.1 27.8 61.7 22.8 of classification, a value was assigned to each variable RESULTS considering the relative importance with regard to nutritional assessment of CP, NDF, ADF, and IVDMD in consumption, The contrasting seasons present in the Colombian dry tropics use, and rumen degradability-diet composition (Van Soest, 1982; might explain the differences found in this research regarding the Barahona-Rosales and Sánchez-Pinzón, 2005). The Nutritional agronomic and nutritional behavior of M. maximus. Flowering, Classification Index was calculated as follows: plant height, BDM, and CP decreased during the dry season NCI = (IVDMD R ∗8 + IVDMD D ∗7 + CP R ∗6 + CP D ∗5 compared with the rainy season at 64.8, 57.8, 43.1, and + NDF R∗4+ NDF D ∗3+ ADF R∗2+ ADF D ∗1)/8, 27.7%, respectively (Table 3). Low precipitation, the lowest where NCI is the Nutritional Classification Index, IVDMD R relative humidity, and the highest temperature (Table 2) were is the in vitro dry matter digestibility rainy season, IVDMD D is determining factors for the changes observed mainly in the the IVDMD dry season, CP R, is the crude protein rainy season, agronomic variables. The average NDF, ADF, and IVDMD CP D is the CP dry season, NDF R is the neutral detergent fiber contents of the M. maximus collection differ from 1 to 2% from rainy season, NDF D is the NDF dry season, ADF R is the acid one season to the other. The Wilcoxon test for comparison of detergent fiber rainy season, and ADF D is the ADF dry season. means indicates statistical differences when the accessions are To select accessions without significant changes in nutritional under different rainfall conditions (Table 3). composition in the evaluation from one season to the next, Commercial cultivars of M. maximus show a similar the Hotelling T-squared test was performed using the Hotelling nutritional behavior as the rest of the studied collection. During library and package corpcor in R (Schafer et al., 2017). the dry season, NDF content increased slightly except in Frontiers in Sustainable Food Systems | www.frontiersin.org 742 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons TABLE 3 | Descriptive statistics and significance between seasons of the nutritional composition and agronomic traits of a collection of Megathyrsus maximus in Colombian dry tropical. Variable Season x Median SD Minimum Maximum p-value NDF (%) Rainy 66.5 66.5 1.47 63.2 70.7 0.00118 Dry 67.2 67.1 2.17 62.1 74.0 ADF (%) Rainy 39.2 39.0 1.48 35.3 42.6 0.00000 Dry 38.3 38.2 1.54 34.7 44.0 CP (%) Rainy 10.1 10.1 0.95 7.6 13.9 0.00000 Dry 7.3 7.3 0.98 4.9 10.5 IVDMD (%) Rainy 57.9 58.0 2.13 52.3 62.6 0.00126 Dry 59 59.2 2.78 50.0 65.3 Height (cm) Rainy 130.7 132.7 19.27 74 163.3 0.00000 Dry 55.2 55.0 7.87 35 76.7 Biomass (t/ha) Rainy 5.8 5.6 1.42 2.5 9.5 0.00000 Dry 3.3 3.2 0.79 1.6 5.3 Flowering (%) Rainy 76.2 100 34.19 34.1 100 0.00000 Dry 26.8 20 25.78 0 100 NDF, neutral detergent fiber; ADF, acid detergent fiber; CP, crude protein; IVDDM, in vitro digestibility of dry matter. Mombasa, Massai, and Coloniao. In contrast, ADF content For the cluster analysis, three clusters (Cl) were defined decreased, except in Tanzania. Tanzania shows higher CP content (Table 4 and Figure 5) considering the degree of resemblance and the lowest NDF y ADF content during the rainy season. in specific characteristics of the accessions for each cluster. Mombasa and Coloniao stand out for featuring the lowest NDF For both seasons, the best nutritional composition corresponds and ADF content during the dry season. Vencedor and Coloniao to accessions of Cl 1; some accessions and material of genus showed high IVDMD during the rainy season and Mombasa in Urochloa have lower NDF and ADF and higher CP and the dry season (Figure 3). IVDMD, contrary to what Cl3 shows, with accessions having Analysis using Pearson’s correlation coefficient shows that lower nutritional content with higher NDF and ADF and lower different degrees of associativity exist, highlighting values highly CP. Cl2 materials are characterized by having an intermediate significant and superior (r ≥ 0.3). Among the agronomic composition between Cl1 and Cl3 (Tables 4, 5). In dry and rainy measurements, plant height is directly related to DMB in a seasons, 51.2 and 19.4% of the collection, respectively, stands positive manner (r = 0.41 and 0.48, rainy and dry season, out for its nutritional profile. Therefore, a higher number of respectively), whereas with flowering, it is related in a negative accessions have a great nutritional profile during the dry season manner in the rainy season (r = 0.39). This could be in the tropics and are available for further study. interpreted as a high forage yield being estimated for the The distribution of the clusters (Figure 5) shows the tall accessions in the rainy season during 42 days, and not description of the correlations and the different nutritional presenting flowering or having low flowering upon finalizing the behavior from Megathyrsus and Urochloa species, during both cutting period. seasons. Also, during the rainy season, the response of Tanzania The positive relationship existing between flowering stands out. and structural carbohydrate content is evidenced in the In each season, the following accessions stand out for being two seasons. This suggests that physiological traits such part of the 41.9% of the collection with DMB above average at 5.9 as flowering could have a stronger relationship with the and 3.4 t/ha in the rainy and dry season, respectively, and being nutritional parameters in the M. maximus collection classified in the cluster with the best nutritional profile (Cl). under the edaphoclimatic conditions of the Colombian In the rainy season, accessions CIAT 6,501, 6,842, 6,868, dry tropical forest. Likewise, in Figure 4, a higher degree 16,004, 16,023, 16,048, 16,062, 16,071, and 26,723 stand out; in of associativity is noted among the traits estimated in the the dry season, accessions CIAT 693, 6,171, 6,497, 6,658, 6,836, nutritional evaluation. 6,891, 6,898, 6,903, 16,005, 16,011, 16,025, 16,027, 16,034, 16,035, In both seasons, the structural carbohydrate content of M. 16,036, 16,038, 16,039, 16,044, 16,049, 16,058, 16,059, 26,936, maximus influenced CP content in a negative manner. The 26,937 and Massai stand out. correlation is higher for ADF content. For the NCI, the highest indices correspond to accessions 685 In the rainy season, ADF (r = 0.65) shows a moderate and (199.05) and 6,864 (197.30), belonging to Cl1 in both seasons. negative correlation with IVDMD, higher than when we refer Accession CIAT 26,911 had one of the highest values for NDF, to NDF (r = 0.49). NDF and ADF have an evident positive also standing out for its value in NCI (198.91). correlation, resulting from the use of NDF content in the ADF On the other hand, Hotelling’s multivariate T-squared test calculation (Figure 4). showed that accessions 6,968, 26,360, and 26,947 did not feature Frontiers in Sustainable Food Systems | www.frontiersin.org 753 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons FIGURE 3 | Comparative analysis between commercial cultivars of Megathyrsus maximus in terms of CP, crude protein; NDF, neutral detergent fiber; ADF, acid detergent fiber; IVDMD, in vitro dry matter digestibility. significant changes from the rainy to dry season in NDF, ADF, CP, those registered in other tropical regions (Machado, 2013; and IVDMD, and their NCI surpassed 189.94. Benabderrahim and Elfalleh, 2021), with fertilization (Braz et al., 2017) or higher rainfall (Macedo et al., 2017). Discussion Studies with commercial varieties suggest that, at 70-to 90- Edaphoclimatic stress factors are abiotic indicators that become cm height, a higher quantity of biomass is generated with important in the search for forage material adapted for intensive adequate grassland recovery for the next grazing (Soares Filho production in a sustainable manner (Rao, 2013). In the Patía et al., 2015; Carvalho et al., 2017). In the rainy season, the Valley region, a representative dry tropical agroecosystem, the entire collection reached the mínimum value of the range; evaluations set up in this research during contrasting seasons whereas, in the dry season, this was obtained only by accessions allowed us to compare the agronomic and nutritional behavior 16,035, 691, 6,982, 6,960, and 6,915 (Supplementary Material). of a collection of M. maximus, helping to identify physiological For DMB, an important variable for adoption processes by mechanisms and the association of flowering with nutritional farmers in tropical countries (Mwendia et al., 2019), the mean traits, which contributes to the selection of interesting traits. and maximum values (5.8 and 9.5 t/ha, respectively) of the This provides tools so that breeding programs can broaden their collection during the rainy season were similar to those reported research when seeking forage material resilient to climate change. in previous studies in the same zone with commercial cultivars Plant height, flowering, DMB and crude protein of the (6.3 and 9.8 t/ha, every 45 days) (Vivas-Quila et al., 2015). collection were higher during the rainy season, contrasting with In spite of the dry season, the average and maximum values stress, growth, and production limitations during the dry season of DMB declined notably (3.3 and 5.3 t/ha, respectively). The (Hare et al., 2015), which indicates that the water supply favors values obtained were also higher than those obtained with agronomic characteristics and protein content (Larsen et al., naturalized species in the Patía Valley region, and in different 2021). Weather characteristics have an effect on agronomic and tropical regions such as Brazil (Macedo et al., 2017) and nutritional parameters for M. maximus (Machado, 2013; Lemos Cuba (Machado, 2013). These values were improved only in et al., 2017; Maranhão et al., 2021; Marcillo et al., 2021). Thailand with nitrogen fertilization (Hare et al., 2015). In addition, the positive correlation between plant height and DMB Productive Measurements and Flowering (Figure 4) might indicate that the evaluated collection presents The mean values for plant height and DMB reached by adequate DMB yield under the edaphoclimatic conditions of the the M. maximus germplasm were similar and superior to Patía Valley. Frontiers in Sustainable Food Systems | www.frontiersin.org 764 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons FIGURE 4 | Correlograms with Pearson coefficient to visualize correlation among agronomic and nutritional variables of the Megathyrsus maximus collection in the Patía Valley of Colombia. BIOMASS_R, biomassa dry matter in rainy season; BIOMASS_D, biomassa dry matter in dry season; Heigh_R, in rainy season; Heigh_D, in dry season; FW_R, flowering in rainy season; FW_D, flowering in dry season; NDF_R, neutral detergent fiber in rainy season; NDF_D, neutral detergent fiber in dry season; ADF_R, acid detergent fiber in rainy season; ADF_D, acid detergent fiber in dry season; CP_R, crude protein in rainy season; CP_R, in dry season; IVDMD_R, in vitro dry matter digestibility in rainy season; IVDMD_D, in vitro dry matter digestibility in dry season. TABLE 4 | Nutritional behavior per cluster in a Megathyrsus maximus collection during rainy and dry seasons in Colombian dry tropical forests. Cluster Number of accessions NDF (%) ADF (%) CP (%) IVDMD (%) Rainy Dry Rainy Dry Rainy Dry Rainy Dry Rainy Dry 1 25 66 64.7 ± 1.6c 65.9 ± 1.7c 37.0 ± 1.4c 37.2 ± 1.1c 11.4 ± 0.7a 8.0 ± 0.8a 59.9 ± 1.7a 60.2 ± 2.0a 2 55 30 66.6 ± 1.3b 67.4 ± 1.8b 38.6 ± 0.7b 38.6 ± 1.0b 10.0 ± 0.7b 7.1 ± 0.6b 59.0 ± 1.0b 55.9 ± 1.9c 3 51 35 67.4 ± 1.1a 69.5 ± 1.9a 40.6 ± 0.8a 40.2 ± 1.3a 9.5 ± 06c 6.4 ± 0.6c 55.8 ± 1.3c 60.0 ± 1.9b Note. NDF, neutral detergent fiber; ADF, acid detergent fiber; CP, crude protein; IVDDM, in vitro digestibility of dry matter. Different letters denote statistical differences according to analysis of variance and Tukey HSD test (α = 0.05). Megathyrsus maximus is usually described as drought resistant NDF andADF content and persistency in the field. Light intensity (Rodríguez et al., 2017) with adaptation to varied edaphoclimatic might also affect flowering (Tavares de Castro and Carvalho, conditions because of its clumps and strong root system 2000). During the dry season, no flowering occurred, or it was (Kissmann and Groth, 1995; Benabderrahim and Elfalleh, 2021). lower than 10% for accessions: 622, 688, 693, 6,094, 6,175, 6,299 However, it expresses its productive potential during the rainy Tobiatá, 6,497, 6,500, 6,525, 6,658, 6,796, 6,837, 6,857, 6,868, season. Under the edaphoclimatic conditions of the Patía Valley 6,897, 6,901, 6,906, 6,918, 6,923, 6,927, 6,928, 6,948, 6,962, 6,963, and during the rainy period, it is possible to consider a recovery 6,968, 16,003, 16,017, 16,023, 16,027, 16,028, 16,034, 16,035, period of about 35 days, and it is advised to consider irrigation 16,036, 16,038, 16,039, 16,048, 16,049, 16,051, 16,055, 16,061, during the dry season to reach the potential of the species. 16,062, 16,069, 16,071, 26,360, 26,900 vencedor, 26,906, 26,923, Flowering is a determining variable for plant breeding 26,924, 26,925, 26,937, and 26,939 (39.5% of the collection), technology adoption processes. It is related to forage yield (Casler and during the rainy season for accessions 6,299 Tobiatá, 6,962 et al., 2018; Casler, 2019). Flowering determines nutritional Mambasa, 6,963, 16,027, 16,028, 16,035, 16,044, 16,051, 16,061, composition (Gusha et al., 2019), specifically in this research with 16,069, 16,071, 26,723, and 26,925. Frontiers in Sustainable Food Systems | www.frontiersin.org 775 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons FIGURE 5 | Cluster analysis based on principal components of the germplasm collection of Megathyrsus maximus. Cumulative variance accounts for 86 and 80% for the rainy and dry season, respectively. ADF, acid detergent fiber; CP, crude protein; IVDMD, in vitro dry matter digestibility; NDF, neutral detergent fiber. (A) Rainy season. (B) Dry season. Flowering was the variable that declined the most when (Van Soest, 1982; Velásquez et al., 2010; Santiago-Hernández it was evaluated in the dry season vis-à-vis the rainy et al., 2016; de Vasconcelos et al., 2019; Schnellmann et al., season. Lower flowering in germplasm during the dry 2020; Tesk et al., 2020), which affects digestibility in animals season despite better light conditions in the tropics could (Valente et al., 2010). Variability in structural carbohydrates be associated with hydric stress (Wilson and Ng, 1975) and (NDF, ADF) in the M. maximus collection might be influenced high evaporation, with the possibility that this could generate by characteristics related to the accessions’ own physiological and a negative hydric balance for forage production and the metabolic aspects such as the conversion efficiency of nitrogen production process of grasses (Rao, 2013). According to and flowering rate (dos Costa et al., 2017), which might generate (Atencio Solano et al., 2018) , there is an evident effect of a wide range of available accessions and could be used in the dry season on vegetative development, which influences plant breeding programs (Deo et al., 2020) to produce or select flowering of the species. This matches the negative correlation materials with the best IVDMD (Barahona-Rosales and Sánchez- between flowering and plant height in the rainy season Pinzón, 2005). (r = 0.39). The protein content decline during low precipitation periods, similar to that found by Larsen et al. (2021), might be caused Nutritional Composition by the lack of production of new leaves and tillers. Also, Factors such as management, regrowth age, fertilization, cut the senescent material decreases cellular content, in particular, height, phonological aspects, growth under shade, and season protein (Vargas Junior et al., 2013). M. maximus shows a might have a significant effect on the nutritional value of forages higher protein content during the rainy season and under shady Frontiers in Sustainable Food Systems | www.frontiersin.org 786 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons TABLE 5 | Grouping of the M. maximus collection by nutritional behavior in rainy most of the plants for a complementary diet are grasses, fodder and dry seasons of the Patía Valley, Cauca, Colombia. legumes, and other plants rich in protein, the contribution ofM. maximus could be ideal to avoid a loss of rumen functionality and Season Cluster 1 to support livestock production during the dry season. Rainy 685, 6,501, 6,787, 6842, 6,843, 6,864, 6,868, 6923, 6,928, 6,968, 16,003, 16,004, 16,018, 16,021, 16,023, A high negative correlation exists between structural 16,025, 16,031, 16,048, 16,051, 16,057, 16,062, carbohydrate content and digestibility (Jung et al., 1997) in the 16,071, 26,723, 26,924 and Urochloa hibrido cv M. maximus collection in the rainy season. This might have Cayman incremented IVDMD by 1.86% during the dry season. Therefore, Dry 673, 685, 688, 693, 6,171, 6,461, 6,497, 6,501, 6525, the results of this parameter highlight the potential of this species 6,658, 6,787, 6,826, 6,831, 6,836, 6,837, 6,839, 6,864, as an alternative during low-precipitation periods, for both 6,866, 6,868, 6,872, 6,890, 6,891, 6,898, 6903, 6,906, 6,912, 6,918, 6,927, 6,962, 6,968, 6,983, 6,984, 6,986, biomass production (Morales-Velasco et al., 2016) and steady 6996, 16,003, 16,005, 16,011, 16,018, 16,021, 16,023, relative quality. 16,025, 16,027, 16,034, 16,035, 16,036, 16,038, During the dry season, Tobiatá, Mombasa, Tanzania, 16,039, 16,044, 16,048, 16,049, 16,057, 16,058, Vencedor, Massai, and Coloniao had protein content of 7.09, 16,059, 16,060, 16,061, 16,062, 16,071, 26,360, 26,917, 26,924, 26,936, 26,937, 26,947, Massai, 6.24, 6.13, 6.72, 7.82, and 8.30%, respectively. These values were Urochloa brizantha cv toledo and Urochloa hibrido cv higher than those found in commercial cultivars in important Cayman tropical livestock areas (dos Costa et al., 2017; Silva et al., 2017; Cluster 2 da Silva et al., 2018). However, in the same research location Rainy 622, 693, 6,094, 6,175, 6461, 6,497, 6,500, 6,571, where this experiment took place, and with a similar number of 6,784, 6,796, 6,799, 6,805, 6,826, 6,831, 6,837, 6,839, regrowing days and average height in Massai, Ruiz et al. (2015) 6,855, 6,872, 6,890, 6,901, 6,903, 6,927, 6,929, 6,944, showed 14.20% CP. This could possibly be due to fertilization at 6,948, 6,960, 6,962, 6,969, 6,982, 16,005, 16,017, establishment and evaluation during the rainy season. 16,028, 16,034, 16,035, 16,036, 16,038, 16,039, 16,044, 16,046, 16,049, 16,055, 16,059, 16,061, In tropical regions of Colombia, productive differences exist 16,064, 26,360, 26,900, 26,906, 26,911, 26,923, between commercial cultivars and genotypes of the evaluated 26,925, 26,937, 26,939, 26,944, 26,947 and Urochloa collection in this research, which could be associated with brizantha cv toledo aspects inherent to morphology (Patiño-Pardo et al., 2018) and Dry 622, 691, 692, 6,094, 6,175, 6,299, 6,500, 6,536, nutritional profile. These are advantageous characteristics in 6,571, 6,805, 6,840, 6,842, 6,857, 6,893, 6,897, 6,901, 6,928, 6,929, 6,944, 6,948, 6,954, 6,967, 6,969, 6,975, terms of adaptation to different livestock systems. 6,982, 16,017, 16,019, 16,031, 16,051, 16,069, 26,900, Some studies suggest that in vitro and in vivo digestibility of 26,906, 26,923, 26,925 and 26,939 organic matter increases with the rainy season (Vargas Junior Cluster 3 et al., 2013; Silva et al., 2017), and others show that water stress Rainy 673, 688, 691, 692, 6,095, 6,171, 6,299, 6,525, 6,536, did not significantly affect organic matter digestibility (OMD), 6,658, 6,836, 6,840, 6,857, 6,866, 6,891, 6,893, 6,897, (Fariaszewska et al., 2020). The findings in this research suggested 6,898, 6,900, 6,906, 6,912, 6,915, 6,918, 6,945, 6,949, that ADF decreased similar to that reported by Larsen et al. 6,951, 6,954, 6,955, 6,963, 6,967, 6,975, 6,981, 6,983, 6,984, 6,986, 6,990, 6,996, 16,011, 16,019, 16,027, (2021) and IVDMD increased slightly during the dry season 16,041, 16,054, 16,058, 16,060, 16,065, 16,068, vis-à-vis the rainy season. This condition might be related to 16,069, 26,917, 26,936, 26,942 and Massai the average height of germplasm of 130.7 vs. 55.2 cm during Dry 6,095, 6,784, 6,796, 6,799, 6,843, 6,855, 6,900, 6,915, the rainy and dry seasons, respectively. Therefore, growth in 6,923, 6,945, 6,949, 6,951, 6,955, 6,960, 6,963, 6,981, height could result from a decrease in leaf material and the 6,990, 16,004, 16,028, 16,041, 16,046, 16,054, 16,055, respective digestibility (Kalmbacher et al., 1980), and drought 16,064, 16,065, 16,068, 26,723, 26,911, 26,942 and 26,944 stress might delay maturity, which can improve the OMD of forages (Fariaszewska et al., 2020). The correlations found in the M. maximus collection were similar to those reported by Stabile conditions (Dele et al., 2017; Barragán-Hernández and Cajas- et al. (2010) with commercial cultivars. Girón, 2019). In contrast, other authors argue that higher values The classification of the accessions undermultivariate tests (by for protein can be found during the dry season (Rodríguez et al., cluster analysis and Hotelling’s T-squared test) and NCI shows 2017). that the genotypic and physical characteristics specific to each The preservation of beef cattle is an important goal in the accession (not included in this study) as well as morphological Patía Valley region, where animals lose weight and mortality aspects (Santos et al., 2010), leaf-to-stem ratio (Homen et al., increases because of the lack of water and good-quality feed. 2010), and maturity or metabolism rate (dos Costa et al., 2017) Considering the challenging hydric conditions of the tropical may have influenced the classification of materials with a low or zone during the dry season, the average protein content of 7.3% high nutritional profile. and the maximum of 10.5% in M. maximus stand out. These This classification shows that some accessions respond to nutritional values contribute to preserving rumen functionality. prolonged tropical dry periods and possibly show promise for A relevant consideration to keep a functional rumen in bovines resilient nutritional quality with adequate DMB. In addition, is the minimum required nitrogen amount equivalent to 8% of M. maximus outperforms other forage species used for grazing CP (Gaviria et al., 2015). Also, considering that in this region under semiarid or dry tropical conditions (Coêlho et al., Frontiers in Sustainable Food Systems | www.frontiersin.org 797 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons 2018). For a diversity of agronomic parameters and nutritional AUTHOR CONTRIBUTIONS composition related to genetic aspects, M. maximus shows promise for breeding programs. JC-T carried out the experimental work, statistical analyses, Agronomic and nutritional analysis, in general terms, allows wrote the manuscript, the original draft, and the methodology. us to learn about a large group of Megathyrsus maximus JM performed the experiment based on NIRS Technology. accessions as potential options for the establishment and NV-Q handled the supervision, the project administration, management of productive and efficient cattle raising under the the acquisition of funds, helped on the conceptualization, agro ecological conditions of the Patía Valley, thus, contributing validation, and the writing of the original draft. All to the agricultural development of the region and the quality of authors contributed to the analysis and interpretation life of its producers. of data. The M. maximus collection contains several materials that stand out for their nutritional value (CP, NDF, ADF, and ACKNOWLEDGMENTS IVDMD), which, although they did not show a relationship with DMB, have sufficient productive yield. They also have The authors express their gratitude for the contributions to adaptation potential for drought or low-rainfall conditions in this study to the National Open and Distance University of tropical regions. Therefore, they represent a suitable option for Colombia—UNAD, the Government of Cauca; the Colombian sustainable livestock systems. Furthermore, they help subsequent General System of Royalties (SGR); the Universidad del plant breeding programs to contribute to finding alternative Cauca and its School of Agricultural Sciences, its Research materials to maintain adequate feeding efficiency for cattle and Group NUTRIFACA, and the Cooperative of Producers from mitigate the effects of climate change. Patía Valley (COOAGROUSUARIOS—Cooperativa de Usuarios Both the genotypic characteristics of M. maximus and Campesinos del Patia—Peasant Users Cooperative of the Patia environmental conditions during contrasting seasons are Valley). This research was conducted as part of the CGIAR factors that might influence the variability of nutritional Research Program on Livestock and is supported by contributors content, productive parameters, and flowering of the evaluated to the CGIAR Trust Fund. CGIAR is a global research germplasm. This allows a classification of forage material partnership for a food-secure future. Its science is carried out according to specific or preferential criteria of farmers and by 15 Research Centers in close collaboration with hundreds of plant breeders. partners across the (globe. www.cgiar.org). DATA AVAILABILITY STATEMENT SUPPLEMENTARY MATERIAL The original contributions presented in the study are included The Supplementary Material for this article can be found in the article/Supplementary Material, further inquiries can be online at: https://www.frontiersin.org/articles/10.3389/fsufs. directed to the corresponding author. 2021.684747/full#supplementary-material REFERENCES Panicum maximum Jacq. Ciência Rural 47, 1–6. doi: 10.1590/0103-8478cr201 60599 AOAC International (2002). AOAC Official Method 2001.11 Protein (Crude) Carvajal-Tapia, J., Morales Velasco, S., Villegas, D. M., Arango, J., and Vivas in Animal Feed, Forage (Plant Tissue), Grain, and Oilseeds. Rockville, MD: Quila, N. J. (2021). Biological nitrification inhibition and forage productivity of AOAC International. Available online at: http://www.eoma.aoac.org/methods/ Megathyrsus maximus in Colombian dry tropics. Plant Soil Environ 5, 270-277. info.asp?ID$=$32924 (accessed March 15, 2020). doi: 10.17221/445/2020-PSE Atencio Solano, L., Tapia Coronado, J. J., Barragán Hernández, W., Mojica Carvalho, S. A. L., Martuscello, J. A., de Almeida, O. G., dos Santos Braz, T. G., Rodriguez, J. E., Suárez, E., Martínez, A., et al. (2018). Cultivar de pasto Guinea DaCunha, D. D. N., and Jank, L. (2017). Production and quality of Mombaça (Megathyrsus maximus) Gramínea forrajera de alta producción de forraje, grass forage under different residual heights. Acta Scientiarum. Animal Sci. excelente calidad nutricional y abundante producción de semilla AGROSAVIA. 39:143. doi: 10.4025/actascianimsci.v39i2.34599 Available online at: https://repository.agrosavia.co/handle/20.500.12324/34646 Casler, M. D. (2019). Selection for flowering time as a mechanism to (accessed October 15, 2019). increase biomass yield of upland switchgrass. Bioenergy Res. 13, 100–108. Barahona-Rosales, R., and Sánchez-Pinzón, S. (2005). Physical and chemical doi: 10.1007/s12155-019-10044-3 limitations to the digestibility of tropical forages and strategies to overcome Casler, M. D., Vogel, K. P., Lee, D. K., Mitchell, R. B., Adler, P. R., Sulc, R. M., et al. them. Dialnet 6, 69–82. doi: 10.21930/rcta.vol6_num1_art:39 (2018). 30 years of progress toward increased biomass yield of switchgrass and Barragán-Hernández, W. A., and Cajas-Girón, Y. S. (2019). Bromatological big bluestem. Crop Sci. 58, 1242–1254. doi: 10.2135/cropsci2017.12.0729 and structural changes in Megathyrsus maximus in four silvopastoral Castañeda, L., Olivera, Y., and Wencomo, H. B. (2015). Selection of Pennisetum arrangement systems. Corpoica Cienc. Tecnol. Agropecu. 20, 245–258. purpureum accessions for livestock feeding systems. Pastos y Forrajes, doi: 10.21930/rcta.vol20_num2_art:1458 38, 170–175. Available online at: http://scielo.sld.cu/pdf/pyf/v38n2/pyf03215. Benabderrahim, M. A., and Elfalleh, W. (2021). Forage potential of non-native pdf guinea grass in North African agroecosystems: genetic, agronomic, and Coêlho, J. J., de Mello, A. C. L., dos Santos, M. V. F., Dubeux Junior, J. C. B., da adaptive traits. Agronomy 11:1071. doi: 10.3390/agronomy11061071 Cunha, M. V., Lira, M., et al. (2018). Prediction of the nutritional value of grass Braz, D. S. T. G., Martuscello, J. A., Jank, L., da Fonseca, D. M., Resende, M. species in the semiarid region by repeatability analysis. Pesqui. Agropecu. Bras. D. V., and Evaristo, A. B. (2017). Genotypic value in hybrid progenies of 53, 378–385. doi: 10.1590/s0100-204x2018000300013 Frontiers in Sustainable Food Systems | www.frontiersin.org 1780 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons Contreras, I., Hinojosa, M. A., and Mármol, A. (2004). Multicriteria weighted dry matter and neutral detergent fiber. J. Dairy Sci. 80, 1622–1628. indices with ordinal information. Estadística Española 46, 95–117. Available doi: 10.3168/jds.S0022-0302(97)76093-4 online at: https://dialnet.unirioja.es/servlet/articulo?codigo=831086 Kalmbacher, R., Hodges, E., and Martin, F. (1980). Effect of plant height and Cook, B. G., and Schultze-Kraft, R. (2015). Botanical name changes: nuisance or a cutting height on yield and quality of Indigofera hirsuta. Trop. Grassl. 14, 14–18. quest for precision? Trop. Grassl. 3, 34–40. doi: 10.17138/TGFT(3)34-40 Kassambara, A., and Mundt, F. (2020). Factoextra: Extract and Visualize the Cooke, R. F., Daigle, C. L., Moriel, P., Smith, S. B., Tedeschi, L. O., and Vendramini, Results of Multivariate Data Analyses. R package version 1.0.7. Available online J. M. B. (2020). Cattle adapted to tropical and subtropical environments: at: https://CRAN.R-project.org/package=factoextra (accessed September 09, social, nutritional, and carcass quality considerations. J. Anim. Sci. 98:skaa014. 2021). doi: 10.1093/jas/skaa014 Kissmann, K., and Groth, D. (1995). Plantas infestantes e nocivas. In Tomo 3. da Silva, A. B., de Carvalho, C. A. B., Morenz, D. A., da Silva, P. H. F., dos Santos, Available online at: http://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=agrissa. A. J., Santos, F. C., et al. (2018). Agricultural answers and chemical composition xisandmethod=postandformato=2andcantidad=1andexpresion=mfn=003492 of Massai grass under different nitrogen doses and urea sources. Semina: Ciênc. (accessed December 12, 2018). Agrár. 39:1225. doi: 10.5433/1679-0359.2018v39n3p1225 Larsen, R. E., Shapero, M. W. K., Striby, K., Althouse, L. D., Meade, D. E., Brown, de Vasconcelos, A. M., Dutra, M. C. A., Silveira, R. M. F., da Silva, V. J., Nunes, L. K., et al. (2021). Forage quantity and quality dynamics due to weathering A. P. L., and Ferreira, J. B. (2019). Production and nutritive value of canarana over the dry season on California annual rangelands. Rangel. Ecol. Manag. 76, erecta lisa (Echinocloa piramidalis Lam.) in response to harvest intervals. Ciênc. 150–156. doi: 10.1016/j.rama.2021.02.010 Anim. Bras. 20, 1–11. doi: 10.1590/1809-6891v20e-52300 Lemos, S. N. L., Rodrigues Cavlcante, A. C., Freire Da Silva, T., Macedo Pezzopane, Dele, P., Akinyemi, B., Amole, T., Okukenu, O., Sangodele, O., Sosande, O., et al. J. R., Santos, P. M., and Duarte Candido, M. J. (2017). Agro-climatic suitability (2017). Effect of manure type and season of harvest on the forage yield, quality and water requirement for Tanzania guineagrass cultivation in the state of and macro-elements of two Panicum maximum varieties. Niger. J. Anim. Sci. Ceará. Rev. Caatinga 30, 1028–1038. doi: 10.1590/1983-21252017v30n424rc 19, 265–282. Available online at: https://www.ajol.info/index.php/tjas/article/ Macedo, V., Quadros Cunha, A., Cândido, E. P., Domingues, F. N., Melo, view/163832 D., de, M., et al. (2017). Estructura e productividade de Campim-Tanzania Deo, T. G., Ferreira, R. C. U., Lara, L. A. C., Moraes, A. C. L., Alves-Pereira, submetido a diferentes frquencias de desfolhacao. Ciênc. Anim. Bras. 18, 1-10. A., de Oliveira, F. A., et al. (2020). High-resolution linkage map with allele doi: 10.1590/1089-6891v18e-38984 dosage allows the identification of regions governing complex traits and Machado, R. (2013). Comportamiento de 19 accesiones de Panicum maximum apospory in guinea grass (Megathyrsus maximus). Front. Plant Sci. 11:15. Jacq. bajo condiciones de pastoreo en un suelo de mediana fertilidad. Pastos doi: 10.3389/fpls.2020.00015 y Forrajes, 36, 202–208. Available online at: http://ve.scielo.org/scielo.php? dos Costa, C. S., Rodrigues, R. C., de Araújo, R. A., Cândido, M. J. D., Santos, script=sci_arttext&pid=S0798-72692010000200012&lng=es&nrm=iso F. N., et al. (2017). Agronomic and nutritional characteristics of Massai grass Maranhão, S. R., Franco Pompeu, R. C. F., de Araújo, R. A., Lopes, M. N., subjected to deferred grazing and nitrogen fertilization. Semin. Cienc. Agrar. Duarte Cândido, M. J., de Souza, H. A., et al. (2021). Morphophysiology 38, 1617–1624. doi: 10.5433/1679-0359.2017v38n3p1607 of tropical grasses under different water supply in two growing seasons: II. Fariaszewska, A., Aper, J., Van Huylenbroeck, J., De Swaef, T., Baert, J., and Pecio, BRS Massai and BRS Tamani grasses. Semina: Cienc. Agrar. 42, 301–318. L. (2020). Physiological and biochemical responses of forage grass varieties doi: 10.5433/1679-0359.2021v42n1p301 to mild drought stress under field conditions. Int. J. Plant Prod. 14, 335–353. Marcillo, R. L. G., Guamàn, W. E. C., Pincay, A. E. G., Zambrano, P. A. doi: 10.1007/s42106-020-00088-3 V., Naveda, N. R. O., and Rivera, S. A. G. (2021). Assessment of guinea Gándara, L., Borrajo, C., Fernández, J., and Pereira, M. (2017). Efecto de la grass Panicum maximum under silvopastoral systems in combination with fertilización nitrogenada y la edad del rebrote sobre el valor nutritivo de two management systems in Orellana Province, Ecuador. Agriculture 11:117. Brachiaria brizantha cv. Marandú. Rev. FCA UNCUYO 49, 69–77. Available doi: 10.3390/agriculture11020117 online at: https://www.redalyc.org/articulo.oa?id=382852189006 Matínez-Mamian, C., Vivas-Quila, N. J., and Morales-Velasco, S. (2020). Gaviria, X., Naranjo, J. F., and Barahona, R. (2015). Cinética de fermentación Agronomic response of forage mixtures in a silvopastoral system in the in vitro de Leucaena leucocephala y Megathyrsus maximus y sus mezclas, Colombian dry tropics. Dyna 87, 80–84. doi: 10.15446/dyna.v87n213.79900 con o sin suplementación energética. Pastos y Forrajes 38, 55–63. Available Mazabel, J., Worthington, M., Castiblanco, V., Peters, M., and Arango, J. (2020). online at: http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0864- Using near infrared reflectance spectroscopy for estimating nutritional quality 03942015000100006 of Brachiaria humidicola in breeding selections. Agrosyst. Geosci. Environ. 3, Gerber, P. J., Mottet, A., Opio, C. I., Falcucci, A., and Teillard, 1–9. doi: 10.1002/agg2.20070 F. (2015). Environmental impacts of beef production: review of Molano, M. L., Cortés, M. L., Ávila, P., Martens, S. D., and Muñoz, L. S. (2016). challenges and perspectives for durability. Meat Sci. 109, 2–12. Ecuaciones de calibración en espectroscopía de reflectancia en el infrarrojo doi: 10.1016/j.meatsci.2015.05.013 cercano (NIRS) para predicción de parámetros nutritivos en forrajes tropicales. Gusha, J., Halimani, T. E., Ngongoni, N. T., Masocha, M., Katsande, S., and Trop. Grassl. 4:139. doi: 10.17138/TGFT(4)139-145 Mugabe, P. H. (2019). Effect of growth stage and method of conservation of Morales-Vallecilla, F., and Ortiz-Grisales, S. (2018). Productivity and efficiency of H. filipendula and H. dissoluta on nutrient composition and digestibility. Trop. specialized dairy farms in the Valley of Cauca (Colombia). Rev. de la Facultad Subtrop. Agroecosyst. 22, 71–77. Available online at: https://www.revista.ccba. de Med. Vet. y de Zootec. 65, 252–268. doi: 10.15446/rfmvz.v65n3.76463 uady.mx/ojs/index.php/TSA/article/view/2693/1217 Morales-Velasco, S., Vivas-Quila, N. J., and Teran-Gómez, V. F. (2016). Ganadería Hare, M. D., Phengphet, S., Songsiri, T., and Sutin, N. (2015). Effect of eco-eficiente y la adaptación al cambio climático. Biotecnol. en el Sector nitrogen on yield and quality of Panicum maximum cvv. Mombasa and Agropecuario y Agroind. 14, 135–144. doi: 10.18684/BSAA(14)135-144 Tanzania in Northeast Thailand. Trop. Grassl. 3:27. doi: 10.17138/TGFT(3) Mwendia, S. W., Maass, B., Njenga, D., and Notenbaert, A. (2019). Perennial 27-33 ryegrass and novel festulolium forage grasses in the tropical highlands Homen, M., Entrena, I., Arriojas, L., and Ramia, M. (2010). Biomasa y valor of Central Kenya: preliminary assessment. Trop. Grassl. 7, 234–243. nutritivo del pasto Guinea Megathyrsus maximus (Jacq.) BK Simon and S:W:L doi: 10.17138/tgft(7)234-243 Jacobs Gamelote en diferentes periodos del año en la zona de bosque húmedo Parrini, S., Acciaioli, A., Crovetti, A., and Bozzi, R. (2018). Use of FT-NIRS tropical, Barlovento estado Miranda. Zootec. Trop. 28, 255–265. Available for determination of chemical components and nutritional value of natural online at: http://ve.scielo.org/pdf/zt/v28n2/art11.pdf pasture. Ital. J. Anim. Sci. 17, 87–91. doi: 10.1080/1828051X.2017.1345659 ISO 12099:2017. (2017). Animal Feeding Stuffs, Cereals and Milled Cereal Patiño-Pardo, R., Gómez-Salcedo, R., and Navarro-Mejía, O. (2018). Nutritional Products—Guidelines for the Application of Near Infrared Spectrometry. quality of Mombasa and Tanzania (Megathyrsus maximus Jacq.) managed at Available online at: https://www.iso.org/obp/ui/#iso:std:iso:12099:ed-2:v1:en different frequencies and cutting heights in Sucre, Colombia. Rev. CES Med. (accessed December 15, 2019). Vet. y Zootec. 13, 17–30. doi: 10.21615/cesmvz.13.1.2 Jung, H. G., Mertens, D. R., and Payne, A. J. (1997). Correlation of Paul, B. K., Koge, J., Maass, B. L., Notenbaert, A., Peters, M., Groot, J. C. acid detergent lignin and klason lignin with digestibility of forage J., et al. (2020). Tropical forage technologies can deliver multiple benefits Frontiers in Sustainable Food Systems | www.frontiersin.org 1791 October 2021 | Volume 5 | Article 684747 Carvajal-Tapia et al. Guinea Nutritional Assessment in Contrasting Seasons in Sub-Saharan Africa. A meta-analysis. Agron. Sustain. Dev. 40, 1–17. Tilley, J. M., and Terry, R. (1963). A two stage technique for the in vitro doi: 10.1007/s,13593-020-00626-3 digestión of forage crops. (British Gr). Grass Forage Sci. 18, 104–111. R Core Team (2020). R: A Language and Environment for Statistical Computing. doi: 10.1111/j.1365-2494.1963.tb00335.x Vienna: R Foundation for Statistical Computing. Toledo, J., and Schultze-Kraft, R. (1982). “Metodología para la evaluación Ramakrishnan, P., Babu, C., and Iyanar, K. (2014). Genetic diversity in agronómica de pastos tropicales,” in Manual para la evaluación agronómica, Guinea grass (Panicum maximum Jacq.) for fodder yield and quality using Red Internacional de Evaluación de Pastos Tropicales, ed M. Toledo (Cali: morphological markers. Int. J. Plant Biol. Res. 2:1006. Available online at: CIAT), 91–116. https://www.jscimedcentral.com/PlantBiology/plantbiology-2-1006.pdf Valente, B. S. M., Cândido, M. J. D., Junior, J. A. A. C., Pereira, E. S., Bomfim, Rao, I. (2013). “Advances in improving adaptation of common bean andBrachiaria M. A. D., and Feitosa, J. V. (2010). Chemical composition, digestibility and Forage Grasses to abiotic stresses in the tropics,” in Handbook of Plant in situ degradation of sheep diet on Tanzania grass with three defoliation and Crop Physiology, ed P. Mohammad (Boca Raton, FL: CRC), 847–889. frequencies. Rev. Bras. Zootec. 39, 113–120. doi: 10.1590/S1516-35982010000 doi: 10.1201/b16675-49 100015 Rodríguez, M., Amaro, O., Machado-Martínez, H., and Machado-Castro, R. Van Soest, P. (1982). Nutritional Ecology of the Ruminant. Ithaca, NY: Cornell (2017). Megathyrsus maximus. Resultados científicos y potencialidades ante University Press. el cambio climático en el trópico. Av. Investig. Agropecu. 21, 41–61. Available Van Soest, P., Robertson, J., and Lewis, B. (1991). Methods for dietary fiber, neutral online at: http://ww.ucol.mx/revaia/portal/pdf/2017/sept/4.pdf detergent fiber, and non-starch polysaccharides in relation to animal nutrition. Ruiz, F., Rodriguez, E., Pinzón, J., Anzola, H., and Castro, L. (2015). Dairy Sci. 74, 3583–3597. doi: 10.3168/jds.S0022-0302(91)78551-2 Establecimiento y evaluación del guinea Panicum máximum cv Massai en la Vargas Junior, F. M., Socorro, M. M., de Setti, J. C. A., Pinto, G. hacienda Guachicono del Bordo, Patía (Cauca). Rev. Ciencia Anim. 9, 125–154. S., Martins, C. F., et al. (2013). Disponibilidade e valor nutritivo de Santiago-Hernández, F., López-Ortiz, S., Ávila-Reséndiz, C., Jarillo-Rodríguez, J., gramíneas tropicais sob pastejo com ovinos. Arch. Zootec. 62, 295–298. Pérez-Hernández, P., and de Dios Guerrero-Rodríguez, J. (2016). Physiological doi: 10.4321/S0004-05922013000200016 and production responses of four grasses from the genera Urochloa and Velásquez, P. A. T., Berchielli, T. T., Reis, R. A., Rivera, A. R., Dian, P. H. Megathyrsus to shade from Melia azedarach L. Agrofor. Syst. 90, 339–349. M., Teixeira, I. A. M., et al. (2010). Composição química, fracionamento doi: 10.1007/s10457-015-9858-y de carboidratos e proteínas e digestibilidade in vitro de forrageiras Santos, M. E. R., Miranda Da Fonseca, D., Márcio Balbino, E., Pedro tropicais em diferentes idades de corte. Rev. Bras. Zootec. 39, 1206–1213. Da Silva, S., Ismério, J. P., and Monnerat, S. (2010). Valor nutritivo doi: 10.1590/S1516-35982010000600007 de perfilhos e componentes morfológicos em pastos de capim-braquiária Vivas-Quila, N. J., Carrillo, S., Galindez, J., Morales-Velasco, S., Gutierrez-Solis, diferidos e adubados com nitrogênio. Rev. Bras. Zootec. 39, 1919–1927. J. F., and Peters, M. (2015). “Evaluation of the establishment of livestock feed doi: 10.1590/S1516-35982010000900009 association for tropical American system ID310 in Pastoralism and forage SAS (2016). SAS Institute Inc., Version 9.4. Software 9.4 (TS1M5). Cary, NC: SAS. systems,” in Posters 239 (Bonn). Schafer, J., Opgen-Rhein, R., Zuber, V., Ahdesmaki, M., Silva, A. P. D., and Wei, T., and Simko, V. (2017). R Package “corrplot”: Visualization of a Correlation Strimmer, K. (2017). Corpcor: Efficient Estimation of Covariance and (Partial) Matrix (Version 0.84). Available online at: https://github.com/taiyun/corrplot Correlation. R Package Version 1.6.9. Available online at: https://CRAN.R- (accessed September 09, 2021). project.org/package=corpcor (accessed September 09, 2021). Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. New York, NY: Schnellmann, L. P., Verdoljak, J. J. O., Bernardis, A., Martínez-González, J. C., Springer-Verlag. doi: 10.1007/978-3-319-24277-4_9 Castillo-Rodríguez, S. P., and Limas-Martínez, A. G. (2020). Cutting frequency Wilson, J., and Ng, T. (1975). Influence of water stress on parameters associated and height on the quality ofMegathyrsus maximus (cv. Gatton panic). Corpoica with herbage quality of Panicummaximum var. trichoglume. Aust. J. Agric. Res. Cienc. Tecnol. Agropecu. 21:e1402. doi: 10.21930/rcta.vol21_num3_art:1402 26, 127–136. doi: 10.1071/AR9750127 Silva, T. V. S., Sousa, L. F., Santos, A. C., dos, Ferreira, A. C. H., Cardoso, R. R., Sousa, J. T. L., et al. (2017). Nutritional quality of massai grass fertilized Conflict of Interest: The authors declare that the research was conducted in the with phosphorus and nitrogen and its influence on intake and weight gain of absence of any commercial or financial relationships that could be construed as a sheep under rotational grazing on quartzipsamment soil. Semina: Ciênc. Agrár. potential conflict of interest. 38:1427. doi: 10.5433/1679-0359.2017v38n3p1417 Soares Filho, C. V., Cecato, U., Ribeiro, O. L., Roma, C. F., da, C., and Publisher’s Note: All claims expressed in this article are solely those of the authors Beloni, T. (2015). Morphogenesis in pastures with Tanzania grass fertilized and do not necessarily represent those of their affiliated organizations, or those of with nitrogen doses under a grazing system. Acta Sci.-Anim. Sci. 37:235. the publisher, the editors and the reviewers. Any product that may be evaluated in doi: 10.4025/actascianimsci.v37i3.27101 this article, or claim that may be made by its manufacturer, is not guaranteed or Stabile, S., dos, S., Salazar, D. R., Jank, L., Renn, F. P., and Silva, L. F. P. e. (2010). Características de produçao e qualidade nutricional de genoipos de endorsed by the publisher. capim-coloniao colhidos em tres estádios de maturidade. Rev. Bras. Zootec. 39, 1418–1428. doi: 10.1590/S1516-35982010000700004 Copyright © 2021 Carvajal-Tapia, Mazabel and Vivas-Quila. This is an open-access Tavares de Castro, C. R., and Carvalho, M. M. (2000). Florescimento de gramíneas article distributed under the terms of the Creative Commons Attribution License (CC forrageiras cultivadas sob luminosidade reduzida. Cienc. Rural 30, 163–166. BY). The use, distribution or reproduction in other forums is permitted, provided doi: 10.1590/S0103-84782000000100026 the original author(s) and the copyright owner(s) are credited and that the original Tesk, C. R. M., Cavalli, J., Pina, D. S., Pereira, D. H., Pedreira, C. G. S., Jank, L., publication in this journal is cited, in accordance with accepted academic practice. et al. (2020). Herbage responses of Tamani and Quênia guineagrasses to grazing No use, distribution or reproduction is permitted which does not comply with these intensity. Agron. J. 112, 2081–2091. doi: 10.1002/agj2.20189 terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1802 October 2021 | Volume 5 | Article 684747 ORIGINAL RESEARCH published: 11 November 2021 doi: 10.3389/fsufs.2021.758308 Avena sativa AV25-T (Altoandina) Supplementation as Alternative for Colombia’s High-Altitude Dairy Systems: An Economic Analysis Karen Enciso 1, Javier Castillo 2, Luis Orlando Albarracín 2, Luis Fernando Campuzano 2, Mauricio Sotelo 1 and Stefan Burkart 1* 1 The Alliance of Bioversity International and the International Center for Tropical Agriculture (CIAT), Cali, Colombia, 2 The Colombian Agricultural Research Corporation (Agrosavia), Villavicencio, Colombia In the Colombian high-altitude tropics (2,200–3,000m.a.s.l.), Kikuyu grass (Cenchrus clandestinus) is the main feed source for the dairy system. This grass species has good characteristics regarding adaptability and productivity, but is affected by frost, grass bugs (Collaria spp.) and precipitation-related production seasonality. Forage deficits might Edited by: thus be a problem at several times in a year. As a strategy to maintain production Michel A. Wattiaux, University of Wisconsin-Madison, stable, dairy farmers use commercial feed concentrates increasing their production United States costs. Agrosavia, as a response to this, started in 2005 with the evaluation and selection Reviewed by: of new forage species for the Colombian high-altitude tropics. The oat Avena sativa Carlos Gomez, AV25-T was identified as promising alternative to supply the requirements of dry matter National Agrarian University, Peru Carlos Manuel Arriaga-Jordán, in times of deficit and released as cultivar in 2018 under the name Altoandina. The Universidad Autónoma del Estado de objective of this study was to evaluate the economic viability of Altoandina in Colombia’s México, Mexico high-altitude dairy systems. Altoandina (Aa) was provided as silage in two different diets: *Correspondence: Stefan Burkart 35%Aa−65% Kikuyu (Yellow Diet) and 65%Aa-35% Kikuyu (Red Diet). The diet for s.burkart@cgiar.org comparison was traditional grazing with 100% Kikuyu grass (Blue Diet). All diets were supplemented with 6kg commercial feed concentrate, 0.5 kg cotton seeds and 0.5 kg Specialty section: Alfalfa meal per cow/day, respectively. To estimate economic indicators, we used a This article was submitted to Climate-Smart Food Systems, cashflow model and risk assessment under a Monte Carlo simulation model. Including a section of the journal Altoandina incremented productivity per hectare by 82.3 and 220% in the Yellow and Red Frontiers in Sustainable Food Systems Diets, respectively. According to the results of our economic model, the Yellow Diet is the Received: 13 August 2021 Accepted: 21 October 2021 best alternative. Its average Net Present Value (NPV) was superior in >80% and showed Published: 11 November 2021 a lower variability. The indicators Value at Risk (VaR) and probability (NPV < 0) show Citation: the Yellow Diet to have the lowest risk for economic loss under different yield/market Enciso K, Castillo J, Albarracín LO, scenarios. The Yellow Diet also has the lowest unit production costs and uncertainty of Campuzano LF, Sotelo M and Burkart S (2021) Avena sativa AV25-T productive parameters. According to our findings, supplementation with Altoandina at (Altoandina) Supplementation as 35%, i.e., during critical times, has high potential to improve efficiency and profitability. Alternative for Colombia’s High-Altitude Dairy Systems: An This information is key for the decision-making process of dairy farmers on whether to Economic Analysis. adopt this technology. Front. Sustain. Food Syst. 5:758308. doi: 10.3389/fsufs.2021.758308 Keywords: sustainability, Monte Carlo simulation, silage, oat, dairy system Frontiers in Sustainable Food Systems | www.frontiersin.org 811 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems INTRODUCTION decreases of on average 4.9% in years with presence of the El Niño phenomenon [UNGRD (Unidad Nacional para la Gestión The livestock sector and, particularly the cattle subsector, is del Riesgo de Desastres-Colombia), 2016]. a critical component of food systems since it provides food In the specialized dairy systems of Colombia, the predominant with high quality protein (i.e., 14% of the calorie and 33% feed base is grazing of Kikuyu grass (Cenchrus clandestinus) of the protein intake of the global human diet comes from and the use of supplementation with commercial concentrates, livestock) that is in most cases produced on marginal lands not the latter representing a significant percentage of the total suitable for crop production. Additionally, livestock provides production costs (∼37%) (Cárdenas, 2003; Campuzano et al., people with incomes, assets, alternative energy, animal draft 2018; Castillo et al., 2019). Kikuyu grass, although with good power, and livelihoods (FAO, 2018). Especially, dairy production characteristics in terms of adaptability and productivity (biomass is crucial for income generation and food security, mainly in production), is affected by frost and grass bugs (Collaria scenica) (the rural areas of) developing countries where the dairy sector (Campuzano et al., 2018). It also has nutritional limitations is dominated by smallholder production systems (World Bank, that can affect the production and compositional quality of 2005; Reisinger and Clark, 2018). Globally, there are around milk, such as high levels of soluble nitrogen and low levels of 300 million poor people whose livelihoods depend on the daily non-structural carbohydrates (Correa et al., 2008). In addition, income and nutrition provided through milk production (World the production systems based on Kikuyu are associated with Bank, 2005). The dairy sector is of great economic and social deficient pasture management, mainly in terms of fertilization importance in Colombia. It contributes with 36.7% to the (Campuzano et al., 2018), and residual grass management, national livestock and 12% to the agricultural Gross Domestic restricting both levels of production and productivity. This Product (GDP), respectively, and generates 20% of the jobs in the leads to impacts at the environmental level, since soil and agricultural sector (MADR, 2020). According to the Colombian water are being contaminated with nitrogen (N) that is not Cattle Federation (FEDEGAN, 2018), there are about 319,000 usable by the animal and released with the urine (given the milk-producing families in Colombia, and the dairy sector is levels of soluble N in Kikuyu, the inadequate management of predominated by small-scale or subsistence producers (with grazing and low levels of supplementation) (J. Castillo, Agrosavia, less than 10 animals). Milk production in the country happens personal communication). under two differentiated systems linked to specific environmental Consequently, there are important bottlenecks related to the conditions. First, the specialized dairy systems, located in the deficit of forage at different times of the year, high production higher tropics (>2,000m.a.s.l.), mainly in the departments of costs of animal feed and negative effects at the environmental Antioquia, Boyacá, Cundinamarca, and Nariño, which provide level. Considering the climate change scenarios for the region, 45% of the total national milk supply and use only 6% of the this situation is likely to worsen: The Colombian Institute of total cattle inventory (1.72 million heads) (Carulla and Ortega, Hydrology, Meteorology and Environmental Studies (IDEAM) 2016; FEDEGAN, 2020b). Second, the dual-purpose production forecasts for the Departments of Cundinamarca, Boyacá, and systems, located in the lower tropics (<1,200m.a.s.l.), which Antioquia (which make up 40% of the national dairy production contribute with 55% of the national milk supply using 39% of mainly under specialized dairy systems) increases in precipitation the total cattle inventory (10.08million heads) (FEDEGAN, 2018, levels of more than 4% and in temperature of at least 2◦C until the 2020a). year 2100 (IDEAM, 2015). This would lead to a lower water use The dairy sector has had high growth rates in the last two efficiency and possibly greater water stress for the Kikuyu grass decades, with an increase in total milk supply of 35% between (Vargas-Martínez et al., 2018) and largely affect dairy production 2000 and 2019, which is equivalent to a production of 5,295 in those regions. and 7,257ml, respectively (FEDEGAN, 2020b). Production and In this sense, the Colombian Agricultural Research productivity, however, are strongly linked to the local climatic Corporation (ICA and CORPOICA before, now Agrosavia) conditions present in the production areas (FEDEGAN, 2018), has conducted forage research to improve the efficiency and making the dairy sector dependent on rainfall regimes and reduce the seasonality of milk production in the higher tropics periods of drought that affect the availability and quality of of Colombia. These studies have focused on seeking strategies the forages used as animal feed (FEDEGAN, 2018). Because for soil recovery and renovation of pastures, establishment of climate change, this situation has been aggravating in and management of forage grazing systems, and production of recent years, given the progressive increase in global and local forage crops for ruminant feeding systems (Castillo et al., 2019). average temperatures and variations in rainfall patterns. This is Although there is no germplasm improvement and evaluation directly affecting cattle production through impacts on pasture program specifically for the higher tropics, the research processes availability, animal comfort (heat stress), water availability and carried out by Agrosavia have led to the release of six oat cultivars biodiversity (Rojas-Downing et al., 2017). In addition to the in the country since the 1960s: ICA Bacatá (Avena fauta) (1963), above, the increasingly frequent occurrence of extreme climatic ICA Soracá (Avena byzantina) (1965), ICA Gualcalá (Avena phenomena in the country, such as La Niña and El Niño, byzantina) (1968), ICA Cajicá (Avena sativa) (1976), Avena causing heavy rainfall, flooding, and extreme droughts, makes the Obonuco Avenar (Avena sativa) (2003) and Avena Altoandina situation even more critical, particularly when it comes to milk (AV25; High-Andean Oat) (2018) (Bustamante, 1965; Arias production, since dairy cows are more susceptible to heat stress et al., 1972; Bolaños-Alomía et al., 2003; Campuzano et al., (SIPSA/DANE, 2016). This is evidenced by milk production 2018). Despite its release over 45 years ago and the release of Frontiers in Sustainable Food Systems | www.frontiersin.org 822 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems other cultivars thereafter, ICA Cajicá still predominates on the Diet) and 65%Aa−35% Kikuyu (Red Diet). The diet for market and is one of the most used oats for animal feeding comparison was traditional grazing with 100% Kikuyu grass (through silage). It is, however, susceptible to rust (Puccinia (Blue Diet). Through a discounted cash flow model and a spp.) which is predominant in many parts of the Colombian quantitative risk analysis using a Monte Carlo simulation, we higher tropics. The cultivar Altoandina, released in 2018, is the provide economic indicators, such as Net Present Value (NPV), most recent oat made available to dairy producers, and is the Internal Rate of Return (IRR), and Benefit-Cost Ratio (B/C), result of an evaluation process which began in 2005. Compared that help in identifying the best diet for the system under to the previously released materials and commercial oats used evaluation. This document is structured as follows: after this in the region, Altoandina stands out for its higher biomass introduction, the main characteristics of the evaluated variety production, better nutritional quality, and greater resistance to are presented [Section Description of the technology: Avena rust and overturning (Campuzano et al., 2018, 2020), making AV25-T (Altoandina)]. The methodology, assumptions, and data it a promising alternative for supplying the forage deficit of sources used are explained in Section Materials and Methods, the the prairies in times of scarcity (drought) and improving the results are provided in Section Results and discussed in Section productivity of the specialized dairy systems in the Colombian Discussion, and conclusions and recommendations for various higher tropics. In general terms, oats stand out as a forage crop stakeholders are presented in Section Conclusion. widely used as a source of animal nutrition throughout the world, especially in European countries and the United States (Fraser and McCartney, 2004; Suttie and Reynolds, 2004; Harper DESCRIPTION OF THE TECHNOLOGY: et al., 2017). Avena sativa is predominant there and used either in AVENA AV25-T (ALTOANDINA) grazing systems or as supplement in the form of hay and silage. In South America, a harvested area of 806,000 hectares was In 1992, the oat accession with the experimental name AV25 registered for 2019, with an average annual growth rate of 8% was introduced to the National Germplasm Bank System between 2010 and 2019 (FAOSTAT, 2021), indicating the interest for Food and Agriculture of Colombia (SBGNAA) managed of dairy producers in this material. In Colombia, oats are mainly by Corpoica (now Agrosavia). The accession was delivered used as basis for silage production in the higher tropics, but, to a by the International Maize and Wheat Improvement Center limited extent also for grazing in the lower to medium tropics. (CIMMYT) from Mexico. The evaluation process of this Using oats has been gaining importance in cattle production, accession began in 2005 with the aim of offering forage especially in the technified dairy systems in the higher tropics, alternatives for the cattle systems in the Colombian higher but adoption rates remain low on farms with less technical level tropics. In total, 18 oat genotypes from New Zealand, CIMMYT, (FEDEGAN, 2012). SBGNAA and commercial national varieties were evaluated. The technical evaluation of oats in Colombia is being led The AV25 genotypes were selected for presenting high Dry by Agrosavia, which has focused on evaluating the effects of Matter yields, tolerance to overturn and resistance to leaf using it as a supplementation strategy in critical times (through and stem rust (Campuzano et al., 2020). From 2016 to 2017, silage) on the production and composition of milk in the higher agronomic evaluations were carried out in eight locations in tropics (Barahona et al., 2003; León et al., 2008; Mojica et al., the Colombian Andean region, selecting the cultivar AV25-T 2009; Campuzano et al., 2018, 2020). Although variable effects (Altoandina) as most promising material for covering the feed on production have been reported, most of these studies have requirements of the high-altitude dairy systems during critical shown how the use of oats allows maintaining milk production times (Campuzano et al., 2018), particularly for milk production stable when compared to feeding strategies solely based on in the subregions of the savannas of Bogotá, upper Chicamocha, Kikuyu grass (León et al., 2008; Mojica et al., 2009; Campuzano the Ubaté and Chiquinquirá valleys, and the highlands of the et al., 2018, 2020). Studies on the economic viability of including Nariño Department (Campuzano et al., 2018). oat varieties in cattle systems were, however, not conducted Altoandina is a forage oat with a semi-erect growth habit with yet for Colombia. Even though oats (due to their beneficial an average height of 108–143 cm and an average density of 27 characteristics such as higher biomass availability, maintenance leaves per plant. It adapts well to altitudes between 2,600 and of production levels in critical times, and reduction in the use 3,000m.a.s.l. and to soils with a moderately acidic to neutral of commercial concentrates) have positive impacts on economic PH value. Compared to other commercial oats (e.g., Cayuse), viability and economic indicators, it is also evident that the Altoandina has a shorter flowering time (92–107 days compared implementation of feeding strategies based on oats imply higher to 110-150), being considered an intermediate cycle oat. The costs at the productive level compared to grazing systems, average harvest period until a state of milky to pasty grains making it necessary to provide information on the profitability [7.9 points on the Zadoks growth scale (Zadoks et al., 1974)] is of these technologies in order to facilitate dissemination and reached, varies between 130 to 140 days. It is characterized by adoption processes. high biomass production (up to 64.9 t ha−1 of green forage and In this sense, the present study aims to evaluate, from an up to 25 t ha−1 of Dry Matter, depending on the management economic perspective, the viability of the oat Avena AV25- and environmental conditions), resistance to overturning (5.2% T (Altoandina) as a feeding strategy for dairy systems in compared to 30% for commercial varieties), low incidence of the Colombian higher tropics. Altoandina (Aa) was provided leaf and stem rust (Puccinia spp.) (<20% compared to 60% for as silage in two different diets: 35%Aa−65% Kikuyu (Yellow commercial varieties), and higher crude protein values in the Frontiers in Sustainable Food Systems | www.frontiersin.org 833 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems TABLE 1 | Forage production and nutritional quality of Altoandina and commercial TABLE 2 | Composition of the evaluated diets. oat varieties. Category Composition Evaluated diets Variable Altoandina Commercial varieties (Mean ± SD)* (Mean ± SD)* Blue Yellow Red Biomass production (t DM−1** ha−1) 10.6-24.8 3.6-19.3 Forage composition Kikuyu grass 100% 65% 35% Crude protein (%) 7.5 ± 1.4 4.7 ± 1.27 (%) Altoandina silage 0% 35% 65% Neutral Detergent Fiber (NDF, %) 57 ± 3.15 58 ± 3.16 Supplements Feed concentrate 6.0 6.0 6.0 (kg AU−1* −1 Total digestible nutrients (TDN, %) 51 ± 3.15 50 ± 3.24 d ) Standard 70 (kg/DM) Cotton seeds (kg/DM) 0.5 0.5 0.5 *Mean values and standard deviations reported for a total of 6 evaluations: two each in Alfalfa flour (kg/DM) 0.5 0.5 0.5 the Nariño, Boyacá, and Cundinamarca Departments; **DM, Dry Matter. Source: Own elaboration based on the study carried out by AGROSAVIA “Evaluación y Consumption Kikuyu grass 57.5 33.4 16.7 selección de nuevas especies forrajeras, and estrategias para mejorar la competitividad (kg AU−1 −1 d ) Altoandina silage 0.0 12.0 25.9 y sostenibilidad de los sistemas de producción de leche y/o carne en la región andina” Supplements 7.0 7.0 7.0 (Campuzano et al., 2018, 2020; LF. Campuzano, Agrosavia, personal communication). The technical parameters obtained by Campuzano et al., were used for the economic *AU, Animal Unit. One Animal Unit is equivalent to an adult cow of 450 kg live weight. evaluation presented in this article. The experiment was carried out between July and August 2007, milky to pasty grain state, where starch levels are at their highest during the dry season of the second semester of the year. The point and improve the nutritional quality of the forage (59% average temperature there is 13◦C with fluctuations between 0 higher than for the commercial varieties Cayuse and Cajicá) and 20◦C and a relative humidity of 80 to 85%. Frosts occur in (Campuzano et al., 2018). A summary of the characteristics the area in the months of January, February and early August, of Altoandina is provided in Table 1. Altoandina was released the average annual rainfall is 528.9mm. Altoandina was sown by Agrosavia in 2018 and is commercially available to cattle in an area of 5,500 m2, on soils with moderate to strong acidity producers since then. (PH 5.9), medium percentages of organic matter, medium levels In the present study, Altoandina was evaluated as silage for of Phosphorus (P) and Sulfur (S), and a low level of Boron (B). supplementation in times of feed scarcity in the higher tropics The oat harvest for silage production was carried out 119 days of Colombia. The evaluation considered two different silage after sowing when 70% of the crop was in the state of milky to supplementation percentages of the total diet: 35% (Yellow Diet) pasty grains, with an approximate Dry Matter production of 20 t and 65% (RedDiet) of Altoandina silage. This was compared with ha−1. Animal productivity was evaluated in 15 Holstein cows in a traditional grazing scenario with 100%Kikuyu grass (Blue Diet) a specialized dairy system under conditions of the higher tropics (see Table 2). Prior to the entry of the animals to the systems, the (2,200–3,000m.a.s.l.). The animal productivity evaluations were chemical composition of the Kikuyu grass and the Altoandina performed in a crossover design with three treatments, where the silage were measured. In the case of the Altoandina silage, the experimental unit consisted of five Holstein cows in the first third levels of Crude Protein were 8.7%, Neutral Detergent Fiber of the lactation period. Each treatment involved three groups 51.5%, and Total Digestible Nutrients 52.6%, respectively. For the each of five cows who had between three and five calvings in Kikuyu grass, the levels of Crude Protein were 17.8%, Neutral the past. The silage supply was offered individually in the pasture Detergent Fiber 58.1%, and Total Digestible Nutrients 24.7%, with portable feeders, dividing the daily amount of silage into two respectively (J. Castillo, Agrosavia, personal communication). fractions supplied after eachmilking process. The total evaluation The composition of the diet presented in Table 2 refers to the period was 21 days, with daily milk yield measurements in seven- percentages available and supplied to the animals. The actual day blocks. To determine grazing area in each diet, the total consumption of the animals, might differ since animals were available forage was calculated, and to determine the dry matter offered voluntary feed intake. To ensure that each cow ate the intake, the weight of the cows was measured. The measurements planned amount, the silage was supplied individually, and the of forage availability were made before and after grazing to silage surplus was weighed daily. The residual silage did not determine the consumption of Kikuyu grass. For the Blue Diet reach higher levels than 3.9 and 3.6% for the two evaluated diets (100% Kikuyu grass), forage was provided to the animals through (65 and 35% of Altoandina silage) (A. Albarracín, Agrosavia, grazing on a daily plot size of 241 m2 and the total area used personal communication). was 4824 m2. For the Yellow (35% Altoandina silage) and Red In the three diets, additional supplementation was carried (65% Altoandina silage) Diets, Kikuyu forage was provided to the out with Standard 70 feed concentrate, cotton seed and Alfalfa animals through grazing on a daily plot size of 140.1 and 69.9 m2, flour, at an amount of 6, 0.5, and 0.5 kg AU−1 d−1, respectively. and the total area used was 2802 and 1398 m2, respectively. These amounts are assumed as constant throughout the year and are identical for the three evaluated diets. The productivity MATERIALS AND METHODS data for Altoandina were obtained from field evaluations carried out by Agrosavia in 2008 in the municipality of Tibasosa in Discounted Cash Flow Model the Boyacá Department in Colombia (5◦44′53′′ north latitude A cost-benefit analysis (CBA) was carried out to determine and 72◦59′56′′ west longitude, at an altitude of 2,528m.a.s.l.). the viability of the different interventions with Altoandina Frontiers in Sustainable Food Systems | www.frontiersin.org 844 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems as a supplementation strategy in critical times. The CBA is 2025), according to the productive lifespan of the Holstein cows based on a discounted free cash flow model and a quantitative used in the specialized dairy system in the Colombian higher risk analysis. The analysis was carried out by comparing the tropics (M. Sotelo, Alliance of Bioversity International and CIAT, profitability indicators of the technology in different diets (Red personal communication). Diet and Yellow Diet) and the traditional scenario (Blue Diet) for the study region. For each case, the economic costs and Discount Rate benefits were determined. Regarding the cost categories, the The financing cost is chosen as the discount rate in accordance following have been considered (per hectare): total costs of with the rural credit lines of the Colombian Fund for the establishment and maintenance, opportunity costs of capital, Financing of the Agricultural Sector (FINAGRO). This financing and operating costs (e.g., for animal health, supplementation, cost is considered the opportunity cost of capital and is associated permanent and occasional labor). The benefits are derived from with a risk factor present in the activities of the rural sector. the production of milk in a specialized dairy system, according Therefore, the following discount rate was established: Fixed- to the animal response indicators obtained for each diet. The term deposit rate (DTF) + 5% effective annual interest rate. estimated profitability indicators include the total production The projection of the discount rate in the corresponding periods costs, the gross income, the net profit, the profit margin per liter was carried out following the DTF projections, according to of milk, and financial indicators such as the Net Present Value the Annual Report of Economic Projections Colombia 2020 (NPV) and the Internal Rate of Return (IRR). (Bancolombia, 2020). Model Assumptions Permanent Labor For the construction of the cash flow, it was necessary to establish The need for permanent labor was established according to different economic and technical assumptions, which are in detail the labor weights of FEDEGAN (2003), referring to a need of described below. 7.8 permanent workers for every 100 animals in specialized dairy systems. The 2019 basic salary, transportation assistance, Technical Parameters of Dairy Production social security contributions, social and parafiscal benefits were Since animal productivity was only measured in terms of milk considered for establishing the cost of one permanent farm production per day, the other technical parameters are the same worker, which is US$ 422 per month. For the projection of wages for the three diets according to the average indicators for the during the period of analysis, the universal rule was assumed: study area: (i) a milk production period of 305 days; (ii) a calving Variation of the minimum salary (in %) = expected inflation (in interval of 401–450 days; and (iii) a productive lifespan of dairy %)+ observed variation of workforce productivity (WP, in %). A cattle of 6 years. The purchase price of dairy cattle (US$ 812 WP of 1% is assumed, according to historical estimates derived AU−1) was amortized for the period of analysis and the price for from the National Administrative Department of Statistics of culled cows was adjusted for inflation at 6 years and added in the Colombia (DANE, 2020a). last year (US$ 406 AU−1). Taxes Sowing Frequency of Altoandina Income tax was considered as dictated by law 2010 of 2019 Altoandina is sown twice a year—in March/April and (Congress of the Republic, 2020). Here a rate of 32% was October/November. Oat silage is prepared and offered to established for 2020, 31% for 2021 and 30% for 2022, remaining the animals in periods of frost or drought to cover the supply of fixed at the latter value for the subsequent years. forage required in the diet—usually from December to February and July to September. In other words, oat supplementation Currency at Current Prices is assumed for a total of 180 days per year for the Red and Inflation was considered to estimate income flows and costs Yellow Diets. It is necessary to emphasize that the planting of in the evaluation period. In the case of income, the projection Altoandina must be linked to a farm development plan to fulfill of the Consumer Price Index (CPI) estimated by Bancolombia this assumption. If the supply of forage is low, two sowings are (2020) for the period 2020–2023 was considered. For production planned, otherwise the producers sow oats, especially between costs, the Producer Price Index (PPI) provided by the National March and April. Administrative Department of Statistics of Colombia (DANE, 2020b) was considered. Pasture Renewal of Kikuyu Grass The renewal is assumed once every 2 years, according to the trend Milk Price in the region (J. Castillo, Agrosavia, personal communication). Price information was obtained from the Milk Price Monitoring This is done to improve the physical and chemical quality of the Unit for Region 1, where specialized dairy production systems soil, as well as to recover the productive capacity and quality of predominant (MADR/USP, 2020). The prices were projected the Kikuyu grass. according to the CPI projections. Additionally, this projection included variations in milk prices, associated with the presence of Evaluation Horizon extreme weather events such as El Niño and La Niña. According The evaluation horizon is established according to the lifespan to Abril et al. (2017), the occurrence of these phenomena caused of the main assets for each diet. In the case of Altoandina, a significant increase in food inflation, particularly when the an evaluation period of 6 years was considered (from 2020 to phenomenon is of a strong category. In Colombia, milk prices Frontiers in Sustainable Food Systems | www.frontiersin.org 855 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems have had variations of more than 7% in the years with the TABLE 3 | Variables simulated in the Monte Carlo model. presence of these events, compared to variations of less than 1% Variable Distribution Most likely Lower Upper in the years without phenomenon (DANE, 2020b,c). value limit limit Quantitative Risk Analysis Milk price (US$ l−1) Triangular 0.31 0.28 0.34 Risk is defined as the possibility that the real return on Milk productivity Blue Diet* Pert 20.48 17.63 23.32 an investment is less than the expected return (Park, 2007). (l AU−1 d−1) Therefore, profitability is associated with the variability of the Milk productivity Yellow Pert 21.67 19.09 24.24 flows of benefits and costs, and these in turn of the randomness of Diet** (l AU−1 d−1) the main variables of the investment project (e.g., yields, market Milk productivity Red Diet*** Pert 19.01 16.85 21.17 prices). Investment projects at the rural level pose a high risk, (l AU−1 d−1) resulting from a dependence on a wide set of variables, in many Fertilizer/corrective costs for Triangular 80 54 303 cases, not controlled by the producer (e.g., climatic factors). In Kikuyu renewal (US$ ha−1) this sense, it is necessary to incorporate risk levels associated Periodicity of the El Niño Discreet n.a. 2 7 phenomenon uniform with the profitability indicators of each of the diets evaluated. Variation of the discount Triangular 0% 1% 2% For this, a Monte Carlo simulation model was carried out. The rate (%) simulation was performed for a total of 5,000 simulations or Variation of the CPI (%) Triangular −0.50 0 0.50 iterations, with a 95% confidence level, with the software package @Risk (Paladise Corporation). The objective of this analysis is to *100% Kikuyu grass, **35% Altoandina silage and 65% Kikuyu grass, ***65% Altoandina silage and 35% Kikuyu grass. determine the standard deviation mean values of the profitability indicators through the variable parameters: price per liter of milk, milk production per day in each of the diets, fertilization costs, variation in the discount rate and in the CPI indicator. These r∗ = Internal Rate of Return variables are assigned a probability distribution according to t= Evaluation horizon of the project their empirical behavior, literature or based on expert interviews. The NPV at risk indicator (VaR) and the probability of success The yields were modeled according to expert knowledge and of the evaluated diets [Prob (NPV (Medium)>0] were also the best fit in @Risk following a Pert distribution, where the estimated. The VaR is defined as the maximum expected loss predominance of values in the most probable range was assumed. of the investment project in a time interval and with a certain In the case of costs and price variations, a triangular distribution level of confidence (Manotas and Toro, 2009). Additionally, a was assumed according to the reported minimum and maximum sensitivity analysis was performed using a tornado graph, which values and assigning a greater probability to the extremes. sensitizes each variable in order to measure its impact on the Table 3 shows the simulated variables, the range values, and the profitability indicators and to identify within the critical variables probability distributions used. In the simulation, values of the those with the greatest effects on the profitability indicators. variables identified as critical are randomly assigned, according to their probability distribution functions, to later calculate the determined profitability indicators. RESULTS Decision Criteria Figure 1 shows the information corresponding to the technical As decision criteria, the mean values and the variance of the indicators of animal productivity for each of the evaluated diets. profitability indicators resulting from the simulation are used. These indicators show that the inclusion of Altoandina silage The use of the mean value criterion is based on the law of large in a percentage of 35% (Yellow Diet) allowed to increase the numbers, which states that if many repetitions of an experiment daily milk production per cow by 5.8% and per hectare by 82.3% are carried out, the average result will tend toward the expected compared to the Kikuyu grazing system (Blue Diet). When the value (Park, 2007). The variance of the indicators determines the percentage of silage in the diet increased by 65% (Red Diet), daily degree of spread or dispersion on both sides of the mean value milk production per cow was reduced by 7.7% and per hectare (Park, 2007). In other words, the lower the variance, the lower increased by 220% compared to the Blue Diet. The higher per the variability (loss potential) associated with the indicators. hectare milk production is associated with the higher availability of forage and, therefore, an increase in the animal stocking rate ∑n E(FCt) NPV of 42% and 71% for the Yellow and Red Diets, respectively. In (Mean) = (1) t=0 (1+ r)t addition, the inclusion of Altoandina silage makes it possible to ∑n E(FCt) reduce the rate of milk production decline in critical times and, IRR(Mean) = 2) t=0 (1+ r∗)t = 0 ( in the end, to increase milk production per unit area. It should be noted that, of the evaluated diets, the highest variability in Where, animal production is observed for the Red Diet, measured by E (FCt)= Expected value of the net profit flow for period t the standard deviation indicators and coefficient of variation. It Var (FCt)= Net profit flow variance for period t is important to highlight that, as mentioned in the methodology, r= Real discount rate the data were collected during the dry season of the second Frontiers in Sustainable Food Systems | www.frontiersin.org 866 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems FIGURE 1 | Milk production per three cycles for the diets with Altoandina and the Kikuyu diet (each cycle was a 7-day evaluation, the total evaluation period was 21 days). *100% Kikuyu grass, **35% Altoandina silage and 65% Kikuyu grass, ***65% Altoandina silage and 35% Kikuyu grass. semester and were used to estimate the total annual production TABLE 4 | Overview of principal economic indicators per diet. under each diet. However, given that production levels tend to Economic indicator Blue Diet* Yellow Diet** Red Diet*** be higher in rainy seasons, which is associated with the better forage availability, the data estimations used in this study could Milk production (l ha−1 y−1) 31,544 57,316 101,544 be underestimating production levels for the whole year. In this Gross income from milk sales 11,355 20,631 36,552 sense, better annual milk yields could be expected. (US$ ha−1 y−1) Table 4 presents the summary of the average costs and income Production Costs (US$ ha−1 y−1) 9,695 16,815 34,383 for each of the evaluated diets. The cash flow models include the Net utility (US$ ha−1 y−1) 1,381 2,949 2,646 variable costs and revenues associated with the establishment of Unit Production Cost (US$ l−1) 0.31 0.29 0.34 each technology (Altoandina, Kikuyu). The income results from Milk price (US$ l−1) 0.36 0.36 0.36 the sale of raw milk under a specialized dairy production system, Unit Profit Margin (US$ l−1 ) 0.05 0.07 0.02 according to the technical parameters presented in Figure 1. The Financial Viability indicatorsa average annual milk yields are 31,522, 57,316 and 101,543 L/ha NPV_mean 5,194 11,842 7,853 for the Blue, Yellow and Red Diets, respectively. This results in IRR 40.8% 49.9% 23.5% a gross income for the sale of raw milk of US$ 10,091 for the a Blue, US$ 18,335 for the Yellow, and US$ 32,483 for the Red Diet, NPV and IRR; NPV mean value obtained through Monte Carlo simulation (5,000 repetitions with a 95% confidence level). respectively. Regarding production costs, animal feed and labor *100% Kikuyu grass, **35% Altoandina silage and 65% Kikuyu grass, ***65% Altoandina costs are the most significant items in this production system, silage and 35% Kikuyu grass. making up 52 ± 3% and 23 ± 1% of the total cost of each diet. The costs corresponding to inputs for pastures, animal health, and others add up to the remaining 25%, which results in a amount is assumed constant throughout the year and the same production cost per liter of milk of US $0.31 for the Blue, US$ for the three evaluated diets. The net profit per hectare and year 0.29 for the Yellow, and US$ 0.34 for the Red Diets, respectively. was US$ 1,226, US$ 2,620, andUS$ 2,351 for the Blue, Yellow and The feed cost includes those costs related to supplementation Red Diets, respectively. with Standard 70 concentrate, cotton seed and Alfalfa flour, at an From a purely technical point of view, the Red Diet presents amount of 6 kg, 0.5 kg, and 0.5 kg AU−1 d−1, respectively, adding the highest values for the indicator milk production per hectare. to a total cost of US$ 2.34AU d−1 and US$ 836AU y−1. This When estimating the costs and economic viability indicators, Frontiers in Sustainable Food Systems | www.frontiersin.org 877 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems FIGURE 2 | Probability density of the NPV per evaluated diet. *100% Kikuyu grass, **35% Altoandina silage and 65% Kikuyu grass, ***65% Altoandina silage and 35% Kikuyu grass. however, the Yellow Diet turns out to be the more efficient US$ 27,278, where 10% of the simulated scenarios presented one with lower unit production costs and higher daily milk an NPV<0. productivity per cow. Therefore, a higher profit margin can be For all three evaluated diets, the economic viability indicators obtained per liter of milk produced. The cost of establishing one are highly sensitive to changes in the daily milk production hectare of Altoandina is estimated at US$ 886, which includes the variable, meaning that 70, 62.9, and 60% of the variations in costs required in its establishment and for ensilaging. The green the NPV indicator of the Blue, Yellow and Red Diets can be forage yield is 46,545, the amount silage obtained from that is explained by variations in daily milk production. The second 41,891, and the DM production is 14,155 kg ha−1, respectively. most impactful variable is milk price, which explains on average The cost per kg of DM produced is estimated at US$ 0.06. 30% of the variations in the NPV. The Red Diet is the most The summary of the main financial indicators obtained from sensitive to changes regarding milk price (38.7%), which suggests the Monte Carlo simulation is presented in Table 4. Under that it would pose a greater risk in the face of market conditions the assumptions used for the modeling, all diets result in that cause price reductions (Figure 3). economically viable alternatives (NPV>0). The best indicators are, however, associated the Yellow Diet. Its mean NPV is 128% DISCUSSION and 55% higher than the ones of the Blue and Red Diets, respectively, and a lower dispersion of the indicators is observed The use of Altoandina as a supplementation strategy in times of according to the Coefficient of Variation (29%, compared food scarcity proved to be a viable alternative at both the technical to 41% and 76% for the Blue and Red Diets, respectively). and economic levels in specializedmilk production systems in the Regarding the probability of not obtaining financial feasibility Colombian higher tropics. The higher availability of feed in the of the three diets, the results of the probability distribution evaluated diets based on Altoandina silage allow to increase milk of the NPV are presented in Figure 2. Here, the amplitude of production per hectare substantially (82 and 220% for the Yellow the variation for the NPV indicator can be observed with a and Red Diets). The daily milk production is, however, 7.7% confidence level of 95%. For the Blue Diet, the indicator can lower for the Red Diet (which has the highest share of Altoandina take negative values close to US$ 990 and positive values close silage with 65%) than for the Blue Diet (control scenario, 100% to US$ 11,554, with a probability of economic loss of less than Kikuyu), which is associated with the lower nutritional quality 1%. For the Yellow Diet, the distribution curve shifts to the of the silage compared to the higher quality of Kikuyu grass. right, with a range that varied between US $2,075 and US$ According to literature, although the effects on milk production 23,050. The curve for the indicator for the Red Diet presents can be highly variable, most studies have reported how the use a more dispersed behavior around the mean value, reaching of oats has allowed to maintain and even improve production minimum values close to -US$ 9,862 and maximum values of in critical times. For example, some studies report that the Frontiers in Sustainable Food Systems | www.frontiersin.org 888 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems FIGURE 3 | Contribution of variables to the NPV variance for the evaluated diets. *100% Kikuyu grass, **35% Altoandina silage and 65% Kikuyu grass, ***65% Altoandina silage and 35% Kikuyu grass. Frontiers in Sustainable Food Systems | www.frontiersin.org 899 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems supplementation with oat silage has allowed increases in the of this feeding strategy to maintain production levels in places production and percentage of milk fat, without detriments to where grazing conditions are limited. Likewise, the use of oat protein and total solids (Campuzano et al., 2018). This increase silage makes it possible to reduce the use of feed concentrates is associated with the greater supply of forage available in diets or expensive by-products for feeding animals—which are mainly that include silage, which balances a diet rich in protein and imported at high prices and are subject to often strong price energy (J. Castillo, Agrosavia, personal communication). Mojica fluctuations. Both are also important attributes observed in our et al. (2009) found a higher milk production in cows fed with study. In addition, Altoandina has tolerance to rust (Puccinia Kikuyu grass with a supply of oat silage (Avena sativa) of 0.7 kg spp.), higher drought tolerance and resistance to frost, which DM per 100 kg of live weight (equivalent to a supplementation make it an option less likely to be affected by specific climatic of 17.5% of the total diet), although this increase in production conditions and pests present in the Colombian higher tropics. was statistically similar to the diets where only Kikuyu grass Altoandina can also be conserved for up to 3e years when was fed. Similarly, León et al. (2008), Harper et al. (2017), proper oat conservation processes are guaranteed (silo, silage), Burbano-Muñoz et al. (2018), and Castro-Rincón et al. (2020) which helps in reducing production seasonality and improving report no significant differences in the DM consumption, milk productive parameters. production and composition for supplementation diets with Given the presence of periods of drought or frost that reduce 10–35% oat silage (Avena sativa). These results show that the the biomass supply in grazing systems in the Colombian high inclusion of oat silage in low percentages of the diet does not tropics, alternatives, such as supplementation with oat silage, affect the nutritional value of forage and, therefore, production that allow to maintain milk production levels stable throughout is maintained. On the contrary, León et al. (2008) and Mojica the year, are of great importance for the dairy sector. Achieving et al. (2009) reported reductions in milk production when up to stable milk production would improve the income level of 1.4 kg DM of oat silage per 100 kg liveweight were incorporated producers, contributing to their livelihoods, but also to food into the diet (33–36% of the total diet). This effect was associated security and a better nutrition in the region. Although there with a possible negative effect on the nutrient balance since is a visible trend toward using feed supplementation strategies DM consumption was similar with respect to the diet based in dairy farms in the high tropics (e.g., hay and silage in only on Kikuyu grass. Barahona et al. (2003), however, reported critical times), this rather applies to the more technified farms. an optimal level of silage utilization for supplementation of up Farms with low to medium technification are more reluctant to 75% of the total diet, with acceptable and profitable levels resulting in low levels of adoption of such supplementation of milk production. In general, these variable results regarding strategies, which is evidenced by less than 5% and 20% of the the effects of oat silage on milk production can be associated producers using hay and silage supplementation, respectively with multiple factors, such as nutritional quality and cutting (FEDEGAN, 2012). Among the main barriers that limit the age of the oat (variation in the amount of nutrients), the type adoption of supplementation strategies are the lack of equipment of silage and its interaction with the grass feed base, lactation to chop the silage (Reiber et al., 2010, 2013; Bernardes and do (differences in nutritional requirements), availability and level of Rêgo, 2014), and the lack of labor (Bernardes and do Rêgo, DM consumption, and level of energy consumption (Bhandari 2014). On the other hand, factors that favor the adoption et al., 2008; León et al., 2008; Mojica et al., 2009; Harper et al., of supplementation strategies are financial and agricultural 2017). resources, continuity and intensity in rural extension, access to At an economic level, the results indicate the Yellow Diet demonstration farms and the participation of key innovators, as the best alternative, yielding an average NPV higher than the lack of alternative feeds for the dry season, the perceived for the other alternatives and a lower variability for said benefits of silage feeding, and the presence of a favorable indicator. Similarly, the risk indicators VaR (Value at Risk at milk market (Reiber et al., 2010, 2013). This highlights the 95% confidence) and Prob (NPV < 0) are more favorable for importance of providing support in the diffusion processes of this diet. These results are associated with greater efficiency these technologies in terms of training and education on the in terms of production costs, which allows for increasing the use of supplementation strategies as well as their technical and profit margin per liter of milk produced. The Yellow Diet with economic benefits. Likewise, facilities for producers to access the 35% Altoandina silage can therefore be considered the best required equipment (e.g., machine rings) can help in technology alternative from an economic point of view under different adoption and diffusion processes. performance scenarios andmarket conditions. Sections 1 and 2 of The inclusion of oat silage in animal diets can also have this article evidenced the lack of economic studies regarding the positive effects at the environmental level, given the reduction implementing of oat supplementation strategies in the Colombia. of greenhouse gas emissions in the specialized dairy systems In fact, the only study we found was conducted in the highlands of the higher tropics. In Colombia, those systems present a of Mexico (Burbano-Muñoz et al., 2018). According to the high level of emissions of both Nitrogen (N) and Phosphorus results, production costs per kilogram of milk increased by 25 (P) (León et al., 2008), which is associated with the levels of and 50% for inclusion levels of Avena sativa cv. Chihuahua conventional fertilization with N used for the maintenance of oat silage of 3 and 6 kg DM per cow and day, respectively. (Kikuyu) pastures (around 400 kg N ha−1 y−1 are used), the Since there were no significant differences in yields or milk high levels of protein consumption (e.g., 17–21% of protein levels composition, the diet with only Kikuyu grass had the highest in Kikuyu), and the consumption of P (through mineralized profit margin. This study, however, highlights the importance salts) not fully used at the ruminal level (León et al., 2008). Frontiers in Sustainable Food Systems | www.frontiersin.org 190 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems Different studies have proposed the use of cereal silages rich use of supplements to lower the excess protein levels that in starches as a strategy to reduce the consumption of N Kikuyu grass could present, according to the productive potential and P, increasing the efficiency in the use of these minerals of the animals and the goals proposed in farm development and, therefore, reducing greenhouse gas emission levels. For plans. In addition, we recommend including the supply of example, León et al. (2008) evaluated the balance of N and supplements, such as Altoandina oat silage, into forage budget P in 18 cows under grazing of Kikuyu grass and compared calculations (feed budget) to estimate the actual supply and the results with a diet based on the inclusion of oat silage demand of feed of the dairy herd, and to assess production (Avena sativa). According to their results, the decrease in nutrient costs for grass and supplements. Finally, it is important to consumption through supplementation with oat silage decreased carry out or publish results of the protein-energy balance in the excretion of N in the urine and reduced the P balance. the Colombian higher tropics, focusing on the efficiency and On the other hand, it increased the excretion of N in feces importance of balancing diets based on forage crops such which is associated with the lower degradability of the silage as oats. compared to Kikuyu grass. The above-described changes were According to the economic evaluation, the Yellow Diet not affecting milk production levels and composition. The turned out to be the best alternative to improve efficiency authors state that the reduction of N in the urine significantly and profitability at the farm level when facing problems of contributes to the reduction of greenhouse gas emissions, since seasonality in dairy production and increasing the income it degrades faster than fecal N. Dhiman and Satter (1997) of producers. The evaluation also shows that implementing observed that the total excretion of N to the environment this diet is less risky than implementing the traditional was reduced from 6 to 15% with diets that contained corn diet based on Kikuyu (Blue Diet) and, considering the risk silage. Ramin et al. (2021) described that a higher inclusion aversive behavior of many dairy farmers, this is a key of oats linearly reduced CH4 emissions from 467 to 445 g aspect to promote diffusion and adoption. Altoandina also d−1, and the intensity of CH4 from 14.7 to 14.0 g per kg shows tolerance to stem rust (Puccinia ssp.) and drought, of milk, without having adverse effects on productivity or as well as resistance to frost, which makes it a valuable energy balances. Other studies have confirmed that reducing option for specific climatic conditions and pests in the the level of protein in the diet (i.e., from 18% to 15%) does Colombian higher tropics that can contribute both to reducing not affect production, but reduces the excretion of N into the the seasonality of production and improving production environment (Wattiaux and Karg, 2004; León et al., 2008). In parameters. Likewise, when there is an excess of protein in summary, including grain silage, such as Altoandina, into the the pasture (as in the case of the 100% Kikuyu grass diet), cattle diet may help to reduce greenhouse gas emissions without supplying oat silage with high starch levels helps balancing affecting productivity levels and thus, has positive effects on the protein:energy ratio and thus, improves the efficiency of the environment when compared with traditional diets based the system. on grazing (of Kikuyu) and feed concentrates. To achieve the The use of supplementation alternatives such as oats maximum benefits in this regard, it is, however, important to contributes to achieving more sustainable food systems, through ensure that the oats are being harvested at the optimum time improving the efficiency of animal feeding. This leads to an (milky-pasty grains) and that the grains are being mixed with increase in the availability of milk for consumption, which is the forage. key to nutrition and food security, and to improvements in the livelihoods of the producers. Commercial seed for growing oats is easily accessible and the establishment of the materials CONCLUSIONS is relatively easy for the producers, making supplementation an attractive alternative to them. The use of Altoandina as The results of this study suggest that supplementation with supplementation thus helps improving the feeding efficiency by Altoandina oat silage is an efficient alternative to meet feed either maintaining the same production levels but reducing the requirements in critical times of milk production in the use of more expensive feeds (e.g., concentrates) or producing Colombian higher tropics. The inclusion of Altoandina silage more milk at lower per unit costs. This stabilizes the income as supplement into the Kikuyu dairy cattle diet in a 35% :65% flow of the dairy producers and, therefore, improves their proportion (Yellow Diet) results in the best per animal milk livelihoods. The increased availability of milk for consumption productivity indicators, whereas in a proportion of 75:25% also contributes to improving food security and the nutrition (Red Diet), daily milk production declines. This is associated of, above all, the rural population. In addition, oats can with the loss of nutritional quality of the forage at a level of also be a nutrient-rich food source for human consumption 75% oat silage supplementation, affecting the nutrient balance and contribute to the nutrition of the producer households. and, therefore, the daily per animal milk productivity. This Likewise, the use of oats as a supplementation strategy also is consistent with other studies, which suggest oat silage contributes to the reduction of N and P emissions to the supplementation as a promising alternative to maintain milk environment, since oats, in their milky to pasty grain state, production levels in times of forage scarcity. Prior to the increase starch levels and balance the protein:energy ratio, and planting forage crops such as oats, it is, however, important thus, contribute to reducing greenhouse gas emissions while to conduct technical and economic evaluations focused on the improving economic efficiency. This makes oat supplementation Frontiers in Sustainable Food Systems | www.frontiersin.org 191 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems a triple win alternative: more efficient production, increased DATA AVAILABILITY STATEMENT livelihoods, reduced emissions. Although the experiments used as a basis for this study were carried out in the Boyacá Department The raw data supporting the conclusions of this article will be of Colombia, it is important to note that they served as an made available by the authors, without undue reservation. important input for technology scaling processes and further evaluations in other high-altitude regions of the country with AUTHOR CONTRIBUTIONS similar specialized dairy systems, such as in the Nariño (Castro- Rincón et al., 2020), Cundinamarca, and Antioquia Departments SB, KE, and JC: conceptualization, methodology, and formal as well as in other areas of the Boyacá Department (J. Castillo, analysis. KE, LA, LC, and SB: writing the original draft and Agrosavia, personal communication). Likewise, the economic review and editing. JC, KE, LA, LC, MS, and SB: resources. SB: results obtained in this study have been key to identifying supervision and funding acquisition and project administration. the percentage of the diet with the best economic viability at All authors contributed to the article and approved the the producer level and helped to define a pathway for scaling submitted version. this technology package in larger areas of the high-altitude tropics of Colombia. In this sense, Agrosavia in 2021 has been FUNDING working on a plan for promoting Altoandina at the regional level, by providing dairy producers with technical recommendations This work was funded by the CGIAR Research Program on and supporting them in increasing the planted areas. It is Livestock and by the Colombian Ministry of Agriculture and recommended, however, to conduct further trials and analyses Rural Development (MADR). The funders had no role in the in other countries with similar conditions (e.g., Ecuador, Peru, design of the study; in the collection, analyses, or interpretation Bolivia) to support technology release and adoption processes of data; in the writing of the manuscript, or in the decision to there, too. publish the results. We also recommend including measurements at the environmental level in future studies on Altoandina, so that the ACKNOWLEDGMENTS technology’s potential for reducing greenhouse gas emissions can be quantified and other potential ecosystem services identified. This work was carried out as part of the CGIAR Research Such measurements should be included in the agronomic Program on Livestock. We thank all donors who globally evaluations, which would then allow for accounting greenhouse support our work through their contributions to the CGIAR gas emission reductions in the economic valuation exercise System. The views expressed in this document may not be and to project them as additional benefits derived from the taken as the official views of these organizations. CGIAR is a dairy system. Likewise, we recommend evaluating the use of global research partnership for a food-secure future. Its science Altoandina as dual-purpose crop, meaning in a mixed grazing- is carried out by 15 Research Centers in close collaboration cutting system, where the animals graze the oat in the stuffing with hundreds of partners across the globe. This work was state, and after that fertilizer is being applied and the oat is conducted as part of the project “Evaluación multilocacional de being harvested for silage production once the grains reach nuevo Germoplasma Forrajero en convenio Agrosavia—CIAT”, the milky-pasty state. This approach could increase system funded by MADR. Additionally, this work was part of the efficiency and land use optimization. In addition, Altoandina projects “Evaluación y selección de nuevas especies forrajeras, and is frost resistant, and intercropping with Kikuyu grass could estrategias para mejorar la competitividad y sostenibilidad de los help mitigating the effects of frost on the production system sistemas de producción de leche y/o carne en la región andina” through improving the total on-farm DM availability. We thus of Agrosavia, funded by MADR, and “Estrategias para mejorar recommend evaluations for determining the intercropping la competitividad y sostenibilidad de los sistemas de producción potential of Altoandina and its effects when it comes to the de leche y/o carne en la Región Andina” of Agrosavia, funded adaptation to climate change. by MADR. REFERENCES Barahona, R., Cuesta, P. A., Baez, F., and León, M. I. (2003). Producción y evaluación del uso de ensilajes en sistemas de producción de lechería especializada Abril, D. S., Melo, L. F., and Parra, D. (2017). “Impactos de los fenómenos de Nariño. Bogotá: Corporación colombiana de investigación agropecuaria climáticos sobre el precio de los alimentos en Colombia,” in El desarrollo (AGROSAVIA); Federación Colombiana de Ganaderos (FEDEGAN). Available equitativo, competitivo y sostenible del sector agropecuario en Colombia, eds. online at: http://hdl.handle.net/20.500.12324/16535 C.G. Cano, A.M. Iregui, M.T. Ramirez, A.M. Tribin (Banco de Desarrollo de Bernardes, T. F., and do Rêgo, A. C. (2014). Study on the practices of silage América Latina), 315–347. Available online at: https://www.banrep.gov.co/es/ production and utilization on Brazilian dairy farms. J. Dairy Sci. 97, 1852–1861. espe80-4 doi: 10.3168/jds.2013-7181 Arias, J., Reyes, R., and Celis, A. (1972). Registro de variedades de avena (Avena sp). Bhandari, S. K., Li, S., Ominski, K. H., Wittenberg, K. M., and Plaizier, J. C. (2008). Bogotá: Instituto Colombiano Agropecuario (ICA). Available online at: http:// Effects of the chop lengths of alfalfa silage and oat silage on feed intake, milk hdl.handle.net/20.500.12324/22645 production, feeding behavior, and rumen fermentation of dairy cows. J. Dairy Bancolombia (2020). Actualización de proyecciones económicas para Colombia— Sci. 91, 1942–1958. doi: 10.3168/jds.2007-0358 segundo trimestre de 2020. Bogotá, Colombia. Available online at: http:// Bolaños-Alomía, A., Arcila-González, B., Apraéz, G., J. E., and Moncayo-Otero, shorturl.at/bfrBY O. (2003). Obonuco Avenar: Nueva variedad mejorada de avena forrajera Frontiers in Sustainable Food Systems | www.frontiersin.org 192 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems para la alimentación de bovinos de los sistemas de producción del Antiplano Fraser, J., and McCartney, D. (2004). “Fodder oats in North America. Chapter III,” de Nariño. Bogotá: Corporación Colombiana de Investigación Agropecuaria in Oats: A World Overview, eds J. Suttie, M. Reynolds, (Rome: FAO), 19–35. (CORPOICA). Available online at: http://hdl.handle.net/20.500.12324/16578 Available online at: http://www.fao.org/docrep/008/y5765e/y5765e07.htm Burbano-Muñoz, V. A., López-González, F., Estrada-Flores, J. G., Sainz- Harper, M. T., Oh, J., Giallongo, F., Lopes, J. C., Roth, G. W., Hristov, A. Sánchez, P. A., and Arriaga-Jordán, C. M. (2018). Oat silage for grazing N. (2017). Using brown midrib-6 dwarf forage sorghum silage and fall- dairy cows in small-scale dairy systems in the highlands of central grown oat silage in lactating dairy cows rations. J. Dairy Sci. 100, 5250–5265. Mexico. Afric. J. Range Forage Sci. 35, 63–70. doi: 10.2989/10220119.2018.14 doi: 10.3168/jds0.2017-12552 73493 IDEAM, PNUD, MADS, DNP Cancillería (2015). Nuevos escenarios de Bustamante, R. E. (1965). ICA-BACATA, una nueva variedad forrajera de avena. cambio climático para Colombia 2011– 2100 Herramientas Científicas Agricultura Tropic. 21, 271–274. para la Toma de Decisiones—Enfoque Nacional—Departamental: Tercera Campuzano, L. F., Castro, E., Castillo, J., Torres, D., Cuesta, P. A., Portillo, P. Comunicación Nacional de Cambio Climático. Bogotá, Colombia: Instituto A., Nieto, D. F., and Yepes, D. B. (2018). Avena Forrajera Alto andina: nueva de Hidrología, Meteorología y Estudios Ambientales de Colombia (IDEAM). variedad de avena forrajera para el trópico alto colombiano. Bogotá, Colombia: Available online at: http://documentacion.ideam.gov.co/openbiblio/bvirtual/ Corporación colombiana de investigación agropecuaria (AGROSAVIA). 022964/documento_nacional_departamental.pdf Campuzano, L. F., Castro, E., Castillo, J., Torres, D., Nieto, D., and Portillo, P. A. León, J. M., Mojica, J. E., Castro, E., Cárdenas, E. A., Pabón, M. L., Carulla, J. (2020). Altoandina: new variety of forage oats for the Andean area in Colombia. E. (2008). “Balance de nitrógeno y fósforo de vacas lecheras en pastoreo con Agronomia Mesoamericana 31, 581–595. doi: 10.15517/AM.V31I3.38999 diferentes ofertas de Kikuyu (Pennisetum clandestinum) suplementadas con Cárdenas, E. A. (2003). Estrategias de la Investigación en forrajes en tierra fría ensilaje de avena (Avena sativa),” in Revista Colombiana de Ciencias Pecuarias, en Colombia y avances en la Universidad Nacional de Colombia-Bogotá. 21:559-570. Available online at: https://revistas.udea.edu.co/index.php/rccp/ Revista de la Facultad de Medicina Veterinaria y de Zootecnia 50, 20–24. article/view/324328/20781501 doi: 10.15446/rfmvz MADR (2020). Sector lácteo Abril de 2020. Bogotá, Colombia. Available Carulla, J. E., and Ortega, E. (2016). Dairy production systems of Colombia: online at: https://sioc.minagricultura.gov.co/SICLA/Documentos/2020-06-30 challenges and opportunities. Archivos Latinoamericanos de Producción Anim. %20Cifras%20Sectoriales.pdf, 24, 83–87. MADR/USP. (2020). Precio pagado al productor Res 0017 de 2002. Bogotá, Castillo, J., Benavides, J., Vargas, J., Avellaneda, Y., and García, G. (2019). Applied Colombia. Available online at: http://uspleche.minagricultura.gov.co/ research on dairy cattle feeding systems in Colombian high tropics. Revista de Manotas, D. F., and Toro, H. H. (2009). “Análisis de decisiones de Ciencias Agrícolas. 36, 108–122. doi: 10.22267/rcia.193602.122 inversión utilizando el criterio valor presente neto en riesgo (VPN en Castro-Rincón, E., Cardona-Iglesias, J. L., Hernández-Oviedo, F., and Valenzuela- riesgo),” in Revista Facultad de Ingeniería Universidad de Antioquia, Chiran, M. (2020). Efecto del ensilaje de Avena sativa L. en la productividad de 199–213. Available online at: http://www.scielo.org.co/scielo.php?script=sci_ vacas lactantes en pastoreo. Pastos y Forrajes, 43. 150–158. Available online at: arttextandpid=S0120--62302009000300020 https://www.redalyc.org/journal/2691/269164290009/html/ (accessed October Mojica, J. E., Castro, E., León, J. M., Cárdenas, E. A., Pabón, M. L., Carulla, J. 27, 2021). E. (2009). Efecto de la oferta de pasto Kikuyu y ensilaje de avena sobre la Correa, H. J., Pabon, R., and Carulla, E. (2008). Nutritional value of kikuyu grass producción y calidad composicional de la leche bovina. Ciencia and Tecnología (Pennisetum clandestinumHoechst Ex Chiov.) formilk production in Colombia: Agropecuaria10, 81–90. doi: 10.21930/rcta.vol10_num1_art:132 a review. I. Chemical composition, ruminal and posruminal digestibility. Park, C. S. (2007). Contemporary Engineering Economics (4th ed). Prentice Hall, Livestock Res. Rural Develop. 20:2008. Available online at: http://www.lrrd.org/ Upper Saddle River, N.J. lrrd20/4/corra20059.htm (accessed October 27, 2021). Ramin, M., Fant, P., Huhtanen, P. (2021). The effects of gradual replacement DANE (2020a). Productividad Total de los Factores (PTF). Bogotá, Colombia. of barley with oats on enteric methane emissions, rumen fermentation, milk Available online at: https://www.dane.gov.co/index.php/estadisticas-por-tema/ production, and energy utilization in dairy cows. J. Dairy Sci. 104, 5617–5630. cuentas-nacionales/productividad doi: 10.3168/jds.2020-19644 DANE (2020b). Índice de precios al Productor (IPP). Bogotá, Colombia. Available Reiber, C., Schultze-Kraft, R., Peters, M., and Hoffmann, V. (2013). Lessons online at: https://www.dane.gov.co/index.php/estadisticas-por-tema/precios- from silage adoption studies in Honduras. Tropic. Grassland. 1,235–239. y-costos/indice-de-precios-del-productor-ipp doi: 10.17138/TGFT(1)235-239 DANE (2020c). Índice de precios al consumidor (IPC). Bogotá, Colombia. Available Reiber, C., Shultze-Kraft, R., Peters,; M., Lentes,; P., Hoffmann, V. (2010). online at: https://www.dane.gov.co/index.php/estadisticas-por-tema/precios- Promotion and adoption of silage technologies in drought constrained areas y-costos/indice-de-precios-al-consumidor-ipc/ipc-historico of Honduras. Tropic. Grasslands. 44m 231–245. doi: 10.10568/43976 Dhiman, T. R., and Satter, L. D. (1997). Yield response of dairy cows fed different Reisinger, A; Clark, H. (2018). How much do direct livestock emissions proportions of alfalfa silage and corn silage. J. Dairy Sci. 80, 2069–2082. actually contribute to global warming? Glob. Chang. Biol. 24, 1749–1761. doi: 10.3168/jds.S0022-0302(97)76152-6 doi: 10.1111/gcb.13975 FAO (2018). World Livestock: Transforming the livestock sector through the Rojas-Downing, M., Pouyan, A., Harrigan, T., Woznicki, S. A. (2017). Climate Sustainable Development Goals. Rome, Italy. 222. change and livestock: impacts, adaptation, and mitigation. Climate Risk FAOSTAT (2021). FAOSTAT Cultivos. Rome, Italy. Available online at: http://www. Manage. 16, 145–163. doi: 10.1016/j.crm,0.2017.02.001 fao.org/faostat/es/?#data/QC SIPSA/DANE. (2016). Boletín mensual insumos y factores asociados a la producción FEDEGAN (2003). “Índice de costos ganaderos diciembre 2002—marzo 2003,” in agropecuaria: Efectos del clima en la producción de la ganadería de leche. Bogotá, Carta Fedegán Magazine No. 79. Bogotá, Colombia: Federación Colombiana de Colombia. Available online at: https://www.dane.gov.co/files/investigaciones/ Ganaderos, 17–32. agropecuario/sipsa/Bol_Insumos_mar_2016.pdf FEDEGAN (2012). “Alimentación, elemento clave en la cría,” in Carta Suttie, J. M., and Reynolds, S. G. (2004). Fodder oats: A world overview. Rome, Fedegán Magazine No. 129. Bogotá, Colombia: Federación Colombiana de Italy: Food and Agriculture Organization of the United Nations (FAO). Available Ganaderos, 74–80. online at: http://www.fao.org/3/y5765e/y5765e00.htm FEDEGAN (2018). Ganadería Colombiana Hoja De Ruta 2018-−2022. Bogotá, UNGRD (Unidad Nacional para la Gestión del Riesgo de Desastres-Colombia) Colombia. Available online at: https://www.fedegan.org.co/noticias/ganaderia- (2016). Fenómeno El Niño Análisis Comparativo 1997-1998//2014-2016. Bogotá, colombiana-hoja-de-ruta-2018--2022 Colombia. Available online at: http://hdl.handle.net/20.500.11762/20564 FEDEGAN (2020a). Orientación del hato ganadero. Bogotá. Colombia. Available Vargas-Martínez, J. J., Sierra-Alarcón, A. M., Mancipe-Muñoz, E. A., Avellaneda- online at: https://www.fedegan.org.co/estadisticas/inventario-ganadero Avellaneda, Y. (2018). El Kikuyu, una gramínea presente en los sistemas de FEDEGAN (2020b). Producción y acopio de leche en Colombia. Bogotá. Colombia. rumiantes en trópico alto colombiano. CES Medicina Veterinaria y Zootecnia Available online at: https://www.fedegan.org.co/estadisticas/produccion-0 13, 137–156. doi: 10.21615/cesmvz.13.2.4 Frontiers in Sustainable Food Systems | www.frontiersin.org 193 November 2021 | Volume 5 | Article 758308 Enciso et al. Altoandina Supplementation for Dairy Systems Wattiaux, M. A., and Karg, K. L. (2004). Protein level for alfalfa and corn silage- Publisher’s Note: All claims expressed in this article are solely those of the authors based diets. II. Nitrogen balance and manure characteristics. J Dairy Sci. 87, and do not necessarily represent those of their affiliated organizations, or those of 3492–3502. doi: 10.3168/jds.S0022-0302(04)73484-0 the publisher, the editors and the reviewers. Any product that may be evaluated in World Bank. (2005). Agriculture investment sourcebook. Agriculture and Rural this article, or claim that may be made by its manufacturer, is not guaranteed or Development. Washington, DC: World Bank. Available online at: https:// endorsed by the publisher. openknowledge.worldbank.org/handle/10986/7308 Zadoks, J. C., Chang, T. T., Konza,. C. F. (1974). A decimal Copyright © 2021 Enciso, Castillo, Albarracín, Campuzano, Sotelo and Burkart. code for the growth stages of cereals. Weed Res. 14, 415–421. This is an open-access article distributed under the terms of the Creative Commons doi: 10.1111/j.1365-3180.1974.tb01084.x Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited Conflict of Interest: The authors declare that the research was conducted in the and that the original publication in this journal is cited, in accordance with accepted absence of any commercial or financial relationships that could be construed as a academic practice. No use, distribution or reproduction is permitted which does not potential conflict of interest. comply with these terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 194 November 2021 | Volume 5 | Article 758308 PERSPECTIVE published: 11 November 2021 doi: 10.3389/fsufs.2021.724628 Forage-Fed Insects as Food and Feed Source: Opportunities and Constraints of Edible Insects in the Tropics Paula Andrea Espitia Buitrago 1, Luis Miguel Hernández 1, Stefan Burkart 1, Neil Palmer 2 and Juan Andrés Cardoso Arango 1* 1 Alliance Bioversity International and CIAT, Cali, Colombia, 2 Independent Researcher, Cardiff, United Kingdom Farmed insects can provide an alternative protein source for humans, livestock, and fish, while supporting adaptation to climate change, generating income for smallholder farmers, and reducing the negative impacts of conventional food production, especially in the tropics. However, the quantity, nutritional quality and safety of insects greatly relies on their feed intake. Tropical forages (grasses and legumes) can provide a valuable and yet untapped source of feed for several farmed insect species. In this perspective paper, we provide a viewpoint of how tropical forages can support edible insect production. We also Edited by: Ngonidzashe Chirinda, highlight the potential of tropical forage-based diets over those using organic agricultural Mohammed VI Polytechnic or urban by-product substrates, due to their versatility, low cost, and lower risk of University, Morocco microbial and chemical hazards. The main bottlenecks relate to dependence on the small Reviewed by: Abdullahi Ahmed Yusuf, number of farmed insect species, and in public policy and market frameworks regarding University of Pretoria, South Africa the use of edible insects as food, feed and in industrial processes. This perspective Heinrich Hagel, will serve interested stakeholders in identifying urgent issues at the research, ethical, University of Hohenheim, Germany marketing and policy levels that can prevent the emergence of new, insect-based value *Correspondence: Juan Andrés Cardoso Arango chains and business models, and the nutritional, economic and environmental benefits j.a.cardoso@cgiar.org they promise. Specialty section: Keywords: edible insects, food security, sustainable development, business models, entomophagy policies This article was submitted to Climate-Smart Food Systems, a section of the journal INTRODUCTION Frontiers in Sustainable Food Systems Received: 14 June 2021 Rapid population growth, climate change, and environmental degradation have put food security Accepted: 20 October 2021 and nutrition at risk, especially in the global tropics. The need to feeding a growing population Published: 11 November 2021 has resulted in the exploration of new food sources for humans, livestock, and fisheries. In recent Citation: years, insects have been proposed as an alternative food source for humans and livestock. Food Espitia Buitrago PA, Hernández LM, derived from insects is considered more resource efficient (needing less land and water) than Burkart S, Palmer N and Cardoso traditional livestock production systems (Payne et al., 2016). Several studies highlight the benefits Arango JA (2021) Forage-Fed Insects of edible insects for human and animal health. Crickets (Orthoptera), flies (Diptera), and beetles as Food and Feed Source: (Coleoptera) do not differ significantly in their nutritional composition from traditional protein Opportunities and Constraints of Edible Insects in the Tropics. sources such as beef, chicken, and pork (van Huis et al., 2013; Payne et al., 2016; Frigerio et al., Front. Sustain. Food Syst. 5:724628. 2020; Stull, 2021). The use of insects as food for humans or feed for livestock is, however, not a doi: 10.3389/fsufs.2021.724628 new concept. Humans have used insects in their diets throughout history (van Huis et al., 2013). Frontiers in Sustainable Food Systems | www.frontiersin.org 915 November 2021 | Volume 5 | Article 724628 Espitia Buitrago et al. Forage-Fed Insects as Food-Feed Source More recently, insects have been seen as viable and sustainable the existence of around 2,100 edible species (Jongema, 2017). protein sources for livestock (Chia et al., 2019). The increased This can exacerbate problems that exist in other food chains relevance of insects as feed is reflected by a rapid increase (e.g., crops, livestock) (Tisdell, 2001; Fanzo and Mattei, 2010; in the number of patent applications related to insect food Bruford et al., 2015), such as diversity loss from overexploitation processing methods; a growing number of companies offering (Ramos-Elorduy, 2006; Malinga et al., 2020) and the risk of insects for human and animal consumption; and increased biological invasion in non-native regions, as well as create research on edible insects and greater social acceptance of such genetic erosion if no preventive measures are taken. (Müller et al., 2016; Kim et al., 2019). The boom in interest in Insects also constitute a feasible alternative for animal feed, insects as food and feed is tracking attention across the globe such as soybean and fishmeal, which is generally the largest as evidenced by the development of legislative frameworks for expense in livestock production, representing 60–70% of the insect-based products (European Food Safety Authority, 2021); total production costs (Alqaisi et al., 2011; van Huis et al., and projected increases in the global market volume from US$ 2013). As a result, small- and medium-scale farmers need 400 million to between US$700 million and US$1.2 billion by alternatives that are both effective and affordable (Chia et al., 2024 (Dunkel and Payne, 2016). 2019). Several cost factors are involved in insect farming, In this perspective article, we provide a viewpoint of how including facilities (i.e., laboratories and other infrastructure different tropical forage crops available from international gene and resources), labor requirements (e.g., natural oviposition vs. banks and grown on farms can support the current insect artificial larvae infestation in the substrate), lifecycles and diets of farming industry, and how their incorporation in insect diets has insects (Chia et al., 2019). potential for addressing food safety concerns while maintaining the high nutritional quality of insects for human and animal nutrition. The article is structured as follows: section Insect TROPICAL FORAGES AS A FEED Farming as a Food Source in the Tropics provides an overview ALTERNATIVE FOR FARMED INSECTS of insect farming as a feed and food source in the tropics; section Tropical Forages as a Feed Alternative for Farmed Insects focuses For insects to be considered viable as a food for humans or on feeding insects with tropical forages; section Examples of livestock, they must be provided with an adequate diet. Most Successful Projects provides insights into some successful pilot often, small-scale farmed insects are herbivores that rely on projects; and section Toward Responsible Insect Farming in crop residues (Chia et al., 2018; Jansson et al., 2019). Larger- the Tropics sheds light on how to move toward responsible scale insect farming is sometimes based on feeds that are in insect farming in the tropics. Section Concluding Remarks and direct competition with human diets (e.g., maize, soybean, oats, Forward Look provides concluding remarks that help interested wheat; see Table 1), and may contain ingredients with associated stakeholders in developing forage-based insect value chains in environmental impacts (Miglietta et al., 2015). For instance, some the tropics. commercial diets for crickets include grains and fish meal to supply protein requirements, decreasing the sustainability of the entire chain (Lundy and Parrella, 2015; Bawa et al., 2020). Based INSECT FARMING AS A FOOD SOURCE IN on that, we propose that tropical forages can be used as an THE TROPICS additional feed source in insect production. Leakey (2020) projects increasing food insecurity and environmental degradation in the tropics if the business- as-usual scenario continues. As a result, there is an urgent need TABLE 1 | Commonly farmed insects for food and feed. for a paradigm shift where environmental sustainability, dietary Common name Species diversity and productivity have equal value. Insect farming to produce food is a promising intervention. Compared to Industry-scale farmed insects for food and feeda traditional livestock production systems, insect farming uses Crickets Acheta domesticus 50–90% less land per kg of protein produced and 40–80% less Gryllodes sigillatus feed per kg of edible weight; produces 1.2–2.7 kg less greenhouse Gryllus bimaculatus gas emissions per kg of live weight gain; and uses 1,000 L Mealworms Tenebrio molitor less water per kg of live weight gain (Payne et al., 2016). The Zophobas morio tropics, where most insect species occur (Chapman, 2005), are Alphitobius diaperinus very favorable for insect production since the edaphoclimatic Black soldier flies Hermetia illucens conditions assure a steady production throughout the year under House flies Musca domestica constant environmental conditions, and the natural occurrence Wax moths Galleria mellonella of a broad variety of insect species eliminates the need to Locusts Locusta migratoria introduce non-native species that represent a risk of biological Sun beetles Pachnoda marginata peregrina invasion (Jansson et al., 2019; Bang and Courchamp, 2020). Cockroaches Blaptica dubia Currently, most farmed insects at the industrial scale, however, belong to few species (Jansson et al., 2019), 12 in total, despite Source: own elaboration based on aJansson et al. (2019). Frontiers in Sustainable Food Systems | www.frontiersin.org 926 November 2021 | Volume 5 | Article 724628 Espitia Buitrago et al. Forage-Fed Insects as Food-Feed Source Tropical forages refer to planted grasses and legumes that are 2018). An important collection of tropical forage diversity used to feed livestock in the tropics and include species such as is safeguarded in the CGIAR gene banks of the Alliance Megathyrsus maximus (syn. Panicum maximum), Urochloa spp. of Bioversity International and the International Center for (syn. Brachiaria spp.) or Arachis pintoi (see Table 1). Most often, Tropical Agriculture (CIAT) and the International Livestock tropical forages are used in places where other crops cannot Research Institute (ILRI), with over 22,000 accessions of tropical be produced (e.g., on low-fertility and marginal soils). Among forage grasses and legumes from over 75 countries (The Alliance the common features of this group of plants are their relatively of Bioversity International CIAT, 2021). This diversity is a high biomass production and adaptation to continuous clipping, forage resource yet to be explored and used in insect farming. browsing, or grazing from animals, followed by vegetative re- Table 1 provides an overview of commonly farmed insects growth (Capstaff and Miller, 2018). Tropical forages can supply and Table 2 on the forages that could potentially be used enough biomass and serve as a steady supply of vegetative as diet, based on the comparison of the nutritional contents material to feed herbivore and omnivorous insects over one to of commonly used diets and tropical forages. For crickets, several seasons. Tropical forages can also be conserved when Andropogon spp. could potentially replace whole yellow corn there is a production surplus, e.g., as hay or silage with potential flour, mealworms could be fed with Megathyrsus maximus for insect feeding. instead of white wheat, and sun beetle diets could be changed It is possible to enhance the nutritional content of insects from brewer’s yeast to Arachis pintoi, among others. Creative by using tropical forages (Oonincx et al., 2020). Recent studies approaches are needed to identify the best-suited forages and report that the protein content of crickets increases according to mix them in adequate ratios to supply insects with the to the protein supplementation of feed. Feeding for example dry required nutrients, increasing their productivity, and thereby, pumpkin pulp or enriched flaxseed oil increases the vitamin B contributing to the sustainable intensification of animal-source and omega 3 and 6 contents, respectively (Bawa et al., 2020; food production systems. Oonincx et al., 2020). Tropical forages have better nutritional Tropical forages available in the international gene banks, values than e.g., crop residues, and herbivore insects prefer but also on farms, have the potential to become a part of the most often soft (e.g., green leaves from forage crops) over hard diets of farmed herbivorous insects. Forage-based insect diets plant material (e.g., stubble from crop residues) (Caldwell et al., would also contribute to the transition to circular economies 2016). Additionally, insects fed with tropical forages would not for the agricultural sector. Insects produced with such diets compete with food production for human consumption as is can be used for both human consumption and as feed for the case with grain-based insect feeds. In Uganda, the edible poultry, swine, or fish. This would lead to numerous benefits cricket Ruspolia differens (Orthoptera: Tettigoniidae) was found and opportunities, such as the creation of new industries, feeding on 19 grasses, includingMegathyrsus maximus, Urochloa small-scale businesses and jobs, income diversification, more ruziziensis, Chloris gayana, Cynodon dactylon, Setaria sphacelate, balanced human diets, the protection of endangered species and and Pennisetum purpureum, preferring inflorescences or seeds ecosystems (e.g., marine ecosystems or forests), the reduction of over stems or leaves and showing a variability in host plant greenhouse gas emissions, increases in above- and below-ground preference through the different life stages (Opoke et al., 2019). biodiversity and the protection of water resources, and thus Also, diets based on grass inflorescences from different species contribute to achieving some of the Sustainable Development influence maximal weight, survival, shorter development time Goals (UN, 2021), i.e., those related to ending poverty, zero and content of fatty acids of R. differens, being U. ruziziensis, hunger, climate action, clean water and sanitation, decent work P. purpureum, S. sphacelata, and C. gayana efficient for rearing and economic growth, industry innovation and infrastructure, insects for food and feed in sub-Saharan Africa (Rutaro et al., responsible consumption and production, life below water and 2018; Malinga et al., 2020). life on land (Chia et al., 2019). However, there is significant uncertainty about what constitutes optimal diets for farmed insects. Insects can compensate for the detrimental effects of an unbalanced diet EXAMPLES OF SUCCESSFUL PROJECTS through different physiological and behavioral mechanisms. Adequate food ingestion with the proper protein and Two projects in Kenya and Colombia show the impact of carbohydrate ratios, however, results in better insect performance insect production as feed in small and medium-sized farms. (Barragán-Fonseca, 2018). The nutritional requirements vary for In Kenya, the International Centre for Insect Physiology and each insect species and diets determine their nutritional content. Ecology (ICIPE) and Wageningen University trained more For omnivorous farmed insects, these are complex and difficult than 1,000 farmers on the production of black soldier fly to determine because of the broad variety of feed sources and larvae in organic waste substrates for feeding their animals substrates, but this characteristic also allows for more versatile and selling larvae to feed mills, resulting in 37 new insect- diets to ensure their growth and development (Cortes Ortiz et al., based enterprises and the establishment of cost-effective modular 2016; Barragán-Fonseca et al., 2017; Hanboonsong and Durst, insect production systems (Dicke, 2019; Barragán-Fonseca et al., 2020). 2020). In Colombia, the National University of Colombia There exists a large diversity of tropical forages, with great implemented different projects related to insect production for variation in terms of forage yield, agricultural suitability, nutrient replacing 15% of traditional fish feed by black soldier fly larvae, content, and production constraints (Martens et al., 2012; Lee, with ex-combatants of the FARC-EP guerrilla in the Tolima Frontiers in Sustainable Food Systems | www.frontiersin.org 937 November 2021 | Volume 5 | Article 724628 Espitia Buitrago et al. Forage-Fed Insects as Food-Feed Source TABLE 2 | Content of common diets use in large-scale insect industry and potential forage species as alternatives for insect feed. Common diets - nutritional contenta Potential forages as alternatives for insect feedc Source Protein Crude fiber Proteinc Crude fiberb Species Whole yellow corn flour 6.9 7.3 8.3 31.6 Andropogon spp. Carrot, dehydrated 8.1 23.6 9.7 36.1 Pennisetum purpureum Dry potato flour 8.3 6.6 9.8 31.3 Cynodon dactylon (cultivars and hybrids) White wheat 11.3 12.2 11.2 37.3 Megathyrsus maximus Crude wheat bran 15.5 42.8 14 34.2 Stylosanthes spp. Alfalfa pellets 16 27 14.2 31.5 Paspalum notatum Dry egg yolk 32.2 0 14.6 29.9 Urochloa spp. (cultivars and hybrids) Whole soy flour 34.5 9.6 18.9 30.7 Centrosema molle Dry milk, skim 36.2 0 20.6 26.1 Cratylia argentea Baker’s yeast 38.3 21 20.6 26.1 Desmodium heterophyllum Brewer’s yeast 53.3 20 21.4 27.3 Arachis pintoi Dry beef liver 68 0 23.3 19.9 Leucaena leucocephala 9.0 36.9 Chloris gayana 7.7 38 Setaria sphacelata Source: own elaboration based on aCortes Ortiz et al. (2016); bOf fresh aerial part; INRAE et al. (2020); cRao et al. (2015); Schultze-Kraft et al. (2018). Department, also addressing SDG 16 on peace, justice and TOWARD RESPONSIBLE INSECT strong institutions (Barragán-Fonseca et al., 2020). Currently FARMING IN THE TROPICS there are research initiatives led by the International Centre of Insect Physiology and Ecology (ICIPE), academic institutions The European Union (EU) followed by the United States and (e.g., University of Copenhagen, Wageningen University) and Canada leads the global edible insect market and industry governmental institutions (e.g., The Netherlands Organization (Bermúdez-Serrano, 2020). Consequently, the most complete for Scientific Research), such as GREEiNSECT and ILIPA, which and strict legislation related to the use of edible insects is aim at producing scientific evidence for insect production in found in the EU, where the insects (whole or parts of) are small-, medium- and large-scale industries and developing the considered a novelty food that can be marketed throughout commercial potential for food and feed, contributing enormously the region. Policies that regulate the type and quality of insect to the growth of this sector in the tropics. feed, insect commercialization, and more recently, the safety Apart from their use as food and livestock feed, insects can of specific species for human consumption are decreed by the also be sold (alive or processed) on other niche markets with European Food Safety Authority (EFSA), EU member countries, price premiums, such as to zoos or pet owners, generating and Switzerland (Der Schweizerische Bundesrat, 2021). In additional income for producers. Processing methods range from January 2021, dried larvae of the species Tenebrio molitor more artisanal (e.g., sun and oven drying, smoking, curing, (mealworms) were declared safe for human consumption by grounding) to more refined industrial techniques (Melgar- the EFSA, highlighting that the levels of contaminants will Lalanne et al., 2019). New products are being developed depend on those present in the substrates used as insect constantly to satisfy the increasing demands of different niche feed. A review by Lähteenmäki-Uutela et al. (2017) showed markets. For human diets, a broad range of insect-based that, despite the increasing number of companies involved in ingredients and products are already available on the market, the development of insect-based products and the growing which include cricket powder and food coloring or oils, as insect market, the United States, Canada, China and Mexico well as dishes in restaurants and snacks. For instance, in lack regulations regarding the safety of insect food and feed Thailand, where most of the sector is on a small-scale in products. Australia and New Zealand have regulations in the rural areas, new market opportunities in gourmet restaurants Food Standard Code for the species Zophobas morio, Acheta and gastronomy tourism allowed the development of edible domesticus, and Tenebrio molitor, without clear definitions crickets and silkworm products and their industrialization in regarding food and feed safety (Lähteenmäki-Uutela et al., 2021). the main cities of the country (Halloran et al., 2016). Forage- A high quantity of biological, chemical and allergenic risks are based insect diets help to reduce the microbiological and associated with this industry, as with any other kind of food chemical hazard (i.e., microorganisms, viruses, prions, pesticide (EFSA Scientific Committee, 2015), highlighting the urgent need residues) associated with substrates like animal or agriculture for research on this matter. In addition, the participation of by-products or kitchen waste (EFSA Scientific Committee, 2015; non-governmental institutions like the Food and Agriculture Dobermann et al., 2017; Gałecki and Sokół, 2019), resulting in Organization of the United Nations (FAO) and theWorld Health higher food safety of the derived products for both human and Organization (WHO) is necessary to guarantee the safety of animal consumption. insect products and to establish an international market, yet Frontiers in Sustainable Food Systems | www.frontiersin.org 948 November 2021 | Volume 5 | Article 724628 Espitia Buitrago et al. Forage-Fed Insects as Food-Feed Source no such standards are included in the Codex Alimentarius commercial diets, tropical forages are a low-cost feed source for Commission (Lähteenmäki-Uutela et al., 2021). insects, with high dietary versatility, that provide opportunities In tropical countries in Asia and America, legislative for the transition to sustainable, circular economies. We found frameworks for insect production, commercialization and the main bottlenecks in the lack of specific regulations, the consumption are either insufficient or non-existent. In several dependence on few species for large-scale industrial insect countries, insects are not even considered food, undermining production and consumer food safety. their potential role in the diets of humans and animals Further studies should focus on assessing several species of (Bermúdez-Serrano, 2020). In Thailand, the use of edible insects tropical forages to be included in the diets of commonly farmed is an ancestral practice and although there are no food safety insects Also, studies comparing the ease of using tropical forages policies, licenses are needed to establish large-scale cricket as insect feed against that of conventional feed (commercial farms, which are issued by the Food and Drug Administration diets or organic waste) need to be performed. There also exists of Thailand. Also, governmental institutions have released a need to further harmonize rearing, mass production, genetic guidelines for cricket farming (Halloran et al., 2015, 2017; FAO, diversity and harvesting of insects with consumption practices 2021). The situation is similar inMexico, where insect production and strengthening of value chains and legislations. Knowledge is regulated by the organic products law, which focuses on the from communities traditionally using insects as feed and food promotion, conservation and avoidance of overexploitation of need to be considered since they can provide valuable insights. only four species: Aegiale hesperiaris, Liometopum apiculatum, The synergies of these approaches will help the development of Cerambycidae larvae and ant eggs (Lähteenmäki-Uutela et al., alternatives to feed both humans and livestock in a nutritious, 2021). Other Latin American countries, such as Colombia, Brazil, secure and sustainable way. or Argentina, do not have explicit regulations in this regard and tend to follow the Codex Alimentarius Commission standards. DATA AVAILABILITY STATEMENT In contrast, there is legislation in place regarding edible insects in most tropical African countries (Grabowski et al., 2020). Kenya The original contributions presented in the study are included and Uganda are the two counties currently leading the setting in the article/supplementary material, further inquiries can be up of standards for the use of insects as food and feed on the directed to the corresponding author/s. African continent (Egonyu et al., 2021). However, such standards still need to fully facilitate the potential of edible insects as an AUTHOR CONTRIBUTIONS industrial endeavor (Musundire et al., 2021). PE, LH, SB, and JC: conceptualization, methodology, and CONCLUDING REMARKS AND FORWARD resources. PE and LH: formal analysis. PE, LH, SB, NP, and LOOK JC: writing the original draft and review and editing. SB and JC: supervision, funding acquisition, and project administration. Insects are a viable option for supplying the growing demand All authors contributed to the article and approved the for protein in the tropics, especially given the need to adapt submitted version. to and mitigate climate change, potentially contributing to the UN’s 2030 agenda. The advantages of insect farming in the FUNDING tropics include a greater biodiversity, production throughout the year under stable environmental conditions and the contribution This work was undertaken as part of the CGIAR Research to at least 8 Sustainable Development Goals. This has led to Program (CRP) on Livestock. In addition, it was supported by the development of an emerging industry through initiatives the LivestockPlus project funded by the CRP on Climate Change, based on black soldier fly production for fisheries in Kenya and Agriculture and Food Security (CCAFS), which is a strategic Colombia. Organic residues and substrates, commonly used for partnership of CGIAR and Future Earth. this purpose, may, however, represent a hazard for both fishery and human health. We propose a new approach for insect- ACKNOWLEDGMENTS based value chains by integrating tropical forage-based diets in edible insect production systems, given the yet untapped forage We thank all donors that globally support the work of the CRP diversity in international gene banks and on farms. Compared to programs through their contributions to the CGIAR system. REFERENCES view-on-feed-cost-and-feed-efficiency-on-dairy-farms/ (accessed October 27, 2021). Alliance of Bioversity International and CIAT (2021). Tropical Forage Diversity. Bang, A., and Courchamp, F. (2020). Industrial rearing of edible insects could Cali, Colombia: The Alliance of Bioversity International and CIAT. be a major source of new biological invasions. Ecol. Lett. 24, 393–397. Available online at: https://ciat.cgiar.org/what-we-do/crop-conservation-and- doi: 10.1111/ele.13646 use/tropical-forage-diversity/ (accessed May 21, 2021). Barragán-Fonseca, K. (2018). Flies Are What They Eat - Tailoring Alqaisi, O., Asaah, O., and Hemme, T. (2011). Global view on feed cost Nutrition of BSF (Hermetia illucens) for Larval Biomass Production and feed efficiency on dairy farms. All About Feed 2, 1–5. Available and Fitness. (dissertation)]. Wageningen, Netherlands: Wageningen online at: https://www.allaboutfeed.net/animal-feed/feed-processing/global- University. Frontiers in Sustainable Food Systems | www.frontiersin.org 959 November 2021 | Volume 5 | Article 724628 Espitia Buitrago et al. Forage-Fed Insects as Food-Feed Source Barragán-Fonseca, K., Cortés Urquijo, J., Dicke, M., and Quintana, A. P. (2020). FAO (2021). Looking at Edible Insects From a Food Safety Perspective. Challenges “South-south inspiration to connect SDG2 and SDG16 in former conflict and Opportunities for the Sector. Rome: FAO. areas: promoting sustainable livelihoods of ex-insurgents in Colombia by insect Frigerio, J., Agostinetto, G., Sandionigi, A., Mezzasalma, V., Berterame, farming,” inWageningen Livestock Research, Public Report, 1289. N. M., Casiraghi, M., et al. (2020). The hidden ‘plant side’ of insect Barragán-Fonseca, K. B., Dicke, M., and van Loon, J. J. A. (2017). Nutritional novel foods: a DNA-based assessment. Food Res. Int. 128:108751. value of the black soldier fly (Hermetia illucens L.) and its suitability as doi: 10.1016/j.foodres.2019.108751 animal feed - a review. J. Insects Food Feed 3, 105–120. doi: 10.3920/JIFF201 Gałecki, R., and Sokół, R. (2019). A parasitological evaluation of edible insects and 6.0055 their role in the transmission of parasitic diseases to humans and animals. PLoS Bawa, M., Songsermpong, S., Kaewtapee, C., and Chanput,W. (2020). Effect of diet ONE 14:e0219303. doi: 10.1371/journal.pone.0219303 on the growth performance, feed conversion, and nutrient content of the house Grabowski, N. T., Tchibozo, S., Abdulmawjood, A., Acheuk, F., M’Saad Guerfali, cricket. J. Insect Sci. 20, 1–10. doi: 10.1093/jisesa/ieaa014 M., Sayed, W. A., et al. (2020). Edible insects in Africa in terms of Bermúdez-Serrano, I. M. (2020). Challenges and opportunities for the food, wildlife resource, and pest management legislation. Foods 9:502. development of an edible insect food industry in Latin America. J. Insects Food doi: 10.3390/foods9040502 Feed 6, 537–556. doi: 10.3920/JIFF2020.0009 Halloran, A., Hanboonsong, Y., Roos, N., and Bruun, S. (2017). Life cycle Bruford, M.W., Ginja, C., Hoffmann, I., Joost, S., Wengel, P. O., Alberto, F. J., et al. assessment of cricket farming in north-eastern Thailand. J. Clean. Prod. 156, (2015). Prospects and challenges for the conservation of farm animal genomic 83–94. doi: 10.1016/j.jclepro.2017.04.017 resources, 2015-2025. Front. Genet. 6:314. doi: 10.3389/fgene.2015.00333 Halloran, A., Roos, N., Eilenberg, J., Cerutti, A., and Bruun, S. (2016). Life cycle Caldwell, E., Read, J., and Sanson, G. D. (2016). Which leaf mechanical traits assessment of edible insects for food protein: a review. Agron. Sustain. Dev. correlate with insect herbivory among feeding guilds? Ann. Bot. 117, 349–361. 36:57. doi: 10.1007/s13593-016-0392-8 doi: 10.1093/aob/mcv178 Halloran, A., Vantomme, P., Hanboonsong, Y., and Ekesi, S. (2015). Regulating Capstaff, N.M., andMiller, A. J. (2018). Improving the yield and nutritional quality edible insects: the challenge of addressing food security, nature conservation, of forage crops. Front. Plant Sci. 9:535. doi: 10.3389/fpls.2018.00535 and the erosion of traditional food culture. Food Secur. 7, 739–746. Chapman, A. (2005). Numbers of Living Species in Australia and the doi: 10.1007/s12571-015-0463-8 World. Canberra, Australia: Department of Environment and Heritage, Hanboonsong, A., and Durst, P. (2020). Guidance on Sustainable Cricket Farming Australian Government. - A Practical Manual. Bangkok: FAO Chia, S. Y., Tanga, C. M., Osuga, I. M., Mohamed, S. A., Khamis, F. M., Salifu, D., INRAE, CIRAD, AFZ, and FAO (2020). Feedipedia - Animal Feed Resources et al. (2018). Effects of waste stream combinations from brewing industry on Information System. List of Feeds. Available online at: https://www.feedipedia. performance of black soldier fly, Hermetia illucens (Diptera: Stratiomyidae). org/content/feeds?category=13593 (accessed October 27, 2021). PeerJ 6:e5885. doi: 10.7717/peerj.5885 Jansson, A., Hunter, D., and Berggren, Å. (2019). Insects as Food – An Option Chia, S. Y., Tanga, C. M., van Loon, J. J., and Dicke, M. (2019). Insects for Sustainable Food Production? Uppsala, Sweden: Swedish University of for sustainable animal feed: inclusive business models involving Agricultural Sciences. smallholder farmers. Curr. Opin. Environ. Sustain. 41, 23–30. Jongema, Y. (2017). List of Edible Insects of the World, 2017. Available online doi: 10.1016/j.cosust.2019.09.003 at: https://www.wur.nl/en/Research-Results/Chair-groups/Plant-Sciences/ Cortes Ortiz, J., Ruiz, A., Morales-Ramos, J., Thomas, M., Rojas, M., Tomberlin, J., Laboratory-of-Entomology/Edible-insects/Worldwide-species-list.htm et al. (2016). “Insect mass production technologies,” in Insects as Sustainable (accessed April 29, 2020). Food Ingredients: Production, Processing and Food Applications, eds. A. Kim, T. K., Yong, H. I., Kim, Y. B., Kim, H. W., and Choi, Y. S. (2019). T. Dossey, J. A. Morales-Ramos, and M. G. Rojas (London: Academic Edible insects as a protein source: a review of public perception, processing Press), 153–201. technology, and research trends. Food Sci. Anim. Resour. 39, 521–540. Der Schweizerische Bundesrat (2021). Verordnung über tierische Nebenprodukte doi: 10.5851/kosfa.2019.e53 (VTNP) vom 25. Mai 2011 (Stand am 1. Mai 2021) Fassung gemäss Ziff. I der V Lähteenmäki-Uutela, A., Grmelová, N., Hénault-Ethier, L., Deschamps, M. H., vom 25. April 2018, in Kraft seit 1. Juni 2018 (AS 2018 2097). Bern, Switzerland: Vandenberg, G. W., Zhao, A., et al. (2017). Insects as food and feed: laws of Der Schweizerische Bundesrat. Available online at: https://www.fedlex.admin. the European union, United States, Canada, Mexico, Australia, and China. Eur. ch/eli/cc/2011/372/de (accessed October 27, 2021). Food Feed Law Rev. 12, 22–36. Available online at: https://effl.lexxion.eu/article/ Dicke, M. (2019). “Improving livelihood by increasing livestock production in EFFL/2017/1/6 (accessed October 27, 2021). Africa: An agribusiness model to commercially produce high quality insect- Lähteenmäki-Uutela, A., Marimuthu, S., and Meijer, N. (2021). Regulations on based protein ingredients for chicken, fish and pig industries,” in Food and insects as food and feed: a global comparison. J. Insects as Food Feed 7, 1–8. Business Global Challenges Programme. Final Report. Netherlands Organisation doi: 10.3920/JIFF2020.0066 for Scientific Research – NWO. Leakey, R. R. B. (2020). A re-boot of tropical agriculture benefits food production, Dobermann, D., Swift, J. A., and Field, L. M. (2017). Opportunities and hurdles of rural economies, health, social justice and the environment. Nat. Food 1, edible insects for food and feed.Nutr. Bull. 42, 293–308. doi: 10.1111/nbu.12291 260–265. doi: 10.1038/s43016-020-0076-z Dunkel, F. V., and Payne, C. (2016). “Introduction to edible insects” in Insects Lee, M. A. (2018). A global comparison of the nutritive values of forage as Sustainable Food Ingredients: Production, Processing and Food Applications, plants grown in contrasting environments. J. Plant Res. 131, 641–654. eds. A. T. Dossey, J. A. Morales-Ramos, and M. G. Rojas (London: Academic doi: 10.1007/s10265-018-1024-y Press), 1–27. Lundy, M. E., and Parrella, M. P. (2015). Crickets are not a free lunch: protein EFSA Scientific Committee (2015). Scientific Opinion on a risk profile related capture from scalable organic side-streams via high-density populations of to production and consumption of insects as food and feed. EFSA J. 13:60. acheta domesticus. PLoS ONE 10:118785. doi: 10.1371/journal.pone.0118785 doi: 10.2903/j.efsa.2015.4257 Malinga, G. M., Valtonen, A., Hiltunen, M., Lehtovaara, V. J., Nyeko, P., and Egonyu, J. P., Kinyuru, J., Fombong, F., Ng’ang’a, J., Abdullahi Ahmed, Roininen, H. (2020). Performance of the African edible bush-cricket, Ruspolia Y., and Niassy, S. (2021). Advances in insects for food and feed. differens, on single andmixed diets containing inflorescences of their host plant Int. J. Trop Insect. Sci. 41, 1903–1911. doi: 10.1007/s42690-021-0 species. Entomol. Exp. Appl. 168, 448–459. doi: 10.1111/eea.12932 0610-8 Martens, S. D., Tiemann, T. T., Bindelle, J., Peters, M., and Lascano, C. E. European Food Safety Authority (2021). Edible Insects: The Science of Novel Food (2012). Alternative plant protein sources for pigs and chickens in the tropics Evaluations. Available online at: https://www.efsa.europa.eu/en/news/edible- - Nutritional value and constraints: a review. J. Agric. Rural Dev. Trop. Subtrop. insects-science-novel-food-evaluations (accessed May 10, 2021). 113, 101–123. Available online at: http://nbn-resolving.de/urn:nbn:de:hebis: Fanzo, J., and Mattei, F. (2010). “Ensuring agriculture, biodiversity and nutrition 34-2012092441794 (accessed October 27, 2021). remains central to addressing the MDG1 hunger target,” in Biodiversity and Melgar-Lalanne, G., Hernández-Álvarez, A. J., and Salinas-Castro, A. (2019). Sustainable Diets United Against Hunger, eds. B. Burlingame and S. Dernini Edible insects processing: traditional and innovative technologies. Compr. Rev. (Rome: FAO), 44–54. Food Sci. Food Saf. 18, 1166–1191. doi: 10.1111/1541-4337.12463 Frontiers in Sustainable Food Systems | www.frontiersin.org 1600 November 2021 | Volume 5 | Article 724628 Espitia Buitrago et al. Forage-Fed Insects as Food-Feed Source Miglietta, P. P., De Leo, F., Ruberti, M., and Massari, S. (2015). Stull, V. J. (2021). Impacts of insect consumption on human health. J. Insects Food Mealworms for food: a water footprint perspective. Water 7, 6190–6203. Feed 7, 1–20. doi: 10.3920/JIFF2020.0115 doi: 10.3390/w7116190 Tisdell, C. (2001). Socioeconomic causes of loss of animal genetic diversity: Müller, A., Evans, J., Payne, C. L. R., and Roberts, R. (2016). Entomophagy and analysis and assessment. Ecol. Econ. 45, 365–376. doi: 10.1016/S0921-8009(03)0 power. J. Insects Food Feed 2, 121–136. doi: 10.3920/JIFF2016.0010 0091-0 Musundire, R., Ngonyama, D., Chemura, A., Ngadze, R. T., Jackson, J., Matanda, UN (2021). The 17 Goals. United Nations – Department of Economic and M. J., Tarakini, T., Langton, M., and Chiwona-Karltun, L. (2021). Stewardship Social Affairs, Sustainable Development. New York City, NY. Available online of wild and farmed edible insects as food and feed in Sub-Saharan Africa: a at: https://sdgs.un.org/goals (accessed October 27, 2021). perspective. Front. Vet. Sci. 8:102. doi: 10.3389/fvets.2021.601386 van Huis, A., van Itterbeeck, J., Klunder, H., Mertens, E., Halloran, A., Muir, G., Oonincx, D. G. A. B., Laurent, S., Veenenbos, M. E., and van Loon, J. J. A. (2020). et al. (2013). Edible Insects. Future Prospects for Food and Feed Security. Rome, Dietary enrichment of edible insects with omega 3 fatty acids. Insect Sci. 27, Italy: Food and Agriculture Organization of the United Nations. 500–509. doi: 10.1111/1744-7917.12669 Opoke, R., Nyeko, P., Malinga, G. M., Rutaro, K., Roininen, H., and Valtonen, A. Conflict of Interest: The authors declare that the research was conducted in the (2019). Host plants of the non-swarming edible bush cricket Ruspolia differens. absence of any commercial or financial relationships that could be construed as a Ecol. Evol. 9, 3899–3908. doi: 10.1002/ece3.5016 potential conflict of interest. Payne, C. L. R., Scarborough, P., Rayner, M., and Nonaka, K. (2016). Are edible insects more or less “healthy” than commonly consumed meats? A The handling editor is currently editing co-organizing a Research Topic with the comparison using two nutrient profilingmodels developed to combat over- and author SB and confirms the absence of any other collaboration. undernutrition. Eur. J. Clin. Nutr. 70, 285–291. doi: 10.1038/ejcn.2015.149 Ramos-Elorduy, J. (2006). Threatened edible insects in Hidalgo, Mexico Publisher’s Note: All claims expressed in this article are solely those of the authors and some measures to preserve them. J. Ethnobiol. Ethnomed. 2:51. and do not necessarily represent those of their affiliated organizations, or those of doi: 10.1186/1746-4269-2-51 the publisher, the editors and the reviewers. Any product that may be evaluated in Rao, I., Peters, M., Castro, A., Schultze-Kraft, R.,White, D., Fisher, M., et al. (2015). this article, or claim that may be made by its manufacturer, is not guaranteed or LivestockPlus - the sustainable intensification of forage-based agricultural systems to improve livelihoods and ecosystem services in the tropics. Trop. endorsed by the publisher. Grasslands Forrajes Trop. 3, 59–82. doi: 10.17138/TGFT(3)59-82 Rutaro, K., Malinga, G. M., Lehtovaara, V. J., Opoke, R., Nyeko, P., Roininen, Copyright © 2021 Espitia Buitrago, Hernández, Burkart, Palmer and Cardoso H., et al. (2018). Fatty acid content and composition in edible Ruspolia Arango. This is an open-access article distributed under the terms of the Creative differens feeding on mixtures of natural food plants. BMC Res. Notes 11:687. Commons Attribution License (CC BY). The use, distribution or reproduction in doi: 10.1186/s13104-018-3792-9 other forums is permitted, provided the original author(s) and the copyright owner(s) Schultze-Kraft, R., Rao, I. M., Peters, M., Clements, R. J., Bai, C., and Liu, G. are credited and that the original publication in this journal is cited, in accordance (2018). Tropical forage legumes for environmental benefits: an overview. Trop. with accepted academic practice. No use, distribution or reproduction is permitted Grasslands Forrajes Trop. 6, 1–14. doi: 10.17138/TGFT(6)1-14 which does not comply with these terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1701 November 2021 | Volume 5 | Article 724628 REVIEW published: 11 November 2021 doi: 10.3389/fsufs.2021.742842 Tapping Into the Environmental Co-benefits of Improved Tropical Forages for an Agroecological Transformation of Livestock Production Systems An M. O. Notenbaert 1*, Sabine Douxchamps 2, Daniel M. Villegas 3, Jacobo Arango 3, Birthe K. Paul 1, Stefan Burkart 3, Idupulapati Rao 3, Chris J. Kettle 4,5, Thomas Rudel 6, Eduardo Vázquez 7, Nikola Teutscherova 8, Ngonidzashe Chirinda 9, Jeroen C. J. Groot 10, Michael Wironen 11, Mirjam Pulleman 3, Mounir Louhaichi 12, Sawsan Hassan 13, Astrid Oberson 5, Sylvia S. Nyawira 1, Cesar S. Pinares-Patino 14 and Michael Peters 1 1 Alliance of Bioversity International and International Center for Tropical Agriculture, Africa Hub, Nairobi, Kenya, 2 Alliance of Edited by: Bioversity International and International Center for Tropical Agriculture, Hanoi, Vietnam, 3 Alliance of Bioversity International Rein Van Der Hoek, and International Center for Tropical Agriculture, Latin-America Hub, Cali, Colombia, 4 Alliance of Bioversity International and Alliance Bioversity International and International Center for Tropical Agriculture, Rome, Italy, 5Department of Environmental System Science, ETH Zurich, Zurich, CIAT, France Switzerland, 6Department of Human Ecology, Rutgers University, New Brunswick, NJ, United States, 7Department of Soil Reviewed by: Ecology, Bayreuth Center of Ecology and Environmental Research, University of Bayreuth, Bayreuth, Germany, 8 Faculty of Danilo Pezo, Tropical AgriSciences, Czech University of Life Sciences Prague, Prague, Czechia, 9Mohammed VI Polytechnic University, Centro Agronomico Tropical De AgroBioSciences, Agricultural Innovations and Technology Transfer Centre (AITTC), Ben Guerir, Morocco, 10 Farming Investigacion Y. Ensenanza Catie, Systems Ecology, Wageningen University & Research, Wageningen, Netherlands, 11 The Nature Conservancy, Arlington, VA, Costa Rica United States, 12 International Center for Agricultural Research in the Dry Areas, Tunis, Tunisia, 13 International Center for Sandrine Freguin Gresh, Agricultural Research in the Dry Areas, Amman, Jordan, 14Mazingira Centre, Sustainable Livestock Systems, International UMR ART-Dev, CIRAD, France Livestock Research Institute, Nairobi, Kenya *Correspondence: An M. O. Notenbaert Livestock are critical for incomes, livelihoods, nutrition and ecosystems management a.notenbaert@cgiar.org throughout the global South. Livestock production and the consumption of Specialty section: livestock-based foods such as meat, cheese, and milk is, however, under global scrutiny This article was submitted to for its contribution to global warming, deforestation, biodiversity loss, water use, pollution, Climate-Smart Food Systems, a section of the journal and land/soil degradation. This paper argues that, although the environmental footprint Frontiers in Sustainable Food Systems of livestock production presents a real threat to planetary sustainability, also in the global Received: 16 July 2021 south, this is highly contextual. Under certain context-specific management regimes Accepted: 15 October 2021 livestock can deliver multiple benefits for people and planet. We provide evidence that Published: 11 November 2021 a move toward sustainable intensification of livestock production is possible and could Citation: Notenbaert AMO, Douxchamps S, mitigate negative environmental impacts and even provide critical ecosystem services, Villegas DM, Arango J, Paul BK, such as improved soil health, carbon sequestration, and enhanced biodiversity on farms. Burkart S, Rao I, Kettle CJ, Rudel T, Vázquez E, Teutscherova N, The use of cultivated forages, many improved through selection or breeding and including Chirinda N, Groot JCJ, Wironen M, grasses, legumes and trees, in integrated crop-tree-livestock systems is proposed as a Pulleman M, Louhaichi M, Hassan S, stepping stone toward agroecological transformation. We introduce cultivated forages, Oberson A, Nyawira SS, Pinares-Patino CS and Peters M explain their multi-functionality and provide an overview of where and to what extent (2021) Tapping Into the Environmental the forages have been applied and how this has benefited people and the planet alike. Co-benefits of Improved Tropical Forages for an Agroecological We then examine their potential to contribute to the 13 principles of agroecology and Transformation of Livestock find that integrating cultivated forages in mixed crop-tree-livestock systems follows a Production Systems. wide range of agroecological principles and increases the sustainability of livestock Front. Sustain. Food Syst. 5:742842. doi: 10.3389/fsufs.2021.742842 production across the globe. More research is, however, needed at the food system Frontiers in Sustainable Food Systems | www.frontiersin.org 1102 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology scale to fully understand the role of forages in the sociological and process aspects of agroecology. We make the case for further genetic improvement of cultivated forages and strong multi-disciplinary systems research to strengthen our understanding of the multidimensional impacts of forages and for managing agro-environmental trade-offs. We finish with a call for action, for the agroecological and livestock research and development communities to improve communication and join hands for a sustainable agri-food system transformation. Keywords: tropical forages, improved forages, cultivated forages, agroecology, mixed crop-tree-livestock systems, environmental co-benefits IMPORTANCE OF SUSTAINABLE emissions (Bai et al., 2018). Hence, specialized crop production LIVESTOCK PRODUCTION SYSTEMS systems increasingly rely on synthetic fertilizers, and have higher environmental costs per unit of crop product (Zhao et al., 2017). Even though the role of animal based proteins as part of a Lastly, the proportion of grain-based feed ingredients and thus sustainable twenty-first century food system is a highly debated direct competition with human nutrition typically increases in topic (Meybeck and Gitz, 2017), the livestock sector currently the specialized livestock production systems. At the same time, plays a key role in food and nutrition security, particularly in their dependence on antibiotics and growth promoters is harmful developing countries. Livestock products (meat, milk and eggs) for public health (antibiotic resistance, foodborne, and zoonotic contribute 15% and 31% of the global per capita calorie and diseases) (Peterson et al., 2020). protein supply, respectively (Godde et al., 2021). Large regional Globally, the livestock sector has a huge environmental differences characterize the nutritional contributions of livestock, footprint. It is responsible for emitting 14.5% of the total with low intakes of animal-source food in the Global South anthropogenic GHG emissions (Adegbeye et al., 2020), 33% of compared with excesses in the Global North (Meyfroidt, 2018). the total reactive nitrogen emissions (Mueller and Lassaletta, Livestock are kept by more than half of rural households (FAO, 2020), and is utilizing 30% of the total ice-free land area (Havlík 2018, 2021), with more than 844 million people worldwide et al., 2012). While large regional differences exist, many of receiving some income from agriculture, and the livestock the current livestock production systems in the tropics are sector contributing about 40% of the value-added in agriculture responsible for undesirable environmental effects. Expansion of (Gontijo de Lima et al., 2015). grazing land for livestock is a major driver for deforestation In general, family farming—often by smallholders cultivating especially in Latin America, leading to about 57% of pasture less than two hectares—is still the predominant form of livestock land replacement with forests over the last decades (Graesser production in the global South, in terms of numbers as well et al., 2015). Overgrazing in pasture and rangelands has resulted as occupied area (Lowder et al., 2021). On these family farms, in severe soil degradation through compaction and erosion livestock production mainly occurs in mixed crop-livestock (Martinez and Zinck, 2004), especially in the drylands, with SOC systems (Herrero et al., 2010), where livestock has a multitude losses creating a large carbon deficit in soils globally (Sanderman of functions, ranging from the provision of food, nutrition, et al., 2017). In addition, livestock production is associated with income and risk reduction to farmers as well as the contribution biodiversity loss and high water use (Alkemade et al., 2013; of essential nutrients and draft power to reduce drudgery and Heinke et al., 2020) Among the most recognized and studied side improve crop productivity. The farms are further connected effects of livestock production related to environmental damage to—mostly local, regional, and national—markets where they in the tropical areas are: GHG emissions contributing to global generate a plethora of other jobs along livestock value chains (Lie warming, deforestation, biodiversity loss, high water use, and et al., 2017; Bravo et al., 2018; Enciso et al., 2018). land/soil degradation (Martinez and Zinck, 2004; Alkemade et al., In response to increasing demand for livestock products, 2013; Chirinda et al., 2019; Boddey et al., 2020; Butterbach-Bahl these traditionally mixed systems increasingly intensify and are et al., 2020). Widely publicized recent reports, such as EAT- thereby replaced by specialized livestock production systems Lancet (Willett et al., 2019), prompted a wave of media outreach with spatially decoupled crop and livestock production and arguing that one of the main solutions to the climate change and high levels of resource depletion and/or environmental pollution human health crises, globally, is to eat no or little animal-source (Garrett et al., 2017a; Jin et al., 2020). For instance, about 51% foods (Paul et al., 2020a). Although we concur that the growing of total feed nitrogen (N) in China was imported in 2015, demand for livestock products presents a threat to environmental greatly increasing energy requirements for transport, greenhouse sustainability, we question the notion that stopping livestock gas (GHG) emissions abroad, and causing nutrient surpluses production altogether is the most suitable or feasible option. in China (Du et al., 2018; Zhang et al., 2020). The spatial Firstly, the political will is lacking and the necessary behavioral decoupling of crop and livestock production is further associated change of themajority of consumers is unlikely to occur (Winders with smaller fractions of manure returned to cropland and larger and Ransom, 2019). Under these circumstances, it is important losses of manure N to surface and ground waters and GHG to have complimentary strategies that do not eliminate livestock Frontiers in Sustainable Food Systems | www.frontiersin.org 1203 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology but instead transform its production to reduce the environmental (see Supplementary Material). We report the number of hits in damages from the livestock sector. Secondly, livestock is not Web of Science as a metric for the availability of evidence of this only of vital importance for low-income societies in socio- contribution from the perspective of the scientific community. economical terms, but—when managed well—also plays various After reviewing the science at the forage-agroecology nexus, complex and often positive environmental and social benefits section Future Outlook finally identifies critical knowledge gaps (Paul et al., 2020b). To reduce the consumption of animal source and recommends the next steps for scaling up the contribution of food could be a valid option for the Global North where diets cultivated tropical forages to the agroecological transformation show an excess in protein and energy consumption, but not for of agri-food systems. low and middle income countries where most people are under recommended nutrition standards. There, it is, thus, critical THE AGROECOLOGICAL FRAMEWORK to identify sustainable management strategies. These strategies should be applicable to the local context, socially-acceptable, The principles of agroecology have evolved in history, from economically viable and avoid the environmental degradation agriculture-centered to a holistic food system approach that in the long-term undermines their existence. (Gliessman, 2018; Wezel et al., 2020). The most common Agroecology has been put forward as a solution to modern definition of agroecology, “the application of ecological concepts crises such as climate change and malnutrition, contrasting with and principles to the design and management of sustainable the dominant industrial agricultural model based on the use of agroecosystems, or the science of sustainable agriculture,” external inputs (Wezel et al., 2020), while improved forages have has recently evolved into an integrated concept bringing the been proposed as an important entry point for the sustainable three dimensions of sustainability—ecological, economic, intensification of livestock production systems (Rao et al., 2015). and social—to all parts of the food system. The approach is This paper takes a closer look at and links up both these proposed grounded in ecological thinking where a holistic, systems- solutions. It explores the benefits of including improved forages level understanding of food system sustainability is required in integrated crop-livestock-tree systems and investigates the role (Gliessman, 2018). An agroecological perspective on agri-food of such forage-based systems in agroecological transformation. systems links the nutritional value of food and dietary choices We thereby specifically focus on mixed cropping systems and to the environmental and social impacts of food production cultivated forages in the tropics, i.e., crops that are specifically (Lamine and Dawson, 2018). Hilbeck et al. (2015) write that grown as animal feed, be it for grazing or cut-and-carry purposes; “agroecology is neither a defined system of production nor and exclude from our analyses the native and naturalized pastures a production technique. It is a set of principles and practices and rangelands. intended to enhance the sustainability of a farming system, and it Based on a review of literature and expert opinion, we aim is a movement that seeks a new way of food production. Scholars to demonstrate the importance of cultivated tropical forages, thereby agree that the term incorporates three components with their emerging environmental co-benefits, for ensuring (IFOAM EU, 2019). First, it is a scientific discipline, studying sustainable livestock production based on agroecological the ecology of agricultural systems. Second, it has evolved principles. In section The Agroecological Framework, it starts into a set of agricultural practices. Finally, it has turned into by briefly introducing agroecology as (i) a science, (ii) a a movement that incorporates social justice, food sovereignty practice and (iii) a movement supporting the application of and the preservation of cultural identities (Méndez et al., 2013). 13 principles—and their underlying values—to the design of As such, it operates at different levels and engages different farming and food systems. The next section, section Ensuring stakeholders ranging from scientists to farmers and communities System Sustainability Through Integrating Improved Forages in in the context of the sustainable agri-food systems. Mixed Crop-Tree-Livestock Systems in the Tropics, summarizes As happens with multi-dimensional concepts, how cultivated forages have been put into practice by farmers in operationalization often ends up focusing on one or a few the global south and how this provides benefits across different components and fails to maintain a holistic approach. While sustainability domains and barriers to further adoption at promoting unidimensional agroecological practices, oftenmainly scale. Section Contributions of Improved Cultivated Forages technical, still contributes to an agroecological transformation, to Agroecological Transformation proceeds by (i) outlining these approaches are less sustainable as they often lack the through which pathways and mechanisms this practice is in line sociopolitical support needed e.g., to reverse the power balance with each of the agroecological principles and (ii) assessing to with conventional agriculture (Le Coq et al., 2020). Practically, which extent applying these principles is covered in the scientific neglecting the multidimensionality of the agroecology concept literature about forage-based livestock production systems in results in confusion with other concepts like organic agriculture, the tropics. Based on field experience and literature review, we conservation agriculture, nature-positive agriculture or the summarize our understanding of the mechanisms and pathways more recent regenerative agriculture. Organic and conservation through which the integration of forages in animal production agriculture are based on simple principles around soil fertility systems can contribute or has shown to contribute to each of management at plot level, aiming at avoiding the use of the 13 agroecological principles. Based on this understanding, agrochemical and protecting the soil through permanent soil search strings were developed for agroecology as a whole and cover. The two differ in their market orientation, with organic separately for each principle. They were combined with a general agriculture strongly driven by product certification. Regenerative search string capturing the integration of cultivated forages in agriculture proposes a more holistic approach, trying to smallholder mixed crop-tree-livestock systems in the tropics reconcile agroecology and sustainable intensification under the Frontiers in Sustainable Food Systems | www.frontiersin.org 1304 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology same banner, but seems to generate just more confusion (Giller milk, eggs) occurs in mixed crop-livestock systems (Herrero et al., 2021). Nature-positive solutions, in turn, are less specific et al., 2010). Cultivated forages include a wide variety of sown and englobe anything where nature works to address societal or planted grasses, herbaceous legumes, trees and shrubs (mostly challenges, in agriculture or other sectors (Seddon et al., 2021), legumes) that are integrated in a variety of mixed systems, which includes the agroecology concept. The difference would including intensive or extensive mixed agricultural systems be that nature-positive agriculture focusses on practices, whereas with grazing or cut-and-carry systems, agro-pastoral and silvo- agroecology focusses on processes. But a common feature pastoral systems (Rao et al., 2015). In Latin America and the between all these different concepts is their meager integration of Caribbean, permanent pastures are the most common use of the livestock component. Until 2015, only 5% of indexed studies forages, while in Sub-Saharan Africa and Southeast Asia cut-and- concerning agroecology dealt with livestock (Soussana et al., carry systems prevail. 2015). There exists a large diversity of forages allowing adaptation to As the concept gains prominence as a way to sustainably various production contexts. The so-called genetic improvement transform agriculture and food systems, particularly in a post- of tropical forages is relatively recent and was for several COVID world (Altieri and Nicholls, 2020), attempts to recognize decades relying heavily on the agronomic selection of wild all its dimensions and make it operational have culminated relatives. The agronomic/genetic evaluation of forages has been recently with the development of a clear framework and focused not only on productivity and feed quality but also evaluation tool (FAO, 2018, 2021; Mottet et al., 2020). The on tolerance to biotic (insects, diseases) and abiotic (low framework is composed of ten interlinked and interdependent soil fertility, aluminum toxicity, drought, waterlogging) stress elements: (i) diversity, (ii) synergies, (iii) efficiency, (iv) resilience, factors. Through this selection from the wild it was possible (v) recycling, (vi) co-creation and sharing of knowledge, (vi) to identify superior germplasm which resulted in substantial human and social values, (vii) culture and food traditions, (viii) and sustainable productivity gains (per head and per unit responsible governance, (ix) circular, and (x) solidarity economy. area) as well as enhanced resilience (e.g., Peters et al., 2013; The first five describe common characteristics of agroecological Rao et al., 2015; Schultze-Kraft et al., 2018). Recently the systems, the sixth and seventh describe foundational practices importance of bred forages has increased (Jank et al., 2014) and innovation approaches, and the last three describe context and this has allowed attention to specific constraints, where features and enabling environment (FAO, 2018, 2021). These diversity in the natural populations reached limitations in 10 elements imply a series of requirements for farming system identifying productive, nutritive and stress-tolerant materials. management that can be articulated in 13 principles: recycling, For example, in well-drained environments in Latin America and input reduction, soil health, animal health, biodiversity, synergy, the Caribbean with a wide distribution of Urochloa (previously economic diversification, co-creation of knowledge, social values known as Brachiaria; Cook et al., 2020) decumbens, resistance and diets, fairness, connectivity, land and natural resource to a major insect, spittlebug, became an issue to be addressed governance, and participation (Wezel et al., 2020). A farming by the breeding efforts, while for waterlogged environments system that scores high in these principles can be seen as there remains a scarcity of high-quality forages (Argel et al., transitioning toward a sustainable food system via agroecological 2007). Bred forages with a combination of desirable traits transformation. Figure 1 presents a schematic overview of the (e.g., productivity, quality and resistance to biotic and abiotic different agroecological principles at play in a mixed crop-tree- factors) are also attractive to seed suppliers for targeting specific livestock farm. agro-ecological niches, allowing a greater market differentiation In section Contributions of Improved Cultivated Forages to providing incentives for development of the forage seed sector. Agroecological Transformation, we assess the role of improved For example, in the case of crop-livestock systems in Latin tropical forages as a potential catalyst for enabling livestock America and the Caribbean (LAC), we see expanding demand for systems to contribute to the 13 principles and support an forages requiring soil fertility management and greater attention agroecological transformation. As a background, the next section to environmental concerns. There is also an increasing demand defines improved forages, summarizes documented uptake, the for shade-tolerant forages for silvopastoral systems with high multi-dimensional impacts of this uptake and barriers to more resilience to vulnerable climates with extreme and unpredictable wide-spread uptake. weather conditions. Throughout the rest of this paper we will use the term “improved forages” when we refer to forages that ENSURING SYSTEM SUSTAINABILITY have gone through a process of agronomic selection from wild THROUGH INTEGRATING IMPROVED relatives or breeding and selection leading to genetic gain in desirable traits. FORAGES IN MIXED At first sight, such improved forages seem similar to the CROP-TREE-LIVESTOCK SYSTEMS IN high yielding crops such as wheat and rice, widely promoted by THE TROPICS the international agricultural research centers in the 1960s and 1970s and adopted as part of the Green Revolution (Byerlee and Livestock production in the global South takes place in a variety Lynam, 2020). We do, however, not expect the well-documented of livestock production systems. The grassland-based systems, drawbacks, such as high input prices, environmental pollution in which crop-based agriculture is minimal, cover the largest and increased inequality, of the green revolution to re-occur areas (Robinson et al., 2011), while most production (i.e., meat, with improved forages. First, the technology in itself differs Frontiers in Sustainable Food Systems | www.frontiersin.org 1405 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology FIGURE 1 | The agroecological principles at work in a forage-based mixed croptree-livestock systems. significantly, with the improved forages not requiring intensive to have a closer look at some successful scaling examples. application of pesticides, herbicides and synthetic fertilizers. On Maass et al. (2015) estimated that the adoption of hybrid the contrary, many have been selected or are specifically bred for Urochloa cultivars in East Africa was about 1,000 hectares their capacity to perform well in marginal areas facing climate (20,000 households). Labarta et al. (2017) and ISPC (2018) variability and change, low fertility or acid soils, water logging, reported that adoption of improved Urochloa cultivars in and for pest and disease resistance. In addition, they are being Colombia, Peru, Nicaragua, Costa Rica and Honduras occurred promoted as a component of mixed cropping systems to improve on approximately 7.9 million hectares. According to White et al. the overall system performance and efficiency in using local (2013), Stylosanthes varieties (from the CGIAR genebank) have resources. Finally, a wide variety of forage species and varieties, been adopted on at least 200,000 hectares. Valentim and Andrade including indigenous trees and so-called neglected or orphan (2005) estimated the early adoption of Arachis pintoi for the crops, are considered for system improvement. Amazon region of Brazil to have reached 1,000 cattle producers Decades of efforts to promote cultivated forages for their and to have generated a gross profit of US$ 4,000 per year productivity and environmental benefits have contributed to per producer. Wunscher et al. (2004) and Lascano et al. (2005) widespread adoption, particularly grasses in LAC (White et al., reported a successful early adoption ofArachis pintoi in Colombia 2013; Baptistella et al., 2020, REDE ILPF ref). It is worthwhile and Costa Rica. Frontiers in Sustainable Food Systems | www.frontiersin.org 1506 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology The benefits of integrating improved forages in livestock IRR of 49.9% (Rivas and Holmann, 2000). The implementation production systems have previously been described as part of spittlebug-resistant Urochloa hybrids was estimated to have of the LivestockPlus concept (Rao et al., 2015). The authors potential benefits equivalent to 43% of Colombia’s beef and describe how the sustainable intensification of forage-based dairy production volume of 2003 (Rivas and Holmann, 2004a,b). systems, combining genetic, ecological and socio-economic The implementation of different planted forages in West Africa intensification processes, increases the efficiency of the systems, during the period from 1977 to 1997 was estimated to result in has the potential to improve livelihoods, and yields a range an social internal rate of return3 on investments of 38% over 20 of environmental co-benefits—including improved soil health, years (Elbasha et al., 1999). reduced erosion, reduced GHG emissions and improved GHG Examples also abound around the dual economic- balances (emissions vs. carbon accumulation/life cycle), and environmental benefits associated with forage legumes. The improved adaptation to climate variability and change. Figure 2 introduction of forage legumes in the crop-livestock systems illustrates how forages can be integrated in mixed crop-tree- of Nicaragua has proven benefits to tackling degradation and livestock systems and summarizes how this positively impacts on restoring land and soil health. When introduced into the livelihoods and the environment. smallholder traditional crop-livestock production system of The relatively wide adoption of improved tropical forages in the Nicaraguan hillsides, Canavalia brasiliensis derived on LAC has convincingly demonstrated their capacity to increase average 69% of its N from the atmosphere by symbiotic N2- productivity while reducing livestock-related GHG emissions fixation, and increased the soil N balance when used as green per unit product. On one side, their ability to increase soil manure (Douxchamps et al., 2010). In this case, 12% of the N carbon sequestration has been demonstrated (Fisher et al., from Canavalia was recovered in the subsequent maize crop 1994) while the ability of certain grasses (e.g., Urochloa and (Douxchamps et al., 2011). However, when used as forage to Megathyrsus) to modulate the rhizosphere interactions through increase milk yields and annual net income, Canavalia bears biological nitrification inhibition has proven to reduce soil- the risk of triggering soil N depletion, unless animal manure borne N2O emissions up to 60% (compared to similar genotypes is recycled. Therefore, biophysical and socioeconomic trade- without this ability) either after fertilization or urine deposition offs must be carefully balanced at the farm level to maximize (Subbarao et al., 2009; Byrnes et al., 2017). Another strategy is nutrient use efficiency and ensure a sustainable farming system the improvement of cattle diets through supplementation with intensification (Douxchamps et al., 2014). Pastures on highly forage legumes, which has the potential to reduce up to 67% weathered soil in forest margins in Caquetá, Colombia increased cattle enteric CH4 emissions based on a legume (i.e., Leucaena) dry matter and N/protein yield in farmers pastures containing inclusion proportion of 36% when compared to a grass alone diet legumes; because of additional N input via symbiotic N2 (Gaviria-Uribe et al., 2020; Montoya-Flores et al., 2020). fixation; greater P uptake in productive grass-legume than In addition to these environmental co-benefits there is a grass-alone pastures in spite of low plant available P in soils, huge body of evidence about their economic benefits. Zooming which likely resulted in greater P recycling (Villegas et al., 2020). into forage grasses, the implementation of improved forage- Furthermore, the inclusion of the legume Arachis pintoi in grass- based cattle production systems in Latin America, for example, legume associations in the same study area doubles beef and increases the Internal Rate of Return (IRR)1 by 10–100% milk production and leads to an IRR of between 19.3 and 21.1%, compared to traditional grazing systems (Seré and Estrada, 1982; which is significantly higher than for a traditional production Seré et al., 1993). The implementation of improved Urochloa system (Rivas and Holmann, 2000). For Costa Rica, grass-legume brizantha cultivars in Colombian beef cattle systems is expected associations with Arachis pintoi and Cratylia argentea (Rivas to reduce the producer’s risk of obtaining economic losses and and Holmann, 2000) lead to an estimated 30% reduction in lead to economic benefits of US$ 11.3 million at the national level production costs per kilogram of milk (Peters et al., 2001). (2022–2048) from which 62.5% would fall on the producer and Profitability evaluations in Costa Rica, Michoacán (Mexico) and 37.5% on the consumer. Supplementation by 35% with the forage the Colombian Caribbean region report an IRR that oscillates oats (Avena sativa AV25T cv. Altoandina) in a Kikuyu grass around 33% for a Leucaena leucocephala-grass association dairy system increases the net present value (NPV)2 by >100% (Jimenez-Trujillo et al., 2011; González, 2013; Murgueitio et al., when compared with a Kikuyu monoculture and leads to an 2015). The inclusion of Leucaena diversifolia in a Urochloa brizantha cv. Cayman hybrid production system in Colombia 1The IRR is a financial indicator for estimating the profitability of potential is financially profitable and improves all risk and performance investment projects. Although the IRR calculations are based on the same formula indicators when compared with Cayman as a monoculture. used for estimating the Net Present Value (NPV) of an investment project, it does This legume increases the Net Present Value (NPV) and the not estimate the actual dollar value of the project but the expected annual return. Those potential investments with the highest IRR are generally the ones most desirable. 3The social IRR is a financial indicator that refers to the costs and benefits to 2The NPV is an economic indicator that describes the difference between the society of a potential investment. It considers the opportunity costs of people present values of cash in- and outflows over a defined period of time and is used in not participating and the full cost of a potential investment for society, which investment planning for analyzing the profitability of a potential investment. The makes it different from the general IRR indicator which only considers costs at NPV considers the time value of money, is used to compare different investment the individual level. Apart from potential productivity increases derived from alternatives, and relies on a discount rate related to the cost of required capital for a potential investment, the social IRR also considers a broad range of possible making the investment. Investment options with a negative NPV are most likely non-economic benefits, such as better nutrition or a higher availability of end not profitable and should be neglected. products. Frontiers in Sustainable Food Systems | www.frontiersin.org 1607 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology FIGURE 2 | Productivity and environmental co-benefits of tropical forage technologies. IRR and decreases the minimum area required for generating used to incentivise restoration for example in Burkina Faso two basic salaries, the payback period and the risk of obtaining (Vinceti, 2020) leading to more resilient restoration outcomes economic loss (Enciso et al., 2020). Also in south-east Asia, and great adoption of restoration by farmers. Dry forest species forage legumes have proven to play multiple roles, supporting can provide critical reserves during extreme drought offering at farm level an increase of N recycling intensity, of N balances important food and fodder for communities (Valette, 2019). Early and of land productivity. However, the magnitude of the effects effects of silvopastoral systems with improved forages also show there depends strongly on the type of farming system, with more improved soil health and increased abundance and diversity of important effects where potential for improvement was high soil macrofauna as documented by e.g., Barros et al. (2003), Lira (Epper et al., 2019). While in Queensland, Australia, Leucaena et al. (2020), and Vazquez et al. (2020). Mixed systems with a leucocephala has been identified as the most productive and strong tree component are thus gaining prominence because of profitable legume, doubling the gross margin (expressed per unit their true multiple environmental wins: increased soil quality, of area), when compared with perennial grasses. At the regional GHG emission mitigation, higher biodiversity and improved level, economic benefits from the adoption of L. leucocephala water use efficiency. have been estimated to be more than US$ 69 million/yr for 2006 As a final example, cactus pear (Opuntia ficus-indica) is in a planted area of 150,000 ha (Shelton and Dalzell, 2007; Bowen gaining increasing interest across the globe because of its unique et al., 2016). features that could help alleviate hunger in arid regions thanks to Also tree-based forage species have been demonstrated to have its ability to survive in harsh conditions. This spineless species is multiple benefits. Pilot sites in Mali, Burkina Faso and Niger, not invasive and is used as livestock feed that can improve meat for example, show that more successful restoration outcomes and milk production for cash earnings, while helping to reduce are achieved when combining slow-growing indigenous trees groundwater use through its high-water use efficiency (species or shrubs with fast growing native fodder species for livestock with CAM photosynthetic pathway). Furthermore, its evergreen (Sacande and Berrahmouni, 2016). Fodder species have been cladodes can provide “at any time of the year” high palatable Frontiers in Sustainable Food Systems | www.frontiersin.org 1708 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology green fodder with a high Ca to P ratio. Despite its low crude 2019), social capital, and membership of farmer groups (Oulu, protein and fiber content, the cactus pear cladodes are high in 2020). Likewise, structural conditions can influence the adoption water, sugars, ash and vitamins A and C representing a digestible of improved forages, such as the prevailing extensive nature energy-rich feed when incorporated into livestock diets (Rocha of the cattle production systems, low land prices (which can Filho et al., 2021). Because of their high-water content, cactus lead to an expansion of area instead of intensification) (White pears also reduce the need for livestock watering. In fact, cactus et al., 2001), land tenure rights (Kaimowitz and Angelsen, 2008), pear is a very versatile, resilient crop. It is very easy to establish land speculation (Smith et al., 1997), political violence and and able to grow on lands where no other crops can grow. Cactus warfare (ISPC, 2018), and missing regulatory and monitoring pear is a multi-functional plant that can be utilized to restore frameworks. When it comes to promoting the adoption of forage degraded land, control soil and water erosion, regulate climate technologies, it is also important to analyze and understand how through carbon sequestration, and its fruits and cladodes are livestock producers make their decisions and how their decision- consumed by humans (Inglese et al., 2018; Hassan et al., 2019). making process is influenced by factors such as trust (in the Even though the research on gender and social benefits has information provided or in its sources), social networks and started later, good evidence on positive impacts in that dimension socio-cultural contexts (e.g., Jones et al., 2013; Martínez-García of sustainability is also emerging. A case study from Kenya et al., 2013; Rossi Borges and Oude Lansink, 2016; Ambrosius shows that the adoption of improved planted forages in dairy et al., 2019; Hidano et al., 2019). systems leads to additional roles of women in feed and dairy production and thus more control over the derived incomes from the production system, but also to higher labor burdens, which CONTRIBUTIONS OF IMPROVED might affect technology adoption (Lukuyu et al., 2021). Ba et al. CULTIVATED FORAGES TO (2013) report an average of 50% reduction in amount of labor and AGROECOLOGICAL TRANSFORMATION time spent by smallholder farmers in supplying forages to their animals in south Central Vietnam. The adoption of Urochloa As partly demonstrated in the previous section, integrating hybrids and other improved forages in Ugandan pig production improved forages in mixed crop-tree-livestock systems is systems has led to time savings among male and female farmers associated with a wide variety of practice changes. These changes (reduced time for collecting feed) and thus made it possible include agronomic and animal husbandry practice change, for the producers to engage in other economic activities (e.g., awareness creation, capacity building, and multi-stakeholder farming, small-scale enterprises). It also changed the decision- engagement approaches to actions associated with the broader making structures in the households and empowered women to food systems, such as waste reductions and dietary shifts. As join their husbands in the decision on which forage to adopt and amply described in the scientific literature (see Table 1), they how to grow and manage it (Lukuyu et al., 2020). In Ethiopia thereby align well to all 13 agroecological principles. and Kenya, women and youth are increasingly starting to engage The first principle, recycling, prescribes to use local renewable in forage businesses, from which they retain income, and which resources as much as possible and close as far as possible resource is a promising pathway for women’s economic empowerment cycles of nutrients and biomass. Forages take up nutrients (Njuguna-Mungai et al., under review). available in the system, including from deep soil layers, and make Despite the growing evidence on the multiple benefits these available to livestock. This results in improved nutrient of integrating cultivated forages in mixed crop-tree-livestock use efficiency. More options to close nutrient cycles through systems and some successful scaling examples, overall the animal manure also exist. In terms of input reduction, the adoption rates of improved forages remain relatively low, second principle, forages are associated with a reduced need for especially outside Brazil and Latin America. Many of the external inputs, such as feeds, agro-chemicals and water. First, determining factors for the adoption of forage technologies they are associated with a reduction of the need for commercial have been studied and include risk factors (perception of risk feed/supplements/concentrates through higher feed efficiency about future returns from implementing the technology, risk and quality. Well-managed high-quality forages can eliminate aversion of the producer) (e.g., Marra et al., 2003; van Winsen or minimize the need for concentrates by moderate producing et al., 2014; Trujillo-Barrera et al., 2016), the availability of animals, because intensive utilization of forages (cutting or commercial seeds, forage establishment costs, the availability of grazing at the right moment of the phenology) increases the technical information on the establishment and management, production of metabolizable energy and protein per unit of area. the promotion and availability of knowledge about potential Second, they often are associated with a reduction of the need benefits and risks (CIAT, 2004; Wunscher et al., 2004; Lascano for off-farm manure or chemical fertilizers. This is facilitated et al., 2005), labor requirements (Kaimowitz andAngelsen, 2008), through symbiotic N2 fixation by forage legumes and the use of farm size and farm management, the proximity to input markets forages (partly/fully) as greenmanure. In addition, there is higher (ISPC, 2018), the growth of output markets (Kaimowitz and availability of on-farm animal manure because of increased Angelsen, 2008), as well as the general access to productive livestock productivity (through higher stocking rates and better- inputs (e.g., fertilizer, manure, pesticides), capital (e.g., credits, fed animals) and increased availability of crop residues for soil payments for ecosystem services, product differentiation) (e.g., amendments as they can be replaced by forages in the feed basket. Charry et al., 2019), and extension/technical assistance (Ruiz Third, the use of forages as a cover crop reduces the need for et al., 2016; Bravo et al., 2018; Enciso et al., 2018; Charry et al., weeding and chemical weed control, while the use of forages with Frontiers in Sustainable Food Systems | www.frontiersin.org 1809 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology TABLE 1 | Key references describing the contribution of tropical forages in mixed TABLE 1 | Continued crop-tree-livestock (MCTL) systems to the 13 agroecological principles described by Wezel et al. (2020). B. Forage businesses: Pezo et al., 2007; Nakamanee et al., 2008; Gontijo de Lima et al., 2015; Recycling Negassa et al., 2016; Charry et al., 2019; Creemers and Alvarez Aranguiz, 2019; Andriarimalala et al., 2013; Epper et al., 2019; Paul et al., 2019; Dias et al., Harrison et al., 2019; Mwendia et al., 2019; Burkart and Urrea-Benítez, 2020; 2020; Dahlin et al., 2021 Ntakyo et al., 2020; Ohmstedt, 2020a,b; Dey et al., 2021; Neres et al., 2021 Input reduction Co-creation of knowledge A. Reduction of the need for commercial Peters and Lascano, 2003; Pezo et al., 2007; Bautista Solís, 2012; Geng et al., feed/supplements/concentrates through higher feed efficiency and 2017; Dumont et al., 2019; David et al., 2020 quality: Social values and diets Snijders et al., 2011; Lukuyu et al., 2013; Silva et al., 2017 Rudel et al., 2015; Gupta, 2016; Charry et al., 2019; Shapiro et al., 2019; Ruden B. Reduction of the need for off-farm manure or chemical fertilizers: et al., 2020 Nyambati et al., 2006; Douxchamps et al., 2010, 2014; Schultze-Kraft et al., Fairness 2018; Boddey et al., 2020 Calle et al., 2009; Broom et al., 2013; Cibils et al., 2015 C. Decreased use of chemical weed and pest control: Connectivity Chakoma et al., 2016; Lie et al., 2017; Lema et al., 2021 Xuan et al., 2006; Njeru et al., 2020 Land and natural resources governance D. Decreased water requirements: Kaimowitz and Angelsen, 2008; de Oliveira Silva et al., 2016; Garrett et al., Ríos et al., 2006; Nefzaoui et al., 2014; Mayer and Cushman, 2019; Rocha Filho 2017b; Tapasco et al., 2019 et al., 2021 Participation Soil health Ayele et al., 2012; Lie et al., 2017, 2018; Bravo et al., 2018; Enciso et al., 2018; A. Improved chemical soil health: Tapasco et al., 2019; Burkart and Urrea-Benítez, 2020 Fisher et al., 1994; Schultze-Kraft et al., 2018; Baptistella et al., 2020; Lira et al., 2020; Olaya-Montes et al., 2020; Vazquez et al., 2020 B. Improved physical properties: Schultze-Kraft et al., 2018; Baptistella et al., 2020; Boddey et al., 2020 C. Increased below-ground biodiversity and biological activity: Vazquez et al., 2020 genetic tolerance against certain pests and diseases or the use of D. Climate change mitigation: forages in the push-pull system replaces chemical pest control Byrnes et al., 2017; Boddey et al., 2020; Vazquez et al., 2020 measures (e.g., against stemborer and striga). Fourth, forages are associated with decreased water requirements. Increased Animal health soil water retention and infiltration is observed as a result of A. Improved animal nutrition: forages used as a cover crop or green manure to improve soil Hoste et al., 2012; Sousa et al., 2015; Améndola et al., 2016; Sordillo, 2016; Nwafor et al., 2017; Mangwe et al., 2019; Mayberry et al., 2020 structure and limit run-off and in the case of improved forages B. Increased animal welfare: established in areas previously covered by degraded pastures. García-Cruz et al., 2013; Cuartas et al., 2014; Lerner et al., 2015; Pezo et al., Drought-tolerant and water-saver forages reduce dependence on 2018 water for irrigation compared to currently used forages grown in C. Positive indirect effects on human health: similar conditions. Hoffmann et al., in review Integrating cultivated forages in the systems enhances Biodiversity different dimensions of soil health, the third principle. The A. Increased biodiversity across the landscape: chemical soil health is improved through root exudation or Alkemade et al., 2013 forages used as greenmanure, through the stimulation of nutrient B. Increased forage diversity: cycling, soil organic matter (SOM) accumulation, increased soil Giraldo et al., 2011; Rivera et al., 2013; De Farias et al., 2015 carbon stocks and sequestration. The physical soil properties are C. Increased agro-ecosystem diversity compared to monocultures: improved as a result of increased soil aggregation, improved soil D’Annolfo et al., 2021 structure and aeration, increases in particulate organic matter in soil, roots remaining in soil after harvest/grazing, forages as D. Habitats: green manure or cover crop, or the use of forages to prevent Harvey et al., 2006; Moreno and Pulido, 2010; Rivera et al., 2013; soil erosion. Below-ground biodiversity and biological activity is Montoya-Flores et al., 2020 increased through increased soil microbial diversity and activity, Synergy presence of rhizobia. Diverse pastures (mix of various species) of Khan et al., 2008; Descheemaeker et al., 2010; Peters et al., 2012; Cheruíyot diverse functions (secondary compounds, root system) improve et al., 2020; Wan et al., 2020; Zahoor et al., 2021 the conditions for biological activity at deeper horizons, while Economic diversification increased use of tree-based forages can improve soil quality A. Commercial livestock production: through improved mycorrhizal networks. The integration of Rivas and Holmann, 2000, 2004a,b; Peters et al., 2001; Shelton and Dalzell, forages, with their capacity to sequester and store carbon in the 2007; Murgueitio et al., 2015; Bowen et al., 2016; Schiek et al., 2018; Charry soil and to inhibit biological nitrification, finally, can significantly et al., 2019; Enciso et al., 2019, 2020; Chizmar et al., 2020; Ruden et al., 2020 enhance the climate change mitigation function of the soil. (Continued) Frontiers in Sustainable Food Systems | www.frontiersin.org 1910 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology Different mechanisms are at play for improving animal health Different mechanisms contribute to economic diversification, and welfare, the fourth agroecological principle. High-quality the seventh principle. In first instance, forages enable further forages (incl. legumes) in the systems improve the overall quality commercialization of livestock production. Feed represents and quantity feeding and thus animal health, amongst others the highest cost of production in any livestock system and through enhanced immunity and resistance to pathogens. The cultivated forages can substantially reduce the feed input costs. In conservation of forages (e.g., hay, silage, pellets) thereby increases combination with enhanced productivity, this results in increased the availability of feed during seasons where scarcity of feed rates of return and opens opportunities for income diversification leaves the animals most vulnerable to disease. Forages from with cattle fattening or commercial milk production. Also the diverse pastures (a mix of various species) complement each forages in themselves allow for income-diversification. Income- other in their contents of critical nutrients for the animal generating opportunities along the forage value chain include and secondary compounds. Some can, for example, be more forage seed supply, marketing and distribution, the sale of hay, efficient in utilizing P or pumping Cu or Mg, providing balanced silage, pellets and timber or fruits in the case of forage trees. nutrients and secondary compounds (antibloat, antiparasite Approaches that encourage co-creation of knowledge and agents), while recent results indicate that bioactive tanniniferous horizontal learning used in research and development efforts plants represent a valuable option as an alternative to commercial around cultivated and improved forages include: on-farm variety drugs for the control of gastrointestinal nematodes. Animal trials and participatory monitoring and evaluation, capacity welfare is increased in silvopastoral systems. The trees/shade building and knowledge exchange activities such as field days create more favorable microclimatic conditions and reduce heat and farmer exchanges. These approaches promote farmer-to- stress, which has in turn been associated with more stable farmer contacts as well as more equal relationships between social/hierarchical behavior. In addition to animal health and farmers and researchers. This encourages sharing knowledge and welfare, also positive indirect effects on human health have been skills and triggers innovation in combination with encouraging documented. Improved plant health, including those of forages, community-level seed production and “passing on the gift,” the under minimal use of agrochemicals improves animal and existing technology (and associated management practices) scale human health through reduced exposure to chemical residues. out quickly. Well-fed animals require less antibiotics thus reducing the need In terms of social values and diets, principle number nine, for antibiotics and risk of antimicrobial resistance. Well-fed and animal sourced foods (ASF) are an important source of proteins healthy animals cause a lower pathogen load in manure that and readily available micro-nutrients, especially important for can be transmitted through the food chain and feeding healthy improving the nutritional status of especially young children forages can reduce feeding of feeds with high aflatoxins such as and pregnant and lactating women. Integrating cultivated forages maize in East Africa. in livestock production systems can increase both the quantity The fifth agroecological principle, biodiversity, can be and quality of ASF production. The forages also enable the enhanced by increasing biodiversity across the landscape. production of sustainably produced ASF, with simultaneous Enhancing land productivity, through high-yielding forages, social, economic and environmental benefits. can spare land for biodiversity conservation and prevent Efforts to ensure the affordability of quality and the need for further land conversion to agriculture. The environmentally-friendly animal products and the creation introduction of alternative forage species increases the diversity of opportunities for smallholders, including for women and of species and genetic resources at farm and landscape level youth align well to principle ten, fairness. Forages support as compared to grass monocultures or degraded/intensively- dignified and robust livelihoods along the livestock value chains. managed pastures. This can include the use (and in-situ In line with connectivity, the eleventh principle, local feed, seed, conservation) of local/neglected species. The broader variety of and ASF production allow re-embedding food systems into forage species in combination with reduced use of chemical local economies. Actors along the forages and ASF value chains weed/pest control is likely to attract/maintain wider diversity have more proximity and confidence and are better connected of e.g., pollinators and below-ground fauna. such well-managed to markets. Principle twelve, land and natural resources pastures increase the natural introduction of native plant governance, prescribes to strengthen institutional arrangements species with desired feeding value and resilience to extreme to improve, including the recognition and support of family environmental conditions. In silvopastoral systems, the presence farmers, smallholders and peasant food producers as sustainable of shrubs and trees has been demonstrated to have a positive managers of natural and genetic resources. Forages create a need impact on biodiversity by creating complex habitats for wild for land-use planning and offer opportunities for development animals and plants and harboring a richer soil biota as compared of new resource management strategies, for instance to mitigate to conventional grazing systems. Cultivated forages enhance soil degradation (e.g., fanya juu terraces). Participatory land-use positive ecological interactions and complementarities among planning processes can ensure the optimal use of land areas that system components at the interface between the system’s soil, would not be suitable for crops, use in rotation/intercropping/life plant, and animal components and thus align well with the barriers/under trees and at times promote land use options for sixth agroecological principle of synergy. Using for example carbon-neutral agriculture. In line with the last principle, tree-based forages can help to increase on-farm above and participation, the Forage community has started to apply a wide below ground carbon storage, leading to additional climate array of participatory approaches. Through participatory system mitigation benefits. dynamics modeling and participation in multi-stakeholder Frontiers in Sustainable Food Systems | www.frontiersin.org 1101 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology innovation platforms or round-table discussions, farmers can be during the period 2005–2020, with some promising peaks included in the design of livestock and forage sector strategies. for animal health and synergy. More research is needed at These approaches promote equal relationships and balanced the food system scale to fully understand the role of forages powers between farmers, researchers and policy makers. in agroecology, particularly on sociological and process Between 2005 and 2021, a total of 1,183 peer-reviewed aspects, which are both at the core of the four principles less publications addressed the use of cultivated forages in documented. This also indicates a yet to be filled opportunity smallholder systems. The most studied principles concerning for forage experts to engage more with the agroecological the forages are economic diversification, social values and diets, movement and make forages part of sustainable agri-food biodiversity, and recycling, all illustrated by more than 200 system transformation. The finding that despite the existence peer-reviewed publications, mostly at farm scale. Animal health of scientific literature about cultivated forages and each of the renders 126 hits, then the other principles with less than a agroecological principles, only 38 out of the 1,183 publications hundred. Connectivity was the least represented, with only five in our WoS search explicitly mention agroecology corroborates hits. These results show that the most evident agroecological this action gap. impact of forages, according to the scientific community, can be observed in terms of market opportunities and income diversification. The high number of hits for social value and FUTURE OUTLOOK diets illustrates how high the topic of animal-source food and vegetarianism is currently on the global agenda. The principle As illustrated in sections Ensuring System Sustainability Through of biodiversity includes particularly papers reporting options Integrating Improved Forages in Mixed Crop-Tree-Livestock to include forages in rotation or intercropping with different Systems in the Tropics and Contributions of Improved types of systems and pastures’ diversity. Finally, the capacity Cultivated Forages to Agroecological Transformation, there is of forages to provide options to close nutrient cycles at the increased research interest and understanding of the economic, farm level was well-documented. The scientific community’s social and agroecological dynamics related to improved forages interest in these topics has evolved: social values and diets are and their integration in mixed crop-tree-livestock systems. high on the agenda since 2012, recycling emerged a bit later in However, several knowledge and technology gaps still exist. At 2015, while economic diversification and biodiversity display a the actual technology level, it is important to continue the sawtooth but generally increasing interest (Figure 2). Besides genetic improvement and identify or develop forage varieties connectivity and participation, which are both only sporadically tolerant to a wide range of biotic and abiotic stress factors. addressed, the documentation of the other principles increased Supported by state-of-art genomics and phenomics, this can be FIGURE 3 | Evolution of the interest of the scientific community for the different nexi between forages and principles. Frontiers in Sustainable Food Systems | www.frontiersin.org 1112 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology done more efficiently and rapidly than before (Chang et al., CONCLUSION 2019). Ensuring genetic diversity at forage level provides an insurance with respect to the impact of biotic and abiotic stress The environmental and social consequences of the prevailing factors on yield and quality (Finckh, 2008). Livestock production, agri-food system have sparked a lively societal discussion on however, does not only take place in heterogeneous agro-climatic how to feed an increasing population in a socio-ecologically conditions, but also in a wide diversity in farm systems, and sustainable and equitable way. In response, agroecology has been socioeconomic or policy contexts (Umunezero et al., 2016). To presented as a practice, scientific discipline, and socio-political guide the choice of forage species and their integration into movement that applies ecological concepts in the sustainable farming systems more systems agronomy is needed to produce management of agricultural systems. Although some literature robust socio-ecological niches for various systems that can be highlights the important role livestock play in sustainable food scaled (Paul et al., 2020c). This must be combined with increased systems and specifically agroecology, the prevailing narrative, research investments in the forages-soil health nexus which seem especially so in the popular media, argues that one of the leading to have remained stable but low, with <100 WoS hits in total solutions to climate change and human health crises is to eat no (Figure 3). or little animal-source foods. Further research is also required to strengthen our In this paper, however, we point out that the narrow understanding of the multiple interacting impacts of improved climate/diet framing misses the valuable role livestock can forages at the food system level. An increased understanding play, especially for family farmers in the south. Integrated of particularly the social dimension has a lot to offer, also in systems present an opportunity to improve livestock production, terms of understanding the drivers, underlying causes and support livelihoods, enhance and protect biodiversity, close impacts of changes linked to the productivity, economic, nutrient loops etc. and forages play a key role in catalyzing this environmental and human dimensions (Rietveld et al., 2021), transformation. Scientific literature and documented practice while our WoS search results show a low coverage of these change by farmers indicate that integrating cultivated forages issues in the scientific literature. Based on empirical data, in mixed crop-tree-livestock systems follows a wide range of foresight analyses and farming systems modeling can be used to agroecological principles and increases the sustainability of estimate multidimensional impacts of forages and for reducing livestock production across the globe. We, therefore, have reason agro-environmental trade-offs (Groot et al., 2012; Paul et al., to believe that livestock production in the tropics based on 2020c). In addition to developing context-specific data on improved forages can boost the sustainability indicators of this the potential trade-offs associated with integrating forages system, moving toward an agroecological transformation of the in mixed crop-tree-livestock systems, a better understanding food system. It is, however, clear that a lot of this promise of what drives uptake of improved forages, especially within is yet to materialize and calls for an urgent coming together agroecological initiatives, is needed for guiding large-scale of the agroecological and livestock research and development investments and supporting the decision-making processes communities. The specific role of the scientific community around that. is therein to generate and use nuanced evidence on what is At a more immediate action level, to ensure agroecological- possible and what is not (taking multi-scale trade-offs into based farming sustainability, there is a need for demand for account). As part of the overall movement, they can help the resultant products driven by sufficient public attention. ensuring that forages gain more prominence in agroecological To achieve the level of attention that results in changes in initiatives and that more investments are made in sustainable policy and consumer demand, there is a need for influential agri-food system transformation with explicit livestock and communication targeting policymakers and the different publics. forage components. Raising awareness at different decision-making levels should aim to differentiate, label and promote livestock products AUTHOR CONTRIBUTIONS derived from agroecosystems based on agroecological principles. Concurrently, cultivated forages should be promoted as a AN, SD, JA, and BP: conceptualized the study and did a general versatile and multi-purpose crop through public campaigns literature review. DV: conducted the quantitative literature search (social media, workshops, leaflets, lobbying) (Louhaichi et al., in Web of Science. AN: led the writing of all drafts and revisions. 2018). However, from the literature search (Figure 2) these MPe: contributed to forage breeding and agronomy and provided aspects seem to be understudied which would imply limited overall scientific oversight. CK: tree-based systems. MPu: study innovation in awareness raising. Yet, by highlighting the design. TR and MW: context and framing. EV, NT, and AO: evidence-based benefits of integrating cultivated forages in soil health. SN: soil organic carbon. CP-P: adoption factors. agroecosystems, we can increase the visibility of crop-livestock NC: GHGe. SB: economics and adoption. All authors gaps systems and inform the flow of scaling-up investments. In and conclusions. addition, promotional and educational activities, along with results from further research involving farmer participation, in combination economic incentives, such as payments for FUNDING ecosystem services and the development of inclusive business models, should be further explored (Schultze-Kraft et al., This work was undertaken as part of the CGIAR Research 2018). Program on Livestock, which is carried out with support Frontiers in Sustainable Food Systems | www.frontiersin.org 1123 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology from the CGIAR Fund to Donors and bilateral funding Todras-Whitehill and Mireille Ferrari and beautiful illustrations agreements (https://www.cgiar.org/funders). by Sonja Niederhumer. ACKNOWLEDGMENTS SUPPLEMENTARY MATERIAL We wish to extend a special thank to Jose Luis Urrea Benitez for The Supplementary Material for this article can be found designing Figure 1 and contributing to Figure 2. For Figure 2, online at: https://www.frontiersin.org/articles/10.3389/fsufs. we further want to acknowledge the skillful design by Tara 2021.742842/full#supplementary-material REFERENCES Bowen MK., Chudleigh F., Buck S., and Hopkins, K. (2016). Productivity and profitability of forage options for beef production in the subtropics of northern Adegbeye, M. J., Ravi Kanth Reddy, P., Obaisi, A. I., Elghandour, M. M. Australia. Anim. Product. Sci. 58, 332–342. doi: 10.1071/AN16180 M. Y., Oyebamiji, K. J., Salem, A. Z. M., et al. (2020). Sustainable Bravo, A., Enciso, K., Hurtado, J. J., del Cairo, J. R., Jäger,M., and Charry, A. (2018). agriculture options for production, Greenhouse gasses and pollution Estrategia Sectorial de la Cadena de Ganadería Doble Propósito en Guaviare, alleviation, and nutrient recycling in emerging and transitional nations - Con Enfoque Agroambiental y Cero Deforestación. Cali: Centro Internacional de An overview. J. Clean. Product. 242:118319. doi: 10.1016/j.jclepro.2019.1 Agricultura Tropical (CIAT). Available online at: https://hdl.handle.net/10568/ 18319 91289 (accessed November 14, 2019). Alkemade, R., Reid, R. S., van den Berg, M., de Leeuw, J., and Jeuken, Broom, D. M., Galindo, F. A., and Murgueitio, E. (2013). Sustainable, efficient M. (2013). Assessing the impacts of livestock production on biodiversity livestock production with high biodiversity and good welfare for animals. Proc. in rangeland ecosystems. Proc. Natl. Acad. Sci. U.S.A. 110, 20900–20905. R. Soc. B Biol. Sci. 280:20132025. doi: 10.1098/rspb.2013.2025 doi: 10.1073/pnas.1011013108 Burkart, S., and Urrea-Benítez, J. L. (2020). The Colombian Roundtable for Altieri, M. A., and Nicholls, C. I. (2020). Agroecology and the emergence Sustainable Beef and Dairy: 2020 Activities. Cali: Alliance of Bioversity of a post COVID-19 agriculture. Agric. Hum. Values 37, 525–526. International and CIAT. doi: 10.1007/s10460-020-10043-7 Butterbach-Bahl, K., Gettel, G., Kiese, R., Fuchs, K., Werner, C., Rahimi, Ambrosius, F. H. W., Hofstede, G. J., Bokkers, E. A. M., Bock, B. B., and Beulens, J., et al. (2020). Livestock enclosures in drylands of Sub-Saharan Africa A. J. M. (2019). The social influence of investment decisions: a game about the are overlooked hotspots of N 2 O emissions. Nat. Commun. 11, 1–6 Dutch pork sector. Livestock Sci. 220, 111–122. doi: 10.1016/j.livsci.2018.12.018 doi: 10.1038/s41467-020-18359-y Améndola, L., Solorio, F. J., Ku-Vera, J. C., Améndola-Massiotti, R. D., Zarza, H., Byerlee, D., and Lynam, J. K. (2020). The development of the international and Galindo, F. (2016). Social behaviour of cattle in tropical silvopastoral and center model for agricultural research: a prehistory of the CGIAR. World Dev. monoculture systems. Animal 10, 863–867. doi: 10.1017/S1751731115002475 135:105080. doi: 10.1016/j.worlddev.2020.105080 Andriarimalala, J. H., Rakotozandriny, J. D. N., Andriamandroso, A. L. H., Byrnes, R. C., Nùñez, J., Arenas, L., Rao, I., Trujillo, C., Alvarez, C., et al. (2017). Penot, E., Naudin, K., Dugué, P., et al. (2013). Creating synergies between Biological nitrification inhibition by Brachiaria grasses mitigates soil nitrous conservation agriculture and cattle production in crop-livestock farms: a study oxide emissions from bovine urine patches. Soil Biol. Biochem. 107, 156–163. case in the Lake Alaotra Region of Madagascar. Exp. Agric. 49, 352–365 doi: 10.1016/j.soilbio.2016.12.029 doi: 10.1017/S0014479713000112 Calle, A., Montagnini, F., and Zuluaga, A. F. (2009). Farmer’s perceptions of Argel, M., Pedro, J., Miles, J. W., Guiot García, J. D., Cuadrado Capella, H., and silvopastoral system promotion in Quindío, Colombia. Bois et forets des Lascano, C. E. (2007). Cultivar Mulato II (Brachiaria hybrid CIAT 36087): tropiques 300, 79–94. doi: 10.19182/bft2009.300.a20417 A High-Quality Forage Grass, Resistant to Spittlebugs and Adapted to Well- Chakoma, I., Gwiriri, L. C., Manyawu, G., Dube, S., Shumba, M., and Gora, A. Drained, Acid Tropical Soils. CIAT. (2016). Forage seed production and trade as a pathway out of poverty in the Ayele, S., Duncan, A., Larbi, A., and Khanh, T. T. (2012). Enhancing smallholder sector: lessons from the Zimbabwe Crop Livestock Integration innovation in livestock value chains through networks: lessons from fodder for Food Security (ZimCLIFS) project. Afr. J. Range Forage Sci. 33, 181–184. innovation case studies in developing countries. Sci. Public Policy 39, 333–346. doi: 10.2989/10220119.2016.1173097 doi: 10.1093/scipol/scs022 Chang, T.-G., Chang, S., Song, Q.-F., Perveen, S., and Zhu, X.-G. (2019). Ba, N. X., Lane, P. A., Parsons, D., Van, N. H., Khanh, H. L. P., Corfield, J. P., Systems models, phenomics and genomics: three pillars for developing et al. (2013). Forages improve livelihoods of smallholder farmers with beef high-yielding photosynthetically efficient crops. in silico Plants 1:diy003. cattle in South Central Coastal Vietnam. Trop. Grasslands Forrajes Tropicales doi: 10.1093/insilicoplants/diy003 1, 225–229. doi: 10.17138/TGFT(1)225-229 Charry, A., Narjes, M., Enciso, K., Peters, M., and Burkart, S. (2019). Bai, Z., Lee, M. R. F., Ma, L., Ledgard, S., Oenema, O., Velthof, G. L., et al. (2018). Sustainable intensification of beef production in Colombia - chances Global environmental costs of China’s thirst for milk. Glob. Change Biol. 24, for product differentiation and price premiums. Agric. Food Econ. 7:22. 2198–2211. doi: 10.1111/gcb.14047 doi: 10.1186/s40100-019-0143-7 Baptistella, J. L. C., Andrade, S. A. L., Favarin, J. L., and Mazzafera, P. Cheruíyot, D., Midega, C. A. O., Pittchar, J. O., Pickett, J. A., and Khan, Z. R. (2020). Urochloa in tropical agroecosystems. Front. Sustain. Food Syst. 4:119. (2020). Farmers’ perception and evaluation of Brachiaria Grass (Brachiaria doi: 10.3389/fsufs.2020.00119 spp.) genotypes for smallholder cereal-livestock production in East Africa. Barros, E., Neves, A., Blanchart, E., Fernandes, E. C. M., Wandelli, E., Lavelle, Agriculture 10:268. doi: 10.3390/agriculture10070268 P., et al. (2003). Development of the soil macrofauna community under Chirinda, N., Loaiza, S., Arenas, L., Ruiz, V., Faverín, C., Alvarez, C., et al. (2019). silvopastoral and agrosilvicultural systems in Amazonia. Pedobiologia 47, Adequate vegetative cover decreases nitrous oxide emissions from cattle urine 273–280. doi: 10.1078/0031-4056-00190 deposited in grazed pastures under rainy season conditions. Sci. Rep. 9, 1–9. Bautista Solís, P. (2012). Are we learning? Strengthening local people’s capacities to doi: 10.1038/s41598-018-37453-2 facilitate the recuperation of degraded pasture lands in Central America (Ph.D. Chizmar, S., Castillo, M., Pizarro, D., Vasquez, H., Bernal, W., Rivera, R., et al. thesis). CATIE, Bangor University, Bangor, United Kingdom. (2020). A discounted cash flow and capital budgeting analysis of silvopastoral Boddey, R. M., Casagrande, D. R., Homem, B. G. C., and Alves, B. J. R. systems in the Amazonas region of Peru. Land 9:353. doi: 10.3390/land9100353 (2020). Forage legumes in grass pastures in tropical Brazil and likely CIAT (2004). Tropical Grasses and Legumes: Optimizing Genetic Diversity for impacts on greenhouse gas emissions: a review. Grass For. Sci. 75, 357–371. Multipurpose Use (Project IP5). Annual Report 2004. Cali: Centro Internacional doi: 10.1111/gfs.12498 de Agricultura Tropical. Frontiers in Sustainable Food Systems | www.frontiersin.org 1134 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology Cibils, A. F., McGrew, D., Kassambara, B., Bengaly, K., Sissoko, B., and Enciso, K., Bravo, A., Charry, A., Rosas, G., Jäger, M., Hurtado, J. J., et al. (2018). Acharya, R. N. (2015). Challenges and opportunities for agro-pastoral livestock Estrategia Sectorial de la Cadena de Ganadería Doble Propósito en Caquetá, smallholders in Mali. Outlook Agric. 44, 69-80. doi: 10.5367/oa.2015.0198 Con Enfoque Agroambiental y cero Deforestación. Cali: Centro Internacional de Cook, B. G., Pengelly, B. C., Schultze-Kraft, R., Taylor, M., Burkart, S., Cardoso Agricultura Tropical (CIAT). Available online at: https://hdl.handle.net/10568/ Arango, J. A., et al. (2020). Tropical Forages: An Interactive Selection Tool. Cali: 91981 (accessed October 21, 2019). International Center for Tropical Agriculture (CIAT). Nairobi: International Enciso, K., Castillo, J., Burkart, S., Avellaneda, Y., Vargas, J., Campuzano, L. F., et al. Livestock Research Institute (ILRI). (2020). Evaluación Económica de la Avena Forrajera Altoandina para Sistemas Creemers, J. J. H. M., and Alvarez Aranguiz, A. (2019). White Paper: Pathways to Lecheros del Trópico Alto de Colombia. Mosquera. Available onlineat: https:// Intensify Sustainable Forage Production in Kenya - NEADAP. Available onlune hdl.handle.net/10568/111083 at: https://edepot.wur.nl/504127 Enciso, K., Sotelo, M., Peters, M., and Burkart, S. (2019). The inclusion Cuartas, C. C. A., Naranjo, R. J. F., Tarazona, M. A. M., Murgueitio, R. E., of Leucaena diversifolia in a Colombian beef cattle production system: Chará, O. J. D., Ku-Vera, J. C., et al. (2014). Contribution of intensive an economic perspective. Trop. Grasslands Forrajes Tropicales 7, 359–369. silvopastoral systems to animal performance and to adaptation and mitigation doi: 10.17138/tgft(7)359-369 of climate change. Revista Colombiana de Ciencias Pecuarias 27, 76–94. Epper, C. A., Paul, B., Burra, D. D., Phengsavanh, P., Ritzema, R. S., Syfongxay, doi: 10.17533/udea.rccp C., et al. (2019). Nutrient flows and intensification options for smallholder Dahlin, A. S., Mukangango, M., Naramabuye, F. X., Nduwamungu, J., and Nyberg, farmers of the Lao uplands. Agric. Syst. 177:102694. doi: 10.1016/j.agsy.2019.1 G. (2021). Effect of grass-diet and grass-legume-diet manure applied to planting 02694 holes on smallholder maize production in Rwanda. Field Crops Res. 263:108057. FAO (2018). Livestock and Agroecology. Available online at: http://www.fao.org/3/ doi: 10.1016/j.fcr.2021.108057 I8926EN/i8926en.pdf D’Annolfo, R., Gemmill-Herren, B., Amudavi, D., Shiraku, H. W., Piva, M., and FAO (2021). FAOSTAT Food and Agricultural Data. Food and Agriculture Garibaldi, L. A. (2021). The effects of agroecological farming systems on Organization (FAO) of the United Nations, Rome. Available online at: http:// smallholder livelihoods: a case study on push-pull system fromWestern Kenya. www.fao.org/faostat/en/#data Int. J. Agric. Sustain. 19, 56–70, doi: 10.1080/14735903.2020.1822639 Finckh, M. (2008). Integration of breeding and technology into diversification David, M., Bernard, B., Anthony, E., Michael, M. S., James, W., Andrew, strategies for disease control in modern agriculture. Eur. J. Plant Pathol. 121, A., et al. (2020). The role of indigenous knowledge (IK) in adaptation to 399–409. doi: 10.1007/s10658-008-9273-6 drought by agropastoral smallholder farmers in Uganda. Indian J. Trad. Fisher, M. J., Tao, I. M., Ayarza, M. A., Lascano, C. E., Sanz, J. I., Thomas, R. J., Knowledge19, 44–52. et al. (1994). Carbon storage by introduced deep-rooted grasses in the South De Farias, P. M., Arellano, L., Hernández, M. I. M., and Ortiz, S. L. American savannas. Nature 371, 236–238. doi: 10.1038/371236a0 (2015). Response of the copro-necrophagous beetle (Coleoptera: García-Cruz, F., Ibrahim, M., and Pezo, D. (2013). “Los árboles en los potreros Scarabaeinae) assemblage to a range of soil characteristics and livestock para la reducción del estrés calórico del ganado en los trópicos,” in Estado management in a tropical landscape. J. Insect Conserv. 19, 947–960. del recurso arbóreo en fincas ganaderas y su contribución en la producción en doi: 10.1007/s10841-015-9812-3 Rivas, Nicaragua, eds D. Sánchez, C. Villanueva, G. Rusch, M. Ibrahim, and F. de Oliveira Silva, R., Barioni, L. G., Hall, J. A. J., Matsuura, M. F., Albertini, DeClerck (Turrialba: CATIE), 36–41. T. Z., Fernandes, F. A., et al. (2016). Increasing beef production could lower Garrett, R. D., Niles, M. T., Gil, J. D. B., Gaudin, A., Chaplin-Kramer, R., Assmann, greenhouse gas emissions in Brazil if decoupled from deforestation. Nat. Clim. A., et al. (2017b). Social and ecological analysis of commercial integrated crop Change 6, 493–497. doi: 10.1038/nclimate2916 livestock systems: current knowledge and remaining uncertainty. Agric. Syst. Descheemaeker, K., Amede, T., and Haileslassie, A. (2010). Improving water 155, 136–146. doi: 10.1016/j.agsy.2017.05.003 productivity in mixed crop-livestock farming systems of sub-Saharan Africa. Garrett, R. D., Niles, M. T., Gil, J. D. B., Gaudin, A., Chaplin-Kramer, R., Agric. Water Manage. 97, 579–586. doi: 10.1016/j.agwat.2009.11.012 Assmann, A., Assmann, T. S., et al. (2017a). Social and ecological analysis Dey, B., Notenbaert, A., Makkar, H., Mwendia, S., Peters, M., and Sahlu, Y. (2021). of commercial integrated crop livestock systems: Current knowledge and Forage Seed Systems and Feed Reserves: Business Propositions, Case for Ethiopia. remaining uncertainty. Agric. Syst. 155, 136–146. Washington, DC: USAID. Gaviria-Uribe, X., Bolivar, D. M., Rosenstock, T. S., Molina-Botero, I. C., Dias, M., Costa, K., Severiano, E., Bilego, U., Neto, A., Almeida, D., et al. (2020). Chirinda, N., Barahona, R., et al. (2020). Nutritional quality, voluntary intake Brachiaria and Panicum maximum in an integrated crop-livestock system and and enteric methane emissions of diets based on novel Cayman grass and a second-crop maize system in succession with soybean. J. Agric. Sci. 158, its associations with two Leucaena shrub legumes. Front. Vet. Sci. 7:764. 206–217. doi: 10.1017/S0021859620000532 doi: 10.3389/fvets.2020.579189 Douxchamps, S., Frossard, E., Bernasconi, S. M., van der Hoek, R., Schmidt, A., Geng, Y., Hu, G., Ranjitkar, S., Wang, Y., Bu, D., Pei, S., et al. (2017). Prioritizing Rao, I. M., et al. (2011). Nitrogen recoveries from organic amendments in crop fodder species based on traditional knowledge: a case study of mithun (Bos and soil assessed by isotope techniques under tropical field conditions. Plant frontalis) in Dulongjiang area, Yunnan Province, Southwest China. J. Ethnobiol. Soil 341, 179–192. doi: 10.1007/s11104-010-0633-6 Ethnomed. 13, 1–15. doi: 10.1186/s13002-017-0153-z Douxchamps, S., Humbert, F., van der Hoek, R., Mena, M., Bernasconi, S. M., Giller, K. E., Hijbeek, R., Andersson, J. A., and Sumberg, J. (2021). Schmidt, A., et al. (2010). Nitrogen balances in farmers’ fields under alternative Regenerative agriculture: an agronomic perspective. Outlook Agric. 50, uses of a cover crop legume - a case study from Nicaragua. Nutr. Cycl. 13-25. doi: 10.1177/0030727021998063 Agroecosyst. 88, 447–462. doi: 10.1007/s10705-010-9368-2 Giraldo, C., Escobar, F., Chara, J. D., and Calle, Z. (2011). The adoption of Douxchamps, S., Rao, I. M., Peters, M., van der Hoek, R., Schmidt, A., Martens, silvopastoral systems promotes the recovery of ecological processes regulated S., et al. (2014). Farm-scale trade-offs between legume use as forage vs. green by dung beetles in the Colombian Andes. Insect Conserv. Divers. 4, 115–122. manure: the case of Canavalia brasiliensis. Agroecol. Sustain. Food Syst. 38, doi: 10.1111/j.1752-4598.2010.00112.x 25–45. doi: 10.1080/21683565.2013.828667 Gliessman, S. (2018). Defining agroecology. Agroecol. Sustain. Food Syst. 42, Du, Y., Ge, Y., Ren, Y., Fan, X., Pan, K., Lin, L., et al. (2018). A global strategy 599–600. doi: 10.1080/21683565.2018.1432329 to mitigate the environmental impact of China’s ruminant consumption boom. Godde, C. M., Mason-D’Croz, D., Mayberry, D. E., Thornton, P. K., and Nat Commun. 9:4133. doi: 10.1038/s41467-018-06381-0 Herrero, M. (2021). Impacts of climate change on the livestock food Dumont, E. S., Bonhomme, S., Pagella, T. F., and Sinclair, F. L. (2019). Structured supply chain; a review of the evidence. Glob. Food Security 28:100488. stakeholder engagement leads to development of more diverse and inclusive doi: 10.1016/j.gfs.2020.100488 agroforestry options. Exp. Agric. 55, 252–274. doi: 10.1017/S0014479716000788 Gontijo de Lima, F., Lee, S. T., Pfister, J. A., Sayuri Miyagi, E., Lage Costa, G., Elbasha, E., Thornton, P. K., and Tarawali, G. (1999). An Ex-post Economic Dias da Silva, R., et al. (2015). The effect of ensiling and haymaking on the Assessment of Planted Forages in West Africa. Nairobi: International Livestock concentrations of steroidal saponin in two Brachiaria grass species.Cienc. Rural Research Institute. 45, 858-863. doi: 10.1590/0103-8478cr20141305 Frontiers in Sustainable Food Systems | www.frontiersin.org 1145 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology González, J. M. (2013). Costos y beneficios de un sistema silvopastoril intensivo Jin, S., Zhang, B., Wu, B., Han, D., Hu, Y., Ren, C., et al. (2020). Decoupling (SSPi), con base en Leucaena leucocephala (Estudio de caso en el municipio livestock and crop production at the household level in China. Nat. Sustain. de Tepalcatepec, Michoacán, México). Avances En Investigación Agropecuaria 4, 48–55. doi: 10.1038/s41893-020-00596-0 17, 35–50. Jones, A. K., Jones, D. L., Edwards-Jones, G., and Cross, P. (2013). Informing Graesser, J., Aide,. M. T., Grau, R. H., and Ramankutty, N. (2015). decision making in agricultural greenhouse gas mitigation policy: a Best-Worst Cropland/pastureland dynamics and the slowdown of deforestation in Latin Scaling survey of expert and farmer opinion in the sheep industry. Environ. Sci. America. Environ. Res. Lett. 10:034017. doi: 10.1088/1748-9326/10/3/034017 Policy 29, 46–56. doi: 10.1016/j.envsci.2013.02.003 Groot, J. C. J., Oomen, G. J. M., and Rossing, W. A. H. (2012). Multi-objective Kaimowitz, D., and Angelsen, A. (2008). Will livestock intensification optimization and design of farming systems. Agric. Syst. 110, 63–77. help save Latin America’s tropical forests? J. Sustain. Forestry 27, 6–24. Gupta, S. (2016). Brain food: clever eating. Nature 531, S12–S13. doi: 10.1080/10549810802225168 doi: 10.1038/531S12a Khan, Z. R., Midega, C. A., Amudavi, D. M., Hassanali, A., and Pickett, J. A. (2008). Harrison, S., Srisomporn, W., and Nakamanee, G. (2019). Production of Leucaena On-farm evaluation of the ‘push-pull’ technology for the control of stemborers leucocephala ‘silage’ for sale as animal feed: a case study from Sikiew and striga weed on maize in western Kenya. Field Crops Res. 106, 224–233. District, Northeast Thailand. Trop. Grasslands Forrajes Tropicales 7, 455–458. doi: 10.1016/j.fcr.2007.12.002 doi: 10.17138/tgft(7)455-458 Labarta, R., Martínez, J. M., Yaccelga, A., Reyes, B., Gómez, L., Maredia, M., et al. Harvey, C. A., Medina, A., Sánchez Merlo, D., Vĺchez, S., Hernández, B., Saenz, J., (2017). Assessing the Adoption and Economic and Environmental Impacts of et al. (2006). Patterns of animal diversity associated with different forms of tree Brachiaria Grass Forage Cultivars in Latin America Focusing in the Experience cover retained in agricultural landscapes. Ecol. Appl. 16, 1986-1999. of Latin America. Research Report to the Standing Panel of Impact Assessment Hassan, S., Inglese, P., Gristina, L., Liguori, G., Novara, A., Louhaichi, M., (SPIA) under the SIAC project. Cali. et al. (2019). Root growth and soil carbon turnover in Opuntia ficus- Lamine, C., and Dawson, J. (2018). The agroecology of food systems: Reconnecting indica as affected by soil volume availability. Eur. J. Agron. 105, 104–110 agriculture, food, and the environment. Agroecol. Sustain. Food Syst. 42, doi: 10.1016/j.eja.2019.02.012 629–636. doi: 10.1080/21683565.2018.1432517 Havlík, P., Valin, H., Mosnier, A., Obersteiner, M., Baker, J. S., Herrero, M., et al. Lascano, C. E., Peters, M., and Holmann, F. (2005). Arachis pintoi in the humid (2012). Crop productivity and the global livestock sector: implications for land tropics of Colombia: a forage legume success story. Trop. Grasslands 39:220. use change and greenhouse gas emissions. Am. J. Agric. Econ. 95, 442–448. Le Coq, J., Sabourin, E., Bonin, M., Gresh, S., Marzin, J., Niederle, P., et al. doi: 10.1093/ajae/aas085 (2020). Public policy support for agroecology in Latin America: lessons and Heinke, J., Lannerstad, M., Gerten, D., Havlík, P., Herrero, M., Notenbaert, A. perspectives. Glob. J. Ecol. 129–138. doi: 10.17352/gje.000032 M. O., et al. (2020). Water use in global livestock production-opportunities Lema, Z., de Bruyn, L. A. L., Marshall, G. R., Roschinsky, R., and and constraints for increasing water productivity. Water Resour. Res. 56:12. Duncan, A. J. (2021). Multilevel innovation platforms for development of doi: 10.1029/2019WR026995 smallholder livestock systems: how effective are they? Agric. Syst. 189:103047. Herrero, M., Thornton, P. K., Notenbaert, A. M., Wood, S., Msangi, S., doi: 10.1016/j.agsy.2020.103047 Freeman, H. A., et al. (2010). Smart investments in sustainable food Lerner, A., Rudel, T. K., Schneider, L., McGroddy, M., Burbano, D., and Mena, production: revisiting mixed crop-livestock systems. Science 327, 822–825. C. (2015). The spontaneous emergence of silvo-pastoral landscapes in the doi: 10.1126/science.1183725 Ecuadorian amazon: patterns and processes. Reg. Environ. Change 15, 357–371. Hidano, A., Gates, M. C., and Enticott, G. (2019). Farmers’ decision doi: 10.1007/s10113-014-0699-4 making on livestock trading practices: cowshed culture and behavioral Lie, H., Rich, K. M., and Burkart, S. (2017). Participatory system dynamics triggers amongst New Zealand Dairy Farmers. Front. Vet. Sci. 7:130. modelling for dairy value chain development in Nicaragua. Dev. Pract. 27, doi: 10.3389/fvets.2019.00320 785–800. doi: 10.1080/09614524.2017.1343800 Hilbeck, A., Hoffmann, U., Home, R., Levidow, L., Muller, A., Nelson, E., et al. Lie, H., Rich, K. M., van der Hoek, R., and Dizyee, K. (2018). An empirical (2015). Feeding the People - Agroecology for Nourishing the World and Feeding evaluation of policy options for inclusive dairy value chain development the Agri-Food System. IFOAM EU, 2015. Available online at: https://www. in Nicaragua: a system dynamics approach. Agric. Syst. 164, 193–222. ifoameu.org/sites/default/files/ifoameu_policy_ffe_feedingthepeople.pdf doi: 10.1016/j.agsy.2018.03.008 Hoffmann, V., Paul, B., Falade, T., Ramankutty, N., Moodley, A., Olawoye, Lira M. A. Jr., Fracetto, F. J. C., Ferreira, J. D. S., Silva, M. B., and Fracetto, G. G. J., et al. (in review). A one health approach to plant health. Submitted to M. (2020). Legume silvopastoral systems enhance soil organic matter quality food policy. in a subhumid tropical environment. Soil Sci. Society of America Journal 84, Hoste, H., Martinez-Ortiz-De-Montellano, C., Manolaraki, F., Brunet, S., Ojeda- 1209–1218. doi: 10.1002/saj2.20106 Robertos, N., Fourquaux, I., et al. (2012). Direct and indirect effects of bioactive Louhaichi,M., Kumar, S., Tiwari, S., Islam,M., Hassan, S., Yadav, O. P., et al. (2018). tannin-rich tropical and temperate legumes against nematode infections. Vet. Adoption and utilization of Cactus Pear in South Asia-Smallholder farmers’ Parasitol. 186, 18–27. doi: 10.1016/j.vetpar.2011.11.042 perceptions. Sustainability 10:3625. doi: 10.3390/su10103625 IFOAM EU (2019). Position Paper on Agro-Ecology. Available online at: https:// Lowder, S. K., Sánchez, M. V., and Bertini, R. (2021). Which farms feed the www.organicseurope.bio/content/uploads/2020/06/ifoameu_position_paper_ world and has farmland become more concentrated? World Dev. 142:105455. agroecology.pdf?dd doi: 10.1016/j.worlddev.2021.105455 Inglese, P., Mondragon, C., Nefzaoui, A., and Saenz, C. (2018). Crop Ecology, Lukuyu, B., Baker, D., Baltenweck, I., Poole, J., Kabi, F., Katongole, C., Cultivation and Uses of Cactus Pear. Food and Agriculture Organization of the et al. (2013). The Concentrate Feeds Supply Chain in Uganda: Emerging United Nations and the International Center for Agricultural Research in the Trends and Implications on Quality and Access to Smallholder Farmers and Dry Areas. Rome. Chain Efficiency. Heifer International and East Africa Dairy Development. ISPC (2018). Tropical Forages and the Diffusion of Brachiaria Cultivars in Latin Available online at: https://cgspace.cgiar.org/bitstream/handle/10568/34469/ America. Rome: CGIAR Independent Science and Partnership Council. Concentrate%20Feeds%20Supply%20chain%20in%20Uganda.pdf?sequence=1 Jank, L., Barrios, S. C., Valle, C. B., Simeaio, R. M., and Alves, G. F. (2014). The Lukuyu, B., Mutambo, I., and Ouma, E. (2020). Gender Dynamics and Social value of improved pastures to Brazilian beef production. Crop Past. Sci. 65, Implications of Improved Planted Forages in Smallholder Piggery Systems 1132–1137. doi: 10.1071/CP13319 in Uganda. Nairobi: ILRI. Available online at: https://hdl.handle.net/10568/ Jimenez-Trujillo, J. A., Ibrahim, M., Pezo, D., Guevara-Hernandez, F., 108297 Gomez-Castro, H., Nahed-Toral, J., et al. (2011). Comparison of animal Lukuyu, B., Mutambo, I., and Ouma, E. (2021). Gender Dynamics and Social productivity and profitability between a silvopastoral system (Brachiaria Implications of Improved Planted Forages in Smallholder Dairy Systems in brizantha associated with Leucaena leucocephala) and a conventional Kenya. Nairobi: ILRI. Available online at: https://hdl.handle.net/10568/113636 system (B. brizantha + chicken manure). Res. J. Biol. Sci. 6, 75–81. Maass, B. L., Midega, C. A. O., Mutimura, M., Rahetlah, V. B., Salgado, P., doi: 10.3923/rjbsci.2011.75.81 Kabirizi, J. M., et al. (2015). Homecoming of Brachiaria: improved hybrids Frontiers in Sustainable Food Systems | www.frontiersin.org 1156 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology prove useful for African animal agriculture. East Afr. Agric. Forest. J. 81, 71–78. Njuguna-Mungai et al. (under review). Gender dynamics surrounding the doi: 10.1080/00128325.2015.1041263 introduction of improved forages in Kenya and Ethiopia. Mangwe, M. C., Bryant, R. H., Beck, M. R., Beale, N., Bunt, C., and Gregorini, Ntakyo, R. P., Kirunda, H., Tugume, G., and Natuha, S. (2020). Dry season feeding P. (2019). Forage herbs as an alternative to ryegrass-white clover to alter technologies: assessing the nutritional and economic benefits of feeding hay and urination patterns in grazing dairy systems. Anim. Feed Sci. Technol. 252, silage to dairy cattle in South-Western Uganda. Open J. Anim. Sci. 10, 627-648. 11–22. doi: 10.1016/j.anifeedsci.2019.04.001 doi: 10.4236/ojas.2020.103041 Marra, M., Pannell, D. J., and Abadi Ghadim, A. (2003). The economics Nwafor, I. C., Shale, K., and Achilonu, M. C. (2017). Chemical composition and of risk, uncertainty and learning in the adoption of new agricultural nutritive benefits of chicory (Cichorium intybus) as an ideal complementary technologies: where are we on the learning curve? Agric. Syst. 75, 215–234. and/or alternative livestock feed supplement. ScientificWorldJournal doi: 10.1016/S0308-521X(02)00066-5 2017:7343928. doi: 10.1155/2017/7343928 Martinez, L. J., and Zinck, J. A. (2004). Temporal variation of soil compaction Nyambati, E. M., Sollenberger, L. E., Hiebsch, C. K., and Rono, S. C. (2006). and deterioration of soil quality in pasture areas of Colombian Amazonia. Soil On-farm productivity of relay-cropped mucuna and lablab in smallholder Tillage Res. 75, 3–18. doi: 10.1016/j.still.2002.12.001 crop-livestock systems in northwestern Kenya. J. Sustain. Agric. 28, 97–116. Martínez-García, C. G., Dorward, P., and Rehman, T. (2013). Factors doi: 10.1300/J064v28n01_09 influencing adoption of improved grassland management by small-scale Ohmstedt, U. (2020a). Forage Growing and on Farm Feeding of the Produced dairy farmers in central Mexico and the implications for future research on Forages: A Business Case. Nairobi: Alliance of Bioversity International smallholder adoption in developing countries. Livestock Sci. 152, 228–238. and CIAT. doi: 10.1016/j.livsci.2012.10.007 Ohmstedt, U. (2020b). Factsheets on Forage-Related Business Approaches for Kenya. Mayberry, D., Hau, D. K., Dida, P. R., Bria, D., Praing, J., Mata, A. D., Nairobi: Alliance of Bioversity International and CIAT. et al. (2020). Herbaceous legumes provide several options for increasing Olaya-Montes, A., Llanos-Cabrera, M. P., Cherubin, M. R., Herrera-Valencia, W., beef cattle productivity in eastern Indonesia. Anim. Product. Sci. 61 698–707 Ortiz-Morea, F. A., and Silva-Olaya, A. M. (2020). Restoring soil carbon and doi: 10.1071/AN20545 chemical properties through silvopastoral adoption in the Colombian Amazon Mayer, J. A., and Cushman, J. C. (2019). Nutritional and mineral content of prickly region. Land Degrad. Dev. 32, 3720–3730. doi: 10.1002/ldr.3832 pear cactus: a highly water-use efficient forage, fodder and food species. J. Oulu, M., and Notenbaert, A. (2020). Adoption of Improved Forages in Western Agron. Crop Sci. 205, 625–634. doi: 10.1111/jac.12353 Kenya: Key Underlying Factors. [Presentation done November 24, 2020]. 46 Méndez, V. E., Bacon, C. M., and Cohen, R. (2013). Agroecology as slides. Available online at: https://hdl.handle.net/10568/110543 a transdisciplinary, participatory, and action-oriented approach. Agroecol. Paul, B. K., Butterbach-Bahl, K., Notenbaert, A., Nderi, A. N., and Ericksen, P. Sustain. Food Syst. 37, 3–18. (2020a). Sustainable livestock development in low andmiddle income countries Meybeck, A., andGitz, V. (2017). Sustainable diets within sustainable food systems. - shedding light on evidence-based solutions. Environ. Res. Lett. 16:011001. Proc. Nutr. Soc. 76, 1–11. doi: 10.1017/S0029665116000653 doi: 10.1088/1748-9326/abc278 Meyfroidt, P. (2018). Trade offs between environment and livelihoods: bridging Paul, B. K., Groot, J. C., Maass, B. L., Notenbaert, A.M., Herrero, M., and Tittonell, the global land use and food security discussions. Glob. Food Security 16, 9–16. P. A. (2020c). Improved feeding and forages at a crossroads: farming systems doi: 10.1016/j.gfs.2017.08.001 approaches for sustainable livestock development in East Africa.Outlook Agric. Montoya-Flores, M. D., Molina-Botero, I. C., Arango, J., Romano-Muñoz, J. 49, 13-20. doi: 10.1177/2F0030727020906170 L., Solorio-Sánchez, F. J., Aguilar-Pérez, C. F., et al. (2020). Effect of dried Paul, B. K., Groot, J. C. J., Birnholz, C. A., Nzogela, B., Notenbaert, A., Woyessa, leaves of Leucaena leucocephala on rumen fermentation, rumen microbial K., et al. (2019). Reducing agro-environmental trade-offs through sustainable population, and enteric methane production in crossbred heifers. Animals livestock intensification across smallholder systems in Northern Tanzania. Int. 10:300. doi: 10.3390/ani10020300 J. Agric. Sustain. 18, 1–20. doi: 10.1080/14735903.2019.1695348 Mottet, A., Bicksler, A., Lucantoni, D., De Rosa, F., Scherf, B., Scopel, E., et al. Paul, B. K., Maass, B., Koge, J., Notenbaert, A., Peters, M., Groot, J. (2020). Assessing transitions to sustainable agricultural and food systems: a G. J., et al. (2020b). Tropical forage technologies can deliver multiple tool for agroecology performance evaluation (TAPE). Front. Sustain. Food Syst. benefits in Sub-Sahara Africa: a meta-analysis. Agron. Sustain. Dev. 40:22. 4:579154. doi: 10.3389/fsufs.2020.579154 doi: 10.1007/s13593-020-00626-3 Mueller, N. D., and Lassaletta, L. (2020). Nitrogen challenges in global livestock Peters, M., Herrero, M., Fisher, M., Erb, K.-H., Rao, I., Subbarao, G. V.,et al. (2013). systems. Nature Food. 1, 400–401. doi: 10.1038/s43016-020-0117-7 Challenges and opportunities for improving eco-efficiency of tropical forage- Murgueitio, E., Barahona, R., Chará, J. D., Flores, M. X., Mauricio, R. M., and based systems to mitigate greenhouse gas emissions. Trop. Grasslands Forrajes Molina, J. J. (2015). The intensive silvopastoral systems in Latin America Trop. 1, 137–148. doi: 10.17138/TGFT(1)156-167 sustainable alternative to face climatic change in animal husbandry. Cuban J. Peters, M., Horne, P., Schmidt, A., Holmann, F., Kerridge, P. C., Tarawali, S. A., Agric. Sci. 49, 541–554. et al. (2001).The Role of Forages in Reducing Poverty and Degradation of Natural Mwendia, S., Ohmstedt, U., and Peters, M. (2019). “Make money from forage hay Resources in Tropical Production Systems. Agricultural Research and Extension production as a business” in Poster prepared for the Maziwa Zaidi Agribusiness Network. Available online at: https://cdn.odi.org/media/documents/5218.pdf Forum, Moshi, Tanzania (Cali: CIAT). Available online at: https://hdl.handle. Peters, M., and Lascano, C. E. (2003). Forage technology adoption: linking on- net/10568/105484 station research with participatory methods. Trop. Grasslands 37, 197–204. Nakamanee, G., Srisomporn,W., Phengsavanh, P., Samson, J., and Stür, W. (2008). Peters, M., Rao, I., Fisher, M., Subbarao, G., Martens, S., Herrero, M., et al. (2012). Sale of fresh forage - a new cash crop for smallholder farmers in Yasothon, “Tropical forage-based systems to mitigate greenhouse gas emissions,” in CIAT. Thailand. Trop. Grasslands 42, 65–74. 2012. Eco-Efficiency: From Vision to Reality - Issues in Tropical Agriculture Nefzaoui, A., Louhaichi, M., and Ben Salem, H. (2014). Cactus as a tool to mitigate (Cali: CIAT). drought and to combat desertification. J. Arid Land Stud. 24, 121–124. Peterson, C. A., Deiss, L., and Gaudin, A. C. M. (2020). Integrated crop-livestock Negassa, A., Shapiro, B., Kidane, T., Abdena, A., and Hanson, J. (2016). Ex-Ante systems achieve comparable crop yields to specialized systems: a meta analysis. Assessment of Demand for Improved Forage Seed and Planting Materials Among PLoS ONE 15:e0231840. doi: 10.1371/journal.pone.0231840 Ethiopian Smallholder Farmers: A Contingent Valuation Analysis. ILRI Project Pezo, D., and Cruz, J., Piniero, M. (2007). Escuelas de Campo para Ganaderos: Report. Nairobi: ILRI. Available online at: https://hdl.handle.net/10568/78657 Una estrategia para la rehabilitación y diversificación de fincas con pasturas Neres, M. A., Nath, C. D., and Hoppen, S. M. (2021). Expansion of hay production degradadas. Archivos ALPA 15(Suppl. 1), 42–48. and marketing in Brazil. Heliyon 7:E06787. doi: 10.1016/j.heliyon.2021.e06787 Pezo, D., Ríos, N., Ibrahim, M., and Gómez, M. (2018). Silvopastoral Systems for Njeru, N. K., Midega, C. A. O., Muthomi, J. W., Wagacha, J. M., and Khan, Intensifying Cattle Production and Enhancing Forest Cover: The Case of Costa Z. R. (2020). Impact of push-pull cropping system on pest management and Rica. Washington, DC: World Bank. occurrence of ear rots and mycotoxin contamination of maize in western Pulido, F., García, E., Obrador, J. J., and Moreno, G. (2010). Multiple pathways Kenya. Plant Pathol. 69, 1644-1654. doi: 10.1111/ppa.13259 for tree regeneration in anthropogenic savannas: incorporating biotic and Frontiers in Sustainable Food Systems | www.frontiersin.org 1167 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology abiotic drivers into management schemes. J. Appl. Ecol. 47, 1272–1281. Seré, C., and Estrada, R. (1982). “Análisis económico de sistemas de ceba en pastos doi: 10.1111/j.1365-2664.2010.01865.x mejorados en los Llanos Orientales de Colombia,” in Referencias y ayudas Rao, I., Peters, M., Castro, A., Schultze-Kraft, R.,White, D., Fisher, M., et al. (2015). utilizadas en el programa de capacitación científica en investigación para la LivestockPlus - the sustainable intensification of forage-based agricultural producción y utilización de pastos tropicales, ed J. M. Spain (Cali, Colombia: systems to improve livelihoods and ecosystem services in the tropics. Trop. Centro Internacional de Agricultura Tropical), 1063–1075. Grassl. Forrajes Trop. 3, 59–82. doi: 10.17138/TGFT(3)59-82 Seré, C., Estrada, R., and Ferguson, J. (1993). Estudios de adopción e impacto en Rietveld, A. M., Groot, J. C. J., and van der Burg, M. (2021). Predictable pasturas tropicales, investigación con pasturas en fincas. Centro Internacional patterns of unsustainable intensification. Int. J. Agric. Sustain. 1–17. de Agricultura Tropical (CIAT), Cali. Available online at: https://hdl.handle. doi: 10.1080/14735903.2021.1940731 net/10568/55753 Ríos, N., Cárdenas, A. Y., Andrade, H. J., Ibrahim, M., Jiménez, F., Sancho, Shapiro, M. J., Downs, S. M., Swartz, H. J., Parker, M., Quelhas, D., F., et al. (2006). Escorrentía superficial e infiltración en sistemas ganaderos Kreis, K., et al. (2019). A systematic review investigating the relation convencionales y silvopastoriles en el trópico sub-húmedo de Nicaragua y between animal-source food consumption and stunting in children aged 6- Costa Rica. Agroforestería en las Américas 45, 66–71. 60 months in low-and middle-income countries. Adv. Nutr. 10, 827–847. Rivas, L., and Holmann, F. (2000). Early Adoption of Arachis Pintoi in the Humid doi: 10.1093/advances/nmz018 Tropics: The Case of Dual-Purpose Livestock Systems in Caquetá, Colombia. Shelton M., and Dalzell, S. (2007). Production, economic and environmental Livestock Research for Rural Development. Available online at: http://www. benefits of leucaena pastures. Trop. Grasslands 41, 174–190. lrrd.org/lrrd12/3/riva123.htm Silva, J. A., de Paula Sousa, D., de Paula, N. F., da Silva Carvalho, A. P., Gomes Rivas, L., and Holmann, F. (2004a). Impacto económico potencial de la adopción Macedo, B., da Costa Júnior, W. S., et al. (2017). Supplementation strategies de nuevas Brachiarias resistentes a cercópidos. Pasturas Tropicales 26, 39–55. for dairy cows kept in tropical grass pastures. Semina Ciências Agrárias 38, Rivas, L., and Holmann, F. (2004b). Impacto de la Adopción de Híbridos de 401–416. doi: 10.5433/1679-0359.2017v38n1p401 Brachiarias Resistentes al Salivazo: Colombia, México, y Centroamérica. Cali: Smith, J., Cadavid, J. V., Rincón, A., and Vera, R. (1997). Land speculation and Centro Internacional de Agricultura Tropical (CIAT). intensification at the Frontier: a seeming paradox in the Colombian Savanna. Rivera, L. F., Armbrecht, I., and Calle, Z. (2013). Silvopastoral systems and Agric. Syst. 54, 501–520. doi: 10.1016/S0308-521X(96)00088-1 ant diversity conservation in a cattle-dominated landscape of the Colombian Snijders, P. J. M., Wouters, B. P., and Kariuki, J. N. (2011). Effect of Cutting Andes. Agric. Ecosyst. Environ. 181, 188–194. doi: 10.1016/j.agee.2013. Management and Nitrogen Supply on Yield and Quality of Napier grass 09.011 (Pennisetum purpureum). Wageningen UR Livestock Research. Available Robinson, T. P., Thornton, P. K., Franceschini, G., Kruska, R. L., Chiozza, F., online at: https://www.wur.nl/en/Publication-details.htm?publicationId= Notenbaert, A., et al. (2011). Global Livestock Production Systems. Rome: Food publication-way-343137363539 and Agriculture Organization of the United Nations (FAO) and International Sordillo, L. M. (2016). Nutritional strategies to optimize dairy cattle immunity. J. Livestock Research Institute (ILRI). Dairy Sci.99, 4967–4982. doi: 10.3168/jds.2015-10354 Rocha Filho, R. R., Santos, D. C., Véras, A. S. C., Siqueira, M. C. B., Sousa, L. F., Maurício, R. M., Paciullo, D. S. C., Silveira, S. R., Ribeiro, R. Novaes, L. P., Mora-Luna, R., et al. (2021). Can spineless forage cactus be S., Calsavara, L. H., et al. (2015). Forage intake, feeding behavior and the queen of forage crops in dryland areas? J. Arid Environ. 186:104426. bio-climatological indices of pasture grass, under the influence of trees, doi: 10.1016/j.jaridenv.2020.104426 in a silvopastoral system. Trop. Grasslands Forrajes Tropicales 3, 129–141. Rossi Borges, J. A., and Oude Lansink, A. G. J. M. (2016). Identifying psychological doi: 10.17138/TGFT(3)129-141 factors that determine cattle farmers’ intention to use improved natural Soussana J.-F., Muriel, T., Philippe, L., and Bertrand, D. (2015). Agroecology: grassland. J. Environ. Psychol. 45, 89–96. doi: 10.1016/j.jenvp.2015.12.001 integration with livestock. In: International Symposium on Agroecology for Food Rudel, T. K., Paul, B., White, D., Rao, I. M., Van Der Hoek, R., Castro, A., et al. Security and Nutrition (Rome: FAO), 225-249. Available online at: http://www. (2015). LivestockPlus: forages, sustainable intensification, and food security in fao.org/3/a-i4729e.pdf the tropics. Ambio 44, 685–693. doi: 10.1007/s13280-015-0676-2 Subbarao, G. V., Nakahara, K., Hurtado, M. D. P., Ono, H., Moreta, D. E., Ruden, A., Castro, J. P., Gutiérrez, J. F., Koenig, S., and Arango, J. (2020). GANSO: Salcedo, A. F., et al. (2009). Evidence for biological nitrification inhibition New Business Model and Technical Assistance for the Professionalization of in Brachiaria pastures. Proc. Natl. Acad. Sci. U.S.A. 106, 17302–17307. Sustainable Livestock Farming in the Colombian Orinoquia region. CCAFS Info doi: 10.1073/pnas.0903694106 Note. Cali: CGIAR Research Program on Climate Change, Agriculture and Tapasco, J., LeCoq, J. F., Ruden, A., Rivas, J. S., and Ortiz, J. (2019). The Food Security (CCAFS). livestock sector in Colombia: toward a program to facilitate large-scale Ruiz, L. R., Burkart, S., Muñoz Quiceno, J. J., Enciso, K., Gutierrez Solis, J. adoption of mitigation and adaptation practices. Front. Sustain. Food Syst. 3:61. F., Charry, A., et al. (2016). “Inhibiting factors and promotion strategies doi: 10.3389/fsufs.2019.00061 for increasing adoption levels of improved forages in cattle production,” in Trujillo-Barrera, A., Pennings, J. M. E., and Hofenk, D. (2016). Understanding Tropentag 2016 “Solidarity in a Competing World Fair Use of Resources” producers’ motives for adopting sustainable practices: the role of expected (Vienna: Centro Internacional de Agricultura Tropical). Available online at: rewards, risk perception and risk tolerance. Eur. Rev. Agric. Econ. 43, 359–382. https://hdl.handle.net/10568/77030 (accessed August 28, 2019). doi: 10.1093/erae/jbv038 Sacande, M., and Berrahmouni, N. (2016). Community participation and Umunezero, O., Mwendia, S., Paul, B. K., et al. (2016). Identifying and ecological criteria for selecting species and restoring natural capital with native Characterizing Areas for Potential Forage Production in Rwanda. Cali: species in the Sahel: restoring natural capital in the Sahel. Restor. Ecol. 24, International Center for Tropical Agriculture (CIAT). 479–488 doi: 10.1111/rec.12337 Valentim, J. F., and Andrade, C. M. S. (2005). Forage peanut (Arachis pintoi): a Sanderman, J., Heng, T., and Fiske, G. J. (2017). Soil carbon debt of 12,000 high yielding and high-quality tropical legume for sustainable cattle production years of human land use. Proc. Natl Acad. Sci. U.S.A. 114, 9575–9580. systems in the western Brazilian Amazon. Trop. Grasslands 39:222. doi: 10.1073/pnas.1706103114 Valette, M., et al. (2019). How diverse is tree planting in the Central Plateau Schiek, B., González, C., Mwendia, S., and Prager, S. D. (2018). Got forages? of Burkina Faso? Comparing small-scale restoration with other planting Understanding potential returns on investment in Brachiaria spp. for dairy initiatives. Forests 10.3:227. doi: 10.3390/f10030227 producers in Eastern Africa. Trop. Grasslands Forrajes Tropicales 6, 117–133. van Winsen, F., de Mey, Y., Lauwers, L., Van Passel, S., Vancauteren, M., and doi: 10.17138/tgft(6)117-133 Wauters, E. (2014). Determinants of risk behaviour: effects of perceived risks Schultze-Kraft, R., Rao, I. M., Peters, M., Clements, R. J., Bai, C., and Liu, G. (2018). and risk attitude on farmer’s adoption of risk management strategies. J. Risk Tropical forage legumes for environmental benefits: an overview. Trop. Grassl. Res. 19, 56–78. doi: 10.1080/13669877.2014.940597 Forrajes Trop. 6, 1–14. doi: 10.17138/TGFT(6)1-14 Vazquez, E., Teutscherova, N., Lojka, B., Arango, J., and Pulleman, M. (2020). Seddon, N., Smith, A., Smith, P., Key, I., Chausson, A., Girardin, C., et al. (2021). Pasture diversification affects soil macrofauna and soil biophysical properties Getting the message right on nature-based solutions to climate change. Glob. in tropical (silvo) pastoral systems. Agric. Ecosyst. Environ. 302:107083. Change Biol. 27, 1518-1546. doi: 10.1111/gcb.15513 doi: 10.1016/j.agee.2020.107083 Frontiers in Sustainable Food Systems | www.frontiersin.org 1178 November 2021 | Volume 5 | Article 742842 Notenbaert et al. Improved Forages and Agroecology Villegas, D. M., Velasquez, J., Arango, J., Obregon, K., Rao, I. M., Rosas, G., Zahoor, N., Abdullah, N., and Zakaria, N. (2021). The role of high performance et al. (2020). Urochloa grasses swap nitrogen source when grown in association work practices, work-family conflict, job stress and personality in affecting with legumes in tropical pastures. Diversity 12:419. doi: 10.3390/d121 work life balance.Manage. Sci. Lett. 11, 1367-1378. 10419 Zhang, X., Fang, Q., Zhang, T., Ma, W., Velthof, G. L., Hou, Y., et al. (2020). Vinceti, B., et al. (2020). How is forest landscape restoration being implemented Benefits and trade-offs of replacing synthetic fertilizers by animal manures in in Burkina Faso? Overview of ongoing initiatives. Sustainability 12:10430. crop production in China: a meta-analysis. Global Change Biol. 26, 888–900 doi: 10.3390/su122410430 doi: 10.1111/gcb.14826 Wan, N.-F., Zheng, X.-R., Fu, L.-W., Kiær, L. P., Zhang, Z., Chaplin- Zhao, C., Liu, B., Piao, S., Wang, X., Lobell, D. B., Huang, Y., et al. Kramer, R., et al. (2020). Global synthesis of effects of plant species (2017). Temperature increase reduces global yields of major crops in diversity on trophic groups and interactions. Nat Plants 6, 503–510. four independent estimates. Proc. Natl. Acad. Sci. U.S.A. 114, 9326-9331. doi: 10.1038/s41477-020-0654-y doi: 10.1073/pnas.1701762114 Wezel, A., Herren, B. G., Kerr, R. B., Barrios, E., Rodrigues, A. L., and Sinclair, F. (2020). Agroecological principles and elements and their implications for Conflict of Interest: The authors declare that the research was conducted in the transitioning to sustainable food systems. A review. Agron. Sustain. Dev. 40:40. absence of any commercial or financial relationships that could be construed as a doi: 10.1007/s13593-020-00646-z potential conflict of interest. White, D., Holmann, F., Fujisaki, S., Reategui, K., and Lascano, C. (2001). “Will intensifying pasture management in Latin America protect forests - Or is it the The handling editor is currently editing co-organizing a Research Topic other way around?,” in Agricultural Technologies and Tropical Deforestation, with several of the authors AN, SB, NC, MPe and confirms the absence of any eds A. Angelsen and D. Kaimowitz (Wallingford: CABI Publishing), 91–113. other collaboration. doi: 10.1079/9780851994512.0091 White, D., Peters, M., and Horne, P. (2013). Global impacts from improved Publisher’s Note: All claims expressed in this article are solely those of the authors tropical forages: a meta-analysis revealing overlooked benefits and costs, and do not necessarily represent those of their affiliated organizations, or those of evolving values and new priorities. Trop. Grasslands Forrajes Tropicales 1, the publisher, the editors and the reviewers. Any product that may be evaluated in 12–24. doi: 10.17138/TGFT(1)12-24 this article, or claim that may be made by its manufacturer, is not guaranteed or Willett, W., Rockström, J., Loken, B., Springmann, M., Lang, T., Vermeulen, S., et al. (2019). Food in the anthropocene: the EAT-Lancet Commission on endorsed by the publisher. healthy diets from sustainable food systems. Lancet Commissions 393, 447–492. doi: 10.1016/S0140-6736(18)31788-4 Copyright © 2021 Notenbaert, Douxchamps, Villegas, Arango, Paul, Burkart, Winders, W., and Ransom, E. (2019). Global Meat: The Social and Environmental Rao, Kettle, Rudel, Vázquez, Teutscherova, Chirinda, Groot, Wironen, Pulleman, Implications of the Expanding Meat Industry. Cambridge, MA: MIT Press. Louhaichi, Hassan, Oberson, Nyawira, Pinares-Patino and Peters. This is an open- doi: 10.7551/mitpress/11868.001.0001 access article distributed under the terms of the Creative Commons Attribution Wunscher, T., Schultze-Kraft, R., Peters, M., and Rivas, L. (2004). Early adoption License (CC BY). The use, distribution or reproduction in other forums is permitted, of the tropical forage legume Arachis Pintoi in Huetar norte, Costa Rica. Exp. provided the original author(s) and the copyright owner(s) are credited and that the Agric. 40, 257–268. doi: 10.1017/S0014479703001583 original publication in this journal is cited, in accordance with accepted academic Xuan T. D., Elzaawely A. A., Deba F., Fukuta M., and Tawata S. (2006). Mimosine practice. No use, distribution or reproduction is permitted which does not comply in Leucaena as a potent bio-herbicide. Agron. Sustain. Dev. 26, 89-97. with these terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1189 November 2021 | Volume 5 | Article 742842 ORIGINAL RESEARCH published: 25 November 2021 doi: 10.3389/fsufs.2021.725774 Geographic Distribution of Colombian Spittlebugs (Hemiptera: Cercopidae) via Ecological Niche Modeling: A Prediction for the Main Tropical Forages’ Pest in the Neotropics Luis M. Hernández 1*, Paula Espitia 1, David Florian 2, Valheria Castiblanco 1, Juan Andrés Cardoso 1 and María I. Gómez-Jiménez 3 1 Tropical Forages Program, Alliance Bioversity International – CIAT, Cali, Colombia, 2 Semillas Papalotla S.A. de C.V., Mexico, Edited by: 3Nutrition and Health, Alliance Bioversity International – CIAT, Cali, Colombia Ngonidzashe Chirinda, Mohammed VI Polytechnic University, Morocco Spittlebugs (Hemiptera: Cercopidae) are the main tropical pests in Central and South Reviewed by: America of cultivated pastures. We aimed to estimate the potential distribution of Tiago Teixeira De Resende, Aeneolamia varia, A. lepidior, A. reducta, Prosapia simulans, Zulia carbonaria, and Z. Brazilian Agricultural Research Corporation (EMBRAPA), Brazil pubescens throughout the Neotropics using ecological niche modeling. These six insect David A Moo Llanes, species are common in Colombia and cause large economic losses. Records of these National Institute of Public species, prior to the year 2000, were compiled from human observations, specimens Health, Mexico Andressa Paladini, from CIAT Arthropod Reference Collection (CIATARC), Global Biodiversity Information Federal University of Santa Facility (GBIF), speciesLink (splink), and an extensive literature review. Different ecological Maria, Brazil niche models (ENMs) were generated for each species: Maximum Entropy (MaxEnt), *Correspondence: Luis M. Hernández generalized linear (GLM), multivariate adaptive regression spline (MARS), and random l.hernandez@cgiar.org forest model (RF). Bioclimatic datasets were obtained from WorldClim and the 19 available variables were used as predictors. Future changes in the potential geographical Specialty section: distribution were simulated in ENMs generated based on climate change projections for This article was submitted to Climate-Smart Food Systems, 2050 in two scenarios: optimistic and pessimistic. The results suggest that (i) Colombian a section of the journal spittlebugs impose an important threat to Urochloa production in different South Frontiers in Sustainable Food Systems American countries, (ii) each spittlebug species has a unique geographic distribution Received: 15 June 2021 Accepted: 26 October 2021 pattern, (iii) in the future the six species are likely to invade new geographic areas even in Published: 25 November 2021 an optimistic scenario, (iv) A. lepidior and A. reducta showed a higher number of suitable Citation: habitats across Colombia, Venezuela, Brazil, Peru, and Ecuador, where predicted risk is Hernández LM, Espitia P, Florian D, more severe. Our data will allow to (i) monitor the dispersion of these spittlebug species, Castiblanco V, Cardoso JA and Gómez-Jiménez MI (2021) (ii) design strategies for integrated spittlebug management that include resistant cultivars Geographic Distribution of Colombian adoption to mitigate potential economic damage, and (iii) implement regulatory actions Spittlebugs (Hemiptera: Cercopidae) via Ecological Niche Modeling: A to prevent their introduction and spread in geographic areas where the species are not Prediction for the Main Tropical yet found. Forages’ Pest in the Neotropics. Front. Sustain. Food Syst. 5:725774. Keywords: ecological niche modeling, climatic change, pest distribution, future risk, Aeneolamia, Zulia, Prosapia, doi: 10.3389/fsufs.2021.725774 Brachiaria Frontiers in Sustainable Food Systems | www.frontiersin.org 1120 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling INTRODUCTION for pest species in Europe, e.g., Helicoverpa zea (Lepidoptera: Noctuidae), Aleurocanthus spiniferus (Hemiptera: Aleyrodidae), In the neotropics wide areas are planted in grasses, being under climate change scenarios (Grünig et al., 2020). Thus, Urochloa spp. P. Beauv. (syn. Brachiaria spp.) the most extensive characterizing the effect of climate change in Colombian forage monoculture (Ghimire et al., 2015; Worthington et al., spittlebugs geographic distribution and identifying niches where 2021). Its economic impact is estimated at USD12.4 million these species would become key pests is important in the in Mexico, Central America, Colombia, and Brazil, the largest transition to more sustainable livestock systems. contribution comes from U. brizantha (Hochst. ex A. Rich.) R.D. In this context, ecological niche models (ENMs) provide an Webster cv.Marandu in Brazil with USD 6.3million (White et al., approximation to estimate potential geographical zones with 2013). The major biotic stress affecting forage production and environmental conditions that a species requires to maintain its quality in this region is caused by spittlebugs (Hemiptera: its populations (Peterson et al., 2011). This tool is widely used Cercopidae). A large group of species causes severe damage in insect pest management programs to anticipate unknown in susceptible grasslands (Cardona et al., 2004) with economic distributional areas, geographic potential of invasive species, and losses estimated at USD 840–2,100 million per year in all host response to changing environmental conditions (Peterson and crops (Thompson, 2004). Soberón, 2012). ENMs can be built based on occurrence data Although spittlebugs are found in most terrestrial ecosystems, (inductive or correlative niche models; Elith and Leathwick, the tropics are the most diverse ecozone harboring 70% of known 2009) or based on physiological data [deductive or mechanistic species (Thompson, 2004; Dietrich, 2009). In the Neotropics, niche models; (Kearney and Porter, 2009)]. For spittlebugs species are reported from the southeastern United States to associated with grasses, we identified only two studies focused on northern Argentina (Peck and Thompson, 2008). Different changes in suitability of geographical areas under climatic change spittlebug species coincide in each country. The main species scenarios. The first, based on physiological data of Mahanarva that occur in Brazil are from the genus Mahanarva (Distant, spectabilis (Distant) (Fonseca et al., 2016), and the second, based 1909),Notozulia (Berg, 1879) andDeois (Fennah, 1949) (Resende on occurrence data of four Mahanarva species (Schöbel and et al., 2012). In Mexico, the species Aeneolamia albofasciata Carvalho, 2020). (Lallemand, 1939), A. contigua (Walker, 1851), and A. postica This paper responds to the need to know whether A. (Walker, 1858) aremajor pests of sugarcane and grasses (Cardona varia, A. lepidior, A. reducta, P. simulans, Z. carbonaria, et al., 2004; Thompson and León González, 2005; Parada and Z. pubescens are potential key pests in new sites under Domínguez et al., 2019). Whereas in Colombia the predominant climate change scenarios that consider the impact of human species are A. varia (Fabricius, 1787), A. lepidior (Fowler, 1897), activities. Hence, spittlebug ENMs contribute to the development A. reducta (Lallemand, 1924), Prosapia simulans (Walker, 1858), of adaptation strategies for tropical America climate-smart Zulia carbonaria (Lallemand, 1924), and Z. pubescens (Fabricius, perennial grasslands, and sugarcane production, by addressing 1803) (Peck, 2001). the need for shift toward more sustainable pest management Climate change can modify the distribution of species by practices (Macfadyen et al., 2018). For instance, adoption expanding their presence to new locations and disappearing from of cultivars with host plant resistance incorporated in high previously suitable areas (Hughes, 2000). Anthropic movement, suitability predicted areas, or establishment of susceptible land-use change, environmental degradation (e.g., habitat loss crops in low suitability sites, within intensive livestock and and fragmentation) and biotic interactions (e.g., competition, agriculture systems. species introduction, and plant host distribution) produced by Our main objective was to determine the current distribution the on-going climate change are factors that influence this of these six species and estimate the potential distribution under distribution (Wagner et al., 2021). Insects are well-known two future climate scenarios via ecological niche methods based for being particularly susceptible to environmental changes of on presence-only data. temperature, humidity, radiation, and resource availability driven by those factors (Larson et al., 2019). Processes that homogenize MATERIALS AND METHODS and simplify the landscapes as extensive agriculture, allow the growth of pests over native species (Cardoso et al., 2020). Several Occurrence Data studies in recent years have warned about the decline of insect Information about occurrence records of A. lepidior, A. reducta, populations to extinction caused by changes in the seasonality A. varia, P. simulans, Z. carbonaria, and Z. pubescens were and, consequently, in their life cycles. This reduction in the collected from a variety of sources: (1) human observations, populations has great impact over the ecosystems as the loss of (2) CIAT’s Arthropod Reference Collection (CIATARC), (3) abundance and richness of species continue to occur (Hallmann websites Global Biodiversity Information Facility (GBIF.org., et al., 2017; Goulson, 2019; Halsch et al., 2021). 2020a,b,c,d,e) and speciesLink (https://splink.cria.org.br/), and Despite insect pest outbreaks are expected for the short term (4) from extensive scientific papers revision (Hamilton, 1977; (Heeb et al., 2019; Liu and Shi, 2020), its severity may not Avila de Moreno and Umaña, 1988; Peck, 1998; Sáenz et al., be evenly increased due to the narrow environmental niche 1999; Cardona et al., 2000; Peck et al., 2001; Rodríguez Chalarca requirements, physiological tolerances of insects, and differential et al., 2002; Rodriguez Chalarca et al., 2003; Ferrer et al., 2004; effects of climate variables on their life cycle (Lehmann et al., Castro et al., 2005; Castillo, 2006; Valbuena, 2010; Figueredo 2020). Previous models show an increase in suitable areas et al., 2012; Matabanchoy Solarte et al., 2012; de la Cruz-Zapata Frontiers in Sustainable Food Systems | www.frontiersin.org 121 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling et al., 2016; García-González et al., 2017; Paladini et al., 2018). Multivariate Adaptive Regression Spline (MARS), and Random Human observations data were obtained from CIAT historical Forest (RF) models. MaxEnt was used as default settings since records. These were captured by CIAT’S entomology department it has shown the ability to achieve good performance as a expert sampling in different locations. To georeference records default (Phillips and Dudík, 2008). Models are fitted with sdm from CIATARC without coordinates but with known location function using two replication techniques (subsampling and data, first, the geographic information available was verified and bootstrapping) establishing 70% of the occurrence data as corrected according to National Statistics Offices (e.g., DANE training data and 30% as test data. This process was repeated 3 to Colombia) and GeoNames (https://www.geonames.org/), times. As a result of our methodological procedure, a total of second, coordinates were obtained via GoogleMaps (https:// 24 different projections (4 models ∗ 2 replication techniques ∗ 3 www.google.com/maps). A cleansing process was performed to repetitions) were generated for each species. this first base, removing the duplicates (i.e., more than one occurrence record in 10 km2) and the records after the year 2000 Model Prediction and Ensemble to preserve the same temporal distribution between distribution We consider the accessible area of species under study as the data and climate data. entire neotropical ecoregion and that the species do not have restrictions since in this ecoregion there is a large pasture Climatic Data monoculture for livestock and it has a wide sugarcane planted Elevation layer and 19 bioclimatic layers (bio_1 to bio_19) area where cercopids can be established (Jank et al., 2014; Schöbel were obtained from Worldclim from 1970 to 2000 using and Carvalho, 2021). The hypothesis was that climate change will raster::getData function. For the current climate data, the Version impact or lead to an increase of future potential distributions of 2 Bioclimatic variables with a spatial resolution of 2.5min were the species under study. Models obtained were used to estimate selected (Fick and Hijmans, 2017) with the aim of maintaining the current distribution in South America using the predict the same spatial resolution of the species georeferenced (Sillero function from the sdm package. This function allows making a and Barbosa, 2021). To extract values from the bioclimatic layers, raster object with predictions from several fitted models (Naimi the extract function was used. Finally, the species names were and Araújo, 2016). All 24 predictions were ensemble in one using combined with coordinates (latitude, longitude), bio_1 to bio_19, the ensemble function which provides a consensus of multiple and elevation values into a single data.frame. models. By combining projections from different models, errors tend to be canceled out thus aiding predictive accuracy (Diniz- Ecological Niche Models Filho et al., 2010). All analyses were performed in R studio version 4.1.0 (R. Core Team, 2021) according to Naimi and Araújo (2016) methodology Model Evaluation (https://www.biogeoinformatics.org/), using the package sdm To evaluate model outputs, we used the receiver operated (Naimi and Araujo, 2019; R. Core Team, 2021). characteristics, analyzing the area under curve (AUC) (Fielding and Bell, 1997) and the true skill statistic (TSS) (Allouche et al., Collinear Variables Removal 2006). The AUC value is a standardmethod to assess the accuracy To prevent any multicollinearity-related bias in the models, of predictive distribution models, AUC values below 0.7 were a collinearity test among bioclimatic variables was performed considered poor, 0.7–0.9 moderate, and >0.9 good (Araújo et al., using the vifstep function. Collinearity describes the situation 2005). TSS compares the number of correct forecasts, minus where two or more predictor variables in a statistical model are those attributable to random guessing, to that of a hypothetical linearly correlated (Alin, 2010). Therefore, it could inflate both set of perfect forecasts. TSS values close to one denote an ideal the standard error and the confidence intervals, and prevent prediction; values of zero or less denote a prediction that is not the determination of the significance of each variable on the better than random (Allouche et al., 2006). For each species, the dependent variable (Quinn and Keough, 2002). Variables with relative importance of bioclimatic variables selected based on VIF (Variance Inflation Factors; Chatterjee and Hadi, 2006) multicollinearity analysis and AUC metric were plotted. values < 0.7 were selected for the subsequent analyzes. We created a sdmData object including species and previously Future Distribution Model selected variables, which means low collinearity, as predictors. To build future potential distribution, we used the BCC- Approximately 1,000 ‘pseudo-absences’ points were randomly CSM2-MR global climate model from the Coupled Model selected over the study geographical area for each species using Intercomparison Project 6 [CMIP6; available for use in argument method=‘gRandom’. Pseudo-absence refers to cells in the WorldClim (https://www.worldclim.org/data/cmip6/ which the species has not yet been recorded, not to cells in which cmip6climate.html); (O’Neill et al., 2016)] and two shared the species is necessarily absent (Phillips et al., 2009). socio-economic pathways [(SSP); (1) SSP126: an optimistic scenario increasing shift toward sustainable practices with low Model Fitting greenhouse gas concentration levels and (2) SSP585: a pessimistic We used four species distribution models to predict the scenario that assumes an energy intensive, fossil-based economy distribution of each spittlebug species under study. All with increasing greenhouse gas emissions over time (O’Neill models were based on presence and pseudo-absence data: et al., 2017; Riahi et al., 2017)] in a 2.5-min resolution. Habitat Maximum Entropy (MaxEnt), Generalized Linear Model (GLM), suitability was modeled using selected previously bioclimatic Frontiers in Sustainable Food Systems | www.frontiersin.org 1322 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling layers under each SSP scenario. In this study, only one time estimated a suitable area in southern Costa Rica and Panama, period was used for near future prediction: 2050 (average as well as Eastern Ranges and Caribbean coast in Colombia, for 2041–2060). To quantify the change between current and and Andean Venezuela (Figure 2). Bioclimatic layers with high future distribution, maps were converted from probability of contribution were minimum temperature of coldest month occurrence to presence and absence. For this, the mean threshold (bio_6) and isothermality (bio_3), showing high suitability with (occurrence probability values) was used in the ifelse function high values of both bio_6 and bio_3 (Figure 7). Average of AUC which allows reviewing the probability values. If the probability and TSS (± SD) was 0.94 ± 0.01 and 0.88 ± 0.05, respectively. values are greater than or equal to the average threshold, the new An increase in suitable areas and possible invasions are expected value assigned is 1 (presence) and if the probability value is less for the future optimistic scenario in Colombian and Venezuelan on the average threshold, the new value assigned is 0 (absence). Llanos and Colombian Caribbean region. In the pessimistic Later, the current distribution raster was subtracted from the scenario, Amazonas ecoregion of Peru and Brazil, along with future distribution raster, as a result, possible extinction and some sites in southern Costa Rica, Panama, Dominican Republic, invasion were plotted. and Mexico are predicted to be susceptible to new invasions (Figure 2). A. varia occurred in central and southwestern Colombia RESULTS and northwestern Venezuela. The ENM estimated a suitable area in Amazonas ecoregion of Colombia, Venezuela, and In total 590 occurrence records were obtained: 115 from human northern Brazil, and a smaller region in northern Peru (Figure 3). observations, 299 from CIATARC, 108 from GBIF, 24 from Bioclimatic layers with high contribution were precipitation of SpeciesLink, and 44 from literature review. After data cleansing, the coldest quarter (bio_19), temperature seasonality (bio_4), 48, 186, 19, 71, 55, and 120 points were used for A. lepidior, A. and precipitation seasonality (bio_15) (Figure 7). Average AUC reducta, A. varia, P. simulans, Z. carbonaria, and Z. pubescens, and TSS (± SD) was 0.97 ± 0.01 and 0.89 ± 0.05, respectively. respectively. Maps showing the occurrence records, estimation A decrease in suitable areas is expected for future scenarios of current distribution and future potential distribution (2041– compared to the same sites in current sites. Also, extinction is 2060) under SSP126 - SSP585 scenarios, and comparison between predicted in a few areas of Colombian and Venezuelan Llanos current and future scenarios (change SSP126 and SSP585) are (Figure 3). presented in Figures 1–6. Suitable areas and suitability values P. simulans was the most widespread species in this as well as bioclimatic layers selected based on multicollinearity study. Occurrence records were obtained mostly from North analysis differed according to the species in the study (Figure 7). America (Mexico) and Central America, with fewer records Consequently, probability of occurrence (i.e., suitability) in the in western Colombia (Figure 4). Bioclimatic layers with high niches of each species as a function of two most representative contribution were precipitation of the wettest month (bio_13) biovariables (Figure 8) varied according to species. In general, and precipitation of the coldest quarter (bio_18), showing high the ensembled models reached acceptable values for metrics used suitability with values <1,060 of bio_18 and values between 468 to evaluate ENMs accuracy (see Supplementary Table S1). The and 900 of bio_13 (Figure 7). Average of AUC and TSS (± SD) most used, AUC and TSS metrics, showed high scores for all was 0.91 ± 0.06 and 0.73 ± 0.12, respectively. ENMs showed species under study indicating robust performance (Figure 9). more habitats in South America and a small area in the Pacific A. lepidior occurred in southern and central Costa Rica, Coast of Central America but with low suitability. An increase in central Panama, and northern Colombia. The ENM estimated suitability and possible invasions for small areas of Brazil Cerrado a suitable area in central and north Colombia and some areas in both scenarios, along with Venezuelan Llanos in the optimistic of Venezuela (AUC 0.97 ± 0.05, TSS 0.80 ± 0.1) (Figure 1). scenario, and a noticeable decrease in Costa Rica is expected Bioclimatic layers with high contribution were isothermality (Figure 4). (bio_3) and temperature seasonality (bio_4), showing high Z. carbonaria has been recorded only in western Colombia, suitability with high values of bio_3 (>70 %) and low values across central Andes. The ENM estimated higher suitability of bio_4 (<77.45%) (Figure 7). Averages of AUC and TSS (± in Colombian and Ecuadorian Andes (middle tropic) and the SD) were 0.97 ± 0.05 and 0.80 ± 0.1, respectively (Figure 9, Amazonian Piedmont of Colombia, decreasing its values to zero Supplementary Table S1). A considerable increase in suitability in Colombian and Venezuelan Llanos (low tropic) (Figure 5). is expected for large areas of Amazonas ecoregion of Peru, Bioclimatic layers with high contribution were isothermality Venezuela, and the north of Brazil even in the optimistic (bio_3) and precipitation seasonality (bio_15), showing high scenario, with possible invasions in those sites and western suitability with values close to 40 of bio_15 and high values of Ecuador, northeastern Peru and northern Bolivia (Figure 1). bio_15 (Figure 7). Average of AUC and TSS (± SD) was 0.99 ± Also in Panama, Costa Rica, and, in the pessimistic scenario, in 0.02 and 0.93 ± 0.07, respectively. A decrease in suitability for Guatemala and Belize. Small areas in a few sites of the Pacific the Amazonian Piedmont of Colombia and the Andes is expected coast of Central America and tropical South America show a (Figure 5). decrease in suitable areas for this species. Finally, Z. pubescens occurred widely in western and central A. reducta occurred in Costa Rica, central Panama, and central Andes of Colombia, northern Ecuador and western Brazil, and northern Caribbean Colombia. Fewer records were obtained including Amazon and Cerrado biogeographic zones. Fewer in northwestern Venezuela and northern Brazil. The ENM records were obtained in southern Peru and northern Suriname Frontiers in Sustainable Food Systems | www.frontiersin.org 1423 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 1 | Ecological niche models of Aeneolamia lepidior. Distribution records, current potential distribution, future potential distribution (2041–2060) under SSP126 and SSP585 scenarios, and comparison between current and future scenarios (change SSP126 and SSP585). The scale shows the habitat suitability being 1 = higher suitability. Scale in change maps −1 = possible extinction and 1 = possible invasion. Frontiers in Sustainable Food Systems | www.frontiersin.org 1524 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 2 | Ecological niche models of Aeneolamia reducta. Distribution records (red point indicates the most recent report in a new niche), current potential distribution, future potential distribution (2041–2060) under SSP126 and SSP585 scenarios, and comparison between current and future scenarios (change SSP126 and SSP585). The scale shows the habitat suitability being 1 = higher suitability. Scale in change maps −1 = possible extinction and 1 = possible invasion. Frontiers in Sustainable Food Systems | www.frontiersin.org 1625 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 3 | Ecological niche models of Aeneolamia varia. Distribution records, current potential distribution, future potential distribution (2041–2060) under SSP126 and SSP585 scenarios, and comparison between current and future scenarios (change SSP126 and SSP585). The scale shows the habitat suitability being 1 = higher suitability. Scale in change maps −1 = possible extinction and 1 = possible invasion. Frontiers in Sustainable Food Systems | www.frontiersin.org 1726 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 4 | Ecological niche models of Prosapia simulans. Distribution records, current potential distribution, future potential distribution (2041–2060) under SSP126 and SSP585 scenarios, and comparison between current and future scenarios (change SSP126 and SSP585). The scale shows the habitat suitability being 1 = higher suitability. Scale in change maps −1 = possible extinction and 1 = possible invasion. Frontiers in Sustainable Food Systems | www.frontiersin.org 1827 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 5 | Ecological niche models of Zulia carbonaria. Distribution records, current potential distribution, future potential distribution (2041–2060) under SSP126 and SSP585 scenarios, and comparison between current and future scenarios (change SSP126 and SSP585). The scale shows the habitat suitability being 1 = higher suitability. Scale in change maps −1 = possible extinction and 1 = possible invasion. Frontiers in Sustainable Food Systems | www.frontiersin.org 1928 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 6 | Ecological niche models of Zulia pubescens. Distribution records, current potential distribution, future potential distribution (2041–2060) under SSP126 and SSP585 scenarios, and comparison between current and future scenarios (change SSP126 and SSP585). The scale shows the habitat suitability being 1 = higher suitability. Scale in change maps −1 = possible extinction and 1 = possible invasion. Frontiers in Sustainable Food Systems | www.frontiersin.org 1209 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 7 | Relative variable importance in modeling the ecological niche of each species of spittlebugs. Error bars represent the standard deviation of all 24 models. The graphs show only bioclimatic layers selected based on multicollinearity analysis for each species. Frontiers in Sustainable Food Systems | www.frontiersin.org 1310 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 8 | Observed niche of Colombian spittlebugs as a function of two most representative biovariables. The scale shows occurrence probabilities. Frontiers in Sustainable Food Systems | www.frontiersin.org 1321 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling FIGURE 9 | Evaluation of ecological niche models of spittlebugs species across different metrics obtained from 24 model by each species. (Figure 6). Bioclimatic layers with high contribution were TSS (± SD) was 0.89 ± 0.03 and 0.66 ± 0.09, respectively. An temperature seasonality (bio_4) and precipitation seasonality increase in suitability is expected for some areas of Ecuador, Peru, (bio_15), showing high suitability with low values of bio_4 (<10) and Brazil in both climate change scenarios, being greater in the and values close to 40 of bio_15 (Figure 7). Average of AUC and pessimistic scenario (Figure 6). Frontiers in Sustainable Food Systems | www.frontiersin.org 1332 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling DISCUSSION season start (Peck et al., 2001, 2002; Sujii et al., 2002; Olán- Hernández et al., 2016). Hence, a strong effect of the biovariables In our study ENMs of the occurrence data had a high grade 12 to 19 in the models, related with precipitation, in the of accuracy given the sample size of five species, except for models was expected but in our estimations, the distribution of A. varia, for modeling (>25 records) (van Proosdij et al., habitat suitability of these six species also involved environmental 2016; Schöbel and Carvalho, 2020). Despite small sample sizes variables related to temperature suggesting that variables derived methodologies based on calculation p-values through Jackknife from temperature has a strong effect on the biology of these are implemented in the SDM R package used in this study species. For P. simulans, precipitation was more important (Naimi and Araújo, 2016), more records may increase the model than temperature to determine its distribution with a relative accuracy (van Proosdij et al., 2016). Low records for spittlebugs importance over 0.4 for precipitation of the wettest month, were previously reported for Mahanarva in Brazil (Schöbel and thus, greater probabilities of occurrence happen in precipitation Carvalho, 2020) being underrepresented in occurrence databases. between 500 and 940mm. In general, the habitat suitability This phenomenon was also observed for the six species studied as estimated for two-dimensional niches was low as the biovariables’ most of the records were obtained from CIATARC collection and relative importance varied among all the species with values expert’s reports through the years (human observation). below 0.4 (Figure 8). Similar results were obtained by Schöbel The ENMs also revealed differences in the distribution and and Carvalho (2020) in ENMof fourMahanarva species showing ecological niche of the six spittlebug species in South America that most of the WorldClim variables did not contribute to showing that these species ecological niche varies widely in their analysis and that for M. fimbriolata and M. spectabilis the the Neotropic, and has the potential to invade large areas, biovariables had contribution percentages from 15 to 27%. where livestock systems coincide. A. reducta y A. lepidior have Regarding the climate change scenarios proposed, we found great potential to impact grassland mainly in Colombian and that these have a significant influence on the potential Venezuelan Llanos where susceptible pastures (e.g., Urochloa distribution of the species in study, increasing the suitability value decumbens) and sugarcane are planted in large areas. Another and suitable area for some (mainly for A. reducta and A. lepidior) ecoregion where these two species have high suitability is the or decreasing them for others (A. varia). Previous studies showed Amazonian ecoregion in Colombia and Brazil, where livestock a declining tendency in suitability for Mahanarva across Central extensive systems are increasing indiscriminately. and South America (Fonseca et al., 2016; Schöbel and Carvalho, The evidence showed that Z. pubescens is distributed in a 2020) and Philaenus spumarius in North America (Karban and wide altitudinal range (8–3225m.a.s.l) but with a local reduced Huntzinger, 2018). Global warming and longer drought periods temperature seasonality. Elevation has been reported as the contribute to accelerate this phenomenon as spittlebug biology most important variable with the highest contribution in the is highly dependent on plant water status. Being xylem feeders, ENMs in other spittlebugs (Schöbel and Carvalho, 2020). Few they require excessive amounts of sap which flow is subject to species have such a wide altitudinal range, which allows us transpiration (Novotny and Wilson, 1997). Under water stress to propose two hypotheses: (1) Z. pubescens presents extreme conditions transpiration rates decrease as well as food availability thermal limits and (2) the species presents geographically for spittlebugs, particularly in the nymphal stages. Besides, these separated populations. A case of biotypes is observed for the conditions may affect nymph thermoregulation by foam or spittlebug Calitettix versicolor in China, which diverged in two “spittle” production, composed mainly of excreted semi-digested lineages consistent with biogeographical regions separated by plant fluid, fatty acids, carbohydrates, mucopolysaccharides, and Hengduan Mountains (Yang et al., 2016). Similarly, this could proteins produced by Malpighian tubules (Rakitov, 2002; Tonelli be happening with Z. pubescens influenced by the Colombian et al., 2018). Since the six species are Urochloa spp. key pests, Andes. Although the species is reported in Brazil (27 occurrence a future limitation of ecological niche in future scenarios in records; average of 400m.a.s.l), the suitability values are lower livestock production zones should be taken into account as than in Colombia and Ecuador (93 occurrence records; average improved resistant grasses to spittlebug attack and increase the of 1079m.a.s.l.). The higher number of records in the highlands number of forage species are considered a sustainable strategy of Colombia and Ecuador could be causing an overestimation for the livestock systems under climate change (Rao et al., of the occurrence probability at these areas over the records 2016; Schiek et al., 2018). Competition can influence species of Cerrado places in Brazil, this would explain the current future distribution as well. Despite reaching the spittlebug potential distribution estimated, and also could be reflecting the habitat’s food limits is unlikely (Schöbel and Carvalho, 2020), possible existence of, at least, two populations with different the variation among species’ life cycles may determine the ecological niches. success of one species over others. A. reducta was reported The position of a species within an ecosystem is determined for the first time in 2019 in Cauca River Valley, Colombia by the interactions with their biotic and abiotic environment (Hernandez et al., 2021) where A. varia is a key pest of (Polechová and Storch, 2019). Tropical spittlebugs have a sugarcane and P. simulans of signalgrass [Urochloa decumbens seasonal dynamic strongly synchronized with rainfall patterns. cv. Basilisk; (Rodriguez Chalarca et al., 2003; Gómez, 2007)]. For instance, Z. carbonaria and A. reducta in Colombia, In Colombian Caribbean coast, A. reducta’s entire life cycle is P. simulans in Colombia and Venezuela, D. flavopicta in Brazil, shorter (45.2 days) compared with A. varia (62 days) or P. as well as A. contigua and A. contigua in Mexico, reduce diapause simulans (71.9 days) in Cauca River Valley conditions (Peck rates and a higher abundance of nymphs is observed after rain et al., 2002; Rodriguez Chalarca et al., 2003; Castro Valderrama Frontiers in Sustainable Food Systems | www.frontiersin.org 1343 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling et al., 2011). Thus, A. reducta can coexist or even displace FUNDING these two species in sugarcane and signalgrass for potentially having more generations per year in the region where ∼208 This work was funded by the CGIAR Research Program on thousand ha of sugarcane was harvested in 2018 (Asocaña., Livestock. The funders had no role in the design of the study; in 2019). the collection, analyses, or interpretation of data; in the writing The current study contributes to the ecological knowledge of of the manuscript, or in the decision to publish the results. We spittlebugs, which will be useful in the development of prevention also acknowledge the financial assistance of GROW Colombia and control strategies for this pest in South America. Finally, from the UK Research and Innovation (UKRI) Global Challenges we suggest carrying out studies of physiology and genetics Research Fund (GCRF) (BB/P028098/1). of populations to determine the thermal limits of the species and to corroborate if there are genetic divergences between ACKNOWLEDGMENTS geographically separated populations. We would like to thank the person who enriched the spittlebugs DATA AVAILABILITY STATEMENT collection deposited in CIATARC: Daniel Peck. Also, to the organizations that allowed the use of their data for our research: The raw data supporting the conclusions of this article will be GBIF and SpeciesLink. This work was carried out as part of the made available by the authors, without undue reservation. CGIAR Research Program on Livestock. We thank all donors who globally support our work through their contributions to AUTHOR CONTRIBUTIONS the CGIAR System. CGIAR is a global research partnership for a food-secure future. Its science is carried out by 15 Research LH and PE contributed to the data collection, data Centers in close collaboration with hundreds of partners across curation, analysis and interpretation of maps, manuscript the globe. We also thank the reviewers for their constructive preparation, and supervision. DF contributed to data comments that helped to improve the manuscript. collection and manuscript preparation. VC contributed to manuscript preparation. JC contributed to interpretation SUPPLEMENTARY MATERIAL and manuscript preparation. MG-J contributed to data collection, interpretation of maps, and manuscript preparation. The Supplementary Material for this article can be found All authors contributed to the article and approved the online at: https://www.frontiersin.org/articles/10.3389/fsufs. submitted version. 2021.725774/full#supplementary-material REFERENCES de Educación para el Desarrollo y la Conservación del Centro Agronómico Tropical de Investigación y Enseñanza, Turrialba, Costa Rica. Alin, A. (2010). Multicollinearity.Wiley Interdiscip. Rev. Comput. Stat. 2, 370–374. Castro Valderrama, U., Cuarán, V. L., Ramírez Sánchez, G., Bustillo Pardey, A. E., doi: 10.1002/wics.84 and Gómez Laverde, L. A. (2011). Resistencia varietal en el manejo del salivazo Allouche, O., Tsoar, A., and Kadmon, R., (2006). Assessing the accuracy de la caña, Aeneolamia varia (F.) (Hemiptera: Cercopidae). Método demedición of species distribution models: prevalence, kappa and the true skill en la caña de azúcar. Cali, Colombia: Cenicaña. statistic (TSS). J. Appl. Ecol., 43, 1223–1232. doi: 10.1111/j.1365-2664.2006.0 Castro, U., Morales, A., and Peck, D. C. (2005). Dinámica poblacional y 1214.x fenología del salivazo de los pastos Zulia carbonaria (Lallemand) (Homoptera: Araújo, M. B., Pearson, R. G., Thuiller, W., and Erhard, M. (2005). Validation of Cercopidae) en el Valle geográfico del Río Cauca, Colombia. Neotrop. Entomol. species-climate impact models under climate change. Glob. Change. Biol. 11, 34, 459–470. doi: 10.1590/S1519-566X2005000300015 1504–1513. doi: 10.1111/j.1365-2486.2005.01000.x Chatterjee, S., and Hadi, A. S. (2006). Regression Analysis by Example, Vol. 607. Asocaña. (2019). Aspectos generales del sector agroindustrial de la caña Hoboken, NJ: John Wiley & Sons. doi: 10.1002/0470055464 2018 – 2019. Informe Anual. Available online at: https://www.asocana. de la Cruz-Zapata, G., García-López, E., Sánchez-Soto, S., Bautista-Martínez, org/documentos/2352019-D0CA1EED-00FF00,000A000,878787,C3C3C3, N., Ortiz-Díaz, J. J., and Osorio-Osorio, R. (2016). Identidad de mosca 0F0F0F,B4B4B4,FF00FF,2D2D2D,A3C4B5.pdf (accesed June 15, 2021). pinta (Hemiptera: Cercopidae) y sus hospederas en cañaverales en Cárdenas, Avila de Moreno, C., and Umaña, M. I. (1988). Aspectos De La Biología y Tabasco, México. Southwest. Entomol. 41, 145–152. doi: 10.3958/059.041.0116 patogenicidad del hongoMetarhizium anisopliae (Metchnikoff) Sorokin, sobre Dietrich, C. H. (2009). “Auchenorrhyncha: (Cicadas, Spittlebugs, Leafhoppers, Aeneolamia varia (F). Rev. ICA. 23, 155–161. Treehoppers, and Planthoppers),” In Encyclopedia of Insects, eds. V. Resh Cardona, C., Fory, P., Sotelo, G., Pabon, A., Diaz, G., and Miles, J. W. (2004). and R. Cardé (San Diego, California: Academic Press Inc.), 56–64. Antibiosis and tolerance to five species of spittlebug (Homoptera: Cercopidae) doi: 10.1016/B978-0-12-374144-8.00015-1 in Brachiaria spp.: implications for breeding for resistance. J. Econ. Entomol. 97, Diniz-Filho, J. A. F., Nabout J. C., Bini, L. M., Loyola, R. D., Rangel, T. F., Nogues- 635–645. doi: 10.1093/jee/97.2.635 Bravo, D., et al. (2010). Ensemble forecasting shifts in climatically suitable areas Cardona, C., Sotelo, G., and Miles, J. (2000). Avances en investigaciones sobre for Tropidacris cristata (Orthoptera: Acridoidea: Romaleidae). Insect Conserv. resistencia de Brachiaria a salivazo. Gramíneas y Legum. Trop. IP.·5, 1–8. Divers. 3, 213–221. doi: 10.1111/j.1752-4598.2010.00090.x Cardoso, P., Barton, P. S., Birkhofer, K., Chichorro, F., Deacon, C., Fartmann, Elith, J., and Leathwick, J. R. (2009). Species distribution models: ecological T., et al. (2020). Scientists’ warning to humanity on insect extinctions. Biol. explanation and prediction across space and time. Annu. Rev. Ecol. Systema. Conserv. 242:108426. doi: 10.1016/j.biocon.2020.108426 40, 677–697. doi: 10.1146/annurev.ecolsys.110308.120159 Castillo, S. (2006). Uso de Metarhizium anisopliae para el control biológico del Ferrer, F., Arias, M., Trelles, A., Palencia, G., Navarro, J. M., and Colmenarez, R. salivazo (Aeneolamia spp. y Prosapia spp.) en pastizales de Brachiaria decumbens (2004). Posibilidades del uso de nematodos entomopatógenos para el control de en El Petén, Guatemala. (master’s thesis). Escuela de Posgrado, Programa Aeneolamia varia en caña de azúcar.Manejo Integr. Plagas y Agroecol. 72, 39–43 Frontiers in Sustainable Food Systems | www.frontiersin.org 1354 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling Fick, S. E., and Hijmans, R. J. (2017). WorldClim 2: new 1-km spatial resolution Larson, E. L., Tinghitella, R. M., and Taylor, S. A. (2019). Insect hybridization and climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315. climate change. Front. Ecol. Evol. 7. doi: 10.3389/fevo.2019.00348 doi: 10.1002/joc.5086 Lehmann, P., Ammunét, T., Barton, M., Battisti, A., Eigenbrode, S. D., Jepsen, J. U., Fielding, A. H., and Bell, J. F. (1997). A review of methods for the assessment of and Björkman, C. (2020). Complex responses of global insect pests to climate prediction errors in conservation presence/absence models. Environ. Conserv. warming. Front. Ecol. Environm. 18, 141–150. doi: 10.1002/fee.2160 24, 38–49. doi: 10.1017/S0376892997000088 Liu, Y., and Shi, J. (2020). Predicting the potential global geographical Figueredo, L., Andrade, O., Cova, J., Mora, O., and Aza, G. (2012). Distribución distribution of Two Icerya species under climate change. Forests. 11, 684. espacio temporal de ninfas de Aeneolamia varia fabricius (1787) (Hemiptera: doi: 10.3390/f11060684 Cercopidae) en caña de azúcar a través de un sistema de información geográfica. Macfadyen, S., McDonald, G., and Hill, M. P. (2018). From species distributions Entomotropica. 27, 7–18. to climate change adaptation: Knowledge gaps in managing invertebrate Fonseca, M. G., Auad, A. M., Resende, T. T., Hott, M. C., and Borges, C. A. V. pests in broad-acre grain crops. Agric. Ecosyst. Environ. 253, 208–219. (2016). How will Mahanarva spectabilis (Hemiptera: Cercopidae) respond to doi: 10.1016/j.agee.2016.08.029 global warming? J. Insect Sci. 16, 1–6. doi: 10.1093/jisesa/iew005 Matabanchoy Solarte, J. A., Bustillo Pardey, A. E., Castro Valderrama, U., Mesa García-González, J. C., López-Collado, J., Gilberto, C., Villanueva-Jiménez, J. A., Cobo, N. C., and Moreno Gil, C. A., (2012). Eficacia deMetarhizium anisopliae and Nava-Tablada, M. A. (2017). Factores bióticos, abióticos y agronómicos para controlar Aeneolamia varia (Hemiptera: Cercopidae), en caña de azúcar. que afectan las poblaciones de adultos de mosca pinta (Hemiptera: Cercopidae) Rev. Colomb. Entomol. 38, 177–181. en cultivos de caña de azúcar en Veracruz, México. Acta. Zoológica Mex. 33, Naimi, B., and Araújo, M. B. (2016). Sdm: A Reproducible and Extensible 508–517. doi: 10.21829/azm.2017.3331152 R Platform for Species Distribution Modelling. Ecography. 39, 368–75. GBIF.org. (2020a). (10 August 2021) GBIF occurrence download, A. reducta. doi: 10.1111/ecog.01881 doi: 10.15468/dl.sjr4w9 Naimi, B., and Araujo, M. B. (2019). Package “sdm.” R CRAN Proj. 1–10. GBIF.org. (2020b). (10 August 2021) GBIF occurrence download, P. simulans. Novotny, V., and Wilson, M. R. (1997). Why are there no small species among doi: 10.15468/dl.xsf4dz xylem-sucking insects? Evol. Ecol. 11, 419–437. doi: 10.1023/A:10184328 GBIF.org. (2020c). (10 August 2021) GBIF occurrence download, Z. carbonaria. 07165 doi: 10.15468/dl.sw7esa Olán-Hernández, J. F., Sánchez-Soto, S., Bautista-Martínez, N., Zaldivar-Cruz, J. GBIF.org. (2020d). (10 August 2021) GBIF occurrence download, Z. pubescens. M., and Cortez-Madrigal, H. (2016). Fluctuación poblacional de Aeneolamia doi: 10.15468/dl.zesguw contigua (WALKER) en el cultivo de caña (Saccharum spp.) en Tabasco, GBIF.org. (2020e). (10 August 2021) GBIF occurrence download, A. lepidior. México. Agroproductividad. 9, 10–14. doi: 10.15468/dl.47jaqb O’Neill, B. C., Kriegler, E., Ebi, K. L., Kemp-Benedict, E., Riahi, K., Rothman, D. S., Ghimire, S., Njarui, D., Mutimura, M., Cardoso, J. A., Johnson, L., Gichangi, E. et al. (2017). The roads ahead: Narratives for shared socioeconomic pathways M., et al. (2015). “Climate-smart Brachiaria grasses for improving livestock describing world futures in the 21st century.Glob. Environ. Chang. 42, 169–180. production in East Africa,” in 23rd International Grassland Congress 2015 (New doi: 10.1016/j.gloenvcha.2015.01.004 Delhi: New South Wales Department of Primary Industry), 361–370. O’Neill, B. C., Tebaldi, C., Vuuren, D. P. V., Eyring, V., Friedlingstein, P., Gómez, L. A. (2007). Manejo del salivazo Aeneolamia varia en cultivos de caña de Hurtt, G., and Sanderson, B. M. (2016). The scenario model intercomparison azúcar en el valle del río Cauca. Valle del Cauca, Colombia. Available online project (ScenarioMIP) for CMIP6. Geosci. Model Dev. 9, 3461–3482 at: http://www.cenicana.org/pdf/carta_trimestral/ct2007/ct2y3_07/ct2y3_07_ doi: 10.5194/gmd-9-3461-2016 p10-17.pdf. (accessed April 16, 2021). Paladini, A., Domahovski, A. C., Krinski, D., and Foerster, L. A. (2018). Reports Goulson, D. (2019). The insect apocalypse, and why it matters. Curr. Biol. 29, of new wing color polymorphism and taxonomic information to cercopids R942–R995. doi: 10.1016/j.cub.2019.06.069 (Auchenorrhyncha: Cercopidae) from upland rice crop, Pará state, Brazil. Grünig, M., Mazzi, D., Calanca, P., Karger, D. N., and Pellissier, L. (2020). Crop Brazilian J. Biol. 78, 728–735. doi: 10.1590/1519-6984.175519 and forest pest metawebs shift towards increased linkage and suitability overlap Parada Domínguez, O., Alatorre Rosas, R., Guzmán-Franco, A. W., Hernández under climate change. Commun. Biol. 3, 1–10. doi: 10.1038/s42003-020-0962-9 Rosas, F., Rojas Avelizapa, L. I., and Ruíz Vera, V. M. (2019). Effect of Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., et al. entomopathogenic nematodes on nymphs of Aeneolamia albofasciata and its (2017). More than 75 percent decline over 27 years in total flying insect biomass persistence in sugarcane soils of Veracruz. Rev. Mex. Ciencias Agrícolas. 22, in protected areas. PLoS ONE. 12, e0185809. doi: 10.1371/journal.pone.0185809 115–127. doi: 10.29312/remexca.v0i22.1863 Halsch, C. A., Shapiro, A. M., Fordyce, J. A., Nice, C. C., Thorne, J. H., Waetjen, D. Peck, D., Perez, A., andMedina, J. (2002). Biología y hábitos deAeneolamia reducta P., et al. (2021). Insects and recent climate change. Proc. Natl. Acad. Sci. U. S. A. y A. lepidior en la costa caribe de Colombia. Pasturas Trop. 24, 16–26. 118, 1–9. doi: 10.1073/pnas.2002543117 Peck, D. C. (1998). Use of Alternative Food Plants Exclusively by Adult Hamilton, K. G. A. (1977). Review of the world species of Prosapia Male Froghoppers (Homoptera: Cercopidae). Biotropica. 30, 639–644. Fennah (Rhynchota: Homoptera: Cercopidae). Can. Entomol. 109, 621–630. doi: 10.1111/j.1744-7429.1998.tb00103.x doi: 10.4039/Ent109621-4 Peck, D. C. (2001). Diversidad y distribución geográfica del salivazo (Homoptera: Heeb, L., Jenner, E., and Cock, M. J. W. (2019). Climate-smart pest management: Cercopidae) asociado con gramíneas en Colombia y Ecuador. Rev. Colomb. building resilience of farms and landscapes to changing pest threats. J. Pest Sci. Entomol. 27, 129–136. 92, 951–969. doi: 10.1007/s10340-019-01083-y Peck, D. C., Castro, U., López, F., Morales, A., and Rodríguez Chalarca, J. (2001). Hernandez, L. M., Bonilla, X., and Espitia-Buitrago, P. (2021). Primer registro de First records of the sugar cane and forage grass pest, Prosapia simulans Aeneolamia reducta (Hemiptera: Cercopidae) en el Valle del Cauca (Colombia). (Homoptera: Cercopidae), from South America. Florida Entomol. 84, 402–409. Boletín del Mus. Entomol. la Univ. del Val. 20, 1–6. doi: 10.2307/3496499 Hughes, L. (2000). Biological consequences of global warming: Is Peck, D. C., and Thompson, V. (2008). “Spittlebugs (Hemiptera:Cercopoidea),” In the signal al- ready apparent? Trends Ecol. Evol. 15, 56–61. Encyclopedia of entomology, ed. J. Capinera (Dordrecht: Springer), 3512–3515. doi: 10.1016/S0169-5347(99)01764-4 Peterson, A. T., and Soberón, J. (2012). Species distribution modeling and Jank, L., Barrios, S. C., do Valle, C. B., Simeão, R. M., and Alves, G. F. (2014). The ecological niche modeling: getting the concepts right.Natureza & Conservacao. value of improved pastures to Brazilian beef production. Crop. Pasture. Sci. 65 10, 102–107. doi: 10.4322/natcon.2012.019 1132–1137. doi: 10.1071/CP13319 Peterson, A. T., Soberón, J., Pearson, R. G., Anderson, R. P., Martínez- Karban, R., and Huntzinger, M. (2018). Decline of meadow spittlebugs, a Meyer, E., Nakamura, M., et al. (2011). Ecological Niches and Geographic previously abundant insect, along the California coast. Ecology. 99, 2614–2616. Distributions. Princeton, NJ; Oxford: Princeton University Press. doi: 10.1002/ecy.2456 doi: 10.23943/princeton/9780691136868.003.0003 Kearney, M., and Porter, W. (2009). Mechanistic niche modelling: Combining Phillips, S. J., andDudík,M. (2008).Modeling of species distributions withMaxent: physiological and spatial data to predict species’ ranges. Ecol. Lett. 12, 334–350. new extensions and a comprehensive evaluation. Ecography. 31, 161–175. doi: 10.1111/j.1461-0248.2008.01277.x doi: 10.1111/j.0906-7590.2008.5203.x Frontiers in Sustainable Food Systems | www.frontiersin.org 1365 November 2021 | Volume 5 | Article 725774 Hernández et al. Distribution Colombian Spittlebugs Niche Modeling Phillips, S. J., Dudík, M., Elith, J., Graham, C. H., Lehmann, A., Leathwick, J., Deois flavopicta (Homoptera: Cercopidae). Environ. Entomol. 31, 299–305. et al. (2009). Sample selection bias and presence-only distribution models: doi: 10.1603/0046-225X-31.2.299 implications for background and pseudo-absence data. Ecol. Appl., 19, 181–197. Thompson, V. (2004). Associative nitrogen fixation, C4 photosynthesis, and doi: 10.1890/07-2153.1 the evolution of spittlebugs (Hemiptera: Cercopidae) as major pests of Polechová, J., and Storch, D. (2019). “Ecological niche,” In neotropical sugarcane and forage grasses. Bull. Entomol. Res. 94, 189–200. Encyclopedia of Ecology 2nd ed., ed. B. D. Fath (Elsevier), 72–80. doi: 10.1079/BER2004293 doi: 10.1016/B978-0-12-409548-9.11113-3 Thompson, V., and León González, R. (2005). La identificación y distribución de Quinn, G. P., and Keough, M. J. (2002) Experimental design and los salivazos de la caña de azúcar y los pastos (Homoptera : Cercopidae).Manejo data analysis for biologists. Cambridge University Press, Melbourne. Integr. Plagas y Agroecol., 75: 43–51. doi: 10.1017/CBO9780511806384 Tonelli, M., Gomes, G., Silva, W. D., Magri, N. T. C., Vieira, D. M., Aguiar, C. L., Rakitov, R. A. (2002). Structure and function of the Malpighian tubules, et al. (2018). Spittlebugs produce foam as a thermoregulatory adaptation. Sci. and related behaviors in juvenile Cicadas: Evidence of homology with Rep. 8, 4729. doi: 10.1038/s41598-018-23031-z spittlebugs (Hemiptera: Cicadoidea and Cercopoidea). Zool. Anz. 241, 117–130. Valbuena, N. (2010). Dinámica y fenología de Aeneolamia spp. en dos especies doi: 10.1078/0044-5231-00025 forrajeras. Rev. UNELLEZ Cienc. y Tecnol. Volumen especial. 20–24. Rao, I. M., Miles, J. W., Beebe, S. E., and Horst, W. J. (2016). Root adaptations van Proosdij, A. S. J., Sosef, M. S. M.,Wieringa, J. J., and Raes, N. (2016). Minimum to soils with low fertility and aluminium toxicity. Ann. Bot. 118, 593–605. required number of specimen records to develop accurate species distribution doi: 10.1093/aob/mcw073 models. Ecography (Cop.). 39, 542–552. doi: 10.1111/ecog.01509 R. Core Team. (2021). R: A language and environment for statistical computing. Wagner, D. L., Grames, E. M., Forister, M. L., Berenbaum, M. R., and Stopak, D. R Foundation for Statistical Computing, Vienna, Austria. Available online (2021). Insect decline in the Anthropocene: Death by a thousand cuts. Proc. at: https://www.R-project.org/. Natl. Acad. Sci. U.S.A. 118, e2023989118. doi: 10.1073/pnas.2023989118 Resende, T. T., Auad, A. M. H., Fonseca, M. D. G., Dos Santos, T. H., and Vieira, T. White, D. S., Peters, M., and Horne, P. (2013). Global impacts from improved M. (2012). Impact of the spittlebug Mahanarva spectabilis on signal grass. Sci. tropical forages: A meta-analysis revealing overlooked benefits and costs, World J. 926715. doi: 10.1100/2012/926715 evolving values and new priorities. Trop. Grasslands – Forrajes Trop. 1, 12–24. Riahi, K., van Vuuren, D. P., Kriegler, E., Edmonds, J., O’Neill, B. C., Fujimori, doi: 10.17138/TGFT(1)12-24 S., et al. (2017). The Shared Socioeconomic Pathways and their energy, land Worthington, M., Perez, J. G., Mussurova, S., Silva-Cordoba, A., Castiblanco, V., use, and greenhouse gas emissions implications: An overview. Glob. Environ. Cardoso Arango, J. A., et al. (2021). A new genome allows the identification of Chang. 42, 153–168. doi: 10.1016/j.gloenvcha.2016.05.009 genes associated with natural variation in aluminium tolerance in Brachiaria Rodriguez Chalarca, J., Castro, U., Morales, A., and Peck, D. C. (2003). Biología del grasses. J. Exp. Bot. 72, 302–319. doi: 10.1093/jxb/eraa469 salivazo Prosapia simulans (Homoptera:Cercopidae), nueva plaga de gramíneas Yang, H., Lin, C. P., and Liang, A. P. (2016). Phylogeography of the rice spittle bug cultivadas en Colombia. Rev. Colomb. Entomol. 29, 149–155. (callitettix versicolor) implies two long-termmountain barriers in South China. Rodríguez Chalarca, J., Peck, D. C., and Canal, N. A., (2002). Biología comparada Zoolog. Sci. 33, 592–602. doi: 10.2108/zs160042 de tres especies de salivazo de los pastos del género Zulia (Homoptera: Cercopidae). Rev. Colomb. Entomol. 28, 17–25. Conflict of Interest: DF was employed by the company Semillas Papalotla S.A. de Sáenz, C., Salazar, D., Rodriguez, A., Alfaro, D., and Oviedo, R., (1999). Manejo C.V. integrado del salivazo, Aeneolamia sp. y Prosapia sp. (Hom: Cercopidae) en las regiones cañeras de Costa Rica. In XI Congreso Nacional Agronómico, V The remaining authors declare that the research was conducted in the absence of Congreso Nacional de Entomología. 155–159. any commercial or financial relationships that could be construed as a potential Schiek, B., González, C., Mwendia, S., and Prager, S. D. (2018). Got forages? conflict of interest. Understanding potential returns on investment in Brachiaria spp. for dairy producers in Eastern Africa. Trop. Grasslands-Forrajes Trop. 6, 117–133. Publisher’s Note: All claims expressed in this article are solely those of the authors doi: 10.17138/tgft(6)117-133 Schöbel, C., and Carvalho, G. S. (2020). Nichemodeling of economically important and do not necessarily represent those of their affiliated organizations, or those of Mahanarva (Hemiptera, Cercopidae) Species in South and Central America: the publisher, the editors and the reviewers. Any product that may be evaluated in Are brazilian spittlebug sugarcane pests potential invaders of South and Central this article, or claim that may be made by its manufacturer, is not guaranteed or America? J. Econ. Entomol. 113, 115–125. doi: 10.1093/jee/toz252 endorsed by the publisher. Schöbel, C., and Carvalho, G. S. (2021). The “State of Art” of Mahanarva (Hemiptera: Cercopidae) research. An economically important New World Copyright © 2021 Hernández, Espitia, Florian, Castiblanco, Cardoso and Gómez- spittlebug genus. Appl. Entomol. Zool. 1–11. doi: 10.1007/s13355-021-00744-8 Jiménez. This is an open-access article distributed under the terms of the Creative Sillero, N., and Barbosa, A. M. (2021). Common mistakes in ecological Commons Attribution License (CC BY). The use, distribution or reproduction in niche models. International Int J. Geogr. Inf. Sci. 35, 213–226. other forums is permitted, provided the original author(s) and the copyright owner(s) doi: 10.1080/13658816.2020.1798968 are credited and that the original publication in this journal is cited, in accordance Sujii, E. R., Garcia, M. A., Fontes, E. M. G., Pires, C. S., and O’Neil, R. J. (2002). with accepted academic practice. No use, distribution or reproduction is permitted Effects of meteorological variation on mortality in populations of the spittlebug which does not comply with these terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1376 November 2021 | Volume 5 | Article 725774 ORIGINAL RESEARCH published: 01 December 2021 doi: 10.3389/fsufs.2021.682653 In vitro Fermentation Profile and Methane Production of Kikuyu Grass Harvested at Different Sward Heights Alejandra Marín 1,2,3*, Jérôme Bindelle 4, Ángel S. Zubieta 2, Guillermo Correa 1, Jacobo Arango 3, Ngonidzashe Chirinda 3,5 and Paulo César de Faccio Carvalho 2 1Departamento de Producción Animal, Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, Medellín, Colombia, 2Grazing Ecology Research Group, Department of Forage Plants and Agrometeorology, Faculty of Agronomy, Federal University of Rio Grande Do Sul (UFRGS), Porto Alegre, Brazil, 3 International Center for Tropical Agriculture (CIAT), Cali, Colombia, 4 Precision Livestock and Nutrition Unit, AgricultureIsLife, TERRA Teaching and Research Center, Gembloux Agro-Bio Tech, Liège University, Gembloux, Belgium, 5 Agricultural Innovation and Technology Transfer Center, Mohammed VI Polytechnic University, Ben Guerir, Morocco Edited by: Isabel Cristina Molina- Botero, Highly digestible forages are associated with an in vitro low-methane (CH4) rumen National Agrarian University, Peru fermentation profile and thus the possibility of reducing CH4 emissions from forage-based Reviewed by: systems. We aimed to assess the in vitro ruminal fermentation profile, including CH4 Xiomara Gaviria Uribe, National University of Colombia, production, of the top stratum of Kikuyu grass (Cenchrus clandestinus - Hochst. ex Medellin, Colombia Chiov) harvested at different sward heights (10, 15, 20, 25, and 30 cm). Herbage samples Maria Denisse Montoya Flores, (incubating substrate) were analyzed for their chemical composition, in vitro organic Instituto Nacional de Investigación Forestal, Agropecuaria matter digestibility (IVOMD), and morphological components. In vitro incubations were (INIFAP), Mexico performed under a randomized complete block design with four independent runs of Sara Stephanie Valencia Salazar, The South Border College each treatment. Gas production (GP), in vitro dry matter digestibility (IVDMD), CH4 (ECOSUR), Mexico production, total volatile fatty acid (VFA) concentration, and their acetate, propionate, *Correspondence: and butyrate proportions were measured following 24 and 48 h of incubation. Herbage Alejandra Marín samples had similar contents of organic matter, neutral detergent fiber, and crude protein amaring@unal.edu.co for all treatments. However, a higher acid detergent fiber (ADF) content in taller sward Specialty section: heights than in smaller sward heights and a tendency for metabolizable energy (ME) This article was submitted to and IVOMD to decrease as sward height increased were found. Similarly, the stem + Climate-Smart Food Systems, a section of the journal sheath mass tended to increase with increasing sward height. Amongst the nutrients, Frontiers in Sustainable Food Systems ME (r = −0.65) and IVDMD (r = −0.64) were negatively correlated with sward height Received: 18 March 2021 (p < 0.001) and ADF was positively correlated with sward height (r = 0.73, p < 0.001). Accepted: 29 October 2021 Both the GP and IVDMD were negatively related to the sward height at both incubation Published: 01 December 2021 times. Sward heights of Kikuyu grass below 30 cm display an in vitro profile of VFAs high Citation: Marín A, Bindelle J, Zubieta ÁS, in propionate and low in acetate, with a trend toward lower methane production of CH4 Correa G, Arango J, Chirinda N and per unit of IVDMD. These findings are important to aid decision-making on the optimal de Faccio Carvalho PC (2021) In vitro Fermentation Profile and Methane sward height of Kikuyu grass and manage animal grazing with the opportunity to reduce Production of Kikuyu Grass Harvested CH4 production. at Different Sward Heights. Front. Sustain. Food Syst. 5:682653. Keywords: methane mitigation strategy, methanogenic potential, sward structure, tropical grass, forage nutritive doi: 10.3389/fsufs.2021.682653 value, grazing management Frontiers in Sustainable Food Systems | www.frontiersin.org 1137 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards INTRODUCTION correctly, Kikuyu grass is recognized for its moderate to good quality and high yield potential, especially in high-fertility soils Livestock is under fire of critics for its major share in the (Reeves et al., 1996; Fulkerson et al., 2006; García et al., 2014). environmental impact of the agricultural sector. Total global Commonly, grazing management goals of Kikuyu grass are greenhouse gas (GHG) emissions from livestock (animals, based on plant characteristics associated with the regrowth age, manure, feed production, and land-use change) are estimated to phenological state, leaf stage, critical leaf area index, among account for 14.5% of total anthropogenic emissions (Gerber et al., others (Reeves et al., 1996; Fulkerson andDonaghy, 2001; Schmitt 2013). Among livestock production systems, grassland-based et al., 2019b). Currently, and for several forage species, including ruminants are themost controversial in the present-day literature Kikuyu grass, the sward height is proposed as an easy-to-use (Teague et al., 2016; Gerssen-Gondelach et al., 2017). On the one grazing management criterion and a key performance predictor hand, ruminants produce methane (CH4) as a natural byproduct (Marin et al., 2017; de Souza Filho et al., 2019; Kunrath et al., of microbial fermentation of feed in the rumen, contributing 2020), as there is a strong relationship with the quantity and approximately 6% of the global anthropogenic GHG emissions quality of the herbage that animals ingest. On the other hand, in (40% of all livestock emissions; Gerber et al., 2013; Beauchemin vitro studies may predict enteric CH4 production with reasonable et al., 2020). On the other hand, grazed pastures which are accuracy and precision (Danielsson et al., 2017) and can help the basis of those systems, when properly managed, potentially to identify promising strategies for in vivo studies oriented to improve the sustainability of livestock production (Lobato et al., reduce the environmental impact of livestock (Danielsson et al., 2014; Elgersma, 2015; French et al., 2015), provide many social 2017; Valencia Echavarria et al., 2019; Molina-Botero et al., 2020). and environmental services (Werling et al., 2014; Mottet et al., Previous studies examined the effects of stage of regrowth on the 2017; Horrocks et al., 2019; Zubieta et al., 2020), and improve nutritive value of whole plants of Kikuyu pastures and on the soil health indicators in tropical systems (Teutscherová et al., in vitro fermentation parameters (Ramírez et al., 2015; Vargas 2021). Hence, current grazing systems are being redesigned to et al., 2018). Basic and key information regarding the sward link animal production with environmental management (Boval height relationship with the nutritive attributes of Kikuyu grass and Dixon, 2012; Carvalho, 2013) in light of current demands for and the main ruminal fermentation parameters, including CH4 sustainable agricultural production around the world (Herrero production, has not yet been established. et al., 2010; Mottet et al., 2017). We hypothesized that the top stratum of the Kikuyu grass The profitability and sustainability of forage-based dairy harvested at intermediate sward heights (15, 20, and 25 cm) has systems depend on efficient management (Herrero et al., highly digestible leaves and displays an in vitro low-CH4 rumen 2000). In this regard, grazing management is of particular fermentation profile with similar chemical and sward structural importance since when properly managed, it can improve the characteristics. Thus, this study aimed to assess the effect of the quantity and quality of herbage consumed by the animals sward height of Kikuyu grass from herbage samples of the top and ultimately reduce CH4 emissions (Congio et al., 2018; stratum (incubating substrate that reflects the potentially grazed Savian et al., 2018, 2021). Previous studies have shown that the stratum) on the in vitro ruminal fermentation profile. We also sward height is a useful and reliable tool to optimize pasture evaluated the in vitro CH4 production and identified the sward management (Carvalho et al., 2011; Kunrath et al., 2020). The heights that may offer the largest opportunity to mitigate enteric literature suggests that under moderate- to low-intensity grazing CH4 production from grazing cattle fed with Kikuyu grass. management, animals ingest a diet with high nutritive value composed primarily of leaf lamina from the top stratum of the sward (Savian et al., 2018, 2020; Zubieta et al., 2021). Likewise, MATERIALS AND METHODS it is well known that diet digestibility declines from the top to the bottom of the sward, showing a vertical quality gradient of Origin of Herbage Material forages (Delagarde et al., 2000; Benvenutti et al., 2016, 2020). Herbage samples for the in vitro incubations were produced Moreover, as pasture matures, the sward height increases and the within a grazing trial with dairy heifers at the Agricultural nutritive value decreases (Benvenutti et al., 2020). High forage Research and Rural Extension Company of Santa Catarina digestibility is associated with a fermentation profile in the rumen (EPAGRI), municipality of Lages, S.C., Brazil (27◦47′10.5′′S, that is unfavorable to CH4 production (Hristov et al., 2013; 50◦18′20.5′′W, 937m a.s.l.). According to Köppen’s climate Muñoz et al., 2016). Therefore, if grazed herbage is the main classification, the region is humid subtropical under oceanic source of nutrients for animals, it is pivotal to offer a highly influences. It has an annual average temperature of 17◦C and digestible forage that may have a high potential for mitigating annual average precipitation of 1460mm (Alvares et al., 2013). enteric CH4 emissions. The soil was classified as Humudept (with an umbric epipedon) Kikuyu grass (Cenchrus clandestinus - Hochst. ex Chiov), according to the USDA Soil Taxonomy (Soil Survey Staff, 2014). widely known as Pennisetum clandestinum Hochst, is a highly The soil is developed from sedimentary rocks (sandstone and productive subtropical grass of African origin that is well adapted siltstone) and has an acidic pH, high aluminum content and low to the forage-based dairy systems of some countries of Latin sum and base saturation (Rauber et al., 2021). and Central America (e.g., Colombia, Brazil, and Mexico) and The grazing trial was carried out in a 5000-m2 permanent Oceania [e.g., Australia and New Zealand; (García et al., 2014; pasture of Kikuyu grass (Cenchrus clandestinus - Hochst. ex Sbrissia et al., 2018; Marín-Santana et al., 2020)]. When managed Chiov) established in the early 1990s and grazed by dairy and Frontiers in Sustainable Food Systems | www.frontiersin.org 1238 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards beef cattle since then. The whole area wasmowed homogeneously Chemical Composition and in vitro Organic until 5 cm of height and divided into ten paddocks of 500 ± Matter Digestibility 5 m2. Fertilizers were split into two applications depending on The herbage samples were analyzed in duplicate for dry matter rainfall occurrence and considering a two-period evaluation. The (DM, method 930.04; AOAC, 2016), ash (method 930.05; AOAC, pasture received one application of 250 kg/ha of fertilizer (N- 2016), and for neutral detergent fiber (NDF) and acid detergent P-K, 9–33–12) and 135 kg/ha of urea on 26 January 2017 (first fiber (ADF) (Van Soest et al., 1991) by using an Ankom 200 evaluation period). On 22 March 2017, 67.5 kg/ha of urea was fiber analyzer without heat-stable alpha-amylase. ADF and NDF applied (second evaluation period). Due to the frost event and procedures are not ash-free. Samples were also characterized for low temperatures in winter and sometimes in spring, the Kikuyu N content by the Kjeldahl digestion. The crude protein amount growth season is from the final period of spring and early autumn was calculated as N × 6.25 (N, method 984.13; AOAC, 2016). (Sbrissia et al., 2018); therefore, the herbage collection in both The two-stage Tilley and Terry (1963) technique (incubation periods lasted from 28 Feb to 15 Apr 2017. with rumen fluid followed by acid-pepsin digestion) was used to estimate the in vitro organic matter digestibility (IVOMD). The Treatments and Experimental Design total digestible nutrient (TDN) concentration of the simulated Treatments consisted of herbage samples from the top stratum grazing samples was estimated as a percentage of IVOMD of Kikuyu grass harvested at five sward heights (10, 15, 20, 25, (Moore et al., 1999). The metabolizable energy (ME) were and 30 cm). The grazing trial was conducted in a randomized estimated using the following equations of NRC (NRC, 2001): DE complete block design with two spatial (paddocks) and two (Mcal/kg) = 0.04409 × TDN (%), and ME (Mcal/kg) = 1.01 × temporal (morning or afternoon) replicates. The blocking DE (Mcal/kg)−0.45. criterion was the time of day due to differences that may exist in the herbage chemical composition and dry matter yield within a day (Delagarde et al., 2000; Gregorini, 2012). Each sward height In vitro Ruminal Fermentation of the Kikuyu grass was randomly assigned in two paddocks, Procedures involving animals were carried out in accordance each one evaluated once in the morning and once in the with the relevant guidelines, regulations, and requirements of afternoon (two periods of evaluation), in an alternated scheme Colombian law No 84/1989 and the following protocol, approved with random start. Once target sward height was achieved after by the Ethics Committee of the International Center for Tropical the initial mowing and before to start a grazing assessment, Agriculture (CIAT). herbage sampling was performed (i.e., in the morning, period The in vitro incubations were conducted according to one). After that, the sward was mowed again to half of the Theodorou et al. (1994) in the Forage Quality and Animal treatment sward height (residuals were retired), and when it Nutrition Laboratory (certified by the FAO-IAG proficiency test reached the set sward height again, a second herbage sampling of feed constituents 2017 including in vitro gas production) was conducted (i.e., in the afternoon, period two). A total of at CIAT located in the Valle del Cauca department, Colombia (3◦29′34′′four herbage samples from the top stratum per treatment were N, 76◦21′37′′W, 965m a.s.l.). Rumen fluid was collected collected for in vitro incubations. at 7:30 am from two rumen-fistulated Bos indicus Brahman steers The in vitro incubation experimental design was carried with an average body weight of 720 ± 42 kg, which were grazed out through four independent runs of each treatment, two on Cynodon plectostachyus (star grass) pasture, with free access to ruminal liquids from steers (unmixed), and two independent sets water and mineral salts. corresponding to 24 and 48 h of incubation. In addition, four The rumen fluid was filtered using a 250µm nylon pore size blanks (no substrate) for each incubation time were included. cloth, dispensed into two thermal flasks prewarmed to 39 ± 0.5◦C, and immediately transferred to the laboratory. The time between rumen fluid collection and inoculation did not exceed Sward Measurement and Herbage 30min. Five-hundred milligrams of each herbage sample (DM Sampling basis) was incubated in 160mL glass bottles, prewarmed in an The sward height was measured at 150 random points per incubator at 39◦C, with 20mL filtered rumen fluid mixed with paddock using a sward stick (Barthram, 1985). When the 80mL rumen medium in a 1:4 ratio (Menke and Steingass, treatment sward height of individual paddocks was confirmed, 1988), and dispensed with continuous flushing of CO2. The metallic quadrants (0.25m2) were placed at three random sites; bottles were slightly stirred, sealed with rubber stoppers and average sward heights were calculated from five readings taken aluminum caps, and incubated in a water bath at 39◦C in two inside the quadrants with the sward stick to perform herbage different sets corresponding to incubation times of 24 and 48 h. clipping at half of the canopy height (samples representing the Four blanks of rumen medium (bottles without substrate that grazing stratum). Half of the herbage samples were separated contained only inoculum and medium) per each set were also into morphological components (leaf lamina, stem+ sheath, and incubated. The gas production was measured at 3, 6, 9, 12, deadmaterial) and dried in a forced-air oven at 55◦C for 72 h. The 24, and 48 h using a pressure transducer (Lutron Electronic dry weights of morphological components were used to calculate Enterprise Co. Ltd., Taipei, Taiwan) connected to a digital wide- total herbage mass (kg DM/ha) as the sum of each component’s range manometer (Sper Scientific, Arizona, USA) and a 60mL mass. The other half was also dried and then pooled per paddock syringe through a three-way valve (Theodorou et al., 1994). and time of the day for chemical analysis and in vitro incubations. After each measurement, the gas of the bottles was released Frontiers in Sustainable Food Systems | www.frontiersin.org 139 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards to avoid partial dissolution of CO2 (Tagliapietra et al., 2010) variable, µ is the overall mean, αi treatments (herbage samples and possible disturbance of microbial activity (Theodorou et al., from the top stratum), βj is the effect of the block (time of the 1994). Cumulative pressure values were converted into volume day), and ǫijk is the residual error. HSD Tukey’s test was used (GP, mL) from measured pressure changes at incubation times to compare means among treatments; significance was declared and after correction for blank pressure values using the ideal gas at p ≤ 0.05 and tendencies at 0.05 < p ≤ 0.10. The nutritive law and expressed per unit of dry matter incubated (DMi) and in value (NDF, ADF, CP, ME, IVDMD) and in vitro fermentation vitro dry matter degraded (IVDMD) (López et al., 2007). parameter (GP, acetate, propionate, and butyrate) results were submitted to Pearson’s correlations and visualized using the R In vitro Methane Production and package corrplot (Wei et al., 2017). Calculations The in vitro fermentation data were analyzed as linear (Y = Methane (CH4) analyses were carried out in the Greenhouse Gas β0+ β1SH+ ε), quadratic (Y = β0+ β1SH+β2SH2+ε), and a Laboratory CIAT. A gas sample in the headspace was collected double linear function of sward height (Y = f{p+ a1× (SH− v), into a 5mL vacuum vial (Labco Ltd., High Wycombe, England) p + a2 × (SH − v)}), where Y is IVDMD, GP, in vitro CH4, VFA at 24 and 48 h. The CH4 concentration was determined using a (acetate, propionate, and butyrate), f is the min or max function, gas chromatograph (Shimadzu GC-2014, Kyoto, Japan) equipped v and p are the coordinates of the crossing point of sward height, with a Hayesep N packed column (0.5m × 1/8" × 2mm ID) SH are the observed values of sward height, and a1 and a2 and flame ionization detector (FID). The operating temperatures are the slopes of the component lines adapted from Mezzalira of the column, detector, methanizer, and valves were 80, 250, et al. (2017). Linear and quadratic regression models were fitted 380, and 80◦C respectively. Ultrahigh purity 5.0-grade N was by using R lm{stats} function and double linear models were used as the carrier gas with a linear velocity of 35 mL/min. The fitted by deviance minimization with the optim{stats} function. CH4 concentration was calculated using a standard of 10% CH4 After fitting a regression model, the residual plots were checked balanced in N (Scott-Marrin Inc., Riverside, CA) and corrected and the Shapiro–Wilk test was carried out using the R function for the CH4 blank values. The volume of CH4 (mL) produced shapiro.teststats. The best model was selected by the smaller value at the end of each incubation time (24 and 48 h) was calculated of Akaike’s information criterion (AIC). The objective of the as a product of the total gas produced (mL) multiplied by the regression analysis was to understand how the nutritive value concentration of CH4 (%) in the analyzed sample, as described of the top stratum of Kikuyu grass, harvested at different sward by Lopez and Newbold (2007). heights, influences the in vitro ruminal fermentation profile. Volatile Fatty Acids and in vitro dry Matter RESULTS Digestibility Following 24 and 48 h of incubation, the fermentation was Sward Characteristics and Chemical stopped by dipping the bottles in cold water with ice and then Composition of the Herbage Incubated processing to determine volatile fatty acids (VFAs) and the in The sward heights obtained were close to the nominal treatment vitro digestibility of dry matter (IVDMD). Ruminal fluid samples heights and different between treatments (p < 0.001, Table 1). (10mL) were centrifuged at 3000 rpm for 10min at 4◦C. The Herbage mass in 10 cm swards was less than in the 30 cm swards supernatant (1.6mL) was transferred into a 2mL Eppendorf tube, but did not differ among the other sward heights. The 25 and and 0.4mL ofmetaphosphoric acid (25%w/v) was added for VFA 30 cm sward heights resulted in a higher green leaf mass than analysis. Samples were then stored frozen at −20◦C and later the 10 cm sward height (p < 0.01) but did not differ between 15 analyzed for acetate, propionate, and butyrate concentrations and 20 cm (p > 0.05, Table 1). The stem+ sheath mass tended to by high-performance liquid chromatography (HPLC) with an increase with increasing sward height (p= 0.09, Table 1). SPD-20AV UV-VIS detector (SHIMADZU, Prominence UFLC No differences were found for OM, NDF, and CP contents (p System) fitted with a BIO-RAD Aminex HPX-87H, 300 × > 0.05, Table 2), however, the ADF concentration was greater 7.8mm Ion Exclusion Column. The total VFA concentration was at 30 cm sward heights than at 10 cm sward heights, but not calculated as the sum of the individual VFA concentrations in different from other sward heights (p = 0.02, Table 2). The the ruminal fluid and was corrected for the blank values. Based IVOMD andME tended to decrease with increasing sward height on the obtained results, the proportion of each VFA in the total (p= 0.16 and p= 0.10, respectively; Table 2). VFA amount was calculated. The acetic: propionic ratio was also calculated. All contents remaining in the bottle were finally Relationship Between Sward Height, filtered through preweighed sintered glass crucible pore number 1 (Pyrex©R ) and dried in a forced-air oven at 105◦C for 24 h to Chemical Composition, and in vitro determine the IVDMD. Fermentation Parameters The correlation values among the sward height, nutritive value Statistical Analysis and in vitro fermentation parameters at 48 h are presented All statistical analyses were performed using R 3.5.3 (R in Figure 1. The sward height showed a moderate negative Core Team, 2018). Herbage chemical composition and sward correlation with IVDMD (r = −0.64), GP (r = −0.46), CP characteristics were analyzed with ANOVA in a randomized (r = −0.45), and ME (r = −0.65). Conversely, a high and block design: Yijk = µ+ αi+βj+εijk, where: Yijk is the response positive correlation (r = 0.73) between the ADF (g/kg) and Frontiers in Sustainable Food Systems | www.frontiersin.org 140 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards TABLE 1 | Sward characteristics of herbage samples from the top stratum of five Kikuyu sward height. Item Sward heights (cm) p-value SEM 10 15 20 25 30 Sward height (cm) 9.8e 15.1d 20.1c 24.3b 31.3a <0.0001 0.51 Herbage mass (kg DM/ha) 426.0b 502.0ab 796.0ab 870.3ab 950.3a 0.01 107.2 Green leaf mass (kg DM/ha) 363.9b 463.1ab 737.4ab 791.3a 842.8a 0.01 93.6 Stem + sheath mass (kg DM/ha) 31.9 24.25 52.94 73.88 91.1 0.09 18.0 Common superscript letters among the same row denote non-significant difference at 0.05 level, as determined by HSD Tukey’s test. DM, dry matter; S.E.M, standard error of the mean. TABLE 2 | Chemical composition and in vitro organic matter digestibility (IVOMD) of herbage samples from the top stratum of five Kikuyu sward heights. Item Sward heights (cm) p-value SEM 10 15 20 25 30 DM (g/kg of DM) 923.7 913.0 918.0 923.9 919.8 0.10 2.8 OM (g/kg of OM) 907.1 911.6 905.3 905.8 902.1 0.22 2.7 NDF (g/kg of DM) 535.9 541.9 543.1 541.1 545.6 0.98 11.0 ADF (g/kg of DM) 194.1b 198.7ab 210.9ab 213.1ab 218.8a 0.02 3.8 CP (g/kg of DM) 316.8 301.8 305.0 302.9 281.3 0.22 8.0 IVOMD (g/kg of OM) 686.6 657.5 635.1 610.7 592.3 0.16 31.0 ME (Mcal/kg of DM) 2.3 2.2 2.1 2.0 1.9 0.10 0.1 Common superscript letters among the same row denote non-significant difference at 0.05 level, as determined by HSD Tukey’s test. SEM, standard error of the mean; DM, dry matter; OM, organic matter; NDF, neutral detergent fiber; ADF, acid detergent fiber; CP, crude protein; IVOMD, in vitro organic matter digestibility; ME, metabolizable energy. sward height was observed (Figure 1). The GP exhibited a high different between 10 and 20 cm (a1 = −0.22 g mL/IVDMD/cm, positive correlation with IVDMD (r = 0.74) and ME (r = 0.62), p = 0.32), and then increased with the sward height (a2 = and at the same time, IVDMD was highly and positively related 0.61 g mL/IVDMD/cm, p = 0.02) (Figure 3A). Likewise, CH4 to ME (r = 0.84) (Figure 1). The total CH4 had a moderate production (mL/g IVDMD) at 48 h tended to increase linearly and positive correlation with GP (r = 0.39); however, it was as a function of sward height (Figure 3B). poorly related to the other variables evaluated. In addition, Meanwhile, the total VFA (mM/L) concentration did not acetic acid had a strong negative correlation with propionic acid differ between treatments for any incubation time, but it was close (r = −0.79, Figure 1). Pearson’s correlation of dataset at 24 h to double at 48 h relative to 24 h (data not shown). The main VFA (Supplementary Figure 1) and the correlation matrix at 24 and proportions, acetate, propionate, and butyrate (mol/100mol), 48 h (Supplementary Tables 1, 2, respectively). were unrelated to sward height at 24 h (data not shown) but significant changes were found after 48 h of incubation. Overall, The in vitro Fermentation Parameters the acetate, propionate, and acetate: propionate ratio following The GP, expressed as milliliters per unit of dry matter incubated 48 h of fermentation showed that the minimum methanogenic (mL/g DMi), and IVDMD (g) linearly decreased with sward profile occurred below 30 cm (Figures 4A,B,D). The acetate and height at both incubation times (24 and 48 h are shown propionate molar proportions and the acetate: propionate ratio in Figures 2A,B, respectively). However, when the GP was were well described by a double linear model (Figures 4A,B,D, expressed as milliliters per unit of in vitro digestible dry respectively). The relationship between acetate (mol/100mol) matter (mL/g IVDMD), it was not related to the sward height and sward height first described a straight line slightly inclined either at any incubation time (data not shown). There was no (a1 = −0.09 mol/100 mol/cm, p = 0.06) and after 28.4 cm tall, relationship between the total in vitroCH4 production, expressed it showed a steeper line with a higher and more significant in terms of milliliters per dry matter incubated (mL/g DMi), slope (a2 = 1.55 mol/100 mol/cm, p < 0.0001). Conversely, the and the sward heights studied at any incubation time (data not propionate (mol/100mol) first increased (increasing slope, a1 shown). However, after 24 h of fermentation, the in vitro CH4 = 0.20 mol/100 mol/cm, p = 0.002) until 28.42 cm and then production expressed as milliliters per unit of in vitro digestible decreased (decreasing slope, a2 = −1.34 mol/100 mol/cm, p < dry matter (mL/g IVDMD) fitted a double linear trend model 0.0001) with sward height. The butyrate showed a negative and (p = 0.060). The minimum value of CH4 production at 24 h linear fit as the sward heights increased (p < 0.0001, Figure 4C). (15.4 mL/g IVDMD) occurred at 21.3 cm (Figure 3A). CH4 The acetate: propionate ratio subtly decreased with sward height production, first described a straight line slightly inclined but not between 10 and 28.8 cm (decreasing slope, a1=−0.013 units/cm, Frontiers in Sustainable Food Systems | www.frontiersin.org 1541 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards FIGURE 1 | Correlation plot between the sward height, nutritive value, and in vitro fermentation parameters at 48 h of Kikuyu grass harvested at different sward heights (n = 36). Positive and negative correlation coefficients are displayed in blue and brown scale, respectively. Sward_height, (cm); NDF, neutral detergent fiber (g/kg of DM); ADF, acid detergent (g/kg of DM), CP, crude protein (g/kg of DM); ME, metabolizable energy Mcal/kg of DM; IVDMD, in vitro dry matter digestibility (g); GP, Gas production (mL/ g DMi). DMi, dry matter incubated. Methane (total in vitro CH4 production, ml), acetate, propionate, and butyrate (mol/100 mol). Significance level (*** p < 0.001, ** p < 0.01, and * p < 0.05). p = 0.004) and then increased at sward heights taller than FIGURE 2 | Relationship between gas production (GP, mL/g DMi; gray dots) 28.8 cm (increasing slope, a2 = 0.14 units/cm, p = 0.0001, and in vitro dry matter digestibility (IVDMD, g; black dots) and sward height Figure 4D). (SH, cm) of kikuyu grass. (A) include all data of GP and IVDMD at 24 h of fermentation (n = 40); equation for: GP = 110.74–0.90SH, p < 0.01), R2 = 0.12. IVDMD = 0.32–0.002SH, p < 0.0001, R2 = 0.40. (B) include all data of DISCUSSION GP and IVDMD at 48 h of fermentation (n = 40); equation for: GP = 177.42–1.19SH, p < 0.05, R2 = 0.16; IVDMD = 0.32–0.002SH, p < 0.0001, R2 = 0.32. DMi, dry matter incubated. Moderate to low-intensity grazing management strategies favor animals to select bites of the top stratum of plants, whose diet is mainly composed of highly digestible leaves with high CP and low fiber content (Savian et al., 2018; Zubieta et al., 2021). This study assessed the effect of the sward height of Sward Characteristics and Chemical Kikuyu grass from herbage samples of the top stratum on the Composition in vitro ruminal fermentation profile and its relationship with The chemical composition of herbage from the top stratum of the chemical composition and IVDMD. The key finding was that the Kikuyu grass showed many similarities between the sward the sward heights of Kikuyu grass below 30 cm display a profile heights. The overall tendency to decrease IVOMD and increase of VFAs high in propionate and low in acetate, with a trend ADF contents with sward height is consistent with the changes toward lower CH4 production per unit of IVDMD. Although the in the relative proportions of the leaves and stems + sheath chemical composition between the treatments was similar, the within the top stratum as the sward height increases. In swards tendency for stem and sheath mass to increase led to an increase of Cenchrus clandestinus, Schmitt et al. (2019a) observed that in ADF contents and a tendency to decrease the IVOMD with NDF and ADF contents of herbage samples from the upper sward height, shifting the fermentation profile toward an in vitro stratum did not change between 10 and 25 cm heights. Previous rumen environment more favorable to CH4 production at sward studies on the vertical distribution of chemical composition and heights above 28 cm. digestibility of a perennial ryegrass sward showed little variation Frontiers in Sustainable Food Systems | www.frontiersin.org 1642 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards of this species (Schmitt et al., 2019a). Nonetheless, when the nutritional value was evaluated by strata through the vertical distribution, the observed CP values were consistent with the CP content of the upper layer of the plant (Benvenutti et al., 2020). Previous studies have shown that the CP contents of leaves change significantly with anatomical characteristics along the length of leaf blades (Garcia et al., 2021). In addition to the high CP content of the upper stratum due to green leaves, the higher N levels due to fertilization could have influenced the results. According to Correa et al. (2008), the higher CP content (true protein and nonprotein nitrogen (NPN)) in highly fertilized Kikuyu swards is closely related to the higher amounts of ruminal ammonia (N-NH3) and lower N use efficiency. Even though high N fertilizer rates are common for Kikuyu ryegrass pasture systems, animal excreta on pasture can negatively affect the Nitrogen efficiency of the cows (Marais, 2001; Viljoen et al., 2020) and contribute to nitrous oxide (N2O) emissions (Maire et al., 2020). Relationship Between Chemical Constituents and in vitro Fermentation Parameters The strong and positive correlation between GP and the IVDMD at 48 h and the high and positive correlation between ME and GP and IVDMD were expected once GP was directly related to the amount of OM fermented by rumen bacteria, which is consistent with the principles of the in vitro gas production technique (Theodorou et al., 1994; Mauricio et al., 1999). It is widely known that GP can be a good index of forage ME content and provides an effective method for assessing the nutritive value of the feeds (Menke and Steingass, 1988). On the other hand, FIGURE 3 | Relationship between in vitro CH4 (mL/g IVDM) and sward height (SH, cm) of kikuyu grass. Equation for: CH the negative correlation between sward height and GP and 4 = min [15.4–0.22 (SH−21.3)], [(15.4+ 0.61 (SH−21.3)], p < 0.06, R2 = 0.11, following 24 (A); and CH4 = chemical components such as ME, IVDMD, CP and at the 20.1–0.26SH, p < 0.12, R2 = 0.04, following 48 (B). same time the positive correlation between sward height with the ADF is an interesting result; since the sward height has a consistent correlation with herbage mass and it is a practical and reliable indicator to optimize grazing management in NDF and organic matter digestibility at different regrowth (Carvalho et al., 2011; Kunrath et al., 2020). ages and at different times of the day (Delagarde et al., 2000). The chemical composition of forages is influenced by several Regardless of the regrowth age, leaves were located mainly in factors, including sward structure, stage of maturity, season of the top stratum, while steams were present mainly in the bottom harvest, and stratum harvested (Benvenutti et al., 2020; Marín- stratum of Kikuyu pastures; consequently, CP decreased, and Santana et al., 2020). In general, the correlations between pasture NDF and ADF increased with age of regrowth and from top chemical components and in vitro fermentation parameters in to bottom of the swards (Benvenutti et al., 2020). For a given this study are consistent with previous studies with tropical stratum of the sward, the differences between regrowth age are grasses (Bezabih et al., 2014; Kulivand and Kafilzadeh, 2015), commonly more marked between vegetative and reproductive and with other studies using different types of feeds and stages (Schmitt et al., 2019a; Benvenutti et al., 2020). In the forages (Getachew et al., 2004). However, unlike expected, CH4 vegetative stage, the nutritive value differs little among plant parts production had a poor and negative relationship with NDF (Laca et al., 2001; Benvenutti et al., 2020). and ADF content. This discrepancy is probably due to the The results concerning the NDF, ADF, CP, ME, and IVOMD high variability of CH4 data at both incubation times. The are consistent with those values found from the upper stratum highly significant correlation between ME and butyrate and of the Kikuyu sward (Benvenutti et al., 2020). However, CP the negative relationship between ADF and butyrate indicate exhibited higher values than usually reported for the whole plant the contribution of these components to VFA production (Correa et al., 2008; García et al., 2014) or the upper stratum (Ungerfeld, 2015). Frontiers in Sustainable Food Systems | www.frontiersin.org 1743 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards FIGURE 4 | Relationship between VFAs (mol/100mol) and acetate to propionate ratio with sward height (SH, cm) of kikuyu grass following 48 h of fermentation. Equation for: Acetate = min [59.33–0.09 (SH−28.4)], [59.33 + 1.55 (SH−28.4)], p < 0.0001, R2 = 0.54, (A); Propionate = min [35.04 + 0.20 (SH−28.42)], [35.04–1.34 (SH – 28.42)], p < 0.001, R2 = 0.30, (B); Butyrate = 8.94–0.12SH, p < 0.0001, R2 = 0.34, (C); and Acetate: propionate ratio = min [1.70–0.013 (SH−28.8)], [1.70 + 0.14 (SH−28.8)], p < 0.0001, R2 = 0.44, (D). In vitro Fermentation Parameters acetate and lower propionate, and therefore a higher acetate: The sward height of Kikuyu grass influenced its nutritive value proportionate ratio and higher CH4 production per unit of and in vitro rumen fermentation profile. Since the stems+ sheath degraded dry matter (Boadi et al., 2002; Beauchemin et al., 2008; mass tended to increase and IVOMD tended to decrease as a Navarro-Villa et al., 2011; Purcell et al., 2011). In our study, function of sward height, the GP and IVDMD also decreased. the GP reduction as a function of sward height may reflect a As stated above, in vitro gas production is a suitable indicator higher structural carbohydrate content at taller heights than at to predict the carbohydrate degradation of forages (Menke et al., shorter heights. Likewise, the trend toward lower in vitro CH4 1979; Theodorou et al., 1994; Danielsson et al., 2017). It is production with sward height is explained by the lower IVDMD widely accepted that the higher the IVDMD is, the higher as a function of sward height. Assessing the in vitro CH4 output the GP (Durmic et al., 2010; Meale et al., 2011). Consistently, from different maturity stages of Kikuyu grass, other studies have taller sward heights (>28 cm) displayed a higher methanogenic shown a lower CH4 production per unit of degraded organic profile than shorter (10 cm) and intermediate (15, 20, and matter (Vargas et al., 2018) and per gram of digestible dry matter 25 cm) sward heights due to the changes in morphological (Ramírez et al., 2015), in the youngest forages than in the most components and chemical composition, which resulted in a mature forages. higher acetate: propionate ratio at 48 h of fermentation. The The end products of in vitro ruminal fermentation, such as highest methanogenic profile of sward heights of Kikuyu grass the acetate, propionate, and butyrate proportions, are consistent above 28 cm, is due to the tendency of more stems + sheath with the data published by other authors (Burke et al., 2006; with the sward height, and the tendency of the ME and IVDMD Marín et al., 2014; Ramírez et al., 2015; Vargas et al., 2018) who diminished with the sward height. CH4 production in an in also evaluated the in vitro fermentation of Kikuyu grass. The vitro gas system is strongly associated with the fermentation of lack of differences found in the total VFA concentration and structural carbohydrates. It has been previously reported that the molar proportions of the main VFAs measured at 24 h may decreasing the digestibility of herbage and increasing the fiber be associated with subtle changes in the fermentation pathways content with advancing plant maturity influences not only total during the first h of fermentation. In agreement with (Meale et al., VFA production but also the molar proportions, with greater 2011), batch culture in vitro fermentation has a low sensitivity Frontiers in Sustainable Food Systems | www.frontiersin.org 1844 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards to elucidate small differences between the same type of substrate to 25 cm) may be a promising strategy to reduce CH4 emissions. (e.g., herbage) in the early fermentation. However, prolonged Further studies based on in vivomeasurements may be necessary incubation in a closed system potentially favors VFA production before practical application. changes and their proportions (Ungerfeld and Kohn, 2006), as observed at 48 h. The high molar proportion of acetate and the DATA AVAILABILITY STATEMENT low of propionate in Kikuyu pastures harvested above 28 cm of sward height matched with a tendency toward more in vitro The raw data supporting the conclusions of this article will be CH4 output (mL/g IVDMD) and suggested a low in vitro rumen made available by the authors, without undue reservation. fermentation efficiency at tall sward heights. It is also widely known that forages that increase propionate and decrease acetate ETHICS STATEMENT are often associated with reducing ruminal CH4 production (Moss et al., 2000; Beauchemin et al., 2009; Meale et al., 2011). Procedures involving animals were carried out in accordance Nevertheless, the lower proportion of propionate at smaller with the relevant guidelines, regulations, and requirements of heights was unexpected due to the similarities of the chemical Colombian Law No 84/1989 and following protocol, approved composition and IVDMD at sward heights below 25 cm. A by the Ethics Committee of the International Center for Tropical possible explanation of this finding could be related to the Agriculture (CIAT). increase in butyrate concentration at the expense of propionate, as the sward height increases. In this study, the butyrate seems to AUTHOR CONTRIBUTIONS have acted as an alternative H2 sink (Moss et al., 2000; Ungerfeld, 2015), which is also in agreement with the trend toward lower AM, JB, AZ, and PF: conceptualization and methodology. AM CH4 production per unit of IVDMD (mL/g IVDMD) at sward and GC: performed the statistical analysis. AM: writing – heights below 28 cm. Changes in the fermentation pathways original draft preparation. AM, JB, AZ, PF, GC, JA, and NC: could be associated with superior CP concentrations and, writing – review & editing. JB, PF, and JA: supervision. JA: probably, with the higher nitrate concentration in the evaluated project administration. PF, NC, and JA: funding acquisition. Kikuyu structures as a product of the high N fertilization of All authors contributed to the article and approved the the Kikuyu, as suggested by Lovett et al. (2004). Nitrate is an submitted version. alternative H2 sink and an effective inhibitor of methanogenesis (McAllister and Newbold, 2008; Van Zijderveld et al., 2010; Yang FUNDING et al., 2016; Patra et al., 2017). Other studies have suggested that the inclusion of nitrate in in vitro ruminal fermentation could This research was funded by a doctoral grant from Colciencias increase the molar proportion of acetic acid and reduce the molar Scholarship Program No. 647 of Colombia. This study also was proportion of propionic acid (Navarro-Villa et al., 2011). funded by the Company of Agricultural Research and Rural The similar chemical composition of herbage samples from Extension of Santa Catarina (EPAGRI) through the CNPq, swards heights of 10, 15, 20, and 25 cm in this study MDA/CNPq Edital 38/2014 (Proceso CNPq 472977/2014-8) of suggests an in vitro rumen environment less favorable to Brazil and by the International Center for Tropical Agriculture CH4 production, therefore the possibility of flexible grazing (CIAT) as part of the Livestock CGIAR Research Program (CRP), management. However, Kikuyu swards managed with the 10 cm and by the LivestockPlus project and CLIFF program funded sward height target could result in low herbage and green leaf by the CRP on Climate Change, Agriculture and Food Security mass, which may affect herbage intake and animal performance (CCAFS). For details, please visit https://ccafs.cgiar.org/donors. (Marin et al., 2017; Schmitt et al., 2019b). Therefore, grazing managers must make strategic decisions considering a holistic ACKNOWLEDGMENTS management framework. Another important consideration is that in vitro CH4 We are grateful to those who assisted with data collection, production may not reflect the in vivo conditions and should supported our animal facilities, or provided technical support be interpreted with care (McAllister et al., 2011; Klop et al., with our experimental design. We are thankful to the Grazing 2017). Therefore, it is recommended to carry out long-term Ecology Research Group from UFRGS, Brazil, for all their grazing studies that include in vivo CH4 and dry matter intake guidance with data analysis and feedback and the Forage Quality measurements (Yáñez-Ruiz et al., 2016). and Animal Nutrition Laboratory at the International Center for Tropical Agriculture (CIAT) for facilitating work at their CONCLUSIONS respective research facilities. We conclude that Kikuyu grass harvested below 30 cm displays SUPPLEMENTARY MATERIAL an in vitro profile of VFAs high in propionate and low in acetate, with a performance less favorable to CH4 production per unit of The Supplementary Material for this article can be found IVDMD. Our findings suggest that grazing management sward online at: https://www.frontiersin.org/articles/10.3389/fsufs. height targets of Kikuyu grass at intermediate sward heights (15 2021.682653/full#supplementary-material Frontiers in Sustainable Food Systems | www.frontiersin.org 1945 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards REFERENCES Delagarde, R., Peyraud, J. L., Delaby, L., and Faverdin, P. (2000). Vertical distribution of biomass, chemical composition and pepsin—-cellulase Alvares, C. A., Stape, J. L., Sentelhas, P. C., de Moraes Gonçalves, J. L., and digestibility in a perennial ryegrass sward: interaction with month of Sparovek, G. (2013). Köppen’s climate classification map for Brazil. Meteorol. year, regrowth age and time of day. Anim. Feed Sci. Technol. 84, 49–68. Zeitschrift 22, 711–728. doi: 10.1127/0941-2948/2013/0507 doi: 10.1016/S0377-8401(00)00114-0 AOAC (2016). Official Methods of Analysis. 20th ed., ed. AOAC International Durmic, Z., Hutton, P., Revell, D. K., Emms, J., Hughes, S., and Vercoe, P. E. Rockville, Maryland, USA. (2010). In vitro fermentative traits of Australian woody perennial plant species Barthram, G. T. (1985). Experimental techniques: the HFRO sward stick. In: that may be considered as potential sources of feed for grazing ruminants. Biennial Report of the Hill Farming Research Organization. ed. M. M. Alcock Anim. Feed Sci. Technol. 160, 98–109. doi: 10.1016/j.anifeedsci.2010.07.006 Midlothian, UK. p. 29–30. Elgersma, A. (2015). Grazing increases the unsaturated fatty acid concentration Beauchemin, K., McAllister, T. A., and McGinn, S. M. (2009). Dietary mitigation of milk from grass-fed cows: A review of the contributing factors, of enteric methane from cattle. CAB Rev. Perspect. Agric. Vet. Sci. Nutr. Nat. challenges and future perspectives. Eur. J. Lipid Sci. Technol. 117, 1345–1369. Resour. 4, 1–18. doi: 10.1079/PAVSNNR20094035 doi: 10.1002/ejlt.201400469 Beauchemin, K. A., Kreuzer, M., O’Mara, F., and McAllister, T. A. (2008). French, P., O’Brien, B., and Shalloo, L. (2015). Development and adoption of Nutritional management for enteric methane abatement: a review. Aust. J. Exp. new technologies to increase the efficiency and sustainability of pasture-based Agric. 48, 21–27. doi: 10.1071/EA07199 systems. Anim. Prod. Sci. 55, 931. doi: 10.1071/AN14896 Beauchemin, K. A., Ungerfeld, E. M., Eckard, R. J., and Wang, M. (2020). Fulkerson, W. J., and Donaghy, D. J. (2001). Plant-soluble carbohydrate reserves Review: fifty years of research on rumen methanogenesis: Lessons and senescence - key criteria for developing an effective grazing management learned and future challenges for mitigation. Animal. 14, S2–S16. system for ryegrass-based pastures: a review. Aust. J. Exp. Agric. 41, 261. doi: 10.1017/S1751731119003100 doi: 10.1071/EA00062 Benvenutti, M. A., Findsen, C., Savian, J. V., Mayer, D. G., and Barber, D. G. (2020). Fulkerson, W. J., Neal, J. S., Clark, C. F., Horadagoda, A., Nandra, K. S., and The effect of stage of regrowth on the physical composition and nutritive value Barchia, I. (2006). Nutritive value of forage species grown in the warm of the various vertical strata of kikuyu (Cenchrus clandestinus) pastures. Trop. temperate climate of Australia for dairy cows: Grasses and legumes. Livest. Sci. Grasslands-Forrajes Trop. 8, 141–146. doi: 10.17138/tgft(8)141-146 107, 253–264. doi: 10.1016/j.livsci.2006.09.029 Benvenutti, M. A., Pavetti, D. R., Poppi, D. P., Gordon, I. J., and Cangiano, C. Garcia, L. F., Silva, G. P., Geremia, E. V., Goulart, L. B. L., Dias, C. T. D. S., and da A. (2016). Defoliation patterns and their implications for the management of Silva, S. C. (2021). Central rib and the nutritive value of leaves in forage grasses. vegetative tropical pastures to control intake and diet quality by cattle. Grass Sci. Rep. 11, 5440. doi: 10.1038/s41598-021-84844-z Forage Sci. 71, 424–436. doi: 10.1111/gfs.12186 García, S. C., Islam, M. R., Clark, C. E. F., and Martin, P. M. (2014). Kikuyu- Bezabih, M., Pellikaan, W. F., Tolera, A., Khan, N. A., and Hendriks, W. H. (2014). based pasture for dairy production: a review. Crop Pasture Sci. 65, 787. Chemical composition and in vitro total gas and methane production of forage doi: 10.1071/CP13414 species from the Mid Rift Valley grasslands of Ethiopia. Grass Forage Sci. 69, Gerber, P. J., Steinfeld, H., Henderson, B., Mottet, A., Opio, C., Dijkman, J., et al. 635–643. doi: 10.1111/gfs.12091 (2013). Tackling Climate Change Through Livestock - A Global Assessment Boadi, D. A., Wittenberg, K. M., and McCaughey, W. (2002). Effects of grain of Emissions and Mitigation Opportunities. eds. Gerber, P.J., Steinfeld, H., supplementation on methane production of grazing steers using the sulphur Henderson, B., Mottet, A., Opio, C., Dijkman, J., Falcucci, A. T. Roma: FAO. (SF6) tracer gas technique.Can. J. Anim. Sci. 82, 151–157. doi: 10.4141/A01-038 Available online at: https://www.fao.org/3/i3437e/i3437e.pdf (accessed October Boval, M., and Dixon, R. M. (2012). The importance of grasslands for animal 18, 2021). production and other functions: a review on management and methodological Gerssen-Gondelach, S. J., Lauwerijssen, R. B., Havlík, P., Herrero, M., Valin, H., progress in the tropics. Animal 6, 748–762. doi: 10.1017/S1751731112000304 Faaij, A. P. C., et al. (2017). Intensification pathways for beef and dairy cattle Burke, J. L., Waghor, G. C., Brookes, I. M., Chaves, A. V., and Attwood, G. T. production systems: Impacts on GHG emissions, land occupation and land use (2006). In vitro production of volatile fatty acids from forages. In: Proceedings- change. Agric. Ecosyst. Environ. 240, 135–147. doi: 10.1016/j.agee.2017.02.012 New Zealand Society of Animal Production (New Zealand Society of Animal Getachew, G., Robinson, P. H., DePeters, E. J., and Taylor, S. J. (2004). Production; 1999), p. 50. Relationships between chemical composition, dry matter degradation and in Carvalho, P. C. F. (2013). Harry stobbs memorial lecture: can grazing behaviour vitro gas production of several ruminant feeds. Anim. Feed Sci. Technol. 111, support innovations in grassland management? In 22nd Trop. Grassl. (Sidney, 57–71. doi: 10.1016/S0377-8401(03)00217-7 Australia) p. 137–155. doi: 10.17138/TGFT(1)137-155 Gregorini, P. (2012). Diurnal grazing pattern: Its physiological basis and strategic Carvalho, P. C. F., Barro, R. S., Kunrath, T. R., Silva, F. D., Da, Barth Neto, A., management. Anim. Prod. Sci. 52, 416–430. doi: 10.1071/AN11250 Savian, J. V., et al. (2011). Experiências de integração lavoura-pecuária no Rio Herrero, M., Fawcett, R. H., Silveira, V., Busqu,é, J., Bernués, A., and Dent, J. Grande do Sul. Synerg. Scyentifica p. 6. Available at: http://revistas.utfpr.edu.br/ B. (2000). Modelling the growth and utilisation of kikuyu grass (Pennisetum pb/index.php/SysScy/article/viewArticle/1432 (accessed November 10, 2021). clandestinum) under grazing. 1. Model definition and parameterisation. Agric. Congio, G. F. S., Batalha, C. D. A., Chiavegato, M. B., Berndt, A., Oliveira, P. Syst. 65, 73–97. doi: 10.1016/S0308-521X(00)00028-7 P. A., Frighetto, R. T. S., et al. (2018). Strategic grazing management towards Herrero, M., Thornton, P. K., Notenbaert, A. M., Wood, S., Msangi, S., sustainable intensification at tropical pasture-based dairy systems. Sci. Total Freeman, H. A., et al. (2010). Smart investments in sustainable food Environ. 636, 872–880. doi: 10.1016/j.scitotenv.2018.04.301 production: revisiting mixed crop-livestock systems. Science. 327, 822–825. Correa, H. J., Pabón, M. L., and Carulla, J. E. (2008). Valor nutricional del doi: 10.1126/science.1183725 pasto kikuyo (Pennisetum clandestinum Hoechst Ex Chiov.) para la producción Horrocks, C. A., Arango, J., Arevalo, A., Nuñez, J., Cardoso, J. A., and Dungait, J. de leche en Colombia (Una revisión): II. Contenido de energía, consumo, A. J. (2019). Smart forage selection could significantly improve soil health in the producción y eficiencia nutricional. Livest. Res. Rural Dev. 20:59. Available tropics. Sci. Total Environ. 688, 609–621. doi: 10.1016/j.scitotenv.2019.06.152 online at: http://www.lrrd.org/lrrd20/4/corr20061.htm (accessed February Hristov, A. N., Oh, J., Firkins, J. L., Dijkstra, J., Kebreab, E., Waghorn, G., et al. 18, 2020). (2013). Special topics — mitigation of methane and nitrous oxide emissions Danielsson, R., Ramin, M., Bertilsson, J., Lund, P., and Huhtanen, P. (2017). from animal operations: I. a review of enteric methane mitigation options1. J. Evaluation of a gas in vitro system for predicting methane production in vivo. Anim. Sci. 91, 5045–5069. doi: 10.2527/jas.2013-6583 J. Dairy Sci. 100, 8881–8894. doi: 10.3168/jds.2017-12675 Klop, G., van Laar-van Schuppen, S., Pellikaan, W. F., Hendriks, W. H., Bannink, de Souza Filho, W., Nunes, P. A., de, A., Barro, R. S., Kunrath, T. R., and de A., and Dijkstra, J. (2017). Changes in in vitro gas and methane production Almeida, G. M., Genro, T. C. M., et al. (2019). Mitigation of enteric methane from rumen fluid from dairy cows during adaptation to feed additives in vivo. emissions through pasture management in integrated crop-livestock systems: Animal 11, 591–599. doi: 10.1017/S1751731116002019 Trade-offs between animal performance and environmental impacts. J. Clean. Kulivand, M., and Kafilzadeh, F. (2015). Correlação entre a composição Prod. 213, 968–975. doi: 10.1016/j.jclepro.2018.12.245 química, cinética de fermentação e produção de metano de oito Frontiers in Sustainable Food Systems | www.frontiersin.org 1406 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards tipos de capim de pastagem. Acta Sci. - Anim. Sci. 37, 9–14. Molina-Botero, I. C., Mazabel, J., Arceo-Castillo, J., Urrea-Benítez, J. L., Olivera- doi: 10.4025/actascianimsci.v37i1.24336 Castillo, L., Barahona-Rosales, R., et al. (2020). Effect of the addition of Kunrath, T. R., de Nunes, P. A., de Souza Filho, W., Cadenazzi, M., and Bremm, Enterolobium cyclocarpum pods and Gliricidia sepium forage to Brachiaria C., Martins, A. P., et al. (2020). Sward height determines pasture production brizantha on dry matter degradation, volatile fatty acid concentration, and and animal performance in a long-term soybean-beef cattle integrated system. in vitro methane production. Trop. Anim. Health Prod. 52, 2787–2798. Agric. Syst. 177, 102716. doi: 10.1016/j.agsy.2019.102716 doi: 10.1007/s11250-020-02324-4 Laca, E. A., Shipley, L. A., and Reid, E. D. (2001). Structural anti-quality Moore, J. E., Brant, M. H., Kunkle, W. E., and Hopkins, D. I. (1999). Effects characteristics of range and pasture plants. J. Range Manag. 54, 413–419. of supplementation on voluntary forage intake, diet digestibility, and animal doi: 10.2307/4003112 performance. J. Anim. Sci. 77, 122–135. doi: 10.2527/1999.77suppl_2122x Lobato, J. F. P., Freitas, A.k., Devincenzi, T., Cardoso, L. L., Tarouco, J. U., Vieira, R. Moss, A. R., Jouany, J.-P., and Newbold, J. (2000). Methane production by M., et al. (2014). Brazilian beef produced on pastures: sustainable and healthy. ruminants: its contribution to global warming. Ann. Zootech. 49, 231–253. Meat Sci. 98, 336–345. doi: 10.1016/j.meatsci.2014.06.022 doi: 10.1051/animres:2000119 López, S., Dhanoa, M. S., Dijkstra, J., Bannink, A., Kebreab, E., and France, Mottet, A., de Haan, C., Falcucci, A., Tempio, G., Opio, C., and Gerber, P. (2017). J. (2007). Some methodological and analytical considerations regarding Livestock: on our plates or eating at our table? A new analysis of the feed/food application of the gas production technique. Anim. Feed Sci. Technol. 135, debate. Glob. Food Sec. 14, 1–8. doi: 10.1016/j.gfs.2017.01.001 139–156. doi: 10.1016/j.anifeedsci.2006.06.005 Muñoz, C., Letelier, P. A., Ungerfeld, E. M., Morales, J. M., Hube, S., and Pérez- Lopez, S., and Newbold, C. J. (2007). Analysis of methane. In:Measuring Methane Prieto, L. A. (2016). Effects of pregrazing herbage mass in late spring on enteric Production From Ruminants, p. 1–13. doi: 10.1007/978-1-4020-6133-2_1 methane emissions, dry matter intake, and milk production of dairy cows. J. Lovett, D. K., Bortolozzo, A., Conaghan, P., O’Kiely, P., and O’Mara, F. P. (2004). Dairy Sci. 99, 7945–7955. doi: 10.3168/jds.2016-10919 In vitro total and methane gas production as influenced by rate of nitrogen Navarro-Villa, A., O’Brien, M., López, S., Boland, T. M., and O’Kiely, P. (2011). In application, season of harvest and perennial ryegrass cultivar. Grass Forage Sci. vitro rumen methane output of red clover and perennial ryegrass assayed using 59, 227–232. doi: 10.1111/j.1365-2494.2004.00421.x the gas production technique (GPT). Anim. Feed Sci. Technol. 168, 152–164. Maire, J., Krol, D., Pasquier, D., Cowan, N., Skiba, U., Rees, R. M., et al. doi: 10.1016/j.anifeedsci.2011.04.091 (2020). Nitrogen fertiliser interactions with urine deposit affect nitrous NRC (2001). Nutrient Requirements of Dairy Cattle. 7th ed. Washington, D.C.: oxide emissions from grazed grasslands. Agric. Ecosyst. Environ. 290:106784. National Academies Press doi: 10.1016/j.agee.2019.106784 Patra, A., Park, T., Kim,M., and Yu, Z. (2017). Rumenmethanogens andmitigation Marais, J. P. (2001). Factors affecting the nutritive value of kikuyu grass of methane emission by anti-methanogenic compounds and substances. J. (Pennisetum clandestinum)- a review. Trop. Grassl. 35, 65–84. Anim. Sci. Biotechnol. 8:13. doi: 10.1186/s40104-017-0145-9 Marin, A., Baldissera, T., Pinto, C., Garagorry, F., Zubieta, A., Giraldo, L., et al. Purcell, P. J., O’Brien, M., Boland, T. M., and O’Kiely, P. (2011). In vitro (2017). Grazing management innovation as a strategy to improve animal rumen methane output of perennial ryegrass samples prepared by freeze production and reduce GHG emissions. In: CCAFS Info Note Wageningen, drying or thermal drying (40◦C). Anim. Feed Sci. Technol. 166, 175–182. Netherlands CGIAR Res. Progr. Clim. Chang. Agric. Food Secur. (CCAFS). doi: 10.1016/j.anifeedsci.2011.04.065 Available online at: https://hdl.handle.net/10568/89803 (accessed November R Core Team (2018). R: A language and environment for statistical computing. 8, 2021). R Foundation for Statistical Computing, Vienna, Austria. Available online Marín, A., Giraldo, L., and Correa, G. (2014). Parámetros de fermentación at: http://www.R-project.org (accessed September 15, 2021). ruminal in vitro del pasto Kikuyo (Pennisetum clandestinum). Liv. Res. Rural Ramírez, J., Posada, O., and Noguera, R. (2015). Effects of Kikuyu grass Dev. 26:6. Available online at: http://www.lrrd.org/lrrd26/3/mari26057.html (Pennisetum clandestinum) age and different forage: concentrate ratios on (accessed September 18, 2021). methanogenesis. Rev. MVZ Córdoba 20, 4726–4738. doi: 10.21897/rmvz.43 Marín-Santana, M. N., López-González, F., Hernández-Mendo, O., and Arriaga- Rauber, L. R., Sequinatto, L., Kaiser, D. R., Bertol, I., Baldissera, T. C., Garagorry, Jordán, C. M. (2020). Kikuyu pastures associated with tall fescue grazed in F. C., et al. (2021). Soil physical properties in a natural highland grassland in autumn in small-scale dairy systems in the highlands of Mexico. Trop. Anim. southern Brazil subjected to a range of grazing heights. Agric. Ecosyst. Environ. Health Prod. 52, 1919–1926. doi: 10.1007/s11250-020-02216-7 319, 107515. doi: 10.1016/j.agee.2021.107515 Mauricio, R. M., Mould, F. L., Dhanoa, M. S., Owen, E., Channa, K. S., and Reeves, M., Fulkerson, W., and Kellaway, R. (1996). Forage quality of kikuyu Theodorou, M. K. (1999). A semi-automated in vitro gas production technique (Pennisetum clandestinum): the effect of time of defoliation and nitrogen for ruminant feedstuff evaluation. Anim. Feed Sci. Technol. 79, 321–330. fertiliser application and in comparison with perennial ryegrass (Lolium doi: 10.1016/S0377-8401(99)00033-4 perenne). Aust. J. Agric. Res. 47, 1349. doi: 10.1071/AR9961349 McAllister, T., a., Beauchemin, K., a., McGinn, S. M., Hao, X., and Robinson, Savian, J. V., Schons, R. M. T., de Souza Filho, W., Zubieta, A. S., Kindlein, L., P. H. (2011). Greenhouse gases in animal agriculture—Finding a balance Bindelle, J., et al. (2021). ‘Rotatinuous’ stocking as a climate-smart grazing between food production and emissions. Anim. Feed Sci. Technol. 166, 1–6. management strategy for sheep production. Sci. Total Environ. 753, 141790. doi: 10.1016/j.anifeedsci.2011.04.057 doi: 10.1016/j.scitotenv.2020.141790 McAllister, T. A., and Newbold, C. J. (2008). Redirecting rumen fermentation to Savian, J. V., Schons, R. M. T., Marchi, D. E., Freitas, T. S., de, da Silva Neto, G. reduce methanogenesis. Aust. J. Exp. Agric. 48, 7. doi: 10.1071/EA07218 F., Mezzalira, J. C., et al. (2018). Rotatinuous stocking: A grazing management Meale, S. J., Chaves, A. V., Baah, J., and McAllister, T. A. (2011). Methane innovation that has high potential to mitigate methane emissions by sheep. J. production of different forages in in vitro ruminal fermentation. Asian- Clean. Prod. 186, 602–608. doi: 10.1016/j.jclepro.2018.03.162 Australasian J. Anim. Sci. 25, 86–91. doi: 10.5713/ajas.2011.11249 Savian, J. V., Schons, R. M. T., Mezzalira, J. C., Barth Neto, A., Da Silva Neto, G. Menke, K. H., Raab, L., Salewski, A., Steingass, H., Fritz, D., and Schneider, F., Benvenutti, M. A., et al. (2020). A comparison of two rotational stocking W. (1979). The estimation of the digestibility and metabolizable energy strategies on the foraging behaviour and herbage intake by grazing sheep. content of ruminant feedingstuffs from the gas production when they Animal 14, 2503–2510. doi: 10.1017/S1751731120001251 are incubated with rumen liquor in vitro. J. Agric. Sci. 93, 217–222. Sbrissia, A. F., Duchini, P. G., Zanini, G. D., Santos, G. T., Padilha, D. A., and doi: 10.1017/S0021859600086305 Schmitt, D. (2018). Defoliation strategies in pastures submitted to intermittent Menke, K. H., and Steingass, H. (1988). Estimation of the energetic feed value stocking method: underlying mechanisms buffering forage accumulation over obtained from chemical analysis and in vitro gas production using rumen fluid. a range of grazing heights. Crop Sci. 58, 945. doi: 10.2135/cropsci2017.07.0447 Anim. Res. Dev. 28, 7–55. Schmitt, D., Padilha, D. A., Dias, K. M., Santos, G. T., Rodolfo, G. R., Zanini, Mezzalira, J. C., Bonnet, O. J. F., de Carvalho, P. C. F., Fonseca, L., and G. D., et al. (2019a). Chemical composition of two warm-season perennial Bremm, C., Mezzalira, C. C., et al. (2017). Mechanisms and implications grasses subjected to proportions of defoliation. Grassl. Sci. 65, 171–178. of a type IV functional response for short-term intake rate of dry doi: 10.1111/grs.12236 matter in large mammalian herbivores. J. Anim. Ecol. 86, 1159–1168. Schmitt, D., Padilha, D. A., Medeiros-Neto, C., Ribeiro Filho, H. M. N., doi: 10.1111/1365-2656.12698 Sollenberger, L. E., and Sbrissia, A. F. (2019b). Herbage intake by cattle Frontiers in Sustainable Food Systems | www.frontiersin.org 1417 December 2021 | Volume 5 | Article 682653 Marín et al. Methanogenic Profile of Kikuyu Swards in kikuyugrass pastures under intermittent stocking method. Rev. Ciência Wei, T., Simko, V., Levy, M., Xie, Y., Jin, Y., and Zemla, J. (2017). Package Agronômica 50, 493–501. doi: 10.5935/1806-6690.20190058 ‘corrplot’. Statistician. 56:e24. Soil Survey Staff (2014). Keys to Soil Taxonomy. 12th ed. Washington, DC. Werling, B. P., Dickson, T. L., Isaacs, R., Gaines, H., Gratton, C., Gross, K. L., Tagliapietra, F., Cattani, M., Bailoni, L., and Schiavon, S. (2010). In vitro rumen et al. (2014). Perennial grasslands enhance biodiversity and multiple ecosystem fermentation: Effect of headspace pressure on the gas production kinetics services in bioenergy landscapes. Proc. Natl. Acad. Sci. 111, 1652–1657. of corn meal and meadow hay. Anim. Feed Sci. Technol. 158, 197–201. doi: 10.1073/pnas.1309492111 doi: 10.1016/j.anifeedsci.2010.04.003 Yáñez-Ruiz, D. R., Bannink, A., Dijkstra, J., Kebreab, E., Morgavi, D. P., Teague, W. R., Apfelbaum, S., Lal, R., Kreuter, U. P., Rowntree, J., Davies, C. A., O’Kiely, P., et al. (2016). Design, implementation and interpretation of et al. (2016). The role of ruminants in reducing agriculture’s carbon footprint in in vitro batch culture experiments to assess enteric methane mitigation North America. J. Soil Water Conserv. 71, 156–164. doi: 10.2489/jswc.71.2.156 in ruminants-a review. Anim. Feed Sci. Technol. 216, 1–18. 2016.03.016. Teutscherová, N., Vázquez, E., Sotelo, M., Villegas, D., Velásquez, N., Baquero, doi: 10.1016/j.anifeedsci.2016.03.016 D., et al. (2021). Intensive short-duration rotational grazing is associated with Yang, C., Rooke, J. A., Cabeza, I., and Wallace, R. J. (2016). Nitrate and inhibition improved soil quality within one year after establishment in Colombia. Appl. of ruminal methanogenesis: microbial ecology, obstacles, and opportunities for Soil Ecol. 159, 103835. doi: 10.1016/j.apsoil.2020.103835 lowering methane emissions from ruminant livestock. Front. Microbiol. 7, 132. Theodorou, M. K., Williams, B. A., Dhanoa, M. S., McAllan, A. B., and France, doi: 10.3389/fmicb.2016.00132 J. (1994). A simple gas production method using a pressure transducer to Zubieta, A. S., Marín, A., Savian, J. V., Soares Bolzan, A. M., Rossetto, J., Barreto, determine the fermentation kinetics of ruminant feeds.Anim. Feed Sci. Technol. M. T., et al. (2021). Low-intensity, high-frequency grazing positively affects 48, 185–197. doi: 10.1016/0377-8401(94)90171-6 defoliating behavior, nutrient intake and blood indicators of nutrition and stress Tilley, J. M. A., and Terry, R. A. (1963). A two-stage technique for in sheep. Front. Vet. Sci. 8, 1–13. doi: 10.3389/fvets.2021.631820 the in vitro digestion of forage crops. Grass Forage Sci. 18, 104–111. Zubieta, Á. S., Savian, J. V., de Souza Filho, W., Wallau, M. O., Gómez, A. M., doi: 10.1111/j.1365-2494.1963.tb00335.x Bindelle, J., et al. (2020). Does grazing management provide opportunities to Ungerfeld, E.M. (2015). Shifts inmetabolic hydrogen sinks in themethanogenesis- mitigate methane emissions by ruminants in pastoral ecosystems? Sci. Total inhibited ruminal fermentation: a meta-analysis. Front. Microbiol. 6, 37. Environ. 754, 142029. doi: 10.1016/j.scitotenv.2020.142029 doi: 10.3389/fmicb.2015.00037 Ungerfeld, E. M., and Kohn, R. A. (2006). The role of thermodynamics in the control Conflict of Interest: The authors declare that the research was conducted in the of ruminal fermentation. In: Ruminant physiology: digestion, metabolism and absence of any commercial or financial relationships that could be construed as a impact of nutrition on gene expression, immunology and stress (Wageningen potential conflict of interest. Academic Publishers, Wageningen, the Netherlands) 55–85. Valencia Echavarria, D. M., Giraldo Valderrama, L. A., and Marín Gómez, A. The reviewer XG declared a shared affiliation with two of the authors, AM (2019). In vitro fermentation of Pennisetum clandestinum Hochst. Ex Chiov and GC, to the handling editor at time of review. increased methane production with ruminal fluid adapted to crude glycerol. Trop. Anim. Health Prod. 52, 565–571. doi: 10.1007/s11250-019-02043-5 Publisher’s Note: All claims expressed in this article are solely those of the authors Van Soest, P. J., Robertson, J. B., and Lewis, B. A. (1991). Methods for dietary fiber, and do not necessarily represent those of their affiliated organizations, or those of neutral detergent fiber, and nonstarch polysaccharides in relation to animal the publisher, the editors and the reviewers. Any product that may be evaluated in nutrition. J. Dairy Sci. 74, 3583–3597. doi: 10.3168/jds.S0022-0302(91)78551-2 this article, or claim that may be made by its manufacturer, is not guaranteed or Van Zijderveld, S. M., Gerrits, W. J. J., Apajalahti, J. A., Newbold, J. R., Dijkstra, J., Leng, R. A., et al. (2010). Nitrate and sulfate: effective alternative hydrogen endorsed by the publisher. sinks for mitigation of ruminal methane production in sheep. J. Dairy Sci. 93, 5856–5866. doi: 10.3168/jds.2010-3281 Copyright © 2021 Marín, Bindelle, Zubieta, Correa, Arango, Chirinda and de Faccio Vargas, J. J., Pabón, M. L., and Carulla, J. E. (2018). Methane production from Carvalho. This is an open-access article distributed under the terms of the Creative four forages at three maturity stages in a ruminal in vitro system. Rev. Colomb. Commons Attribution License (CC BY). The use, distribution or reproduction in Ciencias Pecu. 31, 120–129. doi: 10.17533/udea.rccp.v31n2a05 other forums is permitted, provided the original author(s) and the copyright owner(s) Viljoen, C., van der Colf, J., and Swanepoel, P. A. (2020). Benefits are limited with are credited and that the original publication in this journal is cited, in accordance high nitrogen fertiliser rates in Kikuyu-ryegrass pasture systems. Land. 9:173. with accepted academic practice. No use, distribution or reproduction is permitted doi: 10.3390/land9060173 which does not comply with these terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1428 December 2021 | Volume 5 | Article 682653 PERSPECTIVE published: 02 December 2021 doi: 10.3389/fsufs.2021.726482 Perspectives on Reducing the National Milk Deficit and Accelerating the Transition to a Sustainable Dairy Value Chain in Zimbabwe Ngonidzashe Chirinda 1*, Chrispen Murungweni 2, Addmore Waniwa 3*, Justice Nyamangara 4, Aziza Tangi 1, Michael Peters 5, An Notenbaert 5 and Stefan Burkart 6 1 AgroBioSciences, Agricultural Innovations and Technology Transfer Centre, Mohammed VI Polytechnic University (UM6P), Ben Guerir, Morocco, 2 School of Agricultural Sciences and Technology, Chinhoyi University of Technology (CUT), Chinhoyi, Zimbabwe, 3Department of Veterinary Services, Ministry of Lands, Agriculture, Fisheries, Water and Rural Development, Harare, Zimbabwe, 4Department of Environmental Science and Technology, Marondera University of Agricultural Sciences and Technology (MUAST), Marondera, Zimbabwe, 5Crops for Nutrition and Health, Tropical Forages Program, Alliance Bioversity International and CIAT, Nairobi, Kenya, 6Crops for Nutrition and Health, Tropical Forages Program, Alliance Bioversity International and CIAT, Cali, Colombia The Zimbabwean dairy industry is massively underperforming, as evidenced by a Edited by: reduction in milk yield from 262 million liters in 1990 to <37 million liters in 2009 and Rein Van Der Hoek, a steady but slow increase to 82 million liters in 2021. The current demand for milk in Alliance Bioversity International and Zimbabwe stands at 130 million liters, and there is a national capacity for processing CIAT, France 400 million liters per annum. This study used literature, stakeholder inputs and expert Reviewed by: Helene Lie, knowledge to provide a perspective on practical options to reduce the national milk Norges Vel, Norway deficit and, simultaneously, accelerate the transition to a sustainable dairy value chain Heinrich Hagel, University of Hohenheim, Germany in Zimbabwe. Following a discussion on the key barriers and constraints to developing *Correspondence: the milk value chain, we explored opportunities to improve the performance of the Ngonidzashe Chirinda underperforming smallholder andmedium-scale dairy farmers. Specifically, we discussed Ngonidzashe.Chirinda@um6p.ma innovativemanagement, creative policy instruments and alternative technological options Addmore Waniwa waniwaa@gmail.com to maximize milk production in Zimbabwe. We also highlight the need for an inclusive and creatively organized dairy value chain to optimize stakeholder linkages and improve Specialty section: information flow and equity. Examples of crucial investments and incentive structures This article was submitted to Climate-Smart Food Systems, for upgrading the existing value chain and monitoring greenhouse gas emissions and a section of the journal carbon uptake are discussed. Furthermore, the socio-economic effects (i.e., profitability, Frontiers in Sustainable Food Systems women empowerment and employment creation), milk quality, safety and traceability Received: 16 June 2021 issues linked to a better organized and performing dairy value chain are highlighted. Accepted: 10 November 2021 Published: 02 December 2021 Keywords: greenhouse gas emissions, gender roles, employment creation, innovation, policy, milk productivity Citation: Chirinda N, Murungweni C, Waniwa A, Nyamangara J, Tangi A, Peters M, INTRODUCTION Notenbaert A and Burkart S (2021) Perspectives on Reducing the The agricultural sector in Zimbabwe supports the livelihoods of approximately 70% of National Milk Deficit and Accelerating the population and contributes approximately 17% of GDP (FAO, 2021). In a baseline the Transition to a Sustainable Dairy Value Chain in Zimbabwe. survey conducted by Transforming Zimbabwe’s Dairy Value Chain for the Future Front. Sustain. Food Syst. 5:726482. Action (TranZ DVC) (2019), income from milk and milk by-products were reported doi: 10.3389/fsufs.2021.726482 to contribute only 0.3% of the total GDP, and the milk processing component of the Frontiers in Sustainable Food Systems | www.frontiersin.org 1149 December 2021 | Volume 5 | Article 726482 Chirinda et al. Transitioning Toward Sustainable Dairy VC dairy value chain was reported to employ 282 male and 86 female MILK PRODUCTION REGIONS AND youth (<35 years). Moreover, of the total number of jobs that PRODUCTION SYSTEMS offer a fair income and social protection (descent jobs), along the dairy value-chain, 39.5% and 23% were reported to be held by Zimbabwe is divided into five agro-ecological regions (AER) women and youth, respectively (Transforming Zimbabwe’s Dairy based on the amount of received rainfall. Large-scale commercial Value Chain for the Future Action (TranZ DVC), 2019). dairy production is mainly conducted in AER I (>1,000mm, From the mid-90s, the dairy cattle herd decreased due 1,100–2,600 masl), AER IIA and IIB (750–1,000mm, 1,100– to recurrent droughts, economic contraction, and the land 1,800 masl), AER III (650–800mm, 1,100–1,200m) [Marongwe reform programme that disrupted large-scale dairy operations et al., 1998; FAO, 2006a; Government of Zimbabwe (GoZ), responsible for >95% of the national milk pool (Kagoro and 2013]. Mean annual temperatures in areas supporting large-scale Chatiza, 2012). The land reform programme, which involved dairy production range between 15–18◦C, 16–19◦C and 18– redistributing land from the large-scale commercial sector to 22◦C in AER I, II and III, respectively (Mugandani et al., 2012). households from the overcrowded communal areas, and the Smallholder dairy farmers are located in all AER, including the resultant lack of clarity in the security of land tenure were dry regions (<650mm annual rainfall), AER IV (600–1,200masl) probably the most important factors that negatively impacted and AER V (300–900 masl). A visual representation of the spatial the dairy sector (Mzumara, 2012; Marecha, 2013). The difficult distribution of the AERs is given by Kashagura (2014). operational conditions created by the factors mentioned above Smallholder farmers, with an average of three cows per farmer, resulted in a decrease in the number of registered commercial generally practice dairying for household consumption and sales dairy farmers from 559 in 1987 to 165 in 2012 (SNV, 2012). of excess production to informal markets (Kagoro and Chatiza, Over the same period, 1987-2012, the dairy herd decreased 2012). While milk production levels vary between different from 113,006 to 27,400 resulting in the underperformance of farms, low milk yields (<200 liters per farm per day) in the the value chain, as evidenced by a reduction in milk yield smallholder sector contribute to their small share of the national from 262 million liters in 1990 to <37 million liters in milk pool (∼2–3%) (Hanyani-Mlambo, 2000; Munangi, 2007). 2009 (Dairy Services, 2020). Therefore, while smallholder production is essential for food Although recent public and private sector interventions security, low milk yields partly due to reliance on low-yielding contributed to a steady but slow increase in annual national local breeds and cross-breeds (4–6 L per cow per day) result in milk outputs, which stood at 80 million liters in 2019 (Dairy their contribution to the national milk pool being largely invisible Services, 2020), these are below the national capacity for milk (Chinogaramombe et al., 2008; SNV, 2012). The contribution consumption which is 130 million and the capacity for the of medium-scale farmers (200–500 L per farm per day) to the processing which is 400 million liters per annum (Ministry national milk pool is variable as some of these farmers have of Lands, Agriculture and Rural Resettlement, 2016). Since a large number of animals with low milk productivity. This national milk demand stands at 130 million liters (Dairy Services, variability in production levels was one of the reasons that 2020), milk deficits are covered by importing milk and dairy led to dairy farmers now being classified based on total milk products (TrendEconomy, 2020). Meeting this demand through yields per day rather than cattle numbers. Currently, natural local production instead of imports presents an opportunity grasslands and crop residues are the primary feed resources used to improve the welfare of producers and support sectors by smallholder and medium-scale dairy producers (Gwiriri et al., through increased income and employment generated along 2016). Consequently, the low milk yields experienced in the the value chain. This perspective article is aimed at exploring smallholder and some medium-scale farms are partially due to practical options for reducing Zimbabwe’s milk deficit by low yielding cattle breeds, seasonality in the availability of quality improving the performance of smallholder (<200 liters per and adequate feed resources (Ngongoni et al., 2006). farm per day) and medium-scale (200–500 liters perfarm per Large-scale commercial dairy producers (>500 L per farm day) dairy farmers. To achieve this objective, in early 2021, we per day) that contribute to >95% of the national milk pool are reviewed existing literature (e.g., scientific articles, databases, primarily located in AERs receiving relatively high (>650mm) gray literature) and sought inputs from key stakeholders and rainfall and relatively high (>1100 masl) altitude. The large dairy experts with knowledge on the dairy value chain in Zimbabwe producers mainly use pure exotic cattle breeds (e.g., Holstein- (most of them involved as co-authors). With these inputs, Friesian breeds, Red Dane, Jersey, Guernsey), with a productivity we provide our perspective on (i) how milk production is range of 14–25 liters per cow per day (Mandiwanza, 2007; organized in Zimbabwe, (ii) where and how milk is being Matekenya, 2016). Besides high yielding cattle breeds, the high processed and marketed, (iii) who the key stakeholders along productivity of cattle in the large-scale producers is partially due the dairy value chain are, (iv) what the environmental impacts to access to extensive grazing areas and financial resources to buy of dairy production are, and (v) the barriers and constraints supplementary stock feeds during dry periods (Matekenya, 2016). for improving the performance of the dairy value chain. Based on this, we then provide a discussion where we suggest key MILK MARKETS interventions that could help improve the dairy value chain performance and improve the livelihoods of various value Viable markets are crucial for incentivizing the increased chain actors. competitiveness of any commercial enterprise. A major challenge Frontiers in Sustainable Food Systems | www.frontiersin.org 1250 December 2021 | Volume 5 | Article 726482 Chirinda et al. Transitioning Toward Sustainable Dairy VC that needs to be tackled in the dairy sector is that smallholder and TABLE 1 | Summary of Zimbabwe milk value chain actors. medium-scale farmers (<500 L per day) are underperforming, Category Main actors thus not significantly contributing to the national milk pool. There are milk collection centers (MCCs) strategically located Farmer Organizations advocating for dairy farmer interests in the milk-producing regions for easy access to dairy farmers. representation include Zimbabwe Association of Dairy Farmers Farmers deliver their milk to these centers, where it is tested (ZADF), Commercial Farmers Union (CFU), for quality before being added into bulk milk tanks. In 2020, 17 Zimbabwe Farmers’ Union (ZFU). operational farmer-owned MCCs were reported to have received Farmer extension and Departments in the Ministry of Lands, Agriculture veterinary services and several NGOs, milk processors, milk from 386 farmers [Zimbabwe Dairy Industry Trust (ZDIT), Research services The setting of research priorities is mainly done by 2021]. Several MCCs (e.g., Nharira and Honde Valley) have (Research Institutes, the Zimbabwe Dairy Industry Trust, Research ventured into small-scale value addition producing products such NGOs and institutes and universities as yogurts and cheese and increased their profitability (Kandjou, Universities) 2012). Otherwise, medium and large-scale (e.g., Dairibord) Animal and milk Cooperatives processors collect bulk milk from the milk collection centers and traders transport it to their processing factories. Smallholder farmers’ Milk processors Dairibord Holdings, Nestle, Kefalos, Dendairy, contribution to the national milk pool was about 1.1 million Prodairy, Kershelmar, Alpha Omega, Yomilk. liters (2% of national production) in 2012. In the same year Input provision and Private sector dealers, banks and micro-credit (2012), only six smallholder producer associations were reported financial support for providers. farmers to have produced sufficient quantities of milk to deliver to a Regulatory services Government ministries and Parastatals, and civil major milk processor (Kagoro and Chatiza, 2012). In 2019, a society actors study conducted across 60 districts in the country’s ten provinces Consumer protection Organizations interested in consumer interests (i.e., reported monthly milk production levels of 1,703,666 liters quality and prices), including the Consumer Council per month and 5,020,034 liters per month in the large-scale of Zimbabwe (CCZ) and the Standards Association commercial sector (Transforming Zimbabwe’s Dairy Value Chain of Zimbabwe (SAZ) for the Future Action (TranZ DVC), 2019). Milk processing is dominated by five out of the eight registered large-scale dairy processors (see Table 1) that are processing 85% of the milk [Zimbabwe Dairy Industry Trust emissions. These default emission factors are mainly determined (ZDIT), 2021]. On the other hand, 27 registered small-scale using studies almost exclusively conducted in Western countries and 12 medium-scale processors correspondingly process 8% (Goopy et al., 2018), which have enormous uncertainties for and 2% of the milk [Zimbabwe Dairy Industry Trust (ZDIT), African livestock systems. In the study by Svinurai et al. (2018), 2021]. Dairibord Holdings (2019), a major dairy processor in which covered 35 years, 58–75% of total annual emissions Zimbabwe, reported that about 3.4 million liters of the raw from livestock were estimated from the smallholder sector. The milk processed in 2019 were collected from smallholders. The smallholder sectors’ low productivity is associated with high increase in quantities of smallholder milk annually sold on the GHG emissions per unit of milk. A study conducted in Kenya, formal market (i.e., 1.1 million liters in 2012 to 3.4 million under similar low intake dairy production systems, shows that liters in 2019) signify progress in overall milk production (SNV, increased feed intake increases milk production and the total 2012). However, relative to their current annual production GHG emissions from enteric fermentation (Ndung’u et al., 2018). levels (∼20 million liters), the amount of milk entering formal If herd sizes grow to meet the demand and reduce the milk markets from smallholder and medium-scale dairy producers is deficit, the total GHG emissions and water use are also likely still low. to increase. To counteract this, herd growth needs to co-occur with productivity increases to reduce GHG emissions and water use (e.g., Douxchamps et al., 2021; Hawkins et al., 2021) per ENVIRONMENTAL IMPACTS liter of milk. Increased productivity has to go hand-in-hand with increased land and water productivity (more animal nutrition Cattle production heavily relies on natural resources and has per area of land and liter of water) and feed efficiency (more a substantial environmental footprint due to methane and animal product per unit of feed), to avoid clearing of more nitrous oxide emissions from enteric fermentation and manure; land to produce feed, and enhance milk production per unit ammonia loss duringmanure handling and storage; deforestation animal, water and land, respectively. A range of resource-use- and biodiversity loss when clearing land for grazing; and efficient and climate-smart practices (e.g., forage production and degradation linked in review to poor pasture management, conservation, water management, manure management) exist, overgrazing and soil erosion (FAO, 2006b; Gerber et al., 2013). but adoption is low due to various financial, communication and Studies on the environmental impacts of dairy production socio-economic factors (CIAT and World Bank, 2017). systems in Zimbabwe are limited. For example, we only found Addressing productivity challenges should coincide with one study on greenhouse gas emissions from livestock systems tackling the environmental impacts of the dairy sector. in Zimbabwe. A drawback of the study was that Tier 1 Land degradation, water scarcity and climate change should (default) IPCC emission factors were used to quantify GHG be addressed through pursuing management practices with Frontiers in Sustainable Food Systems | www.frontiersin.org 1351 December 2021 | Volume 5 | Article 726482 Chirinda et al. Transitioning Toward Sustainable Dairy VC environmental co-benefits. Generally, most technologies and projects, such as establishing improved forages or purchasing practices that reduce GHG emissions have economic benefits milking machines, cannot be readily financed under these as they often increase productivity (Gerber et al., 2013). In conditions (Chari and Ngcamu, 2017b), discouraging farmers addition, Svinurai et al. (2018) showed that current livestock from technology adoption. populations, production and emissions trends suggest that even Furthermore, productive inputs are expensive in Zimbabwe, if Zimbabwe’s national livestock herd doubled in 2030, relative to affecting the dairy value chain. For example, both the purchase 2014, methane emission intensities (per capita) would be similar of heifers and on-farm breeding are costly (Hahlani and Garwi, to those observed in 1980. Therefore, there is potential to increase 2014), forage seeds are often unavailable, high labor costs reduce productivity and reduce the milk deficit without significantly returns along the value chain, and electricity is expensive and increasing GHG emissions. frequently disrupted, boosting the use of less efficient and more expensive energy sources for production and processing (SNV, KEY STAKEHOLDERS 2012). Regarding policy-based constraints, Zimbabwe was facing a phase of instability from 1998 to 2000, followed by a fast Several previous studies have mapped the key public, track land reform program that affected the dairy sector. Large private and civil society actors along the dairy value chain dairy farmers lost their farms, and land titles for the resettled (Marecha, 2009; Kagoro and Chatiza, 2012; Matekenya, farmers are still unclear (Marecha, 2013), and this, combined 2016). Based on this already existing information, a summary with unresolved land disputes between farmers, leads to low long- of the roles different value chain actors play is presented term investments in farm improvement plans (Marecha, 2013; in Table 1. Chari and Ngcamu, 2017a). Compared to other countries (e.g., South Africa, Kenya), raw milk prices are substantially higher in Zimbabwe (Kawambwa et al., 2014), probably due to the BARRIERS AND CONSTRAINTS TO described production constraints and inefficiencies (Gadzikwa, OPTIMAL PERFORMANCE OF THE MILK 2013). The lack of infrastructure, technologies and adequate VALUE CHAIN management affect milk quantity and quality, the latter being a major bottleneck for milk processing (Chari and Ngcamu, It is unambiguous that the Zimbabwean dairy value chain 2019). The situation is further aggravated by limited technical is far from optimal performance resulting from multiple assistance schemes provided to dairy farmers (Smith et al., 2002). factors affecting local milk production. At the farm level, Gender inequality is a significant constraint in the development low milk yields and calving rates, late age at first calving of the dairy value chain. Men, women and youth play essential and long calving intervals prevail and are directly related roles in the livestock sector, but the level of participation to nutritional aspects, the use of inappropriate breeds, poor differs significantly. Although the situation is gradually changing, farm management, limited disease control and poor extension men continue dominating livestock production, mainly for (Smith et al., 2002; Ngongoni et al., 2006; Munangi, 2007). cultural reasons, overshadowing women’s ownership of livestock, The already limited availability of suitable farmland and water decision-making and control (Chawatama et al., 2005; Daniels, are declining due to climate change and climate variations 2008; Mupawaenda et al., 2009). Gender roles are based (Brown et al., 2012). Changing rainfall patterns, heat waves on dynamic cultural beliefs for which the pace of change or droughts (e.g., 2015–2017) lead to poor pasture conditions, is determined by increased awareness and incentives. Thus, feed and forage seasonality, yield decreases and price increases targeted social awareness campaigns, combined with appropriate (resulting in difficulties for animal breeding; Masama, 2013), and policies and incentive mechanisms, can harness the perspectives high susceptibility to pests and diseases—all having immediate and capacities of men, women, and youth to improve value chain adverse effects on milk yields and production costs. At the performance and gender equity. macro and value chain level, extreme climatic conditions are causing damages to infrastructure (i.e., water and energy supply), resulting in higher costs for milk cooling, disruptions DISCUSSION ON KEY INTERVENTIONS TO in the transport of perishable goods such as milk (Chari IMPROVE THE MILK VALUE CHAIN IN and Ngcamu, 2017a), increased processing and transport costs, ZIMBABWE consumer prices, vulnerability and food insecurity (Chari and Ngcamu, 2019). In our view, the dairy sector requires In Table 2, we present a range of interventions to improve the strategic investments along the value chain to achieve its performance of the dairy value chain in Zimbabwe. Briefly, the full potential, e.g., in cooling facilities, milking machines or interventions are disaggregated based on value chain links. While road and transportation infrastructure. Zimbabwe, however, has needed interventions are primarily known, the challenge is on high burdens (bureaucracy, complex procedures) for accessing ensuring that the needed actions for their actual implementation financing (Hahlani and Garwi, 2014). In addition, credit are taken. Taking the needed actions is not an easy task as providers are reluctant to lend money to farmers who do not smallholder dairy farmers, who include many underperforming possess collateral (Chari and Ngcamu, 2019); their credit rates are farmers, are mainly resource-constrained and, at times, located high (up to 14%; Commercial Farmers Union, 2014) and more in remote areas with limited supporting infrastructure. Post- oriented toward short-term investments. Long-term investment land reform, the government of Zimbabwe has targeted the Frontiers in Sustainable Food Systems | www.frontiersin.org 1452 December 2021 | Volume 5 | Article 726482 Chirinda et al. Transitioning Toward Sustainable Dairy VC TABLE 2 | Key interventions for improving the dairy value chain in Zimbabwe. Value chain segment Interventions Inputs • Availability and access to affordable improved forage seeds (including vegetative propagation) to increase the supply of forage/forage quality • Support local feed and forage seed production and seed distribution • Where necessary, support local businesses that import seeds of improved grasses and feedstock that cannot be produced locally due to physiological constraints • Accelerate the speed of input importation and the registration of new varieties • Feed conservation and associated business models • Access to regular and uninterrupted energy and water supplies • Installation of irrigation infrastructure • community-based animal health services, para-extension and artificial insemination Production • Improved availability of and access to in-calf heifers • Development of formal dairy training centers • Improved mechanization of dairy systems for improving efficiency in feed production, feed processing, cattle management, milking and milk processing. • Adoption of cattle breeds with high milk production potential (which need to go hand in hand with): ◦ Good on-farm feed and animal management practices ◦ Appropriate animal health measures • Improved farmer technical support, extension and education • Harmonization of efforts and concepts and training of technical assistants/extensionists among government agencies and NGOs Processing • Set up and rehabilitate processing infrastructure and quality assurance systems • Increase number of technical experts and their availability • Improve extension/training and access to inputs required for milk processing and value addition (e.g., cheese and yogurt production) Distribution and marketing • Improved distribution infrastructure (e.g., milk collection centers, road infrastructure) • Improve farmer access to information (e.g. price information systems; information fora, multi-actor platforms) • Support more collective actions, e.g., cooperatives, bulking of milk and guaranteed prices Consumers • Product differentiation and niche markets (e.g., denominated origin, quality attributes, environmental attributes, fair trade, animal welfare) • Consumer awareness campaigns on milk and milk products • Increase consumer promotional material Financing • Easy access to financing programs • Risk insurance • Affordable credit and general credit accessibility; credit lines for sustainable intensification efforts • International assistance, e.g., necessary assistance vs. reduction of dependence • Strengthening safety nets • Training on investment prioritization Entrepreneurial support • Local transformation and formalization • Increased number of local value addition and milk transformation plants (e.g., cheese, milk, yogurts) • Support of inclusive business models Institutional, policy and regulatory support • Better institutional coordination among value chain actors • Evidence-based policy support/legislation Cross-cutting • Women and youth empowerment (i.e., increasing women involvement in the dairy value chain) • Design interventions in the dairy value chain to allow women to change their lives (production of milk-based products value additions) • Strengthening collaboration among direct value chain actors but also with value chain framework • Access to in-depth education on the dairy industry (from a young age) • Organization and Training/capacity-building of Dairy farmers dairy industry in its vision of transforming the nation into a Programme funded in review through the Dairy Resuscitation middle-income country by 2030. Therefore, there have been Fund and aimed to increase national production to 200 million several efforts to resuscitate the local dairy industry. For instance, liters per year by 2025. Also, in 2019, supported by the E.U., in 2017, the government launched the Dairy Revitalisation the government launched the Zimbabwe Agricultural Growth Frontiers in Sustainable Food Systems | www.frontiersin.org 153 December 2021 | Volume 5 | Article 726482 Chirinda et al. Transitioning Toward Sustainable Dairy VC Programme (ZAGP) to address weaknesses and gaps in livestock on-farm productivity. For instance, in the case of improving value chains. This programme aims to increase investments, feed supply, a practical solution could be for the youth to propose institutional reforms and policy alignment to support receive support for establishing local seed supply systems the dairy sector [Zimbabwe Agricultural Growth Programme (i.e., for forage legumes). The local seed supply systems could (ZAGP), 2019]. However, over-reliance on external funding to improve dairy farmers access to affordable, high-quality seed revive the dairy sector may not be a sustainable solution; shifting to sow on their private or communally owned pasturelands. tomore local and continuous investmentsmay be amore prudent This forage-based basal diet can be complemented by strategic approach (Washaya and Chifamba, 2018). The Zimbabwean supplementation with several crops grown in the rural areas diaspora, estimated at four million [International Organization (i.e., maize, groundnut, sunflower, pearl millet, sorghum and for Migration (IOM), 2015], presents a vast potential source of cowpea). Dependence on local crops presents farmers with capital investment in the dairy sector (Madziva et al., 2018). an opportunity for cost-effective feed-level interventions that However, the government may need to highlight challenges can improve market competitiveness and productivity of their and investment opportunities along the dairy value chain, systems (Murungweni et al., 2004; Ngongoni et al., 2006; Gusha create proper incentives, and develop regulatory mechanisms to et al., 2013; Mashanda, 2014; Gwiriri et al., 2016; Chifamba protect investments. In addition, by creating spaces for national et al., 2018). To overcome periods of feed scarcity, high-quality discussions, including the diaspora, the country could also tap forages and feed crops could also be conserved as hay or silage into their experiences and expertise to innovate along the dairy and become the basis of densified feeds; densification may value chain. allow an easier transfer from one region to another (Dey et al., It would be strategic for the public and private sector to 2021, unpublished). increase research investments tailored to generate knowledge on Youth could establish feed processing businesses based on technologies and practices that result in efficiency gains along the high-quality feed mixes based on local grains to provide dairy dairy value chain. For instance, due to high costs for feed, limited farmers with local high-value supplements or concentrates access to affordable finance and insecure land holdings, most (Chifamba et al., 2018). We expect local sourcing to reduce farms have dairy animal herds below their potential [Zimbabwe feed costs and increase the profitability of dairy operations. In Dairy Industry Trust (ZDIT), 2021]. Therefore, besides focusing addition, youth can be trained as para-extension agents that on efficiency gains along the dairy value chain, investments can support artificial insemination programmes to improve the need to increase the dairy herd in smallholder and medium- local breeds and veterinary services to support animal health scale farms. For example, smallholder farmers with an average (Kagoro and Chatiza, 2012). The engagement of youth (as local of 3 cows per farm (Kagoro and Chatiza, 2012), with each cow entrepreneurs) to supply improved seeds, deliver animal health producing 5 liters per day (Chinogaramombe et al., 2008). Even services and improve cattle breeds will contribute to employment if the average milk productivity per cow were to match the higher creation and the intake of quality feed by healthy and high end of cows on large-scale farms (25 liters per day; Matekenya, yielding cattle breeds and ultimately improve milk supply and 2016), their production levels would remain small-scale (<200 quality from smallholder and medium-scale dairy producers. liters per farm per day). Therefore, to transition from a small to Youth participation in the local economy may also prevent their a medium-scale or a large-scale dairy producer, the initial focus migration to crowded urban areas. should be on increasing dairy herd sizes per farm. Mhlanga et al. (2018) projected that without a global reduction After increasing the dairy herd per farm, the next step in atmospheric CO2 concentrations and the resultant high air would be to find creative, feasible and context based-solutions temperatures would reduce feed availability and the area suitable to overcome the low and seasonal supply of high-quality animal for dairy farming and have devastating impacts on the local feed. Improved feed availability could be done by introducing dairy industry. To maintain milk yield stability even during dry and promoting improved forages tolerant to abiotic (excess and periods, dairy farmers may need to consider drought-tolerant scarcity of water) and biotic (pest and diseases) stresses as the forage crops that better use available moisture. One example basis of feeding. Although the planting of improved forages of this is Cactus pear (Opuntia spp.), which efficiently converts is considered to be scale-neutral, meaning that the technology water into dry matter (Galizzi et al., 2004). Opuntia species are can be used by smallholders as well as medium- to large- known for developing physiological, phenological and structural scale producers, the private forage seed suppliers estimate that adaptations (Guevara et al., 2011), making them productive in mostly smallholder to medium-scale livestock producers adopt these drier environments (Nobel and Zutta, 2008). On average, them to sustainably intensify their production systems (Labarta the biomass production from cactus per unit of water is about et al., 2017; Fuglie et al., 2021). Forages compete less with three times as high as with C4 plants and five times as high human nutrition, e.g., grain crops, and have the co-benefit of as with C3 plants (Snyman, 2013), making Opuntia cladodes maintaining soil fertility, enhancing carbon accumulation and a valuable option for successfully balancing parts of the cattle improving GHG balances and Water-Use-Efficiency. However, diet (Einkamerer et al., 2009; de Waal et al., 2013). From a this would require functional seed systems, ensuring seed well-managed cactus pear plantation of 800 to 1000 plants/ha, availability, accessibility, and affordability (Peters et al., 2021). around 10 t/ha cladode dry matter and 20 t/ha fruit biomass With appropriate training and the proper incentive can be obtained, but values vary with genotype (Fouché and mechanisms, the estimated 8% of youth unemployed (World Coetzer, 2013). To improve the adoption ofOpuntia, investments Bank, 2021) can be engaged to co-explore solutions to improve are needed in research and awareness-raising on its use and Frontiers in Sustainable Food Systems | www.frontiersin.org 1654 December 2021 | Volume 5 | Article 726482 Chirinda et al. Transitioning Toward Sustainable Dairy VC potential benefits. In addition, investments in technical support value-chain interventions that creatively balance investments, for establishing fodder banks with Opuntia, could stimulate livelihoods, and profits within the local context. its adoption as a feed option during dry and drought periods (Makumbe, 2010). DATA AVAILABILITY STATEMENT The smartphone penetration rate is 52 per 100 inhabitants (∼7.7 million users) (Econet Wireless Zimbabwe, 2020). The original contributions presented in the study are included However, considering that several inhabitants may have more in the article/supplementary material, further inquiries can be than one smartphone, while the exact number of smartphone directed to the corresponding author/s. users is uncertain, it is probably lower than 52%. On the other hand, mobile subscriptions are very high (90 per 100 AUTHOR CONTRIBUTIONS inhabitants; ∼ 13 million subscribers) (ITU, 2021). To support the complete transition toward digital agriculture, government The introduction was written by NC, AW, and CM. The and private sector actors need to innovate and improve sections on milk production regions and production systems smartphone affordability and reduce the cost of mobile data. and milk markets were written by CM, JN, and AT. The These actions may incentivize the adoption of digital tools section on environmental impacts was written by AN, MP, that will have cascading benefits across the dairy value chain. and NC. The section on key stakeholders was written For instance, tools like smartphone applications and online by AW, CM, AT, and NC. The section on barriers and platforms can help connect dairy value chain stakeholders constraints to optimal performance of the milk value chain and improve farmer participation, actor coordination, and was written by SB, MP, AN, and AT. The discussions information flow across the value chain. Other benefits include on key interventions to improve the milk value chain in reducing the length of the value chain (by avoiding unnecessary Zimbabwe and conclusions were written by all the authors. intermediaries and associated costs), improving milk traceability All authors contributed to the article and approved the and monitoring milk quality, using digital records to apply submitted version. for credit, supporting decision-making, and optimizing farm operations (Born et al., 2020). FUNDING CONCLUSIONS This work was funded by the CGIAR Research Program on Livestock. The funders had no role in the design of the Several previous studies and reports have presented what needs study; in the collection, analyses, or interpretation of data; in to be done by the different actors to create a sustainable and the writing of the manuscript, or in the decision to publish inclusive dairy value chain, yet progress remains limited. While the results. there are certainly no silver bullets, actions that support improved performance at different value chain stages are needed.Moreover, ACKNOWLEDGMENTS increased productivity in the dairy sector could return Zimbabwe to being a net exporter of dairy products and contribute toward This work was carried out as part of the CGIAR Research meeting the ambitious national goal of transforming the nation Program on Livestock. We thank all donors who globally support into a middle-income country within a decade (by 2030). In our our work through their contributions to the CGIAR System. opinion, to sustainably solve challenges along the dairy value CGIAR is a global research partnership for a food-secure future. chain, more attention should be placed on the underperforming Its science is carried out by 15 Research Centers in close smallholder and medium-scale dairy farmers and supporting collaboration with hundreds of partners across the globe. REFERENCES Challenges in the Dairy Industry, eds S. A. Ibrahim, T. Zimmerman, and R. Gyawali. London: IntechOpen. Born, L., Chirinda, N., Mabaya, E., Afun-Ogidan, O., Girvetz, E., Jarvis, A., et al. Chawatama, S., Mutisi, C., and Mupawaenda, A. C. (2005). The socio-economic (2020).Digital Agriculture Profile, South Africa. FAO. Available online at: http:// status of smallholder livestock production in Zimbabwe: a diagnostic study. www.fao.org/3/cb2506en/CB2506EN.pdf (accessed June 15, 2021). Livestock Res. Rural Dev. 17, 1–2. Available online at: http://www.lrrd.org/ Brown, D., Chanakira, R., Chatiza, K., Dhliwayo, M., Dodman, D., Masiiwa, lrrd17/12/chaw1714.html (accessed June 15, 2021). M., et al. (2012). Climate Change Impacts, Vulnerability and Adaptation Chifamba, E., Ngongoni, T. N., Nyanga, L. K., Nyagura, S., and Maasdrop, B. in Zimbabwe. IIED Climate Change Working Paper No. 3. Available (2018). Effect of mixed maize-legume silages on milk quality and quantity from online at: https://pubs.iied.org/sites/default/files/pdfs/migrate/10034IIED.pdf lactating smallholder dairy cows. Trop. Anim. Health Prod. 50, 1255–1260. (accessed October, 2012). doi: 10.1007/s11250-018-1552-4 Chari, F., and Ngcamu, B. S. (2017b). The impact of collaborative strategies on Chinogaramombe, G. N. C., Muchenje, V., Mapiye, C., Ndlovu, T., Chimonyo, disaster risk reduction in Zimbabwe dairy supply chains in 2016. J. Transdiscip. N., and Musemwa, L. (2008). Challenges for improving smallholder dairy Res. Southern Africa 13:a433. doi: 10.4102/td.v13i1.433 production in the semiarid areas of Zimbabwe. Livestock Res. Rural Dev. 20:34. Chari, F., and Ngcamu, S. B. (2017a). An assessment of the impact of disaster Available online at: http://www.lrrd.org/lrrd20/3/chin20034.html (accessed risks on dairy supply chain performance in Zimbabwe. Cogent Eng. 4:1. June 15, 2021). doi: 10.1080/23311916.2017.1409389 CIAT and World Bank (2017). Climate-Smart Agriculture in Zimbabwe. CSA Chari, F., and Ngcamu, S. B. (2019). “A synthesis of risks in dairy value chains in Country Profiles for Africa Series. Washington, DC: International Center for Southern Africa: cases of South Africa and Zimbabwe,” in Current Issues and Tropical Agriculture (CIAT). Frontiers in Sustainable Food Systems | www.frontiersin.org 1755 December 2021 | Volume 5 | Article 726482 Chirinda et al. Transitioning Toward Sustainable Dairy VC Commercial Farmers Union (2014). “Zimbabwean agriculture within an African Gusha, J., Manyuchi, C. R., Imbayarwo-Chikosi, V. E., Hamandishe, global context,” in 71st Annual Congress Report. Available online at: http://www. V. R., Katsande, S., and Zvinorova, P. I. (2013). Production cfuzim.org/~cfuzimb/images/brochure2014.pdf (accessed October 28, 2014). and economic performance of F1-crossbred dairy cattle fed Dairibord Holdings (2019). Annual Report. Available online at: https://www. non-conventional protein supplements in Zimbabwe. Trop. dairibord.com/wp-content/uploads/2020/09/DAIRIBORD-HOLDINGS- Anim. Health Prod. 46, 1257–1263. doi: 10.1007/s11250-013- LIMITED-2019-ANNUAL-REPORT-FINAL.pdf (accessed May 14, 2021). 0481-5 Dairy Services (2020).Dairy Services Unit Annual Report 2020. Harare, Zimbabwe: Gwiriri, L. C., Manyawu, G., Mashanda, P. B., Chakoma, I., Moyo, S., Chakoma, Department of Veterinary Services. C., et al. (2016). The potential of replacing conventional dairy supplements Daniels, R. C. (2008). Gender dimensions to the incidence of tariff liberalization. with forage legume-based diets in Zimbabwe’s smallholder dairy sector. Afric. Dev. Rev. 201, 67–93. doi: 10.1111/j.1467-8268.2008.00177.x Afric. J. Range Forage Sci. 33, 155–163. doi: 10.2989/10220119.2016.11 de Waal, H. O., Combrinck, W. J., and Fouché, H. J. (2013). “Preserving masked 70727 cactus pear (Opuntia ficus-indica) fruit with wheat straw, maize hay or lucerne Hahlani, C. D., and Garwi, J. (2014). Operational challenges to small dairy hay,” in Paper presented at the VIII International Congress on Cactus Pear and farming: the case of maryfield dairy settlement scheme in Chipinge Cochineal, 28–31 October 2013, Palermo, Italy. District of Zimbabwe. IOSR J. Human. Social Sci. 19, 87–94. Available Dey, B., Notenbaert, A., Makkar, H., Mwendia, S., Sahlu, Y., and Peters, M. (2021) online at: https://iosrjournals.org/iosr-jhss/papers/Vol19-issue1/Version-4/ Realizing Economic and Environmental Gains from Cultivated Forages and Feed P019148794.pdf?id=8729 (accessed June 15, 2021). Reserves in Ethiopia. Unpublished manuscript. Hanyani-Mlambo, B. T. (2000). Smallholder Dairy Production and Marketing in Douxchamps, S., Notenbaert, A., Cardoso, J. A., Romero, M., and Peters, M. (2021) Zimbabwe: A Socio-Economic Study of the Gokwe, Rusitu andMarirangwe Dairy “The role of improved forages in solving the water scarcity issue of 4 billion Development Projects.Working Paper, AEE 3/2000 Department of Agricultural people,” in Poster prepared for The International Grassland and International Economics and Extension, University of Zimbabwe, Harare. Rangeland Kenya 2021 Virtual Congress, 25–29 October 2021. Cali (Colombia): Hawkins, J., Yesuf, G., Zijlstra, M., Schoneveld, G. C., and Rufino, M. C. (2021). Alliance of Bioversity and CIAT. Feeding efficiency gains can increase the greenhouse gas mitigation potential Econet Wireless Zimbabwe (2020). Annual Report. Available online at: https:// of the Tanzanian dairy sector. Sci. Rep. 11:4190. doi: 10.1038/s41598-021-8 news.ewzinvestor.com/?news_id=78020 (accessed May 13, 2021). 3475-8 Einkamerer, O. B., de Waal, H. O., Combrinck, W. J., and Fair, M. D. (2009). Feed International Organization for Migration (IOM) (2015). IOM Zimbabwe Strategic utilization and growth of Dorper wethers on Opuntia-based diets. South Afric. plan 2015–2018. Available online at: https://zimbabwe.iom.int/sites/zimbabwe/ J. Anim. Sci. 39, 53–57. doi: 10.4314/sajas.v39i1.61178 files/Docs/IOM%20Zimbabwe%20Strategic%20Plan.pdf (accessed May 16, FAO (2006a). Fertilizer Use by Crop in Zimbabwe. Rome: Food and Agriculture 2021). Organization of the United Nations. Available online at: https://www.fao.org/ ITU (2021) Available online at: https://www.itu.int/en/ITU-D/Statistics/Pages/ 3/a0395e/a0395e00.htm (accessed June 15, 2021). stat/default.asp (accessed May 13, 2021). FAO (2006b). Livestock’s Long Shadow—Environmental Issues and Options, eds H. Kagoro, J. M., and Chatiza, K. (2012). Zimbabwe’s Dairy Subsector Study. Harare: Steinfeld, P. J. Gerber, T. Wassenaar, V. Castel, M. Rosales and C. de Haan. SNV Country Office. Rome: FAO. Available online at: https://www.fao.org/3/a0701e/a0701e00.htm Kandjou,M. J. (2012)Technical challenges and Agribusiness prospects for developing (accessed June 15, 2021). pro-poor small scale dairy processing schemes in Omaheke Region on Namibia: FAO (2021). Zimbabwe at a Glance. Available online at: http://www.fao. Lessons from Zimbabwe’s Dairy Development Program (Ph.D thesis). University org/zimbabwe/fao-in-zimbabwe/zimbabwe-at-a-glance/en/ (accessed June 15, of Zimbabwe. Available online at: http://www.library.uz.ac.zw/handle/10646/ 2021). 773 Fouché, H. J., and Coetzer, G. M. (2013). “Response of cactus pear (Opuntia spp.) Kashagura, C. (2014). “Policy issues for possible temporal and spatial rainfall biomass production to fruit load,” in Paper presented at the VIII International distribution changes due to climate change,” in Conference Proceedings: Water Congress on Cactus Pear and Cochineal, 28–31 October 2013, Palermo, Italy. Forum on Water Security and Water-related Disaster Challenges: Policy Issues Fuglie, K., Peters, M., and Burkart, S. (2021) The extent and economic significance for Discussion. of cultivated forage crops in developing countries. Front. Sustain. Food Syst. Kawambwa, P., Hendriksen, G., Zandonda, E., and Wanga, L. (2014). Business 5:712136. doi: 10.3389/fsufs.2021.712136 Viability Assessment Study of Smallholder Dairy Farming in Zambia. Gadzikwa, E. C. (2013). “The future of the manufacturing sector in Zimbabwe,” Wageningen: Alterra. Available online at: https://agriprofocus.com/upload/ in Institute of Chartered Accountants of Zimbabwe Congress, 18–20 July Business_Viability_assessment_study_of_small_holder_dairy_farming_in_ 2013, Victoria Falls. Available onine at: https://www.icaz.org.zw/iMISDocs/ Zambia1425011596.pdf (accessed June 15, 2021). manufacture.pdf (accessed June 15, 2021). Labarta, R., Martinez, J. M., Yaccelga, A., Reyes, B., Gomez, L., Maredia, M., Galizzi, F. A., Felker, P., González, C., and Gardiner, D. (2004). Correlations et al.(2017). Assessing the Adoption and Economic and Environmental Impacts between soil and cladode nutrient concentrations and fruit yield and quality of Brachiaria Grass Forage Cultivars in Latin America Focusing in the Experience in cactus pears, Opuntia ficus-indica in a traditional farm setting in Argentina. of Colombia SPIA Technical Report. Rome, Italy: Standing Panel for Impact J. Arid Environ. 59, 115–132. doi: 10.1016/j.jaridenv.2004.01.015 Assessment (SPIA). Gerber, P. J., Steinfeld, H., Henderson, B., Mottet, A., Opio, C., Dijkman, J., Madziva, R., Siwale, J., and Thondhlana, J. (2018). “Exploring gender and diaspora et al. (2013). Tackling Climate Change Through Livestock—A Global Assessment investment among diaspora women in the U.K.” in African Diaspora Direct of Emissions and Mitigation Opportunities. Rome: Food and Agriculture Investment (Cham, Palgrave Macmillan), 211–37. Organization of the United Nations (FAO). Makumbe, M. T. (2010). “A review of the distribution, use and potential of Goopy, J. P., Onyango, A. A., Dickhoefer, U., and Butterbach-Bahl, K. (2018). cactus pear (Opuntia ficus-indica (L.) Mill.) as ruminant feed in Zimbabwe,” in A new approach for improving emission factors for enteric methane Improved Utilization of Cactus Pear for Food, Feed, Soil andWater Conservation emissions of cattle in smallholder systems of East Africa—results for and Other Products in Africa. Proceedings of International Workshop, Mekelle Nyando, Western Kenya. Agric. Syst. 161, 72–80. doi: 10.1016/j.agsy.2017. (Ethiopia), 19–21 October 2009, eds A. Nefzaoui, P. Inglese, and T. Belay, 12.004 p. 36–42. Government of Zimbabwe (GoZ). (2013). Ministry of Agriculture, Mechanization Mandiwanza, A. S. (2007). “The current state of the dairy industry in Zimbabwe,” and Irrigation Development Agricultural Sector Gender Assessment Report. in Proceedings, National Dairy Symposium on Reviving the Zimbabwe Dairy Harare: GoZ. Industry, Harare, Zimbabwe. Guevara, J. C., Felker, P., Balzarini, M. G., Páez, S. A., Estevez, O. R., Páez, M. Marecha, T. C. (2009). An Explorative Study of Raw Milk Chains in Zimbabwe. A N., et al. (2011). Productivity, cold hardiness and forage quality of spineless Case Study of Seke District. Leeuwarden: Van Hall Larenstein progeny of the Opuntia ficus indica 1281 x O. lindheimerii 1250 cross in Marecha, T. C. (2013). “A case study of the Zimbabwe dairy industry,” in SADC Mendoza plain, Argentina. J. Profess. Assoc. Cactus Dev. 13, 47–61. Available Stakeholders Sanitary and Phytosanitary Awareness Workshop (Presentation), online at: https://jpacd.net/jpacd/article/view/88 (accessed June 15, 2021). Pretoria, 12–13 September 2013 Frontiers in Sustainable Food Systems | www.frontiersin.org 1856 December 2021 | Volume 5 | Article 726482 Chirinda et al. Transitioning Toward Sustainable Dairy VC Marongwe, N., Made, J. M., Dengu, E., Mukahanana, M., Vhudzijena, V., and Available online at: https://hdl.handle.net/10568/113619 (accessed June 15, Moyo, M. (1998) “Land Resources,” in The State of Zimbabwe’s Environment 2021). 1998, eds M. Chenje, L. Sola and D. Paleczny. Harare: Government of the Smith, T., Moyo, S., Richards, J. I., and Morton, J. F. (2002). The Role Republic of Zimbabwe, Ministry of Mines, Environment and Tourism. of Indigenous and Cross-Bred Cattle for Smallholder Dairy Production in Masama, E. (2013). Research note: Impact of climate change on livestock Zimbabwe. Harare: UADY. production in Zimbabwe. Int Open Dist Learn J. (2013) 2, 47–53. Available SNV (2012). Evaluation of Smallholder Dairy Programmes in Zimbabwe, Final online at: https://www.zimagrihub.org.zw/sites/default/files/documents/ Report. Available online at: https://snv.org/cms/sites/default/files/explore/ Resaerch%20note%20Impact%20of%20climate%20change%20on%20livestock download/an_evaluation_of_smallholder_dairy_production_in_zimbabwe. %20production.pdf (accessed June 15, 2021). pdf (accessed 15 June 2021). Mashanda, P. (2014). Potential of Mucuna pruriens and Vigna unguiculata Snyman, H. A. (2013). Growth rate and water-use efficiency of cactus pear as Replacement Feed for Commercial Concentrates in a Smallholder Dairy Opuntia ficus-indica and O. robusta. Arid Land Res. Manag. 27, 337–348. Enterprise. MSc thesis, University of Zimbabwe, Harare, Zimbabwe. doi: 10.1080/15324982.2013.771232 Matekenya, D. T. (2016). “Large scale dairy value chain in Zimbabwe,” in A paper Svinurai, W., Mapanda, F., Sithole, D., Moyo, E. N., Ndidzano, K., presented to the division of Livestock Research DRandSS. et al. (2018). Enteric methane emissions and their response to agro- Mhlanga, I., Ndaimani, H., Mpakairi, K., and Mujere, N. (2018). Climate change: ecological and livestock production systems dynamics in Zimbabwe. an uncertain future for dairy farming in Zimbabwe. Trans. R. Soc. South Africa. Sci. Total Environ. 616–617:710–719. doi: 10.1016/j.scitotenv.2017. 73, 237–242. doi: 10.1080/0035919X.2018.1503203 10.257 Ministry of Lands, Agriculture and Rural Resettlement (2016). Overview of Transforming Zimbabwe’s Dairy Value Chain for the Future Action (TranZ DVC) Zimbabwe’s Dairy Industry. Available online at: http://www.agriculture.gov. (2019). Baseline Report: August 2019. Borrowdale: The Zimbabwe Agricultural zw/phlmbeta/index.php/commodities/90-commodities/dairy/119-dairy- Growth Programme (ZAGP). Available online at: http://zagp.org.zw/ industry-overview (accessed 15 June 2021). TrendEconomy (2020). Zimbabwe Imports and Exports. Available online at: Mugandani, R., Wuta, M., Makarau, A., and Chipindu, B. (2012). Re-classification https://trendeconomy.com/data (accessed May 14, 2021). of agro-ecological regions of Zimbabwe in conformity with climate variability Washaya, S., and Chifamba, E. (2018). Smallholder dairy farming: a and change. Afric. Crop Sci. J. 20, 361–369. Available online at: https://hdl. solution to low milk production in Zimbabwe. Dairy Vet Sci J. 8:555735. handle.net/1807/47599 (accessed June 15, 2021). doi: 10.19080/JDVS.2018.08.555735 Munangi, W. (2007). “Strategies for improving the contribution of smallholder World Bank (2021). World Development Indicators. Available online dairy sector to supply milk in Zimbabwe,” in Proceedings, National Dairy at: https://databank.worldbank.org/reports.aspx?source=world-development- Symposium on Reviving the Zimbabwe Dairy Industry, 5–6 July 2007. indicators# (accessed June 15, 2021). Harare, Zimbabwe. Zimbabwe Agricultural Growth Programme (ZAGP) (2019). Available online Mupawaenda, A. C., Chawatama, S., and Muvavarirwa, P. (2009). Gender issues in at: http://zagp.org.zw/Content/Uploads/ZAGP_Profile.pdf (accessed June 15, livestock production: a case study of Zimbabwe. Trop. Anim. Health Prod. 41, 2021). 1017–1021. doi: 10.1007/s11250-008-9268-5 Zimbabwe Dairy Industry Trust (ZDIT) (2021). Dairy Sector Strategic Plan for Murungweni, E. C., Mabuku, O., and Manyawu, G. J. (2004).” Mucuna, lablab improved performance of the Dairy Value Chain in Zimbabwe 2021–2025. and paprika calyx as substitutes for commercial protein sources used in Harare, Zimbabwe: ZDIT. dairy and pen-fattening diets by smallholder farmers of Zimbabwe,” in: Tropical Legumes for Sustainable Farming Systems in southern Africa and Author Disclaimer: The views expressed in this document may not be taken as the Australia. ACIAR Proceedings no. 115, eds A. M. Whitbread and B. C. official views of these organizations. Pengelly (Canberra: Australian Centre for International Agricultural Research), 126–135 Conflict of Interest: The authors declare that the research was conducted in the Mzumara, M. (2012). An overview of Zimbabwe’s absence of any commercial or financial relationships that could be construed as a macroeconomic environment. Int. J. Econ. Res. v3i1, potential conflict of interest. 33–69. Available online at: http://www.ijeronline.com/documents/volumes/ vol1issue1/Vol%203%20issue%201/ijer20120301JF(4).pdf (accessed June 15, The handling editor is currently editing co-organizing a Research Topic 2021). with several of the authors AN, SB, NC, and MP and confirms the absence of any Ndung’u, P., Bebe, B. O., Ondiek, J. O., Butterbach-Bahl, K., Merbold, L., and other collaboration. Goopy, J. P. (2018). Improved region-specific emission factors for enteric methane emissions from cattle in smallholder mixed crop: livestock systems of Publisher’s Note: All claims expressed in this article are solely those of the authors Nandi County, Kenya. Anim. Prod. Sci. 59, 1136–1146. doi: 10.1071/AN17809 and do not necessarily represent those of their affiliated organizations, or those of Ngongoni, N. T., Mapiye, C., Mwale, M., and Mupeta, B. (2006). Factors affecting the publisher, the editors and the reviewers. Any product that may be evaluated in milk production in the smallholder dairy sector of Zimbabwe. Livestock Res. this article, or claim that may be made by its manufacturer, is not guaranteed or Rural Dev. 18, 1–21. Available online at: https://www.lrrd.cipav.org.co/lrrd18/ 6/ngon18089.htm#:~:text=The%20poor%20performance%20of%20cows, endorsed by the publisher. limiting%20in%20the%20smallholder%20sector (accessed June 15, 2021). Nobel, P. S., and Zutta, B. R. (2008). Temperature tolerances for stems Copyright © 2021 Chirinda, Murungweni, Waniwa, Nyamangara, Tangi, Peters, and roots of two cultivated cacti, Napalea cochinillifera and Opuntia Notenbaert and Burkart. This is an open-access article distributed under the terms robusta: acclimation, light, and drought. J. Arid Environ. 72, 633–642. of the Creative Commons Attribution License (CC BY). The use, distribution or doi: 10.1016/j.jaridenv.2007.08.005 reproduction in other forums is permitted, provided the original author(s) and the Peters, M., Mwendia, S., Arango, J., Urrea-Benítez, J. L., and Ohmstedt, U. copyright owner(s) are credited and that the original publication in this journal (2021). Connecting Formal and Informal Systems for Forage Crop Improvement is cited, in accordance with accepted academic practice. No use, distribution or and Scaling. Nairobi (Kenya): Alliance of Bioversity International and CIAT. reproduction is permitted which does not comply with these terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1957 December 2021 | Volume 5 | Article 726482 ORIGINAL RESEARCH published: 15 December 2021 doi: 10.3389/fsufs.2021.719655 Performance of Urochloa and Megathyrsus Forage Grasses in Smallholder Farms in Western Kenya Solomon Waweru Mwendia 1*, Ruth Odhiambo 1, Alfred Juma 2, David Mwangi 3 and An Notenbaert 1 1 International Center for Tropical Agriculture, CIAT, Nairobi, Kenya, 2 Send a Cow-Kenya, Kakamega, Kenya, 3 Kenya Agricultural and Livestock Research Organization (KALRO), Kakamega, Kenya Livestock productivity has remained low in sub-Saharan African countries compared to other places on the globe. The feeding component is the major limitation, in both quantity and quality. Among other inputs, feeding takes 55–70% of the costs involved. Livestock play a major role especially in smallholder mixed farms through provision of household nutrition and income through milk and meat. Equally, fertilization of cropland benefits from livestock manure, and livestock often act as insurance and savings by providing Edited by: liquidity for unforeseen and urgent financial needs. Increasing livestock productivity Stefan Burkart, would enhance the fore-mentioned benefits contributing to well-being and livelihoods. Alliance Bioversity International and CIAT, France Toward this endeavor and with smallholder dairy farmers’ participation, we undertook an Reviewed by: evaluation of 10 selected forages from Urochloa Syn. Brachiaria and Megathyrsus syn. Sarah Palmer, Panicum genus and compared them with Napier grass, i.e., Cenchrus purpureus Syn. Aberystwyth University, Pennisetum purpureum commonly grown by farmers. For detailed and robust evaluation, United Kingdom Juan De La Cruz Jiménez, we established the species in eight trial sites spread in four administrative counties in Nagoya University, Japan Western Kenya (Bungoma, Busia, Kakamega, and Siaya). In each site, the forages were Sara Stephanie Valencia Salazar, The South Border College established in plots in a randomized complete block design, replicated three times. Each (ECOSUR), Mexico site was linked to a group of farmers interested in dairy. For 2 years, drymatter production, *Correspondence: plant height, and leaf-to-stem ratio was determined across all sites. Further, we guided Solomon Waweru Mwendia farmers to generate participatory forage evaluation criteria, which they later administered s.mwendia@cgiar.org across their respective forage demonstration sites individually on plot-by-plot basis to Specialty section: generate preference rating compared to what they normally grow—Napier grass. The This article was submitted to results showed significant differences across the forage types within and between the Climate-Smart Food Systems, a section of the journal sites. Cumulative dry matter yields ranged 13.7–49.9 t/ha over 10 harvestings across Frontiers in Sustainable Food Systems forage types and the counties, while values for crude protein were 1.85–6.23 t/ha and Received: 02 June 2021 110,222–375,988 MJ/ha for metabolizable energy. Farmer preferences emerged that Accepted: 02 November 2021 highlighted forages with likely better chances of adoption with weighed scores ranging Published: 15 December 2021 5.5–7.6 against a scale of 1–9, across the counties. The observations provide additional Citation: Mwendia SW, Odhiambo R, Juma A, and well-performing forage options for the farmers and possibly in similar production Mwangi D and Notenbaert A (2021) systems and ecologies. Awareness creation targeting livestock and dairy producers Performance of Urochloa and Megathyrsus Forage Grasses in would be key, reaching, and informing them on alternative forage options, with potential Smallholder Farms in Western Kenya. to increase livestock productivity. Front. Sustain. Food Syst. 5:719655. doi: 10.3389/fsufs.2021.719655 Keywords: leaf to stem ratio, farmer evaluation, forage quality, dry matter yield, forage grass Frontiers in Sustainable Food Systems | www.frontiersin.org 1158 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation INTRODUCTION MATERIALS AND METHODS Tenacious low livestock productivity in sub-Saharan African Site Selection (SSA) countries is by and large due to inadequate feeding Four counties in western Kenya were selected based on their high (Alejandro et al., 2007). Feeds and forages account for up to bio-physical potential for dairy and commercialization, namely, 70% of costs in livestock production (Odero-Waitituh, 2017). Bungoma, Busia, Kakamega, and Siaya (Figure 1). Despite the Hitherto, meat and milk demands in SSA are growing at 3.4 areas being in mid-altitude 900–1,800m, they differ agro- and 2.9% annually, respectively (Latino et al., 2020). As such, ecologically (Jaetzold et al., 2006). In addition, soils we analyzed the estimated consumers’ demand of 35 and 83 billion tons for from the specific trial sites showed significant differences in meat and milk, respectively, by 2050 (World Bank, 2014) will key soil attributes (Table 1). With a soil auger, we collected remain a challenge unless livestock feeding is addressed. Land soil samples at 0–50 cm depth, and 3 samples along a replicate, as a production resource is limited especially in intensifying hence 9 samples per site, and 72 samples from the 8 sites. In smallholder systems, and it is no longer possible to allocate partnership with Send a Cow Kenya (SACK), a development land for free grazing. However, cultivated forage presents a partner, in these sites we linked up with farmer groups that have realistic avenue to meet ruminant roughage requirements under been engaged in SACK initiatives on improving human nutrition such circumstances. Albeit extensive forage catalogs exist, efforts and incomes and selected two farmer groups with a keen interest toward forage improvement through selection and/or breeding in dairy per county, resulting in eight trial sites (Figure 1). are limited compared to food crops globally. In SSA this has Soil sample analysis was done at International Livestock resulted in use of non-nutritious crop residues (FAO, 2018) Research Institute (ILRI), Nairobi, focusing on pH, total and limited forage options developed decades ago. Use of low carbon, nitrogen, and phosphorus and contents of clay, sand, nutritious roughages in turn results in undesirable high emission and silt. of methane gas per unit of product, associated with global warming (Makkar, 2016). Forage Technologies, Trial Design, Therefore, there is need to identify and deploy improved Planting, and Management forage technologies in SSA to bolster livestock productivity. At the start of the project, we sensitized the selected farmer Use of grasses from genus Brachiaria (now Urochloa) and groups on dairy improvement and the importance of animal Panicum (now Megathyrsus) present realistic options toward feeding. Consequently, we offered them to try out several forage quality and quantitative roughage production. For example, options with potential to grow well in the region. In the end, use of Urochloa hybrids has been successful in Latin America, the groups offered land where we established demonstration supporting improved livestock productivity, especially beef trials. While the project provided forage seeds and technical (Rivas and Holmann, 2005).With temporal and spatial variations advice, farmers agreed to provide labor for land preparation, to environments, matching forage genotypes to biophysical planting, weeding, harvesting, and monitoring the performance environment and agricultural context remains unsatisfactory of the grasses. We selected 10 forage grasses covering 3 hybrids in SSA. We therefore set out to evaluate the performance and 4 cultivars from genera Urochloa. The hybrids include of selected grass lines from Urochloa and Megathyrsus under Cayman, Cobra, and Mulato II and the cultivars Basilisk, farmers’ context in western Kenya. Involving farmers who are the Piata, Xaraes, and MG4. Xaraes and MG4 are also known as end users is desirable as participation brings to the fore farmers’ Toledo and La Libertad, respectively. For Megathyrsus genera, perspective on attributes/characteristics they use on choice of we included cultivars Mombasa, Tanzania, and Massai. Napier forages to grow and therefore guide on forage breeding and grass (Cenchrus purpureus Syn. Pennisetum purpureum) from selection in order to meet desired traits. The importance of the farmers’ farms was included as a control. The trial design participatory approaches have been underscored (Abeyasekere, was a randomized complete block design with three replicates 2001), and for example, Mwendia et al. (2017a) used the same per site and in eight sites. Farmers manually prepared the land to evaluate oat varieties for forage production in central Kenya. by digging with hoes to about 0.2m depth. To get sufficiently Largely, western Kenya is moving toward intensified livestock fine seedbed, farmers broke down big soil clods to the required production owing to high and growing human population soil tilth. Using wooden pegs, we marked out 15 m2 plots (3 coupled with land subdivision over generations reducing areas × 5m) with 33 of them per site, to allow 3 replicates of the of free grazing (Waithaka et al., 2002). As such, there is limited 11 grasses selected. Therefore, in the 4 counties we had 8 sites grazing on natural pasture and there is a buildup on cattle and 264 plots in total. Because of acidic soils in western Kenya in confinement under cut-and-carry systems. The genotypes (Kanyanjua et al., 2002), we applied lime at 2 t/ha prior to Urochloa and Megathyrsus trace their origin in tropical Africa planting. At planting in May 2018, we randomly allocated the and only improved through selection and/or breeding (Cook grasses to the prepared plots. We used the recommended seed et al., 2020). Therefore, the forages stand a good chance in rate for each genus, i.e., 6 kg/ha for Urochloa (Njarui et al., 2016) fitting under cut-and-carry intensified systems. We hypothesized and 3 kg/ha for Megathyrsus, while for Napier grass we used variable performance of these grasses under different locations splits spacing at 1 × 1m grids (Mwendia et al., 2017a,b). We and varying farmers’ preference, results that would have potential applied NPK inorganic MEA fertilizer©R (NPK fertilizer 23:23:0) to influence wider scaling of these grasses in western Kenya at the rate of 50 kg N/ha. Because of small seed size in Urochloa and beyond. and Megathyrsus, shallow hills of about 0.02m depth, 0.3m Frontiers in Sustainable Food Systems | www.frontiersin.org 1259 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation FIGURE 1 | Experimental sites in Busia, Bungoma, Kakamega, and Siaya counties in western Kenya indicating farmer groups linked to the sites during the experiment in 2019–20. TABLE 1 | Summary of rainfall, altitude, agro-ecological zones, soil characteristics, and farmer groups selected in the trial sites in Bungoma, Busia, Kakamega, and Siaya counties in western Kenya. Attribute Bungoma Busia Kakamega Siaya Precipitation (mm) 1,536–1,681 1,585–1,690 1,800 1,320 Altitude (m) 1,433–1,829 1,200–1,440 1,300–1,550 890–1,020 Agro-ecological zone Low Midland 2 Low Midland 1 Low Midland 1 Low Midland 4 Selected Farmer groups Joy, Nateo Nasira, Nasietike Isongo A, Isongo B Pionare; Mowar Jorit Kiye Soil characteristics lsd pH 5.6a 5.4bc 5.5ab 5.3c 0.13 Total C (%) 0.83c 1.34a 0.95b 0.83c 0.117 Total N (%) 0.073c 0.11a 0.075c 0.082bc 0.008 P (Mg/kg) 6.9b 3.55c 9.24a 4.06c 1.97 Clay (%) 28.2b 45.2a 27.2b 43.9a 5.88 Sand (%) 65.2a 35.7c 62.4a 45.7b 7.49 Silt (%) 6.7c 19.1a 10.4b 10.4b 1.93 For soil characteristics n = 18 per county and means with different superscript in a row differ p < 0.05. between hills in a row, and 0.45m row-to-row for Urochloa manually maintained plots weed-free as necessary. The grasses were used, and shallow furrows of about 0.02m depth spaced took 3 months to establish, and standardization cut was done in at 0.3m row to row for Megathyrsus. After planting, farmers September 2018. Frontiers in Sustainable Food Systems | www.frontiersin.org 1360 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation Forage Participatory Evaluation and Dry scores by farmers and multiplied with the criteria scoring by the Matter Yield Measurements group, to generate weighted scores (Abeyasekere, 2001; Mwendia In each of the counties we selected one group (Nasietike, et al., 2017a) and subsequent ranking of the forages on county- Joy, Mowar Jorit Kiye, Isongo B) to undertake participatory by-county basis. evaluation at the demonstration sites. The evaluations took place when the forages had established well and just before the third RESULTS harvesting (described below). We guided each of the four farmer groups in developing criteria that describe the attributes they Analysis of Variance Summary Across Main prefer in a forage grass. On a scale of 1–9, the farmers as a group Effects and Interactions scored each criterion where 1 = least important and 9 = most Significant differences were found in all traits for both county and important (Mwendia et al., 2017a). Subsequently, each farmer forage grass type (Table 2).Where interactions were observed, we was provided with a printed sheet containing 33 plots numbered focused on their means for results and discussion. serially in a column and the criteria developed by the group earlier along the topmost row. At the demonstration site, each Soil Characteristics and Dry Matter Yields farmer scored each plot across all the criteria, until all the plots The soils were significantly acidic in Siaya (p < 0.05) than were complete. We collected all data sheets for later weighted Bungoma and Kakamega (Table 1). Busia had greater carbon score analysis (Abeyasekere, 2001). and nitrogen content than the other counties but had the least For dry matter yields the first harvest after standardization was January 2019. We allowed growth cycles of about 8 weeks (Njarui et al., 2016) after which the grasses were harvested at a stubble height of about 5–10 cm. Before cutting, we randomly TABLE 2 | Significance of main effects and interactions for cumulative dry matter yields, leaf:stem ratio, cumulative crude protein yield, metabolizable energy, and selected and measured plant height of five tillers in each plot digestible organic matter. from the soil level to the tip of the topmost standing height. Fresh yield weight was measured with a digital weighing balance Attribute Main effects/interaction P Significance (KERN CH 50K50 with 10 g precision) and recorded on plot- by-plot basis each measuring 15 m2. A sample of about 450 g Mean DM (repeated Time <0.001 *** measures) (t/ha) per plot was randomly selected after mixing thoroughly the Time × County <0.001 *** whole harvested biomass from each plot, for dry matter content Time × group <0.001 *** determination. The sample as weighed and put inside a sample Time × forage <0.001 *** bag labeled and taken to the International Center for Tropical Time × county × forage 0.008 ** Agriculture (CIAT) sample processing room in Kisumu, western Time × group × forage 1 NS Kenya. Samples were manually separated into leaves and stems, Cumulative DM yield Block/replicate 0.042 * labeled, and dried in an oven at 65◦C for 48 h to determine (t/ha) County <0.001 *** dry matter content and leaf: stem ratio. Corresponding leaf and Group <0.001 *** stem samples were combined back for further nutrition analysis Forage <0.001 *** (described below). The process was repeated for 10 consecutive County × forage <0.001 *** cuttings, running in 2019 and 2020 except for nutritional Group × forage 1.00 NS analysis done only for the third harvest that had undergone Leaf:stem ratio Block/replicate 0.452 NS rain season. County <0.001 *** Group 0.928 NS Forage Nutritive Value Determination Forage <0.001 *** Dried samples were ground to pass through 1mm sieve, County × forage 0.008 ** packed in plastic zip-lock bags and sent for near-infrared- Group × forage 1.00 NS system (NIRs) analysis at Crop Nutrition Laboratory Services Cumulative CP yield Block/replicate 0.202 NS Ltd, Limuru, Kenya (https://cropnuts.com/service/animal-feed- (t/ha) County 0.019 * analysis/). Analysis targeted metabolizable energy (ME), crude Forage <0.001 *** protein (CP), and in vitro organic matter digestibility (IVOMD). County × forage 0.002 ** Cumulative ME (MJ/ha) Block/replicate 0.346 NS Data Analyses County <0.001 *** All data were managed in Microsoft Excel, and statistical analysis Forage <0.001 *** was carried out in GenStat 18th edition. We carried out repeated County × forage <0.001 *** measures analyses of variance (ANOVA) where fixed variables Cumulative digestible Block/replicate 0.316 NS included harvest number/time, site/location, and test forage organic matter (t/ha) County <0.001 *** grasses, while response variables included plant height, dry Forage <0.001 *** matter yields, leaf:stem ratio, ME, CP, and digestible organic County × forage <0.001 *** matter, with the means separated by least significance difference (lsd). For the participatory evaluation we pooled individual P < 0.05*; P < 0.01**; P < 0.001***; NS, Not significant. Frontiers in Sustainable Food Systems | www.frontiersin.org 1461 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation phosphorus content, only similar to Siaya. By the proportions the counties the order of dry matter yield was Bungoma > (%) of clay, sand, and silt, soil types in the sites were found to be Kakamega > Busia > Siaya (Figure 2). In Joy group site in as follows: sandy–clay–loam, clay, sandy–clay–loam, and sandy– Bungoma, Napier grass produced more biomass than Mulato II, clay for Bungoma, Busia, Kakamega, and Siaya, respectively. The MGA, and Basilisk but similar to the other grasses. This was mean drymatter per harvest showed significant differences across different for Nateo group in the same county, where Napier the harvests and interactions between sites and harvest, forage grass only produced more than Mulato II but significantly genotype and harvest, and sites and forage genotype (Table 3). less than Cayman, MG4, Xaraes, Piata, Tanzania, Mombasa, The second and third harvests showed the least and greatest and Massai. In this site, Xaraes accumulated the most biomass dry matter yields, respectively. In Bungoma and Busia sites, significantly greater than all the grasses, except similar to Massai the second and fourth harvests presented the least and greatest cultivar. In Busia County and at Nasietike group site, Napier dry matter yields, respectively, unlike in Kakamega and Siaya grass produced the least biomass against all the other grasses. where the greatest biomass yield was in the third and seventh Megathyrsus cv Massai produced the most, significantly greater harvests, respectively. On forage genotype–harvest interaction, than all grasses, except similar to Basilisk and Mombasa. In Busia forage type producing the most dry matter yield varied across the second site, Nasira group, maintained the yield pattern for the harvestings. In the first harvest, Basilisk produced most, the grasses. Although Napier grass accumulated the least, it was and Napier grass in second and third. From the fourth to the similar to all the other grasses except for the three Megathyrsus tenth harvests, Massai dry matter yield surpassed all the others species, Cayman, and Basilisk that produced significantly greater except in the ninth harvest wherein Napier grass produced the biomass. In Kakamega County and at Isongo A group site, most. On site–forage interaction, the most dry matter production Basilisk accumulated greater biomass than all grasses except was from Xaraes in Bungoma and Massai for Busia, Kakamega, for Megathyrsus cv Massai which had similar biomass. Among and Siaya. Urochloa hybrids, only Cayman had similar biomass to Napier Cumulative dry matter yields over 10 cuttings showed grass. At Kakamega second site, Isongo B, Napier grass produced interaction between the county and the grasses. Generally, across similar biomass to Mombasa and Massai, and the rest had TABLE 3 | Mean dry matter yields (t/ha) per harvest over ten harvests and interactions for site × harvest, forage genotype × harvest, and site × forage genotype for 3 Urochloa hybrids (Cayman, Cobra, Mulato II) 4 Urochloa cultivars (Basilisk, MG4, Piata, Xareas), 3 Megathyrsus cultivars (Maasai, Mombasa, Tanzania) and Napier grass. Attribute County/forage Harvest P lsd type 1 2 3 4 5 6 7 8 9 10 Harvest 2.69e 0.98f 4.29a 4.05a 3.74b 3.15c 3.60b 3.42c 3.20c 2.97de <0.001 0.29 Site × harvest Bungoma 3.85de 0.42l 5.04b 6.22a 4.18cd 3.77e 2.99gh 4.04cd 4.48c 2.89gh Busia 2.98gh 2.35ij 3.46ef 3.69ef 2.58ij 2.05jk 3.17fg 3.34ef 2.67gh 2.71gh <0.001 0.53 Kakamega 1.76k 0.64l 5.08b 3.52ef 4.10cd 3.14g 3.71e 2.82gh 2.96gh 3.67ef Siaya 2.16ijk 0.50l 3.56ef 2.77gh 4.11cd 3.64ef 4.50c 3.49ef 2.67gh 2.59hi Forage genotype Napier 2.30gh 1.19h 4.85ab 3.67ef 3.19ef 3.30ef 3.05ef 3.81cd 3.98cd 3.70ef × harvest Cayman 3.43ef 1.10i 3.98cd 3.56ef 3.23ef 2.38g 3.07ef 3.04ef 2.56g 2.33g Cobra 2.68g 1.05i 3.97cd 3.49ef 3.72de 2.77g 3.21ef 2.70g 2.81ef 2.33g Mulato II 1.15i 0.76i 3.24ef 2.08gh 2.74g 1.99gh 2.80ef 2.34g 2.57g 2.59g Xareas 2.60g 0.95i 4.62cd 3.95cd 3.72de 3.33ef 3.63ef 3.76cd 3.49ef 3.14ef <0.001 0.93 MG4 2.61g 0.82i 4.71ab 3.77cd 3.69ef 2.68g 3.87cd 3.03ef 3.03ef 2.59g Basilisk 3.62ef 0.81i 4.39cd 3.64ef 3.90cd 3.39ef 3.88cd 3.29ef 2.92ef 2.84ef Piata 2.78fg 1.00i 4.76ab 4.63cd 3.49ef 3.15ef 3.71ef 3.44ef 3.18ef 2.88ef Mombasa 2.70g 0.95i 4.00cd 5.62a 4.56cd 4.12cd 3.88cd 4.11cd 3.39ef 3.39ef Tanzania 3.21ef 1.00i 3.90cd 4.48cd 3.47ef 3.24ef 3.76cd 3.70ef 3.59ef 3.12ef Maasai 2.50g 1.11i 4.72ab 5.64a 5.46ab 4.30cd 4.68bc 4.40cd 3.64ef 3.71ef Site × forage Basilisk Cayman Cobra Massai MG4 Mombasa Mulato II Napier Piata Tanzania Xaraes genotype Bungoma 3.47cd 3.87ab 3.58cd 4.13ab 3.57cd 4.07ab 2.63ef 3.89ab 4.20ab 3.87ab 4.40a Busia 3.15cde 2.97de 2.96e 3.68bc 2.69ef 3.42cd 2.25g 2.26fg 2.57ef 3.22cde 2.72ef <0.001 0.65 Kakamega 3.20cde 2.77ef 2.87ef 3.92ab 3.19cde 3.31cd 2.65ef 3.46cd 3.10cde 2.88ef 3.18cde Siaya 3.25cd 1.85gh 2.08g 4.34a 2.87ef 3.89ab 1.38h 3.60cd 3.34cd 3.43cd 2.98de In Bungoma, Busia, Kakamega and Siaya counties in western Kenya in 2018–2021. Means without common superscript within an attribute category differ significantly. Frontiers in Sustainable Food Systems | www.frontiersin.org 1562 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation FIGURE 2 | Mean cumulative dry matter yield t/ha over 10 harvestings in 2 years, for 3 Urochloa hybrids, (Cayman, Cobra, Mulato II), 4 Urochloa cultivars (MG4, Basilisk, Piata, Xaraes) and 3 Megathyrsus cv (Mombasa, Tanzania, Maasai), compared to Napier grass in four counties, each with two farmer groups namely, Bungoma (Joy, Nateo), Busia (Nasietike, Nasira), Kakamega (Isongo A, Isongo B) and Siaya (Mowar Jorit kiye, Pionare) in western Kenya. Bars with different letter differ significantly p < 0.05. significantly lower biomass (Figure 2). In this site, Megathyrsus tall and short plants, respectively. However, the order was cv Massai accumulated most dry matter significantly. In Siaya Napier grass > Mombasa > Tanzania > Massai > Xaraes > County and at Mowar Jorit Kiye farmer group site, Megathyrsus Basilisk ≈ MG4 > Piata > Cobra > Cayman > Mulato II. cv Massai accumulated the greatest biomass only similar to Leaf:stem ratio varied within and between counties. Across the Napier grass but significantly greater than all the other grasses. counties, only Mulato II hybrid, Xaraes cultivar, and the three The three Urochloa hybrids accumulated significantly low Megathyrsus attained leaf:stem ratio of 2. In Bungoma and biomass than all the Urochloa cultivars, Megathyrsus cultivars, Busia Counties, Mulato II attained the highest, Megathyrsus cv and Napier grass. In the second site of this county, Megathyrsus Mombasa in Kakamega, andMegathyrsus cv Massai in Siaya. The cv Mombasa accumulated greater biomass than all the other least leaf:stem ratio was by Napier grass in Bungoma and Basilisk grasses, while the three Urochloa hybrids accumulated the least in the other three counties. (Figure 2). CP yield (t/ha) varied across the grasses and within and between counties (Table 4). In Bungoma most of the grasses Plant Height, Leaf–Stem Ratio, Crude produced statistically similar CP yield including Piata, Massai, Protein, and Metabolizable Energy Mombasa, Tanzania, Xaraes, Basilisk, MG4, Cobra, and Cayman. Plant height significantly varied across counties and forage Mulato II and Napier grass accumulated statistically low CP grasses (Table 4). Napier grass and Mulato II consistently had yield compared to Piata. In Busia County, there was a change in Frontiers in Sustainable Food Systems | www.frontiersin.org 163 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation TABLE 4 | Mean plant height (m), leaf to stem ratio, crude protein (t/ha), metabolizable energy (ME MJ/ha), and digestible organic matter (t/ha) for Napier grass, Urochloa hybrids (Cayman, Cobra, Mulato II), Urochloa cultivars (MG4, Basilisk, Xaraes, Piata), and Megathyrsus cultivars (Tanzania, Mombasa, Maasai) over 10 harvestings in 2019 and 2020 in western Kenya. Attribute County Napier Cayman Cobra Mulato II MG4 Basilisk Xaraes Piata Tanzania Mombasa Massai P lsd Plant height Bungoma 1.23a 0.40kl 0.45ji 0.27nop 0.46jl 0.46jl 0.58hi 0.50ij 0.62fg 0.67fg 0.59hi (m) Busia 0.80cd 0.35mop 0.37m 0.30mop 0.41jl 0.45jl 0.49j 0.35mop 0.56hi 0.67fg 0.60gh <0.001 0.09** Kakamega 1.00b 0.35mop 0.37m 0.29mop 0.38lm 0.40kl 0.51hi 0.40kl 0.56hi 0.64fg 0.55hi Siaya 1.14a 0.34mop 0.36mo 0.26p 0.50ij 0.44jl 0.51hi 0.47jl 0.78de 0.71ef 0.63fg Leaf: Stem Bungoma 1.12g 1.64de 1.48ef 2.20ab 1.80cd 1.17g 1.99ab 1.88cd 1.90cd 2.18ab 2.12ab ratio Busia 1.58ef 1.95bc 1.83cd 2.28a 1.99ab 1.20g 2.15ab 1.78cd 2.15ab 2.13ab 1.91cd 0.007 0.30** Kakamega 1.25g 1.37ef 1.32fg 1.84cd 1.84cd 1.12g 2.01ab 1.78cd 2.15ab 2.23ab 1.90cd Siaya 1.15g 1.62ef 1.52ef 1.85cd 1.52ef 1.05g 1.87cd 1.54ef 1.72cd 1.75cd 2.05ab Cumulative Bungoma 3.28de 4.07cd 4.06cd 2.99ef 4.02cd 3.75cd 4.41cd 4.74c 3.64cd 4.16cd 4.59cd CP yield Busia 5.69abc 4.46bcd 4.54bcd 2.83ef 3.72cd 5.36ab 3.63cd 3.94cd 4.80bc 4.74c 4.29cd t/ha Kakamega 5.01ab 4.18cd 3.71cd 4.32cd 4.48cd 6.00a 3.87cd 4.11cd 3.49cd 3.80cd 4.92ab 0.002 1.37** Siaya 4.44cd 2.56ef 2.78ef 1.85f 3.80cd 4.29cd 3.59cd 3.85cd 3.84cd 4.79c 6.23a Cumulative Bungoma 238778cd 272997cd 268066cd 184435e 260554cd 255259cd 327951ab 326060ab 275467cd 293008c 305066ab Me MJ/ha Busia 202349e 234097cd 229936cd 169085ef 213675de 236998cd 204489e 189494e 250604cd 293404bc 288773c <0.001 71377.5*** Kakamega 272373cd 257685cd 223583cd 262288cd 292982c 359970ab 270479cd 261986cd 238141cd 253733cd 309929a Siaya 322384ab 145105ef 165401ef 110222f 262374cd 255720cd 257754cd 263601cd 264696cd 282990cd 375988a Cumulative Bungoma 17.02cd 19.87cd 19.46cd 13.40ef 18.84cd 18.37cd 23.58ab 23.54ab 19.75cd 21.14cd 21.88bcd digestible Busia 15.09ef 17.37cd 17.04cd 12.33efg 15.67ef 17.95cd 15.02ef 14.12ef 18.54cd 21.46cd 20.95cd <0.001 5.20*** organic Kakamega 19.94cd 18.89cd 16.39de 19.18cd 21.30cd 26.28ab 19.63cd 19.10cd 17.27cd 18.43cd 22.52ab matter (t/ha) Siaya 23.14ab 10.61fg 12.07efg 8.01g 18.97cd 18.56cd 18.51cd 19.00cd 19.09cd 20.69cd 27.29a Means with different superscripts within an attribute category are significantly different. **P < 0.01, ***P < 0.001. the order. Napier grass produced the most that was statistically greater than all the other grasses except forMG4 andMegathyrsus similar to those of Cayman, Cobra, Basilisk, Tanzania, Mombasa, cv Massai. In Siaya County, Megathyrsus cv Massai accumulated and Massai. Only Mulato II, MG4, Xaraes, and Piata have the most and similar to Napier grass. The values for Mulato II statistically low CP yield compared to Napier grass. In Kakamega, were the lowest in this county and by 3.4 times compared to cultivar Piata accumulated the most CP yield statistically greater Megathyrsus cv Massai. than all the other grasses except for Napier grass andMegathyrsus cv Massai. In Siaya, Megathyrsus cv Massai yielded the most Participatory Evaluation CP that was statistically greater than for all the other grasses To connect biophysical performance of the grasses with end- (Table 4). users, we undertook farmers’ participatory evaluation. Farmers Cumulative ME yield (MJ/ha) varied cross the counties and from the counties and linked to the trial site’s groups developed among grasses (Table 4). In Bungoma, Xaraes accumulated the criteria that were closely related as follows. Nasietike from most that was statistically greater than all the grasses except for Busia identified disease tolerance, fast germination, fast regrowth, Piata and Massai. In Busia County, Megathyrsus cv Mombasa high germination rate, leafiness, more milk, softness, upright accumulated the most that was statistically greater than those of growth, drought tolerance, high biomass, and palatable as key Piata, MG4, Mulato II, and Napier grass but similar to the other considerations. This was similar for the other groups except grasses. In Kakamega County, Basilisk accumulated statistically Bungoma Joy group, which did not identify upright growth greater ME than all the grasses except Megathyrsus cv Massai. while Siaya’s Mowar Jorit Kiye and Kakamega’s Isongo B groups Hybrid Cobra produced the least in the county compared to other identified greenness that was not identified by Nasietike or grasses. In Siaya County, Megathyrsus cv Massai accumulated Joy. Pooled ratings across the groups and by grass type varied statistically greater ME than all the grasses except Napier grass, (Figure 3). According to Nasietike group the order of preference while Mulato II produced the least. emerged as Cayman >Xareas > Cobra ≈ Mombasa > Tanzania On cumulative digestible matter in Bungoma County, Xaraes > Piata Massai ≈ Mulato II > MG4 > Napier ≈ Basilisk. For produced the most and statistically more than Napier grass and Joy group the order started the same as Nasietike for the first Mulato II (Table 4). Although Mulato II had the least, it was two but followed by interchange of the subsequent grasses. The similar to that of Napier grass and Basilisk. In Busia County, order was Cayman > Xaraes > MG4 ≈ Mombasa > Piata > the order was different. Megathyrsus cv Mombasa had the most Basilisk > Cobra > Massai≈ Tanzania > Mulato II > Napier. In digestible organic matter, statistically greater than those of Napier Siaya by Mowar Jorit Kiye group the order sorted differently as grass, Mulato II, MG4, Xaraes, and Piata. This was unlike in Cobra ≈ Napier > Xaraes > Piata ≈ MG4 > Cayman > Massai Kakamega County where Basilisk had the most and statistically > Mombasa > Mulato II > Basilisk > Tanzania. Kakamega by Frontiers in Sustainable Food Systems | www.frontiersin.org 1764 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation FIGURE 3 | Weighted Scores on 1–9 scale, where 1 = least important, 9 = most important against forage grass types for Nasietike farmer group (A), Joy farmer group (B), Mowar Jorit Kiye farmer group (C,D) Isongo B farmer group before third harvesting in 2019 in western Kenya. Isongo B further presented a different order as MG4≈Mulato II Dry matter yields realized in the study show the grasses and ≈ Massai > Basilisk > Cayman ≈ Cobra ≈ Piata ≈ Tanzania > performance in the different sites. Clearly, a grass doing well Napier > Mombasa > Tanzania (Figure 3). in one location did not necessarily do so in another location. This is governed by grass genotype–environment interaction with environmental attributes including temperatures, soil type, DISCUSSIONS and rainfall coming into play. Even within areas that are in close proximity, differences are likely to emerge because of The overall objective of identifying performance of the different transient conditions that may exist in one site and not the other. forages in different locations and engaging the end users was For example, while Napier grass at the Joy site in Bungoma met. Indeed, in western Kenya with trial sites characterized by accumulated significantly greater biomass than other grasses temporal and spatial differences, the sites equally showed variable (Figure 2), this was remarkably reversed in Nateo site in the performance (Tables 2–4) and farmers’ ratings (Figure 3). The same county. The essence of placing the grass technologies results present important information that would connect well in an agricultural context, therefore, serve to get the actual with intensions of improving forage production in the region, performance to inform recommendations, rather than providing to contribute to improved livestock productivity especially generalized recommendations, but advise based on empirical cattle under the smallholder mixed farming in the area. The evidence derived. As such, it would not be advisable to grow importance of matching forage with biophysical environment Urochloa hybrids in Siaya and other areas similar to the site, and agricultural context is reported in previous research efforts but the Megathyrsus or Urochloa cultivar stands a better chance. (Tilman et al., 2011; Mwendia, 2015), and this work adds onto While Napier grass is the most grown fodder in the study the basket of options toward this endeavor. counties (Khan et al., 2014), results here show that it does not Frontiers in Sustainable Food Systems | www.frontiersin.org 1865 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation produce well in Busia compared to theUrochloa andMegathyrsus Mulato II with slightly less than a foot height would varieties considered in this case study, indicating the latter two be relatively difficult for proper hand grip during harvest, could successfully be used for livestock by producers in the area. which may make it less attractive in smallholder cut-and-carry However, in Joy and Mowar Jorit Kiye sites, Napier grass would systems. However, Mulato II’s leafiness, an attribute important be more advantageous especially on dry matter quantity than in ruminants, as they select for leaves as opposed to stems either Cobra, Mulato II, MG4, Basilisk, and all the other grasses (Mwendia et al., 2017b), is preferable. Short forages could fit except Massai for the two sites respectively. The suitability of the better in systems where cattle graze directly without trampling Megathyrsus and Urochloa grasses in the current study clearly that could lead to forage wastage/losses. Forage improvement, emerged. Specifically, in Busia County, Cayman, Cobra, Massai, e.g., breeding, should therefore take into consideration the traits Tanzania, and Mombasa are better options than Napier grass, that fit under a given agricultural context as explained, in especially in Nasietike site. In Kakamega and similar ecologies smallholder cut-and-carry systems. to the study sites, Basilisk could be a grass of choice at Isongo Despite the low plant height for Mulato II, its great leaf:stem A site and Megathyrsus cv Massai in Isongo B. Equally, Massai ratio compensates for its relatively low biomass yield, as most would also be a cultivar of choice at Mowar Jorit Kiye and nutrients are in the leaves, and in effect the CP yield, ME, and Mombasa at Pionare site, both in Siaya County. Choice of digestible organic matter were similar to most of the grasses, cultivar could make a huge difference in bridging the forage e.g., in Kakamega and Bungoma. As such, Mulato II presents quantity gap, which is often characteristic in intensified mixed good quality also often a challenge in livestock production, smallholder systems in SSA (FAO, 2018). As observed in Busia, and breeding for leafiness in forage would be preferable. While the cultivar Massai nearly doubled the biomass of Napier grass, harvesting could pose a challenge to smallholder livestock which means providing roughage for nearly double the number producers dealing with Mulato II, its good quality should of feeding days of Napier grass. Similarly, in Bungoma, Mulato warrant investigating and devising cheap tools that could help in II and Xaraes outperformed Napier grass (Figure 2). Any extra harvesting and make it friendly to grow. biomass production from the same unit of land is preferable, The ratings by farmers (Figure 3) largely relied on what demonstrating improved resource-use efficiency, key especially they could discern phenotypically, and it is interesting to note in the face of global warming (Makkar, 2016). Extra feeding days that this assessment is fully in line with the quantified physical for dairy producers translate into extra milk yield and a clear and laboratory assessment. For example, in the Nasietike group livelihood benefit. from Busia where they ranked Cayman, Xaraes, Cobra, and While all the forage grasses in this study follow the C4 Mombasa highly, we see that the same varieties also did well on photosynthetic pathway, being tropical grasses, their differences leaf:stem ratio, plant height, CP and ME yields, and digestible in performance could most probably be explained by physiology organic matter (Table 4). This underscores the importance of and/or adaptations that were not measured in the current study. including farmers’ preferable traits in forage selection and For example, the grasses doing well in the relatively dry areas are breeding, to end with products that adapt to not only ecological likely to have better stomatal control when faced with limited soil niche but agricultural content under consideration. Participatory moisture, exhibit osmotic adjustment, or may be accumulating evaluation would indicate high chances of adoption, while good greater root biomass to aid in nutrient and water exploration biophysical characteristics ensures that this adoption also has a (Mwendia et al., 2013). Having greater leaf area index could also positive impact on livestock productivity. be beneficial in intercepting more light for photosynthesis and hence growth. Equally, some of the grasses have better nutrient and water use efficiency. This is an area worth investigating CONCLUSIONS further in a physiological study to unravel key drivers responsible for the differences observed. In situ evaluation of the forages revealed how the forages perform While plant height is positively correlated with biomass, on biomass production, quality, and farmers’ preferences. A and inversely with forage quality (Tessema et al., 2010), plant mixed order of performance emerged from the study sites. height also has implications especially where manual forage While Napier grass is the prevalent forage grown across the harvesting is practiced in smallholder farms (Mwendia et al., study sites, evidence we show here reveals that there are 2017a,b). For the 11 grasses evaluated, none exhibited prostrate alternative forage grasses that can be grown and provide great growth habit, and all had upright tillers. Tall plants facilitate and quality roughages for ruminant production. In Siaya, which easier handling/grasping when cutting to the required stubble is relatively dry, the Megathyrsus, Napier grass, and Urochloa height. In this regard, Napier grass, the Megathyrsus and ecotypes are better suited. However, in Busia, Napier grass Urochloa cultivars, and the hybrids, in that order, would suit is least suitable with options of Urochloa hybrids (Cayman manual harvesting by farmers. However, there is a need to and Cobra) and the three Megathyrsus cultivars being better compromise and ensure forages are not allowed to overgrow possibilities. All the grasses except Mulato II performed well in as quality deteriorates. Although we did not report neutral Bungoma, of which the farmers prefer Cayman, Xaraes, MG4, detergent fiber, it is usually negatively correlated with organic and Mombasa. In Kakamega, both the farmers’ selection and matter digestibility (Roche et al., 2009); thus, the lower values agronomic performance indicate the virtuous grasses would be for digestible organic matter (Table 4) suggest greater neutral Megathyrsus cv Massai, Urochloa cultivars Basilisk and MG4, detergent fiber. and Urochloa hybrid Mulato II. It is paramount that future Frontiers in Sustainable Food Systems | www.frontiersin.org 1966 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation forage selection and breeding take into consideration farmers’ trials and editing the manuscript. AN participated in design of preferable traits in a given agricultural context. Following forage the trial and engaging the partners during the trial as well as evaluation for 2 years and farmers’ involvement, the inferences writing the manuscript. All authors contributed to the article and we believe provide a strong basis for practical implementation approved the submitted version. and promotion of the forages in the areas and by extension in other similar ecologies. FUNDING DATA AVAILABILITY STATEMENT This work received financial support from the German Federal Ministry for Economic Cooperation and Development The raw data supporting the conclusions of this article will be (BMZ) commissioned and administered through the Deutsche made available by the authors, without undue reservation. Gesellschaft für Internationale Zusammenarbeit (GIZ) Fund for International Agricultural Research (FIA), Grant Number: AUTHOR CONTRIBUTIONS 81219431, which is highly appreciated. The authors participated in various ways regarding the work ACKNOWLEDGMENTS reported in the manuscript and they have all agreed the manuscript to be summited to Frontiers special issue on forages. We want to acknowledge the farmers who took their time SM designed and established the trials, analyzed data, and wrote and showed interest in the forages, without which this the manuscript. RO participated in data collection and engaging work would not be complete. The Send a Cow—Kenya the farmers. AJ identified the farmers groups discussed the trials staff who participated in one way or another on following and also engaged the farmers during the trials. DM participated the forage trials in different locations in western Kenya is in engaging farmers and observing agronomic measures in the highly appreciated. REFERENCES Mwendia, S. W., Yunusa, I. A. M., Sindel, B. M., Whalley, R. D. B., and Kariuki, I. W. (2017b). Assessment of napier grass accessions in lowland and highland Abeyasekere, A. (2001). Analysis Approaches in Participatory Work Involving tropical environments in East Africa: productivity and forage quality. Exp Ranks and Scores. Reading: Statistical Services Centre, University of Reading. Agricult. 53, 27–43. doi: 10.1017/S001447971600003X Available online at http://www.reading.ac.uk/ssc/ (accessed February 23, 2021). Mwendia, S. W., Yunusa, I. A. M., Whalley, R. D. B., Sindel, B. M., Kenney, D., and Alejandro, N., Ehui, S., and Benin,. S. (2007). Livestock productivity in developing Kariuki, I. W. (2013). Use of plant water relations to assess forage quality and countries: an assessment. Handbook of Agricultural Economics 3, 2461–2532. growth for two cultivars of napier grass (Pennisetum purpureum) subjected to doi: 10.1016/S1574-0072(06)03047-7 different levels of soil water supply and temperature Regimes. Crop Pasture Sci. Cook, B. G., Pengelly, B. C., Schultze-Kraft, R., Taylor, M., Burkart, S., Cardoso 64, 1008–1019. doi: 10.1071/CP13254 Arango, J. A., et al. (2020). Tropical Forages: An Interactive Selection Tool. Njarui, D. M. G., Gichangi, E. L. M., and Gatheru, M. (2016). “Biophysical 2nd and Revised Edn. International Center for Tropical Agriculture (CIAT), environment and farming systems of selected regions for integrating Cali, Colombia and International Livestock Research Institute (ILRI), Nairobi, brachiaria grasses in Kenya,” in Proceedings of the Workshop Held in Kenya. www.tropicalforages.info. Naivasha, Kenya. FAO (2018). Ethiopia: Report on Feed Inventory and Feed Balance 2018. Odero-Waitituh, J. A. (2017). Smallholder dairy production in Kenya; a review. Rome: Italy. Livestock Res, Rural Dev. 29:139. Available online at: http://www.lrrd.org/ Jaetzold, R., Schimidt, H., Hornetz, B., and Shisanya, C. (2006). FarmManagement lrrd29/7/atiw29139.html Handbook of Kenya Vol. II. Natural Conditions and Farm Management Rivas, L., and Holmann, F. (2005). Potential economic impact from the Information, 2nd edn. Nairobi: Ministry of Agriculture. adoption of new Brachiaria hybrids resistant to spittlebugs in livestock Kanyanjua, S. M., Ireri, L., Wambua, S., and Nandwa, S. M. (2002). Technical, Kari systems of Colombia, Mexico and Central America. Livestock Res. Rural Dev. and Note No. 2002. “TecNote11.” (11). 17, 1–21. Available online at: http://www.lrrd.org/lrrd17/5/holm17054.htm Khan, Z. R., Midega, C. A. O., Nyang’au, I. M., Murage, A., Pittchar, J., Agutu, Roche, J. R., Turner, L. R., Lee, J. M., Edmeades, D. C., Donaghy, D. J., L. O., et al. (2014). Farmers’ knowledge and perceptions of the stunting Macdonald, K. A., et al. (2009). Weather, herbage quality and milk production disease of napier grass in western kenya. Plant Pathol. 63, 1426–1435. in pastoral systems. 2. Temporal patterns and intra-relationships in herbage doi: 10.1111/ppa.12215 quality and mineral concentration parameters. Anim. Produc. Sci. 49, 200–210. Latino, L. R., Ciamarra, P., and Wisser, D. (2020). Africa: The livestock revolution doi: 10.1071/EA07308 urbanizes. Global Food Security 26. doi: 10.1016/j.gfs.2020.100399 Tessema, Z. K., Mihret, J., and Solomon, M. (2010). Effect of defoliation frequency Makkar, H. P. S. (2016). Animal nutrition in a 360-degree view and a framework for and cutting height on growth, dry matter yield and nutritive value of Napier future RandD work: towards sustainable livestock production. Animal Produc. grass (Pennisetum purpureum (L.) Schumach). Grass Forage Sci. 65, 421–430. Sci. 56, 1561–1568. doi: 10.1071/AN15265 doi: 10.1111/j.1365-2494.2010.00761.x Mwendia, S. W. (2015). Physiological and Productivity Evaluation of Napier Grass Tilman, D., Balzer, C., Hill, J., and Befort, B. L. (2011). Global food demand and (’Pennisetum purpureum’ Schumach.) Cultivars Under Variable Water Supply, the sustainable intensification of agriculture. Proc. Natl. Acad. Sci. U.S.A. 108, Temperature and Carbon Dioxide Conditions. Ph.D. thesis, University of New 20260–20264. doi: 10.1073/pnas.1116437108 England, Australia. Available online at: https://hdl.handle.net/1959.11/18376 Waithaka, M. M., Nyangaga, J. N., Staal, S. J., Wokabi, A. W., Njubi, D., Mwendia, S. W., Maass, B. L., Njenga, D. G., Nyakundi, F. N., and Notenbaert, A. Muriuki, K. G., et al. (2002). Characterization of Dairy Systems in the M.O. (2017a). Evaluating oat cultivars for dairy forage production in the central Western Kenya Region. Report of Dairy and Crop Characterisation Activities kenyan highlands. African J. Range Forage Sci. 34. Available online at: http:// in Western Kenya. Smallholder Dairy (RandD) Project P.O. Box 30028 www.tandfonline.com/loi/tarf20 Nairobi, Kenya. Frontiers in Sustainable Food Systems | www.frontiersin.org 1607 December 2021 | Volume 5 | Article 719655 Mwendia et al. Participatory Forage Grasses Evaluation World Bank (2014). Business and Livelihoods in African livestock. Available online the publisher, the editors and the reviewers. Any product that may be evaluated in at: http://www.fao.org/3/a-i3724e.pdf this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. Conflict of Interest: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a Copyright © 2021 Mwendia, Odhiambo, Juma, Mwangi and Notenbaert. potential conflict of interest. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction The handling editor is currently editing co-organizing a Research Topic with the in other forums is permitted, provided the original author(s) and the author AN and confirms the absence of any other collaboration. copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, Publisher’s Note: All claims expressed in this article are solely those of the authors distribution or reproduction is permitted which does not comply with these and do not necessarily represent those of their affiliated organizations, or those of terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 1618 December 2021 | Volume 5 | Article 719655 ORIGINAL RESEARCH published: 11 January 2022 doi: 10.3389/fsufs.2021.741057 On (Dis)Connections and Transformations: The Role of the Agricultural Innovation System in the Adoption of Improved Forages in Colombia Karen Enciso, Natalia Triana, Manuel Díaz and Stefan Burkart* Alliance Bioversity International and CIAT, Tropical Forages Program, Cali, Colombia Feeding improvement strategies are key in increasing cattle productivity and reducing its environmental footprint. Nevertheless, Colombian tropical cattle systems still feature serious deficiencies in both forage quality and availability. As a result of past and on- going forage Research and Development (R&D) processes, institutions have released 23 grass and legume cultivars of superior characteristics in terms of forage quality, Edited by: supply, or adaptation to different soil and climate conditions, while providing numerous Ngonidzashe Chirinda, environmental benefits. However, low levels of adoption are observed: although R&D Mohammed VI Polytechnic University, Morocco processes are a necessary condition for adoption, they are still not sufficient to guarantee Reviewed by: agricultural technification in Colombia. The ultimate success occurs only when end- Heinrich Hagel, users make effective use of a technology–a link constantly interrupted. Agricultural University of Hohenheim, Germany innovation requires complex processes of interaction in which knowledge is shared Chrystian Camilo Sosa Arango, Pontificia Universidad Javeriana amongst organizations involved in the Agricultural Innovation System (AIS), namely: Cali, Colombia suitable links, attitudes, practices, governance structures, and policies. The objective Lorena Campuzano Duque, Binghamton University, United States of this study is to identify limitations and opportunities in R&D, adoption, and diffusion *Correspondence: of forage technologies in Colombia from an AIS perspective. Particularly, we present a Stefan Burkart study case pertaining to research institutions only, to (a) map the involved actors and s.burkart@cgiar.org describe their roles and links, and (b) identify the events that marked the evolution of the AIS and the course of forage R&D in its research-related components. We applied a Specialty section: This article was submitted to qualitative methodology based on focus group discussions, in-depth interviews, literature Climate-Smart Food Systems, review, and historical analysis. Results show that the complex nature of institutions and a section of the journal Frontiers in Sustainable Food Systems the interactions between them determine the historical transformation of diffusion of Received: 14 July 2021 forage technologies. The lack of connection between institutions and the weak intensity Accepted: 14 December 2021 of the relationships, prevent the convergence of interests and objectives, leading to Published: 11 January 2022 vicious cycles that hamper technology adoption. Insufficient synchronization between Citation: institutions of different nature (and even between those that share similar objectives) Enciso K, Triana N, Díaz M and Burkart S (2022) On (Dis)Connections results in efficiency losses due to an unnecessary repetition of activities and processes. and Transformations: The Role of the We provide recommendations for policy- and decision-makers that will help in both a Agricultural Innovation System in the Adoption of Improved Forages in restructuration of the AIS and a better allocation of funds for R&D, and thus support the Colombia. development of more effective pathways for forage adoption and scaling. Front. Sustain. Food Syst. 5:741057. doi: 10.3389/fsufs.2021.741057 Keywords: improved forages, research and development, AIS, technology adoption, sustainable intensification Frontiers in Sustainable Food Systems | www.frontiersin.org 1169 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption INTRODUCTION adaptation to different soil and climate conditions, and various environmental benefits (Peters et al., 2012; Rao et al., 2015; Enciso It is no secret to anyone that the livestock industry is constantly et al., 2019). growing and evolving. It is estimated that by 2027, the demand However, and despite the fact that there is little evidence in this for livestock products will increase by 15.5% worldwide in regard, low levels of adoption of these forage technologies have response to population growth, urbanization and increased been observed (Shelton et al., 2005; White et al., 2013; Labarta incomes in developing countries (OECD/FAO, 2020). It is also et al., 2017). This shows, at least partially, that while research well-known that Latin America and the Caribbean at large hold processes are a necessary condition, they are not sufficient to an essential place and role in the livestock sector worldwide, as guarantee agricultural innovation. The success of R&D processes they contribute more than 25% of the production of beef and occurs when producers make effective use of technology, a link 10% of milk (CEPAL, 2017). This activity generates internal and that still falters in the Colombian case. Globally, the impacts on external benefits, guaranteeing to a certain extent food security adoption have been evaluated for less than half of the 118 million goals in countries, boosting their economies. This livestock hectares (Mhas) documented to have improved forages (White trend in the region is not only historically traceable, but is et al., 2013). In the Colombian case, the national forage adoption projected into a promising future. According to the Inter- rate is around 62% with respect to the total area in pastures in the American Development Bank–BID (2018) and based on world lower tropics, being the varieties B. humidicola and B. decumbens population growth, it is projected that by 2050meat consumption (pastures introduced in the 70s) the most adopted (Labarta et al., will increase by 100%, a scenario that would favor Latin American 2017). Yet, many of these areas are in some state of degradation producers given its geographic location and access to human and (IDEAMUDCA, 2015; Rincón et al., 2018). An adoption of <1% natural resources. Hence, the supply response to this increase will is estimated for the case of hybrids of the Brachiaria genus, as be located mainly in developing countries (where forage-based a result of the breeding work carried out by the International systems predominate), according to the availability of resources Center for Tropical Agriculture (CIAT) in Colombia (Labarta and the possibilities of increasing productivity (OECD/FAO, et al., 2017). 2020). Although historically larger livestock production numbers The analysis of forage technology adoption processes in have been achieved in comparable periods (for example, it tripled Colombia indicate decisive elements in the understanding of between 1980 and 2002 according to Rajalahti et al., 2008), the causal relationship between producers and their adoption the context has now radically changed. There is a growing behavior, but to date there are no explanatory studies that scarcity of natural resources (e.g., soil fertility, water and soil offer a macro perspective to understand the barriers in the availability), as well as political pressure on the incorporation access to technology and dissemination mechanisms (see Vera of better environmental practices. This constant political and and Seré, 1989; Seré et al., 1993; Rivas and Holmann, 2004; social pressure seeks to promote actions aimed at reducing the and more recent approaches in White et al., 2013 and Labarta environmental impacts of the livestock sector, being then the et al., 2017). Available literature has explained, to a certain main challenge of tropical ranching to increase the efficiency extent, the factors that limit or promote the adoption of of productive systems, mitigate the environmental impact, and technologies from the perspective of the primary producer, advance in adaptative efforts in the advent of climate change. In delving into the socio-demographic characteristics of the unity, addition to this, other impacts and improvements in the livestock and the conditions of the enablers, such as access to credit industry and its actors become urgent, not only at the primary and technical assistance (e.g., Lapar and Ehui, 2004; Jera and producer level (in terms of the promotion and implementation Ajayi, 2008; Dill et al., 2015). Some revised studies mainly of sustainable intensification practices) (Rao et al., 2015), but describe adoption processes in regions of East Africa and also in the more equitable and environmentally sustainable value Latin America, focusing on the identification of adoption chain structuring processes, as they encourage the elaboration factors mostly from a primary producer’s perspective with of differentiated products (Charry et al., 2019). Currently, a both quantitative and qualitative approaches. Although still multiplicity of actors and sectors, political, economic, and privileging primary producer’s perspectives, qualitative studies academic, are promoting livestock agendas toward sustainability. have done more to document and unveil the experiences and In a context of urgent reinvention and growing demand, lessons learned related to the adoption of improved forages, the livestock industry finds it decisive to implement agricultural taking analysis one step further (e.g., Reiber et al., 2013; Gil innovations, such as improved forages. The deficiencies in the et al., 2015; Ashley et al., 2018). Although theoretically and quality of the forages appear as a constant in the tropical methodologically vital, here we point out that these studies territories where cattle activity takes place (Peters et al., 2012). lack deeper perspectives that allow historical decision-making, Improving said quality, as well as the availability of food, has been and thus highlight the complex relationships between agents established as one of the key strategies to increase productivity and institutions that participate in the adoption and diffusion and reduce the environmental footprint (Gerber et al., 2013; of agricultural technologies. Although it is undeniable that Herrero et al., 2013). Thus, and as a result of the Research and the scientific and research sector plays a fundamental role in Development processes in Latin America (R&D) (some of which the creation of technologies that help to increase productivity, we address in this article), 26 cultivars have been released in mitigate the effects of climate change, and improve the quality Colombia, including grasses and legumes that have shown to of life of small producers (especially when working in partnering have better characteristics in terms of quality, forage supply, with the public sector and non-governmental organizations), Frontiers in Sustainable Food Systems | www.frontiersin.org 1270 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption these investments turn out to be insufficient to enable agricultural the analysis. Subsequently, it delves into the historical context innovation. This process requires the existence of broader that has directed the course of research and dissemination of competencies, links, enabling attitudes, practices, governance forage technologies in the country, laying the foundations for structures, and policies that facilitate the productive use of the the analysis. Thirdly, links and levels of influence between the knowledge generated (The World Bank, 2006). This comprises different actors and institutions of the research component the set of all organizations and people (public and private) are analyzed and mapped. The last two sections expose the involved in the generation, dissemination, adoption, and social bottlenecks and main obstacles that stand in the way of the and economic use of new agricultural technologies (The World proper development of the innovation and diffusion processes Bank, 2006; Hambly et al., 2012). The network formed in this in general, and provide some ideas on future steps to follow in process, and the conceptual lens of this study, is called the the matter. Agricultural Innovation System (AIS). The AIS approach recognizes that innovation is a dynamic MATERIALS AND METHODS and complex process of interaction between different activities, actors and relationships associated with the creation and In order to identify the factors that limit or promote the transmission of innovation to its productive use (The World development, diffusion, and adoption of forage technologies in Bank, 2006). This approach recognizes the role of actors, markets, Colombia, this study used qualitative methodologies, including: institutions, political contexts, and networks in the adoption of literature review, focus groups, and in-depth interviews. TheNet- new technologies and, therefore, in the evolution of innovation map tool was used to identify actors, their roles and importance in a system (Rajalahti et al., 2008). Different authors have used in the AIS. The qualitative data generated was analyzed using the the AIS approach as a framework to identify conditions that following tools: (i) transcription of interviews and focus group limit or promote the adoption of technologies in the rural sector meeting; (ii) coding and categorization of key aspects; and (iii) (e.g., Spielman et al., 2011; Kebebe, 2018). Among the factors interpretation of the information. The analytical purpose of the commonly mentioned are: (1) the scarce presence of public instruments used is explained in detail below. policies on innovation and agriculture; (2) problems related to asymmetries in communication; (3) weak links and lack of trust Net Map Tool between actors; and (4) norms and cultural attributes of society Net-map is a participatory mapping research method developed that impede development and innovation processes, as well as by Schiffer (2007), and has been applied in different agricultural behaviors, practices and attitudes that condition the roles and research problems to analyze networks and power dynamics interactions between actors. in the promotion of technologies (e.g., Aberman et al., 2015; Taking into account the comprehensive nature of the AIS Ilukor et al., 2015; Daum and Birner, 2017; Lubungue and approach, the objective of this study is, through the use of Birner, 2018). In the present study, the application of the it, to identify limitations and opportunities in the process of tool was carried out through a focus group session, made up development, adoption, and diffusion of forage technologies in of five participants (active researchers from CIAT’s Tropical Colombia for the case of the actors related to the research/science Forages program), in-depth interviews, and a review of secondary component. For this we have decided to integrate qualitative sources. The application of this tool was directed to the approaches when addressing the phenomenon, with the intention research component of the AIS of forage technologies. Thus, of providing a detailed analysis that addresses the nature of the following objectives were proposed for the focus group inter-actor relationships and the contingencies that determine discussion: (i) identify the actors that are part of the AIS in their transformations. To do so, we rethink the processes of forage technologies at the national level, and (ii) describe the adoption and diffusion of forage technologies through a historical roles, links, and attitudes of the agents involved in the activities perspective, highlighting the variables and actors that participate of the AIS. in said processes. In addition to highlighting the importance and The Net-map process was divided into two main activities. delving into the investigative component, this article identifies First, the participants identified the main people, institutions, some of the main events that have directed the course of research and organizations that participate in the process of development, and dissemination of forage technologies in the country; and dissemination, and adoption of forage technologies in Colombia. maps the actors that are part of the innovation system, describing Each participant wrote the name of the identified actors their roles, links and attitudes, and the way in which they have on separate cards (one actor per card), also writing down catapulted or hindered forage innovation processes. information about the role they play within the process and As mentioned before, the network formed in this process is their level of influence in the AIS. The latter was defined called the Agricultural Innovation System (AIS), a network of as the actor’s ability to influence the specific problem. The actors and institutions that we are just beginning to elucidate. measurement of the level of influence was established using Thus, identifying the limitations and opportunities in the process a Likert-type scale from 0 (no influence) to 4 (greater degree of development, adoption and diffusion of forage technologies of influence). At this point, it should be mentioned that the in Colombia implies an understanding of the dynamics that participants in the group session are part of the population shaped inter-institutional relations, as well as their internal under study, and each one has experienced the process from functioning mechanisms. This document is then structured as different perspectives. For this reason, different colored cards follows: first, it specifies the methodological tools used for were assigned to each participant, in order to identify the Frontiers in Sustainable Food Systems | www.frontiersin.org 1371 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption responses of each one. Next, the cards were collected and Literature Review grouped according to the different components and distributed Regarding secondary sources, long-standing studies were on a sheet of paper. During this activity, various questions for integrated on the establishment of livestock in Colombia and discussion and reflection were generated among the participants, the continuous state and private searches to promote through related to the absence of actors in some component, and the use of selected pastures) a productive and extensive and the divergences between roles and influences presented by continuous livestock sector throughout the Twentieth century the participants. (1900–2000). This selection was focused in the existing literature Second, the links, influences, and attitudes of the actors regarding livestock, livestock practices in Colombia and Latin identified in the previous activity were identified. In this section, America at large, and improved forages. Our query included an open discussion was held among the participants, based reports published by research institutions, peer-reviewed articles on the following questions posed by the facilitator: which of and databases. The search included documents published from the identified actors have any link to each other? What is the 1980 to 2020. Conducting in-depth interviews allowed the direction of the link (one-way or two-way)? What is the type of integration of issues related to the change of research institutions exchange (information flow, use of resources, planning, training, and agendas, while delving into the gradual transformation of etc.)? And what is the strength of this relationship (weak, social relations that determine the course of research programs medium, strong)? According to the response of the participants, and projects. Choosing as informants subjects with a long history arrows were drawn, indicating the existence of a relationship in their respective institutions enabled us to obtain a more and its characteristics. In the development of this activity, precise overview of the changes over time of the institutions and various discussion questions were generated associated with the professionals linked to the research field in livestock. characteristics of the relationships perceived between the actors, about the attitudes and practices that have restricted and/or promoted the interaction, and about the possible limitations that CONTEXTUAL AND HISTORICAL may have hindered or restricted the linking activities between the FRAMEWORK different actors. The full program of the focus group session and an implementation guide for the facilitator are presented in the Scientific literature conceptualizes improved forages as species Supplementary Material. that present superior agronomic characteristics compared to native forages and that, in addition, adapt to the agroecological conditions of a given region (Shelton et al., 2005; White In-depth Interviews et al., 2013; Labarta et al., 2017). These forages are the Based on the focus group session and the review of secondary result of improvement processes, which may include: (i) sources, some of the different actors that are part of the AIS selection of materials from germplasm banks according to a were identified, which belong to various components. This previous evaluation of visual characteristics, adaptability, forage information was organized in a spreadsheet, grouping the actors production, seed, nutritional quality, and animal response (e.g., according to their membership in each component. Based Brachiaria, Megathyrsus, Cenchrus, Leucaena, Cratylia, Arachis, on this information, the people to interview were selected, among others); and (ii) genetic improvement of a material according to their experience and relevance within the processes in which desirable characteristics of the parents are combined of development, dissemination, and adoption of improved (e.g., Brachiaria hybrid CIAT 36061 cv. Mulato I, Brachiaria forages. The in-depth interviews (12 in total) were conducted hybrid CIAT 36087 cv. Mulato II, and Brachiaria hybrid CIAT between September 2019 and March 2020. Of these interviews, BR 02/1752 cv. Cayman). In general terms, the process of six focused on relevant actors in agricultural research (CIAT, multiplication and diffusion of the seeds/vegetative materials of Agrosavia, CIPAV), five on private sector agents (PAPALOTLA, varieties already formally released, usually follows two routes: ALQUERIA, MATSUDA, SEMILLANO, SAENZ FETY) (to formal and informal. understand their relationship with the research component and In the formal route, cultivars are developed by a national its actors) and a relevant actor in the field of politics in research institution (e.g., Agrosavia) or private company (e.g., agriculture in Colombia that offered a general panorama on Papalotla) based on a release proposal (breeding by selection or the matter (ICA). The interviews followed a logical format of plant breeding). Some materials in this group are: Brachiaria open questions, each one lasting ∼1.5 h. For each interview, brizantha cv. Toledo, Brachiaria humidicola cv. Humidicola, between 5 and 7 questions were selected from a comprehensive Arachis pintoi cv. Forage Mani. Under this route, 26 cultivars guide that included relevant topics for this research, previously have been released in Colombia, mainly for low-tropical carried out by the authors. This guide contains a general list of conditions. In Table 1, we present a list of the total improved questions that are grouped into the following categories: (i) roles, forages released in Colombia. On the other side, in the informal attitudes, and practices, (ii) historical moments, (iii) patterns route, the cultivar is introduced to the country by an individual of interaction between actors, (iv) facilitating environment, and and/or national seed company which initiates the distribution (v) gender inclusion. The selection of the questions was made and/or dissemination. As an example, there are materials in according to the profile of each actor to be interviewed, prior to commercial use such as: Decumbens grass (Brachiaria decumbens the interview. Six of the 12 interviews were conducted remotely, CIAT 606), Tanzania 1 grass (Megathyrsus maximus CIAT and the remainder in person. 16031), Maralfalfa grass, Guinea Massai grass (Megathyrsus Frontiers in Sustainable Food Systems | www.frontiersin.org 1472 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption Frontiers in Sustainable Food Systems | www.frontiersin.org January 2022 | Volume 5 | Article 741057 TABLE 1 | Forage species released in Colombia. Region Genus and species Accession Variety name Year of release Releasing Adoption Adoption rate Commercialization institution registration (%) year Gramineae Lower tropics Brachiaria brizantha CIAT 26646 La libertad 1987 ICA 2016 2.8 No (0–2,000m elevation) CIAT 26110 Toledo 2002 Corpoica 2016 1.24 Yes CIAT Caporal 2021 Corpoica N.D ND No 26124 Brachiaria humidicola CIAT 679 Pasto 1992 Corpoica 2016 22.6 Yes humidicola CIAT 6133 Llanero 1987 ICA 2016 8.15 Yes Brachiaria hibrido CIAT 36061 Mulato 2003 Papalotla 2016 0.05 Yes CIAT 36087 Mulato II 2005 Papalotla 2016 0.03 Yes BR02/1752 Cayman 2013 Papalotla N.D N.D Yes Sorgo forrajero JJT-18 Sorgo dulce 2014 Corpoica N.D N.D No Corpoic JJT-18 Andropogon gayanus CIAT 621 Carimagua 1 1980 ICA N.D N.D No Megathyrsus maximus CIAT 6799 Agrosavia 2018 Agrosavia N.D N.D No sabanera Fabaceae Lower tropics Arachis pintoi 17434 Mani forrajero 1992 Corpoica 2016 0.1 Yes (0–2,000m elevation) 22160 Centauro 2020 Agrosavia N.D N.D No Centrosema acutifolium 5277 Vichada 1987 ICA N.D N.D No Cratylia argentea CIAT Veranera 2002 Corpoica N.D N.D No 18516+18668 Desmodium 13651 Maquenque 2002 Corpoica N.D N.D No heterocarpon Leucaena leucocephala 21888 Romelia 1992 Cenicafe N.D N.D No Stylosanthes capitata 10280 Capica 1983 Corpoica N.D N.D Yes Vigna unguiculata Sinu Corpoica Avena Higher tropics ICA Bacatá 1963 ICA N.D N.D No ICA Soracá 1965 ICA N.D N.D No ICA Gualcalá 1968 ICA N.D N.D No lCA Cajicá 1976 ICA N.D N.D Yes Avena Obonuco Avenar 2003 Corpoica N.D N.D Yes Avena Forrajera 2018 Agrosavia N.D N.D No Altoandina Own elaboration based on Peters et al. (2011), Labarta et al. (2017), and expert consultation and information provided by seed distributors. ND: no data available. Note: In 1992, ICA was restructured and the research activities passed to the newly created Corpoica; Corpoica is now called AGROSAVIA. 173 Enciso et al. AIS and Forage Technology Adoption maximus cv. Massai), Stylosanthes cv. Campo Grande (Mix advent of neoliberal economic policies in developing Latin between Stylosanthes capitata and Stylosanthes macrocephala), American countries (Lynam and Byerlee, 2017). The first Pennisetum cv. Cuba 22, and Pennisetum cv. Clone 51. moment took place between the 1960s and 1970s, and At the national level, we find that there is an adoption level was marked by an increase in agricultural investment and of 34.97% of fodder released under formality channels. Of this marked concerns about productivity and quality of life in percentage, 34.89% corresponded to introduced species of the rural settings, triggered by the need to promote agricultural genus B. humidicola and B. brizantha; introduced ∼30 years ago development in a world increasingly unequal caught up in (Labarta et al., 2017). In relation to hybrid forages (Mulato I and the political ups and downs of the Cold War (Lynam and Mulato II) an adoption level of 0.08% was registered (Labarta Byerlee, 2017; Ponce de León-Calero, 2019). The flourishing et al., 2017), while the varieties released informally such as B. and consolidation of programs such as CIAT’s Tropical decumbens, M. maximus cv. Tanzania, and cv. Mombaza report Forages and Agrosavia (Colombian Agricultural Research an adoption percentage of 0.98, 0.29, and 1.61%, respectively Corporation former CORPOICA, in Colombia) are also (Labarta et al., 2017). highlighted here, which shows a growing multilateral interest Different studies have carried out, during the last nine in promoting agricultural innovation processes (Lynam and decades, documentations of the benefits and costs associated Byerlee, 2017). with the adoption of improved forages (see Table 2). These The second moment is framed by the political and economic studies show the potential of improved forages to improve agendas of Latin American governments (including Colombia) at animal production and contribute to the sustainability of the beginning of the 1990s, within the framework of neoliberal production systems at different scales. In particular, CIAT transformations and economic flexibility (Tirado-Mejia, 1997; developed the LivestockPlus concept, demonstrating how Palacios and Stoller, 2006; Van Ausdal, 2012; Ponce de León- the introduction of improved forages in the tropics can Calero, 2019). Previously solid institutions dedicated to research lead to sustainable intensification, producing multiple social, (such as Agrosavia) underwent important restructuring processes economic, and environmental benefits (Rao et al., 2015). due to budget cuts limiting their research possibilities, the These benefits are mainly associated with the increase in the continuation and monitoring of ongoing projects and adequate availability and quality of pastures, which results in better and complete process of technological diffusion. The changes indicators of animal development, productivity, and profitability and contingencies experienced by institutions such as Agrosavia of the livestock activity. In addition, improvements in the show that, as far as agricultural research processes and actors quality of feed allows improving the ruminal fermentation are concerned, continued state funding is necessary. From the process and, therefore, reducing greenhouse gas (GHG) interviews carried out with the actors in agricultural research emissions, and achieving greater intensification of the livestock circuits, we were able to establish the causality between state activity (Oliveira et al., 2007; Hristov et al., 2013). It is funding and the success or continuity of research programs, necessary to clarify that these potential benefits of the use of as several of the interviewed informants narrated the processes improved forages depend on the appropriate agroecological and of transformation and historical decline of their scientific management conditions. agendas because of budget cuts. Untimely budget reductions, The introduction of technologies to improve the livestock as well as the relegation of investigative processes to second sector has taken place for more than a century (Van Ausdal, place, have undoubtedly been determining factors for efficient 2012). Between 1850 and 1950, the nascent cattle ranchers of dissemination processes, thus affecting the viability of adoption Colombia made significant efforts to improve their agricultural processes. It should be noted that since the 1980s the national practices through the introduction of new breeds and bovine research institution Agrosavia has released new forage species, crosses, the improvement of fences and farm care, as well as grasses, and legumes, previously evaluated by CIAT. Among the introduction of Africanized pastures [e.g., Pará (Brachiaria these, the cultivars of Brachiaria dictyoneura (cv. Pasto Llanero, mutica), guinea (Panicum maximum)], among others (Rao 1987), B. brizantha (cv. La Libertad, 1987), and B. humidicola et al., 1998; Rincón et al., 2010). Since the introduction of (cv. Humidicola, 1990) stand out. Likewise, the creation in pastures of the Brachiaria genus, there has been a rapid and 1979 of the International Tropical Pasture Evaluation Network sustained growth of grazing areas in the country: by 1900 there Foundation (RIEPT) stands out as a fundamental milestone were already two million hectares sown in Pará and Guinea, to promote research in the subject and discuss the use of and by 1958 this number amounted to 10 million, this is, methodologies for evaluating forage technologies (Lynam and one third of the grazing land of the entire national territory Byerlee, 2017). The existence of the RIEPT originated an (Van Ausdal, 2012). Said dissemination and adoption processes invaluable database of forages studied and analyzed in detail were spontaneous and massive, they did not follow established and allowed the distribution of germplasm among researchers guidelines or regulations. They obeyed, rather, to the commercial dedicated to the matter, materializing the advances of their need to establish a solid industry (especially meat) with an research and strengthening institutional relationships between export industry that was never consolidated (Rao et al., 1998; various groups and scientific niches (Lynam and Byerlee, Rincón et al., 2010; Van Ausdal, 2012; Ponce de León-Calero, 2017).Below are explained in more detail (i) key processes and 2019). their influence on the R&D processes of forage technologies Two historical moments stand out as decisive in regards in Colombia and (ii) the agents of the process and their to R&D processes: the so-called “green revolution” and the respective interactions. Frontiers in Sustainable Food Systems | www.frontiersin.org 1674 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption TABLE 2 | Benefits and costs of improved forages. Benefits and costs Effects at different scales References Direct benefit Impact Farm Regional Global Increment in the availability and Increment in milk and beef production Rincón et al., 2010; Rao et al., nutritional quality of forage 2014, 2015; Maass et al., 2015 Higher number of animal heads per unit area ✓ ✓ Better productive parameters of animal development (e.g., mortality and birth rate) Social impact: improvement in income, food security and nutrition. Reduction of enteric methane Reduction of GHG emissions per unit of livestock Oliveira et al., 2007; Hristov emissions (CH4) product, given the improvement in feed efficiency. et al., 2013; Peters et al., 2013; Mitigation and adaptation to climate change Herrero et al., 2016 Increase in atmospheric nitrogen (N) Shelton and Dalzell, 2007; fixation (legumes) Reckling et al., 2016 Carbon (CO2) accumulation in the soil Oliveira et al., 2007; Soussana et al., 2010; Peters et al., 2013; Rao et al., 2015 Reduction of nitrous oxide (NO2) ✓ ✓ Subbarao et al., 2009, 2017; emissions, associated with Biological Moreta et al., 2014; Karwat Nitrification Inhibition (BNI) et al., 2017; Nuñez et al., 2018 Improvement of soil quality indicators Improvement of the biological conditions of the soil Rousseau et al., 2013; Lavelle (increase of biological indices of diversity of micro et al., 2014; Rao et al., 2015 and macro fauna) Improvement of the physical conditions of the soil (reduction of erosion, compaction, and apparent density) Costs Establishment of materials (increased use of inputs, labor, equipment) ✓ Carey and Zilberman, 2002; Pannell et al., 2006 New knowledge and skills to maintain the technologies Thomas and Sumberg, 1995; Lapar and Ehui, 2004 Development of appropriate extension and training packages ✓ Reiber et al., 2013 High perceived risk/uncertainty of technology ✓ Marra et al., 2003 Own elaboration based on the references mentioned. RESULTS national research, Agrosavia, is the main public organization dedicated to research in the sector. It has 13 regional research Mapping of Actors centers (CIR) spread throughout the country, as well as offices The information collected shows that the AIS in Colombia in 10 locations. Of the total number of Agrosavia centers, eight for improved forages includes actors from both public and include livestock and forages within their research lines. Mainly, private sectors. Table 3 presents the list of actors and functions Agrosavia has had a great impact on the development and release of the AIS for improved forages in Colombia, according to of new forage materials through the evaluation and selection secondary sources, the focus group, and interviews. These actors of germplasm. At the international level, the Tropical Forages can be grouped into the following six main components: (i) program of the International Center for Tropical Agriculture Politics; (ii) R&D; (iii) Extension, training and information; (iv) (CIAT) stands out for its role in the development of plant Supply of seeds; (v) Financing, and (vi) Primary producer. Each breeding hybrids, evaluation of materials, and the promotion organization can fulfill one or different functions within the of concepts of sustainable intensification through improved system: generation of knowledge, coordination, supervision and pastures. Likewise, CIAT has one of the largest collections of control of dissemination processes, bridging, or intermediary forage accessions in its germplasm bank, estimated at 22,694 institutions, generation of spaces for the articulation of actors, accessions (from 75 countries). Historically, both CIAT and or support structures at the institutional and political level Agrosavia were identified as vital agents and leaders within (Figure 1). the improved forage development processes. At the regional The component of R&D consists of a total of 11 institutions level, public universities have played a fundamental role both dedicated to research on tropical forages. It includes national, in the evaluation of technologies and in their application and regional, international and private research institutions. Among promotion, through specific scaling-up projects. Among these, Frontiers in Sustainable Food Systems | www.frontiersin.org 175 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption Frontiers in Sustainable Food Systems | www.frontiersin.org January 2022 | Volume 5 | Article 741057 TABLE 3 | List of actors and functions of the AIS for improved forages in Colombia. Component/Category actor Functions F1 F2 F3 F4 F5 F6 F7 F8 F9 F10 F11 F12 F13 F14 F15 F16 Policy Ministry of Agriculture and Rural x x x x x x x Development (MADR) Ministry of Environment and Sustainable x x Development (MADS) Colombian Roundtable for Sustainable x x x Cattle (MGS-Col) Colombian Agricultural Institute (ICA) x x x Rural Agricultural Planning Unit (UPRA) x x Departmental Agriculture Secretariats x x x x Research and National research The Colombian x x x x x development Agricultural Research Corporation (Agrosavia) Center for x x x x x Research in Sustainable Systems of Agricultural Production (CIPAV) International International x x x x research Center for Tropical Agriculture (CIAT), Tropical forages program The Tropical x x x x Agricultural Research and Higher Education Center (CATIE) Regional University of x x x research Cauca- Research group NUTRIFACA National University x x x of Colombia University of x x Antioquia- Agricultural Sciences (Continued) 176 Enciso et al. AIS and Forage Technology Adoption Frontiers in Sustainable Food Systems | www.frontiersin.org January 2022 | Volume 5 | Article 741057 TABLE 3 | Continued Component/Category actor Functions F1 F2 F3 F4 F5 F6 F7 F8 F9 F10 F11 F12 F13 F14 F15 F16 University of x x Llanos- Research group in Agroforestry University of x x Nariño-FISE PROBIOTEC University of x x Córdoba- Research group in tropical animal production Private research Papalotla x x x Extension, Colombian Cattle x x x x training, and Federation information (FEDEGÁN) Agricultural Municipal Units for x extension Technical Assistance in Agriculture (UMATAs) Training and National Training x x education Service (SENA) Private sector x (e.g., Nestlé, Alquería, Alpina) and Outreach initiatives (e.g., Sustainable Colombian Cattle Project) NGO’s Food and x x Agriculture Organization of the United Nations –(FAO) GANSO x x Seed supply Papalotla x x x x x x Colombia SAS (Continued) 177 Enciso et al. AIS and Forage Technology Adoption Frontiers in Sustainable Food Systems | www.frontiersin.org January 2022 | Volume 5 | Article 741057 TABLE 3 | Continued Component/Category actor Functions F1 F2 F3 F4 F5 F6 F7 F8 F9 F10 F11 F12 F13 F14 F15 F16 Sáenz Faety, x x Impulsores Internacionales, Semillas & Semillas, Agrosemillas, among others Seed producers in x x x Brazil (e.g., EMBRAPA) Financing Financial services The Colombian x Fund for the Financing of the Agricultural Sector (FINAGRO) Banco Agrario of x Colombia Private banks x Producer x associations and cooperatives Informal credit x R&D financing Ministry of x Agriculture and Rural Development (MADR), Grupo Papalotla, high-income countries and international agencies, donors Primary Producer x x x x producer associations and cooperatives Individual cattle producers x x F1 Promotion of spaces for articulation, coordination and integration of actors. F9 Promotion and demonstration of technology. Source: Own elaboration. F2 Design of regulatory and normative frameworks. F10 Technical advice and information. F3 Execution and supervision of public policies. F11 Extension and/or agricultural technical assistance. F4 Design and execution of programs and/or projects. F12 Training and certification of labor competencies. F5 Coordination, supervision and control within the dissemination processes. F13 Seed multiplication and/or distribution. F6 Technology development. F14 Financial services. F7 Technology assessment (at the experimental level). F15 Research and development financing. F8 Technology release. F16 Demand and use of technology. 178 Enciso et al. AIS and Forage Technology Adoption FIGURE 1 | Main agents of AIS for improved forages in Colombia. the following stand out: The National University of Colombia PDEA are regulated by the Ministry of Agriculture and Rural and the University of Nariño (research conditions of the Development (MADR, as per its acronym in Spanish) in the high tropics). resolution 407 of 2018. According to these guidelines, there Bridging organizations or intermediaries, in particular, are key stakeholders for delivering extension services such as extension and training services, seed supply, and producers’ local units of technical assistance for agricultural production organizations, facilitate interaction and/or link knowledge (also known as UMATAs, as per their acronym in Spanish), generation of R&D agents with users of technologies. Extension provincial centers of agrobusiness management (CPGA, as per services for agricultural production in Colombia go back their acronym in Spanish), the national service for vocational to the 1950s. At that time, the international trend for education (SENA, as per its acronym in Spanish), professional the creation of agricultural research institutes and extension associations of the sector, unions, associations, and community- services began to grow. From that moment, rural extension based organizations. services have been through important transformations and Regarding the national seed supply of improved pastures, it organizational arrangements toward a decentralized technical is carried out by commercializing companies that import seeds assistance at the territorial level. Currently, the national technical from Brazil, Mexico, the United States, and Canada (comparative assistance has a framework in the law 1876 of 2017 and advantages from geographical conditions). Figure 2 shows the the guidelines for the formulation of departmental plans of network of importing and exporting companies of improved agricultural extension (PDEA, as per its acronym in Spanish). forage in Colombia. These companies can be divided in two Frontiers in Sustainable Food Systems | www.frontiersin.org 1719 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption FIGURE 2 | Network of companies that import and export improved forage seeds in Colombia. Own elaboration based on trade statistics from Legiscomex (2020). Note. The blue nodes refer to the importing companies, and the yellow nodes refer to the exporting companies. The size of each node represents the level of participation regarding to the total in imports and exports, respectively. groups: importers of introduced varieties and importers of hybrid support or limit innovation processes. Stakeholders here varieties. The market of introduced varieties has a share of recognize the role of the MADR for its relevance in the the 98% of all seeds commercialized nationally. This group is formulation, coordination, evaluation of agricultural and comprised of 27 companies. The most relevant are SAENZ rural development policies, sustainable livestock production FETY, Impulsores Internacionales, and Semillas & Semillas with policy, and financing of programs and/or projects related a market share of 20, 15, and 10, 1%, respectively. These to the development of forage technologies. Furthermore, companies commercialize and distribute varieties from Brazil. stakeholders highlight the role of MADR in the establishment For low tropics conditions (mainly the species Brachiaria and and regulation of the national policy of technical assistance for Panicum) and for high tropics conditions (mainly varieties such agricultural production. as Ryegrass, Alfalfa, Festucas, Pasto Azul, and clover) sourcing from the United States and Canada. The second group refers to Actors and Levels of Influence the market of hybrids, still under development with a share of Here, a linkage mapping exercise is presented, in which CIAT’s <2% of all commercialized seeds nationally. In this group, from relationships with other actors (that CIAT recognizes as key 2017, the company Papalotla Colombia SAS imports and directly agents in the development and dissemination processes of distributes through sales advisors and authorized distributors. improved pastures) in Colombia are analyzed. The following Direct presence of Papalotla has increased the market of hybrids results are based on the focus group discussion. since 2017. They import hybrid grasses from Semillas Papalotla Relationships between R&D institutions mainly occur for in Mexico and Brazil. The nationally commercialized seeds are collaborative research as part of specific projects. The links are Brachiaria hybrids cv. Cayman andMulato II, with a share of 75% strong between some institutions (e.g., Agrosavia and CIAT and (32 tons in 2018) and 25% (10 tons in 2018), respectively (Rosales their Forages Network). In most cases, however, we observe and Papalotla, 2019, personal communication). weak links that generate duplication of research efforts and All stakeholders are influenced by a context of agricultural competition for resources. There are not many strong links policy, institutions, and informal general practices that might between R&D institutions and intermediary agents such as seed Frontiers in Sustainable Food Systems | www.frontiersin.org 1820 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption supply companies. CIAT, as exemption, has a strong link with the field of forages, but also provides insights to deepen and Papalotla regarding the financing, co-development, and exchange contextualize the existence of serious and persistent bottlenecks of information on forage hybrids. The lack of other possible that affect agricultural innovation in forage matters. Below we examples denotes a relational crisis between institutions that describe the limitations that have had a direct impact on the still needs to be overcome. Seed companies play a key role in technology adoption and diffusion processes, identified by the providing technical assistance and training to primary producers, actors interviewed during the study. although mainly at the regional level. National universities have a high level of influence regarding the application of technologies Extensive Tradition of Livestock (e.g., University of Cauca, University of Antioquia, Amazonia Structural conditions are evident factors in discouraging University, and National University of Colombia). However, sustainable intensification and, along with it, the adoption of this is done through specific scaling projects and requiring improved species. For example, for traditional extensive ranching allies. In the interviews, it was pointed out that the impacts it is much more efficient (cost-effective) to acquire more land of dissemination processes depend on the collaboration among for the establishment of the crop than to intensify the use of a institutions, and that the competitive nature of funds increases certain amount of land through the adoption of technologies. the participation of universities in R&D processes. Deforestation as a result of livestock activity, an increasingly Milk and meat trading companies have high potential in critical and urgent topic, also stands as one of the bottlenecks as terms of technology diffusion due to their direct relationship far as livestock is identified as one of the main culprits behind with producers. Although these companies are key players in the invasion of conservation/protected areas for the agricultural accompanying producers, they require a better communication exploitation. The low cost of land in pastoral areas, and the with technical knowledge research and development institutions still precarious controls over land tenure due to long-standing that effectively bring technological innovations closer to their historical dynamics in which a fragile state predominates, favors target populations, harmonizing concepts, and reducing the land accumulation. This not only encourages sustained land circulation of confusing information. Currently, there are accumulation by illegal actors (who havemonopolized or decades initiatives and approaches between private companies and large tracts of land, some of which are indeed dedicated to research institutions (e.g., Fundación Alpina and CIAT). extensive livestock projects) but also encourages small livestock Associations and/or cooperatives of producers are recognized as producers to upsurge agricultural areas instead of intensifying having a strong role in the processes of diffusion and scaling their production. In this way, a trend toward the purchase of land of forage technologies. Among the roles they can fulfill are or expansion of the agricultural frontier is promoted. the collaboration with the research component and/or in the selection of pilot farms for the evaluation of technologies, the Low Budget for Research dissemination of information on technologies, supply of inputs, Budget cuts in the 1990s limited Colombian scientists and as well as training and extension among associated producers. researchers, both in the formulation and in the follow-up and The MADR is identified as an actor with high influence monitoring of ongoing projects. The paradigm shift in funding within the processes of development and diffusion of forage brought new consequences: scientists, who were dedicated solely technologies. This influence is associated with its role in the to research work, now have as their main mission a systematic construction of a sustainable livestock policy at the national level, procurement of resources. This led to important distortions in the financing of research programs in forage technologies, and the development of research agendas, fragmented personal and the contribution to the Colombian Roundtable for Sustainable institutional relationships, and weakened sustained advances in Cattle (MGS-Col). In recent years, the MADR and the Ministry the matter (e.g., programs such as the International Network for of Environment and Sustainable Development (MADS) have the Evaluation of Tropical Pastures -RIEPT) were eliminated. increasingly aligned their agendas supporting sustainability more Even today there are certain misunderstandings derived from the strongly. Thus, the lack of association between most of the new role of the scientist/extension worker. innovation actors and the support structures has resulted in the existence of a generally weak innovation system. However, Influence of Public Order Problems on Technology it is important to highlight outreach initiatives to strengthen Diffusion Processes institutional links and communication between actors that have On the one hand, technology transfer processes were affected been taking place in recent years, such as the participation of as a consequence of the various dynamics of the armed conflict the main actors of the livestock sector in multi-actor platforms between the Colombian state, guerrillas, and paramilitary groups. such as the MGS-Col, and approaches of the sector private sector Concrete examples of this correlation are found in the narratives and research institutions. The Rural Agricultural Planning Unit about kidnappings and threats to research personnel, as well (UPRA) has a growing level of influence on livestock policy given as in the uncertainty in the arrival of seeds to conflict zones. the zoning exercise they conducted for livestock production in The manifest weakness of the state in disputed territories, the country. as well as the fluctuating (and violent) political order in certain areas of the country has, without a doubt, affected the Bottlenecks adequate implementation of extension projects, leading seed The mapping exercise carried out here allows us not only supply companies to register large economic losses. On the other to identify the complexity of the AIS research component in hand, the consequence of the illegal drug trafficking market and Frontiers in Sustainable Food Systems | www.frontiersin.org 1831 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption the scarce state regulation of the seed market led, between the Cultural Gaps and Personal Relationships 80s and 90s, to the importation of large quantities of them for Personal relationships are key in the scaling of technologies money laundering. The existence of a poorly regulated industry (insofar as they allow or hinder the interaction of various agents facilitated its use as a “facade” between drug traffickers and and entities, the continuation of projects and their follow-up); cartels, which resulted in the importation of large quantities of they prevent or facilitate access to information and resources and seed with low quality standards, affecting the domestic market. at the same time chain inter-institutional relations to the personal sphere. Expedited and transparent interpersonal relationships facilitate scientific praxis, while rivalries, budgetary struggles, Different Objectives Causing a Low Articulation and fragile ties hinder the viability of a given project. The Between National R&D Institutions and Seed interviews carried out shed important light in this regard, where Companies testimonies or narratives such as “our relationship was not good” With the help of donors, research entities aim to evaluate and or “relations between institutions depend on those who work in release forage seeds. However, seed production is determined it” were a constant that allowed us to elucidate the importance primarily by their own perspective on actual demand and of assertive interpersonal relationships for the development, profitability. This disparity causes the processes of diffusion and achievement and continuity of research projects and initiatives releasement of seeds to be distorted, and that results in turn in that, by default, affect the processes of diffusion and adoption of a low impact on the adoption processes: materials are released agricultural technologies. without commercially available seed, or else, these materials are not suitable for the territories in which they are that are Weakness of Extension Processes in the Promotion traded informally. of Forage Technologies The neoliberal reforms of the 1990s (e.g., protectionist and decentralization policies at municipal and departmental levels) Absence/Weakness in the Social Support of the also weakened the key components of the national technical Research assistance system, which led to its progressive exhaustion and According to informants, the average duration of projects for disarticulation. The lack of permanent updating in knowledge, the promotion and adoption of forage technologies is 3 years. methodologies, and technologies is highlighted in the UMATAS This period constitutes a limitation because it makes it difficult (Municipal Units of Agricultural Technical Assistance), and later, to adequately measure the impact and scope of the introduction in the CPGA (Provincial Centers of Agribusiness Management) of a new species, and furtherly impossible to obtain accurate and EPSAGROS (Providers of Agricultural Technical Assistance data about the adoption of technologies. Scarce times hinder the Services). This has generated a knowledge gap between the evaluation of the sustained use of new species, so a complete generation of technologies and demanding users. In addition, the picture on the adoption of improved pastures at the national creation of EPSAGRO led to the attraction of resources and to the level remains a long way off. The foregoing is also a consequence detriment of the quality of the service provided. To this is added of the disarticulation between different areas and research that the service has focused primarily on agricultural issues, professionals, as well as between centers and entities in charge leaving aside the components of livestock development. All of the of formulating and executing technological innovation projects. above is reflected in an institutionally weakened extension system where access to information, particularly on livestock technology issues, is seen as an important bottleneck. Speculation in the Brazilian Market as a Determinant of the Livestock Landscape in Colombia Traditionally, Credit Lines Have Not Promoted The geographical and climatic conditions of the country limit Investment in Sustainable Intensification Systems the production of forage seeds, making Colombia dependent on The actors recognize the importance that credit has had for seeds from its Brazilian partner, the main producer in the world. agricultural development in the country, however, they highlight This high level of dependency makes Colombia susceptible to key bottlenecks associated with the low provision of credit in suffering from internal shocks to the economy in Brazil; that is, in rural areas, information asymmetries that mainly affect small the face of a change in the perception or in the projections about producers, and credit orientation rather toward productivity than the profitability of a certain crop (e.g., sorghum, corn, soybeans) sustainability. Despite the fact that the Fund for the Financing or between forage varieties, companies may prefer to produce of the Agricultural Sector (FINAGRO) has established Special seeds of the crop or a certain variety of pasture perceived as Credit Lines (LEC) for the promotion and renovation of pastures, more profitable in the short term. These changes not only occur as well as productive intensification through silvo-pastoral between substitute varieties but also between crops that are not systems (e.g., Colombia Siembra, Livestock Sustainability), a directly related to livestock, which greatly limits the options of pronounced effect has not been observed in the application of the demanding countries. Thus, changes in the Brazilian supply these lines, as the credits for livestock are mainly oriented to the derived from speculative processes lead to an impact on the price purchase of animals. This has been accentuated as a consequence level and availability of seeds in Colombia, so that a producer can of credit dynamics such as growth in the substitute portfolio, in turn vary the level of preferences without having been able to where resources have been directed toward links in the chain evaluate the effectiveness of a previously acquired species. with less risk than toward small producers (e.g., transformation Frontiers in Sustainable Food Systems | www.frontiersin.org 1842 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption and commercialization). The previous dynamics suggest that the the identification of their demands, making rural subjects spirit of agricultural credit is being lost, as it works more to participants of their own transformation (Ardila, 2010). This has attenuate the asymmetries and inequalities between the actors of been due to theoretical transformations and methodologies on the Colombian rurality. However, it is important to note that, how to think, intervene, and transform rural livelihoods, a trend in recent years, credit institutions have established mechanisms that has been growing since the late 1990s known as participatory for adoption such as the Rural Capitalization Incentive (ICR), research (World Bank, 2012). In the case of the CGIAR, the whose objective is to help subsidize up to 40% of the debt of budget (in inflation-adjusted terms) remained fairly flat between small producers that request credits for the establishment of 1980 and 2000, even though its mandate was broadened to cover silvopastoral systems. a wide range of research topics. As a result, the continued search The aforementioned issue clearly indicates, in the voice of for sustained funding for public agricultural research at the global some of the main agents and historical moments that play a role and national levels remains one of the main challenges (Beintema in the processes of diffusion and adoption of forage technologies, and Echeverría, 2020). The data indicate that, in general, the the difficulties that persist and hinder the way of a sustained and participation of the private sector in agricultural research in Latin successful technification. Despite the many advances obtained American countries has been increasing over time, and currently in the matter and the valuable and decisive work of research it is private companies that supply most of the seeds and animal institutions, there is still a long way to go, not only in the genetics to farmers in the region (Stads and Beintema, 2009). transformation of livestock landscapes in Colombia and the Regarding one of our main findings, which is the explicitness efficient implementation of improved pastures, but also in the that most of the intra-actoral exchanges registered are weak, understanding and study of agricultural innovation systems as unidirectional and without feedback loops, several authors refer historical processes, contingent, subject to change, and deeply to the existence of weak links between national agricultural affected by inter-actoral relationships. In closing, here are some research institutions and rural extension actors in most possible insights on how these R&D processes can be refined. developing economies (e.g., Anderson, 2004). It is noted that the information used by extension institutions is not necessarily accurate or generated by research institutions, and research DISCUSSION priorities do not necessarily align with the needs of extension institutions. Also, on many occasions both types of organization Although mapping the interactions and dialoguing with key compete for resources (Anderson, 2004). A study carried out by agents allowed the identification of the main actors and FAO/BID (2016) illustrates this problem. This study evaluated their interactions in the research and dissemination of forages the technical assistance service in South America. For the case of in Colombia evidence important findings that we explain Colombia, 117 surveys were applied to service providers and 38 in detail, trends in academic literature show the changing to producers. According to the results, 38% of the organizations historicity of R&D of agricultural technologies, its challenges and stated that they had weak ties with other organizations, 30% had opportunities and the complex nature of inter-actoral relations moderate ties, and 20% had close ties (11% did not respond). and the contexts under which it takes place. This discussion is The strongest links are with local government agencies and banks then framed taking into account these three key elements. We and microcredit institutions (31%). In the case of Colombia, first address the historical context and the main transformations a manifested weakness is evident in the relationship between of the AIS. Next, we delve into the conceptualization of inter- the organizations that provide technical assistance (UMATA, actoral relations and their importance within the AIS, and lastly, EPSAGRO, NGOs, or unions) and the organizations that can we discuss the main bottlenecks found to be key in the AIS contribute to the provision of the service. For example, the in Colombia. link between research centers and UMATA and EPSAGRO was Investments in agricultural research have had important considered by 50% as weak, and only 43% of the unions consider changes over time with relevant effects affecting the development it strong (FAO/BID, 2016). of research processes. For example, in the case of the CGIAR, Thus, a key to improving rural extension is the articulation research funding has changed dramatically: it went from being between the actors that provide technical assistance services historically constituted in the long-term and directed through with the research actors, and so is strengthening of their central institutions that were in charge of coordinating and capacities (Garrido-Rubiano et al., 2021). Therefore, one of managing projects, to being based on short- and medium- the greatest challenges is to achieve coordination between the term programs, oriented to smaller projects, and of less scope. actors (Garrido-Rubiano et al., 2021). Problems related to weak The mode of financing has also been significantly transformed, links and lack of trust between actors, as well as asymmetries moving from unrestricted institutional allocations to concrete in communication between them, are recognized as factors projects with concrete deadlines and strict budgets (Beintema commonlymentioned in the literature that uses the AIS approach and Echeverría, 2020). In turn, the thematic focus of the research to examine the problems of adoption of agricultural technologies has expanded significantly, withmuchmore emphasis on politics, (e.g., Spielman et al., 2011; Kebebe, 2018). the environment, and biodiversity conservation (Beintema and Although there is a historical presence of national and Echeverría, 2020). international institutions promoting research and innovation in Both research and extension components have been oriented agricultural technologies (forages for the example that concerns more toward the direct involvement of the producers in us here), we find that the assertiveness of interpersonal links has Frontiers in Sustainable Food Systems | www.frontiersin.org 1853 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption determined immensely the adoption processes. For example, in countries of the region in the 1980s and 1990’s. These reports this case-study, CIAT plays a leading role in the development highlight direct effects of this reduction in research centers, such of new and improved technologies for the country. However, as the elimination of several long-standing research programs, the prominence of institutions has not translated into a higher and the deterioration of facilities and laboratories. Similarly, adoption rate or a more expeditious path toward the goal, insofar changes in the financing model since the 1990s (from long- as, as mentioned above, personal relationships directly influence term to short-term projects) and the constant struggle to obtain inter-institutional ones. resources affected institutions such as the CGIAR, which in turn Literature on this subject defines how the domain of transformed the way of doing research and research and duration intermediaries and/or bridging institutions (e.g., extension and impact of the projects themselves (Beintema and Echeverría, services that facilitate the transfer of knowledge and information 2020). between domains) is essential in the case of a successful AIS, In Colombia, the most relevant reform associated with which for the Colombian context, as mentioned, is in deficit. technical assistance services was related to the State’s Thus, new technologies resulting from R&D processes in the decentralization processes, through which the National agricultural sector have improved the quantity and quality Government delegated the provision of this service to the of production and, therefore, have contributed to economic territories. However, the limited capacity of the municipalities development, agricultural development, and poverty reduction to assume obligations of such magnitude was not considered. in Latin America (Stads and Beintema, 2009). However, properly Most local governments did not have the required capacities, designed national agricultural research systems and adequate the necessary administrative procedures, the external financing levels of investment are important prerequisites for agricultural mechanisms, or the sufficient skills for the investment project development, food security and poverty reduction in all countries management process (such as planning, monitoring, and in the region (Stads and Beintema, 2009). Some recent research evaluation) (FAO/BID, 2016). According to the National indicates that problems at the institutional and policy levels Agricultural Census (DANE, 2014), only 16.5% of the producers explain the low adoption of technology by small producers more have access to extension services. Thus, among the bottlenecks than aspects of the producer (e.g., Birner and Resnick, 2010; identified in the technical assistance service in the country are Schut et al., 2016). the lack of capacities installed in the regions, the institutional Widely discussed bottlenecks, such as extensive livestock disarticulation among those who generate, disseminate and farming, reductions in research budgets, weakness of the accumulate knowledge, the low levels of associativity of extension processes in the promotion of forage technologies, the producers, the loss of confidence of the latter in the effectiveness low impact of agricultural credit lines, scarce articulation between of the service, and a deficient monitoring and evaluation system R&D institutions and seed companies, as well as unpredictable (Hurtado et al., 2020). speculation in the Brazilian seed market, have largely affected Another element worth bringing to the discussion is that the Colombian context. First, the extensive nature of livestock of credit lines. Although actors recognize the importance of can be explained here from structural conditions that discourage credit for agricultural development in the country, they also sustainable intensification, since inmany cases, it is more efficient highlight key bottlenecks associated with the low provision of to acquire more land than to intensify. Low land prices, as well credit in rural areas, asymmetries in access to information that as the predominance of a fragile state to control access to it, have mainly affect small producers, and a credit orientation more played a decisive role. Thus, structural factors that affect extensive geared toward productivity than toward sustainability. Different livestock are (i) the higher profitability associated with new forage studies have found empirical evidence where access to credit technologies that could lead producers to increase their herd size has a positive and significant effect on the adoption of new and hence the pasture area (Kaimowitz and Angelsen, 2008), technologies and practices in the livestock sector (e.g., Lapar and (ii) low land prices in many regions (e.g., Orinoquia) that and Ehui, 2004; Turinawe et al., 2012). According to DNP make acquiring new landmore efficient than intensifying existing calculations (2015), FINAGRO condition credits only reach land (White et al., 2001). Likewise, profitable technologies can 38% of the rural producers in Colombia, and credit lines have also provide farmers with the additional capital they need to been directed toward profitability instead of sustainability in finance livestock expansion (Kaimowitz and Angelsen, 2008). the livestock sector. According to FINAGRO’s accountability Thus, if one of the main reasons for planting pastures is to figures (FINAGRO, 2020), credit applications from the livestock have secure land tenure, the forest conversion to pasture can sector at the national level have been mainly channeled toward (and will) continue (Kaimowitz and Angelsen, 2008). This can the purchase of animals, machinery, or the payment of the be favored by price speculation processes, where acquiring more labor force, while credit applications designed to promote land would increase capital gains (Smith et al., 1997; Van Ausdal, sustainable intensification systems, such as pasture renewal or the 2012; Gutiérrez-Sanín and Vargas, 2017; Ponce de León-Calero, establishment of silvopastoral systems, have been very limited. 2019). This orientation is more pronounced in small and medium In the research component, budget reductions experienced producers with participation percentages of 96.5 and 75.75%, during the 1990s were decisive. Different reports of the ASTI respectively. For its part, the investment dedicated to sowing (Indicators of Agricultural Science and Technology) (Stads and forages does not exceed 2% (FINAGRO, 2020). The advance of Beintema, 2009; Stads et al., 2016) evaluate trends in R&D in the substitute portfolio constitutes a problem in the accentuation Latin America, pointing out the reduction of resources in all of inequalities in the rural sector: despite the fact that the Frontiers in Sustainable Food Systems | www.frontiersin.org 1864 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption resources for agricultural credit lines have increased over time, relationships between institutions, it is urgent to promote greater the majority of resources have been directed toward other links in communication and exchange between them, though research, the value chain with a lower level of risk. Regarding total credit by dissemination platforms in which they present results, trends, type of producer, there has been a decrease in the share of credit and research proposals (future and ongoing). The temporary granted to small producers, and an increase for large producers. exchange of personnel, as well as guided visits between entities, While in 2010 small producers participated with 26% of total could play vital roles in strengthening ties, increasing bonds credit, for 2019 this percentage was 23% (FINAGRO, 2020). For of trust and maintaining this symbiosis over time. We also their part, the large producers in 2010 participated with 28%, consider it essential to promote articulation between research and while in 2019 this participation increased to 59% (FINAGRO, dissemination institutions and distributors of improved seeds, 2020). companies, and actors that are part of sustainable livestock Besides this, a poor coordination between national R&D strategies (e.g., Sustainable Livestock Table Colombia, zero institutions and seed companies is also profoundly telling. As deforestation agreements) in order to improve the dissemination institutions of diverse nature, both have different goals, and in and opening channels of communication between them, many opportunities the release of materials is carried out without establishing dialogues that facilitate the development of public being able to guarantee the availability of seed at a commercial policies for the sector and contributing to the development level. To illustrate, materials such as Andropogon gayanus cv. of institutional and field capacities. Likewise, and as far as Carimagua 1, Brachiaria dictyoneura cv. Llanero, and Brachiaria “third parties” are concerned, we maintain that it is of the brizantha cv. La Libertad, released by ICA (now AGROSAVIA) utmost importance to take advantage of the potential of the in the 1980s, failed despite promotional efforts due to the lack milk processing industries to reach the primary producer: the of basic and commercial seed supply (Ferguson, 1993). The low direct link that has been created between these companies articulation between research institutions and seed companies and producing communities can be useful for disseminating was a priority issue during the workshops carried out by the technologies through training and education programs. Since International Network for Tropical Pasture Evaluation (RIEPT companies do not have the technical knowledge related to forage for its acronym in Spanish) (Ferguson, 1993), which denotes management, it is important to promote projects in association that the research sector identified a poor relationship with seed with research and extension institutions. companies as one of the great obstacles to generating an impact Solid relationships with policy makers, in which the benefits on the adoption of improved forages. (economic, productive, competitive, and environmental) that the Finally, speculation in the Brazilian market stands as one of country has from promoting plans and projects that contribute the main bottlenecks, applicable to the Colombian case due to to the implementation of forage technologies in Colombia is also its high dependence on market conditions in the neighboring a necessity for the sector. The involvement of public institutions country. According to Legiscomex (2020), of the total imported with private actors in the development of technologies should be seed in Colombia, more than 90% comes from Brazil, from established in the agendas, not only of universities and research where varieties mainly of the Brachiaria and Panicum species centers, but also between them and government agencies. Said are imported. Forage seed production began in Colombia in dialogues could be aimed at consolidating strategies that allow the 1970s, a period in which seed production and marketing the articulation at municipal, departmental, and national levels companies emerged (Ferguson, 1993). At this time, companies of each of the local initiatives where the nascent extension such as Semillano Ltda. directly produced seed in the company system can play an important role. It is well-known in of farmers and in their own lots for varieties such as B. academic literature that producer cooperatives and associations decumbens, B. dyctionerura, Stylosanthes capitata, and Arachis are fundamental actors in technology diffusion processes. Here, pintoi. Only a small amount of seed was imported from Brazil we propose to encourage the creation of these institutions in to meet the demand. However, the forage seed industry in territories where they do not yet exist or in territories where Brazil took an important advantage. This was mainly favored existing ones are located far away from the producers. This can by the environmental conditions that are particularly conducive be done during vaccination periods or during technical visits by to seed production, such as the altitudinal level that allows control bodies (e.g., ICA). It is also useful to point out that, in longer periods of light and, therefore, greater flowering and those consolidated associations, the sharing of experiences and better synchronization (Hopkinson, 1981). These comparative cultural practices in the management of pastures and properties advantages allowed the Brazilian industry to specialize and is encouraged. Together with extension agents, knowledge about become one of the most important producers, consumers, and scientific innovations can be addressed, thus generating fertile exporters of forage seed worldwide. and lasting exchanges. Through the creation of innovation networks (such as the Forages Network between CIAT and Agrosavia), alliances CONCLUSIONS between research institutes, higher training centers, rural extension services, and producer associations can also be fostered By way of conclusion, we highlight firstly and as a constitutive in order to advance faster in technology adoption processes. and conclusive element of this research, the importance of Another possibility for improvement and transformation of the institutional alliances as a cross-cutting element in the adoption R&D system lies in the promotion of incentives for adoption. The of agricultural technologies. We believe that, in addition to the creation of credit instruments for the adoption of technologies Frontiers in Sustainable Food Systems | www.frontiersin.org 1875 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption and the articulation of agricultural credit lines with extension International and CIAT. The patients/participants provided their services, can positively transform the panorama in terms of the written informed consent to participate in this study. adoption of improved forages. This is important not only for forage technologies but also for silvopastoral systems, which tend AUTHOR CONTRIBUTIONS to be long-term investments as well. Finally, the strengthening and prioritization of livestock NT, KE, MD, and SB: conceptualization, methodology, writing production chains in the Departmental Agricultural Extension the original draft and review and editing, and resources. NT, KE, Plans (PDEA) in those territories where livestock predominates and MD: formal analysis. SB: supervision, funding acquisition, and there are high levels of deforestation and low adoption and project administration. All authors contributed to the article of forage technologies is a fundamental and unquestionable and approved the submitted version. axis. The training that is established for this purpose should not only involve the management of pastures and forages; FUNDING For success to be sustainable over time, we are convinced, extension strategies must include a holistic campaign in This work was funded by the CGIAR Research Program on which producers are interested in the effective use of support Livestock. The funders had no role in the design of the study; in information, social appropriation of knowledge, and problem the collection, analyses, or interpretation of data; in the writing solving, mainly through open or collaborative innovation, of the manuscript, or in the decision to publish the results. participatory research, and the use of Information and Communication Technologies. ACKNOWLEDGMENTS DATA AVAILABILITY STATEMENT This work was carried out as part of the CGIAR Research Program on Livestock. We thank all donors who globally support The raw data supporting the conclusions of this article will be our work through their contributions to the CGIAR System. made available by the authors, without undue reservation. SUPPLEMENTARY MATERIAL ETHICS STATEMENT The Supplementary Material for this article can be found The studies involving human participants were reviewed and online at: https://www.frontiersin.org/articles/10.3389/fsufs. approved by Ethics Committee of the Alliance of Bioversity 2021.741057/full#supplementary-material REFERENCES CEPAL, FAO, and IICA (2017). Perspectivas de la agricultura y del desarrollo rural en las Américas: una mirada hacia América Latina y el Caribe. San Jose, CA: Aberman, N., Birner, R., Haglund, E., Ngigi, M., Ali, S., Okoba, B., et al. CEPAL, FAO, IICA. Available online at: http://hdl.handle.net/11362/45111 (2015). Understanding the Policy Landscape for Climate Change Adaptation: Charry, A., Narjes, M., Enciso, K., Peters, M., and Burkart, S. (2019). A Cross-Country Comparison Using the Net-Map Method. Washington, DC: Sustainable intensification of beef production in Colombia—Chances for International Food Policy Research Institute (IFPRI). product differentiation and price premiums. Agric. Food Econ. 7:22. Anderson, J. R. (2004). Agricultural extension: good intentions and hard realities. doi: 10.1186/s40100-019-0143-7 World Bank Res. Observ. 19, 41–60. doi: 10.1093/wbro/lkh013 DANE (2014). Data From: Censo Nacional Agropecuario, 2014. Available Ardila, J. (2010). Extensión rural para el desarrollo de la agricultura y la seguridad online at: https://www.datos.gov.co/widgets/6pmq-2i7c (accessed December alimentaria: aspectos conceptuales, situación y una visión de futuro. San José, 21, 2021). CA: Instituto Interamericano de Cooperación para la Agricultura (IICA). Daum, T., and Birner, R. (2017). The neglected governance challenges of Ashley, K., Wilson, S., Young, J. R., Chan, H. P., Vitou, S., Suon, S., et al. agricultural mechanisation in Africa – insights from Ghana. Food Sec. 9, (2018). Drivers, challenges and opportunities of forage technology adoption 959–979. doi: 10.1007/s12571017-0716-9 by smallholder cattle households in Cambodia. Trop. Anim. Health Prod. 50, Dill, M. D., Emvalomatis, G., Saatkamp, H., Rossi, J. A., Pereira, G. R., and 63–73. doi: 10.1007/s11250-017-1400-y Barcellos, J. O. J. (2015). Factors affecting adoption of economic management Beintema, N. M., and Echeverría, R. G. (2020). Evolution of CGIAR Funding. practices in beef cattle production in Rio Grande do Sul state, Brazil. J. Rural Washington, DC: International Food Policy Research Institute (IFPRI). Stud. 42, 21–28. doi: 10.1016/j.jrurstud.2015.09.004 Available online at: https://www.asti.cgiar.org/publications/asti-20-cgiar Enciso, K., Triana, N., Diaz, M. F., and Burkart, S. (2019). Limitations and (accessed December 21, 2021). Opportunities in the Process of Adoption and Dissemination of Forages BID (2018). Plataforma latinoamericana y del Caribe para la intensificación Technologies in Colombia. Cali: International Center for Agricultural sostenible de la ganadería: una estrategia regional para la adaptación al cambio Tropical (CIAT). climático y lamitigación de sus efectos. San José: BID. Available online at: https:// FAO/BID (2016). Estrategias, reformas e inversiones en los sistemas de extensión n9.cl/lo9og rural y asistencia técnica en América del Sur. Lima: Organización de las Birner, R., and Resnick, D. (2010). The political economy of Naciones Unidas para la Alimentación la Agricultura (FAO) and Banco policies for smallholder agriculture. World Dev. 38, 1442–1452. Interamericano de Desarrollo (BID). Available online at: https://www.fao.org/ doi: 10.1016/j.worlddev.2010.06.001 3/i6055s/i6055s.pdf (accessed December 21, 2021). Carey, J., and Zilberman, D. (2002). A model of investment under Ferguson, J. E. (1993). El Proceso de Liberación de Nuevos Cultivares de Forrajeras: uncertainty: modern irrigation technology and emerging markets Experiencias y Perspectivas. In: Ferguson, JE (Ed). Semilla de Especies Forrajeras in water. Am. J. Agric. Econ. 84, 171–183. doi: 10.1111/1467-8276. Tropicales Conceptos, casos y enfoque de la investigación y la producción. Cali: 00251 Centro Internacional de Agricultura Tropical (CIAT). Frontiers in Sustainable Food Systems | www.frontiersin.org 1886 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption FINAGRO (2020).Data From: Rendición de cuentas Finagro, 2019. Available online Brachiaria Grass Forage Cultivars in Latin America Focusing in the Experience at: https://www.finagro.com.co/webform/rendici3n-de-cuentas-2019 of Colombia. SPIA Technical Report. Rome: Standing Panel for Impact Garrido-Rubiano, M. F., Pulido Castro, S. X., Lesmes Chavur, A. R., Assessment (SPIA). Buitrago Albarado, C. P., Molano Bernal, L. C., Montes Vergara, J. C., Lapar, M. A., and Ehui, S. K. (2004). Factors affecting adoption of dual- et al. (2021). La extensión agropecuaria para la innovación. Bogotá, DC: purpose forages in the Philippine uplands. Agric. Syst. 81, 95–114. Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA). doi: 10.1016/j.agsy.2003.09.003 doi: 10.21930/agrosavia.analisis.7404722 Lavelle, P., Rodríguez, N., Arguello, O., Bernal, J., Botero, C., Chaparro, P., Gerber, P. J., Steinfeld, H., Henderson, B., Mottet, A., Opio, C., Dijkman, et al. (2014). Soil ecosystem services and land use in the rapidly changing J., et al. (2013). Enfrentando el cambio climático a través de la ganadería Orinoco river basin of Colombia. Agric. Ecosyst. Environ. 185, 106–117. – Una evaluación global de las emisiones y oportunidades de mitigación. doi: 10.1016/j.agee.2013.12.020 Roma: Organización de las naciones unidas para la alimentación y la Legiscomex (2020). Data from: Sistema de inteligencia comercial. Estadísticas de agricultura (FAO). comercio exterior. Available online at: https://www.legiscomex.com/ (accessed Gil, J., Siebold, M., and Berger, T. (2015). Adoption and development of integrated December 21, 2021). crop–livestock–forestry systems inMato Grosso, Brazil.Agric. Ecosyst. Environ. Lubungue, M., and Birner, R. (2018). Using process net-map to analyse governance 199, 394–406. doi: 10.1016/j.agee.2014.10.008 challenges: A case study of livestock vaccination campaigns in Zambia. Gutiérrez-Sanín, F., and Vargas, J. (2017). Agrarian elite participation in Preventive Veterinary Medicine 156. doi: 10.1016/j.prevetmed.2018.05.009 Colombia’s civil war. J. Agrarian Change 17, 739–748. doi: 10.1111/joac.12235 Lynam, J. K., and Byerlee, D. (2017). Forever Pioneers–CIAT: 50 Years Contributing Hambly, H., Hall, A., and Dorai, K. (2012). “Assessing, prioritizing, to A Sustainable Food Future. . . and Counting. Cali: International Center for monitoring, and evaluating agricultural innovation systems,” in Agricultural Tropical Agriculture (CIAT). Innovation Systems: An Investment Sourcebook, ed The World Bank Maass, B. L., Midega, C. A. O., Mutimura, M., Rahetlah, V. B., Salgado, P., (Washington, DC: The World Bank), 539–628. Available online Kabirizi, J. M., et al. (2015). Homecoming of Brachiaria: Improved hybrids at: https://elibrary.worldbank.org/doi/abs/10.1596/9780821386842_CH07 prove useful for African animal agriculture. East Afr. Agr. Forestry J. 81, 71–78. Herrero, M., Havlík, P., Valin, H., Notenbaert, A., Ru no, M. C., Thornton, P. doi: 10.1080/00128325.2015.1041263 K., et al. (2013). Biomass use, production, feed e ciencies, and greenhouse Marra, M., Pannell, D. J., and Abadi-Ghadim, A. (2003). The economics gas emissions from global livestock systems. Proc. Natl. Acad. Sci. U.S.A. 110, of risk, uncertainty and learning in the adoption of new agricultural 20888–20893. doi: 10.1073/pnas.1308149110 technologies: where are we on the learning curve? Agric. Syst. 75, 215–234. Herrero, M., Henderson, B., Havlík, P., Thornton, P. K., Conant, R. T., Smith, P., doi: 10.1016/S0308-521X(02)00066-5 et al. (2016). Greenhouse gas mitigation potentials in the livestock sector. Nat. Moreta, D. E., Arango, J., Sotelo, M., Vergara, D., Rincón, A., Ishitani, M., et al. Clim. Change 6, 452–461. doi: 10.1038/nclimate2925 (2014). Biological nitrification inhibition (BNI) in Brachiaria pastures: a novel Hopkinson, J. M. (1981). “Seed release to commerce,” in Collecting and strategy to improve eco-efficiency of crop-livestock systems and to mitigate Testing Tropical Forage Plants, eds R. J. Clements, and D. R. Cameron climate change. Trop. Grassl. 2, 88–91. doi: 10.17138/TGFT(2)88-91 (Melbourne, VIC: Commonwealth Scientific and Industrial Research Nuñez, J., Arevalo, A., Karwat, H., Egenolf, K., Miles, J., Chirinda, N., et al. Organisation (CSIRO)), 133–141. (2018). Biological nitrification inhibition activity in a soil-grown biparental Hristov, A. N., Oh, J., Meinen, R., Montes, F., Ott, T., Firkins, J., et al. population of the forage grass, Brachiaria humidicola. Plant Soil 426, 401–411. (2013). “Mitigation of greenhouse gas emissions in livestock production – doi: 10.1007/s11104-018-3626-5 a review of technical options for non-CO2 emissions,” in FAO Animal. OECD/FAO (2020). OECD-FAO Agricultural Outlook 2020-2029. Rome, Paris: Production and Health, eds P. Gerber, B. Henderson, and H. Makkar (Rome: FAO; OECD Publishing. doi: 10.1787/1112c23b-en Food and Agriculture Organization of the United Nations (FAO)). Available Oliveira, S. G., Berchielli, T. T., Pedreira, M. S., Primavesi, O., Frighetto, R., and online at: https://www.fao.org/publications/card/en/c/87178c51-d4d1-515d- Lima, M. A. (2007). Effect of tannin levels in sorghum silage and concentrate 9d0e-b5a6937fa631/ (accessed December 21, 2021). supplementation on apparent digestibility and methane emission in beef cattle. Hurtado, A., Diaz, M. F., Enciso, K., and Burkart, S. (2020). A extensión rural Anim. Feed Sci. Technol. 135, 236–248. doi: 10.1016/j.anifeedsci.2006.07.012 para la actividad ganadera en Colombia: legislación, desarrollos, brechas y Palacios, M., and Stoller, R. (2006). Between Legitimacy and Violence: A oportunidades. Cali: Centro Internacional de Agricultura Tropical. Available History of Colombia, 1875–2002. Durham; London: Duke University Press. online at: https://hdl.handle.net,/10568/111045 doi: 10.2307/j.ctv1220mkn IDEAM UDCA (2015). Síntesis del estudio nacional de la degradación de suelos Pannell, D. J., Marshall, G. R., Barr, N., Curtis, A., and Vanclay, F. W. R. (2006). por erosión en Colombia - 2015. Bogotá: Instituto de Hidrología, Meteorología Understanding and promoting adoption of conservation practices by rural y Estudios Ambientales de Colombia (IDEAM); Ministerio de Ambiente y landholders. Austr. J. Exp. Agric. 43, 1407–1424. doi: 10.1071/EA05037 Desarrollo Sostenible (MADS). Peters, M., Franco, L. H., Schmidt, A., and Hincapie, B. (2011). Especies Ilukor, J., Birner, R., Rwamigisa, P. B., and Nantima, N. (2015). The provision forrajeras multipropósito: opciones para productores del trópico Americano. of veterinary services: who are the influential actors and what are the Centro Internacional de Agricultura Tropical (CIAT); Bundesministerium für governance challenges? A case study of Uganda. Exp. Agric. 51, 408–434. Wirtschaftliche Zusammenarbeit und Entwicklung (BMZ); Deutsche Gesellschaft doi: 10.1017/S0014479714000398 fTechnische Zusammenarbeit (GIZ), Cali, CO. vii, 212. Available online at: Jera, R., and Ajayi, O. C. (2008). Logistic modelling of smallholder https://hdl.handle.net/10568/54681 (accessed December 21, 2021). livestock farmers’ adoption of tree-based fodder technology in Peters,M., Herrero,M., Fisher,M., Erb, K.-H., Rao, I., Subbarao, G. V., et al. (2013). Zimbabwe. Agric. Econ. Res. Policy Pract. Southern Afr. 47, 379–392. Challenges and opportunities for improving eco-efficiency of tropical forage- doi: 10.1080/03031853.2008.9523806 based systems to mitigate greenhouse gas emissions. Trop. Grassl. 1, 137–148. Kaimowitz, D., and Angelsen, A. (2008). Will livestock intensification help doi: 10.17138/ TGFT(1)156-167 save Latin America’s Tropical Forests?. J. Sustain. Forestry 27, 6–24. Peters, M., Rao, I., Fisher, M., Subbarao, G., Martens, S., Herrero, M, et al. doi: 10.1080/10549810802225168 (2012). “Tropical forage based systems to mitigate greenhouse gas emissions,” Karwat, H., Moreta, D., Arango, J., Núñez, J., Rao, I., Rincón, A., et al. in Ecoeficiency: From Vision to Reality, ed C. H. Hershey (Cali: International (2017). Residual effect of BNI by Brachiaria humidicola pasture on nitrogen Center for Tropical Agriculture (CIAT)). Available online at: https://hdl.handle. recovery and grain yield of subsequent maize. Plant Soil 420, 389–406. net/10568/55611 (accessed December 21, 2021). doi: 10.1007/s11104-017-3381-z Ponce de León-Calero, A. (2019). En medio de la violencia: recursos, Kebebe, E. (2018). Bridging technology adoption gaps in livestock sector tácticas y violencia contra el sector ganadero. Revista CS 19, 19–45. in Ethiopia: an innovation system perspective. Technol. Soc. 57, 30–37. doi: 10.18046/recs.i28.3199 doi: 10.1016/j.techsoc.2018.12.002 Rajalahti, R., Janssen, W., and Pehu, E. (2008). Agricultural Innovation Labarta, R., Martinez, J. M., Yaccelga, A., Reyes, B., Gomez, L., Maredia, M., Systems: From Diagnostics Toward Operational Practices, Agriculture & Rural et al. (2017). Assessing the Adoption and Economic & Environmental Impacts of Development Department. Washington, DC: The World Bank. Frontiers in Sustainable Food Systems | www.frontiersin.org 1897 January 2022 | Volume 5 | Article 741057 Enciso et al. AIS and Forage Technology Adoption Rao, I., Kerridge, P. C., and Macedo, M. C. M. (1998). “Requerimientos Stads, G., and Beintema, N. M. (2009). Investigación Agrícola Pública en América nutricionales y adaptación a los suelos ácidos de especies de Brachiaria,” In: Latina y el Caribe Tendencias de capacidad e inversión. Informe de síntesis ASTI. Brachiaria: biología, agronomía y mejoramiento, eds J. W. Miles, B. L. Maass, Washington, DC: Agricultural Science and Technology Indicators (ASTI); and C. B. do Valle. Cali; Campo Grande: Centro Internacional de Agricultura International Food Policy Research Institute (IFPRI); The Inter-American Tropical (CIAT); Empresa Brasileira de Pesquisa Agropecuaria (EMBRAPA). Development Bank (IDB). Available online at: https://hdl.handle.net/10568/54362 Subbarao, G., Nakahara, K., Hurtado, M., Ono, H., Moreta, D., Salcedo, A. F., et al. Rao, I., Peters, M., Castro, A., Schultze-Kraft, R.,White, D., Fisher, M., et al. (2015). (2009). Evidence for biological nitrification inhibition in Brachiaria pastures. LivestockPlus - the sustainable intensification of forage-based agricultural Proc. Natl. Acad. Sci. U.S.A. 106, 17302–17307. doi: 10.1073/pnas.0903694106 systems to improve livelihoods and ecosystem services in the tropics. Trop. Subbarao, G. V., Arango, J., Masahiro, K., Hooper, A. M., Yoshihashi, T., Ando, Grassl. 3, 59–82. doi: 10.17138/TGFT(3)59-82 Y., et al. (2017). Genetic mitigation strategies to tackle agricultural GHG Rao, I., Peters, M., van der Hoek, R., Castro, A., Subbarao, G., Cadisch, G., et al. emissions: the case for biological nitrification inhibition technology. Plant Sci. (2014). Tropical forage-based systems for climate-smart livestock production 262, 165–168. doi: 10.1016/j.plantsci.2017.05.004 in Latin America. Rural21 4, 12–15. Available online at: http://hdl.handle.net/ TheWorld Bank (2006). Enhancing Agricultural Innovation: How to Go Beyond the 10986/2247 (accessed December 21, 2021). Strengthening of Research Systems. Washington, DC: The World Bank. Reckling, M., Bergkvist, G., Watson, C. A., Stoddard, F. L., Zander, P. M., Walker, Thomas, D., and Sumberg, J. E. (1995). A review of the evaluation R. L., et al. (2016). Trade-offs between economic and environmental impacts and use of tropical forage legumes in sub-Saharan Africa. of introducing legumes into cropping systems. Front. Plant Sci. 7, 1–15. Agric. Ecosyst. Environ. 54, 151–163. doi: 10.1016/0167-8809(95) doi: 10.3389/fpls.2016.00669 00584-F Reiber, C., Schultze-Kraft, R., Peters, M., Lentes, P., and Hoffmann, V. (2013). Tirado-Mejia, A. (1997). Integración y democracia en América Latina y el Caribe, Lessons from silage adoption studies in Honduras. Trop. Grassl. 1:235–239. 1997. Buenos Aires: Banco Interamericano de Desarrollo (BID) y - Instituto doi: 10.17138/TGFT(1)235-239 para la Integración de América Latina y el Caribe (INTAL). Rincón, A., Bueno, G. A., Álvarez, M., Pardo, Ó., and Pérez, O., Caicedo, S. Turinawe, A., and Mugisha, J., Kabirizibi, J. (2012). Socio-economic evaluation of (2010). Establecimiento, manejo y utilización de recursos forrajeros en sistemas improved forage technologies in smallholder dairy cattle farming systems in ganaderos de suelos ácidos. Villavicencio; Meta: Corporación Colombiana Uganda. J. Agric. Sci. Arch. 4:163. doi: 10.5539/jas.v4n3p163 de Investigación Agropecuaria (CORPOICA). Available online at: http://hdl. Van Ausdal, S. (2012). Productivity gains and the limits of tropical ranching in handle.net/20.500.12324/12703 Colombia, 1850-1950. Agric. History 86, 1–32. doi: 10.3098/ah.2012.86.3.1 Rincón, A., Flórez, H., Ballesteros, H., and León, L. M. (2018). Efectos de la Vera, R. R., and Seré, R. C. (1989). “Resultados obtenidos conAndropogon gayanus fertilización en la productividad de una pastura de Brachiaria humidicola cv. en las fincas de los productores de ganado,” in Andropogon gayanus Kunth: Llanero en el Piedemonte de los Llanos Orientales de Colombia. Trop. Grassl. Un pasto para los suelos ácidos del trópico, eds J. M. Toledo, R. R. Vera, 6, 158–168. doi: 10.17138/TGFT(6)158-168 C. E. Lascano, and J. M. Lenné (Cali: Centro Internacional de Agricultura Rivas, L., and Holmann, F. (2004). Impacto de la adopción de híbridos Tropical), 323–355. de Brachiarias resistentes al salivazo: Colombia, México, y Centroamérica. White, D., Holmann, F., Fujisaki, S., Reategui, K., and Lascano, C. (2001). “Will Cali: Centro Internacional de Agricultura Tropical (CIAT). Available online intensifying pasture management in Latin America protect forests – Or is it the at: https://hdl.handle.net/10568/1747 (accessed December 21, 2021). other way around?,” in Agricultural Technologies and Tropical Deforestation, Rousseau, L., Fonte, S. J., Téllez, O., Van der Hoek, R., and Lavelle, P. eds A. Angelsen, and D. Kaimowitz (Wallingford: CABI Publishing), 91–113. (2013). Soil macrofauna as indicators of land use impacts and soil quality doi: 10.1079/9780851994512.0091 in agricultural landscapes of northern Nicaragua. Ecol. Indic. 27, 71–82. White, D. S., Peters, M., and Hornes, P. (2013). Global impacts from doi: 10.1016/j.ecolind.2012.11.020 improved tropical forages: a meta-analysis revealing overlooked benefits Schiffer, E. (2007). The Power Mapping Tool: A Method for the Empirical Research and costs, evolving values and new priorities. Trop. Grassl. 1, 12–24. of Power Relations. Washington, DC: International Food Policy Research doi: 10.17138/tgft(1)12-24 Institute (IFPRI). World Bank (2012). Agricultural Innovation Systems: An Investment Sourcebook. Schut, M., van Asten, P., Okafor, C., Hicintuka, C., Mapatano, S., Nabahungu, Agricultural and Rural Development. Washington, DC: World Bank. Available N. L., et al. (2016). Sustainable intensification of agricultural systems in the online at: http://hdl.handle.net/10986/2247 (accessed December 21, 2021). Central African Highlands: the need for institutional innovation. Agric. Syst. 145, 165–176. doi: 10.1016/j.agsy.2016.03.005 Author Disclaimer: The views expressed in this document may not be taken as Seré, C., Estrada, R.,., and Ferguson, J. (1993). Estudios de adopción e impacto the official views of these organizations. CGIAR is a global research partnership en pasturas tropicales, investigación con pasturas en fincas. Cali: Centro for a food-secure future. Its science is carried out by 15 Research Centers in close Internacional de Agricultura Tropical (CIAT). Available online at: https://hdl. collaboration with hundreds of partners across the globe. handle.net/10568/55753 Shelton, HM; Franzel, S; Peters, M. (2005). Adoption of tropical legume Conflict of Interest: The authors declare that the research was conducted in the technology around the world: analysis of success. Trop. Grassl. 39, 198–209. absence of any commercial or financial relationships that could be construed as a doi: 10.3920/978-90-8686-551-2 potential conflict of interest. Shelton, M., and Dalzell, S. (2007). Production, economic and environmental benefits of leucaena pastures. Trop. Grassl. 41, 174–190. Available The handling editor is currently editing co-organizing a Research Topic with the online at: https://www.tropicalgrasslands.info/index.php/tgft/pages/view/ author SB and confirms the absence of any other collaboration. tropicalGrasslands (accessed December 21, 2021). Smith, J., Cadavid, J. V., Rincón, A., and Vera, R. (1997). Land speculation and Publisher’s Note: All claims expressed in this article are solely those of the authors intensification at the Frontier: a seeming paradox in the Colombian Savanna. and do not necessarily represent those of their affiliated organizations, or those of Agric. Syst. 54, 501–520. the publisher, the editors and the reviewers. Any product that may be evaluated in Soussana, J. F., Tallec, T., and Blanfort, V. (2010). Mitigating the greenhouse this article, or claim that may be made by its manufacturer, is not guaranteed or gas balance of ruminant production systems through carbon sequestration in grasslands. Animal 4, 334–350. doi: 10.1017/s1751731109990784 endorsed by the publisher. Spielman, D., Davis, K. E., Negash, M., and Ayele, G. (2011). Rural innovation systems and networks: Findings from a study of Ethiopian smallholders. Agric. Copyright © 2022 Enciso, Triana, Díaz and Burkart. This is an open-access article Hum. Values 28, 195–212. doi: 10.1007/s10460 distributed under the terms of the Creative Commons Attribution License (CC BY). Stads, G., Beintema, N., Pérez, S., Flaherty, K., and Falconi, C. (2016). Investigación The use, distribution or reproduction in other forums is permitted, provided the Agropecuaria en Latinoamérica y el Caribe Un análisis de las instituciones, original author(s) and the copyright owner(s) are credited and that the original la inversión y las capacidades entre países. Washington, DC: Agricultural publication in this journal is cited, in accordance with accepted academic practice. Science and Technology Indicators (ASTI), International Food Policy Research No use, distribution or reproduction is permitted which does not comply with these Institute (IFPRI); The Inter-American Development Bank (IDB). terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 12808 January 2022 | Volume 5 | Article 741057 ORIGINAL RESEARCH published: 11 March 2022 doi: 10.3389/fsufs.2022.722522 Public Policies for the Development of a Sustainable Cattle Sector in Colombia, Argentina, and Costa Rica: A Comparative Analysis (2010–2020) Leonardo Moreno Lerma 1, Manuel Francisco Díaz Baca 2 and Stefan Burkart 2* 1 Independent Researcher, Cali, Colombia, 2 Alliance Bioversity International and CIAT, Cali, Colombia Projected food demand increases highlight the importance of Latin America as one of the big global future food suppliers, due to its agricultural potential, in particular regarding cattle farming. Despite the importance of the cattle sector for the region, its negative environmental impacts are numerous and the shift toward sustainability is perceived as slow and uncoordinated. This study aims at identifying successes and difficulties in the implementation of public policies for a sustainable cattle sector in Colombia, Argentina, Edited by: and Costa Rica. Based on the review of scientific articles, government reports, and Lars Otto Naess, Institute of Development Studies (IDS), publications of international organizations, a qualitative comparative analysis was carried United Kingdom out, documenting the political developments between 2010 and 2020. Our findings Reviewed by: suggest that public policies mainly focus on the reduction of greenhouse gas emissions Rosina Soler, Consejo Nacional de Investigaciones and the implementation of silvo-pastoral systems. Common successes exist among the Científicas y Técnicas three countries, e.g., a large number of public policies for promoting sustainable cattle (CONICET), Argentina farming or the inclusion of goals to reduce greenhouse gas emissions and implement Chrystian Camilo Sosa Arango, Pontificia Universidad Javeriana silvo-pastoral systems, but they also coincide in difficulties, e.g., disconnection between Cali, Colombia policies and the lack of continuity of development programs. The efforts made with *Correspondence: regional and national public policies, in addition to legislative advances, can be seen Stefan Burkart s.burkart@cgiar.org as initial steps in a long-term process toward sustainable cattle farming, and thus, recommendations are provided for increasing their success at different stages, from Specialty section: the identification of the problem to its evaluation, particularly in the face of financing This article was submitted to difficulties, disconnection among policies and initiatives, and participation of citizens and Climate-Smart Food Systems, a section of the journal livestock producers. Frontiers in Sustainable Food Systems Keywords: public policies, sustainable intensification, cattle, silvo-pastoral systems, climate change Received: 08 June 2021 Accepted: 11 February 2022 Published: 11 March 2022 INTRODUCTION Citation: Lerma LM, Díaz Baca MF and Framework of Reference Burkart S (2022) Public Policies for the Latin America and the Caribbean plays an essential role in the global cattle industry since it Development of a Sustainable Cattle contributes with more than 25% to the global beef and 10% to the global milk supply (CEPAL, Sector in Colombia, Argentina, and 2017). The cattle sector generates both external and internal benefits, as it supports both the region’s Costa Rica: A Comparative Analysis (2010–2020). and global food security and contributes to the economy of the countries, highlighting the need to Front. Sustain. Food Syst. 6:722522. increase the efforts to preserve the growth of the sector (Núñez et al., 2015). Cattle production doi: 10.3389/fsufs.2022.722522 in the region not only goes back a long way, but also appears to be facing a promising future. Frontiers in Sustainable Food Systems | www.frontiersin.org 1189 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle The Inter-American Development Bank (BID, 2018) projects y Ministerio de Agricultura de la República Dominicana, 2016; a growth in global meat production by 100% until 2050, Buitrago Guillen et al., 2018). Murgueitio et al. (2014) add that considering the global population growth—a scenario that the presence of trees and shrubs contributes to mitigating climate would favor Latin American cattle producers due to the change through mechanisms such as increased carbon deposits region’s geographical position, experience, and human and in the soil and lower nitrogen losses. They also state that the use natural resources. of silvo-pastoral systems can increase beef production levels by Despite the importance of the sector for the region and 12 and 4.5 times, compared to extensive grazing and improved its growth potential, the environmental effects of traditional pastures without trees, respectively, while methane emissions per or conventional cattle production systems are multiple and unit beef product are 1.8 times lower. include e.g., impacts on water sources, soil resources, a loss The implementation of such actions or innovations requires of biodiversity and greenhouse gas emissions (IDB, 2018). The the commitment of different actors along the beef and dairy principal greenhouse gases generated by the cattle sector are value chains, service providers (e.g., for credit, extension), and, methane (CH4), produced in the enteric fermentation process of above all, the support from the public sector. In this regard, cattle, carbon dioxide (CO2), resulting from land-use and land- this study differentiates between governmental policies and public use changes, and nitrous oxide (N2O), emitted during manure policies. Governmental policies are all the actions carried out by and slurry management (Rao et al., 2015). The cattle sector a government at different levels (e.g., national, departmental, or contributes significantly to global warming and climate change municipal) in response to social problems, without considering because of deforestation for feed and forage crops, degradation citizen participation. Public policies, although part of the of pastures and greenhouse gas emissions from cattle production previous ones, are more complex processes that involve a strong (Abbasi et al., 2015). intervention of the communities and involve four stages: (i) This has led to discussions about the transition from a identification of the problem, (ii) design of the policy, (iii) conventional to a sustainable cattle sector. A sustainable implementation, and (iv) evaluation (Arias and Herrera, 2012). cattle sector is characterized as economically viable for Yalmanov (2021) delves into this differentiation by pointing out farmers, respectful of the environment, and socially accepted that public policies cannot be reduced to a technical function (Varijakshapanicker et al., 2019). Related to this is the concept of governments, but rather are complex dynamics influenced of sustainable intensification, understood as an approach that by socio-political forces that alter both processes and results. uses innovations to strengthen agricultural productivity, while Likewise, it is necessary to consider the existence of individuals reducing the environmental footprint (e.g., greenhouse gas and groups that try to shape public policies in search of their emissions), promoting ecosystem services (e.g., soil quality particular interests, thus constituting a power struggle (Cochran improvements, reduced erosion, increased biodiversity) and and Malone, 2014). supporting social development of rural communities (Rao et al., To understand how governments support and manage such 2015).The challenge is to provide quality food for a growing processes, it is necessary to have an in-depth look at how they human population, while managing to reduce the negative have responded to social demands in the past, i.e., through environmental impacts caused by food production (Tedeschi the implementation of policies. This is precisely the objective et al., 2015). In this regard, sustainable intensification is not of this article: to identify successes and difficulties in the reduced to specific practices, but rather involves heterogeneous implementation of public policies for the development of a processes and therefore, its implementation requires adjusting to sustainable cattle sector in Colombia, Argentina, and Costa Rica the different agricultural systems and socioeconomic conditions between the years 2010–2020. The selection of these countries of the target populations (Xie et al., 2019). takes into consideration that they present different social and To achieve sustainable intensification, it is necessary to economic realities, which allows for a comparative analysis. The implement a broad set of different actions and innovations, such countries were also selected because of the strong efforts they as the use of environmentally responsible technologies, already made toward the transition to a sustainable cattle sector, the implementation of silvo-pastoral systems, or good evidenced by the existence of e.g., multi-actor platforms for animal husbandry practices, among others (Departamento sustainable cattle (in Colombia and Argentina) or the carbon- Administrativo Nacional de Estadística, 2015). Silvo-pastoral neutrality objective set by the Costa Rican government. It is systems are defined as the integrated use of grasses, legumes, worthwhile to answer the question why this study is justified. forage shrubs and trees in livestock production systems. There Primarily, because it adjusts to the reality of a global climate exist different types of them, which include e.g., trees in pastures crisis that requires concrete actions, such as public policies, (living fences, scattered trees, and forest area), protein banks and for both adaptation and mitigation. Likewise, the study is shrubs, or the integration of fruit and timber trees. The benefits justified to the extent that the evaluation of such policies of silvo-pastoral systems are diverse and range from productivity generates knowledge that can allow their reformulation in the increases (more forage biomass and higher nutritional quality), medium- and long-term, overcoming the difficulties identified animal welfare (e.g., reduced heat stress, better diet), income in pursuit of sustainability objectives. The study thus serves as a increases and diversification (e.g., more meat and milk, fruits reference document for various actors, such as national and local or timber), to environmental benefits such as better rainwater governments, cattle producers, and value chain actors, and helps capture, soil protection and recovery, biodiversity conservation, in the design, implementation, and evaluation of existing and and greenhouse gas emissions reductions, among others (IICA future policies. Frontiers in Sustainable Food Systems | www.frontiersin.org 1290 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle This article is structured as follows: Section Materials and deforestation hotspots), forests have almost disappeared in El Methods explains the methodological approach used; Section Salvador (Sanhueza and Antonissen, 2014). Results provides first insights into the successes and difficulties of Apart from the abovementioned implications of the cattle implementing policies in the three countries of analysis, namely sector on climate change and environmental degradation, climate Colombia, Argentina and Costa Rica; Section Comparative change itself is also affecting the cattle sector, resulting in a need Analysis and Discussion deals with the comparative analysis for climate change adaptation strategies and policies. Changes of the results among the three countries and a corresponding in the global climate affect the quality of water and animal discussion; in Section Conclusions the conclusions of this study feed, influence the physiological conditions of cattle, and lead to are presented; and Section Recommendations for Public Policy extreme climatic events (e.g., drought, flooding), among others, provides useful recommendations for a broad set of stakeholders. all contributing to variations in productivity and a reduction of areas suitable for cattle production. These ambivalent The Latin American Cattle Sector interactions between cattle farming and climate change, in The Latin American cattle sector currently faces a series of addition to environmental problems caused by other economic circumstances that determine its development and, consequently, sectors, have led the Latin American countries to adhere to the public policies that govern it. Among these, productivity environmental commitments, such as the Paris Agreement in increases to meet the growing demand for animal-source food, 2015. In general terms, the treaty seeks to control the future climate change and the search for environmental sustainability temperature increases, protect food production systems, and stand out (CEPAL, 2015; FAO, 2019). promote sustainable agricultural production systems (FAO, Regarding cattle production and productivity increases, beef 2019). The Latin American countries have also subscribed to production in the western hemisphere had a recent displacement the Sustainable Development Goals (SDG) promoted by the toward South America, resulting from a reduction in cattle United Nations, which contain 17 goals that aim at guaranteeing numbers and several years of droughts that affected both the prosperity at a global level. All goals set for the 2015–2030 period United States and almost all of the Central American countries, include components related to the livestock sector, in particular mainly El Salvador, Guatemala and Honduras, but also to a lesser sustainable cities and communities, responsible production and extent Nicaragua, Costa Rica and Panama. Between 2000 and consumption, climate action, and life in terrestrial ecosystems 2013, Latin America doubled its beef exports, with exemplary (ONU, 2021). cases such as Uruguay and Paraguay that exported almost It should be noted that, beyond the aforementioned factors, two-thirds of what was produced (CEPAL, 2015). However, the livestock sector in the region is complex and affected by this contrasts with the situation on Argentina over the same multiple elements. These range from the economic liberalization period, whose cattle sector was affected by the 2008 drought processes of the 1980s and 1990s that still lead to repercussions, and the sale of cattle in 2009, which caused a 44% drop such as job insecurity and the excessive use of natural resources in its beef exports (CEPAL, 2015), although with a notable (FAO, 2013; Rojas Villagra et al., 2015), to issues such as political recovery since 2015 (Cano, 2019). Although the United States uncertainty, foreign investments, production technologies and have managed to overcome the drought-related crisis and are animal diseases (CEPAL, 2017). now again an important competitor at the global level, beef production volumes are almost 70% higher in Latin America. For their part and despite the signing of free trade agreements, MATERIALS AND METHODS the competitiveness of countries in Central America are lagging behind due to a negative perception of their animal health and To address the proposed objective, we decided to write a review food safety systems (CEPAL, 2017). Brazil is the beef export article with a qualitative-descriptive approach. Literature review leader in the region, contributing 19.3% of the global beef trade was used as the main data collection technique. In the analysis (SAGARPA, 2018). The highlighted increases in beef production we related fragmented knowledge, contrasted different sources, and exports in Latin American countries has also led to a greater and updated the existing literature, aiming at clarifying the state co-responsibility for mitigating climate change. Regarding the of the art of public policies that have promoted the development adverse effects of cattle production on the environment, the fact of a sustainable cattle sector. We selected three Latin American that the region generates 30% of the greenhouse gas emissions of countries, namely Colombia, Argentina and Costa Rica and the global cattle sector stands out (FAO, 2019). This is further focused on the analysis of policies implemented during the years aggravated by the on-going deforestation, which, in addition 2010–2020. This selection corresponds to the efforts made by to contributing to generating greenhouse gas emissions, causes the countries to develop a sustainable cattle sector: all of them the extinction of hundreds of species of flora and fauna and have ratified the Paris Agreement and adopted the Sustainable the destruction of ecosystems. In Central America the situation Development Goals (SDGs), and both Colombia and Argentina is particularly worrying since the forest area had a reduction have implemented roundtables for sustainable cattle. For its part, of 40% between 1960 and 2000 (FAO, 2010). Regarding Latin Costa Rica has set out the goal of achieving carbon neutrality, America as a whole, the scenarios vary depending on the climatic, which stands out at the Latin American level. It is also noteworthy historical, political, and economic conditions of each country. that, despite the efforts mentioned, in the three countries the While in Brazil, for example, there still exist large forest areas agricultural sector is the main cause of GHG emissions (Banco in the Amazon (which at the same time is one of the global Mundial, 2014), which shows the importance of investigating Frontiers in Sustainable Food Systems | www.frontiersin.org 1391 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle their public policies to understand how they have faced both regions they are aimed at for respective national cattle sector of this and other environmental problems. Brazil is excluded from each country were selected. the study despite being the largest exporter of beef in the region (SAGARPA, 2018), since it still has excessively high figures RESULTS of deforestation and GHG emissions (Observatorio do Clima, 2020), which contrasts with the progress made by the three Colombia selected countries, where, despite room for improvement, a Context relatively favorable outlook is observed. This, however, does not Unliske many other Latin American countries and despite the state that Brazil does not have laws or public policies oriented internal armed conflict that lasted for more than 60 years, toward achieving sustainability of its cattle sector, but rather that Colombia has a relatively stable political and economic system. the study prioritized slightly more successful experiences that The first neoliberal reforms were presented in the 1980s and allow it to be a point of reference for other countries. consolidated in 1989 with the Washington Consensus, including Data collection was carried out from January to May 2021 elements such as a reduction of the role of the State in and prioritized three types of data sources: (A) Scientific articles, social intervention, privatizing public institutions and promoting which were especially used for defining concepts and theoretical private ownership and enterprises (Tejedor Estupiñán, 2012). principles regarding sustainable cattle, particularly but not With a more or less rigorous application of these principles, exclusively in the introduction. (B) Government reports and all national governments have since then followed the same other official documents, which include publications of national guideline, without making abrupt changes. It is within this and local governments, ministries, secretaries, congresses, and framework that the various economic sectors have developed, other public entities of the respective countries. National and including the agricultural and livestock sectors. local public policies were searched in these documents (including Regarding the cattle sector, its contribution to the national budget figures and intervened areas), and the legislation economy is highlighted by generating 1.1 million jobs, which is promoted in each of the contexts addressed. They were used equivalent to 6% of the national employment (Fedegán, 2021). in both the results and analysis sections. (C) Publications by With ∼35 million hectares, the sector uses most of the available international organizations, such as the Food and Agriculture land for agricultural purposes, most of it under extensive cattle Organization of the United Nations (FAO), the Economic ranching systems (Banco Mundial, 2019). In relation to this Commission for Latin America and the Caribbean (CEPAL), figure, the Rural Agricultural Planning Unit (UPRA, 2015) has and the Inter-American Institute for Cooperation on Agriculture stated that the sector exceeds the maximum amount of land use (IICA). Such sources were consulted to contrast the official by 15 million hectares, making it necessary to rethink the rural figures and positions of the countries, specifically in the analysis land use. Colombia is the 17th largest beef producer in the world section. Among the three categories, 115 sources were cited. and contributes with 1.2% of the global beef supply. Exports to With the aim of presenting a picture as complete as possible countries from the Middle East, Russia, and Vietnam, however, of each of the studied scenarios, the results considered five make up only 4% of the overall production volume while the factors, namely (i) the context, (ii) National Development Plans, rest is consumed domestically (Venugopal et al., 2021). Despite (iii) legislative advances, (iv) multi-sector initiatives, and (v) the occurrence of the COVID-19 pandemic and the fear of its regional policies. At the end of the section corresponding to implications on the sector, beef export figures showed a positive each country, a table-summary of successes and difficulties in development at the end of 2020, with 3,247 tons of beef exported the implementation of public policies is presented (Tables 2, 4, in September, exceeding the figures in the same months of 2019 6). These arise from the authors’ own interpretation, considering (1,681 tons) and 2018 (1,899 tons) (Fedegán, 2021). the five elements previously exposed, while at the same time To this extent, the public policies addressed are located in allowing the formulation of a set of recommendations for the a scenario where two characteristics stand out: (i) the stability development of the different stages of the policies (Table 7). of the political-economic model for more than three decades, Regarding the analysis, to evaluate the impact of the public and (ii) a cattle sector that, despite its limited international policies described in each of the three scenarios, figures related to importance, is fundamental at the national level in terms of job deforestation, GHG emissions and conservation of natural areas creation and food security. were consulted. Hernández et al. (2014) describe that in qualitative studies, National Development Plans the research process is holistic, since it is not reduced to the During the last decade, the different national governments analysis of the parts, but rather addresses the whole picture. of Colombia have indicated the importance of environmental This was especially important for the present study, as it sought protection as the basis of their policies. In this regard, the to understand how the set of policies have contributed to National Development Plan 2010–2014 stated that environmental the transition toward a sustainable cattle sector. Despite the sustainability should be a priority and an essential practice for qualitative focus of this research, the importance of quantitative the wellbeing and equity of future generations (DNP, 2011). For information was not neglected. In turn, it is necessary to point out the 2014–2018 period, this premise continued, emphasizingmore that, due to the breadth of identified policies and the complexity strongly the importance of protecting natural reserves, regulating of exposing them in their entirety, those with the greatest impact land use and preventing socio-environmental conflicts (DNP, in terms of budgets, intervened areas, and importance of the 2015). The current National Development Plan for the period Frontiers in Sustainable Food Systems | www.frontiersin.org 1492 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle FIGURE 1 | Actors involved in the design and execution of public policies in Colombia. 2018–2022 adds to that a long-term project perspective, which Multi-Sector Initiatives allows achieving the SDGs by 2030 (DNP, 2019). As a further effort to adapt to and mitigate the effects of climate change, multi-sector initiatives have emerged in Colombia, such Legislative Advances as the National Plan for Adaptation to Climate Change and the Although the legislative framework for the cattle sector is Colombian Strategy for Low Carbon Development (ECDBC). In very broad and involves elements such as animal welfare and the same sense, but focusing entirely on the cattle sector, the marketing there are three regulations that stand out in the Colombian Roundtable for Sustainable Cattle (MGS-Col, made period of analysis for their influence on the sector in terms up of one national and 12 regional roundtables, was established of sustainability: in 2014 and is an inter-institutional space where the public • Decree 870: Establishes the framework for payments for and private sectors, academy and NGOs converge with the aim ecosystem services, in addition to other incentives for of being a benchmark in the design and implementation of conservation (Presidencia de la República de Colombia, 2017). sustainable cattle programs and policies, capacity building in • Law 1876: Creates the National Agricultural Innovation rural areas, inter-institutional exchange and link with global System (SNIA) with the purpose of improving the productivity initiatives such as the Global Roundtable for Sustainable Beef and sustainability of the national agricultural sector (Congreso (GRSB) (Figure 1). Recently, the MGS-Col presented a technical de la República de Colombia, 2017). proposal for the formulation of a national level sustainable • Law 1931: Establishes guidelines for the management of cattle policy to the Ministry of Agriculture, which is now under climate change in the decisions of public and private entities revision. Among the objectives of this proposal is the promotion (Congreso de la República de Colombia, 2018). of the cattle sector from the green growth paradigm and the Frontiers in Sustainable Food Systems | www.frontiersin.org 1593 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle TABLE 1 | Overview on the objectives and geographical reach of the Departmental Agricultural Extension Plans (PDEA) in Colombia. Department Objectives related to sustainable cattle farming Source Antioquia - Increase productivity, competitiveness, and sustainability in coordination with rural actors Gobernación de Antioquia, 2020 Boyacá - Promote the development of productive systems aimed at the conservation and proper management of Gobernación de Boyacá, 2020 natural resources Casanare - Improve the competitiveness and sustainability of the sector Asamblea Departamental de - Strengthen the contribution to food security and the development of the agricultural producer as an integral Casanare, 2020 human being Cauca - Develop skills in producers to increase the knowledge base and support behavioral change with the aim of improving Gobernación del Cauca, 2020 competitiveness and sustainability Cesar - Strengthen the capacities of producers to make decisions about their agricultural production systems, so that they Gobernación del Cesar, 2020 can develop processes that respect the ecosystem Guainía - Improve cattle production facilities for associations in the department Gobernación del Guainía, 2019 - Complement and articulate actions through the project “Implementation of a comprehensive and fair rural extension plan” - Raise awareness about cattle regulations Santander - Encourage producers to use water resources efficiently and develop soil conservation practices Secretaría de Agricultura de Santander, 2020 Vichada - Increase the profitability of the cattle sector through genetic improvement, balanced nutrition and more and better Gobernación del Vichada, 2020 pastures - Reduce the negative environmental impacts of traditional cattle farming through the development of low carbon cattle systems and silvo-pastoral systems conservation of the environment and natural resources (Mesa de and the foothills of Magdalena Medio and the Orinoco, where Ganadería Sostenible Colombia, 2019). Likewise, it is pertinent pilots have been carried out on integrating live fences, forage to refer to the zero deforestation value chains initiative for beef hedges and mixed forage banks into the traditional livestock and dairy, which is part of the Zero Deforestation Agreements systems (Lozano, 2020; Colombia Sostenible, 2021). contemplated in the National Development Plan for 2018– Finally, as one of the Nationally Appropriate Mitigation 2022. The initiative, understood as a voluntary commitment Actions (NAMAs), the Colombian Sustainable Cattle NAMA to collective action among the public and private sectors, is being developed among a broad group of stakeholders. commits the involved entities to stopping cattle-farming-related This future policy will be focused on involving public-private deforestation and, at the same time, developing processes of sector participation, addressing the mitigation of climate change ecological restoration, such as the reestablishment of a degraded through the reduction of greenhouse gas emissions as well as areas, among others (Alianza Colombia TFA, 2021). an increase of carbon sequestration (Ministerio de Ambiente Another multi-sector initiative was the Sustainable Colombian y Desarrollo Sostenible, 2019). Its actions will impact 434 Cattle Project (GCS), executed from 2010 to 2019 and municipalities and 3.6 million hectares (Banco Mundial et al., financed by World Bank, the Global Environment Fund, 2021). the Government of the United Kingdom, which aimed at strengthening the Colombian cattle production through the Sub-national Regional Level Public Policies integration of environmentally friendly practices. Among the Parallel to the above-mentioned initiatives, there also exist specific objectives of this project were e.g., the transformation various public policies implemented at the regional level. Among of 35,500 hectares of traditional production systems into silvo- these, the Departmental Agricultural Extension Plans (PDEA) pastoral systems, the preservation of 15 hectares of native stand out, which, although they are still in the initial phase of forests, the development of payment schemes for ecosystem design and implementation, are macro level policies that define services, the creation of forage nurseries, and technical assistance the provision of agricultural extension at departmental level for 3,900 cattle farms to support sustainable intensification (Table 1). For the transition toward sustainable cattle systems, efforts (Ganadería Colombiana Sostenible, 2018). The Integral credit is needed. The Colombian government launched a credit Program for Productive and Environmental Reconversion of the line program for silvo-pastoral systems in 2020, which is being Cattle Sector (PIRPAG), whose objective is to support the implemented at a regional level (mainly in 82 municipalities) and transition of the national cattle sector toward sustainability seeks to promote sustainable practices, such as the conservation over a period of 30 years, is another example of multi-actor of biodiversity and the protection of water and soil resources, initiatives in Colombia. It focuses on the modification of in the different cattle regions of the country. The credits are traditional cattle landscapes into more productive systems that directed to the purchase and planting of tree species and the include environmental commitments, allowing for a reduction implementation of living fences, among others, and is the first and capture of greenhouse gas emissions. The initiative works in initiative in this regard (Ministerio de Agricultura y Desarrollo several selected regions, such as the humid and dry Caribbean Rural, 2020). Frontiers in Sustainable Food Systems | www.frontiersin.org 1694 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle National Level Public Policies TABLE 2 | Successes and difficulties in the implementation of public policies in In 2019, the 2018–2022 Agricultural and Rural Development Colombia. Policy: a field for equity was launched. This policy aims Successes Stability of the political-economic system for more than three at promoting agricultural competitiveness and productive decades transformation based on three pillars: (i) rural development, Continuity of the promotion of a sustainable cattle sector in the (ii) productivity + profitability = competitiveness, and (iii) National Development Plans modern and technical institutions. The sustainability component Existence of a national level Roundtable for Sustainable Cattle is in the second pillar and has the objective of positioning Strong progress in the formulation of a national level public policy the country as leading actor at international level, boosting on sustainable cattle employment, diversifying the productive offer, and encouraging Promotion of silvo-pastoral systems through on regional and environmentally responsible production practices. To achieve national policies this, farm planning, the establishment of silvo-pastoral systems, Existence of a credit line for the establishment of silvo-pastoral systems the division of pasture areas and the use of aqueducts that Difficulties The national public policy framework is still very young and at its prevent contamination of water sources by animals, are the early stages most prominent approaches. The National Conversion Strategy The Departmental Agricultural Extension Plans are still very young focuses on three main objectives: (i) technology (access and and at their early stages, and they also do not exist for all implementation), (ii) agricultural extension (in correspondence departments with relevance to the cattle sector with Law 1876 of 2017), and (iii) financial instruments. In Insufficient coordination between national and regional level public addition to these objectives, the policy aims at establishing a pilot policies cattle farm in each of the country’s cattle regions (Antioquia, Lack of clear budgets to carry out some of the policies, particularly Boyacá, Caquetá, Cauca, Humid Caribbean (Córdoba and from the National Development Plan and the Departmental Agricultural Extension Plans Sucre), Coffee Triangle and northern Valle del Cauca, Guajira, Different levels of acceptance of public policies by producers, Magdalena Medio, Nariño, Orinoquía (plains), Orinoquía many of whom relate sustainable cattle farming with the need for (flooded savannas), and Tolima-Huila), and at strengthening economic investment the 12 regional roundtables. Once the initial network has been completed, progress will be made so that in 2022, the implementation of silvo-pastoral systems on 75,000 ha in 25,000 properties will be achieved (Ministerio de Agricultura y 2015, Argentina has had two governments with opposing Desarrollo Rural, 2019). views, with clear tendencies toward the former development models: between 2015 and 2019, liberal policies adjusted to Successes and Difficulties in the Implementation of the requirements of the International Monetary Fund were Public Policies prioritized (Morresi and Vicente, 2019), while in 2019, the path From the reading and analysis of the aforementioned policies, that started in 2003 was resumed (Scaletta, 2020). it is possible to identify a set of successes and difficulties Regarding the cattle sector, a reactivation was sought in 2015 in their implementation (Table 2). Successes and difficulties with the lifting of various obstacles, such as export controls arise both from the political and economic context, as well as and interventions in the internal market (Patrouilleau et al., from the content of the policies and the relationship between 2017). According to recent figures, the Argentinian cattle herd them. The existence of macro policies stands out, such as the counts approximately 53 million heads (Secretaría de Gobierno National Development Plans and legislative advances, but also do de Agroindustria de la Nación, 2019). Despite the increase in beef regional programs with specific objectives, facilitating short-term sales on the international market, particularly to China, and the implementation, monitoring and evaluation. One of the main decline in domestic demand for beef due to high inflation and successes is the promotion of silvo-pastoral systems, which is lower wages, domestic consumption continues to be the basis strengthened by the creation of a specific credit line. Financial of the sector. Argentina has recovered its privileged position in resources are precisely one of the main problems since some the global beef market, occupying the fifth place in production policies show a lack of clarity on how to finance their objectives. and fourth in exports (Cano, 2019). The COVID-19 pandemic, although having effects on the sector, did not slow the growth Argentina rate significantly and by October 2020, 730,000 tons of beef had Context been exported (Villamil, 2020). An additional aspect to highlight In recent decades, the political, economic and social narratives is the expansion of the agricultural frontier, particularly resulting for development pathways of Argentina have been determined from plantations of monocultures such as soy. Their growth has by two clearly differentiable and opposed development models: displaced livestock, pushing it to less productive lands and into the first, established between 1990 and 2002, gave a fundamental forests (Pincén et al., 2010). role to foreign investment and was characterized by an outward- In summary, a context is revealed in which the changes in oriented economy; the second, between 2003 and 2015, appealed the political model and economic instability are elements of great to a state with greater regulation of markets, internal savings, influence on the cattle sector, despite the preservation of growth food production with social inclusion and strengthening of and export levels making Argentina one of the global leaders commercial ties at the regional level (Taraborrelli, 2017). Since for beef. Frontiers in Sustainable Food Systems | www.frontiersin.org 1795 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle National Development and Land-Use Management has more than 40 members committed to the development Plans of specific goals, such as proposing innovations in inputs The Participative Federal Agri-food and Agroindustry Strategic and services, anticipating the response to market trends, and Plan for 2010–2016 presented some of the challenges the promoting the improvement of the beef value chain (MACS, Argentinian cattle sector was facing, such as a water deficit and 2021). Another multi-sector initiative is Carne del Pastizal, drought in 2008, which obliged cattle farmers to sell their animals which has the objective to stimulate cattle production based earlier than planned (lack of feed and water) and led to lower calf on practices that respect biodiversity, in addition to generating birth rates in 2009, among others. To counteract these problems, positive impacts in economic and social terms. One of its main the plan proposed that by 2015 all national policies should achievements was the export of certified grass-fed beef to Europe integrate the principles of sustainable development and thus (INTA, 2014). At this point, it is worth mentioning that there reverse the loss of natural resources (Ministerio de Agricultura exists no policy for the cattle sector yet that properly responds Ganadería y Pesca, 2010). For its part, the Territorial Strategic to the NAMA concept, although (see subchapters below) there Plan (PET), launched in 2011, recognized the cattle sector as are various actions aimed at reducing the sector’s greenhouse cause of desertification, particularly through pasture overgrazing. gas emissions according to the NDCs defined at the COP21 in Although the plan did not delve into the cattle sector, it proposed Paris in 2015 (Centro Agronómico Tropical de Investigación y that all citizens need to achieve environmental sustainability and Enseñanza, 2019). included the promotion of a sustainable productive development in the guidelines for territorial and land-use planning in rural Sub-national Regional Level Public Policies areas (Ministerio de Planificación Federal Inversión Pública y Regarding the traditional cattle provinces in Argentina, it Servicios, 2011). The National Policy and Strategy for Territorial is necessary to refer to four important policies (Table 3). Development and Planning, launched in 2016, defined the In these, the importance of protecting grasslands, good achievement of an environmentally sustainable society as the animal husbandry practices, and sustainable grazing stand out. main objective, for which it proposed a series of strategies, such Likewise, the policies consider the quality of life of ranchers as improving knowledge about natural resources and including and productivity, jointly exposing a sustainability project the environmental dimension as a transversal axis in public in which economic benefits and environmental guarantees territorial policies and actions at the federal, provincial and local are integrated. levels (Ministerio de Planificación Federal Inversión Pública y Servicios, 2016). National Level Public Policies With the aim of finding solutions to make forests profitable for Legislative Advances their owners and, at the same time, provide goods and services Although there are several laws that directly and indirectly to the society, the National Management Plan for Forests with influence the Argentinian cattle sector and its sustainable Integrated Cattle (MBGI) was launched in 2015, responding to development, three stand out in this regard: Law 26.331 of 2007 and promoting the design and monitoring of forests with integrated cattle, as well as the implementation • Law 26.331, Minimum Budgets for Environmental Protection of of silvo-pastoral systems (Presidencia de la Nación Argentina, Native Forests: promotes the sustainable management of forest 2018). As pointed out by Borrás et al. (2017), the plan is an reserves, in addition to creating the National Fund for the agreement that seeks to articulate national, provincial, productive Enrichment and Conservation of Native Forests (Congreso de and conservation public policies. The National Program on la Nación Argentina, 2007). Natural Resources, Environmental Management and Eco-regions • Law 27.066. Regime for the Promotion of Cattle Production (PNNAT), developed in 2015, aims at contributing to the in Arid and Semi-arid Zones: aims at increasing the supply protection of the environment in the agricultural sector through of bovine livestock (by-)products, which follow the principle a progressive improvement of sustainability in rural areas and of environmental balance (Congreso de la Nación Argentina, production systems. Regarding cattle, two projects of the plan 2014). focus on the measurement of greenhouse gas emissions and • Law 27.520. Law of Minimum Budgets for Adaptation to wastewater treatment, through which it is intended to contribute and Mitigation of the Global Climate Change: establishes to both prevention and environmental remediation based on strategies that allow guaranteeing human and environmental methodological tools for diagnosis and evaluation, technology development. Article 24, in particular, refers to practices to development, among other measures (INTA, 2017). As one of mitigate climate change linked to the agricultural and livestock the most important public policy instruments at the national sector (Congreso de la Nación Argentina, 2019). level, Rural Change II, Innovation, and Investment (CRII) stands out. The program emerged in 1993 but was relaunched in Multi-Sector Initiatives 2013 with the objective to support the association of small One of the principal multi-sector initiatives is the Argentine and medium-sized enterprises, agri-food, and agroindustry Sustainable Beef Board (MACS), an association of public and to strengthen the sector. For smallholder cattle producers, private entities, NGOs, academia, and other organizations (e.g., which are the main group of beneficiaries of the initiative, input and service providers), with the aim of promoting an improvement plan instrument was developed that contains sustainability policies for the cattle sector (Figure 2). It currently an environmental sustainability component, in which aspects Frontiers in Sustainable Food Systems | www.frontiersin.org 1896 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle FIGURE 2 | Actors involved in the design and execution of public policies in Argentina. TABLE 3 | Overview on the provincial cattle plans of Argentina. Province Objectives related to sustainable cattle farming Source Buenos Aires, Pastures and Savannas of the Southern Cone of South America: initiatives for their conservation in Miñarro and Marino, 2013 Corrientes, Entre Ríos, Argentina (2010): and Santa Fe - To promote sustainable cattle ranching in grasslands by integrating environmental conservation practices into agricultural production. Santa Fé Santafesino Cattle Plan (2018): Ministerio de Producción Ciencia - Launched with the purpose of generating suitable conditions for the growth of cattle production and the y Tecnología, 2018 adoption of good animal husbandry practices. - Overarching purpose of guaranteeing the quality of life of the Santa Fé citizens and the sustainability of the sector. Entre Ríos Enterriano Cattle Plan (2020): Ministerio de Producción - Beef differentiation and certification. Turismo y Desarrollo Económico, - Implementation of good animal husbandry practices. 2020; Secretaría de Agricultura y Ganadería, 2020 Neuquén Plan Ganadero Bovino Provincial (2021): Gobernación de Neuquén, 2021 - Implementation of technologies in the management of grasslands and water. - Development and dissemination of sustainable grazing techniques. - Improvement of the meadow productivity. - Strengthening the adaptability to environmental changes. Frontiers in Sustainable Food Systems | www.frontiersin.org 197 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle TABLE 4 | Successes and difficulties in the implementation of public policies in by low inflation and stable exchange rates, as well as an Argentina. internationally competitive export sector. However, there are lags in infrastructure, which affect the different productive sectors Successes National Development Plan with an environmental sustainability component and, particularly, green economy efforts (Gobierno de Costa Rica, Existence of laws that promote forest protection, environmental 2019). balance, and climate change mitigation strategies The Costa Rican cattle sector is present all over the country, Development of multi-sector initiatives that promote sustainable with major concentration in the regions Huetar Norte (34%), beef production Chorotega (22%) and Central (15%), while Brunca (12 %), Existence of the Argentine Sustainable Beef Board the Caribbean (9%), and the Central Pacific (8%) regions are National public policies articulated with the provinces less important (Ministerio de Agricultura y Ganadería, 2019). Regional policies that promote the adoption of silvo-pastoral The cattle sector generates annual profits of close to US$ 1.5 systems and good animal husbandry practices billion and involves 500,000 people, highlighting its social and Difficulties Environmental conditions that affected and still affect the cattle economic importance (Ministerio de Agricultura y Ganadería, sector 2017). According to the National Institute of Statistics and High political instability that has led to changes in the development Censuses (INEC, 2020), the country’s cattle herd counts with model ∼1,600,000 animals, out of which 15.4% correspond to dairy Increased inflation and unstable exchange rate cattle, 62.7% to beef cattle, 21.7% to dual-purpose cattle and 0.2% Decrease in wages and reduction in national beef consumption to cattle used for farm work. In terms of beef exports, China and Unequal implementation of the MGBI in the provinces the United States are the most important buyers. In 2019, China imported 14,014 tons of beef with a value of US$ 56.72 million, representing 57% of Costa Rica’s beef export volume (Barquero, such as the use of agrochemicals and good water management 2020). The United States bought 23% of the beef export volume are included (Ministerio de Agricultura Ganadería y Pesca, in the same year for a value of US$ 26.5 million (Procomer, 2013). 2020). It is important tomention that the livestock sector remains stable despite the crisis generated by the COVID-19 pandemic, Successes and Difficulties in the Implementation of which is due to factors such as the productive system, local Public Policies consumption, and the use of national productive inputs (Garza, As highlighted in Table 4, the aforementioned policies present 2020). both individually and collectively a diversity of successes. Consequently, the sector operates in a stable political and The presence of a sustainable beef board, as well as the economic situation, which has allowed its development and inclusion of an environmental component in the National the opening of important international markets. However, Development Plan and legislative advances, configure a context Costa Rica has not yet established itself as a fundamental for the development of the cattle sector in accordance with actor on the global beef market, generating contributions international treaties. The policies implemented at the regional mainly at the national level in terms of employment and level are contributing significantly to achieving sustainability food security. of the sector, since they set specific objectives and focus on results. Nevertheless, there also exist some difficulties, which mainly respond to conjunctural factors, such as inflation, National Development Plans unemployment, and the reduction of consumption, which are The 2011–2014 National Development Plan sets out largely dependent on the national government in power and environmental protection as one of its main objectives. can vary positively or negatively in the medium- and long-term, It suggests the incorporation of fundamental elements of making it difficult to determine how they will affect the cattle sustainable development into the national policies and the sector. Faced with this uncertain panorama, the international reversion of natural resource degradation, while promoting an treaties signed, and the legislation developed to date become economy with minimum levels of greenhouse gas emissions in more relevant, guaranteeing that the sustainability of the sector search of carbon neutrality by 2021 (Ministerio de Planificación can be preserved. Nacional y Política Económica, 2010). This last goal is reiterated in the 2015–2018 National Development Plan, as well as the Costa Rica need for climate change mitigation and adaptation actions of Context the agricultural sector (Ministerio de Planificación Nacional y Costa Rica has shown continuous economic progress over the Política Económica, 2014). For the period of 2019–2022, these last 25 years because of opening up to foreign investments precepts are continued by proposing specific measures, such and trade liberalization. The balance between political stability as interventions on cattle farms applying the NAMA model and sustained growth is reflected in human development and the strengthening of the capacities of micro-producers indicators and one of the lowest poverty rates in Latin America through silvo-pastoral system and agroforestry models (Banco Mundial, 2021). Costa Rica’s economy has focused (Ministerio de Planificación Nacional y Política Económica, on the export of goods and services and is characterized 2019). Frontiers in Sustainable Food Systems | www.frontiersin.org 1908 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle FIGURE 3 | Actors involved in the design and execution of public policies in Costa Rica. Legislative Advances Multi-Sector Initiatives The regulations regarding environmental sustainability are very In connection with the previously described policies, the Costa broad in Costa Rica, but there exist two important decrees with Rican Cattle NAMA stands out as an example for multi- direct effects on the cattle sector1: sector initiatives (Figure 3). The strategy was developed in 2013 and aims at transitioning the cattle sector toward productive • Executive Decree 37.017: authorizes the use of cattle slurry efficiency, adaptation to climate change and greenhouse gas to improve the chemical, physical and microbiological emission reductions. The mitigation potential of the NAMA is characteristics of the soil (Presidencia de la República de Costa understood from the promoted practices, being mainly increased Rica, 2012). forest cover, rational grazing, living fences and improvement of • Executive Decree 39,482: declares theNational Strategy for Low pastures and fertilization (Ministerio de Agricultura y Ganadería, Carbon Cattle (ENGBC) 2015-2034 as of public interest, taking 2019). In turn, the NAMA is expected to improve the quality of into consideration the objective of becoming a carbon-neutral life and income of ranchers, while raising consumer awareness country (Presidencia de la República de Costa Rica, 2012). of the need to reduce GHG emissions from the cattle sector (UNFCCC, 2014). 1Although there exist other regulations that stimulate sustainable cattle farming Sub-national Regional Level Public Policies in the country, they are not cited because they were launched prior to 2010. The In 2015, the design of Regional Livestock Development Plans present study covers developments between 2010 and 2020. Law 7837 of 1998 (Law for the Creation of the Cattle Corporation), Law 8408 of 2004 (Program for the started, which respond to local problems, but conform to the Promotion of Sustainable Agricultural Production), among others, stand out. national purpose of carbon neutral cattle production. These plans Frontiers in Sustainable Food Systems | www.frontiersin.org 1919 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle TABLE 5 | Regional level development objectives for a sustainable Costa Rican cattle sector. Region Objectives Source Central Oriental - Development of sustainable cattle practices for the conservation of natural resources Ministerio de Agricultura y Ganadería, 2019 Central Sur - Implementation of technical assistance programs Ministerio de Agricultura y Ganadería, 2019 - Promotion of climate change mitigation and adaptation practices on cattle farms Central Occidental - Consolidation of the payments for ecosystem services program for individuals or entities that Dirección Regional Central Occidental, 2015 promote silvo-pastoral systems Huetar Norte - Promotion of ecosystem service programs Ministerio de Agricultura y Ganadería, 2019 - Establishment of silvo-pastoral systems and agroforestry for adaptation to climate change - Enabling the access to environmentally friendly technologies at primary producer level Brunca - Promotion of actions to adapt production processes to climate change Comité Sectorial Regional Agropecuario, 2015 are being carried out in Central Oriental, Central Sur, Central TABLE 6 | Successes and difficulties in the implementation of public policies in Occidental, Brunca and Huetar Norte, while Chorotega, as well Costa Rica. as the Central Pacific and the Caribbean regions show delays Successes Political stability for several decades (Table 5). Low inflation and stable exchange rates National Development Plans include sustainable production components National Level Public Policies Diversity of national and regional public policies framed in the In addition to the aforementioned initiatives, Costa Rica started objective of carbon neutrality the National Strategy for Low Carbon Cattle 2015–2034, which, Regional Livestock Development Plans with focus on environmental sustainability among others, proposes the promotion of cattle production in Promotion of silvo-pastoral systems through both national and areas with less exposure to climate vulnerability, an increase regional policies the establishment of silvo-pastoral systems, and a set of low- Existence of payment schemes for ecosystem services and carbon technologies, which e.g., includes living fences, improved agroforestry programs pastures, forage banks, rational grazing and the moderate use Difficulties Absence of a sustainable cattle roundtable or any similar initiative of slurry (Ministerio de Agricultura y Ganadería, 2019). These Postponement of the carbon neutrality objective purposes continue with theNational Decarbonization Plan 2018– 2050, whose ninth axis2 exposes the importance of consolidating the eco-competitive cattle productionmodel based on productive efficiency and the reduction of greenhouse gas emissions Successes and Difficulties in the Implementation of (Gobierno de Costa Rica, 2018). The Costa Rican Policy for the Public Policies Agri-Food Sector and Rural Development 2010–2021 incorporates As shown in Table 6, the political and economic stability of climate change and agri-environmental management as one of Costa Rica, in addition to the commitments acquired through its four pillars. It also refers to the need of promoting sustainable the Paris Agreement and the 2015–2030 SDGs, has allowed production systems through an ecosystem approach, for which continuity to a set of governmental initiatives focused on payment schemes for ecosystem services were adopted as an sustainable production models. The commitment to achieve instrument (Ministerio de Agricultura y Ganadería, 2011). The carbon neutrality is also reiterative, which is promoted at both Policy for the Agricultural Sector and the Development of Rural the national and regional levels. However, the absence of a Territories 2015–2018 emphasizes on some mitigation strategies, sustainable cattle roundtable or any similar initiative stands out such as economic incentives for producers that contribute to the as an important bottleneck, despite its potential to contribute reduction of greenhouse gas emissions or the promotion of silvo- to the articulation of public policies, information exchange and pastoral systems (Secretaría Ejecutiva de Planificación Sectorial validation, and the promotion of new practices and technologies. Agropecuaria, 2015). COMPARATIVE ANALYSIS AND DISCUSSION 2The 10 axes of the National Decarbonization Plan 2018–2015 are: (1) Development of an efficient and renewable mobility system. (2) Conversion From the elements raised, it is possible to identify relationships of the vehicle fleet to zero emissions. (3) Boosting cargo transportation with between the studied countries Colombia, Argentina, and Costa zero emissions. (4) Consolidation of a national electricity system of renewable Rica. To this extent, macro and micro aspects are highlighted energy. (5) Promotion of buildings with low emissions. (6) Modernization of that allow understanding the public policies developed, while the industry. (7) Promotion of a waste management system. (8) Development of evaluating their impacts through e.g., figures on deforestation efficient agri-food systems. (9) Promotion of an eco-competitive livestock model. (10). Promotion of a territorial management model that allows the protection or greenhouse gas emissions, among other indicators, taking of biodiversity. into consideration an international scenario from which Frontiers in Sustainable Food Systems | www.frontiersin.org 21020 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle environmental sustainability strategies are formulated and results The situation in Colombia, however, has not been so favorable, from the individual governments are demanded. since for many years, there was no public policy that coordinated local sustainability efforts, and thus, they rather developed Explanatory Factors of Public Policies independently and in a disorderly manner. As has been outlined, public policies involve a set of stages These macro-level factors, which are related to the actions of that go from the identification of the problem to the evaluation governments and institutions, converge with the way in which of the implemented actions. Macro-level factors intervene in producers perceive the public policies that seek to integrate them. this process, such as the political will of the state institutions, In relation to silvo-pastoral systems, Braun et al. (2016) describe understood as an ideological commitment to respond to the their numerous advantages, but also warn of their disadvantages demands of citizens (Goldfrank, 2006), the articulation among and, consequently, occurring preventions of producers toward the involved actors or the continuity and linkage of the programs. the implementation of related policies. Some of these difficulties At the same time, micro-level factors related to the perception refer to the lack of familiarity with the new strategies, in addition of the unions, associations and producers about sustainability to the need for higher initial investments and a certain level of strategies become relevant. To understand the policies outlined complexity compared to traditional cattle farming systems. The in this document, it is necessary to delve into both aspects. Ministry of Agriculture and Livestock of Costa Rica (Ministerio At the macro-level, the National Development Plans and de Agricultura y Ganadería, 2019) reaffirms these arguments, legislative advances of the three countries show a willingness adding that new technologies including silvo-pastoral systems, of state institutions to promote a sustainable cattle sector. This face a conservative attitude by the producers, which is due circumstance is expressed in their National Development Plans to risk aversion, minimal interest in on-farm investments, and and legislative advances. The strategies proposed by all are quite a lack of available information. In the studied scenarios and similar, focusing on the need to reverse the loss of natural countries, micro-factors are present to a stronger or lesser extent, resources, reduce greenhouse gas emissions, stop deforestation, with the common denominator of difficulties in financing and and promote the use of silvo-pastoral systems. Although these training for change, which leads producers to perpetuate their documents usually contain general lines regarding the problems, traditional practices. The continuation of the public policies often without being expressed in tangible indicators or results, developed in Costa Rica and Argentina, however, suggests a it is necessary to recognize that they have also been the gradual overcoming of these barriers, while they are still more starting point for large-scale initiatives. In relation to this, the present in Colombia. carbon-neutrality objective proposed by Costa Rica stands out, The convergence of macro- and micro-level factors has a commitment that has made the country an international made the implementation of public policies a complex process benchmark for sustainability. The political will of the three in different regards, which highlights the importance of countries is also expressed by the existence of national and strengthening collaborative actions among state institutions, regional multi-sector initiatives. In this regard, the capacity for private sector, and other organizations, since this helps articulation among the actors stands out, linking public, private, overcoming the fears producers have regarding sustainability- academic, and various other entities to achieve a common goal— related policies. the sustainability of the cattle sector and value chains. This aspect is fundamental since it responds to the very concept of public From International Requirements to policy where decisions are not made by a top-down decision National Results but are the result of collaborative efforts. It should be noted There exist various high-level environmental commitments that that the Roundtable for Sustainable Cattle in Colombia and the involve Colombia, Argentina, and Costa Rica, such as the Paris Argentine Sustainable Beef Board have had a preponderant role Agreement and the SDGs 2015–2030. These agreements are in the processes, since they are considered as important pools mechanisms of the international community to put pressure of national and international actors with different institutional on national governments to regulate their production systems, backgrounds. Both institutions support the sharing of feedback beyond political or economic interests. This is how the adhesion and experiences made by their members with sustainable cattle of the countries to these initiatives, although voluntary, is not practices. In the case of Colombia, its main contribution has precisely due to a genuine interest, but to an imperative to which been the creation of a base document for the formulation of a it is necessary to respond. To understand how the analyzed National Public Policy on Sustainable Cattle, which is currently countries have acted in the face of such international demands under review by the Ministry of Agriculture and would not have by developing and adjusting their public policies and, at the been developed without the initiative of the Roundtable. same time, analyze their impact, it is important to consider Regarding the continuity and association of the programs, some figures. In this regard, reference is made to factors such disparate circumstances are evident. In the case of Costa Rica, the as forest cover, deforestation, and GHG emissions, which offers carbon-neutrality objective has been preserved by the different an overview of the current situation in terms of sustainability governments and National Development Plans, as well as in advances.3 the multi-sector and regional initiatives, such as the Cattle NAMA. In Argentina, although not as well as defined as in 3It should be noted that comparisons between countries are not exact due to Costa Rica, national policies have managed to articulate with the the availability of data, which may vary over time or by the way in which they provinces, i.e., regarding the adoption of silvo-pastoral systems. are disaggregated. Frontiers in Sustainable Food Systems | www.frontiersin.org 21031 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle Argentina currently counts with 53,654,545 hectares of native and 2016, however, the country’s forest cover has increased forest (Ministerio de Ambiente y Desarrollo Sostenible de permanently, going from 46.53 to 54.56% in this period (OCDE, Colombia, 2021). As indicated by the Dirección Nacional de 2020). There are also notable advances related to the payment Bosques (2021), however, the loss of forest land for 2020 was of ecosystem services, which between 2010 and 2020 supported 333,222 hectares, a rather worrying figure, and 27.8% of this the protection of 585,945 hectares of forest land (FONAFIFO, deforestation corresponds to agriculture and livestock sector 2021). (only surpassed by fires, with 57.3%). According to the latest Consequently, the elements exposed for the three countries National Inventory of Greenhouse Gases, the country’s total configure a mixture of successes, difficulties, and contrasts. In emissions for 2016 were 364 million tons of CO2, of which 21.6% the first place, it should be noted that external demands must be correspond to the livestock sector (Secretaría de Ambiente y understood in positive terms, since they allow the development Desarrollo Sustentable, 2019). of strategies that would not be carried out spontaneously. In Colombia, the achievements in terms of environmental In other words, the importance of international organizations sustainability are mixed. For the 2018–2022 period, the national and treaties is recognized in a role of oversight of national government intends to implement 150,000 hectares of silvo- governments so that they respond, through public policies and pastoral systems, agroforestry systems, productive reconversion, legislative advances, to the demands and problems of their and fish farming (DNP, 2019), a low figure when compared citizens. Likewise, it is important to recognize that international to other countries. It has also set the goal of planting 180 organizations not only exercise a controlling role over national million trees by the end of the period, an initiative to which governments, but also promote financing mechanisms for the departmental governments have adhered (Ministerio de the benefit of developing countries. Deforestation and GHG Ambiente y Desarrollo Sostenible de Argentina, 2021). Beyond emissions continue to be a common problem in the three these objectives, which will have to be evaluated in due course, countries, although with more worrying figures in Colombia and recent figures are worrying: By 2020, according to official figures, Argentina. This highlights that those public policies that aremore the country generated approximately 298 million tons of CO2 closely coordinated with each other and implemented over a across all economic sectors (Gobierno de Colombia, 2021). long-term period are reflected in more encouraging processes Likewise, deforestation affected 2.8 million and 159,000 hectares and impacts, such as in Costa Rica. of forest land from 2000 to 2019 and in 2020, respectively (CONPES, 2020). Although the causes of this phenomenon are multiple, including the exploitation of timber, the construction CONCLUSIONS of roads, illicit crops, among others, extensive cattle farming has a share of this responsibility, and as Kaimowitz (2019) points out, The sustainable development of the cattle sector is an largely explains the destruction of ecosystems both in Colombia unquestionable need. International demands, in addition to and in the rest of Latin America. The author also states that the role of different actors, deny any possibility of continuing cattle farming is a placeholder for guaranteeing land possession, with traditional production practices. This scenario commits which is much more lucrative than the production of beef or the national governments to take forceful actions, which are milk. This scenario is worrisome, since if sustainability initiatives not always reflected in the same ways, since each country has in many cases have little effects on real cattle farmers, much particularities that determine the processes and, therefore, the less will they have effects if cattle farming is not the main results. Colombia, Argentina, and Costa Rica demonstrate such activity. Another factor that needs to be taken into consideration contrasts, and understanding their public policies implies going is the Peace Agreement signed between the Colombian State beyond the figures, taking into consideration their social and and the Revolutionary Armed Forces of Colombia (FARC) economic conditions. in 2016, with the aim of ending the internal armed conflict To this extent and although the three countries express a that lasted for over 60 years. Contrary to what might be political will to promote sustainable cattle practices, they are at expected, the Peace Agreement intensified the already existing different stages. This does not mean, however, that the realities environmental problems, including deforestation, since the State are completely opposite to each other. On the contrary, the has not taken control of the territories abandoned by the general perception is relatively similar insofar as they are all in guerrilla, and reconfigured the relationships between the actors a process of evolution and still have many objectives to achieve who dispute the land (e.g., landowners, peasants, illegal armed in the framework of the commitments made at the COP21 in groups) (Armenteras, 2019). Paris in 2015 and with the SDGs 2015–2030. Even though the Costa Rica exhibits both a stable political system and results achieved so far are not fully satisfactory, the implemented significant progress in terms of sustainability: Between 2011 policies should not be abandoned, but rather persist and be and 2016, CO2 emissions were ∼7 million tons per year expressed in tangible effects. It is necessary to strengthen both (Gobierno de Costa Rica, 2020) and in 2018 11.7 million the articulation between the initiatives and their actors, while tons (RAND Corporation, 2020), very low figures compared overcoming the fears producers to adhere to the transition to Colombia and Argentina. For its part, it should be noted process toward sustainability. that deforestation continues to be a major problem, mainly It is important to point out that the public policies analyzed linked to the cattle sector, an activity that occupies a large in this document have positive impacts in at least two senses. part of the affected areas (MINAE et al., 2018). Between 2000 In the first place, their contributions to the environment Frontiers in Sustainable Food Systems | www.frontiersin.org 21042 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle TABLE 7 | Recommendations for the design and implementation of public RECOMMENDATIONS FOR PUBLIC policies. POLICY Stage Recommendations We recommend that for all the evaluated countries, public (1) Financing - Promote taxes for the responsible entities/individuals of GHG policies should be developed that contain clear objectives emissions or deforestation and budgets, facilitating their development, application, and - Strengthen payment systems for ecosystem services evaluation. The national extension systems and technical - Involve the private sector in public initiatives and projects assistance programs need to be strengthened to provide (2) Identification of - Update the figures on deforestation, GHG emissions, and the involved actors (i.e., cattle producers) with required the problem other environmental indicators to identify the most affected information and knowledge and stimulate the transition toward territories sustainable cattle farming. For Argentina, we recommend - Develop spaces for dialogue with communities and producers to hear their opinions the state institutions to increase their efforts regarding - Evaluate previous public policies to identify successes and deforestation policies, mainly for the Gran Chaco region. difficulties and thus determine aspects for continuance or Colombia should formulate more ambitious objectives in reformulation terms of the implementation of silvo-pastoral systems, and in (3) Design - Articulate local public policies with regional and national Costa Rica actions of national and international institutions policies should be articulated with the objective of establishing a multi- - Socialize the policies with the different actors (producers, sector platform for sustainable cattle (like the Roundtable for communities, and others) Sustainable Cattle in Colombia or the Argentine Sustainable - Prioritize sustainability goals over private interests Beef Board). Such platforms stimulate sharing the different (4) Implementation - Involve communities in projects experiences made within the sector and thus help in both their - Strengthen technical training plans for producers achievement and in coordinating common objectives at the - Support producers in the development of infrastructure national level. Likewise, we recommend that in Colombia, (5) Evaluation - Create digital platforms where citizens know budgets, objectives, and other characteristics of the initiatives the advances made with the Colombian Roundtable for - Periodically evaluate the set objectives (promoted by the Sustainable Cattle should continue, since they allow for the governments, but with citizen participation) consolidation of efforts and, in the future, the monitoring of the - Publish final reports comparing objectives and results National Public Policy of Sustainable Cattle. For all countries, we recommend the consolidation of using technological innovations that contribute to the monitoring of deforestation. stand out, fostering the protection of natural resources for Finally, communication channels should be established between present and future generations. These include, for example, the the studied (and other Latin American) countries that support implementation of a significant number of silvo-pastoral and knowledge exchange, mutual learning and the sharing of agroforestry systems in Colombia, the conservation of forests successes and difficulties in the implementation of public in Argentina, or the advances in carbon neutrality in Costa policies related to the sustainable intensification of the cattle Rica. Second, they lead to the benefits for the cattle sector, sector. Table 7 proposes more specific recommendations for making it essential that producers understand that they favor the three countries, considering the difficulties identified themselves when implementing the strategies. This is because (Tables 2, 4, 6) in our study. Common problems are highlighted, environmentally responsible measures prevent problems such as such as the lack of economic resources to develop public climate change and land degradation, phenomena with direct policies and enforce laws, for which some financing options impacts on cattle production. In the short term, the attitude are proposed. Likewise, the importance of promoting citizen of certain international markets reluctant to buy beef and participation in each of the stages of the policies is highlighted, dairy products from deforestation areas stands out: sustainable achieving not only that the objectives are consistent with practices can capture new buyers and contribute to the economic the needs of the territories and communities, but also that profitability of the sector at a time when socially responsible the processes carry out an adequate management of public consumption is gaining strength worldwide, meaning that resources. It should be noted that, while the differences between consumer choices are being made increasingly by considering the three countries are recognized, such recommendations environmental and social repercussions products and services fit all of them, whether in the national context or in local might involve (Izquierdo et al., 2018). settings. In turn, due to the economic, cultural, and political Finally, it is emphasized that although the policies achieved similarities in Latin America, the points made are relevant at the so far provide valuable contributions, it is necessary to assume regional level. them as a first stage in a long-term process. As such, it is critical to support their continuity and increase their scalability, to achieve the goal of a wider adoption of sustainable production DATA AVAILABILITY STATEMENT alternatives, such as silvo-pastoral systems. This process implies the contribution of all actors, from international organizations The original contributions presented in the study are included to public entities, cattle producers, unions and associations, the in the article/supplementary material, further inquiries can be private sector, academia, and society. directed to the corresponding author. Frontiers in Sustainable Food Systems | www.frontiersin.org 21053 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle AUTHOR CONTRIBUTIONS the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. LL, MD, and SB: conceptualization, methodology, writing the original draft and review and editing, and resources. LL and MD: ACKNOWLEDGMENTS formal analysis. SB andMD: supervision. SB: funding acquisition and project administration. All authors contributed to the article We thank all donors who globally support our work through and approved the submitted version. their contributions to the CGIAR System. The views expressed in this document may not be taken as the official views of FUNDING these organizations. CGIAR is a global research partnership for a food-secure future. Its science is carried out by 15 Research This work was funded by the CGIAR Research Program on Centers in close collaboration with hundreds of partners across Livestock. The funders had no role in the design of the study; in the globe. REFERENCES la región de América Latina y el Caribe. Available online at: https://bit.ly/3485DUr Abbasi, T., Abbasi, T., and Abbasi, S. A. (2015). Reducing the global CEPAL, FAO, and IICA (2015). Perspectivas de la agricultura y del desarrollo rural environmental impact of livestock production: the minilivestock en las Américas: una mirada hacia América Latina y el Caribe 2015-2016. San option. J. Clean. Prod. 112, 1754–1766. doi: 10.1016/j.jclepro.2015. José: IICA, 213. Available online at: https://bit.ly/33wPzy,M 02.094 CEPAL, FAO, and IICA (2017). Perspectivas de la agricultura y del desarrollo rural Alianza Colombia TFA (2021). Cero deforestación en Colombia: ABC de las cadenas en las Américas: una mirada hacia América Latina y el Caribe. San José: IICA, cero deforestación de palma, cacao, carne y leche en Colombia. Bogotá. Available 267. Available online at: https://n9.cl/pyzh online at: https://bit.ly/3g6dW8J (accessed February 24, 2022). Cochran, C., and Malone, E. (2014). Public Policy: Perspectives and Choices. 5th Arias, D., and Herrera, H. (2012). Entre Políticas Gubernamentales y Políticas Edn. Boulder, CO: Lynne Rienner Publishers, 425. Available online at: https:// Públicas. Análisis del ciclo de las políticas de desarrollo del gobierno del Estado de bit.ly/3pgIlWa Michoacán, México, 2003-2010. Instituto Nacional de Administración Pública, Colombia Sostenible (2021). PIRPAG: el camino de Colombia hacia una ganadería A.C.. México, D.F., Mexico. Available online at: https://bit.ly/3qHxCWS sostenible. Bogotá: Colombia Sostenible. Available online at: https://bit.ly/ Armenteras, D. (2019). Luego de la paz con las FARC, los conflictos ambientales 3fPjSDz en Colombia cambiaron pero no desaparecieron. Entrevista por Antonio Paz. Comité and Sectorial Regional Agropecuario (2015). Plan Regional de Desarrollo Bogotá: Mongabay. Available online at: https://bit.ly/3oaNcrj Agropecuario y Rural 2015-2018. San José. Available online at: https://bit.ly/ Asamblea Departamental de Casanare (2020). Plan Departamental de Extensión 3eo7sBc Agropecuaria 2020-2023. Yopal. Available online at: https://n9.cl/zvozd Congreso de la Nación Argentina (2007). Ley 26.331. Presupuestos Mínimos de Banco Mundial (2019). Caso de negocios para la ganadería sostenible en Colombia. Protección Ambiental de los Bosques Nativos. Buenos Aires. Available online Bogotá: Banco Mundial. Available online at: https://bit.ly/3goLXTx at: https://bit.ly/3uOawx6 Banco Mundial (2021). Costa Rica: Panorama General. San José: Banco Mundial. Congreso de la Nación Argentina (2014). Ley 27.066. Régimen de Promoción de la Available online at: https://bit.ly/3ncjuS6 Ganadería Bovina en Zonas Áridas y Semiáridas. Buenos Aires. Available online Banco Mundial, CIAT, and CATIE (2014). Climate-Smart Agriculture Country at: https://bit.ly/3e29hnf Profiles: Latin America and the Caribbean. Washington, DC: Banco Mundial. Congreso de la Nación Argentina (2019). Ley 27520 de 2019. Ley de presupuestos Available online at: https://hdl.handle.net/10568/52993 mínimos de adaptación y mitigación al cambio climático global. Buenos Aires. Banco Mundial, CIPAV, CIAT, Fedegán, and NTC y Fondo Acción para el Available online at: https://bit.ly/3dgCkEk Ambiente y la Niñez (2021). Acción de Mitigación Nacionalmente Apropiada Congreso de la República de Colombia (2017). Ley 1876. Bogotá. Available online NAMA. Bogotá: Banco Mundial. Available online at: https://bit.ly/3fPl5e5 at: https://bit.ly/3eKkyZO Barquero, M. (2020). Exportaciones de carne de res crecen con la Congreso de la República de Colombia (2018). Ley 1931. Bogotá. Available online fuerte demanda de China. San José: La Nación. Available online at: at: https://bit.ly/3nmMnve https://bit.ly/3A6HEE1 CONPES (2020). Política Nacional para el Control de la Deforestación y la Gestión BID (2018). Plataforma Latinoamericana y del Caribe para la Intensificación Sostenible de los Bosques. Bogotá: Consejo Nacional de Política Económica y Sostenible de la Ganadería: una Estrategia Regional para la Adaptación al Social. Available online at: https://cutt.ly/iIsZcl1 Cambio Climático y laMitigación de sus Efectos. San José: Banco Interamericano Departamento Administrativo Nacional de Estadística (2015). La ganadería bovina de Desarrollo. Available online at: https://n9.cl/lo9og de doble propósito, una actividad productiva sostenible bajo las buenas prácticas Borrás, M., Manghi, E., Miñarro, F., Mónaco, M., Navall, M., Peri, P., et al. (2017). ganaderas. Abril 2015, Número 34. Bogotá: Departamento Administrativo Acercando el manejo de bosques con ganadería integrada al monte chaqueño. Nacional de Estadística. Available online at: https://n9.cl/d553 Buenos Aires: Fundación Vida Silvestre Argentina. Available online at: https:// Dirección Nacional de Bosques (2021).Monitoreo de la superficie de bosque nativo bit.ly/3uRvLxX de la República Argentina. Buenos Aires. Available online at: https://bit.ly/ Braun, A., van Dije, S., and Grulke, M. (2016). Incremento de los sistemas 3Kagcdj silvopastoriles en América del Sur. Banco Interamericano de Desarrollo. Dirección Regional Central Occidental (2015). Plan Regional de Desarrollo Available online at: https://bit.ly/2S7iW4P Agropecuario y Rural 2015-2018. San José. Available online at: https://bit.ly/ Buitrago Guillen, M. E., Ospina Daza, L. A., and Narváez Solarte, W. (2018). 3avJiUm Sistemas silvopastoriles: alternativa en la mitigación y adaptación de la DNP (2011). Plan Nacional de Desarrollo 2010-2014. Bogotá: Departamento producción bovina al cambio climático. Boletín Científico Centro de Museos Nacional de Planeación. Available online at: https://n9.cl/xtuf Museo de Historia Natural. Available online at: https://bit.ly/3Ad3SnY DNP (2015). Plan Nacional de Desarrollo 2014-2018. Todos por un nuevo país. Cano, M. (2019). Producción y exportaciones de carne bovina. El peso de China Bogotá: Departamento Nacional de Planeación. Available online at: https://n9. en la ecuación exportadora argentina. Buenos Aires: KPMG. Available online cl/wox2 at: https://bit.ly/2QtsSEA DNP (2019). Plan Nacional de Desarrollo 2018-2022. Pacto por Colombia. Pacto Centro Agronómico Tropical de Investigación y Enseñanza (2019). por la equidad. Bogotá: Departamento Nacional de Planeación. Available online Análisis de aspectos técnicos de las NAMA de ganadería de at: https://bit.ly/3HZZMCg Frontiers in Sustainable Food Systems | www.frontiersin.org 21064 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle FAO (2010). Ganadería y deforestación. Políticas Pecuarias No. 3. Subdirección MINAE, SINAC, CONAGEBIO, and FONAFIFO (2018). Resumen del Sexto de Información Ganadera y De Análisis y Política del Sector Dirección de Informe Nacional de Costa Rica ante el Convenio de Diversidad Biológica. San Producción y Sanidad Animal. Rome. Available online at: https://n9.cl/hqvru José. Available online at: https://bit.ly/33vkCur FAO (2013). Pobreza rural y políticas públicas en América Latina y el Caribe. Miñarro, F., and Marino, D. (2013). Ganadería sustentable de pastizal. Producir y Santiago de Chile. Available online at: https://n9.cl/q4tg conservar es posible. Buenos Aires: Aves Argentinas y Fundación Vida Silvestre FAO (2019). Cambio climático y seguridad alimentaria y nutricional en América Argentina. Available online at: https://bit.ly/3e8kF0M Latina y el Caribe. Santiago de Chile. Available online at: https://n9.cl/1k60e Ministerio de Agricultura Ganadería y Pesca (2010). Plan Estratégico Territorial. Fedegán (2021). Exportaciones de carne bovina (toneladas). Bogotá: Fedegán. Buenos Aires. Available online at: https://bit.ly/2QkTsjo Available online at: https://bit.ly/3fyvTNl Ministerio de Agricultura Ganadería y Pesca (2013). Cambio Rural II, Innovación FONAFIFO (2021). Distribución de las hectáreas y árboles por actividad PSA. San e Inversión. Buenos Aires: Manual Operativo. Available online at: https://bit.ly/ José. Available online at: https://bit.ly/3fxsjCY 3djY2ay Ganadería Colombiana Sostenible (2018). ¿En qué consiste el proyecto Ganadería Ministerio de Agricultura y Desarrollo Rural (2019). Política agropecuaria y de Colombiana Sostenible? Bogotá. Available online at: https://bit.ly/32IkHat desarrollo rural 2018-2022: un campo para la equidad. Bogotá. Available online Garza, J. (2020). Ganadería es inmune a la crisis. San José: La República. Available at: https://n9.cl/yjgle online at: https://bit.ly/3fGZX9u Ministerio de Agricultura y Desarrollo Rural (2020). MinAgricultura Rodolfo Zea Gobernación de Antioquia (2020). Plan Departamental de Extensión Agropecuaria lanza nueva línea para financiar los sistemas silvopastoriles. Bogotá. Available 2020-2023. Medellín: Unidos por la vida. Available online at: https://n9.cl/t7pv9 online at: https://bit.ly/3sNo6ze Gobernación de Boyacá (2020). Plan Departamental de Extensión Agropecuaria Ministerio de Agricultura y Ganadería (2011). Política de Estado para el Sector 2020-2023. Tunja. Available online at: https://n9.cl/fha49 Agroalimentario y el Desarrollo Rural Costarricense 2010-2021. San José. Gobernación de Neuquén (2021). Plan Ganadero Bovino Provincial. Neuquén. Available online at: https://bit.ly/2QlzRjr Available online at: https://bit.ly/3Kk8Y6L Ministerio de Agricultura y Ganadería (2017). La ganadería en el contexto Gobernación del Cauca (2020). Plan Departamental de Extensión Agropecuaria agroalimentario, la generación de empleo y los retos del cambio climático: hacia 2020-2023. Popayán. Available online at: https://n9.cl/43cvs una nueva política de sostenibilidad competitiva. San José. Available online Gobernación del Cesar (2020). Plan Departamental de Extensión Agropecuaria at: https://bit.ly/3xqGulp 2020-2023. Valledupar. Available online at: https://n9.cl/nzfm Ministerio de Agricultura y Ganadería (2019). Costa Rica, en ruta hacia la Gobernación del Guainía (2019). Plan Departamental de Extensión Agropecuaria. descarbonización de la ganadería 2013-2018. San José. Available online Inírida. Available online at: https://n9.cl/yueyi at: https://bit.ly/3najylF Gobernación del Vichada (2020). Plan Departamental de Extensión Agropecuaria Ministerio de Ambiente y Desarrollo Sostenible (2019). Informe de gestión. Bogotá. 2020-2023. Puerto Carreño. Available online at: https://n9.cl/w3iij Available online at: https://acortar.link/lPNZa2 Gobierno de Colombia (2021). Estrategia climática de largo plazo de Colombia para Ministerio de Ambiente y Desarrollo Sostenible de Argentina (2021). Datos cumplir con el Acuerdo de París (E2050). Bogotá. Available online at: https:// nacionales. Superficie de bosque nativo según OTBN. Buenos Aires. Available acortar.link/u6ECpv online at: https://bit.ly/33hVVSo Gobierno de Costa Rica (2018). Plan de Descarbonización. Compromiso del Ministerio de Ambiente y Desarrollo Sostenible de Colombia (2021). Primer Gobierno del Bicentenario. San José. Available online at: https://bit.ly/3xixE91 informe de cumplimiento de hitos bajo la modalidad 1 de la Declaración Gobierno de Costa Rica (2019). Plan Nacional de Descarbonización. San José: Conjunta de Intención Renovada. Bogotá. Available online at: https://acortar. Descarbonicemos Costa Rica. Available online at: https://bit.ly/3egbD3f link/vIZupc Gobierno de Costa Rica (2020). II Informe Nacional Voluntario. Objetivos de Ministerio de Planificación Federal and Inversión Pública y Servicios (2011). Plan Desarrollo Sostenible Costa Rica 2020. San José. Available online at: https://bit. Estratégico Territorial. Buenos Aires. Available online at: https://bit.ly/3tlpSsL ly/3zWcfUL Ministerio de Planificación Federal and Inversión Pública y Servicios (2016). Goldfrank, B. (2006). Los procesos de presupuesto participativo en Política y Estrategia Nacional de Desarrollo y Ordenamiento Territorial. Buenos América Latina: éxito, fracaso y cambio. Universidad de Nuevo México. Aires. Available online at: https://bit.ly/3teHHJT doi: 10.4067/S0718-090X2006000200001 Ministerio de Planificación Nacional y Política Económica (2010). Plan Hernández, R., Fernández, C., and Baptista, M. (2014). Metodología de la Nacional de Desarrollo 2011-2014. San José. Available online at: investigación. Sexta edición. México, D.F., Mexico: McGraw Hill, 600. Available https://bit.ly/2QJt8jg online at: https://n9.cl/65f Ministerio de Planificación Nacional y Política Económica (2014). Plan Nacional IICA y Ministerio de Agricultura de la República Dominicana (2016). de Desarrollo 2015-2018. San José. Available online at: https://bit.ly/3tFC2Nd Establecimiento y uso de sistemas silvopastoriles en República Dominicana. Santo Ministerio de Planificación Nacional y Política Económica (2019). Plan Nacional Domingo. Available online at: https://bit.ly/3vg4DJj de Desarrollo y de Inversión Pública 2019-2022. San José. Available online INEC (2020). Encuesta Nacional Agropecuaria 2019. San José. Available online at: https://bit.ly/3xeHTeq at: https://bit.ly/3tk8ZO2 Ministerio de Producción and Ciencia y Tecnología (2018). Plan Ganadero INTA (2014). Cuidar el ambiente tiene beneficios. Buenos Aires: Ganadería Santafesino. Buenos Aires. Available online at: https://bit.ly/3edM1mu sustentable. Available online at: https://bit.ly/2QuPrJ3 Ministerio de Producción and Turismo y Desarrollo Económico (2020). La INTA (2017). Programa Nacional Recursos Naturales, Gestión Ambiental y provincia propicia el crecimiento sustentable de la ganadería entrerriana. Buenos Ecorregiones. Buenos Aires: Plan de Programa Nacional. Available online Aires. Available online at: https://bit.ly/3fwMeCg at: https://bit.ly/3ged9nV Morresi, S., and Vicente, M. (2019). El ocaso del macrismo: entre liberalismo y Izquierdo, C., Vaca, I., and Mena, R. (2018). El nuevo sujeto social del consumo neoliberalismo. Buenos Aires: Nueva Sociedad. Available online at: https://bit. responsable. Quito 4, 97–123. doi: 10.32719/25506641.2018.4.5 ly/32bLpIl Kaimowitz, D. (2019). La ganadería extensiva explica la mayoría de la deforestación Murgueitio, R., Chará, J., Barahona, R., Cuartas, C., and Naranjo, J. en América Latina. Centro de los Objetivos de Desarrollo Sostenible para América (2014). Los sistemas silvopastoriles intensivos (SSPi), herramienta de Latina y el Caribe. Bogotá: Entrevista por Lorenzo Morales. Available online mitigación y adaptación al cambio climático. Trop. Subtrop. Agroecosyst. 3, at: https://bit.ly/3w565OX 501–507. Available online at: https://www.redalyc.org/pdf/939/9393572800 Lozano, N. (2020). Políticas para el fortalecimiento de la producción ganadera 1.pdf sostenible. Bogotá. Available online at: https://bit.ly/33kY28k Núñez, R., Fernández, S., Araujo, O., and García, M. (2015). La ganadería en MACS (2021). ¿Quiénes somos?. Buenos Aires: MACS. Available online at: https:// América Latina y el Caribe. Montecillo: Colegio de Posgraduados. Available bit.ly/32bNvrM online at: https://bit.ly/2TEiGei Mesa de Ganadería Sostenible Colombia (2019). Bases técnicas para la formulación Observatorio do Clima (2020). Análise das emissões brasileiras de gases de efeito de la política nacional de ganadería bovina sostenible. Bogotá. Available online estufa e suas implicações para as metas de clima do Brasil. Brasil. Available online at: https://n9.cl/3ziy3 at: https://bit.ly/3I9EORD Frontiers in Sustainable Food Systems | www.frontiersin.org 21075 March 2022 | Volume 6 | Article 722522 Lerma et al. Public Policies and Sustainable Cattle OCDE (2020). Estudios económicos de la OCDE. San José. Available online Taraborrelli, D. (2017). Políticas públicas rurales y modelos de desarrollo en at: https://bit.ly/33jZyXZ Argentina. El Programa Cambio Rural entre 1993 y 2015. Estud. Soc. Estado ONU (2021). 17 objetivos para transformar nuestro mundo. ONU. Available online 3, 164–188. doi: 10.35305/ese.v3i5.110 at: https://bit.ly/3wk7kKs Tedeschi, L., Muir, J., Riley, D., and Fox, D. (2015). “Future implications for Patrouilleau, M. M., Mioni, W. F., and Aranguren, C. I. (2017). Políticas públicas animal production: a perspective on sustainable livestock intensification,” in en la ruralidad argentina. Buenos Aires: INTA Ediciones. Available online Proceedings of the 52nd Annual Meeting of the Brazilian Society of Animal at: https://bit.ly/3teH7vH Science 2015. Belo Horizonte. Available online at: https://bit.ly/3iiccvK Pincén, D., Viglizzo, E., Carreño, L., and Frank, F. (2010). “La relación soja- Tejedor Estupiñán, J. M. (2012). El modelo económico y su relación con los ecología-ambiente. Entre el mito y la realidad,” eds E. Viglizzo, and E. Jobbágy. derechos humanos en Colombia. Finan. Polít. Econ. 1, 55–82. Available online Expansión de la frontera agropecuaria agrícola en Argentina y su impacto at: https://revfinypolecon.ucatolica.edu.co/article/view/508/520 ecológico-ambiental (Buenos Aires: INTA). Available online at: https://bit.ly/ UNFCCC (2014). NS-71. Costa Rica: Livestock NAMA, United Nations 3rrWS2O Framework Convention on Climate Change. Available online at: https://bit.ly/ Presidencia de la Nación Argentina (2018). Objetivos de desarrollo sostenible. 3Gd3Q0T Buenos Aires. Available online at: https://bit.ly/3tlDzbb UPRA (2015). UPRA, fundamental en la red de gestión Presidencia de la República de Colombia (2017). Decreto 870. Bogotá. Available territorial para el desarrollo rural. Bogotá. Available online at: online at: https://bit.ly/3gvqBnD https://bit.ly/3nQ2K3z Presidencia de la República de Costa Rica (2012).Decreto Ejecutivo 37017. San José. Varijakshapanicker, P., Mckune, S., Miller, L., Hendrickx, S., Balehegn, M., Dahl, Available online at: https://bit.ly/3tAJuZX G., et al. (2019). Sustainable livestock systems to improve human health, Procomer (2020). Suministro de carne en los Estados Unidos bajo amenaza por nutrition, and economic status. Anim. Front. 9, 39–50. doi: 10.1093/af/vfz041 coronavirus. San José: Procomer. Available online at: https://bit.ly/3eklvJr Venugopal, S., Walther, M., Harper, K., and McGlynn, E. (2021). Informe RAND Corporation (2020). The benefits and costs of decarbonizing Costa Rica’s de análisis de riesgos de transición climática. La carne bovina colombiana. economy. Santa Mónica, CA. Available online at: https://bit.ly/33x4yIu Washington, DC: Orbitas – Navigating Climate Transition Risks. Available Rao, I., Peters, M., Castro, A., Schultze-Kraft, R.,White, D., Fisher, M., et al. (2015). online at: https://bit.ly/3nzpbuU LivestockPlus - The sustainable intensification of forage-based agricultural Villamil, L. (2020). El coronavirus no pudo frenar el boom exportador de la carne systems to improve livelihoods and ecosystem services in the tropics. Trop. argentina. Argentina: Clarín Rural. Available online at: https://bit.ly/3vH4m2d Grasslands 3, 59–82. doi: 10.17138/TGFT(3)59-82 Xie, H., Huang, Y., Chen, Q., Zhang, Y., and Wu, Q. Rojas Villagra, L., Puello-Socarrás, J. F., Elías, A., Gambina, J. C., and Benítez, (2019). Prospects for agricultural sustainable intensification: E. (2015). Neoliberalismo en América Latina. Crisis, tendencias y alternativas. a review of research. Land 8, 157. doi: 10.3390/land811 Argentina. 1a Edn. Asunción: Grupos de trabao de CLASCO. Available online 0157 at: https://bit.ly/3pm4aDF Yalmanov, N. (2021). “Public policy and policy-making,” in XXIII International SAGARPA, ASERCA, and CIMA (2018). Reporte del mercado de carne de bovino. Conference Culture, Personality, Society in the Conditions of Digitalization: México, D.F., Mexico. Available online at: https://n9.cl/f1t88 Methodology and Experience of Empirical Research Conference. Volume 2020 Sanhueza, J. E., and Antonissen, M. (2014). REDD+ en América Latina. Estado (Yekaterinburg: KnE Social Sciences). doi: 10.18502/kss.v5i2.8400 actual de las estrategias de reducción de emisiones por deforestación y degradación forestal. Santiago de Chile: Comisión Económica para América Conflict of Interest: The authors declare that the research was conducted in the Latina y el Caribe (CEPAL). Available online at: https://n9.cl/585x absence of any commercial or financial relationships that could be construed as a Scaletta, C. (2020). Alberto Fernández aplica un programa económico similar al potential conflict of interest. primer kirchnerismo. Buenos Aires: Página 12. Available online at: https://bit. ly/3wTbZnK Publisher’s Note: All claims expressed in this article are solely those of the authors Secretaría de Agricultura de Santander (2020). Plan Departamental de Extensión and do not necessarily represent those of their affiliated organizations, or those of Agropecuaria 2020-2023. Bucaramanga. Available online at: https://n9.cl/w0kgz the publisher, the editors and the reviewers. Any product that may be evaluated in Secretaría de Agricultura y Ganadería (2020). Ciclo de capacitaciones. Buenos this article, or claim that may be made by its manufacturer, is not guaranteed or Aires: Plan Ganadero Enterriano. Available online at: https://bit.ly/3gjSaQJ Secretaría de Ambiente y Desarrollo Sustentable (2019). Inventario Nacional de endorsed by the publisher. Gases de Efecto Invernadero. Buenos Aires. Available online at: https://bit.ly/ 3I4ugDp Copyright © 2022 Lerma, Díaz Baca and Burkart. This is an open-access article Secretaría de Gobierno de Agroindustria de la Nación (2019). Agroindustria distributed under the terms of the Creative Commons Attribution License (CC BY). difundió el informe sobre stock bovino. Buenos Aires. Available online at: https:// The use, distribution or reproduction in other forums is permitted, provided the bit.ly/3y37588 original author(s) and the copyright owner(s) are credited and that the original Secretaría Ejecutiva de Planificación Sectorial Agropecuaria (2015). Política para publication in this journal is cited, in accordance with accepted academic practice. el Sector Agropecuario y el Desarrollo de los Territorios Rurales 2015-2018. San No use, distribution or reproduction is permitted which does not comply with these José. Available online at: https://bit.ly/2RYZRSb terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 21086 March 2022 | Volume 6 | Article 722522 ORIGINAL RESEARCH published: 29 March 2022 doi: 10.3389/fsufs.2022.725656 A Transcriptomic Analysis of Stylo [Stylosanthes guianensis (Aubl.) Sw.] Provides Novel Insights Into the Basis of Salinity Tolerance Yiming Liu 1, Danyu Kong 2, Hubiao Yang 1, Sabine Douxchamps 3, Mary Atieno 3, Bin Xu 4, Wenqiang Wang 1* and Guodao Liu 1* 1 Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences (CATAS), Ministry of Agriculture and Rural Affairs, Danzhou, China, 2 Lushan Botanical Garden, Chinese Academy of Sciences, Jiujiang, China, 3 Tropical Forages Program, Alliance Bioversity-CIAT, Hanoi, Vietnam, 4College of Agro-Grassland Science, Nanjing Agricultural University, Nanjing, China Edited by: Tropical areas have a large distribution of saline soils and tidal flats with a high salinity Stephen Whitfield, University of Leeds, United Kingdom level. Salinity stress is a key factor limiting the widespread use of tropical forage such Reviewed by: as Stylosanthes guianensis (Aubl.) Sw. This study was designed to screen the salinity Teodardo Calles, tolerance of 84 S. guianensis accessions; In a greenhouse experiment, plants were Food and Agriculture Organization of the United Nations, Italy subjected to Hoagland solution or Hoagland solution with 200mM NaCl for up to 15 Yan Xie, days. Salinity tolerant accession CIAT11365 and salinity sensitive accession FM05- Wuhan Botanical Garden (CAS), China 2 were obtained based on withered leaf rate (WLR). Further verification of salinity Jiamin Miao, Gansu Agricultural University, China tolerance in CIAT11365 and FM05-2 with different salinity gradients showed that salinity *Correspondence: stress increased WLR and decreased relative chlorophyll content (SPAD), maximum Guodao Liu photochemical efficiency of photosystem II (Fv/Fm), and photosynthetic rate (Pn) in liuguodao2008@163.com Wenqiang Wang FM05-2, but CIAT11365 exhibited lower WLR and higher SPAD, Fv/Fm, and Pn. Leaf wwqnmg@163.com RNA-Seq revealed that Ca2+ signal transduction and Na+ transport ability, salinity tolerance-related transcription factors and antioxidant ability, an increase of auxin, and Specialty section: This article was submitted to inhibition of cytokinin may play key roles in CIAT11365 response to salinity stress. The Climate-Smart Food Systems, results of this study may contribute to our understanding of the molecular mechanism a section of the journal underlying the responses of S. guianensis to salinity stress and also provide important Frontiers in Sustainable Food Systems clues for further study and in-depth characterization of salinity resistance breeding Received: 15 June 2021 Accepted: 31 January 2022 candidate genes in S. guianensis. Published: 29 March 2022 Keywords: Stylosanthes guianensis (Aubl.) Sw., salinity tolerance, differentially expressed genes, transporter, Citation: hormones Liu Y, Kong D, Yang H, Douxchamps S, Atieno M, Xu B, Wang W and Liu G (2022) A INTRODUCTION Transcriptomic Analysis of Stylo [Stylosanthes guianensis (Aubl.) Sw.] Soil salinity is a major limiting factor in agriculture in terms of yield and productivity (Munns and Provides Novel Insights Into the Basis of Salinity Tolerance. Tester, 2008). Most forage species are salt sensitive; the effect of NaCl on forage is caused by both the reduction of water availability caused by high Na+Front. Sustain. Food Syst. 6:725656. concentration and the toxic effect of Na+ doi: 10.3389/fsufs.2022.725656 and Cl− on plants. Elucidating salinity-tolerant mechanisms, mining salinity-tolerant genes, and Frontiers in Sustainable Food Systems | www.frontiersin.org 2107 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes improving crop salinity tolerance are good strategies to deal with of each S. guianensis accessions were taken from the field gene increased saline soil (Deinlein et al., 2014). Research on the salt- bank of CATAS, wrapped with sponge, and planted on a foam tolerant mechanism of plant includes forage, improvement, and board. The foam board was floated in a plastic box (110 × 90 × utilization of saline soil, which have become the focus of recent 20 cm) filled with 40 L Hoagland solution. Pumps supply with studies (Abiala et al., 2018; Zelm et al., 2020; Zhao et al., 2020). oxygen to each plastic box. The equivalent of water lost through Stylo (Stylosanthes spp.) is an important forage legume that evaporation and transpiration was supplied into the plastic is grown in tropical and subtropical areas, mainly used for box every day, and solutions were changed every week. Salinity pasture and green manure. The Chinese Academy of Tropical treatment was conducted with 200mM NaCl after 2 months’ Agricultural Sciences (CATAS) introduced more than 500 Stylo cultivation when the height of seedlings reached 20–25 cm; NaCl accessions to China from the International Center for Tropical concentration was gradually increased to 200mM by adding Agriculture (CIAT) or other countries since the 1960’s. Stylo has 50mM NaCl per 12 h to avoid sudden death. Withered leaf rate become a very important tropical forage legume in tropical areas (WLR) was measured at 15 days of salinity treatment; and a few of China. Till now, CATAS has cultivated 15 nationally approved yellow leaves were removed before salt treatment to avoid impact Stylo varieties (Huang et al., 2017). Stylosanthes guianensis of WLR. WLR (%) = number of leaves with withered symptoms (Aubl.) Sw. is one of the most important species in Stylosanthes more than 50%/total number of leaves× 100 (Liu et al., 2017). spp., a subshrub with height ranging from 0.6 to 1.2m and a A split plot design was used with salt stress treatments as the stem diameter of 0.3–0.8 cm, which grows well in tropical and main plots and the accessions as the subplots. Each treatment had subtropical climates, and is adapted to acid and drought soils. 3 replicates. The 84 S. guianensis accessions grown in the plastic S. guianensis also has the earliest origin, the most branches, box were randomly placed. the richest genetic diversity, and the widest distribution in Stylosanthes spp. Almost half of stylo accessions in the CATAS seed bank are S. guianensis (249 accessions) (Jiang et al., 2017). Experiment 2: Physiological Responses of Coastal saline soils and tidal flats are distributed in vast 2 Accessions of S. guianensis to Different areas in tropical regions (Ivushkin et al., 2019), and have an Salinity Levels and Transcriptomic Analysis adverse effect on tropical forage yield and quality. Screening of Two S. guianensis accessions, CIAT11365 (salinity tolerant, ST) salinity-tolerant tropical forage such as Stylo is a sustainable and and FM05-2 (salinity sensitive, SS), were selected based on economical viable option of improving and utilizing such coastal experiment 1. Seeds of both accessions were sowed into plastic saline soils. Previous studies have shown the high variation of pots with 20 cm diameter and 24 cm height, filled with sand. salinity tolerance in 67 accessions from 23 species of Stylosanthes Plants were maintained in the greenhouse for 2 months and then spp., S. erecta P.Beauv. CIAT11900, and S. hippocompoides treated with 100, 200, 300, and 400mM NaCl. Both accessions Mohlenbr. Fine stem, S. hamata (L.) Taub. CIAT1010, S. fruticosa were irrigated daily with 400ml of Hoagland solution or salt (Retz.) Alston CIAT11052, S. debilis M.B. Ferreira & Sousa solution for 15 days, and the redundant solution at the bottom Costa CIAT11927, and S. hamata Verano have the relatively of the pot was drained to avoid salinity accumulation. Each best salinity tolerance with 200mM NaCl for 15 days. Only treatment had 4 replicates. The exposure of plants to increasing 10 S. guianensis accessions were evaluated for their salinity salt concentration allowed a gradual acclimation to salinity tolerance and most of them had intermediate- or above-level conditions to avoid sudden death at high salt concentration. performance (Liu et al., 2017). Considering the high biomass Leaf samples were collected at 5 days with 200mM NaCl for advantage and the high diversity of S. guianensis, it is essential transcriptomic analysis. to evaluate the salinity tolerance of S. guianensis in a wider range WLR, relative chlorophyll content (SPAD), maximum of accessions and explore the molecular mechanism of response photochemical efficiency of photosystem II (Fv/Fm), and to salinity stress. photosynthetic rate (Pn) were estimated in this experiment. The objectives of this study were to (1) Examine the SPAD value was measured on upper-middle leaves with a SPAD salinity tolerance of 84 accessions of S. guianensis; (2) Clarify meter (TYS-B, Zhejiang, China); Fv/Fm was estimated with the performance of salinity-tolerant and salinity-sensitive S. a chlorophyll fluorometer (PAM-2500, Heinz Walz GmbH, guianensis with different salinity concentrations; and (3) Explore Effeltrich, Germany) after leaves were dark-adapted for 15min, the salinity-tolerant mechanisms and differentially expressed and Pn was measured using a portable photosynthesis system genes (DEGs) by transcriptomic analysis. (Li-6400 XT, LICOR, Inc, Lincoln, NE, USA). MATERIALS AND METHODS Transcriptomic Analysis Total RNA and mRNA Isolation Experiment 1: Screening of Salinity Total RNA was extracted using Trizol reagent (Invitrogen, Tolerance in 84 S. guianensis Accessions CA, USA) purified using the RNeasy Plant Mini kit (Qiagen) This study was carried out in the greenhouses of CATAS, according to the manufacturer’s protocol. RNA purity was Danzhou, Hainan, China. A total of 84 S. guianensis checked using the kaiaoK5500©R spectrophotometer (Kaiao, accessions were screened for their salinity tolerance Beijing, China); RNA integrity and concentration were assessed (Supplementary Material 1). About 6- to 8-cm-long stems using the RNA Nano 6000 Assay Kit of the Bioanalyzer Frontiers in Sustainable Food Systems | www.frontiersin.org 2208 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 1 | The range in WLR vertical bars of 84 S. guianensis accessions treated with 200mM NaCl for 15 days. The LSD 0.05 was 45.39. Values are means (n = 3). Frontiers in Sustainable Food Systems | www.frontiersin.org 2309 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 2 | Phenotype of two S. guianensis accessions CIAT11365 (salinity tolerant, ST) and FM05-2 (salinity sensitive, SS) under different NaCl concentrations (100–400mM) at 15 days. FIGURE 3 | Effect of different salinity concentrations to WLR, SPAD, Fv/Fm, and Pn in ST and SS. ST, CIAT11365; SS, FM05-2. 2100 system (Agilent Technologies, CA, USA) and agarose sequences to each sample. mRNA was purified from total RNA gel electrophoresis. using poly-T oligo-attached magnetic beads. Fragmentation was carried out using divalent cations under elevated temperature Transcriptome Sample Preparation and in NEBNext First-Strand Synthesis Reaction Buffer (5X). First- Transcriptome Sequencing strand cDNA was synthesized using random hexamer primer A total amount of 2 µg of RNA per leaf sample was used and RNase H. Second-strand cDNA synthesis was subsequently for the RNA sample preparations, sequencing libraries were performed using buffer, dNTPs, DNA polymerase I, and RNase generated using NEBNext©R UltraTM RNA Library Prep Kit for H. The library fragments were purified with QiaQuick PCR Illumina©R (#E7530L, NEB, USA) following the manufacturer’s kits and eluted with EB buffer, and then terminal repair, recommendations, and index codes were added to attribute A-tailing, and the added adapter were implemented. The aimed Frontiers in Sustainable Food Systems | www.frontiersin.org 2410 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 4 | Histogram of gene ontology (GO) classification. The results are summarized in three main categories: biological process, cellular component, and molecular function. products were retrieved, PCR was performed to complete the quality, including Q30, data quantity and quality, base content library. Preliminary quantification of RNA concentration of statistics, etc. library was obtained using Qubit©R RNA Assay Kit in Qubit©R The software Trinity was used for de novo assembly, which 3.0 then diluted to 1 ng/µl. Insert size was assessed using was developed at the Broad Institute and the Hebrew University the Agilent Bioanalyzer 2100 system (Agilent Technologies, of Jerusalem. Trinity represents a novel method for the efficient CA, USA), and qualified insert size was accurately quantified and robust de novo reconstruction of transcriptomes from RNA- using the StepOnePlusTM Real-Time PCR System (Library valid seq data. Trinity partitions the sequence data into many de Bruijn concentration >10 nM). The clustering of the index-coded graphs, each representing the transcriptional complexity at a samples was performed on a cBot cluster generation system using given gene or locus. Each graph was processed independently HiSeq PE Cluster Kit v4-cBot-HS (Illumina) according to the to extract the full-length splicing isoforms and to tease apart manufacturer’s instructions. After cluster generation, the libraries transcripts derived from paralogous genes. were sequenced on an Illumina platform and 150-bp paired-end reads were generated. Unigene Annotation and Classification Trinotate was used for performing the functional annotation of unigenes and ORFs. Trinotate is a comprehensive Preprocessing and de novo Assembly annotation suite designed for automatic functional annotation De novo assembly was employed to construct transcripts from of transcriptomes, particularly for de novo assembled these RNA-Seq reads because of the absence of reference genomic transcriptomes, from model to non-model organisms. Trinotate sequences. Trinity software was used for de novo assembly of the makes use of a number of different well-referenced methods Illumina reads. For a quality control before subsequent analysis, for functional annotation including homology search to raw data were processed with Perl scripts. The raw reads were known sequence data (BLAST+/SwissProt), protein domain processed by removing reads containing adapter, the adaptor- identification (HMMER/PFAM), protein signal peptide and polluted reads, the low-quality reads, and reads with number transmembrane domain prediction (singalP/tmHMM), and of N bases accounting for more than 5%. The obtained Clean comparison to current annotation databases (EMBL Uniprot Data after filtering will be subjected to statistics analyses on its eggNOG/GO Pathways databases). Frontiers in Sustainable Food Systems | www.frontiersin.org 2511 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 5 | The euKaryotic Ortholog Groups (KOG) annotation of putative proteins. All 14,313 putative proteins showing significant homology to those in the KOG database were functionally classified into 26 molecular families. Quantification of Gene Expression Levels and The GO (Gene Ontology, http://geneontology.org/) Differential Expression Analysis enrichment of DEGs was implemented by the hypergeometric Read count for each gene in each sample was counted by HTSeq test, in which p-value is calculated and adjusted as q-value, v0.6.0, and RPKM (Reads Per Kilobase Millon Mapped Reads) and data background is genes in the whole genome. GO terms was then calculated to estimate the expression level of genes in with q < 0.05 were considered to be significantly enriched. GO each sample (Guo et al., 2013). DEGseq v1.18.0 was used for enrichment analysis could exhibit the biological functions of differential gene expression analysis between two samples with the DEGs. KEGG (Kyoto Encyclopedia of Genes and Genomes, non-biological replicates. Under the assumption that the number http://www.kegg.jp/) is a database resource containing a of reads deriving from a gene (or transcript isoform) follows a collection of manually drawn pathway maps representing our binomial distribution, DEGseq is proposed based onMAplot and knowledge on the molecular interaction and reaction networks. widely used for differential gene expression analysis. The p-value The KEGG enrichment of DEGs was implemented by the could be assigned to each gene and adjusted by the Benjamini hypergeometric test, in which p-value was adjusted by multiple and Hochberg’s approach for controlling the false discovery rate. comparisons as q-value. KEGG terms with q < 0.05 were Genes with q ≤ 0.05 and |log2_ratio| ≥ 1 are identified as considered to be significantly enriched. DEGs. DESeq (v1.16) was used for differential gene expression analysis between two samples with biological replicates using a Quantitative Real-Time PCR Analysis model based on the negative binomial distribution. The p-value The expression of selected genes was validated by quantitative could be assigned to each gene and adjusted by the Benjamini real-time PCR (qRT-PCR); the same RNA samples as the RNA- and Hochberg’s approach for controlling the false discovery seq library construction were used. First-strand cDNA fragments rate. Genes with q ≤ 0.05 and |log2_ratio| ≥ 1 are identified were synthesized using the cDNA synthesis kit (Fermentas, as DEGs. Burlington, Ontario, Canada). Gene primers were designed using Frontiers in Sustainable Food Systems | www.frontiersin.org 2612 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 6 | Differentially expressed genes (DEGs) were identified between 4 comparisons, including A (control ST_control SS), B (salt ST_control ST), C (salt SS_ control SS), and D (salt ST_salt SS). Primer 5 software. Ef1A gene was used as reference gene. Physiological Responses of 2 Accessions Each sample had three biological replicates and each biological of S. guianensis to Different Salinity Levels replicate had three technical replicates; 20 µl of reaction includes Based on WLR (Figure 1), two accessions, CIAT11365 (salinity 5 µl of cDNA, 10 µl of 2 × SYBR©R Premix Ex TaqTM (Tli tolerant, ST) and FM 05-2 (salinity sensitive, SS), were selected RNaseH Plus), and 0.5µl of the forward and reverse primers. The for physiological responses at different salinity levels, and the synthesis reaction lasted 39 cycles at 95◦C for 10 S and 60◦C for result showed that ST can survive at 15 days of 200mM treatment 34 S. (WLR = 46.67%) whereas SS almost have no green leaves left (WLR = 100%) (Figures 2, 3). WLR, SPAD, Fv/Fm, and Pn Data Analysis showed that ST and SS had a decline trend under 100–400mM All data were subjected to analysis of variance (SAS 8.1; SAS NaCl treatment, but ST had a significant higher value of WLR, Institute Inc., Cary, NC). Differences among the mean values SPAD, Fv/Fm, and Pn at 15 days of 100–200mMNaCl treatment were assessed by the least significant difference (LSD) test at than SS (Figure 3). p= 0.05. Transcriptome Sequencing and Assembly An overview of the RNA-Seq reads is presented in RESULTS Supplementary Material 2. A total of 151,356 contigs were obtained from the clean reads with a mean length Screening of Salinity Tolerance in 84 S. of 1,118.6 bp and length ranging from 201 to 16,419 bp guianensis Accessions (Supplementary Material 3). Among the 151,356 contigs, WLR showed that S. guianensis accessions had large variation 74,515 unigenes were obtained with an average length of 879.4 in salinity tolerance (Figure 1). Schofield, L1-82, CIAT25, bp. The length of a unigene ranged from 201 bp to 16,419 bp; NF01078, Fitzory, Oxley, TPRC90139, ReyanNo.5, CIAT11365, N50 was 1,617 bp and N90 was 320 bp. RNA-seq data from CIAT10594, USF873015, and CIAT10390 had relatively lower this article can be found in the NCBI SRA database under the WLR (<14%) at 15 days of 200mM NaCl stress, and these BioProject ID: PRJNA771864. accessions were considered to be salinity tolerant. In contrast, CIAT74, GC1557, GC1480, FM05-2, CIAT11369, E9, TPRC87, Gene Annotation CIAT11279, CIAT75, GC1517, CIAT2950, and CIAT2659 were The unigenes were annotated by searching against the seven considered to be salt-sensitive accessions with a relatively higher public databases (Supplementary Material 4). A total of 38,426 WLR (>96%) at 15 days of 200mM NaCl stress. unigenes (51.57%) were matched in the NR database, 30,953 Frontiers in Sustainable Food Systems | www.frontiersin.org 2713 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 7 | Hierarchical clustering of the differentially expressed genes. Frontiers in Sustainable Food Systems | www.frontiersin.org 2814 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 8 | Venn diagram of differentially expressed genes. The sum of the numbers in each large circle represents the total number of differentially expressed genes between comparison, and the overlap part of the circles represents common differentially expressed genes between comparisons. ST: salinity-tolerant accession CIAT11365, SS: salinity-sensitive accession FM 05-2. (41.54%) in the BLASTX database, 30,420 (40.82%) in the prediction only” (2,143), “Translation, ribosomal structure, Prot database, 29,963 (40.21%) in the GO database, and and biogenesis” (1,973), “Posttranslational modification, protein 23,209 (31.15%) in the PFAM database. A total of 50,529 turnover, chaperones” (1,555), and “Energy production and unigenes (67.81%) were successfully annotated in NR, BLASTX, conversion” (1,252), respectively. Prot, GO, PFAM, BLASTP, NT, eggnog, KO, TmHMM, or SignalP databases. Differential Expression Genes Analysis Under Salinity Treatments Gene Ontology Classification DEGs (padj < q ≤ 0.05 and log2FoldChange|log2_ratio| ≥ 1) For GO analysis, there were 29,963 unigenes divided into were identified between 4 comparisons, including A (control three ontologies (Figure 4). “Cellular process”-, “metabolic ST_control SS), B (salt ST_control ST), C (salt SS_ control SS), process”-, and “single-organism process”-related genes were and D (salt ST_salt SS). The number of DEGs detected in A, B, C, mainly included in the biological process category; “cell and Dwere 6,892, 1,199, 2,080, and 4,706, respectively (Figure 6). part”-, “organelle”-, and “organelle part”-related genes were DEGs are clustered by hierarchical clustering using up and down mainly included in the cellular component category; for gene regulation and gene enrichment analysis (Figure 7). The the molecular function category, “binding,” “catalytic,” and blue color represents low gene expression quantity, and the “transporter” were the main genes. There were 14,313 unigenes yellow represent high gene expression quantity. Figure 6 showed assigned to KOG classification divided into 26 function that more DEGs were detected in comparison A and D than classes (Figure 5). The top 4 classes were “General functional in B and C, suggesting that there are more DEGs in different Frontiers in Sustainable Food Systems | www.frontiersin.org 2915 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 9 | Heatmap of KEGG pathway enrichment analysis for DEGs of four comparisons, namely, control ST_control SS, salt ST_control ST, salt SS_ control SS, and salt ST_salt SS. accessions than in the same accession, and more up-expressed in comparison to salt ST_salt SS; and plant hormone signal genes in salt and control of ST than in salt and control of transduction was a common pathway in comparison to control SS (Figure 7). ST_control SS, salt SS_ control SS, and salt ST_control ST but Venn diagram analysis revealed the unigenes were not enriched in salt ST_control ST (Figure 9). overlapping between the four comparisons (Figure 8). There were (a) 74 DEGs in two hybrid combinations of B and D, 18 Validate the DEGs by Real-Time RT-PCR Analysis DEGs in two hybrid combinations of B, C, and D, and 282 DEGs To validate the data from RNA-sequencing, 41 DEGs mainly in two hybrid combinations of B and C; and (b) 74 DEGs in including salt response genes from 74 (a), 282, 18, 74 (b), two hybrid combinations of A, B, and C, and 58 DEGs in four and 58 groups of Venn diagram were selected for real- hybrid combinations of A, B, C, and D. The DEGs were either time RT-PCR analysis in ST and SS accessions in response up- or downregulated; those five groups may contain the most to salt stress (Figure 8). The primers of selected genes are important DEGs that contributed to the salinity tolerance of ST. listed in Supplementary Material 5. The qRT-PCR results Heatmap of KEGG pathway enrichment analysis for DEGs showed a strong correlation with the RNA-seq-generated showed that circadian rhythm-plant was a special pathway in data (Table 1). Among the 41 DEGs, 14 had a significant comparison to salt ST_control ST; pentose phosphate pathway, difference between salt ST and salt SS according to the RT- glutathione metabolism, carbon fixation in photosynthetic PCR result (Table 4 in Supplementary Material 6), 12 DEGs organisms, and oxidative phosphorylation were special pathways in salt ST had a significant increase compared to salt SS, Frontiers in Sustainable Food Systems | www.frontiersin.org 21106 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes TABLE 1 | Comparisons of RNA-Seq and RT-PCR in 41 DEGs of ST and SS. Gene id Venn GO_biological_process RNA- RT- RNA- RT- RT-PCR group Seq PCR Seq PCR result (Figure 8) result result result result of of ST of of ST SS SS Exp Exp Signi Up/ Signi Up/ Exp Exp Signi Up/ Signi Up/ Signi ression ression ficant down ficant down ression ressionficant down ficant down ficance of of salt of of of salt ST control control salt vs. salt SS c38854_g1 74a, PREDICTED: 756.5 Yes Down * Down 1968.6 924.0 Yes Down ** Down Significant 18, 58, cytokinin 2136.2 high 282, dehydrogenase 74b 6-like [Glycine max] c25614_g1 74a, PREDICTED: 1030.7 73.8 Yes Down * Down 1072.8 31.6 Yes Down *** Down Significant 18, 58, cation/H(+) high 282, antiporter 15-like 74b [Cicer arietinum] c34374_g1 74a, Nodulin 56.2 123.3 Yes Up ** Up 57.3 122.2 Yes Down ns Significant 18, 58, MtN21/EamA-like high 282, transporter family 74b protein [Medicago truncatula] c41938_g5 74a, Peroxidase 2 43.0 107.0 Yes Up ** Up 48.1 102.0 Yes Up ns Significant 18, 58, [Sesbania rostrata] high 282, 74b c31061_g1 74a, PREDICTED: 81.1 20.2 Yes Down ns 81.9 19.4 Yes Down * Down ns 18, 58, transmembrane 282, protein 45A-like 74b [Cicer arietinum] c25356_g1 74a, Oligopeptide 274.9 98.4 Yes Down * Down 271.6 101.6 Yes Down ns ns 18, 58, transporter OPT 282, family protein 74b [Medicago truncatula] c34262_g1 74a, Annexin [Arachis 2600.6 5916.6 Yes Up ns 1903.3 #### Yes Up ns Significant 18, hypogaea]; high 282, response to salt 74b stress c36834_g1 18, 58, FAD binding 229.4 98.3 Yes Down ns 240.5 87.1 Yes Down ns ns 282, domain; |response 74b to oxidative stress c39804_g2 74b, PREDICTED: 174.2 48.2 Yes Down ns 206.2 16.2 Yes Down ** Down ns 18, cysteine-rich 282 receptor-like protein kinase 10-like isoform X2 [Glycine max]; Salt stress response/antifungal c18276_g1 74b,18, Putative aquaporin 318.7 122.1 Yes Down * Down 351.9 88.9 Yes Down ** Down ns 282 PIP-type 7a [Glycine soja]; response to stress c34502_g2 74a, Vacuolar amino acid 138.2 58.5 Yes Down * Down 149.0 47.6 Yes Down *** Down Significant 282 transporter 1 high [Glycine soja] c41881_g1 74a Cysteine-rich 84.5 31.9 Yes Down ** Down No Down ns ns receptor-kinase-like protein [Medicago truncatula] [Medicago truncatula] (Continued) Frontiers in Sustainable Food Systems | www.frontiersin.org 21117 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes TABLE 1 | Continued Gene id Venn GO_biological_process RNA- RT- RNA- RT- RT-PCR group Seq PCR Seq PCR result (Figure 8) result result result result of of ST of of ST SS SS Exp Exp Signi Up/ Signi Up/ Exp Exp Signi Up/ Signi Up/ Signi ression ression ficant down ficant down ression ressionficant down ficant down ficance of of salt of of of salt ST control control salt vs. salt SS c40459_g1 74a Auxin-induced 790.7 Yes Down * Down No Down ns Significant protein [Vigna 2020.2 high radiata] c32634_g1 74a NAC-like 21.9 253.0 Yes Up ** Up No Down ns Significant transcription factor high [Arachis hypogaea] stress related c33712_g1 74a Disease resistance 77.9 25.0 Yes Down ns No Down ** Down Significant protein low (CC-NBS-LRR class) family protein [Medicago truncatula] c33369_g1 74a Redoxin [Tilletiaria 12.1 102.9 Yes Down ns No Down ns Significant anomala UBC 951] low c61867_g1 74a PREDICTED: 357.0 97.9 Yes Down ns No Down ** Down ns cation/calcium exchanger 1-like [Glycine max] c57911_g1 74a PREDICTED: LOW 15.6 2.5 Yes Down ns No Down ** Down ns QUALITY PROTEIN: myb-related protein Zm1 [Glycine max] check downstream genes in Arabidopsis c51380_g1 74a Triose-phosphate 94.0 42.7 Yes Down * Down No Down ns ns transporter family protein [Medicago truncatula] c41881_g3 74a PREDICTED: 11.2 2.4 Yes Down * Down No Down * Down Significant cysteine-rich high receptor-like protein kinase 25-like [Glycine max] c34633_g2 74a Vacuolar 75.8 36.0 Yes Down ns No Down * Down ns cation/proton exchanger [Medicago truncatula] c34566_g1 74a Vacuolar 1029.7 230.1 Yes Down ns No Down * Down ns cation/proton exchanger[Medicago truncatula] c32315_g1 74a PREDICTED: 105.6 31.7 Yes Down * Down No Down ns ns potassium channel SKOR-like [Glycine max] c31504_g2 74a Plant-pathogen 30.4 7.7 Yes Down ns No Down ** Down ns c27440_g1 74a GRA–TF 306.7 134.7 Yes Down * Down NO DOWN ** Down ns (Continued) Frontiers in Sustainable Food Systems | www.frontiersin.org 21128 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes TABLE 1 | Continued Gene id Venn GO_biological_process RNA- RT- RNA- RT- RT-PCR group Seq PCR Seq PCR result (Figure 8) result result result result of of ST of of ST SS SS Exp Exp Signi Up/ Signi Up/ Exp Exp Signi Up/ Signi Up/ Signi ression ression ficant down ficant down ression ressionficant down ficant down ficance of of salt of of of salt ST control control salt vs. salt SS c27130_g2 74a PREDICTED: NAC 52.6 16.7 Yes Down ns NO DOWN * Down ns domain-containing protein 73-like [Cicer arietinum] c23342_g1 74a RING-H2 18.4 6.2 Yes Down ** Down No Down ** Down ns c10949_g1 74a K(+)/H(+) antiporter 171.0 61.5 Yes Down ** Down No Down * Down ns [Medicago truncatula] c42060_g8 74a Plant-pathogen 13.7 89.0 Yes Up ns No Down * Down ns c41837_g4 74a plant-pathogen 6.6 31.1 Yes Up ns No Down * Down ns c25043_g1 74a PREDICTED: 36.4 74.4 Yes Up * up No Down ns ns putative oxidoreductase TDA3 [Gossypium raimondii] c20795_g1 74a PREDICTED: 13.1 56.2 Yes Up ns 2.4 66.9 Yes Up ** Up ns probable glutathione S-transferase parA [Cicer arietinum] c34262_g2 282 Calcium ion 50.6 191.8 Yes Up ** Up 55.8 186.6 Yes Up ns Significant transmembrane high transport; response to cold; heat; oxidative stress; salt c32133_g1 282 Uncharacterized 388.0 921.0 Yes Up * Up 428.4 880.6 Yes Up ns Significant protein high LOC100305594 [Glycine max]; Universal stress protein family c36998_g2 282 PREDICTED: 250.6 39.9 Yes Down * Down 230.7 59.9 Yes Down *** Down ns cysteine-rich receptor-like protein kinase 10-like [Glycine max]; Salt stress response/antifungal c27912_g1 282 Medicago sativa 812.8 297.8 Yes Down ns 909.8 200.8 Yes Down ** Down ns aquaporin-like transmembrane channel protein (pAFI 8-1) mRNA, complete cds c47236_g1 282 PREDICTED: 11.8 140.1 Yes Up * Up 15.4 136.5 Yes Up * Up ns Glycine max translocator protein homolog (LOC100785785), mRNA; response to salt stress; transport (Continued) Frontiers in Sustainable Food Systems | www.frontiersin.org 21139 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes TABLE 1 | Continued Gene id Venn GO_biological_process RNA- RT- RNA- RT- RT-PCR group Seq PCR Seq PCR result (Figure 8) result result result result of of ST of of ST SS SS Exp Exp Signi Up/ Signi Up/ Exp Exp Signi Up/ Signi Up/ Signi ression ression ficant down ficant down ression ressionficant down ficant down ficance of of salt of of of salt ST control control salt vs. salt SS c41642_g5 282 Sophora davidii 694.6 Yes Up ** Up 331.9 #### Yes Up ** Up ns dehydrin (DHN) 7787.3 mRNA, complete cds; response to stress c40061_g6 282 Phaseolus vulgaris 3795.1 7784.4 Yes Up ** up 2870.6 #### Yes Up ns ns clone BE5D1976 In2-1 protein mRNA, complete cds; response to stress c38817_g1 282 Glutathione 8781.9 Yes Up * Up 2153.6 #### Yes Up * Up ns S-transferase 2800.5 [Medicago truncatula]; response to salt stress c35733_g1 282 Hypothetical protein 73.5 184.8 Yes Up ** Up 64.8 193.5 Yes Up ns ns PHAVU_006G159300g [Phaseolus vulgaris]; response to stress and 2 DEGs in salt ST had a significant decrease compared content or SPAD, Fv/Fm, Pn, EL and RWC are conventional and to salt SS. The functions of the 12 increased DEGs are reliable. mainly ion transporter (c25614_g1, c34374_g1, c34262_g1, c34502_g2, and c34262_g2), plant hormone (c38854_g1 and Salinity Tolerance of S. guianensis c40459_g1), antioxidant enzyme (c41938_g5), transcription Accessions Ranged From 100 to 200mM factor (c32634_g1), aquaporin (c18276_g1), and other functions NaCl (c41881_g1 and c32133_g1). The functions of the 2 decreased The phenotype of two S. guianensis accessions ST and DEGs are mainly redoxin (c33369_g1) and disease resistance SS under different NaCl concentrations (100–400mM) for protein (c33712_g1). 15 days confirmed that the screening result from WLR is reliable. SPAD, Fv/Fm, and Pn were further proof of different salinity tolerance between ST and SS, as these DISCUSSION physiological parameters were consistant with WLR. Previous studies showed that the salinity-tolerant ability of Stylosanthes High Variation of Salinity Tolerance in S. spp. is between 0.9% and 1.2% NaCl (Wu et al., 2013; Dong et al., guianensis Accessions 2017). In this study, phenotype and physiological parameters High variation of salinity tolerance in 84 S. guianensis accessions showed that salinity-tolerant S. guianensis ST can endure was observed according to WLR, ranging between relative 100–200mM NaCl, which confirms the findings of former salinity tolerant (ST) with 13.0% WLR at 15 days of 200mM studies, so that ST could be applied in moderate saline soil of NaCl stress and relatively salinity sensitive (SS) with 100%WLR. tropical areas. The high variation of salinity tolerance may come from the high genetic diversity of S. guianensis (Tang et al., 2009; Jiang The Expression Pattern of Genes Involved et al., 2017). Based on our previous study, WLR is a good in Signaling and Transporters physiological parameter for the screening of salinity-tolerant Ca2+ is one of the very important intracellular second messenger Stylosanthes spp. (Liu et al., 2017). This study showed that molecules involved in many signal transduction pathways in WLR is also a good parameter for S. guianensis accessions. plants (Seifikalhor et al., 2019). The latest research showed WLR can reflect the salinity stress symptoms from the whole that glycosyl inositol phosphorylceramide (GIPC) sphingolipids plant level. Other physiological parameters such as chlorophyll in the plasma membrane act as Na+ receptors for sensing Frontiers in Sustainable Food Systems | www.frontiersin.org 21240 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes FIGURE 10 | Differentially expressed genes in zeatin biosynthesis KEGG pathway in comparisons of salt ST_salt SS; red denotes upregulated genes. Frontiers in Sustainable Food Systems | www.frontiersin.org 21251 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes Na+ in the apoplastic and then gate Ca2+ influx channels Auxin plays a major role in regulating plant growth and in plants (Jiang et al., 2019). Increased concentrations of the development. Some studies report that high salt stress is linked Ca2+ activate the classical salt overly sensitive (SOS) signaling with greatly remodeled root architecture by altering auxin pathway (SOS1, SOS2, and SOS3) (Zhang et al., 2021). The accumulation and its redistribution (Petersson et al., 2009; Wang activity of the SOS1 exchanger is regulated through protein et al., 2009). In this study, auxin-induced protein (c40459_g1) phosphorylation by the SOS2/SOS3 kinase complex; SOS2 is had a significant increase in salt ST compared to salt SS, a Ser-Thr protein kinase belonging to the SNF1-related kinase indicating that auxin may increase in ST than in SS and (SnRK) family and SOS3 is a myristoylated Ca2+ sensor contribute to salinity tolerance of ST. CKs are involved in many (Manishankar et al., 2018). Annexins are calcium-dependent physiological and biochemical processes in plants, including cell lipid-binding proteins spread through the fungi, plants, animals, division, reproductive capacity, leaf senescence, and adaptation archaea, and prokaryotes, which exhibit the conserved core to abiotic stresses; however, CKs play negative roles in plant salt domains in their protein structure (Yadav et al., 2018). Annexins tolerance (Yu et al., 2020). Cytokinin dehydrogenase (CKXs) is are Ca2+ and phospholipid binding proteins, facilitate Ca2+ the key enzyme involved in CK metabolism and can effectively conductance across the plasma membrane, and sense the Ca2+ reduce the CK concentration in plants, an increase of CKXs changes in the cell (Saad and Ben Romdhane, 2020). Ca2+ has been shown to cause sensitivity to salt stress in Arabidopsis transmembrane transport (c34262_g2) and annexin (c34262_g1) (Nishiyama et al., 2011). RT-PCR showed that CKXs (c38854_g1) showed a significant increase in salt ST compared to salt SS, had a significant increase in salt ST, and that in consequence indicating that higher Ca2+ accumulation in ST cytoplasm may zeatin biosynthesis KEGG pathway showed that CKX was lead to activate SOS pathway or other salinity tolerance pathways significantly increased as well in salt ST compared to salt SS in ST, which contribute to the high salinity tolerance of ST. (Figure 10). A reduction of cytokinin biosynthesis in the root Cysteine-rich receptor-like kinases (CRKs) are one kind of system and the subsequent reduction of the cytokinin supply in upstream signalingmolecules and act as sensing stress signals and the shoot could alter the gene expression network and could elicit responses to various abiotic stresses in plant (Zhang et al., 2018). appropriate responses to ameliorate salinity stress (Tran et al., About 37–170 members of the CRK family in monocots and 2010; Nishiyama et al., 2011). dicots were found, but their physiological roles and functions on a biochemical and cellular level remain largely uncharacterized. A previous study found that the extracellular domains of typical The Expression Pattern of Genes Involved CRKs contain two unknown function 26 (DUF26) configuration in Transcription Factor and Antioxidant of conserved cysteines C-X8-C-X2-C, the DUF26 domain has Enzyme antifungal activity and plays a crucial role in salt stress resistance NAC transcription factors (TFs) belong to a unique class of (Zhang et al., 2009). Cysteine receptor-like protein kinase 25 transcription factors in plants, which play important roles (c41881_g3) showed a significant increase in salt ST compared in multiple biological processes including salinity tolerance to salt SS, indicating that CRK may contribute to the salinity (Dudhate et al., 2021). A recent study found that NAC tolerance of ST. TFs could cause the accumulation of proline and glycine Maintaining a dynamic balance of ions under salinity betaine to alleviate or avoid the negative effects of ROS in stress is an important strategy for plants, salinity-tolerant plants maintain the ion balance by excreting Na+ soybean (Li et al., 2021). RT-PCR showed that NAC-like out of the transcription factor (c32634_g1) and peroxidase (c41938_g5) cell or compartmentalizing Na+ into the vacuole to avoid had a significant increase in salt ST compared to salt SS, salinity damages (Zhao et al., 2020). Plasma membrane and suggesting that high antioxidant ability may play an essential vacuolar membrane transporters or ion channels such as Na+ role in salinity tolerance of salt ST. Interestingly, overexpression /H+ antiporters (NHX), Ca2+/H+ antiporter (CAX), high- of the annexin gene TdANN12 in transgenic tobacco improves affinity K+ transporter (HKT), Ca2+-activated vacuolar channel stress tolerance through ROS removal (Saad and Ben Romdhane, (TPK1/VK), and slow anion channel-associated 1 (SLAC1) 2020). play a leading role in mediating the excretion or deposit of Na+ in plants (Pantoja, 2021). In this study, cation/H+ antiporter (c25614_g1), nodulin MtN21/EamA-like transporter family protein (c34374_g1), and vacuolar amino acid transporter CONCLUSIONS (c34502_g2) were significant increased in salt ST compared to salt SS, indicating that salinity stress upregulated many ion There was high variation of salinity tolerance in S. guianensis transporters, which led to a better ion homeostasis in ST. accessions, CIAT11365 was a relatively salinity-tolerant accession, which can survive between 100 and 200mM NaCl. Transcriptomic analysis showed that an increase of The Expression Pattern of Genes Involved Ca2+ signal transduction and Na+ transport ability, salinity in Plant Hormone tolerance-related transcription factors and antioxidant ability, Response to salinity stress requires the integration and as well as an increase of auxin, and inhibition of cytokinin coordination of multiple hormones such as abscisic acid (ABA), may contribute to the salinity tolerance of CIAT11365. In jasmonic acid (JA), gibberellic acid (GA), ethylene (ET), salicylic consequence, CIAT 11365 could be utilized in moderate saline acid (SA), cytokinin (CKs), and auxin (Ryu and Cho, 2015). soil of tropical areas. Frontiers in Sustainable Food Systems | www.frontiersin.org 21262 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes DATA AVAILABILITY STATEMENT FUNDING The datasets presented in this study can be found in online This work was funded by the Central Public-interest Scientific repositories. The names of the repository/repositories Institution Basal Research Fund for Chinese Academy of and accession number(s) can be found at: NCBI Tropical Agricultural Sciences (1630032021005), the Key [accession: PRJNA771864]. Research and Development Program of Hainan (ZDYF2019078), the Hainan Provincial Natural Science Foundation of China (321RC646), the National Science and Technology Basic AUTHOR CONTRIBUTIONS Resources Investigation Project (2017FY100600), the National Tropical Plants Germplasm Resource Center, and the Modern YL and GL conceived the study as well as participated Agro-industry Technology Research System (CARS-34). in its design and coordination. YL carried out all salinity treatment experiments. YL, DK, and WW SUPPLEMENTARY MATERIAL analyzed the data. YL, HY, SD, MA, BX, and WW wrote the manuscript and revised the manuscript. All The Supplementary Material for this article can be found authors contributed to the article and approved the online at: https://www.frontiersin.org/articles/10.3389/fsufs. submitted version. 2022.725656/full#supplementary-material REFERENCES Pantoja, O. (2021). Recent advances in the physiology of ion channels in plants. Annu. Rev. Plant Biol. 72, 463–495. Abiala, M. A., Abdelrahman, M., Burritt, D. J., and Tran, L.-S. P. (2018). doi: 10.1146/annurev-arplant-081519-035925 Salt stress tolerance mechanisms and potential applications of legumes Petersson, S. V., Johansson, A. I., Kowalczyk, M., Makoveychuk, A., Wang, for sustainable reclamation of salt-degraded soils. Land Degrad. Dev. 29, J. Y., Moritz, T., et al. (2009). An auxin gradient and maximum in the 3812–3822. doi: 10.1002/ldr.3095 Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA Deinlein, U., Stephan, A. B., Horie, T., Luo, W., Xu, G. H., and Schroeder, J. distribution and synthesis. Plant Cell 21, 1659–1668. doi: 10.1105/tpc.109.06 I. (2014). Plant salt-tolerance mechanisms. Trends Plant Sci. 19, 371–379. 6480 doi: 10.1016/j.tplants.2014.02.001 Ryu, H., and Cho, Y.-G. (2015). Plant hormones in salt stress tolerance. J. Plant Dong, R., Zhang, J., Huan, H., Bai, C., Chen, Z., and Liu, G. (2017). High salt Biol. 58, 147–155. doi: 10.1007/s12374-015-0103-z tolerance of a bradyrhizobium strain and its promotion of the growth of Saad, R. B., and Ben Romdhane, W. (2020). Insights into plant annexins Stylosanthes guianensis. Int. J. Mol. Sci. 18:1625. doi: 10.3390/ijms18081625 function in abiotic and biotic stress tolerance. Plant Signal. Behav. 15:1699264. Dudhate, A., Shinde, H., Yu, P., Tsugama, D., Gupta, S. K., Liu, S., et al. doi: 10.1080/15592324.2019.1699264 (2021). Comprehensive analysis of NAC transcription factor family uncovers Seifikalhor, M., Aliniaeifard, S., and Shomali, A. (2019). Calcium signaling and drought and salinity stress response in pearl millet (Pennisetum glaucum). BMC salt tolerance are diversely entwined in plants. Plant Signal. Behav. 14:1665455. Genomics 22:70. doi: 10.1186/s12864-021-07382-y doi: 10.1080/15592324.2019.1665455 Guo, Y., Sheng, Q., Li, J., Ye, F., Samuels, D. C., and Shyr, Y. (2013). Large scale Tang, Y., Hu, X., Guo, J., Bai, C., and He, H. (2009). Genetic diversity of comparison of gene expression levels by microarrays and RNAseq using TCGA Stylosanthes revealed by ISSR markers. Acta Pratacultuae Sinica 18, 57–64. data. PLoS ONE 8, e71462. doi: 10.1371/journal.pone.0071462 Tran, L.-S. P., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010). Role of Huang, C., Liu, G., and Bai, C. (2017). Identification of 12 stylosanthes cultivars by cytokinin responsive two-component system in ABA and osmotic stress SRAP molecular markers.Mol. Plant Breed. 15, 2856–2862. signalings. Plant Signal. Behav. 5, 148–150. doi: 10.4161/psb.5.2.10411 Ivushkin, K., Bartholomeus, H., Bregt, A. K., Pulatov, A., Kempen, B., and De Wang, Y., Li, K., and Li, X. (2009). Auxin redistribution modulates plastic Sousa, L. (2019). Global mapping of soil salinity change. Remote Sens. Environ. development of root system architecture under salt stress in Arabidopsis 231:111260. doi: 10.1016/j.rse.2019.111260 thaliana. J. Plant Physiol. 166, 1637–1645. doi: 10.1016/j.jplph.2009.04.009 Jiang, Y., Shen, Q., Ding, X., Yan, L., Liu, G., and Bai, C. (2017). Phenotypic Wu, F., Yu, X., Liu, F., Bai, C., and Liu, G. (2013). Comparative analysis of salt diversity analysis of Stylosanthes germplasms. Pratacult. Sci. 34, 1032–1041. tolerance of four cultivars of stylosanthes. J. Trop. Biol. 4, 36–42. Jiang, Z., Zhou, X., Tao, M., Yuan, F., Liu, L., Wu, F., et al. (2019). Plant cell-surface Yadav, D., Boyidi, P., Ahmed, I., and Kirti, P. B. (2018). Plant annexins and GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572, 341–346. their involvement in stress responses. Environ. Exp. Bot. 155, 293–306. doi: 10.1038/s41586-019-1449-z doi: 10.1016/j.envexpbot.2018.07.002 Li, M., Chen, R., Jiang, Q., Sun, X., Zhang, H., and Hu, Z. (2021). GmNAC06, Yu, Z., Duan, X., Luo, L., Dai, S., Ding, Z., and Xia, G. (2020). How plant a NAC domain transcription factor enhances salt stress tolerance in soybean. hormones mediate salt stress responses. Trends Plant Sci. 25, 1117–1130. Plant Mol. Biol. 105, 333–345. doi: 10.1007/s11103-020-01091-y doi: 10.1016/j.tplants.2020.06.008 Liu, Y., Feng, Y., Ding, X., Chen, Z., Huang, C., Dong, R., et al. (2017). Synthetical Zelm, E. V., Zhang, Y., and Testerink, C. (2020). Salt tolerance evaluation of salinity tolerance of 67 Stylosanthes Sw. materials. Chin. J. Trop. mechanisms of plants. Annu. Rev. Plant Biol. 71, 403–433. Crops 38, 1–7. doi: 10.1146/annurev-arplant-050718-100005 Manishankar, P., Wang, N., Köster, P., Alatar, A. A., and Kudla, J. (2018). Calcium Zhang, H., Zhu, J., Gong, Z., and Zhu, J.-K. (2021). Abiotic stress signaling during salt stress and in the regulation of ion homeostasis. J. Exp. Bot. responses in plants. Nat. Rev. Genet. 23, 104–119. doi: 10.1038/ 69, 4215–4226. doi: 10.1093/jxb/ery201 s41576-021-00413-0 Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Zhang, L., Tian, L. H., Zhao, J. F., Song, Y., Zhang, C. J., and Guo, Y. (2009). Plant Biol. 59, 651–681. doi: 10.1146/annurev.arplant.59.032607.092911 Identification of an apoplastic protein involved in the initial phase of salt stress Nishiyama, R., Watanabe, Y., Fujita, Y., Le, D. T., Kojima, M., Werner, T., et al. response in rice root by two-dimensional electrophoresis. Plant Physiol. 149, (2011). Analysis of cytokinin mutants and regulation of cytokinin metabolic 916–928. doi: 10.1104/pp.108.131144 genes reveals important regulatory roles of cytokinins in drought, salt and Zhang, Z.W. J., Jin,W., Ge, D., Liu, K., Lü, F., and Sun, J. (2018). Identification and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23, 2169–2183. expression analysis of CRK gene family in upland cotton. Sci. Agricult. Sinica 51, doi: 10.1105/tpc.111.087395 2442–2461. Frontiers in Sustainable Food Systems | www.frontiersin.org 21273 March 2022 | Volume 6 | Article 725656 Liu et al. Salinity Tolerance Mechanism in Stylosanthes Zhao, C., Zhang, H., Song, C., Zhu, J.-K., and Shabala, S. (2020). Mechanisms this article, or claim that may be made by its manufacturer, is not guaranteed or of plant responses and adaptation to soil salinity. Innovation 1:100017. endorsed by the publisher. doi: 10.1016/j.xinn.2020.100017 Copyright © 2022 Liu, Kong, Yang, Douxchamps, Atieno, Xu, Wang and Conflict of Interest: The authors declare that the research was conducted in the Liu. This is an open-access article distributed under the terms of the absence of any commercial or financial relationships that could be construed as a Creative Commons Attribution License (CC BY). The use, distribution or potential conflict of interest. reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in Publisher’s Note: All claims expressed in this article are solely those of the authors this journal is cited, in accordance with accepted academic practice. No use, and do not necessarily represent those of their affiliated organizations, or those of distribution or reproduction is permitted which does not comply with these the publisher, the editors and the reviewers. Any product that may be evaluated in terms. Frontiers in Sustainable Food Systems | www.frontiersin.org 21284 March 2022 | Volume 6 | Article 725656 Advantages 90 of publishing OPEN ACCESS FAST PUBLICATION Articles are free to read Around 90 days in Frontiers for greatest visibility from submission and readership to decision HIGH QUALITY PEER-REVIEW TRANSPARENT PEER-REVIEW Rigorous, collaborative, Editors and reviewers and constructive acknowledged by name peer-review on published articles Frontiers Avenue du Tribunal-Fédéral 34 1005 Lausanne | Switzerland Visit us: www.frontiersin.org Contact us: frontiersin.org/about/contact REPRODUCIBILITY OF DIGITAL PUBLISHING RESEARCH Articles designed Support open data for optimal readership and methods to enhance across devices research reproducibility FOLLOW US IMPACT METRICS EXTENSIVE PROMOTION LOOP RESEARCH NETWORK @frontiersin Advanced article metrics Marketing Our network track visibility across and promotion increases your digital media of impactful research article’s readership