Received: 12 April 2021 Revised: 9 July 2021 Accepted: 14 July 2021 DOI: 10.1002/ppp3.10225 R E S E A R CH A R T I C L E Extinction risk of Mesoamerican crop wild relatives Bárbara Goettsch1 | Tania Urquiza-Haas2 | Patricia Koleff2 | Francisca Acevedo Gasman2 | Araceli Aguilar-Meléndez3 | Valeria Alavez4,5 | Gabriel Alejandre-Iturbide6 | Flavio Aragon Cuevas7 | César Azurdia Pérez8 | Jamie A. Carr9 | Gabriela Castellanos-Morales10 | Gabriel Cerén11 | Aremi R. Contreras-Toledo12 | María Eugenia Correa-Cano13 | Lino De la Cruz Larios14 | Daniel G. Debouck15 | Alfonso Delgado-Salinas16 | Emma P. Gomez-Ruiz17 | Manuel González-Ledesma18 | Enrique González-Pérez19 | Mariana Hernández-Apolinar20 | Braulio E. Herrera-Cabrera21 | Megan Jefferson22 | Shelagh Kell23 | Rafael Lira-Saade24 | Francisco Lorea-Hernández25 | Mahinda Martínez26 | Alicia Mastretta-Yanes2,27 | Nigel Maxted23 | Jenny Menjívar11 | María de los Angeles Mérida Guzmán28 | Aura J. Morales Herrera29 | Oswaldo Oliveros-Galindo2 | M. Andrea Orjuela-R.2 | Caroline M. Pollock1 | Martín Quintana-Camargo12 | Aaron Rodríguez30,31 | José Ariel Ruiz Corral14 | José de Jesús Sánchez González14 | Guillermo Sánchez-de la Vega32 | Mariella Superina33 | Wolke Tobon Niedfeldt2 | Marcelo F. Tognelli34 | Ofelia Vargas-Ponce30,31 | Melania Vega4,5 | Ana Wegier4 | Pilar Zamora Tavares35 | Richard K. B. Jenkins1 1Global Species Programme, International Union for Conservation of Nature (IUCN), Cambridge, UK 2Comision Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO), Mexico City, Mexico 3Centro de Investigaciones Tropicales, Universidad Veracruzana, Xalapa, Mexico 4Laboratorio de Genética de la Conservacion, Jardín Botánico, Instituto de Biología, Universidad Nacional Autonoma de México, Mexico City, Mexico 5Posgrado en Ciencias Biologicas, Universidad Nacional Autonoma de México, Mexico City, Mexico 6CIIDIR Unidad Durango, Instituto Politécnico Nacional COFAA, Durango, Mexico 7Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Etla, Mexico 8Consejo Nacional de Areas Protegidas (CONAP), Guatemala City, Guatemala 9Sustainability Research Institute, School of Earth and Environment, Faculty of Environment, University of Leeds, Leeds, UK 10Departamento de Conservacion de la Biodiversidad, El Colegio de la Frontera Sur, Unidad Villahermosa, Villahermosa, Mexico 11Museo de Historia Natural de El Salvador. Ministerio de Cultura, San Salvador, El Salvador 12Centro Nacional de Recursos Genéticos, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Tepatitlán de Morelos, Mexico 13Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn, UK 14Departamento de Produccion Agrícola, Centro Universitario de Ciencias Biologicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Mexico 15Programa de Recursos Genéticos, Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia 16Departamento de Botánica, Instituto de Biología, Universidad Nacional Autonoma de México, Mexico City, Mexico This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. © 2021 International Union for Conservation of Nature. Plants, People, Planet published by John Wiley & Sons Ltd on behalf of New Phytologist Foundation. Plants People Planet. 2021;3:775–795. wileyonlinelibrary.com/journal/ppp3 775 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 776 GOETTSCH ET AL. 17Facultad de Ciencias Biologicas, Universidad Autonoma de Nuevo Leon, San Nicolás de los Garza, Mexico 18Centro de Investigaciones Biologicas, Universidad Autonoma del Estado de Hidalgo, Pachuca, Mexico 19Campo Experimental Bajío-INIFAP, Celaya, Mexico 20Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autonoma de México, Mexico City, Mexico 21Programa de Postgrado Estrategias para el Desarrollo Agrícola Regional, Colegio de Postgraduados-Campus Puebla, Santiago Momoxpan, Puebla, Mexico 22School of Life Sciences, Anglia Ruskin University, Cambridge Campus, Cambridge, UK 23School of Biosciences, University of Birmingham, Birmingham, UK 24Laboratorio de Recursos Naturales, UBIPRO, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autonoma de México, Tlalnepantla, Mexico 25Instituto de Ecología, A. C., Xalapa, Mexico 26Licenciatura en Biología, Facultad de Ciencias Naturales, Universidad Autonoma de Querétaro, Querétaro, Mexico 27Consejo Nacional de Ciencia y Tecnología (CONACyT), Mexico City, Mexico 28Disciplina de Recursos Genéticos, Instituto de Ciencia y Tecnología Agrícolas (ICTA), Villa Nueva, Guatemala 29Centro Nacional de Tecnología Agropecuaria y Forestal “Enrique A lvarez Cordova” (CENTA), Ciudad Arce, El Salvador 30Herbario Luz María Villarreal de Puga, Instituto de Botánica (IBUG), Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biologicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Mexico 31Laboratorio Nacional de Identificacion y Caracterizacion Vegetal (LaniVeg), Centro Universitario de Ciencias Biologicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Mexico 32Laboratorio de Evolucion Molecular y Experimental, Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autonoma de México, Mexico City, Mexico 33Instituto de Medicina y Biología Experimental de Cuyo, CCT CONICET Mendoza-UNCuyo, Mendoza, Argentina 34American Bird Conservancy, The Plains, Virginia, USA 35Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biologicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Mexico Correspondence Bárbara Goettsch, Global Species Programme, Societal Impact Statement International Union for Conservation of Crop wild relatives (CWR) are plant taxa closely related to crops and are a source of Nature (IUCN), Cambridge, UK. Email: bgoettsch1@gmail.com high genetic diversity that can help adapt crops to the impacts of global change, par- ticularly to meet increasing consumer demand in the face of the climate crisis. CWR Funding information Darwin Initiative, Grant/Award Number: provide vital ecosystem services and are increasingly important for food and nutrition 23-007; Toyota Motor Company, Grant/Award security and sustainable and resilient agriculture. They therefore are of major biologi- Number: IUCN-Toyota Red List Partnership cal, social, cultural and economic importance. Assessing the extinction risk of CWR is essential to prioritise in situ and ex situ conservation strategies in Mesoamerica to guarantee the long-term survival and availability of these resources for present and future generations worldwide. Summary • Ensuring food security is one of the world's most critical issues as agricultural sys- tems are already being impacted by global change. Crop wild relatives (CWR)—wild plants related to crops—possess genetic variability that can help adapt agriculture to a changing environment and sustainably increase crop yields to meet the food security challenge. • Here we report the results of an extinction risk assessment of 224 wild relatives of some of the world's most important crops (i.e. chilli pepper, maize, common bean, avocado, cotton, potato, squash, vanilla and husk tomato) in Mesoamerica— an area of global significance as a centre of crop origin, domestication and of high CWR diversity. • We show that 35% of the selected CWR taxa are threatened with extinction according to The International Union for Conservation of Nature (IUCN) Red List demonstrates that these valuable genetic resources are under high anthropogenic 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GOETTSCH ET AL. 777 threat. The dominant threat processes are land use change for agriculture and farming, invasive and other problematic species (e.g. pests, genetically modified organisms) and use of biological resources, including overcollection and logging. The most significant drivers of extinction relate to smallholder agriculture—given its high incidence and ongoing shifts from traditional agriculture to modern practices (e.g. use of herbicides)—smallholder ranching and housing and urban development and introduced genetic material. • There is an urgent need to increase knowledge and research around different aspects of CWR. Policies that support in situ and ex situ conservation of CWR and promote sustainable agriculture are pivotal to secure these resources for the benefit of current and future generations. K E YWORD S agrobiodiversity, conservation, crop wild relatives, extinction risk, food security, IUCN Red List, threat drivers, threatened species 1 | INTRODUCTION conditions, and have not passed through the domestication genetic bottleneck (Maxted et al., 1997; Tanksley & McCouch, 1997). There- Reducing the environmental impact of agriculture and simultaneously fore, it is so far recognised that they have undergone evolutionary feeding an exponentially growing human population in the face of processes without human intervention and sustain a breadth of climate change (Godfray et al., 2010; Vermeulen et al., 2012) is one of genetic diversity not found in crops (FAO, 2008; Flores-Hernández the world's most pressing challenges. The effects of climate change et al., 2018; Hawkes et al., 2000; Mariac et al., 2006; Maxted & on agriculture are already observed (Banerjee et al., 2018; Brás Kell, 2009; van de Wouw et al., 2001; Vaughan, 1994). However, et al., 2021; Gourdji et al., 2015; Huq et al., 2015; Jaramillo there is ethnobotanical evidence that suggests that some artificial et al., 2011; Läderach et al., 2017) and are expected to worsen with- selection could have been exerted on CWR. Recent studies indicate a out mitigation and adaptation actions (Barros & Field, 2014; Campbell range of human management practices of wild resources, including et al., 2016; Dawson et al., 2016; Lobell et al., 2011; Porter Mesoamerican CWR, which probably were sustained over long et al., 2014) with overall global crop yield declines between 3% and periods of time (Casas et al., 2016; de Luna-Ruiz et al., 2018; Levis 10% predicted with each degree of warming (Challinor et al., 2014). et al., 2018). Changes to crops and varietal production resulting from climate The importance of CWR in achieving food security has long been change or through synergistic effects with other drivers caused by recognised (Ford-Lloyd et al., 2011; Harlan, 1976; Hoyt, 1988; land use change (e.g. soil degradation or loss of pollination services) Maxted et al., 1997; McCouch et al., 2013; Prescott-Allen & Prescott- include reduced genetic diversity, variable crop yields and increased Allen, 1990). Food security has become an integral element of both vulnerability to emerging pathogens and pests (FAO, 2010; Foley the agricultural and environmental sectors as is reflected in et al., 2005; Groenen, 2018; Keneni et al., 2012; Ricketts et al., 2008; international policy frameworks, including the United Nations Scheffers et al., 2016). The adaptation of crops to environmental Sustainable Development Goals (SDG). Aichi Biodiversity Target 13 of stresses such as drought, soil salinity and flooding, as well as to conse- the Convention on Biological Diversity (CBD) Strategic Plan for quent changes in the prevalence of pests and diseases, while ensuring Biodiversity 2011–2020 called for the maintenance and safeguarding high nutritional value and yields, will be key in responding to food of the genetic diversity of CWR (CBD, 2010), which is also demand (Campbell et al., 2016; FAO, 2008, 2010, 2011; Ford-Lloyd highlighted in the Post 2020 Biodiversity Framework (e.g. Target et al., 2011; Guarino & Lobell, 2011; Maxted et al., 2012; Maxted 8 and Target 9; CBD, 2019). Target 2.5 of SDG 2 (Zero Hunger) calls et al., 2014; Nabhan et al., 2020; Ortiz, 2015; Zamir, 2001). For to maintain the genetic diversity of seeds, cultivated plants and example, the Mexican wild potato Solanum demissum has been used farmed and domesticated animals and their related wild species extensively in breeding programs against late blight (Ross, 1986). Like- (United Nations, 2015). wise, S. pinnatisectum and S. cardiophyllum show resistance to the Mesoamerica is a centre of origin, diversity and domestication of Colorado potato beetle (Chen et al., 2004). Thus, a rich source of crops and of important CWR diversity (Maxted & Vincent, 2021; genetic variability to help adapt crops to changing environmental con- Vavilov, 1935; Vincent et al., 2019). An estimated 8% of the world's ditions can be found in crop wild relatives (CWR)—wild plant species most important crops (Vavilov, 1935), including maize, squash, chilli related to crops—including their ancestors, which persist in a wide pepper, bean, avocado, vanilla and cotton, were domesticated in the variety of habitats and under heterogeneous environmental region around 10,000 to 5000 years ago (Clement et al., 2021; 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 778 GOETTSCH ET AL. Hummer & Hancock, 2015; Piperno & Smith, 2012). The evolutionary 2.2 | Taxa selection criteria process that results from human manipulation of plant genotypes to satisfy human requirements is still part of the domestication process in A list of approximately 3000 CWR taxa (i.e. species, subspecies, varieties the region (Hajjar & Hodgkin, 2007). Further, agriculture is a production and subpopulations; Dataset S1) belonging to the same genus of a crop process in which both cultivation and domestication of plants were cultivated or domesticated in Mesoamerica was compiled from different involved (Casas & Caballero, 1995; Perry & Flannery, 2007). sources (e.g. Acevedo Gasman et al., 2009; Azurdia et al., 2011; Bellon Accordingly, and because many of these crops are considered of global et al., 2009; Perales & Aguirre, 2008). The list included 310 high priority importance due to their food, nutritional, economic and other values CWR for Mexico (Contreras-Toledo et al., 2018), 105 taxa in Guatemala (CONABIO et al., 2019a, 2019b; Shiferaw et al., 2011; Wei (Azurdia et al., 2011), 50 taxa in El Salvador (Chízmar-Fernández et al., 2012), Mesoamerica has been identified as a global conservation et al., 2009; Echeverría et al., 2008) and around 54 taxa in Honduras priority centre in which to conduct in situ and ex situ conservation of (Núñez & Alvarado, 1995). A subset of genera and their taxa (with the CWR (Castañeda-A lvarez et al., 2016; Vincent et al., 2019). exception of Tripsacum, a tertiary gene pool relative of Zea mays) was There are good reasons to believe that a high proportion of CWR selected for the present study following a set of criteria considered occurring in Mesoamerica are threatened with extinction. Mesoamerica most relevant for the social, economic and biological characteristics of harbours an estimated 3000 endemic flowering plant species yet the region, identified during a stakeholder workshop (Methods S1). had lost more than 80% of its original native vegetation cover by the beginning of the 21st century (Mittermeier et al., 2011). The annual deforestation was calculated in 395,000 ha between 2005 and 2010 2.3 | Extinction risk assessment (Elizondo et al., 2015), making it one of the world's 36 biodiversity hotspots (Rodríguez Olivet & Asquith, 2004). Mesoamerica will We evaluated extinction risk for the selected taxa of Mesoamerican suffer severe impacts from climate change (BID and CEPAL, 2010; CWR according to the International Union for Conservation of Nature Thomas et al., 2016), yet its biodiversity holds key adaptive solutions (IUCN) Red List Categories and Criteria (IUCN, 2012) during an expert that should be conserved (e.g. genetic diversity and functional workshop (Methods S2). Information on the distribution, population genomics; Mastretta-Yanes et al., 2018). Although national trends, ecology, conservation actions, use and trade was reviewed for (e.g. SEMARNAT-2010-NOM-059; DOF, 2010) and international each taxon. As part of this process, range maps were generated using extinction risk assessments have been completed for some plant groups over 28,000 reviewed occurrence data points from different sources in the region (Goettsch et al., 2015; IUCN, 2020; Rivers, 2017), CWR (e.g. CONABIO, 2016; Crop Trust, 2016; GBIF, 2016; and personal have not been targeted. databases; Dataset S2). Data are also available on the IUCN Red List We present here the first assessment of extinction risk of wild website (IUCN, 2020). These data were used to show the spatial relatives of some of the world's most important crops that occur distribution of CWR as well as to generate richness maps (Methods within Mesoamerica. We focus on the nature of the threats affecting S3) showing areas of high CWR diversity and areas with high diversity them and discuss actions and policies that can be implemented to of threatened taxa (Methods S4). Detailed data on the threats affect- strengthen their conservation. We included CWR of six Mesoamerican ing taxa were also collated from the literature and from direct obser- staple foods of which maize, common bean, chilli pepper, husk tomato vations of the experts participating in the assessment process and and squash are typically part of the ancestral multicrop milpa system. were coded following the IUCN Threats Classification Scheme (based The milpa remains the main means of production and subsistence by on Salafsky et al., 2008; version 3.2 available from https://www. direct consumption and trade of surplus for smallholder farmers in the iucnredlist.org/resources/threat-classification-scheme). Because the region (Bellon et al., 2018; Lopez-Ridaura et al., 2021; Zizumbo- assessments for the IUCN Red List of Threatened Species are global, Villarreal & Colunga-GarcíaMarín, 2010). we assessed the extinction risk of taxa throughout their entire range. 2 | MATERIALS AND METHODS 3 | RESULTS 2.1 | Study area 3.1 | Selected taxa and their extinction risk The study focused mainly on the Mesoamerican region (Figure 1a; A total of 224 taxa of wild relatives of the following crops were selected: Kirchhoff, 1960), which includes central and southern Mexico, chilli pepper (Capsicum spp.), squash (Cucurbita spp.), cotton (Gossypium Guatemala, El Salvador and Honduras. In some instances, areas out- spp.), avocado (Persea spp.), bean (Phaseolus spp.), husk tomato (Physalis side Mesoamerica that are part of the Aridamerica region (Nabhan spp.), potato (Solanum sect. Petota), maize (Zea spp. and Tripsacum spp.) et al., 2020) such as northern Mexico were considered in the analyses and vanilla (Vanilla spp.) (Table S1). For each of the taxonomic groups, all to evaluate complete genera in which some taxa were not strictly taxa occurring within the four countries were included. In the case of distributed within Mesoamerica, thus accounting for the full extent of Solanum and Vanilla, they represent less than 10% of the total number of the geographic range of a taxon (Figure 1b,c). known taxa globally, while all known Zea taxa are included (Table S2). 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GOETTSCH ET AL. 779 F IGURE 1 (a) Mesoamerican region highlighted in yellow according to Kirchhnoff (1960). (b) Spatial distribution pattern of crop wild relative taxa based on occurrence records from herbaria. (c) Hotspots of threatened (critically endangered, endangered and vulnerable) and near-threatened crop wild relatives (see Table 1 for the respective list of taxa). In both figures, the numbers correspond to the number of taxa found in the cell; the dark green colour corresponds to the lowest number of taxa, and the dark brown colour corresponds to highest number of taxa found in a 20  20-km cell. The study area is shown in dark grey [Correction added on 17 September 2021, after first online publication: This figure was previously incorrect and has been replaced.] A high proportion (35%) (Methods S5) of the Mesoamerican CWR 3.2 | Patterns of diversity taxa assessed are threatened with extinction, including 7 Critically Endangered (CR), 48 Endangered (EN) and 16 Vulnerable (VU). Nine taxa The highest number of CWR taxa assessed in 20 km  20 km grid were assessed as Near Threatened (NT), 125 as Least Concern (LC) and cells are located in the Mexican states of Jalisco and Oaxaca with 19 as Data Deficient (DD) (Table S1). Vanilla has the highest proportion 31 and 28 taxa, respectively (Figure 1b). Other areas with high to of threatened taxa with 100% of them (eight taxa) threatened, followed medium richness, ranging from 15 to 27 taxa, are found in northern by cotton (Gossypium) with 92% (12 taxa), avocado (Persea) with 60% Mesoamerica, that is, in central Mexico, from the western states of (9 taxa) and the relatives of maize Zea and Tripsacum with 44% (four Nayarit and Jalisco through to Michoacán, Mexico State, Mexico City, taxa) and 33% (four taxa) threatened taxa, respectively (Figure 2). Puebla and Veracruz in the east (Figure 1b). 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 780 GOETTSCH ET AL. F IGURE 2 Proportion of taxa in each genus related to the selected crops by IUCN Red List category (CR = critically endangered, EN = endangered, VU = vulnerable, NT = near threatened, DD = data deficient, LC = least concern). Solanum (n = 26), Physalis (n = 67, 63 species and 4 subspecies), Capsicum (n = 4), Gossypium (n = 13), Cucurbita (n = 11, 9 species and 2 subspecies), Phaseolus (n = 55), Zea (n = 11, 4 species, 3 subspecies and 4 subpopulations), Tripsacum (n = 11), Vanilla (n = 8) and Persea (n = 18) 3.3 | Hotspots of threatened taxa is agriculture. In Mesoamerica agricultural production systems and their associated management intensity can vary, but smallholder The highest number of threatened (CR, EN and VU) and NT taxa is agriculture and cattle ranching occupy the majority of agricultural found in a grid cell in the eastern Mexican state of Veracruz and lands. Invasive and other problematic species is the next most includes seven threatened CWR, including four Persea, two Vanilla common threat, reported for 38% (51) of taxa with identified threats, and one Phaseolus (Cell 1, Figure 1c; Table 1). Seven other areas con- followed by biological resource use (threats from consumptive use of tain six threatened and NT taxa each. Four of them are in Veracruz “wild” biological resources, including genetic resources, organisms or (Cells 3–6, Figure 1c), and together they harbour four Persea and two parts thereof, populations, or any other biotic component of the Physalis taxa and one taxon each of Cucurbita and Capsicum (Table 1). ecosystem with actual or potential use or value for humanity, resulting Another hotspot borders the state of Veracruz and Hidalgo and from removing them from the system or destroying them) affecting includes two Persea taxa, two Solanum, one Physalis and one 32% (43) of taxa with threats (Figure S1). Other salient threats are Phaseolus, while a hotspot in Oaxaca harbours five Persea and one residential and commercial development disturbing 25% (34) of these Vanilla (Cell 2, Table 1). Finally, an area bordering Chiapas and taxa and climate change and severe weather impacting 21% (28; Guatemala has six threatened Vanilla. Seven more cells with five Figure S2). threatened taxa each (one Capsicum, one Persea, two Phaseolus and Across all taxonomic groups, the more frequent proximate drivers one Solanum) were found in Guatemala in parts of the departments of of threats (i.e. the ultimate factor enabling or contributing to the Chimaltenango, Sacatepéquez, Guatemala and Escuintla and in threat process; Salafsky et al., 2008) varied. Smallholder agriculture Mexico in the states of Jalisco, Puebla, Oaxaca and Veracruz (Cells affects 32% of taxa (43), and smallholder ranching affects 31% 9–15, Figure 1c). Note that in all 15 cells mentioned above, only (42 taxa), possibly because of its frequency and extent, as smallholder 32 taxa out 80 threatened taxa are represented and only 2 CR taxa agriculture generally has a lower impact than agro-industrial farming (Vanilla cribbiana and Zea perennis) are found (Table 1). Also, taxa in systems and can sometimes provide evosystem services (Faith different cells might represent different populations and hence et al., 2010). Other threat drivers are housing and urban development genetic variability (Tobon et al. unpublished). (22%, 29 taxa), introduced genetic material (16%, 21 taxa), problem- atic native species such as pests (15%, 20 taxa), agro-industrial farming, small-scale incidental logging and climate change in the form 3.4 | Threats to Mesoamerican CWR of habitat shifting or alteration, each affecting 14% (19 taxa) (Figure 3). Threats were identified and coded according to the IUCN Threat Clas- The main drivers of threat differ for each taxonomic group. Persea sification Scheme (version 3.2) for 134 taxa (60% of evaluated taxa). (71% of taxa), Physalis (54%) and Solanum (46%) are affected by small- The most common threat process (i.e. direct human activities holder ranching, while for Capsicum (75%) and Zea (67%) the most fre- responsible for the degradation, destruction and/or impairment of quent driver of threat is smallholder agriculture and for Cucurbita biodiversity; Salafsky et al., 2008) affecting 65% (87) of these 134 taxa (100%) agro-industrial farming. The most common threat driver 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GOETTSCH ET AL. 781 TABLE 1 Cells in Mexico (except number 15 in Guatemala) with the highest number of threatened (IUCN category CR = critically endangered, EN = endangered and VU = vulnerable) and near-threatened (NT) taxa as shown in Figure 1c Cell number as shown Number of threatened State/department Taxa found at the cell and in Figure 1c taxa in the cell the cell is in their IUCN category in (). 1 7 Veracruz Persea chamissonis (EN) Persea cinerascens (EN) Persea longipes (EN) Persea schiedeana (EN) Phaseolus chiapasanus (EN) Vanilla inodora (EN) Vanilla pompona (EN) 2 6 Puebla Persea cinerascens (EN) Persea schiedeana (EN) Phaseolus dasycarpus (EN) Physalis campánula (NT) Solanum oxycarpum (EN) Solanum tarnii (EN) 3 6 Veracruz Capsicum lanceolatum (EN) Persea chamissonis (EN) Persea longipes (EN) Persea pallescens (EN) Persea schiedeana (EN) Physalis greenmanii (EN) 4 6 Veracruz Capsicum lanceolatum (EN) Persea chamissonis (EN) Persea longipes (EN) Physalis campanula (NT) Physalis greenmanii (EN) Solanum oxycarpum (EN) 5 6 Veracruz Cucurbita okeechobeensis ssp. martinezii (NT) Persea longipes (EN) Persea schiedeana (EN) Physalis campanula (EN) Physalis greenmanii (EN) Solanum oxycarpum (EN) 6 6 Veracruz Cucurbita okeechobeensis ssp. martinezii (NT) Persea schiedeana (EN) Physalis campanula (EN) Physalis greenmanii (EN) Solanum oxycarpum (EN) Vanilla insignis (EN) 7 6 Oaxaca Persea albida (EN) Persea cinerascens (EN) Persea longipes (EN) Persea pallescens (EN) Persea rufescens (EN) Vanilla planifolia (EN) 8 6 Chiapas Vanilla cribbiana (CR) Vanilla hartii (EN) (Continues) 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 782 GOETTSCH ET AL. TABLE 1 (Continued) Cell number as shown Number of threatened State/department Taxa found at the cell and in Figure 1c taxa in the cell the cell is in their IUCN category in (). Vanilla inodora (EN) Vanilla insignis (EN) Vanilla odorata (EN) Vanilla planifolia (EN) 9 5 Jalisco Cucurbita radicans (EN) Persea hintonii (VU) Phaseolus albescens (VU) Physalis aggregata (VU) Solanum trifidum (NT) 10 5 Jalisco Persea hintonii (VU) Phaseolus albescens (VU) Physalis lignescens (EN) Solanum trifidum (NT) Zea perennis (CR) 11 5 Veracruz Cucurbita okeechobeensis ssp. martinezii (NT) Persea schiedeana (EN) Physalis greenmanii (EN) Solanum schenckii (EN) Vanilla insignis (EN) 12 5 Veracruz Persea pallescens (EN) Persea schiedeana (EN) Physalis greenmanii (EN) Solanum schenckii (EN) Vanilla odorata (EN) 13 5 Oaxaca Persea albida (EN) Persea chamissonis (EN) Persea pallescens (EN) Persea rufescens (EN) Persea schiedeana (EN) 14 5 Oaxaca Persea longipes (EN) Persea schiedeana (EN) Vanilla inodora (EN) Vanilla planifolia (EN) Vanilla pompona (EN) 15 5 Sacatepequez Capsicum lanceolatum (EN) Persea schiedeana (EN) Phaseolus dumosus (EN) Phaseolus macrolepis (EN) Solanum clarum (VU) Note that only 32 taxa/80 threatened taxa are represented, 24/48 (EN), 2/7 (CR), 4/16 (VU) and 2/7 (NT) affecting Gossypium (46%) is development for tourism and recreation For 12% (26) of taxa assessed the threats are unknown, and these and overcollection for Vanilla (100%). For Phaseolus (50%), native corresponded to taxa categorised as DD (13 taxa), LC (10 taxa) and pests and diseases are the main driver, while Tripsacum (70%) are EN (three taxa). For 28% (62 taxa), there are no known threats or no mainly affected by nonnative invasive species (Figure 3). significant threats; this is particularly true for wide-ranging taxa. In 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GOETTSCH ET AL. 783 F IGURE 3 Proportion of taxa in each genus related to the selected crops affected by the different threat drivers according to the International Union for Conservation of Nature (IUCN) Threat Classification Scheme (version 3.2). Only those taxa with threat information were included (n = 134). 1.1 housing and urban areas, 1.2 commercial and industrial areas, 1.3 tourism and recreation areas, 2.1.1 shifting agriculture, 2.1.2 smallholder agriculture, 2.1.3 agro-industry farming, 2.2.1 smallholder plantations, 2.2.2 agro-industry plantations, 2.3.1 nomadic grazing, 2.3.2 smallholder grazing or ranching, 2.3.3 agro-industry grazing, ranching or farming, 2.3.4 scale unknown/unrecorded, 3.1 oil and gas drilling, 3.2 mining and quarrying, 4.1 roads and railroads, 5.2.1 intentional human use, 5.2.3 persecution/control, 5.3.3 unintentional effects of small scale wood harvesting, 5.3.4 unintentional effects of large scale logging, 5.3.5 motivation unknown/unrecorded, 6.1 recreational activities, 6.2 war, civil unrest and military exercises, 7.1 fire and fire suppression, 7.2 dams and water management/use, 7.3 other ecosystem modifications, 8.1 invasive alien species, 8.2 problematic native species, 8.3 introduced genetic material, 8.4 problematic species/disease of unknown origin, 8.5 viral/prion - induced diseases, 8.6 diseases of unknown cause, 9.3.3 herbicides and pesticides, 10.1 volcanoes, 11.1 habitat shifting and alteration, 11.2 drought, 11.3 temperature extremes and 11.4 storms and flooding many cases the latter are exposed to stressors in parts of their range taxa (91%) followed by Vanilla (75%) and Solanum (65%) (Figure S3). but no evidence linked these to significant wider population declines. The most common direct end use is for human food (48%) with 31% Note that because threats at the subspecific level are also recorded at corresponding to Physalis, 26% to Solanum and 11% to Phaseolus the species level, for those taxa assessed at the subspecific level, (Figure 4). Research (an indirect use), mainly for potential crop threats were considered for the taxon only (i.e. subspecies, varieties improvement, is the second most common end use (46% of taxa) with or subpopulations) to avoid duplication. 39% of taxa being Solanum, 23% Cucurbita and 16% Vanilla (Figure 4). Finally, 22% of taxa have been indirectly utilised for crop improve- ment with Solanum representing 62%, Phaseolus 19% and 6% 3.5 | Utilisation of Mesoamerican CWR corresponding each to Cucurbita, Persea and Zea taxa. Other not so common but relevant uses are medicinal, forage and ornamental. Thirty three percent of taxa assessed in this study are directly or indi- The genera with the highest number of taxa utilised across all rectly utilised. Cucurbita has the highest percentage of directly utilised different end uses were Cucurbita (96%), Vanilla (83%) and Solanum 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 784 GOETTSCH ET AL. F IGURE 4 Proportion of taxa for which a direct or indirect use was recorded across the most common end use categories. Food-human (n = 35), research (n = 34), establishing ex situ production (n = 16), medicine- human and veterinary (n = 12), food - animal (n = 7), horticulture (n = 6), other household goods (n = 5), poisons (n = 2) and handicrafts, jewellery (n = 2). End uses according to the IUCN General Use and Trade Classification Scheme (version 1.0) (74%) (Figure S4), while Tripsacum, Phaseolus and Physalis have the plant community which, despite covering a relatively small geographi- lowest number of utilised taxa (17%, 18% and 25%, respectively). The cal area, is renowned for its extraordinary biological diversity, diver- genera with the highest number of different uses recorded are gence among lineages and complex evolutionary history (Ornelas Gossypium, Persea and Cucurbita with 9, 8 and 7 end uses, respectively et al., 2013; Venkatraman et al., 2019). Cloud forests are also among (Figure S4). the most threatened habitats. In Mexico they cover only 1% of the land area, but 73% of their original vegetation has been lost or degraded (INEGI, 2003, 2016). Up to 99% of Mexican cloud forest 4 | DISCUSSION could disappear by 2080 due to forest clearing and climate change (Ponce-Reyes et al., 2012). Cloud forests in other parts of 4.1 | Hotspots of threatened taxa in Mesoamerica Mesoamerica have also been disappearing at an increasing rate in recent decades (Pope et al., 2015). Protected areas in this habitat play A high proportion of Mesoamerican CWR is threatened with extinc- a key role in protecting cryptic CWR (Bosland & Gonzalez, 2000); tion. With 35% of taxa being threatened (based on a best estimate; therefore, the protection of the remnants of cloud forest habitat Methods S5), levels are comparable to those reported for other plant should be a priority (CONABIO, 2010). groups such as conifers (34% threatened; IUCN, 2020) and cacti (31% Critically Endangered taxa, with the exceptions of Vanilla threatened; Goettsch et al., 2015). However, the value is more than cribbiana and Zea perennis, do not occur within hotspots of threatened twice as high as that reported for a regional assessment of European taxa. Instead, they tend to occur in areas with lower taxonomic diver- CWR (Bilz et al., 2011), where 16% (n = 572; Methods S5) of taxa sity and threatened taxa richness. This suggests that approaches were assessed as threatened. aiming to maximise the number of threatened taxa to be conserved CWR and those that are threatened are unevenly distributed (e.g. by focusing on areas harbouring high numbers of threatened across Mesoamerica. The highest values of species richness taxa) will only be useful in certain instances and that additional actions (Figure 1b) and richness of threatened taxa (Figure 1c) are found in will be required to ensure that more narrowly distributed and threat- the Mexican Transition Zone (Morrone, 2010) where the Nearctic- ened taxa are also accounted for. In addition, an important factor to Neotropic biotas overlap in a region of great geological and ecological consider in such analysis, and in particular for CWR, is the representa- complexity (Halffter, 1978; Rzedowski, 1978). The transition zone tion of genetic diversity within each taxon (Kell et al., 2012; Maxted encompasses the convergence of the Trans-Mexican Volcanic Belt in et al., 1997; Maxted & Vincent, 2021; Riordan & Nabhan, 2019). central Mexico (TMVB), Sierra Madre Oriental, Sierra Madre Occidental and Sierra Madre del Sur. The TMVB is renowned for its high plant species richness (Mastretta-Yanes et al., 2015; Rodríguez 4.2 | Threats to Mesoamerican CWR and threat et al., 2018; Sosa et al., 2018; Villaseñor et al., 2020). The transition patterns zone and other mountains of southern Mexico and Central America belong to a region known as the Mesoamerican forests, which con- As much as for the rest of biodiversity, a large proportion of assessed tains one of the richest biotas on Earth, both in terms of species rich- taxa (65%) is affected by significant habitat loss caused by human ness and endemism (Espinosa et al., 2008; Mittermeier et al., 2011). activities and in particular agriculture and farming (Maxwell Within the Mesoamerican mountains, threatened CWR taxa are et al., 2016). Mesoamerica has lost more than 80% of its native vege- often associated with cloud forest habitat—a naturally fragmented tation due to intensified agriculture in the last decades, with a recent 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GOETTSCH ET AL. 785 tendency to convert diverse, traditional and smallholder of CWR taxa (DOF, 2012; MAGA, 2019) are of great importance agroecosystems to agro-industrial systems dependent on inorganic in the region. fertilisers, pesticides and fungicides and mechanisation (Harvey Biological resource use is the third most prevalent threat process, et al., 2008). In contrast to most wild species, many CWR are adapted affecting 32% of the CWR taxa assessed (Figure S1). Though all to disturbance and can even thrive in perturbed habitats where they Vanilla, 75% of Capsicum, 53% of Persea and 18% of Phaseolus taxa are tolerated and sometimes fostered, and therefore inadvertently are affected by biological resource use, the drivers and stresses conserved (Casas & Caballero, 1995; Delgado-Salinas et al., 2004). For (i.e. the impact of a threat on a taxon) vary between taxonomic example, the threatened common bean wild relative Phaseolus groups. All Vanilla taxa are targeted for collection, making direct use dasycarpus (EN) is tolerated and abundant at the edge of smallholder the threat driving them to extinction in the wild. In contrast, taxa of arable lands (Delgado-Salinas, 2019). Similarly, the wild squash the genera Persea (e.g. P. cinerascens), Phaseolus (e.g. P. albescens) and Cucurbita radicans (EN), the wild relative of the scarlet runner bean Capsicum (e.g. C. lanceolatum) are unintentionally affected by the use Phaseolus coccineus and wild chilli pepper Capsicum annuum var. of biological resources in the form of logging and wood harvesting glabriusculum and C. frutescens are often found and fostered in agricul- activities (Figure 3), which result in both species stresses (species mor- tural fields (Aragon Cuevas, Sánchez de la Vega, et al., 2019). Con- tality) and ecosystem stresses (i.e., habitat conversion and/or habitat trastingly, other taxa are considered weeds of crops and are typically degradation; Figure 5). destroyed by farmers (e.g. in Mexico, wild populations of Cucurbita Although CWR may hold solutions to help adapt crops to argyrosperma which correspond to C. argyrosperma ssp. sororia; changing climatic conditions, they are not exempt to the effects of Castellanos Morales et al., 2019; Aguirre Dugua et al., 2020). Switches climate change themselves (Jarvis et al., 2008; Redden et al., 2015); from weed tolerant traditional agriculture to industrial agriculture, 21% of taxa are affected by the effects of climate change where herbicide and pesticide use is prevalent, are severely affecting (Figure S2), mainly through shifting and altering habitats and wild squash (Cucurbita spp.), chilli pepper wild relatives (populations of droughts (Figure 3). Capsicum annuum which correspond to the variety glabriusculum), wild While some threats can occur across multiple taxonomic groups, cotton (Gossypium aridum) and teosinte related to maize (Zea others appear specific to particular crop gene pools (Figure 3). For luxurians). Conversion of natural habitat into arable lands, including for instance, the cotton wild relatives (Gossypium aridum, G. davidsonii, G. extensive agriculture, mainly affects those wild relatives associated harkenssii and G. hirsutum) are threatened by social unsettlement as with more pristine areas. These include the wild relative of chilli pep- they occur in areas where illegal crops are grown and it is unsafe to per, Capsicum lanceolatum (EN) and the wild relative of avocado Persea conduct research or implement conservation actions for those pallescens (EN), both of which grow in the highly threatened cloud for- populations. Here we focused on the effects of individual threats on ests of Mexico (CONABIO, 2010). Similarly, much of the pine-oak taxa, yet in many instances taxa are affected by multiple threats forest, which is the natural habitat of the wild relative of maize, Zea (Figures S1 and 3) that, in conjunction, can result in a diverse suite of perennis (CR), has been converted to large avocado plantations species and ecosystem stresses (Figure 5). Although our analyses pro- (Sánchez et al., 2019) in order to supply the high demand of interna- vide useful, taxon-specific information, tools to map the spatial distri- tional markets (de la Fuente Stevens, 2014). bution of threats would be valuable for conservation planning Invasive and other problematic species is the second most purposes. common threat process identified affecting 38% of taxa assessed (Figures S1 and S2). Notably, 28% of Phaseolus taxa are impacted by pests and diseases caused by native problematic species that 4.3 | Knowledge gaps and research needs can potentially worsen with climate change. Invasive alien species (e.g. grasses such as Megathyrsus maximus and Rottboellia coc- Nineteen taxa (8.5% of all assessed) grouped in Cucurbita, Persea, hinchinensis) are affecting 23% of Tripsacum taxa (Figure 3), includ- Phaseolus, Physalis and Solanum are assessed as DD (Figure 2 and ing the EN taxa: Tripsacum intermedium, T. maizar and T. zopilotensis Table S1), meaning information is insufficient to evaluate their and also the CR wild relative of cotton Gossypium armourianum, an extinction risk and is comparable to other plant groups (e.g. cacti insular species whose habitat is affected by introduced feral goats 8.7%). This is relatively low and probably attributable to the high and cats (Wegier et al., 2017). Introduced genetic material availability of plant occurrence point data required for these threatens taxa of the genera Cucurbita, Gossypium, Zea and, to a assessments (Goettsch et al., 2015). Such data availability is the lesser extent, Tripsacum (Figure 3), through hybridisation of geneti- result of enormous efforts by numerous academic, governmental cally modified crops with wild taxa. This facilitates genetic erosion, and nongovernmental organisations to collect, compile and analyse modifies plant-insect interactions (e.g. Gossypium aridum, data and make it available, for example, through CONABIO's Wegier, 2013; G. hirsutum, Vázquez-Barrios et al., 2021) and causes National Biodiversity Information System and the Global Biodiver- habit change (e.g. Cucurbita argyrosperma ssp. sororia; Cruz-Reyes sity Information Facility (GBIF) (Troudet et al., 2017). However, et al., 2015). Therefore, efforts to frame the use and release of liv- large numbers of records remain undigitised and scattered, particu- ing modified organisms in Mesoamerica (Acevedo et al., 2016) and larly for collections in El Salvador and Honduras. A few taxa are to protect the species and areas that include the genetic diversity listed as DD because of taxonomic uncertainty (e.g. Physalis 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 786 GOETTSCH ET AL. F IGURE 5 Proportion of species and ecosystem stresses caused by different threat drivers recorded for each taxon related to the selected crops. EC = ecosystem conversion, SM = species mortality, SP = species perturbance, ISE = indirect species effect, IEE = indirect ecosystem effects, and ED = ecosystem degradation. The bars correspond to the proportion of taxa impacted by the different threat drivers. Only the main threat drivers are shown. 1.1 housing and urban areas, 1.3 tourism and recreation areas, 2.1.1 shifting agriculture, 2.1.2 smallholder agriculture, 2.1.3 agro-industry farming, 2.2.2 agro-industry plantations, 2.3.2 smallholder grazing or ranching, 4.1 roads and railroads, 5.2.1 intentional human use, 5.3.3 unintentional effects of small scale wood harvesting, 5.3.4 unintentional effects of large scale logging, 6.1 recreational activities, 7.1 fire and fire suppression, 8.1 invasive alien species, 8.2 problematic native species, 8.3 introduce genetic material, 11.1 habitat shifting and alteration and 11.3 temperature extremes longicaulis). However, for 17 taxa categorised as DD, the main their gene pool and characterize them to make these genetic constraint was the lack of accurate information on their distribu- resources more readily available for use in breeding programs tion, population status and trend and on threats and their effects. (FAO, 2017). In addition, we need to identify those plants that are Some of these taxa (e.g. Persea sessilis and Solanum guerreroense) used along the domestication gradient, as occurs in Mesoamerica were last collected over 78 years ago, while others are only known (Carrillo-Galván et al., 2020, and references therein). The most fre- from their type localities (e.g. Phaseolus leptophyllus, Physalis quent research needs identified across all taxa and for threatened latecorollata, P. parvianthera and Persea sessilis). Some taxa taxa were the generation of more information on the population (e.g. Cucurbita palmata, Persea rufescens and Solanum lesteri) are size, distribution range and trend, followed by research/monitoring reportedly known only from small areas or from a few specimens of threats and their effects on future population trends (Figure 6), and are therefore likely to be threatened. For all these taxa, which is also seen as a priority for European CWR (Bilz research to generate information on their distributions, threats and et al., 2011). For example, research is needed on the potential risk population sizes/trends is a priority (Figure 6) to assess their and monitoring of the laurel wilt pathogen (Rafaella lauricola) intro- extinction risk. Field research to locate any remaining individuals or duced by the redbay ambrosia beetle (Xyleborus glabratus), originally populations is also urgently needed for Gossypium armourianum and from Asia, which has caused vascular wilt disease and major mortal- Physalis tehuacanensis, which have been identified as Critically ity of redbay (Persea borbonia) and other species of Lauraceae in the Endangered and Possibly Extinct. United States (Harrington et al., 2008; Harrington et al., 2011). The Given their importance for food security and adaptation to most suitable areas for the introduction of X. glabratus into Mexico climate change and the level of threat they face reported here, correspond to the tropical humid, tropical subhumid and some tem- there is a need to complete floristic inventories, identify CWR and perate regions, which will impact avocado production (Lira-Noriega assess their extinction risk, also including other countries in the et al., 2018) and also its CWR. Therefore, studies of synergic effects region. Equally important is to promote research on their genetic under global change scenarios and monitoring programs are diversity to inform in situ and ex situ conservation and to establish important to design tailored CWR conservation actions. 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GOETTSCH ET AL. 787 F IGURE 6 Number of taxa in each International Union for Conservation of Nature (IUCN) Red List Category for which a research need was recorded in terms of (a) research, (b) conservation planning and/or (c) monitoring. Research needs are arranged in order of frequency. CR = critically endangered, EN = endangered, VU = vulnerable, NT = near threatened, DD = data deficient, LC = least concern 4.4 | Red listing CWR with other components of biodiversity, this process is particularly challenging for CWR because they are often directly utilised by There are at least three aspects that need to be considered when humans and thus purposefully transported and moved, making it assessing the extinction risk of CWR following the IUCN Red List Cat- common to encounter records of specimens outside their natural dis- egories and Criteria (IUCN, 2012), (1) taxonomic understanding of the tribution. Furthermore, records may belong to taxa that have escaped taxa assessed—it is common that the taxon described at the species from cultivation and present traits of the wild specimens without level belongs to the cultivated form and the CWR can be the same being strictly wild (e.g. Phaseolus coccineus; Gossypium hirsutum); these species, a subspecies or a variety. This depends on the evolutionary are known as ‘feral crops’ and when possible should not be mapped history of crop domestication; which can be complex processes within the taxon's natural range (d'Eeckenbrugge & Lacape, 2014; in species that conform to wild-to-domesticated continuums Guerra-García et al., 2017; Wegier et al., 2011). Records of hybrid (e.g. Gossypium hirsutum, Velázquez-Lopez et al., 2018; Capsicum taxa between cultivated and wild specimens should also be excluded annuum, de Luna-Ruiz et al., 2018) often resulting in different human when possible. Lastly, (3) participation of experts from the biological modifications due to cultural diversity and management heterogene- sciences, including botanists and conservationists, as well as from the ity, which can hinder the identification of CWR. The IUCN Red List agronomical sciences proved to be essential to gain a comprehensive only includes assessments of wild species (i.e. excludes cultivated view from biological, conservation, agricultural production and social species), and in order to evaluate a subspecies, variety or subpopula- perspectives. tion, the species as a whole needs to be assessed first. Therefore, a clear understanding of which taxa or populations are cultivated and which are wild is essential. (2) The generation of the native distribu- 4.5 | Indirect and direct uses of tion maps of taxa is one of the most important steps for assessing Mesoamerican CWR their extinction risk. In this process, a critical step is data cleansing, for example, elimination of misidentifications, historical records and Given the genetic proximity to crops, all taxa included in the present cultivated populations (Castañeda-A lvarez et al., 2016). Compared study have the potential to donate genes and therefore have indirect 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 788 GOETTSCH ET AL. utilisation potential. However, the taxa in the primary (i.e. same spe- mays ssp. mexicana ‘Nobogame’ subpopulation and the EN Zea mays cies as the crop) and secondary gene pools are those most closely ssp. huehuetenanguensis. Given that at least part of the geographic related to crops and thus are more likely to be used as gene donors range of a high proportion of Mesoamerican CWR taxa (60%) occurs because of the relative ease of trait transfer to the crop and their con- within protected areas (Figure 8), there is a need to develop or adapt servation is commonly prioritised (Maxted et al., 2020). Having existing management plans specifically to actively monitor and stressed this point, although taxa in the tertiary gene pool are gener- manage CWR populations, as well as to raise awareness (Figure 7) ally more difficult to cross with the crop, they are also used by among the general public and particularly protected area managers, breeders if the CWR contains known and required adaptive traits. Six- about what CWR are and their importance (Holness et al., 2019). As teen taxa included in this study are already utilised in crop improve- stressed before, conservation of CWR presents different challenges ment, conferring crops resistance to viruses and pests (e.g. Cucurbita and opportunities, which demand creative approaches for planning in lundelliana, Solanum bulbocastanum, S. stoloniferum), drought tolerance situ or circa situm conservation. For many CWR, protected areas are (e.g. Solanum pinnatisectum, S. stoloniferum) or yield improvement (Zea not necessarily the best means of protection. Many taxa are adapted diploperennis; Table S1 and also see taxa assessments on the IUCN to disturbed areas where they are tolerated and often fostered; mean- Red List), and at least 34 taxa are being researched for this purpose ing that alternative conservation approaches are necessary. An (Figure 4). extreme case is the EN Zea diploperennis which has an intricate rela- Moreover, many Mesoamerican CWR are utilised directly for tionship with fire cycles associated with slash-burn agriculture. Man- traditional uses such as food, fodder and as medicine (Figure S4). aging fire within the Sierra de Manantlán Biosphere Reserve, where These taxa are collected from the wild (e.g. Capsicum spp., Physalis the majority of the remaining populations occur, is challenging, and spp.) or are fostered in agricultural fields or their edges and are left to existing management plans are difficult to implement (Aragon Cuevas, grow in home gardens (e.g. Cucurbita spp., wild Phaseolus coccineus, Contreras, et al., 2019; Sánchez-Velásquez et al., 2002). Cucurbita Physalis spp.). The direct uses of CWR present an opportunity to pro- lundelliana and C. okeechobeensis ssp. martinezii are rarely found within mote their conservation through the recovery of the knowledge protected areas but thrive in nearby rural human settlements where around their traditional and sustainable use, including the acknowl- people allow them to grow in home-gardens and along fences and on edgment of their importance for communities. road sides (Sánchez de la Vega et al., 2019). The genetic diversity of Capsicum annuum var. glabriusculum in home-gardens in Guatemala was found to be as high as that found in gene banks (Guzmán 4.6 | CWR conservation needs in Mesoamerica et al., 2005). Therefore, in situ and circa situm conservation approaches for CWR should, where applicable, integrate the direct Ex situ conservation in gene banks is the most common conservation sustainable uses of taxa and expand beyond protected areas. need identified across all assessed taxa, followed by site or area pro- Recently, the active in situ conservation of CWR outside protected tection and habitat protection (Figure 7), especially for threatened areas by farmers within traditional farming systems has been reviewed taxa as 46% do not occur inside protected areas (Figure 8). Both of alongside the level of public good financing that might be attached to these conservation actions are of notable urgency for Critically reward the farmers for their CWR population management activities Endangered taxa, especially for Gossypium turneri, Zea perennis and Z. (Wainwright et al., 2019). F IGURE 7 Number of taxa in each International Union for Conservation of Nature (IUCN) Red List Category for which a conservation action need was recorded. CR = critically endangered, EN = endangered, VU = vulnerable, NT = near threatened, DD = data deficient, LC = least concern 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GOETTSCH ET AL. 789 F IGURE 8 Proportion of taxa across all taxonomic groups that were recorded as occurring within protected areas, not occurring in protected areas or as unknown. CR = critically endangered, EN = endangered, VU = vulnerable, NT = near threatened, DD = data deficient, LC = least concern 4.7 | Final considerations could prove valuable for the region, given that it harbours the totality of the genetic diversity of many crop gene pools. Conservation and Conservation actions for Mesoamerican CWR are urgent given their knowledge of CWR can be significantly improved by developing pro- high levels of threat and their importance in maintaining the genetic grams to strengthen the collaboration between agencies dealing with diversity that provide important resources for our diverse global food species and habitat conservation, agricultural policy, breeding pro- systems. The genetic complexes present in centres of origin like grams, conservation of genetic resources and indispensably with the Mesoamerica are crucial to humankind's future well-being. Policies communities that utilise them. setting targets for plant species and specifically for CWR conservation Mesoamerican people have been managing wild and cultivated (FAO Second GPA, GSPC, ITPGRFA, Aichi target 13, SDG Target 2) plants for thousands of years using a diverse range of agricultural and have helped align efforts, and continuation in post-2020 targets will in situ vegetation management techniques (Casas et al., 2007; be key to secure genetic resources. Clement et al., 2021). One of the best documented examples is the Gains in biodiversity protection could be maximised if actions are ancient Mayans, who expanded and intensified agricultural production implemented in areas with high concentrations of CWR and that ide- to sustain very large populations that altered most of the landscape ally also contain taxa in more urgent need of conservation and that (DeClerck et al., 2010, and references therein). Evidence indicates no are threatened with extinction. However, special attention should be apparent decrease in floristic biodiversity in the last 5000–6000 years, placed on Critically Endangered taxa given the limited overlap with which can possibly be explained by the management of complex areas with high numbers of EN and VU taxa. Conserving habitats such forest-agriculture mosaics such as those found today (e.g. less man- as cloud forests and seasonally dry forests should be a priority, and aged forests, agroforestry systems and abandoned agricultural land; different types of policies to halt forest cover change or to foster nat- Gomez-Pompa & Kaus, 1999; Correa-Cano, 2004; Dalle et al., 2006; ural regeneration could be promoted (CONABIO et al., 2019a, 2019b). Dalle et al., 2011). If agricultural sustainability and food security are to These should include community-based forest management, carefully be attained in Mesoamerica, innovation has to involve the return designed payments for ecosystem services programmes (Tyack to and maximisation of traditional and more diverse and sustainable et al., 2020), elimination of perverse agricultural subsidies production systems (CONANP, 2019). This must include the improve- (Whetstone, 1999) and holistic land use planning, among others initia- ment of smallholder yields, supported through policies oriented to tives that support rural economies and livelihoods (Chazdon improve economic and social mechanisms (Godfray et al., 2010; et al., 2020; Min-Venditti et al., 2017; Wainwright et al., 2019). Ibarrola-Rivas & Galicia, 2017) as well as gaining better understanding The development of a multiscale and stakeholder approach is of their multicrop food production systems, such as the milpa. It is also imperative to ensure that CWR species and their genetic diversity are necessary to develop systematic and novel ways of measuring pro- well represented and preserved in herbaria, botanical gardens and ductivity considering all the elements of these complex systems and gene banks and to strengthen knowledge and in situ conservation the many ecosystem services and the benefits they provide in both through the implementation of different policies and measures across the short term and long term (Bellon et al., 2018; González, 2012; landscapes (Estrada-Carmona et al., 2014; Hunter & Heywood, 2011). Lopez-Ridaura et al., 2021). Efforts should take place especially within priority areas recently iden- This analysis has identified, within the selected taxa of tified for Mesoamerica (Tobon et al., unpublished). This should aim at, Mesoamerican CWR, those most at threat. It also provides an in- for example, transforming agriculture into more sustainable food sys- depth understanding of the diversity of threats they face that should tems (see http://teebweb.org/agrifood/). Efforts to understand how be expanded to other taxa and countries in the region. The collated staple foods (e.g. maize) and their genetic diversity depend on and/or occurrence point data and identified conservation and research needs are impacted by traditional production systems (CONABIO, 2017) can facilitate both in situ and ex situ conservation planning. We hope 25722611, 2021, 6, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10225 by Cochrane Colombia, Wiley Online Library on [03/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 790 GOETTSCH ET AL. that this will set the basis upon which national and regional Acevedo Gasman, F., Huerta Ocampo, E., Lorenzo Alonso, S., & Ortiz multistakeholder conservation strategies of these vital resources can García, S., (2009). La bioseguridad en México y los organismos gen- éticamente modificados: Como enfrentar un nuevo desafío. In Capital be developed. Natural de México, Vol. II: Estado de Conservacion y Tendencias de Cambio (pp. 319–353). COANBIO. ACKNOWLEDGEMENTS Aguirre Dugua, X., Sánchez de la Vega, G., Aguirre, E., Eguiarte, L., & Lira This study is the result of the collaborative project ‘Safeguarding Saade, R. (2020). Los parientes pobres de la agricultura: Las calabazas silvestres, riqueza para nuestro futuro. Biodiversitas, 150, 12–16. Mesoamerican crop wild relatives’ funded by the Darwin Initiative Aragon Cuevas, F., Contreras, A., de la Cruz Larios, L., González (project number 23-007) and Toyota Motor Corporation through the Ledesma, M., Ruíz Corral, J. A. R. & Menjivar, J. (2019). Zea IUCN-Toyota Red List Partnership, to whom we are grateful. We diploperennis. IUCN Red List of threatened species. https://doi.org/ thank Moisés Cortes, Mario Parada Jaco, Caroline Burgeff, Albaro 10.2305/IUCN.UK.2019-2.RLTS.T77726057A77726102.en Aragon Cuevas, F., Sánchez de la Vega, G., Castellanos Morales, G., Orellana, Karina Hernández Cibrián and Francy Nohemy Castañeda Contreras-Toledo, A. & Lira Saade, R. (2019). Cucurbita radicans. IUCN for their contributions in the development of the criteria for species Red List of threatened species. https://doi.org/10.2305/IUCN.UK. selection and species selection process. We are thankful to Alejandra 2020-2.RLTS.T109928871A173925627.en Barrios† for her advice on Mexico's national process of assessing spe- Azurdia, C., Williams, K. A., Van Damme, V., Jarvis, A., & Castaño, S. E. cies extinction risk and for her particular view and understanding of (2011). Atlas of Guatemalan Crop Wild Relatives. United States Department of Agriculture/Agricultural Research Service (USDA/ARS); CWR policy-related matters. We are grateful to CONABIO's technical Bioversity International; International Center for Tropical team, Jesús Alarcon, Angela Cuervo Robayo, Cuauhtémoc Enriquez, Agriculture (CIAT); and the University of San Carlos in Guatemala Diana Hernández, Diana Ramírez, Sylvia P. Ruiz González, Susana (FAUSAC). Ocegueda, Edgar Saavedra and Adriana Varela and IUCN's SSC staff Banerjee, S., Samanta, S., & Chakraborti, P. K. (2018). Impact of climate change on coastal agro-ecosystems. Sustainable Agriculture Reviews, Ariany García and Jesús Morales who supported the Red List 33, 115–133. https://doi.org/10.1007/978-3-319-99076-7_4 workshop. We thank Ligia Boueres for her help drafting assessments. Barros, V. R., & Field, C. B. (2014). Climate Change 2014: Impacts, Adapta- We thank all researchers and institutions that have collaborated with tion, and Vulnerability. Part B: Regional Aspects. Cambridge University CONABIO in the National Biodiversity Information System. Gabriel Press. Bellon, M. R., Barrientos-Priego, A. F., Colunga-GarcíaMarín, P., Alejandre thanks Instituto Politécnico Nacional and COFAA for the Perales, H., Reyes Agüero, J. A., Rosales-Serna, R., & Zizumbo- economic support and the SIBE exclusivity grant provided. Villarreal, D. (2009). Diversidad y conservacion de recursos genéticos en plantas cultivadas. In Capital Natural de México, Vol. II: Estado de CONFLICT OF INTEREST Conservacion y Tendencias de Cambio (pp. 355–382). Conabio. Bellon, M. R., Mastretta-Yanes, A., Ponce-Mendoza, A., Ortiz- The authors declare they have no competing interests. Santamaría, D., Oliveros-Galindo, O., Perales, H., Acevedo, F., & Sarukhán, J. (2018). Evolutionary and food supply implications of AUTHOR CONTRIBUTIONS ongoing maize domestication by Mexican campesinos. Proceedings BG, TU-H, PK, FAG, ARC, RKBJ, NM, MMG and AJMH jointly created, of the Royal Society B: Biological Sciences, 285(1885), 20181049. https://doi.org/10.1098/rspb.2018.1049 developed and led the project. FAG, AA-M, VA, GA-I, FAC, CAP, JAC, BID, & CEPAL. (2010). Cambio climático: Una perspectiva regional. CEPAL. GC-M, GC, ARC-T, LDL, DGD, AD-S, EPG-R, MG-L, EG-P, MH-A, https://www.cepal.org/es/publicaciones/1405-cambio-climatico- BEH-C, MJ, SK, RL-S, FL-H, MM, AM-Y, JM, OO-G, MAO-R, MQ-C, perspectiva-regional AR, JARC, JJSG, GSD, MS, WTN, MFT, OV-P, MV, AW and PZT Bilz, M., Kell, S. P., Maxted, N., & Lansdown, R. (2011). European Red List of contributed to the species assessment process. BG, TU, MECC and Vascular Plants. Publications Office of the European Union. Bosland, P. W., & Gonzalez, M. M. (2000). The rediscovery of Capsicum CMP conducted the analyses. BG, TU-H and PK drafted the lanceolatum (Solanaceae), and the importance of nature reserves in manuscript and all authors commented and agreed on it. preserving cryptic biodiversity. Biodiversity and Conservation, 9(10), 1391–1397. https://doi.org/10.1023/A:1008930931976 DATA AVAILABILITY STATEMENT Brás, T. A., Seixas, J., Carvalhais, N., & Jägermeyr, J. (2021). Severity of drought and heatwave crop losses tripled over the last five decades in The data that supports the findings of this study are published in the Europe. Environmental Research Letters, 16. https://doi.org/10.1088/ supplementary material and The IUCN Red List https://www. 1748-9326/abf004 iucnredlist.org/. Campbell, B. M., Vermeulen, S. J., Aggarwal, P. 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