Biodivers Conserv DOI 10.1007/s10531-016-1109-7 ORIGINAL PAPER Twenty-five years of international exchanges of plant genetic resources facilitated by the CGIAR genebanks: a case study on global interdependence Gea Galluzzi1 • Michael Halewood1 • Isabel López Noriega1 • Ronnie Vernooy1 Received: 31 August 2015 / Revised: 12 April 2016 / Accepted: 16 April 2016  The Author(s) 2016. This article is published with open access at Springerlink.com Abstract This article analyses 25 years of data about international movements of plant genetic resources for food and agriculture (PGRFA), facilitated by the gene banks hosted by seven centres of the Consultative Group on International Agricultural Research. It identifies trends in the movements of PGRFA for use in research and development, and describes the diversity of those resources transferred over time. The paper also presents data on the number of countries involved in the global exchanges, analyses their devel- opment status and describes their role as providers and/or recipients, providing a picture of the breadth of these global exchanges. We highlight that it is primarily developing and transition economies that have participated in the flows, and that the transferred germplasm has been largely used within their public agricultural research and development pro- grammes. We conclude that, when provided the opportunity of facilitated access, countries will use a wide diversity of germplasm from many other countries, sub-regions and con- tinents as inputs into their agricultural research and development programmes. We high- light the importance of enabling the continuation of the non-monetary benefits from international access to germplasm. We discuss the implications for the process of devel- opment and reform of the multilateral system of access and benefit sharing under Inter- national Treaty on Plant Genetic Resources for Food and Agriculture. Keywords Plant genetic resources  Interdependence  International Treaty on Plant Genetic Resources for Food and Agriculture  Multilateral system  Conservation  Breeding Communicated by Anurag chaurasia. & Gea Galluzzi geagalluzzi@gmail.com 1 Bioversity International, Via dei Tre Denari 472/a, Maccarese, Rome, Italy 123 Biodivers Conserv Introduction Plant genetic resources for food and agriculture (PGRFA) are the basic building blocks of crop improvement and adaptation and, by extension, of food security. As a result of the history of crop domestication and global dispersal and adaptation, all countries are now highly dependent upon plant genetic resources located (or originally collected from) beyond their borders. Global interdependence on plant genetic resources has been previ- ously discussed (Crosby 1972, 1986; Diamond 1997; Fowler et al. 2001; Halewood et al. 2014; Mann 2011; SGRP 2011), and predictions have been made of increased future interdependence as a result of challenges such as climate change (Lane and Jarvis 2007; Burke et al. 2009; Jarvis et al. 2010; Fujisaka et al. 2011; Ramirez-Villegas et al. 2013) and the evolution of food systems and diets (Khoury et al. 2014). Global recognition of the policy significance of interdependence on PGRFA arguably reached its zenith in 2001 when ‘interdependence’ was explicitly included in Article 11 of the International Treaty on Plant Genetic Resources for Food and Agriculture (ITPGRFA) as one of two criteria—the other being relevance for food security—for including crops or forages in the multilateral system of access and benefit sharing (MLS).1 Through the MLS, ITPGRFA parties agree to create a global, virtual pool of genetic resources for 64 crops and forages (these are listed in the Treaty’s Annex 1). In addition to conservation, this germplasm is intended to be utilized for the purposes of training, breeding and research for food and agriculture. Member states agree to provide facilitated access to one another (including natural and legal persons within their borders) on the understanding that monetary benefits will be shared if the recipients incorporate materials in new, commercialized PGRFA products that are not available to others for research, training or breeding. The multilateral architecture of access and benefit sharing under the ITPGRFA was designed to reflect countries’ current and future interdependence on PGRFA. The system was meant to minimize transaction costs that could otherwise mul- tiply beyond acceptable limits, given the magnitude of international exchanges of genetic resources that accompany agricultural research, development and plant breeding. In recent years, ITPGRFA member states have expressed concerns that the MLS has not been functioning at the anticipated levels, either in terms of generating financial benefits by users to be shared through the international Benefit-Sharing Fund (BSF) or in terms of materials being made available to, and accessed through, the MLS. Based on this concern, the ITPGRFA’s Governing Body created the Ad Hoc Open Ended Working Group to Enhance the Functioning of the MLS. Its mandate is to develop a range of optional measures to both increase user-based payments and contributions to the BSF in a sus- tainable and predictable long-term manner and enhance the functioning of the Multilateral System by additional measures. This article focuses on an issue at the heart of the MLS—the state of global interde- pendence on PGRFA. We hope that the data presented here will be useful within any process aimed at revising or reforming the terms and conditions of the MLS. It is critically important to keep interdependence in mind when developing policies concerning the conditions under which genetic resources can be accessed and used as well as the ways in which benefits derived from their use should be shared. Illustrating the volume, diversity and geographical spread of global flows of plant genetic resources mediated by Consul- tative Group on International Agricultural Research (CGIAR) centres, the findings 1 International Treaty on Plant Genetic Resources for Food and Agriculture, 29 June 2004, http://www. planttreaty.org/content/texts-treaty-official-versions (accessed 15 December 2015). 123 Biodivers Conserv highlight the benefits accrued by virtually all countries in the world—namely, being granted access to a rich variety of materials (and associated technology and information) otherwise unavailable within their own borders and difficult to access under bilateral conditions. The resulting conclusions highlight the importance of the system’s non-mon- etary modalities for sharing benefits, most of which have involved users in developing countries. We hope that such evidence will encourage efforts to maintain and enhance these mechanisms, in addition to improving the mechanisms associated with monetary payments to the BSF. Data sources and methods Data on the holdings, acquisitions and distributions of nine CGIAR genebanks was retrieved from the CGIAR’s System-wide Information Network on Genetic Resources (SINGER).2 A system-wide database such as SINGER has never been established for the distribution of germplasm from the CGIAR’s breeding programmes, and, therefore, our study focuses on genebank distributions only. We asked each of the genebank curators to validate the accuracy of the data stored in SINGER and/or to provide updates or inte- grations. In the end, we obtained validated or updated data for seven genebanks, which are those included in this study (Table 1). Given the magnitude of the distributions from the other centres whose data is not included in this research, i.e., CIMMYT, CIAT, IITA, the final conclusions regarding the extent of international interdependence would likely have been even stronger had their data been included. Distribution data followed a standard format gathering information according to the fields shown in Table 2. Distribution records were available beginning in 1973 for some of the genebanks included in the study, but there were large gaps in the records until 1985 (due to data storage and reporting systems not being fully in place in all centres). Thereafter, the data were more uniform, which led to the decision to consider only the data from 1985 onwards. Since our focus was the germplasm sent to countries and within-country recipients, intra- and inter-CGIAR centre distributions were removed as well as those from CGIAR gene- banks to the Svalbard Global Seed Vault. The total number of distributed samples shown in Table 1 was the basis for our analysis. These centres’ mandate crops (and their wild relatives) include key staples for worldwide food security, such as rice, tropical and dry- land legumes and cereals, potatoes and other roots and tubers, bananas and plantains and tropical forages (see Appendix, Tables 6, 7 for details on the collections hosted at all CGIAR centres). Various ways of measuring international PGRFA movements were explored. We considered the total number of samples distributed [a single sample consisting ideally of between 50 and 100 viable seeds or less vegetative propagules (CGKB 2014)], the number of accessions distributed (excluding the repeated distributions of the same accession) and the number of species distributed. The latter two statistics provide a picture of the diversity, rather than the sheer volume, of the flows. Further analyses qualified the international germplasm flows facilitated by the gene- banks using the number of countries from which the materials distributed were originally 2 SINGER has been discontinued, with much of its data and functionality—minus distribution data— incorporated into GENESYS, http://www.genesys-pgr.org (accessed 20 November 2014). 123 Biodivers Conserv Table 1 Total number of samples sent to national recipients from the seven CGIAR genebanks (1985–2009) AfricaRice Bioversity CIP ICARDA ICRISAT ILRI IRRI Samples distributed 38,963 13,436 84,380 246,026 418,934 30,830 166,681 Table 2 Fields of information CGIAR centre Transfer year included in the distribution data from CGIAR genebanks Accession number Recipient country code Genus Recipient country name Species Recipient institute Country of origin Recipient last name Biological status Recipient first name Recipient code Recipient user type Recipient region Transfer date collected or improved, the number of recipient countries and types of recipient institutions, the number of genera and species distributed, and the type of materials exchanged. Countries were classified based on their development status according to the United Nations classification system (UN 2012), which helped to analyse the germplasm contri- butions according to the economy of the donor or recipient country. All data handling and analyses were performed in R (R Development Core Team 2011). Results and discussion Global flows of PGRFA, 1985–2009: volumes and diversity Between 1985 and 2009, germplasm conserved in the selected CGIAR genebanks was distributed to a broad range of users. According to the available data, 999,250 samples of 262,872 accessions belonging to 1470 different plant species were distributed during that period. The average number of samples distributed per year (39,970) is below that of the U.S. National Plant Germplasm System (NPGS), where total annual distributions have increased from around 120,000 (Bretting 2007) to more than 200,000 (Heisey and Day Rubenstein 2015) over the past few years. About 30 % of NPGS yearly distributions are typically to requestors from outside the U.S. However, in making this comparison, our lack of data from three important CGIAR genebanks should be kept in mind. Notwithstanding the missing data, the yearly volumes described are much higher than the average number of distributions of other important germplasm systems, such as the Russian Vavilov Institute (6400) (FAO 2009), the German Institute of Plant Genetics and Crop Plant Resources (4400 of barley only) (Ullrich 2011), the Centre for Genetic Resources in the Netherlands (2500) (Centre for Genetic Resources 2008), the Brazilian Empresa Brasileira de Pesquisa Agropecuária (1800) (Da Silva Mariante et al. 2009), the Institute of Crop Germpasm Resources in China (1550) (ICGR 2015), the Plant Genetic Resources Institute of Canada (1500) (Fowler and Hodgkin 2004). These numbers are useful for providing a general idea of the CGIAR’s relative contribution on the international scene, but they should be 123 Biodivers Conserv considered with caution because of the differences in the reporting periods and the limi- tations of our data. Virtually all countries in the world have been involved in the exchange of germplasm. The materials listed in Table 1 were originally collected in, or provided by, at least 189 countries and distributed to at least 191 countries. In addition to distributions from the various genebanks, large amounts of germplasm in different stages of improvement have been sent out by the centres’ breeding programmes, although no system-wide mechanism has ever been set up to document these distributions over time. However, data provided by the centres3 for the fourth session of the ITPGRFA’s Governing Body indicate that from August 2008 to December 2009 these breeding programmes sent out over 500,000 samples (SGRP 2011). This amount points to the outstanding contribution that the CGIAR breeders make to international flows of germplasm, in addition to the centres’ genebanks. According to data available through the GENESYS portal, which gathers information on numerous national and international genebanks, the international ex situ collections hosted by the CGIAR centres currently include 712,834 accessions of their mandate crops and related gene pools, originally collected from a vast number of countries (Appendix, Tables 6, 7, 8). The genebanks that were analysed in this study, currently host 445,785 accessions of 2848 species.4 Our data suggest that samples of roughly half the diversity held have been distributed at least once by these genebanks. During the period analysed, there appears to be have been a slight downward trend in the overall number of samples distributed, as already highlighted elsewhere (Halewood et al. 2013). A similar decline was observed in the diversity of the materials distributed, which was measured according to the number of accessions distributed and the number of species represented (Table 3). This trend may be attributed to the fact that the requests became more targeted as more characterization and evaluation data became available, which led to breeders and researchers making requests for smaller sets of materials (Halewood et al. 2013; López Noriega et al. 2013a). For those CGIAR genebanks actively distributing sets of materials for international adaptation trials, the decline could also be due to decreases in the funding made available for these multi-location field operations. It could be that some of the requests that were traditionally made to the CGIAR are now being directed to other genebanks. In addition to institutions that have always been at the forefront of international distributions, alongside the CGIAR, such as the US Department of Agriculture (USDA), a number of national institutions in other countries have been increasing their collections and may be receiving more germplasm requests (FAO 2010). In addition, some private sector users—those most likely to apply some form of intellectual property rights to the final PGRFA products—may have refrained in recent years from requesting germplasm from the CGIAR because of their reluctance to accept the benefit- sharing clauses of the MLS (Halewood and Nnadozie 2008). It is important to note that traditionally these companies have been an extremely small portion of the users of CGIAR materials, as described later. Types of materials and frequency of distribution According to GENESYS, over 50 % of the total germplasm distributed by the CGIAR genebanks over the 25 years analysed are landraces or traditional cultivars, which are predominant within these collections (Fowler et al. 2001; Genesys 2014). Breeding and 3 Except IITA, which did not provide information for this report. 4 GENESYS, http://www.genesys-pgr.org (accessed 20 November 2014). 123 Biodivers Conserv Table 3 Results of the models used for analysing trends in the overall flows over time (1979–2009) Parameter/year Estimate P value Method Samples -0.031 \2e-16 Generalized linear model with Poisson error distribution Accessions -0.065 \2e-16 Generalized linear model with Poisson error distribution Species -0.013 \2e-16 Generalized linear model with Poisson error distribution research lines constitute less than 20 % of the materials distributed, while advanced or improved cultivars comprise only 7 % of the distributions. Wild and weedy relatives amount to 12 % of the samples sent out by the analysed genebanks, not only suggesting their importance as sources of useful traits but also reflecting the greater difficulty of using them in breeding compared to other materials (Fig. 1). The decision about which materials to con- serve in the long term is made by each centre independently, often following the outcomes of economic analyses on the costs and benefits of conserving materials in genebanks or breeding programmes (Koo et al. 2004). The data in this study reveal that most centres give priority for long-term storage in their genebanks to materials that belong to the primary genepools – that is, the landraces and wild relatives of their mandate crops. This strategy also reflects the fact that all centres with genebanks also have breeding programmes that actively exchange research, breeding and improved lines with partners worldwide, making the conservation of these sets by the genebank neither necessary nor efficient. However, research, breeding and advanced lines are sometimes included in long-term collections, when the properties, or the use of the material, justify it. For instance, this may be the case with materials that have accumulated unique genetic properties (for example, allele com- binations), those that are laborious to reproduce (for example, inter-specific hybrids) or those that are commonly used as benchmark varieties in evaluation trials. Based on the number of samples per accession sent to recipients, there appears to be enormous variation in the popularity of any single accession. Almost 60 % of the accessions in the dataset have been distributed between two and ten times, while only 5.7 % (150 accessions) have been distributed more than 100 times. Most of the latter come from ILRI, CIP and ICRISAT and have been distributed to an average of over 38 countries (SD 20.5) (see Appendix, Table 9 for details on the top 50 most ‘popular’ accessions of our dataset). Fig. 1 Proportion of the different types of germplasm distributed by the selected CGIAR genebanks based on accession data (1985–2009) 123 Biodivers Conserv More than half of these frequently distributed materials are improved lines, whereas lan- draces, wild relatives and, to a lesser extent, breeding materials constitute the bulk of the accessions transferred less frequently. Among the possible reasons for the ‘popular’ mate- rials to be more frequently requested (that is, by many institutions worldwide) is the fact that the characterization and/or evaluation data already accumulated on them increases their value for breeding and research. This information, in turn, facilitates their use including in institutions and countries with limited capacity or infrastructure for conducting lengthy and costly pre-breeding research using non-adapted populations and wild relatives (FAO 2010). Providers and recipients Of the total 189 countries from which material distributed by the seven CGIAR genebanks was obtained, 112 are developing countries, 54 are developed countries and 23 have economies in transition. Of the total 191 recipients, 116 are developing countries, 19 are economies in transition and 56 are developed countries. Data for developing countries and countries with economies in transition has been combined in our analyses. Both developed and developing countries are net recipients—that is, they receive more diversity than they contribute to international gene banks. While this ‘sink’ behaviour is more evident for developed countries, which tend to harbour comparatively less indigenous genetic diversity in their territories, the majority of global exchanges of germplasm mediated by the CGIAR genebanks is distributed South to South—that is, between developing countries (Fig. 2). In their analysis of the flows from six of the CGIAR genebanks and from the USDA’s National Plant Germplasm System (NPGS) between 1990 and 1999, Smale and Kelly Day Rubenstein (2002) also observed that a predominance of developing countries and tran- sition economies were providers and recipients. So too did the CGIAR’s System-wide Genetic Resources Programme (2011) in its biannual reports to the Governing Body of the ITPGRFA. Tables 4a, b provide more detail on the amount, diversity and geographical coverage of the distributions facilitated by the international genebanks for the top 25 provider countries and the top 25 recipient countries. Almost all of the top providers listed in Table 4 are developing countries. Many of them are important centres of origin, domestication or diversification of the crops curated by the Fig. 2 Number of accessions exchanged between developed (the ‘North’) and developing and transition countries (the ‘South’) 123 Biodivers Conserv 123 Table 4 Top 25 provider countries (including total number of samples, genera and accessions originally sourced in these countries and circulated by the CGIAR genebanks analysed in this study as well as the number of recipient countries) and top 25 recipient countries (total number of samples, genera and accessions received as well as the number of countries where these materials were originally sourced) (1985–2009) Provider Total samples Accessions Genera Recipient Recipient Total samples Accessions Genera Provider country provided provided provided countries country received received received countries India 188,911 48,635 35 144 India 284,454 115,849 70 181 Peru 67,899 16,216 23 158 United States 45,992 39,963 97 178 Ethiopia 40,143 13,683 94 120 China 33,690 18,664 48 151 United States 36,652 6294 30 156 Ethiopia 28,863 17,572 175 150 Iran 29,829 9779 26 87 Australia 20,218 17,566 63 150 Turkey 29,579 9634 29 83 Japan 17,628 12,022 32 141 Syrian Arab 26,029 7487 27 78 United 17,231 14,283 89 144 Republic Kingdom Sudan 24,262 3457 17 61 Morocco 16,362 14,618 38 97 The Philippines 21,626 4016 7 109 The Philippines 16,332 8798 50 107 Côte d’Ivoire 20,494 3037 4 78 Tunisia 13,399 9706 18 70 China 18,559 7225 21 125 Iran 13,083 12,301 18 135 Nigeria 16,060 3462 27 126 Austria 12,703 12,657 24 92 Zimbabwe 15,477 4500 19 62 Italy 12,345 10,003 36 116 Cameroon 15,216 2942 13 67 Syrian Arab 10,598 8610 19 92 Republic Jordan 12,328 3319 20 66 South Korea 10,195 8423 26 137 Morocco 12,257 4106 34 69 Russia 9614 8636 12 92 Bangladesh 12,092 3839 14 94 Pakistan 9512 7901 64 139 Indonesia 11,696 3774 12 93 Turkey 9295 7221 25 96 Uganda 11,172 2565 13 103 Canada 9160 7709 38 121 Tunisia 10,799 3523 22 74 Indonesia 8965 8395 32 110 Pakistan 10,587 2950 23 99 Peru 7953 4053 33 75 Kenya 10,509 2205 38 104 Egypt 7921 6685 54 126 Biodivers Conserv 123 Table 4 continued Provider Total samples Accessions Genera Recipient Recipient Total samples Accessions Genera Provider country provided provided provided countries country received received received countries Algeria 9743 3522 24 65 Germany 7276 6253 63 130 Tanzania 8438 2132 37 96 Brazil 6903 6030 34 129 Nepal 7725 2745 19 73 Thailand 6821 4899 27 103 Biodivers Conserv genebanks considered in this study, including India (rice, millet), Peru (potatoes), Syria and Turkey (wheat and barley), China (rice) and a number of African countries (particu- larly for tropical forages). Many of the top recipients are also developing countries, and, again, many of them are centres of origin or diversity of crops or forages that they have requested, underscoring the fact that even diversity-rich countries are not self-sufficient in terms of their PGRFA needs. As an example, the difference in the amount of germplasm flowing in and out of India, compared to other countries, stands out as very significant. India has provided and received massive quantities of germplasm. Interestingly, a signif- icant percentage of the materials originally collected in, or obtained from, India ends up going back to Indian recipients (59 % of the samples and over 70 % of the accessions), which makes it the largest recipient of CGIAR-hosted materials originally obtained from within its own borders. A high percentage of ‘reabsorption’ of their own materials through CGIAR-mediated flows are also recorded for Tunisia and Morocco (48 and 42 % respectively), the Philippines (37 %), Iran and Jordan (30 and 25 %) and others to lesser extents. These observations highlight the additional benefit of germplasm deposited in international collections since it provides long-term secure conservation and availability of quality material (and often value-added characterization and evaluation data) originating from one’s own territory, in addition to access to diversity from hundreds of other coun- tries. The latter benefit is particularly relevant for those countries with limited capacity to establish and maintain national conservation programmes for their own local materials. Differences exist not only in the amount, but also in the type of materials provided by developed and developing countries. While developed countries provide an overall lower quantity of materials compared to developing countries, they contribute a proportionally higher share of materials for which some formal research, pre-breeding or other form of improvement has been conducted. In total, 27 % of the samples ‘distributed’ by our seven CGIAR genebanks from developed countries were research materials and improved/elite lines (with the United States supplying as much as 80 % of this category); only 14 % of the samples distributed from developing and transition countries belonged to these categories. On the recipient side, the share of germplasm that carried some degree of research and improvement flowing into developing countries and transition economies is 30 % of the overall incoming samples, while it is 14 % for developed countries. In both developed and developing nations, public institutions (including the National Agricultural Research System (NARS), universities and genebanks) are by far the pre- dominant recipients of CGIAR materials (Table 5; Fig. 3). These public sector recipients are located in developing countries in over 75 % of the cases. The share of samples sent to commercial companies is only around 3 % of the total, and the recipients are primarily (77 %) in developing countries. These findings are also consistent with those of Smale and Day Rubenstein (2002) who found that most recipients of germplasm from the US NPGS, another important worldwide facilitator of PGRFA for research and breeding, were in the public sector. The volume and diversity of the PGRFA flows described in this study, albeit only a small sample of worldwide exchanges, demonstrate the extent of countries’ interdependence on PGRFA for crop improvement and, ultimately, food security. While acknowledging the limits of our dataset, we believe that the conclusions regarding the extent of international interdepen- dence would likely have been even stronger had the data from important genebanks such as those at CIMMYT, CIAT and IITA been included. The emerging picture confirms an established description of modern agriculture as an interdependent network of seed and germplasm sources, in which very few countries or farming systems in the world do not 123 Biodivers Conserv Table 5 Type of recipients, samples and accessions and percentages over the total Recipient type Samples received Percentage Accessions received Percentage NARS 573,456 57.39 374,714 61.87 University 297,034 29.73 161,845 26.72 Genebank 53,198 5.32 33,967 5.61 Commercial company 32,020 3.20 10,985 1.81 Other 24,739 2.48 13,650 2.25 Non-governmental organization 14,821 1.48 7905 1.31 Regional organization 2727 0.27 2054 0.34 Farmer 1255 0.13 528 0.09 Fig. 3 Share of accessions received by different recipient categories (1985–2009) rely to some degree on the international system that moves crop germplasm, breeding lines and improved varieties across international borders (Duvick 1984). Analyses by other authors confirm these patterns, describing how crop improvement has benefited from access to a wide range of materials with different origins. Fowler, Smale and Gaiji (2001) undertook an analysis of CGIAR data focusing on a different time frame and different measures than those presented here. Smale et al. (2002) used the case of spring bread wheat released by national programmes in developing countries. Warburton et al. (2006) and Dreisigacker et al. (2005) looked at synthetic hexaploids to illustrate the significance of access to wild relatives from centres of diversity in wheat improvement. Voysest et al. (2003) took the case of beans in Latin America (Fowler et al. 2001; Smale et al. 2002; Voysest et al. 2003; Dreisigacker et al. 2005; Warburton et al. 2006). Addi- tional studies have focused on those countries that are the centres of crop diversity. Rejesus et al. (1996) reported that 45.6 % of the germplasm used by wheat breeders in Western Asia, the Vavilov centre for the species, comes from international sources. Evenson and Gollin (1997) documented the dependence of Asian countries, including the Vavilov- centre countries such as India, Burma, Bangladesh, Nepal and Vietnam, on IRRI for rice 123 Biodivers Conserv germplasm of different provenance (65.0 % in India and 98.1 % in Vietnam) (Rejesus et al. 1996; Evenson and Gollin 1997). All of this evidence points to the ‘international public good’ nature of the materials held and made available by the CGIAR as well as by other actors who make such materials available. It highlights the importance of supporting the continuation and enhancement of conservation as well as the internationally facilitated sharing of germplasm within the framework of the ITPGRFA. Conclusions It is clear that access to globally pooled genetic resources is a fundamentally important benefit that all countries have historically exploited when systems were set up to facilitate such access. Any effort to improve the MLS must be guided by the necessity of supporting and improving countries’ ability to further capitalize on this benefit. This is particularly true considering the contemporary challenges associated with climate change (Fujisaka et al. 2011), population growth and the harmonization of diets across the world (Khoury et al. 2014). While acknowledging the importance of improving the monetary benefit-sharing mechanisms, we believe that one should not lose sight of the need to maintain the non-monetary benefit-sharing mechanisms when evaluating the effectiveness of the MLS and considering options for its reform. Significant knowledge and opportunities for crop improvement accompany the materials distributed by the CGIAR genebanks, so focusing exclusively on the monetary benefits that can potentially result from germplasm flows represent too narrow a view of its overall impact. Indeed, it has been argued that non-monetary benefits from the MLS (as outlined in Articles 13.1 and 13.2(a)–(c) of the ITPGRFA) can generate much greater eco- nomic return than developing countries would ever gain through the BSF. With respect to monetary benefit sharing, it is important to underscore the fact that the primary users of germplasm from the CGIAR and the MLS have been public sector orga- nizations (in developing countries) rather than private sector entities. Indeed, it has been pointed out that a crucial factor that determines the demand for genetic resources in the seed and crop protection industries is the effort required to turn them into usable materials. Genetic resources that widen a company’s gene pool, but without the identified properties of interest, are typically considered to have little commercial value since they require con- siderable investment and the return on investment is often risky (Smolders 2005). Although new technology can assist in the search for a specific trait, the expense of doing so is generally prohibitive, particularly for smaller companies (Laird and Wynberg 2006). Larger companies that would most likely trigger the mandatory financial benefit-sharing provisions associated with the MLS tend to opt out of receiving materials from the system (Halewood and Nnadozie 2008). These kinds of reasons likely underlie the failure of efforts to ‘pri- vatize’ monetary benefit sharing through the adoption of mechanisms for mandatory pay- ments from companies based on sales of products that incorporate materials from the MLS. We believe that some other approach to monetary benefit sharing, linked to the operation of the MLS, is necessary. Such an approach should more closely reflect the public goods nature of PGRFA as well as the historical development of the international and national collections that host most of the materials that do, and will, constitute theMLS. It should also be as simple as possible, and less administratively burdensome on both the providers and users of PGRFA, to encourage, rather than discourage, participation. In particular, it could be useful not to link the collection of financial benefits to the privatization of products incor- porating materials from the MLS. Rather, it could be governments or public authorities 123 Biodivers Conserv which devise means to assume the costs of the MLS’ proper functioning, in a more familiar form of state assumed responsibility on publically valuable assets. Governments could then decide if and how they would need to recoup some of those costs; one option, which was actually discussed in early Treaty days, could be some sort of contribution from the com- mercial sector based on their annual seed sales. This approach would also be in line with the way public organizations have historically supported the collections. Of course, there are other ways to improve and enhance the functioning of theMLS and to acknowledge countries’ increasing interdependence on PGRFA, beyond adopting a new approach to monetary benefit sharing. No matter how well the system is designed or reformulated, there are practical, institutional and capacity limitations for all countries and all potential beneficiaries (from farmers to breeders and researchers) to take advantage of the MLS, even once their legal ability to do so has been established. This may be particularly true in some developing countries. Capacities and strong partnerships need to be established among the broadest possible range of stakeholders, enabling them to recognize specific trait- based needs, identify where the potentially useful materials could be within the MLS, and request, receive and use the materials concerned. A more proactive and widespread par- ticipation would contribute to a greater willingness to voluntarily introduce materials into the MLS, increasing the diversity available to agricultural research and development and giving rise to additional monetary and non-monetary benefits to be shared. It has been argued that capacity building, technology transfer and information exchange in the context of the MLS should take place in close relation to other ITPGRFA objectives, particularly the recognition and protection of farmers’ rights (Article 9). Indeed, a number of countries have flagged their concern about the MLS having too narrow a focus to the detri- ment of issues that are more closely related to farmers and their role in on-farm conservation (López Noriega et al. 2013b). After all, most of the ex situ materials that are being, or will be, circulated globally thanks to the MLS are landraces or naturally adapted resources developed and conserved by small farmers, often from developing countries. Their role today is ever more crucial for allowing the continued conservation, evolution and development of genetic resources with the potential to adapt to changing climates. Greater synergy between the architecture of the MLS and the implementation of farmers’ rights would also contribute to moving the ITPGRFA forward as a package of integrated measures, building confidence among a wider range of key stakeholders and truly reflecting global interdependence. Acknowledgments The authors are grateful to Ruaraidh Sackville Hamilton (IRRI), Daniel Debouck (CIAT), Evert Thomas (Bioversity International), Colin Khoury (CIAT) and Anne Bjorkman (Wageningen University), for their valuable suggestions and analytical inputs. They also wish to thank those CGIAR genebank curators, David Ellis (CIP), Ruaraidh Sackville Hamilton (IRRI), Jean Hansen (ILRI), Marie- Noelle Ndjiondjop (Africa Rice), and Ines Van Denhouwe (Bioversity International), who validated the data presented in the paper or corrected it by sharing internal data. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 Inter- national License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Appendix See Tables 6, 7, 8 and 9. 123 Biodivers Conserv Table 6 Current numbers of Centre Number of accessions held accessions of plant germplasm held by the genebanks of the CGIAR system Data from Gene- Africa Rice 26,098 sys, http://www.genesys-pgr.org Bioversity International 1516 (accessed on 20 November 2014) CIAT 64,721 CIMMYT 164,320 CIP 16,061 ICARDA 147,076 ICRAF 2005 ICRISAT 119,524 IITA 27,232 ILRI 20,229 IRRI 124,052 Table 7 Plant genera repre- Collection Genus Number of accessions sented in the genebank collec- tions of all CGIAR centres (genera represented by less than Africa Rice Oryza 131,840 50 accessions are grouped as Other 22 ‘‘other’’; numbers of accessions Bioversity Musa 1525 refer to those received and Ensete 4 reported by centres over time and may overestimate the current CIAT Phaseolus 36,124 living material available for dis- Manihot 5458 tribution in each genebank) Data Stylosanthes 4276 from Genesys, http://www. genesys-pgr.org (accessed on 20 Desmodium 3561 November 2014) Centrosema 2874 Aeschynomene 1209 Macroptilium 1052 Vigna 1050 Zornia 967 Brachiaria 601 Panicum 563 Galactia 561 Calopogonium 553 Rhynchosia 389 Teramnus 372 Chamaecrista 339 Desmanthus 325 Crotalaria 274 Alysicarpus 259 Pueraria 255 Canavalia 215 Dioclea 199 Leucaena 198 Indigofera 184 123 Biodivers Conserv Table 7 continued Collection Genus Number of accessions Flemingia 179 Uraria 176 Arachis 171 Clitoria 157 Lablab 155 Paspalum 155 Tephrosia 153 Phyllodium 139 Cajanus 135 Tadehagi 108 Andropogon 93 Pseudarthria 72 Neonotonia 68 Dendrolobium 62 Sesbania 62 Cratylia 52 Other 926 CIMMYT Triticum 103,780 Zea 27,279 Triticosecale 16,004 Hordeum 14,221 Aegilops 1316 X Triticoaegilops 991 Secale 438 Tripsacum 156 X Aegilotriticum 128 Other 7 CIP Ipomoea 7783 Solanum 7112 Oxalis 520 Ullucus 435 Tropaeolum 54 Other 157 ICARDA Triticum 37,214 Hordeum 31,619 Vicia 16,151 Cicer 14,906 Lens 12,463 Medicago 9418 Pisum 6110 Trifolium 5010 Aegilops 4257 Lathyrus 4184 123 Biodivers Conserv Table 7 continued Collection Genus Number of accessions Astragalus 956 Onobrychis 733 Avena 593 Scorpiurus 500 Hippocrepis 319 Trigonella 280 Coronilla 251 Lotus 246 Hymenocarpos 223 Melilotus 219 Lupinus 134 Elymus 81 Hedysarum 81 Brachypodium 78 Secale 73 Other 977 ICRAF Prosopis 929 Calycophyllum 390 Guazuma 390 Leucaena 80 Gliricidia 55 Desmodium 52 Other 109 ICRISAT Sorghum 37,901 Pennisetum 22,200 Cicer 20,140 Arachis 15,440 Cajanus 13,289 Eleusine 5957 Setaria 1542 Panicum 1306 Echinochloa 749 Paspalum 665 Rhynchosia 290 Other 45 IITA Vigna 18,237 Dioscorea 3169 Manihot 2984 Glycine 1749 Zea 798 Musa 150 Sphenostylis 145 Other 0 123 Biodivers Conserv Table 7 continued Collection Genus Number of accessions ILRI Trifolium 1649 Vigna 1161 Stylosanthes 1160 Leucaena 801 Sesbania 674 Indigofera 669 Brachiaria 663 Alysicarpus 516 Neonotonia 508 Rhynchosia 501 X Triticale 459 Macroptilium 431 Panicum 423 Tephrosia 395 Lablab 374 Centrosema 323 Teramnus 322 Cenchrus 294 Zornia 283 Phaseolus 282 Vicia 258 Digitaria 255 Medicago 252 Acacia 248 Pennisetum 245 Crotalaria 237 Paspalum 223 Cytisus 220 Chloris 194 Glycine 192 Galactia 188 Desmodium 177 Lathyrus 166 Cajanus 164 Urochloa 162 Chamaecrista 160 Aeschynomene 158 Calopogonium 152 Avena 147 Gliricidia 141 Eragrostis 136 Cynodon 130 Lotononis 130 123 Biodivers Conserv Table 7 continued Collection Genus Number of accessions Setaria 130 Pisum 126 Clitoria 122 Andropogon 109 Desmanthus 107 Echinochloa 93 Pseudarthria 93 Bothriochloa 89 Senna 89 Uraria 89 Pueraria 76 Lolium 75 Sorghum 72 Cassia 71 Hordeum 71 Festuca 64 Argyrolobium 57 Erythrina 57 Lupinus 53 Amaranthus 51 Cymbopogon 51 Hyparrhenia 51 Dolichos 50 Other 2160 IRRI Oryza 124,052 Other 22 Table 8 Countries from which accessions held by CGIAR genebanks were originally collected or improved Data from Genesys, http://www.genesys-pgr.org (accessed on 20 November 2014) Country code in Genesys Country Number of accessions in the CGIAR genebanks AFG Afghanistan 4962 ALB Albania 75 DZA Algeria 3828 AGO Angola 110 ATG Antigua and Barbuda 116 ANT Antilles 9 ARG Argentina 3991 ARM Armenia 1304 AUT Austria 564 AZE Azerbaijan 1723 BHS Bahamas 4 123 Biodivers Conserv Table 8 continued Country code in Genesys Country Number of accessions in the CGIAR genebanks BHR Bahrain 2 BRN Baker Island 215 BGD Bangladesh 8009 BRB Barbados 57 BLR Belarus 324 BEL Belgium 347 BLZ Belize 376 BEN Benin 1455 BTN Bhutan 507 BOL Bolivia 3289 BIH Bosnia and Herzegovina 59 BWA Botswana 1078 BRA Brazil 14,765 IOT British Indian Ocean Territory 1 VGB British Virgin Islands 55 BGR Bulgaria 1570 BFA Burkina Faso 2995 MMR Burma 3550 BDI Burundi 867 KHM Cambodia 4885 CMR Cameroon 5320 CAN Canada 914 CPV Cape Verde 22 CAF Central African Republic 849 TCD Chad 909 CHL Chile 2431 CHN China 15,294 COL Colombia 12,829 COM Comoros 8 COG Congo 334 COD Congo (Democratic Republic of) 687 COK Cook Islands 7 AUS Coral Sea Islands 2172 CRI Costa Rica 1543 CIV Cote d’Ivoire 10,018 HRV Croatia 63 CUB Cuba 980 CYP Cyprus 1103 CZE Czech Republic 556 DNK Denmark 206 DJI Djibouti 6 DOM Dominican Republic 497 ECU Ecuador 3934 123 Biodivers Conserv Table 8 continued Country code in Genesys Country Number of accessions in the CGIAR genebanks EGY Egypt 1831 SLV El Salvador 562 GNQ Equatorial Guinea 28 ERI Eritrea 97 EST Estonia 10 ETH Ethiopia 22,113 FLK Falkland Islands (Islas Malvinas) 2 FSM Federated States of Micronesia 7 FJI Fiji 53 FIN Finland 91 YUG Former Yugoslavia 222 FRA France 1136 GUF French Guiana 20 PYF French Polynesia 2 GAB Gabon 100 GMB Gambia 695 PSE Gaza Strip 129 GEO Georgia 1230 DEU Germany 2357 GHA Ghana 2006 GRC Greece 3921 GRD Grenada 50 GLP Guadeloupe 62 GUM Guam 9 GTM Guatemala 4447 GIN Guinea 1678 GNB Guinea-Bissau 151 GUY Guyana 156 HTI Haiti 233 HND Honduras 1476 HKG Hong Kong 21 HUN Hungary 1625 IND India 44,216 IDN Indonesia 12,087 IRN Iran 21,347 IRQ Iraq 1652 IRL Ireland 3 ISR Israel 1663 ITA Italy 2720 JAM Jamaica 189 JPN Japan 2555 JOR Jordan 5023 KAZ Kazakhstan 613 123 Biodivers Conserv Table 8 continued Country code in Genesys Country Number of accessions in the CGIAR genebanks KEN Kenya 4048 KIR Kiribati 1 KGZ Kyrgyzstan 226 LAO Laos 15,642 LVA Latvia 32 LBN Lebanon 2208 LSO Lesotho 587 LBR Liberia 3616 LBY Libya 762 LTU Lithuania 38 MAC Macau 1 MKD Macedonia 766 MDG Madagascar 4296 MWI Malawi 3214 MYS Malaysia 4832 MDV Maldives 23 MLI Mali 4850 MLT Malta 35 MTQ Martinique 17 MRT Mauritania 162 MUS Mauritius 31 MEX Mexico 77,448 MDA Moldova 94 MNG Mongolia 232 MNE Montenegro 43 MSR Montserrat 11 MAR Morocco 4989 MOZ Mozambique 413 BUR Myanmar 323 NAM Namibia 1546 NPL Nepal 5858 NLD Netherlands 780 NCL New Caledonia 11 NZL New Zealand 117 NIC Nicaragua 646 NER Niger 4983 NGA Nigeria 14,636 NIU Niue 4 PRK North Korea 2592 NOR Norway 29 OMN Oman 324 PAK Pakistan 5604 PLW Palau 2 123 Biodivers Conserv Table 8 continued Country code in Genesys Country Number of accessions in the CGIAR genebanks VUT Palestine 3 PAN Panama 1000 PNG Papua New Guinea 991 PRY Paraguay 1375 PER Peru 14,412 PHL Philippines 9224 POL Poland 426 PRT Portugal 2381 PRI Puerto Rico 364 REU Reunion 1 ROU Romania 572 RUS Russia 3529 SUN Russia 1259 RWA Rwanda 874 KNA Saint Kitts and Nevis 33 LCA Saint Lucia 37 VCT Saint Vincent and the Grenadines 54 WSM Samoa 2 SMR San Marino 3 SAU Saudi Arabia 84 SEN Senegal 3540 SRB Serbia 99 SYC Seychelles 3 SLE Sierra Leone 1997 SGP Singapore 6 SVK Slovakia 105 SVN Slovenia 8 SLB Solomon Islands 56 SOM Somalia 562 ZAF South Africa 2138 KOR South Korea 2153 ESP Spain 3567 LKA Sri Lanka 2740 SDN Sudan 3528 SUR Suriname 188 SWZ Swaziland 276 SWE Sweden 554 CHE Switzerland 1102 SYR Syria 10,776 TWN Taiwan 3075 TJK Tajikistan 2275 TZA Tanzania 4094 THA Thailand 7870 123 Biodivers Conserv Table 8 continued Country code in Genesys Country Number of accessions in the CGIAR genebanks TGO Togo 2817 TON Tonga 15 TTO Trinidad and Tobago 201 TUN Tunisia 4382 TUR Turkey 16,775 TKM Turkmenistan 587 TUV Tuvalu 1 UGA Uganda 3532 UKR Ukraine 1610 ARE United Arab Emirates 4 GBR United Kingdom 801 USA United States 12,969 UNK Unknown 6870 URY Uruguay 1229 UZB Uzbekistan 987 VEN Venezuela 4075 VNM Vietnam 3787 VIR Virgin Islands 17 YEM Yemen 2816 ZMB Zambia 2733 ZWE Zimbabwe 5717 Table 9 Top 50 most popular accessions of our distribution dataset (based on how many samples of each accession have been distributed), with information on the distributing centre, genus, frequency of distri- bution, number of recipient countries, biological status and country of origin. Data elaborated from SINGER Accession Centre Genus Frequency of Number of Biological Country of number distribution recipients status origin 328 IRRI Oryza 321 42 Landrace Philippines CIP 985003 CIP Solanum 312 76 Improved Peru 10865 ILRI Sesbania 268 66 Weedy/ Unknown wild 104 ILRI Desmodium 253 51 Improved Australia CIP 720088 CIP Solanum 252 101 Improved Argentina 4 ILRI Stylosanthes 247 53 Improved Colombia 69 ILRI Macroptilium 247 59 Improved Unknown 4918 ICRISAT Cicer 246 13 Improved India 5159 IRRI Oryza 246 21 Landrace Philippines 30333 IRRI Oryza 245 23 Landrace Philippines 6765 ILRI Desmodium 240 50 Improved Unknown 140 ILRI Stylosanthes 232 49 Improved Brazil 123 Biodivers Conserv Table 9 continued Accession Centre Genus Frequency of Number of Biological Country of number distribution recipients status origin CIP CIP Solanum 220 88 Improved Peru 379706.27 70 ILRI Leucaena 219 55 Improved Unknown 30416 IRRI Oryza 213 41 Improved Philippines ITC0249 Bioversity Musa 213 50 Weedy/ Unknown wild 75 ILRI Stylosanthes 212 50 Improved Venezuela ITC0504 Bioversity Musa 212 77 Improved Unknown ITC1123 Bioversity Musa 212 67 Landrace Unknown 599 IRRI Oryza 210 18 Breeding/ Philippines research CIP CIP Solanum 210 88 Breeding/ Peru 378017.2 research CIP 720087 CIP Solanum 209 91 Improved Argentina 6756 ILRI Macrotyloma 208 51 Improved Unknown 7035 ICRISAT Cajanus 207 16 Improved India CIP CIP Solanum 203 67 Improved Peru 374080.5 CIP 800827 CIP Solanum 199 70 Improved United States CIP 978001 CIP Solanum 195 54 Breeding/ Peru research 4973 ICRISAT Cicer 194 14 Improved India 6984 ILRI Medicago 179 37 Improved Unknown 10320 IRRI Oryza 178 30 Improved Philippines 12048 IRRI Oryza 178 38 Other Guinea ITC0506 Bioversity Musa 178 74 Improved Unknown 27748 IRRI Oryza 177 29 Landrace Thailand 71 ILRI Leucaena 176 43 Improved Unknown CIP 978004 CIP Solanum 176 64 Breeding/ Peru research 66970 IRRI Oryza 175 38 Improved Philippines CIP 984001 CIP Solanum 174 60 Breeding/ Peru research 167 ILRI Stylosanthes 173 51 Weedy/ Venezuela wild 147 ILRI Lablab 169 42 Improved Unknown 17159 ICRISAT Cicer 169 7 Weedy/ Turkey wild 5003 ICRISAT Cicer 169 12 Improved India 15036 ILRI Sesbania 167 54 Improved Uganda 6633 ILRI Chloris 167 40 Improved Unknown 11575 ILRI Cajanus 163 50 Weedy/ Unknown wild 15019 ILRI Sesbania 163 53 Weedy/ DR Congo wild 123 Biodivers Conserv Table 9 continued Accession Centre Genus Frequency of Number of Biological Country of number distribution recipients status origin 23364 IRRI Oryza 163 29 Landrace Philippines ITC0505 Bioversity Musa 163 68 Improved Unknown CIP 980003 CIP Solanum 159 54 Breeding/ Peru research 15632 ICRISAT Cajanus 158 5 Weedy/ India wild 312 ILRI Desmanthus 157 42 Weedy/ Belize wild References Bretting PK (2007) The U.S. National Plant Germplasm System in an Era of Shifting International Norms for Germplasm Exchange. 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