CAPÍTULO 1: NATIONAL INVENTORY AND PRIORITIZATION OF CROP WILD RELATIVES IN SPAIN

Manuscript published

Rubio Teso, ML, Torres Lamas, E; Parra-Quijano, M; de la Rosa L; Fajardo, J and Iriondo, JM (2018). National Inventory and Prioritization of Crop Wild Relatives in Spain. Genetic Resources and Crop Evolution 65: 1237–1253.
https://doi.org/10.1007/s10722-018-0610-0

Abstract

Crop Wild Relatives (CWR) have recently received significant attention due to their value as plant genetic resources and their contribution to world food security. We present a prioritized checklist of CWR in Spain, where the criteria of crossability with crops of economic importance, endemicity and threat status have been taken into account. First, we generated a list of the most relevant crops for Spain and at the international level. These crops were assigned to one of four use categories depending the major crop of the genus (Food, Forage & Fodder, Ornamental and Industrial & Other uses). Subsequently, the corresponding native CWR related to these crops were listed. After evaluation by national experts in plant breeding, the resulting checklist contained 930 species which was then prioritized to obtain the prioritized Spanish checklist of CWR containing 578 species. The representation of the use categories in this list ranges from 32% (Forage & Fodder) to 16% (Industrial & Other Uses). Thirty-five percent of the prioritized species are endemic to Spain and over one-fourth of them are classified under some category of threat according to the International Union for Conservation of Nature. Endemicity or threat status rates in the prioritized Spanish checklist of CWR were higher than those found in the prioritized CWR inventories of other countries. An ex situ conservation assessment for the Food and Forage & Fodder categories was also performed showing that around 71% of the species in these groups were present in genebanks.

Keywords: Food Security; Plant Diversity Conservation; Spanish Plant Genetic Resources; Checklist; Threatened Plants

Introduction

Crop quality and yields are known to be affected by climate change. Some models, using diverse climate change scenarios, crops and territories, predict a decrease of up to 40% in crop yields from 2010-2050 (Müller and Robertson 2014). At the same time, production risks are expected to increase, which may lead to an increase in world hunger (Tubiello and Fischer 2007). In Southern Europe, not only are temperatures expected to rise and precipitations expected to decrease under a climate change scenario, but the frequency of extreme events is also predicted to increase (Lotze-Campen 2011). In a conclusive meta-analysis, Challinor et al. (2014) report a highly significant negative impact of climate warming on crop yields that will be more pronounced in the second half of the century especially in tropical regions, as well as increases in yield variability that will further compromise food security. These hypothetical scenarios are already becoming apparent. In 2016 the greatest increase in global temperatures and variations in precipitation patterns were reported for the 137-year period of record (NOAA 2017). In Spain, the average temperature was 0.7°C higher than the mean of the reference series (1981-2010), placing 2016 among the warmest years on record (AEMET 2017).

In this context, farmers need to change their agricultural practices to effectively adapt to climate change, if they are to maintain and improve crop quality and yields. Such practices include adjusting planting times to avoid drought or heat stress and adopting new crop varieties, amongst others (Howden et al. 2007). However, these measures may not be sufficient (Turner and Meyer 2011), as modern cultivars may lack the ability to adapt to environmental change due to their narrow genetic base, resulting from selection applied in previous domestication and breeding processes (Stamp and Visser 2012).

Crop Wild Relatives (CWR) are wild plant species that are genetically related to crops (Heywood et al. 2007). As potential gene donors of desired traits for crops (Maxted et al. 2012), they have been successfully used in breeding for new traits and adaptations (Zamir 2001; Hajjar and Hodgkin 2007; Tester and Langridge 2010; Honnay et al. 2012). The wide range of adaptations found in CWR can be used as a genetic resource to mitigate the effects of climate change on crops, thereby helping to maintain and improve yields, and guarantee food security (Brozynska et al. 2016). The great value of CWR as a component of the Plant Genetic Resources for Food and Agriculture has been recognized in the United Nations Sustainable Development Goals (UN 2015), the Food and Agriculture Organization of the United Nations’ Second Global Plan of Action for Plant Genetic Resources for Food and Agriculture (FAO 2011) as well as the Convention of Biological Diversity (UN CBD 2010).

In global terms, CWR are seriously threatened by processes driven by human activities such as habitat fragmentation and loss, competition with invasive species, nitrogen depositions or changes in land uses, just like any other component of biological diversity (Ford-Lloyd et al. 2011; Heywood, 2011; Kell et al. 2012). The importance of CWR conservation and the best approaches to preserve these natural resources have been largely discussed (Heywood et al. 2007; Magos-Brehm et al. 2010; Maxted 2003; Pautasso 2012; Maxted et al. 2013) and over the past few years, several international projects have been implemented to conserve and manage CWR (see Online Resource 1). The in situ conservation of CWR in protected areas (Hunter and Heywood 2011), the establishment of genetic reserves (Pinheiro de Carvalho et al. 2012; Fielder et al. 2015a) and the identification of priorities and efficient sampling approaches for ex situ conservation (Khoury et al. 2015, García et al. 2017) are some of the procedures recently addressed for CWR conservation. In this context, the generation of CWR inventories is an essential first step in identifying the conservation needs of this group of species. Thus, listing and prioritizing existing CWR at the appropriate scale helps direct management efforts and underpins agrobiodiversity conservation. Two different approaches can be used to generate the inventories. The “crop list” approach uses a priority list of important crops to obtain their corresponding wild relatives. Alternatively, the “floristic” approach uses the flora of a territory as a starting point and matches it against a previously-existing catalogue of CWR species in the region or an exhaustive database of plants of economic use. To the best of our knowledge, seventeen CWR checklists have been published in the scientific literature: fifteen at the national level and two at the subnational level. These were generated for India (Arora and Nayar 1984), the United Kingdom (Maxted et al. 2007), Portugal (Magos-Brehm et al. 2008), Russia (Smekalova 2008), Israel (Barazani et al. 2008), Denmark (Bjørn et al. 2011), Venezuela (Berlingeri and Crespo 2012), Finland (Fitzgerald 2013), Benin (Idohou et al. 2013), the United States (Khoury et al. 2013), Italy (Panella et al. 2014), Cyprus (Phillips et al. 2014), China (Kell et al. 2014), the Czech Republic (Taylor et al. 2017), the Netherlands (van Treuren et al. 2017), England (Fielder et al. 2015a) and Scotland (Fielder et al. 2015b). Furthermore, a global inventory (Vincent et al. 2013), two European catalogues (Heywood and Zohary 1995; Kell et al. 2005) and a prioritized checklist of North Africa (Lala et al. 2017) have also been published. Similarly, some regional and country red lists of CWR have been generated (VMABCC-BIOVERSITY 2009; Bilz et al. 2011).

Governments and institutions dealing with wild and cultivated biodiversity conservation should take responsibility for the in situ and ex situ conservation of CWR. This is especially relevant for Spain, as it is one of the countries with the greatest number of plant species in Europe (7071 species, Aedo et al. 2013). In fact, it is the second country with the greatest number of CWR in Europe, hosting 26% of the Euro-Mediterranean CWR species (Kell et al. 2008). In addition, many of them are only found in this country, as the Iberian Peninsula is one of the two main centers of biodiversity in the Mediterranean Basin and presents a high number of endemics (Medail & Quezel 1999). The interest of the research community in CWR native to Spain is not new. Significant efforts have been made in the last few decades to explore, conserve and characterize wild gramineae (Soler et al. 1997), Brassica L. (Gomez-Campo et al. 2005), Vitis L. (De Andrés et al. 2012) and Medicago L. (Prosperi et al. 2006), among others. Although CWR conservation in Spain has been historically neglected by both the departments of wildlife conservation and agriculture at the national and autonomous community levels, its importance is becoming more widely recognized. Consequently, CWR have been included in the Spanish National Strategy of Plant Conservation (MAGRAMA 2014) and the Spanish Plant Genetic Resources Center has set some initiatives for the collection and preservation of CWR seed accessions. CWR germplasm is also stored in the César Gómez Campo genebank at the Polytechnic University of Madrid and the Agrifood Research and Technology Center of Aragón. REDBAG, the network of seedbanks associated with the Ibero- Macaronesian Association of Botanical Gardens, also preserves CWR seeds as part of their efforts to preserve threatened plant species. In parallel, native and exotic CWR have been actively used in breeding in Spain. For instance, Pico et al. (1999), Pérez de Castro et al. (2005), Caro et al. (2015) and Campos et al. (2017) worked on the development and evaluation of breeding tomato lines partially resistant to Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus derived from Solanum chilense (Dunal) Reiche and S. peruvianum L.. Similarly, Martín-Sánchez et al. (2003) and Fernández-Martínez et al. (2000) used different wild accessions of Aegilops and Helianthus species stored in Spanish germplasm banks to deal with Hessian fly pests in wheat and Sunflower broomrape, respectively. So far, we have barely begun to explore the potential use of crop wild relatives from Spain. Some examples of how they are being used for breeding are found in Table 1. Taking all this into account, from a national strategy perspective, it is essential to list the main CWR taxa that occur in the country and prioritize the CWR species in need of active conservation measures.

The aim of this paper was to develop a checklist of CWR of importance in Spain and a prioritized list for the implementation of conservation plans. In this context, we asked: a) What criteria should be applied to prioritize CWR in Spain? b) What is the threat status of the prioritized CWR checklist at the national and European levels? c) Are these species under any legal protection in Spain? d) What are the levels of endemicity of the prioritized CWR checklist? e) How are their populations distributed and preserved ex situ in Spain?

Material and Methods

The process involved in the generation of the prioritized CWR list is summarized in Figure 1.

Baseline List of Crop Genera and List of Selected Crop Genera

More than 6500 CWR species can be found in Spain according to the PGR Forum project (Kell et al. 2008). This large number of species, comprising over 80% of Spanish flora, is simply too big to manage for conservation purposes or use. Consequently, the first step in generating the national CWR checklist was to identify crops that contributed to global food security and were of economic importance in Spain and obtain a list of the corresponding genera. This was achieved in two stages: a) compilation of the Baseline List of Crop Genera and associated information and b) selection of crop genera. Crops under consideration were classified into four use categories: 1) Food, 2) Forage & Fodder, 3) Ornamental and 4) Industrial & Other uses.

a) Compilation of the Baseline List of Crop Genera and associated information: The crops considered under the Food, Forage & Fodder and Industrial & Other uses categories were obtained from those listed in Annex 1 of the International Treaty on Plant Genetic Resources for Food and Agriculture (FAO 2010) and in the Spanish Annual Directory of Agricultural Statistics of 2010 (MAGRAMA 2011). From the latter, we extracted information on production and cultivated area for each crop. For the ornamental crops category, we recorded the most important crops in Europe according to the number of applications for registration of new varieties from the Annual Report of the Community Plant Variety Office in Europe (2011). The list of the taxa protected by the members of the Union by the International Union for the Protection of New Varieties of Plants (UPOV 2011) and the Germplasm Resources Information Network database of the United States Department of Agriculture (GRIN-USDA 2017) were also consulted to check for other crops of importance not yet incorporated in the list. The UPOV database was also used to collect data on the number of species, infraspecific taxa and/or hybrids associated with a particular crop. Similarly, specialized publications on trends in plant breeding were checked (Kole 2011a, b, c, d, e) as well as inventories from other countries and CWR checklists (Berlingeri and Crespo 2012; Labokas et al. 2010; Magos-Brehm et al. 2010; Markkola, 2005). The genera corresponding to these crops were listed in a database including all the information collated from the above-mentioned data sources.

This database was completed with information on whether these genera contained wild species native to Spain following Flora Iberica (Castroviejo 1986-2012) for Peninsular Spain and the Balearic Islands and Acebes Ginovés et al. (2010) for the Canary Islands.

b) Selection of crop genera: After careful consideration of all compiled data, we selected a list of genera based on the following criteria: 1) the genus must contain at least one species native to Spain and 2) it must comply with at least one of the following items: a) is listed in Annex 1 of the International Treaty for Plant Genetic Resources for Food and Agriculture, indicating its relevance as a contributor to global food security, b) contains a crop in the Spanish Annual Directory of Agricultural Statistics (MAGRAMA 2011) or c) contains a crop that has at least one registered variety in Spain in the period 1973-2010, as an unequivocal sign of economic concern to the country. The resulting reduced list of crop genera was assessed by experts from institutions dealing with crop breeding in Spain. They validated all selected genera and proposed some additional genera valuable for breeding according to their expertise.

Spanish Checklist of Crop Wild Relatives

Wild species within the selected crop genera native to Spain were identified using Flora Iberica - the national flora of reference in Spain (Castroviejo 1986-2012) -, or the Anthos project -linked to Flora Iberica experts - (Anthos 2017). The wild species native to the Canary Islands were identified following Acebes Ginovés et al. (2010). When the genera were not yet published in any of these references, other bibliography was consulted (Romero Zarco 1996; Pascual 2004; Killian et al. 2011). The CWR checklist was set at the taxonomic level of species: infraspecific taxa levels were not included as separate entities.

Information regarding primary use category, IUCN threat category and number of infraspecific taxa belonging to the species included in the Red List of Spanish Vascular Flora (Moreno 2008), endemicity, crossability potential with crops of reference and number of chromosomes, was gathered for each CWR species on the list. The content and source of each field is shown in Online Resource 2. Crossability potential was assessed according to the gene pool concept by Harlan and de Wet (1971) (possibility of gene transfer between wild and cultivated species) and the taxon group concept by Maxted et al. (2006) (assimilation of taxonomic hierarchy to the gene pool concept). Crossability information was obtained for each species following Flora Iberica chapters, the Harlan and de Wet Inventory (https://www.cwrdiversity.org/checklist/), the Germplasm Resources Information Network database of the United States Department of Agriculture (GRIN-USDA 2017) or additional references. Taxonomical information was obtained following Flora Iberica chapters, the Anthos project or additional references. All sources used for this assessment are indicated in Online Resource 3. To apply the crossability potential according to the gene pool concept, a complementary list of cultivated species was generated for each selected genus using the Germplasm Resources Information Network database of the United States Department of Agriculture (GRIN-USDA 2017) as reference. Each species was assigned to its corresponding gene pool or taxon group concept. Moreover, when available, information on confirmed or potential use of the species was registered in the database.

Prioritized Spanish Checklist of Crop Wild Relatives

To generate a manageable list of CWR species that could be subjected to conservation status assessment and conservation measures, the Spanish Checklist of Crop Wild Relatives was prioritized using the previously gathered information. Criteria used for prioritization included: crossability potential (gene pool and taxon group concepts), threat status and endemicity for the Food and Forage & Fodder categories and only crossability potential for the Ornamental and Industrial & Other uses categories. Prioritized species were those found in gene pool categories 1 (primary gene pool: cultivated and wild forms of the crop) and 2 (secondary genepool: gene transfer is possible using conventional breeding techniques) (Harlan & de Wet 1971) or taxon group category 2 (same series or section as a crop) and 3 (same subgenus as a crop) (Maxted et al. 2006). The gene pool concept always prevailed over the taxon group concept, but when information on crossability between species was unavailable, the taxon group concept criterion was applied. For the Food and Forage & Fodder use categories, species belonging to any of the IUCN threat categories (critically endangered, endangered, vulnerable and near threatened) or endemic to Spain were also included in the Prioritized Spanish Checklist of Crop Wild Relatives (Table 2).

The resulting list was checked against the National Catalogue of Threatened Species in Spain promoted under Law 42/2007, royal decree 139/2011 (B.O.E. 46, 2011). The inclusion of species in this catalogue provides them with legal protection. This entails the design and implementation of appropriate conservation plans and the commitment to regularly assess their conservation status. Furthermore, the European CWR threat assessment by Bilz et al. (2011) was used to identify the species on the checklist that are threatened in the European context.

Because the seventeen Autonomous Communities in Spain hold have responsibility for the conservation of biodiversity and genetic resources in their territories, the number of species on the priority CWR checklist present in each autonomous community was estimated using occurrence data. Data were downloaded from the data portal of the Global Biodiversity Information Facility (GBIF 2011-2013) (for 500 species out of the 578 taxa on the Prioritized Spanish Checklist of Crop Wild Relatives. Data were not available for the remaining 78 species at that moment. All data were subject to taxonomic harmonization and quality assessment to only select data of good quality. The criteria applied for quality selection were: 1) Geographic coordinates had at least two decimal digits of decimal degree (around 1 km resolution); 2) Data records also included the name of the locality, which was congruent with the given coordinates. Data records not complying with both requirements were eliminated. Duplicated records, according to the geographic coordinates, were also eliminated.

Finally, all prioritized species were checked against the databases of the Spanish Plant Genetic Resources Center which gathers information from 19 different seed banks related to plant genetic resources in Spain. Furthermore, ten germplasm banks belonging to the REDBAG network, i.e., the Spanish Network of Germplasm Banks for Wild Plants and Autochthonous Plant Genetic Resources, associated with the Ibero-Macaronesian Association of Botanical Gardens, were also consulted. The curators of the corresponding germplasm banks were individually contacted to gather this information. The EURISCO catalogue (EURISCO 2017), the Germplasm Resources Information Network database of the United States Department of Agriculture (GRIN-USDA 2017) and the GENESYS Global Portal on Plant Genetic Resources (GENESYS 2017) databases were also consulted to complete the dataset with worldwide data. The data from each institution included number of accessions for each species (only those collected in Spain) and the coordinates of the collecting sites, when available. The information on number of accessions was added to the database associated with the Prioritized Spanish Checklist of Crop Wild Relatives. To identify the species in the most urgent need of collection to improve CWR collections in germplasm banks, we selected species categorized in genepools 1b and 2, or taxon group 2, under any category of threat according to the International Union for Conservation of Nature (IUCN), endemic to Spain and with less than five accessions in germplasm banks. We used five accessions as a threshold, as this is considered the minimum number of populations needed to conserve the genetic diversity of a species (Brown & Briggs, 1991). Priority for collection was assigned as follows: 1) Urgent priority. Primary or secondary gene pool and taxon group, endemic and threatened. No representation in gene banks; 2) Urgent. Species not represented in gene banks; 3) Need collecting. Less than five populations represented in gene banks; 4) Non prioritary for collection. More than five accessions in gene banks for each species.

Results

Baseline List of Crop Genera and List of Selected Crop Genera

The baseline list of crops of importance and associated genera comprised 203 genera (Online Resource 4). The list of selected crop genera used to generate the CWR checklist contained 61 genera. This list is shown in Online Resource 5 together with the information on family, use category and reason for inclusion in the list.

When categorized by use, the Food category contained 33 genera in 13 families; the Forage & Fodder category 12 genera in 2 families; the Ornamental category 5 genera in 5 families and the Industrial & Other uses category 10 genera in 7 families. Fabaceae and Poaceae are the two most important families with 11 genera each, followed by Brassicaceae with 7 genera.

Spanish Checklist of Crop Wild Relatives

The Spanish Checklist of CWR species rendered a total of 929 species. The Food category included 223 species, the Forage & Fodder category had 260, the Ornamental category had 240 and the Industrial & Other uses category had 206 (Figure 2).

This checklist of species together with information gathered on priority use, taxonomic classification, gene pool or taxon group concepts, threat status, endemicity, and number of chromosomes was compiled into the Spanish Checklist of Crop Wild Relatives database which is available at: https://pgrsecurespain.weebly.com/crop-wild-relatives-in-spain-ndash-spanish-checklist-of-cwr.html. As information on gene pool was only found for 243 of the 929 species, the rest of the species were assigned their corresponding taxon group category.

Prioritized Spanish Checklist of Crop Wild Relatives

Applying the agreed criteria to each use category reduced the number of species on the list to 578 (62% of the original checklist). All genera on the original checklist had species on the prioritized checklist except for Fragaria L. (strawberry relatives) whose species native to Spain did not meet the crossability criteria.

The Prioritized Spanish Checklist of Crop Wild Relatives contains 137 species related to Food crops, 185 to Forage & Fodder crops, 161 to Ornamental crops and 95 to Industrial & Other uses crops (Figure 2). All prioritized species, together with all gathered information during the process is available at the Prioritized Spanish Checklist of Crop Wild Relatives (https://pgrsecurespain.weebly.com/ crop-wild-relatives-in-spain---prioritization-of-the-checklist.html) and in the Supplementary Material Section of this Chapter (Annex 1).

In compliance with the prioritization criteria used, the selected species mainly belonged to the primary or secondary gene pools (107 and 95 species, respectively) or to taxon group 2 (203 species) (same section or subsection as the crop) (Figure 3a). Thus, over 70% of the selected species have a direct potential use in plant breeding. Forty percent of the prioritized species are endemic to Spain Over one-fourth of the species (155 out of 578) are classified under one of the IUCN threat categories at the national level, including the Near Threatened category (Figure 3b), and 15 species are threatened at the European scale (Table 3). Furthermore, 43 species of the Prioritized Spanish checklist of Crop Wild Relatives are included in the National Catalogue of Protected Species under law 42/2007, royal decree 139/2011 (B.O.E. 46, 2011) (Online Resource 6).

Prioritized Spanish CWR were quite homogeneously distributed in all Autonomous Communities of Spain. Andalucía, the largest autonomous community, also had the greatest number of of priority CWR species, followed by Castilla-León and Castilla-La Mancha in Central Spain (Figure 4).

The ex situ assessment showed that germplasm banks hold accessions of approximately 70% of the prioritized CWR. Thus, 176 species are not represented in any of the institutions contacted. The Prioritized Spanish Cheklist of Crop Wild Relatives (https://pgrsecurespain.weebly.com/crop-wild-relatives-in-spain--- prioritization-of-the-checklist.html) shows the number of accessions preserved in genebanks for all prioritized species. Less than 13% of the species represented in genebanks has 20 or more accessions in ex situ collections, while 34% has between only 1 and 4 accessions.

A total of 51 species of primary importance (because they were endemic to Spain, threatened according to IUCN, and belonged to the primary or secondary genepools or taxon group 2) had less than five accessions in germplasm banks. Of these, twenty-three had no representation in genebanks (Priority 1). One hundred and fifty-three species are found to be in priority collecting category 2 (Urgent. Species not represented in gene banks), 195 in priority collecting category 3 (Need collecting. Less than five populations represented in gene banks) and finally 207 in priority collecting category 4 (Non priority for collection. More than five accessions in gene banks). All this information can be consulted for each species in the Prioritized Spanish Checklist of Crop Wild Relatives (https://pgrsecurespain.weebly.com/crop-wild-relatives-in-spain---prioritization-of-the- checklist.html).

Discussion

Currently published CWR checklists and inventories provide a good background that exposes the regional and global importance of these species and the idiosyncrasy of each country in their development process. Our study fills an important gap in this area, as Spain has one of the largest and most diverse flora in the Euro-Mediterranean region (Médail and Quézel 1997; Molina-Venegas et al. 2015).

Crop list vs. floristic approach

The development of the Spanish Checklist of Crop Wild Relatives followed a “crop list” approach. We preferred this approach because the CWR European catalogue returns more than 6500 species for Spain (Kell et al. 2008), which represents almost 80% of Spanish flora. Such an extensive list is far too large to be operational for designing an effective strategy for CWR conservation, management and use. Furthermore, many species in this catalogue are already managed by other interest groups in the public administration, e.g. forestry species, which have their own National Inventory and conservation program (MIMA 2006). Thus, we generated the CWR checklist directly from a list of important crops to efficiently use economic resources and avoid duplication and overlap in the case of species that were already managed by the public administration.

The creation of a crop list according to global, national and regional socio-economic criteria and the subsequent identification of its CWR significantly simplified the procedure. It allowed us to focus on the most important CWR for Spain without neglecting any of the crops that contribute to the country’s economy and to worldwide food security. This approach, also followed by Berlingeri and Crespo (2012) in Venezuela, and Idohou et al (2013) in Benin, may be a valid alternative for countries with large floras that require a manageable list in which the most important CWR are represented.

In most other cases, national CWR checklists have been developed following a “floristic” approach. Thus, the CWR checklists of the United Kingdom, Portugal, Italy, Cyprus, the Czech Republic, England and Scotland were generated by matching the corresponding floras against the Crop Wild Relative Catalogue for Europe and the Mediterranean (Kell et al. 2005), and this initial checklist was then prioritized. Similarly, in the generation of the CWR checklist of the United States (Khoury et al. 2013), the completed volumes of Flora of North America (FNA 1993+) and other sources of native flora were crossed against the Germplasm Resources Information Network database (GRIN-USDA 2017), based on Wiersema and León (1999). A similar approach was followed to generate the CWR checklist of China (Kell et al. 2014). However, the CWR Checklist of Israel was directly generated by consulting a multidisciplinary panel of experts including botanists, ecologists and plant breeders (Barazani et al. 2008).

Despite the differences in the approach to generating these national checklists, similar use categories are found in all lists consulted. The food and forages groups were considered in all of them, whereas the ornamental, environmental, medicinal or industrial uses were included in all inventories except for the Venezuelan checklist (Berlingeri and Crespo 2012). This broad perspective on plant genetic resources is important because different economic sectors could benefit from it.

Delimitation of Crop Wild Relatives in the Spanish Checklist

Non-native species were excluded from the Spanish Checklist of Crop Wild Relatives due to the large number of CWR species naturally occurring in Spain and the need for strict prioritization. Furthermore, introduced species growing far from their centers of diversity (“geographical areas where the botanical species shows a higher degree of variation and where there are significant genetic variants represented by alleles” (Corinto 2014)) may lack high genetic variability, which is fundamental for breeding purposes. However, according to Bossdorf et al. (2005), non-native species might be a source of genetic variation that should not be undervalued. These species were considered in all the consulted checklists except those for Italy and Cyprus. Our CWR checklist was equally restrictive from a taxonomical point of view, and only taxa at the species level were included. Consequently, the reference CWR checklist for Spain (929 species) is smaller than those generated for other countries, such as Finland (1905 taxa), UK (1955 species), Portugal (2261 taxa), USA (2495 taxa), the Czech Republic (3283 species) or China (almost 24500 species). In our opinion, national CWR checklists should be taxonomically robust, manageable, useful and dynamic, even if this means trading the exhaustiveness of the list for these properties. The generation of an initially delimited list of CWR also facilitates their subsequent prioritization to take direct actions. The maintenance of the checklist as a database available in the web allows for subsequent updates to adjust for potential taxonomic changes and variation in the assessment of the list of the most important crops.

Prioritized Spanish Checklist of Crop Wild Relatives

The criteria used to further prioritize the CWR of Spain was similar to those used by other authors in other countries and involved the concepts of crossability, threat and endemicity. With regard to crossability, it is noteworthy that only 26% of the species on the checklist could be classified according to the gene pool concept. Information on crossability between CWR and cultivated species is generated (and held) by plant breeders. This type of valuable feedback needs to be captured by those documenting plant genetic resources, but this is not always easy because the information may be confidential and not available as published material. This lack of available information concerning direct crossability experiments is in consonance with the results found in previous studies (Kell et al. 2014; Fielder et al. 2015a, b). Although the taxon group concept can be a useful proxy to make decisions when genepool information is not available, these results clearly show that crossability experiments between crops and their wild relatives are essential to assess and facilitate the potential use of CWR in plant breeding.

Threat assessment showed that 23% of the species on the prioritized list were under a threat category described by the IUCN. This percentage is higher compared to other countries like Cyprus (9%), Germany (16%), Lithuania (16%), Norway (13%), the UK (12%) and even compared to the large flora of China (17%), but lower compared to countries such as the Czech Republic (54%), Finland (71%), Jordan (32%) or Portugal (65%) (Kell et al. 2014, Iriondo et al. 2016). Regarding European threat assessment, 12% of the species on the list (66 of the 578 prioritized CWR) are classified in some category of threat at the European level. Some national or subnational strategies already include the identification of the level of threat of CWR species at the European level (Fielder et al. 2015a, b). However, if all national or subnational strategies included this objective, integrated preservation plans could be designed among countries, making better use of conservation resources and constructing effective conservation networks. Transboundary conservation efforts through protected areas complexes have been already reported as beneficial (Sheppard 1999), and some claim that would be the most sensible path to achieving real conservation success (Chester 2005). However, the final boost and distribution of efforts, considering both the European and national idiosyncrasy, should depend on the interested countries and their specific needs, efficiently managing national resources.

Despite the socio-economic importance of CWR and the large number of threatened CWR species (135 according to the IUCN criteria), only 43 CWR species on the prioritized list are under legal protection in Spain. We must underline that nine species are threatened at both the Spanish and European levels (see Table 3). Three of these species (endangered Asparagus fallax Svent. and Cicer canariense A. Santos & G. P. Lewis and critically endangered Medicago citrina (Font Quer) Greuter) are already protected in Spain by law and considered a priority for conservation (BOE 46, 2011). As a result, conservation plans are being designed and implemented for these species, and their conservation status is regularly assessed. However, the other six species require urgent conservation measures and should be included in the catalogue of protected species. Furthermore, species threatened at the European level which have not been assessed in the Spanish Red list should be evaluated in future editions of the Spanish Red List of Vascular Flora. The publication of the present list can also be very helpful in subsequent reviews of the national catalogue of protected species to include all endangered priority CWR species under legal protection. The specific mention of CWR in the Spanish National Strategy of Plant Conservation (MAGRAMA 2014) is an important step in recognising the importance of conserving CWR at the national level, even though implementing active conservation plans is the responsibility of the autonomous communities.

Regarding endemicity data, the Prioritized Spanish Checklist of Crop Wild Relatives contains a notably higher percentage of endemics (35%) than the priority lists of other countries, except Portugal (65%). According to Iriondo et al. (2016), other European countries have far fewer endemics on their prioritized lists compared to the Iberian Peninsula: the priority Czech CWR list has 13% endemic species, followed by Germany with 10%. Even lower percentages are found in the priority lists of Cyprus (3%), the United Kingdom (1%), Lithuania (1%), Finland 0% and Norway 0%. These numbers highlight the value of Iberian biodiversity as an essential component of the Euro-Mediterranean region.

According to Brown and Briggs (1991) and Maxted et al. (2008), a minimum of five accessions from five different populations should be represented in germplasm banks to properly represent the genetic diversity of a species. Based on this premise, in addition to prioritizing the collection of the 176 species on the prioritized list that have no accessions in genebanks, CWR germplasm collections should also concentrate on improving the representation of conserved species to obtain the minimum number of sampled populations to represent their genetic diversity. From these two sets, the 51 species of the prioritized list that are endemic, threatened, and have less than five seed accessions preserved should have the highest priority. An important point to consider is that the coordinates of the accessions have not been evaluated in this study (unavailable in many cases), which may lead to duplicates in entries among the different institutions contacted. Hence, the representation of population diversity may be overestimated.

In contrast to the above-mentioned criterion of including seed accessions from a minimum of five populations in genebank collections, Whitlock et al. (2016) propose that over 35% percent of the populations should be preserved to cover the recommendations of the Convention of Biological Diversity. Although this study was designed for the implementation of in situ conservation plans, it could also be applied to ex situ conservation, as its major objective was also to preserve enough genetic diversity to adequately represent the species. Considering that ex situ conservation aims to preserve as much genetic diversity as possible (Bachetta et al. 2008), the most adequate number of accessions to preserve should actually be estimated on a species-per-species basis, taking into account the breeding system of the species as well as the distribution and size of the populations along with their environmental conditions (Brown & Marshall 1995). In addition, the use of existing molecular data can also help to determine the minimum number of accessions required to properly represent the genetic diversity contained by a species (Camadro 2012).This suggests that the “minimum of five populations” criterion should be replaced in the long term by a more ambitious goal in which the number of accessions to be collected is estimated on a species-per-species basis, in a proportional way to the genetic diversity of the species. Recent publications (Parra-Quijano et al. 2012a, b, Phillips et al. 2014, 2016) advocate the inclusion of ecogeographic information when planning collecting missions and in situ conservation measures, making use of the ecogeographic characterization of the accessions or population data. This ecogeographic information can also be used as a proxy to estimate genetic diversity (Maxted et al. 2012) and infer possible genetic adaptation patterns that the species may contain (Parra-Quijano et al. 2012a).

Concluding remarks

Existing CWR species, along with the rest of biodiversity components, should be conserved using strategies based on the establishment and management of protected areas and the sustainable use by humans of the rest of the territory, as well as species-specific approaches. In this context, the proper identification of priority CWR is essential. The generated Spanish Checklist of Crop Wild Relatives should be coordinately managed by the agriculture and environment departments of the public administration, and continuously revised in a participatory way to include species with real potential that meet the needs of the changing trends in agriculture and plant breeding.

However, the mere generation of a CWR checklist does not assure proper conservation. The conservation status of priority CWR should be properly assessed, and species-specific in situ and ex situ conservation actions should be implemented when needed. In this sense, the Spanish Checklist and Prioritized Checklist of CWR are already being used to assess the ex situ conservation of CWR in the collections of the Spanish Plant Genetic Resources Center (De la Rosa et al. 2013). Furthermore, they are also being used to plan new CWR seed collecting campaigns to improve their ex situ conservation status (García et al. 2015).

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Supplementary material

Online Resource 1: Selection of projects for the conservation of CWR developed over the last few years. Available at: https://link.springer.com/article/10.1007/s10722-018-0610-0, Supplementary Material 1.

Online Resource 2: Information gathered for each CWR species listed for the generation of the Prioritized Spanish Checklist of Crop Wild Relatives. Available at: https://link.springer.com/article/10.1007/s10722-018-0610-0, Supplementary Material 2.

Online Resource 3: List of references used for the compilation of associated information of the Spanish crop wild relatives. Available at https://link.springer.com/article/10.1007/s10722-018-0610-0, Supplementary Material 3.

Online Resource 4: Database with the baseline list of crops of importance and associated information for each genus. Information on use of the crop, inclusion of the crop in the Annex 1 of the International Treaty of Plant Genetic Resources for Food and Agriculture, nativeness, economic importance and use in breeding is displayed. Available at https://link.springer.com/article/10.1007/s10722-018-0610-0, Supplementary Material 4

Online Resource 5: List of prioritized genera obtained for the generation of the Spanish Checklist of CWRs. Information on families, use categories to which they have been assigned and the reason for their inclusion on the list. Genera ordered by use category and alphabetically. Codes: 1 = Included in Annex 1 of the International Treaty for Food and Agriculture; 2 = Included in Spanish Annual Directory 2010; 3 = Included in the list of registered varieties, period 1973-2010; 4 = Experts in agrobiodiversity advice. Available at https://link.springer.com/article/10.1007/s10722-018-0610-0, Supplementary Material 5

Online Resource 6: List of protected species under law 2007/42, royal decree 139/2011 and on the Checklist or on the Prioritized Checklist of Spanish of Crop Wild Relatives. Codes for categories: 1 = Food; 2 = Forage & Fodder; 3 = Ornamental; 4 = Industrial & Other uses. * = The species are not prioritized but are listed on the Spanish Checklist of Crop Wild Relatives. ** = These species are not included on the Spanish Checklist of Crop Wild Relatives nor in the Prioritized Checklist because Diplotaxis was one of the genera recommended by experts and only those species suggested by them were included. *** = These species are not included on the Spanish Checklist of Crop Wild Relatives nor on the Prioritized Checklist because Flora Ibérica does not include them in the publication of their respective chapters. Available at https://link.springer.com/article/10.1007/s10722-018-0610-0, Supplementary Material 6.