High proportion of cactus species threatened with extinction

ARTICLES PUBLISHED: 5 OCTOBER 2015 | ARTICLE NUMBER: 15142 | DOI: 10.1038/NPLANTS.2015.142 High proportion of cactus species threatened with extinction Bárbara Goettsch et al.* A high proportion of plant species is predicted to be threatened with extinction in the near future. However, the threat status of only a small number has been evaluated compared with key animal groups, rendering the magnitude and nature of the risks plants face unclear. Here we report the results of a global species assessment for the largest plant taxon evaluated to date under the International Union for Conservation of Nature (IUCN) Red List Categories and Criteria, the iconic Cactaceae (cacti). We show that cacti are among the most threatened taxonomic groups assessed to date, with 31% of the 1,478 evaluated species threatened, demonstrating the high anthropogenic pressures on biodiversity in arid lands. The distribution of threatened species and the predominant threatening processes and drivers are different to those described for other taxa. The most significant threat processes comprise land conversion to agriculture and aquaculture, collection as biological resources, and residential and commercial development. The dominant drivers of extinction risk are the unscrupulous collection of live plants and seeds for horticultural trade and private ornamental collections, smallholder livestock ranching and smallholder annual agriculture. Our findings demonstrate that global species assessments are readily achievable for major groups of plants with relatively moderate resources, and highlight different conservation priorities and actions to those derived from species assessments of key animal groups. lants are of fundamental importance to much of the rest of biodiversity and to many ecosystem functions, processes and services. However, the global status of plant species, that is their likelihood of extinction in the near future, remains poorly understood. Only 19,374 (6%) of an estimated ∼300,000 species1 have been evaluated against the current IUCN Red List Criteria2. Moreover, global species assessments, in which the extinction risk of every extant species in a taxonomic group is systematically assessed, have been conducted only for very few plant groups (such as cycads, conifers, mangroves, sea grasses3–5) of which most are not especially diverse. This situation is troublesome because there is evidence suggesting that the conservation status of plant species is of particular concern. Despite the small proportion of plants whose threat status has been evaluated, they nonetheless constitute a high proportion (47%) of all threatened species (across all kingdoms) currently on the IUCN Red List5. In addition, plant species are known to have geographic range sizes, a key correlate of extinction risk, that are on average smaller than those of many other groups; the smallest ranges are typically also much smaller than their equivalents among vertebrate groups6. Estimates of likely levels of recent and future plant extinction also indicate that these may be high7,8. Responding to this concern, determining the threat status of all known plant species, as far as is possible, has been identified as a key target for the Global Strategy for Plant Conservation 2011– 2020 (ref. 9). This follows the global failure to meet the previous incarnation of this target as of 2010 (ref. 10). It is difficult to determine why, in contrast to vertebrates5,11,12, progress has been so slow, and comprehensive assessments of plant groups are so scarce. Likely reasons include the assumption that there is insufficient information available to assess most plant species against the IUCN Red List Criteria, including data on species’ geographic distributions (although much valuable distributional data undoubtedly reside, unsynthesized, in herbaria and botanical collections). In addition, P plants lack the popular appeal of some animal groups, making it difficult to attract the funding to support global species assessments. And the costs of such assessments are thought to be restrictively high13–18. Here we challenge these assumptions, presenting the results of the largest comprehensive assessment to date of an entire plant taxon, the cacti, against the IUCN Red List Categories and Criteria (1,480 extant species of which 1,478 were evaluated, with two species for which no information could be obtained). We focus on the levels of threat to species, how species at different levels of threat are distributed, the nature of the threats and the practicality of such global species assessments for plants. The cacti are a culturally significant group, perceived as amongst the more charismatic of plant taxa. This has led to a long history of human use, including for private and public ornamental plant collections, leading to major conservation concerns. Surprisingly, only 11% of cactus species had been evaluated for the Red List before 2013. Cacti are distributed predominantly in, and are somewhat emblematic of, New World arid lands (only one species naturally occurs in Africa and Asia; Supplementary Table 1). Despite huge anthropogenic pressures, these regions have not attracted the conservation attention associated with other biomes, particularly tropical forests19,20. Levels of threat Using the IUCN Red List Categories and Criteria, we found that cacti are the fifth most threatened5 of any major taxonomic group to be completely assessed to date, with 31% of species threatened. The only groups to contain a higher proportion of threatened species are cycads (63% threatened species5), amphibians (41%5,11), corals (33%5,21) and conifers (34%5). Therefore, three of the five most threatened groups assessed to date are plants. By comparison, 25% of mammal species5,12 and 13% of bird species are threatened5. Among the cacti, 99 (6.7%) species are classified as Critically Endangered, 177 (12%) as Endangered and 140 (9.4%) as Vulnerable (Supplementary Table 2). *A full list of authors and their affiliations appears at the end of the paper. NATURE PLANTS | www.nature.com/natureplants 1 ARTICLES a NATURE PLANTS Threats b 14 31 1 1 c d 27 36 1 1 Figure 1 | Geographic distribution of threatened species. a–d, Number of threatened species (IUCN Red List Categories Vulnerable, Endangered and Critically Endangered) of cacti (a), amphibians (b), birds (c) and mammals (d) (see Methods). Hotspots of threat The hotspots of threatened cactus species overlap little, if at all, with those that have been highlighted for other taxonomic groups and that consequently have driven much thinking about the role of such areas in conservation planning (Fig. 1). Whereas hotspots of threatened cacti are inevitably found in arid regions, those of threatened species of amphibians, birds and mammals tend to be found in more mesic habitats. The peak of threatened cactus species richness is found in a highly restricted area in southern Rio Grande do Sul, Brazil, and northern Artigas, Uruguay (area ∼500 km2; Fig. 1a). This region also shows a peak in the proportion of species threatened with extinction (Fig. 2a). Other hotspots of threatened cacti are found in the states of Querétaro and San Luis Potosí, and in Oaxaca and Puebla in the Tehuacán-Cuicatlán region, Mexico; in Brazil in eastern Bahia and northern Minas Gerais; in Chile in the southern portion of Antofagasta; and in eastern Uruguay (Fig. 1a). The narrowness of the peaks of threatened species richness of cacti reflects their particularly small geographic range sizes (first quartile <1,332 km2, median range size of threatened species is 1,529 km2). Other areas with a low overall richness but a high proportion of threatened species occur in Guatemala, Colombia and several parts of Peru and Chile (Fig. 2a). The main centres of cactus diversity are found in the Chihuahuan Desert and in the Tehuacán-Cuicatlán region, in northern and central Mexico respectively, and in southern Bolivia and eastern Brazil (Fig. 2a; ref. 22). Some of these species-rich areas coincide with hotspots of threatened cactus species (Fig. 1a). 2 DOI: 10.1038/NPLANTS.2015.142 Cacti experience a diverse range of threats, the predominant processes (that is the direct human activities responsible for the degradation, destruction and/or impairment of biodiversity23) being land conversion to agriculture and aquaculture, collection as biological resources, and residential and commercial development (Figs 3a and 4a). Agriculture is the most widespread threat to cacti, affecting species in large parts of northern Mexico, Mesoamerica and the southern portion of South America (Fig. 3a). Cacti in coastal areas, such as the Baja California peninsula in Mexico and the Caribbean, are mainly affected by residential and commercial development. The latter threat, in conjunction with agriculture, affects cacti along the Pacific coast of Mexico and the central coast of Brazil. Collecting cacti for biological resources (for instance for ornamental collections and wood) is the main threat process affecting species distributed along the Peruvian and Chilean coasts. Unsurprisingly, areas where all three threat processes act together are often regions harbouring the highest concentrations of threatened species, such as central Mexico and eastern Brazil (Fig. 3a). The most important proximate drivers of extinction risk, that is the ultimate factors contributing to or enabling the threat process23 among threatened cacti, are unscrupulous collection of live plants and seeds for the horticultural trade and for private ornamental collections (affecting 47% of threatened cacti), smallholder livestock ranching (31%) and smallholder annual agriculture (24%; Fig. 4b). In eastern and southern Brazil, the two main drivers of land use change are smallholder ranching and smallholder agriculture, affecting 61 and 46 species, respectively (Fig. 3b,e). However, an additional driver of land use change in southern Brazil is agroindustrial plantations of Eucalyptus (Fig. 3c); land conversion for plantations affects at least 27 species, including the Endangered Parodia muricata, but also the leaf litter from these trees shades cacti, preventing them from being pollinated and from flowering, and often kills adult specimens. In eastern Brazil, the situation is exacerbated by a relatively high number of species (15 in Bahia and 19 in Minas Gerais) that are affected by quarrying, the fifth most frequent threat driver for threatened cacti (Fig. 4b). Edaphic specificity is common among these plants24 and a large number of Brazilian species, such as Arthrocereus glaziovii and Coleocephalocereus purpureus, only grow on iron-rich canga or on inselbergs, both of which are sought after by the mining industry. An extreme case is that of Arrojadoa marylaniae, which may become extinct in the near future, for the single white quartz rock on which it is exclusively found is threatened by mining. In north-central Mexico the two main drivers of land use change are the same as in Brazil, with nomadic grazing as an additional driver of land use change in this region (Fig. 3b,d,e). In the northwestern part of Mexico, species such as Mammillaria bocensis and Corynopuntia reflexispina are unexpectedly becoming threatened by aquaculture, as shrimp farming expands into the desert. Cactaceae are a key component of the arid floras of the New World. They are probably more susceptible to collection activities than other groups of plants that are characteristic of these environments. However, until similar assessments are completed for such other groups it is hard to speculate on how the threats will differ, especially for plants with more ephemeral life cycles. Human use Unlike most other groups that have been completely globally assessed to date, more than a half of all cactus species (57%) are used by people. The most common use is for ornamental horticulture (674 species), which in most cases is related to gathering plants and seeds for specialized collections. People also use cacti as food for human consumption (154 species) and medicine (both human and veterinary; 64 species; Fig. 4c). Among the threatened cacti species, NATURE PLANTS | www.nature.com/natureplants NATURE PLANTS ARTICLES DOI: 10.1038/NPLANTS.2015.142 a b 100 81 1 1 Figure 2 | Patterns of biodiversity of Cactaceae. a, Proportion of species that are threatened (Vulnerable, Endangered and Critically Endangered). b, Total species richness. a b c 9 13 1 1 d e Biological resource use Agriculture and aquaculture Residential and commercial development Species absent or values of all three threats are low 4 12 1 1 Figure 3 | Threatening processes and drivers impacting cacti. a, Geographical distribution of the three most common threat processes. Green, agriculture/ aquaculture; red, overexploitation; and blue, residential/commercial development. These colours change as the threats combine, turning white when all three threats are present in an area. The brighter the colour, the higher the number of species affected by that particular threat. Black corresponds to those areas where all three threat values are low. b–e, Geographic distribution of threat drivers: smallholder ranching (b), wood agroindustry plantations (c), nomadic grazing (d) and annual smallholder farming (non-timber crops) (e). NATURE PLANTS | www.nature.com/natureplants 3 ARTICLES NATURE PLANTS DOI: 10.1038/NPLANTS.2015.142 % of threatened species a 40 20 0 Natural Invasive Transportation Human Agriculture Biological Residential Energy species and intrusions and resource and production system service and aquaculture use commercial and modifications corridors disturbance development mining Climate change Pollution % of threatened species b 40 30 20 10 0 Gathering Livestock Smallholder smallholder farming plants Housing Mining and and urban areas quarrying Increase Annuals Tourism Wood in fire agroindustry agroindustry and farming plantations recreation areas Invasive species c % of species 40 30 20 10 0 Horticulture Food for humans Medicine (human and veterinary) Construction materials Food for animals Horticulture Food for humans Medicine (human and veterinary) Food for animals Handicrafts d % of threatened species 50 40 30 20 10 0 Figure 4 | Cactus species affected by different threat processes and drivers, and used for different purposes. a, Percentage of threatened cactus species threatened by different processes. b, Percentage of threatened cactus species experiencing different proximate threat drivers. c, Percentage of cactus species used for different purposes. d, Percentage of threatened cactus species used for different purposes. Only the main threats and uses are shown; for complete lists of threat processes, threat drivers and uses see Supplementary Tables 3–6. 4 NATURE PLANTS | www.nature.com/natureplants NATURE PLANTS ARTICLES DOI: 10.1038/NPLANTS.2015.142 64% are utilized by humans in some form and 57% (236 species) are used in horticulture (Fig. 4d). Ever since Europeans first discovered cacti, they have been regarded as precious collectable objects sought by collectors for their unique appearance, unpredictably beautiful flowers and their rarity in terms of the narrowness of their geographic ranges. Large cacti are sought after as major exhibition pieces, but smaller ones are more readily discreetly collected. A general linear model identified significant differences in height between threat categories, between cacti that are utilized and those which are not, and with mean elevation, although the explanatory power of the final model was low (R 2 = 0.106); whether the species was in a protected area or not was also retained in the model but was not significant (full details Supplementary Information Tables 7 and 8). Height was different between threat categories (F[4,693] = 8.29, P < 0.0001) with Least Concern and Near Threatened species being significantly taller than Critically Endangered ones (difference in mean Least Concern (mean = 2.51 m, s.e. = 0.154 m, n = 475) and Critically Endangered (mean = 1.27 m, s.e. = 0.41 m, n = 41) 1.241 m; Near Threatened (mean = 4.59 m, s.e. = 2.4 m, n = 41) and Critically Endangered difference in mean 3.32 m). Cacti which are utilized were significantly smaller than those which are not (F[2,693] = 17.94, P < 0.0001), and there was a significant inverse relationship between cactus height and mean elevation (F[1,693] = 15.07, P < 0.001). A cumulative link model exploring factors affecting the IUCN threat category of each species also had low explanatory power (pseudo R 2 = 0.104). It did, however, identify significant differences in threat category between species found in protected areas compared with those which were unprotected (likelihood ratio statistic = 19.37, P < 0.001 see Supplementary Table 9 for full model results). The proportion of Least Concern species was much greater in protected areas, and unprotected areas had greater proportions of Vulnerable, Endangered and Critically Endangered species. The model also highlighted height (z = 1.98, P = 0.047) and upper elevation (z = 1.9, P = 0.057) as having marginally significant effects on threat category. Trade in cactus species takes place at both national and international levels, and it is often illegal25. We found that 86% of threatened cacti used in horticulture are extracted from wild populations. Illegal trade has been reduced to a certain extent by the inclusion, since 1975, of the whole family (with a few exemptions) in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) and by the availability of plants grown from seed in international markets. However, the threat of collection prevails, especially in those countries where the implementation of CITES has only recently been enforced, such as in Peru, where the proportion of species in peril from trade is high. Illegal trade is a latent threat for all newly described cactus species. For example, the precise locality of Mammillaria luethyi is known to only a small number of experts to protect the wild population from unsustainable collecting. Knowledge and practicality In contrast to many animal groups assessed to date, levels of Data Deficient (DD) listings among cacti are relatively low. Only 129 species (8.7%) of cacti were assessed as DD (Supplementary Table 1), meaning that there was inadequate information to assess their extinction risk based on distribution and/or population data. This is markedly lower than for vertebrate groups: 15% for mammals, 25% for amphibians and 46% for sharks and rays5,26. Low levels of DD cactus assessments mirror those of other less speciose plant groups that have been fully assessed to date (for example conifers, 1%; cycads, 1%; mangroves, 4%; sea grasses, 12%5,26). This is likely to be a consequence of the relatively greater ease of gathering data on the occurrence of plants than for many mobile cryptic animal species. It suggests that in practice assessing the status of NATURE PLANTS | www.nature.com/natureplants at least some major plant groups is not substantially more challenging in terms of data availability than for animal groups that have attracted considerably more conservation attention. For cacti, the global species assessment process took about 6 h per species and cost US$167 per taxon, including paid staff time, volunteered expert and staff time and workshop costs. Thus in a year, one full-time person looking at all aspects of an assessment (contacting experts, organizing workshops, fundraising) could evaluate around 363 species. Combined with the above results this clearly demonstrates that, with relatively moderate resources, global species assessments can be undertaken for major plant taxa; overall, the assessment for cacti cost less than many standard research grants issued through major funding bodies. Moreover, as evidenced here, such exercises can reveal patterns in the distribution and prevalence of threats that are fundamentally different from those for other groups that have been globally assessed. Indeed, these exercises are integral to planning conservation activities to protect more effectively all threatened biodiversity at a global scale. To assess all described plant species by 2020, based on the resources used for the global cactus assessment, it would take at least 157 people working fulltime on assessments for 5 years at a cost of approximately US$47 million. The goal of evaluating a substantial proportion of plant species and thereby contributing to the achievement of the Global Strategy for Plant Conservation is thus both undoubtedly achievable and vital. Methods Existing data were gathered from the literature for each of 1,478 cactus species on their distribution, population trend, habitat preference and ecology, conservation actions, use and trade (see Materials and Methods for details). This included over 38,000 occurrence point records, which were used to generate preliminary range maps. This information was evaluated at a series of nine formal expert workshops, and then used by the participants to evaluate the extinction risk of each species using the IUCN Red List Categories and Criteria2. Received 24 October 2014; accepted 29 August 2015; published online 5 October 2015 References 1. Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B. & Worm, B. How many species are there on Earth and in the ocean. PLoS Biol. 9, e1001127 (2011). 2. IUCN Red List Categories and Criteria Version 3.1 (IUCN Species Survival Commission, 2001). 3. Polidoro, B. A. et al. The loss of species: mangrove extinction risk and geographic areas of global concern. PLoS ONE e13636 (2010). 4. Short, F. T. et al. Extinction risk assessment of the world’s seagrass species. Biol. Cons. 144, 1961–1971 (2011). 5. The IUCN Red List of Threatened Species Version 2014.1; http://www.iucnredlist. org. 6. Gaston, K. J. The Structure and Dynamics of Geographic Ranges (Oxford Univ. Press, 2003). 7. Pitman, N. C. A. & Jørgensen, P. M. Estimating the size of the world’s threatened flora. Science 298, 989 (2002). 8. Hubbell, S. P. et al. How many tree species are there in the Amazon and how many of them will go extinct? Proc. Natl Acad. Sci. USA 105 (suppl.), 11498–11504 (2008). 9. Joppa, L. N., Visconti, P., Jenkins, C. N. & Pimm, S. L. Achieving the Convention on Biological Diversity’s goals for plant conservation. Science 341, 1100–1103 (2013). 10. Paton, A. & Nic Lughada, E. The irresistible target meets the unachievable objective: what have 8 years of GSPC implementation taught us about target setting and achievable objectives? Bot. J. Linn. Soc. 166, 250–260 (2011). 11. Stuart, S. N. et al. Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 (2004). 12. Schipper, J. et al. The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science 322, 225–230 (2008). 13. Bramwell, D., Raven, P. & Synge, H. Implementing the Global Strategy for Plant Conservation. Plant Talk 30, 32–37 (2002). 14. Burton, J. On the Red Lists and IUCN. Plant Talk 32, 5 (2003). 15. Heywood, V. H. Red listing – too clever by half? Plant Talk 31, 5 (2003). 16. Heywood, V. H. & Iriondo, J. M. Plant conservation: old problems, new perspectives. Biol. Conserv. 113, 321–335 (2003). 5 ARTICLES 17. Callmander, M. W., Schatz, G. & Porter, P. P. IUCN Red List assessment and the Global Strategy for Plant Conservation taxonomist must act now. Taxon 54, 1047–1050 (2005). 18. Schussler, E. E., Link-Perez, M. A., Weber, K. M. & Dollo, V. H. Exploring animal and plant content in elementary science textbooks. J. Biol. Educ. 44, 123–128 (2010). 19. Mares, M. A. Neotropical mammals and the myth of Amazonian biodiversity. Science 255, 976–979 (1992). 20. Durant, S. M. et al. Forgotten biodiversity in desert ecosystems. Science 336, 1379–1380 (2012). 21. Carpenter, K. E. et al. One-Third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560–563 (2008). 22. Taylor, N. P. in Cactus and Succulent Plants - Status survey and Conservation Action Plan (ed. Oldfield, S.) Comp. 18–19 (IUCN, 1997). 23. Salafsky, N. et al. A standard lexicon for biodiversity conservation: unified classifications of threats and actions. Conserv. Biol. 22, 897–911 (2008). 24. Hernández, H. M. & Gómez-Hinostrosa, C. Studies on Mexican Cactaceae IV. A new subspecies of Echinocereus palmeri Britton & Rose, first record of the species in the Chihuahuan Desert. Bradleya 22, 1–8 (2004). 25. Sajeva, M., Augugliaro, C., Smith, M. J. & Oddo, E. Regulating internet trade in CITES species. Conserv. Biol. 27, 429–430 (2013). 26. Hoffmann, M. et al. The impact of conservation on the status of the world’s vertebrates. Science 330, 1503–1509 (2010). Acknowledgements In memory of Betty Fitz-Maurice and Eduardo Méndez. We are grateful to the University of Sheffield and the University of Exeter for housing the Global Cactus Assessment (GCA); for the institutional support of IUCN, in particular staff of the Global Species Programme, the IUCN Species Survival Commission and the IUCN SSC Cactus and Succulent Specialist Group and the office of the Chair of IUCN SSC which made available valuable resources, via the Environment Agency of Abu Dhabi, at a critical juncture in the project; to the donors and hosts who made the eight GCA workshops possible as well as the individuals (in parentheses) who helped with the organization and logistics—Mexico’s Comisión Nacional de Areas Naturales Protegidas, Comisión Nacional para Conocimiento y Uso de la Biodiversidad (S. Cariaga and A. López) and Instituto Nacional de Ecología, Conservation International, the North of England Zoological Society, Jardín Botánico Regional de NATURE PLANTS DOI: 10.1038/NPLANTS.2015.142 Cadereyta (E. Sánchez and M. Magdalena Hernández Martínez), Desert Botanical Garden (C. Butterworth), the Cactus and Succulent Society of America, Jardin Exotique de Monaco (J.-M. Solichon), the Prince Albert II of Monaco Foundation, Conservation InternationalBrazil, Instituto Chico Mendes, Instituto Argentino de Investigaciones de Zonas Áridas (R. Kiesling and M. Superina), The Mohamed bin Zayed Species Conservation Fund, Instituto de Ecología y Biodiversidad project P05-002 ICM, Universidad de Chile (P. Guerrero), Fairchild Tropical Botanic Garden (J. Maschinski), National Fish and Wildlife Foundation, Laboratorio de Cactología at the Insituto de Biología UNAM (H. Hernández and C. Gómez-Hinostrosa) and Keidanren Nature Conservation Fund; and to G. Charles, P. Hoxey, J. A. Hawkins, C. Yesson and Sukkulenten-Sammlung Zürich who provided point locality data. B.G. was partially funded by Consejo Nacional de Ciencia y Tecnología grant 0000000000118202. We are indebted to the hard work put in by volunteers P. Durán, E. Hounslow, R. Lee, C. Malone, C. F. Rose, K. Watt and S. Willhoit; to L. Bacigalupe and J. Bennie for assistance with analyses; and to M.L. Ávila-Jiménez, J. Bennie, M.G. Gaston, S. Gaston and five anonymous reviewers for comments on the manuscript. Author contributions B.G. and K.J.G. jointly created, developed and led the project. C.H.T., A.F., H.M.H., J.S., M.S., N.P.T., M.T., A.M.A, S.A., H.J.A.N., M.A.B., R.T.B., D.B., P.B., C.A.B., A.B., F.C., M.C.B., R.C.D., M.D.V.P., P.H.D., W.A.D.B., R.D., L.F.Y., R.S.F., B.F.M., W.A.F.M., G.G., C.G.H., L.R.G.T., M.P.G., P.C.G., B.H., K.D.H., J.G.H.O., M.H., M.I.I., R.K., J.L., J.L.L.D., C.R.L.S., M.L., M.C.M., L.C.M., J.G.M.A., C.M., J.M., E.M., R.A.M., J.M.N., V.N., L.J.O., P.O.B., A.B.P.F., D.J.P., J.M.P., R.P., J.R.G., P.S.P., E.S.M., M.S., J.M.S.M.C., S.N.S., J.L.T.M., T.T., M.T., M.T., T.V., T.R.V., M.E.V., H.E.W., S.A.W., D.Z., J.A.Z.H. contributed to the species assessment process. G.C.P., J.P.D., R.I. and C.P. conducted the analyses. B.G. and K.J.G. drafted the manuscript and this was commented on by all of the authors. Additional information Supplementary information is available online. Reprints and permissions information is available online at www.nature.com/reprints. Correspondence and requests for materials should be addressed to B.B. and K.J.G. Competing interests The authors declare no competing financial interests. Bárbara Goettsch1*, Craig Hilton-Taylor1, Gabriela Cruz-Piñón2, James P. Duffy3, Anne Frances4, Héctor M. Hernández5, Richard Inger3, Caroline Pollock1, Jan Schipper6,7, Mariella Superina8, Nigel P. Taylor9, Marcelo Tognelli10, Agustín M. Abba11, Salvador Arias12, Hilda J. Arreola-Nava13, Marc A. Baker14, Rolando T. Bárcenas15, Duniel Barrios16, Pierre Braun17, Charles A. Butterworth14, Alberto Búrquez18, Fátima Caceres19, Miguel Chazaro-Basañez20, Rafael Corral-Díaz21, Mario del Valle Perea22, Pablo H. Demaio23, Williams A. Duarte de Barros24, Rafael Durán25, Luis Faúndez Yancas26,27, Richard S. Felger28, Betty Fitz-Maurice29†, Walter A. Fitz-Maurice29, George Gann30, Carlos Gómez-Hinostrosa5, Luis R. Gonzales-Torres31, M. Patrick Griffith32, Pablo C. Guerrero33,34, Barry Hammel35, Kenneth D. Heil36, José Guadalupe Hernández-Oria37, Michael Hoffmann38,39, Mario Ishiki Ishihara40, Roberto Kiesling41, João Larocca42, José Luis León-de la Luz43, Christian R. Loaiza S.44, Martin Lowry45, Marlon C. Machado46, Lucas C. Majure47,48, José Guadalupe Martínez Ávalos49, Carlos Martorell50, Joyce Maschinski51, Eduardo Méndez52†, Russell A. Mittermeier53, Jafet M. Nassar54, Vivian Negrón-Ortiz55,56, Luis J. Oakley57, Pablo Ortega-Baes58, Ana Beatriz Pin Ferreira59, Donald J. Pinkava48, J. Mark Porter60, Raul Puente-Martinez48, José Roque Gamarra61, Patricio Saldivia Pérez27, Emiliano Sánchez Martínez62, Martin Smith63, J. Manuel Sotomayor M. del C.64, Simon N. Stuart38,39,53,65,66, José Luis Tapia Muñoz25, Teresa Terrazas5, Martin Terry67, Marcelo Trevisson68, Teresa Valverde50, Thomas R. Van Devender69, Mario Esteban Véliz-Pérez70, Helmut E. Walter71, Sarah A. Wyatt72, Daniela Zappi73, J. Alejandro Zavala-Hurtado74 and Kevin J. Gaston3* 1 International Union for Conservation of Nature, Global Species Programme, Sheraton House, Castle Park, Cambridge CB3 0AX, UK. 2 Departamento Académico de Biología Marina Carretera al Sur Km 5.5, Universidad Autónoma de Baja California Sur, Col. El Mezquitito, La Paz, BCS C.P. 23080, Mexico. 3 Environment and Sustainability Institute, University of Exeter, Penryn, Cornwall TR10 9FE, UK. 4 NatureServe, 4600 N. Fairfax Dr., 7th Floor, Arlington, Virginia 22203, USA. 5 Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Deleg. Coyoacán, México, D.F. C.P. 04510, Mexico. 6 School of Life Sciences, Arizona State University, Tempe, Arizona 85287, USA. 7 Conservation & Science Department, Phoenix Zoo, 455 N. Galvin Parkway, Phoenix, Arizona 85008, USA. 8 Laboratorio de Endocrinología de la Fauna Silvestre, IMBECU, CCT CONICET Mendoza, Avda. Dr. Adrián Ruiz Leal, S/N°, Parque General San Martín, Mendoza 5500, Argentina. 9 Singapore Botanic Gardens and National Parks Board, 1 Cluny Road, Singapore 259569, Singapore. 10 International Union for Conservation of Nature-Conservation International, Biodiversity Assessment Unit, Betty & Gordon Moore Center for Science & Oceans, Conservation International, 2011 Crystal Drive, Suite 500, Arlington, Virginia 22202, USA. 11 División Zoología Vertebrados, Facultad de Ciencias Naturales y Museo, UNLP, CONICET, Paseo del Bosque s/n, La Plata 1900, Argentina. 12 Jardín Botánico, Instituto de Biología, Universidad Nacional Autónoma de México, México, D.F. C.P. 04510, Mexico. 13 Instituto de Botánica del Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, km. 15.5 carr. a Nogales, Zapopan, Jalisco C.P. 45110, Mexico. 14 College of Liberal Arts and Sciences, School of Life Sciences, Arizona State University, PO Box 874501, Tempe, Arizona 85287-4501, USA. 15 Laboratorio de Genética Molecular y Ecología Evolutiva, Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Campus Aeropuerto, Carretera a Chichimequillas km. 2.5, Querétaro, Querétaro C.P. 76140, Mexico. 16 Jardín Botánico Nacional, Universidad de La Habana, Carretera El Rocío Km 3 1/2 Calabazar, Boyeros, La Habana, Cuba. 17 Im Fusstal 37, Kerpen D 50171, Germany. 18 Unidad Hermosillo, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 1354, Hermosillo, Sonora C.P. 83000, México. 19 Herbarium arequipense HUSA, Departamento de Biología, Facultad 6 NATURE PLANTS | www.nature.com/natureplants NATURE PLANTS DOI: 10.1038/NPLANTS.2015.142 ARTICLES de Ciencias Biológicas, Universidad Nacional de San Agustín, Av. Daniel Alcides Carrión s/n, Arequipa, Peru. 20 Facultad de Biología, Universidad Veracruzana, Zona Universitaria, Xalapa, Veracruz C.P. 91000, Mexico. 21 Pulsar Group, LLC, Environmental Consulting and Services, 565 Bluff Canyon Circle, El Paso, TX 79912, USA. 22 Facultad de Ciencias Exactas y Naturales, UNCA, Avenida General Belgrano 300, San Fernando del Valle de Catamarca, Argentina. 23 Temperate South American Plants, Specialist Group, IUCN, Colanchanga S/N, Río Ceballos, Córdoba 5111, Argentina. 24 Herbario MVM, Museo Nacional de Historia Natural, 25 de Mayo 582, Casilla de Correo 399, Montevideo C.P. 11.000, Uruguay. 25 Centro de Investigación Científica de Yucatán, Calle 43 # 130 Col. Chuburná, Mérida, Yucatán C.P. 97200, México. 26 Facultad de Ciencias Agronómicas, Universidad de Chile, Santiago, Chile. 27 BIOTA, Gestión y Consultorías Ambientales Ltda., Av. Miguel Claro 1224, Providencia, Santiago, Chile. 28 Herbarium, University of Arizona, Tucson, Arizona 85721, USA. 29 Hermanos Infante 225, San Luis Potosí C.P. 78250, SLP, Mexico. 30 The Institute for Regional Conservation, Delray Beach, Florida, USA. 31 Cuban Botanical Society, Hernan Behn No. 171, La Habana C.P. 10900, Cuba. 32 Montgomery Botanical Center, 11901 Old Cutler Road, Miami, Florida, USA. 33 Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160C, Concepción, Chile. 34 Departamento de Ciencias Ecológicas, Instituto de Ecología y Biodiversidad, Universidad de Chile, Casilla 653, Santiago 780-0024, Chile. 35 Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 23166-0299, USA. 36 San Juan College, Farmington, New Mexico 87402, USA. 37 Laboratorio de Ecofisiología Tropical, Instituto de Ecología, Universidad Nacional Autónoma de México, Circuito Exterior, Ciudad Universitaria, México, D.F. C.P. 04510, Mexico. 38 International Union for Conservation of Nature, Gland CH-1196, Switzerland. 39 United Nations Environment Programme, World Conservation Monitoring Centre, Cambridge CB3 0DL, UK. 40 El Colegio de La Frontera Sur (ECOSUR), Carr. Panamericana y Periférico Sur s/n, Barrio de María Auxiliadora, San Cristóbal de Las Casas, Chiapas C.P. 29290, Mexico. 41 IADIZA-CONICET, Casilla de Correo 507, Mendoza 5500, Argentina. 42 Fundação Gaia-Estrada Capão da Fonte, s/n°, Caixa Postal: 353, Cep: 96690-000, Pantano, Grande/RS, Brazil. 43 Herbarium HCIB, Centro de Investigaciones Biológicas del Noroeste, SC, Apdo. postal 128, La Paz, Baja California Sur C.P. 23000, Mexico. 44 Casa de la Cultura Ecuatoriana “Benjamín Carrión”, Núcleo de Loja/Sección de Ciencias Naturales y Ecología, Colón 13 - 12 y Bernardo Valdivieso, Loja, Ecuador. 45 International Organization for Succulent Plant Study, 83, Seaton Road, Hessle, Hull, UK. 46 Herbario HUEFS, Universidade Estadual de Feira de Santana, Feira de Santana, Bahia CEP 44036-900, Brazil. 47 Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA. 48 Desert Botanical Garden, 1201 N Galvin Parkway, Phoenix, AZ 85281, USA. 49 Instituto de Ecología Aplicada, Universidad Autónoma de Tamaulipas, Calle División del Golfo No 356, Col. Libertad, Cd. Victoria, Tamaulipas C.P 87019, México. 50 Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad Universitaria, Deleg. Coyoacán, México, D.F. C.P. 04510, Mexico. 51 Kushlan Tropical Science Institute, Fairchild Tropical Botanic Garden, 10901 Old Cutler Rd., Coral Gables, Miami, Florida 33156, USA. 52 Botánica y Fitosociología- IADIZA-CCT-CONICET-MENDOZA, Avda. Dr. Adrián Ruiz Leal, S/N°, Parque General San Martín, C.P. 5500, Mendoza, Mendoza, Argentina. 53 Conservation International, 2011 Crystal Drive, Arlington, Virginia 22202, USA. 54 Centro de Ecología, Instituto Venezolano de Investigaciones Científicas, Carretera Panamericana km 11, Apdo. 20632, Altos de Pipe, Miranda, Venezuela. 55 US Fish & Wildlife Service, 1601 Balboa, Ave., Panama City, Florida 32405, USA. 56 Department of Biology, Miami University, 501 East High Street, Oxford, Ohio 45056, USA. 57 Facultad de Ciencias Agrarias, UNR, C.C. N° 14, S2125ZAA, Zavalla, Argentina. 58 LABIBO, Facultad de Ciencias Naturales, Universidad Nacional de SaltaCONICET, Av. Bolivia 5150, Salta 4400, Argentina. 59 Asociación Etnobotánica Paraguaya, Dr. Hassler 6378 entre R.I.4 Curupayty y R.I. 2 Ytororó, Asunción, Paraguay. 60 Rancho Santa Ana Botanic Garden, 1500 N. College Ave., Claremont, California 91711, USA. 61 Museo de Historia Natural, Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos, Lima, Peru. 62 Jardín Botánico Regional de Cadereyta “Ing. Manuel González de Cosío”, Consejo de Ciencia y Tecnología del Estado de Querétaro, Camino a la antigua Hacienda de Tovares sin número, Cadereyta de Montes, Querétaro C.P. 76500, Mexico. 63 33 Rossington Road, Sheffield S11 8SA, UK. 64 Volcán Toliman 6100, Guadalajara, Jalisco C.P. 44250, Mexico. 65 Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK. 66 Al Ain Zoo, Abu Dhabi, United Arab Emirates. 67 Sul Ross State University, Alpine, Texas 79832, USA. 68 Instituto Superior “Arturo U. Illia” (ISAUI), Olsacher 99, Villa Carlos Paz, Córdoba, Argentina. 69 Sky Island Alliance, Inc, 300 E. University Blvd., Suite 270, Tucson, Arizona 85705, USA. 70 Herbario BIGU, Escuela de Biología, Facultad CC. QQ. y Farmacia, Universidad de San Carlos de Guatemala, Guatemala. 71 The EXSIS project: cactaceae ex-situ & in-situ conservation, Casilla 175, Buin, Chile. 72 Global Environment Facility, 1818 H St NW P4-400, Washington, DC 20433, USA. 73 HLAA, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK. 74 Departamento de Biología, Universidad Autónoma Metropolitana, Ap. Postal 55-535, México, D.F. 09340, Mexico. † Deceased. *e-mail: barbara.goettsch@iucn.org; k.j.gaston@exeter.ac.uk NATURE PLANTS | www.nature.com/natureplants 7