Biological Conservation 204 (2016) 94–102 Contents lists available at ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/bioc Identifying global priorities for the conservation of vipers Bryan Maritz a,⁎, Johannes Penner b,MarcioMartinsc, Jelka Crnobrnja-Isailović d,e, Stephen Spear f, Laura R.V. Alencar c, Jesús Sigala-Rodriguez g, Kevin Messenger h,i, Rulon W. Clark j,PritpalSooraek, Luca Luiselli l, Chris Jenkins f, Harry W. Greene m a Department of Biodiversity and Conservation Biology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa b Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstrasse 43, 10115 Berlin, Germany c Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, 05508-090 São Paulo, SP, Brazil d Department of Biology and Ecology, Faculty of Sciences and Mathematics, University of Niš, 18000 Niš, Serbia e Department of Evolutionary Biology, Institute for Biological Research “S. Stanković”, University of Belgrade, 11000 Belgrade, Serbia f Orianne Society, 100 Phoenix Road, Athens, GA 30605, USA g Colección Zoológica, Universidad Autónoma de Aguascalientes, Aguascalientes, Ags. 20131, México h Department of Biological and Environmental Sciences, Alabama A & M University, 4900 Meridian St N, Huntsville, AL 35811, USA i Department of Zoology, Nanjing Forestry University, 159 Longpan Rd, Nanjing, Jiangsu, China j Department of Biology, San Diego State University, 5500 Campanile Dr, San Diego, CA 92116, USA k Terrestrial Assessment & Monitoring, Environment Agency, PO Box 45553, Abu Dhabi, United Arab Emirates l Centre of Environmental Studies Demetra, Rome, Italy m Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca 14850, USA article info abstract Article history: Vipers are among the most misunderstood and persecuted animals. They occupy most terrestrial ecosystems Received 30 November 2015 around the world, often at high population densities. However, certain aspects of their biology (e.g., low fecundity Received in revised form 3 April 2016 and slow growth) have resulted in vipers being disproportionately threatened by extinction. Despite increased Accepted 9 May 2016 extinction risk, relatively little is known about viper biology, severely limiting the development and implemen- Available online 24 May 2016 tation of conservation initiatives. Here, we review the conservation status of vipers globally, map species richness, and develop three indices (one reactive; one proactive; one combined index emphasising irreplaceable species Keywords: Viperidae facing severe threats) to identify species for which conservation action should be prioritised. Moreover, we Conservation prioritisation map species richness weighted by each index to identify regions for conservation prioritisation. We ranked Threat Index prioritisation scores for all species for which data were available. In doing so we identify species for which valu- Ecological and Evolutionary Distinctiveness able data are missing and that should be prioritised for research. We additionally show that 17 species, currently IUCN Red List listed as Not Assessed or Data Deficient by the IUCN, score sufficiently high on our Threat Index to be considered Viper Action Plan as Threatened in the future. We identify multiple regions for which viper conservation action should be prioritised. These areas broadly correlate with species richness patterns, suggesting that species richness may be an effective proxy for conservation planning. Finally, we discuss the major gaps in knowledge, as well as the major threats facing vipers. © 2016 Elsevier Ltd. All rights reserved. 1. Introduction terrestrial ecosystems, from deserts to moist tropical forests (e.g., Mallow et al., 2003; Campbell and Lamar, 2004; Gumprecht et al., Snakes are among the most misunderstood and persecuted groups 2004). Vipers are characterized by advanced venom delivery mecha- of all animals (Dodd, 1987; Greene and Campbell, 1992; Beaupre and nisms (Young et al., 2001; Cundall, 2002) and highly complex, potent Duvall, 1998). The widely-held negative perceptions of snakes, coupled natural toxins (Norris, 2004), such that they are an important contribu- with relatively poor understanding of even their basic biology, pose fun- tor to the global public health problem of venomous snakebite (e.g., damental challenges to snake conservation (Burghardt et al., 2009). Chippaux, 1998; Gutiérrez et al., 2010). These challenges are particularly apparent in the case of vipers (Family Vipers are characterized by phylogenetically widespread viviparity Viperidae, ~330 species), a clade of advanced snakes that inhabit all and parental care (Fenwick et al., 2011; Greene et al., 2002), ambush continents except Australia and Antarctica, and are found in nearly all foraging (Cundall and Greene, 2000) for prey as diverse as centipedes, insects, fish, amphibians, reptiles, birds, and mammals (Greene, 1997; ⁎ Corresponding author. Martins et al., 2002), and relatively low metabolic rates and energy re- E-mail address: [email protected] (B. Maritz). quirements (Nowak et al., 2008). These traits have contributed to vipers http://dx.doi.org/10.1016/j.biocon.2016.05.004 0006-3207/© 2016 Elsevier Ltd. All rights reserved. B. Maritz et al. / Biological Conservation 204 (2016) 94–102 95 reaching the highest latitudes (over 65° North in Vipera berus and 47° measures of TI and EED for each species to identify ecologically and evo- South in Bothrops ammodytoides) and elevations (up to 4800 m above lutionarily distinct species that are highly threatened. We mapped our sea level in Gloydius himalayanus in Nepal or up to 4570 m a.s.l. in conservation priority indices by summing the index scores of all species Crotalus triseriatus in Mexico) of any snake species. However, several present in a particular grid cell, resulting in prioritisation-index-weight- of these traits associated with “slow” life-histories (e.g., ambush forag- ed species richness maps (Fig. 1B/D/F/G). Finally, we identify hotspots ing resulting in infrequent feeding on large prey; Greene, 1983) may by mapping the highest scoring 10% of cells globally for each index. also make vipers particularly vulnerable to extinction (Greene and Campbell, 1992; Reed and Shine, 2002). Accordingly, Böhm et al. 2.1. Threat Index (TI) (2013) found that vipers were significantly more threatened than ex- pected in an analysis of 1500 randomly selected reptile species. Indeed, We calculated the size of the geographic distribution (GD, area of the although vipers represent only 9% of all snakes (Uetz and Hošek, 2015), geographic distribution polygon) of each species, the degree of human they currently comprise 20% of the 226 snakes listed as threatened on impact (HI; from the HII of the Global Human Influence Index (WCS the IUCN Red List (IUCN, 2015a). Globally, 20 species of vipers are listed and CIESIN, 2005)) within that distribution, and the percentage of as Vulnerable, 23 as Endangered, and eleven as Critically Endangered each distribution formally protected (PA; IUCN protected area category (IUCN, 2015a; M. Martins et al. unpublished data). I–IV from the World Database of Protected Areas (IUCN and UNEP- Conservation prioritisation offers a useful tool to direct limited re- WCMC, 2015), plus Biosphere Reserve protected areas in Mexico and sources toward actions that return the greatest conservation impacts National Parks in South Africa for which IUCN categories are not relative to a priori objectives (Myers, 1988; Myers et al., 2000). These reported in the WDPA). We additionally used expert opinion, facilitated conservation objectives produce prioritisation plans that are proactive through IUCN Viper Specialist Group (URL: http://www.oriannesociety. (emphasising irreplaceability of biodiversity) or reactive (emphasising org/iucn-viper-specialist-group) regional coordinators, to estimate the vulnerability of biodiversity; Brooks et al., 2006).Whilereactiveindices ability of each species to persist in altered habitats (AAH: after Filippi tend to map similar threat processes (human population, habitat trans- and Luiselli, 2000, in categories ranging from 1 (high persistence) to 4 formation and fragmentation etc.), proactive indices vary widely in (low persistence)). metrics used, from endemic species richness (Myers et al., 2000)toevo- We rationalised that species with small, highly transformed and lutionary distinctiveness (May, 1990; Isaac et al., 2007) and functional poorly protected geographic distributions, that were perceived to have diversity (Petchey and Gaston, 2006). Moreover, proactive indices are a limited capacity to persist in altered habitats were likely to be most often produced based on the geographic patterns of relatively well- threatened and used this hypothesis to dictate the rank ordering of spe- known indicator taxa (Böhm et al., 2013), despite variable congruence cies. We normalized each variable to range between 0 and 1, including of such patterns among different taxa (Grenyer et al., 2006). Thus, only species for which data were available. Autocorrelation among var- taxon-specific conservation priorities may be overlooked by some glob- iables was low (max: r = 0.44) so no variables were excluded from the al prioritisation procedures (e.g. compare to Meiri and Chapple, in this calculation of the index. We excluded species for which fewer than issue), stifling access to conservation resources, especially when