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CONSERVATION cess of regulating trade in threatened species lags considerably behind the IUCN identifi- cation of species in need of protection from Long delays in banning trade trade. Such delay in the application of scien- tific knowledge to policy formulation could result in species extinctions. With signatories in threatened species to CITES set to gather in May to determine which species merit protection, we suggest Scientific knowledge should be applied with more urgency opportunities to improve this process.

By Eyal G. Frank1 and David S. Wilcove2 trade is the Convention on International IMPORTANT TOOLS Trade in Endangered Species of Wild Fauna The CITES treaty, which has been ratified by he harvesting of wild animals and and Flora (CITES). Given that CITES aims to 183 party members, was formalized in 1973 plants for international trade affects be as scientifically based as possible (6), we and entered into force in 1975 in order to co- thousands of species, and compounds analyzed how quickly species that are identi- ordinate and regulate international trade in ongoing extinction threats such as fied by the International Union for Conser- wildlife products. The strongest tool CITES habitat loss and climate change (1–4). vation of Nature (IUCN) Red List as being has is to list a species in Appendix I, which The loss of overexploited species can threatened from trade are subsequently pro- restricts trade in that species to “exceptional Tresult in cascading effects that reduce over- tected under CITES. The Red List represents circumstances” only (7). This, in effect, places all ecosystem functioning (4, 5). The primary an authoritative body of scientific knowledge a trade ban on specimens or their body parts international framework for preventing the regarding extinction risks. We find that in that are caught in the wild for commercial

loss of species due to international wildlife nearly two-thirds of the cases, the CITES pro- purposes, although it still allows trade for ARK/ PHOTO GEOGRAPHIC SARTORE/NATIONAL JOEL PHOTO: COLLECTION IMAGE GEOGRAPHIC NATIONAL

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Published by AAAS International wildlife trade can develop quickly, Endangered in 2015 (10). The Tapah Islands dangered and Critically Endangered species threatening species with extinction, such as this race of the white-rumped shama (Copsy- that are traded internationally and have an helmeted hornbill, in just a few years. chus malabaricus opisthochrus) went from intentional use impact factor of 9 are listed being common to nearly extinct in the wild in CITES Appendix I or II; only one Vulner- personal or scientific reasons, such as the after only 5 to 7 years of intensive trapping able species with an intentional use impact shipping of pets and trophies or the moving for the pet trade (10). An estimated one mil- score of 9 remains unlisted. Thus, trade in of live specimens for captive propagation. lion pangolins (Manidae) were trafficked the most highly exploited and threatened CITES can also list species in Appendix from 2000 to 2013 (11). Although all pango- species has indeed been banned or restricted II, which requires monitoring of trade in lin species had been added to Appendix II via CITES. However, for species with impact those species. Trade in species listed in Ap- by 2000, with trade quotas for some species scores of 8 and below, there are many En- pendix II requires an export permit after a set to zero, seven of the eight species were dangered and even Critically Endangered determination that the level of trade is not added to Appendix I only in 2017 in the face species that, to date, have received no pro- detrimental to the survival of the species and of rapidly escalating international trade. tection under CITES. that the specimens were obtained in a legal Beyond examining whether species re- manner (under domestic laws). Signatories IUCN ASSESSMENT AND CITES LISTING ceive protection under CITES, there is the to the treaty meet every 2 to 3 years at a Con- We collected data on how species targeted by issue of how long it takes them to receive ference of Parties (CoP) where they vote on the international wildlife trade were classi- that protection. We focus on three catego- listing decisions. Listing in Appendix I or II fied by the IUCN and treated by CITES (12, ries: (i) species assessed by the IUCN as requires approval by a two-thirds majority of 13) (see supplementary materials for details). threatened at least partly by international party members. We started with species that the IUCN has trade and subsequently protected by CITES, The overall effectiveness of CITES at pro- assessed as Vulnerable, Endangered, or Criti- (ii) species assessed as threatened at least Downloaded from tecting species from international trade cally Endangered and for which the IUCN partly by international trade and not pro- remains an open empirical question. Plac- has listed direct harvesting (intentional use) tected by CITES (as of 2018), and (iii) spe- ing restrictions on trade can potentially in- as a threatening factor. We then drew infor- cies that CITES protected ahead of any Red crease demand if doing so signals that the mation from IUCN assessments, academic ar- List determination that they were threat- species might become extinct in the near fu- ticles, and reports to determine how many of ened at least partly by international trade. ture. Also, if trade shifts from legal to illegal these species were involved in international We also summarize the gap (in years) be- http://science.sciencemag.org/ markets, it becomes harder to monitor and trade (eliminating those for which direct har- tween when each species was assessed by enforce a trade ban. Nonetheless, CITES is vesting appeared to be for domestic use only). the IUCN as threatened and when it was the only global agreement of its kind and, we This resulted in 958 threatened species protected under CITES (see the figure, bot- would argue, an important tool in stemming for which we can link international trade tom). Out of 958 species that the Red List extinctions due to international trade. as a factor in their endangerment. Because classifies as threatened due to intentional Estimating the true degree of threat fac- CITES held its two most recent CoPs in 2013 use and which are traded internationally, ing wildlife populations is challenging. The and 2016, we restricted our data to IUCN sta- 271 (28.18%) lack CITES protection, 334 IUCN is widely considered to be the global tus assessments from 1994 to 2013, to ensure (34.86%) received CITES protection after authority on the extinction risk of different that assessments were based on the IUCN’s they were assessed by the Red List, and 353

species, which it assesses using quantitative more rigorous criteria implemented in 1994 species (36.84%) were protected under CITES on July 23, 2019 criteria and compiles into the Red List. The (14) and to allow CITES a minimum of 3 before they were assessed by the IUCN as be- IUCN compiles data on factors that imperil years to respond to the IUCN assessments. ing threatened by international trade. species, such as population declines, habi- Information spanning from 1975 to 2018 is For this last group of 353 species, it is pos- tat loss, and direct harvesting. These assess- presented in fig. S1 and table S3. sible that the parties to CITES had access ments follow a systematic process that aims Of the 958 threatened, internationally to information indicating threats posed by to make them comparable through time and traded species that warranted CITES pro- trade before such information was available across taxonomic groups (8, 9). Species clas- tection under Appendix I or II, 28.18% were to the IUCN. However, it is also the case that sified as Vulnerable, Endangered, or Criti- not listed in either appendix. This is a strik- many of the species listed by CITES ahead cally Endangered (hereafter “threatened”) ing, heretofore unrecorded gap in protec- of the IUCN were the result of higher taxo- are considered to be at risk of extinction; tion from international trade. There were, nomic groups (for example, entire genera or a species identified as having “intentional however, notable differences in protection families) being added en masse to Appendix use” as a threat is one that is being directly relative to the severity of harvest pressure. I or II. This is sometimes done to ensure that targeted by collectors, hunters, or trappers. The Red List assesses the severity of harvest- threatened species cannot be easily misla- With growth in international commerce ing by assigning species an intentional use beled as similar-looking, nonthreatened spe- and wildlife markets, coupled with unsus- impact score of 0 (lowest rate of harvest cies and therefore slipped into trade. tainable levels of legal and/or illegal trade, but harvest definitely occurring) to 9 (high- Moreover, the process of evaluating species species can become endangered quickly est). For each impact score, we determined for the Red List is subject to constraints on (1, 2). For example, the helmeted hornbill the percentage of Red List threatened spe- staffing, funding, or the gathering of scientific (Rhinoplax vigil) was listed as only Near- cies that actually received protection under information. As a result, certain taxonomic Threatened in the Red List in 2012, but a CITES Appendix I or II (see the figure, top). groups have been evaluated by the Red List sudden increase in demand around 2011 For threatened species for which direct only relatively recently (15). Thus, the large resulted in it being upgraded to Critically harvesting is an extremely severe threat outlier of 127 species added to CITES 18 years (impact score 9) and which can be linked before they were assessed by the IUCN (see 1Harris School of Public Policy and the Energy Policy Institute, with international trade, 75% of species were the figure, bottom) is driven by one group of at the University of Chicago (EPIC), Chicago, IL, USA. listed in Appendix I, 20.83% were listed in species: CITES listed 118 corals (class Antho- 2Woodrow Wilson School of Public and International Affairs and Department of Ecology and Evolutionary Biology, Princeton Appendix II, and 4.17% were not listed in zoa) in 1990, whereas the IUCN did not as- University, Princeton, NJ, USA. Email: [email protected] either appendix. All of the Red List’s En- sess corals until 2008. Mammals were mostly

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Published by AAAS INSIGHTS | POLICY FORUM assessed and added to the Red Overlap and lags between CITES and IUCN listings of such species under Article List after 1996 and in 2008, Percentage of species under escalating degrees of threat from trade (intentional use XII(2)(e). The ultimate goal and amphibians were mostly impact score) that are listed in CITES Appendix I or II, or are not listed. See figs. S3 and should be to create a near- assessed and added in 2004. S4 for additional details. automatic pathway by which We also identified 96 and unprotected species identified 100 747 species listed on CITES Ap- by the IUCN as threatened by pendices I and II, respectively, Not listed Appendix II Appendix I international trade receive a that are also considered threat- prompt vote for inclusion in ened by the IUCN yet are not 75 CITES Appendix I or II. classified by the IUCN as hav- Third, species that are ing intentional use as a threat listed in CITES Appendix I factor. This may reflect an in- 50 or II but are not classified complete cataloging of threats by the IUCN as threatened to these species by the IUCN. (%) age Percent should be reassessed by the On average, when the IUCN 25 IUCN as soon as practicable, preempts CITES, CITES lists in case CITES has identified species in Appendix I or II a growing trade threat ahead 10.3 years after the IUCN as- 0 of the IUCN. Taken together, sesses them as being threat- 0 1 2 3 4 5 6 7 8 9 Average these steps will improve the Severity of threat posed by intentional use [low (0) to high (9)] ened by international trade. degree to which conservation When CITES preempts the The number of species that CITES protected before (brown) or after (gray) an science informs conservation Downloaded from IUCN, species are assessed IUCN assessment as threatened by trade as well as the number of species that IUCN policy and may help to avert as threatened by the IUCN assessed as threatened by trade but which CITES has not yet protected (teal). the extinction of species due 19.8 years, on average, after to escalating international they were protected under 120 CITES listing, followed by IUCN listing trade in wildlife. j CITES. For species that are IUCN listing, followed by CITES listing REFERENCES AND NOTES considered by the Red List 100 http://science.sciencemag.org/ IUCN listing, not listed by CITES 1. E. R. Bush, S. E. Baker, D. W. Macdonald, to be threatened by interna- Conserv. Biol. 28, 663 (2014). CITES preempts IUCN preempts tional trade but have yet to 80 2. M. Lenzen et al., Nature 486, 109 be protected under CITES, we (2012). 3. K. R. Jones et al., Science 360, 788 cannot know how long they 60 (2018). will have to wait to receive 4. H. M. Pereira et al., Science 330, 1496 protection under Appendix (2010). 5. B. J. Cardinale et al., Nature 486, 59

Number of species Number of 40 I or II. For those species, we (2012). calculate their lag time as 6. CITES, “Resolution Conference 16.3 the time since their listing as (Rev. CoP17), CITES Strategic Vision: 20 2008–2020” (CITES, 2016).

threatened on the Red List un-

7. Convention on International Trade in on July 23, 2019 til the end of 2018, which is, on Endangered Species of Wild Fauna and 0 average, 12.4 years. We obtain –35 –30 –25 –20 –15 –10 –5 0 5 10 15 20 25 Flora, 3 March 1973 (United Nations similar results when focusing Treaty Series, vol. 993, 1976), p. 243. Years from IUCN assessment 8. IUCN, IUCN Red List Categories and on internationally traded En- Criteria, Version 3.1 (IUCN, ed. 2, 2012). dangered and Critically Endangered species RECOMMENDATIONS 9. G. M. Mace et al., Conserv. Biol. 22, 1424 (2008). with intentional use impact scores of 6 and To increase the efficacy by which overex- 10. J. A. Eaton et al., Forktail 31, 1 (2015). 11. D. W. S. Challender, C. Waterman, J. E. M. Baillie, “Scaling above (fig. S2). ploited species receive protection, we offer Up Pangolin Conservation: IUCN SSC Pangolin Specialist We consider the situation in which CITES three recommendations. First, indepen- Group Conservation Action Plan” (Zoological Society of protection is delayed relative to the Red List dently from CITES, all countries can use London, 2014). 12. IUCN, The IUCN Red List of Threatened Species, version finding to be a more severe problem than the the Red List as a source of information and 2017-2 (IUCN, 2017); https://www.iucnredlist.org/ reverse situation, when CITES acts ahead of take measures to protect threatened spe- [accessed 27 September 2017]. the Red List. The IUCN Red List is purely in- cies found within their borders, including 13. CITES trade statistics derived from the CITES Trade Database, United Nations Environment Programme formational and provides no legal protection protection from trade. Also, in addition (UNEP) World Conservation Monitoring Centre, to imperiled species, whereas CITES does. to coordinating trade restrictions, CITES Cambridge, UK. Although a species’ Red List status by itself identifies data collection needs and acts 14. A. S. L. Rodrigues, J. D. Pilgrim, J. F. Lamoreux, M. Hoffmann, T. M. Brooks, Trends Ecol. Evol. 21, 71 (2006). does not convey any legal protection, it can as a repository for data; countries can con- 15. C. Rondinini, M. Di Marco, P. Visconti, S. H. M. Butchart, L. play an important role in the allocation of tribute to this process. Boitani, Conserv. Lett. 7, 126 (2014). conservation resources and in drawing atten- Second, hundreds of species that the tion to the species’ plight. IUCN classifies as Critically Endangered, ACKNOWLEDGMENTS The authors thank S. Rochikashvili and M. Beattie for research It is important to note that listing under Endangered, or Vulnerable due to interna- assistance on this paper. E.G.F. completed this work during CITES is not sufficient by itself for conserva- tional trade currently lack CITES protec- his time as a Postdoctoral Research Fellow at the Woodrow tion. CITES coordinates efforts between coun- tion. To begin to clear this backlog, any Wilson School, Princeton University. The authors thank the High tries, facilitates the flow of information, and signatory nation (party) to CITES can pro- Meadows Foundation for its support of this work. SCIENCE aggregates reports about the levels of trade, pose that these species be added to Appen- SUPPLEMENTARY MATERIALS but the party members must implement dix I or II at the next CoP [per Article IV(1) www.sciencemag.org/content/363/6428/686/suppl/DC1 steps through their respective enforcement (a)]. Failing that, the CITES Secretariat can

institutions for there to be real protections. at least alert the signatories to the plight 10.1126/science.aav4013 DESAI/ N. GRAPHIC:

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