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A risk assessment framework to improve the efficiency of CITES
Biological Conservation 239 (2019) 108260
Contents lists available at ScienceDirect
Biological Conservation journal homepage: www.elsevier.com/locate/biocon
Policy Analysis
A risk assessment framework to improve the efficiency of CITES a, ,1
Louise Mair * , Francesca A. Ridley a b
a,1
b
, L. Vincent Fleming , Philip J.K. McGowan
T a
School of Natural and Environmental Sciences, Ridley Building 2, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK Joint Nature Conservation Committee, Monkstone House, City Road, Peterborough, PE1 1JY, UK
A R T I C LE I N FO
A B S T R A C T
Keywords: IUCN Red List CITES trade database Species extinction Species conservation Wildlife trade
Over-exploitation is a major threat to species and reported wildlife trade has quadrupled over the last four decades. The Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) therefore remains an important mechanism in tackling species declines. Appropriate listing of species on CITES Appendices avoids both unwarranted trade-controls and unsustainable trade and is, therefore, essential for the effective functioning and integrity of the Convention. The current process for assessing the appropriateness of existing species listings is considered time-consuming and inefficient. Here, we introduce a rapid risk assessment framework that combines assessments of species Red List conservation status with quantity of reported trade to provide insights into the risk posed to species from legal trade. We demonstrate the approach for ∼2500 vertebrate species listed on CITES Appendix II and identify a group of > 1000 species that are not threatened (Red List category Least Concern) and had zero or an average of fewer than ten trade records per year. For these species, international trade is highly unlikely to pose a risk and so they may not merit inclusion on Appendix II on the basis of trade posing a threat to species survival. We suggest that the efficient risk assessment approach we apply here could be used to rapidly assess the appropriateness of species listings and, therefore, has the potential to improve the effectiveness of the Convention.
1. Introduction: the need to improve the efficiency of CITES The deteriorating conservation status of the world’s species has led to the suggestion that we are entering the sixth mass extinction event (Barnosky et al., 2011). Pressures causing species declines are largely human driven and show little sign of reducing (Tittensor et al., 2014). Over-exploitation is a major threat to species (Ducatez and Shine, 2017; Maxwell et al., 2016) and reported wildlife trade has quadrupled over the last four decades (Harfoot et al., 2018), with some high profile threatened species known to suffer from high and increasing volumes of, predominantly, illegal trade (e.g. pangolins, Ingram et al., 2018; and snow leopards, Maheshwari and Niraj, 2018). The Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES), therefore, continues to be an essential tool in tackling species declines caused by over-exploitation. CITES entered into force in 1975 and has now been signed by 183 Parties (182 countries and the European Union). The Convention was one of the earliest multilateral environmental agreements and is the only one with compliance mechanisms; non-compliance by Parties can result in trade sanctions. CITES centres on Appendices that list species
for which international trade for commercial purposes is either prohibited or controlled (hereafter any references to ‘trade’ refer to international trade as defined by the Convention; namely import, (re)export and introduction from the sea), as a means of ensuring that trade does not lead to reductions in populations and, potentially, their extinction (see Table 1 for descriptions of the Convention Appendices). Appropriate listing of species is essential for the effective functioning and integrity of the Convention, as unwarranted trade controls could have negative socio-economic impacts and impose unnecessary administrative burdens, while failure to list species when necessary could result in unsustainable trade (Challender et al., 2015). Moreover, funding is a principal constraint on CITES implementation (Phelps et al., 2010) and so inappropriate listing, and the resulting trade control obligations, is likely to put further strain on limited resources. Although this Convention attracts considerable attention, there has been little strategic research that could inform ways in which it might be more efficient. Here, we introduce a framework based on risk assessment that has the potential to contribute to informing species listing and enhancing the efficiency of the Convention. We suggest that an analysis of species’ documented conservation status against levels of reported trade would
⁎
Corresponding author. E-mail addresses: [email protected] (L. Mair), [email protected] (F.A. Ridley), vin.fl[email protected] (L.V. Fleming), [email protected] (P.J.K. McGowan). 1 Louise Mair and Francesca A. Ridley should be considered joint first author. https://doi.org/10.1016/j.biocon.2019.108260 Received 4 April 2019; Received in revised form 13 August 2019; Accepted 20 September 2019 0006-3207/ © 2019 Elsevier Ltd. All rights reserved.
Biological Conservation 239 (2019) 108260
L. Mair, et al.
Table 1 Definition of CITES Appendices. CITES lists species in three Appendices, which are subject to different levels of trade control. A single species cannot appear on multiple Appendices, however subspecies or populations of a species can be included in different Appendices, resulting in ‘split-listing’ for that species. Appendix
Definition of species listing
I II
Species are threatened with extinction and commercial trade is prohibited. Species are not necessarily threatened but may become so without trade control. Includes “look-alike” species, which are similar in appearance to species that are listed for conservation reasons. International trade of Appendix II species can be authorised provided (re)export permits are obtained and trade is not detrimental to the survival of the species. Species are protected in at least one country, which has requested that other CITES Parties assist in controlling trade in these species.
III
These deficiencies are now being discussed in the run up to CITES’ 18th Conference of the Parties in 2019. In a working document submitted by some of the Parties to the Convention, they state that “consideration should be given to initiating an accelerated process of review of the scope and coverage of the Appendices” (CITES, 2019a). In response, the CITES Secretariat acknowledges that the current process for the Periodic Review of the Appendices “is not producing the results for which it was initially designed”; nor has a separate Decision for a rapid assessment of species in Appendix I been implemented (CITES, 2019a). We thus provide a case study that directly addresses the recommendation from some Parties that “an urgent but comprehensive review of the listing of species” is conducted, by providing a rapid, objective assessment of whether or not species merit listing in Appendix II based purely on the risk of extinction and the levels of legal international trade. Our intent is to demonstrate that a risk assessment approach could provide an effective and efficient alternative to, or an alternative first sift for, the current Periodic Review process. We assume that CITES Appendix II species classified as Least Concern and with a mean annual trade of zero are at the lowest risk and, therefore, are unlikely to merit inclusion on Appendix II. Conversely, we consider species classified as Endangered or Critically Endangered according to the IUCN Red List to be at high risk from even low volumes of trade due to the severity of the impacts that any trade would have and, therefore, these species require the regulated international trade and monitoring that Appendix II supplies. Furthermore, we suggest that using such a risk assessment framework to take a strategic overview of species listings in the Appendices could allow interrogation of changes in Convention efficiency over time and between taxonomic groups, and we discuss these potential applications below.
provide insights into the risk posed to species from legally recorded trade and, therefore, whether species are appropriately listed under the Convention. Ultimately, whether or not species are added to, or removed from, the CITES Appendices is subject to political negotiation when decisions are being taken at the Conference of the Parties (Bauer et al., 2018) and there may be range State resistance to proposed changes for reasons not related to the adopted, scientific criteria, such as public opinion and/or economic reasons (Lindsay et al., 2017; Bauer et al., 2018). However, we suggest that a rapid, objective risk-based assessment could provide a strategic overview of the Convention and an appropriate first-step in improving the efficiency and, ultimately, the effectiveness of the Convention. We first provide an outline of the risk assessment approach, and then demonstrate the utility of the approach with a case study of vertebrate species on CITES Appendix II. 2. A risk assessment approach to improving species listing An objective approach to assessing the scientific basis for species inclusion in CITES Appendices can be carried out within the framework of a risk assessment. Risk is quantified as the magnitude or impact of a potential consequence, multiplied by the probability or likelihood of a particular level of consequence occurring (Fletcher, 2005). Here, we are studying the risk to species as a consequence of international trade. We propose that species Red List status provides a qualitative measure of the impact of such trade. The IUCN Red List applies a range of criteria to categorise species extinction risk; we assume that the greater species extinction risk is, the greater the potential negative impact of trade on the survival of that species. We use the volume of recorded trade for each species as a proxy for likelihood, assuming that larger volumes of recorded trade reflect a greater likelihood of negative impacts of trade on the species.
3.2. Use of open-source global data 3. Case study: vertebrate species on CITES Appendix II As there are > 34,000 species on Appendix II, we began this process by analysing the 2779 vertebrate species classified as either Appendix II or I/II. We downloaded data on taxa listed in CITES Appendix II from the Checklist of CITES Species (http://checklist.cites.org) for the year 2015 and combined these with their conservation status obtained from the IUCN Red List (IUCN, 2017). Only species for which Red List status has been evaluated were included in the risk assessment. Risk could not be assessed for species categorised as Data Deficient and species categorised as Extinct were excluded, giving a sample size of 2411 species. Species trade data were downloaded, using the full shipment by shipment output, from the UNEP-WCMC managed CITES Trade database (https://trade.cites.org/) and the period 2006–2015 was selected. The number of trade records for each species was averaged over the 10-year study period to give the mean number of trade records per year. This gave an indication of the varying volume of trade amongst species, with the assumption that more frequent trade records indicated a larger number of individuals (and/or their parts) being traded. Full details of the methods and data used are provided in Appendix A.
3.1. The pressing need for a rapid assessment of CITES Appendix II Appendix II lists species that are not necessarily now threatened with extinction but that may become so unless trade is closely controlled (see Table 1); trade should only be permitted if it can be shown to be non-detrimental to the survival of the species. Many species were listed on this Appendix when the Convention was drafted in the 1970s and Appendix II now includes > 34,000 species (compared with ∼1000 on Appendix I). Criteria for inclusion on Appendix II have been revised over the years (CITES, 2016a), and the early listing of many of the species on Appendix II has not been tested against the current listing criteria (first adopted in 1994). There is an agreed, but non-binding, Periodic Review process which assesses selected groups of species listed in Appendices I and II to determine whether they are appropriately listed (CITES, 2016b). However, the implementation of the Periodic Review process remains problematic. A limited number of species are selected, from a first sift, for review and subsequently only a proportion of these might actually be reviewed; for example, 71 animal species were selected for review between the 13th and 15th meetings of the Conference of the Parties (from both Appendix I and II), but only 30 species reviews reached completion (CITES, 2017a).
3.3. Results of the risk assessment of CITES Appendix II species We found that 216 species (9.0%) species were classified as Least 2
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proposal, rather than as a single species. We determined the frequency of genus-, family- and order-level listings for Least Concern species with no recorded trade using listing information for Appendix II species downloaded from Species+ (www.speciesplus.net). Of the 216 species that were Least Concern with no recorded trade, 208 (96%) were included in Appendix II as group-, family- or orderlistings. Thus, only eight species were listed under their own species name (Appendix A). Of the 208 species probably listed for look-alike reasons, 53 were genus-listings (spread across 21 genera), 45 were family-listings (across seven families) and 110 were order-listings (across six orders). The implication of these findings is that the removal of a ‘target’ taxon or taxa (i.e. those not listed for look-alike reasons) from Appendix II could potentially result in the concurrent removal of a larger number of related look-alike species. We suggest that the rapid risk assessment approach demonstrated here could provide the baseline data required to assess the appropriateness of some entire higher-taxon listings.
4. Interpreting the results of the risk assessment A risk assessment approach allows the rapid identification of groups of species that are more or less likely to require the protection from trade that listing on CITES Appendices offers. Our case study comparing species extinction risk against recorded trade for 2411 of the 2779 vertebrate species on CITES Appendix II identified a group of species for which international trade is highly unlikely to pose a risk to survival, a second group for which such trade could be a significant risk if not properly managed, and a final group that lies somewhere in between. Appendix II should contain species for which international trade must be controlled so that their use does not threaten the survival of the species and other (typically morphologically similar) species that need to be regulated so that ‘target’ species can be effectively controlled. Yet it contains > 1300 vertebrate species for which the risk from international trade to survival is probably low, unless individual transactions contain a significant proportion of a species’ population. These species would be strong candidates for removal from Appendix II in order to relieve some of the burden placed on trade control agencies and to permit better targeting of resources towards species in real need of regulation. The listing of these non-threatened species with little or no trade contrasts with the inclusion of 233 species that are either Endangered or Critically Endangered and are subject to at least some trade, suggesting that international trade may well pose a risk of extinction to these species, if not carefully regulated. The 849 species that lie between these two extremes might be placed into three groups based on threat status and level of trade (and hence risk): a) there are 143 Endangered and Critically Endangered species that were subject to no reported trade; b) 353 Vulnerable species, of which 101 had no recorded trade; and c) 353 non-threatened species (i.e. Least Concern and Near-threatened) that had an average of more than 10 transactions per year. Closer scrutiny of these species would inform whether they might be considered at risk from international trade. As part of the Periodic Review (CITES, 2016b), an assessment of the volume of trade in Appendix I and II species is produced to enable the Animals Committee to establish a schedule of species for review (CITES, 2017b). This assessment provides, amongst other things, information on Appendix II species with low trade (≤5 trade records over a ten-year period) and includes their Red List status (see Annex in CITES, 2017b). While this approach is similar to that presented here, we emphasise that our expanded analysis offers a far more strategic approach by clustering all species, including those with high trade volumes, within a risk assessment framework and so provides a clear indication of the risk to species from unregulated trade.
Fig. 1. The number of vertebrate species within each category of trade volume (measured as average number of trade records per year) by species IUCN Red List conservation status (total N = 2557; the number of vertebrate species on Appendix II categorised on the IUCN Red List as LC, NT, VU, EN or CR). The size of the grey circles is indicative of the number of species in each group. The dashed box indicates the category at the lowest risk from trade, while the dotted box indicates the categories at the highest risk.
Concern and had no recorded trade during the 10-year study period (Fig. 1). These species are at the lowest risk from trade, and so this assessment suggests that they might not merit listing on Appendix II. The majority of Least Concern species (62%) had an average of > 0-10 trade records per year. This group can also be considered low risk and, therefore, potentially might not merit listing on Appendix II. Of the 216 species classified as Least Concern and with no recorded trade, only two have been considered by the Periodic Review during the period 2004–2016 (CITES, 2017a). These are one amphibian, Euphlyctis hexadactylus, and one mammal, Prionailurus iriomotensis, and in both cases the species were deleted from the process because no volunteers came forward to undertake the in-depth review required (CITES, 2017a), emphasising the resource-limitations faced during the Periodic Review process. 376 species (16%) were classified as Endangered or Critically Endangered (Fig. 1). The vast majority of these species (N = 328; 87%) had a mean annual trade of ten or fewer trade records. We consider Endangered or Critically Endangered species with even low volumes of trade to be at high risk due to the impact that any level of trade could have on these highly threatened species. Low levels of recorded trade for threatened species in these IUCN Red List Categories could be interpreted as successful trade control under the Convention (because, under the Convention, trade should only be permitted if it is ‘non-detrimental’), however, it is worth noting that without counterfactuals, the impact on trade of CITES listing is very difficult to ascertain. 3.4. Look-alike species on CITES Appendix II Species with no recorded trade and that are not of conservation concern may have been placed on Appendix II because they look very similar to one or more species that are threatened by trade (see Table 1). The available records do not state explicitly whether a species has been listed for look-alike reasons, however, such look-alike species are often included as part of a genus-, family- or order-level listing 3
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5. Opportunities from adopting a robust, transparent approach to review species listing
species that are more, or less, likely to be threatened by trade, and provides an objective, transparent and simple process that can inform subsequent decisions by the Parties. We suggest that such an approach could inform and enhance the efficiency of the Periodic Review process, make best use of the scarce and limited resources available, and so has the potential to ultimately improve the effectiveness of the Convention.
Given the considerable pressure on resources (e.g. financial, expertise, time) available to implement all aspects of CITES, there should be a compelling argument why each species merits inclusion on CITES Appendices. Some species may be listed for look-alike reasons, and our analysis indicated that the vast majority of Least Concern species with no recorded trade are likely to be look-alikes. In the case where a species is considered for removal from an Appendix, we suggest that the risk assessment approach here could provide the information required to determine whether the entire suite of associated look-alike species could simultaneously be removed (see 3.4 Look-alike species on CITES Appendix II above). Where the listing of look-alikes is necessary to control trade in the target species, carrying out non-detriment findings (which are required to obtain species export permits) for look-alike species could be considered an unnecessary use of resources, although it may be that authorities are able to adjust effort accordingly and carry out less stringent assessments. Look-alikes may not be the only reason for the inclusion on Appendices of species at low risk from international trade, as the listing process is subject to bargaining and decisions are not necessarily based solely on scientific rationale (Gehring and Ruffing, 2008; Lindsay et al., 2017; Bauer et al., 2018). However, it is helpful for the scientific reasoning behind species listings to be transparent in order to inform the political debate. Furthermore, relatively few species have been selected for Periodic Review to assess the appropriateness of their listing and fewer still are actually reviewed. A rapid risk assessment approach could objectively inform the Periodic Review process and so increase efficiency. The risk assessment approach demonstrated here also presents opportunities to address other questions concerning species listing. For example, a comparison could be made between taxa; differences in the proportion of species that are Least Concern with no recorded trade may suggest biases between taxa in risk-averse listing decisions. Comparisons could also be made over time; for example, a reduction in the proportion of Least Concern species with no recorded trade listed following the adoption of revised listing criteria in 1995 (CITES, 2016a) would suggest that the listing process has become more efficient. The approach could contribute to the rapid assessment of the conservation status of, and trade in, Appendix I species called for in draft Decisions to the 19th Conference of the Parties (CITES, 2019b), previous Decisions on which have not progressed (CITES, 2019a).
Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. All sources of funding are disclosed in the acknowledgements. Acknowledgement We thank Carolina Caceres for helpful comments on the manuscript. FAR was supported by a Newcastle University Research Scholarship. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.biocon.2019.108260. References Barnosky, A.D., et al., 2011. Has the Earth/’s sixth mass extinction already arrived? Nature 471, 51–57. Bauer, H., Nowell, K., Sillero-Zubiri, C., Macdonald, D.W., 2018. Lions in the modern arena of CITES. Conserv. Lett., e12444. Challender, D.W.S., Harrop, S.R., MacMillan, D.C., 2015. Towards informed and multifaceted wildlife trade interventions. Glob. Ecol. Conserv. 3, 129–148. CITES, 2016a. Criteria for Amendment of Appendix I and II [Resolution Conf. 9.24 (Rev. CoP17)]. Johannesburg, South Africa. . CITES, 2016b. Periodic Review of Species Included in Appendices I and II [Resolution Conf. 14.8 (Rev. CoP17)]. Johannesburg, South Africa. . CITES, 2017a. Overview of Species under Periodic Review [AC29 Doc. 33.1]. CITES, Geneva, Switzerland. CITES, 2017b. Selection of Species for the Periodic Review [AC29 Doc. 33.2]. CITES, Geneva, Switzerland. CITES, 2019a. Strategic matters: Review of the Convention. Working document for CITES CoP18 (CoP18 Doc.11), Colombo, Sri Lanka. CITES, 2019b. Species Specific Matters: Appendix I-Listed Species [CoP18 Doc.92]. CITES, Colombo, Sri Lanka. Ducatez, S., Shine, R., 2017. Drivers of extinction risk in terrestrial vertebrates. Conserv. Lett. 10, 186–194. Fletcher, W.J., 2005. The application of qualitative risk assessment methodology to prioritize issues for fisheries management. Ices J. Mar. Sci. 62, 1576–1587. Gehring, T., Ruffing, E., 2008. When arguments prevail over power: the CITES procedure for the listing of endangered species. Glob. Environ. Polit. 8 123-+. Harfoot, M., Glaser, S.A.M., Tittensor, D.P., Britten, G.L., McLardy, C., Malsch, K., Burgess, N.D., 2018. Unveiling the patterns and trends in 40 years of global trade in CITES-listed wildlife. Biol. Conserv. 223, 47–57. Harris, J.B.C., et al., 2017. Measuring the impact of the pet trade on Indonesian birds. Conserv. Biol. 31, 394–405. Ingram, D.J., et al., 2018. Assessing africa-wide pangolin exploitation by scaling local data. Conserv. Lett. 11, e12389. IUCN, 2017. The IUCN Red List of Threatened Species. Version 2017-3. http://www. iucnredlist.org. Lindsay, K., Chase, M., Landen, K., Nowak, K., 2017. The shared nature of Africa’s elephants. Biol. Conserv. 215, 260–267. Maheshwari, A., Niraj, S.K., 2018. Monitoring illegal trade in snow leopards: 2003–2014. Glob. Ecol. Conserv. 14, e00387. Maxwell, S., Fuller, R.A., Brooks, T.M., Watson, J.E.M., 2016. The ravages of guns, nets and bulldozers. Nature 536, 143–145. Phelps, J., Webb, E.L., Bickford, D., Nijman, V., Sodhi, N.S., 2010. Boosting CITES. Science 330, 1752. Tittensor, D.P., et al., 2014. A mid-term analysis of progress toward international biodiversity targets. Science 346, 241–244.
6. Increasing the impact of CITES Given the extent to which over-exploitation is considered to be a threat to species (Maxwell et al., 2016), and the role of international trade in that (Harris et al., 2017), increasing the impact of CITES could play a significant role in the post-2020 biodiversity framework that is being discussed in the Convention on Biological Diversity and which, in turn, will influence the UN Sustainable Development Goals between 2021 and 2030. Strategic research designed to inform the Convention’s effectiveness and efficiency, as we have undertaken here, could facilitate increased impact of CITES in supporting national and global species conservation targets, such as the Convention on Biological Diversity’s target on reducing extinctions and reversing the declines of the most threatened species. Our risk assessment approach makes use of publicly available data and offers an impartial assessment of the risk to species from recorded trade. The assessment rapidly identifies groups of
4
Contents lists available at ScienceDirect
Biological Conservation journal homepage: www.elsevier.com/locate/biocon
Policy Analysis
A risk assessment framework to improve the efficiency of CITES a, ,1
Louise Mair * , Francesca A. Ridley a b
a,1
b
, L. Vincent Fleming , Philip J.K. McGowan
T a
School of Natural and Environmental Sciences, Ridley Building 2, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK Joint Nature Conservation Committee, Monkstone House, City Road, Peterborough, PE1 1JY, UK
A R T I C LE I N FO
A B S T R A C T
Keywords: IUCN Red List CITES trade database Species extinction Species conservation Wildlife trade
Over-exploitation is a major threat to species and reported wildlife trade has quadrupled over the last four decades. The Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) therefore remains an important mechanism in tackling species declines. Appropriate listing of species on CITES Appendices avoids both unwarranted trade-controls and unsustainable trade and is, therefore, essential for the effective functioning and integrity of the Convention. The current process for assessing the appropriateness of existing species listings is considered time-consuming and inefficient. Here, we introduce a rapid risk assessment framework that combines assessments of species Red List conservation status with quantity of reported trade to provide insights into the risk posed to species from legal trade. We demonstrate the approach for ∼2500 vertebrate species listed on CITES Appendix II and identify a group of > 1000 species that are not threatened (Red List category Least Concern) and had zero or an average of fewer than ten trade records per year. For these species, international trade is highly unlikely to pose a risk and so they may not merit inclusion on Appendix II on the basis of trade posing a threat to species survival. We suggest that the efficient risk assessment approach we apply here could be used to rapidly assess the appropriateness of species listings and, therefore, has the potential to improve the effectiveness of the Convention.
1. Introduction: the need to improve the efficiency of CITES The deteriorating conservation status of the world’s species has led to the suggestion that we are entering the sixth mass extinction event (Barnosky et al., 2011). Pressures causing species declines are largely human driven and show little sign of reducing (Tittensor et al., 2014). Over-exploitation is a major threat to species (Ducatez and Shine, 2017; Maxwell et al., 2016) and reported wildlife trade has quadrupled over the last four decades (Harfoot et al., 2018), with some high profile threatened species known to suffer from high and increasing volumes of, predominantly, illegal trade (e.g. pangolins, Ingram et al., 2018; and snow leopards, Maheshwari and Niraj, 2018). The Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES), therefore, continues to be an essential tool in tackling species declines caused by over-exploitation. CITES entered into force in 1975 and has now been signed by 183 Parties (182 countries and the European Union). The Convention was one of the earliest multilateral environmental agreements and is the only one with compliance mechanisms; non-compliance by Parties can result in trade sanctions. CITES centres on Appendices that list species
for which international trade for commercial purposes is either prohibited or controlled (hereafter any references to ‘trade’ refer to international trade as defined by the Convention; namely import, (re)export and introduction from the sea), as a means of ensuring that trade does not lead to reductions in populations and, potentially, their extinction (see Table 1 for descriptions of the Convention Appendices). Appropriate listing of species is essential for the effective functioning and integrity of the Convention, as unwarranted trade controls could have negative socio-economic impacts and impose unnecessary administrative burdens, while failure to list species when necessary could result in unsustainable trade (Challender et al., 2015). Moreover, funding is a principal constraint on CITES implementation (Phelps et al., 2010) and so inappropriate listing, and the resulting trade control obligations, is likely to put further strain on limited resources. Although this Convention attracts considerable attention, there has been little strategic research that could inform ways in which it might be more efficient. Here, we introduce a framework based on risk assessment that has the potential to contribute to informing species listing and enhancing the efficiency of the Convention. We suggest that an analysis of species’ documented conservation status against levels of reported trade would
⁎
Corresponding author. E-mail addresses: [email protected] (L. Mair), [email protected] (F.A. Ridley), vin.fl[email protected] (L.V. Fleming), [email protected] (P.J.K. McGowan). 1 Louise Mair and Francesca A. Ridley should be considered joint first author. https://doi.org/10.1016/j.biocon.2019.108260 Received 4 April 2019; Received in revised form 13 August 2019; Accepted 20 September 2019 0006-3207/ © 2019 Elsevier Ltd. All rights reserved.
Biological Conservation 239 (2019) 108260
L. Mair, et al.
Table 1 Definition of CITES Appendices. CITES lists species in three Appendices, which are subject to different levels of trade control. A single species cannot appear on multiple Appendices, however subspecies or populations of a species can be included in different Appendices, resulting in ‘split-listing’ for that species. Appendix
Definition of species listing
I II
Species are threatened with extinction and commercial trade is prohibited. Species are not necessarily threatened but may become so without trade control. Includes “look-alike” species, which are similar in appearance to species that are listed for conservation reasons. International trade of Appendix II species can be authorised provided (re)export permits are obtained and trade is not detrimental to the survival of the species. Species are protected in at least one country, which has requested that other CITES Parties assist in controlling trade in these species.
III
These deficiencies are now being discussed in the run up to CITES’ 18th Conference of the Parties in 2019. In a working document submitted by some of the Parties to the Convention, they state that “consideration should be given to initiating an accelerated process of review of the scope and coverage of the Appendices” (CITES, 2019a). In response, the CITES Secretariat acknowledges that the current process for the Periodic Review of the Appendices “is not producing the results for which it was initially designed”; nor has a separate Decision for a rapid assessment of species in Appendix I been implemented (CITES, 2019a). We thus provide a case study that directly addresses the recommendation from some Parties that “an urgent but comprehensive review of the listing of species” is conducted, by providing a rapid, objective assessment of whether or not species merit listing in Appendix II based purely on the risk of extinction and the levels of legal international trade. Our intent is to demonstrate that a risk assessment approach could provide an effective and efficient alternative to, or an alternative first sift for, the current Periodic Review process. We assume that CITES Appendix II species classified as Least Concern and with a mean annual trade of zero are at the lowest risk and, therefore, are unlikely to merit inclusion on Appendix II. Conversely, we consider species classified as Endangered or Critically Endangered according to the IUCN Red List to be at high risk from even low volumes of trade due to the severity of the impacts that any trade would have and, therefore, these species require the regulated international trade and monitoring that Appendix II supplies. Furthermore, we suggest that using such a risk assessment framework to take a strategic overview of species listings in the Appendices could allow interrogation of changes in Convention efficiency over time and between taxonomic groups, and we discuss these potential applications below.
provide insights into the risk posed to species from legally recorded trade and, therefore, whether species are appropriately listed under the Convention. Ultimately, whether or not species are added to, or removed from, the CITES Appendices is subject to political negotiation when decisions are being taken at the Conference of the Parties (Bauer et al., 2018) and there may be range State resistance to proposed changes for reasons not related to the adopted, scientific criteria, such as public opinion and/or economic reasons (Lindsay et al., 2017; Bauer et al., 2018). However, we suggest that a rapid, objective risk-based assessment could provide a strategic overview of the Convention and an appropriate first-step in improving the efficiency and, ultimately, the effectiveness of the Convention. We first provide an outline of the risk assessment approach, and then demonstrate the utility of the approach with a case study of vertebrate species on CITES Appendix II. 2. A risk assessment approach to improving species listing An objective approach to assessing the scientific basis for species inclusion in CITES Appendices can be carried out within the framework of a risk assessment. Risk is quantified as the magnitude or impact of a potential consequence, multiplied by the probability or likelihood of a particular level of consequence occurring (Fletcher, 2005). Here, we are studying the risk to species as a consequence of international trade. We propose that species Red List status provides a qualitative measure of the impact of such trade. The IUCN Red List applies a range of criteria to categorise species extinction risk; we assume that the greater species extinction risk is, the greater the potential negative impact of trade on the survival of that species. We use the volume of recorded trade for each species as a proxy for likelihood, assuming that larger volumes of recorded trade reflect a greater likelihood of negative impacts of trade on the species.
3.2. Use of open-source global data 3. Case study: vertebrate species on CITES Appendix II As there are > 34,000 species on Appendix II, we began this process by analysing the 2779 vertebrate species classified as either Appendix II or I/II. We downloaded data on taxa listed in CITES Appendix II from the Checklist of CITES Species (http://checklist.cites.org) for the year 2015 and combined these with their conservation status obtained from the IUCN Red List (IUCN, 2017). Only species for which Red List status has been evaluated were included in the risk assessment. Risk could not be assessed for species categorised as Data Deficient and species categorised as Extinct were excluded, giving a sample size of 2411 species. Species trade data were downloaded, using the full shipment by shipment output, from the UNEP-WCMC managed CITES Trade database (https://trade.cites.org/) and the period 2006–2015 was selected. The number of trade records for each species was averaged over the 10-year study period to give the mean number of trade records per year. This gave an indication of the varying volume of trade amongst species, with the assumption that more frequent trade records indicated a larger number of individuals (and/or their parts) being traded. Full details of the methods and data used are provided in Appendix A.
3.1. The pressing need for a rapid assessment of CITES Appendix II Appendix II lists species that are not necessarily now threatened with extinction but that may become so unless trade is closely controlled (see Table 1); trade should only be permitted if it can be shown to be non-detrimental to the survival of the species. Many species were listed on this Appendix when the Convention was drafted in the 1970s and Appendix II now includes > 34,000 species (compared with ∼1000 on Appendix I). Criteria for inclusion on Appendix II have been revised over the years (CITES, 2016a), and the early listing of many of the species on Appendix II has not been tested against the current listing criteria (first adopted in 1994). There is an agreed, but non-binding, Periodic Review process which assesses selected groups of species listed in Appendices I and II to determine whether they are appropriately listed (CITES, 2016b). However, the implementation of the Periodic Review process remains problematic. A limited number of species are selected, from a first sift, for review and subsequently only a proportion of these might actually be reviewed; for example, 71 animal species were selected for review between the 13th and 15th meetings of the Conference of the Parties (from both Appendix I and II), but only 30 species reviews reached completion (CITES, 2017a).
3.3. Results of the risk assessment of CITES Appendix II species We found that 216 species (9.0%) species were classified as Least 2
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proposal, rather than as a single species. We determined the frequency of genus-, family- and order-level listings for Least Concern species with no recorded trade using listing information for Appendix II species downloaded from Species+ (www.speciesplus.net). Of the 216 species that were Least Concern with no recorded trade, 208 (96%) were included in Appendix II as group-, family- or orderlistings. Thus, only eight species were listed under their own species name (Appendix A). Of the 208 species probably listed for look-alike reasons, 53 were genus-listings (spread across 21 genera), 45 were family-listings (across seven families) and 110 were order-listings (across six orders). The implication of these findings is that the removal of a ‘target’ taxon or taxa (i.e. those not listed for look-alike reasons) from Appendix II could potentially result in the concurrent removal of a larger number of related look-alike species. We suggest that the rapid risk assessment approach demonstrated here could provide the baseline data required to assess the appropriateness of some entire higher-taxon listings.
4. Interpreting the results of the risk assessment A risk assessment approach allows the rapid identification of groups of species that are more or less likely to require the protection from trade that listing on CITES Appendices offers. Our case study comparing species extinction risk against recorded trade for 2411 of the 2779 vertebrate species on CITES Appendix II identified a group of species for which international trade is highly unlikely to pose a risk to survival, a second group for which such trade could be a significant risk if not properly managed, and a final group that lies somewhere in between. Appendix II should contain species for which international trade must be controlled so that their use does not threaten the survival of the species and other (typically morphologically similar) species that need to be regulated so that ‘target’ species can be effectively controlled. Yet it contains > 1300 vertebrate species for which the risk from international trade to survival is probably low, unless individual transactions contain a significant proportion of a species’ population. These species would be strong candidates for removal from Appendix II in order to relieve some of the burden placed on trade control agencies and to permit better targeting of resources towards species in real need of regulation. The listing of these non-threatened species with little or no trade contrasts with the inclusion of 233 species that are either Endangered or Critically Endangered and are subject to at least some trade, suggesting that international trade may well pose a risk of extinction to these species, if not carefully regulated. The 849 species that lie between these two extremes might be placed into three groups based on threat status and level of trade (and hence risk): a) there are 143 Endangered and Critically Endangered species that were subject to no reported trade; b) 353 Vulnerable species, of which 101 had no recorded trade; and c) 353 non-threatened species (i.e. Least Concern and Near-threatened) that had an average of more than 10 transactions per year. Closer scrutiny of these species would inform whether they might be considered at risk from international trade. As part of the Periodic Review (CITES, 2016b), an assessment of the volume of trade in Appendix I and II species is produced to enable the Animals Committee to establish a schedule of species for review (CITES, 2017b). This assessment provides, amongst other things, information on Appendix II species with low trade (≤5 trade records over a ten-year period) and includes their Red List status (see Annex in CITES, 2017b). While this approach is similar to that presented here, we emphasise that our expanded analysis offers a far more strategic approach by clustering all species, including those with high trade volumes, within a risk assessment framework and so provides a clear indication of the risk to species from unregulated trade.
Fig. 1. The number of vertebrate species within each category of trade volume (measured as average number of trade records per year) by species IUCN Red List conservation status (total N = 2557; the number of vertebrate species on Appendix II categorised on the IUCN Red List as LC, NT, VU, EN or CR). The size of the grey circles is indicative of the number of species in each group. The dashed box indicates the category at the lowest risk from trade, while the dotted box indicates the categories at the highest risk.
Concern and had no recorded trade during the 10-year study period (Fig. 1). These species are at the lowest risk from trade, and so this assessment suggests that they might not merit listing on Appendix II. The majority of Least Concern species (62%) had an average of > 0-10 trade records per year. This group can also be considered low risk and, therefore, potentially might not merit listing on Appendix II. Of the 216 species classified as Least Concern and with no recorded trade, only two have been considered by the Periodic Review during the period 2004–2016 (CITES, 2017a). These are one amphibian, Euphlyctis hexadactylus, and one mammal, Prionailurus iriomotensis, and in both cases the species were deleted from the process because no volunteers came forward to undertake the in-depth review required (CITES, 2017a), emphasising the resource-limitations faced during the Periodic Review process. 376 species (16%) were classified as Endangered or Critically Endangered (Fig. 1). The vast majority of these species (N = 328; 87%) had a mean annual trade of ten or fewer trade records. We consider Endangered or Critically Endangered species with even low volumes of trade to be at high risk due to the impact that any level of trade could have on these highly threatened species. Low levels of recorded trade for threatened species in these IUCN Red List Categories could be interpreted as successful trade control under the Convention (because, under the Convention, trade should only be permitted if it is ‘non-detrimental’), however, it is worth noting that without counterfactuals, the impact on trade of CITES listing is very difficult to ascertain. 3.4. Look-alike species on CITES Appendix II Species with no recorded trade and that are not of conservation concern may have been placed on Appendix II because they look very similar to one or more species that are threatened by trade (see Table 1). The available records do not state explicitly whether a species has been listed for look-alike reasons, however, such look-alike species are often included as part of a genus-, family- or order-level listing 3
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5. Opportunities from adopting a robust, transparent approach to review species listing
species that are more, or less, likely to be threatened by trade, and provides an objective, transparent and simple process that can inform subsequent decisions by the Parties. We suggest that such an approach could inform and enhance the efficiency of the Periodic Review process, make best use of the scarce and limited resources available, and so has the potential to ultimately improve the effectiveness of the Convention.
Given the considerable pressure on resources (e.g. financial, expertise, time) available to implement all aspects of CITES, there should be a compelling argument why each species merits inclusion on CITES Appendices. Some species may be listed for look-alike reasons, and our analysis indicated that the vast majority of Least Concern species with no recorded trade are likely to be look-alikes. In the case where a species is considered for removal from an Appendix, we suggest that the risk assessment approach here could provide the information required to determine whether the entire suite of associated look-alike species could simultaneously be removed (see 3.4 Look-alike species on CITES Appendix II above). Where the listing of look-alikes is necessary to control trade in the target species, carrying out non-detriment findings (which are required to obtain species export permits) for look-alike species could be considered an unnecessary use of resources, although it may be that authorities are able to adjust effort accordingly and carry out less stringent assessments. Look-alikes may not be the only reason for the inclusion on Appendices of species at low risk from international trade, as the listing process is subject to bargaining and decisions are not necessarily based solely on scientific rationale (Gehring and Ruffing, 2008; Lindsay et al., 2017; Bauer et al., 2018). However, it is helpful for the scientific reasoning behind species listings to be transparent in order to inform the political debate. Furthermore, relatively few species have been selected for Periodic Review to assess the appropriateness of their listing and fewer still are actually reviewed. A rapid risk assessment approach could objectively inform the Periodic Review process and so increase efficiency. The risk assessment approach demonstrated here also presents opportunities to address other questions concerning species listing. For example, a comparison could be made between taxa; differences in the proportion of species that are Least Concern with no recorded trade may suggest biases between taxa in risk-averse listing decisions. Comparisons could also be made over time; for example, a reduction in the proportion of Least Concern species with no recorded trade listed following the adoption of revised listing criteria in 1995 (CITES, 2016a) would suggest that the listing process has become more efficient. The approach could contribute to the rapid assessment of the conservation status of, and trade in, Appendix I species called for in draft Decisions to the 19th Conference of the Parties (CITES, 2019b), previous Decisions on which have not progressed (CITES, 2019a).
Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. All sources of funding are disclosed in the acknowledgements. Acknowledgement We thank Carolina Caceres for helpful comments on the manuscript. FAR was supported by a Newcastle University Research Scholarship. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.biocon.2019.108260. References Barnosky, A.D., et al., 2011. Has the Earth/’s sixth mass extinction already arrived? Nature 471, 51–57. Bauer, H., Nowell, K., Sillero-Zubiri, C., Macdonald, D.W., 2018. Lions in the modern arena of CITES. Conserv. Lett., e12444. Challender, D.W.S., Harrop, S.R., MacMillan, D.C., 2015. Towards informed and multifaceted wildlife trade interventions. Glob. Ecol. Conserv. 3, 129–148. CITES, 2016a. Criteria for Amendment of Appendix I and II [Resolution Conf. 9.24 (Rev. CoP17)]. Johannesburg, South Africa. . CITES, 2016b. Periodic Review of Species Included in Appendices I and II [Resolution Conf. 14.8 (Rev. CoP17)]. Johannesburg, South Africa. . CITES, 2017a. Overview of Species under Periodic Review [AC29 Doc. 33.1]. CITES, Geneva, Switzerland. CITES, 2017b. Selection of Species for the Periodic Review [AC29 Doc. 33.2]. CITES, Geneva, Switzerland. CITES, 2019a. Strategic matters: Review of the Convention. Working document for CITES CoP18 (CoP18 Doc.11), Colombo, Sri Lanka. CITES, 2019b. Species Specific Matters: Appendix I-Listed Species [CoP18 Doc.92]. CITES, Colombo, Sri Lanka. Ducatez, S., Shine, R., 2017. Drivers of extinction risk in terrestrial vertebrates. Conserv. Lett. 10, 186–194. Fletcher, W.J., 2005. The application of qualitative risk assessment methodology to prioritize issues for fisheries management. Ices J. Mar. Sci. 62, 1576–1587. Gehring, T., Ruffing, E., 2008. When arguments prevail over power: the CITES procedure for the listing of endangered species. Glob. Environ. Polit. 8 123-+. Harfoot, M., Glaser, S.A.M., Tittensor, D.P., Britten, G.L., McLardy, C., Malsch, K., Burgess, N.D., 2018. Unveiling the patterns and trends in 40 years of global trade in CITES-listed wildlife. Biol. Conserv. 223, 47–57. Harris, J.B.C., et al., 2017. Measuring the impact of the pet trade on Indonesian birds. Conserv. Biol. 31, 394–405. Ingram, D.J., et al., 2018. Assessing africa-wide pangolin exploitation by scaling local data. Conserv. Lett. 11, e12389. IUCN, 2017. The IUCN Red List of Threatened Species. Version 2017-3. http://www. iucnredlist.org. Lindsay, K., Chase, M., Landen, K., Nowak, K., 2017. The shared nature of Africa’s elephants. Biol. Conserv. 215, 260–267. Maheshwari, A., Niraj, S.K., 2018. Monitoring illegal trade in snow leopards: 2003–2014. Glob. Ecol. Conserv. 14, e00387. Maxwell, S., Fuller, R.A., Brooks, T.M., Watson, J.E.M., 2016. The ravages of guns, nets and bulldozers. Nature 536, 143–145. Phelps, J., Webb, E.L., Bickford, D., Nijman, V., Sodhi, N.S., 2010. Boosting CITES. Science 330, 1752. Tittensor, D.P., et al., 2014. A mid-term analysis of progress toward international biodiversity targets. Science 346, 241–244.
6. Increasing the impact of CITES Given the extent to which over-exploitation is considered to be a threat to species (Maxwell et al., 2016), and the role of international trade in that (Harris et al., 2017), increasing the impact of CITES could play a significant role in the post-2020 biodiversity framework that is being discussed in the Convention on Biological Diversity and which, in turn, will influence the UN Sustainable Development Goals between 2021 and 2030. Strategic research designed to inform the Convention’s effectiveness and efficiency, as we have undertaken here, could facilitate increased impact of CITES in supporting national and global species conservation targets, such as the Convention on Biological Diversity’s target on reducing extinctions and reversing the declines of the most threatened species. Our risk assessment approach makes use of publicly available data and offers an impartial assessment of the risk to species from recorded trade. The assessment rapidly identifies groups of
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