Global wildlife trade across the tree of life
A heavy toll
Trade in wildlife, and their parts, is well recognized for a few key species, such as elephants and rhinos, but it occurs globally, across a wide array of species. Scheffers et al. looked across tens of thousands of vertebrate species and found that one in every five species is affected by trade of some sort. The impacts of trade tend to be concentrated in certain phylogenetic groups, thus the potential for long-term impact on certain lineages is substantial. This analysis allows for prediction of potential for trade where it does not yet occur, facilitating proactive prevention.
Science, this issue p. 71
Abstract
Wildlife trade is a multibillion dollar industry that is driving species toward extinction. Of >31,500 terrestrial bird, mammal, amphibian, and squamate reptile species, ~24% (N = 7638) are traded globally. Trade is strongly phylogenetically conserved, and the hotspots of this trade are concentrated in the biologically diverse tropics. Using different assessment approaches, we predict that, owing to their phylogenetic replacement and trait similarity to currently traded species, future trade will affect up to 4064 additional species—totaling 11,702 species at risk of extinction from trade. Our assessment underscores the need for a strategic plan to combat trade with policies that are proactive rather than reactive, which is especially important because species can quickly transition from being safe to being endangered as humans continue to harvest and trade across the tree of life.
Get full access to this article
View all available purchase options and get full access to this article.
Supplementary Material
Summary
Materials and Methods
Figs. S1 to S8
Tables S1 to S10
Resources
File (aav5327_original_tables.zip)
File (aav5327_scheffers_sm.pdf)
File (aav5327_scheffers_sm_rev.pdf)
File (aav5327_tables10.xlsx)
File (aav5327_tables10_rev.xlsx)
File (aav5327_tables3.xlsx)
File (aav5327_tables3_rev.xlsx)
File (aav5327_tables5.xlsx)
File (aav5327_tables5_rev.xlsx)
File (aav5327_tables7.xlsx)
File (aav5327_tables7_rev.xlsx)
References and Notes
1
S. L. Pimm, C. N. Jenkins, R. Abell, T. M. Brooks, J. L. Gittleman, L. N. Joppa, P. H. Raven, C. M. Roberts, J. O. Sexton, The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 1246752 (2014).
2
L. Gibson, T. M. Lee, L. P. Koh, B. W. Brook, T. A. Gardner, J. Barlow, C. A. Peres, C. J. A. Bradshaw, W. F. Laurance, T. E. Lovejoy, N. S. Sodhi, Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478, 378–381 (2011).
3
S. L. Maxwell, R. A. Fuller, T. M. Brooks, J. E. M. Watson, Biodiversity: The ravages of guns, nets and bulldozers. Nature 536, 143–145 (2016).
4
V. Nijman, An overview of international wildlife trade from Southeast Asia. Biodivers. Conserv. 19, 1101–1114 (2010).
5
TRAFFIC, Wildlife Trade Monitoring Network, Illegal Wildlife Trade; www.traffic.org/about-us/illegal-wildlife-trade/.
6
L. S. Wyler, P. A. Sheikh, “International illegal trade in wildlife: Threats and U.S. policy,” CRS Report for Congress (Library of Congress, Congressional Research Service, 2008).
7
E. L. Bennett, Another inconvenient truth: The failure of enforcement systems to save charismatic species. Oryx 45, 476–479 (2011).
8
D. S. Wilcove, X. Giam, D. P. Edwards, B. Fisher, L. P. Koh, Navjot’s nightmare revisited: Logging, agriculture, and biodiversity in Southeast Asia. Trends Ecol. Evol. 28, 531–540 (2013).
9
D. Challender, T. Nguyen Van, C. Shepherd, K. Krishnasamy, A. Wang, B. Lee, E. Panjang, L. Fletcher, S. Heng, J. Seah Han Ming, A. Olsson, A. Nguyen The Truong, Q. Nguyen Van, Y. Chung, “Sunda Pangolin: Manis javanica,” The IUCN Red List of Threatened Species (2014); www.iucnredlist.org/species/12763/45222303.
10
C. Beastall, C. R. Shepherd, Y. Hadiprakarsa, D. Martyr, Trade in the Helmeted Hornbill Rhinoplax vigil: The ‘ivory hornbill’. Bird Conserv. Int. 26, 137–146 (2016).
11
N. J. Collar, Helmeted Hornbills and the ivory trade: The crisis that came out of nowhere. BirdingASIA 24, 12–17 (2015).
12
S. J. O’Hanlon, A. Rieux, R. A. Farrer, G. M. Rosa, B. Waldman, A. Bataille, T. A. Kosch, K. A. Murray, B. Brankovics, M. Fumagalli, M. D. Martin, N. Wales, M. Alvarado-Rybak, K. A. Bates, L. Berger, S. Böll, L. Brookes, F. Clare, E. A. Courtois, A. A. Cunningham, T. M. Doherty-Bone, P. Ghosh, D. J. Gower, W. E. Hintz, J. Höglund, T. S. Jenkinson, C.-F. Lin, A. Laurila, A. Loyau, A. Martel, S. Meurling, C. Miaud, P. Minting, F. Pasmans, D. S. Schmeller, B. R. Schmidt, J. M. G. Shelton, L. F. Skerratt, F. Smith, C. Soto-Azat, M. Spagnoletti, G. Tessa, L. F. Toledo, A. Valenzuela-Sánchez, R. Verster, J. Vörös, R. J. Webb, C. Wierzbicki, E. Wombwell, K. R. Zamudio, D. M. Aanensen, T. Y. James, M. T. P. Gilbert, C. Weldon, J. Bosch, F. Balloux, T. W. J. Garner, M. C. Fisher, Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360, 621–627 (2018).
13
R. Engeman, E. Jacobson, M. L. Avery, W. E. Meshaka Jr., The aggressive invasion of exotic reptiles in Florida with a focus on prominent species: A review. Curr. Zool. 57, 599–612 (2011).
14
BirdLife International, Data zone; http://datazone.birdlife.org/home.
15
CITES, The CITES species; www.cites.org/eng/disc/species.php.
16
S. A. Fritz, A. Purvis, Selectivity in mammalian extinction risk and threat types: A new measure of phylogenetic signal strength in binary traits. Conserv. Biol. 24, 1042–1051 (2010).
17
L. Santini, M. González-Suárez, C. Rondinini, M. Di Marco, Shifting baseline in macroecology? Unravelling the influence of human impact on mammalian body mass. Divers. Distrib. 23, 640–649 (2017).
18
G. Rapacciuolo, J. Marin, G. C. Costa, M. R. Helmus, J. E. Behm, T. M. Brooks, S. B. Hedges, V. C. Radeloff, B. E. Young, C. H. Graham, The signature of human pressure history on the biogeography of body mass in tetrapods. Glob. Ecol. Biogeogr. 26, 1022–1034 (2017).
19
D. W. Redding, C. V. DeWolff, A. Ø. Mooers, Evolutionary distinctiveness, threat status, and ecological oddity in primates. Conserv. Biol. 24, 1052–1058 (2010).
20
R. I. Vane-Wright, C. J. Humphries, P. H. Williams, What to protect?—Systematics and the agony of choice. Biol. Conserv. 55, 235–254 (1991).
21
W. S. Symes, D. P. Edwards, J. Miettinen, F. E. Rheindt, L. R. Carrasco, Combined impacts of deforestation and wildlife trade on tropical biodiversity are severely underestimated. Nat. Commun. 9, 4052 (2018).
22
J. B. C. Harris, M. W. Tingley, F. Hua, D. L. Yong, J. M. Adeney, T. M. Lee, W. Marthy, D. M. Prawiradilaga, C. H. Sekercioglu, N. Suyadi, N. Winarni, D. S. Wilcove, Measuring the impact of the pet trade on Indonesian birds. Conserv. Biol. 31, 394–405 (2017).
23
A. Benítez-López, R. Alkemade, A. M. Schipper, D. J. Ingram, P. A. Verweij, J. A. J. Eikelboom, M. A. J. Huijbregts, The impact of hunting on tropical mammal and bird populations. Science 356, 180–183 (2017).
24
F. Courchamp, E. Angulo, P. Rivalan, R. J. Hall, L. Signoret, L. Bull, Y. Meinard, Rarity value and species extinction: The anthropogenic Allee effect. PLOS Biol. 4, e415 (2006).
25
M. M. Mambeya, F. Baker, B. R. Momboua, A. F. Koumba Pambo, M. Hega, V. J. Okouyi Okouyi, M. Onanga, D. W. S. Challender, D. J. Ingram, H. Wang, K. Abernethy, The emergence of a commercial trade in pangolins from Gabon. Afr. J. Ecol. 56, 601–609 (2018).
26
V. Nijman, K. A.-I. Nekaris, The Harry Potter effect: The rise in trade of owls as pets in Java and Bali, Indonesia. Glob. Ecol. Conserv. 11, 84–94 (2017).
27
E. G. Frank, D. S. Wilcove, Long delays in banning trade in threatened species. Science 363, 686–688 (2019).
28
J. R. Harrison, D. L. Roberts, J. Hernandez-Castro, Assessing the extent and nature of wildlife trade on the dark web. Conserv. Biol. 30, 900–904 (2016).
29
J. Hernandez-Castro, D. L. Roberts, Automatic detection of potentially illegal online sales of elephant ivory via data mining. PeerJ Comput. Sci. 1, e10 (2015).
30
E. Di Minin, C. Fink, T. Hiippala, H. Tenkanen, A framework for investigating illegal wildlife trade on social media with machine learning. Conserv. Biol. 33, 210–213 (2019).
31
N. Hanley, O. Sheremet, M. Bozzola, D. C. MacMillan, The allure of the illegal: Choice modeling of rhino horn demand in Vietnam. Conserv. Lett. 11, e12417 (2018).
32
R. Cooney, D. Roe, H. Dublin, J. Phelps, D. Wilkie, A. Keane, H. Travers, D. Skinner, D. W. S. Challender, J. R. Allan, D. Biggs, From poachers to protectors: Engaging local communities in solutions to illegal wildlife trade. Conserv. Lett. 10, 367–374 (2017).
33
N. G. Patel, C. Rorres, D. O. Joly, J. S. Brownstein, R. Boston, M. Z. Levy, G. Smith, Quantitative methods of identifying the key nodes in the illegal wildlife trade network. Proc. Natl. Acad. Sci. U.S.A. 112, 7948–7953 (2015).
34
W. S. Symes, F. L. McGrath, M. Rao, L. R. Carrasco, The gravity of wildlife trade. Biol. Conserv. 218, 268–276 (2018).
35
C. A. Peres, T. Emilio, J. Schietti, S. J. M. Desmoulière, T. Levi, Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proc. Natl. Acad. Sci. U.S.A. 113, 892–897 (2016).
36
R Core Team, R: A Language and Environment for Statistical Computing Version 3.5.2 (2018).
37
S. Chamberlain, ROpenSci, M. Salmon, rredlist: ‘IUCN’ Red List Client, R package version 0.5.0 (2018); https://CRAN.R-project.org/package=rredlist..
38
M. W. Tingley, J. B. C. Harris, F. Hua, D. S. Wilcove, D. L. Yong, The pet trade’s role in defaunation. Science 356, 916 (2017).
39
U. Roll, A. Feldman, M. Novosolov, A. Allison, A. M. Bauer, R. Bernard, M. Böhm, F. Castro-Herrera, L. Chirio, B. Collen, G. R. Colli, L. Dabool, I. Das, T. M. Doan, L. L. Grismer, M. Hoogmoed, Y. Itescu, F. Kraus, M. LeBreton, A. Lewin, M. Martins, E. Maza, D. Meirte, Z. T. Nagy, C. de C Nogueira, O. S. G. Pauwels, D. Pincheira-Donoso, G. D. Powney, R. Sindaco, O. J. S. Tallowin, O. Torres-Carvajal, J. F. Trape, E. Vidan, P. Uetz, P. Wagner, Y. Wang, C. D. L. Orme, R. Grenyer, S. Meiri, The global distribution of tetrapods reveals a need for targeted reptile conservation. Nat. Ecol. Evol. 1, 1677–1682 (2017).
40
D. M. Olson, E. Dinerstein, E. D. Wikramanayake, N. D. Burgess, G. V. N. Powell, E. C. Underwood, J. A. D’amico, I. Itoua, H. E. Strand, J. C. Morrison, C. J. Loucks, T. F. Allnutt, T. H. Ricketts, Y. Kura, J. F. Lamoreux, W. W. Wettengel, P. Hedao, K. R. Kassem, Terrestrial ecoregions of the world: A new map of life on Earth. Bioscience 51, 933 (2001).
41
B. G. Holt, J.-P. Lessard, M. K. Borregaard, S. A. Fritz, M. B. Araújo, D. Dimitrov, P.-H. Fabre, C. H. Graham, G. R. Graves, K. A. Jønsson, D. Nogués-Bravo, Z. Wang, R. J. Whittaker, J. Fjeldså, C. Rahbek, An update of Wallace’s zoogeographic regions of the world. Science 339, 74–78 (2013).
42
F. Osorio, R. Vallejos, F. Cuevas, D. Mancilla, SpatialPack: Tools for the assessment of the association between two spatial processes, version 0.3-8 (2019); http://spatialpack.mat.utfsm.cl.
43
W. Jetz, G. H. Thomas, J. B. Joy, K. Hartmann, A. O. Mooers, The global diversity of birds in space and time. Nature 491, 444–448 (2012).
44
T. S. Kuhn, A. Ø. Mooers, G. H. Thomas, A simple polytomy resolver for dated phylogenies. Methods Ecol. Evol. 2, 427–436 (2011).
45
O. R. P. Bininda-Emonds, M. Cardillo, K. E. Jones, R. D. E. MacPhee, R. M. D. Beck, R. Grenyer, S. A. Price, R. A. Vos, J. L. Gittleman, A. Purvis, The delayed rise of present-day mammals. Nature 446, 507–512 (2007).
46
S. A. Fritz, O. R. P. Bininda-Emonds, A. Purvis, Geographical variation in predictors of mammalian extinction risk: Big is bad, but only in the tropics. Ecol. Lett. 12, 538–549 (2009).
47
W. Jetz, R. A. Pyron, The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat. Ecol. Evol. 2, 850–858 (2018).
48
J. F. R. Tonini, K. H. Beard, R. B. Ferreira, W. Jetz, R. A. Pyron, Fully-sampled phylogenies of squamates reveal evolutionary patterns in threat status. Biol. Conserv. 204, 23–31 (2016).
49
K. P. Schliep, phangorn: Phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).
50
C. D. L. Orme, R. Freckleton, G. Thomas, T. Petzoldt, S. Fritz, N. Isaac, W. Pearse, caper: Comparative Analyses of Phylogenetics and Evolution in R, version 1.0.1 (2018); https://cran.r-project.org/web/packages/caper/.
51
T. Garland, A. W. Dickerman, C. M. Janis, J. A. Jones, Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42, 265–292 (1993).
52
A. R. Ives, T. Garland Jr., ., Phylogenetic logistic regression for binary dependent variables. Syst. Biol. 59, 9–26 (2010).
53
N. J. B. Isaac, S. T. Turvey, B. Collen, C. Waterman, J. E. M. Baillie, Mammals on the EDGE: Conservation priorities based on threat and phylogeny. PLOS ONE 2, e296 (2007).
54
B. F. Oliveira, V. A. São-Pedro, G. Santos-Barrera, C. Penone, G. C. Costa, AmphiBIO, a global database for amphibian ecological traits. Sci. Data 4, 170123 (2017).
55
A. Slavenko, O. J. S. Tallowin, Y. Itescu, P. Raia, S. Meiri, Late Quaternary reptile extinctions: Size matters, insularity dominates. Glob. Ecol. Biogeogr. 25, 1308–1320 (2016).
56
D. J. Stekhoven, P. Bühlmann, MissForest—Non-parametric missing value imputation for mixed-type data. Bioinformatics 28, 112–118 (2012).
57
J. A. F. Diniz-Filho, L. M. Bini, T. F. Rangel, I. Morales-Castilla, M. Á. Olalla-Tárraga, M. Á. Rodríguez, B. A. Hawkins, On the selection of phylogenetic eigenvectors for ecological analyses. Ecography 35, 239–249 (2012).
58
T. Santos, PVR: Phylogenetic Eigenvectors Regression and Phylogentic Signal-Representation Curve, R package version 0.3 (2018); https://cran.r-project.org/web/packages/PVR/index.html.
59
H. Wilman, J. Belmaker, J. Simpson, C. de la Rosa, M. M. Rivadeneira, W. Jetz, EltonTraits 1.0: Species-level foraging attributes of the world’s birds and mammals. Ecology 95, 2027–2027 (2014).
60
D. W. Redding, A. O. Mooers, Incorporating evolutionary measures into conservation prioritization. Conserv. Biol. 20, 1670–1678 (2006).
61
S. W. Kembel, P. D. Cowan, M. R. Helmus, W. K. Cornwell, H. Morlon, D. D. Ackerly, S. P. Blomberg, C. O. Webb, Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).
62
P. Dutilleul, P. Clifford, S. Richardson, D. Hemon, Modifying the t test for assessing the correlation between two spatial processes. Biometrics 49, 305 (1993).
(0)eLetters
eLetters is an online forum for ongoing peer review. Submission of eLetters are open to all. eLetters are not edited, proofread, or indexed. Please read our Terms of Service before submitting your own eLetter.
Log In to Submit a ResponseNo eLetters have been published for this article yet.
Information & Authors
Information
Published In
Science
Volume 366 | Issue 6461
4 October 2019
4 October 2019
Copyright
Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
This is an article distributed under the terms of the Science Journals Default License.
Submission history
Received: 25 September 2018
Accepted: 4 September 2019
Published in print: 4 October 2019
Acknowledgments
We dedicate this paper to all researchers and park guards who have lost their lives in protecting wildlife from illegal trade. Funding: B.R.S. received financial support from the UF/IFAS Early Career Seed Grant. Author contributions: B.R.S., B.F.O., and D.P.E. conceptualized the idea and methodology, I.L. and B.F.O. collected data, B.F.O. analyzed data, B.R.S. and D.P.E. wrote the original draft, and all authors revised the work. Competing interests: None declared. Data and materials availability: All data related to this work are provided in the supplementary materials.
Authors
Metrics & Citations
Metrics
Article Usage
Altmetrics
Citations
Export citation
Select the format you want to export the citation of this publication.
Cited by
- Admirable Redbelly Toad: The Amphibian That Defied a Hydropower Plant, Imperiled: The Encyclopedia of Conservation, (597-608), (2022).https://doi.org/10.1016/B978-0-12-821139-7.00100-8
- The costs and benefits of primary prevention of zoonotic pandemics, Science Advances, 8, 5, (2022)./doi/10.1126/sciadv.abl4183
- What are TCM doctors’ attitudes towards replacing animal-origin medicinal materials with plant-origin alternatives?, Global Ecology and Conservation, 34, (e02045), (2022).https://doi.org/10.1016/j.gecco.2022.e02045
- Wildlife trade targets colorful birds and threatens the aesthetic value of nature, Current Biology, 32, 19, (4299-4305.e4), (2022).https://doi.org/10.1016/j.cub.2022.07.066
- Genomic analyses show extremely perilous conservation status of African and Asiatic cheetahs ( Acinonyx jubatus ) , Molecular Ecology, 31, 16, (4208-4223), (2022).https://doi.org/10.1111/mec.16577
- Economic incentives for the wildlife trade and costs of epidemics compared across individual, national, and global scales, Conservation Science and Practice, 4, 7, (2022).https://doi.org/10.1111/csp2.12735
- Unraveling the mystery of confiscated “jackal horns” in India using wildlife forensic tools, International Journal of Legal Medicine, 136, 6, (1767-1771), (2022).https://doi.org/10.1007/s00414-022-02773-6
- Recovering trace reptile DNA from the illegal wildlife trade, Forensic Science International: Animals and Environments, 2, (100040), (2022).https://doi.org/10.1016/j.fsiae.2021.100040
- Wildlife Trade, Reference Module in Life Sciences, (2022).https://doi.org/10.1016/B978-0-12-822562-2.00004-9
- Frog in the well: A review of the scientific literature for evidence of amphibian sentience, Applied Animal Behaviour Science, 247, (105559), (2022).https://doi.org/10.1016/j.applanim.2022.105559
- See more
Loading...
View Options
Check Access
Log in to view the full text
AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.
- Become a AAAS Member
- Activate your AAAS ID
- Purchase Access to Other Journals in the Science Family
- Account Help
Log in via OpenAthens.
Log in via Shibboleth.
More options
Register for free to read this article
As a service to the community, this article is available for free. Login or register for free to read this article.
Buy a single issue of Science for just $15 USD.
Mischaracterizing the conservation benefits of trade
Challender et al. [1] raise three areas of concern about our study [2]. Our study uses a rigorously assembled database to make a global assessment of traded species—both legal and illegal, and from national to international scales—and to identify the global hotspots of trade diversity.
First, Challender et al. argue that trade does not necessarily equate to enhanced extinction risk, and that sustainable trade can improve the conservation of traded species and mitigate other threats. This does not contradict our findings of the vast diversity of traded species, nor that many species have recently been (e.g. Peru stubfoot toad Atelopus peruensis; [3]) or are presently being (e.g., helmeted hornbill Rhinoplax vigil; [4]) driven towards extinction by trade. For example, of traded mammal species, 51% (N=595) are threatened whereas 20% (N=641) are least concern; while trade is a bigger driver of population loss than deforestation for 58 of 77 forest bird species in South-east Asia [5]. Thus, trade is demonstrably and unequivocally a major driver of extinction risk for many species.
In arguing that trade can improve species conservation status, Challender et al. cite an article from the secondary literature on crocodiles, a group not in our study. We are unaware of rigorous assessments showing widespread population benefits of trade across the hyper-diversity of species we assessed. The authors also suggest that trade can mitigate other conservation threats to biodiversity, yet do not cite any data-based assessments supporting this assertion (see Footnote 1). Indeed, trade in combination with habitat loss, road building, and other disturbances synergistically accelerates extinction risk (e.g., [5-7]). Moreover, some research suggests that wildlife trade provides little incentive for enhanced stewardship of traded species and their habitats [8]. The wider conservation benefits of trade remain unclear and we encourage researchers to test this hypothesis with rigorous data-based assessments.
Second, Challender et al. argued that we included IUCN-identified species used for subsistence and CITES-listed 'look-alikes' of traded species. Each IUCN species account was read to confirm trade, not subsistence use. Of the 5,579 species identified as traded, only 413 (7%) were included as CITES look-alikes. Their inclusion is justified because: (1) 197 (48%) of these species were identified as traded by a newly usable trade database (N=45; [9]) and the IUCN's Red List 'check-box' of use and trade (N=181)—information not available via our method of API download; (2) the trade in some species has been overlooked by IUCN/CITES (e.g., the parrot Amazonas kwaralli [10] and several Abronia lizard species [11]); and (3) projecting trade for species already under CITES conservation action is pointless. Precautionary reanalysis after removing these 413 look-alikes confirms that trade remains phylogenetically clustered, indicating that humans non-randomly target species (birds: D=0.08, random probability D, p<0.001 and Brownian probability D, not significant (NS); mammals: D=0.02, random probability D, p<0.001 and Brownian probability D, not significant (NS); amphibians: D=0.43, random probability D, p <0.001 and Brownian probability D, p <0.001; reptiles: D=0.17, random probability D, p <0.001 and Brownian probability D, p <0.001).
Finally, Challender et al. argue hotspot maps denote diversity (richness) of trade, as clearly stated both in our methods and main article. We did not identify hotspots of trade volume across the diversity of traded species, which remains a critical knowledge gap at global scale. Rather than relying upon unsubstantiated hypotheses, future progress will be made through using advanced analytical methods combining phylogenetic and large-scale data interrogation to inform deeper understanding of the impacts and sustainable management of trade. Our article represents a key step in this direction.
Footnotes
1. In making this claim, Challender et al. cite a review ('t Sas-Rolfes, M. et al. 2019), which itself only cites two articles from the secondary literature (refs 8 and 9 therein), neither of which provide any data-based evidence or citations in support of their claim.
References
1. Challender, D.W.S. et al 2019. Mischaracterization of wildlife trade threat. Science, eLetter, 30 October 2019.
2. Scheffers, B.R., Oliveira, B.F., Lamb, I. and Edwards, D.P., 2019. Global wildlife trade across the tree of life. Science, 366(6461), pp.71-76.
3. IUCN SSC Amphibian Specialist Group 2018. Atelopus peruensis. The IUCN Red List of Threatened Species 2018: e.T54539A89196220. http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T54539A89196220.en. Downloaded on 22 October 2019.
4. BirdLife International 2018. Rhinoplax vigil. The IUCN Red List of Threatened Species 2018: e.T22682464A134206677. http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22682464A134206677.en. Downloaded on 22 October 2019.
5. Symes, William S., David P. Edwards, Jukka Miettinen, Frank E. Rheindt, and L. Roman Carrasco. Combined impacts of deforestation and wildlife trade on tropical biodiversity are severely underestimated. Nature communications 9, no. 1 (2018): 4052.
6. Clements, G.R., Lynam, A.J., Gaveau, D., Yap, W.L., Lhota, S., Goosem, M., Laurance, S. and Laurance, W.F., 2014. Where and how are roads endangering mammals in Southeast Asia's forests?. PLoS One, 9(12), p.e115376.
7. Suarez, E., Morales, M., Cueva, R., Bucheli, V.U., Zapata‐Ríos, G., Toral, E., Torres, J., Prado, W. and Olalla, J.V., 2009. Oil industry, wild meat trade and roads: indirect effects of oil extraction activities in a protected area in north‐eastern Ecuador. Animal Conservation, 12(4), pp.364-373.
8. Robinson, J.E., Griffiths, R.A., Fraser, I.M., Raharimalala, J., Roberts, D.L. and St John, F.A., 2018. Supplying the wildlife trade as a livelihood strategy in a biodiversity hotspot. Ecology and Society, 23(1), p.13.
9. Eskew, E.A., White, A.M., Ross, N., Smith, K.M., Smith, K.F., Rodríguez, J.P., Zambrana-Torrelio, C., Karesh, W.B. and Daszak, P., 2019. United States wildlife and wildlife product imports from 2000-2014. BioRxiv, p.780197.
10. Forshaw, J. and Knight, F., 2017. Vanished and vanishing parrots: Profiling extinct and endangered species. CSIRO PUBLISHING.
11. CITES CoP17. 2015. Status of conservation, use, management of and trade in the species of the genus Abronia. Report AC28 Doc. 22.4. https://cites.org/sites/default/files/eng/com/ac/28/E-AC28-22-04.pdf
Mischaracterization of wildlife trade threat
Overexploitation threatens many species (1). We welcome Scheffers et al.'s (Science, 4 October 2019) efforts to investigate global wildlife trade trends using novel predictive techniques, but consider their results insufficiently robust to inform strategic responses to the issue. Scheffers et al. assert that 18% of terrestrial vertebrates globally are traded, using data from The IUCN Red List of Threatened Species and the CITES Appendices. Of concern is that they equate being "traded" with being "at risk of extinction from trade" and identify additional species with a high probability of trade and therefore in need of proactive management. It is incorrect to assume that all trade threatens species; sustainable, well-regulated trade can positively affect the conservation status of species (2), mitigate other threats to biodiversity (3), and provide benefits to local people and economies (4). Further, their identification of species "affected" by trade is flawed. Firstly, the authors identify species in the Red List with "hunting and collecting terrestrial animals" (subcategory "intentional use"), coded as a threat, and through text-mining species accounts. However, many such species are harvested for subsistence purposes and traded at negligible levels; the methods imply that the authors did not distinguish between "use" and "trade" (nor legal and illegal trade). Secondly, the authors assume that all species listed by CITES are traded, overlooking the fact that many species are listed for precautionary purposes (i.e., because they resemble traded species), or as part of listed taxonomic groups (e.g., parrots). Thirdly, the "hotspots" identified, described variously as "hotspots of exploitation" and "hotspots of trade", are misleading because they represent the richness of traded species, not the magnitude of trade, and some species are traded from limited parts of their range. We encourage researchers using publicly available databases to consult with those providing the data to ensure their correct interpretation.
References
1. Joppa, L.N. et al. (2016). Filling in biodiversity threat gaps. Science 352 (6284), 416-418.
2. Hutton, J. Hutton, G. Webb. (2003). Crocodiles: legal trade snaps back. In: S. Oldfield (Ed.), The Trade in Wildlife: Regulation for Conservation, Earthscan Publications Ltd., London (2003), pp. 108-120.
3. 't Sas-Rolfes, M. et al. (2019). Illegal Wildlife Trade: Scale, Processes and Governance. Annual Review of Environment and Resources 44: https://doi.org/10.1146/annurev-environ-101718-033253.
4. CITES (2019). CITES and livelihoods. https://cites.org/eng/prog/livelihoods [8 October 2019].