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Mischaracterizing the conservation benefits of trade (commentary)

  • The authors of a Science paper on global wildlife trade respond to an editorial published on Mongabay that criticized their methodology.
  • Brett R. Scheffers of the University of Florida/IFAS; Brunno F. Oliveira of the University of Florida/IFAS and Auburn University at Montgomery; and Leuan Lamb and David P. Edwards of the University of Sheffield say their paper ‘uses a rigorously assembled database to make the first global assessment of traded species—both legal and illegal, and from national to international scales—and to identify the global hotspots of trade diversity.’
  • This post is a commentary. The views expressed are those of the authors, not necessarily Mongabay.

In May of 2015, ten people were arrested and three charged in Yunnan, China.  They had killed a Giant Panda (Ailuropoda melanoleuca) and were selling its meat. The panda’s paws sold for US$750. Elsewhere, pandas are rented by China to zoos outside its borders for up to US$1 million per year, commercializing the conservation of the species, but at worse representing a pawn in international economic planning.

Yet, in a recent opinion piece written by Jonathan Kolby in Mongabay, the author’s opinion claims that we misused our data in characterizing Giant Panda, one of the 32,000 species we assessed, as traded in our study because CITES states their use is strictly for zoological or conservation purposes. Following a minimal level of investigative journalism, we found recent evidence showing Giant Panda as traded on the illegal market. Furthermore, Giant Panda is scored in the IUCN Redlist database as being traded under the categories of hunting, pets, and food, which is one of the sources of data used in our study of the global wildlife trade.

Our study Global wildlife trade across the tree of life uses a rigorously assembled database to make the first global assessment of traded species—both legal and illegal, and from national to international scales—and to identify the global hotspots of trade diversity. We show that approximately one in five species are traded, and hotspots of trade diversity are concentrated in the biologically rich tropics.

Whether an animal is part of the wildlife trade depends on its set of desirable traits, which served as the second focus of our study. Physical traits are determined by evolution, and tend to show up in clusters of related species. With this in mind, we used a novel analysis to show that people are targeting specific groups of species that are similar in traits. Based on these traits and evolutionary relationships, we then determined which non-traded species are at risk of being traded in the future. Our approach is justified—researchers commonly see this trend in the trade of specific groups of animals (e.g., pangolins)—when one traded species is exhausted, trade switches to the next most similar species. Importantly, our study shows this pattern applies more broadly across the tree of life and our method has the potential to reshape the way we prioritize and think about conservation of species by proactively considering trade-risk for all species, regardless of current trade volume.

White-rumped shama (Kittacincla malabarica) for sale in a bird market in Yogyakarta, Java, Indonesia. Although only of Least Concern according to IUCN Redlist, this species is so heavily exploited for the cage-bird trade that it has declined to near-extinction in some countries within its range. Photo credit: Gabby Salazar
White-rumped shama (Kittacincla malabarica) for sale in a bird market in Yogyakarta, Java, Indonesia. Although only of Least Concern according to IUCN Redlist, this species is so heavily exploited for the cage-bird trade that it has declined to near-extinction in some countries within its range. Photo credit: Gabby Salazar

In his opinion piece, Kolby raised three areas of concern about our study:

First, Kolby 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) and the IUCN’s Red List ‘check-box’ of use and trade (N=181)—information not available via our method of API download (correction pending in Science); (2) the trade in some species has been overlooked by IUCN/CITES (e.g., the parrot Amazonas kwaralli and several Abronia lizard species); and (3) projecting trade for species already under CITES conservation action is pointless.

Kolby ignores a fundamental goal of our study, which is to identify whether humans are non-randomly choosing species in the trade. Instead Kolby focuses on trade legalities (legal vs illegal) and the time frame of trade, neither of which are relevant in this context. Precautionary reanalysis after removing the 413 look-alikes from the 5,579 traded species presented in our original article (correction pending) confirms that trade remains phylogenetically clustered, indicating that humans are targeting specific groups of species (Table 1).

Phylogenetic signal in wildlife trade after removing CITES look-alikes
Table 1. Phylogenetic signal in wildlife trade after removing CITES ‘look-alikes”. The D-statistic is the sum of state changes along the edges of a phylogeny. Observed D values were contrasted against simulated values obtained from two null models: Random and Brownian motion. All groups showed a phylogenetic signal stronger than expected by random, whereas mammals and birds show a signal as strong as expected under a Brownian motion model of evolution indicating high levels of phylogenetic clustering.

Second, Kolby argues 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) or are presently being (e.g., helmeted hornbill Rhinoplax vigil) driven towards extinction by trade. For example, the IUCN Redlist has assessed 86% (N=4680) of the approximately 5,420 mammals species on Earth. Of traded mammal species, 51% (N=595) are threatened according to the Redlist 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. Thus, trade is demonstrably and unequivocally a major driver of extinction risk for many species.

Importantly, Kolby provides no scientific reference in support of his opinion that trade can improve species conservation status. We are unaware of rigorous assessments showing widespread population benefits of trade across the hyper-diversity of species we assessed, nor that trade can mitigate other conservation threats to biodiversity. Indeed, trade in combination with habitat loss, road building, and other disturbances such as disease synergistically accelerates extinction risk. Moreover, some research suggests that wildlife trade provides little incentive for enhanced stewardship of traded species and their habitats. The wider conservation benefits of trade remain unclear and we encourage researchers to test this hypothesis with rigorous data-based assessments.

Finally, Kolby suggests trade volume of a species should be used as a qualifier for the inclusion of species as traded. We disagree, because this would set a dangerous precedent. Often species are flagged for conservation action only after a severe decline is documented.

As mentioned in our study, if cultural preferences change, wildlife trade can rapidly drive a species toward extinction. For instance, the emergence of widespread demand in East Asia for the ivory-like casque of the helmeted hornbill resulted in tens of thousands of birds traded annually since around 2012. This species is now Critically Endangered. Moreover, we also mentioned in our study that trade tracks cultural [e.g., the Harry Potter–inspired trade of owls in Asia] and economic vogue, which again suggests that abundant species may not be safe.  We did not identify hotspots of trade volume across the diversity of traded species, which remains a critical knowledge gap at global scale.

Our study provides an account of the sheer diversity of species in trade and serves as a barometer of the scope of trade. Rather than relying upon unsubstantiated hypotheses and personal opinions, 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.

Hill Myna, Gracula religiosa, for sale in a bird market, Java, Indonesia. photo credit: Gabby Salazar
Hill Myna, Gracula religiosa, for sale in a bird market, Java, Indonesia. photo credit: Gabby Salazar

Cover image: Hill Myna, Gracula religiosa, for sale in a bird market, Java, Indonesia. photo credit: Gabby Salazar

References

  1. BBC News
  2. The Economist
  3. https://news.mongabay.com/
  4. Scheffers, B.R., Oliveira, B.F., Lamb, I. and Edwards, D.P., 2019. Global wildlife trade across the tree of life. Science, 366, 71-76.
  5. Swaisgood, R., Wang, D. & Wei, F. 2016. Ailuropoda melanoleuca (errata version published in 2017). The IUCN Red List of Threatened Species 2016: e.T712A121745669. Downloaded on 05 November 2019.
  6. Collar, N.J. 2004. Species limits in some Indonesian thrushes.Forktail20, 71-87.
  7. BirdLife International 2017. Kittacincla malabarica (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2017: e.T103894856A111179027. http://dx.doi.org/10.2305/IUCN.UK.2017-1.RLTS.T103894856A111179027.en. Downloaded on 05 November 2019.
  8. 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.
  9. Forshaw, J. and Knight, F., 2017. Vanished and vanishing parrots: Profiling extinct and endangered species. CSIRO PUBLISHING.
  10. 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
  11. 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.
  12. 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.
  13. Symes, William S., David P. Edwards, Jukka Miettinen, Frank E. Rheindt, and L. Roman Carrasco. 2018. Combined impacts of deforestation and wildlife trade on tropical biodiversity are severely underestimated.” Nature communications 9, 4052.
  14. 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, p.e115376.
  15. 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, 364-373.
  16. 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, 13.
  17. Beastall, C., Shepherd, C.R., Hadiprakarsa, Y. and Martyr, D., 2016. Trade in the Helmeted Hornbill Rhinoplax vigil: the ‘ivory hornbill’.Bird conservation international,26,137-146.
  18. Collar, N. J. (2015). Helmeted Hornbills Rhinoplax vigil and the ivory trade: the crisis that came out of nowhere.BirdingASIA,24, 12-17.
  19. Nijman, V., & Nekaris, K. A. I. (2017). The Harry Potter effect: The rise in trade of owls as pets in Java and Bali, Indonesia.Global ecology and conservation,11, 84-94.
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