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. 2021 Aug 12:10:e70086.
doi: 10.7554/eLife.70086.

Gaps in global wildlife trade monitoring leave amphibians vulnerable

Affiliations

Gaps in global wildlife trade monitoring leave amphibians vulnerable

Alice C Hughes et al. Elife. .

Abstract

As the biodiversity crisis continues, we must redouble efforts to understand and curb pressures pushing species closer to extinction. One major driver is the unsustainable trade of wildlife. Trade in internationally regulated species gains the most research attention, but this only accounts for a minority of traded species and we risk failing to appreciate the scale and impacts of unregulated legal trade. Despite being legal, trade puts pressure on wild species via direct collection, introduced pathogens, and invasive species. Smaller species-rich vertebrates, such as reptiles, fish, and amphibians, may be particularly vulnerable to trading because of gaps in regulations, small distributions, and demand of novel species. Here, we combine data from five sources: online web searches in six languages, Convention on International Trade in Endangered Species (CITES) trade database, Law Enforcement Management Information System (LEMIS) trade inventory, IUCN assessments, and a recent literature review, to characterise the global trade in amphibians, and also map use by purpose including meat, pets, medicinal, and for research. We show that 1215 species are being traded (17% of amphibian species), almost three times previous recorded numbers, 345 are threatened, and 100 Data Deficient or unassessed. Traded species origin hotspots include South America, China, and Central Africa; sources indicate 42% of amphibians are taken from the wild. Newly described species can be rapidly traded (mean time lag of 6.5 years), including threatened and unassessed species. The scale and limited regulation of the amphibian trade, paired with the triptych of connected pressures (collection, pathogens, invasive species), warrants a re-examination of the wildlife trade status quo, application of the precautionary principle in regard to wildlife trade, and a renewed push to achieve global biodiversity goals.

Keywords: CITES; LEMIS; ecology; endangered species; online trade; regulation; wildlife trade.

Plain language summary

In the last few decades, exotic pets have become much more common. In the UK in 2008, reptiles and amphibians were more popular than dogs, with over eight million in captivity. But while almost all pet cats and dogs are born and bred in captivity, exotic pets are often taken from the wild, putting species and their habitats at risk. An international trade agreement called the Convention on International Trade in Endangered Species (CITES) strives to prevent unsustainable animal trade. But to get CITES protection, species depend on data showing that wildlife trade threatens their survival. In addition, their range countries need to first propose them to be listed. For most wild animal species, there are no data on population size or population decline. In the case of amphibians, CITES regulates the trade of just 2.5% of species. This leaves the rest with no protection from overarching international trade regulations. To protect these animals, researchers need to find out which species are in trade, where they are coming from, and how many are already threatened. To address this, Hughes, Marshall and Strine combined data from five sources, including official CITES trade records, recent research and an online search for amphibian sales in six languages. The data showed evidence of trade in at least 1,215 amphibian species, representing 17% of all amphibians. The figure is three times higher than previous estimates. Of the species in trade, more than one in five is vulnerable to extinction, endangered, or critically endangered. For a further 100 of the traded species, data on population were unavailable. Moreover, analysis of the origins of traded individuals showed that around 42% came from the wild. Tropical parts of the world had the highest number of species in trade, but the data showed exchanges happening across the globe. Unsustainable wildlife trade can have devastating consequences for wild animals. It has already driven at least 21 reptile species to extinction, and data of amphibian species are unknown. To prevent further species going extinct, legal wildlife trade should follow the precautionary principle when it comes to wildlife trade. Rather than allowing people to trade a species until CITES regulates it, a blanket ban should come into force for species that have not been assessed or are threatened. Trade would be able to resume for a species only when assessments show that it would not cause major population decline, or secure, captive breeding facilities can be guaranteed.

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Conflict of interest statement

AH, BM, CS No competing interests declared

Figures

Figure 1.
Figure 1.. Breakdown of IUCN Redlist status of traded and not-traded amphibian species.
IUCN assessments based on data from AmphibiaWeb. Inclusion as a traded species based on appearance in online searches (2004–2019 and 2020 online contemporary sample), Law Enforcement Management Information System (LEMIS) (2000–2014), and Convention on International Trade in Endangered Species (CITES) data sources (1975–2019). Generated using Source code 8 and Source data 10.
Figure 2.
Figure 2.. Percentage of species in trade based on three combined contemporary datasets (Law Enforcement Management Information System [LEMIS], Convention on International Trade in Endangered Species [CITES], Online [yellow (0%)-red-black (100%)]).
Also see Figure 2—figure supplements 1, 2, 3, and 4 for patterns of individual countries and inventories.
Figure 2—figure supplement 1.
Figure 2—figure supplement 1.. Map of trade by country derived from Online, Law Enforcement Management Information System (LEMIS), and Convention on International Trade in Endangered Species (CITES) trade data, and mapped using AmphibiaWeb distribution data.
(A) The number of amphibian species present in a country. (B) The number of species present in that country and also present in the trade. (C) The % of species found in a country that are traded.
Figure 2—figure supplement 2.
Figure 2—figure supplement 2.. Species traded from different trade inventories.
Figure 2—figure supplement 3.
Figure 2—figure supplement 3.. Maps of national statistics of species with different IUCN.
Redlist status and Convention on International Trade in Endangered Species (CITES) listing in trade.
Figure 2—figure supplement 4.
Figure 2—figure supplement 4.. Maps of threatened species in trade based on the three trade inventories.
Figure 3.
Figure 3.. Temporal trends in traded species 2000–2019.
(A) Trends over time of Online, LEMIS, and CITES datasets: (1) Raw counts of numbers of species detected in each year. (2) The number of species traded only in a particular year. (B) Exploration of trends in online trade: (1) Residuals from the linear regression of number of species detected against number of pages (df = 13, intercept = 58.73, number of pages coef. = 0.13). (2) Number of species per year. (3) Number of archived pages retrieved and searched. Generated using Source code 9 and Source data 7, 9, and 10. Also see Figure 3—figure supplements 1–6 for a breakdown of how many individuals are coming from the wild for taxa traded at different volumes.
Figure 3—figure supplement 1.
Figure 3—figure supplement 1.. Bar chart showing the number and origin of imported individuals per genera, subset to genera with over 1,000,000 individuals recorded.
Data from Law Enforcement Management Information System (LEMIS) 2000–2014. Red indicates those originating from the wild. Blue indicates those originating from captive operations (animals bred in captivity, commercially bred, and originating from a ranching operation). Labels top and bottom show the percentage of that genera from the wild or captive sources. Summary statistics per genera are provided in the caption.
Figure 3—figure supplement 2.
Figure 3—figure supplement 2.. Bar chart showing the number and origin of imported individuals per genera, subset to genera with between 1,000,000 and 100,000 individuals recorded.
Data from Law Enforcement Management Information System (LEMIS) 2000–2014. Red indicates those originating from the wild. Blue indicates those originating from captive operations (animals bred in captivity, commercially bred, and originating from a ranching operation). Labels top and bottom show the percentage of that genera from the wild or captive sources. Summary statistics per genera are provided in the caption.
Figure 3—figure supplement 3.
Figure 3—figure supplement 3.. Bar chart showing the number and origin of imported individuals per genera, subset to genera with between 100,000 and 10,000 individuals recorded.
Data from Law Enforcement Management Information System (LEMIS) 2000–2014. Red indicates those originating from the wild. Blue indicates those originating from captive operations (animals bred in captivity, commercially bred, and originating from a ranching operation). Summary statistics per genera are provided in the caption.
Figure 3—figure supplement 4.
Figure 3—figure supplement 4.. Bar chart showing the number and origin of imported individuals per genera, subset to genera with between 10,000 and 1000 individuals recorded.
Data from Law Enforcement Management Information System (LEMIS) 2000–2014. Red indicates those originating from the wild. Blue indicates those originating from captive operations (animals bred in captivity, commercially bred, and originating from a ranching operation). Summary statistics per genera are provided in the caption.
Figure 3—figure supplement 5.
Figure 3—figure supplement 5.. Bar chart showing the number and origin of imported individuals per genera, subset to genera with between 1000 and 100 individuals recorded.
Data from Law Enforcement Management Information System (LEMIS) 2000–2014. Red indicates those originating from the wild. Blue indicates those originating from captive operations (animals bred in captivity, commercially bred, and originating from a ranching operation). Summary statistics per genera are provided in the caption.
Figure 3—figure supplement 6.
Figure 3—figure supplement 6.. Bar chart showing the number and origin of imported individuals per genera, subset to genera with fewer than 100 individuals recorded.
Data from Law Enforcement Management Information System (LEMIS) 2000–2014. Red indicates those originating from the wild. Blue indicates those originating from captive operations (animals bred in captivity, commercially bred, and originating from a ranching operation). Summary statistics per genera are provided in the caption.
Figure 4.
Figure 4.. Summary of post-1999 described species and their presence in the trade.
(A) The species described post-1999 detected in the trade displaying the year of description and the year detected in the trade. (B) Species described post-1999 but were only detected in the 2020 snapshot. Alongside species names in A and B are their IUCN Redlist status; the Convention on International Trade in Endangered Species (CITES) appendix (where listed) is shown on the right of the plot. (C) Frequency plot showing the count of time lags between description and trade, with colours corresponding to broad summaries of IUCN Redlist status. Generated using Source code 11 and 12, and Source data 4, 7, and 10.
Figure 5.
Figure 5.. Number of species detected via each language in the online search.
Light blue shows the total number of species per language, and percentage of the overall online species list. Dark blue shows the number of species unique to a particular language and the percentage of that language’s species that are unique. Lollipop alongside bars describe the number of websites sampled. Generated using Source code 10 and Source data 1 and 3.
Figure 6.
Figure 6.. Upset plot showing the coverage and intersection of the five trade data sources.
The number of species per order is presented as an illustrative tree, alongside the % of the 8212 amphibian species in trade. The number of species that are covered by each CITES appendix is represented in the bottom left plot (red – not listed, light grey – Appendix I, medium grey - Appendix II, black – Appendix III). N.b., M&M 2019 is referring to Mohanty and Measey, 2019. Generated using Source code 8, and Source data 10.
Figure 7.
Figure 7.. Mapping diversity of species in trade for different uses based on the five data sources.
(A) Pet, (B) meat; (C) medicinal, (D) research, and (E) all trade.

References

    1. Altherr S, Lameter K. The rush for the rare: reptiles and amphibians in the european pet trade. Animals. 2020;10:2085. doi: 10.3390/ani10112085. - DOI - PMC - PubMed
    1. AmphibiaWeb AmphibiaWeb. University of California. 2020. [August 29, 2020]. https://amphibiaweb.org/amphib_names.txt
    1. Ashley S, Brown S, Ledford J, Martin J, Nash AE, Terry A, Tristan T, Warwick C. Morbidity and mortality of invertebrates, amphibians, reptiles, and mammals at a major exotic companion animal wholesaler. Journal of Applied Animal Welfare Science. 2014;17:308–321. doi: 10.1080/10888705.2014.918511. - DOI - PubMed
    1. Auliya M, García-Moreno J, Schmidt BR, Schmeller DS, Hoogmoed MS, Fisher MC, Pasmans F, Henle K, Bickford D, Martel A. The global amphibian trade flows through Europe: the need for enforcing and improving legislation. Biodiversity and Conservation. 2016;25:2581–2595. doi: 10.1007/s10531-016-1193-8. - DOI
    1. Bayley AE, Hill BJ, Feist SW. Susceptibility of the european common frog rana temporaria to a panel of Ranavirus isolates from fish and amphibian hosts. Diseases of Aquatic Organisms. 2013;103:171–183. doi: 10.3354/dao02574. - DOI - PubMed

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