Pet Trade

Croaking Science: The International Trade in Reptiles and Amphibians

August 30, 2022 by Roger Downie

Part 2: Amphibians

Roger Downie, Froglife and University of Glasgow

In Croaking Science (July, 2022), I introduced the topic of the international trade in wildlife, and then focused on reptiles. This article is a companion piece, concentrating on amphibians. It will cover the frogs’ legs and pet trades, discussing their impact on wild amphibian populations, disease spread and amphibian welfare. As I was researching the topic, an excellent report on the frogs’ legs trade appeared (Altherr et al., 2022), and I have drawn heavily from it.

The existence of trade implies that people make use of amphibians. Let’s start by summarising such uses. First, amphibians as food. We may think mainly of frogs’ legs as a delicacy in French cuisine (and certainly not as a dietary essential), but amphibians form part of the diet in many cultures, with frog meat for sale in markets across Africa, Asia and Latin America. The mountain chicken (Leptodactylus fallax) was long the national dish of the Caribbean island of Dominica, until declining numbers led to a hunting ban: chytrid then nearly finished the species off, but major conservation efforts are in progress (Nicholson et al. 2020). Second, people have long been aware of the rich variety of substances in amphibian skins. Traditional healers around the world have employed concoctions from frog skin as medicines and the Amerindians of Latin America famously tip their hunting arrows with the secretions of Poison Dart Frog (dendrobatid frog) skin. Modern research is testing amphibian skin derivatives for substances of real medical benefit (see Crump, 2015: reviewed in Natterchat, Spring/Summer 2017) Third, amphibians have long played a role in scientific research: for example, Galvani and Volta’s 18^th century experiments with electrical stimulation of frogs’ legs. More recently, the African clawed frog Xenopus laevis became a fixture of hospital laboratories when it was discovered that urine from pregnant women stimulated female Xenopus to ovulate: the basis of the first reliable pregnancy test. Stimulation of ovulation then allowed Xenopus eggs to be the model of choice for studies on embryonic development. Finally, some people like to keep amphibians as ‘pets’: this often involves colourful and exotic species.

Traditional uses, such as being a small component in a local diet or in medicine, do not necessarily involve international trade, nor are such uses likely to create a conservation threat, unless exploitation becomes unsustainable, as in the case of the mountain chicken. However, the frogs’ legs and pet trades are problematic, and this article focuses on them.

Import/export of frogs as food The USA and Europe are the main importers of frogs for food. The USA imports four species: the bullfrog Lithobates catesbeianus from Mexico, Ecuador and China; the East Asian Hoplobatrachus rugulosus from Thailand and Vietnam; Forrer’s leopard frog Lithobates forreri from Mexico; and the pig frog Lithobates grylio from China. The dominant species was L. catesbeianus, with 14.5 thousand tonnes imported as live individuals or frozen meat over the period 2015-20. Frogs were both wild caught and farmed (note that this species is a USA native, but has been both released and farmed in many other countries).

During the period 2010-19, the European Union (still including the UK) imported 40.7 thousand tonnes of frogs’ legs, derived from 814 million to two billion adult frogs (a wide range because of frog size differences). The most significant importing country was Belgium (69.9%), with France second (16.7%) and the Netherlands third (6.4%). However, much of the Belgian consignments moved on to France which is the predominant consumer country. Indonesia is the main supplier (74%), followed by Vietnam (21%), Turkey (4%) and Albania (1%). India and Bangladesh were formerly major suppliers, but the relevant species were CITES listed in 1985 and exports stopped, with Indonesia becoming the main new source. The species mainly imported into Europe are not reliably known: Ohler and Nicholas (2017) used DNA sequencing to show that 99% of frogs’ legs for sale in French supermarkets were incorrectly labelled as to their species identity. This is not necessarily deliberate: it is common for collectors of wild frogs in Indonesia not to know the identity of the species, and most of the Indonesian ‘crop’ is wild caught. However, this is clearly a problem if there is a need to conserve species from over-harvesting.

The frogs’ leg trade is mainly as frozen meat, so there are no welfare issues in the transportation phase, but there may well be welfare issues during capture and killing, so far negligibly reported. The Indian trade was halted because of worries that natural populations were becoming severely depleted, but also because of a realisation of the ecological role played by healthy frog populations, especially in rice paddy fields where they help control biting insects: the use of pesticides as an alternative is an extra cost to farmers, as well as adding risks of toxicity (Propper et al. 2020). It is so far unclear whether frog harvesting in Indonesia is having similar effects, but shifts in the species make-up of frog imports suggest some impact on native populations.

Frog farming is seen by some as a means of making the frogs’ leg trade sustainable: frog farming will be discussed in a future Croaking Science article.

Amphibians in the international pet trade Tapley et al. (2011) estimated that 127 species of amphibians were on sale from UK pet shops in 2004-5, an increase of 160% from 1992-3. They argue that the pet trade can benefit source economies and provide a stimulus for conservation by providing local people with an incentive for sustainable harvesting (a similar argument is used to justify trophy hunting in countries where there is potential conflict between large mammals like lions, and local farmers). However, Tapley et al. acknowledge the problem that local people are the least likely to obtain significant financial benefit from live frog collecting. Altherr and Lameter (2020) found 352 amphibian species in the German pet trade in 2017-18. Their particular concern was the number of species offered for sale which had only recently been described by science, and whose status in the wild was usually still unknown. They found 46 species of reptiles and amphibians offered for sale that had been first described in the period 2008-17, one within 3 months of description. It was clear that collectors were able to use the locality details in the scientific description to capture individuals which could then be sold at high prices on the basis of their novelty and rarity. It was also clear that the motivation driving some hobbyists is to possess a collection of rare and exotic species: a live animal collection of this kind is therefore more similar to a collection of artefacts like paintings than it is to possessing pets which can be classed as ‘companion animals’. Auliya et al. (2016) contend that the global trade in amphibians has helped bring many species to the brink of extinction, and that trade regulation urgently needs strengthening. It is noteworthy that, while amphibians are the vertebrate group with the highest proportion of species threatened with extinction (about one third of species), only 197 species (2.1% of the total) are listed in CITES appendices 1 and 2.

Oriental fire bellied toad: a popular exotic pet

One of the causes underlying the worldwide declines in amphibian populations is the spread of chytrid disease. Schloegel et al. (2009, 2012) documented the role of the live wildlife trade in the spread of the disease: they found a prevalence of 62% for chytrid and 8.5% for ranavirus in live frogs imported into the USA. Grear et al. (2021) reported on the ban on live urodele importation into the USA, which has so far been effective in stopping the spread of the urodele-specific species of chytrid, Batrachochytrium salamandrivorans : this disease is a particular worry because of the large number of endemic urodeles in the USA. Borzee et al. (2021) note that the amphibian trade may not only have a role in the spread of amphibian diseases: by affecting insect vector populations, amphibian harvesting may contribute to the spread of diseases of humans and domestic animals.

Finally, welfare. It is likely that the risks to individual amphibians from the live animal trade are higher than to reptiles, given their stringent physiological needs, especially for water. Lambert et al. (2022) discuss the risks to amphibians inherent in the way that they are collected, transported, sold and kept. Ashley et al. (2014) reported on the police raid on the warehouse of US Global Exotics that found large numbers of amphibians in such poor condition that 44.5% died within 10 days of discovery, despite skilled efforts to help them recover.

Conclusion Both the frogs’ legs and amphibian pet trades are highly problematic and need further investigation. It is hard to argue against Auliya et al’s (2016) plea for improved regulation. It may be of interest here that in the Australian state of Victoria, only native species of amphibians and reptiles can be kept by private owners, and that they have to be licenced (Howell et al., 2020). Could such a legal framework be effective elsewhere?

References

Altherr, S. and Lambert, K. 2020. The rush for the rare: reptiles and amphibians in the European pet trade. Animals 10, 1-14.

Altherr, S. et al. 2022. Deadly dish- role and responsibility of the European Union in the international frogs’ legs trade. Pro Wildlife and Robin des Bois. Munich and Paris. Published on-line.

Ashley, S. et al. 2014. Morbidity and mortality of invertebrates, amphibians, reptiles and mammals at a major exotic companion animal wholesaler. Journal of applied animal welfare science 17, 308-321.

Auliya, M. et al. 2016. The global amphibian trade flows through Europe : the need for enforcing and improving legislation. Biodiversity and Conservation 25, 2581-2595.

Borzee, A. et al. 2021. Using the global 2020 pandemic as a springboard to highlight the need for amphibian conservation in eastern Asia. Biological Conservation 255, 108973.

Crump, M. 2015. Eye of newt and toe of frog, adder’s fork and lizard’s leg: the lore and mythology of amphibians and reptiles. University of Chicago Press, Chicago.

Grear, D.A. et al. 2021. Evaluation of regulatory action and surveillance as preventive risk-mitigation to an emerging global amphibian pathogen Batrachochytrium salamandrivorans (BSal). Biological Conservation 260, 109222.

Howell, T.J. et al. 2020. Self-reported snake management practices among owners in Victoria, Australia. Veterinary Record 187 (3), 114.

Lambert, H. et al. 2022. Frog in the well: a review of the scientific literature for evidence of amphibian sentience. Applied Animal Behaviour Science 247, 105559.

Nicholson, D.J. et al. 2020. Cultural association and its role in garnering support for conservation: the case of the mountain chicken frog in Dominica. Amphibian and Reptile Conservation 14, 133-144.

Ohler, A. and Nicholas, V. 2017. Which frog’s legs do froggies eat? The use of DNA barcoding for identification of deep-frozen frog legs (Dicroglossidae: Amphibia) commercialized in France. European Journal of Taxonomy 271, 1-19.

Propper, C. et al. 2020. Role of farmer knowledge in agroecosystem science: rice farming and amphibians in the Philippines. Human-Wildlife Interactions 14, 273-286.

Schloegel, L. et al. 2009. Magnitude of the US trade in amphibians and presence of Bd and ranavirus infection in imported North American bullfrogs. Biological Conservation 142, 1420-1426.

Schloegel, L. et al. 2012. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 21, 5162-5177.

Tapley, B. et al. 2011. Dynamics of the trade in reptiles and amphibians within the UK over a ten year period. Herpetological Journal 21, 27-34.

Croaking Science: The international trade in reptiles and amphibians

July 21, 2022 by Roger Downie

Part 1: Reptiles

Roger Downie, Froglife and University of Glasgow

You can read part 2 of this series here.

Froglife recognises that some people derive their interest in and enthusiasm for reptiles and amphibians through keeping them, and that most such hobbyists do their utmost to provide the best conditions they can for the animals in their care. Nevertheless, Froglife’s view is that the life of these animals in captivity rarely meets their needs, especially in the case of animals which have been captured in the wild and then transported over long distances, prior to their sale and eventual residence in an enthusiast’s home. There are three fundamental issues facing the international trade in reptiles and amphibians. First, what impact does the trade have on the conservation status of these species, especially when we consider that amphibians are recognised as the most threatened of the terrestrial vertebrates (and reptiles may not be so different)? Second, to what extent does international trade in live wild animals contribute to the spread of diseases, both of wildlife and of humans? Third, how does the trade impact on the animals’ welfare? In two Croaking Science articles we will examine the international wildlife trade: first, reptiles.

Since 1975, the international trade in wildlife has been partially regulated by the Convention in International Trade in Species (CITES) of wild flora and fauna, which most countries (180+) have ratified. CITES regulates trade in species where trade might threaten their survival. Species are listed under three Appendices: 1- species threatened by extinction: only non-commercial trade under exceptional circumstances is permitted; 2- trade is regulated in order to avoid utilization incompatible with survival; 3- species threatened in a single country which therefore wishes to limit trade. Currently, 6.6% of reptile species (875 of 13,283) are on Appendices 1 and 2, including all crocodilians, sea turtles and boas/pythons.

Analysis of CITES data on the reptile trade by Marshall et al. (2020) shows that five genera (Alligator, Caiman, Python, Crocodylus, Varanus) comprise 84% of legally traded items. Most of this is skins for the fashion industry, and about 50% of this is not wild caught: i.e. it is derived from farmed animals. However, Marshall et al. also show that CITES regulations only cover a small proportion of internationally traded reptile species. Many animals are traded using the internet, mostly as part of the exotic pet trade: their estimate is that at least 36% of all reptile species are traded to some extent (compared to only 6.6% of species being CITES listed). To give a feel for the numbers involved, Auliya et al. (2016) calculated that the EU alone legally imported 20.8 million live reptiles over the period 2004-14. These numbers are certainly underestimates of the full trade. Sung et al. (2021) have shown that many freshwater and terrestrial chelonians are sold without regulation via social media sites (Hong Kong has one of the largest markets), and that much of this involves illegally harvested specimens. Worse, Stringham et al. (2021) report that a proportion of such trade does not occur on ‘observable sections of the internet’ i.e. it happens on the dark web. Vamberger et al. (2020) report that around 100,000 star tortoises are illegally collected and exported from India each year: many are confiscated and released, but the lack of data on where they were collected means that they are released in inappropriate locations, contributing to loss of local adaptations. Harrington et al. (2021) analysed information held by Facebook on wild animal exports from Togo, an important trade hub in west Africa. Of 187 species traded, 102 were reptiles, most of them not evaluated for the IUCN Red List, nor on CITES appendices. Can et al. (2019) found Peru to be the biggest contributor to the trade in live reptiles, 1.7 million individuals over 5 years.

The number of described species of reptiles increases by about 200 each year (see the on-line Reptile Database). One of Marshall et al.’s more disturbing findings is that recently-described species are being traded soon after their formal identification and well before their ranges, ecology and conservation status can be properly assessed. Altherr and Lameter’s (2020) analysis of the live amphibian and reptile trade in Germany (2017-18) found that 46 of the species traded had only been described by science in the previous decade, with most still lacking IUCN assessments: they concluded that for some hobbyists, a major motivation is the rarity and novelty of the animals.

So, is the international trade in reptiles a threat to their survival? One argument is that a well-regulated sustainable trade (i.e. based only on animals which can be harvested without damaging the state of wild populations) can provide an income for people who live in poverty in tropical countries that are rich in wildlife: the income gives an incentive to manage the wildlife resources well, rather than destroying them (Tapley et al. 2011). This is an extension of the idea that big game hunting helps conserve populations of charismatic large mammals in Africa. It is problematic in several ways: for example, do the poor people get much of the income flowing from wildlife harvesting, and which examples show human populations are capable of long-term sustainable wildlife harvesting (certainly not fishing)? For reptiles, Marshall et al. argue that we need a new basis for regulation founded on the precautionary principle: i.e. populations should be shown to be sustainable before any harvesting is permitted. Macdonald et al. (2021) agree: their analysis of the wildlife trade identifies ‘ten tricky issues’ inherent in both the legal and illegal trades, and concludes that the onus should be on traders to demonstrate that their trade is sustainable, humane and safe (with respect to disease and ecological invasion risks). The covid pandemic has concentrated concerns that international movements of wildlife contribute to disease spread (Can et al., 2019), but reptiles have not so far been focused on. And it is well known that exotic species of reptiles are often found in the wild, having been released as no longer wanted pets: depending on their origins, they may be able to establish populations.

Next, issues of welfare. As noted above, most of the trade regulated by CITES is in reptile skins. So any welfare issues relate to how the skins are harvested and how the animals are kept, if farmed (a future Croaking Science will investigate welfare conditions on reptile and amphibian farms). However, the larger reptile trade by species numbers is in live animals for the exotic pet trade. Welfare issues arise during the capture, transport and retail phases of this trade, as well as at the final location that the animals live. Not surprisingly, evidence on welfare in the illegal wildlife trade is hard to come by, but this is true even of the legal trade. Baker et al. (2013) reviewed 292 published papers on the live wildlife trade and found that only 17% included any reference to welfare, and these mainly applied to mammals. Wyatt et al.’s (2022) more recent review shows that this lack of information remains the case, and they argue that welfare issues ought to be at the forefront of discussions on how to reform the live wildlife trade. They quote an EU study that estimated that 70% of animals die within six weeks at commercial animal supply houses, and that 75% of pet reptiles and amphibians die within their first year, as a result of inappropriate care. Ashley et al. (2014) reported on what might seem an extreme case: the entire stock (26,400 animals from 171 species) held by the US company Global Exotics in Texas was confiscated following an inspection which showed 80% of the animals were grossly sick, injured or actually dead, with the remainder judged as in sub-optimal condition. During the 10 days following the confiscation, the mortality rate of the reptiles was 42%. Contributory factors were poor hygiene, poor food, inadequate water and heat provision, high levels of stress, over-crowding and poor or minimal environmental enrichment. In the subsequent court case, the company claimed that their mortality rates were similar to the industry standard! Harrington et al.’s work on the Togo wildlife trade also found welfare standards to be poor: no enrichment; poor shelter provision; inadequate space and water. The complexity and flexibility of reptile behaviour is increasingly being appreciated: see Lambert et al.’s (2019) review on reptile sentience and Downie (2021) on welfare and enrichment in captive reptiles.

In summary, the international trade in live reptiles may be contributing to biodiversity decline and is certainly causing suffering to a huge number of animals, especially when the trade is illegal and unregulated. What can be done? Restricting supply is the approach generally advocated, through attempts to stop poaching and by improved customs checks, but these suffer from poor resources in the countries where the animals live, and most emphasis tends to be on charismatic mammals like elephants and rhinos, rather than on reptiles. Thomas-Walters et al. (2021) focus on the factors that generate demand for wildlife: as noted above, some people are motivated by novelty, or rarity, so possessing a species few others have, rather like rich people who own expensive paintings. Thomas-Walters et al. identified five general motivations: experiential, social, functional, financial and spiritual, and discussed ways of reducing demand in each category. A UK government initiative, the Illegal Wildlife Trade Challenge Fund provides significant funding for projects aimed at combatting the illegal trade in wildlife, mostly in mammals, but projects on reptiles have been supported. Another angle is to focus on improving welfare. This is a tricky argument if one’s basic contention is that keeping captive wild reptiles should be stopped, since improved welfare standards might reduce the force of that overall aim. However, given that keeping wild reptiles in captivity is unlikely to stop soon, it is at least reasonable to urge for improved welfare standards. Williams and Jackson (2016) surveyed information available on welfare standards for reptiles in the UK pet trade, in the context of the UK’s Animal Welfare Act (2006) which provides guidance for the welfare of common companion animals, but not for reptiles. They found that some pet shops provided excellent advice on reptile care, but that many did not: e.g. only 8% gave advice on signs of ill health. The Federation of British Herpetologists has published ‘Good Practice Guidelines, 2015’ for private keepers of reptiles and amphibians, but Warwick’s review (on-line) is very critical of many of its claims, while accepting that some of the advice is helpful.

You can read part 2 of this series here.

References

Alterr, S. and Lameter, K. 2020. The rush for the rare: reptiles and amphibians in the European pet trade. Animals 10, 1-14.

Ashley, S et al. 2014. Morbidity and mortality of invertebrates, amphibians, reptiles and mammals at a major exotic companion animal wholesaler. Journal of applied animal welfare science 17, 308-321.

Auliya, M. et al. 2016. Trade in live reptiles, its impact on wild populations, and the role of the European market. Biological Conservation 204, 103-119.

Baker, S.E. et al. 2013. Rough trade; animal welfare in the global wildlife trade. Bioscience 63, 928-938.

Can, O.E. et al. 2019. Dealing in deadly pathogens: taking stock of the legal trade in live wildlife and potential risks to human health. Global Ecology and Conservation 17, e00515.

Downie, J.R. 2021. Environmental enrichment and welfare in captive reptiles. Natterchat 23, 6-9.

Harrington, L.A. et al. 2021. Live wild animal exports to supply the exotic pet trade: a case study from Togo using publicly available social media data. Conservation Science and Practice 3, e340.

Lambert, H.S. et al. 2019. Given the cold shoulder: a review of the scientific literature for evidence of reptile sentience. Animals 9, 821.

Macdonald, D.W. et al. 2021. Trading animal lives: ten tricky issues on the road to protecting commodified wild animals. Bioscience 71, 846-860.

Marshall, B.M. et al. 2020. Thousands of reptile species threatened by under-regulated global trade. Nature Communications 11, 4738.

Stringham, O.C. et al. 2021. A guide to using the internet to monitor and quantify the wildlife trade. Conservation Biology 35, 1130-1139.

Sung, Y-H. et al. 2021, Prevalence of illegal turtle trade on social media and implications for wildlife trade monitoring. Biological Conservation 261, 109245.

Tapley, B. et al. 2011. Dynamics of the trade in reptiles and amphibians within the UK over a ten year period. Herpetological Journal 21, 27-34.

Thomas-Walters, D. et al. 2021. Motivation for the use and consumption of wildlife products. Conservation Biology 35, 483.

Vamberger, M. et al. 2020. Already too late? Massive trade in Indian star tortoises might have wiped out its phylogenetic differentiation. Amphibia-Reptilia 41, 133-138.

Warwick, C. (on-line). Review: ‘Good practice guidelines for the welfare of privately kept reptiles and amphibians (2015).

Williams, D. and Jackson, R. 2016. Availability of information on reptile health and welfare from stores selling reptiles. Open Journal of Veterinary Medicine 6, 59-67.

Wyatt, T. et al. 2022. The welfare of wildlife : an interdisciplinary analysis of harm in the legal and illegal wildlife trades and possible ways forward. Crime, Law and Social Change 77, 69-89.

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