welfare

Croaking Science: The international trade in reptiles and amphibians

July 21, 2022 by Admin

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.

Croaking Science: Captive Breeding, Conservation and Welfare of Amphibians.

June 15, 2021 by Admin

In general, Froglife does not encourage the keeping of amphibians (or reptiles) in captivity. Unlike the animals which have become used to close contact with people through the long process of domestication (farm animals and those that we treat as pets, or ‘companion animals’), there are no domesticated species of amphibians. We accept that people, especially children, can become fascinated and enthused by keeping newts, frogs or tadpoles, and that this can develop into a life-long interest that may encourage that person to contribute to the cause of wildlife conservation. However, the needs of amphibians are complex, and too often ignorance of these needs can lead to suffering and needless death in captivity. This can be particularly the case for non-native species when we add the traumas of being captured in the wild, international transportation, and being put on display for sale in a pet shop. Captive breeding of non-native species can alleviate some of this stress, but not the lottery of being cared for by enthusiastic but inexperienced keepers. Overall then, it is preferable for people to learn about amphibians from books, the media, wildlife ponds in private gardens and allotments, visits to wildlife sites where they can be encountered in their native habitats….and zoos.

Froglife recognises well-managed zoos (and aquaria) as exceptions to our policy against keeping amphibians in captivity. As well as having a broadly educational role concerning the world’s wildlife, zoos aspire to be an important component of the worldwide effort to conserve biodiversity. Where a species is threatened with extinction in the wild, it may be possible to take a small population into captivity and encourage them to breed, establishing a reserve population which can be used to re-populate the natural habitat when favourable conditions return. This practice is known as ex situ conservation. In this article, I review progress on ex situ conservation of amphibians and ask how well zoos are meeting their welfare needs.

The first Global Amphibian Assessment (Stuart et al., 2004) concluded that amphibians are the most threatened of the vertebrate classes, with about one third of species facing extinction. One response to this finding was the launch in 2007 of the Amphibian Ark (AArk) by a consortium of the IUCN and the World Association of Zoos and Aquaria. Its strategy is to identify threatened species whose survival chances could be improved by an interventionist programme including in-country and out-of-country captive breeding, allied to efforts to mitigate local threats to the species in the wild (Pavajeau et al., 2008). The AArk Newsletter, published quarterly, on open access, provides information on the progress of AArk programmes worldwide.

A major concern is highlighted by a team from Cologne Zoo (Jacken et al., 2020). They surveyed amphibian holdings in 4519 zoos and aquaria. Only about 7% of known amphibian species (=540 species) are currently kept in zoos. The three classes of amphibians are very unevenly represented, with 17.4% of newts and salamanders (=121 species), 6.1% of frogs and toads (=411 species) and only 3.9% of caecilians (= 8 species). Worse still, more than 10% of holdings are just single specimens; breeding success, even when larger populations are kept, is not high; and three quarters of the species kept are not threatened in the wild. Jacken et al. note that their survey did not include a number of good ex situ conservation programmes being run in university departments and museums, but they concluded overall that zoos are not fulfilling the aims of AArk. There can be several explanations for this situation. Although amphibians might seem highly suitable animals for ex situ conservation (for example, they are small, so do not require a lot of space; and they often have high reproductive outputs, with individuals maturing in a short time), in other ways they are highly problematic. For example, they are mostly nocturnal, so active when visitors are absent. Zoos depend for their incomes on paying customers, and need to prioritise species that people like to see. In addition, adult amphibians need live food, mostly insects, and this requires an efficient production facility. The high reproductive output of amphibians can also be a problem: once tadpoles have metamorphosed, how to keep the hundreds, perhaps thousands of offspring when space may be limited? And then there is disease: the high risks to the entire breeding facility from a chytrid outbreak requires a strict biosecure regime, incompatible with visitors (Pessier, 2008).

If AArk is to become successful, it clearly has to do better in encouraging zoos and other wildlife collections to hold more breeding populations of amphibians, prioritising threatened species (as long as a careful assessment concludes that ex situ conservation is an appropriate solution to the threats these species face). However, there is another issue: the psychological welfare of amphibians. There are several manuals of advice on amphibian husbandry, the most authoritative being Poole and Grow’s (2012) resource guide. This deals with food, water, housing, lighting, disease prevention etc. but, like most such guides does not cover behavioural and cognitive aspects of welfare. It has long been recognised that, in captivity, mammals and birds can suffer psychological distress from the lack of stimulation in their environment. This often manifests in the development of repetitive, sometimes self-damaging behaviours known as stereotypies. To avoid these, good zoo-keepers have devised a wide range of husbandry interventions, collectively known as ‘enrichments’, which provide the animals with interests and activities that promote psychological well-being (Young, 2003).

As well as promoting good mental health, enrichments can have another general purpose. Where animals are kept with ex situ conservation in mind, there is a need to prepare them for release into the wild. Enrichments can provide experience of ‘outside’ behaviours such as foraging, predator avoidance and mate-finding, without which survival in the wild is likely to be very brief.

In amphibians (and reptiles), there has been a tendency to believe that their behaviours are so simple and pre-programmed that enrichments are unnecessary. In a rebuttal of Dodd and Seigel’s (1991) critique of ex situ conservation for amphibians, Bloxam and Tonge (1995) wrote that amphibian ‘behaviours are less dependent on learning and environmental experience than those of birds and mammals…It has always seemed apparent to herpetologists that, with their relatively r-selected life history strategies¹and their low levels of behavioural complexity, amphibians should be ideally suited to short or medium-term conservation strategies’. These claims were accompanied by not a single supporting reference. It is worth contrasting these attitudes with work on fish, like amphibians, cold-blooded vertebrates and with a similar level of brain development. Much research, related to improving the welfare of fish in aquaculture, has shown that learning is important and that fish can suffer from pain and distress (Sneddon, 2015; Sloman, 2019). In addition, enrichments can promote the development of life-skills in fish (Salvanes, 2013). If this is the case for fish, why not for amphibians?

The most detailed discussion of enrichment in amphibians is the review by Michaels et al. (2014), subtitled ‘a neglected topic’. In comparison with the hundreds of papers on enrichment in mammals, Michaels et al. found only 14 relevant primary research papers on amphibians, and I have noted only a small number published since 2014. An issue is that ‘enrichment’ is rarely used in the titles, abstracts or key-words of papers related to husbandry in amphibians, whereas it is commonly used in the mammal literature. This in itself indicates that the amphibian research community has not yet taken the concept of enrichment on board. One sign of progress, however, comes from a comparison of the amphibian chapters in the 1999 and 2010 editions of the Universities Federation for Animal Welfare handbook, which recommends good practice for animals kept for use in laboratories. The main laboratory amphibian, since its earlier use in testing for human pregnancies, is still Xenopus laevis. The chapter by Halliday (1999) makes no mention of enrichment, but Tinsley (2010) discusses several aspects of enrichment such as the provision of covers and shelters. In addition to studies on shelters and their behavioural and physiological benefits, Michaels et al. found papers on the benefits of behavioural complexity: ramps, perches and ‘caves’ improved the welfare of bullfrogs. However, papers on the provision of complex habitats for amphibians too rarely investigate which features make a measurable difference in behaviour (for example, McRobert, 2003). In mammals, enrichments which encourage exploration of the enclosure and active foraging for food have been found to have considerable welfare benefits. We tend to think of amphibians as ‘sit-and-wait’ predators, but some species are active foragers. Michaels et al. found a few papers that investigated the welfare effects of varied food delivery techniques. Altering the position of a food dish increased activity levels in dendrobatid frogs, considered as a benefit. This, of course, raises the question: by what criteria do we consider the welfare of a captive amphibian to be improved? The small number of research studies to date means that this key question remains to be fully explored.

This article is intended as an introduction to the topic of welfare and enrichment, with a focus on amphibians. In a future article to appear in Froglife’s magazine Natterchat, I will review studies on reptiles.

Note 1: r-selected species generally have many offspring, limited parental care and short lives, as compared to K-selected species with small numbers of offspring, often prolonged parental care and long lives. Actually, some amphibians have complex parental care provision, small offspring numbers and some have long lives. In any case, it is not clear why Bloxam and Tonge feel there is a link between r-selected life histories and suitability for ex situ conservation.

Written by: Roger Downie Trustee, Froglife; Honorary senior lecturer, University of Glasgow

References

Bloxam and Tonge (1995). Amphibians are suitable candidates for breeding-release programmes. Biodiversity and Conservation 4, 636-644.

Dodd and Seigel (1991). Relocation, repatriation and translocation of amphibians and reptiles: are these conservation strategies that work? Herpetologica 47, 336-350.

Halliday (1991). Amphibians. In: Poole, T., editor. UFAW Handbook, 7th edition volume 2. Ps 90-102.

Jacken et al. (2020). Amphibians in zoos: a global approach on distribution patterns of threatened amphibians in zoological collections. International Zoo Yearbook 54, 146-164.

McRobert (2003). Methodologies for the care, maintenance and breeding of tropical poison frogs. Journal of applied animal welfare science 6, 95-102.

Michaels, Downie and Campbell-Palmer (2014). The importance of enrichment for advancing amphibian welfare and conservation goals: a review of a neglected topic. Amphibian and Reptile Conservation 8, 7-23.

Pavajeau et al. (2008). Amphibian Ark and the Year of the Frog campaign. International Zoo Yearbook 42, 24-29.

Pessier (2008). Management of disease as a threat to amphibian conservation. International Zoo Yearbook 42, 30-39.

Poole and Grow, editors (2012). Amphibian Husbandry Resource Guide. Association of Zoos and Aquariums.

Salvanes et al. (2013). Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proceedings of the Royal Society B 280, 1767.

Sloman et al. (2019). Ethical considerations in fish research. Journal of Fish Biology 94, 556-577.

Sneddon (2015). Pain in aquatic animals. Journal of experimental biology 218, 967-976.

Stuart et al. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783-1786.

Tinsley (2010). Amphibians, with special reference to Xenopus. In: Hubrecht and Kirkwood, editors. UFAW Handbook 8th edition. Ps 741-760.

Young (2003). Environmental enrichment for captive animals. Blackwell, Oxford.

Acknowledgements

Thanks for feedback on the first draft of this article from Kathy Wormald and Sheila Grundy.

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