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Croaking Science: The International Trade in Reptiles and Amphibians

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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 18th 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.

African clawed frog

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

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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: The benefits of green spaces and nature on mental health

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“In every walk with nature, one receives far more than he seeks” – John Muir

As well as the conservation work Froglife does for amphibians and reptiles across the UK, we also run projects that promote education amenities and research activities for the benefit of the public. We run wildlife projects for disadvantaged young people and those with dementia, such as our Green Pathways, Green Pathways for Life and Leaping forward for Dementia projects. A common issue amongst our participants is mental health, especially coming out the other side of the COVID-19 pandemic. Our Eco therapy style project is based on scientific research that suggests being outdoors and connecting with nature, have hugely positive effects on individuals.

As countries become increasingly urbanised, the world’s population is spending increasingly less time exposed to natural environments (Cox et al, 2018). It has been reported that 55% of the world’s population live in urban areas and this is expected to increase to 68% by 2050 (United Nations, 2018). Unfortunately, urbanisation not only means spending less time in natural environments but more time destroying them and reducing the number of green spaces around the globe (Collins, 2014). Aside from the detrimental environmental effects of this, loss of these green spaces and time spent in them could have hugely negative effects on people’s mental health and well-being.

There is growing evidence to suggest that being in nature has positive effects on people’s mental health. Studies have shown that green spaces can lower levels of stress (Wells et al, 2003) and reduce rates of depression and anxiety, reduce cortisol levels (Park et al, 2010) and improve general well-being. Not only can a simple walk in nature boost your mood but also improve your cognitive function and memory (Berman et al, 2012).  Green spaces can provide a buffer against the negative health impacts of stressful life events. A Dutch study showed that residents with a higher area of green spaces within a 3km radius had a better relationship with stressful life events (Van den Berg et al, 2010) which was soon to be increasingly important in recent years with the effects of COVID-19.

So what is it about natural environments that are good for mental health and wellbeing?

Positive Physiological effects

Something as simple as exposure to natural environments can be physiologically restorative (Conniff et al, 2014). This means that being in a natural outdoor environment can have positive mental health effects due to the physical processes elicited in the body. A Japanese study showed that viewing and walking in forest environments can promote lower concentrations of cortisol, lower pulse rates and blood pressure when compared to city environments (Park et al, 2010). These physiological effects are all a counter to the physical effects stress causes in the body and are what happens when you relax. A recent study found that those who had access to natural spaces during the COVID-19 lockdowns had lower levels of stress and those that could view nature from home had reduced psychological distress (Ribeiro et al, 2021).

There are multiple psychological theories as to how nature helps our mental well-being. The two common prevailing theories on how nature brings about these positive effects are the Stress Reduction Theory (SRT) coined by Ulrich (1981) and Kaplan et al’s (1989) Attention Restoration Theory (ART).  SRT suggests that nature promotes recovery from stress and that urban environments have the opposite effect. Ulrich proposes that being in unthreatening natural environments (a green space you would consider safe) activates a positive emotional response. That being in nature produces this as a universal innate connection, promoting the physiological effects of lower blood pressure, heart rate and increases attention which in turn blocks negative thoughts and emotions (Ulrich et al, 1991). Kaplan et al’s ART works around the idea that we have different types of attention: voluntary or involuntary, and that the latter requires no effort. After using voluntary attention we experience ‘attention fatigue’, reducing our cognitive abilities and increasing mental fatigue. According to Kaplan et al, when we use our involuntary attention it gives us time to restore our voluntary attention. From this, Kaplan et al have suggested that what nature provides acts as a restorative power by providing four processes:

  • Being away – an opportunity to distance from routine activities and thoughts.
  • Soft fascination – nature holds attention effortlessly: think about the sunsets, sound of water, leaves blowing in the wind all-natural phenomena allowing your voluntary attention to rest.
  • Extent – nature provides an immersion experience, engaging the mind and rest from concerns.
  • Compatibility – a setting that is well matched to human needs and desires, providing a feeling of being in harmony with a greater whole.

These two theories have much in common: they focus on cognitive vs autonomic processes and both support a change in attention and stress load when an individual interacts with the natural environment (Gregory N. Bratman, 2012). However, they differ in how they suggest the primary mechanisms work. The effects the theories suggest are blurred in the sense of cause and effect: does a reduction in stress levels allow someone to concentrate better or does replenished direct attention help reduce stress?

Both these assertions are controversial in the field of environmental psychology, yet much research falls under either both or one of these theories.

Mental Health and Nature Policy

To what degree these theories influence policy is debated but it is clear that in recent years, especially after the recent pandemic, that nature spaces are becoming an increasing priority for mental health provision. Research has evidenced that we need to shift our attention from focusing on people visiting green spaces to how we interact and connect with nature close to home through simple activities (Mental Health Foundation, 2021). The Mental Health Foundation suggests from their research findings that we need to focus on six main areas in policy:

  1. Facilitating connection with nature
  2. Protecting the natural environment and restoring biodiversity
  3. Improving access to nature
  4. Making green spaces safe for all
  5. Using the planning system and urban design to improve the visibility of nature in every local area
  6. Developing a life – long relationship with nature.

Through our projects at Froglife we provide ways for people to interact with the environment instead of simply just being in it.

Promotion of Physical activity

Green spaces such as nature reserves, wilderness environments and urban parks also promote certain behaviours, such as encouraging physical activity within the space, which is a pro-mental health behaviour. Experimental studies have shown that not only do green spaces promote experience but they may be better for mental health than activity in other environments. Those that perform exercise in natural environments once a week are at about half the risk of poor mental health as those that don’t (Mitchell, 2013). Participation and involvement in nature is often tied to physical activities such as gardening or farming, trekking or running: the evidence of the benefits of this promotes the idea that green spaces should be seen as an essential health resource (Pretty, 2004).

There are many more benefits associated with natural green spaces. However, in terms of mental well-being, greener areas have been associated with a sustained improvement in mental health, highlighting the significance of green spaces, especially in urban areas. They provide not only a habitat for wildlife but also sustainable public health benefits (Alcock et al, 2014). Many studies have shown that more time spent in nature is associated with better mental health, independent of culture and climatic contexts, as well as the promotion of physical activity.

In addition to the wildlife and environmental benefits of conserving nature spaces, especially in urban areas, we also benefit in many ways from these natural spaces. This gives us even more reason to continue to protect our wildlife and conserve our natural areas and green space.

 

References

Alcock, I, et al., 2014. Longitudinal Effects on Mental Health of Moving to Greener and Less Green Urban Areas. Environmental Science & Technology , 48, 1247-1255.

Berman, M.G, et al., 2012. Interacting with nature improves cognition and affect for individuals with depression. Journal of Affective Disorders, 140, 300-305.

Bratman, M.G, et al., 2012. The impacts of nature experience on human cognitive function and mental health. Annals of the New York Academy of Sciences (Issue: The Year in Ecology and Conservation Biology), 1249, 118-136.

Collins, A.M., 2014. Destruction of urban green spaces: A problem beyond urbanization in Kumasi city (Ghana). American Joural of Environmental Protection, 3, 1-9.

Conniff, A, et al., 2016. A methodological approach to understanding the wellbeing and restorative benefits associated with greenspace. Urban Forestry & Urban Greening, 19, 103-109

Cox, D.T.C, et al., 2018. The impact of urbanisation on nature dose and the implications for human health. Landscape and Urban Planning, 179, 72-82.

Kaplan, R, et al., 1989. The Experience of Nature: A Psychological Perspective. New York: Cambridge University Press.

Mental Health Foundation, 2021. Nature- How Connecting with nature benefits our mental health. Published on-line.

Mitchell, R., 2013. Is physical activity in natural environments better for mental health than physical activity in other environments? Social Science & Medicine, 91, 130-134.

Park, B.J, et al., 2010. The physiological effects of Shinrin-yoku (taking in the forest atmosphere or forest bathing): evidence from field experiments in 24 forests across Japan. Environmental Health and Preventative Medicine, 15, 18-26.

Pretty, P. J., 2004. How nature contributes to mental and physical health. Spirituality and Health International, 5, 68-78.

Ribeiro, A.I, et al., 2021. Exposure to nature and mental health outcomes during COVID-19 lockdown. A comparison between Portugal and Spain. Environment International, 154 article 106664.

Ulrich, R. S., 1981. Natural Versus Urban Scenes: Some Psychophysiological Effects. Environment and Behavior 13, 523-556.

Ulrich, R. S., et al., 1991. Stress recovery during exposure to natural and urban environments. Journal of Environmental Psychology, 11, 201-230.

Van den Berg, A. E, et al., 2010. Green space as a buffer between stressful life events and health. Social Science & Medicine, 70, 1203-1210.

Wells, N.M. & Evans, G.W., 2003. Nearby Nature: A Buffer of Life Stress among Rural Children. Environment and Behavior, 35, 311-330.

Parental care in amphibians: research findings from 1705 to the present day

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Writen by Roger Downie, University of Glasgow and Froglife

Croaking Science does not usually urge its readers to study a particular scientific paper, but this is an exception. The paper is Schulte et al.’s (2020) review of research into amphibian parental care, a fascinating and essential read for all amphibian enthusiasts. Parental care is usually defined as ‘non-gametic investments in offspring that incur a cost to the parent’ and which provide some benefit to the offspring. Common examples are egg-guarding, and provisioning of young after hatching. Although some authors restrict discussions of parental care to actions that occur after fertilisation, others include activities like nest-building in preparation for egg laying. For example, we generally consider UK amphibians as lacking parental care: they deposit their eggs in water, then leave. But Schulte et al include the behaviour of female newts that wrap their eggs individually in leaves: this behaviour takes a substantial amount of time, so is costly to the female, and contributes to offspring survival by reducing predation.

Research into parental care tends to focus disproportionately on birds and mammals. Stahlschmidt (2011) in a review of what he termed ‘taxonomic chauvinisn’ found amphibian and reptile parental care much less studied than cases from birds, mammals and even fish. Schulte at al. redress this situation through a vast historically-based review, identifying 685 studies spanning the period 1705-2017. Early studies were mainly simply descriptive, but since 1950, there has been a greater focus on the investigation of explanations: what does parental care achieve, and what does it cost?

The paper’s Table 1 lists each of the parental care modes so far described: four in Caecilians; eight in Urodeles; 28 in Anurans. Some modes occur in all three Orders e.g. terrestrial egg guarding; others occur in only one Order e.g. wrapping of individual eggs in leaves by newts; foam-nest construction by many frogs. Overall, parental care is known from 56 (74%) of the amphibian Families. It is not really surprising that more parental care modes occur in the Anurans than in the other two Orders, since anuran species diversity is so high (Frost, 2021 lists 7406 anurans, 768 urodeles and 212 caecilians).

The first known report of parental care in an amphibian, remarkably, was by a German female natural historian and artist, Maria Sibylla Merian in 1705. Her book was mainly devoted to meticulous drawings of the insects she observed in Suriname, but she also included an illustration and observations on an aquatic frog, later named the Suriname toad (Pipa pipa), which incubates its eggs in individual pockets on its back: she saw the metamorphosed juveniles emerging from the pockets. I was lucky, on my first visit to Trinidad, to see this for myself. We captured a ‘pregnant’ female and the babies later hatched into the water, some still with tail stumps, others fully metamorphosed. Female biologists have been prominent in the study of amphibian parental care: in addition to Maria Sibylla Merian, Martha Crump (1996) and Bertha Lutz (1947) come to mind, as well as the four authors of the review under discussion.

Suriname Toad

Among the 500 or so papers that Schulte et al. cite, I was pleased to see two from the work we have done in Trinidad (Downie et al., 2001; Downie et al., 2005). These are about the Trinidad stream frog Mannophryne trinitatis (see Croaking Science September 2020), where the fathers guard the eggs on land then transport hatchlings on their backs to a pool where they can complete development to metamorphosis. Tadpole transportation is a common aspect of parental care in the neotropical families Dendrobatidae and Aromobatidae. We found that the fathers are choosy over where to deposit their tadpoles, avoiding pools that contain potential predators, and therefore contributing to their survival. The search could take up to four days. We wondered how costly this might be to fathers: to our surprise, transporting a relatively heavy load of tadpoles did not appear to reduce the fathers’ jumping ability, nor did it prevent them from finding food. However, four days away from their territory must count as at least some cost in terms of lost mating opportunities.

A male Trinidad stream frog, Mannophryne trinitatis transporting his tadpoles (photo credit: Joanna Smith)

Schulte et al. conclude with a timely plea for a revival of teaching and research in natural history. As they say, natural history observations – on the distribution, numbers and habits of organisms- form the basis of all new ideas and hypotheses in ecology and evolutionary biology. They note that there remain many amphibian species whose habits are poorly known and that many novel observations have been made on parental care in recent years. They therefore expect that much could be discovered, as long as effort is put into new field work. Over 20 years ago, I wrote lamenting the modern status of natural history (Downie 1997, 1999), and Schulte et al. report that the loss of organism-based teaching and research is widespread. In the UK, there are moves to create a natural history curriculum, to complement biology in schools. I feel that it is much needed.

References

Crump (1996). Parental care among the amphibia. Advances in the Study of Behaviour 25, 109-144.

Downie (1997). Are the naturalists dying off? The Glasgow Naturalist 23 (2), 1.

Downie (1999). What is natural history, and what is its role? The Glasgow Naturalist 23 (4), 1.

Downie et al. (2001). Selection of tadpole deposition sites by male Trinidadian stream frogs (Mannophryne trinitatis; Dendrobatidae): an example of anti-predator behaviour. Herpetological Journal 11, 91-100.

Downie et al. (2005). Are there costs to extended larval transport in the Trinidadian stream frog (Mannophryne trinitatis, Dendrobatidae)? Journal of Natural History 39, 2023-2034.

Frost (2021). Amphibian species of the world : an online reference. Version 6.1 (accessed 29/9/21). Electronic database accessible at http://amphibiansoftheworld.amnh.org/index.php. American Museum of Natural History, New York, USA.

Lutz (1947). Trends towards non-aquatic and direct development in frogs. Copeia 1947, 242-252.

Schulte et al. (2020). Developments in amphibian parental care research: history, present advances, and future perspectives. Herpetological Monographs 34, 71-97.

Stahlschmidt (2011). Taxonomic chauvinism revisited: insight from parental care research. PLoS ONE 6, e24192.

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

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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 strategies1 and 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.

 

 

 

 

Should we count marine turtles as members of the British fauna?

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In August 2020, the media outlet Wales On-line reported that a five-foot long marine turtle had surfaced beside a small fishing boat off the north coast and swum alongside it for an extended period before diving out of sight. The excited boat owner said that he had fished those waters for over 20 years, and never seen a turtle before. Was this an exceptional sighting? The fisherman was certainly lucky. Over the last century or so, the average number of leatherback turtles (the species observed) seen in British waters each year is around 15. However, this is bound to be a vast underestimate of the turtle numbers actually present in British waters. This is due to them being incredibly difficult to locate as they rarely emerge from the depths to breath, nor do they nest on British beaches; so the chances of actually spotting one in the huge expanses of our coastal waters are very slim.

Botterell et al. (2020) have published an analysis of marine turtle sightings, strandings (usually found dead washed up on shore) and captures (by-catch in fishing nets) since 1910. Of 1997 records, 84% are of leatherbacks; 12% of loggerheads, and 3% of Kemp’s ridleys. The remaining 13 records concern tiny numbers of three more species. Until 1980, records were small in number for all species, with substantial increases from the 1990s onwards. Mapping of the records shows that most are predominantly from the western side, including the English Channel, all around Ireland and north to the Orkneys and Shetlands. Leatherbacks and loggerheads have been recorded at all times of the year, with peaks in June-October (leatherbacks) and November-March (loggerheads). Kemp’s ridleys have only been seen from October-February. Measurements on body size, mostly from strandings and captures, suggest that most leatherbacks in British waters are adults, while loggerheads and Kemp’s ridleys are juveniles.

Although they may seem like an exotic species, these data clearly show that we should regard leatherback turtles as normal members of the migratory fauna that inhabits our surrounding seas. Adult leatherbacks manage this by generating enough heat that their body temperature is above ambient, allowing them to remain active in the cold waters of the North Atlantic; even juveniles can raise their body temperature above cold water temperatures by activity and reduction of heat loss (Bostrom et al., 2010).  For loggerheads and Kemp’s ridleys, the majority of records in British waters are strandings of juveniles in winter: these are most likely animals cold-stunned as water temperature declines. What is unknown is the number which venture into our waters, but manage to travel south and survive.

Marine turtles display what are known as cosmopolitan ranges, meaning that they are near-ubiquitous in waters globally. This has led to their incorporation into indigenous cultures around the world, with their size and habits having led to mythological status in many places. In an ecological context, the extensive migrations they undertake between foraging and nesting grounds (which often span entire oceans) are important for connecting ecosystems globally. The three species commonly found in British waters have distinct breeding and foraging grounds, with much information recently derived from satellite tracking of tagged adult females following capture at nesting sites (Fossette et al., 2014). For example, Atlantic leatherbacks consist of two separate populations. South Atlantic turtles breed either along the coast of Brazil or of West Africa, especially Gabon. Foraging takes them across the ocean and southwards, but not into the North Atlantic. The North Atlantic population breeds on the beaches of southern Florida, the islands of the Caribbean and the Guianas. They forage east and north, as far as British waters, as we have seen. Adult females return to nesting beaches every 2-4 years and lay up to 7 clutches, each 60 – 110 eggs, over several months.

Female leatherback turtle nesting on a beach in Tobago.

The males wait near the approaches to the beaches and attempt to mate with any females that turn up; however, they do not come onto land and instead spend their entire lives at sea. Leatherback females show moderately high nesting site fidelity, with all their nests in a season being laid on the same beach which they were born on or ones in close proximity. Hatchlings disperse into the sea and travel east towards open ocean to develop into juveniles. Kemp’s ridleys nest in the Caribbean, nearly all on one 16- mile Mexican beach; juveniles extend across the North Atlantic. Loggerheads are highly cosmopolitan with three distinct Atlantic populations. In the West Atlantic, they nest on beaches as far north as New Jersey and south to Parana in Brazil. Juveniles forage very widely. The Gulf Stream (also called the North Atlantic Gyre) was thought to be the primary determinant of juvenile distribution, as it carries developing individuals into east Atlantic waters. However, active dispersal has been recently documented in loggerhead, green and Kemp’s ridley turtles which suggests a more selective use of habitat than previously thought (Mansfield et al., 2014).

Sources of nutrition are a key determinant of marine turtle distribution. In other words, they go where the food is. The abundance of jellyfish in eastern Atlantic waters brings adult turtles, including loggerhead and Kemp ridley’s, but especially leatherbacks to UK and Irish coasts. As well as helping to predict the position of leatherbacks, the presence of jellyfish affects the depth at which the turtles swim. Jellyfish display a diurnal pattern of vertical migration, following their plankton prey up and down the water column. Plankton move to the water’s surface at night, when they are less visible to potential predators, and are closely followed by the jellyfish and, in turn, the turtles. Leatherbacks are so committed to pursuing their translucent prey that one intrepid individual was found swimming over 1000 metres underneath the surface during a foraging mission. This feat put leatherbacks into the top three diving animals on the planet alongside beaked whales and sperm whales. Their dedication to pursuing cnidarians was also shown by a 12,000 mile foraging journey from Indonesia to the US, which shows the determination present in their feeding habits.

It is these same feeding habits that have become a source of harm in recent times. Ingestion of marine litter, especially plastic bags, is a leading cause of turtle mortality. Particularly affected are leatherback turtles, due to their specialised diet of jellyfish which closely resemble partially degraded plastic bags hanging in the water column. One study analysed historical autopsy records spanning 123 years (1885-2007) and found plastic to be present in the digestive tracts of 34% of the dissected turtles (Mrosovsky et al., 2009). Plastic ingestion has a range of detrimental consequences, including reduced nutritional intake and asphyxiation.

There is a considerable worldwide effort to conserve marine turtle populations. One measure of this is the regularly updated IUCN Red List.  Since the 1980s, there has been a large reduction in leatherback numbers which has led to a ‘vulnerable’ classification by the IUCN. However, there are subpopulations that are doing even worse, such as those of the northwest Atlantic subpopulation who were reclassified from Least Concern to Endangered in 2019. Another case was a subpopulation based in the South China Sea that produced 10,000 yearly nests on the beaches of Malaysia. However, from the 1960s the population dwindled to the point where only two nests were laid in 2008, both of which were infertile (WWF, on-line). This decrease in numbers was partly made worse by misled conservation efforts, which collected and artificially incubated eggs at excessive temperatures, scrambling the sex determination process. As in many other reptile species, sex is determined by the temperature of incubation of the eggs. This shows the need for in depth research when developing conservation measures to deal with anthropogenic threats.

There is a wide range of barriers to the recovery of turtle numbers, with pressures both natural and anthropogenic. Among the natural threats faced by marine turtles is the impact of climate change on temperature-dependent sex determination, which disrupts reproduction and has knock-on effects on population demographics and dynamics. Another prominent challenge to successful reproduction is the predation of eggs and juveniles, which make for easy pickings for a diverse array of coastal predators.

A group of black vultures patrol a nesting beach looking for hatchlings to prey on.

Conservation efforts and scientific surveys are often based around these issues, when the turtles are onshore and accessible for data collection. Studies focused on the reproductive stage of turtle life are very valuable to the implementation of management strategies and can provide a range of insights into their life histories. The Exploration Society operating out of the University of Glasgow has run many research projects along these lines, based in the Caribbean islands of Trinidad and Tobago. These studies have contributed analyses of egg temperatures, tagging efforts to track distribution and last year uncovered a novel female behaviour for nest protection: after burying the eggs, females create a ‘decoy trail’ aimed at misleading predators over the location of the nest (Burns et al., 2020). All of these contributions are helpful to maintaining healthy populations of turtles, but there is still a large gap in the knowledge of turtle life out in the open ocean.

Leatherback hatchlings burst from a concealed nest, heading to the sea to begin their life of roaming the oceans of the world.

Marine turtles spend most of their lives navigating the oceans, across a massive geographic range and at various depths. This makes them pretty tough to track throughout their development from hatchling to mature adult, and even between nesting events. However, as we have seen, the use of satellite tracking has revealed much about adult migrations. In addition to this, the missing pieces of the puzzle can be cleared up with the help of sighting and stranding data collected from coastlines within their range, which can be acquired through citizen science projects and compiled into databases to map distributions at different stages of development. Stranded carcasses can also be inspected to gain an insight into the causes of death, and the larger scale threats to their survival. For example, carcasses with scars on their shells can show the impact of high densities of fishing vessels. The number of sightings can also be used as an indicator of population trends, as was shown by Botterell et al. (2020), summarised above. Tracking sightings and strandings off the British and Irish coasts, the study was able to attribute dips in numbers to major environmental events such as the Deepwater Horizon oil spill in 2010 and link population increases to successful conservation programmes. This shows that despite the challenges facing this fascinating group of reptiles, we can make use of the full range of analysis tools available to more fully understand their life history; from hatching through juvenile to nesting adult. From this, effective conservation strategies can be developed to protect marine turtles throughout their cosmopolitan range.

References

Bostrom, B.L. et al. (2010). Behaviour and physiology: the thermal strategy of leatherback turtles. PLoS ONE 5(11), e13925.

Botterell, Z.R.L. et al. (2020). Long-term insights into marine turtle sightings, strandings and captures around the UK and Ireland (1910-2018). Journal of the Marine Biological Association of the United Kingdom 100, 869-877.

Burns, T.J. et al. (2020). Buried treasure- marine turtles do not ‘disguise’ or ‘camouflage’ their nests but avoid them and create a decoy trail. Royal Society Open Science 7, 200327.

Fossette, S. et al. (2014). Pan-Atlantic analysis of the overlap of a highly migratory species, the leatherback turtle, with pelagic long-line fisheries. Proceedings of the Royal Society B 281, 20133065.

Mrosovsky, N. et al. (2009) Leatherback turtles: The menace of plastic. Marine Pollution Bulletin 58, 287-289.

Mansfield, K.L. et al. (2014) First satellite tracks of neonate sea turtles redefine the ‘lost years’ oceanic niche. Proceedings of the Royal Society B: Biological Sciences 281, 20133039.

WWF on-line. Search at https://www.wwf.org.my/?25625/Marine-Turtles-Malaysias-National-Heritage

Cameron Boyle, Roger Downie and Jack Rawlinson

Photos generously provided by Jack Rawlinson

University of Glasgow

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