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Reproduction without sex: some mother reptiles can do it on their own.

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Roger Downie, Froglife and University of Glasgow

Recently, media outlets summarised the findings of a paper published in Biology Letters (Booth et al., 2023) that reported the first known case of ‘virgin birth’ in a crocodile. Here, I describe the case and put it into the context of other known examples of reproduction without sex in reptiles.

An 18 year old American crocodile (Crocodylus acutus) had been in captivity, in isolation from other crocodiles, in a Costa Rican reptile park since the age of two. To the keepers’ surprise, it produced a clutch of 18 eggs. These were incubated artificially for 3 months, but failed to hatch. They were then opened up: only one contained recognizable contents, a well-developed baby crocodile, sadly dead. Its gonads showed it to be a female, and genetic analysis demonstrated that it was the offspring only of its mother, with no male input.

The technical term for virgin birth, where a female produces offspring without input from a male is ‘parthenogenesis’, and it can be of two general kinds: a) obligate, where it is the only kind of reproduction occurring in that species; b) facultative, where both sexual and non-sexual reproduction can occur.

How common is parthenogenesis? Obligate parthenogernesis is known in about 80 unisexual species of vertebrates, most of them lizards (Neaves and Baumann, 2011). The best-known examples are the whiptail lizards of Mexico and the southern states of USA, with 12 out of over 40 described species of Aspidoscelis (formerly Cnemidophorus) unisexual; and the rock lizards of the Caucasus mountains, with 7 out of 30 Darevskia species unisexual (Spangenburg et al., 2020). The unisexual lizards are nearly all hybrid clones resulting from matings between related species. The unisexual species have either three (triploid) or four (tetraploid) sets of chromosomes which can be identified in terms of the parental species contributing to the cross. It is believed that the unisexual species overcome any disadvantage from the lack of sexual reproduction through the hybrid vigour derived for their extra sets of genes. In Aspidoscelis, Crews et al. (1986) found that the females of unisexual species show female-female courtship behaviour and pseudo-copulation which enhances ovulation.

Obligate parthenogenesis is relatively easy to detect from the complete lack of males in populations of these unisexual species. Facultative parthenogenesis (FP) is more problematic, partly because many species have long-lived sperm which females can retain in their reproductive tracts after mating. The best evidence therefore comes from captive females kept in the absence of males, as in the crocodile case above. It is the first reported example of FP in any crocodilian, and also the first case from a species with temperature-dependent sex determination. In crocodiles, eggs incubated at low and high temperatures develop as females, with males appearing from incubation at intermediate temperatures: the Costa Rican crocodile’s eggs were incubated at 29-300 C, in the female-determining range. FP has been reported from two captive Komodo dragons (Varanus komodoensis) in Chester and London zoos respectively (Watts et al., 2006). The authors note that Komodo dragons kept for the captive breeding of this endangered species are usually housed as single females, with males brought in when the females are in good condition. Their discovery of eggs laid by unmated females (25 eggs, 8 viable in one case; 4 eggs, one viable in the other) may get in the way of the breeding programme. Komodo dragons have ZZ/ZW sex chromosomes, rather than the XX/XY pattern we are more familiar with in mammals. In ZZ/ZW, males are ZZ and females ZW (in XX/XY, males are XY and females XX). Parthenogenetic development from a female Komodo dragon produces ZZ or WW individuals, with ZZ male, and WW probably non-viable. Booth et al. (2012) published the first report of FP in wild snakes: they collected 22 pregnant copperheads (Agkistrodon contortrix) and 37 cottonmouths (A. piscivorus) and examined the litters for signs of FP (few if any male offspring; high proportion developmental failures). Two litters were selected for molecular analysis, to compare the offspring and maternal genomes, and both indicated that they were the products of only the maternal genomes. The authors note that in both cases, one theory for the occurrence of FP did not fit the facts; it has been suggested that females may use FP to overcome a shortage of males in a population, but in neither case was this true. Although unisexuality with obligate parthenogenesis has some advantages over sexual reproduction, it is not clear why FP should occur as an occasional variant on normal sexual reproduction. The finding of FP in a crocodile means that the only reptile taxon where parthenogenesis is unknown is the Chelonia.

The means by which parthenogenesis works as a reproductive mode can be complex. For example, the entry of the sperm into the ripe egg is usually the trigger for development to begin, so how is development triggered in the absence of fertilization? And what happens to the normal chromosomal reduction divisions of meiosis, when no sperm arrives to restore the diploid number? The references to this article will lead you to some of the answers.

You might also ask: does parthenogenesis also occur in amphibians? So far, it has not been reported, but there are unisexual species of amphibians, though they do not reproduce by parthenogenesis: a story for another day.

References

Booth et al. (2012). Facultative parthenogenesis discovered in wild vertebrates. Biology Letters 8, 983-5.

Booth et al. (2023). Discovery of facultative parthenogenesis in a new world crocodile. Biology Letters 19, 20230129.

Crews et al. (1986). Behavioural facilitation of reproduction in sexual and unisexual whiptail lizards. PNAS 83, 9547-9550.

Neaves and Baumann (2011). Unisexual reproduction among vertebrates. Trends in Genetics 27, 81-88.

Spangenburg et al. (2020). Cytogenetic mechanisms of unisexuality in rock lizards. Scientific Reports 10, 8697.

Watts et al. (2006). Parthenogenesis in Komodo dragons. Nature 444, 1021-2.

Croaking Science-The Cane Toad: a cautionary tale

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Roger Downie, University of Glasgow and Froglife

I first encountered cane toads in Trinidad (Rhinella marina, previously Bufo marinus, known locally as crapaud, the French for toad) during my initial visit there aimed at studying the variety of tropical amphibians and their life histories. The visit began in the dry season and cane toads were one of the few species around at that time of year. These large toads (a record-breaker has recently weighed in at 2.7kg in Australia) could often be found sitting in dog food dishes in back yards after consuming the food, with the hungry dog warily watching nearby, having learned that attacking these toads is not a good plan: they are well protected by the toxins in their massive parotoid glands. I also saw cane toad tadpoles – small, jet black, highly numerous and often in shoals – in slow-moving drainage ditches and low dry season rivers: the toads can breed at any time of year, their prolonged rumbling calls audible over a considerable distance. Linnaeus conferred the specific marinus on the basis of the Dutch naturalist Albertus Seba claiming they could live on land or in the sea. This was a partial error: they do not enter the sea, but can inhabit sandy beaches, feeding on the abundant invertebrates present there, and can spawn successfully in rivers close to the sea, where salinity levels may be significantly higher than in normal freshwater.

Record-breaking cane toad- Pic: Queensland Department of Environment and Science/AP

Cane toads are native to the Americas, ranging from southern Texas through central America and down into Peru and Amazonia; the islands of Trinidad and Tobago, adjacent to Venezuela, are considered part of their native range. However, the reason that cane toads are one of the most studied amphibian species is a consequence of their deliberate introduction to other parts of the world. Books and hundreds of scientific papers have been written about this species, and it must be the only anuran to feature in two full length documentary films (Cane toads: an unnatural history, 1988; Cane toads: the conquest, 2010). The toads tend to be found in open grassland areas, rather than forest, and the reason for their introductions elsewhere relates to their usual common name, cane toad: they are considered to predate the pests of sugar cane plantations. During the early 19th century, cane toads were introduced to several Caribbean islands as a control agent for pests such as rats and sugar cane beetles. Although the success of this action was patchy, positive results on the island of Puerto Rico were influential, and other introductions soon followed, to Hawaii and other Pacific islands.

The most consequential introduction was to the continent of Australia: in 1935, 102 toads sourced in Hawaii were brought to Queensland, and used to generate a population of 62,000 toadlets, which were then released into northern Queensland. The aim was to control a native beetle, considered a pest of the growing sugar cane industry. The toad’s colonisation of Australia was initially slow: not until 1959 was the coastal region of Queensland fully colonised; by 1978, the toads were moving south into New South Wales; by 1984 they were into the Northern Territories, and are now fully into Western Australia. Research by Rick Shine’s group has demonstrated rapid evolutionary changes in the characteristics of cane toads in the migration front: longer limbs, larger bodies, faster movement- allowing the front to advance now at 60 km per year.

The effects of cane toads on Australian native species are varied and changeable: they mainly relate to the toxicity of adults and tadpoles, reducing the effects of predators. Some Australian species have shown steep population declines following the arrival of cane toads: examples are the marsupial carnivore, the Northern quoll, and the varanid lizard known as the goanna. However, some predators appear to have adapted to the presence of cane toads and have found ways to avoid their toxins. In the longer term, we might expect that to progress. Overall, although there is considerable alarm over the effects of cane toads in Australia, they remain uncertain.

Many control methods have been tried, but none has been rated as successful so far. The annual Great Cane Toad Bust, lasting a week, has teams of local volunteers capturing adult toads and killing them by freezing. This is unlikely to have a significant effect on a population estimated at around 200 million. A feature that needs more research is what keeps cane toad populations in check within their native range: Lampo has estimated that native population densities are only 1-2% of those reached in Australia.

Finally, how effective were cane toads in controlling sugar cane pests in Australia? Shine’s analysis shows that the effects of cane toads have been complex, but not overall beneficial to sugar cane production. Sugar production did not increase following cane toad introduction. One reason for this is, that as a generalist predator, cane toads consume not only the beetles that are a pest of the cane, but also the ants which help control the beetles. They also poison the varanid lizards, another beetle control. Another factor is that the rodent population is unaffected by toad toxin, allowing them to consume toads and therefore grow their populations, thereby increasing their harmful effects on sugar cane. So despite the toads eating many beetles, their overall effects made matters worse for sugar cane production.

This cautionary tale should be at the forefront of thinking, whenever anyone advocates the introduction of an alien species as the answer to an ecological problem: the consequences are hard to predict.

 

References

Hinchliffe (2023). Public enemy no.1: on the hunt with Queensland’s army of volunteer toad busters. The Guardian 28/1/2023.

Lampo et al. (1998). The invasion ecology of the cane toad from South America to Australia. Ecological Applications 8, 388-396.

Phillips et al. (2010). Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads. Journal of Evolutionary Biology 23, 2595-2601.

Shine (2010). The ecological impact of invasive cane toads in Australia. Quarterly Review of Biology 85, 253-291.

Shine et al. (2020). A famous failure : why were cane toads an ineffective biocontrol in Australia? Conservation Science and Practice 2, e296.

Wikipedia articles on: The cane toad; the cane toad in Australia.

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.