Croaking Science

Croaking Science: The benefits of green spaces and nature on mental health

March 29, 2022 by Briony Nesbitt

“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:

Facilitating connection with nature
Protecting the natural environment and restoring biodiversity
Improving access to nature
Making green spaces safe for all
Using the planning system and urban design to improve the visibility of nature in every local area
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

November 30, 2021 by Roger Downie

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.

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.

June 15, 2021 by Roger Downie

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

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

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

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

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

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

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

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

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

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

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

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Acknowledgements

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

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

March 25, 2021 by Roger Downie

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

Croaking Science: Venomous Amphibians

December 21, 2020 by Xavier Mahele

Venomous animals are able to inject their toxins into another organism while poisons are ingested, inhaled and absorbed. The ability to deliver venom into another animal has distinct evolutionary advantages such as in defence, prey capture and even sexual selection.

Amphibians secrete a wide variety of compounds from their skin glands. Generally, mucous glands help provide a moist coating on their skin to facilitate cutaneous respiration while granular glands secrete substances that amphibians use as a chemical defence against predators (eg. toxic and noxious compounds) and microorganisms (eg. antimicrobial peptides). This is sometimes displayed with bright, aposematic colouration (Duellman and Trueb 1996).

Many different toxic secretions have been found in amphibian skin which act in numerous ways to disrupt the physiology of potential enemies (Daly et al. 2005, Savitzky et al. 2012). For example, newts in the genera Taricha and Notophthalmus synthesise tetrodotoxins in high concentrations and are co-evolving in an evolutionary arms race with Thamnophis garter snakes where toxicity is a selective pressure (Brodie et al. 2005, Mailho-Fontana et al. 2019, Hague et al. 2020). Fire salamanders secrete samandarin alkaloids through their paratoid glands which can cause convulsions, hypertension and respiratory paralysis in potential predators. Frogs can sequester an array of toxins such as the potent neurotoxin Zetekitoxin in the Panamanian golden frog and the batrachotoxins in highly toxic Phyllobates poison frogs (Duellman and Trueb 1996). The bright yellow Australian corroboree frogs of the genus Pseudophryne synthesise their own pseudophrynamine toxins as well as sequestering pumiliotoxins from their environment to deter predators (Smith et al. 2002). Fossorial caecilians are also known to produce defensive toxins with poison glands being discovered on the tails of Siphonops annulatus ringed caecilians as a possible defence against predators as they burrow into the soil (Jared et al. 2019).

Venom, however, is rare in amphibians with only a few species possessing a system to deliver their toxins into another organism.

The Iberian ribbed newt (Pleurodeles waltii) is a fascinating salamandrid from Spain and Portugal with an incredible defence behaviour. They have the ability to use their ribs to protrude through the skin to envenomate and ‘sting’ a predator. When distressed these newts can flatten themselves or arch their backs in an antipredator posture. They will then rotate their ribs 65° forwards which increases the angle of the spine to allow its ribs to penetrate through the skin wall and project as ‘spines’. This allows them to coat their ribs with a viscous, milky substance from their skin tubercles and inject it into the mouth of the predator making them unpalatable and allowing them to escape (Heiss et al. 2010). This defence mechanism doesn’t cause any permanent damage as antimicrobial peptides are able to prevent infection in the lacerated skin and their tissue is able to regenerate remarkably quickly. The tip of the ribs are also covered with a periosteum layer which is also thought to prevent microbial infection when the ribs puncture the skin.

The Echinotriton genus of crocodile newts are a sister group to the sharp ribbed newt and are also able to use their ribs to pierce their body wall when attacked by predators (Brodie et al. 1984).

Brazil is home to two tree frogs which have incredible cranial morphologies and venomous defensive mechanisms. The Greening’s frog Corythomantis greeningi live in the semi-arid caatinga ecosystem of Eastern Brazil and conceal themselves in tree hollows and rock crevices to stay moist and evade predators. Bruno’s casque headed frog Aparasphenodon brunoi is another endemic Brazilian hylid with a fascinating skull morphology. They inhabit lowland tropical forests and shrubland and like C. greeningi, will hide in water-filled tree or bamboo hollows and bromeliad phytotelmata.

Both of these peculiar frogs have flattened, casqued heads with their skin co-ossified with underlying bones. They use their heads to aid in a behaviour known as phragmosis (Jared et al. 2006, Blotto et al. 2020). Phragmosis occurs when an animal enters a hole and blocks the entrance with their head to defend themselves from predators. In the lab, these frogs will exhibit this behaviour by entering test tubes backwards and blocking themselves off with their casqued heads. This phragmotic behaviour along with their venomous spines means these frogs have never been observed being predated in the wild. It is also thought that cranial ossification and phragmosis also indirectly reduces water loss and prevents desiccation by creating a humid microclimate within their tree holes (Jared et al. 2006).

These frogs have bony spines, ridges and protrusions on their skulls in areas with high concentrations of granular and mucous glands which secrete a potent venom. Their mobile heads allow the frogs to deliver the venom into animals via head-butting and jabbing with their spines which are coated with the toxic secretions as the spines pierce their venom glands. This provides a highly effective chemical defensive mechanism as the toxin coupled with the wound caused by the head spines ensures would-be predators have a bad time when they attempt to ingest these frogs (Jared et al. 2015). Their cutaneous secretions include alkaloids and steroids which can induce oedema and intense pain in predators (Mendes et al. 2016). The venom contains both proteolytic and fibrinolytic agents as well as hyaluronidase which aids the toxins in diffusing around their enemies’ bodies (Jared et al. 2015).

The venom of Greening’s frog is thought to be twice as lethal as fer-de-lance snakes of the genus Bothrops while Bruno’s casque headed frog secretes a venom 25x as toxic as these notorious neotropical vipers with an LD₅₀ of 94.8µg in mice. A single gram of A. brunoi venom could kill 300,000 mice or 80 humans (Jared et al. 2015)! However, A. brunoi has smaller spines and granular glands than C. greening and so may not be able to inject as much venom when defending against a predator.

Top: Bruno’s casque headed frog (Aparasphenodon brunoi) L: Renato Augusto Martins R: Carlos Jared

Bottom: Greening’s frogs (Corythomantis greeningi) Carlos Jared

There are many other frogs with complex cranial morphology including immense variation in skull shape and hyperossification which often relate to their interesting and diverse ecologies (Paluh et al. 2020). With an array of other anurans having mineralised and spiny skulls, it is possible that there are a few more venomous frogs which are waiting to be studied. Contenders include the fascinating shovelhead tree frog Triprion, the crowned tree frog Anotheca spinosa and Polypedates ranwellai (Jared et al. 2015).

In a recent paper by Mailho-Fontana et al. 2020, a new set of specialised dental glands were discovered in Brazilian ringed caecilians (Siphonops annulatus) that may produce venomous enzymes – but further research is needed to confirm this. These enzymes were demonstrated to have gelatinolytic, caseinolytic and fibrinogenolytic properties. This incredible discovery may allow researchers to rethink the evolution of venom in vertebrates (since it could have evolved independently in both amphibians and reptiles) and inspire new studies about caecilian toxinology.

Through histological and biochemical analysis of saliva samples, researchers found A2 phospholipase enzymes which could mean that some fossorial caecilians inject venomous saliva via these dental glands into their earthworm prey in order to incapacitate and digest them. These enzymes are found in many other venomous creatures such as scorpions, snakes and insects. It is also worth noting that many venoms have originated as saliva such as in komodo dragons, shrews, bats and slow lorises making the prospect of venomous gymnophiones very exciting!

Other caecilians including the basal genus Rhinatrema showed similar dental glands to the ringed caecilians which could suggest that caecilians evolved to inject oral venom early on in their evolution (Jared et al. 2020).

Written by Xavier Mahele

References

Blotto, B.L., Lyra, M.L., Cardoso, M.C., Trefaut Rodrigues, M., R. Dias, I., Marciano‐Jr, E., Dal Vechio, F., Orrico, V.G., Brandão, R.A., Lopes de Assis, C., Lantyer‐Silva, A.S., Rutherford, M.G., Gagliardi‐Urrutia, G., Solé, M., Baldo, D., Nunes, I., Cajade, R., Torres, A., Grant, T., Jungfer, K.‐H., da Silva, H.R., Haddad, C.F. and Faivovich, J. (2020) The phylogeny of the Casque‐headed Treefrogs (Hylidae: Hylinae: Lophyohylini). Cladistics

Brodie, E.D., Feldman, C.R., Hanifin, C.T. et al. (2005) Parallel Arms Races between Garter Snakes and Newts Involving Tetrodotoxin as the Phenotypic Interface of Coevolution. Journal of Chemical Ecology 31, 343–356.

Brodie, E., Nussbaum, R., & Marianne DiGiovanni. (1984) Antipredator Adaptations of Asian Salamanders (Salamandridae). Herpetologica, 40(1), 56-68.

Daly, J. W., Spande, T. F. & Garraffo, H. M. (2005) Alkaloids from Amphibian Skin: A Tabulation of Over Eight-Hundred Compounds. Journal of Natural Products 68, 1556–1575

Duellman, W. E. & Trueb, L. (1996) Biology of Amphibians. McGraw-Hill.

Hague, M.T.J., Stokes, A.N., Feldman, C.R., Brodie, E.D., Jr. and Brodie, E.D., III. (2020) The geographic mosaic of arms race coevolution is closely matched to prey population structure. Evolution Letters 4: 317-332.

Heiss, E., Natchev, N., Salaberger, D., Gumpenberger, M., Rabanser, A. and Weisgram, J. (2010), Hurt yourself to hurt your enemy: new insights on the function of the bizarre antipredator mechanism in the salamandrid Pleurodeles waltl. Journal of Zoology 280: 156-162.

Jared, C., Antoniazzi, M.M., Navas, C.A., Katchburian, E., Freymüller, E., Tambourgi, D.V. and Rodrigues, M.T. (2005) Head co‐ossification, phragmosis and defence in the casque‐headed tree frog Corythomantis greeningi. Journal of Zoology 265: 1-8.

Jared C, Mailho-Fontana PL, Antoniazzi MM, Mendes VA, Barbaro KC, Rodrigues MT, Brodie ED (2015) Venomous Frogs Use Heads as Weapons. Current Biology Volume 25, Issue 16,

Jared, C., Mailho-Fontana, P.L., Marques-Porto, R. et al. (2018) Skin gland concentrations adapted to different evolutionary pressures in the head and posterior regions of the caecilian Siphonops annulatus. Scientific Reports 8, 3576.

Mailho-Fontana, P.L., Jared, C., Antoniazzi, M.M. et al. (2019) Variations in tetrodotoxin levels in populations of Taricha granulosa are expressed in the morphology of their cutaneous glands. Scientific Reports 9, 18490.

Mailho-Fontana, P. L. et al. (2020) Morphological Evidence for an Oral Venom System in Caecilian Amphibians. iScience 23, 101234.

Mendes VA, Barbaro KC, Sciani JM, Vassão RC, Pimenta DC, Jared C, Antoniazzi MM. (2016) The cutaneous secretion of the casque-headed tree frog Corythomantis greeningi: Biochemical characterization and some biological effects. Toxicon Volume 122.

Paluh D, Stanley EL, Blackburn DC. (2020) Evolution of hyperossification expands skull diversity in frogs. Proceedings of the National Academy of Sciences 117 (15) 8554-8562.

Savitzky, A.H., Mori, A., Hutchinson, D.A. et al. (2012) Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies. Chemoecology 22, 141–158.

Smith, B. P. et al. (2002) Evidence for Biosynthesis of Pseudophrynamine Alkaloids by an Australian Myobatrachid Frog (Pseudophryne) and for Sequestration of Dietary Pumiliotoxins. Journal of Natural Products 65, 439–447.l

Croaking Science: How many amphibian species are there, how do we know, and how many are threatened with extinction?

November 29, 2020 by Roger Downie

I’m sure most Froglife supporters and Croaking Science readers will be aware that the world’s amphibian species are in crisis. However, you may not know just how bad the crisis is, and how we know about it. This Croaking Science article aims to show how strong the evidence is, how it is gathered, and how difficult it is to keep up to date.

Herpetologists began to become aware in the 1990s that, although all kinds of wildlife were in trouble all over the world, amphibians were a special case. Simon Stuart and colleagues put numbers to this feeling in 2004. Their Global Amphibian Assessment estimated that 32.5% of amphibian species were globally threatened (i.e. they fitted into the IUCN Red List categories Critically Endangered, Endangered or Vulnerable: see later for definitions) compared to 12% of birds and 23% of mammals. Further, 22.5% of amphibians fell into the Data Deficient category i.e. too little was known about their status to make an assessment, a substantially higher proportion than for birds and mammals whose status tends to be better known. This meant that only about 44% of amphibian species could be classed as of Least Concern. Stuart and colleagues discussed possible reasons for amphibians being in worse shape than the other mainly terrestrial vertebrate groups (at that time, too little was known about the status of reptiles to make a similar estimate for them). Although anthropogenic habitat loss and change were the underlying main causes for all wildlife declines, amphibian populations seemed to be declining even in good quality habitat, for what Stuart et al. called ‘enigmatic’ reasons. Within a few years, it was clear that the main cause of the ‘enigma’ was the spread of the fungal disease chytridiomycosis against which many amphibian species had no or only very limited resistance. It is interesting in a time of a global pandemic affecting the human population to reflect on the causes and effects of a novel disease affecting wildlife.

Stuart et al.’s assessment was based on the then total number of described amphibian species, 5743. However, James Hanken (1999) had earlier noted the irony that, at a time when amphibian species were in severe decline, the number of known species was rapidly increasing. This trend has continued. The Amphibian Species of the World website (Frost, 2020) currently (October, 2020) lists 8226 species, a 43% increase on the number assessed by Stuart et al. in 2004. Over the last 10 years, the number of described species of amphibians (mostly anurans: frogs and toads) has increased on average by 150 per year.

How has this happened? The biggest discoveries of new species are in the tropics where amphibian diversity is highest, and where, until recently, resources and expertise for amphibian research were very limited. Amphibians are mostly small, mainly active at night, and often quite localised, all of which create difficulties in cataloguing biodiversity. It also turns out that external appearances can conceal underlying differences, so that it is only recently, with the availability of DNA sequencing, that herpetologists can work out that some species, previously thought to have extensive ranges, should really be split into several distinct species. Over my time studying the frogs of Trinidad and Tobago, new species descriptions of this kind have occurred in several cases. For example, the stream frogs of northern Venezuela, Trinidad and Tobago (see Croaking Science September 2020 for an account of colour changes in these frogs) were earlier thought to belong to one species: now they are three, Mannophryne trinitatis, M. olmonae and M. venezuelensis. Will this process of finding new amphibian species come to an end? Presumably it will, but currently there is no sign of the new discovery trend slowing down.

How do we establish the conservation status of a species? The task of keeping tabs on amphibians falls to the IUCN Species Survival Commission’s Amphibian Specialist Group (ASG). Their aim is to ‘provide the scientific foundation to inform effective amphibian conservation around the world’. A key part of their work is the compilation and revision of the Amphibian Red List i.e. an assessment of all species relative to their status in the wild. The main Red List categories (IUCN, 2001), with their definitions, and the current proportions of amphibian species in each category (from a total of 6932 species) are shown below:

Category, definition, percentage of amphibian species

Critically endangered (CR): extremely high risk of extinction in the wild, 8.9%

Endangered (EN): very high risk…, 14.4%

Vulnerable (VU): high risk…., 9.8%

Near threatened (NT): close to qualifying as threatened, 5.6%

Least concern (LC): widespread and abundant, 41.5%

Data deficient (DD): inadequate information available to make an assessment, 19.3%

There is a final category of ‘not evaluated’: these are mainly newly identified species for which information on their population status is often very limited. Where new species have been named from the splitting of a widespread species, this causes a particular problem for the Red Listing process. For example, the widespread small tree frog Dendropsophus minutus is an abundant neotropical LC species; the population in Trinidad is now classed as a Trinidad endemic, D. goughi, so its status now needs assessed separately.

Clearly, a species’ status can change with time, so the Red List needs regular updating. In addition, as noted above, the identification of new species means there is a constant need for new assessments. At present, the ASG is nearing completion of a major re-assessment, due for release in December 2020: it will be fascinating to find how amphibians as a whole have fared since the last major revision in 2010.

What sort of evidence goes into determining a species conservation status? The Red Listing process is as objective as possible and relies on input from experts around the world. Key questions are: have populations changed, and if so, by how much? What is the geographic range of the species, and how much of this range does it occupy? How large or small is the population? These can be quite difficult questions to answer with any degree of certainty. Consider the UK, with its considerable resources and abundant wildlife experts. We only have a small number of amphibian species. How good is our knowledge of their population sizes and trends? Even our presence/absence distribution maps are very variable in quality, and knowledge of populations is very patchy, even for the species that are of conservation concern, like natterjack toads and great crested newts.

Now consider Venezuela: a large country in political and economic turmoil with only a small number of dedicated herpetologists, but over 300 species of amphibians. The task of Red Listing here is immense and likely to be much based on educated guesswork. I have had some involvement over the last year in re-assessing the conservation status of Trinidad and Tobago’s much smaller number (35) of species, including three previously classed as threatened, and which share their ranges with Venezuela. The process has involved several herpetologists knowledgeable about the amphibians of the three territories pooling their information to complete the IUCN’s detailed evaluation forms, and coming to a judgement. The three species are:

Phytotriades auratus, the golden tree frog (see Figure). Formerly CR on the basis of occurrence only on two separate Trinidad mountain peaks, where it lives among the leaves and in the water tanks of huge arboreal bromeliads. Recent discoveries of populations in northern Venezuela and on another Trinidad mountain have led us to revise the assessment to EN.
Hyalinobatrachium orientale, the eastern glass frog (see Croaking Science, July 2020). Found along forest streams in northern Venezuela and in north east Tobago, but not Trinidad. Previously assessed as VU. Because of its limited range in Tobago and threats from deforestation in Venezuela, we retain VU as its Red List status.
Flectonotus fitzgeraldi, the dwarf marsupial tree frog (see Croaking Science October 2020). Found on forest and forest edge vegetation that holds pools of water, such as bromeliads and Heliconia, in northern Venezuela, Trinidad and Tobago. The previous assessment was EN, but when we examined the evidence, it became clear that this was a case where the previous assessors had made a judgment based on very limited data. Fortunately, we had been involved in extensive surveys of the presence/absence of this species in Trinidad and Tobago, as well as population estimates at a few locations. Added to data on the species’ range in Venezuela, we have been able to publish a paper (Smith et al. in press) and to assess this species as LC.

In these three cases, we have two reductions in the estimated threats. In both cases, these are not linked to active conservation effort, but rather to better data on the numbers and distribution of species. Much of the hard work has been done, not by experts, but by students and amateur naturalists taking part in actions like Bioblitzes. Mobilising citizens in this way has been important in the UK for taxa likes birds and butterflies. It needs to be done all over the world for more taxa.

References

Frost, D.R. (2020). Amphibian Species of the World, version 6.0. Available online.

Hanken, J. (1999). Why are there so many new amphibian species when amphibians are declining? Trends in Ecology and Evolution 14, 7-8.

IUCN (2001). IUCN Red List Categories and Criteria, version 3.1. Available online.

Smith, J. et al. (in press). The distribution and conservation status of the dwarf marsupial frog (Flectonotus fitzgeraldi; Anura, Hemiphractidae) in Trinidad, Tobago and Venezuela. Amphibian and Reptile Conservation.

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

Croaking Science

Top: Bruno’s casque headed frog (Aparasphenodon brunoi) L: Renato Augusto Martins R: Carlos Jared

Bottom: Greening’s frogs (Corythomantis greeningi) Carlos Jared

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