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

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

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

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

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

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

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

In amphibians (and reptiles), there has been a tendency to believe that their behaviours are so simple and pre-programmed that enrichments are unnecessary. In a rebuttal of Dodd and Seigel’s (1991) critique of ex situ conservation for amphibians, Bloxam and Tonge (1995) wrote that amphibian ‘behaviours are less dependent on learning and environmental experience than those of birds and mammals…It has always seemed apparent to herpetologists that, with their relatively r-selected life history strategies1 and their low levels of behavioural complexity, amphibians should be ideally suited to short or medium-term conservation strategies’. These claims were accompanied by not a single supporting reference. It is worth contrasting these attitudes with work on fish, like amphibians, cold-blooded vertebrates and with a similar level of brain development. Much research, related to improving the welfare of fish in aquaculture, has shown that learning is important and that fish can suffer from pain and distress (Sneddon, 2015; Sloman, 2019). In addition, enrichments can promote the development of life-skills in fish (Salvanes, 2013). If this is the case for fish, why not for amphibians?

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

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

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

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

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Acknowledgements

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

 

 

 

 

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

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

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

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

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

Female leatherback turtle nesting on a beach in Tobago.

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

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

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

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

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

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

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

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

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

References

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

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

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

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

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

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

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

Cameron Boyle, Roger Downie and Jack Rawlinson

Photos generously provided by Jack Rawlinson

University of Glasgow

Croaking Science: Venomous Amphibians

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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).  

Sharp ribbed newt (Pleurodeles walti)

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?

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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: Amphibians in the ‘Anthropause’

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On damp nights in the spring in temperate regions, amphibians emerge from their winter hideouts to migrate to their breeding pools. Nothing will stop their drive to reach water to spawn and so they brave a barrage of cars and artificial barriers along their route which often results in them getting squashed.

Amphibians have complex, biphasic life histories which makes their conservation challenging. Most species require high quality aquatic and terrestrial habitats which must both be connected by a transition habitat during migrations (Baldwin et al. 2006). 

As urbanisation expands around the world, many aspects of wildlife physiology, movement patterns, population genetics and overall health are affected due to anthropogenic stressors such as habitat loss and artificial light pollution. The unprecedented expansion in transport infrastructure in the past century has had massive impacts on amphibian populations around the world (Beebee 2013, Glista et al. 2008). Roads fragment habitats and cause high mortality as well as being a significant source of chemical contaminants (Petrovan and Schmidt 2016, White et al. 2017, Bird et al. 2019). 

Roads which bisect migratory routes severely restrict the dispersal of amphibians between their breeding areas and terrestrial habitat. This can have catastrophic impacts on gene flow and metapopulation dynamics potentially leading to population declines, genetic isolation and even extinction (Fahrig and Rytwinski 2009, Marsh and Trenham 2001). Therefore, mitigating road-kill and habitat fragmentation is a conservation priority (Puky 2005, Beebee 2013, Cushman 2005). Genetic bottlenecks as a result of fragmentation reduce the viability of populations and can leave amphibians more vulnerable to other synergistic environmental stressors such as climate change, pollution and emerging wildlife diseases (Cushman 2005, Laurence and Useche 2009). Urban fragmentation is known to decrease species diversity and abundance and coupled with wider habitat degradation such as edge effects and loss of breeding habitats, can make cities particularly challenging for amphibians (Bickford et al. 2011, Scheffers and Paszkowski 2012). At some field sites, mass mortality on roads can cause complete extirpation of anurans and salamanders within years (Cooke 2011, Hels and Buchwald 2000). With more and more cars on the roads, it is increasingly difficult for amphibians to avoid them. 

Common toads

Temperate amphibians such as the common toad have experienced significant and continuous declines. In the UK it is estimated that 20 tonnes of common toads (Bufo bufo) are killed annually as they migrate across roads to reach their breeding ponds, with up to 13,000 annual mortalities being recorded even at manned amphibian crossings. This has contributed to a 68% decline in their population size in the past 50 years at a rate of 2.26% per year. The severity of the population reduction means that these toads are no longer ‘common’ toads and could soon qualify as vulnerable on the IUCN Red List (Petrovan and Schmidt 2016).

The COVID-19 pandemic has caused immense human tragedy as it has spread around the world straining healthcare services and paralysing economic systems. Quarantine restrictions imposed by governments in order to slow the spread of the virus, have caused extraordinary disruption to our globalised society but have created rare opportunities for some wildlife species (Zellmer et al. 2020). As bustling metropolises slowed down they were occupied by usually elusive fauna; wild boars were seen roaming Barcelona’s quiet neighbourhoods, flamingos flocked to New Delhi’s lakes, river otters and puma stalked silent streets in Chile and sea turtles thrived on empty Brazilian beaches. A recent paper by Rutz et al. (2020) coined the term ‘anthropause’ for this rapid and unprecedented “global slowing down of modern human activities, notably travel.” It has resulted in profound short term environmental benefits such as improved air and water quality as well as reduced wildlife disturbance. 

Research conducted during the Anthropause has highlighted both known and less known impacts that we are having on the natural world and is providing a unique opportunity to study wildlife populations during a time of reduced human presence all around the world (Forti et al. 2020, Zellmer et al. 2020, Bates et al. 2020). Monitoring the ways wildlife has responded to covid lockdowns in urban areas allows researchers to quantify the impacts human mobility is having on wildlife in the Anthropocene (the term given to our geological age, dominated by human activities) and potentially find strategies to mitigate biodiversity loss (Rutz et al. 2020, Stokstad 2020). This research provides invaluable insight into the mechanisms of human-wildlife interactions that will inform conservation for decades to come. 

Lockdowns in spring and summer of 2020 meant fewer vehicles on the road which has significantly decreased road mortality for many species including amphibians. A “roadkill reprieve” this year may have made amphibian migratory journeys much safer according to Goldfarb (2020).  A study by Grilo et al. (2020) calculated that 194 million birds and 29 million mammals are killed on European roads each year under normal circumstances while in Brazil, road mortality has superseded hunting to become the “leading cause of direct human caused mortality in terrestrial vertebrates” (Carvalho et al. 2014). This year they may not suffer the same fate. Simply driving less could have been “the biggest conservation action” taken by humanity over the past 50 years according to Fraser Shilling of the Road Ecology Centre at UC Davis and could have potentially saved the lives of 500 million vertebrates (Nguyen et al. 2020). 

In March and April as traffic flows dipped by 73% across the US, many creatures received temporary respite from road collisions, with Californian mountain lion fatalities down 58% and a 48% decrease in roadkill deaths in Maine. Although much of the data focuses on large mammals, the same is true for smaller, less mobile animals such as amphibians, snakes and turtles (Katz 2020). 

At amphibian crossings this spring in Maine, wood frogs, salamanders and newts were twice as likely to survive than in previous years, which is great news for these sensitive creatures that are very vulnerable to habitat fragmentation.  Four amphibians successfully crossed the road for every one squashed this year, half as many as in previous years (Goldfarb 2020, Keim 2020).

Wood frog (Photo Credit: Brian Gratwicke)

A study by Manenti et al. (2020) examined the effects of the COVID-19 lockdown and reduced human disturbance on wildlife in Italy and describes both positive and negative effects on biodiversity conservation. As well as allowing wildlife to explore new habitats and extend their activity periods, species richness and reproductive success increased while roadkill diminished in temporarily quieter areas. Some negative ecological effects included reduced enforcement of regulations, and postponed conservation action such as invasive species management. 

A decrease in road traffic led to significantly improved survival of migrating amphibians on Italian roads this spring at eight toad crossings. Data suggests that there was an 80-90% decrease in nocturnal road traffic at these study sites during the anthropause. Four hundred and eight common toads (Bufo bufo) and 16 agile frogs (Rana dalmatina) were recorded as roadkill in 2019, and this dropped to only 38 toads and zero agile frog mortalities in 2020. The median mortality of road killed amphibians at each site decreased from 53 individuals to only one in 2020 (with some sites recording no mortalities) indicating that an increased number of adults made it to their breeding pools this spring giving populations a much needed boost. Manenti et al. (2020) also surveyed transects in Liguria, Northern Italy to quantify the effects of reduced traffic on common wall lizards (Podarcis muralis) and Western green lizards (Lacerta bilineata) and found a similar 10-fold decrease in road mortality. 

Many of the conservation benefits the Anthropause created are ephemeral, as traffic returned to baseline levels once economic activity restarted. Although breeding booms this spring may bring some respite to struggling populations, alone, they will not be able to counteract the extreme loss of genetic diversity as a result of population bottlenecks in the past. 

The information collected over the Anthropause highlights the need to improve the landscape to make it safer for all wildlife and particularly amphibians (Merrow 2007). If we can alter our transport networks to counter the effects of large-scale urban development and increased transport infrastructure we could go some way to mitigating the catastrophic impact of habitat fragmentation. The observed benefits that limiting road traffic can provide for migrating amphibians could inform more decisions about temporary, focused road closures around the world in the future to replicate this effect and to better conserve endangered amphibian and reptile species (Manteni et al. 2020).

Building fauna tunnels and bridges across dangerous roads to link habitat fragments allows animals to cross safely (Dodd et al. 2004, Gonzalez-Gallina 2018, Vartan 2017). Road mortality decreases by up to 85%-95% with animals responding surprisingly quickly to the change as ecosystems are reconnected (Vartan 2019). Wildlife tunnel projects can mitigate the effects of fragmentation and have been shown to allow amphibians to move successfully between sites bisected by roads. Tunnels and drift fences reduce road mortality, promote habitat connectivity, and allow amphibians to colonise new ponds leading to population increases and expansion into reconnected habitat (Jarvis et al. 2019). These movement corridors also allow roads to be permeable to a host of other wildlife species like reptiles and small mammals (Purky 2005, Jarvis et al. 2019). 

The incredible work done by volunteers at amphibian crossings who help migrating amphibians make it across roads (Petrovan and Schmidt 2016) could also contribute to sustaining population increases this spring from quieter road traffic. 

COVID-19 has also highlighted how explicitly intertwined human and wildlife health are and the catastrophic impacts of the overexploitation of nature. Emerging wildlife diseases such as chytrid fungi and ranaviruses threaten amphibians around the world and their spread has been catalysed by anthropogenic trade in our globalised world (O’Hanlon et al. 2019). A slowdown in global trade and human flows as a result of COVID-19 could also have gone a way to mitigating the spread of the pathogens that imperil amphibians (Forti et al. 2020). Although this benefit may only be short-lived as economies restart, there is hope that better regulation of the wildlife trade, in order to decrease the chances that future novel zoonotic diseases spill over from wildlife reservoirs in the future, could benefit amphibians too. Since the wildlife trade is responsible for the translocation of many amphibian pathogens (Kolby et al. 2014, O’Hanlon et al. 2018) better regulation and enforcement of the trade in live animals could help stem the spread of emerging amphibian diseases and invasive species (Forti et al. 2020). 

The Anthropause provides us with an excellent opportunity to reimagine our relationship with nature and our socio-economic systems so that biodiversity can flourish and acts as a reminder that biodiversity is essential for maintaining human health and wellbeing too.

The disruption to the economic status quo that the pandemic has created gives us a pivotal opportunity to consider a greener, more sustainable future where people and wildlife can thrive. In order to effectively stem biodiversity loss in the Anthropocene, we must use this pivotal moment to plan a green recovery which incorporates wildlife conservation into all economic rebound projects. In the UK this means not viewing the protection of  great crested newts as a delay to construction (Howard 2020) but valuing them as integral parts of a plan to balance our economic and environmental ambitions. It is also a perfect opportunity to invest in road mitigation measures such as wildlife tunnels and fauna bridges to reduce the detrimental impact they can have on wildlife populations (Merrow 2007), with the added benefit of being excellent economic multipliers.

November 2020 Croaking Science article by Xavier Mahele 

Bibliography

Baldwin RF, Calhoun AJK and Maynadier PG (2006) Conservation planning for amphibian species with complex habitat requirements: A case study using movements and habitat selection of the wood frog Rana sylvatica Journal of Herpetology 40 (4).

Bates AE, Primack RB, Moraga P and Duarte CM (2020). COVID-19 pandemic and associated lockdown as a “Global Human Confinement Experiment” to investigate biodiversity conservation Biological Conservation 248, 108665.

Beebee TJC (2013). Effects of road mortality and mitigation measures on amphibian populations. Conservation Biology 27(4).

Bickford D, Ng TH, Qie L, Kudavidanage EP and Bradshaw CJA (2010). Forest fragment and breeding habitat characteristics explain frog diversity and abundance in Singapore. Biotropica 42, 119-125.

Bird RJ, Paterson E, Downie JR and Mable BK (2018). Linking water quality with amphibian breeding and development: A case study comparing natural ponds and Sustainable Drainage Systems (SuDS) in East Kilbride, Scotland.The Glasgow Naturalist 27.

Carvalho NC de, Bordignon MO and Shapiro JT (2014). Fast and furious: a look at the death of animals on the highway MS-080, Southwestern Brazil Iheringia. Série Zoologia 104 (1).

Cooke A (2011). The role of road traffic in the near extinction of Common Toads (Bufo bufo) in Ramsey and Bury. Nature in Cambridgeshire 53, 45-50.

Cushman SA (2006). Effects of habitat loss and fragmentation on amphibians: A review and prospectus. Biological Conservation 128, 231-240.

Dodd C, Barichivich WJ and Smith LL (2004). Effectiveness of a barrier wall and culverts in reducing wildlife mortality on a heavily travelled highway in Florida. Biological Conservation 118, 619-631.

Fahrig L and Rytwinski T (2009). Effects of roads on animal abundance: an empirical review and synthesis. Ecology and Society 14(1): 21.

Forti LR, Japyassú HF, Bosch J and Szabo JK (2020). Ecological inheritance for a post COVID-19 world. Biodiversity and Conservation 29, 3491-3494.

Goldfarb B (2020). Lockdowns Could Be the ‘Biggest Conservation Action’ in a Century. The Atlantic.

González-Gallina A, Hidalgo-Mihart MG and Castelazo-Calva V (2018). Conservation implications for jaguars and other neotropical mammals using highway underpasses. PLOS ONE 13(11).

Hels T and Buchwald E (2001). The effect of road kills on amphibian populations. Biological Conservation 99, 331-340.

Howard J (2020). Boris ‘the Builder’ Johnson has found a new scapegoat: the humble newt. The Guardian 2/7/20.

Jarvis LE, Hartup M and Petrovan SO (2019). Road mitigation using tunnels and fences promotes site connectivity and population expansion for a protected amphibian. European Journal of Wildlife Research 65, 27.

Katz C (2020). Roadkill rates fall dramatically as lockdown keeps drivers at home. National Geographic 26/6/20.

Keim B (2020). With the World on Pause, Salamanders Own the Road: Traffic is down thanks to the pandemic. That’s good news for amphibians looking to migrate safely The New York Times

Kolby JE, Smith KM, Berger L, Karesh WB, Preston A, et al. (2014). First Evidence of Amphibian Chytrid Fungus (Batrachochytrium dendrobatidis) and Ranavirus in Hong Kong Amphibian Trade. PLOS ONE 9(3).

Laurence WF and Useche DC (2009). Environmental Synergisms and Extinctions of Tropical Species. Conservation Biology 23,1427-1437.

Manenti R, Mori E, Canio VD, Mercurio S, Picone M, Caffi M, Brambilla M, Ficetola GF, Rubolini D (2020). The good, the bad and the ugly of COVID-19 lockdown effects on wildlife conservation: Insights from the first European locked down country. Biological Conservation 249, 108728.

Marsh DM and Trenham PC (2001). Metapopulation dynamics and amphibian conservation. Conservation Biology 15(1), 40-49.

Merrow J (2007). Effectiveness of amphibian mitigation measures along a new highway. UC Davis: Road Ecology Centre.

O’Hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, Kosch TA, Murray KA, Brankovics B, Fumagalli M, Martin MD, Wales N, Alvarado-Rybak M, Bates KA, Berger L, Böll S, Brookes L, Clare F, Courtois EA, Cunningham AA, Doherty-Bone TM, Ghosh P, Gower DJ, Hintz WE, Höglund J, Jenkinson TS, Lin C-F, Laurila A, Loyau A, Martel A, Meurling S, Miaud C, Minting P, Pasmans F, Schmeller DS, Schmidt BR, Shelton JMG, Skerratt LF, Smith F, Soto-Azat C, Spagnoletti M, Tessa G, Toledo LF, Valenzuela-Sánchez A, Verster R, Vörös J, Webb RJ, Wierzbicki C, Wombwell E, Zamudio KR, Aanensen DM, James TY, Gilbert MTP, Weldon C, Bosch J, Balloux F, Garner TWJ, Fisher MC (2018). Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360, 621-627.

Nguyen T, Saleh M, Kyaw M, Trujillo G, Bejarano M, Tapia K, Waetjen D Shilling F (2020). Road Special Report 4: Impact of COVID-19 Mitigation on Wildlife-Vehicle Conflict. Ecology Centre UC Davis. 

Puky M (2005). Amphibian road kills: a global perspective. UC Davis: Road Ecology Centre UC Davis.

Rutz C, Loretto M, Bates AE et al. (2020). COVID-19 lockdown allows researchers to quantify the effects of human activity on wildlife. Nature Ecology and Evolution 4, 1156-1159.

Scheffers BR and Paszkowski CA (2012). The effects of urbanization on North American amphibian species: Identifying new directions for urban conservation. Urban Ecosystems 15(1).  

Stokstad E (2020). Pandemic lockdown stirs up ecological research. Science 369, 893.

Vartan S (2019). How wildlife bridges over highways make animals—and people—safer. National Geographic 18/4/20.

White KL, Mayes WM and Petrovan SO (2017). Identifying pathways of exposure to highway pollutants in great crested newt (Triturus cristatus) road mitigation tunnels. Water and Environment Journal 31, 310-316.  

Zellmer AJ, Wood EM, Surasinghe T, Putman BJ, Pauly GB, Magle SB, Lewis Js, Kay CAM, Fidino M (2020). What can we learn from wildlife sightings during the COVID-19 global shutdown? Ecosphere. 6:11(8), e03215.

Croaking Science: Red Alert! The alarming state of marsupial frogs

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Amphibians have evolved a fascinating variety of ways to produce and look after their young. Parental care occurs in many families, with either the mother or the father, or occasionally both, spending time and effort to give their young a better chance in life. Recent Croaking Science articles have described the glass frogs (July), where fathers guard incubating eggs on leaves above streams; Phyllomedusa tree frogs (August) where the parents enclose the eggs in folded leaves above water; Mannophryne stream frogs (September), where fathers guard their eggs on land, then transport the hatched tadpoles on their backs to safe water. This month, we look at the marsupial frogs, where mothers carry their developing eggs on their backs. As well as considering their reproductive arrangements, we look at their conservation status: overall, an alarming picture.

The Hemiphractidae are a family of New World frogs, composed of 118 species in six genera. They are distributed across Central and South America, as well as some Caribbean islands. They are very small arboreal frogs, with a primarily nocturnal lifestyle. The main distinguishing feature of the family is the storage and development of eggs on the backs of females, either externally or within a pouch (which has earned some the nickname of marsupial frogs). They also have unusually large embryonic external gills compared to other frogs.

Males of several species have been seen to actively place the eggs on the backs of females during amplexus, during which time they are assumed to contribute their half of the required gametes. They have mostly been seen to breed during wet seasons in tropical areas, as most frogs do. In northern parts of South America there are two wet seasons, a long one lasting from April until August and a shorter one lasting from November until January. Hemiphractid frogs have been seen carrying eggs during both of these, suggesting that they do not possess a strict reproductive timetable but carry out opportunistic breeding when conditions suit.

You can see a range of specialisations between hemiphractid genera, none more apparent than the egg-carrying strategy (to pouch or not to pouch). The genera that utilise enclosed dorsal pouches include Gastrotheca, Flectonotus and Fritziana. Cryptobatrachus, Stefania and Hemiphractus don’t have pouches, instead using mucosal secretions to keep the eggs in place.

Within the pouchless genera, Stefania stand out due to the development of young. In this genus there is no free-swimming tadpole stage, resulting in the hatching of froglets directly from the eggs carried on the female’s back. Female Stefania individuals have been found carrying up to 25 eggs on their back! With a gestation period of around 3 months, those kids are one heck of a burden. Within the pouched or “marsupial” species, the two belonging to the genus Flectonotus stand out due to their mysterious nature, with little research being conducted on either. It is known, however, that hatching occurs within the pouch and that individuals are then deposited into small bodies of water, such as in the ‘tanks’ enclosed by bromeliad leaves; they are at the stage of being well developed tadpoles, which soon metamorphose, without feeding. It is not clear why Flectonotus retains this requirement for a brief aquatic phase, rather than progressing to the froglet stage in the pouch.

Conservation status

Analysis of IUCN’s Red List status for the family Hemiphractidae shows 32% of species in the four threatened categories (critically endangered to near threatened), similar to the figure for amphibians as a whole. However, only 25% of species are in the least concern category, which provides a much more alarming picture. This is because 24% of species are listed as data deficient, and 20% more have yet to be assessed. This is the reality behind some of the global figures for the state of nature. In some parts of the world, especially the tropics, the state of our knowledge of many groups and individual species is very poor. Because of the continuing loss and alteration of natural habitats around the world, the expectation is that species whose status is poorly known are unlikely to be doing well. However, this is not always the case, as we show below for one species of hemiphractid frog.

The dwarf marsupial frog (Flectonotus fitgeraldi) was brought into the spotlight by a recent piece of collaborative research between researchers in Scotland, Trinidad, the USA, Portugal and Venezuela. This study aimed to clarify the conservation status of the species, by establishing an accurate picture of their distribution. Currently, IUCN lists the species as Endangered, but this status appeared to be based on no published original research. Finding these frogs is easier said than done, since they are sized between 2 and 3cm (roughly the size of a 2 pence coin). They have been reported to exist across the islands of Trinidad and Tobago, as well as northern parts of Venezuela. However, there was uncertainty as to whether these three populations fit within a single species, since there had been several cases previously when close examination of widely distributed amphibian species revealed the different populations to be divergent enough to merit description as separate species.

A frog sitting on a wooden surface Description automatically generated
Pictured: F. fitzgeraldi male perched on a leaf, caught mid-croak by Paul Hoskisson

F. fitzgeraldi are most reliably found by identification of the plant species they use as homes and tadpole deposition sites. These are commonly bromeliads, heliconias and aroids. The larval young of F. fitzgeraldi are deposited in phytotelmata, small pools of water contained within plant structures. The hatching tadpoles are at a late non-feeding stage, having been nourished by yolk content of the egg. In the days following deposition in a bromeliad tank, tadpoles develop limbs and emerge from the water as froglets. Metamorphosis is normally complete within 5 days, during which the tail is reabsorbed and froglets graduate to become fully-fledged frogs.

In order to review the Endangered classification of F. fitzgeraldi, the study made use of molecular techniques as well as surveys over the course of several years. Genomic DNA samples were compared for sequence similarity to determine whether the populations in Trinidad, Tobago and Venezuela all belonged to the same species. Surveys were initially conducted to determine the hours of peak activity in F. fitzgeraldi and found that they exclusively call between 6pm and 8pm, roughly an hour either side of sunset. Based on this information, presence/absence surveys were carried out using the call to determine presence (seeing the frogs is difficult, and moving vegetation to attempt to see them disturbs the frogs) at locations across Trinidad, Tobago and Venezuela. These took the form of transects through forested areas, either on foot or in vehicles, while listening for the raspy calls of F. fitzgeraldi, which sound like running your finger along a comb. This presence/absence data was used to build up a map of their distribution.

Pictured: F. fitzgeraldi perched on a leaf

Results from the study showed the three populations belong to the same species, with no taxonomic changes needed. It was also shown that F. fitzgeraldi was distributed more widely across Trinidad,  Tobago and Venezuela than previously thought. This, combined with the lack of evidence showing deforestation on these two islands, was sufficient to demonstrate that ‘Endangered’ is too extreme a label for the species. However, deforestation in Venezuela, mainly for cattle farming, was found to threaten the habitat quality of F. fitzgeraldi, so the study concluded that a categorisation of the species as ‘Vulnerable’ was appropriate.

Pictured: Female F. fitzgeraldi: left- showing slit on the back, entrance to the brood pouch; right- ‘pregnant’ female. Each bump is a developing embryo in the brood pouch.

Although F. fitzgeraldi is sheltered from mainland deforestation by the island refuges provided by Trinidad and Tobago, many other hemiphractid frogs do not share the same luxury. This means that habitat loss caused by deforestation poses a threat to species whose distribution is restricted to northern areas of the South American continent, such as Venezuela and Guyana. For this reason, species of the hemiphractid family must be monitored closely in these areas over the following decade.

The work on F. fitzgeraldi that we summarise here shows that detailed fieldwork can sometimes reveal that the status of a species is better than previously thought. It also shows the value of student expeditions, which can deploy significant numbers of enthusiastic young people to carry out detailed field research which would be prohibitively expensive otherwise.

Acknowledgements

We thank Paul Hoskisson and Joanna Smith for permission to use their photographs.

Further reading

Our account of the conservation status of F. fitzgeraldi is based on a research paper currently under review.

Cameron Boyle and Roger Downie
University of Glasgow

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