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Turtles in UK waters

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By Andrew Smart, Conservation and Science Senior Manager. 

Since it is National Marine Week (22 July to 6 August, organised by the Wildlife Trusts), it is appropriate to return to our only marine reptile species, the marine turtles, last covered by Croaking Science in April 2021: Should we count marine turtles as members of the British fauna? One species, the leatherback turtle (Dermochelys coriacea), is considered to be a member of the British fauna, while the other species, perhaps best described as hard shelled turtles, are vagrants who have moved away from their normal migration paths and, one way or another, end up stranded on UK beaches Turtles stranded on UK beaches after storms send them off course.

These strandings are generally of loggerhead turtles (Caretta caretta) and more recently, Kemp’s ridley, (Lepidochelys kempii). Occasionally green turtle (Chelonia mydas) and very rarely, hawksbill (Eretmochelys imbricata) and olive ridley turtles (Lepidochelys olivacea) (both single records) are washed up on our beaches1. Loggerheads and Kemp’s ridley originate from the Caribbean, most likely from nesting beaches on the Florida coastline and Gulf of Mexico, from where hatchlings travel across the Atlantic.  The hatchlings spend their early years, often called the ‘lost years’, in the North American basin and many move into the North Atlantic gyre2, travelling across the ocean from east to west, then follow the current south past the Azores and Canary Islands before travelling westward back towards their nesting beaches as juveniles3.

Loggerheads are sometimes killed after interactions with boats, caught in longline fisheries4, tangled in pot lines or in ‘ghost nets’, but many animals suffer from ‘cold stunning’ when they move out of warm water into colder temperatures (10 – 15oC) that cause them to effectively ‘shut down’5. Turtle hatchlings will die at temperatures below 10oC6. Animals that have been ‘cold stunned’ or died are stranded along European coasts and are collected and examined. Any UK strandings of turtles (or any other marine animal) can be reported to the Marine Strandings Scheme (or in Scotland SMASS). Many stranded dead turtles have been found to have frequently ingested plastics (69% of individuals examined) which they may mistake for food 7, 8; jellyfish and salps. Animals stranded in the UK tend to be juveniles, with a carapace measurement of less than 40 cm, and tend to be stranded in the winter months1. In the last three decades numbers of loggerhead and Kemp’s ridley turtles have increased, with more than twice the number of animals stranded when compared to the 1980s1.  

Genetic analysis of loggerheads stranded in France indicate that as well as animals from Florida and the Caribbean, some also come from the nesting beach on the Cape Verde Islands,  from where animals are occasionally blown north by storms along the Portuguese and Spanish coasts9 and into the Bay of Biscay.  Loggerheads nesting in the Mediterranean move in and out of the Straits of Gibraltar along with animals from the Caribbean10, which move inwards through the ‘Straits’ and are sometimes recorded off the coast of Algeria. Mediterranean turtles would be unlikely to move northwards into colder water around the UK. However, recent work suggests that there may be a population of juvenile loggerheads using the Bay of Biscay as feeding grounds during warmer periods11.  

Kemp’s ridleys also come from the Gulf of Mexico and are being recorded more frequently as UK strandings in the last three decades. Very occasionally there are strandings of olive ridley, hawksbill and green turtle1.  Green turtles stranded on French coasts have been from African populations not from the Mediterranean12, where the nesting green turtle populations in the east generally travel along the North African coast to feed before returning to nest in Turkey and Syria13.

The leatherback turtle is the largest turtle species; the biggest recorded washed up on a Welsh beach in the 1980s, weighed over 900 kg and was 2.9 m (9 ½ ft) long14. Leatherbacks feed mainly on jellyfish and other gelatinous plankton, such as salps, and spend a lot of their time feeding because this prey is not very nutritious. Strandings are often linked to plastic ingestion because of the similarity to jellyfish, their main prey species. The animal has a remarkable throat structure with backwards pointing barbs that holds jellyfish in place until it’s swallowed14.

Leatherbacks are regularly seen off the UK and Irish coasts and these North Atlantic animals have migrated from their nesting sites along the coast of northern South America and some Caribbean islands15. Females nest at these rookeries, often on a 2 yearly cycle, and animals follow one of three different migration paths based on directions taken by tracked animals. Animals from the North Atlantic population migrate northwards up to the coast of Nova Scotia in Canada, eastwards across the Atlantic towards the Azores and the coast of Africa or north eastwards up to the Atlantic coast of the island of Ireland, the Irish Sea and the Celtic Sea16, 17, where they find jellyfish swarms on which to feed18. They have been recorded as far north as Norway14 and can survive in these cold waters because they are able to generate their own body heat and being large, once warm they take longer to cool down.  They also have heat conservation and heat exchange mechanisms that enable them to feed actively in waters below 15oC, temperatures that would cause ‘cold stunning’ to other turtle species. Leatherbacks that are found further north tend to be larger than those off the Spanish and French coasts19, 20.

The continental shelf around Europe and off Canada are ideal sites for their main food, the barrel jellyfish, Rhizostoma pulmo, but they will feed on other gelatinous or jelly-like plankton. Barrel jellyfish can reach 90 cm in diameter and ‘blooms’, large congregations, of jellyfish can occur when conditions are ideal and food (plankton) is plentiful21.  A leatherback filmed off the Canadian coast22 was found to eat over 50% of their entire annual energy requirement in the 90 days that they spent in northern waters and this is likely to be the case off the UK in the Celtic and Irish seas. Leatherbacks are probably moving into high quality feeding areas where the location of a feeding ‘patch’ will provide them with lots of energy at low cost 23,  24. Unfortunately, some of their foraging areas in the Atlantic align with existing long line fisheries and this has an impact on the population, with estimates in the year 2000, of a leatherback bycatch of between 30,000 and 60,000 animals from both north and south Atlantic populations combined4, 25.

After feeding through the summer the leatherbacks head back south-westerly and generally follow a straight line migration path back to their nesting beaches26. Scientists have been able to track animals leaving nesting beaches and also animals that have been caught in fishing gear off the UK coast and found that when they’re feeding in northern waters they tend to stay close to the surface, feeding in localised patches, suggesting feeding in jellyfish swarms in the surface waters21, 27, 28, 29.  Tracking results indicate that when they travel to and from their nesting beaches they swim much faster and tend to be more prepared to undertake deeper dives to find food29, 30.

How has this leatherback migration pattern developed? One suggestion is that leatherback hatchlings drift out of the gyre, get caught up in the North Atlantic current and drift northwards during the so-called hatchling/juvenile ‘lost years’, finding areas where foraging is high-quality17. Having returned to nesting grounds, they are able to find these sites again as adults, using some form of navigation system15. Whatever the process they use, as long as we have our existing ocean currents, and large jellyfish blooms, we are lucky enough to provide an important feeding area for these migratory turtles, the most widely distributed reptile species in the world.

 

Published work referred to in this article:

1 Botterell ZLR, Penrose R, Witt MJ, Godley BJ (2020) Longterm 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

 2 Putman NF, Seney EE, Verley P, Shaver DJ, López-Castro MC, Cook M, Guzmán V and others (2020) Predicted distributions and abundances of the sea turtle ‘lost years’ in the western North Atlantic Ocean. Ecography 43:506-517

3 Monzo´n-Argu¨ello C., Dell’Amico F,. Morinie`re P,. Marco, A Lo´pez-Jurado L. F.,. Hays G C, Scott R, Marsh R and Lee P, (2012) Lost at sea: genetic, oceanographic and meteorological evidence for storm-forced dispersal Journal of the Royal Society Interface 9, 1725–1732

4 Lewison RL,. Freeman S A and. Crowder  L B (2004) Quantifying the effects of fisheries on threatened species: the impact of pelagic longlines on loggerhead and leatherback sea turtles Ecology Letters, 7: 221–231

5 Bellido J, Castillo J, Pinto F, Marti’n J, Mons J, Ba’ez J and Real R (2010) Differential geographical trends for loggerhead turtles stranding dead or alive along the Andalusian coast, southern Spain Journal of the Marine Biological Association of the United Kingdom, 90(2), 225–231.

6 Kettemer L, Biastoch A, Wagner P,. Coombs E J, Penrose R, and Scott R, (2022) Oceanic drivers of juvenile sea turtle strandings in the UK Endangered Species Research 48: 15–29

7 Darmon, G.; Schulz, M.; Matiddi, M.; Liria Loza, A.; Tom, J.; Camedda, A.; Chaieb, O.; El Hili, H.A.; Bradai, M.N.; Bray, L.; et al. (2022) Drivers of litter ingestion by sea turtles: Three decades of empirical data collected in Atlantic Europe and the Mediterranean. Marine Pollution Bulletin , 185, 114364

8 Sala B, Balasch, A, Eljarrat E, Cardona L (2021) First study on the presence of plastic additives in loggerhead sea turtles (Caretta caretta) from the Mediterranean Sea Environmental Pollution 283 117108

9 Nicolau, L., Ferreira, M., Santos, J. et al. (2016). Sea turtle strandings along the Portuguese mainland coast: spatio-temporal occurrence and main threats. Marine Biology 163, 21 https://doi.org/10.1007/s00227-015-2783-9

10 Garofalo L., Mastrogiacomo A., Casale P., Carlini R., Eleni C., Freggi D., Gelli D. Et al.  (2013). Genetic characterization of central Mediterranean stocks of the loggerhead turtle (Caretta caretta) using mitochondrial and nuclear markers, and conservation implications. Aquatic Conservation: Marine and Freshwater Ecosystems, 23: 868–884.

11 Chambault P, Gaspar P and Dell’Amico F (2021) Ecological Trap or Favorable Habitat? First Evidence That Immature Sea Turtles May Survive at Their Range-Limits in the North-East Atlantic. Frontiers in Marine Science. 8:736604. doi: 10.3389/fmars.2021.736604

12 Avens L and Amico FD (2018) Evaluating viability of sea turtle foraging populations at high latitudes: age and growth of juveniles along the French Atlantic coast. Endangered Species Research 37, 25–36

13 Clusa, M., Carreras, C., Pascual, M. et al. (2014). Fine-scale distribution of juvenile Atlantic and Mediterranean loggerhead turtles (Caretta caretta) in the Mediterranean Sea. Marine Biology 161, 509–519 https://doi.org/10.1007/s00227-013-2353-y

14 Beebee, T.J.C. & Griffiths, R.A. (2000) Amphibians and Reptiles. A Natural History of the British Herpetofauna. Harper Collins Publishers, London, UK

15 Dodge KL, Galuardi B, Lutcavage ME. (2015) Orientation behaviour of leatherback sea turtles within the North Atlantic subtropical gyre. Proceedings of the Royal Society B 282: 20143129. http://dx.doi.org/10.1098/rspb.2014.3129

16 Fossette S, Hobson V J.,  Girard C, Calmettes B , Gaspar P, Georges J-Y ,. Hays G C (2010) Spatio-temporal foraging patterns of a giant zooplanktivore, the leatherback turtle Journal of Marine Systems 81 225–234

17 Fossette S, Girard C, Lo´pez-Mendilaharsu M, Miller P, Domingo A, et al. (2010) Atlantic Leatherback Migratory Paths and Temporary Residence Areas. PLoS ONE 5(11): e13908. doi:10.1371/journal.pone.0013908

18 Bailey H, Fossette S, Bograd SJ, Shillinger GL, Swithenbank AM, et al. (2012) Movement Patterns for a Critically Endangered Species, the Leatherback Turtle (Dermochelys coriacea), Linked to Foraging Success and Population Status. PLoS ONE 7(5): e36401. doi:10.1371/journal.pone.0036401

19 Eckert S A. 2002 Distribution of juvenile leatherback sea turtle Dermochelys coriacea sightings Marine Ecology Progress Series 230: 289–293,

20 Witt MJ, Penrose R, Godley BJ (2006) Spatio-temporal patterns of juvenile marine turtle occurrence in waters of the European continental shelf. Marine Biology 151:873-885

21 Houghton J.D.R., Doyle T.K., Wilson M.W., Davenport J., Hays G.C. (2006) Jellyfish Aggregations and Leatherback Turtle Foraging Patterns in a Temperate Coastal Environment. Ecology.;87:1967–1972. doi: 10.1890/0012-9658(2006)87[1967:JAALTF]2.0.CO;2. – DOI – PubMed

22 Wallace, B.P., Zolkewitz, M. & James, M.C. (2018) Discrete, high-latitude foraging areas are important to energy budgets and population dynamics of migratory leatherback turtles. Science Reports 8, 11017. https://doi.org/10.1038/s41598-018-29106-1

23 Eckert Scott A. (2006) High-use oceanic areas for Atlantic leatherback sea turtles (Dermochelys coriacea) as identified using satellite telemetered location and dive information Marine Biology 149: 1257–1267

24 Chambault P, Roquet F, Benhamou S, Baudena A, Pauthenet E, de Thoisy B, et al. (2017). The Gulf Stream frontal system: A key oceanographic feature in the habitat selection of the leatherback turtle? Deep Sea Research Part I: Oceanographic Research Papers, 123: 35–47.

25 Fossette S, Witt, M. J.  et al. (2014) Pan-Atlantic analysis of the overlap of a highly migratory species, the leatherback turtle, with pelagic longline fisheries. Proceedings of the Royal Society B 281: 20133065. http://dx.doi.org/10.1098/rspb.2013.3065

26 Dodge KL, Galuardi B, Lutcavage ME. (2015) Orientation behaviour of leatherback sea turtles within the North Atlantic subtropical gyre. Proceedings of the Royal Society B 282: 20143129. http://dx.doi.org/10.1098/rspb.2014.3129

27 Doyle TK, Houghton, JD O’Súilleabháin, PF Hobson, VJ Marnell, F Davenport, J Hays, GC and Hobson V (2008) Leatherback turtles satellite-tagged in European waters Endangered Species Research: 4, Pages: 23 – 31,

28 Hays GC Farquhar MR, Luschi P, Steven L.H., Tierney T,. Thys M (2009) Vertical niche overlap by two ocean giants with similar diets: Ocean sunfish and leatherback turtles Journal of Experimental Marine Biology and Ecology 370 134–143

29 Dodge KL, Galuardi B, Miller TJ, Lutcavage ME (2014) Leatherback Turtle Movements, Dive Behavior, and Habitat Characteristics in Ecoregions of the Northwest Atlantic Ocean. PLoS ONE 9(3): e91726. doi:10.1371/journal.pone.0091726

30 Hays, G.C. ; Houghton, J; Myers, A.E. (2004) Endanqered species – Pan-Atlantic leatherback turtle movements. Nature. 429(6991). pp. 522-522

 

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

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Roger Downie, Froglife and University of Glasgow

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

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

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

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

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

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

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

References

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

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

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

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

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

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

Croaking Science-The Cane Toad: a cautionary tale

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Roger Downie, University of Glasgow and Froglife

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

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

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

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

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

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

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

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

 

References

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

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

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

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

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

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

Croaking Science: 2023 so far- what have we learned from the Dragon Finder App?

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As we fast approach the spring and our amphibians and reptiles begin to stir after their winter period of relative dormancy (known as brumation) we can expect sightings to increase in frequency. Whilst the occasional pioneering common lizard (Zootoca vivipara) or adder (Vipera berus) will emerge from their hibernacula to bask in winter sun, it’s the UK’s amphibians that bring the most herptile activity to this time of the year. This is reflected in the sightings that have been reported to Froglife’s Dragon Finder App so far in 2023.

At the time of writing (mid-February 2023), we’ve verified 42 reports submitted to the App; 24 sightings of common frogs (Rana temporaria), 6 encounters with common toads (Bufo bufo), 8 palmate newt sightings (Lissotriton helveticus), 2 smooth newt (Lissotriton vulgaris) sightings and 1 sighting of a great-crested newt (Triturus cristatus) and an alpine newt (Ichthyosaura alpestris) respectively.

All this amphibian action heralds the commencement of their breeding season. Common frogs lead the charge; the earliest report of frogspawn this year came to us from the Isles of Scilly, 45km south-west of mainland Cornwall, reported to us on the 9th January yet seen on Christmas Eve! UK common frogs spawn earliest here due to the archipelago’s unique climate – the moderating oceanic influence on which means that winters are warmer there than anywhere else in the UK and consequently snow and frost (potentially detrimental to spawn) are rare. We’ve received a total of 11 frogspawn reports so far in 2023, with the majority of these coming from Devon & Cornwall, reflecting the relatively warm winters experienced by the southwest more broadly. We’re now looking forward to witnessing reports of frogspawn slowly popping up in increasingly northerly and easterly locations as we pass through February and into March and April.

We’ve received 6 reports of common toads, but only one of common toad spawn, reported from Devon. Interestingly, the Dragon Finder App user that made this sighting was also able to spot a number of instances of a frog and toad engaged with one-another in ‘amplexus’, the act of the male using rough nuptial or ‘thumb’ pads to clasp onto the female whilst she deposits spawn. Common toads often begin to migrate to their ancestral breeding ponds from February, waiting for a comparatively warm and wet evening to do so.

Therefore, be sure to keep a keen eye out for reptiles and amphibians as the winter draws to a close and make sure to report your sightings through our free Dragon Finder App – the data we receive provides a wonderful insight into what our species are up to, as well as when and where this activity is occurring. Happy spotting!

Croaking Science: How glass frogs make themselves (almost) invisible

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Written by Roger Downie

Froglife and University of Glasgow

Back in July 2020, Isabel Byrne, Chris Pollock and I wrote a Croaking Science article that described the Centrolenidae, a neotropical family of 158 species known as glass frogs because of their transparency. In that article, we focused on reproduction in glass frogs. Here I discuss new work on their transparency and its contribution to their survival.

The importance to animals of body surface colours and patterns has long been studied. A key work is Hugh Cott’s book Adaptive Coloration in Animals (1940). Broadly, animals have evolved two different strategies: a) aposematic coloration, where they possess some protection, such as toxicity, and advertise this by being conspicuously coloured and patterned: in amphibians, poison-arrow frogs are an obvious example; b) cryptic coloration, where colours and patterns in some way blend with the background, making the animal difficult to detect: such methods of camouflage may match the background, or disrupt edges, or mimic background features. Cott undertook his doctoral research while lecturing at the University of Glasgow and was supervised by John Graham Kerr, the regius professor of Zoology who had developed an interest in the military uses of camouflage during World War 1. Cott’s thesis (1938) was titled The problem of adaptive coloration with special relevance to the Anura, and he moved to the University of Cambridge soon after completing it. Both he and Kerr were frustrated by the military authorities being unwilling to accept scientific advice on camouflage during both World Wars.

Transparency as a means of camouflage is fairly common in aquatic habitats, but is rare on land. For vertebrates, the red coloration of the haemoglobin in blood is a particular problem. In water, ice fish and eel larvae avoid this problem by having no red blood cells. In glass frogs, new research by Taboada et al. (2022) demonstrates a different strategy: when at rest and requiring concealment from predators, they hide their red blood cells.  

Glass frogs have highly transparent muscles and ventral skin, and the major internal organs: heart, liver and digestive organs, lie within mirrored sacs containing reflective guanine crystals which reflect the incident light. However, when frogs are active, their blood vessels are easily visible because of the circulating red blood cells. Taboada and colleagues compared active, awake glass frogs with individuals asleep and resting on leaves. They found that asleep frogs transmitted 34-61% more light than active individuals, making them more transparent, and that red blood cells were essentially absent from most of the circulatory system when the frogs were asleep. To find where the red cells were, they had to use the technique of Photo-acoustic microscopy, which can penetrate into solid tissue and visualise its contents. They found that the red cells were located in extensible sinuses in the liver, increasing liver volume by 40%. The transition from asleep to active in terms of red cell distribution took about 60 minutes. Measurements of the oxygen content of the blood showed that this decreased by 31% during sleep, suggesting a possible negative aspect of the red cell hiding process. The research team carried out comparative measurements on three other kinds of arboreal frog: none of them showed the transparency found in glass frogs, or the concealment of red blood cells when at rest. The authors speculate that the mechanism underlying red cell hiding in glass frogs may exploit a widespread ability in frogs, where other species have been shown to regulate respiration by temporary storage of red cells in the liver.

In another report, Barnett et al. (2020) question the use of the word ‘transparency’ as applied to glass frogs, since their dorsal green pigmentation renders them ‘translucent’, rather than transparent. Barnett and colleagues showed that translucent model frogs offered protection against avian predators and that translucency made detection of individuals slower. 

This work is a reminder of the many ways in which the physiology of amphibians is unusual, such as the ability of some species to survive freezing, helping them to survive in a changing world.

Acknowledgement

Thanks to Malcolm Kennedy for drawing my attention to the Taboada et al. paper.

References

Barnett, J.B. et al. (2020). Imperfect transparency and camouflage in glass frogs. PNAS 117, 12885-12890.

Byrne, I., Pollock, C. and Downie, J.R. (2020). See-through frogs are worth a look. Froglife eNewsletter Croaking Science July 2020.

Taboada, C. et al. (2022). Glass frogs conceal blood in their liver to maintain transparency. Science 378, 1315-1320.

Croaking Science: Pond Creation Works

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Written by Roger Downie, Froglife and University of Glasgow

 

Froglife’s vision is of a world in which reptile and amphibian populations are flourishing as part of healthy ecosystems. One of the ways in which we work towards this overall aim is by transforming landscapes: increasing the availability of freshwater and terrestrial habitat suitable for amphibians and reptiles. Our ‘living water’ series of projects has addressed this by creating and repairing ponds around the UK. Producing habitats is the first part of the task, but we also need to assess how well these habitats perform in helping populations to grow. Our strategy commits us to evaluating project sites for up to 10 years after completion, with some remedial work possible if damage, such as vandalism is found.

What does the scientific literature tell us about the success of created ponds? Smith et al. (2020) reviewed 28 published studies from around the world, and concluded that pond creation is an effective, beneficial conservation action. Some of the studies concerned small numbers of ponds over a fairly short time, but others were much larger in scope e.g. a Danish study of 3446 ponds over 11 years. Now comes a major study from the Swiss canton of Aargau (Moor et al., 2022) published in the high-profile journal Proceedings of the National Academy of Sciences, USA (PNAS).

Aargau, in the north of the country on the border with Germany, is one of the most densely populated and least hilly parts of Switzerland. Although about one-third wooded, it includes many small towns and an extensive road network with much agricultural land. Following concern about 30 years ago over the decline in amphibian populations (around the time of the creation of IUCN’s Declining Amphibian Populations Taskforce- DAPTF), a pond creation programme began in 1991 and continues. Moor et al. have analysed up to 20 years of data from 856 ponds, 422 of them constructed as part of the conservation programme. The canton is home to 12 species of pond-breeding amphibians (eight anurans and four newts). The authors note that these species differ in their characteristics: life history, habitat preference, and dispersal ability.

Across the whole canton, the number of ponds occupied by amphibians increased over the period 1999-2019 for 10 of the 12 species: the number remained pretty constant for the midwife toad and declined significantly only for the natterjack toad. Results differed between regions: essentially, the more ponds constructed in a region, the more metapopulations increased and the fewer declined (‘metapopulation’ here meaning the number of ponds occupied per species). The authors detected three mechanisms at play in the effects of new ponds on metapopulation sizes. First, the increased number of ponds increases breeding habitat, particularly benefitting mobile generalist species like the common toad. Second, the constant addition of new early succession stage ponds benefits pioneer species such as natterjack toads: they prefer shallow ponds with short hydroperiods, lacking vegetation and predators; it is likely that most of the constructed ponds lacked these features, and that older ponds were losing the features suitable for natterjacks, hence this species was the only one to show a decline across the canton. Third, increased pond density enhances connectivity, a particular benefit for species with low dispersal ability, like newts.

Although new ponds were rapidly colonised by several species, populations did not always persist. This could be the result of several factors, such as eventual colonisation by predators not initially present, or successional changes that made the new ponds less suitable for early colonisers. The only species where persistence probability was higher in new than in old ponds was the tree-frog, Hyla arborea: the reasons for this are not clear, but the result was a particularly sharp increase in metapopulation size across the study from <25 to over 75 sites. Several factors mattered for the success of new ponds: surface area and shape (most often, large pond size led to more species, but one species, the yellow-bellied toad Bombina variegata preferred smaller ponds; the type of surrounding habitat (some species had positive associations with surrounding forest, but natterjack toads and smooth newts preferred less forested surroundings); roads generally had negative effects on dispersal and colonisation.

The authors made the ‘encouraging conclusion’ that ‘no effort in pond construction is really wasted’. The continuous creation of new ponds helped amphibian populations to recover despite the persistence of threats like increasing urbanisation and associated roads, the presence of non-native fish and pathogens, and the effects of agrichemicals. However, there are caveats related to the particular circumstances of this study. The canton of Aargau is 37% forested, providing abundant habitat for amphibian dispersal and shelter; contrast this with the UK at 13% (England even less at 10%). The range of species in Aargau is quite large, with their range of needs being diverse enough that different kinds of ponds can be suitable for some if not all. The authors comment particularly that pond creation in the tropics may have limited value, since so many species are not pond breeders.

Finally, the authors note that it was crucial to the success reported in their study that the authorities in Aargau responded quickly to the evidence of amphibian declines by enabling a long-term pond creation programme with associated monitoring. Froglife has often been able to find funding for pond creation projects in particular areas, but funding the monitoring has been more difficult, and persuading authorities (and funders) to think of pond creation as long-term commitment is more difficult still.

References

Moor, H. et al. (2022). Bending the curve: simple but massive conservation action leads to landscape-scale recovery of amphibians. PNAS 119, e2123070119.

Smith, R.K. et al. (2020). Amphibian Conservation. Ps 9-64, in: Sutherland, W.J. et al. (eds.) What works in conservation 2020. Open Book Publishers, Cambridge, UK.