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Croaking Science: See-through frogs are worth a look

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Glass frogs comprise a family (Centrolenidae) of 158 species found in the forests of the neotropics: Central America and northern South America. They get their name from the transparency of their belly skin, which allows the internal organs to be easily seen. They are adapted to life in the trees, possessing pads on the tips of their digits that allow them to adhere to leaves. These structures appear to have evolved independently in several lineages of frogs, since molecular phylogenetic results show that the main families where these pads occur (Hylidae, Rhacophoridae, Centrolenidae) are not closely related.

One of the special features of glass frogs is their mode of reproduction. Clutches of eggs, as flat round sheets, each egg encased in jelly, are laid on the surfaces of leaves overhanging streams. Once the eggs have developed into larvae, they hatch and fall into the stream below, often from a considerable height. Glass frogs are divided into two main sub-families: the Centroleninae (121 species) which lay on the upper sides of leaves and then leave the eggs to develop on their own; and the Hyalinobatrachinae (35 species) which lay their eggs on the lower sides of leaves; in these species, the father cares for the eggs, sometimes up till the point of hatching.

Figure 1: Several egg clutches on a single leaf

We studied the glass frog Hyalinobatrachium orientale which has distinct populations in northern Venezuela and northeast Tobago: this distribution is a bit of a puzzle. Northeast Tobago is quite distant from Venezuela and between these two locations is the large island of Trinidad, which has abundant forests, but no glass frogs. Walking along the forest streams of Tobago at night, once the rainy season (June to December) has started, you soon hear the high-pitched peeping of male glass frogs, located on the huge leaves of Heliconia bihai that overhang the water. With the aid of a good torch, you can locate the calling frogs; often, near them, you can spot the little patches of eggs. If you are lucky, you may locate a mating pair. We observed the behaviour of a mating pair. It took them about four hours to complete their clutch of around 30 eggs, laid as a spiral pattern, starting at the centre, with the pair turning as they proceeded. Once egg-laying was complete, the female departed, but the male stayed close to the clutch. Often, when searching for egg clutches, we found the father sitting on top of his eggs. We also found that some fathers, presumably good quality males, were looking after more than one egg clutch at a time. These are at different stages of development, so clearly produced on different nights. It is not entirely clear what functions male egg attendance performs, particularly given that it is not constant. However, observers have seen males driving away egg predators such as wasps and ants; it is also likely that males keep the eggs hydrated by reducing evaporation, simply by sitting on them, or by emptying their bladders over the eggs (this is established in some cases of frog parental care). But this raises another mystery. If paternal care is helpful to incubation success in the Hyalinobatrachinae, why does it not occur in other glass frogs, especially when they lay their eggs on leaf upper surfaces, where you would guess that desiccation and predation would be higher risks.

In the Tobago glass frog, hatching occurs around nine days after laying, although the actual time is variable, allowing tadpoles to be earlier or later stages of development when entering the water. Such variability may be quite common in frog development and represents a trade-off. Early hatchers are less well developed and more vulnerable when they enter the water; but it may be better to risk this than to be predated while still in the nest. It therefore pays the developing larvae to monitor conditions: if the father has deserted his clutch, or hot sun and no rain are risking desiccation, better to hatch early and hope for a stream with few predators.

Figure 2: Metamorphosing glass frog tadpole on a leaf; with pen for scale

The streams where glass frog tadpoles are found are fast-flowing when it rains, and are heavily populated with predatory fish and crustaceans. They are also shaded, making plant productivity low. As a consequence, glass frog tadpoles spend much of their time hidden under rocks, reducing the risks of predation and of being swept away by currents (unlike the tadpoles of some species that inhabit fast streams, glass frog tadpoles lack the kind of suctorial mouthparts that can help cling on to rocks). The tadpoles have long muscular tails, indicating an ability to move rapidly, and are relatively unpigmented, associated with a concealed lifestyle. Their behaviour limits foraging opportunities, so growth is slow. Glass frog tadpoles can take a year to reach metamorphosis, very slow by tropical frog standards, where many species reach that stage in a few weeks. We have been able to locate metamorphosing glass frogs near the edges of streams. They climb up on to the upper surfaces of leaves close to the ground, and take about four days to complete the process, reducing their tail to a stump. To our surprise, we found that they do not remain in one place through this process, but occasionally move around, possibly to confuse potential predators.

The transparency of glass frogs has long puzzled biologists. Recently, a research team from Bristol, Canada and Ecuador has tested an explanation. Their evidence suggests that it is not so much transparency that matters, but translucence. When a glass frog is at rest with its limbs tucked in, the translucence of the limbs blurs the edges of the body, and makes detection by predators more difficult.

Further reading

Barnett et al. Imperfect transparency and camouflage in glass frogs. PNAS (2020).

Byrne et al. The behaviour of recently hatched Tobago glass frog tadpoles. Herpetological Bulletin 144, 1-4 (2018).

Byrne et al. Observations of metamorphosing tadpoles of the Tobago glass frog. Phyllomedusa (in press) (2020).

Delia et al. Glass frog embryos hatch early after parental desertion. Proceedings of the Royal Society B 281, 2013-2037 (2014).

Downie et al. The tadpole of the glass frog Hyalinobatrachium orientale from Tobago. Herpetological Bulletin 131, 19-21 (2015).

Nokhbatolfoghahai et al. Oviposition and development in the glass frog Hyalinobatrachium orientale. Phyllomedusa 14, 3-17 (2015).

Contributing authors : Roger Downie, Isabel Byrne, Chris Pollock.

Help Froglife secure funds to improve Cowdenbeath Grasslands (Fife, Scotland)

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Froglife is fundraising to restore and create standing water habitats (ponds) at Cowdenbeath Grasslands.  Cowdenbeath Grassland is a large, predominantly grassland site with numerous over-grown ponds and pools, these will be restored to provide vital, open water for amphibians, reptiles, aquatic invertebrates, wading birds, aquatic plants and small mammals such as water voles, bats and hedgehogs.

Our ambition is to restore four non-functioning ponds and two scrapes and to create thirty new ponds and sixteen scrapes.  Additionally, we will create basking banks, plant a range of native scrub/tree species and hawthorn planting to improve connectivity and provide sheltering habitat.

This project forms part of Froglife’s Living Water programme that operates across the UK creating and restoring amphibian and reptile habitats.  In order to secure the grant we need to show that we have support for our Living Water programme.  Please support us through our social media feeds or by emailing Info@froglife.org.

  • Site Overview
  • Overgrown Pond

Croaking Science: Miniaturisation in amphibians

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Miniaturisation in amphibians – evolutionary specialisation

Amphibians exhibit vast ranges in body size ranging from just 7 mm long in the smallest known species (Paedophryne amanuensis) to 33 cm in the largest frog (Conraua goliath), which represents a 250 fold increase in size. Different body sizes come with distinct advantages and disadvantages. Large amphibians have fewer predators, a lower metabolic rate, and they can more easily maintain their temperature and hydration than small amphibians. Smaller amphibians, although being more prone to predation, are better equipped to hide more easily, exploit alternative food sources, use physically smaller niches, and attain reproductive ability at an earlier age (Leavy & Heald, 2015). By being very small, individuals are able to fully utilise habitat patches and consume the smallest prey, which are also the most numerous. However, living at such small sizes puts constraints on biological processes and as a result, miniature amphibians have evolved unique features to enable them to function effectively. Many miniaturised frogs have a reduced number of skull elements, fewer digits on their limbs, fewer vertebrae and a reduction in webbing on the feet. Many miniature frogs resemble juveniles and retain of their features. Indeed, the frog genus Paedophryne, discovered in 2010 from Papua New Guinea, means ‘juvenile form’ and contains some of the world’s smallest frogs measuring just 10.1–11.3 mm (Kraus, 2010). Most miniature frogs from a range of families are usually found in wet tropical forests and live on the forest floor under leaf litter feeding on minute termites, small ants and similar species (Almeida-Santos et al., 2011).

Miniaturisation within the amphibians has evolved independently several times and in many species adults only grow to 20 mm in length. For example, miniaturisation has evolved 8 times in the puddle frogs (genus Phrynobatrachus) of Sub-Saharan Africa (Zimkus et al., 2012). The unusual reproductive mode of many tropical amphibian species has promoted the evolution of small body size. Miniature amphibian species are usually fully terrestrial with individuals laying a small number of relatively large eggs within the leaf litter which hatch into fully metamorphosed juveniles. For example, the Strabomantid frogs of the Peruvian Andes are fully terrestrial and do not require water to breed. This means that individuals do not need to undergo breeding migrations to water bodies. This promotes the evolution of small body size since individuals are able to occupy very small home ranges (Lehr & Catenazzi, 2009). In addition, the unique physiology of amphibians has allowed the evolution of small body sizes even at high altitudes, especially in the tropics. In many groups of vertebrates there is a relationship between body size and temperature (Bergmann’s Rule) where individuals at higher altitudes or latitudes attain larger body sizes, often as a protection from colder temperatures. However, due to their physiology which allows them to alter their metabolism for activity at lower temperatures, small amphibian species are able to occupy high altitudes. This removes the constraint of temperature on the evolution of body size and allows species to occupy a greater range of ecological niches even at high altitudes.

Figure 1. The pumpkin toadlet (Brachycephalus ephippium) from the Atlantic Forest of southern Brazil is one of the smallest known frog species.

In recent years our knowledge and understanding of miniature amphibians has increased due to discoveries of new species and research into their unique ecology. Frogs within the genus Brachycephalus are all endemic to the Atlantic Forest in Brazil (Figure 1). There are currently 35 known species (Frost, 2018) and 19 of these have been discovered in the past six years. Also known as flea-frogs, these poorly understood species inhabit the moist tropical forest floor within this biodiverse hotspot. Growing to less than 20 mm in length, Brachycephalus didactylus, occurs only in Rio de Janeiro state where it is threatened by encroaching human developments and habitat fragmentation. During the breeding season, females lay just two eggs, probably laying each on a different day (Almeida-Santos et al., 2011). Each egg is laid amongst the leaf litter where it undergoes complete development into a fully metamorphosed juvenile frog with no free-swimming larval stage. The eggs of this species are also relatively large, allowing newly metamorphosed juveniles to emerge at a larger size which offers greater protection from predators.

Figure 2. The miniature Malabar night frog, Nyctibatrachus major, from the Western Ghats, India.

Night frogs, genus Nyctibatrachus, live in close association with mountain streams or marshes in forests of the Western Ghats, India. Species within this genus are extremely small ranging 10 – 77 mm. In 2017 Garg et al. (2017) discovered seven new miniaturised night frog species, four of which are among the smallest frogs in India measuring just 12.2 to 15.4 mm in length. All members of the new species were found under leaf litter or in wet grass near to streams or waterfalls. One male was found clasping a clutch of 10 eggs (Garg et al., 2017). The authors believe that more surveys will discover further new species which will also aid our understanding about the evolutionary advantages of miniaturisation and adaptation to terrestrial life within these and other miniature frogs

 

References

Almeida-Santos, M., Siqueira, C.C., Van Sluys, M. & Rocha, C.F.D. (2011) Ecology of the Brazilian flea frog Brachycephalus didactylus (Terrarana: Brachycephalidae). Journal of Herpetology, 45 (2): 251-255.

Frost, D.R. (2018) Amphibian Species of the World: an Online Reference. Version 6.0 (09 March 2018). Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/index.html. American Museum of Natural History, New York, USA.

Garg, S., Suyesh, R., Sukesan, S. & Biju, S.D. (2017) Seven new species of night frogs (Anura,

Nyctibatrachidae) from the Western Ghats biodiversity hotspot of India, with remarkably high diversity of diminutive forms. PeerJ, 5:e3007; DOI 10.7717/peerj.3007.

Kraus, F. (2010) New genus of diminutive microhylid frogs from Papua New Guinea. ZooKeys 48: 39-59.

Leavy, D.L. & Heald, R. (2015) Biological Scaling Problems and Solutions in Amphibians. In: Additional Perspectives on Size Control in Biology: From Organelles to Organisms. Eds R. Heald, I.K. Hariharan and D.B. Wake. Cold Spring Harbor Laboratory Press, doi: 10.1101/cshperspect.a019166.

Lehr, E. & Catenazzi, A. (2009) A new species of minute Noblella (Anura: Strabomantidae) from Southern Peru: the smallest frog of the Andes. Copeia, 2009 (1): 148–156.

Zimkus, B.M., Lawson, L., Loader, S.P. & Hanken, J. (2012) Terrestrialization, miniaturization and rates of diversification in African puddle frogs (Anura: Phrynobatrachidae). PLoS ONE, 7 (4): e35118. doi:10.1371/journal.pone.0035118.

Amphibian and reptile declines – UK perspective

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Amphibian and reptile declines – UK perspective

The UK supports a range of iconic mammal species including hedgehogs, water voles, badgers and several bat species. However, in recent years, research by various conservation bodies has found startling declines in many of these species. Research led by the Wildlife Trusts indicates there has been a 30% decline in water vole populations since 2006, which represents an approximately 3% loss in populations per year1. Of more concern, is the dramatic decline in the hedgehog which is estimated to have declined by 66% over the past 13 years (5% decline per year)2. Increased agricultural intensification, use of pesticides, habitat loss and fragmentation have all attributed to the decline which has been reported by the British Trust for Ornithology2. In addition, several of the UK’s iconic bat species are in decline, as reported by Bat Conservation, including the brown long-eared bat which has declined by 31.3% since 1999 (2.2%  decline per year)3.

Figure 1: Breeding common toads (Photo Credit- Silviu Petrovan)

Amphibians and reptiles are generally less understood by the public who often perceive these species differently to iconic mammals. However, many populations of our once common amphibian species are in decline. Common frog, common toad and natterjack toad populations have been reported as being in decline since the 1970s4,5. Recent research in 2016 by Froglife and the University of Zurich has shown that common toad populations have declined across the UK by 68% over the past 30 years, which approximates to a 2.26 % decline per year. This value is comparable to the declines in many of our iconic mammal species and highlights that significant declines may be widespread across our native fauna. The reasons for the decline in the common toad are similar to those affecting hedgehogs including habitat loss and fragmentation, pollution and climate change. The adder, being the only native venomous snake in the UK, often has a poor perception from the public. However research by Natural England and Froglife in 2002 has indicated significant population declines in the adder, especially from the Midlands6. In this study one third of adder populations were estimated to consist of less than 10 individuals which puts them at high risk of extinction. These declines are likely to be attributable to poor habitat management including agricultural intensification as well as public pressure (recreation) and persecution6. At Froglife we aim to raise awareness of the declines in our native amphibian and reptile species, especially those which were once common. We wish to highlight that widespread amphibian and reptile species, such as the common toad, are suffering declines equivalent to iconic mammals such as the water vole and hedgehog. At Froglife we carry out extensive practical habitat creation and restoration each year, both locally and nationally, with the aim of improving environmental conditions for our native amphibians and reptiles and aiding to conserve populations of our valuable herpetofauna.

 

References

1Wildlife Trusts (2018). http://www.wildlifetrusts.org/news/2018/02/26/new-report-points-30-decline-water-vole-distribution. Accessed on 13th March 2018.

2BTO (2018) https://www.bto.org/science/monitoring/hedgehogs. Accessed on 13th March 2018.

3Bat Conservation (2018) http://www.bats.org.uk/pages/species_population_trends.html. Accessed on 13th March 2018.

4Beebee, T.J.C. (1973) Observations concerning the decline of the British Amphibia. Biological Conservation, 5 (1): 20-24.

5Beebee, T.J.C. (1977) Environmental change as a cause of natterjack toad (Bufo calamita) declines in Britain. Biological Conservation, 11: 87-102.

6Baker, J.R., Suckling, J. & Carey, R. (2004) Status of the adder Vipera berus and slow-worm Anguis fragilis in England. English Nature Research Report 546, English Nature, Peterborough, UK.

Croaking Science: Amphibians that change colour

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Amphibians that change colour – dichromatism in frogs and salamanders

Size dimorphism, where one sex is larger than the other, is common in amphibians and occurs in approximately 90% of frog and toad families. However, sexual dichromatism, where one sex is a different colour to the other has only been documented in approximately 122 (17%) of frog and toad species. There are two types of dichromatism: dynamic dichromatism, where males undergo a rapid colour change prior to the breeding season; and ontogenetic dichromatism where one sex remains a different colour the entire of its life once it has matured (Bell & Zamudio, 2012). Dynamic dichromatism occurs in 31 frog species but is probably under-recorded due to its ephemeral nature of only occurring for short periods around breeding. Ontogenetic dichromatism appears more common, being documented from 91 anuran species. However, our understanding of the mechanisms behind colour change in frogs is still limiting.

The Wood Frog (Rana sylvatica) exhibits ontogenetic dichromatism with males being tan or dark brown whereas females tend to be redder in colour (Figure 1). Previous experiments have shown that males are attracted to red females but are ambivalent towards darker coloured females. Being able to readily distinguish the sexes is likely to be important for Wood Frog males, as the breeding season may last only 1–3 days in early spring (March and April) and high male-male competition often results in only a small percentage of males succeeding in mating. Research by Lambert et al. (2017) has shown that sexual dichromatism in Wood Frogs is absent immediately after metamorphosis but develops and persists through the second spring and summer. Unlike some frog species, where the body colour change is almost instantaneous and lasts only a few days, the colouration alteration in Wood Frogs takes weeks to develop and lasts for several weeks after the breeding season. Currently, it is unclear which environmental conditions (e.g., light, temperature, food, etc.) influence the colour change after hibernation. It is also unclear why the frogs remain with colour dichromatism for extended periods when breeding only lasts a few days. It seems likely that the colour change has evolved as a result of both sexual and natural selection. Females which are redder in colouration are more easily identifiable by males during the short breeding season. In addition, the colour changes may provide the different sexes protection from predation. Redder females are more camouflaged on the forest floor during terrestrial migration and may benefit from reduced predation. In contrast, the dark tan or brown males have greater camouflage whilst aggregating around ponds when they are at greatest risk from predators. Therefore the differences in colour between males and females in Wood Frogs may offer benefits for reproduction and survival.

Figure 1. Female (left) and male (right) Wood Frogs demonstrating colour dichromatism. (Photo Credit: Lindsey Swierk)

Sexual dichromatism is much rarer in newts and salamanders and has only been reported from a few species. The development of graphic software has enabled researchers to examine in more detail the dorsal patterning in relation to colour quality patterns such as hue, sat­uration, brightness, or quantity of each spot on the dorsal and ventral sides. Using such techniques in salamanders have revealed sexual dichromatism which was previously unnoticed to the naked eye.  For example, in adult Red-spotted Newts (Notophthalamus viridescens) image analysis software was used to demonstrate that males have more intensely red dorsal spots compared to females. Recent work by Balagova and Uhrin (2015) on the Fire Salamander (Salamandra salamandra) has shown that males have a greater amount of yellow dorsal patterns compared to females (Figure 2). Since the reproductive strategy involves female choice, the authors hypothesise that females may be able to select males based on their dorsal patterns. In this species the dorsal patterns indicate toxicity to predators so a brighter individual with a greater amount of patterning may be more effective at deterring predators. The authors suggest that females may select males with brighter and a greater amount of patterning since they offer greater protection from predators and their offspring will inherit this characteristic. In addition, females may have a greater proportion of black colour to absorb more heat which would result in faster egg development.

Figure 2. Male Fire Salamanders (Salamandra salamandra) have a greater proportion of yellow markings compared to females. (Photo Credit: Adobe stock)

Overall, recent research suggests that we are gaining in understanding of the distribution of sexual dichromatism among amphibian species, but that we still know very little about its function. In addition, dichromatism in amphibians offers benefits for investigating the relative roles of natural selection and sexual selection in the evolution and origins of sexual dichromatism and its significance for a range of amphibian species.

References

Bell, R.C. & Zamudio, K.R. (2012) Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity. Proc. R. Soc. B. 279 (4): 4687-4693.

Lambert, M.R., Carlson, B.E., Smylie, M.S. & Swierk, L. (2017) Ontogeny of sexual dichromatism in the explosively breeding wood frog. Herpetological Conservation and Biology 12 (2):447-456.

Balogová, M. & Uhrin, M. (2015) Sex-biased dorsal spotted patterns in the fire salamander (Salamandra salamandra). Salamandra 51 (1): 12-18.

Croaking Science: The Problem of Data Deficiency in Amphibian Conservation

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The problem of Data Deficiency in amphibian conservation

There are currently 7737 recognised species of amphibian and new species are being added to the list each month. This is either due to new species discoveries or as a result of taxonomic revisions where a taxonomic split of one previously recognised species results in several new species. Each species is given an extinction risk by the International Union for the Conservation of Nature (IUCN) which ranges from Extinct through four threatened categories (Extinct in the Wild, Critically Endangered, Endangered and Vulnerable) to Near Threatened, Data Deficient and Not Evaluated (NE). Species with insufficient information available are classed as Data Deficient (DD). High profile vertebrate groups such as mammals and birds have near complete IUCN coverage with few DD species. However, within the amphibians there are many poorly understood species which has resulted in a relatively high proportion of species being classed as DD. The prevalence of DD and NE species is likely to remain high as further taxonomic revisions and species discoveries in remote parts of the globe continues. This is of concern since the IUCN Red List is used in a wide range of conservation decisions, policy making, conservation management decisions and research agendas (Howard & Bickford, 2014). There is pressing need to estimate the level of extinction of DD species for a greater understanding of a group’s overall extinction risk.

Over one third of amphibian species are classified with a threatened status while a quarter of all amphibian species are unable to be assessed by the IUCN and remain DD or NE. Attempts to directly address the problem of DD species are rare since there is not the time or resources to explore the remote parts of the globe where DD species often occur. However, Morias et al. (2013) examined geographical range with time since discovery in an attempt to predict the level of risk posed to DD species in Brazil. Morias et al. (2013) concluded that recently described DD species with a small geographical range have a higher extinction risk. This has proved a useful tool in local policy development for amphibians in Brazil. However, there is still a need to fully assess the level of extinction risk to DD amphibians globally.

In 2014 Howard and Bickford (2014) attempted to address the problem of DD amphibian species at a global scale. They took data for species that had been assigned an extinction category (other than DD) to fit a model relating extinction risk to life history traits (e.g. reproductive mode), environmental variables and habitat loss. They then used this model to predict the extinction risk to DD amphibians and determine whether DD species can be considered more or less at risk compared to fully assessed species. Howard and Bickford (2014) found that DD amphibians are, on average, likely to be more threatened by extinction than fully assessed species. Their model predicted that 63% of amphibians globally are likely to be threatened, compared to the current 32%. Amphibians are already acknowledged to be the most threatened vertebrate group and the findings from this research suggest that the overall level of extinction risk is higher than previously thought. Areas with most at-risk species are likely to be South America, Central Africa and Asia. In particular, amphibian species in Indo-Burma are poorly understood. This region contains many species with DD status, high level of threats to habitat (e.g. habitat loss and pollution) and high rates of species discovery. The annual rates of deforestation are the highest among all tropical regions and less than 10% of these forests have any form of conservation protection (Sodhi et al., 2010).

Figure 1. Anomaloglossus wothujav, a Data Deficient species from Venezuela, which is only known from one locality. (Photo © 2006 Patty Vela)

Overcoming the problems in species identification is a key issue in relation to identifying DD species. In tropical regions cryptic species complexes (i.e. those which look nearly identical) are relatively common making identification, taxonomy and subsequent assessment of level of extinction highly challenging. The genus of frogs belonging to Anomaloglossus are a highly cryptic species group with difficulties in identifying species (Figure 1). There are currently 26 known species, mainly endemic to the Guiana Shield region in South America. Many of these species appear to be restricted to just one or two mountain tops in the Pantepui region (Figure 2). However, others within the genus appear to have more broad distributions. Therefore identifying exact species range, and thus level of extinction risk is a conservation priority. In an attempt to gain a greater understanding of species distribution within the Anomaloglossus, Vacher et al. (2017) tested species boundaries using molecular, morphometric and bioacoustic data. Results from this study highlighted that previous research has greatly underestimated the number of species with the genus. For example, six formally recognised species were found to in fact be 18 species and further species remain to be discovered. Therefore developing effective methods for identifying species and their geographical distributions remains a challenge.

Figure 2. The high mountain peaks of the Pantepui in Surinam support a range of cryptic amphibian species.

Understanding Data Deficiency is of key importance in effective amphibian conservation. Where time and resources are limiting and field studies to determine species distributions are not possible, the use of modelling may be important in estimating the extinction risk facing species. Developing robust and effective conservation strategies is a high priority in protection of many of the world’s threatened amphibians.

 

References

Howard, S.D. & Bickford, D.P. (2014) Amphibians over the edge: silent extinction risk of Data Deficient species. Diversity and Distributions, 2014: 1-10.

Morias, A.R., Siquera, M.N., Lemes, P., Macial, N.M, De Marco, P., Jr & Brito, D. (2013) Unravelling the conservation status of Data Deficient species. Biological Conservation, 166: 98-102.

Sodhi, N.S., Posa, M.R.C., Lee, T.M., Bickford, D., Koh, L.P. & Brokk, B.W. (2010) The state and conservation of Southeast Asian biodiversity. Biodiversity and Conservation, 19: 317-328.

Vacher, J-P., Kok, P.J.R., Rodrigues, M.T., Lima, J.D., Lorenzini, A., Martinez, Q., Fallet, M., Courtois, E.A., Blanc, M., Gaucher, P., Dewynter, M., Jairam, R., Ouboter, P., Thébaud, C. & Fouquet, A. (2017) Cryptic diversity in Amazonian frogs: integrative taxonomy of the genus Anomaloglossus (Amphibia: Anura: Amromobatidae) reveals a unique case of diversification within the Guiana Shield. Molecular Phylogenetics and Evolution, 112: 158-173.