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Croaking Science: Miniaturisation in amphibians
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.
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.
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
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.
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.
Cold Weather Forecast
This weekend (17-18th March) another cold spell of weather has been forecast by the Met Office with further outbreaks of snow and widespread freezing conditions. By now, many common frogs, common toads as well as newts will have made their way to breeding ponds and are at risk from sudden periods of cold weather. Adults in ponds, as well as those migrating towards breeding areas, are prone to winterkill which has already caused a high incidence of mortality in common frogs this year. In addition, spawn laid by common frogs and toads is prone to freezing in hard frosts. Reptiles are at less of a risk since the majority have not yet emerged from hibernation and breeding does not commence until later in the year.
To help common frogs and toads during periods of cold weather there are a few actions that you can take. First, if you have a garden pond, periodically break any ice on the surface to promote oxygen exchange. This will allow amphibians to survive in the water beneath the ice. Second, you can try floating a small object e.g. tennis ball, in the water which prevents ice formation. However, this only works in moderate frosts and in severely cold weather, breaking the ice is the only option. Third, provide piles of leaves or areas of dense vegetation and scrub close to your garden pond as this will provide areas for amphibians to take refuge during periods of cold weather. If you have frog spawn, the upper portions may freeze, but the spawn which is underwater should survive. However, if you have a very small pond and/or it is shallow and prone to freezing throughout, you can temporarily place your frog spawn into a bucket of water and place in a garage, or similar place, out of the freezing conditions. Once the cold weather has passed, ensure that you return the spawn to the original place within the same pond to allow it to continue to develop.
NB: The majority of reptiles have not yet emerged from hibernation
Croaking Science: Amphibians and Climate Change
Amphibians and climate change
Over the past few decades rising global temperatures and associated climate change have been of increasing concern due to rises in atmospheric carbon dioxide and other greenhouse-gas emissions. Over the past century global temperatures have risen on average by 0.7°C and these have been greatest in the last few decades (IPCC, 2007). This has resulted in a range of global climatic changes which have had varied impacts on amphibian species. For example, several species of amphibian have become extinct in southeast Brazil due to the occurrence of frost, and the decline in several tropical amphibian species has been attributed to unusually dry conditions (Blaustein et al. 2010). In the UK an increase in the prevalence of mild and wet winters has negatively affected the common toad Bufo bufo (Reading, 2007) (Figure 1). Range shifts, where species are either forced to higher latitudes or altitudes are a particular problem for many species within Central and South America where there are a high number of range-restricted species. Here, temperatures are predicted to become hotter and drier and may result in species extinctions if there is no other suitable habitat available to expand into. Other potential direct impacts of climate change on amphibians are decreased survival such as that reported in the common toad (Reading, 2007), changes in developmental rates of eggs and larvae, and changes in behaviour of adults and larvae (Blaustein et al. 2010).
Changes in the timing, or phenology, of amphibian breeding have been intensively studied in a range of species across the globe. Within the UK, many studies have shown a trend for earlier breeding in the common frog Rana temporaria, common toad Bufo bufo, natterjack toad Epidalea calamita and two species of newts (smooth newt Lissotriton vulgaris and great crested newt Triturus cristatus). However, findings from several independent studies reveal that the impacts of a changing climate on breeding times may be more complex. For example, Beebee (2002) reported results of thirty years of studying populations of the common frog and found no trend for earlier breeding. Beebee (2002) reported that the two explosive breeding amphibians in the UK, common frog and common toad, showed relatively minimal changes in breeding date. However, the protracted breeders, natterjack toad and newt species showed significantly earlier breeding times (Figure 2). Beebee (2002) predicted that this could have important community effects. Earlier arrival of newts at ponds may increase predation on common frog spawn and this in turn may result in local population declines of the common frog. Similar findings have been found by Reading (1998) who found no evidence of earlier breeding in a population of the common toad. More recent studies have concluded contrasting results. For example, Scott et al. (2008) studied the phenology of the common frog and did find a trend for earlier breeding. However, the authors noted no trend for earlier hatching dates. In addition, Carroll et al. (2009) reported findings from a study from the UK Phenology Network which collected nearly 70,000 records of the first spawn dates of the common frog across the UK between 1998 and 2007. On average, the pattern of spawning followed a consistent pattern across the UK with first spawning dates earliest in the south west and progressively later in the north and east. Although there was variation in spawning dates between years, on average there was a trend for the common frog to breed 10 days earlier at the end of the period. In a more recent study carried out by Loman (2016) in Sweden, local variation in pond conditions was of key importance in determining spawning date of the common frog and in particular pond water temperature, as oppose to air temperature. In addition, Loman (2016) found that the number of frogs breeding at a pond had a significant impact on breeding date. Common frogs spawned earlier in ponds with a higher, rather than lower, number of breeding pairs. For example, a pond with only five breeding individuals spawned 7.2 days later than ponds with 500 individuals (Loman, 2016). Therefore population sizes, as well as climatic changes, may need to be considered when investigating the potential impacts on amphibian breeding phenology.
In addition to the above direct effects of climate change, there are a number of potential indirect effects, such as variations in larval food availability. The larvae of many species of anurans depend on plentiful supplies of algae but rising temperatures in water bodies may trigger early blooms of detrimental filamentous cyanobacteria which may prove detrimental to feeding and growth. In addition, many salamanders and newts rely on small aquatic invertebrates and research by Durance & Ormerod (2007) has found that in the UK, spring macroinvertebrate abundance in headwater streams might decline by 21% for every 1 °C rise in water temperature, which highlights the sensitivity of headwater stream ecosystems to climate change. Finally, emerging infectious diseases have had wide-ranging and negative impacts on amphibian populations across the globe. In particular, chytrid fungus caused by Batrachochytrium dendrobatidis (BD) has been implicated as the proximate cause for crashes in many members of the tropical genus of Atelopus frogs. Pounds et al. (2006) have suggested that changing climatic conditions in mountainous areas of Central and South America have resulted in night time temperatures that have shifted closer to the optimal temperature for BD, while increased daytime cloudiness prevents frogs from finding thermal refuges from the pathogen. This has increased the prevalence of the disease and precipitated declines in many Atelopus species.
The impacts of climate change on amphibian populations are complex with many potential direct and indirect impacts on amphibians at individual and population scales. Global temperatures are predicted to increase by between 1.1 and 6.4 °C by 2100 (IPCC, 2007), so coherent research and conservation measures are required to preserve populations of amphibians across the globe.
References
Beebee, T.J.C. (2002) Amphibian phenology and climate change. Conservation Biology, 16 (6): 1454-1455.
Blaustein, A.R., Walls, S.C., Bancroft, B.A., Lawler, J.J., Searle, C.L. & Gervasi, S.S. (2010) Direct and indirect effects of climate change on amphibian populations. Diversity, 2: 281-313.
Carroll, E.A., Sparks, T.H., Collinson, N. & Beebee, T.J.C. (2009) Influence of temperature on the spatial distribution of first spawning dates of the common frog (Rana temporaria) in the UK. Global Change Biology, 15 (2): 467-473.
Durance, I. & Ormerod, S.J. (2007) Climate change effects on upland stream macroinvertebrates over a 25-year period. Global Change Biology, 13: 942-957.
IPCC. (2007) Climate change 2007: the physical science basis. In Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Eds: S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Avery, M. Tignor & H.L Miller. Cambridge University Press, Cambridge, UK.
Loman, J. (2016) Breeding phenology in Rana temporaria. Local variation is due to pond temperature and population size. Ecology and Evolution, 6 (17): 6202-6209.
Pounds, A., Bustamante, M.R., Coloma, L.A., Consuegra, J.A., Fogden, M.P.L., Foster, P.M., La Marca, E., Masters, K.L., Merino-Viteri, A., Puschendorf, R., Ron, S.R., Sánchez-Azofeifa, G.A., Still, C.J., Young, B.E. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature, 439: 161-167.
Reading, C.J. (1998) The effect of winter temperatures on the timing of breeding activity in the common toad Bufo bufo. Oecologia, 117 (4): 469-475.
Reading, C.J. (2007) Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia, 151: 125-131.
Scott, A.W., Pithart, D. & Adamson, J.K. (2008) Long-term United Kingdom trends in the breeding phenology of the common frog, Rana temporaria. Journal of Herpetology, 42 (1): 89-96.
Croaking Science: Amphibians that change colour
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.
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.
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.