metamorphosis

Croaking Science: Overwintering in Frog Tadpoles

July 27, 2018 by editor

Overwintering in frog tadpoles

During June and July in the UK the majority of Common Frog (Rana temporaria) tadpoles metamorphose into juveniles which leave ponds for terrestrial habitats. They will spend the rest of the summer and autumn foraging and feeding on small invertebrates in preparation for the winter. However, a number of common frog tadpoles each year will remain in ponds and spend the winter in the water, metamorphosing into juveniles the following spring (Figure 1). What causes some tadpoles to metamorphose and others to remain in the water over the winter? Often, ponds drying out or freezing over can limit the capacity for frog tadpoles to overwinter. However, there are many ponds in the UK where this does not occur, which allows for overwintering of tadpoles. Our understanding of the exact factors which trigger overwintering in tadpoles are not fully understood, but research by Walsh et al. (2016) found that temperature and food availability were key factors. In addition, the decision on whether to over‐winter as a tadpole appears to be made relatively early in the season (Walsh et al., 2008). Under laboratory conditions, lower temperatures and reduced food availability during the summer resulted in a higher proportion of individuals remaining as tadpoles during the winter (Walsh et al., 2016). These findings suggest that cold weather conditions in the early autumn may affect tadpole development, perhaps by affecting endocrine function. However, temperature alone does not appear to be enough to trigger overwintering in tadpoles; food availability also appears to be important. Although these two factors play an important role in triggering overwintering in common frog tadpoles, there are other factors, not fully understood, that appear to be involved.

***Figure 1.*** *Common Frog Rana temporaria tadpoles may spend the winter in their natal ponds under certain environmental conditions. (Photo credit: John Roston)*

Living in areas with variations in altitude provides challenges for the development of common frog tadpoles. Higher altitude ponds experience lower temperatures and food availability and these may promote a higher incidence of overwintering in tadpoles. However, Muir at al. (2014) found that in tadpoles living at high altitude in Scotland, individuals had a lower resting metabolic rate which allowed for more energy to be allocated to growth. This is likely to allow individuals to grow faster under cooler environmental conditions and allow tadpoles to metamorphose earlier than expected and prevent the necessity to overwinter. However, if tadpoles developing at high altitudes do need to overwinter, they are able to better tolerate the colder winter temperatures. Muir et al. (2014) found that the tadpoles of Common Frogs at high altitude were able to tolerate freezing for short periods of time. This adaptation provides common frog tadpoles with the ability to withstand the cooler pond conditions at high altitude over the winter and therefore lead to greater survival.

Across Central Europe the incidence of overwintering tadpoles varies by species and is more typical in later breeding species with large tadpoles such as the Midwife Toad Alytes obstetricans, Spadefoot Toad Pelobates fuscus, and water frogs (Pelophylax species) (Gilbert & Harmsel, 2016). The incidence of overwintering in Common Frogs Rana temporaria is rare and was reported for the first time in the Netherlands in 2013 (Gilbert, 2016). This was likely to be due to the unusual weather conditions of 2013/14 along with the sheltered site where this was observed. Overwintering in the Edible Frog (Pelophylax esculentus complex) is a relatively rare phenomenon across Central Europe (Figure 2). Research by Péntek et al. (2018) found that overwintering by tadpoles only seems to occur in unusual weather conditions. In one particular incidence cold temperatures over the winter resulted in late breeding by adults which led to tadpoles getting a late start to their growth and development. Cool conditions early in the autumn (October) appeared to trigger halting of development and the subsequent mild winter promoted successful overwintering by tadpoles of this species (Péntek et al., 2018). Although still relatively rare, overwintering may become more common across Central Europe with changing environmental conditions causing increased variability in seasonal temperatures.

**Figure 2.** Overwintering by the tadpoles of the Edible Frog is relatively rare across Central Europe.

In the United States, 15 species of Ranid frogs occur but only five of these species are known to overwinter as larvae (North American Bullfrog Rana catesbeiana, Pig Frog R. grylio, River Frog R. heckscheri, Red-legged Frog R. aurora, and Southern Mountain Yellow-legged Frog R. muscosa). It appears that pond desiccation is one of the main factors limiting Ranid frog species in North America from overwintering as tadpoles. The Southern Leopard Frog Rana sphenocephala is a common frog inhabiting freshwater ponds across the Northern United States (Figure 3). Tadpoles of this species will remain in the larval stage until reaching a critical metamorphic size and if this is not reached by the end of the autumn, then the tadpoles will overwinter (Pintar & Resetarits, 2018). If winter conditions are suitable, tadpoles will remain in the pond for several years until the critical size for metamorphosis has been reached. This is different to Common Frogs in the UK which do not need a critical size to metamorphose but do require specific environmental conditions. These results highlight the variations that occur across Ranid species in their requirements for metamorphosis.

**Figure 3.** Tadpoles of the Southern Leopard Frog from the United States have to attain a critical body size before they can metamorphose. This can result in the tadpoles spending several years in one pond.

References

Gilbert, M.J. & Harmsel, R. (2016) Hibernating larvae of the common frog (Rana temporaria) in the Netherlands. Herpetology Notes, 9: 27-30.

Muir, A.P., Biek, R., & Mabel, B.K. (2014) Behavioural and physiological adaptations to low-temperature environments in the common frog, Rana temporaria. BMC Evolutionary Biology, 14: 110.

Péntek, A.L., Sárospataki, M., & Zsuga, K. (2018) Larval overwintering of the Pelophylax esculentus complex in a sodic bomb crater pond near Apaj, Hungary. North-western Journal of Zoology, 2018: e1775023/9.

Pintar, M.R. & Resetarits Jr., W.J. (2018) Variation in pond hydroperiod affects larval growth in Southern Leopard Frogs, Lithobates sphenocephalus. Copeia, 106 (1): 70–76.

Walsh, P.T., Downie, J.R. & Monaghan, P. (2016) Factors affecting the overwintering of tadpoles in a temperate amphibian. Journal of Zoology, 298 (3): 183-190.

Walsh, P.T., Downie, J.R. & Monaghan, P. (2008) Larval over‐wintering: plasticity in the timing of life‐history events in the common frog. Journal of Zoology, 276 (4): 394-401.

Croaking Science: Newts that never grow up!

November 21, 2017 by editor

Newts that never grow up – paedomorphosis in salamanders

The majority of pond-breeding salamanders have a biphasic metamorphic life cycle where free-swimming larvae living in ponds and other water bodies metamorphose into terrestrial living adults. The advantage of this life history is that it allows adults to exploit different habitats to larvae, utilise a wider range of ecological niches and escape from potentially hostile environments e.g. a desiccating pond. However, a number of salamander species within Europe and North America have evolved a unique life history where free-swimming larvae to do not metamorphose into terrestrial living adults, but remain within the water and retain larval characteristics. Known as paedomorphosis these individuals develop into sexually reproductive adults but retain larval traits e.g. free-swimming larval form (Figure 1). It appears that the phenomenon of paedomorphosis has evolved several times within salamanders and has been of great interest to biologists for centuries. One theory suggests that paedomorphosis is most likely to evolve when environmental conditions experienced by adults are inhospitable relative to conditions experienced by larvae. For example, if water bodies remain constant throughout the year but temperature regimes and environmental factors on the land are hostile, such as in mountainous regions, arid landscapes or nutrient poor regions, it may be more favourable to remain in the larval form. Within southern Europe, paedomorphic populations often occur in deep, permanent and cool alpine lakes, where the terrestrial habitat has poor nutrient availability (Denoël et al., 2005). In an attempt to resolve many questions relating to the evolution of paedomorphosis in salamanders Bonnett et al. (2014) examined DNA sequences of a sub-family of plethodontid salamanders from North America. The authors concluded that within this group, paedomorphosis is more likely to occur in species dwelling in caves and those occurring in more arid climates. Here there are more resources in water bodies than in terrestrial habitats. An interesting finding of this study is that paedomorphosis has evolved and re-evolved serval times in the same species. The Valdina Farms Salamander (Eurycea troglodytes), from the western Edward Plateau, Texas, existed in a paedomorphic form 22 million years ago, before evolving into a metamorphic form (i.e. larvae metamorphosed into terrestrial adults). Subsequently, several million years later, it re-evolved back into a paedomorphic form (Bonnett et al., 2014). This is likely to be due to changing environmental conditions over this time period. However, there is a cost to being paedomorphic. Bonnett et al. (2014) found that paedomorphic spelerpine plethodontids from eastern North America have significantly smaller geographic range sizes than metamorphosing species and have not dispersed between biogeographic regions. This has resulted in these species being more at risk from environmental events or human disturbance than species with wider geographic ranges and as a result have a higher rate of extinction.

**Figure 1:** Cave salamanders such as the Mexican axolotl (Ambystoma mexicanum) exist in paedomorphic forms due to hostile terrestrial habitats. Note the retention of gills which is normally a characteristic of larvae.

In some populations of salamanders, individuals exhibit facultative paedomorphosis, i.e. when both metamorphic and paedomorphic forms coexist and the occurrence of the latter within a given population depends on the advantages of living in the aquatic and terrestrial habitats. Whether an individual is metamorphic or paedomorphic may depend on a range of environmental factors including temperature, pond desiccation rate, terrestrial aridity and resource availability. Facultative paedomorphosis is an adaptive strategy which has been reported from several European newts. For example, great crested newt (Triturus cristatus), palmate newt (Lissotriton helveticus), alpine newt (Ichthyosaura alpestris) and southern banded newt (Omatotriton vittatus) all exhibit paedomorphosis, especially in the south of their range (Oromi et al., 2014). Facultative paedomorphosis has been regularly observed in populations of the smooth newt (L. vulgaris), particularly those in southern and eastern Europe (Figure 2). In this species, the key environmental factors are prey and predator abundance and habitat composition, with paedomorphosis generally occurring in areas with permanent, nutrient-rich water bodies without predators (Bozkurt et al., 2015). When fish are introduced to water bodies, paedomorphosis generally disappears since the aquatic environment becomes a less favourable habitat (Denoël et al., 2005).

**Figure 2:** Facultative paedomorphosis in the smooth newt (Lissotriton vulgaris) is most common in southern parts of its range. However, it can occur anywhere, such as in this individual from eastern England. Photo © Liz Morrison.

In 2017, Mathiron et al. (2017) tested theories in relation to how climatic factors impact on paedomorphosis in facultative populations of the palmate newt (L. helveticus) living in the Department of Hérault, France. The authors found that temperature and water availability each play a significant role in metamorphosis and explain the persistence of paedomorphosis in certain populations. These results have major implications as they show that droughts through evolutionary history have been a primary factor in promoting the evolution of paedomorphosis in this species. When terrestrial environments experience persistent drought, this has promoted the evolution of paedomorphic populations. This has significance in relation to a warming climate where the occurrence of severe droughts in Mediterranean parts of this species’ range, may result in an increase in paedomorphic populations in the near future. Mathiron et al. (2017) also found a sex-biased effect highlighting the role of sex in the metamorphosis of paedomorphs. Both water level and temperature affected the metamorphosis of males more than females. More metamorphic males occurred than females and, in drying conditions, started metamorphosis earlier than did females, which resulted in a female biased sex-ratio of paedomorphs. The reason why males metamorphose more than do females may be due to differences in levels of hormones in males compared to females. Also, males tend to disperse more than females so being metamorphic and turning into terrestrial adults would allow them to seek new water bodies and promote gene flow between populations.

References

Bonnett, R.M., Steffen, M.A., Lambert, S.M., Wiens, J.J. & Chippindale, P.T. (2014) Evolution of paedomorphosis in plethodontid salamanders: ecological correlates and re-evolution of metamorphosis. Evolution 68 (2): 466–482.

Bozkurt, E., Olgun, K. & Wielstra, B. (2015) First record of facultative paedomorphism in the Kosswig’s newt Lissotriton (vulgaris) kosswigi (Freytag, 1955) (Urodela; Salamandridae), endemic to northwestern Turkey. Turkish Journal of Zoology, 39: 976-980.

Denoël, M., Joly, P. & Whiteman, H.H. (2005) Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biological Reviews, 80: 663–671.

Mathiron, A.G.E., Lena, J., Baouch, S. & Denoël, M. (2017) The ‘male escape hypothesis’: sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian. Proceedings of the Royal Society B: Biological Sciences, 284 (1853):

DOI: 10.1098/rspb.2017.0176.

Oromi, N., Amat, F., Sanuy, D. & Carranza, S. (2014) Life history trait differences between a lake and a stream-dwelling population of the Pyrenean brook newt (Calotriton asper). Amphibia-Reptilia, DOI:10.1163/15685381-00002921.

Croaking Science: Post metamorphic dispersal – random or targeted?

July 26, 2017 by editor

Post metamorphic dispersal – random or targeted?

Late spring and early summer is the time of year that juvenile temperate breeding amphibians undergo post-metamorphic dispersal. Such movements are defined as “unidirectional movements from natal sites which ultimately result in individuals finding new breeding sites” (Semlitsch, 2008). Newly emerged metamorphs are often extremely small and vulnerable to external environmental factors. For example common toad (Bufo bufo) metamorphs may only be 10 mm in length and therefore have less locomotor capacity and are subject to more rapid water loss than adults. In addition, due to their tiny size and very active behaviour during periods of light rain, rates of exposure may be quite high relative to their body mass. This life stage may represent the period when amphibians are most at risk to harmful effects from exposure to pesticides and other chemicals. Due to their small size and vulnerability, in the first year juvenile amphibians are most likely to be limited to areas adjacent to the breeding pond where they feed, continue to grow, and find over-wintering sites. It is not until later in the season or after the second or third year, when juveniles are larger, that they move greater distances and seek alternative breeding sites. Therefore finding suitable resting habitats where they can seek protection is crucial in the early weeks of life.

Since metamorphs have no prior knowledge of the habitats surrounding ponds, it might be expected that individuals disperse randomly into terrestrial habitats. In a review of the dispersal of European and North American amphibians, Semlitsch (2008) concluded that there is little evidence to suggest that juvenile amphibians have specialized abilities to find new or alternative breeding sites, such as a water-finding ability or by using sounds of breeding choruses of anurans, which might indicate that juveniles exhibit target-oriented dispersal. In his review, Semlitsch (2008) suggested that newly metamorphosed individuals disperse from natal ponds in a random pattern relative to landscape features beyond the pond perimeter and subsequently find new or non-natal breeding ponds primarily by chance. For example, results from a study on Red-Spotted Salamanders (Notophthaltnus viridescens) from Missouri, USA indicated that although adults leaving breeding ponds oriented with respect to forested habitat, metamorphs tended to disperse from the pond in all directions, with 42% emigrating towards the forest and 58% emigrating towards the grassland. Both adults and juveniles of this species are unable to cross grassland, with forest habitats favoured. Those metamorphs emigrating towards grassland experienced higher mortality.

*Figure 1. Green and Golden Bell Frog from Australia. Newly emerged metamorphs are able to follow conspecifics to suitable terrestrial habitats.*

However, a growing number of field studies have found that metamorphs of some species do exhibit targeted, non-random movements towards favourable habitats, despite having no prior knowledge of the surrounding habitats. Recent research on Australian Green and Golden Bell frogs (Litoria aurea) suggests that newly emerged metamorphs preferred the habitat closest to the presence of other metamorphs of the same species (Figure 1). The advantages of using conspecific cues to determine dispersal direction is to reduce search costs by spending less time searching in non-suitable habitat and seeking out suitable habitats more effectively.

A field study on Great Crested Newts (Triturus cristatus) and Smooth Newts (Lissotriton vulgaris) indicates that non-random dispersal of both adults and juveniles may occur when leaving ponds. Juveniles of both T. cristatus and L. vulgaris migrated faster and to a much greater distance from the pond than their conspecific adults (Figure 2). A high percentage of freshly metamorphosed juveniles of both species showed the same clear preferences for a woodland habitat like the adults. This is surprising, as the juveniles lack the familiarity with the quality of their terrestrial surroundings. The results therefore indicate that juvenile newts possess a method for detecting and orienting towards favourable habitats that probably become modified later in life by individual experience. In addition, Hayward (2010) demonstrated that great crested newts were able to identify chemical cues left on the substrate and follow the route taken by previous newts. This suggests that metamorphs may follow adults to terrestrial and possibly hibernation sites.

*Figure 2. Juvenile great crested newt (Triturus cristatus). Metamorphs may follow cues left by adults to orient towards forested habitats.*

Conservation implications:

A knowledge of the core terrestrial habitat requirements of a particular amphibian species is required for local protection of populations. Understanding how and in what directions metamorphs may disperse is important in limiting mortality in a human-dominated landscape. If metamorphs of a particular species have the capacity to orient towards favoured woodland habitats, this may avoid unnecessary mortality. However, if individuals disperse randomly from ponds, in a landscape where suitable terrestrial habitat is limited, high rates of mortality may occur if individuals orient towards roads, barriers or other human hazards. Therefore a knowledge of the behavioural tendency of species or stages during dispersal might be critical to directing conservation efforts. However, at present, the phenomenon of dispersal in amphibians is poorly understood and needs more attention. In particular, the potential relationship of sex, body size, density-dependence, population size, habitat quality, and land use to dispersal tendency and behaviour needs to be examined.

References

Defra (2010) Use of agricultural areas by amphibians. Research Project Final Report, PS3240. Defra, UK.

Jehle, R. & Artnzen, J.W. (2000) Post-breeding migrations of newts (Triturus cristatus) and (T. marmoratus) with contrasting ecological requirements. Journal of Zoology 251: 297 – 306.

Hayward, R. (2010) Dispersion and orientation in newly metamorphosed great crested newts (Triturus cristatus). PhD thesis, DeMontford University.

Müllner, A. (2001) Spatial patterns of migrating Great Crested Newts and Smooth Newts: The importance of the terrestrial habitat surrounding the breeding pond. In: Herausgegeben von Andreas Krone (Ed) Rana Sonderheft 4, Der Kammolch (Triturus cristatus) Verbreitung, Biologie, Ökologie und Schutz. Natur & Text, Germany.

Pizzatto, L., Stockwell, M., Clulow, S., Clulow, J. & Mahony, M. (2016) Finding a place to live: conspecific attraction affects habitat selection in juvenile green and golden bell frogs. Acta Ethology, DOI 10.1007/s10211-015-0218-8.

Rittenhouse, T.A.G. & Semlitsch, R.D. (2006) Grasslands as movement barriers for a forest-associated salamander: Migration behavior of adult and juvenile salamanders at a distinct habitat edge. Biological Conservation 131: 14-22.

Semlitsch, R.D. (2008) Differentiating migration and dispersal processes for pond-breeding amphibians. The Journal of Wildlife Management, 72 (1): 260-267.

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