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.
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.
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.
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.
Hot Weather Warning – Amphibians & Reptiles
After a cold start to the year, with weather events such as the ‘Beast from the East’, many people are enjoying the sizzling heat and sun that has now arrived in the UK. It is important to note that these extreme temperatures pose a risk to some of our UK wildlife. Our UK amphibian species struggle in high temperatures, particularly the tiny froglets and toadlets that are just emerging from their tadpole phase.
The most obvious and useful way to help these animals is to #BuildAPond, giving these animals and other wildlife ready access to water, for drinking and bathing. But building a pond doesn’t have to be a big nor expensive endeavour, and small ponds (e.g. bucket-sized) can be just as effective. Read more about building a pond with our FREE online guide Just Add Water.
In these heat extremes, a quick 2-minute job of putting out a small container or dish filled with fresh water will also help wildlife in your garden. If it’s a deep dish, don’t forget to add in a ramp or some stones to allow any animals that may fall a way to climb out. It is best to fill with water from a water butt rather than the tap, if you have one.
Frogs, Toads, Birds and Hedgehogs all eat small invertebrates like worms, which in this hot weather burrow deeper down into the dry soils. With this in mind, it is important to keep plants and soils damp to allow the predators to access their vital food source.
In addition to adding water into your outdoor space, keeping areas wild and sheltered can potentially save amphibian lives. Rockeries and log piles both provide shade to amphibians in the garden, where often the soil beneath will remain damp and the temperature much cooler that the outside.
Even the reptiles, like common lizards and grass snakes that can often be found basking in the sun, need shaded areas for relief from high temperatures. So log piles and rockeries are equally important for these animals to escape from the sun’s rays.
Mutualism: novel interactions between amphibians and other species
Mutualism is widespread within the animal kingdom and involves the close association between two organisms of different species in which both benefit. Within the Amphibia, there are a number of interesting and novel mutualistic interactions. These range from symbiosis with algae to interactions with predatory spiders and living with water buffalo. Our understanding of the range and extent of mutualistic interactions within amphibians remains relatively poorly understood and here we review some recent discoveries.
The mutualistic symbiosis between algae and embryos of the Spotted Salamander (Ambystoma maculatum) from North America was first reported more than 120 years ago (Figure 1). In this relationship, algae live inside the developing embryos and appear to provide many benefits to the salamanders including: earlier hatching, decreased mortality and reaching a larger size at hatching (Kerney et al., 2011). The algae are thought to gain through feeding on the nitrogenous wastes released by the embryos. Research by Kerney et al. (2011) found that this relationship is closer than originally thought. Through imaging and genetic experimentation, the researchers found that the algae actually invade the salamander tissues during embryo development and live inside the cells of the salamanders for a period of several weeks. At the end of larval development algal cell death occurrs in the majority of salamander cells. However, the researchers found genetic material of the algae in the reproductive tracts of adults, suggesting that the algae remains present and is transferred from one generation to another through the reproductive tract of the adults. This research raises the possibility of transfer of DNA between species and provides evidence of highly close relationships between two very different organisms.
Mutualism between larval amphibians and algae has been reported from other species. The tadpoles of the Dwarf American Toad (Bufo americanus charlesmithi) live in warm, shallow and temporary ponds which receive extended periods of sunlight (Figure 2). It has previously been observed that the tadpoles develop a bright green colouration during their development in these conditions. Tumlison & Trauth (2006) conducted a series of experiments and found that the green glow was the result of a symbiotic algae (Chlorogonium) living on the skin of the tadpoles. The tadpoles benefit through receiving oxygen from the algae who photosynthesise in the sunlight. Shallow, temporary ponds experience severe oxygen depletion during periods of high sunlight and warmth so as a result of obtaining oxygen from the algae, the tadpoles are able to survive longer in the ponds and reach a larger size before metamorphosis. In return, the algae received carbon dioxide from the tadpoles during respiration which aids in their growth.
The family of microhylid frogs from Sri Lanka comprises four genera and 10 species. Several of these species have restricted distributions and occur only in the Kanneliya Forest Reserve. The ecology of many of these microhylid frogs is poorly understood but adults appear to breed in tree holes. Karunarathna & Amarasinghe (2009) found a novel mutualistic interaction between the microhylid frog Uperodon nagaoi and two species of tarantula spider (Poecilotheria species). Both amphibian and tarantula species have been observed to share tree holes and it appears that both species protect each other’s eggs. The eggs of both the amphibian and tarantula are attacked by species of ants, mantids and other spider species. On several occasions Karunarathna & Amarasinghe (2009) recorded the tarantula attacking mantids that were feeding on U. nagaoi eggs. Similarly, individual U. nagaoi were observed predating ants that were feeding on the eggs of the tarantula. In addition, the tadpoles of U. nagaoi appeared to benefit from the remains of predated insects falling into water where they were developing.
Many species of herbivorous vertebrate harbour large populations of nematode worms in their guts. Herbivorous tadpoles are no exception with several thousand species of nematode being recorded from larvae. Several researchers have proposed that some species of nematodes may be mutualistic and provide benefits to their host. This appears to be the case with American Bullfrog (Lithobates catesbeiana) tadpoles which harbours the nematode (Gyrinicola batrachiensis) during its larval stage. Research by Pryor & Bjorndal (2005) found that America Bullfrog tadpoles infected with this nematode increased their rate of development by approximately 16 days, allowing the tadpoles to metamorphose earlier than tadpoles without the nematodes. This has many benefits as this promotes higher survival and subsequent reproductive success of the newly metamorphosed froglets. There could be two main reasons to explain this increase in development. First, the increase in gut size to allow the nematode to live may result in increased food intake and absorption by the tadpole. Second, the nematode increases rate of food fermentation in the gut, which allows the tadpole to absorb more food. The results of this study highlights that some gastrointestinal nematodes inhabiting the gut regions of other herbivores may have a beneficial effect on digestion and nutrition in those hosts.
A final form of novel mutualism has been observed between Marsh Frogs (Pelophylax ridibundus) and the Anatolian Water Buffaloes (Bubalus bubalis) in Turkey (Figure 3). Zduniak et al. (2017) reported a unique behaviour in the frogs where individuals climbed up the fur and onto the backs and heads of the buffaloes where they appeared to be predating flies. Up to 31 frogs were observed feeding on a single buffalo at any one time (Zduniak et al., 2017). It appears that both species benefit from this interaction since the frogs gain food and the buffalo has flies removed which may cause irritation. This appears to be the first record of such interaction between these two species and highlights that novel mutualistic interactions may occur more widely between amphibians and other species.
Tumlison, R. & Trauth, S.E. (2006) A novel facultative mutualistic relationship between bufonid tadpoles and flagellated green algae. Herpetological Conservation and Biology, 1 (1): 51-55.
Karunarathna, D.M.S.S. & Amarasinghe, A.A.T. (2009) Mutualism in Ramanella nagaoi Manamendra-Arachchi & Pethiyagoda, 2001 (Amphibia: Microhylidae) and Poecilotheriam species (Arachnida: Thereposidae) from Sri Lanka. Taprobanica, 1 (1): 16-19.
Kerney, R., Kim, E., Hangarter, R.P., Heiss, A.A., Bishop, C.D. & Hall, B.K. (2011) Intracellular invasion of green algae in a salamander host. PNAS, 108 (16): 6497-6502.
Pryor, G.S. & Bjorndal, K.A. (2005) Effects of the nematode Gyrinicola batrachiensis on development, gut morphology, and fermentation in bullfrog tadpoles (Rana catesbeiana): a novel mutualism. Journal of Experimental Biology, 303A: 704–712.
Zduniak, P., Erciyas-Yavuz, K. & Tryjanowski, P. (2017) A possible mutualistic interaction between vertebrates: frogs use water buffaloes as a foraging place. Acta Herpetologica, 12 (1): 113-11.
Amphibians and winterkill – a worse than average year?
Several species of UK amphibians overwinter in ponds, including common frogs and smooth newts. These animals tend to spend the winter in the silt and decaying leaves at the bottom of ponds. Normally this does not harm the animals and they resume breeding as usual the following spring. The advantage to spending the winter in the pond is the individuals are ready to breed as soon as the weather becomes warm enough. However, these individuals rely on absorbing oxygen through their skin, especially during periods of cold weather. This can be a problem as sometimes during the winter months oxygen levels within the pond can fall and toxic chemicals build-up. This occurs more frequently when the surface of the pond freezes over for extended periods. Unfortunately this can result in the death of some amphibians and is commonly known as winterkill. This process is natural and every year a number of amphibians, mainly common frogs, die as a result of winterkill and this has no negative impact on populations.
During January and February 2018 we experienced relatively mild winter conditions across the UK, with only light overnight frosts. This encouraged the early emergence of common frogs and other amphibians, especially within the south of the UK. Froglife had sightings of great crested newts on 25 December 2017 and the first frogspawn was reported on 17th January. The relatively mild conditions continued until late February, which triggered the movements of many common frogs towards breeding ponds. At the end of February, the UK experienced unusually cold and prolonged winter weather with hard frosts and snow. This sudden cold period of weather came quickly, when a large proportion of breeding frogs were already at ponds. Although these individuals may have tried to avoid the cold conditions, the combination of low temperatures, already low oxygen levels in ponds, along with an extended period of ice covering ponds caused mortality in many frogs across the country. The Froglife enquiry service received a sudden and high level of reports of large numbers of mainly common frogs being found dead in ponds. Between 5th and 16th March Froglife received 26 enquiries relating to frozen frogs in ponds. In several cases frogs appeared to have frozen within the ice. The worst case was from a school pond where over 120 common frogs were removed dead from the water. This number of enquiries was higher than average as in most years Froglife only receives a handful of cases of winterkill across the whole winter and spring seasons.
In addition to an increase in number of dead adult common frogs, frogspawn appears to have been affected. Spawn laid early in the season is at risk of damage due to later frosts. The cold period of weather in early March and then again on the weekend of 17-18th March occurred after the majority of frog spawn had been laid. Although spawn in the frost-free zone of the pond (usually underwater) will survive, any eggs near to the surface usually die. These often contract a white fungal infection which can later spread to all the spawn. The combination of frost and fungal infection may have resulted in a higher than average mortality of frog spawn in 2018.
It is too early to determine the impact of winterkill on common frog and other amphibian populations. Amphibians are relatively long-lived so the loss of spawn from one breeding season is unlikely to have significant impacts on populations. However, the loss of a large number of breeding adults may have an impact, especially where populations are small and are already under stress from other factors such as loss of breeding and terrestrial habitats, habitat fragmentation, introduced disease and pollutants. Climate change may impact amphibians in several ways and an increase in extreme weather events may have long-term implications on amphibian populations across the country. Long-term population monitoring is required on amphibian populations to determine whether they are negatively affected by repeated extreme weather events at key times during their breeding cycle.
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