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Croaking Science: Artificial light at night- a problem for amphibians?

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Light pollution from industrialization, urban and suburban development is spreading rapidly across the world. It is estimated that 20% of land on earth is polluted by artificial light (Cinzano et al., 2001). An increasing range of wild animal species are being exposed to levels of night-time light higher than ever before. It is estimated that the average amount of light reaching the ground from one street lamp is 50 lux, compared to 0.1 lux of bright moonlight (Bennie et al., 2016) (Figure 1). Car headlights may reach over 1,000 lux, some 10,000 higher than natural night time light exposure. These levels of artificial light have been shown to affect a range of animal taxa from mammals to birds, reptiles and insects. The impacts of artificial light on amphibians appear to be varied, depending on the species and their ecology (reviewed in Dutta, 2018). For example, the calling behaviour of many frog species appears to be affected, with individuals calling less frequently and moving more often. This has the potential for decreasing mating opportunities and negatively impacting on subsequent spawning success. However, certain species, such as the cane toad (Bufo marinus) appear to benefit from street lights, foraging more often on the insects which congregate beneath them at night. On the contrary, red-backed salamanders (Plethodon cinereus) from North America forage less under artificial light, hiding in the leaf litter. This may have consequences on an individual’s ability to effectively forage and feed at night. Road mortality may be increased in areas of artificial light as has been shown in the American toad (Bufo americanus), which is attracted to street lighting and is more likely to cross roads (Mazerolle, 2004). Indirect effects of artificial light may include increased detection by predators and subsequent mortality of amphibians.

Figure 1. The amount of light generated by one street light can be several hundred or even several thousand times brighter than moonlight.
[Photo credit: Hackspett1265, https://commons.wikimedia.org/wiki/File:Night_light_behind_tree.jpg]

Artificial light may impact a range of amphibian life stages including the growth, development and activity of larvae, juveniles and adults. Our understanding of how artificial light may impact each life-stage is not fully understood. Dananay & Benard (2018) carried out experiments to determine the impacts of artificial light on larval and juvenile American toads. The researchers did not find any significant impact of artificial light on larval growth or behaviour, but juvenile American toads were affected. Juvenile toads under artificial light treatment were more active than those under dark treatments and had growth rates 15% lower than those in dark treatments. This increased nocturnal activity by juveniles under artificial light conditions appears to have resulted in increased energy expenditure and thus reduced growth rates (Dananay & Benard, 2018). This reduced growth may result in delayed reproductive maturity, lower fertility and reduced survival. Combined with other stressors, such as climate change, this could lead to population declines in many of our common amphibian species.

Figure 2. Juvenile toads under artificial light at night experienced lower growth rates which may result in delayed reproductive maturity, lower fertility and reduced survival (Dananay & Benard, 2018).
[Photo credit: Fungus Guy, https://commons.wikimedia.org/wiki/File:Eastern_American_toad_(Sudden_Tract).jpg]

Habitats restored for recreational purposes, as well as for wildlife, including amphibians, are often situated close to towns and cities. The light intensity reaching wetland areas close to cities may be greater than the brightest full moon (Secondi et al., 2017). Common toads (Bufo bufo), may be particularly affected by increased levels of artificial light as they have a very short breeding season and may use light to orient towards ponds and aid in synchronicity in breeding. Touzet et al. (2019) carried out research on the common toad in France to examine toad behaviour under artificial light generated by street and outdoor lighting in semi-urban areas. After 20 days of nocturnal exposure during the breeding period at 5 lux the total time spent active by male common toads decreased by more than half; at 20 lux activity levels dropped by 73%. This was due to male toads being less active during nocturnal periods (Touzet et al., 2019). In addition, common toads decreased their active energy expenditure by 18% at 5 lux and 38% at 20 lux, probably due to increased stress (Touzet et al., 2019). The authors conclude that the alteration of both activity and energy metabolism could have negative impacts on common toad reproduction and ultimately lead to a reduction in survival.

The impacts of artificial light on amphibians may not always be negative and some species seem to be resistant to anthropogenic light sources at night. Underhill & Höbel (2018) tested the effects of artificial light on the breeding behaviour of female eastern gray treefrogs (Hyla versicolor). Contrary to expectation, the researchers found no effects of artificial light on mating preferences and breeding behaviour. In this species, increased levels of artificial light should not affect population persistence nor affect mate choice. This is in contrast to túngara frogs (Engystomops pustulosus) which changed their behaviour under different light conditions in a way that suggested that they felt safer under darker conditions (Rand et al., 1997). Frog species vary in their sensitivity to light and the degree that they use visual cues for orientation and reproduction. The eastern gray treefrog does not rely heavily on visual cues for mate selection which may explain the lack of significant impacts of artificial light on their breeding behaviour (Underhill & Höbel, 2018).

Figure 3. The eastern gray treefrog (Hyla versicolor) from North America appears resistant to the effects of artificial light.
[Photo credit: Cliff, https://commons.wikimedia.org/wiki/File:Grey_Tree_Frog_(Hyla_versicolor)_(3151990943).jpg]

It appears that there is no consistent and universal impact of artificial light on amphibians. The response seems to vary by species depending on their ecology and breeding biology and their reliance on visual cues. In addition, responses by individual populations are likely to vary depending on location and the amount of artificial light. However, in many cases it appears that artificial light may have negative impacts on amphibian populations. Further research is required at a population level to determine the long-term impacts of artificial light and possible synergistic interactions with other environmental stresses such as habitat loss, fragmentation, pollutants and climate change.

References

Bennie, J., Davies, T.W., Cruse, D. & Gaston, K.J. (2016) Ecological effects of artificial light at night on wild plants. Journal of Ecology, 104: 611–620.

Cinzano, P., Falchi, F., & Elvidge, C.D. (2001) The first world atlas of the artificial night sky brightness. Monthly Notices of the Royal Astronomical Society, 328: 689–707. https://doi.org/10.1046/j.1365-8711.2001.04882.x

Dananay, K.L. & Benard, M.F. (2018) Artificial light at night decreases metamorphic duration and juvenile growth in a widespread amphibian. Proceedings of the Royal Society, London B, 285:

20180367. http://dx.doi.org/10.1098/rspb.2018.0367.

Dutta, H. (2018) Insights into the impacts of three current environmental problems on Amphibians. European Journal of Ecology, 4 (2): 15-27, doi:10.2478/eje-2018-0009

Feuka, A.B., Hoffmann, K.E., Hunter Jr, M.L. & Calhoun, A.J.K. (2017) Effects of light pollution on habitat selection in post-metamorphic wood frogs (Rana sylvaticus) and unisexual blue-spotted salamanders (Ambystoma laterale × jeffersonianum). Herpetological Conservation and Biology, 12 (2):470–476

Mazerolle, M.J. (2004) Amphibian road mortality in response to nightly variations in traffic intensity. Herpetologica, 60 (1): 45-53.

Rand, A. S., Bridarolli, M. E., Dries, L., & Ryan, M. J. (1997). Light levels influence female choice in túngara frogs: Predation risk assessment? Copeia, 1997, 447–450. https://doi.org/10.2307/1447770.

Secondi, J., Dupont, V., Davranche, A., Mondy, N., Lengagne, T. & Théry, M. (2017) Variability of surface and underwater nocturnal spectral irradiance with the presence of clouds in urban and peri-urban wetlands. PLoS One, 12: e0186808. doi:10.1371/journal.pone.0186808.

Touzot, M., Teulier, L., Langagne, T., Secondi, J., Théry, M., Libourel, P., Guillard, L. & Mondy, N. (2019) Artificial light at night disturbs the activity and energy allocation of the common toad during the breeding period. Conservation Physiology, 7 (1): coz002; doi:10.1093/conphys/coz002

Underhill, V.A. & Höbel, G. (2018) Mate choice behavior of female Eastern Gray Treefrogs (Hyla versicolor) is robust to anthropogenic light pollution. Ethology, 124: 537–548. doi:10.1111/eth.12759

Croaking Science: Spadefoot toads- unique life-histories and evolution

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Spadefoot toads are one of the best known examples of fossorial frogs. They gained their name because three of the genera have a specially adapted hind foot which enables effective burrowing. Many spadefoot toads live in arid habitats and they are uniquely adapted to harsh, dry environments. The adults are highly secretive, often spending most of the year buried underground. Individuals of some species may burrow to depths of two metres below the surface (AmphibiaWeb, 2008). North American spadefoot toads typically have a highly explosive breeding strategy, often emerging after heavy rains to breed (Figure 1). The adults are able to burrow into sand to avoid hot summer temperatures, while the larvae have an extremely rapid development, enabling some species to metamorphose into terrestrial juveniles within just 30 days (Pfenning, 1992). However, European spadefoot toads have a different life history with a prolonged breeding period of several months and having large larvae which take several months to metamorphose (Degani, 2015).

Figure 1. Spadefoot toads, like the Couch’s spadefoot toad (Scaphiopus couchii) from Texas, are highly adapted to living in harsh, dry environments. [Photo credit: Howcheng, https://commons.wikimedia.org/wiki/File:Scaphiopus_couchii_ANRA.jpg]

Spadefoot toads are spread widely across the whole of the northern Hemisphere from eastern Russia to western United States. Most, but not all, spadefoot toads possess an adapted hind foot (Figure 2) and it was assumed that it was only the species which lived in arid environments which possessed this feature. However, recent evolutionary research by Chen et al. (2016) has suggested that this may not be the case. Chen et al. (2016) report on a new spade-foot bearing fossil toad from eastern Mongolia. The fossil, Prospea holoserisca, is estimated to be 56 million years old and resembles modern spadefoot toads. It is the earliest definite fossil frog with an enlarged hind limb which was used for effective burrowing (Chen et al., 2016). Analysis by Chen et al. (2016) has shown that this fossil is the ancestor of both the living spadefoots which possess the specially adapted hind foot and those which do not. The anatomy of the fossil spadefoot toad suggests that it could burrow, but analysis of the environment at the time indicates that it did not live in an arid environment, like modern spadefoot toads. This has led Chen et al. (2016) to the conclusion that burrowing in an arid environment is an exaptation instead of an adaptation. In other words, burrowing behaviour did not evolve in response to an arid environment, but instead the frogs already had the hind foot morphology which enabled the frogs to burrow in sand when the environment subsequently became arid (Chen et al., 2016). Indeed, another study has suggested that the rapid larval development often observed in North American spadefoot toads did not evolve in response to an increasingly arid environment but relates instead to the size of the frogs’ genome and evolutionary history (Zeng et al. 2014). These studies show that amphibian species may utilise morphology and behaviour which they already possess when environmental conditions change.

Figure 2. The underside of a male spadefoot toad (Pelobates fuscus). Note the spade-like legs on the back legs marked by the red arrows. [Photo credit: Christian Fischer, https://commons.wikimedia.org/wiki/File:PelobatesFuscusVentraltagged.JPG]

There are six species of spadefoot toad belonging to the genus Pelobates which are distributed across Europe, Western Asia and North Africa. Due to their fossorial existence for most of the year, information on their behaviour is generally lacking. The common spadefoot toad, Pelobates fuscus, has a prolonged breeding period lasting from April to June during which time the males defend territories around the pond and, unlike many breeding toads, call underwater (AmphibiaWeb, 2008) (Figure 3). Eggert & Guyétant (2003) carried out a study of calling males in northeast France and found that males with a lower body condition arrived later than males with higher body condition. Males arriving early at the breeding pond experienced high competition for females and it is risky for males in low body condition as they are unlikely to be successful in mating. Therefore, Eggert & Guyétant (2003) propose that males optimise their breeding migration by arriving earlier or later, depending on their body condition. In addition, older (and more experienced) males tended to stay for less time at breeding ponds, presumably because they were able to obtain a mate more quickly (Eggert et al., 2003). Unlike species of toad which have an explosive breeding strategy where males have little time to secure a mate, species with a longer breeding season like the common spadefoot toad have the opportunity to utilise different mating tactics to ensure greater chances of successfully mating.

Figure 3. Male common spadefoot toads (Pelobates fuscus) have alternative breeding tactics. [Photo credit: Bearbeitung von deBild, https://commons.wikimedia.org/wiki/File:Knoblauchkroete_IMGP4749.jpg]

The common spadefoot toad (P. fuscus) and eastern spadefoot toad (P. syriacus) overlap in parts of their range. Both species have highly similar ecology and life history: both burrow underground, are nocturnal, reproduce at the same period of the year, use similar aquatic habitats for reproduction and forage in the same terrestrial habitats (Cogălniceanu et al., 2014). Therefore, there is a high potential for niche overlap and competition between species. In their recent research, Székely et al. (2017) found that each species had different foraging patterns which avoided competition. The eastern spadefoot toad emerged from the soil less often than the common spadefoot toad but was active for much longer and moved over twice the distance. These differences in movement patterns are likely to allow the different species to exploit different prey types which would allow coexistence and reduce competition (Székely et al., 2017). Since the eastern spadefoot toad is a widely foraging species it is likely to encounter more sedentary prey species that are clumped and unpredictable. However, this is likely to be costly in terms of energetic expenditure. The common spadefoot toad is less active, but will be able to exploit larger, faster moving and active prey. However, these are generally fewer in number (Székely et al., 2017). Therefore, each species exploits a different foraging strategy, each with its own advantages and disadvantages. Although these behavioural differences are relatively small, they allow each species to exploit different prey species and coexist in the same habitats. 

References

AmphibiaWeb (2008) Pelobates fuscus: Common spadefoot <http://amphibiaweb.org/species/5270> University of California, Berkeley, CA, USA. Accessed Oct 25, 2019.

Chen, J., Bever, G.S., Yi, H. & Norell, M.A. (2016) A burrowing frog from the late Paleocene of Mongolia uncovers a deep history of spadefoot toads (Pelobatoidea) in East Asia. Nature Scientific Reports, 6: 19209. doi 10.1038/srep19209.

Cogălniceanu, D., Roşioru, D., Székely, P., Székely, D., Buhaciuc, E., Stănescu, F. & Miaud, C.

(2014). Age and body size in populations of two syntopic spadefoot toads (genus Pelobates) at the limit of their ranges. Journal of Herpetology, 48: 537-545.

Degani, G. (2015) The habitats, burrowing behavior, physiology, adaptation and life cycle of spadefoot toads (Pelobates syriacus, Boettger, 1869) at the southern limit of its distribution in Israel. Open Journal of Animal Sciences, 5: 249-257.

Eggert, C. & Guyétant, R. (2003) Reproductive behaviour of spadefoot toads (Pelobates fuscus): daily sex ratios and males’ tactics, ages and physical condition. Canadian Journal of Zoology, 81: 46-51.

Pfenning, D.W. (1992) Polyphenism in spadefoot toads tadpoles as a locally adjusted evolutionarily stable strategy. Evolution, 46 (5): 1408-1420.

Székely, D., Cogălniceanu, D., Székely, P. & Denoël, M. (2017) Out of the ground: coexisting fossorial species differ in their emergence and movement patterns. Zoology, 121: 49-55.

Zeng, C., Gomez-Mestre, I. & Wiens, J.J. (2014) Evolution of rapid development in spadefoot toads is unrelated to arid environments. PLOS ONE, 9: e96637, doi: 10.1371/journal.pone.0096637.

Croaking Science: Cave Salamanders

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Cave salamanders

Cave salamanders belonging to the amphibian genera Hydromantes and Eurycea occur in southern Europe and widely across the United States. There are at least 11 species of salamander which spend their entire lives in cave environments and many more which complete part of their life-cycle in underground environments e.g. fire salamander (Salamandra salamandra). Many salamanders which live in cave environments exhibit two key characteristics: lack of lungs and direct development (i.e. loss of aquatic larval stage). Having no lungs forces these salamanders to rely on absorbing oxygen across their skin and use bucco-pharangeal breathing, which is obtaining oxygen through the moist lining of the mouth. This type of breathing can only occur effectively in specific conditions of high moisture and cool temperature, which are often found in cave environments. Due to their underground existence, the ecology and behaviour of cave salamanders is poorly understood and recent research is only just beginning to understand the biology of these species.

Figure 1. The Ambrosi Salamander (Hydromantes ambrosii) occurs throughout the French and Italian Alps to altitudes of 2,432 m. It does not rely on water for reproduction and often frequents caves and other underground systems to avoid desiccation.
[Photo credit: Benny Trapp, https://commons.wikimedia.org/wiki/File:BennyTrapp_Ambrosis_H%C3%B6hlensalamander_Speleomantes_ambrosii_Italien.jpg]

Previous research on cave salamanders of the genus Hydromantes in southern Italy has shown that these salamanders may reproduce at any time of year, being unconstrained by seasonal environmental changes that affect most non-cave dwelling species. It appears that in most species the female lays a small number of large eggs and protects them until hatching, guarding them from predators and preventing fungal infections (Figure 2). However, the detail of reproductive behaviours such as the number of breeding attempts and nest site selection remain unknown. Recently, Lunghi et al. (2018) carried out a four year study into cave salamanders within the genus Hydromantes at 150 sites in southern Italy. Lunghi et al. (2018) found that in several Hydromantes species the females may retain eggs for many months before releasing them, confirming that the large eggs require a long time to mature in the female before laying. This is followed by a period of at least 6 months of attending eggs and then parental care post-hatching. Therefore, these species require at least two years to complete one reproductive cycle. Given a life-span of only 11 years and maturity at 3-4 years of age, this restricts the number of available reproductive attempts by each female and limits population growth, which is of concern in threatened or vulnerable species. Lunghi et al. (2018) also found that nest site selection was extremely important and that each cave only had a limited number of suitable sites for nesting. Females would occupy only a small number of sites which would vary depending on the year and environmental conditions. This is supported by Lunghi et al. (2014) who found that the wrong choice of nest site can cause breeding failure. Successful breeding seems to occur in nest sites that have high humidity and low temperature. On a yearly basis, different females may use the same nesting site since suitable nests are highly limited. This further suggests that in some species population growth may be limited by suitable areas to breed.

Figure 2. The Italian cave salamander (Hydromantes italicus) lays between 6 and 14 eggs, which take 10 months to hatch into juveniles which resemble the adults (direct development). [Photo credit: Benny Trapp, https://commons.wikimedia.org/wiki/File:BennyTrapp_Speleomantes_italicus.jpg]

Living in cave environments can be challenging for salamanders as often prey densities are low. Relying on freshwater invertebrates may not always provide enough nutrition for species inhabiting these environments. Recent research by Fenolio et al. (2006) has shown that the Ozark Blind Cave Salamander (Eurycea spelaea) exploits another, less obvious food source. During a study to investigate the community ecology of bat caves in Oklahoma, USA, they found to their surprise that the larval salamanders were consuming bat guano. Initially the researchers thought that the ingestion of guano was incidental since consumption of non-food items in amphibians usually only occurs by accident whilst consuming their normal invertebrate prey. Fenolio et al. (2006) investigated this further and found that the salamanders were actually deliberately ingesting the bat guano as a food source. Nutritional analyses of bat guano revealed that it contained nutrients roughly equivalent to those that would be found in a potential prey item in this ecosystem, amphipods. The researchers also found that numbers of E. spelaea increased significantly in the main parts of the cave system where grey bats deposit fresh guano. This study contradicts the general understanding that salamanders are strictly carnivorous and shows that this adaptation enhances the survival of this species in this harsh environment.

Figure 3. The Ozark Blind Cave Salamander (Eurycea spelaea) of Missouri and southern Kansas, USA lives in caves and feeds on bat guano for nutrition.
[Photo credit: Peter Paplanus, https://commons.wikimedia.org/wiki/File:Eurycea_spelaea,_Izard_County,_Arkansas,_by_Peter_Paplanus.jpg]

Cave salamanders may also exhibit several morphological adaptations to living in dark and humid underground environments. The Ozark Blind Cave Salamander is also unique in that it starts life as a fully sighted larva but then metamorphoses underground into a terrestrial adult that loses its pigment and becomes blind, with the eyelids eventually fusing (AmphibiaWeb, 2016). There are several hypotheses to explain the reason for this morphological change. However, the most favoured is the energy economy hypothesis which states that the cost of developing and maintaining eyes is substantial and a large portion of the brain is needed for visual processing with high oxygen consumption rates. Energy savings from the loss of eyes could reduce the amount of time needed for foraging and allow energy to be re-invested into other physiological processes, including reproduction (AmphibiaWeb, 2016). In addition, eye loss may be linked to the process of skull development which is a pattern also observed in blind cavefish.

Cave salamanders are a unique group of amphibians with highly evolved ecology and life history characteristics. Unfortunately, an increasing number of cave salamanders are now threatened and classified as Vulnerable or Endangered on the IUCN Red List. Increasing our understanding of the ecology and biology of these declining species is critical in developing effective conservation initiatives, especially in cave environments which are prone to human-induced and climatic change.

References

AmphibiaWeb (2016) Eurycea spelaea: Grotto Salamander <http://amphibiaweb.org/species/4220> University of California, Berkeley, CA, USA. Accessed 27 September, 2019.

Fenolio, D.B., Graening, G.O., Collier, B.A. & Stout, J.F. (2006) Coprophagy in a cave-adapted salamander; the importance of bat guano examined through nutritional and stable isotope analyses. Proceedings of the Royal Society, London B, 273: 439–443.

Lunghi, E., Manenti, R., Manca, S., Mulargia, M., Pennati, R. & Ficetola, G.F. (2014). Nesting of cave salamanders (Hydromantes flavus and H. italicus) in natural environments. Salamandra, 50 (2): 105-109.

Lunghi, E., Corti, C., Manenti, R., Barzaghi, B., Buschettu, S., Canedoli, C., Cogoni, R., De Falco, G., Fais, F., Manca, A., Mirimin, V., Mulargia, M., Mulas, C., Muraro, M., Murgia, R., Veith, M. & Ficetola, G.F. (2018) Comparative reproductive biology of European cave salamanders (genus Hydromantes): nesting selection and multiple annual breeding. Salamandra, 54 (2): 101-108.

What our animals are doing this month…

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What our animals are doing this month… August 2019

August is the month that young grass snakes are likely to emerge from their eggs.  Previously in the year, gravid female grass snakes will have been seen basking more intensively than other grass snakes as they developed their eggs. During this time, females will fast for roughly 45 days whilst eggs develop and are laid.

Grass snakes usually just lay one clutch in a breeding year and do not necessarily reproduce on an annual basis. Eggs are laid in warm, secluded areas such as compost heaps, manure piles, old mammal holes, log piles or under rocks. These eggs need to be incubated anywhere from 22 days to 45 days depending on the environmental conditions. Areas of higher temperature have shown beneficial results for the numbers of eggs developing, with temperatures of 210C to 310C being preferred.

An average clutch size of eggs for a grass snake is 30 eggs, however many females may lay communally with others which can result in areas with thousands of eggs being incubated together.

By August hatchlings should emerge, measuring 15-20cm with the same identification features as adult grass snakes. Hatchlings use an ‘egg tooth’ to escape their egg by breaking the shell – this tooth is lost shortly after emerging.

Remember to report your sightings (including egg sightings) with our FREE Dragon Finder app.

Figure 1: Juvenile grass snakes can be easily identified being miniature versions of adults

Croaking Science: Heterospecific attraction: using the sounds of others to find the way

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Croaking Science: Heterospecific attraction: using the sounds of others to find the way

Amphibians may use a variety of cues to exploit new habitats including olfactory, visual and celestial cues. Often, individuals may use conspecific cues, i.e. those from individuals of the same species, to locate suitable habitats. For example, many pond-breeding amphibian of the genus Hyla and Rana, have been found to be attracted to calls of the same species (Buxton et al., 2015). However, the use of heterospecific cues, i.e. those from individuals of a different species, is less wide spread and our knowledge and understanding of how species use such cues is generally poorly understood. The heterospecific attraction hypothesis (HAH) has been proposed to describe how individuals may select habitats based on the presence of other species (Mönkkonen et al., 1997). Although initially described for birds, in recent years both field and laboratory experiments have shown an increasing number of amphibian species that use heterospecific cues to locate suitable habitats.

In the tropical forests of Taiwan a number of amphibian species co-exist, with varying degrees of niche overlap. Males of an oriental tree frog species, Rhacophorus prasinatus, form choruses in bushes and produce foam nests on vegetation near or above ephemeral and permanent water (Figure 1). Within the same habitat also lives Babina adenopleura which usually breeds at permanent water bodies and produces an egg mass in the water. This species is therefore a non-competitor as both species have different ecological requirements. However, Polypedates braueri is a resource competitor of R. prasinatus and uses ephemeral and water during the same time period and also produces a foam nest on vegetation. Research by Chang et al. (2018) has found that R. prasinatus frogs initially locate breeding aggregations of males using conspecific cues i.e. the cues of calling males of the same species. However, when these are lacking, they locate suitable habitat using the calls of the non-competitor B. adenopleura, rather than the competitor, P. braueri. This behaviour indicates that the calls of non-competitors could serve as cues for breeding site allocation (Chang et al., 2018). Since breeding sites are limited in this environment, avoiding choruses with heterospecific competitors, such as P. braueri, may reduce competition.

Figure 1. The tree frog Rhacophorus prasinatus from Taiwan may use the cues of another species, Babina adenopleura, to locate potential breeding sites. (Photo credit: Evan Pickett, licensed under the Creative Commons Attribution-Share Alike 4.0 International license. https://commons.wikimedia.org/wiki/File:Rhacophorus_prasinatus.jpg )

Many pond-breeding amphibians living in temperate areas often undergo dispersal to seek alternative breeding sites. In particular, in European newt genera such as Triturus, adults may switch breeding ponds in alternative years (Griffiths & Williams, 2000). The dispersal behaviour of individuals is often influenced by environmental factors such as food supply, predation risk, parasite load, and habitat disturbance (context-dependent dispersal) (Cayuela et al., 2018). However, individuals may also make decisions over dispersal direction, distance and habitat selection using the cues of other individuals (social-dependent dispersal). In central Europe great crested newts (Triturus cristatus), palmate newts (Lissotriton helveticus) and alpine newts (Ichthyosaura alpestris) may all co-habit the same ponds. Such newt species have a high degree of niche overlap, with great crested newts being competitively dominant, feeding on similar prey to the other species (Griffiths, 1994). Research by Cayuela et al. (2018) found that great crested newts make decisions on whether to leave a pond or occupy a new one based on the density of palmate newt and alpine newts. In this study, great crested newts were less likely to disperse from ponds which had a high heterospecifc density, i.e. a high density of palmate and alpine newts. In addition, the researchers found that when emigrating from ponds to seek other suitable breeding sites, great crested newts were more likely to select ponds which had a high density of palmate and alpine newts. These findings suggest that great crested newt adults do not avoid ponds with a high density of heterospecifics to limit the negative effects of interspecific competition on larval development and survival (Cayuela et al., 2018), but instead actively choose ponds where the density of other newt species is high. The presence of other newt species may indicate high pond quality with abundant food and egg laying resources, and since great crested newts are competitively dominant over the other newt species, they will gain by breeding in these ponds. The exact mechanism by which great crested newts can detect the density of other species within a pond is unknown, but is likely to be due to chemical cues (Cayuela et al., 2018).

Figure 2. Great crested (left), alpine (right) and palmate (below) newts all coexist in the same pond. (Photo credits: 1- Great crested newt: Rainer Theuer, licensed under the Creative Commons Attribution-Share Alike 2.5 Generic license. https://commons.wikimedia.org/wiki/File:Kammmolchmaennchen.jpg. 2- Palmate newt: Froglife. 3- Alpine newt: Anevrisme, Creative Commons Attributio)n-Share Alike 3.0 Unported license. https://commons.wikimedia.org/wiki/File:Triturus_alpestris.jpg. 

In Northern Italy, the smooth newt (L. vulgaris) breeds in similar water bodies to both the common toad (Bufo bufo) and green toad (B. viridis). In this region, the common toad breeds in large permanent water bodies and arrives at ponds in early February, whereas the green toad breeds in ephemeral water bodies and has a variable arrival time between February and March, depending on levels of rainfall (Pupin et al., 2007). Since smooth newts will breed in all types of pond, both toad species are therefore potential cues for water presence in a given area and may signal water quality. Research by Pupin et al. (2007) showed that smooth newts positively orientated towards the calls of both species and were using these to indicate location of potential breeding water bodies. Madden & Jehle (2017) carried out similar experiments on the great crested newt and found that individuals oriented to the calls of the common toad, but not common frog (Rana temporaria). They hypothesised that this was because common toads bred later than common frogs, at a more suitable time of year for great crested newts, so orienting towards ponds with common toads was more ecologically adaptive than those of common frogs.

Heterospecific attraction is a relatively newly studied process in amphibians and research has shown a number of examples when individuals use the cues of other species to locate and orientate towards suitable habitats. Such research has conservation significance since it shows the importance of food webs and community cohesion and demonstrates that different species are highly connected. Community level and landscape scale conservation, which targets the conservation of whole groups of species and widespread habitats, may therefore have high benefit to overall biodiversity.

 

References

Buxton, V.L., Ward, M.P. & Sperry, J.H. (2015) Use of chorus sounds for location of breeding habitat in 2 species of anuran amphibians. Behavioral Ecology, 26: 1111-1118.

Cayuela, H., Grolet, O. & Joly, P. (2018) Context‑dependent dispersal, public information, and heterospecific attraction in newts. Oecologia, 188 (4): 1069 – 1080. https://doi.org/10.1007/s00442-018-4267-3.

Chang, C., Cheng, Y. & Lin, S. (2018) Influence of conspecific and heterospecific cues on phonotaxis behaviour in a polyandrous treefrog. Behavioral Ecology and Sociobiology, 72: 179-190. https://doi.org/10.1007/s00265-018-2593-4.

Griffiths, R.A., Wijer P. de & May, R.T. (1994) Predation and competition within an assemblage of larval newts (Triturus). Ecography, 17 (2): 176-181.

Griffiths, R.A. & Williams, C. (2000) Modelling population dynamics of the great crested newt (Triturus cristatus): a population viability analysis. The Herpetological Journal, 10: 157-163.

Madden, N. & Jehle, R. (2017) Acoustic orientation in the great crested newt (Triturus cristatus). Amphibia-Reptilia, 38 (1): 57-65.

Mönkkonen, M., Helle, P., Niemi, G. & Montgomery, K. (1997) Heterospecific attraction affects community structure and migrant abundances in northern breeding bird communities. Canadian Journal of Zoology, 75: 2077-2083.

Pupin, F., Sacchi, R., Gentilli, A., Galeotti, P. & Fasola, M. (2007) Discrimination of toad calls by smooth newts: support for the heterospecific attraction hypothesis. Animal Behaviour, 74: 1683-1690. doi:10.1016/j.anbehav.2007.03.020.

Croaking Science: Caecilians – unusual reproductive ecology

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Croaking Science: Caecilians – unusual reproductive ecology

Caecilians, or blind snakes, as they are also often called, are limbless, elongate amphibians which inhabit tropical regions, with hotspots in South America and Asia (Kupfer et al., 2016; Gomes et al., 2012). Of all the groups of amphibians, caecilians are the most poorly understood, which is in part due to their secretive, fossorial lifestyle (Figure 1). They belong to the order Gymnophiona, one of three orders which comprises the Amphibia. There are currently 209 recognised species, which represents just 3% of the total 7,950 amphibian species worldwide (AmphibiaWeb, 2018). Caecilians are all ground-dwelling tropical amphibians which exhibit a wide range of reproductive modes, from laying eggs which hatch into aquatic larvae to those which hatch into miniature terrestrial juveniles. Little is known of their diverse reproductive modes but in recent years research has elucidated more information on their unusual breeding ecology.

Figure 1. Caecilians have an unusual appearance, being primarily fossorial and elongate in form. [Photo credit: Will Brown – Brown-snouted Blind Snake (Ramphotyphlops wiedii or nirgrogrescens) 3, CC BY 2.0,https://commons.wikimedia.org/w/index.php?curid=71399151]
Oviparous caecilians lay eggs, which are usually laid in a small terrestrial nest (Figure 2). The females of all these species exhibit extensive parental care, guarding their clutches of eggs against predators (Gomes et al., 2012). Eggs will hatch into either free-swimming larvae which develop in small water bodies, or terrestrial juveniles which are independent of their parents. Ichthyophis kohtaoensis inhabits the tropical forests of northern Thailand and belongs to the second largest caecilian family. In this species, breeding coincides with the rainy season with clutches of eggs laid in damp soil at the onset of the first rains (Kupfer et al., 2004). Females lay their eggs in small chambers near to temporary and permanent ponds, pools and slow flowing brooks and rivers. This allows the free-swimming larvae to readily hatch into the water to complete their aquatic development. Research suggests that females eat little or no food during the three month incubation period since the body condition of females attending young clutches is higher than those with older clutches (Kupfer et al., 2004). This, along with the small clutch size, indicates that there are costs to parental investment and attending eggs. In addition, there is a correlation between female body length and clutch size with older females being longer than young females (Kupfer et al., 2004). This implies that older, more experienced females produce larger clutches and more offspring (Kupfer et al., 2004).

Figure 2. A female caecilian guarding her brood of eggs from predators. [Photo credit: Davidvraju, Creative Commons Attribution-Share Alike 4.0 International, https://commons.wikimedia.org/wiki/File:Caecilian_guarding_its_eggs.jpg]
The ringed caecilian, Siphonops annulatus, is an unusual oviparous species inhabiting South America. The eggs hatch into poorly developed terrestrial young which feed on the skin of the female. The young possess specialised teeth which allow them to scrape skin from their mother’s back immediately after hatching (Wilkinson et al., 2008). The feeding behaviour of the young is described as being “quite frenetic with the young frequently tearing pieces of skin by spinning along their long axes and sometimes struggling over the same piece of skin” (Wilkinson et al., 2008) (Figure 3). This maternal dermatophagy is also known from a second, distantly related African caecilian species, Boulengerula taitana (Kupfer et al., 2008), which suggests that skin feeding is an ancient form of caecilian parental care and may have persisted for more than 100 million years (Wilkinson et al., 2008). In addition, Wilkinson et al. (2008) report a previously undocumented behaviour which involves the female raising herself upward, exposing her vent and releasing a clear fluid, which the young consume. This appears to be a form of feeding the young, but further studies are required to ascertain the function of this behaviour.

Figure 3. A caecilian mother with eggs which will hatch into young which feed off her skin. [Photo credit: Wilkinson M, Sherratt E, Starace F, Gower DJ (2013)]
Viviparous caecilians, which give birth to live young, represent another unusual reproductive mode for amphibians. During development inside the female, the foetuses initially obtain their nutrition from a yolk, similar to egg-developing species. After this, the developing young feed on a uterine milk, secreted from the oviducts of the female. The young obtain this through possessing specialised embryonic teeth which they use to scrape at the oviduct wall (Gomes et al., 2012). The evolution of viviparity in caecilians is poorly understood, but since both viviparous and oviparous species possess specialised teeth for scraping (either skin or oviduct milk), this suggests that all these species evolved from a common, oviparous ancestor (Kupfer et al., 2006). Gegeneophis seshachari is the only known species of viviparous caecilian from the Indo-Seychellean region (Gower et al., 2008). In this area the rainy season is short and unpredictable such that laying eggs which hatch into offspring that rely on the presence of water or a damp environment may be highly risky. Water bodies may dry up rapidly before larvae can fully develop. Therefore, Gower et al. (2008) propose that viviparity may have evolved in this species in response to short, unpredictable rainy seasons and the lack of suitable locations to lay and incubate their eggs.

Caecilians possess interesting and unusual reproductive modes, much of which is poorly understood. In addition, many of these species are threatened or Data Deficient and in regions which are undergoing large habitat loss and fragmentation. More primary data are required to fully understand caecilian reproductive ecology and evolution, which will help inform much needed improvements in conservation assessments for these species.

 

References

AmphibiaWeb (2018) https://amphibiaweb.org. University of California, Berkeley, CA, USA. Accessed 15 Nov 2018.

Gomes, A.D., Moreira, R.G., Navas, C.A., Antoniazzi, M.M. and Jared, C. (2012). Review of the reproductive biology of caecilians (Amphibia, Gymnophiona). South American Journal of Herpetology, 7 (3): 191-202.

Gower, D.J., Giri, V., Dharne, M.S. and Shouche, Y.S. (2008) Frequency of independent origins of viviparity among caecilians (Gymnophiona): evidence from the first ‘live-bearing’ Asian amphibian. Journal of Evolutionary Biology, 21: 1220–1226.

Kupfer, A.K., Nabhitabhata, J. and Himstedt, W. (2004) Reproductive ecology of female caecilian amphibians (genus Ichthyophis): a baseline study. Biological Journal of the Linnean Society, 83: 207-217.

Kupfer, A., Müller, H., Antoniazzi, M.M., Jared, C., Greven, H., Nussbaum, R.A. and Wilkinson, M. (2006) Parental investment by skin feeding in a caecilian amphibian. Nature, 440 (13 April 2006), doi:10.1038/nature04403.

Kupfer, A., Wilkinson, M., Gower, D.J. Müller, H. and Jehle, R. (2008) Care and parentage in a skin-feeding caecilian amphibian. Journal of Experimental Biology, 309A: 460–467.

Kupfer, A., Maxwell, E., Reinhard, S. and Kuehnel, S. (2016) The evolution of parental investment in caecilian amphibians: a comparative approach. Biological Journal of the Linnean Society, 119: 4–14.

Wilkinson, M., Kupfer, A., Marques-Porto, R., Jeffkins, H., Antoniazi, M.M. and Jared, C. (2008) One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona). Biological Letters, 4: 358–361.

doi:10.1098/rsbl.2008.0217