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Croaking Science: See-through frogs are worth a look

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

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

Figure 1: Several egg clutches on a single leaf

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

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

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

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

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

Further reading

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

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

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

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

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

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

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

Croaking Science: Mud-packing frogs: new approaches to protecting eggs

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The amphibian family Nyctibatrachidae forms one of the three oldest frog families and these species are found only in India and Sri-Lanka. Within the genus Nyctibatrachus there are currently 36 species, many of which have unique reproductive behaviours (see Croaking Science May 2019: https://www.froglife.org/2019/04/). Three closely related species within the genus occupy similar habitats on the forest floor, close to streams. Two of the species, Jog’s Night Frog (Nyctibatrachus jog) and the Kempholey Night Frog (N. kempholeyensis) both lay small clutches of eggs on leaves or branches overhanging slow-moving or still water bodies. The male then guards the eggs and provides water to prevent them drying out (AmphibiaWeb, 2011). However, the recently discovered Kumbara night frog (Nyctibatrachus kumbara) has a unique strategy for protecting its eggs. After laying a small clutch of between 4 and 6 eggs on a branch over-hanging water, the male collects mud and covers the eggs (Figure 1). This is thought to help protect the eggs from predators and prevent them from drying out (Gururaja et al., 2014). Covering eggs with mud in this way has not been recorded in any other species of frog and represents a unique method of protection (Gururaja et al., 2014). After covering the eggs with mud, the males will call to attract females which lay further clutches nearby. The male remains close to the egg clutches for several days until the eggs hatch. By exhibiting an alternative reproductive strategy, this species reduces competition between closely related species which occupy similar ecological niches.

Figure 1. The male Kumbara night frog (Nyctibatrachus kumbara) covers its eggs with mud. Left: a male starting to cover eggs with mud. Right: the male leaving the eggs once they have been covered with mud.  [Photo credit: Gururaja et al., 2014.]

References

AmphibiaWeb (2011) Nyctibatrachus jog: Jog’s Night Frog <http://amphibiaweb.org/species/7715> University of California, Berkeley, CA, USA. Accessed Jan 3, 2020.

Gururaja, K.V., Dinesh, K.P., Priti, H. & Ravikanth, G. (2014) Mud- packing frog: a novel breeding behaviour and parental care in a stream dwelling new species of Nyctibatrachus (Amphibia, Anura, Nyctibatrachus). Zootaxa, 3796: 33-61.

Croaking Science- Foot flagging: an alternative method of communication in frogs

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Traditionally, frogs and toads are considered to communicate primarily by using acoustic cues, with males typically calling to attract females. However, in noisy tropical rainforests by fast flowing streams, acoustic communication becomes more problematic. In these environments male frogs have evolved an array of visual cues which complement acoustic cues to communicate between each other and to also attract females. Visual communication has evolved independently in several lineages of frog species, mainly in diurnal species inhabiting noisy, stream-side environments.

Figure 1. Male frogs using foot-flagging in male-male communication. [Photo credit: Amézquita & Hödl, 2004.]

Foot-flagging has been observed in 16 frog species (Preininger et al., 2013). The male will typically arch and rotate its back foot in the air, giving a conspicuous visual signal (Figure 1). Males of the Bornean frog genus Staurois have evolved a unique foot-flagging behaviour which males use in a variety of contexts. The Sabah splash frog (Staurois latopalmatus) is found exclusively close to waterfalls where it can be observed regularly on exposed perches. Within this habitat, males signal in close vicinity to each other near to the water (Preininger et al., 2009). Preininger et al. (2009) have identified three types of visual displays: foot flagging, arm waving and vocal sac displays. Foot-flagging displays are mainly performed in the direction of a male opponent and appear to be used in territorial defence. Preininger et al. (2009) hypothesise that foot-flagging behaviour in this species has evolved from physical male-male combat where each male tries to push the other off its perch. The foot-flagging behaviour may be a ritualization of this aggressive combat, avoiding the need for physical contact. The other visual displays, arm waving and throat display appear to be used less frequently than foot-flagging during male-male aggressive encounters.

Figure 2. The Bornean rock frog (Staurois parvus) (left) from Borneo and the small torrent frog (Micrixalus saxicola) (right) from the Western Ghats of India both exhibit foot-flagging behaviour. [Photo credits: (left) Mohamad Jakaria, https://commons.wikimedia.org/wiki/File:Staurois_parvus.jpg; (right) L. Shyamal, https://commons.wikimedia.org/wiki/File:MicrixalusSaxicola1.jpg]

The Bornean rock frog (Staurois parvus) from Borneo and the small torrent frog (Micrixalus saxicola) from the Western Ghats of India belong to different frog families (Figure 2). Males of both species use complex signalling involving high pitched calls, foot flagging, and tapping (foot lifting) to defend perching sites against other males (Preininger et al. 2013). The Bornean rock frog has conspicuous white feet, whereas the small torrent frog has feet which are the same colour as its body. In a study to examine the differences in the behaviour of the two species, Preininger et al. (2013) found that in the Bornean rock frog, foot-flagging achieved a 13 times higher contrast against their visual background than the feet of the small torrent frog. In addition, the Bornean rock frog primarily responded to stimuli with foot flagging, whereas the small torrent frog responded mainly with calls but never foot-flagging on its own (Preininger et al. 2013). The authors propose that in the small torrent frog foot-flagging is in a transient state, evolving from its current use in physical fighting behaviour.

The colouration on the feet of foot-flagging species may signal more than male presence. Research by Stangel et al. (2015) has found that in two species (Staurois parvus and S. guttatus) the brightness of the feet increases with age. The peak brightness seems to coincide with sexual maturity and may be linked to androgen hormone levels in the males. The foot-flagging in these species may therefore convey information on the status of the male and his receptiveness to mate. This may be useful both to intruding males and also females which may be in the area.

African puddle frogs of the genus Phrynobatrachus are unique to Africa and are named after their breeding strategy of often laying large numbers of eggs in slow-moving or stagnant water bodies. In East African mountain streams lives a day time active frog, krefft’s river frog (Phrynobatrachus krefftii). Like other members of its genus males are dull brown in colour but also possess a striking bright yellow vocal sac (Figure 3). Instead of using foot-flagging for visual communication, males of this species communicate using a combination of acoustic cues and exhibiting their bright yellow vocal sac. Sometimes males will utter a call, accompanied by exhibiting their yellow vocal sac, whereas at other times no call will be emitted. Hirschmann & Hödl (2006) propose that the use of their brightly coloured vocal sac in this way has evolved to indicate the aggressive motivational state in the male.

Figure 3. Male krefft’s river frog (Phrynobatrachus krefftii) (right) possess a bright yellow vocal which they use in visual communication. Females (left) lack this colouration. [Photo credit: Hirschmann & Hödl, 2006.]

Further research into foot-flagging and other visual displays at different life stages will help increase our understanding of the function, development and evolution of visual signals in amphibians. Foot-flagging is only confined to a relatively few number of frog species and these are unable to survive in habitats modified for human use. Habitats where many of these unique species occur are increasingly threatened with habitat loss and fragmentation. Understanding the ecology of these species is therefore crucial in identifying and protecting key habitats in the wild.

References

Amézquita, A. & Hödl, W. (2004) How, when and where to perform visual displays: the case of the Amazonian frog Hyla parviceps. Herpetologica, 60 (4): 420–429.

Hirschmann, W. & Hödl, W. (2006) Visual signaling in Phrynobatrachus krefftii Boulenger, 1909 (Anura: Ranidae). Herpetologica, 62 (1): 18–27.

Preininger, D., Boechle, M. & Hödl, W. (2009) Communication in noisy environments II: visual signaling behavior of male foot-flagging frogs Staurois latopalmatus. Herpetologica, 65 (2): 166–173.

Preininger, D., Boechle, M., Sztatecsny, M. & Hödl, W. (2013) Divergent receiver responses to components of multimodal signals in two foot-flagging frog species. PLoS ONE, 8 (1): e55367. doi:10.1371/journal.pone.0055367.

Stangel, J., Preininger, D., Sztatecsny, M. & Hödl, W. (2015) Ontogenetic change of signal brightness in the foot-flagging frog species Staurois parvus and Staurois guttatus. Herpetologica, 71 (1): 1–7.

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.