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Croaking Science: who are the salamanders?

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Written by Elsbeth Leighton, Coalface to Wildspace Project Assistant

The salamanders, or Caudata, are one of the three classes of animals that make up the Amphibians, alongside the Gymnophiona; the worm-like caecilians, and the Anura; the frogs and toads. The salamanders are the second largest group, after the Anura, comprised of over 800 known species. These species are split into 9 main families, with diverse traits and life histories (1).

Gaps in the amphibian fossil record make determining the exact evolutionary relationships between groups challenging and debated. However, it is generally agreed that there are three more basal, i.e. more ancient, families and the rest are younger and form a suborder called the Salamandroidea, otherwise called the advanced salamanders (2). A key difference between the ancient families and the younger families is in their reproduction. The ancient families fertilise their eggs externally, and the younger families fertilise them internally (3).

Cryptobranchidae

The Cryptobranchidae, commonly called the Giant Salamanders, is one of the ancient families and has 6 known living species (1). They live fully aquatic lifestyles as paedomorphic adults, meaning that they keep key features into adulthood that are usually seen in larval states. These features include their gill slits and their lack of eyelids (4). These are considered basal traits, along with their feeding behaviour. They are suction feeders, whose specialised jaw anatomy enables them to grab prey from one side of their mouth at a time (5). Well-known examples from this family include the giant Japanese salamander and the giant Chinese salamander, which can both grow over 100cm (6).

Photo © Andy Murch

Hynobiidae

The Hynobiidae, or the Asian Salamanders, branched from the same common ancestor as the Cryptobranchidae (2). They have 100 known species, distributed across Asia and Russia (1). Unlike the Cryptobranchidae, these salamanders live biphasic life cycles, where they fully metamorphose from aquatic larvae into terrestrial or aquatic adults without gills (4).  

Sirenidae

The Sirenidae, or the Sirens, are unique ancient salamanders that lack back legs entirely and only have small front legs. They have long bodies and external gills, suited to their fully aquatic lifestyles (4). All seven known living species are found in the southeastern USA and northeastern Mexico (1). Interestingly, some siren species eat plants and are omnivorous, whereas all other salamanders are generally believed to be carnivorous (7).

Ambystomatidae

The Ambystomatidae are part of the advanced salamanders and consist of 30 living species (1). They are commonly called mole salamanders because many of these species live a fossorial lifestyle in underground terrestrial burrows, only emerging at nighttime to feed. This is not the case for all species in this family, however, as it also includes aquatic paedomorphic species, such as the famous axolotl (4). The 4 species of Dicamptodon or Pacific Giant Salamanders, are also grouped into this family, having previously been considered a separate group (1).

Photo by Kevin Stohlgren

Salamandridae

The Salamandridae, or the true salamanders and newts, includes our UK native newts and is a large group with 144 species (1). They are found across Europe, Asia, northern Africa, and America and are the only family where some species reproduce viviparously. This means that they give birth to live young as aquatic larvae or fully formed terrestrial young, instead of laying eggs (8). The newts are found in the subfamily Pleurodelinae and can have two (biphasic) or three (triphasic) stage life cycles (4). Triphasic life cycles are unique to the newt and are seen in species such as the Eastern Newt, which develops from aquatic larvae into terrestrial juveniles before returning to the water again as aquatic adults (9).

Proteidae

The Proteidae are a small group, with only 9 species (1). They have long bodies and small limbs, living fully aquatic life cycles as paedomorphs who keep their external gills into adulthood. They include the mudpuppies from North America as well as the Olm, a blind cave-dwelling salamander from Europe (4). The Olm is a unique species and is thought to be the longest-lived salamander with a potential lifespan of over 100 years (10). There has been some confusion around how Olms reproduce and if they give birth to live young, partially due to the challenges their habitat presents for study, but the current understanding is that they lay eggs (11).

Rhyacotritonidae

The Rhyacotritonidae or torrent salamanders are another small group with only 4 species (1). They live a biphasic lifestyle and are semi-aquatic as adults, adapted to live alongside the edge of fast-flowing waterbodies such as streams. To adapt to these environments, their larvae have developed smaller gills to suit the fast-flowing water (4). They live in the Northwestern USA and are strongly associated with intact humid forests,  as damage to this habitat limits their ability to disperse (12).

Amphiumidae

The Amphiumidae or amphiumas are fully aquatic paedomorphic salamanders with gill slits and absent eyelids as adults. They have very small limbs, but unlike the sirens who only have front limbs, they have all four limbs (4). There are 3 known species living today, all of which are restricted to the Southeastern USA (1).

Plethodontidae

The final family, the Plethodontidae is the biggest group with 520 known species (1). They are known as the lungless salamanders because they evolved to lose their lungs and instead breathe entirely through their skin and a patch at the back of their throat containing a special protein (13). They are a very diverse group, occurring in a range of habitats mostly within the Americas, but some species are also known from Southern Europe and Korea (1). They display very varied reproduction, but the most common and ancestral method is direct development, where the larval stage is skipped entirely to produce fully developed terrestrial young from eggs. However, some species have re-evolved the ability to have aquatic larvae and lead biphasic lifestyles or are paedomorphic (8, 14).

 

References

  1. Frost, D. R., 2024. Amphibian Species of the World: an online reference.  Version 6.2 (15.07.2024). Electronic Database accessible at https://amphibiansoftheworld.amnh.org/index.php. American Museum of Natural History, New York, USA. 
  2. Pyron, R. A., John J. Wiens, J. J., 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians, Molecular Phylogenetics and Evolution, Volume 61, Issue 2, Pages 543-583,ISSN 1055-7903, https://doi.org/10.1016/j.ympev.2011.06.012.
  3. Vági, B., Marsh, D., Katona, G. et al. The evolution of parental care in salamanders. Scientific Reports. 12, 16655 https://doi.org/10.1038/s41598-022-20903-3
  4. Information on amphibian biology and conservation. [web application]. 2024. Berkeley, California: AmphibiaWeb. Available: https://amphibiaweb.org/. (Accessed: 2024)
  5. Matsumoto, R., Fujiwara, S.-i.,and Evans, S.E., 2024. The anatomy and feeding mechanism of the Japanese giant salamander (Andrias japonicus). Journal of Anatomy, 244, 679–707. Available from: https://doi.org/10.1111/joa.14004
  6. AmphibiaWeb 2022 Andrias davidianus: Chinese Giant Salamander <https://amphibiaweb.org/species/3858> University of California, Berkeley, CA, USA. Accessed Jul 14, 2024
  7. Schwarz, D., Fedler, M. T., Lukas, P., Kupfer, A., 2021. Form and function of the feeding apparatus of sirenid salamanders (Caudata: Sirenidae): Three-dimensional chewing and herbivory?, Zoologischer Anzeiger, Volume 295, Pages 99-116, ISSN 0044-5231, https://doi.org/10.1016/j.jcz.2021.09.008.
  8. Bonett, R. M., Ledbetter, N. M., Hess, A. J., Herrboldt, M. A., Denoël, M. Repeated ecological and life cycle transitions make salamanders an ideal model for evolution and development. Developmental Dynamics. 251(6): 957 -972. https://doi.org/10.1002/dvdy.373
  9. Species Account Citation: AmphibiaWeb, 2011. Notophthalmus viridescens: Eastern Newt <https://amphibiaweb.org/species/4265> University of California, Berkeley, CA, USA. Accessed Jul 14, 2024.
  10. Voituron, Y., de Fraipont, M., Issartel,, Guillaume, O.,and Clobert, J.,  2011. Extreme lifespan of the human fish (Proteus anguinus): a challenge for ageing mechanisms. Biol. Lett. 7. 105–107http://doi.org/10.1098/rsbl.2010.0539
  11. Recknagel, H., Premate, E., Zakšek, V., Aljančič, G., Kostanjšek, R., and Trontelj, P. 2022. Oviparity, viviparity or plasticity in reproductive mode of the olm Proteus anguinus: an epic misunderstanding caused by prey regurgitation?. Contributions to Zoology, 91(3), 153-165. https://doi.org/10.1163/18759866-bja10029
  12. Emel, S.L., Olson, D. H., Knowles, L. L. et al. Comparative landscape genetics of two endemic torrent salamander species, Rhyacotriton kezeriand R. variegatus: implications for forest management and species conservation. Conservation Genetics. 20, 801–815, https://doi.org/10.1007/s10592-019-01172-6
  13. Lewis, Z. R., Dorantes, J. A., and Hanken, J., 2018. Expression of a novel surfactant protein gene is associated with sites of extrapulmonary respiration in a lungless salamander. Proceedings of the Royal Society B. 28520181589 http://doi.org/10.1098/rspb.2018.1589
  14. Chippindale, P. T., Bonett, R. M., Baldwin, A. S., John J. Wiens, J. J., 2004. Phylogenetic evidence for a major reversal of life‐history evolution in plethodontid salamanders, Evolution, Volume 58, Issue 12, 1, Pages 2809–2822, https://doi.org/10.1111/j.0014-3820.2004.tb01632.x

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.

Croaking Science: Amphibians that change colour

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Amphibians that change colour – dichromatism in frogs and salamanders

Size dimorphism, where one sex is larger than the other, is common in amphibians and occurs in approximately 90% of frog and toad families. However, sexual dichromatism, where one sex is a different colour to the other has only been documented in approximately 122 (17%) of frog and toad species. There are two types of dichromatism: dynamic dichromatism, where males undergo a rapid colour change prior to the breeding season; and ontogenetic dichromatism where one sex remains a different colour the entire of its life once it has matured (Bell & Zamudio, 2012). Dynamic dichromatism occurs in 31 frog species but is probably under-recorded due to its ephemeral nature of only occurring for short periods around breeding. Ontogenetic dichromatism appears more common, being documented from 91 anuran species. However, our understanding of the mechanisms behind colour change in frogs is still limiting.

The Wood Frog (Rana sylvatica) exhibits ontogenetic dichromatism with males being tan or dark brown whereas females tend to be redder in colour (Figure 1). Previous experiments have shown that males are attracted to red females but are ambivalent towards darker coloured females. Being able to readily distinguish the sexes is likely to be important for Wood Frog males, as the breeding season may last only 1–3 days in early spring (March and April) and high male-male competition often results in only a small percentage of males succeeding in mating. Research by Lambert et al. (2017) has shown that sexual dichromatism in Wood Frogs is absent immediately after metamorphosis but develops and persists through the second spring and summer. Unlike some frog species, where the body colour change is almost instantaneous and lasts only a few days, the colouration alteration in Wood Frogs takes weeks to develop and lasts for several weeks after the breeding season. Currently, it is unclear which environmental conditions (e.g., light, temperature, food, etc.) influence the colour change after hibernation. It is also unclear why the frogs remain with colour dichromatism for extended periods when breeding only lasts a few days. It seems likely that the colour change has evolved as a result of both sexual and natural selection. Females which are redder in colouration are more easily identifiable by males during the short breeding season. In addition, the colour changes may provide the different sexes protection from predation. Redder females are more camouflaged on the forest floor during terrestrial migration and may benefit from reduced predation. In contrast, the dark tan or brown males have greater camouflage whilst aggregating around ponds when they are at greatest risk from predators. Therefore the differences in colour between males and females in Wood Frogs may offer benefits for reproduction and survival.

Figure 1. Female (left) and male (right) Wood Frogs demonstrating colour dichromatism. (Photo Credit: Lindsey Swierk)

Sexual dichromatism is much rarer in newts and salamanders and has only been reported from a few species. The development of graphic software has enabled researchers to examine in more detail the dorsal patterning in relation to colour quality patterns such as hue, sat­uration, brightness, or quantity of each spot on the dorsal and ventral sides. Using such techniques in salamanders have revealed sexual dichromatism which was previously unnoticed to the naked eye.  For example, in adult Red-spotted Newts (Notophthalamus viridescens) image analysis software was used to demonstrate that males have more intensely red dorsal spots compared to females. Recent work by Balagova and Uhrin (2015) on the Fire Salamander (Salamandra salamandra) has shown that males have a greater amount of yellow dorsal patterns compared to females (Figure 2). Since the reproductive strategy involves female choice, the authors hypothesise that females may be able to select males based on their dorsal patterns. In this species the dorsal patterns indicate toxicity to predators so a brighter individual with a greater amount of patterning may be more effective at deterring predators. The authors suggest that females may select males with brighter and a greater amount of patterning since they offer greater protection from predators and their offspring will inherit this characteristic. In addition, females may have a greater proportion of black colour to absorb more heat which would result in faster egg development.

Figure 2. Male Fire Salamanders (Salamandra salamandra) have a greater proportion of yellow markings compared to females. (Photo Credit: Adobe stock)

Overall, recent research suggests that we are gaining in understanding of the distribution of sexual dichromatism among amphibian species, but that we still know very little about its function. In addition, dichromatism in amphibians offers benefits for investigating the relative roles of natural selection and sexual selection in the evolution and origins of sexual dichromatism and its significance for a range of amphibian species.

References

Bell, R.C. & Zamudio, K.R. (2012) Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity. Proc. R. Soc. B. 279 (4): 4687-4693.

Lambert, M.R., Carlson, B.E., Smylie, M.S. & Swierk, L. (2017) Ontogeny of sexual dichromatism in the explosively breeding wood frog. Herpetological Conservation and Biology 12 (2):447-456.

Balogová, M. & Uhrin, M. (2015) Sex-biased dorsal spotted patterns in the fire salamander (Salamandra salamandra). Salamandra 51 (1): 12-18.

Croaking Science: Territorial behaviour in frogs and salamanders

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Territorial behaviour in frogs and salamanders

Within the amphibians territorial behaviour is usually confined to the breeding season, when males will often aggregate to attract females. Males from many amphibian species form temporary leks where each male will display or call from a defended area to attract females. These loosely defined territories are usually only temporary and occupy the immediate area around the individual. However, there are several groups of amphibians which exhibit more complex and permanent territoriality such as the plethodontid salamanders from North America and poison dart frogs from South America. Poison dart frogs (Dendrobatidae) exhibit complex spatial behaviour, including territoriality. Individuals typically occupy a defended home range and transport eggs to a variety of small water bodies, usually within the axils of plants. Allobates femoralis is a diurnal dendrobatid poison dart frog, living in moist tropical forests of South America (Figure 1). Males defend a territory of approximately 13 m2 (Pašukonis et al., 2013). Previous research on the territorial behaviour of A. femoralis shows that 80% of males translocated to distances of 200 metres from their territories returned and 30% showed a return success rate when translocated 400 metres from their home site (Pašukonis et al., 2013). Pichler et al. (2017) recently carried out homing behaviour experiments on A. talamancae, which has similar ecology to A. femoralis. Pichler et al. (2017) found that 70% of individuals which were moved over 200 metres from their territories were able to return. In addition, they found considerable differences in the return time between individual frogs. Some frogs which were translocated 20 metres took 11 days to return where as others which were moved 200 metres took only 3 days to find their way back to their territories. These differences could be due to a range of factors including: an individual’s fitness, familiarity of their territory, motivation to return, as well as environmental factors such as habitat type and the number of distinctive homing markers. These studies show that such territorial species have excellent spatial awareness and are able to return to their known territory even after being moved outside of their normal home range.

Figure 1: Allobates femoralis is a poison dart frog which is able to relocate its own territory after translocation. (Photo credit: Alessandro Catenazzi – http://calphotos.berkeley.edu)

Frogs which exhibit territorial behaviour often defend the boundaries of their territories using a variety of vocal calls. However, recent research has shown that males are able to discriminate between established neighbours and unfamiliar strangers. This so called ‘dear enemy’ effect (Fisher, 1954) may serve to allow territory holders to avoid the costs of repeated aggressive encounters with familiar occupants of nearby territories which are likely to pose less of a threat than less familiar individuals. The olive frog (Babina adenopleura) is a common species throughout Southeast Asia. Males defend small territories using distinctive vocal calls and physical combat. Males produce a variety of calls including advertisement, encounter and territorial calls. Recent research by Chuang et al. (2017) has found that territorial males respond more aggressively towards strangers compared to known neighbours. These findings demonstrate that in this species, males are able to perceive and behave differently towards vocal calls from different intruding males.

Many species of plethodontid salamanders native to North America exhibit territoriality, defending cover objects or areas with high prey availability. Territories are defended by pheromone markers and distinctive body postures, which sometimes escalate to biting if the intruder does not withdraw. One territorial behaviour has been termed the ‘‘All Trunk Raised’’ (ATR) posture, where the salamander lifts its entire trunk off the substrate. It is thought that this makes the individual look larger and is energetically costly. In response to threat behaviour, individuals can retreat or assume a submissive posture. The ozark zigzag salamander, Plethodon angusticlavius, occurs in southwestern Missouri, northwestern Arkansas, and western Oklahoma in streamside woodlands under rocks, logs, and leaf litter. Recent research by Bortosky & Mathis (2016) has shown that ATR is an honest signal that shows aggressive intent. Individuals that spent more time in the ATR posture, were more likely to bite intruders than ones which spent less time in ATR. The authors also found a correlation between the ATR posture and energetic activity, which indicates that it is costly to maintain the ATR posture. These findings support the hypothesis that aggressive encounters are more likely to be settled when the ATR posture is used by a male and this is the result of an honest signal.

Figure 2: The ozark zigzag salamander of North America performs honest signalling when they encounter intruders in their territories. (Photo credit: Stanley Trauth – http://calphotos.berkeley.edu)

References 

Bortosky, R. & Mathis, A. (2016) Honest signaling in aggressive contests between ozark zigzag salamanders (Plethodon angusticlavius). Copeia, 104 (1): 60–66.

Chuang, M-F., Kam, Y-C. & Bee, M.A. (2017) Territorial olive frogs display lower aggression towards neighbours than strangers based on individual vocal signatures. Animal Behaviour, 123: 217-228.

Fisher, J.B. (1954) Evolution and bird sociality. In J. Huxley, A.C. Hardy & E.B. Ford (Eds), Evolution as a Process. Pp 71-83, Allen & Unwin, London.

Pašukonis, A., Ringler, M., Brandl, H.B., Mangione, R., Ringler, E. & Hödl, W. (2013) The homing frog: high homing performance in a territorial dendrobatid frog Allobates femoralis (Dendrobatidae). Ethology, 119: 762–768.

Pichler, C., Weinlein, S., Kopeinig, L. & Pašukonis, A. (2017) Homing performance in a territorial dendrobatid frog, Allobates talamancae. Salamandra, 53 (2): 309-313.

Croaking Science: Newts that never grow up!

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Newts that never grow up – paedomorphosis in salamanders

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

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

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

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

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

 

References

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

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

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

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

DOI: 10.1098/rspb.2017.0176.

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

Lethal Chytridiomycosis in Salamanders

by

Fire Salamander

Croaking science is a new way for student volunteers and scientist to explore what’s occurring in the world of Science. Croaking Science looks at science facts, new research or old debates which are inspired by or affect amphibians and reptiles, and then communicates this in layman’s language to a wider audience. The aim of the feature is to provide a platform for those starting their foray into the world of science communications as well as established scientists. We welcome any submissions from students and scientists. Please note that the views expressed in the articles are not those of the Froglife Trust.

Croaking Science reporter Rhiannon Laubach looks at the history of chytridiomycosis and its impacts on the Fire Salamanders in Europe

The current worldwide loss of amphibians has reached crisis level. Some 40% of amphibian species in parts of Central America are at risk of extinction and there are also large scale losses in Europe, North America and Australia.  The main cause for this is an infectious disease known as ‘fungal chytridiomycosis’, chytrid or Bd for short.  Click here for a map showing global chytrid distribution.

Chytrid is a fungus that infects vertebrates with spores that grow in the top keratin layers of the infected host’s skin. Symptoms of chytridiomycosis in amphibians include lethargy, lost righting reflex and an abnormal posture. The amphibian’s skin can be ulcerated and slough off in an uncharacteristic way and haemorrhages can occur in the eyes, muscles and skin. The disease is fatal to almost all amphibians (Martel & al 2014).

The earliest evidence for chytrid has been found in a museum collection of African clawed frogs that were collected in Africa in 1938. The exportation of these frogs around the world, for human pregnancy testing and other research, is the likely vector for the spread of the fungus. The first case of chytrid outside of Africa was recorded in North America in 1961 (Laurence 2008). Its spread is made easier because particular species such as the African clawed frog can be affected by the fungus asymptomatically meaning that they do not show any symptoms of the disease.

It used to be thought that there was only one species – Batrachochytrium dendrobatidis – with several different strains that infected all amphibians. However, Dutch scientists studying high mortality rates in the fire salamander (Salamandra salamandra) have discovered a new species of chytrid known as Batrachochytrium salamandrivorans (meaning salamander skin-eating fungus).

In the Netherlands, the fire salamander population has decreased so dramatically that it has brought it to ‘the edge of extinction’ in this country.  From 2010 to 2013, the salamander population decreased by 96%.  When researchers analysed the dead salamanders to see what was causing the fatalities, they were able to isolate the new species of chytrid.

Salamanders that are affected by this disease, usually die after suffering from anorexia, apathy and ataxia.  The infected animals have deep ulcers and shallow erosions all over their bodies which are then colonised by bacteria.

It was necessary for the researchers to find out if the new chytrid species was definitely the cause of the salamandrid mortality.  These experiments involved infecting salamanders with chytrid.  This research seems quite cruel but was necessary as the researchers needed to see how the fungus infected the salamanders.

Summary of experiment:

  • Healthy salamanders were inoculated with spores of the chytrid fungus, they all died by day 18.  Two healthy salamanders where introduced into the tank, these salamanders where fatally infected.
  • The common midwife toad (Alytes obstetricans) is easily infected by Batrachochytrium dendrobatidis, toads have been experimentally infected with Batrachochytrium salamandrivorans.  The toads where not colonised bythe new fungus species suggesting that it does not affect, or easily affect, other amphibian species such as frogs or toads (Martel & al 2014).

Amphibians are a diverse and charismatic class of species.  On a worldwide scale they are increasingly threatened by a wide range of threats such as habitat loss and climate change. Chyrtrid may be what pushes many vulnerable species to extinction.  As a result of their plight 2014 has been designated as Year of the Salamander by the Amphibian Survival Alliance and their partners.

What you can do

This can be a depressing topic but there are things that we can all do to help protect amphibian populations:

  • Find out more, click here to find out more about Chytrid
  • Try to make your gardens as amphibian friendly as possible
  • Record and monitor the health of amphibian populations.  You can report diseased or dead animals found in your garden to the Garden Wildlife Health project.  This will help researchers build a better picture of the state of our garden wildlife and understand the threats that it faces
  • Support amphibian friendly charities.  There are lots of ways you can support Froglife you can: become a Froglife Friend, donate, shop online with Give as you Live (at no extra cost to you) or volunteer

References

Lawerence, D. (2008). Batrachochytrium dendrobatidis, Chytrid disease. Available: http://depts.washington.edu/oldenlab/wordpress/wp-content/uploads/2013/02/Batrachochytrium-dendrobatidis_Lawrence.pdf. Last accessed 2nd April 2014.

Martel,A., Spitzen-van der Sluijs, Blooi, M., Bert, W., Ducatelle, R., Fisher, M., Woeltjes, Bosman,W., Chiers, K.,Bossuyt,F., Pasmans, F. (2014). Batrachochytrium salamandrivon sp nov. causes lethal chytridiomycosis in amphibians. Available: www.pnas.org/cgi/doi/10.1073/pnas.1307356110. Last accessed 31 March 2014.