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Self and Conspecific Dermatophagy in the Aquatic Salamander Amphiuma tridactylum
Clifford L. Fontenot Jr. and John A. Pojman

Southeastern Naturalist, Volume 15, Issue 3 (2016): N40–N43

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2016 Southeastern Naturalist Notes Vol. 15, No. 3 N40 C.L. Fontenot Jr. and J.A. Pojman Self and Conspecific Dermatophagy in the Aquatic Salamander Amphiuma tridactylum Clifford L. Fontenot Jr.1,* and John A. Pojman2 Abstract - Dermatophagy, the practice of eating shed skin, in amphibians and reptiles has been reported anecdotally in the literature, but the process and purpose remains poorly understood. We document a fortuitous observation of whole-skin shedding and conspecific dermatophagy in Amphiuma tridactylum (Three-toed Amphiuma), and report on 2 additional observations of self-dermatophagy. Shed skins are potential protein and nutrient sources, and we suggest that dermatophagy may be a much more common occurrence than originally thought. Dermatophagy in amphibians and reptiles has been reported anecdotally (Noble 1931), although the function and importance remains poorly understood. A survey and review of dermatophagy (Weldon et al. 1993) substantially increased the number of documented species engaging in the behavior, heightened awareness of its occurrence, and stimulated discussion of its potential nutritional importance to the organism. Possible reasons for dermatophagy have been suggested and include recovery of nutrients (Bustard and Maderson 1965), removal and disposal of pathogens (Cramp et al. 2014), and even maternal care by feeding nutrient-rich skin to offspring (Kupfer et al. 2006). Despite increased attention to the occurrence of dermatophagy in amphibians, there are still many amphibian and reptile species for which dermatophagy is unknown. We do not know if the behavior is incidental or active, if skin is ingested whole or in pieces, and if self-ingested, or ingested by conspecifics. Here, we describe serendipitous observations of whole-skin shedding in Amphiuma tridactylum Cuvier (Three-toed Amphiuma), and the immediate ingestion of this shed skin by a conspecific individual, and self-dermatophagy in 2 addition al observations. As part of another study, we collected Three-toed Amphiuma adults from a roadside ditch in East Baton Rouge Parish, LA, using baited funnel-traps. We maintained the salamanders in the laboratory at ~25 °C in a 45-L cooler filled ~10-cm–deep with tap water for 6–8 days, then released them at the capture site. On 29 April 2013, we observed 2 individuals (sex undetermined) that were housed together in a container that included pieces of 76-mm–diameter PVC pipe as cover items. When one of individuals began mouth gaping, we started photo-documentation. We also observed ecdysis in 2 other adults that were individually housed in separate 45-L coolers. For the pair of adults housed together, ecdysis began for 1 individual at ~1725 h on 2 January 2016, with several mouth gapings over a few minutes. A chronological series of representative images document the ecdysis event (Fig. 1). Mouth gaping seemed to initiate the shedding process (Fig.1a), leading to the skin loosening from the cranial region to the first third of the body. The loosening was followed by frequent changes in head position and flexing right, downward, and left, while rubbing the body against the cooler and PVC pipe edges, and sliding the loose skin progressively from the head toward the tail (Fig. 1b). As the shedding individual entered one of the PVC pipes (Fig. 1c), the skin became increasingly bunched as it was pushed toward the tail (Fig. 1d), which was still protruding from the pipe. The other individual in the cooler then slowly approached the shed skin (Fig. 1e), and by 1Department of Biological Sciences, Southeastern Louisiana University, Hammond, LA 70402. 2Department of Chemistry, Louisiana State University, Baton Rouge, LA 70803. *Corresponding author - cfontenot@selu.edu. Manuscript Editor: Kristen Cecala Notes of the Southeastern Naturalist, Issue 15/3, 2016 N41 2016 Southeastern Naturalist Notes Vol. 15, No. 3 C.L. Fontenot Jr. and J.A. Pojman Figure 1. The arrow indicates the skin being shed. S indicates the shedding animal, and C indicates the consuming animal. (a) 1733 h, (b) 1737 h, (c) 1742 h, (d) 1745 h, (e) 1746 h, and (f) 1747 h. a quick buccal expansion (Erdman and Cundall 1984), sucked the skin into its mouth and pulled the bulk of the skin away in one piece (Fig. 1f). The salamander consumed most of the remaining skin pieces and debris over the next 2 min, with 3–4 more buccal motions, before slowly moving away from the shedding individual at 1748 h. In a separate situation, we observed skin loosening from the body of a female (snout to vent length [SVL] 610 mm) housed alone in a cooler at 1137 h on 2 January 2016), but did not note shedding movements or skin bunching. Shedding was complete by 1432 h, and the doughnut-shaped shed was similar to that described above for the other individual, but was located away from the female’s body. When we returned the next morning at 1000 h, the shed skin was gone, and presumed eaten. 2016 Southeastern Naturalist Notes Vol. 15, No. 3 N42 C.L. Fontenot Jr. and J.A. Pojman On 4 March 2016 at 1753 h, we observed skin loosening on a male (SVL 720 mm, 1695 g). In this case, shedding was complete by 1947 h, and the shed shin was gone (presumed consumed) when we returned the next morning at 0900 h. Our observations documented the ecdysis of the entire skin in essentially one piece within ~20 min. Unlike snakes (which shed their skin whole, inside-out), the skin was progressively loosened and slid along the body, cranial to caudal, becoming bunched together in its original orientation (i.e., not inside-out) as it was pushed toward the tail. Our description of shedding by the first individual represents the first account of dermatophagy by a conspecific individual in Three-toed Amphiuma. We note that this individual ate the shed skin while the shedding individual’s head and most of its body, were in the PVC pipe (Fig. 1e, f), and thus, the conspecific animal could not be deterred by the shedding individual. Our other 2 observations of isolated individuals shedding and presumably eating their own skin confirm self-dermatophagy, also reported by Weldon et al. (1993). Over years of research (since 1987 for C.L. Fontenot), we have housed more than 450 Three-toed Amphiuma individuals, for ~7 days each, and have kept several salamanders for 2–6 y, resulting in more than 3000 cumulative observation days. With all of these anecdotal observations and daily captive-care regimes, we never observed skin sheds in their containers, suggesting that dermatophagy may be common. Brode and Gunter (1959) described similar ecdysis behaviors for A. means Garden in Smith (Two-toed Amphiuma), including expansion of the body, peristalsis, and wriggling, based on at least 7 observations of 3 different individuals in separate aquaria. However, they suggested that “the process starts back of the gill slits with a dorsal gas bubble” in one of the cases, presumably referring to an air bubble released from the spiracle. Although it is common for Amphiuma spp. to release air bubbles after breathing air at the water surface, we observed neither air-breathing events nor the release of air bubbles during our observation of shedding in Three-toed Amphiuma. Brode and Gunter (1959) also indicated that each shedding event concluded with the shedding individual eating its own “roll” of skin from the tip of its tail. Taylor (1943) described similar behaviors for Two-toed Amphiuma, including “jaw stretching”, and substrate rubbing pushing the “roll” of skin toward the tail. However, there was also a Three-toed Amphiuma individual in the aquarium, which ate the shed skin of the Two-toed Amphiuma, thus documenting interspecific dermatophagy. Taylor (1943) strongly suggested that the Three-toed Amphiuma engaged in a distinct foraging mode of olfactory searching en route to the shedding Two-toed Amphiuma, then bit the wad of skin that was still attached to the tail, and began twisting/rolling its body to tear it away from the Twotoed Amphiuma. Why animals eat their skin remains largely unexplained, particularly for salamanders, but accumulating evidence suggests that it is an important nutrient source, particularly protein (Balogova et al. 2015, Bustard and Maderson 1965, Ferenti et al. 2010, Kopecky et al. 2011, Kupfer et al. 2006, Noble 1931, Taylor 1943, Weldon et al 1993). Given that dermatophagy is common in amphibians (Weldon et al 1993), shed skin may be a regular dietary component that is not related to food abundance (Kopecky et al. 2011), and whose proportionate representation in the diet varies with availability of skin (e.g., shed frequency, population density) and other food (Balogova et al. 2015, Ferenti et al. 2010). However, the prevalence of conspecific (this study, Brode and Gunter 1959), interspecific congener (Taylor 1943), and interorder (Kopecky et al. 2011) dermatophagy raises an important question: why don’t shedding individuals always eat their own skin? One of the overlooked results of skin shedding/sloughing is the effect on its epidermal microbial community. Shedding skin reduces the abundance of microorganisms, including N43 2016 Southeastern Naturalist Notes Vol. 15, No. 3 C.L. Fontenot Jr. and J.A. Pojman pathogens in Litoria caerulea White (Green Tree Frog; Cramp et al. 2014). Given the role of Batrachochytrium dendrobatidis Longcore, Pessier & D.K. Nichols (Amphibian Chytrid Fungus) and B. salamandrivorans A. Martel, Blooi, Bossuy & Pasmans (Salamander Chytrid Fungus) in amphibian declines (Lannoo 2005, Olson et al. 2013), dermatophagy may also be an important method of breaking a multistage life cycle, and so defend against such pathogens (Cramp et al. 2014). Microorganism reduction may be particularly important in temperate aquatic salamanders like Amphiuma because the relatively warm water of ponds and swamps they inhabit may serve as perennial pathogen sinks (Chatfield et al. 2012). On the other hand, consumption of skin that contains pathogens (e.g., metacircaria of the trematode parasite Megalodiscus temperatus) would facilitate transmission (Olsen 1974). Whether an individual has the ability to assess its pathogen load, and whether that influences the choice of self-dermatophagy, remains to be tested. Acknowledgments. Methods used in this work follow guidelines of the Society for the Study of Amphibians and Reptiles (http://www.asih.org/files/hacc-final.pdf) and were approved by the Animal Care Committee at SLU (IACUC, Protocol #0015) and LSU (protocol # 09-072). Literature Cited Balogová, M., E. Miková, P. Orendáš, and M. Uhrin. 2015. Trophic spectrum of adult Salamandra salamandra in the Carpathians, with the first note on food intake by the species during winter. Herpetology Notes 8:371–377. Brode, W.E., and G. Gunter. 1959. Peculiar feeding of Amphiuma under conditions of enforced starvation. Science 130:1758–1759. Bustard, H.R., and P.F.A. Maderson. 1965. The eating of shed epidermal material in squamate reptiles. Herpetologica 21:306–308. Chatfield, M.W, P. Moler, and C.L. Richards-Zawacki. 2012. The amphibian chytrid fungus, Batrachochytrium dendrobatidis in fully aquatic salamanders from southeastern North America. PloSone 7:e44821. Cramp, R.L., R.K. McPhee, E.A. Meyer, M.E. Ohmer, and C.E. Franklin. 2014. First line of defense: The role of sloughing in the regulation of cutaneous microbes in frogs. Conservation Physiology 2:doi:10.1093/conphys/cou012. Erdman, S., and D. Cundall. 1984. The feeding apparatus of the salamander Amphiuma tridactylum: Morphology and behavior. Journal of Morphology 181:175–204. Ferenti, S., A. David, and D. Nagy. 2010. Feeding-behavior responses to anthropogenic factors on Salamandra salamandra (Amphibia, Caudata). Biharean Biologist 4:139–143. Kopecký, O., J. Vojar, F. Šusta, and I. Rehak. 2011. Non-prey items in stomachs of Alpine Newts (Mesotriton alpestris Laurenti). Polish Journal of Ecology 59:631–636. Kupfer, A., H. Müller, M.M. Antoniazzi, C. Jared, H. Greven, R.A. Nussbaum, and M. Wilkinson. 2006. Parental investment by skin feeding in a caecilian amphib ian. Nature 440:926–929. Lannoo, Michael J. 2005. Amphibian declines: The Conservation Status of United States Species. University of California Press, Berkeley, CA. 1155 pp. Noble, G.K. 1931. The Biology of the Amphibia. McGraw-Hill, New York, NY. 577 pp. Olsen, O.W. 1974. Animal Parasites: Their Life Cycles and Ecology. 3rd Edition. University Park Press, Baltimore, MD. 562 pp. Olson, D.H, D.M. Aanensen, K.L. Ronnenberg, C.I. Powell, S.F. Walker, J. Bielby, T.W.J. Garner, G. Weaver, The Bd Mapping Group, and M.C. Fisher. 2013. Mapping the Global Emergence of Batrachochytrium dendrobatidis, the Amphibian Chytrid Fungus. PLoS ONE 8(2):e56802. Taylor, E.H. 1943. Skin-shedding in the Salamander, Amphiuma means. University of Kansas Science Bulletin 29:339–341. Weldon, P.J., B.J. Demeter, and R. Rosscoe.1993. A survey of shed-skin eating (dermatophagy) in amphibians and reptiles. Journal of Herpetology 27:219–228.