Coprophagy in a cave-adapted salamander; the importance of bat guano examined through nutritional and stable isotope analyses

Abstract

During a two year population ecology study in a cave environment, 15 Eurycea (ZTyphlotriton) spelaea were observed ingesting bat guano. Furthermore, E. spelaea capture numbers increased significantly during the time that grey bats (Myotis grisescens) deposited fresh guano. We investigated the hypothesis that this behaviour was not incidental to the capture of invertebrate prey, but a diet switch to an energy-rich detritus in an oligotrophic environment. Stable isotope assays determined that guano may be assimilated into salamander muscle tissue, and nutritional analyses revealed that guano is a comparable food source to potential invertebrate prey items. This is the first report of coprophagy in a salamander and in any amphibian for reasons other than intestinal inoculation. Because many temperate subterranean environments are often energy poor and this limitation is thought to select for increased diet breadth, we predict that coprophagy may be common in subterranean vertebrates where it is not currently recognized.

Evolution of coprophagy and nutrient absorption in a Cave Salamander

“…In subterranean salamanders, the evolution of coprophagy may be an unusual foraging strategy to exploit a nutritious and seasonally abundant resource (i.e., bat guano) in an otherwise food-limited environment. While it has been demonstrated that Grotto salamander larvae will regularly employ coprophagy of calorically-rich bat guano (Fenolio et al 2006), our study suggests that Grotto salamander larvae are unable to thrive on a guano-exclusive diet for a prolonged period. So in this case the coprophagous behavior has emerged in evolution prior to the necessary physiological changes to gain nutrition from it.…”

“…The cave is inhabited by a maternity colony (ca. 15,000 individuals) of federally endangered Gray bats (Myotis grisescens A.H. Howell, 1909) from late April through early November (Fenolio et al 2006(Fenolio et al , 2014. Salamanders were randomly assigned to a negative control group, or one of two prey types and one of four feeding treatments based on percentage of initial body mass: 0% (control) 2.5%, 5%, and 10%.…”

“…Shifts in habitat are often linked with dietary shifts, as environmental changes frequently cause organisms to alter foraging behaviors (Rosalino et al 2005;McMeans et al 2015). The transition from surface to subterranean habitats involves dramatic morphological, physiological, and behavioral changes associated with life in complete darkness and often limited energy resources, including a predicted increase in dietary breadth (Culver 1982(Culver , 1994Holyoak and Sachdev 1998;Fenolio et al 2006). In subterranean salamanders, the evolution of coprophagy may be an unusual foraging strategy to exploit a nutritious and seasonally abundant resource (i.e., bat guano) in an otherwise food-limited environment.…”

“…The literature is scarce when it comes to coprophagy in predatory amphibians (Fenolio et al 2006). However, faces consist of a readily available food resource for animals living in energy-limited environments, such as caves.…”

“…Likewise, foraging in aphotic habitats of caves presents significant challenges for animals that potentially may go weeks to months between feeding bouts. Guano produced by seasonally roosting bats represents an important food source for both terrestrial and aquatic invertebrates (Howarth 1983;Poulson and Lavoie 2000), which in turn are prey for fishes and salamanders (Poulson and Lavoie 2000;Graening 2005;Niemiller and Poulson 2010;Fenolio et al 2006Fenolio et al , 2014. Salamanders have been known to be strictly carnivorous but Fenolio et al (2006) showed that obligate cave-dwelling Grotto Salamander larvae (Eurycea spelaea (Stejneger, 1892), Fig.…”