Research Article |
Corresponding author: Daphne Soares ( soares@njit.edu ) Academic editor: Oana Teodora Moldovan
© 2017 Daphne Soares, Rachel Adams, Shea Hammond, Michael E. Slay, Danté B. Fenolio, Matthew L. Niemiller.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Soares D, Adams R, Hammond S, Slay ME, Fenolio DB, Niemiller ML (2017) Evolution of Coprophagy and Nutrient Absorption in a Cave Salamander. Subterranean Biology 24: 1-9. https://doi.org/10.3897/subtbiol.24.15013
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The transition from carnivory to omnivory is poorly understood. The ability to feed at more than one trophic level theoretically increases an animal’s fitness in a novel environment. Because of the absence of light and photosynthesis, most subterranean ecosystems are characterized by very few trophic levels, such that food scarcity is a challenge in many subterranean habitats. One strategy against starvation is to expand diet breadth. Grotto Salamanders (Eurycea spelaea (Stejneger, 1892)) are known to ingest bat guano deliberately, challenging the general understanding that salamanders are strictly carnivorous. Here we tested the hypothesis that grotto salamanders have broadened their diet related to cave adaptation and found that, although coprophagous behavior is present, salamanders are unable to acquire sufficient nutrition from bat guano alone. Our results suggest that the coprophagic behavior has emerged prior to physiological or gut biome adaptations.
Guano feeding, salamander, evolution, physiology, behavior
Coprophagy is a feeding strategy commonly found in invertebrates (
The literature is scarce when it comes to coprophagy in predatory amphibians (
All experiments were conducted under the approval of animal protocol #15022 by the Rutgers Newark Institutional Animal Care and Use Committee that handles NJIT research. We collected 46 specimens of Eurycea spelaea from January-Stansbury Cave located in the Ozark Plateau National Wildlife Refuge in Delaware County, Oklahoma. Salamanders were housed individually in mesocosms submerged in the cave stream. Each mesocosm consisted of a 500 ml plastic bottle with small holes so that the salamanders had continuous access to fresh cave water. All lids were connected to a central line via a short string. Salamanders were collected June 6th but the study did not until June 22nd, salamanders were fed amphipods until the start of the study. During the study, salamanders were fed every four days either a strict diet of live amphipods, bat guano, or nothing. We collected amphipods and bat guano fresh on the day of feeding from the cave. 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 (
All data associated with this study are available from the figshare digital repository: https://doi.org/10.6084/m9.figshare.4805656
Loss of body mass in treatment groups: All treatment groups lost some body mass during the study (34 days; Fig.
Regression lines based on body mass loss of different diet types and amounts. Salamanders were fed nothing (green), live amphipods (red) or guano (blue). Groups were fed every four days based on their initial body weight, with 2.5% (A), 5% (B) or 10% (C). The calculated regression lines were as follows: Control -1.16x+96.01 R2 = 0.54, n = 10; 2.5%amphipod -0.26x+98.49, R2 = 0.39, n = 6; 2.5%guano -0.70x+93.58, R2 = 0.02, n = 6; 5%amphipod -0.28x+102.22, R2 = 0.03, n = 6; 5%guano -1.12x+98.89, R2 = 0.77, n = 6; 10%amphipod -0.35x+103.36, R2 = 0.21, n = 6; 10%guano -0.70x+96.01, R2 = 0.53, n = 6.
Comparisons of weight loss: For salamanders fed 2.5% IBM, body mass loss rates for guano-fed and amphipod-fed groups were slower than the control group (Guano-fed: F = 6.82, P = 0.01; Amphipod-fed: F = 12.14, P = 0.0007) but not different from each other (F = 2.86, P = 0.09). For salamanders fed 5% IBM, guano-fed animals lost body mass at a slower rate than amphipod-fed animals (F = 11.05, P = 0.0012) and control animals (F = 14.75, P = 0.0002), while amphipod-fed animals lost body mass similarly to control animals (F = 0.07, P = 0.795). For salamanders fed 10% IBM, the amphipod-fed group lost body mass slower than the guano-fed group (F = 6.4, P = 0.131) and control group (F = 26.26, P = 1.09e-6), while the guano-fed group was similar to the control group (F = 8.02, P = 0.005).
All amphipod groups had individuals that lost and gained weight within the period of the study. The variability in body mass was smaller in the 10% amphipod IBM compared to the 5% and 2.5%, but a few individuals lost weight making the overall average mass at the end of the study slightly less than the IBM. The large variability in the 5% and 2.5% amphipod groups suggests that individuals may be behaving differently or some individuals may be stressed in the mesocosm. Nonetheless, since guano groups resemble more closely control groups we conclude that amphipods are a better food source for the salamanders.
Shifts in habitat are often linked with dietary shifts, as environmental changes frequently cause organisms to alter foraging behaviors (
The apparent disagreement between coprophagous behavior in Grotto salamanders and the lack of apparent absorption may have several possible explanations. First, Grotto salamander larvae, and salamanders in general, do not possess the morphological and physiological digestive traits necessary to exploit guano as a food resource. Salamanders in general are strict carnivores with short digestive tracts and have buccal enzymes with low amylolytic activity (
We thank Ozarks Plateau National Wildlife Refuge for lodging and cave access, Gal Haspel for help with the analysis, Sheilah Roenfeldt for field assistance, and Oklahoma Department of Wildlife Conservation for collection and research permits. This work was in part a product of Project E-22 entitled “Management and Protection for the Ozark Big-eared Bat, Gray Bat, and Stygobitic Fauna in Oklahoma,” and was funded by the Oklahoma Department of Wildlife Conservation.