Nature or Nurture: Can Prey-Based Diets Influence Species-Specific Physiological Performance Traits of Epidermal Lipid Content and Cutaneous Water Loss?

The physiological and behavioral conservation of water and protecting against dehydration is an important performance trait for many terrestrial species, especially those in arid climates. Species in arid habitats tend to have adaptations for lowering rates of evaporative water loss compared with those species from more mesic or aquatic habitats. Numerous studies have demonstrated the negative correlation between evaporative water loss and habitat aridity (e.g., Bentley and Schmidt-Nielsen 1966; Gans et al. 1968; Prange and Schmidt-Nielsen 1969; Elick and Sealander 1972; Cohen 1975; Baeyens and Rountree 1983; Roberts and Lillywhite 1983; Dmi’el 1998; Lillywhite 2006). Interestingly, evaporative water loss seems to correlate with habitat aridity regardless of taxonomic position (Dmi’el 1998) and is observed in other vertebrate taxa (e.g., Tieleman et al. 2003). Although many of these studies have examined interspecific comparisons of evaporative water loss and habitat aridity among a broad range of ophidian taxa, fewer studies have compared congeneric (Dunson and Freda 1985; Dmi’el 1998; Moen et al. 2005) or conspecific (Agugliaro and Reinert 2005) taxa. Miller and Lutterschmidt (2014) compared copperheads and cottonmouths, two closely related congeneric sister species in the genus Agkistrodon (Parkinson et al. 2000), to investigate if species differences in mesic versus aquatic habitat preferences correlated with their rates of cutaneous water loss (CWL). The species-specific physiological ability for limiting CWL may reflect individual adaptations that serve an important role in differences in habitat preference and resource partitioning (Miller and Lutterschmidt 2014). Because cutaneous (not respiratory) water loss is the primary source of evaporative water loss in squamates (Prange and Schmidt-Nielsen 1969; Cohen 1975; Dmi’el 1985; Dmi’el 2001), epidermal lipids in the integument serve a major role in regulating CWL in reptiles (Roberts and Lillywhite 1980). Potential species-specific differences in epidermal lipids may then serve as a potential mechanism allowing copperheads (Agkistrodon contortrix) to limit CWL and use and forage in more mesic and upland habitats, thus avoiding both direct and indirect competition with sympatric cottonmouths (Agkistrodon piscivorus). Copperheads consume mainly small mammals (Garton and Dimmick 1969; Brown 1979) which contain substantially more lipid than fish and amphibians consumed mainly by cottonmouths (Clark 1949; Kofron 1978). Thus, we raised the question: Is the lower CWL in copperheads (Moen et al. 2005; Miller and Lutterschmidt 2014) an adaptive species-specific physiological performance trait enhancing their ability to use more upland mesic habitats? Or, is the lower CWL in copperheads simply the product of a lipid-rich mammalian prey-preference more readily available in upland mesic habitats? Parkinson et al. (2000) investigated the phylogeography of the North American Agkistrodon species and found that A. contortrix exhibits the ancestral condition of terrestriality, with A. piscivorus exhibiting the only derived shift in aquatic habitat preference. Therefore, a more informed question may be: Is the higher CWL in cottonmouths a derived adaptive trait for lowering energetic cost in maintaining epidermal lipids less needed in an aquatic habitat? Or, is higher CWL in cottonmouths simply the product of lipid-poor prey (i.e., fish and amphibians) more readily available in aquatic habitats? As epidermal lipids (Roberts and Lillywhite 1980) and diets deficient in essential fatty acids influence CWL (Menton 1970; Elias and Brown 1978; Williams and Elias 1987), we compared the rates of CWL and conducted both quantitative and qualitative analyses of epidermal lipids for Northern Cottonmouths (A. piscivorus) fed either diets of fish (low-lipid) or mice (high-lipid). The cottonmouth served as an ideal model because this species is a diet generalist (Burkett 1966) and readily feeds on either fish or mice in the laboratory. This unique opportunity to manipulate diet experimentally allowed us to investigate if skin permeability and increased CWL in the cottonmouth are influenced by prey-based lipid content. Negative results for the influence of diet would then suggest that CWL is a fixed species-specific trait reflective of selection pressures for increased physiological performance in preferred microhabitats.