An energetic and morphological analysis of the adaptation to slug specialization in garter snakes (genus Thamnophis)

Behavioral, physiological, and morphological adaptations associated with diet specialization have been studied using optimal foraging theory based on the energy maximization premise. The premise states that dietary change can occur if the energy gained from eating low value prey is higher than the average energy gained from searching for preferred prey. An evolutionary change in foraging behavior can initiate selection for morphological and physiological adaptations for resource use, however, optimal foraging models often assume fixed digestive efficiency and other traits affecting handling time. I tested the improvement of digestive efficiency in slug foraging garter snakes relative to closely related fish-eating and generalist garter snakes. The Pacific Northwest garter snake, Thamnophis ordinoides, and coastal populations of the Western Terrestrial garter snake, Thamnophis elegans terrestris , specialize on banana slugs (Ariolimax sp.), which is a low energetic prey abundant in the Pacific Northwest, USA. The ranges of the inland populations of T. elegans elegans, which are generalist feeders, and T. couchii, which are fish specialists, do not overlap with banana slugs. The hypothesis that slug specialization leads to an increased assimilation efficiency when digesting slugs was tested in the four populations above. Results suggest that slug specialists may assimilate as much as 28% more energy from slug meals than T. e. elegans, and as much as 14% more than T. couchii. Assimilation efficiency from fish meals were similar among all four populations, suggesting an absence of energetic trade-offs occurring when slug specialists digest fish. Tooth morphology was also analyzed in the four populations in order to detect functional advantages in slug handling and swallowing by garter snakes. Neotropical snake species that specialize on slugs tend to have long, slender teeth thought to be adaptations for feeding on slippery prey. The results from SEM analysis suggest that the dentition of slug specialist garter snakes do not show evidence of homoplasy with the dentition of neotropical species. However, large posterior dental ridges located on the posterior-most maxillary teeth in the two slug predators suggest that more research is needed to determine the functional role of dental ridges in prey manipulation. In total, these studies address the role of digestive efficiency and tooth morphology among diverging populations of predators in using foraging theory to predict diet.