Naïve garter snake chemosensory preferences corroborate diet of wild individuals and reveal behavioral convergence for foraging in deep water

Abstract Garter snakes are semi-aquatic obligate carnivores with diverse diets and behavioral adaptations for foraging at the water’s edge. In this study, we tested the persistence of innate chemosensory prey preference and aquatic prey capture ability in two garter snake species, the Lake Chapala garter snake (Thamnophis eques obscurus) and checkered garter snake (T. marcianus) that were captive bred and naïve to aquatic prey and aquatic prey capture contexts. Using number of tongue flicks, number of attacks, and attack latency as proxy for interest in terrestrial and aquatic prey extracts, we corroborated dietary preferences reported in the literature that described T. e. obscurus as an obligate forager and T. marcianus as a facultative aquatic forager in their native habitat. We then categorized strike mode and quantified several metrics describing prey capture efficiency at two treatment depths – shallow (2 cm; wading depth) and deep (10 cm; submerged depth). At shallow depths, T. e. obscurus used mostly forward strikes, had a greater gape angle, was more accurate at striking live mosquito fish, was faster at capturing fish prey, and had better visual acuity as indicated by pupil constriction. In shallow water, T marcianus used lateral strikes to capture prey. Foraging at increased depth resulted in forward strikes, larger gape angles, longer prey capture latency, longer foraging times, and greater pupil constriction in both species. Moreover, in deeper water, both snake species tended to stay underwater to transport (swallow) prey rather than resurface. We also compared head shape to help explain strike mode and found that T. e. obscurus had narrower and shorter heads compared to T. marcianus who had wider and taller heads. Our work provides insight into the innate prey preference of naïve snakes and their adaptability to aquatic prey capture contexts. Specifically, we show how an aquatic specialist is more efficient at capturing aquatic prey but that a terrestrial-aquatic generalist is flexible and exhibits behavioral variation across aquatic contexts. Finally, we show how the deep-water context requires behavioral convergence in strike mode, pupil constriction to respond to refractive changes in the water, and tests the ability of semi-aquatic snakes to stay underwater for longer periods of time.