Snakes: Morphology, Function, and Ecology
David Penning
Abstract
Over the past two decades snakes have emerged as model organisms in studies focused on the interplay between foraging ecology and digestive physiology. Research on foraging mode in snakes has led to several advances and refinements to the foraging syndrome hypothesis, which links several biological traits of animals to foraging mode, while the integration of ecological and physiological data has resulted in the formulation of the adaptive digestion hypothesis. The adaptive digestion hypothesis posits that ambush foraging snakes feed infrequently due to their low rewards hunting strategy, and thus downregulate their digestive systems between meals as an energy saving adaptation. The accumulation of datasets across a broadening taxonomic base has recently allowed for more rigorous meta-analyses which have tested several of the underlying assumptions underpinning these hypotheses, calling some elements of the hypotheses into question. For example, ambush foraging snakes do not appear to be large meal specialists per se but rather consume a wider range of meal sizes due to morphological adaptations that allow for ingestion of very large meals. Ambush foraging snakes also have a marginally broader dietary breadth than active foragers. Upregulation of the digestive system in response to feeding is metabolically inexpensive and is driven primarily by hypertrophy, while the primary component to the cost of the specific dynamic action (SDA) is postabsorptive protein synthesis. Absorptive and postabsorptive digestive processes are fueled primarily by the metabolism of proteins derived directly from the digesting meal, calling the 'pay before pumping' model into question. Active and ambush foraging snakes have similar total costs of digestion, but SDA has a higher factorial increase and longer duration in ambush foragers. Adaptive regulation of digestive systems appears to be widespread across the Reptilia, and pH-neutral stomachs are likely to be the norm post digestion and are not unique to ambush foraging snakes. Collectively, these findings mean there is no categorical difference in the digestive physiology between foraging modes in snakes. Thus, the adaptive digestive hypothesis cannot stand in its current formulation and can no longer explain the lower standard metabolic rates (SMR) typical of ambush foragers. We present a new explanation of the foraging mode related differences in snakes: The supersizing hypothesis posits that the morphological adaptations allowing for ingestion of large meals in ambush foraging snakes must be matched by the ability to digest these meals. Since digestion of un-masticated meals can be initiated only at the meal surface, the smaller relative surface area of large meals has resulted in the selection of maximal digestive responses in ambushers, which is exemplified by a higher factorial increase in SDA. We support the activity capacity hypothesis, which contends that there is a relationship between SMR and maximum levels of aerobic metabolism, as the explanation of the relatively low SMRs in ambush foragers. Snakes deserve their model organism status, and we suggest several new avenues of investigation. We also contend that, potentially, snakes are important predators and research focused on snake foraging ecology has value in its own right.