The function of oscillatory tongue-flicks in snakes: insights from kinematics of tongue-flicking in the banded water snake (Nerodia fasciata).

Tongue-flicking is an important sensory behavior unique to squamate reptiles in which chemical stimuli gathered by the tongue are delivered the vomeronasal organ situated in the roof of the mouth. Because tongue-flick numbers can easily be quantified, this behavior has been widely used as a measure of vomeronasal sampling in snakes using related variables such as tongue-flick rate or tongue-flick/attack score. Surprisingly, the behavior itself and especially the function of the oscillatory tongue-flicks remains poorly understood. To describe the overall kinematics of tongue-flicking in the colubrid snake Nerodia fasciata and to test predictions on the function of oscillatory tongue-flicks, we filmed the tongue-flicks of 8 adult Nerodia fasciata using 4 synchronized high-speed cameras. Three-dimensional kinematic and performance variables were extracted from the videos in order to quantify tongue movements. Based on the kinematic analysis, we demonstrate the existence of 2 functional and behavioral tongue-flick categories. Tongue-flicks with oscillations meet all the criteria for being adapted to the collection of odorants; simple downward extensions appear better suited for the rapid pick up of nonvolatile chemical stimuli from the substrate or a food item. External stimuli such as tactile and/or vomeronasal stimulation can induce a shift between these categories.

Chemical basis of prey recognition in thamnophiine snakes: the unexpected new roles of parvalbumins.

Detecting and locating prey are key to predatory success within trophic chains. Predators use various signals through specialized visual, olfactory, auditory or tactile sensory systems to pinpoint their prey. Snakes chemically sense their prey through a highly developed auxiliary olfactory sense organ, the vomeronasal organ (VNO). In natricine snakes that are able to feed on land and water, the VNO plays a critical role in predatory behavior by detecting cues, known as vomodors, which are produced by their potential prey. However, the chemical nature of these cues remains unclear. Recently, we demonstrated that specific proteins-parvalbumins-present in the cutaneous mucus of the common frog (Rana temporaria) may be natural chemoattractive proteins for these snakes. Here, we show that parvalbumins and parvalbumin-like proteins, which are mainly intracellular, are physiologically present in the epidermal mucous cells and mucus of several frog and fish genera from both fresh and salt water. These proteins are located in many tissues and function as Ca(2+) buffers. In addition, we clarified the intrinsic role of parvalbumins present in the cutaneous mucus of amphibians and fishes. We demonstrate that these Ca(2+)-binding proteins participate in innate bacterial defense mechanisms by means of calcium chelation. We show that these parvalbumins are chemoattractive for three different thamnophiine snakes, suggesting that these chemicals play a key role in their prey-recognition mechanism. Therefore, we suggest that recognition of parvalbumin-like proteins or other calcium-binding proteins by the VNO could be a generalized prey-recognition process in snakes. Detecting innate prey defense mechanism compounds may have driven the evolution of this predator-prey interaction.