Kinetics of Tongue Projection in Ambystoma tigrinum: Quantitative Kinematics, Muscle Function, and Evolutionary Hypotheses

The projectile tongue of caudate amphibians has been studied from many perspectives, yet a quantitative kinetic model of tongue function has not yet been presented for generalized (nonplethodontid) terrestrial salamanders. The purposes of this paper are to describe quantitatively the kinematics of the feeding mechanism and to present a kinetic model for the function of the tongue in the ambystomatid salamander Ambystoma tigrinum. Six kinematic variables were quantified from high-speed films of adult A. tigrinum feeding on land and in the water. Tongue protrusion reaches its maximum during peak gape, while peak tongue height is reached earlier, 15 ms after the mouth starts to open. Tongue kinematics change considerably during feeding in the water, and the tongue is not protruded past the plane of the gape. Electrical stimulation of the major tongue muscles showed that tongue projection in A. tigrinum is the combined result of activity in four muscles: the geniohyoideus, Subarcualis rectus 1, intermandibularis posterior, and interhyoideus. Stimulation of the Subarcualis rectus 1 alone does not cause tongue projection. The kinetic model produced from the kinematic and stimulation data involves both a dorsal vector (the resultant of the Subarcualis rectus 1, intermandibularis posterior, and interhyoideus) and a ventral vector (the geniohyoideus muscle), which sum to produce a resultant anterior vector that directs tongue motion out of the mouth and toward the prey. This model generates numerous testable predictions about tongue function and provides a mechanistic basis for the hypothesis that tongue projection in salamanders evolved from primitive intraoral manipulative action of the hyobranchial apparatus. The morphology of the tongue projection mechanism in salamanders has been studied for over a century. In its most extreme condition, the tongue is projected up to 80% of the body length out of the mouth to contact prey (Duellman and Trueb, '86). In all salamanders, the tongue is also used after prey capture to hold prey against the roof of the mouth and t o manipulate food in the buccal cavity. Lunged terrestrial salamanders such as Ambystoma tigrinum have partially protrusible tongues and a buccal pump mechanism that is used in respiration. In lungless salamanders, the tongue and hyobranchium are modified to project the tongue greater distances and no longer function in respiration (Wake, '82). Morphological aspects of the tongue projection mechanism in salamanders have been the topic of several studies, and many of these present qualitative hypotheses describing the function of the system. Early discussions of the tongue projection mechanism based on morphological analysis provided detailed anatomical descriptions and proposed functions of the muscles involved (Driiner, '02, '04; Edgeworth, '35; Francis, '34; Krogh and Tanner, '72). Other studies presented interpretations of the functional morphology of salamander feeding mechanisms from com