Lizard and Snake Tongues as Muscular Hydrostats: Morphology, Function, and Diversity.

Evolution of the mobile tetrapod tongue replaced the functional roles of water during feeding in ancestral fish. The tongue as an analogue of water is most clearly manifested in the protean shape changes permitted by hydrostatic mechanisms intrinsic to the complexly muscled tongues of mammals and lepidosaurian reptiles (tuatara, lizards, snakes), which include the orthogonal and circular fiber systems characteristic of muscular hydrostats. I examine the morphology of lepidosaurian tongues and evidence for their use of hydrostatic mechanisms during several behaviors encompassing two major biological roles: feeding and chemoreception. Specifically, I consider, (a) lingual prey capture in iguanian lizards (and tuatara); (b) lingual prey capture in a non-iguanian species, the blue-tongued skink (Tiliqua scincoides); (c) tongue projection in chameleons; and (d) chemosensory tongue-flicking in lizards and snakes (squamates). All behaviors result in significant tongue protrusion beyond the jaw margins. During lingual prey capture in (non-chameleon) iguanians, tongue protrustion is tightly coupled to hyobranchial movement, with little evidence of hydrostatic shape change while visible, whereas lingual prey capture in Tiliqua is entirely dependent on extensive hydrostatic tongue deformation, including elongation, broadening, and elaborate, localized shape changes. Tuatara (Sphenodon) show no evidence of hydrostatic shape change as of yet. Tongue projection in chameleons depends on preloading elastic energy within the accelerator muscle via hydrostatic elongation. In vivo measurements from x-ray film of a chameleon with implanted markers show that elongation continues after projection throughout the ballistic phase until prey capture and that total accelerator muscle elongation is 267% of resting length. Finally, chemosensory tongue-flicking in all squamates, including iguanians, is driven by hydrostatic elongation. However, protrusion distance in iguanians is limited by the tongue's extensive anatomical coupling to the hyobranchium. Snakes exhibit a unique form of rapid, oscillatory tongue-flicking that is reflected in the tongue's derived muscle fiber architecture. I suggest that the extensive phenotypic variation present in lepidosaurian tongues might make them more effective than the better studied mammals as a model system for elucidating form-function relationships in a muscular hydrostat.