Morphology and mechanics of tongue movement in the African pig-nosed frog Hemisus marmoratum: a muscular hydrostatic model.

The goal of this study was to investigate morphological adaptations associated with hydrostatic elongation of the tongue during feeding in the African pig-nosed frog Hemisus marmoratum. Whereas previous studies had suggested that the tongue of H. marmoratum elongates hydraulically, the anatomical observations reported here favour a muscular hydrostatic mechanism of tongue elongation. H. marmoratum possesses a previously undescribed compartment of the m. genioglossus (m. genioglossus dorsoventralis), which is intrinsic to the tongue and whose muscle fibres are oriented perpendicular to the long axis of the tongue. On the basis of the arrangement and orientation of muscle fibres in the m. genioglossus and m. hyoglossus, we propose a muscular hydrostatic model of tongue movement in which contraction of the m. genioglossus dorsoventralis, together with unfolding of the intrinsic musculature of the tongue, results in a doubling in tongue length. Electron micrographs of sarcomeres from resting and elongated tongues show that no special adaptations of the sarcomeres are necessary to accommodate the observed doubling in tongue length during feeding. Rather, the sarcomeres of the m. genioglossus longitudinalis are strikingly similar to those of anuran limb muscles. The ability to elongate the tongue hydrostatically, conferred by the presence of the m. genioglossus dorsoventralis, is associated with the appearance of several novel aspects of feeding behaviour in H. marmoratum. These include the ability to protract the tongue slowly, thereby increasing capture success, and the ability to aim the tongue in azimuth and elevation relative to the head. Compared with other frogs, the muscular hydrostatic system of H. marmoratum allows more precise, localized and diverse tongue movements. This may explain why the m. genioglossus of H. marmoratum is composed of a larger number of motor units than that of other frogs.

[1]  D. Wilkie,et al.  Muscle Physiology , 1959, Nature.

[2]  E. Reynolds.  THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY , 1963, The Journal of cell biology.

[3]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.

[4]  M. Rice.  Supercontracting Striated Muscle in a Vertebrate , 1973, Nature.

[5]  C. Gans,et al.  FUNCTIONAL ASPECTS OF THE EVOLUTION OF FROG TONGUES , 1976, Evolution; international journal of organic evolution.

[6]  Gretchen L. Humason,et al.  Animal Tissue Techniques , 1974 .

[7]  Philippa Horton,et al.  Diversity and Systematic Significance of Anuran Tongue Musculature , 1982 .

[8]  W. Cruce,et al.  Afferent and efferent components of the hypoglossal nerve in the grass frog, Rana pipiens , 1983, The Journal of comparative neurology.

[9]  W. Kier,et al.  Tongues, tentacles and trunks: the biomechanics of movement in muscular‐hydrostats , 1985 .

[10]  C. Gans,et al.  The role of hypoglossal sensory feedback during feeding in the marine toad, Bufo marinus. , 1992, The Journal of experimental zoology.

[11]  K. Nishikawa,et al.  The Kinematics of Prey Capture and the Mechanism of Tongue Protraction in the Green Tree Frog Hyla Cinerea , 1992 .

[12]  R. Olsson.  Functional Aspects I , 1993 .

[13]  D. Cannatella,et al.  THE MAJOR CLADES OF FROGS , 1993 .

[14]  Mechanism of tongue protraction during prey capture in the spadefoot toad Spea multiplicata (Anura: Pelobatidae). , 1995, The Journal of experimental zoology.

[15]  The kinematics and mechanism of prey capture in the African pig-nosed frog (Hemisus marmoratum): description of a radically divergent anuran tongue. , 1995, The Journal of experimental biology.

[16]  Feeding kinematics of phyllomedusine tree frogs. , 1995, The Journal of experimental biology.

[17]  C. Gans,et al.  Mechanisms of tongue protraction and narial closure in the marine toad Bufo marinus. , 1996, The Journal of experimental biology.

[18]  K. Nishikawa.  Emergence of Novel Functions During Brain Evolution , 1997 .

[19]  Distribution of hypoglossal motor neurons innervating the prehensile tongue of the African pig-nosed frog, Hemisus marmoratum , 1998, Neuroscience Letters.

[20]  K. Nishikawa.  CHAPTER 5 – Feeding in Frogs , 2000 .