Evolutionary mechanics of protrusible tentacles and tongues

This paper provides: a comparison at multiple levels of structural organiza tion of the biomechanics of plotrusible muscular systems with different ori gins and phylogenetic history. The high-performance prey capture tentacles in squid, the tongues of frogs and salamanders, and the tongue of the chame leon ale used as examples. The tentacles of squid are muscular organs that lack bony elements. They ar e rapidly elongated during prey capture (typical extension time 25 ms, peak acceleration of approximately 250 m.s(-2)) by extensor muscles that have r emarkably short sarcomeres (myosin filaments are only 0.5 to 1.0 mu m, comp ared with 1.6 mu m in vertebrates). Short sarcomeres generate only relative ly small forces, but relatively high absolute strain rates for a given inte rflamentary sliding velocity (at low external loads). A forward dynamics mo del (VAN LEEUWEN & KiER, 1997) predicts the movements of the tentacles with reasonable accuracy and predicts also that the short sarcomeres provide op timal extension velocity. Several frogs (Hemisotidae and Microhylidae) have a similar extension mechanism in their tongue (denoted as hydrostatic elon gators by NISHIKAWA, 1999b) to that found in the tentacles of squid. The ex tension performance is, however, limited relative to that observed in squid . This can be explained by two factors. First, the extensor fibres run in o ne direction only, while in the squid the fibres are arranged in circumfere ntial arcs as well as in two other fibre groups that run at right angles to each other. The unidirectional fibre orientation results in a smaller exte nsion For a given shortening of the extensor fibres than observed in the te ntacle. Second, the myosin filaments in the extensor muscle of the frog ton gue are similar to those found in other vertebrate skeletal muscle. It is l ikely that the filament lengths are not optimised for a high peak extension velocity although data are lacking thus far. These limitations have been c ircumvented by several groups of frog (Bufonidae, Ranidae and others) that 'throw' their tongue out of the mouth by a rapid jaw movement (inertial elo ngators). The ballistic tongues of many plethodontid salamanders extend in less than 10 ms, The most extreme performance is found in Hydromantes supramontis, wh ich elongates the tongue up to 80% of body length. The paired cylindrical p rotractor muscles envelope two elongate epibranchials, the posterior 'legs' of the tongue skeleton. The complete tongue skeleton is projected with the tongue pad. The normal stress of the protractor muscle on the tapered epib ranchials is postulated to be the main projection force (DEBAN er al., 1997 ). We suggest that a build up of a 'pre-stress' in the protractor and an as sociated storage of elastic energy in connective tissues prior to projectio n may be essential for rapid projection. Detailed kinematic studies of plet hodontid tongue projection are needed. The ballistic chameleon tongue has a remarkable performance, with a reporte d peak acceleration of the tongue during prey capture of about 500 m.s(-2) A cylindrical accelerator muscle envelopes the elongated entoglossal bone a nd is projected out of the mouth with the tongue pad. The extreme performan ce is likely due to a combination of several factors. First, the arrangemen t of muscle fibres in spiral arcs allows for close packing and uniform work output of the accelerator muscle fibres (VAN LEEUWEN, 1997). Second, pre-s tress in hyobranchial muscles and elastic energy storage in connective tiss ues prior to projection may also be an essential element. In future work, mon attention should be paid to the possibility of elastic energy storage mechanisms in high-performance protrusible tentacles and ton gues.