Supercontracting muscle

muscle contraction (Huxley and Niedergerke, 1954; Huxley and Hanson, 1954), dictates a trade-off between the ability of a muscle to generate isometric force and its length. This intrinsic trade-off is the result of the need for overlap between thick and thin filaments upon extension of the sarcomere and of the limitations imposed by the physical interference of thin filaments and thick filaments with the Z-disk upon contraction (Hanson and Huxley, 1955). At extreme elongation or shortening of the muscle, no muscle force can be generated (e.g. Ramsey and Street, 1940; Podolsky, 1964; Gordon et al., 1966). Typical vertebrate striated muscle will consequently be limited to operate at a fairly narrow range of sarcomere lengths situated around the optimal sarcomere length that allows maximal force output (see Burkholder and Lieber, 2001). Some vertebrates, however, do show extreme muscle elongation under natural circumstances. In animals with ballistic tongues, such as frogs and lungless salamanders, the tongue retractor undergoes considerable lengthening during prey capture (Deban et al., 1997; Nishikawa, 2000). Chameleons are probably best known for their ability to project their tongue up to twice body length (>1000 % of the tongue resting length) while catching prey (Wainwright et al., 1991; Meyers and Nishikawa, 2000; Schwenk, 2000). Clearly, such extreme elongation would take the muscle beyond the plateau in its length/tension relationship and, thus, preclude it from producing any more force (Gordon et al., 1966). However, there are other types of muscle that are able to shorten and maintain tension over a much wider length range than the typical cross-striated muscle of vertebrates. Z-disks are absent from smooth muscle, so it is capable of generating tension to lengths of less than one-third of the optimal muscle length (i.e. the length at which force production is maximal) (see Gordon and Siegman, 1971; Small et al., 1990). The drawbacks associated with smooth muscle are its low contraction velocity and its lower maximal force output for a given cross-sectional area (i.e. approximately one-third of that of cross-striated muscle) (Gordon and Siegman, 1971). Yet chameleons are known to eat large prey (Broadley, 1973; Schleich et al., 1996), so they must be able to exert large retraction forces at any given tongue projection distance. Moreover, a reasonably rapid retraction of the tongue with 2167 The Journal of Experimental Biology 205, 2167–2173 (2002) Printed in Great Britain © The Company of Biologists Limited 2002 JEB3935