Evidence for an elastic projection mechanism in the chameleon tongue

Abstract

To capture prey, chameleons ballistically project their tongues as far as 1.5 body lengths with accelerations of up to 500 m s(-2). At the core of a chameleon's tongue is a cylindrical tongue skeleton surrounded by the accelerator muscle. Previously, the cylindrical accelerator muscle was assumed to power tongue projection directly during the actual fast projection of the tongue. However, high-speed recordings of Chamaeleo melleri and C. pardalis reveal that peak powers of 3000 W kg(-1) are necessary to generate the observed accelerations, which exceed the accelerator muscle's capacity by at least five- to 10-fold. Extrinsic structures might power projection via the tongue skeleton. High-speed fluoroscopy suggests that they contribute less than 10% of the required peak instantaneous power. Thus, the projection power must be generated predominantly within the tongue, and an energy-storage-and-release mechanism must be at work. The key structure in the projection mechanism is probably a cylindrical connective-tissue layer, which surrounds the entoglossal process and was previously suggested to act as lubricating tissue. This tissue layer comprises at least 10 sheaths that envelop the entoglossal process. The outer portion connects anteriorly to the accelerator muscle and the inner portion to the retractor structures. The sheaths contain helical arrays of collagen fibres. Prior to projection, the sheaths are longitudinally loaded by the combined radial contraction and hydrostatic lengthening of the accelerator muscle, at an estimated mean power of 144 W kg(-1) in C. melleri. Tongue projection is triggered as the accelerator muscle and the loaded portions of the sheaths start to slide over the tip of the entoglossal process. The springs relax radially while pushing off the rounded tip of the entoglossal process, making the elastic energy stored in the helical fibres available for a simultaneous forward acceleration of the tongue pad, accelerator muscle and retractor structures. The energy release continues as the multilayered spring slides over the tip of the smooth and lubricated entoglossal process. This sliding-spring theory predicts that the sheaths deliver most of the instantaneous power required for tongue projection. The release power of the sliding tubular springs exceeds the work rate of the accelerator muscle by at least a factor of 10 because the elastic-energy release occurs much faster than the loading process. Thus, we have identified a unique catapult mechanism that is very different from standard engineering designs. Our morphological and kinematic observations, as well as the available literature data, are consistent with the proposed mechanism of tongue projection, although experimental tests of the sheath strain and the lubrication of the entoglossal process are currently beyond our technical scope.

Ballistic tongue projection in chameleons maintains high performance at low temperature

“…The effect of T b on muscle physiology has a clear impact on an organism's ability to move, escape predators, and engage in foraging behavior (1-6); for example, a 10°C drop in T b reduces sprint speed in lizards, swimming speed in fish, and jumping distance in frogs by at least 33% (2, 5). We find that, unlike these other dynamic movements, ballistic tongue projection in chameleons maintains extremely high performance over a T b range of 20°C.The mechanism of chameleon prey capture is unique among lizards, relying on ballistic projection of the tongue up to twice the length of the body in as little as 0.07 second (7,8). This feeding mechanism is common to all chameleons and gives these slow, cryptic, sit-and-wait predators the element of surprise.…”

“…As in other species (7), dissection and mass measurements of the tongue apparatus of seven C. calyptratus (12.0-15.5 cm snout-vent length) determined that the circular portion of the accelerator muscle accounts for ∼50% (mean, 48.2% ± 2.9%) of the mass of the accelerator muscle complex and tongue pad, whereas the retractor muscle accounts for ∼25% (mean, 25.8% ± 1.7%) of the mass of the accelerator muscle complex, tongue pad, and retractor muscle. Thus, massspecific power is multiplied by a factor of 2 for projection and by a factor of 4 for retraction (7).…”

“…The mechanism of chameleon prey capture is unique among lizards, relying on ballistic projection of the tongue up to twice the length of the body in as little as 0.07 second (7,8). This feeding mechanism is common to all chameleons and gives these slow, cryptic, sit-and-wait predators the element of surprise.…”

“…This "bow and arrow" mechanism decouples muscle contraction temporally from tongue launch and thereby allows kinetic energy to be imparted to the tongue at a rate far exceeding that possible via direct muscle contraction (7). Once launched-at accelerations exceeding 400 ms −2 (41 g)-the tongue travels to the target on its momentum alone and then adheres to the prey.…”

“…Ballistic tongue projection in chameleons achieves its extreme performance by rapid elastic recoil of collagen tissue within the tongue-tissue that is first stretched by slow contraction of the tongue accelerator muscle (7). This "bow and arrow" mechanism decouples muscle contraction temporally from tongue launch and thereby allows kinetic energy to be imparted to the tongue at a rate far exceeding that possible via direct muscle contraction (7).…”