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Off like a shot: scaling of ballistic tongue projection reveals extremely high performance in small chameleons.

ABSTRACT: Stretching elastic tissues and using their recoil to power movement allows organisms to release energy more rapidly than by muscle contraction directly, thus amplifying power output. Chameleons employ such a mechanism to ballistically project their tongue up to two body lengths, achieving power outputs nearly three times greater than those possible via muscle contraction. Additionally, small organisms tend to be capable of greater performance than larger species performing similar movements. To test the hypothesis that small chameleon species outperform larger species during ballistic tongue projection, performance was examined during feeding among 20 chameleon species in nine genera. This revealed that small species project their tongues proportionately further than large species, achieving projection distances of 2.5 body lengths. Furthermore, feedings with peak accelerations of 2,590?m s(-2), or 264?g, and peak power output values of 14,040?W kg(-1) are reported. These values represent the highest accelerations and power outputs reported for any amniote movement, highlighting the previously underestimated performance capability of the family. These findings show that examining movements in smaller animals may expose movements harbouring cryptic power amplification mechanisms and illustrate how varying metabolic demands may help drive morphological evolution.

SUBMITTER: Anderson CV

PROVIDER: S-EPMC4698635 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Off like a shot: scaling of ballistic tongue projection reveals extremely high performance in small chameleons.

Anderson Christopher V CV

Scientific reports 20160104

Stretching elastic tissues and using their recoil to power movement allows organisms to release energy more rapidly than by muscle contraction directly, thus amplifying power output. Chameleons employ such a mechanism to ballistically project their tongue up to two body lengths, achieving power outputs nearly three times greater than those possible via muscle contraction. Additionally, small organisms tend to be capable of greater performance than larger species performing similar movements. To ...[more]

PMID: 26725508

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Project description: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.

Project description:Phenotypic performance in different environments is central to understanding the evolutionary and ecological processes that drive adaptive divergence and, ultimately, speciation. Because habitat structure can affect an animal's foraging behaviour, anti-predator defences, and communication behaviour, it can influence both natural and sexual selection pressures. These selective pressures, in turn, act upon morphological traits to maximize an animal's performance. For performance traits involved in both social and ecological activities, such as bite force, natural and sexual selection often interact in complex ways, providing an opportunity to understand the adaptive significance of morphological variation with respect to habitat. Dwarf chameleons within the Bradypodion melanocephalum-Bradypodion thamnobates species complex have multiple phenotypic forms, each with a specific head morphology that could reflect its use of either open- or closed-canopy habitats. To determine whether these morphological differences represent adaptations to their habitats, we tested for differences in both absolute and relative bite performance. Only absolute differences were found between forms, with the closed-canopy forms biting harder than their open-canopy counterparts. In contrast, sexual dimorphism was found for both absolute and relative bite force, but the relative differences were limited to the closed-canopy forms. These results indicate that both natural and sexual selection are acting within both habitat types, but to varying degrees. Sexual selection seems to be the predominant force within the closed-canopy habitats, which are more protected from aerial predators, enabling chameleons to invest more in ornamentation for communication. In contrast, natural selection is likely to be the predominant force in the open-canopy habitats, inhibiting the development of conspicuous secondary sexual characteristics and, ultimately, enforcing their overall diminutive body size and constraining performance.

Dataset Information

Off like a shot: scaling of ballistic tongue projection reveals extremely high performance in small chameleons.

Publications

Off like a shot: scaling of ballistic tongue projection reveals extremely high performance in small chameleons.

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