Extremely high-power tongue projection in plethodontid salamanders

Deban, Stephen M.; O’Reilly, James C.; Dicke, Ursula; Leeuwen, J.L. van

doi:10.1242/jeb.02664

Cited by 84 publications

(169 citation statements)

References 42 publications

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“…amplification system (Van Wassenbergh et al, 2008) similar to that seen in other animals with ballistic-like movements, such as plethodontid salamanders (Deban et al, 2007). Cranial elevation during forcepsfish sound production occurs after EP activity but likely results from less power amplification because EP activity duration was correlated with cranial elevation velocity, unlike the independent relationship found in bay pipefish (Van Wassenbergh et al, 2008).…”

Section: Discussionsupporting

confidence: 54%

Sound production in the longnose butterflyfishes (genusForcipiger): cranial kinematics, muscle activity and honest signals

Boyle

Tricas

2011

Journal of Experimental Biology

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SUMMARYMany teleost fishes produce sounds for social communication with mechanisms that do not involve swim bladder musculature. Such sounds may reflect physical attributes of the sound-production mechanism, be constrained by body size and therefore control signal reliability during agonistic behaviors. We examined kinematics of the cranium, median fins and caudal peduncle during sound production in two territorial chaetodontid butterflyfish sister species: forcepsfish (Forcipiger flavissimus) and longnose butterflyfish (F. longirostris). During intraspecific agonistic encounters, both species emit a single pulse sound that precedes rapid cranial rotation at velocities and accelerations that exceed those of prey strikes by many ram-and suction-feeding fishes. Electromyography showed that onsets of activity for anterior epaxialis, sternohyoideus, A1 and A2 adductor mandibulae muscles and sound emission are coincident but precede cranial elevation. Observations indicate that sound production is driven by epaxial muscle contraction whereas a ventral linkage between the head and pectoral girdle is maintained by simultaneous activity from the adductor mandibulae and sternohyoideus. Thus, the girdle, ribs and rostral swim bladder are pulled anteriorly before the head is released and rotated dorsally. Predictions of the hypothesis that acoustic signals are indicators of body size and kinematic performance were confirmed. Variation in forcepsfish sound duration and sound pressure level is explained partly by cranial elevation velocity and epaxial electromyogram duration. Body size, however, explains most variation in duration and sound pressure level. These observed associations indicate that forcepsfish sounds may be accurate indicators of size and condition that are related to resource holding potential during social encounters. Supplementary material available online at

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Section: Discussionsupporting

confidence: 54%

Sound production in the longnose butterflyfishes (genusForcipiger): cranial kinematics, muscle activity and honest signals

Boyle

Tricas

2011

Journal of Experimental Biology

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“…This peak value is well in excess of peak power output of muscle tissue during active contraction as measured or estimated in other vertebrates operating at higher T b , including flying quail during vertical takeoff (1, ) (6). High power outputs for rapid movements using the elastic-recoil mechanism, including jumping in bushbabies (14) and insects (15,16), predatory strikes of mantis shrimp (17), and tongue projection in salamanders (18) and chameleons (7), have been documented in numerous kinematic studies; little focus has been given to the maintenance of performance at low T b , however.…”

Section: Resultsmentioning

confidence: 99%

Ballistic tongue projection in chameleons maintains high performance at low temperature

Anderson

Deban

2010

Proc. Natl. Acad. Sci. U.S.A.

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Environmental temperature impacts the physical activity and ecology of ectothermic animals through its effects on muscle contractile physiology. Sprinting, swimming, and jumping performance of ectotherms decreases by at least 33% over a 10°C drop, accompanied by a similar decline in muscle power. We propose that ballistic movements that are powered by recoil of elastic tissues are less thermally dependent than movements that rely on direct muscular power. We found that an elastically powered movement, ballistic tongue projection in chameleons, maintains high performance over a 20°C range. Peak velocity and power decline by only 10%-19% with a 10°C drop, compared to >42% for nonelastic, muscle-powered tongue retraction. These results indicate that the elastic recoil mechanism circumvents the constraints that low temperature imposes on muscle rate properties and thereby reduces the thermal dependence of tongue projection. We propose that organisms that use elastic recoil mechanisms for ecologically important movements such as feeding and locomotion may benefit from an expanded thermal niche.biomechanics | muscle physiology | elastic storage | thermal ecology | Chamaeleonidae T emperature influences diverse physiological processes, including metabolic rate, muscle dynamics, and nerve conduction velocity, which in turn can affect whole-organism performance. Ectothermic animals are particularly vulnerable to the effects of low ambient temperatures, because their body temperature (T b ) is dictated by environmental conditions. 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. Chameleons feed over a wider range of T b than other lizards, using ballistic tongue projection in habitats ranging from deserts, where T b exceeds 39°C (9), to alpine zones above 3,500 m with temperatures below freezing (10). Some chameleon species feed at a T b of 3.5°C (9), exploiting an early morning peak in alpine insect activity (10) before sympatric lizard species become active (11). This ability to feed at low T b has not been explained; we propose that the elastic-recoil mechanism of tongue projection confers this temperature insensitivity.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 accel...

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“…The release of this energy to the muscle fascicles happens approximately 2.4 times slower and largely subsequent to movement (figure 3). Because rates of energy storage and release in tendon are less limited than in muscle, both power attenuation and amplification mechanisms may allow for movement that is beyond the mechanical range of muscle contraction alone [32,33].…”

Section: Discussionmentioning

confidence: 99%

Muscle power attenuation by tendon during energy dissipation

2011

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An important function of skeletal muscle is deceleration via active muscle fascicle lengthening, which dissipates movement energy. The mechanical interplay between muscle contraction and tendon elasticity is critical when muscles produce energy. However, the role of tendon elasticity during muscular energy dissipation remains unknown. We tested the hypothesis that tendon elasticity functions as a mechanical buffer, preventing high (and probably damaging) velocities and powers during active muscle fascicle lengthening. We directly measured lateral gastrocnemius muscle force and length in wild turkeys during controlled landings requiring rapid energy dissipation. Muscle-tendon unit (MTU) strain was measured via video kinematics, independent of muscle fascicle strain (measured via sonomicrometry). We found that rapid MTU lengthening immediately following impact involved little or no muscle fascicle lengthening. Therefore, joint flexion had to be accommodated by tendon stretch. After the early contact period, muscle fascicles lengthened and absorbed energy. This late lengthening occurred after most of the joint flexion, and was thus mainly driven by tendon recoil. Temporary tendon energy storage led to a significant reduction in muscle fascicle lengthening velocity and the rate of energy absorption. We conclude that tendons function as power attenuators that probably protect muscles against damage from rapid and forceful lengthening during energy dissipation.

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Extremely high-power tongue projection in plethodontid salamanders

Cited by 84 publications

References 42 publications

Sound production in the longnose butterflyfishes (genusForcipiger): cranial kinematics, muscle activity and honest signals

Sound production in the longnose butterflyfishes (genusForcipiger): cranial kinematics, muscle activity and honest signals

Ballistic tongue projection in chameleons maintains high performance at low temperature

Muscle power attenuation by tendon during energy dissipation

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