Jet propulsion in the cold: mechanics of swimming in the Antarctic scallop<i>Adamussium colbecki</i>

Denny, Mark W.; Miller, Luke P.

doi:10.1242/jeb.02538

Cited by 48 publications

(47 citation statements)

References 19 publications

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“…Because the mechanical properties of elastic tissues are known to have low thermal sensitivity (19,22,23), temperature manipulation may be a valuable methodological approach to test for the presence or prevalence of elastic recoil in powering movements. Elastic recoil is implicated if performance of a movement is maintained at a high level over a wide range of body temperatures.…”

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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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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“…The results obtained from E. guttolineata are consistent with the hypotheses that tongue projection in this species is powered at least in part by an elastic-recoil mechanism, exhibiting reduced thermal sensitivity when compared with tongue retraction powered by muscle contraction directly. This dichotomy has been found in a number of integrated systems that incorporate an elastic-recoilpowered movement with an associated muscle-powered movement (Anderson and Deban, 2010;Lappin, 2011, Deban andRichardson, 2011;Sandusky andDeban, 2012, Anderson andHigham and Anderson, 2014) and is indicative of these elastic-recoil-powered mechanisms capitalizing on the weak effect of temperature on muscle contractile force and muscle work during near-isometric contractions (Bennett, 1984;Herrel et al, 2007;Anderson and Deban, 2012;James, 2013) as well as the thermal independence of elastic tissue mechanical properties (Rigby et al, 1959;Alexander, 1966;Denny and Miller, 2006) to impart thermal robustness to these ballistic movements. The strong thermal sensitivity of the elastic-recoil-powered movement in this study in the 4-11°C interval, however, emphasizes that this thermal robustness is contingent on relatively similar amounts of elastic energy being stored in the tongue's elastic elements by the tongueprojector muscles, by way of increased motor activity durations, equal burst intensity and similar tension development as temperature declines, as found previously in other systems (Deban and Lappin, 2011;Anderson and Deban, 2012).…”

Section: Discussion Prey Capture Kinematics and Dynamicsmentioning

confidence: 97%

“…This pattern has been shown to be the result not of any compensatory activation of muscle at low temperature in chameleons and toads (Deban and Lappin, 2011;Anderson and Deban, 2012), nor of any unusually reduced effect of temperature on typical muscle contractile physiology in chameleons (Anderson and Deban, 2012). Instead, the specialized morphology and motor control patterns of these elastic recoil-powered tongue-projection mechanisms capitalize on the weak effect of temperature on muscle contractile force (Bennett, 1984;Herrel et al, 2007;Anderson and Deban, 2012;James, 2013) and the thermal independence of the mechanical properties of elastic tissues (Rigby et al, 1959;Alexander, 1966;Denny and Miller, 2006) to impart thermal robustness to these ballistic movements. Movements such as tongue retraction that are powered directly by muscle contraction, in contrast, suffer typical thermal effects resulting from the strong effect of temperature on muscle contractile dynamics, and thus slow significantly with decreasing temperature (Bennett, 1985;Rome, 1990;Herrel et al, 2007;Anderson and Deban, 2012;James, 2013).…”

Section: Introductionmentioning

confidence: 99%

Thermal effects on the performance, motor control, and muscle dynamics of ballistic feeding in the salamanderEurycea guttolineata

Anderson

Larghi

Deban

2014

Journal of Experimental Biology

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Temperature strongly affects muscle contractile rate properties and thus may influence whole-organism performance. Movements powered by elastic recoil, however, are known to be more thermally robust than muscle-powered movements. We examined the wholeorganism performance, motor control and muscle contractile physiology underlying feeding in the salamander Eurycea guttolineata. We compared elastically powered tongue projection with the associated muscle-powered retraction to determine the thermal robustness of each of these functional levels. We found that tongueprojection distance in E. guttolineata was unaffected by temperature across the entire 4-26°C range, tongue-projection dynamics were significantly affected by temperature across only the 4-11°C interval, and tongue retraction was affected to a higher degree across the entire temperature range. The significant effect of temperature on projection dynamics across the 4-11°C interval corresponds to a significant decline in projector muscle burst intensity and peak contractile force of the projector muscle across the same interval. Across the remaining temperature range, however, projection dynamics were unaffected by temperature, with muscle contractile physiology showing typical thermal effects and motor patterns showing increased activity durations and latencies. These results reveal that elastically powered tongue-projection performance in E. guttolineata is maintained to a higher degree than muscle-powered tongue retraction performance across a wide temperature range. These results further indicate that thermal robustness of the elastically powered movement is dependent on motor control and muscle physiology that results in comparable energy being stored in elastic tissues across a range of temperatures.

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“…The force gauge was placed on the front side of the scallop with a hook between its valves at an opening width, which was observed for the undisturbed scallop (between 0.8 and 1.5 cm depending on the animal). After at least 12 h of recovery, clapping was induced by introducing aqua dest via a thin, gas-tight tube into the mantle cavity (see Bailey et al 2005;Denny and Miller 2006). When the scallop stopped clapping, the stimulation was repeated until animals were fatigue and showed no response to further stimulation (after *50 min).…”

Section: Measurement Of Clapping Performancementioning

confidence: 99%

Impact of ocean acidification on escape performance of the king scallop, Pecten maximus, from Norway

et al. 2012

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The ongoing process of ocean acidification already affects marine life, and according to the concept of oxygen and capacity limitation of thermal tolerance, these effects may be intensified at the borders of the thermal tolerance window. We studied the effects of elevated CO 2 concentrations on clapping performance and energy metabolism of the commercially important scallop Pecten maximus. Individuals were exposed for at least 30 days to 4°C (winter) or to 10°C (spring/summer) at either ambient (0.04 kPa, normocapnia) or predicted future PCO 2 levels (0.11 kPa, hypercapnia). Cold-exposed (4°C) groups revealed thermal stress exacerbated by PCO 2 indicated by a high mortality overall and its increase from 55 % under normocapnia to 90 % under hypercapnia. We therefore excluded the 4°C groups from further experimentation. Scallops at 10°C showed impaired clapping performance following hypercapnic exposure. Force production was significantly reduced although the number of claps was unchanged between normocapnia-and hypercapnia-exposed scallops. The difference between maximal and resting metabolic rate (aerobic scope) of the hypercapnic scallops was significantly reduced compared with normocapnic animals, indicating a reduction in net aerobic scope. Our data confirm that ocean acidification narrows the thermal tolerance range of scallops resulting in elevated vulnerability to temperature extremes and impairs the animal's performance capacity with potentially detrimental consequences for its fitness and survival in the ocean of tomorrow.

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Jet propulsion in the cold: mechanics of swimming in the Antarctic scallopAdamussium colbecki

Cited by 48 publications

References 19 publications

Ballistic tongue projection in chameleons maintains high performance at low temperature

Ballistic tongue projection in chameleons maintains high performance at low temperature

Thermal effects on the performance, motor control, and muscle dynamics of ballistic feeding in the salamanderEurycea guttolineata

Impact of ocean acidification on escape performance of the king scallop, Pecten maximus, from Norway

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