Plasticity of muscle function in a thermoregulating ectotherm (Crocodylus porosus): biomechanics and metabolism

Abstract

Seebacher F, James RS. Plasticity of muscle function in a thermoregulating ectotherm (Crocodylus porosus): biomechanics and metabolism. Am J Physiol Regul Integr Comp Physiol 294: R1024-R1032, 2008. First published January 16, 2007 doi:10.1152/ajpregu.00755.2007.-Thermoregulation and thermal sensitivity of performance are thought to have coevolved so that performance is optimized within the selected body temperature range. However, locomotor performance in thermoregulating crocodiles (Crocodylus porosus) is plastic and maxima shift to different selected body temperatures in different thermal environments. Here we test the hypothesis that muscle metabolic and biomechanical parameters are optimized at the body temperatures selected in different thermal environments. Hence, we related indices of anaerobic (lactate dehydrogenase) and aerobic (cytochrome c oxidase) metabolic capacities and myofibrillar ATPase activity to the biomechanics of isometric and work loop caudofemoralis muscle function. Maximal isometric stress (force per muscle cross-sectional area) did not change with thermal acclimation, but muscle work loop power output increased with cold acclimation as a result of shorter activation and relaxation times. The thermal sensitivity of myofibrillar ATPase activity decreased with cold acclimation in caudofemoralis muscle. Neither aerobic nor anaerobic metabolic capacities were directly linked to changes in muscle performance during thermal acclimation, although there was a negative relationship between anaerobic capacity and isometric twitch stress in cold-acclimated animals. We conclude that by combining thermoregulation with plasticity in biomechanical function, crocodiles maximize performance in environments with highly variable thermal properties. body temperature; thermal acclimation; locomotion; work loop; enzymes PHYSICAL PERFORMANCE OF VERTEBRATES may be constrained by limited capacity to respond to environmental change, and individuals that are most effective in compensating for environmental variability will gain a selective advantage (75). Selection can be partitioned into a performance gradient and a fitness gradient (4). The former relates variation in biochemical, physiological, or morphological traits to a measure of ecologically relevant performance, and the latter quantifies the effect of variance in performance on fitness (4, 56). Locomotion is closely linked to Darwinian fitness because of its influence on foraging success and escape from predators (36,40,45,63,83,84) as well as on social status (23). For example, maximal sprint speed in male lizards (Crotaphytus collaris) is a reliable predictor of territory size and defense (39, 68), and faster lizards have significantly greater reproductive output (38).Although locomotor performance is heritable (21,46,58,88), there is considerable within-generation variability as a result of environmental effects and gene-environment interactions (14, 58, 73). Locomotor performance is determined by underlying intrinsic muscle properties, such as muscl...

Building a dishonest signal: the functional basis of unreliable signals of strength in males of the two-toned fiddler crab,Uca vomeris

“…However, we would expect catabolic pathways to primarily regulate maximal oxygen consumption rate and not resting rate. Resting oxygen consumption rate is driven by ATP demand for protein synthesis and ATPase activity, and is not generally constrained by maximal enzyme activity (Horton et al, 2006;Seebacher and James, 2008;White and Kearney, 2013). The significant differences observed in whole-claw rates of oxygen consumption could be attributed to the reduced muscle mass found in the regenerated claws.…”

Variation in expression of calcium-handling proteins is associated with inter-individual differences in mechanical performance of rat (Rattus norvegicus) skeletal muscle

“…Differences in glycolytic and oxidative metabolic capacities are also used as the basis of muscle fibre classification, where slow, endurance fibres are more oxidatively poised and fast fibres have greater glycolytic capacity (Bottinelli and Reggiani, 2000). However, the molecular traits used to categorize muscle fibre types often do not correspond to the expected patterns of muscle performance and sprint-endurance trade-offs (Gibb and Dickson, 2002;James et al, 2005;Plomgaard et al, 2006;Seebacher and James, 2008). This may be because actual muscle contractile performance is determined by interactions between multiple molecular traits, so that deducing a direct relationship between fibre type categories and muscle performance is difficult.…”

DIVING IN A WARMING WORLD: Thermal constraints on the diving capacity of estuarine crocodiles (Crocodylus porosus)

“…Aquatic and semi-aquatic ectotherms have long been revered for their capacity to acclimate to altered thermal regimens (Hazel and Prosser, 1974;Johnston and Temple, 2002), but the bulk of this research has examined organismal responses to decreases in ambient temperature resembling current habitat conditions (Aho and Vornanen, 2001;Hochscheid et al, 2004;Glanville and Seebacher, 2006;Seebacher and James, 2007;Guderley and Seebacher, 2011). My study here complements this body of work by examining thermal compensation at the other, 'hot', end of the spectrum.…”

“…Previous assessments have identified C. porosus to be physiologically plastic, with the capacity to fully compensate swimming performance, muscle power output and lower level physiological function (i.e. mitochondrial oxygen consumption, membrane fatty acid composition and regulatory enzyme activity) in response to cool temperatures approaching the lower end of its thermal tolerance window (Glanville and Seebacher, 2006;Seebacher and James, 2007). It is presently unclear whether estuarine crocodiles can undergo adequate physiological acclimation at elevated temperatures and potentially offset thermal effects on diving performance.…”

“…mitochondrial oxygen consumption, membrane fatty acid composition and regulatory enzyme activity) in response to cool temperatures approaching the lower end of its thermal tolerance window (Glanville and Seebacher, 2006;Seebacher and James, 2007 …”