Influence of elevated temperature on metabolism during aestivation: implications for muscle disuse atrophy

Abstract

SUMMARYReactive oxygen species (ROS), produced commensurate with aerobic metabolic rate, contribute to muscle disuse atrophy (MDA) in immobilised animals by damaging myoskeletal protein and lipids. Aestivating frogs appear to avoid MDA in part by substantially suppressing metabolic rate. However, as ectotherms, metabolic rate is sensitive to environmental temperature, and the high ambient temperatures that may be experienced by frogs during aestivation could in fact promote MDA. In this study, we investigated the effect of temperature on the metabolic rate of the aestivating frog Cyclorana alboguttata and its skeletal muscles in order to determine their likely susceptibility to MDA. Compared with non-aestivating frogs, a significant decrease in metabolic rate was recorded for aestivating frogs at 20, 24 and 30°C. At 30°C, however, the metabolic rate of aestivating frogs was significantly higher, approximately double that of frogs aestivating at 20 or 24°C, and the magnitude of the metabolic depression was significantly reduced at 30°C compared with that at 20°C. Temperature effects were also observed at the tissue level. At 24 and 30°C the metabolic rate of all muscles from aestivating frogs was significantly depressed compared with that of muscles from non-aestivating frogs. However, during aestivation at 30°C the metabolic rates of gastrocnemius, sartorius and cruralis were significantly elevated compared with those from frogs aestivating at 24°C. Our data show that the metabolism of C. alboguttata and its skeletal muscles is elevated at higher temperatures during aestivation and that the capacity of the whole animal to actively depress metabolism is impaired at 30°C.

Thermal acclimation of interactions: differential responses to temperature change alter predator–prey relationship

“…Maintaining muscle mass and function is advantageous for aestivating frogs because it permits immediate emergence following rainfall. Avoidance of muscle disuse atrophy in aestivating frogs is thought to be facilitated by the reduction of reactive oxygen species resulting from lower metabolic rates [30].…”

Pathogenic challenge reveals immune trade-off in mussels exposed to reduced seawater pH and increased temperature

“…Furthermore, bivalves may also be particularly vulnerable to reduced seawater pH (Hendriks et al, 2010;Kroeker et al, 2010Kroeker et al, , 2013, which impacts on acid-base balance, metabolism and calcification in this group (e.g. Gazeau et al, 2013;Hüning et al, 2013;Melzner et al, 2011), whilst being ectothermic, means environmental temperature also plays an important role in determining body temperature, directly impacting all physiological processes in this group (Pörtner et al, 2006;Young et al, 2011). The need to balance the allocation of energy between competing physiological processes under conditions of environmental stress, and under the combined challenge of reduced seawater pH, increased temperature and pathogen exposures in particular, means marine bivalves are thus an ideal model system for investigating the impact of climate change stressors on the invertebrate immune response.…”

Mechanisms underlying inhibition of muscle disuse atrophy during aestivation in the green-striped burrowing frog, Cyclorana alboguttata

“…alboguttata is likely to be due to a number of factors including increased antioxidant defences relative to oxidant production (Hudson et al, 2006), maintenance of 'random' acetylcholine release at neuromuscular junctions (Hudson et al, 2005), and metabolic depression at the tissue and whole animal level (Hudson and Franklin, 2002b;Young et al, 2011). Despite the results of these and other studies, the molecular and cellular mechanisms responsible for the inhibition of skeletal muscle disuse atrophy in natural models have not been fully characterised.…”

“…Another important feature of endothermic dormancy is the brown adipose tissue highly specialised for non-shivering thermogenesis and the elevation of Tb during arousal (Cannon and Nedergaard, 2004). In contrast, metabolic depression in ectotherms can occur at relatively high environmental temperatures, when for most ectotherms, metabolism is positively correlated with ambient temperature (Young et al, 2011).…”

“…However, recent investigations have examined the structure, function and plasticity of muscles in organisms that experience natural periods of muscle disuse or immobilisation, such as aestivating frogs and hibernating mammals (Cotton and Harlow, 2010;Harlow et al, 2001;Hudson and Franklin, 2002a;Mantle et al, 2009;Nowell et al, 2011;Symonds et al, 2007;Young et al, 2011). These studies have shown that animals which undertake extended bouts of natural immobility (i.e.…”