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First published online March 17, 2006
Journal of Experimental Biology 209, 1159-1168 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02101
Review Article |
Tribute to R. G. Boutilier: The role for skeletal muscle in the hypoxia-induced hypometabolic responses of submerged frogs
1 Imperial College London, Biomedical Sciences, Biological Nanoscience
Section, SAF-Building, South Kensington, London, SW7 2AZ, UK
2 Department of Physiology, Otago School of Medical Sciences, Dunedin, New
Zealand
3 Department of Biology, University of Western Ontario, London, ON, N6A 5B7,
Canada
4 Institute of Integrative and Comparative Biology, University of Leeds,
Leeds, LS2 9JT, UK
* Author for correspondence (e-mail: t.west{at}imperial.ac.uk)
Accepted 17 January 2006
Much of Bob Boutilier's research characterised the subcellular, organ-level and in vivo behavioural responses of frogs to environmental hypoxia. His entirely integrative approach helped to reveal the diversity of tissue-level responses to O2 lack and to advance our understanding of the ecological relevance of hypoxia tolerance in frogs. Work from Bob's lab mainly focused on the role for skeletal muscle in the hypoxic energetics of overwintering frogs. Muscle energy demand affects whole-body metabolism, not only because of its capacity for rapid increases in ATP usage, but also because hypometabolism of the large skeletal muscle mass in inactive animals impacts so greatly on in vivo energetics. The oxyconformance and typical hypoxia-tolerance characteristics (e.g. suppressed heat flux and preserved membrane ion gradients during O2 lack) of skeletal muscle in vitro suggest that muscle hypoperfusion in vivo is possibly a key mechanism for (i) downregulating muscle and whole-body metabolic rates and (ii) redistributing O2 supply to hypoxia-sensitive tissues. The gradual onset of a low-level aerobic metabolic state in the muscle of hypoxic, cold-submerged frogs is indeed important for slowing depletion of on-board fuels and extending overwintering survival time. However, it has long been known that overwintering frogs cannot survive anoxia or even severe hypoxia. Recent work shows that they remain sensitive to ambient O2 and that they emerge rapidly from quiescence in order to actively avoid environmental hypoxia. Hence, overwintering frogs experience periods of hypometabolic quiescence interspersed with episodes of costly hypoxia avoidance behaviour and exercise recovery.
In keeping with this flexible physiology and behaviour, muscle mechanical properties in frogs do not deteriorate during periods of overwintering quiescence. On-going studies inspired by Bob Boutilier's integrative mindset continue to illuminate the cost–benefit(s) of intermittent locomotion in overwintering frogs, the constraints on muscle function during hypoxia, the mechanisms of tissue-level hypometabolism, and the details of possible muscle atrophy resistance in quiescent frogs.
Key words: Rana spp., hypoxia, skeletal muscle, resting metabolism, contraction
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  B. L. Symonds, R. S. James, and C. E. Franklin Getting the jump on skeletal muscle disuse atrophy: preservation of contractile performance in aestivating Cyclorana alboguttata (Gunther 1867) J. Exp. Biol., March 1, 2007; 210(5): 825 - 835. [Abstract] [Full Text] [PDF]
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