Aestivation pp 171-181 | Cite as

Effects of Aestivation on Skeletal Muscle Performance

Chapter
First Online:
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 49)

Abstract

Fitness, ecology, and behaviour of vertebrates are dependent upon locomotor performance. Locomotor performance can be constrained by underlying intrinsic skeletal muscle properties. Skeletal muscle is a highly plastic tissue undergoing phenotypic change in response to alteration in environment. Clinical and experimental models of muscle disuse cause decreases in skeletal muscle size and mechanical performance. However, in natural models of skeletal muscle disuse, both atrophy and changes in mechanical properties are more limited. Aestivation in frogs can cause decreases in muscle cross-sectional area and changes in some enzyme activities, with effects varying among muscles. However, long-term aestivation causes limited changes in muscle mechanics during simulated sprint or endurance type activities. Therefore, at least in frogs, there is maintenance of skeletal muscle performance during prolonged periods of aestivation, allowing avoidance of harsh environmental conditions without compromising the locomotor capacity to perform fitness-related activities when favourable environmental conditions return.

Keywords

Extensor Digitorum Longus Sartorius Muscle Biceps Femoris Muscle Muscle Disuse Endplate Potential 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

References

  1. Bennett AF, Garland T, Else P (1989) Individual correlation of morphology, muscle mechanics, and locomotion in a salamander. Am J Physiol 256:R1200–R1208PubMedGoogle Scholar
  2. Boonyarom O, Inui K (2006) Atrophy and hypertrophy of skeletal muscles: structural and functional aspects. Acta Physiol 188:77–89CrossRefGoogle Scholar
  3. Buller AJ, Eccles JC, Eccles RM (1960) Interactions between motorneurones and muscles in respect of the characteristic speeds of their responses. J Physiol 150:417–439PubMedGoogle Scholar
  4. Calsbeek R, Irschick DB (2007) The quick and the dead: locomotor performance and natural selection in island lizards. Evolution 61:2493–2503CrossRefPubMedGoogle Scholar
  5. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181PubMedGoogle Scholar
  6. Cowan KJ, Storey KB (2001) Tyrosine kinases and phosphatases in the estivating spadefoot toad. Cell Physiol Biochem 11:161–172CrossRefPubMedGoogle Scholar
  7. Fitts RH, Riley DR, Widrick JJ (2000) Physiology of a microgravity environment: microgravity and skeletal muscle. J Appl Physiol 89:823–839PubMedGoogle Scholar
  8. Flanigan J, Withers P, Storey K, Guppy M (1990) Changes in enzyme binding and activity during aestivation in the frog Neobatrachus pelobatoides. Comp Biochem Physiol B 96:67–71CrossRefPubMedGoogle Scholar
  9. Goldspink G (2002) Gene expression in skeletal muscle. Biochem Soc Trans 30:285–290CrossRefPubMedGoogle Scholar
  10. Grundy JE, Storey KB (1998) Antioxidant defenses and lipid peroxidation damage in estivating toads, Scaphiopus couchii. J Comp Physiol B 168:132–142CrossRefPubMedGoogle Scholar
  11. Harlow HJ, Lohuis T, Beck TDI, Iaizzo PA (2001) Muscle strength in overwintering bears. Nature 409:997CrossRefPubMedGoogle Scholar
  12. Hudson NJ, Franklin CE (2002a) Effect of aestivation on muscle characteristics and locomotor performance in the Green-striped burrowing frog, Cyclorana alboguttata. J Comp Physiol B 172:177–182CrossRefPubMedGoogle Scholar
  13. Hudson NJ, Franklin CE (2002b) Maintaining muscle mass during extended disuse: aestivating frogs as a model species. J Exp Biol 205:2297–2303PubMedGoogle Scholar
  14. Hudson NJ, Franklin CE (2003) Preservation of three-dimensional capillary structure in frog muscle during aestivation. J Anat 202:471–474CrossRefPubMedGoogle Scholar
  15. Hudson NJ, Lavidis NA, Choy PT, Franklin CE (2005) Effect of prolonged inactivity on skeletal motor nerve terminals during aestivation in the burrowing frog, Cyclorana alboguttata. J Comp Physiol 191:373–379CrossRefGoogle Scholar
  16. Hudson NJ, Lehnert SA, Ingham AB, Symonds B, Franklin CE, Harper GS (2006) Lessons from an estivating frog: sparing muscle protein despite starvation and disuse. Am J Physiol 290:R836–R843Google Scholar
  17. Hudson NJ, Harper GS, Allingham PG, Franklin CE, Barris W, Lehnert SA (2007) Skeletal muscle extracellular matrix remodelling after aestivation in the green striped burrowing frog, Cyclorana alboguttata. Comp Biochem Physiol A 146:440–445CrossRefGoogle Scholar
  18. Huey R, Bennett AF, John-Alder H, Nagy KA (1984) Locomotor capacity and foraging behaviour of Kalahari lacertid lizards. Anim Behav 32:41–50CrossRefGoogle Scholar
  19. James RS, Navas CA (2008) Are there differences in the effects of temperature on muscle performance between toads of the same species (Bufo granulosus) living in semi arid and forest environments? Comp Biochem Physiol A 150:S72Google Scholar
  20. James RS, Navas CA, Herrel A (2007) How important are skeletal muscle mechanics in setting limits on jumping performance? J Exp Biol 210:923–933CrossRefPubMedGoogle Scholar
  21. Jayne BC, Bennett AF (1990a) Selection of locomotor performance capacity in a natural population of garter snakes. Evolution 44:1204–1229CrossRefGoogle Scholar
  22. Jayne BC, Bennett AF (1990b) Scaling of speed and endurance in garter snakes: a comparison of cross-sectional and longitudinal allometries. J Zool 220:257–277CrossRefGoogle Scholar
  23. Johnston IA, Temple GK (2002) Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour. J Exp Biol 205:2305–2322PubMedGoogle Scholar
  24. Lavidis NA, Hudson NJ, Choy PT, Lehnert SA, Franklin CE (2008) Role of calcium and vesicle docking proteins in remobilising dormant neuromuscular junctions in desert frogs. J Comp Physiol A 194:27–37CrossRefGoogle Scholar
  25. Le Galliard JF, Clobert J, Ferrière R (2004) Physical performance and Darwinian fitness in lizards. Nature 432:502–505CrossRefPubMedGoogle Scholar
  26. Lohuis TD, Harlow HJ, Beck TDI (2007) Hibernating black bears (Ursus americanus) experience skeletal muscle protein balance during winter anorexia. Comp Biochem Physiol B 147:20–28CrossRefPubMedGoogle Scholar
  27. Marsh RL (1994) Jumping ability of anurans. In: Jones JH (ed) Comparative vertebrate exercise physiology. Academic, San Diego, pp 51–111Google Scholar
  28. Miles DB (2004) The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evol Ecol Res 6:63–75Google Scholar
  29. Musacchia XJ, Steffen JM, Fell RD (1988) Disuse atrophy of skeletal muscle: animal models. Exerc Sports Sci Rev 16:61–87CrossRefGoogle Scholar
  30. Navas CA, Antoniazzi MM, Jared C (2004) A preliminary assessment of anuran physiological and morphological adaptation to the Caatinga, a Brazilian semi-arid environment. In: Morris S, Vosloo A (eds) International congress series, vol 1275. Elsevier, Cambridge. pp. 298–305Google Scholar
  31. Navas CA, James RS, Wilson RS (2006) Inter-individual variation in the muscle physiology of vertebrate ectotherms: consequences for behavioural and ecological performance. In: Herrel A, Speck T, Rowe NP (eds) Ecology and biomechanics. CRC, Boca Raton, pp 231–251Google Scholar
  32. Navas CA, Antoniazzi MM, Carvalho JE, Suzuki H, Jared C (2007) Physiological basis for diurnal activity in despersing juvenile Bufo granulosus in the Caatinga, a Brazilian semi-arid environment. Comp Biochem Physiol A 147:647–657CrossRefGoogle Scholar
  33. Oki S, Desaki J, Matsuda Y, Okumura H, Shibata T (1995) Capillaries with fenestrae in the rat soleus muscle after experimental limb immobilization. J Electron Microsc 44:307–310Google Scholar
  34. Oki S, Itoh T, Desaki J, Matsuda Y, Okumura H, Shibata T (1998) Three dimensional structure of the vascular network in normal and immobilised muscles of the rat. Arch Phys Med Rehab 79:31–32CrossRefGoogle Scholar
  35. Pette D, Staron RS (2001) Transitions of muscle fiber phenotypic profiles. Histochem Cell Biol 115:359–372PubMedGoogle Scholar
  36. Pinder AW, Storey KB, Ultsch GR (1992) Estivation and hibernation. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. University of Chicago Press, Chicago, pp 251–274Google Scholar
  37. Powers SK, Kavazis AN, McClung JM (2007) Oxidative stress and disuse muscle atrophy. J Appl Physiol 102:2389–2397CrossRefPubMedGoogle Scholar
  38. Ramnanan CJ, Storey KB (2008) The regulation of thapsigargin-sensitive sarcoendoplasmic reticulum Ca2+-ATPase activity in estivation. J Comp Physiol B 178:33–45CrossRefPubMedGoogle Scholar
  39. Ramnanan CJ, Storey KB (2006) Suppression of Na+/K+-ATPase activity during estivation in the land snail Otala lactea. J Exp Biol 209:677–688CrossRefPubMedGoogle Scholar
  40. Rennie MJ, Wackerhage H, Spangenburg EE, Booth FW (2004) Control of the size of human muscle mass. Annu Rev Physiol 66:799–828CrossRefPubMedGoogle Scholar
  41. Rupert JL (2003) The search for genotypes that underlie human performance phenotypes. Comp Biochem Physiol A 136:191–203CrossRefGoogle Scholar
  42. Shavlakadze T, Grounds M (2006) Of bears, meat, mice and men: complexity of factors affecting skeletal muscle mass and fat. Bioessays 28:994–1009CrossRefPubMedGoogle Scholar
  43. Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65:145–174CrossRefPubMedGoogle Scholar
  44. Storey KB, Storey JM (2007) Tribute to P.L. Lutz: putting life on “pause” – molecular regulation of hypometabolism. J Exp Biol 210:1700–1714CrossRefPubMedGoogle Scholar
  45. Symonds BL, James RS, Franklin CE (2007) Getting the jump on skeletal muscle disuse atrophy: preservation of contractile performance in aestivating Cyclorana alboguttata. J Exp Biol 210:825–835CrossRefPubMedGoogle Scholar
  46. Tabary JC, Tabart C, Tardieu C, Tardieu G, Goldspink G (1972) Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts. J Physiol 224:231–244PubMedGoogle Scholar
  47. Temple GK, Johnston IA (1998) Testing hypotheses concerning the phenotypic plasticity of escape performance in fish of the family Cottidae. J Exp Biol 201:317–331PubMedGoogle Scholar
  48. Thom JM, Thompson MW, Ruell PA, Bryant GJ, Fonda JS, Harmer AR, Janse de Jong XAK, Hunter SK (2001) Effect of 10-day cast immobilization on sarcoplasmic reticulum calcium regulation in humans. Acta Physiol Scand 172:141–147CrossRefPubMedGoogle Scholar
  49. Tinker DB, Harlow HJ, Beck TDI (1998) Protein use and muscle-fibre changes in free-ranging, hibernating bears. Physiol Zool 71:414–424CrossRefPubMedGoogle Scholar
  50. Trappe S, Trappe T, Gallagher P, Harber M, Alkner B, Tesch P (2004) Human muscle fibre function with 84 day bed-rest and resistance exercise. J Physiol 557(2):501–513CrossRefPubMedGoogle Scholar
  51. Tsuji JS, Huey RB, Van Berkum FH, Garland T, Shaw RG (1989) Locomotor performance of hatchling fence lizards (Sceloporus occidentalis): quantitative genetics and morphometric correlates. Evol Ecol 3:240–252CrossRefGoogle Scholar
  52. Vyskočil F, Gutmann E (1977) Contractile and histochemical properties of skeletal muscle in hibernating and awake golden hamsters. J Comp Physiol 122:385–390Google Scholar
  53. West TG, Donohoe PH, Staples JF, Askew GN (2006) The role for skeletal muscle in the hypoxia-induced hypometabolic responses of submerged frogs. J Exp Biol 209:1159–1168CrossRefPubMedGoogle Scholar
  54. Williams PE, Goldspink G (1973) The effect of immobilization on the longitudinal growth of striated muscle fibres. J Anat 116:45–55PubMedGoogle Scholar
  55. Wilson RS, James RS, Johnston IA (2000) Thermal acclimation of locomotor performance in tadpoles and adults of the aquatic frog, Xenopus laevis. J Comp Physiol B 170:117–124CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Department of Biomolecular and Sport SciencesCoventry UniversityCoventryUK

Personalised recommendations