A review of the thermal sensitivity of the mechanics of vertebrate skeletal muscle

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 183, Issue 6, 2013, Pages 723-733

  James, Rob S ^a  

^a Faculty of Engineering and Computing   (United Kingdom)

Author keywords

Force; Power; Q10; Temperature

Indexed keywords

ACCLIMATIZATION; ANIMAL; BIOMECHANICS; ENVIRONMENT; MOTOR ACTIVITY; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE ISOMETRIC CONTRACTION; MUSCLE RELAXATION; PHYSIOLOGY; REVIEW; SKELETAL MUSCLE; TEMPERATURE; VERTEBRATE;

ACCLIMATIZATION; ANIMALS; BIOMECHANICAL PHENOMENA; ENVIRONMENT; ISOMETRIC CONTRACTION; MOTOR ACTIVITY; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE RELAXATION; MUSCLE, SKELETAL; TEMPERATURE; VERTEBRATES;

EID: 84880634806     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-013-0748-1     Document Type: Review

References (110)

1. Altringham JD, Block BA (1997) Why do tuna maintain elevated slow muscle temperatures? Power output of muscle isolated from endothermic and ectothermic fish. J Exp Biol 200: 2617-2627.
2. Angilletta MJ Jr (2009) Thermal adaptation. A theoretical and empirical synthesis. Oxford University Press, Oxford.
3. Angilletta MJ Jr, Cooper BS, Schuler MS, Boyles JG (2010) The evolution of thermal physiology in endotherms. Front Biosci E2: 861-881.
4. Ball D, Johnston IA (1996) Molecular mechanisms underlying the plasticity of muscle contractile properties with temperature acclimation in the marine fish Myoxocephalus scorpius. J Exp Biol 199: 1363-1373.
5. Barany M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50: 197-216.
6. Barclay CJ, Woledge RC, Curtin NA (2010) Is the efficiency of mammalian (mouse) skeletal muscle temperature dependent? J Physiol 588(19): 3819-3831.
7. Beddow TA, Johnston IA (1995) Plasticity of muscle contractile properties following temperature acclimation in the marine fish Myoxocephalus scorpius. J Exp Biol 198: 193-201.
8. Bennett AF (1984) Thermal dependence of muscle function. Am J Physiol 247: R217-R229.
9. Bennett AF (1990) Thermal dependence of locomotor capacity. Am J Physiol 259: R253-R258.
10. Bernal D, Donley JM, Shadwick RE, Syme DA (2005) Mammal-like muscles power swimming in a cold-water shark. Nature 437: 1349-1352.
11. Bershitsky SY, Tsaturyan AK (2002) The elementary force generation process probed by temperature and length perturbations in muscle fibres from rabbit. J Physiol 540: 971-988.
12. Boyles JG, Seebacher F, Smit B, McKechnie AE (2011) Adaptive thermoregulation in endotherms may alter responses to climate change. Integr Comp Biol 51: 676-690.
13. Bradshaw WE, Holzapfel CM (2006) Evolutionary response to rapid climate change. Science 312: 1477-1478.
14. Breau C, Cunjak RA, Peake SJ (2011) Behaviour during elevated water temperatures: can physiology explain movement of juvenile Atlantic salmon to cool water? J Anim Ecol 80: 844-853.
15. Brenner B, Eisenberg E (1986) Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Nat Acad Sci 83: 3542-3546.
16. Caiozzo VJ (2002) Plasticity of skeletal muscle phenotype: mechanical consequences. Muscle Nerve 26: 740-768.
17. Cavieres G, Sabat P (2008) Geographic variation in the response to thermal acclimation in rufous-collared sparrows: are physiological flexibility and environmental heterogeneity correlated? Funct Ecol 22: 509-515.
18. Colombini B, Nocella M, Benelli G, Cecchi G, Bagni MA (2008) Effect of temperature on cross-bridge properties in intact frog muscle fibers. Am J Physiol 294: C1113-C1117.
19. Corp N, Gorman ML, Speakman JR (1997) Seasonal variation in the resting metabolic rate of male wood mice Apodemus sylvaticus from two contrasting habitats 15 km apart. J Comp Physiol B 167: 229-239.
20. Coughlin DJ, Zhang G, Rome LC (1996) Contraction dynamics and power production of pink muscle of the scup (Stenotomus chrysops). J Exp Biol 199: 2703-2712.
21. Coupland ME, Pinniger GJ, Ranatunga KW (2005) Endothermic force generation, temperature-jump experiments and effects of increased [MgADP] in rabbit psoas muscle fibres. J Physiol 567: 471-492.
22. Crockford T, Johnston IA (1990) Temperature acclimation and the expression of contractile protein isoforms in the skeletal muscles of the common carp (Cyprinus carpio L.). J Comp Physiol B 160: 23-30.
23. Crowley SR, Pietruszka RD (1983) Aggressiveness and vocalization in the leopard lizard (Gambelia wislizennii): the influence of temperature. Anim Behav 31: 1055-1060.
24. De Ruiter CJ, De Haan A (2000) Temperature effect on the force/velocity relationship of the fresh and fatigued human adductor pollicis muscle. Pflügers Arch 440: 163-170.
25. Decostre V, Bianco P, Lombardi V, Piazzesi G (2005) Effect of temperature on the working stroke of muscle myosin. PNAS 102: 13927-13932.
26. Donley JM, Shadwick RE, Sepulveda CA, Syme DA (2007) Thermal dependence of contractile properties of the aerobic locomotor muscle in the leopard shark and shortfin mako shark. J Exp Biol 210: 1194-1203.
27. Donley JM, Sepulveda CA, Aalbers SA, McGillivray DG, Syme DA, Bernal D (2012) Effects of temperature on power output and contraction kinetics in the locomotor muscle of the regionally endothermic common thresher shark (Alopias vulpinus). Fish Physiol Biochem 38: 1507-1519.
28. Ducharme MB, VanHelder WP, Radomski MW (1991) Tissue temperature profile in the human forearm during thermal stress at thermal stability. J Appl Physiol 71: 1973-1978.
29. Dunbar MB, Brigham RM (2010) Thermoregulatory variation among populations of bats along a latitudinal gradient. J Comp Physiol B 180: 885-893.
30. Else PL, Bennett AF (1987) The thermal dependence of locomotor performance and muscle contractile function in the salamander Ambystoma tigrinum nebulosum. J Exp Biol 128: 219-233.
31. Fangue NA, Mandic M, Richards JG, Schulte PM (2008) Swimming performance and energetics as a function of temperature in killifish Fundulus heteroclitus. Physiol Biochem Zool 81: 389-401.
32. Fry FEJ, Hart JS (1948) The relation of temperature to oxygen consumption in the goldfish. Biol Bull 94: 66-77.
33. Gabriel W (2005) How stress selects for reversible phenotypic plasticity. J Evolution Biol 18: 873-883.
34. Ganguly AR, Steinhaeuser K, Erickson DJ III, Branstetter M, Parish ES, Singh N, Drake JB, Buja L (2009) Higher trends but larger uncertainty and geographic variability in 21st century temperature and heat waves. Proc Natl Acad Sci USA 106: 15555-15559.
35. Gibbs CL, Chapman JB (1974) Effects of stimulus conditions, temperature, and length on energy output of frog and toad sartorius. Am J Physiol 227: 964-971.
36. Glanville EJ, Seebacher F (2006) Compensation for environmental change by complementary shifts of thermal sensitivity and thermoregulatory behaviour in an ectotherm. J Exp Biol 209: 4869-4877.
37. Glanville EJ, Seebacher F (2010) Plasticity in body temperature and metabolic capacity sustains winter activity in a small endotherm (Rattus fuscipes). Comp Biochem Physiol A 155: 383-391.
38. Gomes FR, Bevier CC, Navas CA (2002) Environmental and physiological factors influence antipredator behaviour in Scinax hiemalis (Anura: Hylidae). Copeia 2002: 994-1005.
39. Guderley H (2004) Metabolic responses to low temperature in fish muscle. Biol Rev 79: 409-427.
40. Guderley H, St-Pierre J (2002) Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change. J Exp Biol 205: 2237-2249.
41. Herrel A, James RS, van Damme R (2007) Fight versus flight: physiological basis for temperature dependent behavioral shifts in lizards. J Exp Biol 210: 1762-1767.
42. Hertz PE, Huey RB, Nevo E (1982) Fight versus flight: body temperature influences defensive responses of lizards. Anim Behav 30: 676-679.
43. Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc B 126: 136-195.
44. Hochachka PW, Somero GN (2002) Biochemical adaptation. Princeton University Press, Princeton.
45. 2+ dissociation rates from parvalbumin of frog muscle fibres. J Physiol 449: 399-410.
46. Huey RB, Kearney MR, Krockenberger A, Holtum JAM, Jess M, Williams SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Phil Trans R Soc B 367: 1665-1679.
47. Husby A, Visser ME, Kruuk LEB (2011) Speeding up microevolution: the effects of increasing temperature on selection and genetic variance in a wild bird population. PLoS Biol 9: e1000585.
48. Imai J-I, Hirayama Y, Kikuchi K, Kakinuma M, Watabe S (1997) cDNA cloning of myosin heavy chain isoforms from carp fast skeletal muscle and their gene expression associated with temperature acclimation. J Exp Biol 200: 27-34.
49. James RS, Tallis J, Herrel A, Bonneaud C (2012) Warmer is better: thermal sensitivity of both maximal and sustained power output in the iliotibialis muscle isolated from adult Xenopus tropicalis. J Exp Biol 215: 552-558.
50. John-Alder HB, Barnhart MC, Bennett AF (1988) Thermal sensitivity of swimming performance and muscle contraction in northern and southern populations of tree frogs (Hyla crucifer). J Exp Biol 142: 357-372.
51. Johnson TP, Bennett AF (1995) The thermal acclimation of burst escape performance in fish: an integrated study of molecular and cellular physiology and organismal performance. J Exp Biol 198: 2165-2175.
52. Johnson TP, Johnston IA (1991) Power output of fish muscle fibres performing oscillatory work: effects of acute and seasonal temperature change. J Exp Biol 157: 409-423.
53. Johnson TP, Johnston IA, Moon TW (1991) Temperature and the energy cost of oscillatory work in teleost fast muscle fibres. Pflugers Arch 419: 177-183.
54. Johnston IA, Altringham JD (1985) Evolutionary adaptation of muscle power output to environmental temperature: force-velocity characteristics of skinned fibres isolated from antarctic, temperate and tropical marine fish. Pflugers Arch 405: 136-140.
55. Johnston IA, Gleeson TT (1984) Thermal dependence of contractile properties of red and white fibres isolated from the iliofibularis muscle of the desert iguana (Dipsosaurus dorsalis). J Exp Biol 113: 123-132.
56. Johnston IA, Gleeson TT (1987) Effect of temperature on contractile properties of skinned muscle fibres from three toad species. Am J Physiol 252: R371-R375.
57. Johnston IA, Temple GK (2002) Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour. J Exp Biol 205: 2305-2322.
58. 2+- activated myofibrillar ATPase induced by temperature acclimation. FEBS Lett 50: 293-295.
59. Josephson RK (1993) Contraction dynamics and power output of skeletal muscle. Ann Rev Physiol 55: 527-546.
60. Kenny GP, Reardon FD, Zaleski W, Reardon ML, Haman F, Ducharm MB (2003) Muscle temperature transients before, during, and after exercise measured using an intramuscular multisensor probe. J Appl Physiol 94: 2350-2357.
61. Kolbe JJ, Kearney M, Shine R (2010) Modeling the consequences of thermal trait variation for the cane toad invasion of Australia. Ecol Appl 20: 2273-2285.
62. Lännergren J, Westerblad H (1987) The temperature dependence of isometric contractions of single, intact fibres dissected from a mouse foot muscle. J Physiol 390: 285-293.
63. Le Galliard JF, Clobert J, Ferrière R (2004) Physical performance and Darwinian fitness in lizards. Nature 432(7016): 502-505.
64. Lieber RL, Friden J (2000) Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23: 1647-1666.
65. Lindstedt SL, McGlothlin T, Percy E, Pifer J (1998) Task-specific design of skeletal muscle: balancing muscle structural composition. Comp Biochem Physiol B: Biochem Mol Biol 120: 35-40.
66. Marsh RL (1994) Jumping ability of anurans. In: Jones JH (ed) Comparative vertebrate exercise physiology. Academic Press, San Diego, pp 51-111.
67. Marsh RL, Bennett AF (1985) Thermal dependence of isotonic contractile properties of skeletal muscle and sprint performance of the lizard Dipsosaurus dorsalis. J Comp Physiol B 155: 541-551.
68. Mautz WJ, Daniels CB, Bennett AF (1992) Thermal dependence of locomotion and aggression in a xantusiid lizard. Herpetologica 48: 271-279.
69. Navas CA, Otani L (2007) Physiology, environmental change, and anuran conservation. Phyllomedusa 6: 83-103.
70. Navas CA, James RS, Wakeling JM, Kemp KM, Johnston IA (1999) An integrative study of the temperature dependence of whole animal and muscle performance during jumping and swimming in the frog Rana temporaria. J Comp Physiol B 169: 588-596.
71. Niehaus AC, Wilson RS, Seebacher F, Franklin CE (2011) Striped marsh frog (Limnodynastes peronii) tadpoles do not acclimate. J Exp Biol 214: 1965-1970.
72. Niehaus AC, Angilletta MJ Jr, Sears MW, Franklin CE, Wilson RS (2012) Predicting the physiological performance of ectotherms in fluctuating thermal environments. J Exp Biol 215: 694-701.
73. Piazzesi G, Reconditi M, Koubassova N, Decostre V, Linari M, Lucii L, Lombardi V (2003) Temperature dependence of the force-generating process in single fibres from frog skeletal muscle. J Physiol 549: 93-106.
74. Place N, Yamada T, Zhang S-J, Westerblad H, Bruton JD (2009) High temperature does not alter fatigability in intact mouse skeletal muscle fibres. J Physiol 587: 4717-4724.
75. Putnam RW, Bennett AF (1983) Histochemical, enzymatic and contractile properties of skeletal muscles of three anuran amphibians. Am J Physiol 244: R558-R567.
76. Racinais S, Oksa J (2010) Temperature and neuromuscular function. Scand J Med Sci Sports 20: 1-18.
77. Rall JA, Woledge RC (1990) Influence of temperature on mechanics and energetics of muscle contraction. Am J Physiol 259: R197-R203.
78. Ranatunga KW (1982) Temperature-dependence of shortening velocity and rate of isometric tension development in rat skeletal muscle. J Physiol 329: 465-483.
79. Ranatunga KW (1998) Temperature dependence of mechanical power output in mammalian (rat) skeletal muscle. Exp Physiol 83: 371-376.
80. Refinetti R (1999) Amplitude of the daily rhythm of body temperature in eleven mammalian species. J Therm Biol 24: 477-481.
81. Renaud JM, Stevens ED (1984) The extent of short-term and long-term compensation to temperature shown by frog and toad sartorius muscle. J Exp Biol 108: 57-75.
82. Rezende EL, Chappell MA, Hammond KA (2004) Cold-acclimation in Peromyscus: temporal effects and individual variation in maximum metabolism and ventilatory traits. J Exp Biol 207: 295-305.
83. Rome LC (1983) The effect of long-term exposure to different temperatures on the mechanical performance of frog muscle. Physiol Zool 56: 33-40.
84. Rome LC, Sosnicki AA (1990) The influence of temperature on mechanics of red muscle in carp. J Physiol 427: 151-169.
85. Rome LC, Swank D (1992) The influence of temperature on power output of scup red muscle during cyclical length changes. J Exp Biol 171: 261-281.
86. Rome LC, Swank D, Coughlin DJ (1999) The influence of temperature on power production during swimming II. Mechanics of red muscle fibres in vivo. J Exp Biol 202: 333-345.
87. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421: 57-60.
88. Roots H, Ball G, Talbot-Ponsonby J, King M, McBeath K, Ranatunga KW (2009) Muscle fatigue examined at different temperatures in experiments on intact mammalian (rat) muscle fibers. J Appl Physiol 106: 378-384.
89. Saltin B, Gagge AP, Stolwijk JA (1968) Muscle temperature during submaximal exercise in man. J Appl Physiol 25: 679-688.
90. Šamajová P, Gvoždík L (2010) Inaccurate or disparate temperature cues? Seasonal acclimation of terrestrial and aquatic locomotor capacity in newts. Funct Ecol 24: 1023-1030.
91. Schaefer J, Ryan A (2006) Developmental plasticity in the thermal tolerance of zebrafish Danio rerio. J Fish Biol 69: 722-734.
92. Seebacher F (2005) A review of thermoregulation and physiological performance in reptiles: what is the role of phenotypic flexibility? J Comp Physiol B 175: 453-461.
93. Seebacher F, Franklin CE (2011) Physiology of invasion: cane toads are constrained by thermal effects on physiological mechanisms that support locomotor performance. J Exp Biol 214: 1437-1444.
94. Seebacher F, James RS (2008) Plasticity of muscle function in a thermoregulating ectotherm (Crocodylus porosus): biomechanics and metabolism. Am J Physiol 294: R1024-R1032.
95. Seebacher F, Holmes S, Roosen NJ, Nouvian M, Wilson RS, Ward AJW (2012) Capacity for thermal acclimation differs between populations and phylogenetic lineages within a species. Funct Ecol 26: 1418-1428.
96. Segal SS, Faulkner JA, White TP (1986) Skeletal muscle fatigue in vitro is temperature dependent. J Appl Physiol 61: 660-665.
97. Sinclair ELE, Thompson MB, Seebacher F (2006) Phenotypic flexibility in the metabolic response of the limpet Cellana tramoserica to thermally different microhabitats. J Exp Mar Biol Ecol 335: 131-141.
98. Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, Lara-Resendiz R, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H, Avila LJ, Morando M, De la Riva IJ, Sepulveda PV, Rocha CFD, Ibargüengoytía N, Puntriano CA, Massot M, Lepetz V, Oksanen TA, Chapple DG, Bauer AM, Branch WR, Clobert J, Sites JW Jr (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328: 894-899.
99. Stein RB, Gordon T, Shriver J (1982) Temperature dependence of mammalian muscle contractions and ATPase activities. Biophys J 40: 97-107.
100. Swank DM, Rome LC (2001) The influence of thermal acclimation on power production during swimming II. Mechanics of scup red muscle under in vivo conditions. J Exp Biol 204: 419-430.
101. Swoap SJ, Johnson TP, Josephson RK, Bennett AF (1993) Temperature, muscle power output, and limitations on burst locomotor performance of the lizard Dipsosaurus dorsalis. J Exp Biol 174: 185-197.
102. Sylvestre E-L, Lapointe D, Dutil J-D, Guderley H (2007) Thermal sensitivity of metabolic rates and swimming performance in two latitudinally separated populations of cod, Gadus morhua L. J Comp Physiol B 177: 447-460.
103. Syme DA (2006) Functional properties of skeletal muscle. In: Shadwick RE, Lauder GV (eds) Fish physiology: fish biomechanics, series Randall DJ, Farrell AP (eds) vol 23, Academic Press, Elsevier pp 179-240.
104. Walther G-R, Roques A, Hulme PE, Sykes MT, Pyšek P, Kühn I, Zobel M, Bacher S, Botta-Dukát Z, Bugmann H, Czúcz B, Dauber J, Hickler T, Jarošík V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov VE, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vilà M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24: 686-693.
105. Wilson RS (2001) Geographic variation in thermal sensitivity of jumping performance in the frog Limnodynastes peronii. J Exp Biol 204: 4227-4236.
106. Wilson RS, Franklin CE (1999) Thermal acclimation of locomotor performance in tadpoles of the frog Limnodynastes peronii. J Comp Physiol B 169: 445-451.
107. 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: 117-124.
108. Wilson RS, James RS, Kohlsdorf T, Cox VM (2004) Inter-individual variation of isolated muscle performance and structure in the toad Bufo viridis. J Comp Physiol B 174: 453-459.
109. Wooden KM, Walsberg GE (2004) Body temperature and locomotor capacity in a heterothermic rodent. J Exp Biol 207: 41-46.
110. Yaicharoen P, Wallman K, Morton A, Bishop D (2012) The effect of warm-up on intermittent sprint performance and selected thermoregulatory parameters. J Sci Med Sport 15: 451-456.