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Journal of Comparative Physiology B

, Volume 188, Issue 4, pp 623–634 | Cite as

Scaling of work and power in a locomotor muscle of a frog

Original Paper

Abstract

Muscle work and power are important determinants of movement performance in animals. How these muscle properties scale determines, in part, the scaling of performance during movements, such as jump height or distance. Muscle-mass-specific work is predicted to remain constant across a range of scales, assuming geometric similarity, while muscle-mass-specific power is expected to decrease with increasing scale. We tested these predictions by examining muscle morphology and contractile properties of plantaris muscles from frogs ranging in mass from 1.28 to 20.60 g. Scaling of muscle work and power was examined using both linear regression on log10-transformed data (LR) and non-linear regressions on untransformed data (NLR). Results depended on the method of regression not because of large changes in scaling slopes, but because of changing levels of statistical significance using corrections for multiple tests, demonstrating the importance of careful consideration of statistical methods when analyzing patterns of scaling. In LR, muscle-mass-specific work decreased with increasing scale, but an accompanying positive allometry of muscle mass predicts constant movement performance at all scales. These relationships were non-significant in NLR, though scaling with geometric similarity also predicts constant jump performance across scales, because of proportional increases in available muscle energy and body mass. Both intrinsic shortening velocity and muscle-mass-specific power were positively allometric in both types of analysis. Nonetheless, scale accounts for little variation in contractile properties overall over the range examined, indicating that other sources of intraspecific variation may be more important in determining muscle performance and its effects on movement.

Keywords

Allometry Osteopilus septentrionalis Jumping Contractile properties 

Notes

Acknowledgements

We thank J. Scales, M.K. O’Donnell, C. Stinson, and C. Ramsay for assistance in obtaining frogs.

Funding

Funding was provided by The National Science Foundation Directorate for Biological Sciences [IOS 1350929 to SMD].

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Data availability

Datasets and R scripts used for analyses are available for download at https://github.com/MyoPhys/muscle-scaling.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in this study were in accordance with the ethical standards of the University of South Florida Institutional Animal Care and Use Committee.

References

  1. Alexander RM, Bennet-Clark HC (1977) Storage of elastic strain energy in muscle and other tissues. Nature 265:114–117CrossRefPubMedGoogle Scholar
  2. Altringham JD, Johnston IA (1990) Scaling effects on muscle function: power output of isolated fish muscle fibres performing oscillatory work. J Exp Biol 151:453–467Google Scholar
  3. Altringham JD, Morris R, James RS, Smith CI (1996) Scaling effects on muscle function in fast and slow muslces of Xenopus laevis. Exp Biol Online 1 (6)Google Scholar
  4. Askew GN, Marsh RL (2002) Muscle designed for maximum short-term power output: quail flight muscle. J Exp Biol 205:2153–2160PubMedGoogle Scholar
  5. Astley HC, Roberts TJ (2012) Evidence for a vertebrate catapult: elastic energy storage in the plantaris tendon during frog jumping. Biol Lett 8(3):386–389.  https://doi.org/10.1098/rsbl.2011.0982 CrossRefPubMedGoogle Scholar
  6. Autumn K, Hsieh ST, Dudek DM, Chen J, Chitphan C, Full RJ (2006) Dynamics of geckos running vertically. J Exp Biol 209(2):260–272.  https://doi.org/10.1242/jeb.01980 CrossRefPubMedGoogle Scholar
  7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc: Ser B (Methodol) 57(1):289–300Google Scholar
  8. Bennet-Clark HC (1977) Scale effects in animal jumping. In: Pedley TJ (ed) Scale effects in animal locomotion. Academic Press Ltd., LondonGoogle Scholar
  9. Bennet-Clark HC, Lucey ECA (1967) The jump of the flea: a study of the energetics and a model of the mechanism. J Exp Biol 47:59–76PubMedGoogle Scholar
  10. Bennett AF, Garland T Jr, Else PL (1989) Individual correlation of morphology, muscle mechanics, and locomotion in a salamander. Am J Physiol 256(6):R1200-R1208Google Scholar
  11. Biewener AA (2003) Animal locomotion. Oxford Animal Biology Series. Oxford University Press Inc., New York, NYGoogle Scholar
  12. Bonner JT (2006) Why size matters: from bacteria to Blue Whales. Princeton University Press, PrincetonGoogle Scholar
  13. Borelli GA (1680) De Motu Animalium (English Translation by P. Maquet). Springer, BerlinGoogle Scholar
  14. Curtin NA, Woledge RC (1988) Power output and force–velocity relationship of live fibres from white myotomal muscle of the dogfish, Scyliorhinus canicula. J Exp Biol 140:187–197Google Scholar
  15. Deban SM, O’Reilly JC (2005) The ontogeny of feeding kinematics in a giant salamander Cryptobranchus alleganiensis: does current function or phylogenetic relatedness predict the scaling patterns of movement? Zoology (Jena) 108(2):155–167.  https://doi.org/10.1016/j.zool.2005.03.006 CrossRefGoogle Scholar
  16. Deban SM, O’Reilly JC, Dicke U, van Leeuwen JL (2007) Extremely high-power tongue projection in plethodontid salamanders. J Exp Biol 210(Pt 4):655–667.  https://doi.org/10.1242/jeb.02664 CrossRefPubMedGoogle Scholar
  17. Emerson SB (1978) Allometry and jumping in frogs: helping the twain to meet. Evolution 32(3):551–564CrossRefPubMedGoogle Scholar
  18. Emerson SB (1985) Jumping and leaping. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Harvard University Press, Cambridge, MAGoogle Scholar
  19. Fischmeister R, Hartzell HC (1987) Cyclic guanosine 3′, 5′-monophosphate regulates the calcium current in single cells from frog ventricle. J Physiol 387:453–472CrossRefPubMedPubMedCentralGoogle Scholar
  20. Glazier DS (2013) Log-transformation is useful for examining proportional relationships in allometric scaling. J Theor Biol 334:200–203.  https://doi.org/10.1016/j.jtbi.2013.06.017 CrossRefPubMedGoogle Scholar
  21. Hill AV (1950) The dimensions of animals and their muscular dynamics. Sci Prog 38:209–230Google Scholar
  22. Hu DL, Chan B, Bush JWM (2003) The hydrodynamics of water strider locomotion. Nature 424:663–666CrossRefPubMedGoogle Scholar
  23. James RS, Johnston IA (1998) Scaling of muscle performance during escape responses in the fish Myoxocephalus scorpius L. J Exp Biol 201:913–923PubMedGoogle Scholar
  24. James RS, Cole NJ, Davies MLF, Johnston IA (1998) Scaling of intrinsic contractile properties and myofibrillar protein composition of fast muscle in the fish Myoxocephhalus scorpius L. J Exp Biol 201:901–912PubMedGoogle Scholar
  25. James RS, Vanhooydonck B, Tallis JA, Herrel A (2015) Larger lacertid lizard species produce higher than expected iliotibialis muscle power output: the evolution of muscle contractile mechanics with body size. J Exp Biol 218(Pt 22):3589–3595.  https://doi.org/10.1242/jeb.124974 CrossRefPubMedGoogle Scholar
  26. Johnson TP, Swoap SJ, Bennett AF, Josephson RK (1993) Body size, muscle power output and limitations on burst locomotor performance in the lizard Dipsosaurus dorsalis. J Exp Biol 174:199–213Google Scholar
  27. Lemaitre JF, Vanpe C, Plard F, Pelabon C, Gaillard JM (2015) Response to Packard: make sure we do not throw out the biological baby with the statistical bath water when performing allometric analyses. Biol Lett 11(6):20150144.  https://doi.org/10.1098/rsbl.2015.0144 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lutz GJ, Rome LC (1994) Built for jumping: the design of the frog muscular system. Science 263:370–372CrossRefPubMedGoogle Scholar
  29. Marsh RL (1988) Ontogenesis of contractile properties of skeletal muscle and sprint performance in the lizard Dipsosaurus dorsalis. J Exp Biol 137:119–139PubMedGoogle Scholar
  30. Marsh RL (1994) Jumping ability of anuran amphibians. In: Jones JH (ed) Comparative vertebrate exercise physiology. Academic Press, Inc., San Diego, pp 51–111Google Scholar
  31. Mascaro J, Litton CM, Hughes RF, Uowolo A, Schnitzer SA (2014) Is logarithmic transformation necessary in allometry? Ten, one-hundred, one-thousand-times yes. Biol J Linn Soc 111:230–233CrossRefGoogle Scholar
  32. McHenry MJ, Lauder GV (2006) Ontogeny of form and function: locomotor morphology and drag in zebrafish (Danio rerio). J Morphol 267(9):1099–1109.  https://doi.org/10.1002/jmor.10462 CrossRefPubMedGoogle Scholar
  33. McMahon TA (1973) Size and shape in biology. Science 179:1201–1204CrossRefPubMedGoogle Scholar
  34. McMahon TA (1975) Using body size to understand the structural design of animals: quadrupedal locomotion. J Appl Physiol 39(4):619–627CrossRefPubMedGoogle Scholar
  35. McMahon TA, Bonner JT (1983) On size and life. Scientific American Books, New YorkGoogle Scholar
  36. Olberding JP, Deban SM (2017) Effects of temperature and force requirements on muscle work and power output. J Exp Biol 220(Pt 11):2017–2025.  https://doi.org/10.1242/jeb.153114 CrossRefPubMedGoogle Scholar
  37. Packard GC (2013) Is logarithmic transformation necessary in allometry? Biol J Linn Soc 109:476–486CrossRefGoogle Scholar
  38. Packard GC, Birchard GF, Boardman TJ (2011) Fitting statistical models in bivariate allometry. Biol Rev Camb Philos Soc 86(3):549–563.  https://doi.org/10.1111/j.1469-185X.2010.00160.x CrossRefPubMedGoogle Scholar
  39. Peplowski MM, Marsh RL (1997) Work and power output in the hindlimb muscles of Cuban tree frogs Osteopilus septentrionalis during jumping. J Exp Biol 200:2861–2870PubMedGoogle Scholar
  40. Reilly SM (1995) The ontogeny of aquatic feeding behavior in Salamandra salamandra: stereotypy and isometry in feeding kinematics. J Exp Biol 198:701–708PubMedGoogle Scholar
  41. Reilly SM, McElroy EJ, Biknevicius AR (2007) Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods. Zoology (Jena) 110(4):271–289.  https://doi.org/10.1016/j.zool.2007.01.003 CrossRefGoogle Scholar
  42. Roberts TJ, Azizi E (2011) Flexible mechanisms: the diverse roles of biological springs in vertebrate movement. J Exp Biol 214(Pt 3):353–361.  https://doi.org/10.1242/jeb.038588 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Roberts TJ, Marsh RL (2003) Probing the limits to muscle-powered accelerations: lessons from jumping bullfrogs. J Exp Biol 206(15):2567–2580.  https://doi.org/10.1242/jeb.00452 CrossRefPubMedGoogle Scholar
  44. Roberts TJ, Abbott EM, Azizi E (2011) The weak link: do muscle properties determine locomotor performance in frogs? Philos Trans R Soc Lond B Biol Sci 366(1570):1488–1495.  https://doi.org/10.1098/rstb.2010.0326 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Robinson MP, Motta PJ (2002) Patterns of growth and the effects of scale on the feeding kinematics of the nurse shark (Ginglymostoma cirratum). J Zool 256:449–462.  https://doi.org/10.1017/S0952836902000493 CrossRefGoogle Scholar
  46. Schmidt-Nielsen K (1984) Scaling: why is animal size so important? Cambridge University Press, CambridgeCrossRefGoogle Scholar
  47. Suter RB (1999) Cheap transport for fishing spiders (Araneae, Pisauridae): the physics of sailing on the water surface. J Arachnol 27:489–496Google Scholar
  48. Thompson DW (1917) On growth and form. Cambridge University Press, LondonCrossRefGoogle Scholar
  49. Van Wassenbergh S, Herrel A, James RS, Aerts P (2007) Scaling of contractile properties of catfish feeding muscles. J Exp Biol 210(Pt 7):1183–1193.  https://doi.org/10.1242/jeb.000109 CrossRefPubMedGoogle Scholar
  50. Wakeling JM, Johnston IA (1998) Muscle power output limits fast-start performance in fish. J Exp Biol 201(10):1505–1526PubMedGoogle Scholar
  51. Wang Z, Wang J, Ji A, Dai Z (2010) Locomotion behavior and dynamics of geckos freely moving on the ceiling. Chin Sci Bull 55(29):3356–3362.  https://doi.org/10.1007/s11434-010-3079-6 CrossRefGoogle Scholar
  52. Wang Z, Dai Z, Ji A, Ren L, Xing Q, Dai L (2015) Biomechanics of gecko locomotion: the patterns of reaction forces on inverted, vertical and horizontal substrates. Bioinspir Biomim 10(1):016019.  https://doi.org/10.1088/1748-3190/10/1/016019 CrossRefPubMedGoogle Scholar
  53. White CR, Kearney MR (2014) Metabolic scaling in animals: methods, empirical results, and theoretical explanations. Compr Physiol 4(1):231–256.  https://doi.org/10.1002/cphy.c110049 CrossRefPubMedGoogle Scholar
  54. Williams TM (1994) A model of rowing propulsion and the ontogeny of locomotion in Artemia larvae. Biol Bull 187:164–173CrossRefPubMedGoogle Scholar
  55. Xiao X, White EP, Hooten MB, Durham SL (2011) On the use of log-transformation vs. nonlinear regression for analyzing biological power laws. Ecology 92(10):1887–1894CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of South FloridaTampaUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA

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