Abstract
Animals perform a vast array of motor activities. Although it has generally been accepted that muscles are well suited to the function that they must perform, specialization for performing one function may compromise their ability for carrying out another. We examined this principle in the toadfish muscular system: slow-twitch red and fast-twitch white myotomal muscles are used for powering swimming at relatively low frequencies, while the superfast swimbladder muscle powers mating calls by contracting at 100 Hz. We measured muscle power output over a wide range of frequencies. The red and white locomotory muscles could not generate power over ca. 2.2 and 12 Hz, respectively and, hence, could not power sound production. In contrast, the swimbladder muscle has many specializations that permit it to generate power at frequencies in excess of 100 Hz. However, these specializations drastically reduce its power output at low frequencies: the swimbladder muscle generated only one-twentieth of the power of the red muscle and one-seventh of the power of the white muscle at the frequencies used during swimming. To generate the same total power needed for swimming would require unfeasibly large amounts of swimbladder muscle that could not fit into the fish. Hence, the designs of the swimbladder and locomotory muscles are mutually exclusive.
Full Text
The Full Text of this article is available as a PDF (152.2 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Altringham J. D., Young I. S. Power output and the frequency of oscillatory work in mammalian diaphragm muscle: the effects of animal size. J Exp Biol. 1991 May;157:381–389. doi: 10.1242/jeb.157.1.381. [DOI] [PubMed] [Google Scholar]
- Appelt D., Shen V., Franzini-Armstrong C. Quantitation of Ca ATPase, feet and mitochondria in superfast muscle fibres from the toadfish, Opsanus tau. J Muscle Res Cell Motil. 1991 Dec;12(6):543–552. doi: 10.1007/BF01738442. [DOI] [PubMed] [Google Scholar]
- HILL A. V. THE EFFICIENCY OF MECHANICAL POWER DEVELOPMENT DURING MUSCULAR SHORTENING AND ITS RELATION TO LOAD. Proc R Soc Lond B Biol Sci. 1964 Jan 14;159:319–324. doi: 10.1098/rspb.1964.0005. [DOI] [PubMed] [Google Scholar]
- James R. S., Young I. S., Cox V. M., Goldspink D. F., Altringham J. D. Isometric and isotonic muscle properties as determinants of work loop power output. Pflugers Arch. 1996 Sep;432(5):767–774. doi: 10.1007/s004240050197. [DOI] [PubMed] [Google Scholar]
- Layland J., Young I. S., Altringham J. D. The effect of cycle frequency on the power output of rat papillary muscles in vitro. J Exp Biol. 1995 Apr;198(Pt 4):1035–1043. doi: 10.1242/jeb.198.4.1035. [DOI] [PubMed] [Google Scholar]
- Rome L. C., Cook C., Syme D. A., Connaughton M. A., Ashley-Ross M., Klimov A., Tikunov B., Goldman Y. E. Trading force for speed: why superfast crossbridge kinetics leads to superlow forces. Proc Natl Acad Sci U S A. 1999 May 11;96(10):5826–5831. doi: 10.1073/pnas.96.10.5826. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rome L. C., Funke R. P., Alexander R. M., Lutz G., Aldridge H., Scott F., Freadman M. Why animals have different muscle fibre types. Nature. 1988 Oct 27;335(6193):824–827. doi: 10.1038/335824a0. [DOI] [PubMed] [Google Scholar]
- Rome L. C., Swank D. The influence of temperature on power output of scup red muscle during cyclical length changes. J Exp Biol. 1992 Oct;171:261–281. doi: 10.1242/jeb.171.1.261. [DOI] [PubMed] [Google Scholar]
- Rome L. C., Syme D. A., Hollingworth S., Lindstedt S. L., Baylor S. M. The whistle and the rattle: the design of sound producing muscles. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):8095–8100. doi: 10.1073/pnas.93.15.8095. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rome Lawrence C., Lindstedt Stan L. The Quest for Speed: Muscles Built for High-Frequency Contractions. News Physiol Sci. 1998 Dec;13(NaN):261–268. doi: 10.1152/physiologyonline.1998.13.6.261. [DOI] [PubMed] [Google Scholar]
- Zhang G., Swank D. M., Rome L. C. Quantitative distribution of muscle fiber types in the scup Stenotomus chrysops. J Morphol. 1996 Jul;229(1):71–81. doi: 10.1002/(SICI)1097-4687(199607)229:1<71::AID-JMOR4>3.0.CO;2-S. [DOI] [PubMed] [Google Scholar]