In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livia)

Andrew A. Biewener, William R. Corning, Bret W. Tobalske

Research output: Contribution to journalArticlepeer-review

Abstract

For the first time, we report in vivo measurements of pectoralis muscle length change obtained using sonomicrometry combined with measurements of its force development via deltopectoral crest strain recordings of a bird in free flight. These measurements allow us to characterize the contractile behavior and mechanical power output of the pectoralis under dynamic conditions of slow level flight in pigeons Columba livia. Our recordings confirm that the pigeon pectoralis generates in vivo work loops that begin with the rapid development of force as the muscle is being stretched or remains nearly isometric near the end of the upstroke. The pectoralis then shortens by a total of 32 % of its resting length during the downstroke, generating an average of 10.3±3.6J kg-1 muscle (mean ± S.D.) of work per cycle for the anterior and posterior sites recorded among the five animals. In contrast to previous kinematic estimates of muscle length change relative to force development, the sonomicrometry measurements of fascicle length change show that force declines during muscle shortening. Simultaneous measurements of fascicle length change at anterior and posterior sites within the same muscle show significant (P<0.001, three of four animals) differences in fractional length (strain) change that averaged 19±12 %, despite exhibiting similar work loop shape. Length changes at both anterior and posterior sites were nearly synchronous and had an asymmetrical pattern, with shortening occupying 63 % of the cycle. This nearly 2:1 phase ratio of shortening to lengthening probably favors the ability of the muscle to do work. Mean muscle shortening velocity was 5.38±1.33 and 4.88±1.27 lengths s-1 at the anterior and posterior sites respectively. Length excursions of the muscle were more variable at the end of the downstroke (maximum shortening), particularly when the birds landed, compared with highly uniform length excursions at the end of the upstroke (maximum lengthening). When averaged for the muscle as a whole, our in vivo work measurements yield a mass-specific net mechanical power output of 70.2 W kg-1 for the muscle when the birds flew at 5-6 m s-1, with a wingbeat frequency of 8.7 Hz. This is 38 % greater than the value that we obtained previously for wild-type pigeons, but still 24-50 % less than that predicted by theory.

Original languageEnglish
Pages (from-to)3293-3307
Number of pages15
JournalJournal of Experimental Biology
Volume201
Issue number24
StatePublished - 1998

Keywords

  • Columba livia
  • Flight
  • Force-length behaviour
  • Mechanical power output
  • Muscle
  • Pectoralis
  • Pigeon
  • Sonomicrometry

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