Work and power output in the hindlimb muscles of Cuban tree frogs Osteopilus septentrionalis during jumping.

It has been suggested that small frogs use a catapult mechanism to amplify muscle power production during the takeoff phase of jumping. This conclusion was based on an apparent discrepancy between the power available from the hindlimb muscles and that required during takeoff. The present study provides integrated data on muscle contractile properties, morphology and jumping performance that support this conclusion. We show here that the predicted power output during takeoff in Cuban tree frogs Osteopilus septentrionalis exceeds that available from the muscles by at least sevenfold. We consider the sartorius muscle as representative of the bulk of the hindlimb muscles of these animals, because this muscle has properties typical of other hindlimb muscles of small frogs. At 25 degrees C, this muscle has a maximum shortening velocity (Vmax) of 8.77 +/- 0.62 L0 s-1 (where L0 is the muscle length yielding maximum isometric force), a maximum isometric force (P0) of 24.1 +/- 2.3 N cm-2 and a maximum isotonic power output of 230 +/- 9.2 W kg-1 of muscle (mean +/- S.E.M.). In contrast, the power required to accelerate the animal in the longest jumps measured (approximately 1.4 m) is more than 800 W kg-1 of total hindlimb muscle. The peak instantaneous power is expected to be twice this value. These estimates are probably conservative because the muscles that probably power jumping make up only 85% of the total hindlimb muscle mass. The total mechanical work required of the muscles is high (up to 60 J kg-1), but is within the work capacities predicted for vertebrate skeletal muscle. Clearly, a substantial portion of this work must be performed and stored prior to takeoff to account for the high power output during jumping. Interestingly, muscle work output during jumping is temperature-dependent, with greater work being produced at higher temperatures. The thermal dependence of work does not follow from simple muscle properties and instead must reflect the interaction between these properties and the other components of the skeletomuscular system during the propulsive phase of the jump.

[1]  G. Zug.  Anuran locomotion--structure and function, 2: jumping performance of semiaquatic, terrestrial, and arboreal frogs , 1978 .

[2]  R. Marsh,et al.  The Enzymatic Basis of High Metabolic Rates in Calling Frogs , 1985, Physiological Zoology.

[3]  R. Marsh,et al.  Thermal dependence of sprint performance of the lizard Sceloporus occidentalis. , 1986, The Journal of experimental biology.

[4]  H. Bennet-Clark,et al.  The jump of the flea: a study of the energetics and a model of the mechanism. , 1967, The Journal of experimental biology.

[5]  Thomas L. Daniel,et al.  SIZE LIMITS IN ESCAPE LOCOMOTION OF CARRIDEAN SHRIMP , 1989 .

[6]  A F Bennett,et al.  Thermal dependence of muscle function. , 1984, The American journal of physiology.

[7]  H. J. de Jongh,et al.  Muscle activity at the ilio‐sacral articulation of frogs , 1980, Journal of morphology.

[8]  R. Marsh,et al.  Power output of scallop adductor muscle during contractions replicating the in vivo mechanical cycle. , 1994, The Journal of experimental biology.

[9]  R. Marsh,et al.  Properties enhancing aerobic capacity of calling muscles in gray tree frogs Hyla versicolor. , 1987, The American journal of physiology.

[10]  L C Rome,et al.  Muscle function during jumping in frogs. II. Mechanical properties of muscle: implications for system design. , 1996, The American journal of physiology.

[11]  Correlation between Relative Weights of Hindlimb Muscles and Locomotor Patterns in Japanese Anurans , 1978 .

[12]  N. Curtin,et al.  Energetic aspects of muscle contraction. , 1985, Monographs of the Physiological Society.

[13]  R. Marsh,et al.  Mechanical performance of scallop adductor muscle during swimming , 1992, Nature.

[14]  L C Rome,et al.  Muscle function during jumping in frogs. I. Sarcomere length change, EMG pattern, and jumping performance. , 1996, The American journal of physiology.

[15]  C. I. Smith,et al.  MYOTOMAL MUSCLE FUNCTION AT DIFFERENT LOCATIONS IN THE BODY OF A SWIMMING FISH , 1993 .

[16]  L. Rome,et al.  Jumping Performance of Frogs (Rana Pipiens) as a Function of Muscle Temperature , 1984 .

[17]  D. G. Dunlap.  The comparative myology of the pelvic appendage in the salientia , 1960, Journal of morphology.

[18]  L. Trueb,et al.  Biology of Amphibians , 1986 .

[19]  P. Lindblom,et al.  Contractile properties of two varieties of twitch muscle fibres in Xenopus laevis. , 1982, Acta physiologica Scandinavica.

[20]  A. F. Bennett,et al.  Histochemical, enzymatic, and contractile proper of skeletal muscles of three anuran amphibians. , 1983, The American journal of physiology.

[21]  J. Renaud,et al.  THE EXTENT OF SHORT-TERM AND LONG-TERM COMPENSATION TO TEMPERATURE SHOWN BY FROG AND TOAD SARTORIUS MUSCLE , 1984 .

[22]  R. Marsh,et al.  Thermal dependence of contractile properties of skeletal muscle from the lizard Sceloporus occidentalis with comments on methods for fitting and comparing force-velocity curves. , 1986, The Journal of experimental biology.

[23]  A. Rand.  Jumping Ability of Certain Anurans, with Notes on Endurance , 1952 .

[24]  L. Rome,et al.  Built for jumping: the design of the frog muscular system. , 1994, Science.

[25]  R. Marsh,et al.  Jumping performance of hylid frogs measured with high-speed cine film. , 1994, The Journal of experimental biology.

[26]  H. John-Alder,et al.  Thermal Physiology, Phenology, and Distribution of Tree Frogs , 1988, The American Naturalist.

[27]  R L Marsh,et al.  Jumping ability of anuran amphibians. , 1994, Advances in veterinary science and comparative medicine.

[28]  A V HILL.  The series elastic component of muscle. , 1950, Proceedings of the Royal Society of London. Series B, Biological sciences.

[29]  L C Rome,et al.  How fish power swimming. , 1993, Science.

[30]  H. Bennet-Clark,et al.  The energetics of the jump of the locust Schistocerca gregaria. , 1975, The Journal of experimental biology.