Mechanics of steady swimming and contractile properties of muscle in elasmobranch fishes

The steady swimming muscle dynamics and the contractile properties of the red aerobic locomotor muscle (RM) were investigated in two elasmobranch fishes, the leopard shark (Triakis semifasciata, Family Triakidae) and the shortfin mako shark (Isurus oxyrinchus, Family Lamnidae). To understand the degree of divergence in dynamic muscle function between sharks and bony fishes, patterns of RM strain and activation and aspects of the dorsal midline kinematics during steady cruise swimming were examined in both sharks and compared to similar observations in teleosts. Unlike most bony fishes, the leopard shark lacked variation in the relative timing of RM activation along the body. Although the mako shark differs from the leopard shark in many aspects of its morphology, physiology, and swimming mode, its relative timing of RM activation was also consistent from anterior to posterior. Thus, the lack of longitudinal variation in patterns of RM activation appears to be a fundamental difference between bony and cartilaginous fishes. To determine the degree to which two groups of high-performance endothermic fishes, the lamnid sharks and tunas, have converged in functional mechanical design, aspects of the kinematics, morphology, and muscle dynamics were investigated in the mako shark. Comparison of patterns of lateral displacement along the body as well as the relationship between the timing of shortening in red and white muscle during swimming between the mako shark and tunas revealed that these two groups are kinematically similar and share a comparable stiff bodied (thunniform) swimming mode. As in tunas, lamnid sharks have the least lateral motion in the mid-body region where the bulk of RM resides and have a reduced body mass in the caudal region where lateral amplitudes are high. Internal RM position and extremely elongated and robust tendons facilitate the physical uncoupling of shortening in the RM and local body curvature. In both groups, RM shortens causing bending at a more posterior body region. The hypaxial lateral tendon in the mako was found to be responsible for the transfer of force from the anterior to the posterior. To further characterize the degree of divergence in RM function between ecto- and endothermic sharks, the effects of axial position and temperature on RM contractile properties were compared in the leopard and mako sharks. Verifying longitudinal patterns of RM activation observed in vivo, there was no difference in the contractile properties along the body in either species. However, the effect of temperature on optimal cycle frequencies for power output differed in the leopard and mako sharks. Optimal frequencies remained relatively constant in the leopard shark but increased with temperature in the mako, and at temperatures which reflect those normally experienced in the mako the optimal cycle frequency is nearly double that of the leopard shark. This study illustrates that bony and cartilaginous fishes have diverged in certain fundamental aspects of the mechanics of locomotion, and that these two distantly related groups of fishes also display a remarkable degree of convergence in mechanical design, as exemplified in the lamnid sharks and tunas.