Resolving Shifting Patterns of Muscle Energy Use in Swimming Fish

Abstract

Muscle metabolism dominates the energy costs of locomotion. Although in vivo measures of muscle strain, activity and force can indicate mechanical function, similar muscle-level measures of energy use are challenging to obtain. Without this information locomotor systems are essentially a black box in terms of the distribution of metabolic energy. Although in situ measurements of muscle metabolism are not practical in multiple muscles, the rate of blood flow to skeletal muscle tissue can be used as a proxy for aerobic metabolism, allowing the cost of particular muscle functions to be estimated. Axial, undulatory swimming is one of the most common modes of vertebrate locomotion. In fish, segmented myotomal muscles are the primary power source, driving undulations of the body axis that transfer momentum to the water. Multiple fins and the associated fin muscles also contribute to thrust production, and stabilization and control of the swimming trajectory. We have used blood flow tracers in swimming rainbow trout (Oncorhynchus mykiss) to estimate the regional distribution of energy use across the myotomal and fin muscle groups to reveal the functional distribution of metabolic energy use within a swimming animal for the first time. Energy use by the myotomal muscle increased with speed to meet thrust requirements, particularly in posterior myotomes where muscle power outputs are greatest. At low speeds, there was high fin muscle energy use, consistent with active stability control. As speed increased, and fins were adducted, overall fin muscle energy use declined, except in the caudal fin muscles where active fin stiffening is required to maintain power transfer to the wake. The present data were obtained under steady-state conditions which rarely apply in natural, physical environments. This approach also has potential to reveal the mechanical factors that underlie changes in locomotor cost associated with movement through unsteady flow regimes.

Field swimming performance of bluegill sunfish, Lepomis macrochirus: implications for field activity cost estimates and laboratory measures of swimming performance

“…The costs of locomotion can also dominate daily energy budgets (Boisclair & Sirois, ; Irschick & Garland, ; Kerr, ). These costs are primarily associated with the muscle activity needed to generate propulsive forces or maintain stability (Gerry & Ellerby, ; Marsh & Ellerby, ). The majority of the available data concerning mechanical performance and energy cost during locomotion were obtained under quasi steady‐state conditions with linear motion and repeated, regular propulsive cycles (Brett, ; Hoyt & Taylor, ; Tucker, ).…”

Convergent evolution of locomotor morphology but not performance in gymnotiform swimmers

“…In a recent study on the little skate, where correction factors similar to those of the current study were applied, the MO 2 data are comparable to those presented here (Di Santo, ; Di Santo & Kenaley, ). In addition, during preliminary analyses, the present data were analysed using a scaling factor of 1 (results not presented), which yielded oxygen consumption results of similar scale to those seen in banded knifefish (McKenzie, Steffensen, Taylor, & Abe, ) and rainbow trout (Gerry & Ellerby, ).…”

“…While fish morphology and swimming performance are each independently well studied (Claverie & Wainwright, 2014;Collar, Quintero, Buttler, Ward, & Mehta, 2016;Dornburg et al, 2011;Oufiero & Whitlow, 2016;Sfakiotakis et al, 1999), the two approaches are rarely combined in a comparative context. In addition, the performance of fish with a gymnotiform gait is relatively poorly understood, with most locomotor research focusing on BCF (Gerry & Ellerby, 2014;Sepulveda & Dickson, 2000;Webb, 1982) and pectoral fin swimmers (Fulton, Johansen, & Steffensen, 2013;Lauder, 2015;Walker & Westneat, 2002). With this study, we aim to test the hypotheses that: (a) Gymnotiform swimmers demonstrate morphological convergence and (b) burst swimming performance and steady-swimming energetic costs shift in correspondence with evolution of the gymnotiform gait.…”

Male sexually coercive behaviour drives increased swimming efficiency in female guppies

“…Our results suggest that the presence of male harassment within a guppy population can alter the degree of variation in swimming mechanics present among females, thus decreasing their costs of locomotion. The actual energetic cost of pectoral fin movements during subcarangiform swimming is relatively small (Gerry & Ellerby ), but the pectoral fins are used to stabilize the fish during forward movement, and excessive fin movement is probably a general indicator of suboptimal and apparently inefficient swimming mechanics (Svendsen et al . ).…”