Biomechanical Analysis of the Slow-Twitch (Red) Muscle Force Transmission Pathways in Tunas

In tunas, the slow-twitch red muscle, which has an elevated temperature, powers thunniform locomotion, a stiff-bodied swimming style. The anatomical placement and operating temperatures of red muscle vary widely among teleosts: in tunas, the red muscle is located centrally in the body, adjacent to the spine, and maintains an elevated temperature. In the majority of ectothermic teleosts, red muscle is located laterally in the body, adjacent to the skin, and operates at ambient temperature. The specialized physiology and biomechanics of red muscle in tunas are often considered important adaptations to their high-performance pelagic lifestyle; however, the mechanics of how muscular work is transmitted to the tail remains largely unknown. The red muscle has a highly pennate architecture and is connected to the spine through a network of bones (epicentral bones) and long tendons (posterior oblique tendons). The network of long tendons has been hypothesized to enhance the power transmitted to the tail. Here, we investigate the morphology and biomechanics of the tuna's red muscle and tendons to determine whether elasticity is exploited to reduce the cost of transport, as is the case in many terrestrial vertebrates. To address this question, we evaluate two hypotheses: (1) tendons stretch during red-muscle-actuated swimming and (2) tendons comprise the primary load transmission pathway from the red muscle to the spine. To evaluate these hypotheses, we measured the mechanical properties of the posterior oblique tendons and performed novel dissections to estimate the peak force that the red muscle can generate. The force-generating capacity of the red muscle is calculated to be much greater than the load-bearing capacity of the posterior oblique tendons. Thus, the long tendons likely stretch under force from the red muscle, but they are not strong enough to be the primary force transmission pathway. These results suggest that other pathways, such as serial load transmission through the red muscle myomeres to the great lateral tendon and/or the anterior oblique tendons to the skin, transmit appreciable force to the tail.