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We conducted in vitro inflations of freshly excised ventral aortas of the Greenland shark, Somniosus microcephalus , and used pressure-diameter data to estimate the point of transition from high to low compliance, which has been shown to occur at the mean blood pressure in other vertebrates including fishes. We also determined the pressure at which the modulus of elasticity of the aorta reached 0.4 MPa, as occurs at the compliance transition in other species. From these analyses, we predict the average ventral aortic blood pressure in S. microcephalus to be about 2.3-2.8 kPa, much lower than reported for other sharks. Our results support the idea that this species is slow moving and has a relatively low aerobic metabolism. Histological investigation of the ventral aorta shows that elastic fibres are present in relatively low abundance and loosely connected, consistent with this aorta having high compliance at a relatively low blood pressure., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

The locomotor system in sharks has been investigated for many decades, starting with the earliest kinematic studies by Sir James Gray in the 1930s. Early work on axial muscle anatomy also included sharks, and the first demonstration of the functional significance of red and white muscle fibre types was made on spinal preparations in sharks. Nevertheless, studies on teleosts dominate the literature on fish swimming. The purpose of this article is to review the current knowledge of muscle function and swimming in sharks, by considering their morphological features related to swimming, the anatomy and physiology of the axial musculature, kinematics and muscle dynamics, and special features of warm-bodied lamnids. In addition, new data are presented on muscle activation in fast-starts. Finally, recent developments in tracking technology that provide insights into shark swimming performance in their natural environment are highlighted., (© 2012 The Authors. Journal of Fish Biology © 2012 The Fisheries Society of the British Isles.)

Fishes with internalized and endothermic red muscles (i.e. tunas and lamnid sharks) are known for a stiff-bodied form of undulatory swimming, based on unique muscle-tendon architecture that limits lateral undulation to the tail region even though the red muscle is shifted anteriorly. A strong convergence between lamnid sharks and tunas in these features suggests that thunniform swimming might be evolutionarily tied to this specialization of red muscle, but recent observations on the common thresher shark (Alopias vulpinus) do not support this view. Here, we review the fundamental features of the locomotor systems in lamnids and tunas, and present data on in vivo muscle function and swimming mechanics in thresher sharks. These results suggest that the presence of endothermic and internalized red muscles alone in a fish does not predict or constrain the swimming mode to be thunniform and, indeed, that the benefits of this type of muscle may vary greatly as a consequence of body size.

The work loop technique was used to examine contractile properties of the red aerobic locomotor muscle (RM) in the ectothermic leopard shark Triakis semifasciata and endothermic shortfin mako shark Isurus oxyrinchus. The effects of axial position and temperature on the twitch kinetics, and the stimulus duration and phase producing maximum net positive work and power output were investigated. Contractile performance was measured over the temperature range of 15 to 25 degrees C for Triakis and 15 to 28 degrees C for Isurus at cycle frequencies (analogous to tailbeat frequencies) ranging from 0.25 to 3 Hz using muscle bundles isolated from anterior (0.4 L where L is total body length) and posterior (0.6-0.65 L) axial positions. Pairwise comparisons of twitch times for anterior and posterior muscle samples indicated that there were no significant differences related to body position, except in mako sharks at unphysiologically cool temperatures (<20 degrees C). We found no significant differences in optimal stimulus duration, phase, net work or power output between anterior and posterior bundles in each species. With increasing cycle frequency the stimulus duration yielding maximum power decreased while optimal phase occurred earlier. The cycle frequency at which peak power was generated in leopard shark RM was only affected slightly by temperature, increasing from about 0.6 to 1.0 Hz between 15 and 25 degrees C. In contrast, mako RM showed a much more dramatic temperature sensitivity, with the peak power frequency rising from <0.25 to 2.25 Hz between 15 and 28 degrees C. These data support the hypothesis that the contractile properties of RM are functionally similar along the body in both species. In addition, our data identify a significant difference in the effect of temperature on net work and power output between these two shark species; at 15 degrees C muscle from the ectothermic leopard shark performs relatively well in comparison with mako, while at higher temperatures, which reflect those normally experienced by the mako, the optimal cycle frequency for power is nearly double that of the leopard shark, suggesting that the mako may be able to maintain greater aerobic swimming speeds.

In contrast to all other sharks, lamnid sharks perform a specialized fast and continuous "thunniform" type of locomotion, more similar to that of tunas than to any other known shark or bony fish. Within sharks, it has evolved from a subcarangiform mode. Experimental data show that the two swimming modes in sharks differ remarkably in kinematic patterns as well as in muscle activation patterns, but the morphology of the underlying musculotendinous system (red muscles and myosepta) that drives continuous locomotion remains largely unknown. The goal of this study was to identify differences in the musculotendinous system of the two swimming types and to evaluate these differences in an evolutionary context. Three subcarangiform sharks (the velvet belly lantern shark, Etmopterus spinax, the smallspotted catshark, Scyliorhinus canicula, and the blackmouth catshark, Galeus melanostomus) from the two major clades (two galeans, one squalean) and one lamnid shark, the shortfin mako, Isurus oxyrhinchus, were compared with respect to 1) the 3D shape of myomeres and myosepta of different body positions; 2) the tendinous architecture (collagenous fiber pathways) of myosepta from different body positions; and 3) the association of red muscles with myoseptal tendons. Results show that the three subcarangiform sharks are morphologically similar but differ remarkably from the lamnid condition. Moreover, the "subcarangiform" morphology is similar to the condition known from teleostomes. Thus, major features of the "subcarangiform" condition in sharks have evolved early in gnathostome history: Myosepta have one main anterior-pointing cone and two posterior-pointing cones that project into the musculature. Within a single myoseptum cones are connected by longitudinally oriented tendons (the hypaxial and epaxial lateral and myorhabdoid tendons). Mediolaterally oriented tendons (epineural and epipleural tendons; mediolateral fibers) connect vertebral axis and skin. An individual lateral tendon spans only a short distance along the body (a fraction between 0.05 and 0.075 of total length, L, of the shark). This span is similar in all tendons along the body. Red muscles insert into the midregion of the lateral tendons. The shortfin mako differs substantially from this condition in several respects: Red muscles are internalized and separated from white muscles by a sheath of lubricative connective tissue. They insert into the anterior part of the hypaxial lateral tendon. Rostrocaudally, this tendon becomes very distinct and its span increases threefold (0.06L anteriorly to 0.19L posteriorly). Mediolateral fibers do not form distinct epineural/epipleural tendons in the mako. Since our morphological findings are in good accordance with experimental data it seems likely that the thunniform swimming mode has evolved along with the described morphological specializations.

Effects of temperature on muscle contraction and powering movement are profound, outwardly obvious, and of great consequence to survival. To cope with the effects of environmental temperature fluctuations, endothermic birds and mammals maintain a relatively warm and constant body temperature, whereas most fishes and other vertebrates are ectothermic and conform to their thermal niche, compromising performance at colder temperatures. However, within the fishes the tunas and lamnid sharks deviate from the ectothermic strategy, maintaining elevated core body temperatures that presumably confer physiological advantages for their roles as fast and continuously swimming pelagic predators. Here we show that the salmon shark, a lamnid inhabiting cold, north Pacific waters, has become so specialized for endothermy that its red, aerobic, locomotor muscles, which power continuous swimming, seem mammal-like, functioning only within a markedly elevated temperature range (20-30 degrees C). These muscles are ineffectual if exposed to the cool water temperatures, and when warmed even 10 degrees C above ambient they still produce only 25-50% of the power produced at 26 degrees C. In contrast, the white muscles, powering burst swimming, do not show such a marked thermal dependence and work well across a wide range of temperatures.

The dynamics of steady swimming were examined in the shortfin mako (Isurus oxyrinchus), a member of the cartilaginous fish family Lamnidae, a family known for their morphological adaptations for high-performance locomotion and their similarity in hydromechanical design to tunas. Patterns of red muscle (RM) strain (i.e. relative length change) and activation were quantified at two axial positions ( approximately 0.4 and 0.6L, where L is total body length), using sonomicrometry and electromyography (EMG), and correlated with simultaneous measurements of dorsal midline kinematics during steady swimming ( approximately 0.5-1 L s(-1)). RM strain varied longitudinally with strain amplitudes ranging from 5.5+/-1.1% (s.e.m.) in the anterior to 8.7+/-0.9% in the posterior. We found no significant longitudinal variation in patterns of RM activation, with mean onset of activation occurring at 83-84 degrees (90 degrees is peak length) and offset at 200-210 degrees at both body positions. Likewise, duty cycles were similar: 35.5+/-1.0% in the anterior and 32.2+/-1.6% in the posterior. Comparison of the timing of waves of dorsal midline curvature and predicted strain relative to measured RM strain revealed a phase shift between RM shortening and local body bending. Furthermore, when the body is bent passively, RM shortens synchronously with the surrounding white muscle (WM) and skin, as expected. During active swimming, peaks in RM strain were delayed relative to peaks in WM strain by a mean of approximately 10% of the tailbeat cycle, with one individual as high as approximately 17% in the anterior and nearly 50% in the posterior. The longitudinal consistency in the EMG/strain phase relationship in the mako is similar to that in the leopard shark, suggesting a consistent trend among sharks using different locomotor modes. However, unlike in the leopard shark, RM shortening in the mako is physically uncoupled from deformation of the surrounding body during steady swimming, a characteristic shared between the mako and tunas.

The evolution of 'thunniform' body shapes in several different groups of vertebrates, including whales, ichthyosaurs and several species of large pelagic fishes supports the view that physical and hydromechanical demands provided important selection pressures to optimize body design for locomotion during vertebrate evolution. Recognition of morphological similarities between lamnid sharks (the most well known being the great white and the mako) and tunas has led to a general expectation that they also have converged in their functional design; however, no quantitative data exist on the mechanical performance of the locomotor system in lamnid sharks. Here we examine the swimming kinematics, in vivo muscle dynamics and functional morphology of the force-transmission system in a lamnid shark, and show that the evolutionary convergence in body shape and mechanical design between the distantly related lamnids and tunas is much more than skin deep; it extends to the depths of the myotendinous architecture and the mechanical basis for propulsive movements. We demonstrate that not only have lamnids and tunas converged to a much greater extent than previously known, but they have also developed morphological and functional adaptations in their locomotor systems that are unlike virtually all other fishes.

Patterns of red muscle strain and activation were examined at three positions along the body (0.42, 0.61 and 0.72 L, where L is total body length) and correlated with simultaneous measurements of midline kinematics during steady swimming (approx. 1.0 L s(-1)) in the leopard shark Triakis semifasciata. Analysis of lateral displacement along the body indicates that the leopard shark is a subcarangiform swimmer. Longitudinal variation in red muscle strain was observed with strain amplitudes ranging from +/-3.9% in the anterior, +/-6.6% in the mid, to +/-4.8% in the posterior body position. Strain was in-phase with local midline curvature. In addition, strain amplitude calculated from a bending beam model closely matched strain measured using sonomicrometry at all three body positions. There is a high degree of similarity in red muscle activation patterns along the body between the leopard shark and many fish species, in that the onset of activation occurs during muscle lengthening while offset occurs during muscle shortening. However, we found no significant longitudinal variation in the EMG/strain phase relationship and duty cycles, with onset of muscle activation occurring at 51.4-61.8 degrees and offset at 159.7-165.2 degrees (90 degrees is peak length). This consistent pattern of activation suggests that red muscle along the entire length of the body contributes to positive power production. Thus, sharks such as Triakis may have no regional specialization in red muscle function like that seen in many teleosts, which may indicate that the evolution of differential muscle function along the body occurred after the divergence of cartilaginous and bony fishes.

Elasmobranchs and bony fishes have evolved independently for more than 400 million years. However, two Recent groups, the lamnid sharks (Family Lamnidae) and tunas (Family Scombridae), display remarkable similarities in features related to swimming performance. Traits separating these two groups from other fishes include a higher degree of body streamlining, a shift in the position of the aerobic, red, locomotor muscle that powers sustained swimming to a more anterior location in the body and nearer to the vertebral column, the capacity to conserve metabolic heat (i.e. regional endothermy), an increased gill surface area with a decreased blood-water barrier thickness, a higher maximum blood oxygen carrying capacity, and greater muscle aerobic and anaerobic enzyme activities at in vivo temperatures. The suite of morphological, physiological, and biochemical specializations that define "high-performance fishes" have been extensively characterized in the tunas. This review examines the convergent features of lamnid sharks and tunas in order to gain insight into the extent that comparable environmental selection pressures have led to the independent origin of similar suites of functional characteristics in these two distinctly different taxa. We propose that, despite differences between teleost and elasmobranch fishes, lamnid sharks and tunas have evolved morphological and physiological specializations that enhance their swimming performance relative to other sharks and most other high performance pelagic fishes.