Thermal effects on red muscle contractile performance in deep-diving, large-bodied fishes.

Bigeye thresher sharks (Alopias superciliosus) and swordfish (Xiphias gladius) are large, pelagic fishes, which make long-duration, diurnal foraging dives from warm, surface waters (18-24 °C) to cold waters beneath the thermocline (5-10 °C). In bigeye thresher sharks, the subcutaneous position of the red, aerobic swimming muscles (RM) suggests that RM temperature mirrors ambient during dives (i.e., ectothermy). In swordfish, the RM is closer to the vertebrae and its associated with vascular counter-current heat exchangers that maintain RM temperature above ambient (i.e., RM endothermy). Here, we sought to determine how exposure to a wide range of ambient temperatures (8, 16, 24 °C) impacted peak power output and optimum cycle (i.e., tailbeat) frequency (0.25, 0.5, 1 Hz) in RM isolated from both species. Bigeye thresher shark RM did not produce substantial power at high cycle frequencies, even at high temperatures; but it did produce relatively high power at slow cycle frequencies regardless of temperature. Swordfish RM produced more power when operating at a combination of fast cycle frequencies and higher temperatures. This suggests that swordfish RM benefits considerably more from warming than bigeye thresher shark RM, while the RM of both species was able to produce power at cold temperatures and slow cycle frequencies. Despite different thermal strategies (i.e., ectothermy vs. RM endothermy), the ability of the RM to power sustained swimming during foraging-related search behaviors may contribute to the unique ability of these fishes to successfully exploit food resources in deep, cold water.

Effects of temperature on power output and contraction kinetics in the locomotor muscle of the regionally endothermic common thresher shark (Alopias vulpinus).

The common thresher shark (Alopias vulpinus) is a pelagic species with medially positioned red aerobic swimming musculature (RM) and regional RM endothermy. This study tested whether the contractile characteristics of the RM are functionally similar along the length of the body and assessed how the contractile properties of the common thresher shark compare with those of other sharks. Contractile properties of the RM were examined at 8, 16 and 24 °C from anterior and posterior axial positions (0.4 and 0.6 fork length, respectively) using the work loop technique. Experiments were performed to determine whether the contractile properties of the RM are similar along the body of the common thresher shark and to document the effects of temperature on muscle power. Axial differences in contractile properties of RM were found to be small or absent. Isometric twitch kinetics of RM were ~fivefold slower than those of white muscle, with RM twitch durations of about 1 s at 24 °C and exceeding 5 s at 8 °C, a Q(10) of nearly 2.5. Power increased approximately tenfold with the 16 °C increase in temperature, while the cycle frequency for maximal power only increased from about 0.5-1.0 Hz over this temperature range. These data support the hypothesis that the RM is functionally similar along the body of the common thresher shark and corroborate previous findings from shark species both with and without medial RM. While twitch kinetics suggest the endothermic RM is not unusually temperature sensitive, measures of power suggest that the RM is not well suited to function at cool temperatures. The cycle frequency at which power is maximized appeared relatively insensitive to temperature in RM, which may reflect the relatively cooler temperature of the thresher RM compared to that observed in lamnid sharks as well as the relatively slow RM phenotype in these large fish.

Function of the medial red muscle during sustained swimming in common thresher sharks: contrast and convergence with thunniform swimmers.

Through convergent evolution tunas and lamnid sharks share thunniform swimming and a medial position of the red, aerobic swimming musculature. During continuous cruise swimming these muscles move uniformly out of phase with local body curvature and the surrounding white muscle tissue. This design results in thrust production primarily from the caudal fin rather than causing whole-body undulations. The common thresher shark (Family Alopiidae) is the only other fish known to share the same medial red muscle anatomy as the thunniform swimmers. However, the overall body shape and extremely heterocercal caudal fin of the common thresher is not shared with the thunniform swimmers, which have both fusiform bodies and high aspect-ratio, lunate caudal fins. Our study used sonomicrometry to measure the dynamics of red and white muscle movement in common thresher sharks swimming in the ocean to test whether the medial position of red muscle is associated with uncoupling of muscle shortening and local body bending as characteristic of thunniform swimmers. Common threshers ( approximately 60-100kg) instrumented with sonomicrometric and electromyographic (EMG) leads swam alongside of the vessel with a tail-beat frequency of approximately 0.5Hz. EMG signals confirmed that only the red muscle was active during sustained swimming. Despite the more medial position of the red muscle relative to the white muscle, its strain was approximately 1.5-times greater than that of the overlying white muscle, and there was a notable phase shift between strain trajectories in the red muscle and adjacent white muscle. These results suggest an uncoupling (shearing) of the red muscle from the adjacent white muscle. Although the magnitude of the phase shift between red and white muscle strain was relatively constant within individuals, it varied among sharks, ranging from near zero (red and white in phase) to almost 180 degrees out of phase. This extent in variability has not been documented previously for thunniform swimmers with a medial red muscle position and may be a characteristic of the thresher's unique body and caudal fin morphology. Nonetheless, the uncoupling of red and white muscle strain remains a consistent character associated with fishes having a medially positioned red muscle.

Structural adaptations for ram ventilation: gill fusions in scombrids and billfishes.

For ram-gill ventilators such as tunas and mackerels (family Scombridae) and billfishes (families Istiophoridae, Xiphiidae), fusions binding the gill lamellae and filaments prevent gill deformation by a fast and continuous ventilatory stream. This study examines the gills from 28 scombrid and seven billfish species in order to determine how factors such as body size, swimming speed, and the degree of dependence upon ram ventilation influence the site of occurrence and type of fusions. In the family Scombridae there is a progressive increase in the reliance on ram ventilation that correlates with the elaboration of gill fusions. This ranges from mackerels (tribe Scombrini), which only utilize ram ventilation at fast cruising speeds and lack gill fusions, to tunas (tribe Thunnini) of the genus Thunnus, which are obligate ram ventilators and have two distinct fusion types (one binding the gill lamellae and a second connecting the gill filaments). The billfishes appear to have independently evolved gill fusions that rival those of tunas in terms of structural complexity. Examination of a wide range of body sizes for some scombrids and billfishes shows that gill fusions begin to develop at lengths as small as 2.0 cm fork length. In addition to securing the spatial configuration of the gill sieve, gill fusions also appear to increase branchial resistance to slow the high-speed current produced by ram ventilation to distribute flow evenly and optimally to the respiratory exchange surfaces.

Archival tagging of subadult and adult common thresher sharks (Alopias vulpinus) off the coast of southern California.

The common thresher shark (Alopias vulpinus) is a secondary target species of the California drift gillnet fishery (CA-DGN) and supports a growing recreational fishery in California waters. This study used archival tags to examine the movement patterns and habitat preferences of common threshers of the size range captured in the CA-DGN (>120 cm fork length). Depth and temperature-logging archival tags were deployed on 57 subadult and adult common threshers in the Southern California Bight. Tags from five individuals (8.8%) were recovered, and 154 days of data were successfully obtained from four of these. By night, shark movements were primarily limited to waters above the thermocline, which ranged in depth from 15 to 20 m. Sharks were significantly deeper by day, and daytime vertical distribution consisted of two distinct modes: a 'shallow mode' (wherein sharks occupied only the upper 20 m of the water column) and a 'deep mode' (characterized by frequent vertical excursions below the thermocline). This modal switch is interpreted as relating to regional differences in abundance of surface-oriented prey and prey in deeper water. Maximum dive depth was 320 m, greatest dive duration was 712 min, minimum temperature experienced during a dive was 9.1°C, and dive descent rate was significantly greater than ascent rate. Sharks inhabited waters corresponding to a sea surface temperature range of 16 to 21°C. The nocturnal depth distribution of common threshers has implications for management of drift gillnet deployment depths in the CA-DGN.