Chugey A. Sepulveda

Convergent evolution in mechanical design of lamnid sharks 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.

Swimming performance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae) I. Energetics.

SUMMARY A large swim tunnel respirometer was used to quantify the swimming energetics of the eastern Pacific bonito Sarda chiliensis (tribe Sardini) (45–50 cm fork length, FL) at speeds between 50 and 120 cm s-1 and at 18±2°C. The bonito rate of oxygen uptake (V̇O2)–speed function is U-shaped with a minimum V̇O2 at 60 cm s-1, an exponential increase in V̇O2 with increased speed, and an elevated increase in V̇O2 at 50 cm s-1 where bonito swimming is unstable. The onset of unstable swimming occurs at speeds predicted by calculation of the minimum speed for bonito hydrostatic equilibrium (1.2 FL s-1). The optimum swimming speed (Uopt) for the bonito at 18±2°C is approximately 70 cm s-1 (1.4 FL s-1) and the gross cost of transport at Uopt is 0.27 J N-1 m-1. The mean standard metabolic rate (SMR), determined by extrapolating swimming V̇O2 to zero speed, is 107±22 mg O2 kg-1 h-1. Plasma lactate determinations at different phases of the experiment showed that capture and handling increased anaerobic metabolism, but plasma lactate concentration returned to pre-experiment levels over the course of the swimming tests. When adjustments are made for differences in temperature, bonito net swimming costs are similar to those of similar-sized yellowfin tuna Thunnus albacares (tribe Thunnini), but the bonito has a significantly lower SMR. Because bonitos are the sister group to tunas, this finding suggests that the elevated SMR of the tunas is an autapomorphic trait of the Thunnini.

Gill morphometrics in relation to gas transfer and ram ventilation in high-energy demand teleosts: Scombrids and billfishes

This comparative study of the gill morphometrics in scombrids (tunas, bonitos, and mackerels) and billfishes (marlins, swordfish) examines features of gill design related to high rates of gas transfer and the high‐pressure branchial flow associated with fast, continuous swimming. Tunas have the largest relative gill surface areas of any fish group, and although the gill areas of non‐tuna scombrids and billfishes are smaller than those of tunas, they are also disproportionally larger than those of most other teleosts. The morphometric features contributing to the large gill surface areas of these high‐energy demand teleosts include: 1) a relative increase in the number and length of gill filaments that have, 2) a high lamellar frequency (i.e., the number of lamellae per length of filament), and 3) lamellae that are long and low in profile (height), which allows a greater number of filaments to be tightly packed into the branchial cavity. Augmentation of gill area through these morphometric changes represents a departure from the general mechanism of area enhancement utilized by most teleosts, which lengthen filaments and increase the size of the lamellae. The gill design of scombrids and billfishes reflects the combined requirements for ram ventilation and elevated energetic demands. The high lamellar frequencies and long lamellae increase branchial resistance to water flow which slows and streamlines the ram ventilatory stream. In general, scombrid and billfish gill surface areas correlate with metabolic requirements and this character may serve to predict the energetic demands of fish species for which direct measurement is not possible. The branching of the gill filaments documented for the swordfish in this study appears to increase its gill surface area above that of other billfishes and may allow it to penetrate oxygen‐poor waters at depth. J. Morphol. 2010.

Comparative studies of high performance swimming in sharks I. Red muscle morphometrics, vascularization and ultrastructure.

SUMMARY Tunas (family Scombridae) and sharks in the family Lamnidae are highly convergent for features commonly related to efficient and high-performance (i.e. sustained, aerobic) swimming. High-performance swimming by fishes requires adaptations augmenting the delivery, transfer and utilization of O2 by the red myotomal muscle (RM), which powers continuous swimming. Tuna swimming performance is enhanced by a unique anterior and centrally positioned RM (i.e. closer to the vertebral column) and by structural features (relatively small fiber diameter, high capillary density and greater myoglobin concentration) increasing O2 flux from RM capillaries to the mitochondria. A study of the structural and biochemical features of the mako shark (Isurus oxyrinchus) RM was undertaken to enable performance-capacity comparisons of tuna and lamnid RM. Similar to tunas, mako RM is positioned centrally and more anterior in the body. Another lamnid, the salmon shark (Lamna ditropis), also has this RM distribution, as does the closely related common thresher shark (Alopias vulpinus; family Alopiidae). However, in both the leopard shark (Triakis semifasciata) and the blue shark (Prionace glauca), RM occupies the position where it is typically found in most fishes; more posterior and along the lateral edge of the body. Comparisons among sharks in this study revealed no differences in the total RM quantity (approximately 2–3% of body mass) and, irrespective of position within the body, RM scaling is isometric in all species. Sharks thus have less RM than do tunas (4–13% of body mass). Relative to published data on other shark species, mako RM appears to have a higher capillary density, a greater capillary-to-fiber ratio and a higher myoglobin concentration. However, mako RM fiber size does not differ from that reported for other shark species and the total volume of mitochondria in mako RM is similar to that reported for other sharks and for tunas. Lamnid RM properties thus suggest a higher O2 flux capacity than in other sharks; however, lamnid RM aerobic capacity appears to be less than that of tuna RM.

Hematological indicators of stress in longline-captured sharks ☆

For many shark species, little information exists about the stress response to capture and release in commercial longline fisheries. Recent studies have used hematological profiling to assess the secondary stress response, but little is known about how, and to what degree, these indicators vary interspecifically. Moreover, there is little understanding of the extent to which the level of relative swimming activity (e.g., sluggish vs. active) or the general ecological classification (e.g., coastal vs. pelagic) correlates to the magnitude of the exercise-induced (capture-related) stress response. This study compared plasma electrolytes (Na(+), Cl(-), Mg(2+), Ca(2+), and K(+)), metabolites (glucose and lactate), blood hematocrit, and heat shock protein (Hsp70) levels between 11 species of longline-captured sharks (n=164). Statistical comparison of hematological parameters revealed species-specific differences in response to longline capture, as well as differences by ecological classification. Taken together, the blood properties of longline-captured sharks appear to be useful indicators of interspecific variation in the secondary stress response to capture, and may prove useful in the future for predicting survivorship of longline-captured sharks where new technologies (i.e., pop-up satellite tags) can verify post-release mortality.

Plasma catecholamine levels as indicators of the post-release survivorship of juvenile pelagic sharks caught on experimental drift longlines in the Southern California Bight

Between 1983 and 2004, nearly 12 000 shortfin mako (Isurus oxyrinchus), common thresher (Alopias vulpinus) and blue (Prionace glauca) sharks were tagged in the Southern California Bight; however, only 1.97% of these have been returned. One possible reason for this low return rate could be post-release mortality caused by capture stress from the experimental longline. Plasma catecholamine levels were analysed to evaluate stress levels in longline-captured, rod-and- reel-captured and unstressed docile sharks. The mean catecholamine values determined for the three tag-release species ranged from 6539 to 22 079 pg mL −1 . The level of adrenaline found in moribund I. oxyrinchus (94 807 pg mL −1 ) was much higher than in either P. glauca (46 845 pg mL −1 )o rA. vulpinus (36 890 pg mL −1 ). In contrast, blood obtained from sharks that were landed within minutes had lower catecholamine values (P. glauca, 889 and 1347 pg mL −1 ; I. oxyrinchus, 2960 and 3946 pg mL −1 , adrenaline and noradrenaline respectively). Among the nine I. oxyrinchus specimens that were recaptured long after their longline capture and release, the highest adrenaline level measured just before release was 33 352 pg mL −1 . Because these mako sharks survived sufficiently long to be recaptured, their time-of-release catecholamine levels provide a conservative estimate of ∼80% viability on the longline-captured and released population.

Diel movement patterns and habitat preferences of the common thresher shark (Alopias vulpinus) in the Southern California Bight

The common thresher shark, Alopias vulpinus, is the basis of the largest commercial shark fishery in California waters. We used acoustic telemetry to determine the diel movement patterns and habitat preferences of this species inthe Southern California Bight (SCB),where commercial fishing for the common thresher sharkis concentrated. Eightcommonthreshers (forklength: 122-203cm) weretaggedwith temperature anddepth-sensingacoustic transmitters and tracked for periods ranging from 22 to 49h. Tracked sharks preferentially utilized deep offshore waters, and avoided shallower waters over the continental shelf. Mean rate of movement (ROMs.d.) was 2.15 � 0.46kmh � 1 . ROM and angularconcentration(r,ameasureofrelativelinearity)bothshowedastrongdaytimepattern,withhighestvaluesatdawn that decreased throughout the day, whereas nocturnal ROM and r were less variable. Daytime vertical movements consisted of either vertical excursions below the thermocline or relatively level swimming within the upper portion of the thermocline. Nocturnally, all sharks remained within the mixed layer. These findings suggest that the common thresher shark is primarily a daytime predator, and have relevance for estimating how the alteration of the set depth of fishing-gear could affect catch rates of this species in the SCB.

Patterns of red muscle strain/activation and body kinematics during steady swimming in a lamnid shark, the shortfin mako (Isurus oxyrinchus).

SUMMARY 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 (∼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 (∼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° (90° is peak length) and offset at 200–210° 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 ∼10% of the tailbeat cycle, with one individual as high as ∼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 red muscle morphology of the thresher sharks (family Alopiidae)

SUMMARY A more medial and anterior position of the red aerobic myotomal muscle (RM) and the presence of a vascular counter-current heat exchange system provide the functional elements that facilitate regional RM endothermy in tunas, lamnid sharks and the common thresher shark (Alopias vulpinus). The convergent RM morphology among all species capable of RM endothermy suggests that RM position is a strong predictor of fish endothermic capacity. The present study investigated the comparative RM morphology of the other two thresher shark species (bigeye thresher, Alopias superciliosus, and the pelagic thresher, Alopias pelagicus), for which there is no information regarding their capacity for RM endothermy, and compared these data with published works on A. vulpinus. The digitization of transverse sections along the body of A. superciliosus and A. pelagicus enabled quantification of the relative amount of RM and the position and placement of the RM along the body. The RM in both A. superciliosus and A. pelagicus is positioned subcutaneously, along the lateral edges of the myotomes, and is distributed relatively evenly over the trunk of the body. The position of maximum RM area is at 50% fork length (FL) for A. superciliosus and at 75% FL for A. pelagicus. The amount of RM (mean ± s.e.m.) is 2.31±0.11% and 3.01±0.10% in A. superciliosus and A. pelagicus, respectively. When compared with A. vulpinus, all three alopiid sharks have a similar amount of RM. However, A. superciliosus and A. pelagicus differ from A. vulpinus in that they do not possess the medial and anterior RM arrangement that would likely facilitate metabolic heat conservation (RM endothermy).

Evidence for Temperature Elevation in the Aerobic Swimming Musculature of the Common Thresher Shark, Alopias vulpinus

Abstract This paper reports on the in vivo temperature measurements for slow-twitch, red aerobic muscle (RM) and fast twitch, white muscle (WM) of 24 Common Thresher Sharks, Alopias vulpinus, captured off the coast of Southern California. Mean (± SE) RM temperature elevation was 2.33 ± 0.30 C warmer than the ambient sea surface temperature (SST, 19.13 ± 0.22 C) and 2.25 ± 0.35 C warmer than the coldest WM temperature measured (19.23 ± 0.30 C). The maximum RM temperature elevation was 5.4 C above SST and up to 7.6 C above the WM. Nine Common Thresher Sharks exhibited RM temperatures that exceeded 3.0 C above SST. No significant relationship was found between fish total length and RM temperature elevation. Although there was individual variability in RM temperature elevation, this study documents that the Common Thresher Shark is capable of significantly elevating its RM temperature above that of the ambient conditions.