Growing out of the fins: Implications of isometric and allometric scaling of morphology relative to increasing mass in blue sharks (Prionace glauca).

Disproportional changes (i.e. allometry) in shark morphology relative to increasing body size have been attributed to shifts in function associated with niche shifts in life history, such as in habitat and diet. Photographs of blue sharks (Prionace glauca, 26-145 kg) were used to analyze changes in parameters of body and fin morphology with increasing mass that are fundamental to swimming and feeding. We hypothesized that blue sharks would demonstrate proportional changes (i.e. isometry) in morphology with increasing mass because they do not undergo profound changes in prey and habitat type; accordingly, due to geometric scaling laws, we predicted that blue sharks would grow into bodies with greater turning inertias and smaller frontal and surface areas, in addition to smaller spans and areas of the fins relative to mass, which are parameters that are associated with the swimming performance in sharks. Many aspects of morphology increased with isometry. However, blue sharks demonstrated negative allometry in body density, whereas surface area, volume and roll inertia of the body, area, span and aspect ratio of both dorsal fins, span and aspect ratio of the ventral caudal fin, and span, length and area of the mouth increased with positive allometry. The dataset was divided in half based on mass to form two groups: smaller and larger sharks. Besides area of both dorsal fins, relative to mass, larger sharks had bodies with significantly greater turning inertia and smaller frontal and surface areas, in addition to fins with smaller spans and areas, compared to smaller sharks. In conclusion, isometric scaling does not necessarily imply functional similarity, and allometric scaling may sometimes be critical in maintaining, rather than shifting, function relative to mass in animals that swim through the water column.

Can temperature-dependent changes in myocardial contractility explain why fish only increase heart rate when exposed to acute warming?

Fish increase heart rate (fH), not stroke volume (VS), when acutely warmed as a way to increase cardiac output (Q). To assess whether aspects of myocardial function may have some basis in determining temperature-dependent cardiac performance, we measured work and power (shortening, lengthening and net) in isolated segments of steelhead trout (Oncorhynchus mykiss) ventricular muscle at the fish's acclimation temperature (14°C), and at 22°C, when subjected to increased rates of contraction (30-105 min-1, emulating increased fH) and strain amplitude (8-14%, mimicking increased VS). At 22°C, shortening power (indicative of Q) increased in proportion to fH, and the work required to re-lengthen (stretch) the myocardium (fill the heart) was largely independent of fH. In contrast, the increase in shortening power was less than proportional when strain was augmented, and lengthening work approximately doubled when strain was increased. Thus, the derived relationships between fH, strain and myocardial shortening power and lengthening work, suggest that increasing fH would be preferable as a mechanism to increase Q at high temperatures, or in fact may be an unavoidable response given constraints on muscle mechanics as temperatures rise. Interestingly, at 14°C, lengthening work increased substantially at higher fH, and the duration of lengthening (i.e. diastole) became severely constrained when fH was increased. These data suggest that myocardial contraction/twitch kinetics greatly constrain maximal fH at cool temperatures, and may underlie observations that fish elevate VS to an equal or greater extent than fH to meet demands for increased Q at lower temperatures.

Temperature effects on the contractile performance and efficiency of oxidative muscle from a eurythermal versus a stenothermal salmonid.

We compared the thermal sensitivity of oxidative muscle function between the eurythermal Atlantic salmon (Salmo salar) and the more stenothermal Arctic char (Salvelinus alpinus; which prefers cooler waters). Power output was measured in red skeletal muscle strips and myocardial trabeculae, and efficiency (net work/energy consumed) was measured for trabeculae, from cold (6°C) and warm (15°C) acclimated fish at temperatures from 2 to 26°C. The mass-specific net power produced by char red muscle was greater than in salmon, by 2-to 5-fold depending on test temperature. Net power first increased, then decreased, when the red muscle of 6°C-acclimated char was exposed to increasing temperature. Acclimation to 15°C significantly impaired mass-specific power in char (by ∼40-50%) from 2 to 15°C, but lessened its relative decrease between 15 and 26°C. In contrast, maximal net power increased, and then plateaued, with increasing temperature in salmon from both acclimation groups. Increasing test temperature resulted in a ∼3- to 5-fold increase in maximal net power produced by ventricular trabeculae in all groups, and this effect was not influenced by acclimation temperature. Nonetheless, lengthening power was higher in trabeculae from warm-acclimated char, and char trabeculae could not contract as fast as those from salmon. Finally, the efficiency of myocardial net work was approximately 2-fold greater in 15°C-acclimated salmon than char (∼15 versus 7%), and highest at 20°C in salmon. This study provides several mechanistic explanations as to their inter-specific difference in upper thermal tolerance, and potentially why southern char populations are being negatively impacted by climate change.

The ocellate river stingray (Potamotrygon motoro) exploits vortices of sediment to bury into the substrate.

Particle image velocimetry and video analysis were employed to determine the pectoral-fin mechanism used by the stingray Potamotrygon motoro to bury into sand. Rapid oscillations of the body and folding motions of the posterior portion of the pectoral fin suspended sediment beneath the pectoral disc and directed vortices of sediment onto the dorsal surface, where they dissipated and the sediment settled. Body coverage was increased by increased fin displacement and speed and also by the occasional collision of vortices that redirected sediment flow towards the head and tail.

Effects of hypoxic acclimation, muscle strain, and contraction frequency on nitric oxide-mediated myocardial performance in steelhead trout (Oncorhynchus mykiss).

Whether hypoxic acclimation influences nitric oxide (NO)-mediated control of fish cardiac function is not known. Thus, we measured the function/performance of myocardial strips from normoxic- and hypoxic-acclimated (40% air saturation; ∼8 kPa O2) trout at several frequencies (20-80 contractions·min-1) and two muscle strain amplitudes (8% and 14%) when exposed to increasing concentrations of the NO donor sodium nitroprusside (SNP) (10-9 to 10-4 M). Further, we examined the influence of 1) nitric oxide synthase (NOS) produced NO [by blocking NOS with 10-4 M NG-monomethyl-l-arginine (l-NMMA)] and 2) soluble guanylyl cyclase mediated, NOS-independent, NO effects (i.e., after blockade with 10-4 M ODQ), on myocardial contractility. Hypoxic acclimation increased twitch duration by 8%-10% and decreased mass-specific net power by ∼35%. However, hypoxic acclimation only had minor impacts on the effects of SNP and the two blockers on myocardial function. The most surprising finding of the current study was the degree to which contraction frequency and strain amplitude influenced NO-mediated effects on myocardial power. For example, at 8% strain, 10-4 SNP resulted in a decrease in net power of ∼30% at 20 min-1 but an increase of ∼20% at 80 min-1, and this effect was magnified at 14% strain. This research suggests that hypoxic acclimation has only minor effects on NO-mediated myocardial contractility in salmonids, is the first to report the high frequency- and strain-dependent nature of NO effects on myocardial contractility in fishes, and supports previous work showing that NO effects on the heart (myocardium) are finely tuned spatiotemporally.

Effects of hypoxic acclimation on contractile properties of the spongy and compact ventricular myocardium of steelhead trout (Oncorhynchus mykiss).

The trout ventricle has an outer compact layer supplied with well-oxygenated arterial blood from the coronary circulation, and an inner spongy myocardium supplied with oxygen poor venous blood. It was hypothesized that: (1) the spongy myocardium of steelhead trout (Oncorhynchus mykiss), given its routine exposure to low partial pressures of oxygen (PO2), would be better able to maintain contractile performance (work) when exposed to acute hypoxia (100 to 10% air saturation) relative to the compact myocardium, and would show little benefit from hypoxic acclimation; and (2) the compact myocardium from hypoxia-acclimated (40% air saturation) fish would be better able to maintain work during acute exposure to hypoxia relative to normoxia-acclimated individuals. Consistent with our expectations, when PO2 was acutely lowered, net work from the compact myocardium of normoxia-acclimated fish declined more (by ~ 73%) than the spongy myocardium (~ 50%), and more than the compact myocardium of hypoxia-acclimated fish (~ 55%), and hypoxic acclimation did not benefit the spongy myocardium in the face of reduced PO2. Further, while hypoxic acclimation resulted in a 25% (but not significant) decrease in net work of the spongy myocardium, the performance of the compact myocardium almost doubled. This research suggests that, in contrast to the spongy myocardium, performance of the compact myocardium is improved by hypoxic acclimation; and supports previous research suggesting that the decreased contractile performance of the myocardium upon exposure to lowered PO2 may be adaptive and mediated by mechanisms within the muscle itself.

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.

Echocardiography and electrocardiography reveal differences in cardiac hemodynamics, electrical characteristics, and thermal sensitivity between northern pike, rainbow trout, and white sturgeon.

Doppler and B-mode ultrasonography and electrocardiography (ECG) were used to determine cardiac hemodynamics and electrical characteristics in 12°C-acclimated and metomidate-anesthetized northern pike, rainbow trout and white sturgeon (7-9 per species) at 12°C and 20°C, and at a comparable heart rate (fH , ~60 beats/min). Despite similar relative ventricle masses and cardiac output (Q), interspecific differences were observed at 12°C in fH , ventricular filling and ejection, stroke volume, the duration ECG intervals, and cardiac valve cross-sectional areas. Vis-a-fronte filling of the atrium due to ventricular contraction was observed in all species. However, biphasic ventricular filling (i.e., due to central venous pressure and then atrial contraction) was only observed in rainbow trout and white sturgeon. Changes in atrial and ventricular performance varied between the species as temperature increased from 12°C to 20°C. Rainbow trout had the highest thermal sensitivity for fH (Q10 = 3.73), which doubled Q, and the largest increase in transvalvular blood velocity during ventricular filling. Conversely, northern pike had the lowest Q10 for fH (1.58) and did not increase Q. At ~60 beats/min, the rainbow trout heart had the shortest period of electrical activity, which also resulted in the longest recovery period (TP interval) between successive beats. The QT interval at ~60 beats/min was also longer in the white sturgeon versus the other species. These results suggest that interspecific differences in fish cardiac hemodynamics may be related to cardiac morphology, the duration of electrical impulses through the heart, cardiac thermal sensitivity, and valve dimensions.

Enhancement of muscle and locomotor performance by a series compliance: A mechanistic simulation study.

The objective was to better understand how a series compliance alters contraction kinetics and power output of muscle to enhance the work done on a load. A mathematical model was created in which a gravitational point load was connected via a linear spring to a muscle (based on the contractile properties of the sartorius of leopard frogs, Rana pipiens). The model explored the effects of load mass, tendon compliance, and delay between onset of contraction and release of the load (catch) on lift height and power output as measures of performance. Series compliance resulted in increased lift height over a relatively narrow range of compliances, and the effect was quite modest without an imposed catch mechanism unless the load was unrealistically small. Peak power of the muscle-tendon complex could be augmented up to four times that produced with a muscle alone, however, lift height was not predicted by peak power. Rather, lift height was improved as a result of the compliance synchronizing the time courses of muscle force and shortening velocity, in particular by stabilizing shortening velocity such that muscle power was sustained rather than rising and immediately falling. With a catch mechanism, enhanced performance resulted largely from energy storage in the compliance during the period of catch, rather than increased time for muscle activation before movement commenced. However, series compliance introduced a trade-off between work done before versus after release of the catch. Thus, the ability of tendons to enhance locomotor performance (i.e. increase the work done by muscle) appears dependent not only on their established role in storing energy and increasing power, but also on their ability to modulate the kinetics of muscle contraction such that power is sustained over more of the contraction, and maximizing the balance of work done before versus after release of a catch.

Effects of epinephrine exposure on contractile performance of compact and spongy myocardium from rainbow trout (Oncorhynchus mykiss) during hypoxia.

Hypoxia results in elevated circulating epinephrine for many fish species, and this is likely important for maintaining cardiac function. The aims of this study were to assess how hypoxia impacts contractile responses of ventricular compact and spongy myocardium from rainbow trout (Oncorhynchus mykiss) and to assess how and if epinephrine may protect myocardial performance from a depressive effect of hypoxia. Work output and maximum contraction rate of isolated preparations of spongy and compact ventricular myocardium from rainbow trout were measured. Tissues were exposed to the blood PO2 that they experience in vivo during environmental normoxia and hypoxia and also to low (5 nM) and high (500 nM) levels of epinephrine in 100% air saturation (PO2 20.2 kPa) and during hypoxia (PO2 2 kPa, 10% air saturation). It was hypothesized that hypoxia would result in a decrease in work output and maximum contraction rate in both tissue types, but that epinephrine exposure would mitigate the effect. Hypoxia resulted in a decline in net work output of both tissue types, but a decline in maximum contraction rate of only compact myocardium. Epinephrine restored the maximum contraction rate of compact myocardium in hypoxia, appeared to slightly enhance work output of only compact myocardium in air saturation but surprisingly not during hypoxia, and restored net work of hypoxic spongy myocardium toward normoxic levels. These results indicate hypoxia has a similar depressive effect on both layers of ventricular myocardium, but that high epinephrine may be important for maintaining inotropy in spongy myocardium and chronotropy in compact myocardium during hypoxia.

Effects of Using Tricaine Methanesulfonate and Metomidate before Euthanasia on the Contractile Properties of Rainbow Trout (Oncorhynchus mykiss) Myocardium.

Because many anesthetics work through depressing cell excitability, unanesthetized euthanasia has become common for research involving excitable tissues (for example muscle and nerve) to avoid these depressive effects. However, anesthetic use during euthanasia may be indicated for studies involving isolated tissues if the potential depressive effects of brief anesthetic exposure dissipate after subsequent tissue isolation, washout, and saline perfusion. We explore this here by measuring whether, when applied prior to euthanasia, standard immersion doses of 2 fish anesthetics, tricaine methanesulfonate (TMS; 100 mg/L, n = 6) and methyl 1-(1-phenylethyl)-1H-imidazole-5-carboxylate (metomidate, 10 mg/L, n = 6), have residual effects on the contractile properties (force and work output) of isolated and saline-perfused ventricular compact myocardium from rainbow trout (Oncorhynchus mykiss). Results suggest that direct exposure of muscle to immersion doses of TMS-but not metomidate-impairs muscle contractile performance. However, brief exposure (2 to 3 min) to either anesthetic during euthanasia only-providing that the agent is washed out prior to tissue experimentation-does not have an effect on the contractile properties of the myocardium. Therefore, the use of TMS, metomidate, and perhaps other anesthetics that depress cell excitability during euthanasia may be indicated when conducting research on isolated and rinsed tissues.

Frequency dependence of power and its implications for contractile function of muscle fibers from the digital flexors of horses.

The digital flexors of horses must produce high force to support the body weight during running, and a need for these muscles to generate power is likely limited during locomotion over level ground. Measurements of power output from horse muscle fibers close to physiological temperatures, and when cyclic strain is imposed, will help to better understand the in vivo performance of the muscles as power absorbers and generators. Skinned fibers from the deep (DDF) and superficial (SDF) digital flexors, and the soleus (SOL) underwent sinusoidal oscillations in length over a range of frequencies (0.5-16 Hz) and strain amplitudes (0.01-0.06) under maximum activation (pCa 5) at 30°C. Results were analyzed using both workloop and Nyquist plot analyses to determine the ability of the fibers to absorb or generate power and the frequency dependence of those abilities. Power absorption was dominant at most cycling frequencies and strain amplitudes in fibers from all three muscles. However, small amounts of power were generated (0.002-0.05 Wkg(-1)) at 0.01 strain by all three muscles at relatively slow cycling frequencies: DDF (4-7 Hz), SDF (4-5 Hz) and SOL (0.5-1 Hz). Nyquist analysis, reflecting the influence of cross-bridge kinetics on power generation, corroborated these results. The similar capacity for power generation by DDF and SDF versus lower for SOL, and the faster frequency at which this power was realized in DDF and SDF fibers, are largely explained by the fast myosin heavy chain isoform content in each muscle. Contractile function of DDF and SDF as power absorbers and generators, respectively, during locomotion may therefore be more dependent on their fiber architectural arrangement than on the physiological properties of their muscle fibers.

Temperature and sex dependent effects on cardiac mitochondrial metabolism in Atlantic cod (Gadus morhua L.).

To test the hypothesis that impaired mitochondrial respiration limits cardiac performance at warm temperatures, and examine if any effect(s) are sex-related, the consequences of high temperature on cardiac mitochondrial oxidative function were examined in 10°C acclimated, sexually immature, male and female Atlantic cod. Active (State 3) and uncoupled (States 2 and 4) respiration were measured in isolated ventricular mitochondria at 10, 16, 20, and 24°C using saturating concentrations of malate and pyruvate, but at a submaximal (physiological) level of ADP (200µM). In addition, citrate synthase (CS) activity was measured at these temperatures, and mitochondrial respiration and the efficiency of oxidative phosphorylation (P:O ratio) were determined at [ADP] ranging from 25-200µM at 10 and 20°C. Cardiac morphometrics and mitochondrial respiration at 10°C, and the thermal sensitivity of CS activity (Q10=1.51), were all similar between the sexes. State 3 respiration at 200µM ADP increased gradually in mitochondria from females between 10 and 24°C (Q10=1.48), but plateaued in males above 16°C, and this resulted in lower values in males vs. females at 20 and 24°C. At 10°C, State 4 was ~10% of State 3 values in both sexes [i.e. a respiratory control ratio (RCR) of ~10] and P:O ratios were approximately 1.5. Between 20 and 24°C, State 4 increased more than State 3 (by ~70 vs. 14%, respectively), and this decreased RCR to ~7.5. The P:O ratio was not affected by temperature at 200µM ADP. However, (1) the sensitivity of State 3 respiration to increasing [ADP] (from 25 to 200µM) was reduced at 20 vs. 10°C in both sexes (Km values 105±7 vs. 68±10µM, respectively); and (2) mitochondria from females had lower P:O values at 25 vs. 100µM ADP at 20°C, whereas males showed a similar effect at 10°C but a much more pronounced effect at 20°C (P:O 1.05 at 25µM ADP vs. 1.78 at 100µMADP). In summary, our results demonstrate several sex-related differences in ventricular mitochondrial function in Atlantic cod, and suggest that myocardial oxidative function and possibly phosphorylation efficiency may be limited at temperatures of 20°C or above, particularly in males. These observations could partially explain why cardiac function in Atlantic cod plateaus just below this species׳ critical thermal maximum (~22°C) and may contribute to yet unidentified sex differences in thermal tolerance and swimming performance.

Controlled chaos: three-dimensional kinematics, fiber histochemistry, and muscle contractile dynamics of autotomized lizard tails.

The ability to shed an appendage occurs in both vertebrates and invertebrates, often as a tactic to avoid predation. The tails of lizards, unlike most autotomized body parts of animals, exhibit complex and vigorous movements once disconnected from the body. Despite the near ubiquity of autotomy across groups of lizards and the fact that this is an extraordinary event involving the self-severing of the spinal cord, our understanding of why and how tails move as they do following autotomy is sparse. We herein explore the histochemistry and physiology of the tail muscles of the leopard gecko (Eublepharis macularius), a species that exhibits vigorous and variable tail movements following autotomy. To confirm that the previously studied tail movements of this species are generally representative of geckos and therefore suitable for in-depth muscle studies, we quantified the three-dimensional kinematics of autotomized tails in three additional species. The movements of the tails of all species were generally similar and included jumps, flips, and swings. Our preliminary analyses suggest that some species of gecko exhibit short but high-frequency movements, whereas others exhibit larger-amplitude but lower-frequency movements. We then compared the ATPase and oxidative capacity of muscle fibers and contractile dynamics of isolated muscle bundles from original tails, muscle from regenerate tails, and fast fibers from an upper limb muscle (iliofibularis) of the leopard gecko. Histochemical analysis revealed that more than 90% of the fibers in original and regenerate caudal muscles had high ATPase but possessed a superficial layer of fibers with low ATPase and high oxidative capacity. We found that contraction kinetics, isometric force, work, power output, and the oscillation frequency at which maximum power was generated were lowest in the original tail, followed by the regenerate tail and then the fast fibers of the iliofibularis. Muscle from the original tail exhibited greater resistance to fatigue, followed by the regenerate tail and then the fast iliofibularis fibers. These results suggest that the relatively slow and oxidative fibers found within the tail musculature have a significant impact on contractile function, which translates into a trade-off between longevity of performance and power after autotomy.

Increased ventricular stiffness and decreased cardiac function in Atlantic cod (Gadus morhua) at high temperatures.

We employed the work loop method to study the ability of ventricular and atrial trabeculae from Atlantic cod to sustain power production during repeated contractions at acclimation temperatures (10°C) and when acutely warmed (20°C). Oxygen tension (Po2) was lowered from 450 to 34% air saturation to augment the thermal stress. Preparations worked under conditions simulating either a large stroke volume (35 contractions/min rate, 8-12% muscle strain) or a high heart rate (70 contractions/min, 2-4% strain), with power initially equal under both conditions. The effect of declining Po2 on power was similar under both conditions but was temperature and tissue dependent. In ventricular trabeculae at 10°C (and atria at 20°C), shortening power declined across the full range of Po2 studied, whereas the power required to lengthen the muscle was unaffected. Conversely, in ventricular trabeculae at 20°C, there was no decline in shortening power but an increase in lengthening power when Po2 fell below 100% air saturation. Finally, when ventricular trabeculae were paced at rates of up to 115 contractions/min at 20°C (vs. the maximum of 70 contractions/min in vivo), they showed marked increases in both shortening and lengthening power. Our results suggest that although elevated heart rates may not impair ventricular power as they commonly do isometric force, limited atrial power and the increased work required to expand the ventricle during diastole may compromise ventricular filling and hence, stroke volume in Atlantic cod at warm temperatures. Neither large strains nor high contraction rates convey an apparent advantage in circumventing this.

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.

Red muscle function in stiff-bodied swimmers: there and almost back again.

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.

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.

Locomotor trade-offs in mice selectively bred for high voluntary wheel running.

We investigated sprint performance and running economy of a unique ;mini-muscle' phenotype that evolved in response to selection for high voluntary wheel running in laboratory mice (Mus domesticus). Mice from four replicate selected (S) lines run nearly three times as far per day as four control lines. The mini-muscle phenotype, resulting from an initially rare autosomal recessive allele, has been favoured by the selection protocol, becoming fixed in one of the two S lines in which it occurred. In homozygotes, hindlimb muscle mass is halved, mass-specific muscle oxidative capacity is doubled, and the medial gastrocnemius exhibits about half the mass-specific isotonic power, less than half the mass-specific cyclic work and power, but doubled fatigue resistance. We hypothesized that mini-muscle mice would have a lower whole-animal energy cost of transport (COT), resulting from lower costs of cycling their lighter limbs, and reduced sprint speed, from reduced maximal force production. We measured sprint speed on a racetrack and slopes (incremental COT, or iCOT) and intercepts of the metabolic rate versus speed relationship during voluntary wheel running in 10 mini-muscle and 20 normal S-line females. Mini-muscle mice ran faster and farther on wheels, but for less time per day. Mini-muscle mice had significantly lower sprint speeds, indicating a functional trade-off. However, contrary to predictions, mini-muscle mice had higher COT, mainly because of higher zero-speed intercepts and postural costs (intercept-resting metabolic rate). Thus, mice with altered limb morphology after intense selection for running long distances do not necessarily run more economically.

Changes in efficiency and myosin expression in the small-muscle phenotype of mice selectively bred for high voluntary running activity.

Mice from lines selectively bred for high levels of voluntary wheel running express a high incidence of a small muscle phenotype ('mini-muscles') that may confer an adaptive advantage with respect to endurance-running capacity. Plantar flexors in the mini-muscle phenotype exhibit a high capacity for aerobic activity, including altered enzyme activities, loss of expression of type IIb myosin heavy chain (MHC), increased expression of type I, IIx and IIa MHC, and mechanical performance consistent with slower, more fatigue-resistant muscles. We hypothesized that these changes may accompany enhanced efficiency of contraction, perhaps in support of the enhanced capacity for endurance running. To assess efficiency, we measured work and associated oxygen consumption from isolated soleus and medial gastrocnemius muscles from mice with mini-muscle and normal phenotypes. We also measured the MHC expression of the plantar flexor muscles to better understand the physiological basis of any differences in efficiency. The proportion of the various MHC isoforms in the soleus was shifted toward a slightly faster phenotype in the mini-muscle mice, whereas in the gastrocnemius and plantaris it was shifted toward a markedly slower phenotype, with large reductions in type IIb MHC and large increases in type I, IIa, and IIx MHC. Soleus muscles from normal and mini-muscle mice showed no statistical differences in efficiency, but medial gastrocnemius from mini-muscle mice were significantly less efficient than those from normal mice, despite the distinctly slower MHC phenotype in mini-muscle mice. Thus, based on measures of efficiency from isolated muscles under conditions near optimal for power output, the shift toward a slower phenotype in 'mini' gastrocnemius muscles does not appear to confer advantages directly through increased efficiency. Rather, the slower phenotype may reduce energy used by the muscles and be permissive to enhanced running ability, perhaps by reducing reliance on anaerobic metabolism.