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(A) Side view of a yellowfin tuna and a skipjack tuna showing the longitudinal extent of the internal red muscle (indicated by the white bar) (adapted from paintings by George Mattson in Joseph et al., 1988). (B) Hemi-transverse sections of yellowfin and skipjack muscle, showing the distribution of internal and superficial red muscle. Also shown is the color gradation in the superficial muscle of both species from dark red in the more anterior locations (matching the internal red muscle) to a lighter color at more posterior locations. Views are of anterior faces of slices from the left side of the body. L, fork length.
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To learn about muscle function in two species of tuna (yellowfin Thunnus albacares and skipjack Katsuwonus pelamis), a series of electromyogram (EMG) electrodes was implanted down the length of the body in the internal red (aerobic) muscle. Additionally, a buckle force transducer was fitted around the deep caudal tendons on the same side of the ped...
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... anatomical features internally. External features include a smooth skin and recesses for retracting many of the fins, the largest cross- sectional area of muscle mass concentrated near the body's midlength, narrow-necking just forward of the caudal fin for reduced drag, and a large-aspect-ratio lunate caudal fin that provides lift-based thrust (Fig. 1A). Internally, tunas differ from most other fishes in having the bulk of their red muscle located medially, near the backbone (Fig. 1B). This internal mass is an integral part of the nested myotome cones, with the concentric rings of red muscle being continuous with the surrounding white muscle. The myotomes in tunas are highly ...
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... sectional area of muscle mass concentrated near the body's midlength, narrow-necking just forward of the caudal fin for reduced drag, and a large-aspect-ratio lunate caudal fin that provides lift-based thrust (Fig. 1A). Internally, tunas differ from most other fishes in having the bulk of their red muscle located medially, near the backbone (Fig. 1B). This internal mass is an integral part of the nested myotome cones, with the concentric rings of red muscle being continuous with the surrounding white muscle. The myotomes in tunas are highly elongated, which directs the force produced by the anteriorly situated muscle mass rearward to the tail. The unusual anatomical arrangement of ...
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... that there would still be a discernible traveling wave of activation in the tunas, but that activation of each side would be more nearly instantaneous than in non-thunniform swimmers, which use more undulatory swimming modes. Additionally, yellowfin and skipjack tunas exhibit subtle morphological differences externally and internally ( Fig. 1), so another goal of this study was to determine whether these design differences are manifested in T. KNOWER AND OTHERS al., 1988). (B) Hemi-transverse sections of yellowfin and skipjack muscle, showing the distribution of internal and superficial red muscle. Also shown is the color gradation in the superficial muscle of both species ...
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... the fish had been anesthetized, 2-6 electromyogram (EMG) electrodes were implanted along the length of the internal red muscle (i.e. the red portion of the nested myotome cones, near the backbone; Fig. 1B) of the left side, using a 22 gauge needle. Initially, bipolar hook-type electrodes were used, constructed of 34 gauge Teflon-coated copper wire (Belden Wire and Cable, 8057) with the ends bared 1-2 mm. However, monopolar electrodes (referenced to a common wire implanted under the skin just behind the top of the skull) were used later ...
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... plans of a yellowfin tuna and a skipjack tuna (Fig. 1A) show the longitudinal extent and internal position of the red muscle. Transverse sections from each species (Fig. 1B) illustrate the continuity between red and white muscle within the nested cones. In yellowfin, the red muscle near the backbone extends from approximately 0.26L to 0.80L (largest cross-sectional area at 0.56L); in ...
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... plans of a yellowfin tuna and a skipjack tuna (Fig. 1A) show the longitudinal extent and internal position of the red muscle. Transverse sections from each species (Fig. 1B) illustrate the continuity between red and white muscle within the nested cones. In yellowfin, the red muscle near the backbone extends from approximately 0.26L to 0.80L (largest cross-sectional area at 0.56L); in skipjack, it extends from 0.28L to 0.77L (largest cross-sectional area at 0.50L). These ranges are comparable with those ...
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... tunas of comparable size swimming in this same tunnel. Therefore, the surgical procedures and implanted wires appear not to affect adversely the swimming behavior of these fish in this regard. Both species exhibited a linear relationship between tailbeat frequency and swimming speed (Fig. 2), which is typical of steady swimming in many fishes. Fig. 3A illustrates 16 consecutive tailbeats of unprocessed EMG signals from the red muscle at 0.40, 0.52 and 0.63L in one side of a swimming skipjack tuna. Fig. 3B shows the same at 0.26, 0.43, 0.52 and 0.67L during four consecutive tailbeats in a swimming yellowfin, except that time is expanded and the EMG traces have been high-pass-filtered and rectified ...
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... different (0.01<P<0.02)]. Yellowfin regression: y=−0.46x+0.56 (r 2 =0.71, P<0.001); skipjack regression: y=−0.63x+0.74 (r 2 =0.74, P=0.001). Points and error bars are means and standard deviations of all tailbeats from all speeds at each location. Tuna red muscle activation patterns area (Magnuson, 1978), and have much smaller pectoral fins (Fig. 1). The last point is particularly pronounced in the size range of fish used for this study: small yellowfin have much larger pectoral fins relative to their body size than do skipjack and therefore derive more hydrodynamic lift (Beamish, 1978). Consequently, skipjack require a faster minimum swimming velocity to maintain hydrostatic ...
Citations
... The differences are attributed to the effect of acceleration. Indeed, most previous studies [62][63][64][65][66] focus on steady thunniform swimming, with unsteady swimming trends gaining traction only recently. For example, one previous study investigated the acceleration of a solitary thunniform swimmer from rest [20]. ...
Optimal fish array hydrodynamics in accelerating phalanx schools are investigated through a computational framework which combines high fidelity Computational Fluid Dynamics (CFD) simulations with a gradient free surrogate-based optimization algorithm. Critical parameters relevant to a phalanx fish school, such as midline kinematics, separation distance and phase synchronization, are investigated in light of efficient propulsion during an accelerating fish motion. Results show that the optimal midline kinematics in accelerating phalanx schools resemble those of accelerating solitary swimmers. The optimal separation distance in a phalanx school for thunniform biologically-inspired swimmers is shown to be around $2L$ (where $L$ is the swimmer's total length). Furthermore, separation distance is shown to have a stronger effect, \textit{ceteris paribus}, on the propulsion efficiency of a school when compared to phase synchronization.
... With maximum myoseptum lengths between 3 and 6.5 centra length, the investigated stomiiforms show myoseptum lengths that are somewhere in between those of non-carangiform and carangiform swimmers. Myoseptum lengths are greatest in thunniform swimmers like tunas, in which they span between 10 and 17 centra in the tail region (Donley et al., 2004;Ellerby et al., 2000;Fierstine & Walters, 1968;Kafuku, 1950;Katz, 2002;Knower et al., 1999;Nakae et al., 2014;Shadwick et al., 2002;Westneat et al., 1993;Westneat & Wainwright, 2001). It has been shown that in comparison with non-carangiform swimmers, the increase in myoseptal elongation over the length of the body is remarkable in carangiform and thunniform swimmers, ranging from anterior to posterior to up to 25% of the body length (Donley et al., 2004;Gemballa & Röder, 2004;). ...
... There, the last five to six myosepta lack a posterior cone and form together the highly elongated great LT and the underlying medial caudal tendon attaching to caudal-fin rays. Direct force measurements in two tuna species have shown that red muscle forces are transmitted via those elongated caudal tendons (LT pathway) to the tail (Knower et al., 1999;Shadwick et al., 2002). However, experimental data on hydrodynamics and physiology are lacking for deep-sea fishes. ...
Every night the greatest migration on Earth starts in the deep pelagic oceans where organisms move up to the meso-and epipelagic to find food and return to the deeper zones during the day. One of the dominant fish taxa undertaking vertical migrations are the dragonfishes (Stomiiformes). However, the functional aspects of locomotion and the architecture of the musculotendinous system (MTS) in these fishes have never been examined. In general, the MTS is organized in segmented blocks of specific three-dimensional 'W-shaped' foldings, the myomeres, separated by thin sheets of connective tissue, the myosepta. Within a myoseptum characteristic intermuscular bones or tendons may be developed. Together with the fins, the MTS forms the functional unit for locomotion in fishes. For this study, microdissections of cleared and double stained specimens of seven stomiiform species (Astronesthes sp., Chauliodus sloani, Malacosteus australis, Eustomias simplex, Polymetme sp., Sigmops elongatus, Argyropelecus affinis) were conducted to investigate their MTS. Soft tissue was investigated non-invasively in E. schmidti using a micro-CT scan of one specimen stained with iodine. Additionally, classical histological serial sections were consulted. The investigated stomiiforms are characterized by the absence of anterior cones in the anteriormost myosepta. These cones are developed in myosepta at the level of the dorsal fin and elongate gradually in more posterior myosepta. In all but one investigated stomiiform taxon the horizontal septum is reduced. The amount of connective tissue in the myosepta is very low anteriorly, but increases gradually with body length. Red musculature overlies laterally the white musculature and exhibits strong tendons in each myomere within the muscle bundles dorsal and ventral to the horizontal midline. The amount of red musculature increases immensely towards the caudal fin. The elongated lateral tendons of the posterior body segments attach in a highly complex pattern on the caudal-fin rays, which indicates that the posterior most myosepta are equipped for a multisegmental force transmission towards the caudal fin. This unique anatomical condition might be essential for steady swimming during diel vertical migrations, when prey is rarely available.
... This dorso-ventral asymmetry persists in larger T. albacares (J. B. Graham, 1975;Knower et al., 1999) and may be a consequence of regional differences in the location of SM stem cell precursors, or possibly the position of the retia in the circulation to and from the SM, which differs among tunas (reviewed in Bushnell et al., 1992;. The SM asymmetry is more pronounced in T. albacares, which has four lateral retia and two small central retia, than in the tuna species that have a large central rete and four small lateral retia, including E. lineatus and K. pelamis, in which SM is adjacent to the vertebral column in both epaxial and hypaxial regions (Stevens et al., 1974, figures;Dickson et al., 2000;J. ...
... The SM asymmetry is more pronounced in T. albacares, which has four lateral retia and two small central retia, than in the tuna species that have a large central rete and four small lateral retia, including E. lineatus and K. pelamis, in which SM is adjacent to the vertebral column in both epaxial and hypaxial regions (Stevens et al., 1974, figures;Dickson et al., 2000;J. B. Graham, 1975;Knower et al., 1999). ...
... The larger minimum size for regional endothermy in T. albacares than in T. orientalis may also be a consequence of T. albacares having more SM located adjacent to the skin (J. B. Graham, 1975;Kishinouye, 1923;Knower et al., 1999;pers. obs.), which would probably result in a higher rate of heat loss by conduction across the body surface. ...
Myotomal slow‐oxidative muscle (SM) powers continuous swimming and generates heat needed to maintain elevated locomotor muscle temperatures (regional endothermy) in tunas. This study describes how the amount and distribution of myotomal SM increases with fish size and age in juvenile yellowfin tuna Thunnus albacares in relationship to the development of regional endothermy. In T. albacares juveniles 40–74 mm fork length (LF; n = 23) raised from fertilised eggs at the Inter‐American Tropical Tuna Commission Achotines Laboratory in Panama and larger juveniles (118–344 mm LF; n = 5) collected by hook and line off of Oahu, Hawaii, USA, SM was identified by histochemical staining for the mitochondrial enzyme succinic dehydrogenase or by colour (in the two largest individuals). The cross‐sectional area of myotomal SM at 60% LF, a position with maximal percentage of SM in larger T. albacares, increased exponentially with LF. The percentage of total cross‐sectional area composed of SM at 60% LF increased significantly with both LF and age, suggesting that SM growth occurs throughout the size range of T. albacares juveniles studied. In addition, the percentage of SM at 60% LF that is medial increased asymptotically with LF. The increases in amount of SM and medial SM, along with the development of the counter‐current heat‐exchanger blood vessels that retain heat, allow larger tuna juveniles to maintain elevated and relatively stable SM temperatures, facilitating range expansion into cooler waters.
... Nonetheless, direct records of swimming speeds are scarce and sometimes inconclusive given the size limitations of controlled experiments and the difficulty of taking measurements in the wild. Regarding cruising speeds, some experiments carried out in water tunnels suggested similar speeds for ectothermic and regional endothermic taxa [86][87][88][89][90][91]. However, the work of Watanabe et al. [85] has recently shed light on this, demonstrating that cruising speeds of fishes with regional endothermy are greater than fishes without it using free-swimming data. ...
Otodontids include some of the largest macropredatory sharks that ever lived, the most extreme case being Otodus (Megaselachus) megalodon. The reasons underlying their gigantism, distribution patterns and extinction have been classically linked with climatic factors and the evolution, radiation and migrations of cetaceans during the Paleogene. However, most of these previous proposals are based on the idea of otodontids as ectothermic sharks regardless of the ecological, energetic and body size constraints that this implies. Interestingly, a few recent studies have suggested the possible existence of endothermy in these sharks thus opening the door to a series of new interpretations. Accordingly, this work proposes that regional endothermy was present in otodontids and some closely related taxa (cretoxyrhinids), playing an important role in the evolution of gigantism and in allowing an active mode of live. The existence of regional endothermy in these groups is supported here by three different approaches including isotopic-based approximations, swimming speed inferences and the application of a novel methodology for assessing energetic budget and cost of swimming in extinct taxa. In addition, this finding has wider implications. It calls into question some previous paleotemperature estimates based partially on these taxa, suggests that the existing hypothesis about the evolution of regional endothermy in fishes requires modification, and provides key evidence for understanding the evolution of gigantism in active macropredators.
... The longissimus (which was activated after the iliocaudalis) exhibited more of a steady-state activity pattern with no significant change in onset time or duration with increasing tail oscillation frequency (Figures 2-4). Differences in EMG activation pattern have been related to different basic swimming mechanics in fish (Knower et al., 1999). The tail of V. salvator accounts for nearly 50% of the total body length; if the longissimus exhibited the same "steady-state" pattern throughout the tail length, then disruption of the oscillation cycle would be likely at higher tail frequencies. ...
Water monitor lizards (Varanus salvator) swim using sinusoidal oscillations generated at the base of their long (50% of total body length) tail. In an effort to determine which level of the structural/organizational hierarchy of muscle is associated with functional segregation between the muscles of the tail base, an array of muscle features—myosin heavy chain profiles, enzymatic fiber types, twitch and tetanic force production, rates of fatigue, muscle compliance, and electrical activity patterns—were quantitated. The two examined axial muscles, longissimus, and iliocaudalis, were generally similar at the molecular, biochemical, and physiological levels, but differed at the biomechanics level and in their activation pattern. The appendicular muscle examined, caudofemoralis, differed from the axial muscles particularly at the molecular and physiological levels, and it exhibited a unique compliance profile and pattern of electrical activation. There were some apparent contradictions between the different structural/organizational levels examined. These contradictions, coupled with a unique myosin heavy chain profile, lead to the hypothesis that there are previously un-described molecular/biochemical specializations within varanid skeletal muscles.
... Open squares, chub mackerel, Scomber japonicus (Dickson et al. 2002); open circles, cod, Gadus morhua (Nelson et al. 1994;Reidy et al. 1995Reidy et al. , 2000Lurman et al. 2007;Petersen and Gamperl 2010). Open triangles, Thunnini Knower et al. 1999;Shadwick et al. 1999;Blank et al. 2007). Closed circles, Salmoninae (Butler and Day 1993;Gallaugher et al. 2001;Jain and Farrell 2003;Lee et al. 2003;Deitch et al. 2006) minimize the presence of internal edges or projections that could disrupt flow. ...
Swimming flumes enable fish swimming behavior, physiology, and performance to be quantified in ways that are not practicable for fish swimming through open water. By placing fish in a water flow, speed can be controlled, fish can be instrumented to monitor a wide range of physiological parameters, and the exchange of materials between the fish and water can be quantified. This can provide vital information regarding fish fitness and health. If meaningful data are to be obtained, however, careful consideration must be given to flume design and operation, experimental protocol and the physiological state of the fish. Modifications to standard flume designs can potentially allow for accommodation of a wider range of species and experimental conditions that will enhance basic understanding of fish physiology and behavior and can potentially be applied in optimizing aquacultural techniques.
... For in vivo experiments, strain is usually measured in one of three ways. First, tendon force buckles have been surgically implanted on the deep caudal tendons of two species of tuna (Thunnus albacares and Katsuwonus pelamis) (Knower et al., 1999). Second, the XROMM technique, mentioned above, requires the implantation of radio-opaque markers directly on skeletal elements and restricted external water volume in aquatic species (Nowroozi and Brainerd, 2013). ...
... In rigid fishes (tunas, lamnid sharks), the elongated lateral tendons are likely to be part of a long distance force transmission system. For continuous swimming, muscle forces are transmitted from the anterior and midbody toward the caudal fin by insertions of either superficially placed or deep red muscles into the lateral tendons (tunas: Knower et al., 1999;Shadwick et al., 1999;Altringham and Shadwick, 2001;Katz et al., 2001;sharks: Donley et al., 2004sharks: Donley et al., , 2005Gemballa et al., 2006;swordfish: Gemballa et al., 2007). In these fishes, activity of anterior muscles causes bending at a more posterior position. ...
The body curvature displayed by fishes differs remarkably between species. Some nonmuscular features (e.g., number of vertebrae) are known to influence axial flexibility, but we have poor knowledge of the influence of the musculotendinous system (myosepta and muscles). Whereas this system has been described in stiff-bodied fishes, we have little data on flexible fishes. In this study, we present new data on the musculotendinous system of a highly flexible fish and compare them to existing data on rigid fishes. We use microdissections with polarized light microscopy to study the three-dimensional anatomy of myoseptal tendons, histology and immunohistology to study the insertion of muscle fiber types into tendons, and μ-CT scans to study skeletal anatomy. Results are compared with published data from stiff-bodied fishes. We identify four important morphological differences between stiff-bodied fishes and Carapus acus: (1) Carapus bears short tendons in the horizontal septum, whereas rigid fishes have elongated tendons. (2) Carapus bears short lateral tendons in its myosepta, whereas stiff-bodied fishes bear elongated tendons. Because of its short myoseptal tendons, Carapus retains high axial flexibility. In contrast, elongated tendons restrict axial flexibility in rigid fishes but are able to transmit anteriorly generated muscle forces through long tendons down to the tail. (3) Carapus bears distinct epineural and epipleural tendons in its myosepta, whereas these tendons are weak or absent in rigid fishes. As these tendons firmly connect vertebral axis and skin in Carapus, we consider them to constrain lateral displacement of the vertebral axis during extreme body flexures. (4) Ossifications of myoseptal tendons are only present in C. acus and other more flexible fishes but are absent in rigid fishes. The functional reasons for this remain unexplained.
... For example, work examining contractile properties along the body in the ectothermic leopard shark (Triakis semifasciata) and the endothermic mako shark (Isurus oxyrinchus) has demonstrated a similar pattern in both species in which the stimulus duration, stimulus phase, net work and power output of the locomotor muscles are relatively consistent in both anterior and posterior portions of the body (Donley et al. 2007). This contrasts that described for bony fishes, where temporal patterns of RM shortening and activation have been shown to differ along the length of the body (Williams et al. 1989;van Leeuwen et al. 1990;Rome et al. 1993;Wardle and Videler 1993;Jayne and Lauder 1995;Gillis 1998;Hammond et al. 1998;Shadwick et al. 1998;Knower et al. 1999;Ellerby and Altringham 2001). In contrast to bony fishes, comparatively few data exist on functional mechanical design in sharks, and no data are available for any species exhibiting an elongate caudal fin, such as the common thresher shark. ...
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.
... In transition to BCF swimming, power is generated from the myotomal muscle mass. At low BCF swimming speeds, power is generated by red muscle, which comprises a small proportion of the entire myotomal muscle mass (Greer-Walker and Pull, 1975;Jayne and Lauder, 1995;Coughlin and Rome, 1996;Knower et al., 1999). However with increasing speed, a greater proportion of the musculature is recruited in the form of pink and white muscle fibers (Rome et al., 1990(Rome et al., , 1993. ...
The laws of physics are rigid and fixed. Animals, therefore, are restricted in their use of available energy in accordance to the constraints of mechanics and thermodynamics. Evolutionary success dictates that a large proportion of the available energy reserves be allocated to reproductive effort despite the demand by other energy consuming functions. Therefore, mechanisms that reduce energy costs for non-reproductive functions relative to total energy reserves have an adaptive benefit for individuals (Fausch, 1984). As the laws of physics are inflexible and the available energy limited, animals have found ways to exploit these laws for their own benefit.
