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.     

Review: Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas.

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.     

Endothermy in fishes: a phylogenetic analysis of constraints,predispositions, and selection pressures

Synopsis Endothermy, the ability to raise body temperature by internal heat production, is unusual in teleost fishes and has only been documented within one suborder, the Scombroidei. Two separate modes of endothermy have evolved in the scombroidei; tunas warm their muscles, brain and viscera using heat exchangers in the circulation to these metabolically active tissues while billfishes and one primitive mackerel have a thermogenic organ situated beneath the brain. Both modes of endothermy emphasize common themes. Large body size coupled with heat exchangers are necessary to reduce convective and conductive heat exchange. A tissue with a high oxidative capacity is required for heat generation. Studies based upon morphology and mitochondrial DNA analyses indicate that endothermy has evolved independently at least three times within the scombroid lineage. Mapping of-morphological and physiological traits on a molecular phylogeny for scombroids provides evidence of selective pressures favoring evolution of diverse endothermic styles. The new results suggest anatomical constraints prevent most fish from using the tuna form of endothermy and indicate a possible linkage between endothermy and locomotory style (thunniform or sub-carangiform).Paper from the International Union of Biological Societies symposium The biology of tunas and billfishes: an examination of life on the knife edge, organized by Richard W. Brill and Kim N. Holland.     

Cranial endothermy and a putative brain heater in the most basal tuna species, Allothunnus fallai

Field studies on the slender tuna Allothunnus fallai revealed cranial temperatures that were 4·8 ± 0·4° C (mean ± s . d .) above the ambient sea surface temperature. Dissections aimed at documenting the cranial heat source revealed a fused extraocular muscle complex positioned beneath the brain of this basal tuna species. The muscle complex is structurally distinct from that documented for any other fish species. In A. fallai , all four extraocular rectus muscle pairs (superior, inferior, medial and lateral rectus) are incorporated into one distinct tissue complex which is positioned between the orbits and in direct contact with the braincase. A combination of morphological, physiological and biochemical techniques were used to characterize the modified muscle tissue, and high-resolution magnetic resonance imaging was used to illustrate its association with the brain and optic nerves. The modified eye muscles lack organized contractile proteins and are perfused by an extensive vascular counter-current system that originates from the internal carotid artery. Vessel diameters, artery–vein configuration, and anatomic position between the systemic circulation and the warm eye muscles all suggest that this system is a heat exchanger. Collectively, these findings suggest that A. fallai has evolved extraocular muscles that may function to warm the brain and eye region. This is the first record of a cranial modification comprised of all four rectus muscles and the only documented occurrence of this mechanism for cranial endothermy among the tunas.     

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 (～ 60–100 kg) instrumented with sonomicrometric and electromyographic (EMG) leads swam alongside of the vessel with a tail-beat frequency of ～ 0.5 Hz. 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° 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.     

Rapid temperature compensation of volitional swimming speeds and lethal temperatures in tropical tunas (Scombridae)

Synopsis Observations on continuously swimming tunas were used to determine effects of temperature upon volitional locomotory activity and to determine upper and lower lethal temperatures. Experimental subjects were 10 skipjack tuna, Katsuwonus pelamis, 9 kawakawa, Euthynnus affinis, and 3 yellowfin tuna, Thunnus albacares.Our results: lower and upper lethal temperatures for the euthynnids (K. pelamis and E. affinis) were 15° and 33° C, respectively. Swimming speed for the euthynnids did not decrease with temperature within most of the zone of thermal tolerance; we observed either temperature independence or increases in speed as the temperature decreased. Yellowfin tuna swam slower as the water temperature decreased, but swimming speed changes lagged behind the water temperature changes. This effect was most certainly due to the large thermal inertia that is a property of tunas. The lag between swim speed and water temperature was eliminated by utilizing an estimate of red muscle temperature, rather than water temperature, as a covariate. Yellowfin tuna swim speed was best correlated with red muscle temperature rather than ambient water or brain temperatures.     

Age and growth of slender tuna (Allothunnus fallai) in an unexploited temperate population

Many large predatory fishes are in decline and tuna sustainability is high on the global agenda. Slender tuna (SLT), Allothunnus fallai, is data-poor and a rare contemporary example of a globally unexploited temperate tuna. This study analysed 214 otoliths for age and growth of fish collected in the South Atlantic. Observed ages varied between 9 and 42 years for a size range of 68–90 cm fork length. We reveal important life history data for SLT before exploitation and underline the relevance of data-poor stocks in understanding wider questions for exploited tuna.     

Evolution and consequences of endothermy in fishes

Regional endothermy, the conservation of metabolic heat by vascular countercurrent heat exchangers to elevate the temperature of the slow-twitch locomotor muscle, eyes and brain, or viscera, has evolved independently among several fish lineages, including lamnid sharks, billfishes, and tunas. All are large, active, pelagic species with high energy demands that undertake long-distance migrations and move vertically within the water column, thereby encountering a range of water temperatures. After summarizing the occurrence of endothermy among fishes, the evidence for two hypothesized advantages of endothermy in fishes, thermal niche expansion and enhancement of aerobic swimming performance, is analyzed using phylogenetic comparisons between endothermic fishes and their ectothermic relatives. Thermal niche expansion is supported by mapping endothermic characters onto phylogenies and by combining information about the thermal niche of extant species, the fossil record, and paleoceanographic conditions during the time that endothermic fishes radiated. However, it is difficult to show that endothermy was required for niche expansion, and adaptations other than endothermy are necessary for repeated diving below the thermocline. Although the convergent evolution of the ability to elevate slow-twitch, oxidative locomotor muscle temperatures suggests a selective advantage for that trait, comparisons of tunas and their ectothermic sister species (mackerels and bonitos) provide no direct support of the hypothesis that endothermy results in increased aerobic swimming speeds, slow-oxidative muscle power, or energetic efficiency. Endothermy is associated with higher standard metabolic rates, which may result from high aerobic capacities required by these high-performance fishes to conduct many aerobic activities simultaneously. A high standard metabolic rate indicates that the benefits of endothermy may be offset by significant energetic costs.     

Elevated Ca2+ ATPase (SERCA2) activity in tuna hearts: comparative aspects of temperature dependence

Tunas have an extraordinary physiology including elevated metabolic rates and high cardiac performance. In some species, retention of metabolic heat warms the slow oxidative swimming muscles and visceral tissues. In all tunas, the heart functions at ambient temperature. Enhanced rates of calcium transport in tuna myocytes are associated with increased expression of proteins involved in the contraction-relaxation cycle. The cardiac SR Ca2+-ATPase (SERCA2) plays a major role during cardiac excitation-contraction (E-C) coupling. Measurements of oxalate-supported Ca2+-uptake in atrial SR vesicles isolated from four species of tunas indicate that bluefin have at least two fold higher Ca2+-uptake than all other tunas examined between 5 and 30 degrees C. The highest atrial Ca2+-uptake was measured in bluefin tuna at 30 degrees C (23.32+/-1.58 nmol Ca2+/mg/min). Differences among tunas in the temperature dependency of Ca2+-uptake were similar for ATP hydrolysis. Western blot analysis revealed a significant increase in SERCA2 content associated with higher Ca2+ uptake rates in the atrial tissues of bluefin tuna and similar RyR expression across species. We propose that the expression of EC coupling proteins in cardiac myocytes, and the higher rates of SERCA2 activity are an important evolutionary step for the maintenance of higher heart rates and endothermy in bluefin tuna.     

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. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Ontogenetic change in the amount and position of slow-oxidative myotomal muscle in relationship to regional endothermy in juvenile yellowfin tuna Thunnus albacares

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 (L_F; n = 23) raised from fertilised eggs at the Inter-American Tropical Tuna Commission Achotines Laboratory in Panama and larger juveniles (118–344 mm L_F; 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% L_F, a position with maximal percentage of SM in larger T. albacares, increased exponentially with L_F. The percentage of total cross-sectional area composed of SM at 60% L_F increased significantly with both L_F and age, suggesting that SM growth occurs throughout the size range of T. albacares juveniles studied. In addition, the percentage of SM at 60% L_F that is medial increased asymptotically with L_F. 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.     

Unique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment

Synopsis Virtually all characteristics of tunas and billfishes reflect their highly charged lifestyles as apex predators in the oceanic pelagic environment. The adaptations they possess for efficient and rapid swimming, efficient and rapid food processing, turnover of nutrients and storage and mobilization of internal fuel supplies, and for rapid recovery rates, are discussed. Overall, tunas and billfishes are designed for high performance, at both sustainable and burst swimming speeds, but there are several differences between tunas and billfishes. Tunas' aerobic metabolic capacities exceed those of ectothermic fishes, including billfishes and other scombrids, by virtue of their elevated red muscle temperatures, and because heart and white muscle aerobic capacities are significantly greater in tunas. The adaptations for high performance involve some costs, including the need for a constant high energy input to sustain high metabolic rates, high activity levels, and endothermy, Yet, tunas and billfishes have adopted successful lifestyles, as evidenced by their large numbers and biomass within the marine environment. Although our knowledge of these fishes has increased dramatically during the past 15 years, there are major gaps in our understanding of the metabolic biochemistry and physiology of these fishes, and these are highlighted so that additional research can be directed towards filling these gaps.Paper from the International Union of Biological Societies symposium The biology of tunas and billfishes: an examination of life on the knife edge, organized by Richard W. Brill and Kim N. Holland.     

Responses of the red blood cells from two high-energy-demand teleosts, yellowfin tuna (Thunnus albacares) and skipjack tuna (Katsuwonus pelamis), to catecholamines

In fishes, catecholamines increase red blood cell intracellular pH through stimulation of a sodium/proton (Na⁺/H⁺) antiporter. This response can counteract potential reductions in blood O₂ carrying capacity (due to Bohr and Root effects) when plasma pH and intracellular pH decrease during hypoxia, hypercapnia, or following exhaustive exercise. Tuna physiology and behavior dictate exceptionally high rates of O₂ delivery to the tissues often under adverse conditions, but especially during recovery from exhaustive exercise when plasma pH may be reduced by as much as 0.4 pH units. We hypothesize that blood O₂ transport during periods of metabolic acidosis could be especially critical in tunas and the response of rbc to catecholamines elevated to an extreme. We therefore investigated the in vitro response of red blood cells from yellowfin tuna (Thunnus albacares) and skipjack tuna (Katsuwonus pelamis) to catecholamines. Tuna red blood cells had a typical response to catecholamines, indicated by a rapid decrease in plasma pH. Amiloride reduced the response, whereas 4,4′diisothiocyanatostilbene-2,2′-disulphonic acid enhanced both the decrease in plasma pH and the increase in intracellular pH. Changes in plasma [Na⁺], [Cl⁻], and [K⁺] were consistent with the hypothesis that tuna red blood cells have a Na⁺/H⁺ antiporter similar to that described for other teleost red blood cells. Red blood cells from both tuna species were more responsive to noradrenaline than adrenaline. At identical catecholamine concentrations, the decrease in plasma pH was greater in skipjack tuna blood, the more active of the two tuna species. Based on changes in plasma pH, the response of red blood cells to catecholamines from both tuna species was less than that of rainbow trout (Oncorhynchus mykiss) red blood cells, but greater than that of cod (Gadus morhua) red blood cells. Noradrenaline had no measurable influence on the O₂ affinity of skipjack tuna blood and only slightly increased the O₂ affinity of yellowfin tuna blood. Our results, therefore, do not support our original hypothesis. The catecholamine response of red blood cells from high-energy-demand teleosts (i.e., tunas) is not enhanced compared to other teleosts. There are data on changes in cardio-respiratory function in tunas caused by acute hypoxia and modest increases in activity, but there are no data on the changes in cardio-respiratory function in tunas accompanying the large increases in metabolic rate seen during recovery from exhaustive exercise. However, we conclude that during those instances where high rates of O₂ delivery to the tissues are needed, tunas' ability to increase cardiac output, ventilation volume, blood O₂ carrying capacity, and effective respiratory (i.e., gill) surface area are probably more important than are the responses of red blood cells to catecholamines. We also use our data to investigate the extent of the Haldane effect and its relationship to blood O₂ and CO₂ transport in yellowfin tuna. Yellowfin tuna blood shows a large Haldane effect; intracellular pH increases 0.20 units during oxygenation. The largest change in intracellular pH occurs between 40–100% O₂ saturation, indicating that yellowfin tuna, like other teleosts, fully exploit the Haldane effect over the normal physiological range of blood O₂ saturation. Accepted: 27 March 1998     

Large‐scale distribution of tuna species in a warming ocean

Tuna are globally distributed species of major commercial importance and some tuna species are a major source of protein in many countries. Tuna are characterized by dynamic distribution patterns that respond to climate variability and long‐term change. Here, we investigated the effect of environmental conditions on the worldwide distribution and relative abundance of six tuna species between 1958 and 2004 and estimated the expected end‐of‐the‐century changes based on a high‐greenhouse gas concentration scenario (RCP8.5). We created species distribution models using a long‐term Japanese longline fishery dataset and two‐step generalized additive models. Over the historical period, suitable habitats shifted poleward for 20 out of 22 tuna stocks, based on their gravity centre (GC) and/or one of their distribution limits. On average, tuna habitat distribution limits have shifted poleward 6.5 km per decade in the northern hemisphere and 5.5 km per decade in the southern hemisphere. Larger tuna distribution shifts and changes in abundance are expected in the future, especially by the end‐of‐the‐century (2080–2099). Temperate tunas (albacore, Atlantic bluefin, and southern bluefin) and the tropical bigeye tuna are expected to decline in the tropics and shift poleward. In contrast, skipjack and yellowfin tunas are projected to become more abundant in tropical areas as well as in most coastal countries' exclusive economic zones (EEZ). These results provide global information on the potential effects of climate change in tuna populations and can assist countries seeking to minimize these effects via adaptive management.     

The vascular morphology and in vivo muscle temperatures of thresher sharks (Alopiidae)

The thresher sharks comprise a single family (Alopiidae) of pelagic sharks most easily recognized by the elongate dorsal lobe of their caudal fin. Despite morphological similarities among the alopiids, the common thresher (Alopias vulpinus) is unique in that its red, aerobic myotomal muscle (RM) is medially positioned (i.e., closer to the vertebrae), its systemic blood is supplied through a lateral circulation which give rise to counter‐current heat exchanging retia, and it is capable of regional RM endothermy. Despite this information, it remains unknown if the other two alopiid species (bigeye thresher, Alopias superciliosus and pelagic thresher, Alopias pelagicus) also possess some or all of the characteristics related to regional RM endothermy. Thus, this study aimed to 1) document the presence of vascular specializations necessary for heat retention and RM endothermy and 2) measure the in vivo muscle temperatures of all three alopiid species. Laboratory dissections of the thresher species showed that only A. vulpinus possesses the lateral branching of the dorsal aorta giving rise to a lateral subcutaneous circulation and retial system, and that RM temperatures are elevated relative to ambient temperature. By contrast, both A. pelagicus and A. superciliosus have a similar systemic blood circulation pathway, in which the dorsal aorta and postcardinal vein form the basis for the central circulation and in vivo RM temperature measurements closely matched those of the ambient temperature at which the sharks were captured. Collectively, the vascular anatomy and in vivo temperature data suggest that only one species of thresher shark (A. vulpinus) possesses the requisite vascular specializations (i.e., lateral subcutaneous vessels and retia mirabilia) that facilitate RM endothermy. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Phylogenetic relationships between tuna species of the genus Thunnus (Scombridae: Teleostei): Inconsistent implications from morphology,nuclear and mitochondrial genomes

In order to infer phylogenetic relationships between tuna species of the genus Thunnus, partial sequences of the mitochondrial cytochrome b and ATPase genes were determined in all eight species. Supplemental restriction analysis on the nuclear rRNA gene was also carried out. Pacific northern bluefin tuna (Thunnus thynnus orientalis) was found to have mtDNA distinct from that of the Atlantic subspecies (T. t. thynnus) but very similar to that from the species albacore (T. alaluga). In contrast, no differentiation in nuclear genome was observed between the Atlantic and Pacific northern bluefin tunas. The Atlantic northern bluefin and southern bluefin tunas possessed mtDNA sequences very similar to species of yellowfin tuna group and not so similar to albacore and bigeye tunas which were morphologically assigned to the bluefin tuna group. The molecular data indicate that (1) mtDNA from albacore has been incorporated into the Pacific population of northern bluefin tuna and has extensively displaced the original mtDNA, and (2) albacore is the earliest offshoot, followed by bigeye tuna in this genus, which is inconsistent with the phylogenetic relationships between these tuna species inferred from morphology. Correspondence to: S. Chow     

Fish functional design and swimming performance

Classifications of fish swimming are reviewed as a prelude to discussing functional design and performance in an ecological context. Webb (1984a , 1998 ) classified fishes based on body shape and locomotor mode into three basic categories: body and caudal fin (BCF) periodic, BCF transient (fast‐starts, turns) and median and paired fin (MPF) swimmers. Swimming performance and functional design is discussed for each of these categories. Webb hypothesized that specialization in any given category would limit performance in any other. For example, routine MPF swimmers should be penalized in BCF transient (fast‐start propulsion). Recent studies offer much support for Webb's construct but also suggest some necessary amendments. In particular, design and performance compromises for different swimming modes are associated with fish that employ the same propulsor for more than one task (coupled, e.g. the same propulsor for routine steady swimming and fast‐starts). For example, pike (BCF transient specialist) achieve better acceleration performance than trout (generalist). Pike steady (BCF periodic) performance, however, is inferior to that of trout. Fish that employ different propulsors for different tasks (decoupled, e.g. MPF propulsion for low‐speed routine swimming and BCF motions for fast‐starts) do not show serious performance compromises. For example, certain MPF low‐speed swimmers show comparable fast‐start performance to BCF forms. Arguably, the evolution of decoupled locomotor systems was a major factor underlying the adaptive radiation of teleosts. Low‐speed routine propulsion releases MPF swimmers from the morphological constraints imposed by streamlining allowing for a high degree of variability in form. This contrasts with BCF periodic swimming specialists where representatives of four vertebrate classes show evolutionary convergence on a single, optimal ‘thunniform’ design. However, recent experimental studies on the comparative performance of carangiform and thunniform swimmers contradict some of the predictions of hydromechanical models. This is addressed in regard to the swimming performance, energetics and muscle physiology of tuna. The concept of gait is reviewed in the context of coupled and decoupled locomotor systems. Biomimetic approaches to the development of Autonomous Underwater Vehicles have given a new context and impetus to research and this is discussed in relation to current views of fish functional design and swimming performance. Suggestions are made for possible future research directions.     

Functional morphology of the gills of the shortfin mako,Isurus oxyrinchus,a lamnid shark

This study examines the functional gill morphology of the shortfin mako, Isurus oxyrinchus, to determine the extent to which its gill structure is convergent with that of tunas for specializations required to increase gas exchange and withstand the forceful branchial flow induced by ram ventilation. Mako gill structure is also compared to that of the blue shark, Prionace glauca, an epipelagic species with lower metabolic requirements and a reduced dependence on fast, continuous swimming to ventilate the gills. The gill surface area of the mako is about one‐half that of a comparably sized tuna, but more than twice that of the blue shark and other nonlamnid shark species. Mako gills are also distinguished from those of other sharks by shorter diffusion distances and a more fully developed diagonal blood‐flow pattern through the gill lamellae, which is similar to that found in tunas. Although the mako lacks the filament and lamellar fusions of tunas and other ram‐ventilating teleosts, its gill filaments are stiffened by the elasmobranch interbranchial septum, and the lamellae appear to be stabilized by one to two vascular sacs that protrude from the lamellar surface and abut sacs of adjacent lamellae. Vasoactive agents and changes in vascular pressure potentially influence sac size, consequently effecting lamellar rigidity and both the volume and speed of water through the interlamellar channels. However, vascular sacs also occur in the blue shark, and no other structural elements of the mako gill appear specialized for ram ventilation. Rather, the basic elasmobranch gill design and pattern of branchial circulation are both conserved. Despite specializations that increase mako gill area and efficacy relative to other sharks, the basic features of the elasmobranch gill design appear to have limited selection for a larger gill surface area, and this may ultimately constrain mako aerobic performance in comparison to tunas. J. Morphol. 271:937–948, 2010. © 2010 Wiley‐Liss, Inc.     

Elevated red myotomal muscle temperatures in the most basal tuna species, Allothunnus fallai

The present study tested the hypothesis that Allothunnus fallai can elevate its slow-oxidative red myotomal muscle (RM) temperature. Measurements on 30 A. fallai (750–850 mm fork length) captured by hook and line off the coast of southern New Zealand revealed that RM temperatures are elevated by mean ± s . d . 8·1 ± 1·3° C (range 6·7–10·0° C) above the mean ± s . d . ambient sea surface temperature 15·3 ± 0·8° C (range 14·3 to 16·4° C). These data provide evidence that the vascular modifications to the central circulation of A. fallai act as a counter-current heat exchanger and that RM heat conservation is a character state present in all extant tuna species.     

Single nucleotide polymorphism discovery in albacore and Atlantic bluefin tuna provides insights into worldwide population structure

The optimal management of the commercially important, but mostly over‐exploited, pelagic tunas, albacore (Thunnus alalunga Bonn., 1788) and Atlantic bluefin tuna (BFT; Thunnus thynnus L., 1758), requires a better understanding of population structure than has been provided by previous molecular methods. Despite numerous studies of both species, their population structures remain controversial. This study reports the development of single nucleotide polymorphisms (SNPs) in albacore and BFT and the application of these SNPs to survey genetic variability across the geographic ranges of these tunas. A total of 616 SNPs were discovered in 35 albacore tuna by comparing sequences of 54 nuclear DNA fragments. A panel of 53 SNPs yielded F_ST values ranging from 0.0 to 0.050 between samples after genotyping 460 albacore collected throughout the distribution of this species. No significant heterogeneity was detected within oceans, but between‐ocean comparisons (Atlantic, Pacific and Indian oceans along with Mediterranean Sea) were significant. Additionally, a 17‐SNP panel was developed in Atlantic BFT by cross‐species amplification in 107 fish. This limited number of SNPs discriminated between samples from the two major spawning areas of Atlantic BFT (F_ST = 0.116). The SNP markers developed in this study can be used to genotype large numbers of fish without the need for standardizing alleles among laboratories.