review: analysis of the evolutionary convergence for high

Ž .Comparative Biochemistry and Physiology Part A 129 2001 695�726

ReviewReview: Analysis of the evolutionary convergence for

high performance swimming in lamnid sharks and tunas

Diego Bernala,�, Kathryn A. Dicksonb, Robert E. Shadwicka,Jeffrey B. Grahama

a Center for Marine Biotechnology and Biomedicine and Marine Biology Research Di�ision, Scripps Institution of Oceanography,UCSD, La Jolla, CA 92093-0204, USA

bDepartment of Biological Science, California State Uni�ersity, Fullerton, CA 92834-6850, USA

Received 26 September 2000; received in revised form 7 February 2001; accepted 19 February 2001

Abstract

Elasmobranchs and bony fishes have evolved independently for more than 400 million years. However, two RecentŽ . Ž .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 bodystreamlining, a shift in the position of the aerobic, red, locomotor muscle that powers sustained swimming to a more

Žanterior 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 suiteof morphological, physiological, and biochemical specializations that define ‘high-performance fishes’ have beenextensively characterized in the tunas. This review examines the convergent features of lamnid sharks and tunas in orderto gain insight into the extent that comparable environmental selection pressures have led to the independent origin ofsimilar suites of functional characteristics in these two distinctly different taxa. We propose that, despite differencesbetween teleost and elasmobranch fishes, lamnid sharks and tunas have evolved morphological and physiologicalspecializations that enhance their swimming performance relative to other sharks and most other high performancepelagic fishes. � 2001 Elsevier Science Inc. All rights reserved.

Keywords: Comparative biology; Convergence; Endothermy; Evolutionary physiology; Lamnidae; Scombridae; Sharks; Tunas

1. Introduction

�Sharks of the Family Lamnidae longfin makoŽ . Ž .Isurus paucus , shortfin mako Isurus oxyrinchus ,

Ž .white shark Carcharodon carcharias , porbeagleŽ . Žshark Lamna nasus , and salmon shark Lamna.� Žditropis and the 15 species of tunas Family

� Corresponding author. Tel.: �1-858-534-8044; fax: �1-858-534-1305.

Ž .E-mail address: [email protected] D. Bernal .

.Scombridae, tribe Thunnini are highly mobile,epipelagic predators that display evolutionaryconvergence for a number of morphological andphysiological properties. The last common ances-tor of the sharks and teleosts must have lived in

Žthe Silurian Period 410�438 million years before.present, mybp; Carroll, 1988 , and the two groups

differ considerably in many aspects of their mor-phology, physiology, and biochemistry. The lam-nid�tuna convergence is evident in both body and

Ž .caudal fin shape Fig. 1 , but also includes: modi-

1095-6433�01�$ - see front matter � 2001 Elsevier Science Inc. All rights reserved.Ž .PII: S 1 0 9 5 - 6 4 3 3 0 1 0 0 3 3 3 - 6

( )D. Bernal et al. � Comparati�e Biochemistry and Physiology Part A 129 2001 695�726696

Ž .Fig. 1. Body form comparisons of a tuna T and a lamnidŽ . Ž . Ž .shark L . a Dorsal views of a bluefin tuna Thunnus thynnus

Ž .and a shortfin mako shark Isurus oxyrinchus . Modified fromŽ . Ž .Carey and Teal 1969a,b . b Lateral view of a southern

Ž .bluefin T. maccoyii and a shortfin mako. Modified from LastŽ . Ž . Ž .and Stevens 1994 and Allen 1997 . c Lateral view of a

Ž .32-cm kawakawa Euthynnus affinis and a 95-cm shortfinmako shark with outlines of cross-sections along the body.Note the vertical ellipsoidal shape of tuna and lamnid sharkbodies throughout most of their lengths. Modified from Mag-

Ž .nuson 1970 .

fications in myotome architecture and a shift inthe position of the slow-twitch, aerobic myotomal

Ž .muscle red muscle, RM which powers sustainedswimming; modification in the vascular supply toand from the RM, eyes and brain, and viscera to

Ž .form counter-current heat exchangers retia thatconserve metabolic heat and allow temperaturesin these regions of the body to be warmer than

Ž .ambient regional endothermy ; a dependenceupon steady swimming both for hydrostatic equi-

Ž .librium lift and for forcing the ventilatory waterŽstream over the branchial surfaces ram ventila-

.tion ; enhancement of the metabolic capacity ofboth RM and the fast-twitch, glycolytic myotomal

Ž .muscle white muscle, WM through increases inaerobic and anaerobic enzyme activities at in vivotemperatures; and cardiorespiratory specializa-tions that ensure high rates of O delivery to2sustain an elevated aerobic metabolism. Whilemany pelagic fishes have specializations for cont-inuous swimming, lamnids and tunas are the onlygroups sharing a unique RM position, heat ex-changing retia that warm the RM, brain and eyes,and viscera, elevated metabolic enzyme activitiesin locomotor and cardiac muscle, relatively large

gill areas with thin secondary lamellae, andthick-walled hearts.

The objective of this review is to describe theevolutionary convergence among lamnid sharksand tunas as it is currently understood. Our ap-proach is first to summarize the unique character-istics of tunas, based on comparisons of tunaswith their sister taxa. Then, we consider how thelamnid sharks compare both to the tunas and toother sharks, and point out what additional stud-ies are needed to complete our understanding ofthe tuna�lamnid convergence. We hypothesizethat similarities between lamnid sharks and tunasare the result of comparable selection pressuresimposed by ecological conditions and hydrody-namic factors, and that the high degree of special-izations for locomotion in both groups hasproceeded by improving the force-transfer linkagebetween RM and the caudal fin, by increasing O2and metabolic fuel delivery to the RM, and bythermally enhancing RM aerobic performance.The many fundamental differences betweensharks and teleost fishes reflects their long andindependent evolutionary history. Documentationof both the manner and degree of evolutionaryconvergence between lamnid sharks and tunas,therefore, provides an opportunity to examinehow natural selection for high-performance loco-motion and endothermy has led to many of thesame functional specializations in these distantlyrelated organisms.

2. Phylogenetic relationships

2.1. Tunas

Morphological analyses reveal several charac-ter differences between the Thunnini and its sis-

Ž . Žter group the Sardini the bonitos Collette andChao, 1975; Collette, 1978; Graham and Dickson,

.2000 , and Fig. 2 shows the hypothesized phyloge-netic relationships for these two tribes. Someadditional characters that distinguish the Thun-nini from the Sardini include differences in RM

�position the bulk of RM is distributed moreanteriorly in the body and is close to the verte-

Ž .�brae i.e. more medial , the presence of vascularŽheat-exchanging retia composed of numerous

juxtaposed arterial and venous vessels perfusing.the RM , and regional endothermy. Because the

family Scombridae has been studied extensively

( )D. Bernal et al. � Comparati�e Biochemistry and Physiology Part A 129 2001 695�726 697

Fig. 2. Hypothesized phylogenetic relationships for the tunas and the bonitos of the family Scombridae. Characters defining each nodeŽ . Ž . Ž .of the tuna clade are: a posterior and lateral red muscle RM position, ectothermy; b anterior-medial RM position, modified central

Ž . Ž . Ž .circulation rete ; c epaxial lateral arteries and veins and associated retia, RM endothermy confirmed; d fronto-parietal fenestrae,Ž . Ž .carotid rete, 1st vertebra partially fused to skull; e hypaxial lateral arteries and veins and associated retia; f 1st vertebra fully fused to

Ž . Ž .the skull, reduced central rete; g visceral retia, loss of central rete; h loss of post cardinal vein. Modified from Graham and DicksonŽ .2000 .

and includes both ectothermic and endothermicspecies, hypotheses about the evolutionary se-quence of events leading to the origin ofendothermy and other specializations have been

Žexplored in a phylogenetic context Block and.Finnerty, 1994; Graham and Dickson, 2000 .

Fig. 2 shows the monotypic Allothunnus fallaiŽ .slender tuna as the basal member of the Thun-nini. This is based on recent findings that Al-lothunnus has both the anterior�medial RM posi-tion typical of tunas and a central circulation thathas been modified to form a rete-like structureŽ .Graham and Dickson, 2000 . Although Allothun-nus does not have the entire suite of circulatory

Žspecializations i.e. lateral circulation and the as-.sociated lateral vascular retia found in other

Žtunas, its two functional characters RM position.and the presence of retia place it at the basalŽ .position in the tuna clade Fig. 2 . It is unknown

if Allothunnus can maintain elevated muscle tem-peratures. If it cannot, this would suggest that theshift in RM position preceded the evolution of

Žendothermy in the tunas Graham and Dickson,.2000; see Fig. 2 .

In contrast to morphologically-based phyloge-Žnies Kishinouye, 1923; Gibbs and Collette, 1967;

.Collette, 1978; Carpenter et al., 1995 , molec-

Žular-based allozymes, restriction fragment lengthpolymorphism, mitochondrial and nuclear gene

.sequences hypotheses for thunniform relation-ships differ in key respects. For example, theseindicate that Thunnus is monophyletic, but do notclarify the interrelationships of the eight species

Žin this genus Chow and Kishino, 1995; Finnerty.and Block, 1995; Alvarado-Bremer et al., 1997 .

Also, a phylogeny based on cytochrome b geneŽsequences for a subset of tuna species not includ-

.ing A. fallai places Thunnus in a more basalŽ .position Finnerty and Block, 1995 . Finally, no

molecular study has included all the tuna species,and analysis of cytochrome b sequences may notadequately resolve this level of phylogenetic rela-

Žtionship Chow and Kishino, 1995; Alvarado-.Bremer et al., 1997 . For these reasons, we adopt

the phylogenetic hypothesis based upon morpho-Ž .logical characteristics Fig. 2 .

2.2. Lamnids

The family Lamnidae is in the Order Lamni-formes which has a fossil record extending back

Žinto the mid-Cretaceous 124�140 mybp; Com-.pagno, 1990a,b; Shirai, 1996; Naylor et al., 1997 .

Seven families of lamniform sharks are recog-


Ž .nized Compagno, 1990b; Shirai, 1996 and thereare several conflicting hypotheses of their interre-lationships. Fig. 3 illustrates the most parsi-monious and widely accepted view, based on mor-phological and gene-sequence data, which is that

Žthe monotypic Family Cetorhinidae Cetorhinus.maximus, the basking shark is sister to the Lam-

Žnidae Compagno, 1990b; Martin and Naylor,.1997; Morrisey et al., 1997; Naylor et al., 1997 .

ŽHowever, at least three families the Ce-.torhinidae, Alopiidae, and Odontaspidae have

been hypothesized to be sister to the LamnidaeŽCompagno, 1973; Maisey, 1984a,b; Compagno,1990b; Dunn and Morrissey, 1995; Long andWaggoner, 1996; Martin, 1996; Shirai, 1996;Martin and Naylor, 1997; Morrisey et al., 1997;

.Naylor et al., 1997 .Fig. 3 suggests that the Lamnidae is mono-

phyletic, but there is no clear agreement on thephylogenetic relationships within the family

ŽCompagno, 1990b; Applegate and Espinosa-Arrubarrena, 1996; Long and Waggoner, 1996;Shirai, 1996; Martin and Naylor, 1997; Morrisey

.et al., 1997 . We adopt the view of most classifi-Ž .cations Fig. 3 which regard Isurus as the most

derived genus and consider Lamna as sister toŽIsurus�Carcharodon Compagno, 1990b; Martin,

1996; Martin and Naylor, 1997; Morrisey et al.,.1997 .

All lamnid sharks have an anterior and medialRM position, heat-exchanging retia, and are en-

Ž .dothermic Carey et al., 1985 . Unlike the Scom-bridae, the Lamnidae does not contain bothendothermic and ectothermic species and it istherefore more difficult to test hypotheses aboutthe evolutionary sequence of the acquisition oflocomotor and endothermy specializations. Ce-

Žtorhinus, the putative sister of the Lamnidae Fig..3 , is a large and relatively inaccessible species

that has not been well studied. Nevertheless, we

ŽFig. 3. Hypothesized phylogenetic relationships for the Order Lamniformes based on morphological characters modified from. ŽCompagno, 1990b . The genera Carcharias and Odontaspis have also been proposed as sister groups to the Cetorhinidae basking

. Ž .shark Martin and Naylor, 1997; Morrisey et al., 1997 . Lamnid shark phylogeny based on cytochrome b sequences, and the arrowsŽ .indicate the approximate time mybp, millions of years before present of divergence of the genera estimated from a molecular clock

Ž .calibrated for the Carcharhinidae. Modified from Martin 1996 . The time of divergence of Lamna ditropis from L. nasus is unresolved.


do know that it does not share the lamnid charac-teristics of an anterior and medial RM position,vascular retia, or regional endothermy. The

Ž .thresher sharks Alopiidae , which have also beenŽ .suggested as the lamnid sister taxa Maisey, 1985 ,

do have both an anterior�medial RM placementand a lateral circulation to RM, and there is someevidence suggesting that threshers are en-

Ždothermic Carey et al., 1971; Carey, 1982b; Boneand Chubb, 1983; Goldman, personal communi-

.cation; Bernal and Sepulveda, unpublished . Iffurther research substantiates the hypothesizedphylogeny shown in Fig. 3, this would mean thatthresher-shark specializations in RM position andits vascular supply, and possibly endothermy,evolved independently within the Lamnidae andAlopiidae. However, if threshers are not en-dothermic, this would suggest, as is hypothesizedfor tunas, that the shift in RM position andmodification of its vascular supply evolved as aresult of different selection pressures not leadingdirectly to endothermy.

In summary, although it is difficult to discernthe sequence of character state changes leadingto endothermy within the Lamnidae, comparisonsof lamnids with other sharks and the elucidationof the lamnid�tuna convergence pattern illustratethe powerful selective force that hydrodynamicfactors impose on the form and function of thesedistantly related groups.

3. Evolutionary history

Available evidence suggests that tunas and lam-nid sharks both diverged from their ancestral

Ž .stocks during the early Tertiary �60 mybp , atime of relatively rapid changes in environmentalconditions. The major radiation of most of thepercomorph fishes took place at that time, andfossil tunas and more basal scombrids appear in

Ž . Ž .Eocene 38�55 mybp deposits Carroll, 1988 .Moreover, based on fossil evidence, BannikovŽ .1985 has hypothesized that the tuna�bonito di-

Ž .vergence occurred in the Paleocene 55�65 mybp .Both molecular and fossil evidence suggest an

Žearly Tertiary form of lamnid shark Martin et al.,.1992; Shirai, 1996 . At the beginning of the Ter-

tiary, a trans-equatorial belt of warm surface wa-ter dominated the ocean circulation pattern. Dur-ing the Eocene, the oceans underwent a generalcooling trend that has continued into Recent

Ž .times Berger, 1981 . Later in the Tertiary, asignificant reorganization of land mass configura-tions, including the closing of the Tethys Seawayand the northward movement of Australia, inter-rupted the equatorial circulation and establishedboth the circumpolar Antarctic Current and

Ždeep-water trans-hemispheric currents Rogers,.1993 . In addition, several physical characteristics

Žof the modern oceans e.g. basin geography,wind-driven gyre circulation, vertical and latitudi-

.nal thermal structure, and upwelling and a num-Žber of momentous biological changes e.g. the

evolutionary radiations of zooplankton, teleost.fishes, and other groups took place during that

Žtime Berger, 1981; Carroll, 1988; Berger et al.,.1989; Macdougall, 1996; Carroll, 1997 .

3.1. Tunas

Early tunas occurred in the warm Tethys SeaŽ .Bannikov, 1985 and are hypothesized to haveexpanded their distribution with the opening ofocean basins. Locomotor specializations that fa-cilitated migration to optimum foraging areas mayhave evolved in concert with ocean�basin expan-sion and development of high-latitude zones ofincreased productivity. Ocean cooling and theconcomitant need to migrate significant distancesin search of food resources and back to warmwaters for spawning have been proposed to havebeen the primary factors driving tuna radiationŽ .Graham and Dickson, 2000 . The radiation ofsome tunas into cooler water could have alsobeen a consequence of tropical compression asso-ciated with the Tertiary cooling of the oceans.

Ž .Graham and Dickson 2000 have argued thatthe anterior�medial RM position in tunas wasthe product of selection for more efficientswimming and may have evolved before en-

Ž .dothermy Fig. 2; Section 4 . With the RMlocated closer to the vertebrae and in a moreanterior position, elaboration of blood vessels toperfuse it may have led first to a central rete andthen to the origin of lateral vessels and lateralretia to enhance RM perfusion. The presence ofretia would allow heat conservation and thus theevolution of endothermy. The ability to conserveheat within the RM, and the subsequent elabora-tion of retia in the circulation to the brain andeye and to the viscera in derived tuna species, isthought to have allowed niche expansion into

Žcooler waters among some lineages Graham et


al., 1983; Block et al., 1993; Graham and Dickson,.2000 . However, the basal Allothunnus inhabits

cool waters and is an exception to this trend.

3.2. Lamnids

Although lamnid shark ecological radiation oc-Ž .curred over the past 30�40 million years Fig. 3 ,

the fossil record for lamnids is mainly limited toteeth and the evolutionary sequence of characterstate changes leading to lamnid body shape, RMposition, and endothermy is unknown. If the se-quence was similar to that postulated for tunas,then changes in body shape and shifts in RMposition would have preceded the transition toendothermy. It might also be expected, assumingendothermy allowed thermal niche expansion, thatlamnid radiation proceeded from warm to coolerwaters. However, Lamna, the most basal genus in

Ž .this family Fig. 3 , occurs in the highest latitudesand has a greater total number of retial vessels

Ž .than does the most derived lamnid genus IsurusŽCarey et al., 1985; Bernal and Sepulveda, unpub-

.lished . This suggests that lamnid endothermyoriginated in cool waters, and that the more de-rived lamnid species invaded warmer waters,which is opposite to the hypothesized scenario for

Ž .the origin of tuna endothermy see Section 5.2 .Alternatively, the ancestors of the Lamna cladecould have invaded cool waters soon after thesplit from the Isurus-Carcharodon ancestor.

4. Locomotor adaptations and swimmingbiomechanics

Tunas and lamnid sharks share the commonfeature of a requirement for continuousswimming, which likely evolved as a result ofecological changes and concomitant opportunitiesfor adaptive radiation and niche expansionŽ .Graham and Dickson, 2000 . The tuna�lamnidconvergence demonstrates that a strong selective

Ž .influence e.g. hydromechanics can lead to themodification of different body plans and charac-ter sets and result in similar morphologies inorganisms that have independently evolved amode of living requiring both continuousswimming and short-duration, high-speed burstswimming.

4.1. The influence of continuous swimming on bodyshape and other properties

Continuous swimming generates hydrodynamiclift, which overcomes negative buoyancy and thetendency to sink. This is important for both lam-nid sharks and tunas, as they are normally nega-

Žtively buoyant Magnuson, 1973, 1978; Alexander,.1993 . Continuous swimming has also led lamnid

sharks and tunas to an obligatory dependenceupon ram ventilation, a mechanism that effec-tively transfers the power requirements for pump-ing water over the gills to the body musculature,thus resulting in a diminution of the branchial

Ž .ventilatory apparatus Roberts, 1978 . MagnusonŽ .1978 calculated that the continuous-swimming-dependent functions of hydrodynamic equilibriumand ram ventilation increased total drag by afactor of 1.7 in tunas and hence required a com-parable augmentation of thrust production by themuscles used for sustained swimming.

Continuous swimming has also influenced theconvergence of many design features in both tu-nas and lamnids. Relative to other fishes, the bulkof the lamnid shark and tuna locomotor muscleoccurs in a more anterior position. This has ac-

Žcentuated body streamlining i.e. a hydrofoil or.teardrop shape that is characterized by a poste-

rior body taper which transitions to the caudal finthrough a narrow and laterally keeled caudal

Ž .peduncle Fig. 1 . Lateral keels streamline thepeduncle, reduce drag, and minimize turbulencein the water impinging on the caudal fin. Inaddition, the transverse body sections of tunasand lamnids tend towards elliptical, with the long

Ž .axis in the vertical direction Fig. 1 . This bodyŽ .profile lessens the recoil yaw response to lateral

Ž .caudal thrust Magnuson, 1978; Webb, 1998 . Thestiff, high-aspect-ratio, symmetrical or nearly sym-

Ž .metrical caudal fin Table 1 increases lift-basedthrust production while decreasing induced dragŽ .Magnuson, 1978; Reif and Weishampel, 1986 .

4.2. Swimming kinematics

Work with tunas has defined the ‘thunniform’swimming mode in which significant lateral dis-placement is restricted primarily to the caudalpeduncle and hydrofoil-like caudal fin, where the


Table 1aŽ .Caudal fin aspect ratios AR of lamnid sharks and tunas

2Ž . Ž . Ž .Species Total length cm S cm A cm AR Source

LamnidsLamna ditropis 105 30.62 272 3.44 This studyŽ . Ž .salmon shark 130 3.25 Reif and Weishampel 1986

201 63.42 954 4.21 This study225 70.24 999 4.93 This study

Ž .Isurus oxyrinchus 90 2.99 Reif and Weishampel 1986Ž .shortfin mako 112 22.49 170 2.97 This study

115 27.27 238 3.10 This study122 27.55 218 3.47 This study178 43.93 469 4.11 This study

TunasŽ .Allothunnus fallai 77.6 4.69 Fierstine and Walters 1968

Ž .slender tunaŽ .Auxis thazard 35.8�43.6; n�7 6.46�7.29 Fierstine and Walters 1968

Ž .frigate tunaŽ .A. rochei 36�41; n�11 6.2�7.1 Magnuson 1978

Ž .bullet tunaŽ .Euthynnus lineatus 31.5�67; n�7 6.74�7.4 Fierstine and Walters 1968

Ž .black skipjack tunaŽ .E. affinis 34�69; n�36 5.8�7.4 Magnuson 1978

Ž .kawakawaŽ .Katsuwonus pelamis 25�82; n�31 5.7�8.1 Magnuson 1978

Ž .skipjack tunaŽ .48.1�67.9; n�16 5.53�8.36 Fierstine and Walters 1968

Ž .Thunnus albacares 28�135; n�31 5.5�7.2 Magnuson 1978Ž .yellowfin tuna

Ž .54.1�98.2; n�19 6.6�8.7 Fierstine and Walters 1968

Ž .T. obesus 48�61; n�21 5.9�6.1 Magnuson 1978Ž .bigeye tuna

Ž .T. alalunga 65.9�85; n�7 6.22�7.63 Fierstine and Walters 1968Ž .albacore tuna

Ž .T. thynnus 103 6.01 Fierstine and Walters 1968Ž .bluefin tuna

aAR calculated from S2 A�1, where S is the span and A is the surface area of one side of the caudal fin. The variability of tunaŽ .AR has been attributed to different methodologies see Magnuson, 1978 .

action of the elongated myotomes is focused toŽgenerate thrust Fierstine and Walters, 1968;

Magnuson, 1970; Westneat et al., 1993; Dewarand Graham, 1994a,b; Knower, 1998; Webb, 1998;

.Knower et al., 1999; Shadwick et al., 1999 . Ananalogous swimming motion has been inferredfor lamnid sharks, which were also classified as

Ž .‘thunniform’ swimmers by Lindsey 1978 . How-ever, this characterization is based solely on bodyand caudal fin morphology, as there are few data

Žon lamnid swimming kinematics Graham et al.,.1990 . Studies that quantify lateral displacement

in swimming lamnid sharks are needed to charac-terize their swimming kinematics and test thehypothesis that lamnids undergo less anterior lat-eral displacement relative to other sharks.

4.3. RM position and quantity

Ž .The anterior, medial RM position Fig. 4 dis-tinguishes lamnid sharks and tunas from virtuallyall other sharks and bony fishes. Only the sword-

Ž .fish Xiphiidae and the thresher sharks have aŽsomewhat similar RM placement Carey et al.,

1971; Bone and Chubb, 1983; Carey, 1990; Block,.1991; Bernal and Dickson, personal observation .

In all other species adapted for cruise swimmingŽe.g. ectothermic scombrids, carangids, and sal-

.monids , RM occurs along the horizontal midline,near the lateral edge of the body, and reaches amaximum in percentage cross-sectional area at

Žapproximately 75% of the body length Greer-


Ž . ŽFig. 4. Longitudinal red muscle RM distribution in six shortfin mako sharks Isurus oxyrinchus �, 5.2�20.6 kg, body mass, 77�125 cm. Ž . Ž .fork length, FL , a salmon shark Lamna ditropis �, 15.8 kg, 105 cm FL and yellowfin tuna Thunnus albacares � . The relative

amount of RM at different positions along the body is expressed as a proportion of the RM area at 50% FL. Values are mean�S.E.M.Ž . Ž .Yellowfin tuna data are from Ellerby et al. 2000 . Transverse sections of a shortfin mako 8.6 kg, 89 cm FL at 45% FL and an albacore

Ž .tuna Thunnus alalunga showing the medial position of RM.

.Walker and Pull, 1975; Graham et al., 1983 . Incontrast, RM is distributed between approxi-

Ž .mately 20 and 80% of fork length FL in bothtunas and lamnid sharks and reaches a maximumfraction of cross-sectional area at 40�50% FL in

Žtunas Graham et al., 1983; Ellerby et al., 2000;.Graham and Dickson, 2000 and at 40�55% FL in

Žlamnid sharks Carey et al., 1985; Bernal, unpub-. Ž .lished Fig. 4 .

Among tunas there are considerable interspeci-fic differences in the relative amount of RMŽTable 2; Kishinouye, 1923; Magnuson, 1973;

.Graham et al., 1983 . For example, in the frigateŽ . Ž .tuna Auxis thazard , bullet tuna A. rochei , and

Ž .black skipjack tuna Euthynnus lineatus , total RMŽ .mass TRMM is more than 10% of body mass,

�whereas in other tunas i.e. Katsuwonus pelamisŽ . Žskipjack tuna , Thunnus albacares yellowfin

. Ž .tuna , T. obesus bigeye tuna , and T. alalungaŽ .�albacore tuna TRMM ranges from 4.1 to 8.4%of body mass, which is similar to amounts in other

Ž .active scombrids Table 2 and see Dickson, 1995 .Tunas, however, have a lower mass-scaling coef-ficient for RM mass than do the ectothermic

Žscombrids that have been studied Graham et al.,.1983 . There is also a positive relationship

between the mean relative RM mass and meanŽrelative heart mass of scombrids Graham and

.Dickson, 2000 , a correlation that is expectedbased on the role of RM in powering sustainedswimming and that of the heart in providing O2and other metabolic substrates to the RM. Theallometric scaling of RM mass in tunas furthersuggests that the relative size of the tuna heartmay decrease with body mass, as was shown for

Ž .some species by Graham et al. 1983 .Less is known about RM amount and distribu-

tion in lamnid sharks. In Isurus oxyrinchus, theŽRM is separated from the vertebrae by WM Fig.

.4 , whereas in Lamna the RM lies deeper in theŽ . Žbody i.e. against the vertebrae Carey et al.,

. Ž .1985 . Carey et al. 1985 compared the RMŽquantities of three lamnid species C. carcharias,

.L. nasus, I. oxyrinchus by measuring the RMcross-sectional area in the vicinity of the dorsal

Ž .fin 42�46% of FL . However, these workers re-ported TRMM as a percentage of axial musclemass rather than total body mass. To express


Table 2aŽ .Relative red muscle RM mass in lamnid sharks and tunas

Ž .Species Body mass kg RM mass RM scaling coefficient Referenceb � 95% CIŽ Ž .mean% of body Mass

.mass�95% CI

LamnidsŽ .Lamna ditropis 15.89 n�1 2.6 � This study

Ž .salmon sharkŽ . Ž .L. nasus n�1 �2 � Carey et al. 1985

Ž .porbeagle sharkŽ . Ž . Ž .Carcharodon carcharias 23�297 n�3 �3�6 1.15 n�4 Carey et al. 1985

Ž . Ž .white shark 1256 n�1Isurus oxyrinchus 5.2�20.6 2�0.25 1.14�0.11 This studyŽ . Ž .shortfin mako n�6

TunasŽ .Allothunnus fallai 1.5�10.4 4.8�0.96 0.81�0.24 Graham and Dickson 2000

Ž . Ž .slender tuna n�6Ž .Auxis thazard 0.43�0.91 12.8�0.97 0.82�0.35 Graham et al. 1983

Ž . Ž .frigate tuna n�14Ž .Euthynnus lineatus 0.29�3.36 11.1�0.83 0.93�0.09 Graham et al. 1983

Ž . Ž .black skipjack tuna n�14Ž .Katsuwonus pelamis 1.09�3.57 7.3�1.06 0.66�0.23 Graham et al. 1983

Ž . Ž .skipjack tuna n�7Ž .Thunnus albacares 0.45�5.82 6.5�1.32 0.92�0.12 Graham et al. 1983

Ž . Ž .yellowfin tuna n�5Ž .T. alalunga 2.37�11.58 4.1�0.12 0.96�0.05 Graham et al. 1983

Ž . Ž .albacore tuna n�17

a Mass-specific scaling coefficient derived from the allometric equation a�M b where a is RM mass, M is body mass and b is theŽ .scaling coefficient. Values of b�1 indicate that total RM quantity increases proportionally with mass isometry , b values less than 1

indicate negative allometry and values greater than 1 indicate positive allometry. Tunas have 2�4 times more relative RM mass thanŽ .lamnids. Note that the relative RM mass of a single specimen of Carcharodon 1256 kg is twice that of other individuals studied. Also,

while tuna RM amounts show a trend towards negative allometry, lamnid RM mass scales isometrically and may even show positivescaling.

percentages in terms of total body mass, we de-termined the TRMM and RM longitudinal dis-

Ž .tribution in six I. oxyrinchus 5.2�20.6 kg andanalyzed thinner transverse body sections than

Ž .did Carey et al. 1985 . Table 2 shows that ourTRMM estimates for the six I. oxyrinchus are2%, which agrees with the results of Carey et al.Ž .1985 who estimated TRMM to be 4% of axial

Žmuscle mass the latter comprising 50% of body.mass in this species. Based on our algorithm, the

Ž .TRMM estimates of Carey et al. 1985 , ex-pressed as a percentage of body mass, are 2% forL. nasus and 3% for C. carcharias. Table 2 alsoshows that the scaling of lamnid RM mass tendstoward isometry or may even show positive al-lometry, at least over the size range of individualsthat have been analyzed.

4.4. Comparati�e myotomal structure and thepossible biomechanical ad�antages afforded by tunaand lamnid RM position

Although lamnid sharks and tunas have similarRM distributions, their myotomal�caudal fin link-age mechanics differ significantly. In tunas, RMfibers occurring within each myotome have bothanterior and posterior sites of tendinous attach-ment to the vertebral column, which span several

Ž .vertebrae Fig. 5 . These tendons, termed theŽanterior and posterior oblique tendons AOT,

.POT , transfer the RM contractile force of se-quentially activated myotomes to the vertebralcolumn in order to bend the body. Moreover, inthe posterior region of the body, the POTs

Ž .coalesce to form the great lateral tendons GLTsŽthat insert on the caudal fin Fierstine and Wal-


Fig. 5. Dorsal view of the posterior region of a yellowfin tuna� .Thunnus albacares, 43 cm FL, 3.2 kg and a shortfin mako

Ž .shark Isurus oxyrinchus, 73 cm FL, 5 kg showing the differentŽ .force-transmission mechanisms from the red muscle RM to

the caudal fin. In the tuna, the epaxial locomotor muscle onthe right side has been removed to expose the horizontalseptum. In the mako, a small portion of epaxial muscle,containing approximately half of the RM on that side of thebody has been removed, while in the left side the entireepaxial muscle has been dissected out. In tunas, the solidarrow shows the path at which a single POT�AOT complextransmits force to the vertebrae. In makos, there is no similartendon network and force-transmission is from the RM to the

Ž .tail solid arrow . Dashed arrows indicate the approximatepath of force transmission to the caudal fin; via vertebrae intunas and via the skin in the mako. See Section 4.4 for details.

ters, 1968; Koval and Butuzov, 1986; Westneat et.al., 1993; Graham and Dickson, 2000 . In lamnid

sharks, tendinous sheaths formed by fusedmyosepta insert into the thickened skin in the

Ž .caudal region Fig. 5 . Thus, the skin of lamnidsharks, as in other sharks, serves the same pur-pose as the GLTs of tunas, as it appears to be akey link in force transmission between locomotor

Žmuscle and the tail Wainwright et al., 1978; Reif.and Weishampel, 1986 .Ž .Graham and Dickson 2000 hypothesized that

the first steps in the evolutionary divergence of

tunas involved improvements in swimming effi-ciency through development of a more stream-lined body profile and a shift in RM position.Several workers have suggested that theanterior�medial RM position has advantages for

Žcruise swimming Graham et al., 1983; Westneatet al., 1993; Block and Finnerty, 1994; Altringham

.and Shadwick, 2001; Katz et al., 2001 , and thedirect connective-tissue linkage between the ante-rior RM and the caudal fin has been demon-

Žstrated Wainwright, 1983; Koval and Butuzov,.1986; Westneat et al., 1993; Knower, 1998 . The

first quantitative evidence for a performance en-hancement has only recently been obtainedŽKnower et al., 1999; Shadwick et al., 1999; Katz

. Ž .et al., 2001 . Knower et al. 1999 showed that, insteadily swimming T. albacares and K. pelamis,force within the GLT begins to rise with activa-tion of the most anteriorly located RM. Studies of

Žmuscle dynamics in K. pelamis Shadwick et al.,. Ž .1999 and T. albacares Katz et al., 2001 demon-

strated that strain in deep RM is uncoupled fromlocal body bending, which means that the wave ofmidline curvature travels along the body in ad-

Ž .vance of the wave of muscle shortening Fig. 6 .In K. pelamis, the temporal separation of RMstrain and local curvature is so pronounced that,in the mid-body region where the bulk of RMoccurs, shortening at each location is in syn-chrony with the body curvature taking place 9�10vertebral segments more posterior. The span ofthis displacement coincides with the length of thehighly elongated myotomes and the distancebetween the origin and insertion of the POTs that

Žlink RM to the vertebrae Fierstine and Walters,. Ž .1968; Westneat et al., 1993 . Katz et al. 2001

showed that the amplitude of shortening in deepRM of T. albacares is twice what local bodycurvature would predict. Furthermore, this largershortening results in a doubling of muscle poweroutput.

These findings confirm that contraction of an-terior�medial tuna RM causes body deformationmore posteriorly, rather than locally, and con-firms the hypothesis that tunas produce thrustprimarily by caudal oscillation as opposed to body

Žundulations Fierstine and Walters, 1968;.Lighthill, 1970 . A further implication of this new

insight is that shear between RM and the adja-Žcent WM which is not recruited at sustained

. Žswimming speeds must be taking place Katz et.al., 2001 . This appears to be possible because the


Ž . Ž .Fig. 6. Length changes recorded for medial red muscle RM at the 63% FL position in a 42.5-cm skipjack tuna Katsuwonus pelamis�1 Ž .swimming at 1.75 body lengths s . When values for the mildline curvature � are above 0 the midline is convex to the left, when ��0

the midline is concave to the left, and when ��0 the midline is straight. Note that the maximum muscle length is phase delayedrelative to the local body curvature and that RM contractions correspond to curvature at a more posterior position along the body; that

Ž .is, medial RM length changes at 63% FL are in phase with body curvature changes at 82% FL arrows . Modified from Shadwick et al.Ž .1999 .

medially positioned RM loin of tunas is separatedfrom the rest of the myotome by connective tissueŽ .Shadwick et al., 1999 . Thus, the biomechanical

Fig. 7. Anterior plane of a transverse body section of aŽ .salmon shark Lamna ditropis, 186 cm FL showing RM shear-

Ž .ing relative to adjacent WM. a RM and WM surfaces are inŽ .the same plane. b Manual advancement of the RM displaces

it approximately 4 cm relative to WM.

properties of tuna RM differ markedly from thosein other fishes in which peripherally positionedRM is mechanically coupled to the skin and RMshortening is phase-locked to skin strain and local

Žbody bending Coughlin et al., 1996; Shadwick et.al., 1998; Katz et al., 1999 .

Despite differences in the RM-caudal fin link-age systems of lamnid sharks and tunas, we sug-gest that the anterior�medial position of lamnidRM contributes to an enhanced swimming perfor-mance by allowing the RM to transfer contractileforce to the caudal fin. Studies of muscle activa-tion, force transmission, and body curvature dur-ing steady swimming in lamnids and other sharksare needed to test this hypothesis. While there

Ž .are presently no data, Carey et al. 1985 didreport that the RM of lamnids is partially sepa-rated from the adjacent WM and is thus free tocontract relative to the inactive WM during slow-speed swimming. Fig. 7 demonstrates the range ofRM shear that can occur in L. ditropis and thusverifies the presence of this tuna-like property.

5. Endothermy

Ž .The steady state body temperature T of mostbfishes is the same as the ambient water tempera-

Ž .ture T because water has a high heat capacityw


and all metabolically produced heat is rapidly losteither by convective transfer via the blood to thegills or by thermal conduction across the body

Ž .surface Brill et al., 1994 . The capacity for en-dothermy, defined as the capacity to conservemetabolic heat and maintain steady state T �T ,b whas evolved independently in the Lamnidae andScombridae. Regional endothermy has also been

Ždocumented in the billfishes Family Istiophori-.dae and the butterfly mackerel, Gasterochisma

Ž . Ž .melampus Family Scombridae Block, 1991 .These groups have only transformed their eyemuscles into thermogenic organs that warm the

Žbrain and eyes billfishes use the superior rectusmuscle, whereas the butterfly mackerel uses the

.lateral rectus; Block, 1986, 1987a,b .The lamnid sharks and tunas have been docu-

mented to maintain elevated T , but neither groupbhas specialized thermogenic tissues. Rather, bothgroups have the capacity to retain the metabolicheat generated by the continuous activity of theRM during swimming and thereby elevate TRMand the surrounding layers of WM, and all lamnidsharks and some tunas can also maintain the

Žtemperature of other regions of the body i.e.. Žviscera, eyes and brain above T Carey andw

Teal, 1966, 1969a,b; Linthicum and Carey, 1972;Carey et al., 1981, 1984; Block and Carey, 1985;

.Wolf et al., 1988; Stevens et al., 2000 .

5.1. Biological significance of endothermy

Rapid movement, both vertically within the wa-ter column and across thermal fronts, is a charac-

Žteristic of most endothermic fishes Carey et al.,1971, 1978; Carey and Robinson, 1981; Carey etal., 1981, 1982, 1984; Carey, 1990; Holland et al.,1990; Holts and Bedford, 1993; Holland and

.Siebert, 1994; Block et al., 1998; Brill et al., 1999 .Thus, changes in T are regularly encountered,wand the ability to conserve T while in coolerRMwater ensures a more thermally stable operatingenvironment for aerobic locomotion, as has been

Žshown in telemetry studies Carey and Lawson,.1973; Holland et al., 1992; Stevens et al., 2000 .

Similarly, vertical movements often correlate withfeeding, and the capacity to maintain T andEYET has been proposed to be a mechanism toBRAINconserve sensory and integrative functions while

Žin the cooler and darker deep water Linthicumand Carey, 1972; Block and Carey, 1985; Wolf et

.al., 1988; Block, 1991; Alexander, 1998 . The sus-

tained locomotor activity of lamnid sharks andtunas requires energy to fuel swimming, and thecapacity of some endothermic species to warmtheir visceral cavity may enhance digestion and

Žassimilation rates Carey et al., 1971, 1981, 1984;Stevens and McLeese, 1984; Dickson, 1995; Brill,

.1996; Goldman, 1997 . It has also been hypothe-sized that maintenance of elevated muscle tem-peratures allows tunas to swim faster and to re-

Žcover faster from burst activity Carey et al., 1971;Graham, 1975; Stevens and Carey, 1981; Brill,

.1996; Altringham and Block, 1997 .

5.2. Circulatory specializations for RM heatconser�ation

Ž .In almost all fishes, the dorsal aorta DA is themain conduit for systemic transport of oxygenated

Ž .blood to the myotomal muscle and other tissues ,Ž .and the post cardinal vein PCV is the principal

means whereby blood returns to the heart. Mostteleosts, including tunas, have a DA and a singlePCV occurring within the hemal arch of the ver-tebral column.

ŽMost tunas Allothunnus, Auxis, Euthynnus,.Katsuwonus, and some Thunnus species have an

enlarged hemal arch that is filled with a centralrete formed by vessels arising from the DA and

Žthe PCV Kishinouye, 1923; Graham, 1975; Gra-.ham and Dickson, 2000 . Also, all tunas except

Allothunnus amplify RM blood supply with arter-ies and veins positioned laterally, just under the

Ž .skin i.e. the lateral or subcutaneous circulationŽKishinouye, 1923; Gibbs and Collette, 1967; Gra-

.ham and Dickson, 2000 . The evolutionary trendwithin the tunas is for the reduction of the centralcirculation and a greater reliance upon the lateral

Žcirculation for RM perfusion Graham, 1975; Col-.lette, 1978; Fig. 2 . The more ancestral tunas

Ž .Auxis and Euthynnus have only epaxial lateralvessels that give rise to one lateral rete on eachside of the body, whereas the more derived tunashave both an epaxial and a hypaxial set of lateralvessels with four large lateral retia. The lateral

Ž .arteries branch from the DA Fig. 8 , proceedposterior-laterally to beneath the skin, and thenextend along the body to the caudal region, termi-nating in a commisure of the ventral and dorsal

Ž .vessels Gibbs and Collette, 1967 . The lateralveins follow the arterial path closely and rejointhe PCV near where it drains into the duct of

Ž .Cuvier Gibbs and Collette, 1967 . Four tuna


Fig. 8. Simplified comparative schematic showing vascular specializations for eye and brain endothermy in lamnid sharks and tunas.Ž . Ž .Arrows indicate the expected blood-flow direction in arteries solid, gray and veins dashed, blue . Lamnid shark diagram is

representative of Isurus oxyrinchus and Carcharodon carcharias and is missing the additional pseudobranchial rete present in bothŽ .Lamna species see Section 5.3 for details . Major differences between the lamnid shark and tuna vascular anatomy related toŽ . Ž . Ž .endothermy are: 1 unlike tunas, lamnids have a red muscle vein RMV that delivers warm blood to the brain and eyes; 2 the heat

Ž .exchanging retia of lamnids lies in close proximity to the eye, in tunas it is relatively farther away; and 3 differences in theŽ . Ž .approximate point of origin � of the lateral cutaneous arteries dashed, red . Abbreviations: APA, afferent pseudobranchial artery;

CA, cerebral artery; CR, carotid rete; CT, collecting trunks for the efferent branchial arteries; DA, dorsal aorta; EC, external carotid;EFA, efferent branchial arteries; HA, hyoidean artery; HR, hyoidean rete; IC, internal carotid; LCA, lateral cutaneous artery; LCR,lateral cutaneous rete; LCV, lateral cutaneous vein; OA, optic artery; OPA, opercular artery; OS, orbital sinus; PA, pseudobranchial

Ž .artery; PCV, post cardinal vein; PDA, paired dorsal aorta; RM, red muscle. Modified from Linthicum and Carey 1972 , Block andŽ . Ž . Ž .Carey 1985 , Wolf et al. 1988 , and Alexander 1998 .

� Ž .species Thunnus maccoyii southern bluefin tuna ,Ž .T. orientalis Pacific bluefin tuna , T. thynnus

Ž . .�Atlantic bluefin tuna , and T. alalunga , do notŽ .have a PCV and thus lack a central rete ; their

lateral veins drain directly into the duct of CuvierŽ .Gibbs and Collette, 1967 .

In many respects circulation in sharks is similarto that of teleosts. Sharks, however, have pairedŽ .right and left PCVs. Relative to other sharks,the PCVs and DA are smaller in lamnids which

also have a lateral circulation and retia that per-fuse the RM. Unlike in most tunas, however,there is no central rete in lamnids. The lateralvessel arrangement in lamnid sharks varies from a

Žsingle artery and vein in I. oxyrinchus, Carcharo-don carcharias, and Lamna ditropis; Bernal, un-

.published to an artery and two veins in LamnaŽ .nasus Burne, 1923 . The origin of the lateralŽarteries from the dorsal root of the fourth effer-

ent branchial arch with vascular connections to


.all arches; Burne, 1923; Carey and Teal, 1969aŽ .also differs from tunas i.e. arising from the DA

Ž .Fig. 8 . Similar to tunas, the lateral arteries oflamnid sharks extend along the body to near thecaudal peduncle, and the lateral veins join withthe PCVs near their point of entry into the ductof Cuvier.

There are interspecific differences among thefive lamnid shark species in both the number ofvessel rows comprising the lateral retia, andwhether they form contiguous blocks of tissue orare separated into smaller sets by perpendicularlyoriented WM fibers. Isurus paucus has the lowest

Ž .number of lateral rete arterial rows 4�6 . NextŽ .are I. oxyrinchus mean of 20 and C. carcharias

Ž . Ž .20�30; mean of 25 , followed by L. nasus 42�46Ž . Ž .and L. ditropis 60�69 Carey et al., 1985 . The

arrangement of vessel bands that form the lateralretia also differs interspecifically. In C. carcharias,and in both Lamna species, the retia form bands,ranging from 2 to 10 or more vessels, which areseparated from one another by WM fibers. In I.oxyrinchus, all the vessels in the lateral retia forma dense band extending from the lateral vessels to

Žthe RM, without intervening WM fibers Carey et.al., 1985 .

Given the lamnid phylogeny in Fig. 3, the basalcondition for lateral retia would be multiple bands

Žof vessels interspersed among WM fibers the.condition in Lamna and Carcharodon and the

derived condition would be rete vessels adjacentto one another without interspersed WM fibersŽ .the condition in Isurus . This sequence supportsthe hypothesis that the lateral vessels initiallyappeared to perfuse the anterior�medial RM andlater took on the function of heat conservation.The arrangement of rete vessels in I. oxyrinchusappears to be optimal for heat conservation be-cause of the increased surface contact betweenthe arteries and veins. Thus, the derived I.oxyrinchus should have the most effective heatexchanger among the lamnid sharks. However,the two Lamna species inhabit the coolest waters

Ž .and their T �T �T exceeds that of allx TISSUE wŽother lamnids Rhodes and Smith, 1983; Carey et

al., 1985; Bernal and Graham, personal observa-.tion . Furthermore, because the two Lamna

species have more blood-vessel rows in the lateralretia and RM positioned deeper in the body than

Ž .other lamnids, Carey et al. 1985 ranked Lamnaas having the greatest potential to elevate T .RM

ŽHence, while the more derived tunas members of

.the genus Thunnus have the greatest en-dothermic capacity and occur in cooler waters, adifferent trend occurs among the lamnid sharks,where the cool-water-dwelling Lamna is the basal

Ž .member of the group Carey et al., 1985 .

5.3. Muscle temperature and thermoregulation

Early tuna T data were obtained by insertingbŽtemperature probes thermocouples or thermis-

.tors into freshly caught fish. Resulting tempera-ture values for different tissues were graphed inrelation to surface T to indicate the magnitudewof the T . Such depictions showed the T of somex xspecies to be constant over a range of T . In thewAtlantic bluefin tuna, T varied inversely with Tx wŽi.e. T is 2�C in 30�C T and approx. 25�C in 6�Cx w

.T , which suggested physiological thermoregula-wŽtion Carey and Teal, 1966; Carey et al., 1971;

.Graham and Dickson, 2001 .Acoustic telemetry determinations of muscle

Ž .temperature T and T in free-swimming tunasm wdocumented the thermoregulatory capacity of the

ŽAtlantic bluefin Carey and Lawson, 1973; Stevens.et al., 2000 , and showed that T. obesus could

adjust rates of heat loss and gain in response toŽchanges in T Holland et al., 1992; Holland andw

.Siebert, 1994 . Laboratory studies show that, inresponse to the magnitude and direction ofchanges in T , tunas have the capacity to modu-x

Ž .late rates of heat production i.e. swimming speedŽor heat loss by presumably altering blood flow

. Žrate and retial heat-transfer efficiency Dizonand Brill, 1979; Graham and Dickson, 1981; Gra-ham, 1983; Brill et al., 1994; Dewar et al., 1994;

.Graham and Dickson, 2001 .Fig. 9 shows all of the available lamnid Tm

data, most of which were obtained from freshspecimens caught by longline or by hook and line.Lamnid T values are 4�12�C above T , butm wstressed and moribund specimens generally had a

ŽT that was close to or the same as T Careym wand Teal, 1969a; Rhodes and Smith, 1983; Blockand Carey, 1985; Carey et al., 1985; Bernal, per-

.sonal observation . Telemetry studies indicatethat, as in tunas, lamnids can also control muscle

ŽT over a range of T Carey and Teal, 1969a;x w.Carey et al., 1978, 1982; Block and Carey, 1985 ,

and work in progress has shown that steadilyswimming mako sharks can alter the rate of heatloss and heat gain in their RM when subjected to

Ž .changes in T Bernal, unpublished .w


Ž . Ž .Fig. 9. Relationship between the body temperature T and surface water temperature T in lamnid sharks. Regression equationsb wŽ . 2 Ž . Ž . 2 Ž .for Isurus oxyrinchus � 0.51 T �13.8, r �0.62, n�38 solid line ; Lamna nasus � 0.72 T �10.8, r �0.68, n�13 dashed line .w w

Ž . Ž . Ž . Ž .Other species: Lamna ditropis X , Carcharodon carcharias � . Sources: Carey and Teal 1969a , Rhodes and Smith 1983 , Block andŽ . Ž . Ž .Carey 1985 , Carey et al. 1985 , and Bernal and Graham personal observation .

5.4. Visceral endothermy

ŽAll lamnid sharks and at least five tunas T.obesus, T. alalunga, T. orientalis, T. maccoyii, and

.T. thynnus share a unique physiological trait, theŽcapacity to elevate visceral temperature Gibbs

and Collette, 1967; Carey and Lawson, 1973;Carey et al., 1984; Fudge and Stevens, 1996;

.Goldman, 1997 . Nonetheless, the two groupsdiffer in the underlying structural specializationssupporting their heat-conserving mechanisms.Tuna visceral temperature appears to increaseafter feeding, whereas lamnid T may be con-viscera

Žstant and independent of T Carey et al., 1978,w.1981, 1984; Goldman, 1997 . In each of the five

Thunnus species listed above, variable numbers ofvisceral retia form along the coeliacomesentericŽ .CM artery at points distal to the hepatic arteriesŽ . ŽFig. 10 Kishinouye, 1923; Gibbs and Collette,

.1967; Carey et al., 1984; Fudge and Stevens, 1996 .These permit heat conservation within the entirevisceral mass except regions of the liver. Althoughthe liver is outside of the heat-conserving ‘net-work’ in tunas, this organ may be warmed, either

as a result of heat transfer from the prominentŽ .blood vessels on its surface liver ‘striations’

Ž .Fudge and Stevens, 1996 , or by conductive heattransfer from the adjacent visceral organs it sur-rounds.

Telemetry records of free-swimming Atlanticbluefin tuna show that T can be approxi-STOMACHmately 6�C above T and, upon food ingestion itw

Ž .will rapidly within 12�20 h increase to as muchas 20�C above T , and then decline over the nextw

Ž20�30 h Carey and Lawson, 1973; Carey et al.,.1984 . These results suggest that stomach heat

results from processes such as increased aerobicŽmetabolism for digestion and assimilation Carey

.et al., 1984; Stevens and McLeese, 1984 . Carey etŽ .al. 1984 reported that the bluefin’s cecal mass

was the warmest visceral organ, which suggeststhat digestion and absorption in this tissue arethe primary visceral heat sources. That TSTOMACHunderwent cyclic changes in relation to feedingmay reflect the bluefin’s capacity to facultativelyadjust post-prandial visceral heat exchange or it

Žmay be an artifact of the feeding schedule. Thesewere impounded fish being held for market deliv-


Fig. 10. Simplified comparative schematic showing of vascular specializations for visceral endothermy in lamnid sharks and the derivedŽ .tunas i.e. Thunnus obesus, T. alalunga, T. maccoyii, T. orientalis and T. thynnus, see Fig. 2 . Arrows indicate the expected direction of

Ž . Ž .blood flow in the arteries solid, gray and veins dashed, blue . The color of the visceral organs indicates its relative temperature;warmer temperatures are in red and cooler temperatures in blue. Within the viscera of the most derived tunas, the individual retia areindicated by an orange circle and arrows show the organs they serve. Note that in contrast to the warm liver of lamnid sharks, the liverof tunas is not within the warm loop and is only partially warm. In lamnids, there are two shunts that may bypass the suprahepatic reteŽ .S : arterial shunt; S , venous shunt see Section 5.4. Abbreviations: C, rete serving the cecum; CA; cecum; CMA, celiaco-mesenteric1 2artery; CS, rete serving the cecum and stomach; CT, collecting trunks for the efferent branchial arteries; DA, dorsal aorta; EFA,efferent branchial arteries; HV, hepatic vein; I, intestine; L, liver; LL, left liver lobe; LM, middle liver lobe; LR, right liver lobe; LSA,lieno-gastric and spermatic arteries; S, rete serving the stomach; SIC, rete serving the spleen, intestine and part of the cecum; SHR,suprahepatic rete; SL, spleen; SP, rete serving the left ventral portion of the stomach attaching near the pylorus, ST, stomach, SV, spiral

Ž . Ž . Ž . Ž . Ž .valve. Modified from Eschricht and Muller 1835 , Burne 1923 , Kishinouye 1923 , Carey et al. 1981 , and Fudge and Stevens 1996 .¨

ery; it is possible that tunas feed more regularlyunder natural conditions and that their visceral

.temperature is more stable.Lamnid shark visceral circulation differs

markedly from that of tunas. The main arterialblood supply to the region is through the greatly

Ž .enlarged pericardial arteries PA, Fig. 10 . Thesearise from the ventral region of the third and

Žfourth efferent branchial arteries Burne, 1923;.Carey et al., 1981; Munoz-Chapuli, 1999 . The˜ ´

PAs extend posteriorly and branch to form thesuprahepatic rete, which is completely enclosedwithin a venous sinus. Prior to exiting this sinus,the rete arterial vessels coalesce to form a collect-ing trunk that sends warm blood to the visceraŽ .Fig. 10 .

Lamnid sharks also differ from tunas in thatthe principal flow to and from the viscera is

through the suprahepatic rete, a single large sys-tem that includes the liver. The circulatory pat-tern adjacent to the suprahepatic rete suggests

Žthat blood flow can be shunted around it Carey.et al., 1981 . On the arterial side, one possible

route for bypassing the rete is via the DA to therelatively reduced CM, spermatic, and lineo-

Žgastric arteries which flow into the viscera Fig..10 . On the venous side, the rete could be by-

passed via a large central channel in the hepaticsinus that empties directly into the sinus venosusŽ .Burne, 1923; Carey et al., 1981 . Carey et al.Ž .1981 described the presence of smooth musclewithin the walls of this venous vessel and sug-gested that this passage may be opened or closedin order to regulate flow to the rete. A renal rete

Ž .has been described for L. ditropis Burne, 1923 ,and recent measurements of a T of 11.4�C in thisx


Ž .region Bernal and Graham, unpublished suggesta highly effective heat-conserving function.

Lamnid visceral temperatures are significantlywarmer than T , and T values rangew STOMACH

Žfrom 4 to 14�C above T Carey et al., 1981;w.McCosker, 1987; Goldman, 1997 . In addition,

lamnid T remains continuously elevatedSTOMACHŽCarey et al., 1978, 1981; McCosker, 1987; Gold-

.man, 1997 and appears to be independent of TwŽ .Goldman, 1997 .

As in tunas, some of the lamnid visceral heatlikely results from digestive processes. Among thevisceral organs, the spiral valve has the highest TxŽCarey et al., 1981, 1985; Bernal and Graham,

.unpublished . This organ digests and assimilatesfood arriving from the stomach, has a large sizeand surface area, and may be a primary source ofheat. However, the role that this and other organsŽ .e.g. the liver play in lamnid visceral heat pro-duction is unknown.

5.5. Eye and brain endothermy

Whereas the eye and brain temperatures ofmost fishes equal T , lamnid sharks and mostwtunas species are able to maintain elevated tem-peratures in these organs through the strategicplacement of heat-exchanging retia and other

Žmodifications of the vascular supply Linthicumand Carey, 1972; Block and Carey, 1985; Wolf et

.al., 1988 .In most teleosts, the carotid arteries are the

main blood supply to the eyes and brain. In mostŽ .tunas i.e. Euthynnus, Katsuwonus, and Thunnus ,

a rete occurs on the internal carotid artery, andblood entering it is warmed on its way to the

Žbrain and eyes Linthicum and Carey, 1972; Fig..8 . These vascular specializations have not been

reported in either Allothunnus or Auxis, althoughŽ . Ž .Schaefer 1985 reported a T in the brain 3.8�CxŽ . Žand eyes 3.9�C of the frigate tuna Auxis thaz-

.ard . In the Atlantic bluefin tuna, T andEYEŽT can be 18�C above T Linthicum andBRAIN w

.Carey, 1972 . The source of heat used to warmthe brain and eyes in tunas has not been de-

Ž .termined, although Linthicum and Carey 1972suggested that heat might be generated within thecentral nervous system. Tunas lack both the spe-cialized heat-conducting RM vein of lamnid

Ž .sharks see below and Fig. 8 and the eye-musclethermogenic specializations of billfishes and Gas-

Ž .terochisma Carey, 1982a; Block, 1991 . Heat may

be conducted to the brain and eyes via the RMŽand epaxial musculature Stevens and Fry, 1971;. ŽLinthicum and Carey, 1972 . Most tunas Euthyn-

.nus, Katsuwonus, and Thunnus have largefronto-parietal foramena in their skulls, just over

Ž .the brain Gibbs and Collette, 1967 , and it hasbeen suggested that these allow conductive heattransfer from the body musculature to the brainŽ .Graham and Dickson, 2000 .

The brain-heating mechanism of lamnid sharksis well documented; they possess a specializedvessel that transports warm venous blood fromthe RM to the brain and eyes. After originatingdeep within the RM at the level of the first dorsalfin, this vessel proceeds anteriorly to merge withthe myelonal vein at about the level of the fifth

Ž .gill slit Wolf et al., 1988; Fig. 8 . The myelonalvein enters a vascular plexus in the meningealmembrane that covers the brain. This venousplexus drains through the posterior cerebral veins

Žinto a large sinus within the orbital cavity i.e. the. Ž .orbital sinus . Wolf et al. 1988 showed that

blood in the RM vein is warm. Work by BlockŽ .and Carey 1985 showed that the T ofBRAIN

lamnid sharks is approximately 3�C above T , andwrecent findings have shown a T of up to 9.4�C inx

Žthe brain of Lamna ditropis Bernal and Graham,.unpublished .

In all sharks the principal arterial supply to theeyes and brain is through the efferent hyoideanand pseudobranchial arteries. In lamnid sharks,these arteries coil extensively and run anterio-

Žmedially and enter the orbital sinus which is. Žfilled with warm venous blood Block and Carey,

1985; Alexander, 1998; Tubbesing and Block,.2000 . Within the sinus, the hyoidean artery

Žbranches into many smaller vessels the hyoidean.rete . These traverse the sinus and coalesce into

Žlarger vessels upon emergence Block and Carey,.1985; Alexander, 1998 . In all lamnids, the pseu-

dobranchial artery coils profusely within the sinusand both its diameter and wall thickness decreasesignificantly. However, a true pseudobranchial reteis not formed in Isurus or CarcharodonŽ .Alexander, 1998 , but is present in the two

ŽLamna species Alexander, 1998; Tubbesing and.Block, 2000 . The arteries exiting the orbital sinus

perfuse the eye and extra-ocular muscles withwarm blood and elevate T by an average ofEYE

Ž2.8�C above T Block and Carey, 1985; Alexan-w.der, 1998 ; a T of 12.9�C has been measured inx

Žthe eye of L. ditropis Bernal and Graham, un-


.published . In addition, the eyes receive warmblood from a tributary of the cerebral arteriesŽ .Fig. 8 , which send warmed blood to the brain

Žafter passing through the orbital sinus Block and.Carey, 1985; Alexander, 1998 .

Some workers have suggested that lamnid sharkextra-ocular eye muscles may contribute meta-

Žbolic heat to the brain and eye Wolf et al., 1988;.Alexander, 1998 . Relative to other sharks, lam-

nids have more than twice the relative extra-oc-Žular eye muscle mass comprising 50�60% of the

.total eye weight , and the extra-ocular eye mus-cles are a deep red color, suggesting high levels of

Žaerobic metabolism Wolf et al., 1988; Alexander,.1998 . It is unknown, however, if lamnid eye mus-

cles have the structural specializations for ther-mogenesis found in the eye muscles of billfishes

Žand Gasterochisma i.e. elevated densities of mito-chondria and sarcoplasmic reticulum, and de-creased amount of contractile proteins; Block,

.1986 .

6. Energetics

In this section we examine patterns of tuna andlamnid convergence in features related to sustain-ing the high level of physiological performancerequired by continuous swimming. We begin witha consideration of metabolic rates and the costsassociated with sustained and burst swimming,review the biochemical properties of the locomo-tor muscle, and then describe the cardiovascular,respiratory, and cellular adaptations for O and2metabolic fuel delivery to active tissues.

6.1. Maintenance and swimming costs: tunas

Measurement of metabolic rate in relation toswimming velocity is the most common method ofestimating swimming costs. The net cost ofswimming is the difference between the metabolicrate at a given speed and the standard metabolic

Ž .rate SMR . In fishes that never stop swimming,estimates of SMR are based on extrapolation of

˙Ž .the oxygen consumption rate VO -swimming ve-2˙locity regression to zero velocity, or on the VO of2

motionless individuals. The SMRs of smallŽ . � Ž .0.5�3.9 kg tunas kawakawa Euthynnus affinis ,

�skipjack tuna, and yellowfin tuna range from 220�1 �1 Žto 476 mg O kg h at 24�25�C Brill, 1987;2

.Dewar and Graham, 1994a . These values are

greater than those of other active fishes and 2�6times higher than that measured for 1.0�2.2-kg

Ž .sockeye salmon Oncorhynchus nerka at 20�CŽ .Brett and Glass, 1973 . At 24�C, juvenile

Ž .kawakawa tuna 0.024�0.265 kg SMRs are sig-nificantly greater than those of comparably sized

Ž .mackerel Scomber japonicus; 0.026�0.156 kgŽ .Sepulveda and Dickson, 2000 . It is commonlyheld that a high SMR reflects specializations forhigh rates of energy turnover and indicates the

Ž .presence of a greater aerobic scope. Brill 1996has argued that the high tuna SMR reflects theunderlying costs of powering the metabolic ma-chinery of the aerobic tissues, growth, andmetabolic maintenance requirements such as ad-ditional osmoregulatory costs imposed by a largegill surface area.

Tunas also have a high ‘maximum metabolicŽ .rate’ MMR . The highest MMRs to be recorded

in tunas, 2200�2700 mg O kg�1 h�1 at 24�C,2Žwere for the skipjack Gooding et al., 1981; De-.war and Graham, 1994a . There are no measure-

ments for similar-sized ectothermic scombrids.˙The tuna VO estimates are approximately three2

times those measured in comparably sized sock-Ž .eye salmon at 20�C Brett and Glass, 1973 . Brill

Ž .1996 suggested that the high MMR of tunasreflects rapid rates of somatic and gonadal growth,rapid digestive turnover, and the potential to re-cover rapidly from exhaustive exercise, all of whichmust take place simultaneously with the om-nipresent costs of aerobic swimming and mainte-nance metabolism. An energy budget analysis ofthese costs has been compiled by Korsmeyer et al.Ž .1996a .

˙Comparisons of the VO -swimming velocity2Ž .functions for skipjack 0.6�4.0 kg and yellowfin

Ž .1.1�2.2 kg tunas at 24�C with the only dataavailable for a similar-sized active, ectothermic

Ž .teleost, the sockeye salmon 1.4 kg , at 15�C indi-cate that tuna total metabolic rates are greater,but that the rate of change in metabolic rate with

Žvelocity is lower in the tunas Brett, 1965; Good-.ing et al., 1981; Dewar and Graham, 1994a . These

observations indicate that the net cost of transportŽthe energy required to move unit mass through

.unit distance for tunas is less than it is in an-other active fish, which may be attributable tomorphological adaptations for drag reduction, in-creased muscle metabolic and biomechanical ef-ficiency, endothermy, the connective-tissue link-ages between RM and the caudal fin, and other


Žfactors Fierstine and Walters, 1968; Magnuson,1973; Westneat et al., 1993; Dewar and Graham,1994a; Korsmeyer et al., 1997b; Knower et al.,

.1999; Shadwick et al., 1999 .However, the above tuna-salmon comparison is

limited because these species are phylogeneticallydivergent and were studied at different tempera-tures. Tests of the hypothesis that tunas are moreefficient swimmers as a result of their morpholog-ical and physiological specializations require com-parative metabolic studies of tunas and membersof their sister group, the bonitos, that control fortemperature, swimming velocity, and body size.The only study that compared swimming costs insimilar-sized tunas and ectothermic scombrids un-der the same conditions was done on juvenile

Ž .kawakawa 0.024�0.265 kg and chub mackerelŽ . Ž .0.026�0.156 kg Sepulveda and Dickson, 2000 .The juvenile kawakawa swam with significantlyless lateral displacement and inter-vertebralbending than did the juvenile chub mackerelŽ .Donley and Dickson, 2000 , but the average netcost of transport, and thus swimming efficiency,did not differ significantly between the two speciesŽ .Sepulveda and Dickson, 2000 . However, thekawakawa in that study did not have a large Txand it may be that differences in swimming effi-ciency appear in larger individuals.

6.2. Maintenance and swimming costs: lamnidsharks

Because lamnid sharks resemble tunas inswimming continuously and in having elevatedtissue temperatures and features suggesting high

Ž .aerobic capacity see below , they are predicted tohave a higher SMR than do other sharks. Theonly lamnid metabolic data available to test this

Ž .are for one shortfin mako shark 3.9 kg swimmingŽ .in a water tunnel 16�20�C at speeds ranging

�1 Ž �1 .from 0.21 to 0.50 body lengths s L s˙Ž .Graham et al., 1990 . Extrapolating the VO -2

swimming velocity relationship for that fish tozero velocity gives an SMR of approximately 240mg O kg�1 h�1. The few mean SMR data for2other active sharks are: 95 mg O kg�1 h�1 for2

Ž .lemon shark Negaprion bre�irostris , 0.8�1.3 kg,Ž .at 22�25�C Bushnell et al., 1989 ; 189 mg O2

�1 �1 Žkg h for scalloped hammerhead Sphyrna. Ž .lewini , 0.5�0.92 kg, at 26�C Lowe, 1998 ; 91.7 mg�1 �1 ŽO kg h for leopard shark Triakis semifasci-2

. Ž .ata , 2.2�5.8 kg, at 14�18�C Scharold et al., 1989 .

Thus, the SMR of the one mako is greater thanthat of the other sharks, and is also greater thanthe value of 129 mg O kg�1 h�1 at 25�C for a2

Ž .3.9-kg yellowfin tuna Brill, 1987 . This is the onlyevidence supporting an elevated SMR for themako and, by extension, other lamnid sharks, incomparison to ectothermic sharks.

There have been some MMR determinationsfor sharks: 100 mg O kg�1 h�1 at 10�C for 2 kg2

Ž . Žspiny dogfish Squalus acanthias Brett and. �1 �1Blackburn, 1978 ; 500 mg O kg h at 26�C2

Žfor 0.5�0.92 kg scalloped hammerheads Lowe,. �1 �11998 ; 418 mg O kg h at 25�C for a 1.6-kg2

�1 Žlemon shark swimming at 1 L s Graham et al.,. �1 �11990 ; and 167.3 mg O kg h at 14�18�C for2

2.2�5.8-kg leopard sharks swimming at maximal�1 Žsustainable speed of 0.93 L s Scharold et al.,

.1989 . MMR was not measured for the 3.9-kgŽ .mako shark studied by Graham et al. 1990 , but

˙the highest VO recorded, at a velocity of 0.3 L2s�1, was 507 mg O kg�1 h�1 at 20�C.2

˙Comparison of the VO -swimming velocity rela-2tionship for the 3.9-kg mako shark with data for

Žlemon sharks 1.5�3.4 kg at 25�C, 0.8�1.3 kg at. Ž .22�C and leopard sharks 2�6 kg at 12�18�C ,

˙shows that the rate of increase of VO with2Žvelocity is greater in the mako Graham et al.,

.1990 , indicating a greater net cost of transportand reduced swimming efficiency, which is oppo-site to what has been found in the tunas. While

˙additional swimming VO data are needed, we2predict that, on the basis of similarities in mor-phology, physiology, and continuous swimmingbehavior, additional data will show that tunas andlamnid sharks have converged on metabolicproperties such as a higher SMR, MMR, andmetabolic scope and a greater swimming effi-ciency relative to other fishes. However, BrillŽ .1996 has pointed out that other tropical, pelagic

Žspecies e.g. Coryphaena, dolphin fish, and Tetrap-.turus, marlin , share with tunas the properties of

rapid somatic and gonadal growth, which maycontribute to high MMRs. Lamnid sharks appearto remain more similar to other sharks and dis-similar to pelagic teleosts in having relatively lowgrowth rates, in maturing relatively late in life, inhaving long gestation times, and in giving birth to

Žrelatively few pups Gilbert, 1981; Cailliet et al.,1983; Stevens, 1983; Compagno, 1990a; Kohler et

.al., 1994 . Therefore, if high growth rates andhigh reproductive outputs make substantial con-tributions to the high MMRs of tunas and other


pelagic teleosts, then the MMRs of lamnids maynot be elevated to the same extent that they arein tunas relative to other teleosts. On the otherhand, because lamnid sharks are viviparous, fe-males need to supply sufficient oxygen to thedeveloping embryos during the long gestation pe-

Ž .riod �12 months , which may elevate metabolicŽ .rates Pratt and Casey, 1983; Stevens, 1983 . One

possible benefit of endothermy may be fasterembryonic growth rates, particularly in the Lamnaspecies that inhabit cool waters. Empirical dataon active metabolic rates in lamnids and othersharks are needed to test these ideas.

6.3. Anaerobic metabolism

Tunas and lamnid sharks have high burstswimming capabilities. There are accounts ofshortfin makos leaping high above the water sur-

Žface Carey and Teal, 1969a; Bernal, personal.observation and of hooked tunas quickly strip-

Žping all the line from a reel Walters and Fiers-.tine, 1964 . Exit speed of a jumping mako was

�1 Žestimated to be approximately 10 m s Carey. �1and Teal, 1969a . Burst speeds of up to 21 m s

Ž �1 .21 L s were measured in both yellowfin tunaŽ .53�98 cm and the ectothermic scombrid, Acan-

Ž . Ž .thocybium solandri wahoo 92�113 cm by Wal-Ž .ters and Fierstine 1964 .

Such high speeds can be maintained only brieflybecause burst swimming requires very rapid ATPturnover within the fast-twitch WM and is fueledby intracellular phosphagen stores and by anaer-obic glycolysis. Of all tissues, WM comprises the

Žlargest percentage of body mass in fishes Bone,.1978a, 1988 . In the shortfin mako, approximately

Ž .48% of body mass is WM Bernal, unpublishedwhereas in tunas WM ranges from 45 to 55% of

Ž .body mass Graham et al., 1983 . Compared withectothermic scombrids and other active sharks,respectively, tunas and the shortfin mako havehigher WM activities of creatine phosphokinaseŽCPK, which catalyzes the reaction creatine-phos-

.phate�ADP � creatine �ATP and lactate de-Žhydrogenase LDH, which catalyzes the reaction

pyruvate�NADH � lactate �NAD��H�, al-lowing redox balance to be maintained during

. Žanaerobiosis Dickson, 1988; Dickson et al., 1993;Dickson, 1995, 1996; Lopez and Dickson, unpub-

.lished . Thus, tunas and lamnid sharks are likelyto have unusually high capacities for anaerobic

ATP production during high-speed bursts.The metabolic consequences of burst activity

include the depletion of muscle creatine-phos-phate and glycogen, as well as the formation oflactate and protons, conditions that must be re-stored following bursts. Post-burst lactate levels

Žin tuna WM are exceptionally high up to 100.mM , and plasma lactate levels in line-caught

Ž .tunas and lamnid sharks 50 mM and 29 mMexceed values measured in other teleosts and

Žsharks Guppy et al., 1979; Hulbert et al., 1979;Wells et al., 1986; Arthur et al., 1992; Lai, unpub-

.lished; Skomal and Chase, unpublished . Themechanisms for lactate clearance following burst

Ž .activity in fishes are reviewed by Gleeson 1996Ž .and Milligan 1996 . Some lactate may diffuse

from WM and be circulated to other organs whereit is converted to pyruvate, which may then be-come an oxidative fuel. However, most WM lac-tate appears to remain in situ and is reconvertedto glycogen during recovery. For skipjack tuna,

Ž .Arthur et al. 1992 showed that in situ glycogensynthesis is the principal fate of WM lactate.These workers also measured fourfold fasterclearance rates for plasma lactate in skipjack tuna

Žcompared to salmonids Arthur et al., 1992; Milli-.gan, 1996 , but there are no data on lactate

clearance for other scombrids or other activesharks.

Whether the protons produced during anaer-obiosis remain in WM or diffuse into the plasma,their effect is to reduce pH, unless there is suffi-cient buffering. Low pH within the WM fibers candisrupt metabolic processes, and a lowered plasmapH can adversely affect a number of functions,

Ž .principally the binding of O to hemoglobin Hb .2

The WM non-bicarbonate buffering capacity oftunas is significantly greater than that of otherteleost species, including ectothermic scombrids,and correlates with the capacity of WM to pro-

Ž .duce lactate Dickson and Somero, 1987 . Thebuffering capacity of WM in the shortfin mako,while less than that in tunas, is greater than in all

Žother shark species that have been studied Dick-son et al., 1993; Grimminger and Dickson, unpub-

.lished . Because lamnid sharks have a lower WMbuffering capacity than do tunas, their burst activ-ity may cause larger excursions in intracellular

Ž .pH and blood pH Wells and Davie, 1985 . WhenŽcompared to the striped marlin Tetrapturus au-


.dax , the blood Hb�O binding affinity in the2shortfin mako was less affected by high acid loads,suggesting that mako shark Hb may be adapted to

Žmaintain function in the face of acidosis Wells.and Davie, 1985 .

6.4. Comparati�e biochemistry of RM and WM

If our hypothesis of elevated aerobic perfor-mance is correct, then the tissues supporting theelevated aerobic metabolism and swimming per-formance of both tunas and lamnid sharks shouldhave high aerobic metabolic capacities or bepresent in greater quantities. Tunas and lamnidsharks do not have greater relative amounts ofthe aerobic tissues supporting locomotion. Thepercentage of body mass comprised by the RMand heart is not consistently greater in tunas than

Žin ectothermic scombrids Graham et al., 1983;.Graham and Dickson, 2000 . Nor is the relative

amount of RM or relative heart mass of lamnidŽsharks greater than that of other sharks Carey et

al., 1985; Emery et al., 1985; Bernal et al., unpub-.lished . To assess tissue metabolic capacities, the

specific activity of several key enzymes in path-ways of energy production have been compared in

Žtunas and their closest relatives Dickson, 1988,.1995, 1996; Freund and Block, 1999 . The en-

zymes for which there are the most comparativeŽdata are citrate synthase CS, which catalyzes the

.first reaction of the Krebs citric acid cycle , anindex of aerobic capacity and mitochondrial den-sity, and LDH, an index of anaerobic capacity. At20�C, CS and LDH activities in tuna WM arehigher than in that of ectothermic scombrids,which means that even greater differences occurat in vivo temperatures. In RM, CS activity isgreater in tunas than in ectothermic scombrids

Ž .because of an elevated T Dickson, 1988, 1996 .RMŽ .Published Dickson et al., 1993 and ongoing

comparisons of enzyme activities in the shortfinmako and several ectothermic sharks support thecontention that, relative to ectothermic sharks,the mako shark has higher CS and LDH activities

Žin WM but about the same RM CS activity Bernal.and Dickson, unpublished . When estimated at in

vivo T , mako RM CS activity is greater than itRMŽis in active ectothermic sharks Bernal, unpub-

.lished .

6.5. The cardiorespiratory system

Lamnid sharks and tunas have specializationsthat enhance O transfer across the gills, increase2the quantity of O transported by the blood,2elevate the delivery rate of oxygenated blood andfuels to tissues, and facilitate the intracellulartransport of O to the mitochondria. These fea-2tures would allow both tunas and lamnid sharksto supply the continuously active, aerobic RMwith sufficient O and nutrients to sustain the2rates of ATP production and muscle contractionrequired by elevated T and continuousRMswimming.

The hearts and gills of sharks and teleostsdiffer in several ways. Shark hearts lack sympa-thetic innervation and have a contractile conusarteriosus, as opposed to the non-contractile bul-

Žbus arteriosus of teleosts Farrell and Jones, 1992;.Graham et al., 1994 . Sharks also have a more

rigid pericardial wall, a larger pericardial volume,and a pericardioperitoneal canal, structures thathave an integrated role in mechanically altering

Ž .cardiac stroke volume Lai et al., 1989, 1996 . Thehemibranchs in shark gills are medially anchoredto a central septum and take the form of elongate

Ž .straps ‘elasmobranch’ means strap gill that areŽspanned by the secondary lamellae Hughes, 1970;

.Hughes and Wright, 1970 . In sharks, the excur-rent branchial water flow exits laterally via five toseven pairs of gill slits, which are not covered byan operculum. Teleost gill filaments, by contrast,are shorter, the hemibranchs are mobile relativeto the supporting aortic arch, and excurrentbranchial flow is via a single pair of operculaŽ .Schmidt-Nielsen, 1993 .

In spite of these major differences betweensharks and teleosts, there are numerous conver-gent properties of the cardiorespiratory system inlamnid sharks and tunas. Both groups have alarger gill surface area and shorter blood�waterdiffusion distances than do most other fishesŽTable 3; Muir and Hughes, 1969; Emery and

.Szczepanski, 1986; Oikawa and Kanda, 1997 .Both groups also have diminished capacities forbranchial pumping and are dependent upon ramventilation. Tuna gills have the secondary lamel-lae fused to form a rigid sieve that both minimizesanatomical dead space and enhances the struc-tural integrity needed to withstand the constant

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Table 3ŽComparisons of cardiorespiratory parameters in tunas and lamnids, including a comparison with the most closely related ectothermic species for which data are available i.e. tunas

a.vs. other scombrids or salmonids; lamnids vs. other sharks

Character Tunas Non-tunas Tuna vs. Lamnids Non- Lamnid vs.non-tuna lamnids non-lamnid

b b c cGill surface Katsuwonus 18.4 Scomber scombrus 4.15 3�4� Carcharodon 5.1 Prionace 1.8 2�2 �1Ž . Žarea cm g pelamis Atlantic higher carcharias glauca higher

Ž . . Ž . Ž .skipjack tuna mackerel white shark blue sharkb c c� �Thunnus albacares 14.3 2 Isurus oxyrinchus 5.2 Carcharhinus 2.0

Ž . Žyellowfin tuna shortfin obscurus. Ž .mako shark dusky shark

b � � � �T. thynnus 14.3 3 3ŽPacific

.bluefin tuna� �1

Lamellar K. pelamis 0.60 S. scombrus 1.21 2� thinner I. oxyrinchus �5 Squalus acanthias 10.14 2�� Ž .epithelial Euthynnus affinis 0.60 2 4 spiny dogfish thinner

Ž .thickness kawakawa Scyliorhinus 11.27Ž .�m T. albacares 0.53 canicula

� � Ž .2 cat sharkErythrocyte K. pelamis 9.6�7.4 Oncorhynchus 16�11 C. carcharias 21�16 P. glauca 22�14

Ž � �size �m, 5 mykiss I. oxyrinchus 21�14Ž . � � � �mean length � rainbow trout 7 7

. � �width 6

Hemoglobin Auxis rochei 19.5 S. scombrus 10.3 1.5� C. carcharias 13.5 P. glauca 3�5 4��1Ž . Ž . � �g 100 ml bullet tuna 9 higher I. oxyrinchus 14.3 C. obscurus 6.2 higher

� � � �E. lineatus 18.2 7 7,8Žblack

.skipjack tunaK. pelamis 16.9T. albacares 16.5T. obesus 15.6Ž .bigeye tunaT. alaunga 16.0Ž .albacore tunaT. thynnus 19.8� �8,9

Hematocrit K. pelamis 40 S. scombrus 34 1.6� C. carcharias 36 P. glauca 15 2�Ž .% T. Albacares 35 O. tshawytscha higher I. oxyrinchus 40 C. obscurus 18 higher

� � Ž . � � � �8 chinook salmon 23 7 7� �8,10

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Ž .Table 3 Continued

Character Tunas Non-tunas Tuna vs. Lamnids Non- Lamnid vs.non-tuna lamnids non-lamnid

Oxygen T. albacares 18 Salmo gairderi �9 2� I. oxyrinchus 9 P. glauca 4 2�� Ž . � � � �carrying 11 rainbow trout higher 12 12 higher

� �capacity 11�1Ž .ml O dl2

Blood volume T. alalunga 31�132 O. mykiss 24�69 up to 2� � S. acanthias 66�79�1Ž . � � � � � �ml kg 13,14 15 higher 15

Relative K. pelamis 0.38 S. scombrus 0.18 1.6� I. oxyrinchus 0.14 S. acanthias 0.08 1.7�� ventricular T. albacares 0.29 16 higher 16 16 higher

Žmass % of T. thynnus 0.31.body mass T. maccoyii 0.29

Žsouthern.bluefin tuna

� �16Relative K. pelamis 0.03�0.06 Sarda chiliensis 0.028 3.4� I. oxyrinchus 0.02 S. acanthias 0.01 2�

Ž . � � � �atrial mass T. albacares 0.04�0.05 Pacific bonito higher 16 16 higherŽ% of body T. maccoyii 0.05 S. scombrus 0.046

. � �mass 16,17 Salmo gairderi 0.017Ž .rainbow trout� �16,17

% compacta K. pelamis 65.6 S. scombrus 43 up to 1.6� C. carcharias 36 P. glauca 17 2�� myocardium T. albacares 55.4 16 higher I. oxyrinchus 40 C. obscurus 19 higher

� � � �in ventricle T. thynnus 39.1 18 18T. maccoyii 48.5T. obesus 73.6� �16

Pericardial � � � � � I. oxyrinchus 5.4 P. glauca 4.9 1.1�� volume 12 21 higher

�1Ž .ml kgVentral aortic T. alalunga 10.8 S. gairderi 5�8 1.3� I. oxyrinchus 9.3 P. glauca 4.4 2�

� � � � � � � �blood 20 16 higher 12 19 higherpressureŽ .kPa

Mean cardiac K. pelamis 50�132 S. gairderi 15�100 1.2� I. oxyrinchus 47 T. semi- 33 1.4�output fascaiata

�1Ž � � � � Žml kg T. albacares 115 16 higher 12 leopard higher�1 . � � .min 16 shark

� �22

a Ž . Ž . Ž . Ž . Ž .References: 1, Muir and Hughes 1969 ; 2, reviewed in Hughes 1984 ; 3, Emery and Szczepanski 1986 ; 4, Oikawa and Kanda 1997 ; 5, Mathieu-Costello et al. 1992 ; 6, NashŽ . Ž . Ž . Ž . Ž . Ž . Ž .and Egginton 1993 ; 7, Emery 1986 ; 8, reviewed in Gallaugher and Farrell 1998 ; 9, reviewed in Dickson 1995 ; 10, Swift 1982 ; 11, Korsmeyer et al. 1997b ; 12, Lai et al. 1997 ;Ž . Ž . Ž . Ž . Ž . Ž . Ž .13, Brill et al. 1998 ; 14, Laurs et al. 1978 ; 15, Olson 1992 ; 16, reviewed in Farrell and Jones 1992 ; 17, Freund 1999 ; 18, Emery et al. 1985 ; 19, Abel et al. 1987 ; 20,Ž . Ž . Ž .Korsmeyer et al. 1997b ; 21, Lai unpublished ; 22, Lai et al. 1989 .

bRegression equation solved for a 1-kg fish.c Regression equation solved for a 10-kg fish.


Ž .branchial flow stream Muir and Kendall, 1968 .Even though lamnid gill lamellae are not fused,they are firmly supported by the filaments andappear to provide increased structural integrityrelative to typical teleost gills.

In comparison to other fish species, the heartsof tunas and lamnid sharks have thicker ventricu-lar walls, a greater coronary blood supply, andgreater aerobic and anaerobic enzyme activitiesŽTota et al., 1983; Emery et al., 1985; Wells andDavie, 1985; Emery, 1986; Emery and Szczepan-ski, 1986; Farrell, 1991; Farrell and Davie, 1991;Bushnell et al., 1992; Dickson et al., 1993; Dick-son, 1995, 1996; Korsmeyer et al., 1996a,b,

.1997a,b; Lai et al., 1997 . Along with billfishesand some ectothermic scombrids, tunas have someof the highest proportions of compact my-

Ž .ocardium in the ventricle Table 3 . Lamind heartshave approximately twice as much compact my-ocardium as do those of other active sharksŽ .Emery et al., 1985 , and speculations have beenmade that lamnid shark heart-fiber geometry ‘im-

Žproves ventricular pumping efficiency’ Sanchez-.Quintana and Hurle, 1987; Tota, 1999 . As might

be predicted from these heart features, the bloodpressure of lamnid sharks and tunas is higher

Žthan those of other fishes Table 3; Brill andBushnell, 1991; Korsmeyer et al., 1997a,b; Lai et

.al., 1997 .The majority of fishes respond to increases in

aerobic metabolic demand by increasing bothŽheart rate and stroke volume Lai et al., 1989;

.Farrell, 1991; Lai et al., 1997 . It has been sug-gested, however, that changes in heart beat fre-quency rather than stroke volume modulate car-

Ždiac output in tunas Farrell, 1991; Farrell et al.,. Ž1992 and lamnids C. carcharias and I.

.oxyrinchus; Emery et al., 1985 . Studies withswimming tunas have confirmed frequency modu-

Žlation of cardiac output Korsmeyer et al.,. Ž .1997a,b . However, a study by Lai et al. 1997 on

restrained makos showed that the mean strokevolume is at the high end of the range for fishesŽ .reviewed by Farrell, 1991 , that heart rate iswithin the range of other elasmobranchs, and thatneither the pharmacological inhibition of cholin-ergic tone nor the excitation of adrenergic recep-tors resulted in significant increases in heart rateto levels observed in comparably treated teleosts.Additional studies of cardiac function during ac-tivity are needed to determine if lamnid sharks

are convergent with tunas with respect to theregulation of cardiac output.

6.6. The O supply to acti�e tissues2

Sustained swimming activity requires a suffi-cient supply of O and metabolic fuels to main-2tain RM metabolism. Fishes respond to abruptchanges in O demand by increasing the volume2of blood that perfuses the working tissues. Thisoccurs through increases in cardiac output and bydiversion of a greater percentage of cardiac out-put to the active tissues.

Other adaptations, such as a high blood O2carrying capacity, allow greater oxygen supply atall times. Both tunas and lamnid sharks havehigher hematocrits and Hb concentrations than

Ždo other fishes Table 3; Carey et al., 1981; Emery,.1985, 1986; Dickson, 1995 . The erythrocytes of

most fishes are nucleated and consequently arelarger than those of mammals. Table 3 shows thatthe erythrocyte dimensions of lamnid sharks are

Žsimilar to those of the pelagic blue shark Prionace.glauca but up to 1.4 times larger than those of

Ž .four other carcharhiniform sharks Emery, 1986and approximately 2.2 times larger than those of

Ž .the skipjack tuna Mathieu-Costello et al., 1992 .Thus, to allow the erythrocytes to pass, capillarydiameters must be significantly larger in lamnidsharks, which increases the diffusion distances forO from the Hb to the mitochondrion. This may2mean that blood volume is greater in lamnidsharks, but there are no blood volume data forthese species. The larger erythrocyte size doesappear to contribute to a larger blood volume in

Ž .sharks relative to teleosts Table 3 . Despite ini-tial data indicating that tunas have an unusuallylarge blood volume, these values are comparable

Ž .to those of other teleosts Table 3 .Highly aerobic tissues have a suite of character-

istics that enhance the delivery of oxygen to cells.Tuna RM has a complex capillary-muscle fibergeometry that significantly increases the ratio ofcapillary surface area to muscle fiber volumeŽ .Mathieu-Costello et al., 1992 . RM capillary den-

Žsity the number of capillaries surrounding a given.fiber can be up to four times higher in tunas than

Ž .in other scombrids mackerels, Scomber spp.ŽBone, 1978b; Dickson, 1988; Mathieu-Costello et

.al., 1996 .RM mitochondrial volume appears to be simi-


lar in most fishes, regardless of typical activityŽ .level Block, 1991 . In teleosts and sharks, RM

mitochondrial volumes range from 28 to 35%ŽTotland et al., 1981; Block, 1991; Moyes et al.,

.1992 , and only anchovy RM and billfish eyeheater muscle have higher mitochondrial volumesŽ .45 and 63% . Tuna RM fibers do appear to havegreater mitochondrial cristae packing densities

Ž .than other aerobic muscles Moyes et al., 1992 ,but no ectothermic scombrids have been analyzedand no data exist for lamind sharks.

Ž .Myoglobin Mb facilitates the diffusion of O2from the capillary blood to its site of utilizationwithin the mitochondria, and a greater Mb con-centration indicates a potentially greater O flux2

Ž .to the mitochondria Wittenberg, 1970 . Com-pared to other fishes including other ectothermicscombrids, tunas have higher concentrations of

ŽMb in RM and cardiac tissue Dickson, 1995,.1996 . Also, the mass-specific cardiac Mb concen-

trations for Atlantic bluefin tuna increaseŽmarkedly in fish larger than 17 kg Poupa et al.,

.1981 . These features are consistent with the needto maximize O delivery to the RM fibers of2tunas which are warm and continually active.However, because tuna hearts are not warm, re-duced cardiac function in cool water has thepotential to limit the delivery of O and fuels to2RM. Thus, during sojourns into cooler water,heart function may ultimately influence tuna

Ž .swimming capacity Brill et al., 1999 . We know ofno muscle Mb data for lamnid sharks, but weexpect that these values will be higher for lamnids

Žcompared to other shark species Kryvi et al.,.1981 .

7. Summary

This review has summarized what is known andwhat remains to be learned about the remarkableconvergence in morphological, physiological, andbiochemical characteristics of tunas and lamnidsharks. We argue that this evolutionary conver-gence has been strongly influenced by hydrody-namic factors governing continuous, sustainedswimming, a fundamental feature of the naturalhistory of both groups. We emphasize the impor-tance of adopting a phylogenetic perspective tocompare the characteristics of the tunas withtheir sister taxa and those of the lamnids withtheir sister taxa.

It is evident that much less is known about theunique features of the lamnid sharks than abouthow the tunas compare with other scombrids.There are few physiological data on lamnid sharkswimming performance and energetics, and onlylimited information exists regarding lamnid sharkaerobic and anaerobic capacity. Understandinghow the anterior, medial RM of lamnid sharkstransfers contractile force to the caudal fin, com-bined with studies of lamnid swimming kinemat-ics and energetics, will test if the shift in RMposition led to improved swimming efficiency.Gaps in our knowledge also remain about sharkmuscle metabolic capacity and structural featuresinvolved in oxygen delivery, and about the influ-ence of scaling on enzyme activities and othermetabolic factors affecting swimming perfor-mance.

A complete understanding of the tuna�lamnidconvergence is also limited by the paucity of dataon the two groups’ sister taxa. Furthermore, thelack of consensus for the phylogenetic relation-ships within the Lamnidae and the order Lamni-formes and within the Scombridae and Thunniniconstrain our ability to map species characteris-tics onto phylogenies in order to test hypothesesabout the sequence of character state changesthat have led to the specializations of tunas andlamnid sharks. In addition to obtaining more datafor the various species of tunas and lamnid sharks,companion studies of the two groups’ sister taxamust be conducted. Studies of these species willlikely provide additional tests of the hypothesesdeveloped for the tuna�lamnid convergence incharacteristics related to locomotion and en-dothermy.

Acknowledgements

We thank Drs R. Rosenblatt, O. Mathieu-Costello, and N. Holland for constructive com-ments and suggestions. We also thank Dr R. Brilland an anonymous reviewer for suggestions thatimproved this paper, Sylvia Maistro, ChugeySepulveda, Gerick Bergsma, and Kenneth Gold-man for help with data collection. Support for D.Bernal was through the U.C., San Diego Fellow-ship and an NSF pre-doctoral fellowship. Thiswork was partially supported by NSF IBN 9318065,NSF IBN 9316621, NSF IBN 9604699, NSF IBN


0077502, NIH R25GM56820, and by grants fromthe University of California San Diego AcademicSenate.

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