Skip to main content

Metabolic biochemistry of cardiac muscle in three tuna species (bigeye, Thunnus obesus; yellowfin, T. albacares; and skipjack, Katsuwonus pelamis) with divergent ambient temperature and oxygen tolerances

Abstract

Bigeye tuna (Thunnus obesus) have much greater vertical mobility than yellowfin (T. albacares) and skipjack (Katsuwonus pelamis) tunas, due to an apparent greater tolerance of the changes in ambient temperature and oxygen occurring with depth. In an attempt to identify physiological processes (e.g., effects of temperature on cardiac function) responsible for these behavioral differences, we examined enzyme activities (at 12 °C, 17 °C, and 25 °C) of cardiac muscle in all three species. Contrary to our expectations, we found few differences and no clear explanatory patterns in maximum enzyme activities (V max ) or enzyme activity ratios. For example, citrate synthase (CS) activity was the same in bigeye and skipjack tunas, but ≈ 40% lower in yellowfin tuna, whereas carnitine palmotoyltransferase (CPT) activity in skipjack tuna was approximately double that in the other two species. The ratio of CPT to pyruvate kinase (PK) activity, a measure of the tissues’ preference for fatty acids as metabolic substrates, was the same in bigeye and yellowfin tunas, but elevated skipjack tuna. The ratios of lactate dehydrogenase (LDH) to CS activity and of PK to CS activity (anaerobic–aerobic enzyme activity ratios – taken as measures of the tissues’ ability to tolerate hypoxia) were both elevated in yellowfin tuna cardiac tissue relative to the other two species. We also found no differences in temperature sensitivity (Q10 values) when comparing cardiac enzyme activities across species, nor effects of temperature on the substrate affinity (K m ) of LDH. In sum, our results do not suggest any clear metabolic difference in the cardiac muscle that would explain the apparent greater tolerance of bigeye tuna to acute hypoxia and ambient temperature changes or their substantially greater vertical mobility.

This is a preview of subscription content, access via your institution.

Abbreviations

ATPase:

total myofibrillar ATPase activity

CPT:

carnitine palmotoyltransferase

CS:

citrate synthase

LDH:

lactate dehydrogenase

PK:

pyruvate kinase

Q10 :

change in reaction velocities per 10 °C change in temperature

Vmax :

maximum enzyme activities

References

  • J.R. Bailey D.H. Sephton W.R. Driedzic (1991) ArticleTitleImpact of an acute temperature change on performance and metabolism of pickerel (Esox niger) and eel (Anguilla rostrata) hearts Physiol. Zool. 64 697–716 Occurrence Handle1:CAS:528:DyaK3MXlsFGms7k%3D

    CAS  Google Scholar 

  • J.R. Bailey W.R. Driedzic (1993) ArticleTitleInfluence of low temperature acclimation on fate of metabolic fuels in rainbow trout (Oncorhynchus mykiss) hearts Can. J. Zool. 71 2167–2173 Occurrence Handle1:CAS:528:DyaK2cXkslyrtb8%3D

    CAS  Google Scholar 

  • R.A. Barkley W.H. Neill R.M. Gooding (1978) ArticleTitleSkipjack tuna, (Katsuwonus pelamis), habitat based on temperature and oxygen requirements Fish. Bull. 76 653–662

    Google Scholar 

  • B.W. Belman J.J. Childress (1975) ArticleTitleCirculatory adaptations to the oxygen minimum layer in the bathypelagic mysid Gnathophausia ingens Biol. Bull. 150 15–37

    Google Scholar 

  • J.M. Blank J.M. Morrissette P.S. Davie B.A. Block (2002) ArticleTitleEffects of temperature, epinepherine and Ca 2+ on the hearts of yellowfin tuna (Thunnus albacares) J. Exp. Biol. 205 1881–1888 Occurrence Handle1:CAS:528:DC%2BD38Xmt1GqsrY%3D Occurrence Handle12077164

    CAS  PubMed  Google Scholar 

  • J.M. Blank J.M. Morrrissette A.M. Landeira-Fernandez S. Blackwell T.D. Williams B.A. Block (2004) ArticleTitle In situcardiac performance of Pacific bluefin tuna hearts in response to acute temperature change J. Exp. Biol. 207 881–890 Occurrence Handle10.1242/jeb.00820 Occurrence Handle14747418

    Article  PubMed  Google Scholar 

  • R.W. Brill (1994) ArticleTitleA review of temperature and oxygen tolerance studies of tunas pertinent to fisheries oceanography, movement models and stock assessments Fish. Oceanogr. 3 204–216

    Google Scholar 

  • R.W. Brill B.A. Block C.H. Boggs K.A. Bigelow E.V. Freund D.J. Marcinek (1999) ArticleTitleHorizontal movements and depth distribution of large, adult yellowfin tuna (Thunnus albacares) near the Hawaiian Islands, recorded using ultrasonic telemetry: Implications for the physiological ecology of pelagic fishes Mar. Biol. 133 395–408 Occurrence Handle10.1007/s002270050478

    Article  Google Scholar 

  • Brill R.W. and Bushnell P.G.(2001). The cardiovascular system of tunas. In: Fish Physiology. Vol. IXX, pp. 79–120. Edited by B.A. Block and E.D. Stevens. Academic Press, San Diego

  • P.G. Bushnell R.W. Brill (1991) ArticleTitleResponses of swimming skipjack (Katsuwonus pelamis) and yellowfin (Thunnus albacares) tunas to acute hypoxia, and a model of their cardiorespiratory function Physiol. Zool. 64 887–911

    Google Scholar 

  • P.G. Bushnell R.W. Brill R.E. Bourke (1990) ArticleTitleCardiorespiratory responses of skipjack tuna, (Katsuwonus pelamis); yellowfin tuna, (Thunnus albacares); and bigeye tuna, (T. obesus), to acute reductions in ambient oxygen Can. J. Zool. 68 1857–1865 Occurrence Handle10.1139/z90-265

    Article  Google Scholar 

  • F.G. Carey J.W. Kanwisher E.D. Stevens (1984) ArticleTitleBluefin tuna warm their viscera during digestion J. Exp. Biol. 109 1–20

    Google Scholar 

  • J.J. Childress (1971) ArticleTitleRespiratory adaptations to the oxygen minimum layer in the bathypelagic mysid Gnathophausia ingens Biol. Bull. 141 109–121

    Google Scholar 

  • J.J. Childress G.N. Somero (1979) ArticleTitleDepth-related enzymic activities in muscle, brain and heart of deep-living pelagic marine teleosts Mar. Biol. 52 273–283 Occurrence Handle10.1007/BF00398141 Occurrence Handle1:CAS:528:DyaE1MXkslWqtb8%3D

    Article  CAS  Google Scholar 

  • Z.L. Coppes G.N. Somero (1990) ArticleTitleTemperature-adaptive differences between the M4 lactate dehyrogenases of stenothermal and eurythermal Sciaenid fishes J. Exp. Zool. 245 127–131

    Google Scholar 

  • L. Dagorn P. Bach E. Josse (2000) ArticleTitleMovement patterns of large bigeye tuna (Thunnus obesus) in the open ocean determined using ultrasonic telemetry Mar. Biol. 136 361–371 Occurrence Handle10.1007/s002270050694

    Article  Google Scholar 

  • K.A. Dickson (1995) ArticleTitleUnique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment Environ. Biol. Fish. 42 65–97 Occurrence Handle10.1007/BF00002352

    Article  Google Scholar 

  • Driedzic W.R.(1992). Cardiac energy metabolism. In: Fish Physiology. Vol. XII part A, pp. 219–267. Edited by W.S. Hoar, D.J. Randall and A.P. Farrell. Academic Press, San Diego

  • W.R. Driedzic T. Hart (1984) ArticleTitleRelationship between exogenous fuel availability and performance by teleost and elasmobranch hearts J. Comp. Physiol. 154 593–599 Occurrence Handle1:CAS:528:DyaL2MXptlegsg%3D%3D

    CAS  Google Scholar 

  • J.B. Graham K.A. Dickson (2001) Anatomical and physiological specializations for endothermy B.A. Block E.D. Stevens (Eds) Fish Physiology Vol.IXX. Academic Press San Diego 167–225

    Google Scholar 

  • J.E. Graves G.N. Somero (1982) ArticleTitleElectrophoretic and functional enzymic evolution in four species of eastern Pacific barracudas from different thermal environments Evolution 36 97–106 Occurrence Handle1:CAS:528:DyaL38XhtF2ms7Y%3D

    CAS  Google Scholar 

  • J.E. Graves R.H. Rosenblatt G.N. Somero (1983) ArticleTitleKinetic and electrophoretic differentiation of lactate dehyrogenase of teleosts species-pairs from the Atlantic and Pacific coasts of Panama Evolution 37 30–37 Occurrence Handle1:CAS:528:DyaL3sXhsVSqs7g%3D

    CAS  Google Scholar 

  • Grubbs R.D. and Holland K.N.(2003). Yellowfin and bigeye tuna in Hawai’i: dietary overlap, prey diversity and the trophic cost of associating with natural and man-made structures. Proceedings of the 54th Annual International Tuna Conference, Lake Arrowhead, California, 13–16 May 2003. SWFSC, NMFS, NOAA, La Jolla, CA.

  • M. Guppy W.C. Hulbert P.W. Hochachka (1979) ArticleTitleMetabolic sources of heat and power in tuna muscles. II. Enzymes and metabolic profiles J. Exp. Biol. 82 303–320 Occurrence Handle1:CAS:528:DyaL3cXjvVSrtA%3D%3D Occurrence Handle11799687

    CAS  PubMed  Google Scholar 

  • E. Hanamoto (1987) ArticleTitleEffect of oceanographic environment on bigeye tuna distribution Bull. Jpn. Soc. Fish. Oceanogr. 51 203–216

    Google Scholar 

  • P. Hochachka G.N. Somero (2002) Biochemical Adaptation Princeton University Press Princeton New Jersey

    Google Scholar 

  • W.C. Hulbert M. Guppy (1978) The tuna power plant and furnace G.D. Sharp A.E. Dizon (Eds) The Physiological Ecology of Tunas. Academic Press New York 153–174

    Google Scholar 

  • K.N. Holland R.W. Brill R.K.C. Chang (1990) ArticleTitleHorizontal and vertical movements of tunas (Thunnus spp.) associated with fish aggregating devices Fish. Bull. 88 493–507

    Google Scholar 

  • K. Holland R. Brill R. Chang J. Sibert D. Fournier (1992) ArticleTitlePhysiological and behavioral thermoregulation in bigeye tuna (Thunnus obesus) Nature 358 410–412 Occurrence Handle10.1038/358410a0 Occurrence Handle1:STN:280:By2A2M%2FivVQ%3D Occurrence Handle1641023

    Article  CAS  PubMed  Google Scholar 

  • J. Keen A.P. Farrell G.F. Tibbitts R.B. Brill (1992) ArticleTitleCardiac physiology in tunas. II. Effects of ryanodine, calcium and adrenaline on force frequency relationships in atrial strips from skipjack tuna, Katsuwonus pelamis Can. J. Zool. 70 1211–1217 Occurrence Handle1:CAS:528:DyaK3sXhvFKltw%3D%3D Occurrence Handle10.1139/z92-168

    Article  CAS  Google Scholar 

  • K.E. Korsmeyer N.C. Lai R.E. Shadwick J.B. Graham (1997) ArticleTitleOxygen transport and cardiovascular responses to exercise in the yellowfin tuna, (Thunnus albacares) J.Exp. Biol. 200 1987–1997 Occurrence Handle1:STN:280:ByiA1cbmsVI%3D Occurrence Handle9246782

    CAS  PubMed  Google Scholar 

  • Landeira A.M. -Fernandez J.M. Morrissette J.M. Blank B.A. Block (2004) ArticleTitleTemperature dependence of Ca 2+ -ATPase (SERCA2) in the ventricles of tuna and mackerel Am. J. Physiol. Intergr. Comp. Physiol. 286 R398–R404

    Google Scholar 

  • T.E. Lowe R.W. Brill K.L. Cousins (2000) ArticleTitleBlood oxygen-binding characteristics of bigeye tuna (Thunnus obesus), a high-energy-demand teleost that is tolerant of low ambient oxygen Mar. Biol. 136 1087–1098 Occurrence Handle10.1007/s002270000255

    Article  Google Scholar 

  • D.J. Marcinek S.B. Blackwell H. Dewear E.V. Freund C. Farwell D. Dau A.C. Seitz B.A. Block (2001) ArticleTitleDepth and muscle temperature of Pacific bluefin tuna examined with acoustic and pop-up satellite archival tags Mar. Biol. 138 869–885 Occurrence Handle10.1007/s002270000492

    Article  Google Scholar 

  • M. Mohri E. Hanamoto S. Takeuchi (1996) ArticleTitleOptimum water temperatures for bigeye tuna in the Indian Ocean as seen from tuna longline catches Nippon Suisan Gakkaishi 62 761–764

    Google Scholar 

  • C.D. Moyes O.A. Mathieu-Costello R.W. Brill P.W. Hochachka (1992) ArticleTitleMitochondrial metabolism of cardiac and skeletal muscles from a fast (Katsuwonus pelamis) and a slow (Cyprinus carpio) fish Can. J. Zool. 70 1246–1253 Occurrence Handle1:CAS:528:DyaK3sXhvFGlsA%3D%3D

    CAS  Google Scholar 

  • M.K. Musyl R.W. Brill C.H. Boggs D.S. Curran T.K. Kazama M.P. Seki (2003) ArticleTitleVertical movements of bigeye tuna (Thunnus obesus) associated with islands, buoys, and seamounts near the main Hawaiian Islands from archival tagging data Fish. Oceanogr. 12 152–169 Occurrence Handle10.1046/j.1365-2419.2003.00229.x

    Article  Google Scholar 

  • E.L. Nakamura (1972) Development and uses of facilities for studying tuna behavior H.E. Winn B.L. Olla (Eds) Behaviour of Marine Animals Vol2. Plenum Publishing Corporation New York 245–277

    Google Scholar 

  • W.H. Neill R.K.C. Chang A.E. Dizon (1976) ArticleTitleMagnitude and ecological implications of thermal inertia in skipjack tuna, (Katsuwonus pelamis) (Linnaeus) Environ. Biol. Fish. 1 61–80 Occurrence Handle10.1007/BF00761729

    Article  Google Scholar 

  • V.A. Pierce D.L. Crawford (1997) ArticleTitlePhylogenetic analysis of thermal acclimation of the glycolytic enzymes in the genus Fundulus. Physiol Zool. 70 597–609 Occurrence Handle1:CAS:528:DyaK2sXntlCjsbY%3D

    CAS  Google Scholar 

  • N.K. Sanders J.J. Childress (1990) ArticleTitleAdaptations to the deep-sea oxygen minimum layer: Oxygen binding by the hemocyanin of the bathypelagic mysid Gnathopsausia ingens.Dohrn Biol. Bull. 178 286–294 Occurrence Handle1:CAS:528:DyaK3MXitVeqtb0%3D

    CAS  Google Scholar 

  • K.M. Schaefer D.W. Fuller (2002) ArticleTitleMovements, behavior, and habitat selection of bigeye tuna (Thunnus obesus) in the eastern equatorial Pacific, ascertained through archival tags Fish. Bull. 100 765–788

    Google Scholar 

  • D. Sephton J. Bailey W.E. Driedzic (1990) ArticleTitleImpact of acute temperature transition on enzyme activity levels, oxygen consumption, and exogenous fuel utilization in sea raven (Hemitripterus americanus) hearts J. Comp. Physiol. 160 511–518

    Google Scholar 

  • D. Sephton W.W. Driedzic (1991) ArticleTitleEffect of acute and chronic temperature transition on enzymes of cardiac metabolism in white perch (Morone americana), yellow perch (Perca flavescens), and smallmouth bass (Micropterus dolomieui) Can. J. Zool. 69 258–262 Occurrence Handle1:CAS:528:DyaK3MXks1yrtbg%3D Occurrence Handle10.1139/z91-040

    Article  CAS  Google Scholar 

  • B.D. Sidell W.R. Driedzic D.B. Stowe I.A. Johnston (1987) ArticleTitleBiochemical correlations of power development and metabolic fuel preferenda in fish hearts Physiol. Zool. 60 221–232

    Google Scholar 

  • H.A. Shiels J.M. Blank A.P. Farrell B.A. Block (2004) ArticleTitleElectrophysiological properties of the L-type Ca 2+ current in cardiomyocytes from bluefin tuna and Pacific mackerel Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 R659–R668 Occurrence Handle1:CAS:528:DC%2BD2cXjtlKrs7k%3D Occurrence Handle14656768

    CAS  PubMed  Google Scholar 

  • H.A. Shiels E.V. Freund A.P. Farrell B.A. Block (1999) ArticleTitleThe sarcoplasmic reticulum plays a major role in isometric contraction in atrial muscle of yellowfin tuna J. Exp. Biol. 202 881–890 Occurrence Handle10069977

    PubMed  Google Scholar 

  • G.N. Somero E. Dahloff J.J. Lin (1996) Stenotherms and eurytherms: mechanisms establishing thermal optima and tolerance ranges I.A. Johnston A.F. Bennett (Eds) Animals and temperature – phenotypic and evolutionary adaptation.Society for Experimental Biology Seminar Series: 59. Cambridge University Press Cambridge 53–78

    Google Scholar 

  • P.N. Sund B. Blackburn F. Williams (1981) ArticleTitleTunas and their environment in the Pacific Ocean: A Review Oceanogr. Mar. Biol. Ann. Rev. 19 443–512

    Google Scholar 

  • S.G. Wilson M.E. Lutcavage R.W. Brill M.P. Genovese A.B. Cooper A.E. Everly (2005) ArticleTitleMovements of bluefin tuna (Thunnus thynnus) in the northwestern Atlantic Ocean recorded by pop-up satellite archival tags Mar. Biol. 146 409–423 Occurrence Handle10.1007/s00227-004-1445-0

    Article  Google Scholar 

  • H. Yang J. Velema M.S. Hedrick G.F. Tibbits C.D. Moyes (2000) ArticleTitleEvolutionary and physiological variation in cardiac troponin C in relation to thermal strategies of fish Physiol. Biochem. Zool. 73 841–849 Occurrence Handle10.1086/318095 Occurrence Handle1:CAS:528:DC%2BD3MXoslOluw%3D%3D Occurrence Handle11121357

    Article  CAS  PubMed  Google Scholar 

  • T.H. Yang N.C. Lai J.B. Graham G.N. Somero (1992) ArticleTitleRespiratory, blood, and heart enzymatic adaptations of Sebastolobus alascanus(Scorpaenidae; Teleostei) to the oxygen minimum zone: A comparative study Biol. Bull. 183 490–499 Occurrence Handle1:CAS:528:DyaK3sXht1Wgs7k%3D

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R Brill.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Swimmer, Y., McNaughton, L., Moyes, C. et al. Metabolic biochemistry of cardiac muscle in three tuna species (bigeye, Thunnus obesus; yellowfin, T. albacares; and skipjack, Katsuwonus pelamis) with divergent ambient temperature and oxygen tolerances. Fish Physiol Biochem 30, 27–35 (2004). https://doi.org/10.1007/s10695-004-5465-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-004-5465-y

Keywords

  • enzymes
  • heart
  • Scombridae