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Ontogeny of regional endothermy in Pacific bluefin tuna (Thunnus orientalis)

Marine Biology volume 167, Article number: 133 (2020) Cite this article

Abstract

Tunas can elevate their red (slow-twitch, oxidative) skeletal muscle, visceral and cranial temperatures significantly above the ambient water temperature (Ta) with the aid of specialized blood vessels (retia mirabilia) that conserve metabolic heat. The ontogeny of this phenomenon, known as regional endothermy, was studied in young [18.5–62.5 cm fork length (FL), 71–5350 g body mass, 2–16 months of age] Pacific bluefin tuna (Thunnus orientalis). Maximal red muscle, visceral and cranial temperatures were measured in parallel with measuring red muscle mass and the size of the red muscle and visceral retia. The maximal thermal excess (maximal tissue temperature – Ta) increased from 1.1 ± 0.3 °C (mean ± SD) to 11.1 ± 3.4 °C in the red muscle, from 0.6 ± 0.3 °C to 3.5 ± 1.4 °C in the viscera and from 0.5 ± 0.4 °C to 2.0 ± 0.6 °C in the cranium in the smallest individuals compared with the largest. Thus, red muscle endothermy was well developed, but visceral and cranial endothermy were still developing, in the largest individuals studied. The scaling coefficients, relative to body mass, for total red muscle mass (0.90 ± 0.03, mean ± SE), red muscle rete (RMR) length (0.84 ± 0.06), maximum number of RMR blood vessel rows (0.43 ± 0.04) and visceral rete cross-sectional area (0.90 ± 0.08), indicated negative allometry for total red muscle mass (< 1.0) but positive allometry for the length of the red muscle retia (> 0.33) and the area of the visceral rete (> 0.67).

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Data availability

The data used to produce this manuscript may be available upon request to the corresponding author.

Abbreviations

T a :

Ambient water temperature

FL:

Fork length

T C :

Maximal cranial temperature

T RM :

Maximal red muscle temperature

T V :

Maximal visceral temperature

RMR:

Red muscle rete

SD:

Standard deviation

SE:

Standard error of the mean

T X :

Thermal excess

VR:

Visceral rete

References

  • Altringham JD, Block BA (1997) Why do tuna maintain elevated slow muscle temperatures? Power output of muscle isolated from endothermic and ectothermic fish. J Exp Biol 200:2617–2627

    CAS  PubMed  Google Scholar 

  • Bayliff WH (2001) Organization, functions, and achievements of the Inter-American Tropical Tuna Commission. Special Report 13 (page 14)

  • Barrett I, Hester FJ (1964) Body temperature of yellowfin and skipjack tunas in relation to sea surface temperature. Nature 203:96–97

    CAS  PubMed  Google Scholar 

  • Bernal D, Sepulveda C, Mathieu-Costello O, Graham JB (2003) Comparative studies of high performance swimming in sharks. I. Red muscle morphometrics, vascularization and ultrastructure. J Exp Biol 206:2831–2843

    CAS  PubMed  Google Scholar 

  • Bernal D, Brill RW, Dickson KA, Shiels HA (2017) Sharing the water column: physiological mechanisms underlying species-specific habitat use in tunas. Rev Fish Biol Fisheries 27:843–880

    Google Scholar 

  • Bestley S, Patterson TA, Hindell MA, Gunn JS (2008) Feeding ecology of wild migratory tunas revealed by archival tag records of visceral warming. J Animal Ecol 77:1223–1233

    Google Scholar 

  • Carey FG, Teal JM (1966) Heat conservation in tuna fish muscle. Proc Natl Acad Sci 56:1464–1469

    CAS  PubMed  Google Scholar 

  • Carey FG, Teal JM (1969) Regulation of body temperature by the bluefin tuna. Comp Biochem Physiol 28:205–213

    CAS  PubMed  Google Scholar 

  • Carey FG, Kanwisher JW, Stevens ED (1984) Bluefin tuna warm their viscera during digestion. J Exp Biol 109:1–20

    Google Scholar 

  • Carey FG, Teal JM, Kanwisher JW, Lawson KD (1971) Warm-bodied fish. Am Zoologist 11:137–145

    Google Scholar 

  • Clark TD, Taylor BD, Seymour RS, Ellis D, Buchanan J, Fitzgibbon QP, Frappell PB (2008) Moving with the beat: heart rate and visceral temperature of free-swimming and feeding bluefin tuna. Proc R Soc Lond B Biol Sci 275:2841–2850

    CAS  Google Scholar 

  • Clark TD, Brandt WT, Nogueira J, Rodriguez LE, Price M, Farwell CJ, Block BA (2010) Postprandial metabolism of Pacific bluefin tuna (Thunnus orientalis). J Exp Biol 213:2379–2385

    CAS  PubMed  Google Scholar 

  • Collette BB (1995) Scombridae. Atunes, bacoretas, bonitos, caballas, estorninos, melva, etc. In: Fischer W, Krupp F, Schneider W, Sommer C, Carpenter KE, Niem V (eds) Guia FAO para Identification de Especies para lo Fines de la Pesca. Pacifico Centro-Oriental. 3 Vols. FAO, Rome. pp 1521–1543

  • Collette BB, Nauen CE (1983) FAO Species Catalogue. Vol. 2. Scombrids of the world. An annotated and illustrated catalogue of tunas, mackerels, bonitos and related species known to date. Rome: FAO. FAO Fish. Synop. 125(2):137 p

  • Dickson KA (1994) Tunas as small as 207 mm fork length can elevate muscle temperatures significantly above ambient water temperature. J Exp Biol 190:79–93

    CAS  PubMed  Google Scholar 

  • Dickson JM, Dickson KA (2019) Ontogenetic change in the amount and position of slow-oxidative myotomal muscle in relationship to regional endothermy in juvenile yellowfin tuna Thunnus albacares. J Fish Biol 95:940–951

    CAS  PubMed  Google Scholar 

  • Dickson KA, Graham JB (2004) Evolution and consequences of endothermy in fishes. Physiol Biochem Zool 77:998–1018

    PubMed  Google Scholar 

  • Dickson KA, Johnson NM, Donley JM, Hoskinson JA, Hansen MW, D'Souza Tessier J (2000) Ontogenetic changes in characteristics required for endothermy in juvenile black skipjack tuna (Euthynnus lineatus). J Exp Biol 203:3077–3087

    CAS  PubMed  Google Scholar 

  • Fudge DS, Stevens ED (1996) The visceral retia mirabilia of tuna and sharks: an annotated translation and discussion of the Eschricht & Müller 1835 paper and related papers. Guelph Ichthyo Rev 4:1–53

    Google Scholar 

  • Fujioka K, Fukuda H, Furukawa S, Tei Y, Okamoto S, Ohshimo S (2018a) Habitat use and movement patterns of small (age-0) juvenile Pacific bluefin tuna (Thunnus orientalis) relative to the Kuroshio. Fish Oceanogr 27:185–198

    Google Scholar 

  • Fujioka K, Fukuda H, Tei Y, Okamoto S, Kiyofuji H, Furukawa S, Takagi J, Estess E, Farwell CJ, Fuller DW, Suzuki N, Ohshimo S, Kitagawa T (2018b) Spatial and temporal variability in the trans-Pacific migration of Pacific bluefin tuna (Thunnus orientalis) revealed by archival tags. Prog Oceanogr 162:52–65

    Google Scholar 

  • Funakoshi S, Wada K, Suzuki T (1985) Development of the rete mirabile with growth and muscle temperature in the young bluefin tuna. Bull Jpn Soc Sci Fish 51:1971–1975

    Google Scholar 

  • Furukawa S, Fujioka K, Fukuda H, Suzuki N, Tei Y, Ohshimo S (2017) Archival tagging reveals swimming depth and ambient and peritoneal cavity temperature in age-0 Pacific bluefin tuna, Thunnus orientalis, off the southern coast of Japan. Environ Biol Fish 100:35–48

    Google Scholar 

  • Graham JB, Dickson KA (1981) Physiological thermoregulation in the albacore tuna Thunnus alalunga. Physiolog Zool 54:470–486

    Google Scholar 

  • Graham JB, Dickson KA (2000) The evolution of thunniform locomotion and heat conservation in scombrid fishes: new insights based on the morphology of Allothunnus fallai. Zoolog J Linnean Soc 129:419–466

    Google Scholar 

  • Graham JB, Dickson KA (2001) Anatomical and physiological specializations for endothermy. In: Block BA, Stevens ED (eds) Tuna: Physiology, Ecology and Evolution. Academic Press, San Diego, California, pp 121–165

    Google Scholar 

  • Graham JB, Dickson KA (2004) Tuna comparative physiology. J Exp Biol 207:4015–4024

    PubMed  Google Scholar 

  • Graham JB, Koehrn FJ, Dickson KA (1983) Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion and endothermy. Can J Zool 61:2087–2096

    Google Scholar 

  • Humason GL (1979) Animal tissue techniques, 4th edn. W.H. Freeman, San Francisco

    Google Scholar 

  • Itoh T, Tsuji S, Nitta A (2003a) Migration patterns of young Pacific bluefin tuna (Thunnus orientalis) determined with archival tags. Fish Bull 101:514–534

    Google Scholar 

  • Itoh T, Tsuji S, Nitta A (2003b) Swimming depth, ambient water temperature preference, and feeding frequency of young Pacific bluefin tuna (Thunnus orientalis) determined with archival tags. Fish Bull 101:535–544

    Google Scholar 

  • Johnston IA, Brill R (1984) Thermal dependence of contractile properties of single skinned muscle fibers from Antarctic and various warm water marine fishes including skipjack tuna (Katsuwonus pelamis) and kawakawa (Euthynnus affinis). J Comp Physiol B 155:63–70

    Google Scholar 

  • Kitagawa T, Fujioka K (2017) Rapid ontogenetic shift in juvenile Pacific bluefin tuna diet. Mar Ecol Prog Ser 571:253–257

    CAS  Google Scholar 

  • Kitagawa T, Nakata H, Kimura S, Itoh T, Tsuji S, Nitta A (2000) Effect of ambient temperature on the vertical distribution and movement of Pacific bluefin tuna Thunnus thynnus orientalis. Mar Ecol Prog Ser 206:251–260

    Google Scholar 

  • Kitagawa T, Nakata H, Kimura S, Tsuji S (2001) Thermoconservation mechanisms inferred from peritoneal cavity temperature in free-swimming Pacific bluefin tuna Thunnus thynnus orientalis. Mar Ecol Prog Ser 220:253–263

    Google Scholar 

  • Kitagawa T, Kimura S, Nakata H, Yamada H (2006) Thermal adaptation of Pacific bluefin tuna Thunnus orientalis to temperate waters. Fish Sci 72:458–458

    CAS  Google Scholar 

  • Kubo T, Sakamoto W, Murata O, Kumai H (2008) Whole-body heat transfer coefficient and body temperature change of juvenile Pacific bluefin tuna Thunnus orientalis according to growth. Fish Sci 74:995–1004

    CAS  Google Scholar 

  • Linthicum DS, Carey FG (1972) Regulation of brain and eye temperatures by the bluefin tuna. Comp Biochem Physiol 43A:425–433

    Google Scholar 

  • Magnuson JJ (1973) Comparative study of adaptations for continuous swimming and hydrostatic equilibrium of scombroid and xiphoid fishes. Fish Bull 71:337–356

    Google Scholar 

  • Magnuson JJ (1978) Locomotion by scombrid fishes: hydromechanics, morphology, and behavior. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol VII. San Diego, California, pp 239–313

  • Marcinek DJ, Blackwell SB, Dewar H, Freund EV, Farwell C, Dau D, Seitz AC, Block BA (2001) Depth and muscle temperature of Pacific bluefin tuna examined with acoustic and pop-up satellite archival tags. Mar Biol 138:869–885

    Google Scholar 

  • Reglero P, Tittensor DP, Álvarez-Berastegui D, Aparicio-González A, Worm B (2014) Worldwide distributions of tuna larvae: revisiting hypotheses on environmental requirements for spawning habitats. Mar Ecol Prog Ser 501:207–224

    Google Scholar 

  • Sawada Y, Okada T, Miyashita S, Murata O, Kumai H (2005) Completion of the Pacific bluefin tuna Thunnus orientalis (Temminck et Schlegel) life cycle. Aquac Res 36:413–421

    Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schaefer KM (1985) Body temperatures in troll-caught frigate tuna, Auxis thazard. Copeia 1985:231–233

    Google Scholar 

  • Sepulveda CA, Wegner NC, Bernal D, Graham JB (2005) The red muscle morphology of the thresher sharks (family Alopiidae). J Exp Biol 208:4255–4261

    CAS  PubMed  Google Scholar 

  • Sepulveda CA, Dickson KA, Frank LR, Graham JB (2007) Cranial endothermy and a putative brain heater in the most basal tuna species, Allothunnus fallai. J Fish Biol 70:1720–1733

    Google Scholar 

  • Sepulveda CA, Dickson KA, Bernal D, Graham JB (2008) Elevated red myotomal muscle temperatures in the most basal tuna species, Allothunnus fallai. J Fish Biol 73:241–249

    Google Scholar 

  • Shimose T, Tanabe T, Chen KS, Hsu CC (2009) Age determination and growth of Pacific bluefin tuna, Thunnus orientalis, off Japan and Taiwan. Fish Res 100:134–139

    Google Scholar 

  • Shimose T, Watanabe H, Tanabe T, Kubodera T (2013) Ontogenetic diet shift of age-0 year Pacific bluefin tuna Thunnus orientalis. J Fish Biol 82:263–276

    CAS  PubMed  Google Scholar 

  • Stevens ED, Fry FEJ (1971) Brain and muscle temperatures in ocean caught and captive skipjack tuna. Comp Biochem Physiol Part A 38:203–211

    Google Scholar 

  • Stevens ED, McLeese JM (1984) Why bluefin tuna have warm tummies: temperature effect on trypsin and chymotrypsin. Am J Physiol 246:R487–R494

    CAS  PubMed  Google Scholar 

  • Temminck CJ, Schlegel H (1844) Pisces. in Fauna Japonica, sive descriptio animalium quae in itinere per Japoniam suscepto annis 1823–30 collegit, notis observationibus et adumbrationibus illustravit P. F de Siebold Parts 5–6:73–112

    Google Scholar 

  • Tsuda Y, Sakamoto W, Yamamoto S, Murata O (2012) Effect of environmental fluctuations on mortality of juvenile Pacific bluefin tuna, Thunnus orientalis, in closed life-cycle aquaculture. Aquaculture 330:142–147

    Google Scholar 

  • Wegner N, Snodgrass OE, Dewar H, Hyde JR (2015) Whole-body endothermy in a mesopelagic fish, the opah, Lampris guttatus. Science 348:786–789

    CAS  PubMed  Google Scholar 

  • Whitlock RE, Walli A, Cermeño P, Rodriguez LE, Farwell C, Block BA (2013) Quantifying energy intake in Pacific bluefin tuna (Thunnus orientalis) using the heat increment of feeding. J Exp Biol 216:4109–4123

    CAS  PubMed  Google Scholar 

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Acknowledgements

This research was supported by the Australian Government through the Australia-Japan Foundation of the Department of Foreign Affairs and Trade, the Atmosphere and Ocean Research Institute (AORI) of the University of Tokyo, Japan, the Fisheries Agency of Japan Cooperative Research Organization Program for the Promotion of International Fisheries Stock Assessment, Flinders University of South Australia, California State University Fullerton, and the United States of America National Science Foundation (NSF). Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the NSF. We would especially like to thank the Japanese fishermen, Mr. Yoshimura in Tsushima and Yoshinori Deki and Tetsushi Oki in Nakatosa, who provided the juvenile tunas for the study. We also gratefully acknowledge the assistance of Yoshinori Aoki, Shigenori Nobata, and Marty Wong in the laboratory and/or in the field. For his assistance in figure editing we would also like to acknowledge David Heinrich from Medical Illustration and Media at Flinders Medical Center. The authors would also like to thank the three anonymous reviewers whose detailed and insightful comments significantly enhanced the interpretation of the data.

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Authors and Affiliations

  1. College of Science and Engineering, Flinders University, Adelaide, South Australia, Australia

    Arif Malik & Kathryn A. Schuller

  2. Department of Biological Science, California State University, Fullerton, CA, USA

    Kathryn A. Dickson, Kristy Forsgren & Jeannette Bush

  3. National Science Foundation, Alexandria, VA, USA

    Kathryn A. Dickson

  4. International Coastal Research Center, Atmosphere and Ocean Research Institute, University of Tokyo, Otsuchi, Iwate, Japan

    Takashi Kitagawa

  5. National Research Institute of Far Seas Fisheries, Japan Fisheries Research and Education Agency, Shizuoka, Japan

    Ko Fujioka

  6. Monterey Bay Aquarium, Monterey, CA, USA

    Ethan E. Estess & Charles Farwell

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  1. Arif Malik
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Ethics approval for all live fish handling procedures was obtained from the Institutional Animal Care and Use Committee of California State University Fullerton (Protocol No. 16-R-07).

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Malik, A., Dickson, K.A., Kitagawa, T. et al. Ontogeny of regional endothermy in Pacific bluefin tuna (Thunnus orientalis). Mar Biol 167, 133 (2020). https://doi.org/10.1007/s00227-020-03753-3

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