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

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

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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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Correspondence to Kathryn A. Schuller.

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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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