Ontogeny of regional endothermy in Pacific bluefin tuna ( Thunnus orientalis )
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ORIGINAL PAPER
Ontogeny of regional endothermy in Pacific bluefin tuna (Thunnus orientalis) Arif Malik1 · Kathryn A. Dickson2,3 · Takashi Kitagawa4 · Ko Fujioka5 · Ethan E. Estess6 · Charles Farwell6 · Kristy Forsgren2 · Jeannette Bush2 · Kathryn A. Schuller1 Received: 11 April 2020 / Accepted: 3 August 2020 / Published online: 27 August 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020
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 ( 0.33) and the area of the visceral rete (> 0.67). Abbreviations Ta Ambient water temperature FL Fork length TC Maximal cranial temperature TRM Maximal red muscle temperature TV Maximal visceral temperature Responsible Editor: A. E. Todgham. Reviewed by D. Bernal and undisclosed experts. * Kathryn A. Schuller [email protected] 1
College of Science and Engineering, Flinders University, Adelaide, South Australia, Australia
2
Department of Biological Science, California State University, Fullerton, CA, USA
3
National Science Foundation, Alexandria, VA, USA
4
International Coastal Research Center, Atmosphere and Ocean Research Institute, University of Tokyo, Otsuchi, Iwate, Japan
5
National Research Institute of Far Seas Fisheries, Japan Fisheries Research and Education Agency, Shizuoka, Japan
6
Monterey Bay Aquarium, Monterey, CA, USA
RMR Red muscle rete SD Standard deviation SE Standard error of the mean TX Thermal excess VR Visceral rete
Introduction Regional endothermy, the ability to maintain elevated temperatures in certain regions of the body by conserving metabolically-generated heat, is unusual in fishes, having been documented only in tunas, billfishes, certain sharks and a limited number of other fish species (Carey et
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