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Temperature effects on the blood oxygen affinity in sharks

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Abstract

In fish, regional endothermy (i.e., the capacity to significantly elevate tissue temperatures above ambient via vascular heat exchangers) in the red swimming muscles (RM) has evolved only in a few marine groups (e.g., sharks: Lamnidae, Alopiidae, and teleosts Scombridae). Within these taxa, several species have also been shown to share similar physiological adaptations to enhance oxygen delivery to the working tissues. Although the hemoglobin (Hb) of most fish has a decreased affinity for oxygen with an increase in temperature, some regionally endothermic teleosts (e.g., tunas) have evolved Hbs that have a very low or even an increased affinity for oxygen with an increase in temperature. For sharks, however, blood oxygen affinities remain largely unknown. We examined the effects of temperature on the blood oxygen affinity in two pelagic species (the regionally endothermic shortfin mako shark and the ectothermic blue shark) at 15, 20, and 25 °C, and two coastal ectothermic species (the leopard shark and brown smooth-hound shark) at 10, 15, and 20 °C. Relative to the effects of temperature on the blood oxygen affinity of ectothermic sharks (e.g., blue shark), shortfin mako shark blood was less affected by an increase in temperature, a scenario similar to that documented in some of the tunas. In the shortfin mako shark, this may act to prevent premature oxygen dissociation from Hb as the blood is warmed during its passage through vascular heat exchangers. Even though the shortfin mako shark and blue shark occupy a similar niche, the effects of temperature on blood oxygen affinity in the latter more closely resembled that of the blood in the two coastal shark species examined in this study. The only exception was a small, reverse temperature effect (an increase in blood oxygen affinity with temperature) observed during the warming of the leopard shark blood under simulated arterial conditions, a finding that is likely related to the estuarine ecology of this species. Taken together, we found species-specific differences in how temperature affects blood oxygen affinity in sharks, with some similarities between the regionally endothermic sharks and several regionally endothermic teleost fishes.

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Acknowledgements

We thank S. Matern for the help with coastal sharks collection; J. Clegg, P. Siri, K. Brown, K. Briggman, and W. Borgeson for the facilities and animal care help at the BML; C. Crocker and H. Boyle for the experimental technique help; R. Kaufman, J. Poletto, and D. Cocherell for the statistical assistance; and P. Cala and J. Payne for the comments on drafts of the manuscript. We thank the three anonymous reviewers for their thoughtful comments and suggestions, which significantly improved the quality of this manuscript.

Funding

We are indebted to T. Tazo, S. Malt, J. Valdez, and T. Reposado, for logistical support. Research was funded via a BML Intercampus Travel Grant to JPR, and a Hatch grant (No. 3455-H) to JJC. This material is based in part upon work supported by the National Science Foundation under Grant Number IOS-1354593 and IOS-1354772. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation. We dedicate this work to “Grandpa” Jeff; he will be missed but not forgotten.

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Correspondence to Diego Bernal.

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Jeffrey B. Graham is permanently resting and missed.

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Bernal, D., Reid, J.P., Roessig, J.M. et al. Temperature effects on the blood oxygen affinity in sharks. Fish Physiol Biochem 44, 949–967 (2018). https://doi.org/10.1007/s10695-018-0484-2

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