Cardiovascular Performance and Excitation-Contraction Couplng in Tuna Hearts

Stanford University, Stanford CA

Investigators

Abstract

Tunas are well known for the exceptional physiological and morphological adaptations that set this group (Thunnini, Scombridae) apart from other teleost fishes. These specializations include unique swimming kinematics, high metabolic rates, high cardiac outputs, and regional endothermy. A number of studies have demonstrated the exceptional performance of the tuna heart at the organ and tissue levels, however little is known about tuna cardiac function at the cellular level. Experiments in this project will test the hypothesis that tuna hearts have specializations in excitation-contraction (EC) coupling that underlie the enhanced performance. Cardiac performance will be examined at the molecular, cellular and organismal levels in endothermic tunas (bluefin and yellowfin) and their ectothermic relatives (mackerel and bonito). Cardiac contraction depends on the precise delivery of Ca2+ to the myofilaments, while relaxation depends on removal of Ca2+ from the cytoplasm. In heart cells of mammals and birds, the intracellular Ca2+ stores of the sarcoplasmic reticulum (SR) reduce diffusion distances and shorten the time course of Ca2+ cycling, permitting higher heart rates than in lower tetrapods. In fish, the contribution of internal and external Ca2+ stores varies with species and temperature, but no cellular studies of tuna heart performance exist. This project will address the hypothesis that the high maximal heart rates of tunas are achieved in part by increased reliance on intracellular SR stores and increased calcium-induced Ca2+ release during EC coupling. In addition, experimental comparisons will be made of cardiovascular function in cold and warm temperate tuna and their ectothermic sister taxa in response to acute temperature change. Such comparisons will test the hypothesis that Ca2+ cycling in yellowfin tunas, which are confined to tropical and warm temperate waters, is more temperature sensitive than in bluefin tunas. Thus, an integrative approach utilizing molecular, biochemical, structural and whole organismal physiological techniques will be employed. Whole-cell voltage-clamp techniques will be used to characterize sarcolemma Ca2+ entry via the L-type Ca 2+ current, and assess its temperature sensitivity in tunas and mackerel. Confocal microscopy will be used to visualize whole cell Ca2+ transients at different temperatures in fluo-4 loaded myocytes isolated from different species Whole organism performance as a function of temperature will be examined by measuring in situ cardiovascular performance of perfused bluefin tuna and bonito hearts. Overall this study will provide comparative data on cardiac function in fishes of the family Scombridae, and will characterize specifically the thermal relationships of voltage-sensitive Ca2+ channels, SR Ca2+ release channels, and the Ca2+ ATPase pump in heart cells from endothermic and ectothermic sister taxa. The results will increase our understanding of how teleost hearts achieve high metabolic rate and maintain function during acute temperature changes. The long-term objective is to understand the evolution of endothermy and high metabolic rate in the scombrid lineage. The proposed research also will yield insights about the role played by cardiac specializations in increasing niche breath of bluefin tuna. The research will contribute to basic knowledge about a small group of fishes that are among the most economically valuable animals on Earth. Dissemination of information from this project will occur by publications, popular articles, a website and public exhibits at the Monterey Bay Aquarium. The Tuna Research and Conservation faculty and students will provide public lectures throughout the year and contribute to efforts at the Monterey Bay Aquarium to educate the public about tuna biology and conservation.