Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Abstract

Despite long evolutionary separations, several sharks and tunas share the ability to maintain slow-twitch, aerobic red muscle (RM) warmer than ambient water. Proximate causes of RM endothermy are well understood, but ultimate causes are unclear. Two advantages often proposed are thermal niche expansion and elevated cruising speeds. The thermal niche hypothesis is generally supported, because fishes with RM endothermy often exhibit greater tolerance to broad temperature ranges. In contrast, whether fishes with RM endothermy cruise faster, and achieve any ecological benefits from doing so, remains unclear. Here, we compiled data recorded by modern animal-tracking tools for a variety of free-swimming marine vertebrates. Using phylogenetically informed allometry, we show that both cruising speeds and maximum annual migration ranges of fishes with RM endothermy are 2-3 times greater than fishes without it, and comparable to nonfish endotherms (i.e., penguins and marine mammals). The estimated cost of transport of fishes with RM endothermy is twice that of fishes without it. We suggest that the high energetic cost of RM endothermy in fishes is offset by the benefit of elevated cruising speeds, which not only increase prey encounter rates, but also enable larger-scale annual migrations and potentially greater access to seasonally available resources. marine predator | swim speed | migration | body temperature I n 1835, the British physician John Davy reported that skipjack tuna have body temperatures 10°C higher than ambient waters and considered this fish an exception to the general rule that fishes are cold-blooded (1). It is currently known that at least 14 species of tuna (family Scombridae) and five species of shark (four species in the family Lamnidae and one species in the family Alopiidae) have the ability to retain metabolic heat via vascular countercurrent heat exchangers, and to maintain the temperature of slow-twitch, aerobic red muscle (hereafter denoted RM) significantly above that of the ambient water (2-7). This "RM endothermy" (see SI Materials and Methods for terminology) in fishes represents a remarkable example of convergent evolution, because bony fishes and cartilaginous fishes diverged as long as 450 million years ago (8). In addition to elevated RM temperature, tunas and endothermic sharks share a number of morphological (e.g., medially located RM), physiological (e.g., high metabolic rates), and ecological (e.g., highly mobile and predatory lifestyle) characteristics (9).RM endothermy is an energetically expensive thermal strategy (9), and its convergent evolution indicates that the extra energetic costs incurred by RM endothermy can be outweighed by some ecological advantages. This topic has been discussed intensively, and two primary, nonmutually exclusive hypotheses have been proposed: expansion of the thermal niche and elevated cruising speeds (2). The thermal niche hypothesis states that fishes with RM endothermy can tolerate a broader range of water temperatures and, thus, can expand thei...

Is the scaling of swim speed in sharks driven by metabolism?

“…The link between metabolism and behaviour, however, is complex and remains poorly understood. In three-dimensional marine landscapes, swim speeds among fish were found to scale positively with body mass raised to a power of 0.08 [1], where highest swim speeds were among species capable of red muscle endothermy [2]. In an early theoretical study, Weihs [3] predicted fish ideal swim speeds should be proportional to body length, with recent empirical support found for this relationship [4]; however, others have predicted a scaling of movement rates of 0.16 in swimming migratory vertebrates [5].…”

“…We test our model empirically using data from 26 species tracked in the wild with the expectation that swim speed will increase with increasing body size in order to meet higher whole-body metabolism relative to gill surface area. We also argue that among sharks, variation in swim speeds may be linked with trophic level of prey types [9] such that higher swim speeds will be associated with more mobile, higher trophic-level prey species [2]. We test for potentially confounding effects using phylogenetic generalized least squares (PGLS).…”

Ecological Influences and Morphological Correlates of Resting and Maximal Metabolic Rates across Teleost Fish Species

“…Teleost fishes may provide a highly relevant model to study the aerobic capacity model for the evolution of endothermy (Bennett and Ruben 1979), given mounting evidence that multiple lineages exhibit some degree of endothermy (Block and Stevens 2001;Wegner et al 2015;Welsh and Bellwood 2012) and that elevated body temperatures translate into detectable ecological effects (Watanabe et al 2015). More generally, our results highlight that, because of their enormous range of phenotypic variation, teleosts constitute an excellent group to investigate how varying lifestyles and evolutionary pressures can ultimately give rise to an astonishing diversity in form and function.…”

“…A few fish species (e.g., some tunas, billfishes, sharks) engage in partial endothermy to maintain the temperature of certain organs at many degrees above the ambient water temperature (Block and Stevens 2001), which also results in increased activity and swimming performance (Watanabe et al 2015). These cases of endothermy in highly active pelagic predators including the recently described endothermic fish Lampis guttatus (Wegner et al 2015), in conjunction with our results showing that MMR and RMR are highly correlated, provide strong support for the aerobic capacity model in some fish lineages.…”

“…The lower and upper limits to energy expenditure, corresponding to resting and maximum metabolic rates (RMR and MMR, respectively), affect several fitness-related traits, such as maintenance-and activity-related energy requirements, locomotor capacity and home-range area (Burton et al 2011;Claireaux and Lefrancois 2007;Watanabe et al 2015), and are consequently expected to be under multiple and often antagonistic selective pressures. Although a low RMR results in reduced maintenance energy requirements, a high MMR may increase foraging rates, behavioural dominance and overall competitive ability (Killen et al 2014;Metcalfe et al 1995;Watanabe et al 2015). If so, this suggests that, in the absence of constraints, organisms should maximize their aerobic scope (i.e., the capacity to raise their level of aerobic metabolism, quantified as the difference between RMR and MMR).…”