Swimming strategy and body plan of the world's largest fish: implications for foraging efficiency and thermoregulation

Mark G Meekan,Michele Thums,Yuval Berger,Randall Davis,Lee A Fuiman

doi:10.3389/fmars.2015.00064

Abstract

The largest animals in the oceans eat prey that are orders of magnitude smaller than themselves, implying strong selection for cost-effective foraging to meet their energy demands. Whale sharks (Rhincodon typus) may be especially challenged by warm seas that elevate their metabolism and contain sparse prey resources. Using a combination of biologging and satellite tagging, we show that whale sharks use four strategies to save energy and improve foraging efficiency: 1) fixed, low power swimming, 2) constant low speed swimming, 3) gliding and 4) asymmetrical diving. These strategies increase foraging efficiency by 22 – 32% relative to swimming horizontally and resolve the energy-budget paradox of whale sharks. However, sharks in the open ocean must access food resources that reside in relatively cold waters (up to 20oC cooler than the surface) at depths of 250-500 m during the daytime, where long, slow gliding descents, continuous ram ventilation of the gills and filter-feeding could rapidly cool the circulating blood and body tissues. We suggest that whale sharks may overcome this problem through their large size and a specialized body plan that isolates highly vascularized red muscle on the dorsal surface, allowing heat to be retained near the centre of the body within a massive core of white muscle. This could allow a warm-adapted species to maintain enhanced function of organs and sensory systems while exploiting food resources in deep, cool water.

Highlights

Through convergent evolution, the three largest species of living sharks and all balaenid whales feed by sieving large volumes of sea water through specialized cranial morphology to extract planktonic and small nektonic prey (Pivorunas, 1979; Taylor et al, 1983)
Our biologging study showed that whale sharks took advantage of their negative buoyancy to incorporate periods of gliding into their descents, a pattern consistent with another study of this species (Gleiss et al, 2011b) and an energy-conservation tactic previously documented in marine mammals and birds (Williams et al, 2000; Davis et al, 2001; Gleiss et al, 2011a)
Other tactics to conserve energy revealed by biologging included asymmetrical diving and constant low speed swimming, implying strong selective pressure for cost-efficient foraging in the species

Summary

Introduction

The three largest species of living sharks and all balaenid whales feed by sieving large volumes of sea water through specialized cranial morphology to extract planktonic and small nektonic prey (Pivorunas, 1979; Taylor et al, 1983). The extreme mass of these sharks and whales and the contrasting small body mass of their food items require that they regularly consume enormous numbers of prey. This demand is especially high for endothermic cetaceans in polar seas that must allocate most of their ingested energy to maintain a core body temperature of 37◦C that may be 25–38◦C warmer than the surrounding sea water. Even though the enhanced productivity of temperate and polar seas relative to the tropics provides for the high energy demands of the great whales, there is evidence that their populations are limited by the availability of prey (Hunt, 2006). The challenge for whale sharks of meeting this higher energetic demand is amplified by the typically oligotrophic conditions of tropical and subtropical seas

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