Physical trade-offs shape the evolution of buoyancy control in sharks

Abstract

Buoyancy control is a fundamental aspect of aquatic life that has major implications for locomotor performance and ecological niche. Unlike terrestrial animals, the densities of aquatic animals are similar to the supporting fluid, thus even small changes in body density may have profound effects on locomotion. Here, we analysed the body composition (lipid versus lean tissue) of 32 shark species to study the evolution of buoyancy. Our comparative phylogenetic analyses indicate that although lean tissue displays minor positive allometry, liver volume exhibits pronounced positive allometry, suggesting that larger sharks evolved bulkier body compositions by adding lipid tissue to lean tissue rather than substituting lean for lipid tissue, particularly in the liver. We revealed a continuum of buoyancy control strategies that ranged from more buoyant sharks with larger livers in deeper ecosystems to relatively denser sharks with small livers in epipelagic habitats. Across this eco-morphological spectrum, our hydrodynamic modelling suggests that neutral buoyancy yields lower drag and more efficient steady swimming, whereas negative buoyancy may be more efficient during accelerated movements. The evolution of buoyancy control in sharks suggests that ecological and physiological factors mediate the selective pressures acting on these traits along two major gradients, body size and habitat depth.

Negative allometric growth during ontogeny in the large pelagic filter-feeding basking shark

“…This phenomenon has been observed in a variety of phylogenetic distant aquatic vertebrates such as sharks, billfishes or cetaceans but also in fossil groups such as placoderms and ichthyosaurs (summarized in Ferrón et al 2017). Additionally, in large fast swimming lamniform sharks, the compensation of lower buoyancy by increase in body size can also be reached by an increase in size of the lipid-rich liver in combination with reduction in tissue densities (Gleiss et al 2017). [As the head of lamniforms (and other fast swimming pelagic vertebrates, e.g., scombrids or dolphins) is conical, it is negligible as a lift generating structure (Thomson and Simanek 1977)].…”

First Insights Into the Fine-Scale Movements of the Sandbar Shark, Carcharhinus plumbeus

“…However, in contrast to sandbar sharks, whale sharks would continuously glide on a majority of descents. A number of factors may be responsible for these inter-specific differences in gliding behavior, including body composition (i.e., ratio lipids to lean tissue) (Gleiss et al, 2017b), morphometrics influencing lift and drag, and the increased drag incurred by smaller sharks carrying relatively large biologging tags.…”

Is the Shark Just Drifting, or Does It Take a Quick Nap?

“…Therefore, a loss of 0.1 m/sec cannot be explained by a simple gliding effect. The relatively rapid loss implies that the hydrostatic lift of the shark did not compensate for her weight once active swimming stopped, and she was not using her pectoral fins to compensate [26] [27].…”