Does the physiology of chondrichthyan fishes constrain their distribution in the deep sea?

Abstract

The deep sea is the largest ecosystem on Earth but organisms living there must contend with high pressure, low temperature, darkness and scarce food. Chondrichthyan fishes (sharks and their relatives) are important consumers in most marine ecosystems but are uncommon deeper than 3000 m and exceedingly rare, or quite possibly absent, from the vast abyss (depths >4000 m). By contrast, teleost (bony) fishes are commonly found to depths of ∼8400 m. Why chondrichthyans are scarce at abyssal depths is a major biogeographical puzzle. Here, after outlining the depth-related physiological trends among chondrichthyans, we discuss several existing and new hypotheses that implicate unique physiological and biochemical characteristics of chondrichthyans as potential constraints on their depth distribution. We highlight three major, and not mutually exclusive, working hypotheses: (1) the urea-based osmoregulatory strategy of chondrichthyans might conflict with the interactive effects of low temperature and high pressure on protein and membrane function at great depth; (2) the reliance on lipid accumulation for buoyancy in chondrichthyans has a unique energetic cost, which might increasingly limit growth and reproductive output as food availability decreases with depth; (3) their osmoregulatory strategy may make chondrichthyans unusually nitrogen limited, a potential liability in the food-poor abyss. These hypotheses acting in concert could help to explain the scarcity of chondrichthyans at great depths: the mechanisms of the first hypothesis may place an absolute, pressure-related depth limit on physiological function, while the mechanisms of the second and third hypotheses may limit depth distribution by constraining performance in the oligotrophic abyss, in ways that preclude the establishment of viable populations or lead to competitive exclusion by teleosts.

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

“…Alexander [10] argued that the transition from a buoyancy control strategy relying on hydrodynamic lift from the body and the pectoral fins (analogous to a fixed-wing aircraft) to one that increasingly relies on hydrostatic forces (analogous to a blimp) would accompany decreasing swimming speeds, because negative buoyancy would result in substantial increases in drag at low swimming speeds compared to neutral buoyancy. The inverse correlation between depth and buoyancy in our dataset supports this hypothesis, given the evidence that metabolic activity generally decreases with depth in a range of marine animals [19,20,44], assumed to reflect a decrease in swimming activity. Swimming speeds of deep-water and arctic elasmobranchs further support this conclusion; six-gill sharks (Hexanchus griseus) and the bramble shark (Echinorhinus cookei) have shown exceptionally slow swimming speeds and densities close to neutral, albeit slightly positive [9].…”

“…Lastly, we tested the predictions of Alexander's theory; namely that the evolution of slower steady swimming speeds is expected to be correlated with decreasing submerged weight. Good depth records are available for most species and it is well established that metabolic rates and enzymatic activity decline with depth of occurrence in fish, including sharks [19,20], leading to extraordinarily low swimming speeds in the deep sea [9,[20][21][22]. Additionally, greater depths feature colder temperatures, which have been shown to reduce swimming speeds of fish both under natural and laboratory conditions [23].…”

“…However, we note that the evolution of lower tissue densities (both in the liver and the remaining tissue) coincides with increases in liver size. This suggests that increasing buoyant forces are not simply due to larger livers, but also reduction in tissue densities [20]. Indeed, Treberg & Speers-Roesch [20] found that both lipid rspb.royalsocietypublishing.org Proc.…”

“…This suggests that increasing buoyant forces are not simply due to larger livers, but also reduction in tissue densities [20]. Indeed, Treberg & Speers-Roesch [20] found that both lipid rspb.royalsocietypublishing.org Proc. R. Soc.…”

Dining in the Deep: The Feeding Ecology of Deep-Sea Fishes

“…At bathyal depths, and certainly over the abyss, where prey biomass is low, many mobile piscivores include scavenging in their trophic repertoire. The absence of sharks, rays, and chimaeras at abyssal depths (Priede et al 2006) applies to a diverse range of taxa, not all of which are piscivores; it is unclear whether their absence is related to energetic constraints or a complex of energetic and physiological constraints (Laxson et al 2011, Treberg & Speers-Roesch 2016.…”