The metabolic cost of developing under hydrostatic pressure: experimental evidence supports macroecological pattern

Abstract

Hydrostatic pressure is the most constant physical parameter on Earth. It increases linearly with water depth and is stable over evolutionary timescales. Despite this, bathymetric shifts in physiological adaptations that are observed in marine invertebrates (e.g. in metabolic rate and egg size) are currently interpreted to result predominantly from decreases in temperature. However, analyses of invertebrate egg size data presented here indicate an increase in egg volume with depth in the absence of a thermal gradient. This suggests hydrostatic pressure may also be important in determining resource allocation to offspring. To test the hypothesis that an increase in energy expenditure during development occurs with increasing hydrostatic pressure, we examined the effects of sustained exposure to pressure (1, 100, 200 and 300 atm) on development of a shallow-water marine gastropod, Buccinum undatum. Embryos developed successfully at 1, 100 and 200 atm, but the rate of development slowed with increasing pressure (by 3 d at 100 atm and 6 d at 200 atm). No development was observed at 300 atm. In embryos reared at 200 atm, veliger dry weight and carbon and nitrogen biomass were significantly reduced. These results indicate that high pressure significantly increases the metabolic cost associated with development, demonstrating a negative and ultimately critical effect. We hypothesise that pressure imposes increased metabolic cost on all physiological processes. This offers an additional explanation for physiological adaptations observed with increasing depth, indicating that hydrostatic pressure is an important and previously underestimated factor contributing to metabolic theory for most of our biosphere. Hydrostatic pressure may represent a critical physiological limit for the maximum depth distribution of shallow-water fauna.