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

The metabolic cost of developing under hydrostatic pressure: experimental evidence supports macroecological pattern
The metabolic cost of developing under hydrostatic pressure: experimental evidence supports macroecological pattern
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 (eg in metabolic rate and egg size) are currently interpreted to result predominantly from decreases in temperature. However, analysis of invertebrate egg size data presented here indicates 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. In order to test the hypothesis that an increase in energy expenditure during development occurs with increasing depth, we examined the effect 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 days at 100 atm and 6 days 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 approximately 99% of our biosphere. This may represent a critical physiological bottleneck for the maximum depth distribution of shallow-water fauna.
71-82
Smith, Kathryn E.
dace2668-69f3-40cc-a526-541c4b41c8b8
Brown, Alastair
909f34db-bc9c-403f-ba8f-31aee1c00161
Thatje, Sven
f1011fe3-1048-40c0-97c1-e93b796e6533
Smith, Kathryn E.
dace2668-69f3-40cc-a526-541c4b41c8b8
Brown, Alastair
909f34db-bc9c-403f-ba8f-31aee1c00161
Thatje, Sven
f1011fe3-1048-40c0-97c1-e93b796e6533

Smith, Kathryn E., Brown, Alastair and Thatje, Sven (2015) The metabolic cost of developing under hydrostatic pressure: experimental evidence supports macroecological pattern. Marine Ecology Progress Series, 524, 71-82. (doi:10.3354/meps11172).

Record type: Article

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 (eg in metabolic rate and egg size) are currently interpreted to result predominantly from decreases in temperature. However, analysis of invertebrate egg size data presented here indicates 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. In order to test the hypothesis that an increase in energy expenditure during development occurs with increasing depth, we examined the effect 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 days at 100 atm and 6 days 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 approximately 99% of our biosphere. This may represent a critical physiological bottleneck for the maximum depth distribution of shallow-water fauna.

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More information

Published date: 2015
Organisations: Ocean and Earth Science, Southampton Marine & Maritime Institute

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Local EPrints ID: 372861
URI: https://eprints.soton.ac.uk/id/eprint/372861
PURE UUID: 0df79644-d4eb-4c0f-9b7c-73ce7f7ec17b

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Date deposited: 22 Dec 2014 09:52
Last modified: 15 Jul 2019 21:35

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