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Metabolic costs imposed by hydrostatic pressure constrain bathymetric range in the lithodid crab Lithodes maja

Metabolic costs imposed by hydrostatic pressure constrain bathymetric range in the lithodid crab Lithodes maja
Metabolic costs imposed by hydrostatic pressure constrain bathymetric range in the lithodid crab Lithodes maja
The changing climate is shifting the distributions of marine species, yet the potential for shifts in depth distributions is virtually unexplored. Hydrostatic pressure is proposed to contribute to a physiological bottleneck constraining depth range extension in shallow-water taxa. However, bathymetric limitation by hydrostatic pressure remains undemonstrated, and the mechanism limiting hyperbaric tolerance remains hypothetical. Here, we assess the effects of hydrostatic pressure in the lithodid crab Lithodes maja (bathymetric range 4-790 m depth, approximately equivalent to 0.1 to 7.9 MPa hydrostatic pressure). Heart rate decreased with increasing hydrostatic pressure, and was significantly lower at ≥10.0 MPa than at 0.1 MPa. Oxygen consumption increased with increasing hydrostatic pressure to 12.5 MPa, before decreasing as hydrostatic pressure increased to 20.0 MPa: oxygen consumption was significantly higher at 7.5-17.5 MPa than at 0.1 MPa. Increases in expression of genes associated with neurotransmission, metabolism and stress were observed between 7.5 and 12.5 MPa. We suggest that hyperbaric tolerance in L. maja may be oxygen-limited by hyperbaric effects on heart rate and metabolic rate, but that L. maja’s bathymetric range is limited by metabolic costs imposed by the effects of high hydrostatic pressure. These results advocate including hydrostatic pressure in a complex model of environmental tolerance, where energy-limitation constrains biogeographic range, and facilitate incorporating hydrostatic pressure into the broader metabolic framework for ecology and evolution. Such an approach is crucial for accurately projecting biogeographic responses to changing climate, and for understanding the ecology and evolution of life at depth.
0022-0949
3916-3926
Brown, Alastair E.
e8ff3585-dd26-47bc-bdcb-55eeda5001d2
Thatje, Sven
f1011fe3-1048-40c0-97c1-e93b796e6533
Morris, James P.
b19074b9-7a65-4a42-bbf8-416dc45f6007
Oliphant, Andrew
c26061c4-bde5-4fdf-ab2e-a1797447cf09
Morgan, Elizabeth
788032a6-1607-4f2e-95a6-74260a6bcddb
Hauton, Christopher
7706f6ba-4497-42b2-8c6d-00df81676331
Jones, Daniel O.B.
44fc07b3-5fb7-4bf5-9cec-78c78022613a
Pond, David W.
3d0d013e-d9e0-4fc3-b30c-12f7f24bec6d
Brown, Alastair E.
e8ff3585-dd26-47bc-bdcb-55eeda5001d2
Thatje, Sven
f1011fe3-1048-40c0-97c1-e93b796e6533
Morris, James P.
b19074b9-7a65-4a42-bbf8-416dc45f6007
Oliphant, Andrew
c26061c4-bde5-4fdf-ab2e-a1797447cf09
Morgan, Elizabeth
788032a6-1607-4f2e-95a6-74260a6bcddb
Hauton, Christopher
7706f6ba-4497-42b2-8c6d-00df81676331
Jones, Daniel O.B.
44fc07b3-5fb7-4bf5-9cec-78c78022613a
Pond, David W.
3d0d013e-d9e0-4fc3-b30c-12f7f24bec6d

Brown, Alastair E., Thatje, Sven, Morris, James P., Oliphant, Andrew, Morgan, Elizabeth, Hauton, Christopher, Jones, Daniel O.B. and Pond, David W. (2017) Metabolic costs imposed by hydrostatic pressure constrain bathymetric range in the lithodid crab Lithodes maja Journal of Experimental Biology, 220, (21), pp. 3916-3926. (doi:10.1242/jeb.158543).

Record type: Article

Abstract

The changing climate is shifting the distributions of marine species, yet the potential for shifts in depth distributions is virtually unexplored. Hydrostatic pressure is proposed to contribute to a physiological bottleneck constraining depth range extension in shallow-water taxa. However, bathymetric limitation by hydrostatic pressure remains undemonstrated, and the mechanism limiting hyperbaric tolerance remains hypothetical. Here, we assess the effects of hydrostatic pressure in the lithodid crab Lithodes maja (bathymetric range 4-790 m depth, approximately equivalent to 0.1 to 7.9 MPa hydrostatic pressure). Heart rate decreased with increasing hydrostatic pressure, and was significantly lower at ≥10.0 MPa than at 0.1 MPa. Oxygen consumption increased with increasing hydrostatic pressure to 12.5 MPa, before decreasing as hydrostatic pressure increased to 20.0 MPa: oxygen consumption was significantly higher at 7.5-17.5 MPa than at 0.1 MPa. Increases in expression of genes associated with neurotransmission, metabolism and stress were observed between 7.5 and 12.5 MPa. We suggest that hyperbaric tolerance in L. maja may be oxygen-limited by hyperbaric effects on heart rate and metabolic rate, but that L. maja’s bathymetric range is limited by metabolic costs imposed by the effects of high hydrostatic pressure. These results advocate including hydrostatic pressure in a complex model of environmental tolerance, where energy-limitation constrains biogeographic range, and facilitate incorporating hydrostatic pressure into the broader metabolic framework for ecology and evolution. Such an approach is crucial for accurately projecting biogeographic responses to changing climate, and for understanding the ecology and evolution of life at depth.

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Accepted/In Press date: 5 September 2017
e-pub ahead of print date: 1 November 2017

Identifiers

Local EPrints ID: 415156
URI: http://eprints.soton.ac.uk/id/eprint/415156
ISSN: 0022-0949
PURE UUID: 76f57490-dd7d-417c-b210-1038f7b06ef0
ORCID for Christopher Hauton: ORCID iD orcid.org/0000-0002-2313-4226

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Date deposited: 02 Nov 2017 17:30
Last modified: 05 Dec 2017 17:30

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Contributors

Author: Alastair E. Brown
Author: Sven Thatje
Author: James P. Morris
Author: Andrew Oliphant
Author: Elizabeth Morgan
Author: Daniel O.B. Jones
Author: David W. Pond

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