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Article: Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism

TitleThermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism
Authors
KeywordsGastropod
Hypometabolism
Littorinidae
Metabolic theory of ecology
Oxygen consumption
Issue Date2011
PublisherThe Company of Biologists Ltd. The Journal's web site is located at http://jeb.biologists.org
Citation
Journal Of Experimental Biology, 2011, v. 214 n. 21, p. 3649-3657 How to Cite?
AbstractContemporary theory for thermal adaptation of ectothermic metazoans focuses on the maximization of energy gain and performance (locomotion and foraging). Little consideration is given to the selection for mechanisms that minimize resting energy loss in organisms whose energy gain is severely constrained. We tested a hypothetical framework for thermal performance of locomotor activity (a proxy for energy gain) and resting metabolism (a proxy for energy loss) in energetically compromised snails in the littoral fringe zone, comparing this with existing theory. In contrast to theory, the thermal ranges and optima for locomotor performance and metabolic performance of Echinolittorina malaccana are mismatched, and energy gain is only possible at relatively cool temperatures. To overcome thermal and temporal constraints on energy gain while experiencing high body temperatures (23-50°C), these snails depress resting metabolism between 35 and 46°C (thermally insensitive zone). The resulting bimodal relationship for metabolism against temperature contrasts with the unimodal or exponential relationships of most ectotherms. Elevation of metabolism above the breakpoint temperature for thermal insensitivity (46°C) coincides with the induction of a heat shock response, and has implications for energy expenditure and natural selection. Time-dependent mortality is initiated at this breakpoint temperature, suggesting a threshold above which the rate of energy demand exceeds the capacity for cellular energy generation (rate of ATP turnover). Mortality in a thermal range that elevates rather than limits aerobic metabolism contrasts with the hypothesis that cellular oxygen deficiency underlies temperature-related mortality. The findings of this study point to the need to incorporate aspects of resting metabolism and energy conservation into theories of thermal adaptation. © 2011. Published by The Company of Biologists Ltd.
Persistent Identifierhttp://hdl.handle.net/10722/147035
ISSN
2015 Impact Factor: 2.914
2015 SCImago Journal Rankings: 1.815
ISI Accession Number ID
Funding AgencyGrant Number
Universiti Brunei DarussalamUBD/PNC2/2/RG/1(112)
Ministry of Development, Brunei DarussalamKPN/RDU/STI-C/2
Sino-British Fellowship Trust
University of Hong Kong
South African Research Chairs Initiative of the Department of Science and Technology
National Research Foundation
Small Project Grant (HKU)200907176196
Funding Information:

D.J.M. received grant funding from the Universiti Brunei Darussalam [UBD/PNC2/2/RG/1(112)] and the Ministry of Development, Brunei Darussalam [KPN/RDU/STI-C/2], Y.D. was supported by a Sino-British Fellowship Trust Visitorship awarded by The University of Hong Kong, C. D. M. was supported by the South African Research Chairs Initiative of the Department of Science and Technology and the National Research Foundation and G. A. W. was supported by a Small Project Grant (HKU) [200907176196].

References

 

DC FieldValueLanguage
dc.contributor.authorMarshall, DJen_HK
dc.contributor.authorDong, YWen_HK
dc.contributor.authorMcQuaid, CDen_HK
dc.contributor.authorWilliams, GAen_HK
dc.date.accessioned2012-05-23T05:54:13Z-
dc.date.available2012-05-23T05:54:13Z-
dc.date.issued2011en_HK
dc.identifier.citationJournal Of Experimental Biology, 2011, v. 214 n. 21, p. 3649-3657en_HK
dc.identifier.issn0022-0949en_HK
dc.identifier.urihttp://hdl.handle.net/10722/147035-
dc.description.abstractContemporary theory for thermal adaptation of ectothermic metazoans focuses on the maximization of energy gain and performance (locomotion and foraging). Little consideration is given to the selection for mechanisms that minimize resting energy loss in organisms whose energy gain is severely constrained. We tested a hypothetical framework for thermal performance of locomotor activity (a proxy for energy gain) and resting metabolism (a proxy for energy loss) in energetically compromised snails in the littoral fringe zone, comparing this with existing theory. In contrast to theory, the thermal ranges and optima for locomotor performance and metabolic performance of Echinolittorina malaccana are mismatched, and energy gain is only possible at relatively cool temperatures. To overcome thermal and temporal constraints on energy gain while experiencing high body temperatures (23-50°C), these snails depress resting metabolism between 35 and 46°C (thermally insensitive zone). The resulting bimodal relationship for metabolism against temperature contrasts with the unimodal or exponential relationships of most ectotherms. Elevation of metabolism above the breakpoint temperature for thermal insensitivity (46°C) coincides with the induction of a heat shock response, and has implications for energy expenditure and natural selection. Time-dependent mortality is initiated at this breakpoint temperature, suggesting a threshold above which the rate of energy demand exceeds the capacity for cellular energy generation (rate of ATP turnover). Mortality in a thermal range that elevates rather than limits aerobic metabolism contrasts with the hypothesis that cellular oxygen deficiency underlies temperature-related mortality. The findings of this study point to the need to incorporate aspects of resting metabolism and energy conservation into theories of thermal adaptation. © 2011. Published by The Company of Biologists Ltd.en_HK
dc.languageengen_US
dc.publisherThe Company of Biologists Ltd. The Journal's web site is located at http://jeb.biologists.org-
dc.relation.ispartofJournal of Experimental Biologyen_HK
dc.subjectGastropoden_HK
dc.subjectHypometabolismen_HK
dc.subjectLittorinidaeen_HK
dc.subjectMetabolic theory of ecologyen_HK
dc.subjectOxygen consumptionen_HK
dc.titleThermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolismen_HK
dc.typeArticleen_HK
dc.identifier.emailWilliams, GA: hrsbwga@hkucc.hku.hken_HK
dc.identifier.authorityWilliams, GA=rp00804en_HK
dc.description.naturelink_to_OA_fulltext-
dc.identifier.doi10.1242/jeb.059899en_HK
dc.identifier.pmid21993794-
dc.identifier.scopuseid_2-s2.0-80054695847en_HK
dc.identifier.hkuros199543en_US
dc.relation.referenceshttp://www.scopus.com/mlt/select.url?eid=2-s2.0-80054695847&selection=ref&src=s&origin=recordpageen_HK
dc.identifier.volume214en_HK
dc.identifier.issue21en_HK
dc.identifier.spage3649en_HK
dc.identifier.epage3657en_HK
dc.identifier.eissn1477-9145-
dc.identifier.isiWOS:000296048000026-
dc.publisher.placeUnited Kingdomen_HK
dc.identifier.scopusauthoridMarshall, DJ=7402186519en_HK
dc.identifier.scopusauthoridDong, YW=13612033100en_HK
dc.identifier.scopusauthoridMcQuaid, CD=7005808952en_HK
dc.identifier.scopusauthoridWilliams, GA=7406082821en_HK

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