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Individual variation in field metabolic rates of wild living fish have phenotypic and ontogenetic underpinnings: insights from stable isotope compositions of otoliths

Individual variation in field metabolic rates of wild living fish have phenotypic and ontogenetic underpinnings: insights from stable isotope compositions of otoliths
Individual variation in field metabolic rates of wild living fish have phenotypic and ontogenetic underpinnings: insights from stable isotope compositions of otoliths

Introduction: individual metabolism has been identified as a key variable for predicting responses of individuals and populations to climate change, particularly for aquatic ectotherms such as fishes. Predictions of organism standard metabolic rate (SMR), and the thermal sensitivity of metabolic rate are typically based on allometric scaling rules and respirometry-based measures of respiratory potential under laboratory conditions. The relevance of laboratory-based measurement and theoretical allometric rules to predict performance of free-ranging animals in complex natural settings has been questioned, but determining time averaged metabolic rate in wild aquatic animals is challenging.

Methods: here we draw on stable isotope compositions of aragonite in fish otoliths to estimate time averaged experienced temperature and expressed field metabolic rate (FMR) simultaneously and retrospectively at an individual level. We apply the otolith FMR proxy to a population of European plaice (Pleuronectes platessa) from the North Sea during a period of rapid warming between the 1980s to the mid-2000s, sampling otolith tissue grown in both juvenile and adult stages. 

Results: among-individual variations in realized mass-specific FMR were large and independent of temperature and scaled positively with body size in adult life stages, contradicting simplistic assumptions that FMR follows scaling relationships inferred for standard metabolic rates (SMR). In the same individuals, FMR in the first summer of life co-varied positively with temperature. 

Discussion: we find strong evidence for the presence of consistent metabolic phenotypes within the sampled population, as FMR in the first year of life was the strongest single predictor for among individual variation in FMR at the point of sampling. Nonetheless, best fitting models explained only 20% of the observed variation, pointing to large among-individual variation in FMR that is unexplained by body mass, temperature or metabolic phenotype. Stable isotope-derived estimates of field metabolic rate have great potential to expand our understanding of ecophysiology in general and especially mechanisms underpinning the relationships between animal performance and changing environmental and ecological conditions.

biomineral, carbon isotope (δC), ecophysiology, fisheries, metabolic theory
Jones, Joseph
38100e23-e135-4154-beb0-5c560c1e13b6
Hunter, Ewan
75352862-16aa-44ee-aa31-ff56bf2305ea
Hambach, Bastian
d144b919-bc71-4793-89ee-7fdfdb7762bb
Wilding, Megan
15e775ce-fdea-4050-8ec8-e701029fccd7
Trueman, Clive N.
d00d3bd6-a47b-4d47-89ae-841c3d506205
Jones, Joseph
38100e23-e135-4154-beb0-5c560c1e13b6
Hunter, Ewan
75352862-16aa-44ee-aa31-ff56bf2305ea
Hambach, Bastian
d144b919-bc71-4793-89ee-7fdfdb7762bb
Wilding, Megan
15e775ce-fdea-4050-8ec8-e701029fccd7
Trueman, Clive N.
d00d3bd6-a47b-4d47-89ae-841c3d506205

Jones, Joseph, Hunter, Ewan, Hambach, Bastian, Wilding, Megan and Trueman, Clive N. (2023) Individual variation in field metabolic rates of wild living fish have phenotypic and ontogenetic underpinnings: insights from stable isotope compositions of otoliths. Frontiers in Ecology and Evolution, 11, [1161105]. (doi:10.3389/fevo.2023.1161105).

Record type: Article

Abstract

Introduction: individual metabolism has been identified as a key variable for predicting responses of individuals and populations to climate change, particularly for aquatic ectotherms such as fishes. Predictions of organism standard metabolic rate (SMR), and the thermal sensitivity of metabolic rate are typically based on allometric scaling rules and respirometry-based measures of respiratory potential under laboratory conditions. The relevance of laboratory-based measurement and theoretical allometric rules to predict performance of free-ranging animals in complex natural settings has been questioned, but determining time averaged metabolic rate in wild aquatic animals is challenging.

Methods: here we draw on stable isotope compositions of aragonite in fish otoliths to estimate time averaged experienced temperature and expressed field metabolic rate (FMR) simultaneously and retrospectively at an individual level. We apply the otolith FMR proxy to a population of European plaice (Pleuronectes platessa) from the North Sea during a period of rapid warming between the 1980s to the mid-2000s, sampling otolith tissue grown in both juvenile and adult stages. 

Results: among-individual variations in realized mass-specific FMR were large and independent of temperature and scaled positively with body size in adult life stages, contradicting simplistic assumptions that FMR follows scaling relationships inferred for standard metabolic rates (SMR). In the same individuals, FMR in the first summer of life co-varied positively with temperature. 

Discussion: we find strong evidence for the presence of consistent metabolic phenotypes within the sampled population, as FMR in the first year of life was the strongest single predictor for among individual variation in FMR at the point of sampling. Nonetheless, best fitting models explained only 20% of the observed variation, pointing to large among-individual variation in FMR that is unexplained by body mass, temperature or metabolic phenotype. Stable isotope-derived estimates of field metabolic rate have great potential to expand our understanding of ecophysiology in general and especially mechanisms underpinning the relationships between animal performance and changing environmental and ecological conditions.

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Accepted/In Press date: 17 May 2023
e-pub ahead of print date: 13 June 2023
Published date: 13 June 2023
Additional Information: Funding Information: This work was funded from NERC Case award NE/P009700/1.
Keywords: biomineral, carbon isotope (δC), ecophysiology, fisheries, metabolic theory

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Local EPrints ID: 480530
URI: http://eprints.soton.ac.uk/id/eprint/480530
PURE UUID: d605a520-cdd3-4ee9-adda-ee725200d58d
ORCID for Bastian Hambach: ORCID iD orcid.org/0000-0003-4546-5672
ORCID for Megan Wilding: ORCID iD orcid.org/0000-0003-0063-2238
ORCID for Clive N. Trueman: ORCID iD orcid.org/0000-0002-4995-736X

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Date deposited: 04 Aug 2023 16:33
Last modified: 18 Mar 2024 03:30

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Contributors

Author: Joseph Jones
Author: Ewan Hunter
Author: Bastian Hambach ORCID iD
Author: Megan Wilding ORCID iD

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