Individual variation in the oxidative costs of personality traits

Kathryn E. Arnold; Katherine A. Herborn; Aileen Adam; Lucille Alexander

doi:10.1111/1365-2435.12375

Individual variation in the oxidative costs of personality traits

Kathryn E. Arnold^*, Katherine A. Herborn, Aileen Adam, Lucille Alexander

^*Corresponding author for this work

School of Biological and Marine Sciences

Research output: Contribution to journal › Article › peer-review

Abstract

Summary ‘Personality traits’ are behavioural differences between individuals that are stable within individuals. Different combinations of personality traits can correlate with fitness variation but the mechanisms remain unclear. There is the suggestion that personality reflects variation in physiology. For example, ‘fast’ (bold, active, fast exploring) individuals are predicted to maintain a higher metabolic rate than ‘slow’ animals. A raised metabolic rate can result in a proliferation of reactive oxygen species (ROS) which, if unchecked, cause oxidative stress. Thus, the ‘extended pace of life theory’ predicts that ‘fast’ individuals will pay higher oxidative costs than ‘slow’ ones. Alternatively, stress hormones, which are often relatively high in ‘slow’ individuals, can also cause proliferation of ROS and subsequent oxidative damage. Here, we assessed co‐variation between personality and oxidative profile in wild blue tits. The personality traits neophobia (latency to approach food near novel objects), activity level in a novel environment and exploratory tendency (controlling for differences in activity) assayed in captivity were repeatable within individuals but were uncorrelated with each other. Reactive oxygen metabolites (ROMs an index of pro‐oxidant status) and OXY (antioxidant capacity) were also uncorrelated with each other and did not vary with age or sex. Blood sampling birds within three minutes of capture from their familiar cage vs. after 15 min of exposure to a standardized stressor did not affect ROMs or OXY. Wintering blue tits that were both highly neophobic and exploratory had low OXY defences and individuals that showed low neophobia and low exploration had high OXY defences. Variation in ROMs was not explained by any personality trait. High exploratory tendency also correlated with a reduction in body condition in captivity, but body condition did not predict ROMs or OXY. Activity level in the exploration trial did not vary with oxidative profile or change in body condition. Personality types differed in antioxidant defences, and it was the combination of an individual's personality traits that proved important. ROS production and antioxidant defences will vary due to many processes for example resource allocation, not just metabolic rate and stress responsiveness. Consequently, the costs of personality traits and thus the predictions regarding fitness are complex.

Original language	English
Pages (from-to)	522-530
Number of pages	0
Journal	Functional Ecology
Volume	29
Issue number	4
Early online date	26 Dec 2014
DOIs	https://doi.org/10.1111/1365-2435.12375
Publication status	Published - Apr 2015

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@article{823cf57669d44969b8f869777cc40a94,

title = "Individual variation in the oxidative costs of personality traits",

abstract = "Summary {\textquoteleft}Personality traits{\textquoteright} are behavioural differences between individuals that are stable within individuals. Different combinations of personality traits can correlate with fitness variation but the mechanisms remain unclear. There is the suggestion that personality reflects variation in physiology. For example, {\textquoteleft}fast{\textquoteright} (bold, active, fast exploring) individuals are predicted to maintain a higher metabolic rate than {\textquoteleft}slow{\textquoteright} animals. A raised metabolic rate can result in a proliferation of reactive oxygen species (ROS) which, if unchecked, cause oxidative stress. Thus, the {\textquoteleft}extended pace of life theory{\textquoteright} predicts that {\textquoteleft}fast{\textquoteright} individuals will pay higher oxidative costs than {\textquoteleft}slow{\textquoteright} ones. Alternatively, stress hormones, which are often relatively high in {\textquoteleft}slow{\textquoteright} individuals, can also cause proliferation of ROS and subsequent oxidative damage. Here, we assessed co‐variation between personality and oxidative profile in wild blue tits. The personality traits neophobia (latency to approach food near novel objects), activity level in a novel environment and exploratory tendency (controlling for differences in activity) assayed in captivity were repeatable within individuals but were uncorrelated with each other. Reactive oxygen metabolites (ROMs an index of pro‐oxidant status) and OXY (antioxidant capacity) were also uncorrelated with each other and did not vary with age or sex. Blood sampling birds within three minutes of capture from their familiar cage vs. after 15 min of exposure to a standardized stressor did not affect ROMs or OXY. Wintering blue tits that were both highly neophobic and exploratory had low OXY defences and individuals that showed low neophobia and low exploration had high OXY defences. Variation in ROMs was not explained by any personality trait. High exploratory tendency also correlated with a reduction in body condition in captivity, but body condition did not predict ROMs or OXY. Activity level in the exploration trial did not vary with oxidative profile or change in body condition. Personality types differed in antioxidant defences, and it was the combination of an individual's personality traits that proved important. ROS production and antioxidant defences will vary due to many processes for example resource allocation, not just metabolic rate and stress responsiveness. Consequently, the costs of personality traits and thus the predictions regarding fitness are complex. ",

author = "Arnold, {Kathryn E.} and Herborn, {Katherine A.} and Aileen Adam and Lucille Alexander",

year = "2015",

month = apr,

doi = "10.1111/1365-2435.12375",

language = "English",

volume = "29",

pages = "522--530",

journal = "Functional Ecology",

issn = "0269-8463",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "4",

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TY - JOUR

T1 - Individual variation in the oxidative costs of personality traits

AU - Arnold, Kathryn E.

AU - Herborn, Katherine A.

AU - Adam, Aileen

AU - Alexander, Lucille

PY - 2015/4

Y1 - 2015/4

N2 - Summary ‘Personality traits’ are behavioural differences between individuals that are stable within individuals. Different combinations of personality traits can correlate with fitness variation but the mechanisms remain unclear. There is the suggestion that personality reflects variation in physiology. For example, ‘fast’ (bold, active, fast exploring) individuals are predicted to maintain a higher metabolic rate than ‘slow’ animals. A raised metabolic rate can result in a proliferation of reactive oxygen species (ROS) which, if unchecked, cause oxidative stress. Thus, the ‘extended pace of life theory’ predicts that ‘fast’ individuals will pay higher oxidative costs than ‘slow’ ones. Alternatively, stress hormones, which are often relatively high in ‘slow’ individuals, can also cause proliferation of ROS and subsequent oxidative damage. Here, we assessed co‐variation between personality and oxidative profile in wild blue tits. The personality traits neophobia (latency to approach food near novel objects), activity level in a novel environment and exploratory tendency (controlling for differences in activity) assayed in captivity were repeatable within individuals but were uncorrelated with each other. Reactive oxygen metabolites (ROMs an index of pro‐oxidant status) and OXY (antioxidant capacity) were also uncorrelated with each other and did not vary with age or sex. Blood sampling birds within three minutes of capture from their familiar cage vs. after 15 min of exposure to a standardized stressor did not affect ROMs or OXY. Wintering blue tits that were both highly neophobic and exploratory had low OXY defences and individuals that showed low neophobia and low exploration had high OXY defences. Variation in ROMs was not explained by any personality trait. High exploratory tendency also correlated with a reduction in body condition in captivity, but body condition did not predict ROMs or OXY. Activity level in the exploration trial did not vary with oxidative profile or change in body condition. Personality types differed in antioxidant defences, and it was the combination of an individual's personality traits that proved important. ROS production and antioxidant defences will vary due to many processes for example resource allocation, not just metabolic rate and stress responsiveness. Consequently, the costs of personality traits and thus the predictions regarding fitness are complex.

AB - Summary ‘Personality traits’ are behavioural differences between individuals that are stable within individuals. Different combinations of personality traits can correlate with fitness variation but the mechanisms remain unclear. There is the suggestion that personality reflects variation in physiology. For example, ‘fast’ (bold, active, fast exploring) individuals are predicted to maintain a higher metabolic rate than ‘slow’ animals. A raised metabolic rate can result in a proliferation of reactive oxygen species (ROS) which, if unchecked, cause oxidative stress. Thus, the ‘extended pace of life theory’ predicts that ‘fast’ individuals will pay higher oxidative costs than ‘slow’ ones. Alternatively, stress hormones, which are often relatively high in ‘slow’ individuals, can also cause proliferation of ROS and subsequent oxidative damage. Here, we assessed co‐variation between personality and oxidative profile in wild blue tits. The personality traits neophobia (latency to approach food near novel objects), activity level in a novel environment and exploratory tendency (controlling for differences in activity) assayed in captivity were repeatable within individuals but were uncorrelated with each other. Reactive oxygen metabolites (ROMs an index of pro‐oxidant status) and OXY (antioxidant capacity) were also uncorrelated with each other and did not vary with age or sex. Blood sampling birds within three minutes of capture from their familiar cage vs. after 15 min of exposure to a standardized stressor did not affect ROMs or OXY. Wintering blue tits that were both highly neophobic and exploratory had low OXY defences and individuals that showed low neophobia and low exploration had high OXY defences. Variation in ROMs was not explained by any personality trait. High exploratory tendency also correlated with a reduction in body condition in captivity, but body condition did not predict ROMs or OXY. Activity level in the exploration trial did not vary with oxidative profile or change in body condition. Personality types differed in antioxidant defences, and it was the combination of an individual's personality traits that proved important. ROS production and antioxidant defences will vary due to many processes for example resource allocation, not just metabolic rate and stress responsiveness. Consequently, the costs of personality traits and thus the predictions regarding fitness are complex.

U2 - 10.1111/1365-2435.12375

DO - 10.1111/1365-2435.12375

M3 - Article

SN - 0269-8463

VL - 29

SP - 522

EP - 530

JO - Functional Ecology

JF - Functional Ecology

IS - 4

ER -

Individual variation in the oxidative costs of personality traits

Abstract

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