To boldly gulp: standard metabolic rate and boldness have context-dependent influences on risk-taking to breathe air in a catfish

David J Mckenzie,Thiago C Belão,F Tadeu Rantin,Shaun S Killen

doi:10.1242/jeb.122903

Abstract

The African sharptooth catfish Clarias gariepinus has bimodal respiration, it has a suprabranchial air-breathing organ alongside substantial gills. We used automated bimodal respirometry to reveal that undisturbed juvenile catfish (N=29) breathed air continuously in normoxia, with a marked diurnal cycle. Air breathing and routine metabolic rate (RMR) increased in darkness when, in the wild, this nocturnal predator forages. Aquatic hypoxia (20% air saturation) greatly increased overall reliance on air breathing. We investigated whether two measures of risk taking to breathe air, namely absolute rates of aerial O2 uptake (ṀO2,air) and the percentage of RMR obtained from air (%ṀO2,air), were influenced by individual standard metabolic rate (SMR) and boldness. In particular, whether any influence varied with resource availability (normoxia versus hypoxia) or relative fear of predation (day versus night). Individual SMR, derived from respirometry, had an overall positive influence on ṀO2,air across all contexts but a positive influence on %ṀO2,air only in hypoxia. Thus, a pervasive effect of SMR on air breathing became most acute in hypoxia, when individuals with higher O2 demand took proportionally more risks. Boldness was estimated as time required to resume air breathing after a fearful stimulus in daylight normoxia (Tres). Although Tres had no overall influence on ṀO2,air or %ṀO2,air, there was a negative relationship between Tres and %ṀO2,air in daylight, in normoxia and hypoxia. There were two Tres response groups, 'bold' phenotypes with Tres below 75 min (N=13) which, in daylight, breathed proportionally more air than 'shy' phenotypes with Tres above 115 min (N=16). Therefore, individual boldness influenced air breathing when fear of predation was high. Thus, individual energy demand and personality did not have parallel influences on the emergent tendency to take risks to obtain a resource; their influences varied in strength with context.

Highlights

In many animal species, individuals show wide individual variation in traits of both energy metabolism and personality (Burton et al, 2011; Careau et al, 2008; Sih et al, 2012)
We investigated whether two measures of risk taking to breathe air, namely absolute rates of aerial O2 uptake (Ṁ O2,air) and the percentage of routine metabolic rate (RMR) obtained from air (%Ṁ O2,air), were influenced by individual standard metabolic rate (SMR) and boldness
General patterns of respiratory partitioning In normoxia, the respirometry data showed a clear diurnal pattern in routine metabolism

Summary

Introduction

Individuals show wide individual variation in traits of both energy metabolism and personality (Burton et al, 2011; Careau et al, 2008; Sih et al, 2012). It could reflect personality, with bolder individuals willing to accept greater risks to secure energetic benefits (Conrad et al, 2011; Sih et al, 2012; Wolf and Weissing, 2012) As variation in both sets of traits would contribute to a similar life-history trade-off, it has been predicted that correlational selection should co-adapt physiology and temperament: animals with higher basal oxygen demands should be bolder (Biro and Stamps, 2010; Careau and Garland, 2012; Jenjan et al, 2013; Réale et al, 2010; Stamps, 2007). There is evidence, that reality is more complex and that the relative strength of these drivers of risk-taking can vary with context, such as resource availability or perceived risks of predation (Frost et al, 2013; Killen et al, 2011, 2012, 2013; Thomson et al, 2012)

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