Spatial variation in the relationship between performance and metabolic rate in wild juvenile <scp>A</scp>tlantic salmon

Robertsen, Grethe; Armstrong, J. D.; Nislow, Keith H.; Herfindal, Ivar; McKelvey, Simon; Einum, Sigurd

doi:10.1111/1365-2656.12182

Cited by 25 publications

(25 citation statements)

References 74 publications

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“…These laboratory experiments, together with field studies showing spatial variation in the correlation between SMR and fitness measures (Álvarez & Nicieza ; Robertsen et al . ), support the hypothesis that variation in these metabolic traits may be maintained by environmental variation that favours different phenotypes in different habitats or at different times within and across years (Burton et al . ).…”

Section: Discussionsupporting

confidence: 74%

“…Correlations between SMR and growth and survival in juvenile salmonid fishes ( S. salar and S. trutta ) have been found to be positive, negative or nonsignificant depending on which stream they are measured in, even when the genetic make‐up of individuals does not differ across streams (Álvarez & Nicieza ; Robertsen et al . ). These studies suggest that the fitness consequences of a given SMR are context‐dependent.…”

Section: Introductionmentioning

confidence: 97%

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The optimal combination of standard metabolic rate and aerobic scope for somatic growth depends on food availability

et al. 2015

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Summary 1.Metabolic rates can vary as much as threefold among individuals of the same size and age in a population, but why such variation persists is unclear given that they determine the energetic cost of living. Relationships between standard metabolic rate (SMR), growth and survival can vary with environmental conditions, suggesting that the fitness consequences of a given metabolic phenotype may be context-dependent. Less attention has focused on the link between absolute aerobic scope (AS, the difference between standard and maximum metabolic rate) and fitness under different environmental conditions, despite the importance of aerobic scope to an organism's total energetic capacity. 2. We examined the links between individual variation in both SMR and AS and somatic growth rates of brown trout (Salmo trutta) under different levels of food availability. 3. Standard metabolic rate and AS were uncorrelated across individuals. However, SMR and AS not only had interactive effects on growth, but these interactions depended on food level: at ad libitum food levels, AS had a positive effect on growth whose magnitude depended on SMR; at intermediate food levels, AS and SMR had interactive effects on growth, but at the low food level, there was no effect of either AS or SMR on growth. As a result, there was no metabolic phenotype that performed best or worst across all food levels. 4. These results demonstrate the importance of aerobic scope in explaining somatic growth rates and support the hypothesis that links between individual variation in metabolism and fitness are context-dependent. 5. The larger metabolic phenotype and the environmental context in which performance is evaluated both need to be considered in order to better understand the link between metabolic rates and fitness and thereby the persistence of individual variation in metabolic rates.

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Section: Discussionsupporting

confidence: 74%

Section: Introductionmentioning

confidence: 97%

The optimal combination of standard metabolic rate and aerobic scope for somatic growth depends on food availability

et al. 2015

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“…g . the natural environment) have found either negative or no correlations (Álvarez & Nicieza, ; Finstad et al , ; Norin & Malte, ; Robertsen et al , ). It has been suggested that the fitness advantages of a given SMR may thus depend upon the context (Burton et al , ), a hypothesis that is supported by recent stream‐tank experiments showing that SMR is positively correlated with growth rate when fishes are competing for access to a plentiful food supply but the relationship becomes negative once access to food is taken into account (Reid et al , , ).…”

Section: Individual Variation In Metabolismmentioning

confidence: 99%

Does individual variation in metabolic phenotype predict fish behaviour and performance?

Metcalfe

Leeuwen

Killen

2015

Journal of Fish Biology

289

318

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There is increasing interest in documenting and explaining the existence of marked intraspecific variation in metabolic rate in animals, with fishes providing some of the best‐studied examples. After accounting for variation due to other factors, there can typically be a two to three‐fold variation among individual fishes for both standard and maximum metabolic rate (SMR and MMR). This variation is reasonably consistent over time (provided that conditions remain stable), and its underlying causes may be influenced by both genes and developmental conditions. In this paper, current knowledge of the extent and causes of individual variation in SMR, MMR and aerobic scope (AS), collectively its metabolic phenotype, is reviewed and potential links among metabolism, behaviour and performance are described. Intraspecific variation in metabolism has been found to be related to other traits: fishes with a relatively high SMR tend to be more dominant and grow faster in high food environments, but may lose their advantage and are more prone to risk‐taking when conditions deteriorate. In contrast to the wide body of research examining links between SMR and behavioural traits, very little work has been directed towards understanding the ecological consequences of individual variation in MMR and AS. Although AS can differ among populations of the same species in response to performance demands, virtually nothing is known about the effects of AS on individual behaviours such as those associated with foraging or predator avoidance. Further, while factors such as food availability, temperature, hypoxia and the fish's social environment are known to alter resting and MMRs in fishes, there is a paucity of studies examining how these effects vary among individuals, and how this variation relates to behaviour. Given the observed links between metabolism and measures of performance, understanding the metabolic responses of individuals to changing environments will be a key area for future research because the environment will have a strong influence on which animals survive predation, become dominant and ultimately have the highest reproductive success. Although current evidence suggests that variation in SMR may be maintained within populations via context‐dependent fitness benefits, it is suggested that a more integrative approach is now required to fully understand how the environment can modulate individual performance via effects on metabolic phenotypes encompassing SMR, MMR and AS.

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“…Nevertheless, further research is needed to sort out the causal pathways involved in how thyroxine affects growth and associated activities. Although high growth rates often entail high metabolic rates (see below), this may not always be so: opposite associations have even been found (Medrano & Gall, 1976;Morgan & Iwama, 1991;Steyermark, 2002;Bayne, 2004;Álvarez & Nicieza, 2005;Careau et al, 2013;Robertsen et al, 2014). Therefore, rates of growth and metabolism can be uncoupled (see also Section III).…”

Section: (2) Cause Versus Effectmentioning

confidence: 99%

Is metabolic rate a universal ‘pacemaker’ for biological processes?

2014

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A common, long-held belief is that metabolic rate drives the rates of various biological, ecological and evolutionary processes. Although this metabolic pacemaker view (as assumed by the recent, influential 'metabolic theory of ecology') may be true in at least some situations (e.g. those involving moderate temperature effects or physiological processes closely linked to metabolism, such as heartbeat and breathing rate), it suffers from several major limitations, including: (i) it is supported chiefly by indirect, correlational evidence (e.g. similarities between the body-size and temperature scaling of metabolic rate and that of other biological processes, which are not always observed) - direct, mechanistic or experimental support is scarce and much needed; (ii) it is contradicted by abundant evidence showing that various intrinsic and extrinsic factors (e.g. hormonal action and temperature changes) can dissociate the rates of metabolism, growth, development and other biological processes; (iii) there are many examples where metabolic rate appears to respond to, rather than drive the rates of various other biological processes (e.g. ontogenetic growth, food intake and locomotor activity); (iv) there are additional examples where metabolic rate appears to be unrelated to the rate of a biological process (e.g. ageing, circadian rhythms, and molecular evolution); and (v) the theoretical foundation for the metabolic pacemaker view focuses only on the energetic control of biological processes, while ignoring the importance of informational control, as mediated by various genetic, cellular, and neuroendocrine regulatory systems. I argue that a comprehensive understanding of the pace of life must include how biological activities depend on both energy and information and their environmentally sensitive interaction. This conclusion is supported by extensive evidence showing that hormones and other regulatory factors and signalling systems coordinate the processes of growth, metabolism and food intake in adaptive ways that are responsive to an organism's internal and external conditions. Metabolic rate does not merely dictate growth rate, but is coadjusted with it. Energy and information use are intimately intertwined in living systems: biological signalling pathways both control and respond to the energetic state of an organism. This review also reveals that we have much to learn about the temporal structure of the pace of life. Are its component processes highly integrated and synchronized, or are they loosely connected and often discordant? And what causes the level of coordination that we see? These questions are of great theoretical and practical importance.

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Spatial variation in the relationship between performance and metabolic rate in wild juvenile Atlantic salmon

Cited by 25 publications

References 74 publications

The optimal combination of standard metabolic rate and aerobic scope for somatic growth depends on food availability

The optimal combination of standard metabolic rate and aerobic scope for somatic growth depends on food availability

Does individual variation in metabolic phenotype predict fish behaviour and performance?

Is metabolic rate a universal ‘pacemaker’ for biological processes?

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