Intraspecific temperature dependence of the scaling of metabolic rate with body mass in fishes and its ecological implications

Abstract

Metabolism constitutes a fundamental property of all organisms. Metabolic rate is commonly described to scale as a power function of body size and exponentially with temperature, thereby treating the effects of body size and temperature independently. Mounting evidence shows that the scaling of metabolic rate with body mass itself depends on temperature. Across‐species analyses in fishes suggest that the mass‐scaling exponent decreases with increasing temperature. However, whether this relationship holds at the within‐species level has rarely been tested. Here, we re‐analyse data on the metabolic rates of four freshwater fish species, two coregonids and two cyprinids, that cover wide ranges of body masses and their naturally experienced temperatures. We show that the standard metabolic rate of the coregonids is best fit when accounting for a linear temperature dependence of the scaling of metabolic rate with body mass, whereas a constant mass‐scaling exponent is supported in case of the cyprinids. Our study shows that phenotypic responses to temperature can result in temperature‐dependent scaling relationships at the species level and that these responses differ between taxa. Together with previous findings, these results indicate that evolutionarily adaptive and phenotypically plastic responses to temperature affect the scaling of metabolic rate with body mass in fishes.

Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

“…For example, a study of the catfish Silurus meridionalis showed that body size and temperature do not have independent effects on metabolic rate, as assumed by the MTE, but rather have significant interactive effects [73]. This study supported extensive past and recent work showing that the metabolic scaling slope in ectothermic organisms often varies with ambient temperature ( [19,20,54,56,57,59,[72][73][74][75][76]; also see Section 3.4), which has been ignored by proponents of the MTE. Therefore, multivariate models incorporating the effects of body size and temperature on metabolic rate should include an interactive term (e.g., [73,74]).…”

“…In addition, the MLBH predicts that surface-area-related resource uptake and metabolic waste excretion (or heat loss) should most influence the scaling of resting metabolic rate when the metabolic intensity of an animal is high. This hypothesis predicts that the scaling exponent should decrease (approaching 2/3) with increasing resting metabolic level, as has been frequently observed both within and among species with respect to differences in lifestyle, physiological status and ambient temperature [19,39,[54][55][56][57]59,[72][73][74][75][76].…”

“…Many investigators (but surprisingly not Kleiber himself, a founder of the 3/4-power law) rejected the thermoregulatory surface-area model of metabolic scaling, because it seemed incapable of explaining 3/4-power scaling, especially in ectothermic organisms that do not actively maintain constant body temperatures (see also [20]). Furthermore, the metabolic scaling slope does not necessarily approximate the theoretical values of 2/3 or 3/4, but may vary extensively between ~0 and >1, in association with differences in taxonomic affiliation, lifestyle, developmental stage, physiological status, and various ecological factors (e.g., [19,20,23,24,26,27,32,34,39,[44][45][46][47][48][49][54][55][56][57][58][59][60][61][72][73][74][75][76][99][100][101][102][103][104][105][106][107][117][118][119][120][121]). …”

Developmental and Immediate Thermal Environments Shape Energetic Trade-Offs, Growth Efficiency, and Metabolic Rate in Divergent Life-History Ecotypes of the Garter SnakeThamnophis elegans

“…The thermal dependence of growth efficiency, energy allocation, and metabolic rate in ectotherms has immense implications not only for the fitness of individual organisms but also for population dynamics (Burton et al 2011;Ohlberger et al 2012;Carey et al 2013), yet mechanistic models of the physiological impacts of temperature are still needed (Angilletta 2009;Somero 2011;da Silva et al 2013). The empirical data provided here offer evidence that important aspects of the phenotype-in this case, metabolic rate and growth-have complex interdependent relationships with both developmental and immediate environments.…”

“…6 for details). Empirical studies testing the MLBH hypothesis with ectotherms across a range of temperatures have demonstrated the ecological dependence and adaptive significance of the relationship between mass and metabolic rate (Killen et al 2010;Vaca and White 2010;Ohlberger et al 2012;Carey et al 2013), but not with universal support (Gifford et al 2013). Our estimates of scaling exponents at 207C (b p 1.33) and 247C (b p 1.23) were significantly higher than those of both adult and month-old snakes from these populations (b p 0.59 [Bronikowski and Vleck 2010]; b p 0.38-0.58 [Robert and Bronikowski 2010]).…”