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Changes in body temperature influence the scaling of VO2max and aerobic scope in mammals.

ABSTRACT: Debate on the mechanism(s) responsible for the scaling of metabolic rate with body size in mammals has focused on why the maximum metabolic rate (VO2max ) appears to scale more steeply with body size than the basal metabolic rate (BMR). Consequently, metabolic scope, defined as VO2max/BMR, systematically increases with body size. These observations have led some to suggest that VO2max, and BMR are controlled by fundamentally different processes, and to discount the generality of models that predict a single power-law scaling exponent for the size dependence of the metabolic rate. We present a model that predicts a steeper size dependence for VO2max than BMR based on the observation that changes in muscle temperature from rest to maximal activity are greater in larger mammals. Empirical data support the model's prediction. This model thus provides a potential theoretical and mechanistic link between BMR and VO2 max.

SUBMITTER: Gillooly JF

PROVIDER: S-EPMC2373824 | biostudies-literature | 2007 Feb

REPOSITORIES: biostudies-literature

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Changes in body temperature influence the scaling of VO2max and aerobic scope in mammals.

Gillooly James F JF Allen Andrew P AP

Biology letters 20070201 1

Debate on the mechanism(s) responsible for the scaling of metabolic rate with body size in mammals has focused on why the maximum metabolic rate (VO2max ) appears to scale more steeply with body size than the basal metabolic rate (BMR). Consequently, metabolic scope, defined as VO2max/BMR, systematically increases with body size. These observations have led some to suggest that VO2max, and BMR are controlled by fundamentally different processes, and to discount the generality of models that pred ...[more]

PMID: 17443976

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Project description:The Aerobic Scope (AS), which reflects the functional capacity for biological fitness, is a highly relevant proxy to determine thermal tolerance in various taxa. Despite the importance of this method, its implementation is often hindered, due to lacking techniques to accurately measure standard- (SMR) and maximal- (MMR) metabolic rates, especially in sluggish marine invertebrates with low oxygen consumption rates, such as sea cucumbers. In this study the AS concept was modified to define a Temperature-induced Aerobic Scope (TAS), based on metabolic rate changes due to temperature adjustments rather than traditionally used physical activity patterns. Consequentially, temperature dependent peak and bottom O2 consumption rates, defined as Temperature-induced Maximal- (TMMR) and Standard Metabolic Rates (TSMR), respectively, served as MMR and SMR alternatives for the sea cucumber Holothuria scabra. TMMR and TSMR were induced through acute temperature change (2°C per hour; 17-41°C) until critical warm (WTcrit) and cold (CTcrit) temperatures were reached, respectively. In addition, Hsp70 gene expression linked to respiration rates served as synergistic markers to confirm critical threshold temperatures. O2 consumption of H. scabra peaked distinctly at WTcrit of 38°C (TMMR = 33.2 ± 4.7 μgO2 g-1 h-1). A clear metabolic bottom line was reached at CTcrit of 22°C (TSMR = 2.2 ± 1.4 μgO2 g-1 h-1). Within the thermal window of 22-38°C H. scabra sustained positive aerobic capacity, with assumed optimal performance range between 29-31.5°C (13.85-18.7 μgO2 g-1 h-1). Between 39-41°C H. scabra decreased respiration progressively, while gene expression levels of Hsp70 increased significantly at 41°C, indicating prioritization of heat shock response (HSR) and homeostatic disruption. At the cold end (17-22°C) homeostatic disruption was visible through incrementally increasing energetic expenses to fuel basal maintenance costs, but no Hsp70 overexpression occurred. TMMR, TSMR and TAS proved to be reliable metrics, similar to the traditional energetic key parameters MMR, SMR and AS, to determine a specific aerobic performance window for the sluggish bottom dwelling species H. scabra. In addition, the linkage between respiration physiology and molecular defense mechanisms showed valuable analytical synergies in terms of mechanistic prioritization as response to thermal stress. Overall, this study will help to define lethal temperatures for aquaculture and to predict the effects of environmental stress, such as ocean warming, in H. scabra.

Project description:Considering that swim-flume or chasing methods fail in the estimation of maximum metabolic rate and in the estimation of Aerobic Scope (AS) of sedentary or sluggish aquatic ectotherms, we propose a novel conceptual approach in which high metabolic rates can be obtained through stimulation of organism metabolic activity using high and low non-lethal temperatures that induce high (HMR) and low metabolic rates (LMR), This method was defined as TIMR: Temperature Induced Metabolic Rate, designed to obtain an aerobic power budget based on temperature-induced metabolic scope which may mirror thermal metabolic scope (TMS = HMR-LMR). Prior to use, the researcher should know the critical thermal maximum (CT max) and minimum (CT min) of animals, and calculate temperature TIMR max (at temperatures -5-10% below CT max) and TIMR min (at temperatures +5-10% above CT min), or choose a high and low non-lethal temperature that provoke a higher and lower metabolic rate than observed in routine conditions. Two sets of experiments were carried out. The first compared swim-flume open respirometry and the TIMR protocol using Centropomus undecimalis (snook), an endurance swimmer, acclimated at different temperatures. Results showed that independent of the method used and of the magnitude of the metabolic response, a similar relationship between maximum metabolic budget and acclimation temperature was observed, demonstrating that the TIMR method allows the identification of TMS. The second evaluated the effect of acclimation temperature in snook, semi-sedentary yellow tail (Ocyurus chrysurus), and sedentary clownfish (Amphiprion ocellaris), using TIMR and the chasing method. Both methods produced similar maximum metabolic rates in snook and yellowtail fish, but strong differences became visible in clownfish. In clownfish, the TIMR method led to a significantly higher TMS than the chasing method indicating that chasing may not fully exploit the aerobic power budget in sedentary species. Thus, the TIMR method provides an alternative way to estimate the difference between high and low metabolic activity under different acclimation conditions that, although not equivalent to AS may allow the standardized estimation of TMS that is relevant for sedentary species where measurement of AS via maximal swimming is inappropriate.

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Changes in body temperature influence the scaling of VO2max and aerobic scope in mammals.

Publications

Changes in body temperature influence the scaling of VO2max and aerobic scope in mammals.

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