Maximum (aerobic) metabolic rate (MMR) is defined here as the maximum rate of oxygen consumption (ṀO 2max ) that a fish can achieve at a given temperature under any ecologically relevant circumstance. Different techniques exist for eliciting MMR of fishes, of which swim-flume respirometry (critical swimming speed tests and burst-swimming protocols) and exhaustive chases are the most common. Available data suggest that the most suitable method for eliciting MMR varies with species and ecotype, and depends on the propensity of the fish to sustain swimming for extended durations as well as its capacity to simultaneously exercise and digest food. MMR varies substantially (>10 fold) between species with different lifestyles (i.e. interspecific variation), and to a lesser extent (
Climate warming is predicted to negatively impact fish populations through impairment of oxygen transport systems when temperatures exceed those which are optimal for aerobic scope (AS). This concept of oxygen-and capacity-limited thermal tolerance (OCLTT) is rapidly gaining popularity within climate change research and has been applied to several fish species. Here, we evaluated the relevance of aerobic performance of juvenile barramundi (Lates calcarifer) in the context of thermal preference and tolerance by (1) measuring standard and maximum metabolic rates (SMR and MMR, respectively) and AS of fish acclimated to 29°C and acutely exposed to temperatures from 23 to 38°C, (2) allowing the fish to behaviourally select a preferred temperature between 29 and 38°C, and (3) quantifying alterations to AS after 5 weeks of acclimation to 29 and 38°C. SMR and MMR both increased continuously with temperature in acutely exposed fish, but the increase was greater for MMR such that AS was highest at 38°C, a temperature approaching the upper lethal limit (40-41°C). Despite 38°C eliciting maximum AS, when given the opportunity the fish selected a median temperature of 31.7±0.5°C and spent only 10±3% of their time at temperatures >36°C. Following acclimation to 38°C, AS measured at 38°C was decreased to the same level as 29°C-acclimated fish measured at 29°C, suggesting that AS may be dynamically modulated independent of temperature to accommodate the requirements of daily life. Together, these results reveal limited power of the OCLTT hypothesis in predicting optimal temperatures and effects of climate warming on juvenile barramundi.
SUMMARYStandard metabolic rate (SMR) and active metabolic rate (AMR) are two fundamental physiological parameters providing the floor and ceiling in aerobic energy metabolism. The total amount of energy available within these two parameters confines constitutes the absolute aerobic scope (AAS). Previous studies on fish have found SMR to closely correlate with dominance and position in the social hierarchy, and to be highly repeatable over time when fish were provided an ad libitum diet. In this study we tested the temporal repeatability of individual SMR, AMR and AAS, as well as repeatability of body mass, in young brown trout (Salmo trutta L.) fed a moderately restricted diet (0.5-0.7% fish mass day -1 ). Metabolism was estimated from measurements of oxygen consumption rate (M O2 ) and repeatability was evaluated four times across a 15-week period. Individual body mass was highly repeatable across the entire 15 week experimental period whereas residual body-mass-corrected SMR, AMR and AAS showed a gradual loss of repeatability over time. Individual residual SMR, AMR and AAS were significantly repeatable in the short term (5 weeks), gradually declined across the medium term (10 weeks) and completely disappeared in the long term (15 weeks). We suggest that this gradual decline in repeatability was due to the slightly restricted feeding regime. This is discussed in the context of phenotypic plasticity, natural selection and ecology.
One contribution of 13 to a theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.Basal or standard metabolic rate reflects the minimum amount of energy required to maintain body processes, while the maximum metabolic rate sets the ceiling for aerobic work. There is typically up to three-fold intraspecific variation in both minimal and maximal rates of metabolism, even after controlling for size, sex and age; these differences are consistent over time within a given context, but both minimal and maximal metabolic rates are plastic and can vary in response to changing environments. Here we explore the causes of intraspecific and phenotypic variation at the organ, tissue and mitochondrial levels. We highlight the growing evidence that individuals differ predictably in the flexibility of their metabolic rates and in the extent to which they can suppress minimal metabolism when food is limiting but increase the capacity for aerobic metabolism when a high work rate is beneficial. It is unclear why this intraspecific variation in metabolic flexibility persists-possibly because of trade-offs with the flexibility of other traits-but it has consequences for the ability of populations to respond to a changing world. It is clear that metabolic rates are targets of selection, but more research is needed on the fitness consequences of rates of metabolism and their plasticity at different life stages, especially in natural conditions. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.
Temperature-induced limitations on the capacity of the cardiorespiratory system to transport oxygen from the environment to the tissues, manifested as a reduced aerobic scope (maximum minus standard metabolic rate), have been proposed as the principal determinant of the upper thermal limits of fishes and other waterbreathing ectotherms. Consequently, the upper thermal niche boundaries of these animals are expected to be highly sensitive to aquatic hypoxia and other environmental stressors that constrain their cardiorespiratory performance. However, the generality of this dogma has recently been questioned, as some species have been shown to maintain aerobic scope at thermal extremes. Here, we experimentally tested whether reduced oxygen availability due to aquatic hypoxia would decrease the upper thermal limits (i.e. the critical thermal maximum, CT max ) of the estuarine red drum (Sciaenops ocellatus) and the marine lumpfish (Cyclopterus lumpus). In both species, CT max was independent of oxygen availability over a wide range of oxygen levels despite substantial (>72%) reductions in aerobic scope. These data show that the upper thermal limits of waterbreathing ectotherms are not always linked to the capacity for oxygen transport. Consequently, we propose a novel metric for classifying the oxygen dependence of thermal tolerance; the oxygen limit for thermal tolerance (P CTmax ), which is the water oxygen tension (Pw O2 ) where an organism's CT max starts to decline. We suggest that this metric can be used for assessing the oxygen sensitivity of upper thermal limits in water-breathing ectotherms, and the susceptibility of their upper thermal niche boundaries to environmental hypoxia.
Summary Individual differences in metabolic rate have been linked with variations in behaviour and key life‐history traits and can affect ecological patterns within animal populations. Yet, almost nothing is known of the plasticity of the metabolic response under dynamically changing conditions that are representative of the natural environment. This is surprising since the capacity for animals to cope with rapidly changing environments depends on phenotypic variation and plasticity among members of the population. We measured the standard metabolic rate (SMR), maximum metabolic rate (MMR) and aerobic scope (AS) of 60 juvenile barramundi (Lates calcarifer) under acclimation conditions (35 ppt salinity, 29 °C, normoxia) and when the fish were sequentially faced with low salinity (10 ppt), high temperature (35 °C) and hypoxia (45% air saturation) with each treatment separated by ∼12 days. The overall degree of interindividual variation in body‐mass‐standardised SMR, MMR and AS changed with environmental conditions, and a metabolic coupling was revealed between SMR and MMR when the fish were faced with the environmental changes. The metabolic response to environmental change differed widely and predictably at an individual level. Individuals that had elevated metabolic attributes under acclimation conditions showed little change in SMR, MMR or AS in response to low salinity and high temperature, but MMR and AS were greatly depressed by hypoxia. In contrast, individuals with low‐metabolic attributes under acclimation conditions displayed a substantial increase in SMR, MMR and AS in response to high temperature and (to a lesser extent) low salinity, but hypoxia had very little effect. These findings reveal how phenotypic diversity in key physiological traits can create differential plasticity towards environmental change within a population by showing how individual fish can remain metabolically insensitive to one environmental stressor at the cost of being highly sensitive to another.
Highly active animals require a high aerobic capacity (i.e., a high maximum metabolic rate [MMR]) to sustain such activity, and it has been speculated that a greater capacity for aerobic performance is reflected in larger organs, which serve as energy processors but are also expensive to maintain and which increase the minimal cost of living (i.e., the basal or standard metabolic rate [SMR]). In this study, we assessed the extent of intraspecific variation in metabolic rate within a group of brown trout (Salmo trutta L.) and tested whether the observed variation in residual (body-mass-corrected) SMR, MMR, and absolute aerobic scope could be explained by variations in the residual size (mass) of metabolically active internal organs. Residual SMR was found to correlate positively with residual MMR, indicating a link between these two metabolic parameters, but no relationship between organ mass and metabolic rate was found for liver, heart, spleen, intestine, or stomach. Instead, activity in the liver of two aerobic mitochondrial enzymes, cytochrome c oxidase and, to a lesser extent, citrate synthase, was found to correlate with whole-animal metabolic rate, indicating that causes for intraspecific variation in the metabolic rate of fish can be found at a lower organizational level than organ size.
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