1.  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.

2.  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.

3.  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.

4.  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.