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Abstract Notothenioidei fishes have evolved under stable cold temperatures; however, ocean conditions are changing globally, with polar regions poised to experience the greatest changes in environmental factors, such as warming. These stressors have the potential to dramatically affect energetic demands, and the persistence of the notothenioids will be dependent on metabolic capacity, or the ability to match energy supply with energy demand, to restore homeostasis in the face of changing climate conditions. In this study we examined aerobic metabolic capacity in three species,Trematomus bernacchii,T. pennelliiandT. newnesi, and between two life stages, juvenile and adult, by assessing mitochondrial function of permeabilized cardiac fibers. Respiratory capacity differed among the adult notothenioids in this study, with greater oxidative phosphorylation (OXPHOS) respiration in the pelagicT. newnesithan the benthicT. bernacchiiandT. pennellii. The variation in mitochondrial respiratory capacity was likely driven by differences in the mitochondrial content, as measured by citrate synthase activity, which was the highest inT. newnesi. In addition to high OXPHOS,T. newnesiexhibited lower LEAK respiration, resulting in greater mitochondrial efficiency than eitherT. bernacchiiorT. pennellii. Life stage largely had an effect on mitochondrial efficiency and excess complex IV capacity, but there were little differences in OXPHOS respiration and electron transfer capacity, pointing to a lack of significant differences in the metabolic capacity between juveniles and adults. Overall, these results demonstrate species-specific differences in cardiac metabolic capacity, which may influence the acclimation potential of notothenioid fishes to changing environmental conditions. 

Synopsis Antarctic fishes have evolved under stable, extreme cold temperatures for millions of years. Adapted to thrive in the cold environment, their specialized phenotypes will likely render them particularly susceptible to future ocean warming and acidification as a result of climate change. Moving from a period of stability to one of environmental change, species persistence will depend on maintaining energetic equilibrium, or sustaining the increased energy demand without compromising important biological functions such as growth and reproduction. Metabolic capacity to acclimate, marked by a return to metabolic equilibrium through physiological compensation of routine metabolic rate (RMR), will likely determine which species will be better poised to cope with shifts in environmental conditions. Focusing on the suborder Notothenioidei, a dominant group of Antarctic fishes, and in particular four well-studied species, Trematomus bernacchii, Pagothenia borchgrevinki, Notothenia rossii, and N. coriiceps, we discuss metabolic acclimation potential to warming and CO2-acidification using an integrative and comparative framework. There are species-specific differences in the physiological compensation of RMR during warming and the duration of acclimation time required to achieve compensation; for some species, RMR fully recovered within 3.5 weeks of exposure, such as P. borchgrevinki, while for other species, such as N. coriiceps, RMR remained significantly elevated past 9 weeks of exposure. In all instances, added exposure to increased PCO2, further compromised the ability of species to return RMR to pre-exposure levels. The period of metabolic imbalance, marked by elevated RMR, was underlined by energetic disturbance and elevated energetic costs, which shifted energy away from fitness-related functions, such as growth. In T. bernacchii and N. coriiceps, long duration of elevated RMR impacted condition factor and/or growth rate. Low growth rate can affect development and ultimately the timing of reproduction, severely compromising the species’ survival potential and the biodiversity of the notothenioid lineage. Therefore, the ability to achieve full compensation of RMR, and in a short-time frame, in order to avoid long term consequences of metabolic imbalance, will likely be an important determinant in a species’ capacity to persist in a changing environment. Much work is still required to develop our understanding of the bioenergetics of Antarctic fishes in the face of environmental change, and a targeted approach of nesting a mechanistic focus in an ecological and comparative framework will better aid our predictions on the effect of global climate change on species persistence in the polar regions.