Elevated temperature causes metabolic trade-offs at the whole organism level in the Antarctic fish Trematomus bernacchii

Abstract

As a response to ocean warming, shifts in fish species distribution and changes in production have been reported that have been partly attributed to temperature effects on the physiology of animals. The Southern Ocean hosts some of the most rapidly warming regions on earth and Antarctic organisms are reported to be especially temperature sensitive. While cellular and molecular organismic levels appear, at least partially, to compensate for elevated temperatures, the consequences of acclimation to elevated temperature for the whole organism are often less clear. Growth and reproduction are the driving factors for population structure and abundance. The aim of this study was to assess the effect of long-term acclimation to elevated temperature on energy budget parameters in the highAntarctic fish Trematomus bernacchii. Our results show a complete temperature compensation for routine metabolic costs after 9 weeks of acclimation to 4°C. However, an up to 84% reduction in mass growth was measured at 2 and 4°C compared with the control group at 0°C, which is best explained by reduced food assimilation rates at warmer temperatures. With regard to a predicted temperature increase of up to 1.4°C in the Ross Sea by 2200, such a significant reduction in growth is likely to affect population structures in nature, for example by delaying sexual maturity and reducing production, with severe impacts on Antarctic fish communities and ecosystems.

Cardiorespiratory responses in an Antarctic fish suggest limited capacity for thermal acclimation

“…In addition, the time scale of imposed changes and the consequent trade-off among, for example, cardiovascular responses and growth/reproduction may alter opinion as more data are gathered (Beers and Jayasundara, 2015). For example, Trematomus bernacchii acclimated to 4°C reduced growth by 84% and suffered a mortality rate of 33% (Sandersfeld et al, 2015). We therefore conclude that although nototheniids may not be as Atropine, muscarinic receptor blockade; atropine+propranolol, complete autonomic receptor blockade.…”

Antarctic emerald rockcod have the capacity to compensate for warming when uncoupled from CO2‐acidification

“…As predicted, several aspects of cardiorespiratory physiology including heart rate ( f H ), ventilation rate ( f V ), and metabolic rate () significantly increased with warming. Most noteworthy, juvenile Trematomus bernacchii demonstrated a degree of thermal compensation and temperature acclimation that was much quicker than observed in the adults under Ambient P CO 2 (Enzor et al., , ; Jayasundara et al., ; Sandersfeld et al., ). The addition of elevated P CO 2 , however, appeared to create an interacting additive effect on hyperventilation, and a potential synergistic effect on (i.e., lower capacity for temperature acclimation when exposed to elevated P CO 2 ).…”

“…Simulated models project that the duration of low pH events in winter may increase in McMurdo Sound, thus exposing marine organisms to deleterious levels of pH for longer periods (Kapsenberg, Kelley, Shaw, Martz, & Hofmann, ). There are numerous studies investigating the effects of high temperature on the physiology of adult Antarctic fishes (Beers & Jayasundara, ; Bilyk & DeVries, ; Egginton & Campbell, ; Peck, Morley, Richard, & Clark, ; Sandersfeld, Davison, Lamare, Knust, & Richter, ; Sandersfeld, Mark, & Knust, ; Seebacher, Davison, Lowe, & Franklin, ; Somero & Hochachka, ; Weinstein & Somero, ); however, there are considerably fewer studies focused on how Antarctic fishes may respond to elevated P CO 2 , and the effects of elevated P CO 2 and temperature concurrently, with the focus on adult fishes (Enzor, Hunter, & Place, ; Enzor & Place, ; Enzor, Zippay, & Place, ; Strobel, Graeve, Pörtner, & Mark, ; Strobel, Leo, Pörtner, & Mark, ; Strobel et al., ) and only one study on an early life stage (i.e., embryos, Flynn, Bjelde, Miller, & Todgham, ). Since sensitivity to environmental stressors can vary across ontogeny (Hamdoun & Epel, ; Pörtner & Peck, ), we cannot predict species vulnerability to ocean changes of elevated P CO 2 and temperature by only evaluating sensitivity to change in adults.…”

“…Studies assessing the physiological impacts of warming on Antarctic fishes in the Nototheniidae family have shown changes to cardiorespiratory and metabolic performance (Egginton & Campbell, ; Enzor et al., , ; Franklin, Davison, & Seebacher, ; Jayasundara, Healy, & Somero, ; Seebacher et al., ); however, the degree of vulnerability and acclimation capacity may be species‐specific (Egginton & Campbell, ; Franklin et al., ; Jayasundara et al., ; Robinson & Davison, ,b; Seebacher et al., ). For example, studies of the emerald rockcod, Trematomus bernacchii , a dominant benthic species by biomass in the Ross Sea (Vacchi, La Mesa, & Greco, ), have demonstrated impacts of warming across several levels of organization, including limitations in cardiac performance (Jayasundara et al., ), sustained elevated metabolic costs (Enzor et al., , ), aerobic to anaerobic fuel switching (Enzor et al., ; Jayasundara et al., ), mitochondria break temperatures (Weinstein & Somero, ), a twofold increase in brain oxygen (O 2 ) consumption (Somero & DeVries, ), and up to an 85% reduction in growth (Sandersfeld et al., ). In comparison, the bald notothen Pagothenia borchgrevinki has exhibited less sensitivity to warming, demonstrating partial compensation for increased metabolic rates (Enzor et al., , ) and a greater capacity to cope marked by modifications in cardiorespiratory and metabolic adjustments (Franklin et al., ; Robinson & Davison, ,b; Seebacher et al., ).…”

Juvenile Antarctic rockcod,Trematomus bernacchii, are physiologically robust to CO2–acidified seawater

“…Several studies have characterized the physiological response of adult T. bernacchii to various environmental changes, including temperature (Todgham et al, 2007;Buckley andSomero, 2009: Jayasundara et al, 2013;Sandersfeld et al, 2015), hypoxia (Davison et al, 1994) and toxicants (Regoli et al, 2005;Borghesi et al, 2008), with recent work on the effects of elevated P CO2 (Enzor et al, 2013;Enzor and Place, 2014). There remains no information on physiological performance of earlier life-history stages in this species.…”