Temperature-dependent metabolism in Antarctic fish: Do habitat temperature conditions affect thermal tolerance ranges?

Polar Biology, Apr 2016

Climatic warming is most pronounced in the polar regions. For marine ectotherms such as fish, temperature is a key abiotic factor, influencing metabolic processes. Species distribution and abundance are driven by reproduction and growth, which depend on available energy exceeding baseline maintenance costs. These routine metabolic costs make up a large part of the energy expenditure. Thermal stress can increase routine metabolism, affecting an organism’s fitness. Data of routine metabolic rates of Antarctic fish are scarce, and comparability of existing data sets is often problematic due to ecological differences between species and in experimental protocols. Our objective was to compare routine metabolism and thermal sensitivity of species with similar ecotypes but different thermal environments to assess possible ecological implications of warming waters on energy expenditure in Antarctic fish, a fauna characterised by geographic isolation, endemism and putative thermal adaptation. We measured routine metabolic rates of three benthic Antarctic fish species from low- and high-Antarctic regions at habitat temperature and during acute temperature increase. Our analysis revealed differences in metabolic rates at the same temperature suggesting local adaptation to habitat temperature. Acute thermal stress induced a comparable response of metabolic rates to increasing temperature. We conclude that higher metabolic rates and thus higher energetic costs could be associated with narrower thermal windows, a potential disadvantage to the endemic high-Antarctic fish fauna facing the challenge of climate change.

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Temperature-dependent metabolism in Antarctic fish: Do habitat temperature conditions affect thermal tolerance ranges?

Temperature-dependent metabolism in Antarctic fish: Do habitat temperature conditions affect thermal tolerance ranges? Tina Sandersfeld 0 1 2 3 Felix C. Mark 0 1 2 3 Rainer Knust 0 1 2 3 0 Department of Marine Zoology , BreMarE - Bremen Marine Ecology, FB 2 , University of Bremen , Leobener Str. NW2, 28359 Bremen , Germany 1 Helmholtz Center for Polar and Marine Research, Alfred Wegener Institute , Am Alten Hafen 26, 27568 Bremerhaven , Germany 2 & Tina Sandersfeld 3 Present Address: Institute for Hydrobiology and Fisheries Science, University of Hamburg , Olbersweg 24, 22767 Hamburg , Germany Climatic warming is most pronounced in the polar regions. For marine ectotherms such as fish, temperature is a key abiotic factor, influencing metabolic processes. Species distribution and abundance are driven by reproduction and growth, which depend on available energy exceeding baseline maintenance costs. These routine metabolic costs make up a large part of the energy expenditure. Thermal stress can increase routine metabolism, affecting an organism's fitness. Data of routine metabolic rates of Antarctic fish are scarce, and comparability of existing data sets is often problematic due to ecological differences between species and in experimental protocols. Our objective was to compare routine metabolism and thermal sensitivity of species with similar ecotypes but different thermal environments to assess possible ecological implications of warming waters on energy expenditure in Antarctic fish, a fauna characterised by geographic isolation, endemism and putative thermal adaptation. We measured routine metabolic rates of three benthic Antarctic fish species from low- and high-Antarctic regions at habitat temperature and during acute temperature increase. Our analysis revealed differences in metabolic rates at the same temperature suggesting local adaptation to habitat temperature. Acute thermal stress induced a comparable response of metabolic rates to increasing temperature. We conclude that higher metabolic rates and thus higher energetic costs could be associated with narrower thermal windows, a potential disadvantage to the endemic high-Antarctic fish fauna facing the challenge of climate change. Routine metabolic rate; Polar fish; Notothenioids; Metabolic cold adaptation; Respiration Introduction The polar regions comprise some of the ‘‘hot spots’’ of climatic warming. Around the Western Antarctic Peninsula, surface waters have risen in temperature about 1 C in the second half of the twentieth century and around South Georgia a temperature increase of 2.3 C has been recorded within the last 81 years (Meredith and King 2005; Whitehouse et al. 2008) . Although temperature changes have not yet been recorded for high-Antarctic regions such as the Weddell Sea, water temperature increases of up to 2 C have been projected by the year 2100 also for these areas (Hellmer et al. 2012; Turner et al. 2014) . Temperature is an abiotic key factor. In some ectotherms, such as many fish species, body temperature is determined by ambient temperature, affecting metabolic processes. The thermal tolerance window of a species yields insight into physiological plasticity regarding changes in ambient temperature. According to the concept of oxygen and capacity limited thermal tolerance (OCLTT) (Po¨ rtner 2012) , the temperature window of an organism is defined by the upper and lower critical and pejus temperatures. At a species’ optimal temperature, low maintenance costs and maximised aerobic scope were found to come along with high growth rates (Koehn and Shumway 1982; Wieser 1994; Brodte et al. 2006) . Even though supporting evidence for the OCLTT concept was found in various species (Mark et al. 2002; Lannig et al. 2004; Po¨ rtner et al. 2004) , its general applicability and how to measure it has been still discussed in the recent literature (Clark et al. 2013; Norin et al. 2014) . Fish play an important role in Antarctic food webs. Being predator and prey alike, they serve as an important link between lower and higher trophic levels (Hureau 1994) . The Southern Ocean has been an oceanographically isolated and thermally very stable environment over geological time scales, leading to the evolution of an endemic Antarctic fish fauna with highly stenothermal species. Antarctic fish exhibit different adaptations to their constantly cold environment, such as a lack of heat shock response, expression of anti-freeze glycoproteins, a lack of haemoglobin and myoglobin, higher mitochondrial densities as well as other compensatory adaptations of the heart and circulatory system (e.g. DeVries and Eastman 1981; Coppes Petricorena and Somero 2007) . Compared to temperate species that experience broader environmental temperature fluctuations, Antarctic fish have very narrow temperature windows (Somero and DeVries 1967; Van Dijk et al. 1999; Brodte et al. 2006) . However, habitat temperature does not only vary on global s (...truncated)


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Tina Sandersfeld, Felix C. Mark, Rainer Knust. Temperature-dependent metabolism in Antarctic fish: Do habitat temperature conditions affect thermal tolerance ranges?, Polar Biology, 2017, pp. 141-149, Volume 40, Issue 1, DOI: 10.1007/s00300-016-1934-x