Comparative analyses of metabolic responses to temperature and starvation in the freshwater species, roach, Rutilus rutilus (L.), and burbot, Lota lota (L.)

In temperate habitats, seasonal temperature cycles correlate with patterns of feeding and fasting in fish which therefore require strategies of behavioural and metabolic adaptations. To examine starvation strategies of fish exposed to seasonal temperature fluctuations, comparative investigations on fasting metabolism were conducted in the freshwater fish, roach, Rutilus rutilus (L.), and burbot, Lota lota (L.). Roach is classified as a typical winter-fasting species, wehereas the unusual thermal tolerance of cold-active burbot, the only freshwater representative of the marine gadoid family, results in a restricted locomotory and foraging behaviour in summer. Starvation provoked, as a common pattern, negative growth rates in both species. The responses to starvation, however, were temperature-dependent and displayed species-specific differences. Oxygen consumption measurements in cold (CA, 4°C) and warm acclimated (WA, 20°C) fish revealed a higher thermal sensitivity of roach (Q10 = 2.7) than burbot (Q10 = 1.9). Starvation provoked more marked alterations in WA specimen. While WA roach showed a delayed response to starvation, the metabolic rate became immediately depressed upon the onset of starvation in WA burbot (metabolic depression). Allocation and consumption of endogenous energy reserves (glycogen, lipid and protein) were quantified by biochemical mobilisation and degradation rates in liver and muscle tissue of CA and WA animals. During starvation, energy consumption was closely correlated with the natural fasting periods of the species. Energy turnover was lowest in CA roach and WA burbot, respectively, and was coupled with an energy efficient allocation of body fuels. In CA roach, fasting metabolism was characterised by a sequential pattern of mobilisation with initial utilisation of hepatic body fuels before drawing mainly on muscle lipid. In burbot, high hepatic lipid reserves account for half of the energy allocation during starvation, supporting high energy turnover in active CA fish while enabling WA burbot to sustain fasting periods in spite of high temperatures. At the cellular level, thermal and nutritional effects on aerobic and oxidative energy metabolism were characterised by analyses of mitochondrial respiration, citrate synthase activity, protein: RNA ratios and intracellular pH. In roach, regulatory adjustments of aerobic and biosynthetic capacities did not become apparent in response to changes in temperature and feeding regime. In contrast, thermal compensation of cellular capacities occurred in burbot. Aerobic and biosynthetic capacities were markedly elevated at low temperatures providing the basis for cold water preference of burbot. Thermal constraints, however, were evident in burbot at high temperatures facilitating metabolic depression at the organismic level. In conclusion, the combined analyses at different levels of biological organisation revealed differential thermal tolerances in roach and burbot that contribute markedly to regulatory adjustments involved in species-specific fasting metabolism. In roach, the winter-fasting strategy appears to be a highly efficient metabolic adaptation to suboptimal environmental conditions. In burbot, the summer-fasting strategy reduced aerobic scope due to the down-regulation of cellular capacities triggering metabolic depression and reductions in energetic costs. The results of the study further highlight the utility of comparative approaches to reveal similarities and differences in biological functions and processes.