Angela Sommer

Temperature induced anaerobiosis in two populations of the polychaete worm Arenicola marina (L.)

Abstract Temperature dependent changes in the mode of energy metabolism and in acid-base status were studied in the range from −1.7 to 26 °C in two populations of Arenicola marina collected in summer as well as in winter from intertidal flats of the North Sea (boreal) and the White Sea (subpolar). Extreme temperatures led to an accumulation of anaerobic end products, indicating the existence of both a low and a high critical temperature, beyond which anaerobic metabolism becomes involved in energy production. In summer animals from the North Sea the high critical temperature was found at temperatures above 20 °C, and the low critical temperature below 5 °C. Latitudinal or seasonal cold adaptation lead to a more or less parallel shift of both high and low critical temperature values to lower values. Between critical temperatures intracellular pH declined with rising temperature. Slopes varied between −0.012 and −0.022 pH- units/°C. In summer animals from the North Sea, the slope was slightly less than in White Sea animals, but differences appeared independent of the season. However, slopes were no longer linear beyond critical temperatures. A drop in intracellular pH at low temperatures coincided with the accumulation of volatile fatty acids in the body wall tissue of North Sea animals. A failure of active pHi adjustment is held responsible for the reduced ΔpHi/ΔT at temperatures above the high critical temperature. Extracellular pH was kept constant over the whole temperature range investigated. The ability of North Sea animals to adapt to temperatures beyond the critical temperature is poor compared to White Sea specimens. The larger range of temperature fluctuations at the White Sea is seen as a reason for the higher adaptational capacity of the subpolar animals. A hypothesis is proposed that among other mechanisms critical temperature values are set by an adjustment of mitochondrial density and thus, aerobic capacity.

Mitochondrial function in seasonal acclimatization versus latitudinal adaptation to cold in the lugworm Arenicola marina (L.).

Previous studies in marine ectotherms from a latitudinal cline have led to the hypothesis that eurythermal adaptation to low mean annual temperatures is energetically costly. To obtain more information on the trade‐offs and with that the constraints of thermal adaptation, mitochondrial functions were studied in subpolar lugworms (Arenicola marina L.) adapted to summer cold at the White Sea and were compared with those in boreal specimens from the North Sea, either acclimatized to summer temperatures or to winter cold. During summer, a comparison of mitochondria from subpolar and boreal worms revealed higher succinate oxidation rates and reduced Arrhenius activation energies (Ea) in state 3 respiration at low temperatures, as well as higher proton leakage rates in subpolar lugworms. These differences reflect a higher aerobic capacity in subpolar worms, which is required to maintain motor activity at low but variable environmental temperatures—however, at the expense of an elevated metabolic rate. The lower activity of citrate synthase (CS) found in subpolar worms may indicate a shift in metabolic control within mitochondria. In contrast, acclimatization of boreal lugworms to winter conditions elicited elevated mitochondrial CS activities in parallel with enhanced mitochondrial respiration rates. With falling acclimation temperatures, the significant Arrhenius break temperature in state 3 respiration (11°C) became insignificant (5°C) or even disappeared (0°C) at lower levels of Arrhenius activation energies in the cold, similar to a phenomenon known from hibernating vertebrates. The efficiency of aerobic energy production in winter mitochondria rose as proton leakage in relation to state 3 decreased with cold acclimation, indicated by higher respiratory control ratio values and increased adenosine diphosphate/oxygen (ADP/O) ratios. These transitions indicate reduced metabolic flexibility, possibly paralleled by a loss in aerobic scope and metabolic depression during winter cold. Accordingly, these patterns contrast those found in summer‐active, cold‐adapted eurytherms at high latitudes.