Wolfgang Wieser

The energetics of starvation and growth after refeeding in juveniles of three cyprinid species

SynopsisExperiments were conducted to monitor changes in body mass and metabolic energy expenditure before, during, and after periods of starvation in juveniles of three species of cyprinids: Leuciscus cephalus, Chalcalburnus chalcoides mento, and Scardinius erythrophthalmus. During the starvation period all fish lost weight at about the same rate and the total amount of oxygen consumed during an experimental period of 20 h was about 40% lower in the starved than in the fed groups. Upon refeeding, both mass specific maintenance; and routine rates of metabolism as well as relative growth rates increased rapidly, the peaks of these increases being directly proportional to the length of the starvation period. Maximum compensatory growth was observed after four weeks of starvation in C. chalcoides and S. erythrophthalmus, with relative growth rates reaching 30% d-1 during the first measuring interval after refeeding. The pattern of ‘time-dependent compensatory growth’ displayed by these fish is similar to the responses of a colonial hydroid in which the rate of catch-up growth increased with the amount of stress to which the animals had been exposed. The exact cost of compensatory growth cannot be calculated because oxygen consumption and growth were not measured simultaneously. However, on the basis of data and calculations reported by Wieser & Medgyesy (1990) it appears that compensatory growth, if fuelled by the metabolic power indicated by our measurements of oxygen consumption, would have to be about twice as efficient as normal growth in the related species Rutilus rutilus.

Metabolic responses to food deprivation and refeeding in juveniles of Rutilus rutilus (Teleostei: Cyprinidae)

SynopsisEffect of food deprivation and refeeding on metabolic parameters were studied in juvenile Rutilus rutilus, weighing 280–460 mg. Tissue hydration increased with the length of the starvation period, reaching a new steady state after 4–5 weeks. Total protein concentration remained constant at about 60% of dry body mass. The concentration of glycogen decreased during food deprivation, a new steady state being reached at about 30% of control values after 4 weeks. Refeeding caused a dramatic increase of glycogen concentration which exceeded the value in fed controls by 6- to 9-fold. This is seen as a tactic for rapid storage of food energy, to be used later for the synthesis of body materials. With respect to their responses to food deprivation the 12 enzymes investigated formed four groups: (1) activity unaffected by food deprivation or refeeding (COX, THIOL, CK, GOT); (2) activity drops to about 60% of control value during the initial phase of food deprivation but remains constant thereafter (PK, LDH, Pase); (3) slow but continuous decrease in activity during the whole period of starvation, i.e. up to 7 weeks (PFK, OGDH, CS, FBPase); (4) activity increases during food deprivation, decreases again upon refeeding (GPT). A model is discussed which distinguishes between four phases in the general response of young fish to food deprivation and refeeding: stress, transition, adaptation, and recovery.

Influence of temperature and ambient oxygen on the swimming energetics of cyprinid larvae and juveniles

SynopsisThe relationship between respiration and swimming speed of larvae and juveniles (2–100 mg fresh mass) of Danube bleak, Chalcalburnus chalcoides (Cyprinidae), was measured at 15° and 20° C under hypoxic (50% air saturation), normoxic, and hyperoxic (140% air saturation) conditions. In a flow-tunnel equipped with a flow-through respirometer the animals swam at speeds of up to 8 lengths · s-1; speeds were sustained for at least two minutes. The mass specific standard, routine, and active respiration rates declined with increasing body mass at both temperatures. Metabolic intensity increased with temperature, but also the critical swimming speed (at which oxygen uptake reached its maximum) was higher at 20° than at 15° C by about 30%. Nevertheless, the oxygen debt incurred by the fish at the highest speeds was about 40%, and the net cost of swimming about 32%, lower at 20° than at 15°C. The standard metabolic rate was more strongly dependent on temperature (Q10 around 2.5) than the maximum active rate (Q10 below 2). Whereas standard and routine respiration rates were well regulated over the pO2-range investigated (8.5–25.8 kPa), the active rates showed a conformer-like pattern, resulting in factorial scopes for activity between 2 and 4. Under hypoxia, the critical swimming speed was lower than under normoxia by about 1.51 · s-1, but the net cost of swimming was also lower by about 30%. On the other hand, hyperoxia neither increased the swimming performance nor did it lead to a further increase of the metabolic cost of swimming. The hypoxia experiments suggest that in response to lowered tensions of ambient oxygen maintenance functions of metabolism not directly related to swimming may be temporarily reduced, leading to increased apparent swimming efficiency under these conditions. The responses of the larvae of Danube bleak to low temperature and low ambient oxygen are discussed in terms of the metabolic strategies by which energy-limited animals meet the challenge of environmental deterioration.

Coupling of Energy Supply and Energy Demand in Isolated Goldfish Hepatocytes

The allocation of metabolic energy under fluctuating conditions of supply and demand was studied in isolated goldfish hepatocytes. Inhibition of glycolytic ATP production resulted in a decrease in the activity of one of the major ATP consuming components of cellular energy budgets, the sodium pump ((Na⁺, K⁺)-ATPase), because of the removal of substrates for the trichloroacetic acid (TCA) cycle. This was confirmed through restoration of activity to control levels by adding pyruvate and malate to the suspension. Ouabain-sensitive oxygen consumption constituted a fairly constant fraction of 15% to 25% of total oxygen consumption, whereas the relative load exerted by the pump on anaerobic energy metabolism (on the basis of measurements of Rb⁺ flux and lactate production) was much higher, ranging from 90% to 50% during the experimental period. Moreover, when pump activity was inhibited by the addition of ouabain, oxidative energy output decreased immediately, whereas under the restricted conditions of glycolytic energy supply a corresponding ouabain-sensitive component of lactate production was not observed. Such an apparent mismatch between supply and demand ofATP is interpreted as reflecting the flexibility of energy allocation under energy-limiting conditions. When ATP production was reduced by inhibiting either glycolysis or oxidative phosphorylation, the concentration of ATP in the hepatocytes dropped within 30 min from the control steady state to a new, lower, steady state that was maintained for at least 60 min.

Contrasting effects of temperature acclimation on mechanisms of ionic regulation in a eurythermic and a stenothermic species of freshwater fish (Rutilus rutilus and salvelinus alpinus)

Abstract 1. 1. Effects of temperature on aspects of ionic regulation in kidney and gills of Rutilus rutilus and Salvelinus alpinus were studied by a variety of techniques. 2. 2. In the kidney tissue of cold acclimated R. rutilus, the maximal number of binding sites per mg protein (Bmax) and the activity of Na+, K+-ATPase, as well as tissue respiration increased significantly, whereas in S. alpinus no changes in these variables were observed. On the other hand, 86Rb+ efflux from kidney tissue was unaffected by temperature in R. rutilus, whereas it was about 60% lower in 5. alpinus acclimated and measured at 5°C, than in specimens acclimated and measured at 15°C. 3. 3. In both species, the activity of gill Na+, K+-ATPase was 1.5- to 2-fold higher in cold-acclimated than in warm-acclimated fish although Bmax decreased in R. rutilus, but remained constant in S. alpinus. 4. 4. Problems of ionic regulation are discussed with regard to differences in temperature sensitivity of passive flows and primary active transport of ions in the tissues of poikilothermic animals.

Growth and habitat separation in eight cohorts of three species of cyprinids in a subalpine lake

SynopsisDistribution and growth of the embryos, larvae and juveniles of Rutilus rutilus (roach), Scardinius erythrophthalmus (rudd) and Leuciscus cephalus (chub) from an oligotrophic subalpine lake in Tyrol, Austria, were studied during the first three to four months after hatching. R. rutilus was the first to spawn, a single cohort hatching around May 23rd. Four cohorts of S. erythrophthalmus hatched between June 19 and August 1. Three cohorts of L. cephalus hatched between July 3 and 25. The length/weight relationship of all species changed at a length of approximately 15–16 mm. R. rutilus, hatching at the lowest temperature, also showed the lowest growth rate during early life (maximum 10.4 per cent fresh body weight day−1). In the other two species relative growth rates up to 20% day−1) were measured. Rudd and chub remained in the shallow littoral during the whole period of observation, whereas roach left the littoral a few weeks after hatching and migrated into deeper water. A subtle shift in vertical distribution was observed for the first cohort of rudd which moved into slightly deeper water when the second cohort made its appearance.

Effects of Temperature on the (Na⁺ + K⁺)-ATPase and Oxygen Consumption in Hepatocytes of Two Species of Freshwater Fish, Roach (Rutilus rutilus) and Brook Trout (Salvelinus fontinalis)

Effects of temperature on the (Na+ + K+)-ATPase were studied in isolated hepatocytes of two species of freshwater fish acclimated to different temperatures. Binding of 3H+-ouabain to hepatocytes was used to determine the density of (Na+ + K+)-ATPase, and oxygen consumption was measured to estimate the cost of cation pumping. Intracellular sodium concentration was manipulated by incubating hepatocytes at 20°C or 0°-4°C before the measurement of oxygen consumption. In hepatocytes of Rutilus rutilus, the maximal number of ouabain binding sites per 10⁶ cells (Bmax) was 1.86 times higher in the 5° C- acclimated than in the 20° C-acclimated group. The equilibrium dissociation constants (Kds) in both acclimation groups were not statistically different. In Salvelinus fontinalis, Bmax and Kd values did not change with temperature acclimation. Ouabain-sensitive oxygen consumption (OS) in hepatocytes of R. rutilus was 1.60-1. 73 times higher in the cold- than in the warm-acclimated group. In S. fontinalis, acclimation temperature did not affect OS. On the other hand, cold preincubation of hepatocytes significantly increased OS in both acclimation groups and species. Results are discussed with regard to species-specific differences in the adaptation to temperature change at the cellular level, the main point being that in response to cold-acclimation R. rutilus adjusts the activity of the (Na+ + K+)-ATPase in a compensatory fashion, whereas S. fontinalis modulates passive ion leakage.

Epilogue: food and feeding, ecomorphology, energy assimilation and conversion in cyprinids

The roach, Rutilus rutilus, may be used as an example for illustrating the scope of the mechanistic and comparative approach to community ecology alluded to in the Introduction. This species has been dealt with, in one way or the other, in 14 of the 21 papers collected in this special issue. How does the information conveyed in these papers relate to the functional role of the roach in European lake and stream ecosystems, and in what way might a deeper knowledge of the reaction norms of this and other species influence the construction of models of population ecology and biological interactions? Overall the roach is the most successful generalist fish in Central European freshwater habitats, occurring in all types of lotic and lentic water bodies in which the summer temperature attains mean levels of at least 15°C. How can this success be explained? What are the biological attributes of a successful generalist within a large group of similar species? Biological success may be evaluated in terms of a species’ ability to: (1) find and incorporate food, (2) assimilate energy, (3) use energy in processes related to fitness, especially growth (in the early life phase) and reproduction, and (4) reduce predation pressure.

Chapter 6 Effects of temperature on cellular ion regulation and membrane transport systems

Publisher Summary The preservation of ionic balance, despite the direct effects of temperature upon metabolism, is of critical importance to the cells of poikilothermic animals. Because temperature differentially affects the transport mechanisms involved in ion balance, changes in the body temperature of poikilothermic animals, such as fish, may disturb the normal cellular steady state. Cells can respond adaptively to this thermal disturbance by adjustments to the transporting apparatus but these responses may be complex and do not necessarily lead to the maintenance of the status quo ante in respect of cell volume, ion balance or the associated energetic costs. From the animals point of view the most appropriate result is one that takes account of the adaptive needs of the animal in relation to the provision of a positive energy balance as well as of maintained physiological performance. When energy intake is limited, during the winter or during periods of enforced inactivity, then cellular pump activity may be reduced thereby lowering transmembrane ion gradients. This chapter discusses the strategies that animal cells might follow and the circumstances under which they would be adaptive. It then discusses the potential mechanisms by which the individual transport systems are adjusted and the evidence in favor of them.

Interactive effects of season and temperature on enzyme activities, tissue and whole animal respiration in roach, Rutilus rutilus

SynopsisThis paper reviews investigations on the ecophysiology of a population of roach, Rutilus rutilus, from a subalpine oligotrophic lake in the Austrian Tirol. Metabolic responses to season and temperature were studied in whole animals, tissues and selected enzymes. The exponent of the relationship between body mass and three levels of the metabolic rate of acclimated fish was 0.82 ± 0.02, 0.60 ± 0.15, and 0.75 ± 0.01 at 4, 12, and 20° C respectively. Various combinations of long-term acclimation to constant or seasonally fluctuating temperatures and long-term (up to 14 days) monitoring of O2 at the acclimation temperature led to the conclusion that the aerobic power of fish swimming in the routine mode does not show any sign of being temperature compensated. On the other hand, there are several indications that the energy expenditure of spontaneously swimming fish is adjusted to the seasonal pattern of environmental change and that these responses of metabolism and behaviour are controlled by both endogenous and exogenous factors. The rate of oxygen consumption of gill and muscle tissue ‘brei’ from fish caught during a seasonal cycle and measured at 15° C appears to follow closely the reproductive and gonadal cycle of the living fish. The same holds for the activities of phosphofructokinase, acetoacetyl-CoA thiolase, and cytochrome oxidase. On the other hand, the Na+, K+-ATPase of the kidney shows near perfect temperature compensation when fish acclimated to 5 and 25° C are compared, whereas an equally pronounced case of inverse temperature acclimation has been reported for the activity of digestive enzymes in the gut. Summarizing these data it is pointed out that the temperature relationship of a poikilothermic organism is the sum of often very diverse temperature relationships of specific metabolic and behavioural functions. In the case of the roach, strong effects of acclimation temperature on the molecular level, sometimes in the opposite direction, combine with seasonal effects on enzyme activities and tissue respiration. However, on the whole animal level the fish behave as strictly non-compensating poikilotherms, the reproductive cycle being the only detectable influence capable of modulating the basic temperature relationship of energy expenditure.