Partitioning of Energy in Fish: Can Reduction of Swimming Activity Compensate for the Cost of Production?

That reduction of locomotor activity may compensate for costs of production was shown long ago in homoeotherms. After fertilization, female rats reduce their bouts of running in an exercising cage to such an extent that the amount of energy thus saved compensates for the cost of producing the new litter (Wang, 1925a,b; Slonaker, 1925). The mechanism responsible for this homoeostatic effect has never been explained but neurohumoural factors are certainly involved since adjustment of the level of activity is fairly rapid. However, the possibility remains that the regulation of body temperature may be part of the overall mechanism through which the stabilization of heat dissipation in warm blooded animals is achieved. Such a function of body temperature has been discussed in connection with the control of food intake (Anand, 1961). In order to assess the role of body temperature as a general regulatory agent it would be pertinent to ask whether the inverse relationship between production and locomotor activity also occurs in poikilothermic animals. Additionally, such a question would address the more general problem of energy partitioning in poikilotherms. This has recently become a very popular issue (e.g. Townsend & Calow, 1981) in which, however, the energy costs of locomotor activity are rarely considered.

We have approached the problem by concurrently measuring oxygen consumption and swimming activity, in groups of roach (Rutilus rutilus), by means of a new video activity monitoring processor (Kaufmann, 1983) during several annual cycles. The fish were collected monthly from a subalpine lake (Seefelder See, Tirol, Austria). In one group (N = 10–20) the weight of the gonads was determined. A second group (N = 10) was acclimated to laboratory conditions for a few days and then placed into large intermittent-flow respirometers (Forstner, 1982) in which oxygen consumption and swimming activity were continuously measured for 7 days at the average temperature prevailing in the natural environment during the month of capture (Koch, 1983).

Fig. 1 shows that from December to June the rates of oxygen consumption and swimming activity are closely related at all temperatures, whereas from July to November activity decreases much more strongly than ⁠.

Spawning takes place in June and is followed by a drastic reduction of the old gonadal tissue. Synthesis of the new gonads begins in July and is completed between November and December (Fig. 2). In order to relate the levels of activity with the gonadal cycle, we have plotted mean activity against temperature separately for the first and the second half of the year (Fig. 3). It is quite apparent that at one and the same temperature the swimming activity of the fish is consistently lower during the period when new gonadal tissue is being synthesized, the reduction ranging from approximately 40% at 18 °C to less than 8% at 6 °C.

Since during the first half of the year there is a linear relationship between temperature-dependent and temperature-dependent locomotor activity (inset Fig. 1) we may express one variable in terms of the other. Under these circumstances the rate of oxygen consumption represents the costs of maintenance, of swimming, and of those processes of production that are not concerned with synthesizing the new gonads. By means of the calibration curve for the first half of the year, the oxygen consumption corresponding to the swimming activity recorded during the second half of the year can be calculated. The difference between the rates of oxygen consumption expected and those actually measured is assumed to represent the cost of producing and maintaining the new gonads. The results of such a comparison are set out in Table 1. Oxygen consumption was converted into energy units by using an oxycaloric value of 19·35 kJ I⁻¹ = 13·54 J mg⁻¹, which is the value recommended for aerobic steady state metabolic studies of fish by Brett & Groves (1979).

About 80% of the roach captured were females and since the ovaries are considerably heavier than the testes we shall assume that the difference between expected and measured group rate of oxygen consumption was mainly due to the synthesis of the new ovaries which increased between July and October from 2% to 7% of the fresh body weight, i.e. by 50 g kg⁻¹. Since the mean energy content of fish ovaries is 23·5 kJ g⁻¹ dry weight (Wootton, 1979) and dry weight varies between 28% and 34% of fresh weight (Koch, 1983), approximately 364kJ of gonadal tissue were synthesized by 1 kg of live fish in 4 months. During this time the reduction of swimming activity led to a calculated saving of 1485 kJ kg⁻¹ (Table 1). Thus the net machine efficiency (defined as P/R × 100; where P = production, R = respiration) for the production of ovarian tissue with metabolizable energy is 364/1485 × 100 or approximately 24·5%. The net caloric efficiency, defined as P/(P + R) × 100, would be 364/1849 ×100= 19·7%.

The metabolizable energy has to meet the costs of mobilizing and transporting the raw materials for tissue growth as well as the costs of building and maintaining the new tissue. It appears to us that this is a realistic approach to calculating production efficiencies in poikilotherms. It is based on the concept of ‘true net efficiency of production’, i.e. production/net energy minus maintenance energy, which has been used to evaluate the productivity of domestic animals for nearly 100 years (see Brody, 1945), but has been ignored in the recent zoological literature on production (see Calow, 1977).

In any organism different energy-consuming processes compete with each other for the same source of energy. The question of how a limited supply of energy may be distributed amongst several competing consumers was asked for the first time by Rubner (1910). During the last decade this question has reappeared as a focal point in ecophysiology under the name of ‘energy partitioning’ (e.g. Townsend & Calow, 1981). It has been shown, for example, that in natural populations the productivity of homoeothermic animals is very low, presumably because so much energy is being used for the maintenance of a high body temperature (Humphreys, 1979; Grodzinski & French, 1982). If the strain of thermoregulation is removed by domestication, thus keeping the animals in a thermoneutral environment, the productivity of mammals may increase by a factor of 30 or so (Blaxter, 1969). The most frequently discussed problem of energy partitioning in poikilothermic animals has been the trade-off between somatic and reproductive growth (Townsend & Calow, 1981). It has been claimed that animals have to make – so to speak – a ‘decision’ whether to invest more energy in somatic growth or in the growth of gametes. In a schematic representation intended to illustrate the switching of energy from growth to reproduction, Townsend & Calow (Fig. 1c, p. 251) indicate an energy compartment ‘the rest of metabolism’ which is supposed to remain constant. However, as the data of our communication show, a poikilothermic animal may very well be able to defray at least part of the costs of reproduction by saving on the energy demand of locomotion - just as could the rats mentioned in the Introduction. We are not aware of similar data on any species of poikilotherm, but in a most interesting paper Testerink (1982) recently showed that of two species of Collembola the one with higher productivity was less mobile and had a lower energy demand for maintenance than the other, less productive, species. The author concluded that ‘the energy required for higher maintenance in Orchesella cincta compared with Tomocerus minor was derived from production’.

The paucity of studies in which locomotor activity of poikilothermic animals is monitored over long periods of time has prevented the energy demand of activity from being given its proper place in energy budgets.

This research was supported by project No. 3307 of the ‘Fonds zur Förderung der wissenschaftlichen Forschung in Österreich’. We thank Dr H. Forstner for discussions and for his advice in technical matters.