Seasonal acclimatization and latitudinal compensation in metabolism: do they exist?

Ecologists and physiologists have long been interested in the way organisms react to the changing of the seasons and to the varying ecological conditions at different latitudes. Although many features of the environment differ between summer and winter, and also with latitude (e.g. photoperiod, precipitation and food availability), a great deal of attention has been directed at understanding the effects of changes in temperature. This is partly because environmental temperature is a simple parameter to measure and record (see Vogel 1981), but also because the effects of temperature on the physiology of organisms appear to be simple and straightforward: everybody knows that a lower temperature slows things down. Studies of metabolic rate in relation to temperature have played a significant role in shaping current ideas of how organisms adapt to a seasonal environment and to latitude. The literature is replete with experimental and observational studies of the effects of temperature on whole-organism metabolic rate (usually measured as oxygen uptake), and the seasonal change in temperature in temperate waters has often been viewed as a key factor regulating growth and reproduction in marine animals. A common experiment is to compare the metabolic rate of organisms in summer and winter. The results are usually interpreted in terms of acclimatization; the implication being that the organism has done something adaptive to cope with the change of season. Similar comparisons have also been made for related species living at different latitudes. Animals undergoing acclimatization in the field are subject to coincident changes in many factors in addition to temperature and so an alternative approach is to expose animals to simulated summer and winter conditions, and compare their metabolic rates. In this laboratory context the response is usually termed acclimation; the assumption being that in a properly controlled experiment only the factor of interest (here temperature) varies between the treatments. However since all physical parameters of water vary with temperature (density, viscosity, ionization, gas solubility, etc.) a properly controlled experiment, in the sense that only temperature is varied, is not strictly possible. It is the purpose of this essay review to suggest that the traditional view of latitudinal and seasonal acclimatization of metabolic rate to temperature has no useful biological meaning. Indeed it acts as a barrier to a fuller understanding of what is actually involved in the process of acclimatization, primarily because it represents respiration (or 'metabolism') as a single process whose behaviour in relation to temperature can be simply portrayed and understood. It thereby ignores the heterogeneous nature of respiratory demand and imposes upon the system an apparent homogeneity that in reality does not exist. First however, it is necessary to discuss the concept of compensation, and then to outline the process involved in respiratory demand. I shall confine my remarks to aquatic organisms. However, much of the argument is relevant to terrestrial organisms, although here interpretation is considerably more difficult because of their more complex thermal environment. In particular, terrestrial organisms have to cope with significant diurnal variations in temperature from which aquatic environments are largely protected by the buffering effect of the large thermal capacity of water. I am also ignoring mammals and birds, where whole-animal considerations of metabolic regulation for heat production overlay the temperature/rate relationships of central relevance to ectotherm physiology. In the first part of this essay I shall therefore ignore the effects of temperature almost completely, and develop the thesis that patterns of metabolic rate that are usually explained in terms of acclimatization to seasonal or latitudinal changes in temperature are related primarily to other factors. Only then will temperature be introduced to show that it does have a role to play in influencing seasonal and latitudinal patterns in metabolic rate, but that this is subtle and difficult to distinguish from other more powerful influences.