Temperature, latitude and reproductive effort

The traditional IBP formulation of the energy budget is unsuitable for many marine organisms, partly because it sets production and respiration as alternative sinks when in reallty they are linked but also because it fails to recognise the heterogeneous nature of respiratory demand. The vanous components of total respiration reflect separate demands for ATP which are hkely to differ in their response to temperature and season. Such subdivision of total respiration emphasizes the difference between reproductive effort (RE, that fraction of the total energy flux diverted to reproduction) and reproductive output (RO, weight-specific gonad production) as measures of reproductive energehcs. Model calculahons demonstrate that the variation of basal metabolic rate with temperature (and hence latitude) influences both RE and RO, but in differing ways. If annual RE is assumed to be roughly constant in tropical, temperate and polar populations, then for organisms of similar size and ecology annual R0 will decrease with increasing latitude. Conversely if R 0 remains constant then annual RE will increase at high latitudes. Similar arguments predict an increase in net growth efficiency at low temperatures. When Lifetime RE is considered in relation to the slower growth rates and increased age of first breeding frequent at high latitudes, then data for the caridean shrimp Pandalus borealis suggest the possibility that there is a balance between basal metabolism and growth rate, resulting in a relatively constant lifetime RE across the latitudinal range. Clearly rather than there being a simple competition between growth and reproduction, energy is divided between several competing sinks which include the costs of maintenance and activity. INTRODUCTION tions and then compared with available data for marine invertebrates. In order to clarify matters, however, it is Consideration of the manner in which an organism necessary first to discuss the formulation of the energy divides incoming energy between growth and reprobudget in marine organisms. duction has played a central role in the development of life-history theory. It is conventional to regard these 2 forms of production as sinks competing for acquired THE ENERGY BUDGET energy (Gadgil & Bossert 1970, Reznick 1983, Calow 1985, Sibly & Calow 1986). When considering broad Adaptation and acclimation patterns of life-history and their energetic consequences, however, it is too simplistic to view matters Many marine organisms are remarkably tolerant of purely as a trade-off between growth and reproduction. short-term changes in temperature. This is particularly For all living organisms there is a cost to merely staylng true for shallow-water marine invertebrates and fish ahve, usually termed basal or maintenance metabolfrom temperate regions, and these organisms have ism. This cost is significant and it vanes with temperabeen much studied as a result. Data from such studies ture. are frequently then extrapolated to consideration of It is the purpose of this paper to examine the influlong-term (evolutionary) adaptation to temperature; ence of temperature, and hence latitude, on the fraction however, these 2 processes differ not only in their time of the total energy intake that is diverted to reproducscale, but also sometimes in the mechanisms involved tion. The argument is developed using model calcula(for a fuller discussion see Clarke 1983, in press). In this O Inter-Research/Pnnted in F. R. Germany 90 Mar. Ecol. Prog. Ser 38: 8 S 9 9 , 1987 paper I am considering only evolutionary adaptation to temperature, that is the energetic consequences of the evolution of genetically fixed variations in basal metabolic rate associated with compensation for mean environmental temperature. Clearly, altering the ambient temperature of a eurythermal organism will affect metabolic rate, growth and other physiological processes, but these short-term responses are not considered here. A physiological approach to the energy budget Most of the energy budgets published for marine organisms have used the formulation suggested for the International Biological Program (IBP) (Phillipson 1966, 1975, Crisp 1971, Klekowski & Duncan 1975), in which consumption where P = production (both somatic and reproductive) ; R = respiration; U = excretion; and F = faeces. The units chosen are usually those of energy although budgets are occasionally expressed in terms of specific elements such as carbon or nitrogen. Despite its wide use, however, the IBP formulation of the energy budget is inappropriate for studies of many marine organisms. A major cause of difficulty is the respiration term, R. Respiration represents the energy used by the organism for work and it is a measure of the heat lost to the environment. Klekowski & Duncan (1975) defined R as 'the energy required for the maintenance of life', and placed respiration in a clear thermodynamic context. They emphasized that the respiration rate measured at any given time is composed of inputs from mechanical work, work in chemical synthesis and the costs of active transport. Klekowski & Duncan also added to R the specific dynamic action (SDA), although they noted that if the correct explanation of SDA was the metabolic cost of synthesising new macromolecules then this was already included within the respiration term. The cost of locomotor activity was not, however, included. This and other early definitions of R recognised clearly the heterogeneous nature of respiration; that is although R is essentially a measure of the demand for ATP, this ATP is used for a variety of separate physiological processes. Physiologists concerned with the effects of temperature, however, have traditionally classified respiration differently, either as active respiration (which includes the cost of mechanical work involved in locomotor activity) or standard (resting) respiration (which does not). Standard respiration is frequently viewed as a single process, a measure of 'metabolism', and moreover a process which would be expected to show compensatory adjustments (both seasonal and evolutionary) to temperature change. The selective value of such adjustments to 'metabolism' is not always clear and this approach has led to a certain amount of confusion as to what is actually involved in temperature adaptation, together with a large and unwieldy nomenclature (Clarke in press). Any physiological approach to the energy budget must take into consideration this heterogeneous nature of respiration, and allow for the possibility that each of the separate processes may vary differently with season or temperature. The respiration component of the energy budget equation is therefore better considered as a summation term, ZR, which represents the total demand for oxygen: where Rb = oxygen required for basal (maintenance) metabolism; R, and R, = respiratory costs of the synthesis of somatic and gonad tissue respectively; and R, = oxygen required to fuel locomotor activity. Standard (resting) respiration, Rstd, is thus: This physiological breakdown of total respiration is shown schematically in Fig. l a , where the various divisions of the energy budget have been grouped together into a number of physiological sinks. Thus (P,+ R,) represents the total cost to the organism of producing somatic tissue, not just the energy equivalent of the newly synthesised tissue (P,) but also the respiratory cost of producing that tissue (R,). There is a similar respiratory cost (R,) to producing new reproductive tissue. a