Animal responses to environmental variation: Physiological mechanisms in ecological models of performance in deer (Cervidae)

Abstract

Context: Proper assessment of the consequences of environmental variation on animals depends on our ability to predict how they will perform under different circumstances. This requires two kinds of information. We need to know which environmental factors influence animal performance and their mode of action, i.e. whether a given factor acts alone or through interaction with other factors, directly or indirectly, instantaneously or after a delay and so on. This essentially correlative process falls within the domain of ecology. We also need to know what determines the direction, amplitude and limits of animal responses to environmental variation and change. This essentially experimental process falls within the domain of physiology. Physiological mechanisms are frequently poorly integrated within the correlative framework of ecological models. This is evident where programmed responses are attributed to environmental forcing and where the effect of environmental factors is evaluated without reference to the physiological state and regulatory capacity of the animal on which they act. Aims: Here we examine ways in which the impacts of external (environmental) stimuli and constraints on performance are moderated by the animals (deer) on which they impinge. Key results: The analysis shows (1) how trade-offs in foraging behaviour, illustrated by the timing of activity under the threat of predation, are modulated by integration of short-term metabolic feedback and animal emotions that influence the motivation to feed, (2) how the influence of thermal and nutritional challenges on performance, illustrated by the effect of weather conditions during gestation on the body mass of reindeer (Rangifer tarandus) calves at weaning, depends on the metabolic state of the female at the time the challenge occurs and (3) how annual cycles of growth, appetite and reproduction in seasonal species of deer are governed by innate circannual timers, such that their responses to seasonal changes in food supply are anticipatory and governed by rheostatic systems that adjust homeostatic set- points, rather than being purely reactive. Conclusions: Concepts like 'maintenance' and 'energy balance', which were originally derived from non-seasonal domestic ruminants, are unable to account for annual cycles in metabolic and nutritional status in seasonal deer. Contrasting seasonal phenotypes (fat and anoestrous in summer, lean and oestrous in winter) represent adaptive solutions to the predictable challenges presented by contrasting seasonal environments, not failure of homeostasis in one season and its success in another. Implications: The analysis and interpretation of responses to environment in terms of interaction between the external stimuli and the internal systems that govern them offer a more comprehensive, multifaceted understanding of the influence of environmental variation on performance in deer and open lines of ecological enquiry defined by non-intuitive aspects of animal function.