No abstract

In this review we consider how small-scale temporal and spatial variation in body temperature, and biochemical/physiological variation among individuals, affect the prediction of organisms' performance in nature. For 'normal' body temperatures -benign temperatures near the species' mean -thermal biology traditionally uses performance curves to describe how physiological capabilities vary with temperature. However, these curves, which are typically measured under static laboratory conditions, can yield incomplete or inaccurate predictions of how organisms respond to natural patterns of temperature variation. For example, scale transition theory predicts that, in a variable environment, peak average performance is lower and occurs at a lower mean temperature than the peak of statically measured performance. We also demonstrate that temporal variation in performance is minimized near this new 'optimal' temperature. These factors add complexity to predictions of the consequences of climate change. We then move beyond the performance curve approach to consider the effects of rare, extreme temperatures. A statistical procedure (the environmental bootstrap) allows for longterm simulations that capture the temporal pattern of extremes (a Poisson interval distribution), which is characterized by clusters of events interspersed with long intervals of benign conditions. The bootstrap can be combined with biophysical models to incorporate temporal, spatial and physiological variation into evolutionary models of thermal tolerance. We conclude with several challenges that must be overcome to more fully develop our understanding of thermal performance in the context of a changing climate by explicitly considering different forms of small-scale variation. These challenges highlight the need to empirically and rigorously test existing theories.

Thermal performance curves enable physiological constraints to be incorporated in predictions of biological responses to shifts in mean temperature. But do thermal performance curves adequately capture the biological impacts of thermal extremes? Organisms incur physiological damage during exposure to extremes, and also mount active compensatory responses leading to acclimatization, both of which alter thermal performance curves and determine the impact that current and future extremes have on organismal performance and fitness. Thus, these sub-lethal responses to extreme temperatures potentially shape evolution of thermal performance curves. We applied a quantitative genetic model and found that beneficial acclimatization and cumulative damage alter the extent to which thermal performance curves evolve in response to thermal extremes. The impacts of extremes on the evolution of thermal performance curves are reduced if extremes cause substantial mortality or otherwise reduce fitness differences among individuals. Further empirical research will be required to understand how responses to extremes aggregate through time and vary across life stages and processes. Such research will enable incorporating passive and active responses to sub-lethal stress when predicting the impacts of thermal extremes.

In complex habitats, environmental variation over small spatial scales can equal or exceed larger-scale gradients. This small-scale variation may allow motile organisms to mitigate stressful conditions by choosing benign microhabitats, whereas sessile organisms may rely on other behaviors to cope with environmental stresses in these variable environments. We developed a monitoring system to track body temperature, valve gaping behavior and posture of individual mussels () in field conditions in the rocky intertidal zone. Neighboring mussels' body temperatures varied by up to 14°C during low tides. Valve gaping during low tide and postural adjustments, which could theoretically lower body temperature, were not commonly observed. Rather, gaping behavior followed a tidal rhythm at a warm, high intertidal site; this rhythm shifted to a circadian period at a low intertidal site and for mussels continuously submerged in a tidepool. However, individuals within a site varied considerably in time spent gaping when submerged. This behavioral variation could be attributed in part to persistent effects of the mussels' developmental environment. Mussels originating from a wave-protected, warm site gaped more widely, and remained open for longer periods during high tide than mussels from a wave-exposed, cool site. Variation in behavior was modulated further by recent wave heights and body temperatures during the preceding low tide. These large ranges in body temperatures and durations of valve closure events - which coincide with anaerobic metabolism - support the conclusion that individuals experience 'homogeneous' aggregations such as mussel beds in dramatically different fashion, ultimately contributing to physiological variation among neighbors.