Thermal variation, thermal extremes and the physiological performance of individuals

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.

Micro-scale environmental variation amplifies physiological variation among individual mussels

“…Future climate projections include shifts in both the mean and the variability of environmental conditions, yet understanding of the interactions between environmental variation and physiological variation remains relatively poorly developed [4,11]. Individuals within populations possess a range of genotypic and phenotypic repertoires [51].…”

“…In addition, evolutionary responses to environmental change can act over short time scales once thought to be the exclusive realm of ecological interactions and/or phenotypic plasticity [9,10], with important implications for species' abilities to resist and adapt to global change. Further complexity arises when considering the often substantial degree of micro-scale variation in how individual organisms experience their environment [4,11], a pattern that likely interacts with genetic variation to contribute to variation among individuals in the physiological capacity to cope with environmental variation. In the context of thermal stress, such considerations have fostered a renewed emphasis on the causes and consequences of spatial and temporal patterns of variation in body temperature per se, in lieu of reliance on habitat temperatures and 'climate envelopes' [12,13].…”

Evolution caused by extreme events

“…In so doing, they can alter selective agents as well as the genetic composition of populations. If associated mortality randomly reduces standing genetic variation, the extreme event will retard future adaptive evolution; but if mortality is selective, the event may enhance future tolerance [31,33,34].…”

“…island uplifts, §4, or myxoma virus, §7). Similarly, artificial selection experiments, which subject experimental lines to an extreme temperature every generation, also typically lead to increased heat tolerance [36]; however, these protocols are poor mimics of most natural extremes, which are rare and episodic [33]. Consequently, such protocols prevent reversion of the genetic constitution of experimental lines towards the pre-extreme state [34].…”

The role of stochastic thermal environments in modulating the thermal physiology of an intertidal limpet, Lottia digitalis

“…To simplify experimental designs, many studies that have incorporated aerial emersion with heat stress have acclimated intertidal organisms under constant ambient ocean conditions rather than simulating tidal cycles (Helmuth et al, 2010;Logan et al, 2012;Dowd and Somero, 2013;Bjelde and Todgham, 2013;Zhang et al, 2014;Bjelde et al, 2015). Although there have been several experimental studies that have acclimated organisms to more realistic tidal cycles, our understanding of the role of repeated daily fluctuations in temperature, more indicative of natural conditions, is still deficient (McMahon et al, 1991;Marshall and McQuaid, 1992;Dong and Williams, 2011;Han et al, 2013;Dowd et al, 2015).…”