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.
Rocky intertidal organisms are often exposed to broadly fluctuating temperatures as the tides rise and fall. Many mobile consumers living on the shore are immobile during low tide, and can be exposed to high temperatures on calm, warm days. Rising body temperatures can raise metabolic rates, induce stress responses, and potentially affect growth and survival, but the effects may differ among species with different microhabitat preferences. We measured aerial and aquatic respiration rates of 4 species of Lottia limpets from central California, and estimated critical thermal maxima. In a variety of microhabitats in the field, we tracked body temperatures and measured limpet growth rates on experimental plates colonized by natural microalgae. Limpet species found higher on the shore had lower peak respiration rates during high temperature aerial exposure, and had higher critical thermal maxima. Using our long-term records of field body temperatures, we estimated cumulative respiration to be 5 to 14% higher in warm microhabitats. Growth rates in the field appear to be driven by an interaction between available microalgal food resources, low tide temperature, and limpet species identity, with limpets from warmer microhabitats responding positively to higher food availability and higher low tide temperatures. Stressful conditions in warm microhabitats make up a small portion of the total lifetime of these limpets, but the greater proportion of time spent at non-stressful, but warm, body temperatures may result in enhanced growth compared to limpets living in cooler microhabitats.
Flexibility is key to survival for seaweeds exposed to the extreme hydrodynamic environment of wave-washed rocky shores. This poses a problem for coralline algae, whose calcified cell walls make them rigid. Through the course of evolution, erect coralline algae have solved this problem by incorporating joints (genicula) into their morphology, allowing their fronds to be as flexible as those of uncalcified seaweeds. To provide the flexibility required by this structural innovation, the joint material of Calliarthron cheilosporioides, a representative articulated coralline alga, relies on an extraordinary tissue that is stronger, more extensible and more fatigue resistant than the tissue of other algal fronds. Here, we report on experiments that reveal the viscoelastic properties of this material. On the one hand, its compliance is independent of the rate of deformation across a wide range of deformation rates, a characteristic of elastic solids. This deformation rate independence allows joints to maintain their flexibility when loaded by the unpredictable -and often rapidly imposed -hydrodynamic force of breaking waves. On the other hand, the genicular material has viscous characteristics that similarly augment its function. The genicular material dissipates much of the energy absorbed as a joint is deformed during cyclic wave loading, which potentially reduces the chance of failure by fatigue, and the material accrues a limited amount of deformation through time. This limited creep increases the flexibility of the joints while preventing them from gradually stretching to the point of failure. These new findings provide the basis for understanding how the microscale architecture of genicular cell walls results in the adaptive mechanical properties of coralline algal joints.
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