Raymond B. Huey

Impacts of climate warming on terrestrial ectotherms across latitude

The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest.

Evolution of thermal sensitivity of ectotherm performance

Most ectothermal animals have variable body temperatures. Because physiological rates are temperature sensitive, an ectotherms behavioural and ecological performance - even its fitness - can be influenced by body temperature. As a result, the thermal sensitivity of ectotherm performance is relevant to diverse issues in physiology, ecology and evolution. This review formalizes an emerging framework for investigating the evolution of thermal sensitivity, outlines some functional and genetical constraints on that evolution, and summarizes comparative and experimental advances in this field.

Cost and Benefits of Lizard Thermoregulation

Lizards thermoregulate by behavioral and physiological adjustments. The resultant control over metabolic processes is generally assumed to be beneficial. However, these thermoregulatory adjustments have associated costs which, if extensive, make thermoregulation impractical. We extend this idea into an abstract mathematical, cost-benefit model of thermoregulation in lizards. Investigation of the model leads to a set of predictions which includes: (1) the physiologically optimal temperature is not always the ecologically optimal temperature; (2) thermoregulation is beneficial only when associated costs are low; (3) thermal specialists will normally thermoregulated more carefully than thermal generalists unless costs are high; and (4) lizards will thermoregulate more carefully if productivity of the habitat is increased or if exploitation competition is reduced. Data on lizards, where available, generally agree with these predictions.

PHYSIOLOGICAL CONSEQUENCES OF HABITAT SELECTION

By determining the microclimates that an animal experiences, habitats influence an animals physiological capacities and ultimately its demographic and ecological performance. As a result, the ecology of organisms-especially of ectotherms-can be profoundly affected by the physiological consequences of habitat selection. Early ecologists such as Shelford and Chapman appreciated these issues, but most later ones tended to ignore physiology and instead focused on biotic interactions (e.g., competition). Recent technical and conceptual developments are now fostering a reintroduction of physiology into ecology. For issues relevant to thermal physiology, three steps are involved. First, the microclimates available in a habitat must be mapped. For ectotherms, this involves determining the operative environmental temperatures (Te)-that is, the potential body temperatures available in a habitat. Biophysical techniques can now generate Te maps with considerable accuracy. Second, the physiological effects of body temperature must be quantified. This requires laboratory studies of the effect of temperature on key performance traits. Third, the physiological suitability of habitats can be predicted by integrating the above environmental and physiological data. Analyses of the physiological consequences of habitat selection are exemplified in several case studies, and the importance of considering food and other factors in the analyses is stressed. An extension to endotherms is briefly discussed.

Putting the Heat on Tropical Animals

I mpacts of climate warming in the tropics— the cradle of biodiversity—are often predicted to be small relative to those in temperate regions (1, 2), because the rate of climate warming in the tropics is lower than at higher latitudes (3). Yet, predictions based only on the magnitude of climate change may be misleading. Models that include organismal physiology suggest that impacts of climate warming may be more severe in the tropics than in temperate regions. The impacts of climate warming on organisms depend not only on the magnitude of the environmental temperature shift but also on the behavior, morphology, physiology, and ecology of the organisms in question (4–6). This added complexity is daunting, but some general principles are emerging from research focused mainly on ectothermal animals (such as insects, fish, reptiles, and amphibians), which cannot maintain a constant internal body temperature. Negative impacts should be greatest on animals that are physiologically specialized with respect to temperature (7) and have limited acclimation capacity (8). Further, species living in warm climates are likely to suffer disproportionately from small increases in temperature (9), and species that live in aseasonal environments may be particularly vulnerable to increases in temperature, because changes in behavior and physiology are less likely to provide relief from rising temperatures (10). Terrestrial ectotherms with these vulnerability traits are typically tropical (7, 11, 12). In the 1960s, Janzen (13) noted that tropical ectotherms should be thermal specialists (see the figure, top) and have limited acclimation capacities, relative to higher-latitude species, because they have evolved in relatively constant, aseasonal environments. These predictions have been largely validated for various terrestrial and aquatic ectotherms (7, 11, 12, 14–17), yet the implications of this pattern for species vulnerabilities to climate change have rarely been investigated (15, 17–19). Tropical ectotherms have other traits that increase vulnerability. Because tropical organisms experience far more warm weather throughout the year than do temperate organisms, tropical animals might be expected to have greater heat tolerance. Surprisingly, that is often not the case: Heat tolerance typically varies very little across latitude in terrestrial ectotherms (7, 12, 15). Thus, many tropical ectotherms live much of the year in environments where equilibrium body (“operative”) temperatures are near or above optimal temperatures for performance (15). Tropical forest species may be particularly vulnerable, because they live in constant shade, are not generally adapted to the high operative temperatures found in warmer open habitats, and have few behavioral options available to evade rising temperatures (10, 15). Any climateinduced increase in operative temperaturecould cause steep declines in thermal performance and Darwinian fitness (see the figure, top). To assess whether independent data support these assertions, longterm demographic data on tropical species are required. Such data are rare, but in the study of frogs and lizards in lowland Costa Rica, densities have declined by ~4% per year between 1970 and 2005 (20). These declines are explained by climatedriven declines in leaf litter on the forest floor over the study period. Theoretically, these patterns can cut both ways: The same factors that make tropical ectotherms vulnerable to changing climate may benefit some temperate ectotherms (15) (see the figure, bottom). Empirical data tell a more complex story. During the last rapid warming event, 50 million years ago, insect damage on temperate plants did increase sharply (21), but data on contemporary temperate-zone insects are mixed: Some species are expanding rapidly (22), occasionally causing large changes to ecosystems and economies (23), whereas others—often specialists relying on day-length cues and species living in disappearing high-elevation habitats—are predicted to decline (6). All these predictions are for terrestrial habitats, and patterns may differ elsewhere. In marine habitats, for example, thermal specialists occur both at low and high latitudes, and thermal generalists appear most common at mid-latitudes (9, 24). Yet this pattern tracks the seasonality of ocean surface temperatures—polar oceans are cold but show little temperature variation throughout the year, and the largest seasonality in ocean surface temperatures are seen at mid-latitudes. Therefore, both tropical and high-latitude species live at near-stressful temperatures and could be vulnerable to warming (24). In intertidal habitats, which Putting the Heat on Tropical Animals ECOLOGY

Why tropical forest lizards are vulnerable to climate warming

Biological impacts of climate warming are predicted to increase with latitude, paralleling increases in warming. However, the magnitude of impacts depends not only on the degree of warming but also on the number of species at risk, their physiological sensitivity to warming and their options for behavioural and physiological compensation. Lizards are useful for evaluating risks of warming because their thermal biology is well studied. We conducted macrophysiological analyses of diurnal lizards from diverse latitudes plus focal species analyses of Puerto Rican Anolis and Sphaerodactyus. Although tropical lowland lizards live in environments that are warm all year, macrophysiological analyses indicate that some tropical lineages (thermoconformers that live in forests) are active at low body temperature and are intolerant of warm temperatures. Focal species analyses show that some tropical forest lizards were already experiencing stressful body temperatures in summer when studied several decades ago. Simulations suggest that warming will not only further depress their physiological performance in summer, but will also enable warm-adapted, open-habitat competitors and predators to invade forests. Forest lizards are key components of tropical ecosystems, but appear vulnerable to the cascading physiological and ecological effects of climate warming, even though rates of tropical warming may be relatively low.

PHYLOGENETIC STUDIES OF COADAPTATION: PREFERRED TEMPERATURES VERSUS OPTIMAL PERFORMANCE TEMPERATURES OF LIZARDS

The view that behavior and physiological performance are tightly coadapted is a central principle of physiological ecology. Here, we test this principle using a comparative study of evolutionary patterns in thermal preferences and the thermal dependence of sprinting in some Australian skinks (Lygosominae). Thermal preferences (Tp) differ strikingly among genera (range 24° to 35°C), but critical thermal maxima (CTMax) (range 38° to 45°C) and optimal temperatures for sprinting (To, 32° to 35°C) vary less. Diurnal genera have relatively high Tp, To, and CTMax. In contrast, nocturnal genera have low Tp but have moderate to high To and CTMax. Both nonphylogenetic and phylogenetic (minimum‐evolution) approaches suggest that coadaptation is tight only for genera with high Tp. Phylogenetic analyses suggest that low Tp and, thus, partial coadaptation are evolutionarily derived, indicating that low thermal preferences can evolve, even if this results in reduced performance. In one instance, thermal preferences and the thermal dependence of sprinting may have evolved in opposite directions, a phenomenon we call “antagonistic coadaptation.” We speculate on factors driving partial coadaptation and antagonistic coadaptation in these skinks.

Global metabolic impacts of recent climate warming

Documented shifts in geographical ranges, seasonal phenology, community interactions, genetics and extinctions have been attributed to recent global warming. Many such biotic shifts have been detected at mid- to high latitudes in the Northern Hemisphere—a latitudinal pattern that is expected because warming is fastest in these regions. In contrast, shifts in tropical regions are expected to be less marked because warming is less pronounced there. However, biotic impacts of warming are mediated through physiology, and metabolic rate, which is a fundamental measure of physiological activity and ecological impact, increases exponentially rather than linearly with temperature in ectotherms. Therefore, tropical ectotherms (with warm baseline temperatures) should experience larger absolute shifts in metabolic rate than the magnitude of tropical temperature change itself would suggest, but the impact of climate warming on metabolic rate has never been quantified on a global scale. Here we show that estimated changes in terrestrial metabolic rates in the tropics are large, are equivalent in magnitude to those in the north temperate-zone regions, and are in fact far greater than those in the Arctic, even though tropical temperature change has been relatively small. Because of temperature’s nonlinear effects on metabolism, tropical organisms, which constitute much of Earth’s biodiversity, should be profoundly affected by recent and projected climate warming.

Behavioral Drive versus Behavioral Inertia in Evolution: A Null Model Approach

Some biologists embrace the classical view that changes in behavior inevitably initiate or drive evolutionary changes in other traits, yet others note that behavior sometimes inhibits evolutionary changes. Here we develop a null model that quantifies the impact of regulatory behaviors (specifically, thermoregulatory behaviors) on body temperature and on performance of ectotherms. We apply the model to data on a lizard (Anolis cristatellus) and show that thermoregulatory behaviors likely inhibit selection for evolutionary shifts in thermal physiology with altitude. Because behavioral adjustments are commonly used by ectotherms to regulate physiological performance, regulatory behaviors should generally constrain rather than drive evolution, a phenomenon we call the “Bogert effect.” We briefly review a few other examples that contradict the classical view of behavior as the inevitable driving force in evolution. Overall, our analysis and brief review challenge the classical view that behavior is invariably the driving force in evolution, and instead our work supports the alternative view that behavior has diverse—and sometimes conflicting—effects on the directions and rates at which other traits evolve.

HOT ROCKS AND NOT-SO-HOT ROCKS: RETREAT-SITE SELECTION BY GARTER SNAKES AND ITS THERMAL CONSEQUENCES'

Studies of behavioral thermoregulation ofectotherms have typically focused only on active animals. However, most temperate-zone ectotherms actually spend more time sequestered in retreats (e.g., under rocks) than active above ground. We documented retreat-site selection during summer by gravid garter snakes (Thamnophis elegans) at Eagle Lake in northeastern California, USA. To explore the thermal consequences of retreat-site selection, we measured potential body temperatures in retreats and combined these with data on thermal tolerances, thermal preferences, and thermal dependence of metabolism and digestion. Garter snakes at Eagle Lake usually retreated under rocks of intermediate thickness (20-30 cm) even though both thinner and thicker rocks were available. Empirical and biophysical analyses of temperatures under rocks of various sizes and shapes demonstrated that rock thickness had the dominant effect on potential Tb available to snakes and in turn on thermal physiology. Snakes selecting thin rocks ( 40 cm thick) or remaining at the bottom of deep burrows would not experience such extreme Tb, but neither would they warm to Tb in their preferred range. However, snakes selecting intermediate-thickness rocks would never overheat but would achieve preferred Tb for long periods-far longer than if they remained on the ground surface or moved up and down within a burrow. Interestingly, snakes selecting burrows or intermediate-thickness rocks may be able to have either the highest energy gain or the lowest overall metabolic rate, depending on the particular Tb they select. Medium-thickness rocks, the size rocks normally selected by the snakes, offer them a variety of suitable thermoregulatory opportunities.