Frank Seebacher

Coadaptation: A Unifying Principle in Evolutionary Thermal Biology*

Over the last 50 yr, thermal biology has shifted from a largely physiological science to a more integrated science of behavior, physiology, ecology, and evolution. Today, the mechanisms that underlie responses to environmental temperature are being scrutinized at levels ranging from genes to organisms. From these investigations, a theory of thermal adaptation has emerged that describes the evolution of thermoregulation, thermal sensitivity, and thermal acclimation. We review and integrate current models to form a conceptual model of coadaptation. We argue that major advances will require a quantitative theory of coadaptation that predicts which strategies should evolve in specific thermal environments. Simply combining current models, however, is insufficient to understand the responses of organisms to thermal heterogeneity; a theory of coadaptation must also consider the biotic interactions that influence the net benefits of behavioral and physiological strategies. Such a theory will be challenging to develop because each organism’s perception of and response to thermal heterogeneity depends on its size, mobility, and life span. Despite the challenges facing thermal biologists, we have never been more pressed to explain the diversity of strategies that organisms use to cope with thermal heterogeneity and to predict the consequences of thermal change for the diversity of communities.

Determining environmental causes of biological effects: the need for a mechanistic physiological dimension in conservation biology

The emerging field of Conservation Physiology links environmental change and ecological success by the application of physiological theory, approaches and tools to elucidate and address conservation problems. Human activity has changed the natural environment to a point where the viability of many ecosystems is now under threat. There are already many descriptions of how changes in biological patterns are correlated with environmental changes. The next important step is to determine the causative relationship between environmental variability and biological systems. Physiology provides the mechanistic link between environmental change and ecological patterns. Physiological research, therefore, should be integrated into conservation to predict the biological consequences of human activity, and to identify those species or populations that are most vulnerable.

A NEW METHOD TO CALCULATE ALLOMETRIC LENGTH-MASS RELATIONSHIPS OF DINOSAURS

Abstract Body mass is an important determinant of most biological functions, and knowing the mass of extinct animals is essential in order to learn about their biology. It was the aim of this paper to develop a method of mass estimation which would make it possible to determine allometric length-mass relationships for the different groups of dinosaurs. Mass is calculated from graphical reconstructions of fossils, or from photos of skeletal mounts or live animals. Body shape of animals is described by high order polynomial equations. Integration of the polynomial gives body mass of a ‘round’ animal, which is then corrected for animal width by intersection with a second equation (Y = 1 − ax2). The method was validated by predicting body mass of extant animals of known mass and with complex body shapes (kangaroos, emu, elephant, giraffe, rhinoceros). Body mass increased allometrically with total length in all groups of dinosaurs (Ankylosauria, Ceratopsia, Ornithopoda, Prosauropoda, Sauropoda, Stegosauria and Theropoda), but 95% confidence intervals were very large for Ankylosauria and Stegosauria so that, for those groups, the resulting regression equations have little predicting power. Scaling exponents were least for the Sauropoda which may have grown less massive to function at their great body size. Scaling exponents were greatest for the Theropoda, but it was speculated that small coelurosaurs, as the precursors of birds, may have grown less massive compared to other theropods. Mass estimated by the ‘polynomial’ method presented here did not differ significantly from mass estimates in the literature where these were available.

A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fishes.

Specialization to a particular environment is one of the main factors used to explain species distributions. Antarctic fishes are often cited as a classic example to illustrate the specialization process and are regarded as the archetypal stenotherms. Here we show that the Antarctic fish Pagothenia borchgrevinki has retained the capacity to compensate for chronic temperature change. By displaying astounding plasticity in cardiovascular response and metabolic control, the fishes maintained locomotory performance at elevated temperatures. Our falsification of the specialization paradigm indicates that the effect of climate change on species distribution and extinction may be overestimated by current models of global warming.

Shelter Microhabitats Determine Body Temperature and Dehydration Rates of a Terrestrial Amphibian (Bufo marinus)

Abstract Selection of diurnal shelter sites varies significantly with season in the cane toad (Bufo marinus), and the aim of this paper is to determine how hydric and thermal conditions of shelter microhabitats changed with season and whether those changes explained seasonal differences in toad behavior. Body temperatures of cane toads were measured by telemetry, and dehydration rates and thermal conditions of shelter microhabitats were measured by using preserved toads as environmental probes. Live toads and preserved toad models were monitored monthly over a 18-month period. Laboratory experiments showed that toad models dehydrated at the same rate as live toads. In the field, dehydration rates varied significantly between seasons and shelter microhabitats, but dehydration rates were always significantly less in shelters compared to a nonshelter control. Daily average body temperature of toads was 16–30°C, and it changed seasonally in proportion to model temperature. Diurnal model temperature was significantly lower in shelters compared to the nonshelter control, but there were significant seasonal differences between shelter sites. It appears that access to suitable diurnal shelter sites is essential for survival of cane toads outside the wet season and that seasonal changes in environmental conditions influence shelter microhabitat selection.

Physiological mechanisms of thermoregulation in reptiles: a review

The thermal dependence of biochemical reaction rates means that many animals regulate their body temperature so that fluctuations in body temperature are small compared to environmental temperature fluctuations. Thermoregulation is a complex process that involves sensing of the environment, and subsequent processing of the environmental information. We suggest that the physiological mechanisms that facilitate thermoregulation transcend phylogenetic boundaries. Reptiles are primarily used as model organisms for ecological and evolutionary research and, unlike in mammals, the physiological basis of many aspects in thermoregulation remains obscure. Here, we review recent research on regulation of body temperature, thermoreception, body temperature set-points, and cardiovascular control of heating and cooling in reptiles. The aim of this review is to place physiological thermoregulation of reptiles in a wider phylogenetic context. Future research on reptilian thermoregulation should focus on the pathways that connect peripheral sensing to central processing which will ultimately lead to the thermoregulatory response.

Seasonal acclimatisation of muscle metabolic enzymes in a reptile (Alligator mississippiensis)

SUMMARY Reptiles living in heterogeneous thermal environments are often thought to show behavioural thermoregulation or to become inactive when environmental conditions prevent the achievement of preferred body temperatures. By contrast, thermally homogeneous environments preclude behavioural thermoregulation, and ectotherms inhabiting these environments (particularly fish in which branchial respiration requires body temperature to follow water temperature) modify their biochemical capacities in response to long-term seasonal temperature fluctuations. Reptiles may also be active at seasonally varying body temperatures and could, therefore, gain selective advantages from regulating biochemical capacities. Hence, we tested the hypothesis that a reptile (the American alligator Alligator mississippiensis) that experiences pronounced seasonal fluctuations in body temperature will show seasonal acclimatisation in the activity of its metabolic enzymes. We measured body temperatures of alligators in the wild in winter and summer (N=7 alligators in each season), and we collected muscle samples from wild alligators (N=31 in each season) for analysis of metabolic enzyme activity (lactate dehydrogenase, citrate synthase and cytochrome c oxidase). There were significant differences in mean daily body temperatures between winter (15.66±0.43°C; mean ± S.E.M.) and summer (29.34±0.21°C), and daily body temperatures fluctuated significantly more in winter compared with summer. Alligators compensated for lower winter temperatures by increasing enzyme activities, and the activities of cytochrome c oxidase and lactate dehydrogenase were significantly greater in winter compared with summer at all assay temperatures. The activity of citrate synthase was significantly greater in the winter samples at the winter body temperature (15°C) but not at the summer body temperature (30°C). The thermal sensitivity (Q10) of mitochondrial enzymes decreased significantly in winter compared with in summer. The activity of mitochondrial enzymes was significantly greater in males than in females, but there were no differences between sexes for lactate dehydrogenase activity. The differences between sexes could be the result of the sex-specific seasonal demands for locomotor performance. Our data indicate that biochemical acclimatisation is important in thermoregulation of reptiles and that it is not sufficient to base conclusions about their thermoregulatory ability entirely on behavioural patterns.

Antarctic fish can compensate for rising temperatures: Thermal acclimation of cardiac performance in Pagothenia borchgrevinki

SUMMARY Antarctic fish Pagothenia borchgrevinki in McMurdo Sound, Antarctica, inhabit one of the coldest and most thermally stable of all environments. Sea temperatures under the sea ice in this region remain a fairly constant –1.86°C year round. This study examined the thermal plasticity of cardiac function in P. borchgrevinki to determine whether specialisation to stable low temperatures has led to the loss of the ability to acclimate physiological function. Fish were acclimated to– 1°C and 4°C for 4–5 weeks and cardiac output was measured at rest and after exhaustive exercise in fish acutely transferred from their acclimation temperature to –1, 2, 4, 6 and 8°C. In the– 1°C acclimated fish, the factorial scope for cardiac output was greatest at –1°C and decreased with increasing temperature. Increases in cardiac output with exercise in the –1°C acclimated fish was achieved by increases in both heart rate and stroke volume. With acclimation to 4°C, resting cardiac output was thermally independent across the test temperatures; furthermore, factorial scope for cardiac output was maintained at 4, 6 and 8°C, demonstrating thermal compensation of cardiac function at the higher temperatures. This was at the expense of cardiac function at –1°C, where there was a significant decrease in factorial scope for cardiac output in the 4°C acclimated fish. Increases in cardiac output with exercise in the 4°C acclimated fish at the higher temperatures was achieved by changes in heart rate alone, with stroke volume not varying between rest and exercise. The thermal compensation of cardiac function in P. borchgrevinki at higher temperatures was the result of a change in pumping strategy from a mixed inotropic/chronotropic modulated heart in –1°C acclimated fish at low temperatures to a purely chronotropic modulated heart in the 4°C acclimated fish at higher temperatures. In spite of living in a highly stenothermal cold environment, P. borchgrevinki demonstrated the capacity to thermally acclimate cardiac function to elevated temperatures, thereby allowing the maintenance of factorial scope and the support of aerobic swimming at higher temperatures.

A review of thermoregulation and physiological performance in reptiles: what is the role of phenotypic flexibility?

Biological functions are dependent on the temperature of the organism. Animals may respond to fluctuation in the thermal environment by regulating their body temperature and by modifying physiological and biochemical rates. Phenotypic flexibility (reversible phenotypic plasticity, acclimation, or acclimatisation) in rate functions occurs in all major taxonomic groups and may be considered as an ancestral condition. Within the Reptilia, representatives from all major groups show phenotypic flexibility in response to long-term or chronic changes in the thermal environment. Acclimation or acclimatisation in reptiles are most commonly assessed by measuring whole animal responses such as oxygen consumption, but whole animal responses are comprised of variation in individual traits such as enzyme activities, hormone expression, and cardiovascular functions. The challenge now lies in connecting the changes in the components to the functioning of the whole animal and its fitness. Experimental designs in research on reptilian thermal physiology should incorporate the capacity for reversible phenotypic plasticity as a null-hypothesis, because the significance of differential body temperature–performance relationships (thermal reaction norms) between individuals, populations, or species cannot be assessed without testing that null-hypothesis.

Adaptive Thermoregulation in Endotherms May Alter Responses to Climate Change

Climate change is one of the major issues facing natural populations and thus a focus of recent research has been to predict the responses of organisms to these changes. Models are becoming more complex and now commonly include physiological traits of the organisms of interest. However, endothermic species have received less attention than have ectotherms in these mechanistic models. Further, it is not clear whether responses of endotherms to climate change are modified by variation in thermoregulatory characteristics associated with phenotypic plasticity and/or adaptation to past selective pressures. Here, we review the empirical data on thermal adaptation and acclimatization in endotherms and discuss how those factors may be important in models of responses to climate change. We begin with a discussion of why thermoregulation and thermal sensitivity at high body temperatures should be co-adapted. Importantly, we show that there is, in fact, considerable variation in the ability of endotherms to tolerate high body temperatures and/or high environmental temperatures, but a better understanding of this variation will likely be critical for predicting responses to future climatic scenarios. Next, we discuss why variation in thermoregulatory characteristics should be considered when modeling the effects of climate change on heterothermic endotherms. Finally, we review some biophysical and biochemical factors that will limit adaptation and acclimation in endotherms. We consider both long-term, directional climate change and short-term (but increasingly common) anomalies in climate such as extreme heat waves and we suggest areas of important future research relating to both our basic understanding of endothermic thermoregulation and the responses of endotherms to climate change.