Danielle L. Levesque

Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures

Thermal performance curves (TPCs), which quantify how an ectotherms body temperature (Tb ) affects its performance or fitness, are often used in an attempt to predict organismal responses to climate change. Here, we examine the key - but often biologically unreasonable - assumptions underlying this approach; for example, that physiology and thermal regimes are invariant over ontogeny, space and time, and also that TPCs are independent of previously experienced Tb. We show how a critical consideration of these assumptions can lead to biologically useful hypotheses and experimental designs. For example, rather than assuming that TPCs are fixed during ontogeny, one can measure TPCs for each major life stage and incorporate these into stage-specific ecological models to reveal the life stage most likely to be vulnerable to climate change. Our overall goal is to explicitly examine the assumptions underlying the integration of TPCs with Tb , to develop a framework within which empiricists can place their work within these limitations, and to facilitate the application of thermal physiology to understanding the biological implications of climate change.

Are Tropical Small Mammals Physiologically Vulnerable to Arrhenius Effects and Climate Change

There is some urgency in the necessity to incorporate physiological data into mechanistic, trait-based, demographic climate change models. Physiological responses at the individual level provide the mechanistic link between environmental changes and individual performances and hence population dynamics. Here we consider the causal relationship between ambient temperature (Ta) and metabolic rate (MR), namely, the Arrhenius effect, which is directly affected by global warming through increases in average global air temperatures and the increase in the frequency and intensity of extreme climate events. We measured and collated data for several small, free-ranging tropical arboreal mammals and evaluated their vulnerability to Arrhenius effects and putative heat stress associated with climate change. Skin temperatures (Tskin) were obtained from free-ranging tarsiers (Tarsius syrichta) on Bohol Island, Philippines. Core body temperature (Tb) was obtained from the greater hedgehog tenrec (Setifer setosus) and the gray brown mouse lemur (Microcebus ravelobensis) from Ankarafantsika, Madagascar. Tskin for another mouse lemur, Microcebus griseorufus, was obtained from the literature. All four species showed evidence of hyperthermia during the daytime rest phase in the form of either Tskin or Tb that was higher than the normothermic Tb during the nighttime active phase. Potentially, tropical arboreal mammals with the lowest MRs and Tb, such as tarsiers, are the most vulnerable to sustained heat stress because their Tb is already close to Ta. Climate change may involve increases in MRs due to Arrhenius effects, especially during the rest phase or during torpor and hibernation. The most likely outcome of increased Arrhenius effects with climate change will be an increase in energy expenditure at the expense of other critical functions such as reproduction or growth and will thus affect fitness. However, we propose that these hypothetical Arrhenius costs can be, and in some species probably are, offset by the use of hyperthermic daily torpor, that is, hypometabolism at high Ta.

Mammal survival at the Cretaceous–Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs

Free-ranging common tenrecs, Tenrec ecaudatus, from sub-tropical Madagascar, displayed long-term (nine months) hibernation which lacked any evidence of periodic interbout arousals (IBAs). IBAs are the dominant feature of the mammalian hibernation phenotype and are thought to periodically restore long-term ischaemia damage and/or metabolic imbalances (depletions and accumulations). However, the lack of IBAs in tenrecs suggests no such pathology at hibernation Tbs > 22°C. The long period of tropical hibernation that we report might explain how the ancestral placental mammal survived the global devastation that drove the dinosaurs and many other vertebrates to extinction at the Cretaceous–Palaeogene boundary following a meteorite impact. The genetics and biochemistry of IBAs are of immense interest to biomedical researchers and space exploration scientists, in the latter case, those envisioning a hibernating state in astronauts for deep space travel. Unravelling the physiological thresholds and temperature dependence of IBAs will provide new impetus to these research quests.

Seasonal torpor and normothermic energy metabolism in the Eastern chipmunk (Tamias striatus)

To assess the changes in thermoregulatory characteristics that accompany the seasonal expression of torpor we measured seasonal differences in body mass adjustments, body temperature (Tb) and metabolic rate (MR) in both summer- and winter-acclimated individuals from a species of food-storing hibernator, the Eastern chipmunk (Tamias striatus). Torpor occurred only in the winter and was associated with lower normothermic Tb, during inter-bout arousal periods than in the summer. Chipmunks increased body mass before the initiation of torpor in winter, and steadily lost mass as the hibernation season progressed. Torpor expression was correlated to initial mass gain, with the individuals who showed the largest mass increase in the fall showing the highest degree of torpor. Acclimation to winter-like conditions produced a decline in normothermic MR at all ambient temperatures examined. The findings indicate that torpor expression is accompanied by a decrease in Tb and MR during normothermy, indicating that a conservation of energy metabolism occurs, not only in torpor, but also during the inter-bout arousal periods.

Tropical Heterothermy: Does the Exception Prove the Rule or Force a Re-Definition?

Recent interest in heterothermy in the tropics and the subtropics has raised issues with the existing definitions of torpor. The current methods used to distinguish and define patterns of heterothermy are insufficient in face of the numerous forms of torpor expression and high daily variation in normothermic body temperature (T b) observed in species inhabiting the tropics. Tropical heterothermy often occurs at highly variable ambient temperatures that may lead to a continuum between hibernation, daily torpor and normothermia with no clear distinction between states. While we do not seek to redefine torpor in this review, by listing torpor patterns that fall outside the usual categories (the exceptions to the rule), we discuss these thermoregulatory behaviours in terms of the energetics and evolution of heterothermy under warm climates.

Increased homeothermy during reproduction in a basal placental mammal

Homeothermic endothermy, the maintenance of a high and stable body temperature (Tb) using heat produced by elevated metabolism, is energetically expensive. There is increasing evidence that the earliest endotherms were heterotherms that, rather than maintaining strict homeothermy, allowed Tb to fluctuate with large variations between active and rest-phase Tb. The high level of homeothermy observed in modern mammals is therefore likely to have evolved from an ancestral heterothermic state. One of the hypotheses for the evolution of endothermy is that homeothermy allows for greater energetic output during reproduction (parental care model). We tested this hypothesis by measuring metabolic rates over a range of ambient temperatures in both reproductive and non-reproductive greater hedgehog tenrecs (Setifer setosus), a physiologically primitive mammal from Madagascar. Tenrecs have some of the lowest metabolic rates and highest levels of Tb variability of any mammal and are therefore good models of the ancestral eutherian state. During pregnancy and lactation, there was an increase in metabolism and Tb below the thermoneutral zone, accompanied by a decrease in Tb variability. The lower critical limit of the thermoneutral zone was estimated at ~25°C. However, whereas increases in resting metabolism were substantial below 20°C (up to 150% higher during reproduction), daytime rest-phase ambient temperatures at the study site rarely reached equivalent low levels. Thus, S. setosus provide an example for how relatively low-cost increases in homeothermy could have led to substantial increases in fitness by allowing for the faster production of young. The mechanisms necessary for increases in thermogenesis during reproduction would have further benefited the development of homeothermy in mammals.

Modelling mammalian energetics: the heterothermy problem

Global climate change is expected to have strong effects on the world’s flora and fauna. As a result, there has been a recent increase in the number of meta-analyses and mechanistic models that attempt to predict potential responses of mammals to changing climates. Many models that seek to explain the effects of environmental temperatures on mammalian energetics and survival assume a constant body temperature. However, despite generally being regarded as strict homeotherms, mammals demonstrate a large degree of daily variability in body temperature, as well as the ability to reduce metabolic costs either by entering torpor, or by increasing body temperatures at high ambient temperatures. Often, changes in body temperature variability are unpredictable, and happen in response to immediate changes in resource abundance or temperature. In this review we provide an overview of variability and unpredictability found in body temperatures of extant mammals, identify potential blind spots in the current literature, and discuss options for incorporating variability into predictive mechanistic models.

Seasonal changes in thermoregulatory responses to hypoxia in the Eastern chipmunk (Tamias striatus)

SUMMARY Mammalian heterotherms are known to be more tolerant of low oxygen levels than homeotherms. However, heterotherms demonstrate extreme seasonality in daily heterothermy and torpor expression. Because hypoxia depresses body temperature (Tb) and metabolism in mammals, it was of interest to see if seasonal comparisons of normothermic animals of a species capable of hibernation produce changes in their responses to hypoxia that would reflect a seasonal change in hypoxia tolerance. The species studied, the Eastern chipmunk (Tamias striatus, Linnaeus 1758), is known to enter into torpor exclusively in the winter. To test for seasonal differences in the metabolic and thermoregulatory responses to hypoxia (9.9 kPa), flow-through respirometry was used to compare oxygen consumption, minimum thermal conductance and Tb under fixed ambient temperature (Ta) conditions whereas a thermal gradient was used to assess selected Ta and Tb in response to hypoxia, in both summer- and winter-acclimated animals. No differences were observed between seasons in resting metabolism or thermal conductance in normoxic, normothermic animals. Providing the animals with a choice of Ta in hypoxia attenuated the hypoxic drop in Tb in both seasons, suggesting that the reported fall in Tb in hypoxia is not fully manifested in the behavioural pathways responsible for thermoregulation in chipmunks. Instead, Tb in hypoxia tends to be more variable and dependent on both Ta and season. Although Tb dropped in hypoxia in both seasons, the decrease was less in the winter with no corresponding decrease in metabolism, indicating that winter chipmunks are more tolerant to hypoxia than summer animals.

Embracing heterothermic diversity: non-stationary waveform analysis of temperature variation in endotherms

Recent research is revealing incredible diversity in the thermoregulatory patterns of wild and captive endotherms. As a result of these findings, classic thermoregulatory categories of ‘homeothermy’, ‘daily heterothermy’, and ‘hibernation’ are becoming harder to delineate, impeding our understanding of the physiological and evolutionary significance of variation within and around these categories. However, we lack a generalized analytical approach for evaluating and comparing the complex and diversified nature of the full breadth of heterothermy expressed by individuals, populations, and species. Here we propose a new approach that decomposes body temperature time series into three inherent properties—waveform, amplitude, and period—using a non-stationary technique that accommodates the temporal variability of body temperature patterns. This approach quantifies circadian and seasonal variation in thermoregulatory patterns, and uses the distribution of observed thermoregulatory patterns as a basis for intra- and inter-specific comparisons. We analyse body temperature time series from multiple species, including classical hibernators, tropical heterotherms, and homeotherms, to highlight the approach’s general usefulness and the major axes of thermoregulatory variation that it reveals.

Lizard colour changes to a daily rhythm

![][1] The ability to change ones skin colour is an extremely useful trait. Some species use dynamic changes in pigmentation to signal to potential mates or rivals. Others use it to camouflage themselves to fit in with their surroundings and avoid predators. Colour change can also