Robyn S. Hetem

Physiological Mechanisms in Coping with Climate Change

Although many studies have modeled the effects of climate change on future species distributions and extinctions, the theoretical approach most commonly used—climate envelope modeling—typically ignores the potential physiological capacity of animals to respond to climate change. We explore the consequences of the phenotypic plasticity available to animals, by examining physiological responses of free‐living animals in their natural habitats and by applying integrative, mechanistic models of heat exchange in invertebrates and humans. Specifically, we explore how behavioral, autonomic, and morphological modifications such as nocturnal activity, selective brain cooling, and body color may potentially serve as buffers to the consequences of climate change. Although some species may adapt to climate change through phenotypic plasticity, there are significant limits to this strategy. Furthermore, predictions of the response of organisms to changes in climate can be erroneous when modeled at large scales using coarse spatial or temporal data. Environmental heterogeneity can provide habitats suitable for species even though large‐scale changes in the climate might predict a species’ extinction. A detailed understanding of physiology, combined with integrative biophysical modeling and ecological manipulation, provides a powerful tool for predicting future ecological patterns and managing their consequences.

Body temperature, thermoregulatory behaviour and pelt characteristics of three colour morphs of springbok (Antidorcas marsupialis).

Using intra-abdominal miniature data loggers, we measured core body temperature in female springbok (Antidorcas marsupialis) of three colour morphs (black, normal and white), free-living in the Karoo, South Africa, for one year. During winter, white springbok displayed lower daily minimum body temperatures (37.4+/-0.5 degrees C), than both black (38.1+/-0.3 degrees C) and normal (38.0+/-0.6 degrees C) springbok. During spring, black springbok displayed higher daily maximum body temperatures (40.7+/-0.1 degrees C) than both white (40.2+/-0.2 degrees C) and normal (40.2+/-0.2 degrees C) springbok. These high maximum body temperatures were associated with larger daily amplitudes of nychthemeral rhythm of body temperature (2.0+/-0.2 degrees C), than that of white (1.6+/-0.1 degrees C) and normal (1.7+/-0.2 degrees C) springbok. Biophysical properties of sample springbok pelts were consistent with these patterns, as the black springbok pelt showed lower reflectance in the visible spectral range, and higher heat load from simulated solar radiation, than did the pelts of the other two springbok. Black springbok had lower diurnal activity in winter, consistent with them having to forage less because their metabolic cost of homeothermy was lower, but were disadvantaged in hot periods. White springbok, by contrast, were more protected from solar heat load, but potentially less able to meet the energy cost of homeothermy in winter. Thus energy considerations may underlie the rarity of the springbok colour morphs.

Social integration confers thermal benefits in a gregarious primate

Sociality has been shown to have adaptive value for gregarious species, with more socially integrated animals within groups experiencing higher reproductive success and longevity. The value of social integration is often suggested to derive from an improved ability to deal with social stress within a group; other potential stressors have received less attention. We investigated the relationship between environmental temperature, an important non-social stressor, and social integration in wild female vervet monkeys (Chlorocebus pygerythrus), using implanted data loggers to obtain direct measures of core body temperature. Heterothermy (as measured by 24-h amplitude of body temperature) increased, and 24-h minima of body temperature decreased, as the 24-h minimum ambient temperature decreased. As winter progressed, monkeys became increasingly heterothermic and displayed lower 24-h minima of body temperature. Monkeys with a greater number of social partners displayed a smaller 24-h amplitude (that is, were more homoeothermic) and higher 24-h minima of body temperature (that is, became less hypothermic), than did animals with fewer social partners. Our findings demonstrate that social integration has a direct influence on thermoregulatory ability: individual animals that form and maintain more social relationships within their group experience improved thermal competence compared to those with fewer social relationships. Given the likely energetic consequences of thermal benefits, our findings offer a viable physiological explanation that can help account for variations in fitness in relation to individual differences in social integration.

Adaptation to heat and water shortage in large, arid-zone mammals.

Although laboratory studies of large mammals have revealed valuable information on thermoregulation, such studies cannot predict accurately how animals respond in their natural habitats. Through insights obtained on thermoregulatory behavior, body temperature variability, and selective brain cooling in free-living mammals, we show here how we can better understand the physiological capacity of large mammals to cope with hotter and drier arid-zone habitats likely with climate change.

Activity re-assignment and microclimate selection of free-living Arabian oryx: responses that could minimise the effects of climate change on homeostasis?

Predicting whether behaviour could buffer the effects of climate change on long-lived mammals requires a better understanding of the long-term behavioural responses of mammals to environmental stress. Using biologging, we measured locomotor activity and microclimate selection, over eight months, in five Arabian oryx (Oryx leucoryx) living free in a Saudi Arabian desert. The oryx displayed seasonal flexibility in activity patterns, shifting from a continuous 24-h activity pattern with crepuscular peaks in cooler months to a predominantly nocturnal activity pattern during the hottest months, without reducing the total 24-h activity level. The proportion of total 24-h activity that occurred during daylight hours was just 29±8% during the hottest months, versus 53±8% (mean±SD, n=5 oryx) in the other months. The attenuation in diurnal activity levels during the hot months was accompanied by the selection of cooler microclimates, presumably via shade seeking, during the heat of the day. Analysis of miniature black globe (miniglobe) temperature from a remote sensor on the collar of two female animals revealed that oryx selected microclimates cooler than the microclimates in direct sun at higher environmental heat loads across all periods, but with enhanced efficiency during the dry periods. We have quantified activity re-assignment and microclimate selection as responses to hot arid conditions in a free-living artiodactyl. Such flexible behavioural processes may act to buffer the adverse effects of the progressively hotter and drier conditions predicted to occur with climate change.

Heterothermy in large mammals: Inevitable or implemented?

Advances in biologging techniques over the past 20 years have allowed for the remote and continuous measurement of body temperatures in free‐living mammals. While there is an abundance of literature on heterothermy in small mammals, fewer studies have investigated the daily variability of body core temperature in larger mammals. Here we review measures of heterothermy and the factors that influence heterothermy in large mammals in their natural habitats, focussing on large mammalian herbivores. The mean 24 h body core temperatures for 17 species of large mammalian herbivores (>10 kg) decreased by ∼1.3°C for each 10‐fold increase in body mass, a relationship that remained significant following phylogenetic correction. The degree of heterothermy, as measured by the 24 h amplitude of body core temperature rhythm, was independent of body mass and appeared to be driven primarily by energy and water limitations. When faced with the competing demands of osmoregulation, energy acquisition and water or energy use for thermoregulation, large mammalian herbivores appear to relax the precision of thermoregulation thereby conserving body water and energy. Such relaxation may entail a cost in that an animal moves closer to its thermal limits for performance. Maintaining homeostasis requires trade‐offs between regulated systems, and homeothermy apparently is not accorded the highest priority; large mammals are able to maintain optimal homeothermy only if they are well nourished, hydrated, and not compromised energetically. We propose that the amplitude of the 24 h rhythm of body core temperature provides a useful index of any compromise experienced by a free‐living large mammal and may predict the performance and fitness of an animal.

Responses of large mammals to climate change

Most large terrestrial mammals, including the charismatic species so important for ecotourism, do not have the luxury of rapid micro-evolution or sufficient range shifts as strategies for adjusting to climate change. The rate of climate change is too fast for genetic adaptation to occur in mammals with longevities of decades, typical of large mammals, and landscape fragmentation and population by humans too widespread to allow spontaneous range shifts of large mammals, leaving only the expression of latent phenotypic plasticity to counter effects of climate change. The expression of phenotypic plasticity includes anatomical variation within the same species, changes in phenology, and employment of intrinsic physiological and behavioral capacity that can buffer an animal against the effects of climate change. Whether that buffer will be realized is unknown, because little is known about the efficacy of the expression of plasticity, particularly for large mammals. Future research in climate change biology requires measurement of physiological characteristics of many identified free-living individual animals for long periods, probably decades, to allow us to detect whether expression of phenotypic plasticity will be sufficient to cope with climate change.

Selective brain cooling in Arabian oryx (Oryx leucoryx): a physiological mechanism for coping with aridity?

SUMMARY Selective brain cooling is a thermoregulatory effector proposed to conserve body water and, as such, may help artiodactyls cope with aridity. We measured brain and carotid blood temperature, using implanted data loggers, in five Arabian oryx (Oryx leucoryx) in the desert of Saudi Arabia. On average, brain temperature was 0.24±0.05°C lower than carotid blood temperature for four oryx in April. Selective brain cooling was enhanced in our Arabian oryx compared with another species from the same genus (gemsbok Oryx gazella gazella) exposed to similar ambient temperatures but less aridity. Arabian oryx displayed a lower threshold (37.8±0.1°C vs 39.8±0.4°C), a higher frequency (87±6% vs 15±15%) and a higher maximum magnitude (1.2±0.2°C vs 0.5±0.3°C) of selective brain cooling than did gemsbok. The dominant male oryx displayed less selective brain cooling than did any of the other oryx, but selective brain cooling was enhanced in this oryx as conditions became hotter and drier. Enhanced selective brain cooling in Arabian oryx supports the hypothesis that selective brain cooling would bestow survival advantages for artiodactyl species inhabiting hot hyper-arid environments.

Cheetah do not abandon hunts because they overheat

Hunting cheetah reportedly store metabolic heat during the chase and abandon chases because they overheat. Using biologging to remotely measure the body temperature (every minute) and locomotor activity (every 5 min) of four free-living cheetah, hunting spontaneously, we found that cheetah abandoned hunts, but not because they overheated. Body temperature averaged 38.4°C when the chase was terminated. Storage of metabolic heat did not compromise hunts. The increase in body temperature following a successful hunt was double that of an unsuccessful hunt (1.3°C ± 0.2°C versus 0.5°C ± 0.1°C), even though the level of activity during the hunts was similar. We propose that the increase in body temperature following a successful hunt is a stress hyperthermia, rather than an exercise-induced hyperthermia.

EFFECTS OF SEROTONIN AGONISTS AND DOXAPRAM ON RESPIRATORY DEPRESSION AND HYPOXEMIA IN ETORPHINE-IMMOBILIZED IMPALA (AEPYCEROS MELAMPUS)

Respiratory depression is a common side effect when opioids are used to immobilize wildlife. Serotonergic ligands have the potential to reverse opioid-induced respiratory depression. We examined whether any of three serotonergic ligands could reverse this depression in etorphine-immobilized (0.07 mg/kg) impala (Aepyceros melampus). The study took place in September–December 2007. Impala received intravenous injections of metoclopramide (10 mg/ kg, n=6), buspirone (0.05 mg/kg, n=8), pimozide (1 mg/kg, n=8), doxapram (1 mg/kg, n=6), and control solutions on separate occasions. During the immobilization, partial pressures of oxygen (PaO2, mmHg) and carbon dioxide (PaCO2, mmHg), respiratory rate (breaths/min), ventilation (l/ min), peripheral O2 saturation (%), tidal volume (l), and respiratory exchange ratio were measured before and after injection of the experimental drugs. Etorphine immobilization caused respiratory depression and hypoxia (mean±SD, PaCO2=51±2 mmHg, PaO2=40±3 mmHg). Metoclopra-mide and buspirone, but not pimozide, attenuated the hypoxic effects of etorphine; 3 min after injection, metoclopramide increased the PaO2 by 7.=66.3 mmHg and buspirone by 666.6 mmHg (F=3.9, P=0.02). These effects were similar to those of doxapram (8±7 mmHg, F=3.9; P>0.05). Neither metoclopramide nor buspirone significantly increased ventilation, but they increased PaO2 by significantly improving the alveolar-arterial oxygen partial pressure gradient (A-a gradient, F=1.4, P<0.05), indicating improved oxygen diffusion. Metoclopramide and buspirone transiently improved blood oxygenation of opioid-immobilized impala, probably by improving ventilation-perfusion ratios, without reversing catatonic immobilization.