In the face of climate change, the life history traits of large terrestrial mammals will prevent them from adapting genetically at a sufficient pace to keep track with changing environments, and habitat fragmentation will preclude them from shifting their distribution range. Predicting how habitat-bound large mammals will respond to environmental change requires measurement of their sensitivity and exposure to changes in the environment, as well as the extent to which phenotypic plasticity can buffer them against the changes. Behavioural modifications, such as a shift to nocturnal foraging or selection of a cool microclimate, may buffer free-living mammals against thermal and water stress, but may carry a cost, for example by reducing foraging time or increasing predation risk. Large mammals also use physiological responses to buffer themselves against changing environments, but those buffers may be compromised by a changing physical environment. A decrease in the available food energy or water leads to a trade-off in which the precision of homeothermy is relaxed, resulting in large daily fluctuations in body temperature. Understanding how large mammals prioritise competing homeostatic systems in changing environments, and the consequences of that prioritisation for their fitness, requires long-term monitoring of identifiable individual animals in their natural habitat. Although body size predicts general ecological and energetic patterns of terrestrial mammals, high intraspecific and interspecific variability means that a species-directed approach is required to accurately model responses of large mammals to climate change.
Abstract While most primates are tropical animals, a number of species experience markedly cold winters. In a high latitude arid environment, wild female vervet monkeys (Chlorocebus pygerythrus) that are socially integrated experience reduced cold stress. Here, we ask whether sociability is similarly salient for male vervet monkeys, who reside in non‐natal groups as adults and who must, therefore, develop social relationships on arrival. We use body temperature and social data from 15 free‐ranging male vervet monkeys to determine whether the number of grooming partners is as important for males during winter and whether the length of residency is positively associated with body temperature. We also assess whether larger body size and higher dominance rank mitigate the need for social partnerships. Like females, male vervets respond to lower 24 h ambient temperatures and winter's progression by decreasing minimum and mean 24 h body temperatures and by regulating their temperatures less precisely. Male rank had no effect, while larger body size was associated primarily with reduced temperature fluctuations. Males with more social partners sustained higher minimum and mean body temperatures but, unexpectedly, regulated their temperatures less tightly. Further analysis revealed that higher minimum and mean temperatures were best accounted for by the number of female partners, while increased temperature fluctuation was driven by the number of male partners. As winter and the mating season overlap, we interpret this as indicating that a need to sustain male associations incurs physiological stress that is reflected as a thermoregulatory cost. Lastly, we show that longer residency is associated with higher minimum body temperatures and lower temperature fluctuations independently of social affiliation.
Aardvarks ( Orycteropus afer ) are elusive burrowing mammals, predominantly nocturnal and distributed widely throughout Africa except for arid deserts. Their survival may be threatened by climate change via direct and indirect effects of increasing heat and aridity. To measure their current physiological plasticity, we implanted biologgers into six adult aardvarks resident in the semi-arid Kalahari. Following a particularly dry and hot summer, five of the study aardvarks and 11 other aardvarks at the study site died. Body temperature records revealed homeothermy (35.4–37.2°C) initially, but heterothermy increased progressively through the summer, with declining troughs in the nychthemeral rhythm of body temperature reaching as low as 25°C before death, likely due to starvation. Activity patterns shifted from the normal nocturnal to a diurnal mode. Our results do not bode well for the future of aardvarks facing climate change. Extirpation of aardvarks, which play a key role as ecosystem engineers, may disrupt stability of African ecosystems.
AbstractReduced energy intake can compromise the ability of a mammal to maintain body temperature within a narrow 24-h range, leading to heterothermy. To investigate the main drivers of heterothermy in a bulk grazer, we compared abdominal temperature, body mass, body condition index, and serum leptin levels in 11 subadult Cape buffalo (Syncerus caffer caffer) during a drought year and a nondrought year. Low food availability during the drought year (as indexed by grass biomass, satellite imagery of vegetation greenness, and fecal chlorophyll) resulted in lower body condition index, lower body mass relative to that expected for an equivalent-aged buffalo, and lower leptin levels. The range of 24-h body temperature rhythm was 2°C during the nondrought year and more than double that during the drought year, and this was caused primarily by a lower minimum 24-h body temperature rhythm during the cool dry winter months. After rain fell and vegetation greenness increased, the minimum 24-h body temperature rhythm increased, and the range of 24-h body temperature rhythm was smaller than 2°C. In order of importance, poor body condition, low minimum 24-h air temperature, and low serum leptin levels were the best predictors of the increase in the range of 24-h body temperature rhythm. While the thermoregulatory role of leptin is not fully understood, the association between range of 24-h body temperature rhythm and serum leptin levels provides clues about the underlying mechanism behind the increased heterothermy in large mammals facing food restriction.
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.
The accuracy of predictive models (also known as mechanistic or causal models) of animal responses to climate change depends on properly incorporating the principles of heat transfer and thermoregulation into those models. Regrettably, proper incorporation of these principles is not always evident. We have revisited the relevant principles of thermal physiology and analysed how they have been applied in predictive models of large mammals, which are particularly vulnerable, to climate change. We considered dry heat exchange, evaporative heat transfer, the thermoneutral zone and homeothermy, and we examined the roles of size and shape in the thermal physiology of large mammals. We report on the following misconceptions in influential predictive models: underestimation of the role of radiant heat transfer, misassignment of the role and misunderstanding of the sustainability of evaporative cooling, misinterpretation of the thermoneutral zone as a zone of thermal tolerance or as a zone of sustainable energetics, confusion of upper critical temperature and critical thermal maximum, overestimation of the metabolic energy cost of evaporative cooling, failure to appreciate that the current advantages of size and shape will become disadvantageous as climate change advances, misassumptions about skin temperature and, lastly, misconceptions about the relationship between body core temperature and its variability with body mass in large mammals. Not all misconceptions invalidate the models, but we believe that preventing inappropriate assumptions from propagating will improve model accuracy, especially as models progress beyond their current typically static format to include genetic and epigenetic adaptation that can result in phenotypic plasticity.
PowerPoint presentation and curriculum vitae of Prof Duncan Mitchell. This Arnold Theiler Memorial Lecture was delivered on August 22, 2019 at the University of Pretoria, Faculty of Veterinary Medicine, Onderstepoort. Professor Duncan Mitchell is is Emeritus Professor of Physiology at the University of the Witwatersrand, Johannesburg, and Honorary Professorial Research Fellow
in its Brain Function Research Group, from which he retired
as director in 2006. He is also Adjunct Professor in the School of Human Sciences
at the University of Western Australia, Perth.
Abstract The physiological performance of a mother during reproduction represents a trade‐off between continued investment in her current offspring, and the mother's own survival and ability to invest in future offspring. Here, we used core body temperature ( T b ) patterns to examine the degree to which maternal body temperatures support the infant during periods of gestation and lactation. We implanted 30 wild vervet monkeys ( Chlorocebus pygerythrus ) with miniature data loggers to obtain continuous measurements of core T b during periods of typical (i.e. non‐drought periods) and limited (i.e. drought period) resource availability. We tracked maternal T b profiles across the gestation and lactation periods, associated with 23 births, and compared those with T b profiles of non‐reproductive females. This allowed us to examine the flexibility in maternal body temperatures and test whether limited resource availability shifts priority away from offspring investment and towards self‐maintenance. Vervet monkeys demonstrated the predicted pattern of gestational hypothermia and improved homeothermy in the gestation period during typical conditions, consistent with the maintenance of a thermal gradient to facilitate heat loss from the foetus. During periods of limited resource availability (i.e. drought), mothers were less homeothermic and more hyperthermic during the gestation period. Vervet monkeys showed no evidence of lactational hyperthermia during typical conditions. During the drought, lactating mothers demonstrated hyperthermia and increased variability in body temperature, consistent with the increased metabolic demands and water requirements for milk production required to support growing infants. Although a mother's degree of homeothermy during gestation and lactation was unrelated to her infant's chance of survival to weaning, mothers did show flexibility in the degree to which they prioritized the maintenance of a thermal environment that supports their infant's development. Together, our findings demonstrate that flexibility in a mother's investment in thermoregulation during gestation and lactation may reflect a bet‐hedging trade‐off between self‐maintenance and offspring investment. Read the free Plain Language Summary for this article on the Journal blog.
Abstract Foot-and-mouth disease (FMD) is one of the most important livestock diseases restricting international trade. While it is clear that African buffalo ( Syncerus caffer ) act as the main wildlife reservoir, viral and immune response dynamics during FMD virus acute infection have not been described before in this species. We used experimental needle inoculation and contact infections with three Southern African Territories serotypes to assess clinical, virological and immunological dynamics for thirty days post infection. Clinical FMD in the needle inoculated buffaloes was mild and characterised by pyrexia. Despite the absence of generalised vesicles, all contact animals were readily infected with their respective serotypes within the first 2-9 days after being mixed with needle challenged buffaloes. Irrespective of the route of infection or serotype there were positive associations between the viral loads in blood and the induction of host innate pro-inflammatory cytokines and acute phase proteins. Viral loads in blood and tonsils were tightly correlated during the acute phase of the infection, however, viraemia significantly declined after a peak at 4 days post infection (dpi), which correlated with the presence of detectable neutralising antibodies. In contrast, infectious virus was isolated in the tonsils until the last sampling point (30 dpi) in most animals. The pattern of virus detection in serum and tonsil swabs was similar for all three serotypes in the direct challenged and contact challenged animals. We have demonstrated for the first time, that African buffalo are indeed systemically affected by FMD virus and clinical FMD in buffalo is characterized by a transient pyrexia. Despite the lack of FMD lesions, infection of African buffalo was characterised by high viral loads in blood and oropharynx, rapid and strong host innate and adaptive immune responses and high transmissibility.
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