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.
Heterothermy, a variability in body temperature beyond the limits of homeothermy, has been advanced as a key adaptation of Arabian oryx (Oryx leucoryx) to their arid-zone life. We measured body temperature using implanted data loggers, for a 1-year period, in five oryx free-living in the deserts of Saudi Arabia. As predicted for adaptive heterothermy, during hot months compared to cooler months, not only were maximum daily body temperatures higher (41.1 ± 0.3 vs. 39.7 ± 0.1°C, P = 0.0002) but minimum daily body temperatures also were lower (36.1 ± 0.3 vs. 36.8 ± 0.2°C, P = 0.04), resulting in a larger daily amplitude of the body temperature rhythm (5.0 ± 0.5 vs. 2.9 ± 0.2°C, P = 0.0007), while mean daily body temperature rose by only 0.4°C. The maximum daily amplitude of the body temperature rhythm reached 7.7°C for two of our oryx during the hot-dry period, the largest amplitude ever recorded for a large mammal. Body temperature variability was influenced not only by ambient temperature but also water availability, with oryx displaying larger daily amplitudes of the body temperature rhythm during warm-dry months compared to warm-wet months (3.6 ± 0.6 vs. 2.3 ± 0.3°C, P = 0.005), even though ambient temperatures were the same. Free-living Arabian oryx therefore employ heterothermy greater than that recorded in any other large mammal, but water limitation, rather than high ambient temperature, seems to be the primary driver of this heterothermy.
Heterothermy, a variability in body temperature beyond the normal limits of homeothermy, is widely viewed as a key adaptation of arid-adapted ungulates. However, desert ungulates with a small body mass, i.e. a relatively large surface area-to-volume ratio and a small thermal inertia, are theoretically less likely to employ adaptive heterothermy than are larger ungulates. We measured body temperature and activity patterns, using implanted data loggers, in free-ranging Arabian oryx (Oryx leucoryx, ±70 kg) and the smaller Arabian sand gazelle (Gazella subgutturosa marica, ±15 kg) inhabiting the same Arabian desert environment, at the same time. Compared to oryx, sand gazelle had higher mean daily body temperatures (F(1,6) = 47.3, P = 0.0005), higher minimum daily body temperatures (F(1,6) = 42.6, P = 0.0006) and higher maximum daily body temperatures (F(1,6) = 11.0, P = 0.02). Despite these differences, both species responded similarly to changes in environmental conditions. As predicted for adaptive heterothermy, maximum daily body temperature increased (F(1,6) = 84.0, P < 0.0001), minimum daily body temperature decreased (F(1,6) = 92.2, P < 0.0001), and daily body temperature amplitude increased (F(1,6) = 97.6, P < 0.0001) as conditions got progressively hotter and drier. There were no species differences in activity levels, however, both gazelle and oryx showed a biphasic or crepuscular rhythm during the warm wet season but shifted to a more nocturnal rhythm during the hot dry season. Activity was attenuated during the heat of the day at times when both species selected cool microclimates. These two species of Arabian ungulates employ heterothermy, cathemerality and shade seeking very similarly to survive the extreme, arid conditions of Arabian deserts, despite their size difference.
Mammals with a carotid rete are capable of reducing brain temperature below that of carotid blood temperature, termed selective brain cooling. In artiodactyls, selective brain cooling conserves body water and may provide them with a selective advantage in conditions of increased temperature and aridity.
SUMMARYSelective 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.
The future of fog-dependent habitats under climate change is unknown but likely precarious; many have experienced recent declines in fog. Fog-dependent deserts particularly will be threatened, because, there, fog can be the main water source for biota. We review the interactions between fog and fauna of the Namib Desert, about which there is 50 yr of research. We resynthesize the data, seeking patterns and mechanisms that could provide a framework for predicting outcomes of changes in fog regime in other fog-dependent deserts. In the Namib, fog constitutes the most-predictable form of free water. At least 48 Namib animal species consume free water from fog, or are likely to do so, employing both liquid and vapor phase. Fog also sustains plants that form the base for metabolic water production and wets the diet to provide pre-formed water. So fog provides or underpins all the water intake of Namib fauna. Only a few species are active fog-harvesters, though. Among Namib beetles, two species are unique in that they fog-bask; they assume stereotyped postures in wind-driven fog and droplets deposit on their carapaces. Some Namib beetle species construct surface ridges that trap fog water, which they consume. Some arthropods emerge from their subsurface habitats, or occupy its wet top layers, to access fog water, at times and in conditions outside their usual surface activity. Many more taxa, including vertebrates, use fog water opportunistically. They do not actively seek it out but use it when available. Acquiring fog water from droplets requires overcoming spherical surface tension so is possible only for animals heavier than~100 mg. Smaller animals extract water from films or acquire it in the vapor phase. Some Namib animals use hygroscopic surfaces to extract vapor from unsaturated air, at ambient humidities attained in fog or sometimes between fogs. Rapid acquisition of water during episodic fog events creates problems for storage and osmoregulation, which some Namib animals have solved in enterprising ways, including long-term internal storage of water and sequestering of osmolytes.Although not yet comprehensive, the body of research reviewed, and the principles that we have elucidated underlying fog usage, should inform future research on fauna throughout fog-dependent deserts.
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