Measurement of microclimates in a warming world: problems and solutions.

As the world warms, it will be tempting to relate the biological responses of terrestrial animals to air temperature. But air temperature typically plays a lesser role in the heat exchange of those animals than does radiant heat. Under radiant load, animals can gain heat even when body surface temperature exceeds air temperature. However, animals can buffer the impacts of radiant heat exposure: burrows and other refuges may block solar radiant heat fully, but trees and agricultural shelters provide only partial relief. For animals that can do so effectively, evaporative cooling will be used to dissipate body heat. Evaporative cooling is dependent directly on the water vapour pressure difference between the body surface and immediate surroundings, but only indirectly on relative humidity. High relative humidity at high air temperature implies a high water vapour pressure, but evaporation into air with 100% relative humidity is not impossible. Evaporation is enhanced by wind, but the wind speed reported by meteorological services is not that experienced by animals; instead, the wind, air temperature, humidity and radiation experienced is that of the animal's microclimate. In this Commentary, we discuss how microclimate should be quantified to ensure accurate assessment of an animal's thermal environment. We propose that the microclimate metric of dry heat load to which the biological responses of animals should be related is black-globe temperature measured on or near the animal, and not air temperature. Finally, when analysing those responses, the metric of humidity should be water vapour pressure, not relative humidity.

Pekin ducks are motivated to lay in their preferred nest substrate.

Nest design is one factor contributing to floor-laying in farmed poultry. We investigated: (i) if ducks (Anas platyrhynchos) prefer a particular nest substrate; and (ii) how important that preference is to them, indicated by stress-induced hyperthermia, egg albumen corticosterone, and behaviour. Twelve female ducks that were trained in a push-door task had temperature data loggers implanted. Preference testing identified the most and least preferred nest substrates between sawdust, astroturf, and hemp fibres. A behavioural demand test then required the ducks to use push-doors to access nests containing either the most or least preferred substrate. The preferred substrate door was loaded with increasing weight (0-120% of bodyweight, four nights per workload) and eventually blocked to prevent nest access. The least preferred substrate door remained unweighted. The overall rank order of substrate preferences was sawdust > hemp > astroturf. Six of the 12 birds pushed all workloads and attempted to push the blocked door. The area under the curve (AUC) of hyperthermia was larger when the preferred substrate door was blocked compared with 0%. The AUC did not differ between nights 2-4 of the blocked door compared with night 1. Egg albumen corticosterone was unaffected. We conclude that laying Pekin ducks prefer manipulatable nest substrates and accessing one is important enough to pay a cost. The results indicate that a manipulatable substrate should be provided to commercially farmed nesting ducks.

Daily temperature cycles prolong lifespan and have sex-specific effects on peripheral clock gene expression in Drosophila melanogaster.

Circadian rhythms optimize health by coordinating the timing of physiological processes to match predictable daily environmental challenges. The circadian rhythm of body temperature is thought to be an important modulator of molecular clocks in peripheral tissues, but how daily temperature cycles affect physiological function is unclear. Here, we examined the effect of constant temperature (Tcon, 25°C) and cycling temperature (Tcyc, 28°C:22°C during light:dark) paradigms on lifespan of Drosophila melanogaster, and the expression of clock genes, heat shock protein 83 (Hsp83), Frost (Fst) and senescence marker protein-30 (smp-30). Male and female D. melanogaster housed at Tcyc had longer median lifespans than those housed at Tcon. Tcyc induced robust Hsp83 rhythms and rescued the age-related decrease in smp-30 expression that was observed in flies at Tcon, potentially indicating an increased capacity to cope with age-related cellular stress. Ageing under Tcon led to a decrease in the amplitude of expression of all clock genes in the bodies of male flies, except for cyc, which was non-rhythmic, and for per and cry in female flies. Strikingly, housing under Tcyc conditions rescued the age-related decrease in amplitude of all clock genes, and generated rhythmicity in cyc expression, in the male flies, but not the female flies. The results suggest that ambient temperature rhythms modulate D. melanogaster lifespan, and that the amplitude of clock gene expression in peripheral body clocks may be a potential link between temperature rhythms and longevity in male D. melanogaster. Longevity due to Tcyc appeared predominantly independent of clock gene amplitude in female D. melanogaster.

How dryland mammals will respond to climate change: the effects of body size, heat load and a lack of food and water.

Mammals in drylands are facing not only increasing heat loads but also reduced water and food availability as a result of climate change. Insufficient water results in suppression of evaporative cooling and therefore increases in body core temperature on hot days, while lack of food reduces the capacity to maintain body core temperature on cold nights. Both food and water shortage will narrow the prescriptive zone, the ambient temperature range over which body core temperature is held relatively constant, which will lead to increased risk of physiological malfunction and death. Behavioural modifications, such as shifting activity between night and day or seeking thermally buffered microclimates, may allow individuals to remain within the prescriptive zone, but can incur costs, such as reduced foraging or increased competition or predation, with consequences for fitness. Body size will play a major role in predicting response patterns, but identifying all the factors that will contribute to how well dryland mammals facing water and food shortage will cope with increasing heat loads requires a better understanding of the sensitivities and responses of mammals exposed to the direct and indirect effects of climate change.

Heat stress and poultry production: impact and amelioration.

Globally, the poultry industry is gaining significant importance among the agricultural and its allied sectors. However, heat stress was found to negatively affect the poultry production particularly in the tropical regions. This review is therefore an attempt to generate information pertaining to the impacts of heat stress on poultry production and its amelioration. Heat stress reduces the growth, reproductive performance, and egg production in poultry birds. The reduction in productive potential of poultry birds on exposure to heat stress may be attributed to the deviation of energy resources from production to adaptation pathway. There are different approaches pertaining to relieving the adverse impacts of heat stress on poultry production. These approaches can be broadly categorized under genetic, management, and nutritional strategies. These approaches may reduce the negative effects of heat stress and enhance the productive performance of poultry birds. The management strategies include appropriate shelter design, providing shade, using sprinklers, implementing cooling devices, and using fans and ventilation systems. The recommended floor space for mature birds weighing 1.7 kg is 0.06 m2/bird while it is 0.13 m2/bird for the birds weighing 3.5 kg with 27.8 kg/m2 bird density in either case. The nutritional interventions comprise ration balancing and providing essential micronutrients to improve the productive and reproductive performance in poultry birds. Fat, antioxidants, yeast, and electrolyte supplementations are some of the most commonly used nutritional strategies to ensure optimum production in the poultry industry. Furthermore, providing adequate water supply and disease surveillance measures may help to ensure optimum meat and egg production in the birds. The advanced biotechnological tools may aid to identify suitable genetic markers in poultry birds which might help in developing new strains of higher thermo-tolerance by designing suitable breeding program involving marker-assisted selection. These strategies may help to optimize and sustain poultry production in the changing climate scenario.

Diet-altered body temperature rhythms are associated with altered rhythms of clock gene expression in peripheral tissues in vivo.

Temperature rhythms can act as potent signals for the modulation of the amplitude and phase of clock gene expression in peripheral organs in vitro, but the relevance of the circadian rhythm of core body temperature (Tc) as a modulating signal in vivo has not yet been investigated. Using calorie restriction and cafeteria feeding, we induced a larger and a dampened Tc amplitude, respectively, in male Wistar rats, and investigated the circadian expression profile of the core clock genes Bmal1, Per2, Cry1, and Rev-erbα, the heat-responsive genes heat shock protein 90 (Hsp90) and cold-inducible RNA binding protein (Cirbp), and Pgc1α, Pparα/γ/δ, Glut1/4, and Chop10 in the liver, skeletal muscle, white adipose tissue (WAT), and adrenal glands. Diet-altered Tc rhythms differentially affected the profiles of clock genes, Hsp90, and Cirbp expression in peripheral tissues. Greater Tc amplitudes elicited by calorie restriction were associated with large amplitudes of Hsp90 and Cirbp expression in the liver and WAT, in which larger amplitudes of clock gene expression were also observed. The amplitudes of metabolic gene expression were greater in the WAT, but not in the liver, in calorie-restricted rats. Conversely, diet-altered Tc rhythms were not translated to distinct changes in the amplitude of Hsp90, Cirbp, or clock or metabolic genes in the skeletal muscle or adrenal glands. While it was not possible to disentangle the effects of diet and temperature in this model, taken together with previous in vitro studies, our study presents novel data consistent with the notion that the circadian Tc rhythm can modulate the amplitude of circadian gene expression in vivo. The different responses of Hsp90 and Cirbp in peripheral tissues may be linked to the tissue-specific responses of peripheral clocks to diet and/or body temperature rhythms, but the association with the amplitude of metabolic gene expression is limited to the WAT.

Keeping cool in the heat: Behavioral thermoregulation and body temperature patterns in wild vervet monkeys.

OBJECTIVES: Climate change is having a significant impact on biodiversity and increasing attention is therefore being devoted to identifying the behavioral strategies that a species uses to cope with climatic stress. We explore how wild vervet monkeys (Chlorocebus pygerythrus) respond to heat stress, and how behavioral adaptations are used to regulate body temperature. MATERIALS AND METHODS: We implanted wild vervet monkeys with temperature-sensitive data loggers and related the body temperature rhythms of these animals to their use of thermoregulatory behaviors. RESULTS: Environmental temperature had a positive effect on the mean, minima and maxima of daily body temperatures. Environmental temperature had a positive effect on the amount of time that vervet monkeys spent in the shade, and animals that spent more time in the shade had lower body temperature maxima. Drinking water did not have a proximate effect on body temperature, most likely a consequence of their regular access to drinking water. Body temperatures were observed to decrease after swimming events, but tended to return to pre-swim temperatures within 1 hr, suggesting a limited thermal benefit of this behavior. CONCLUSIONS: Our data support the view that vervet monkeys cope well in the heat, and use behavior as a means to aid thermoregulation. The ability of primates to be flexible in their use of thermoregulatory behaviors can contribute positively to their capacity to cope with environmental variability. However, given its broad effect on plant productivity and habitat loss, climate change is a major threat to species' biogeographical distribution and survival.

Scaling of cardiac morphology is interrupted by birth in the developing sheep Ovis aries.

Scaling of the heart across development can reveal the degree to which variation in cardiac morphology depends on body mass. In this study, we assessed the scaling of heart mass, left and right ventricular masses, and ventricular mass ratio, as a function of eviscerated body mass across fetal and postnatal development in Horro sheep Ovis aries (~50-fold body mass range; N = 21). Whole hearts were extracted from carcasses, cleaned, dissected into chambers and weighed. We found a biphasic relationship when heart mass was scaled against body mass, with a conspicuous 'breakpoint' around the time of birth, manifest not by a change in the scaling exponent (slope), but rather a jump in the elevation. Fetal heart mass (g) increased with eviscerated body mass (Mb , kg) according to the power equation 4.90 Mb0.88 ± 0.26 (± 95%CI) , whereas postnatal heart mass increased according to 10.0 Mb0.88 ± 0.10 . While the fetal and postnatal scaling exponents are identical (0.88) and reveal a clear dependence of heart mass on body mass, only the postnatal exponent is significantly less than 1.0, indicating the postnatal heart becomes a smaller component of body mass as the body grows, which is a pattern found frequently with postnatal cardiac development among mammals. The rapid doubling in heart mass around the time of birth is independent of any increase in body mass and is consistent with the normalization of wall stress in response to abrupt changes in volume loading and pressure loading at parturition. We discuss variation in scaling patterns of heart mass across development among mammals, and suggest that the variation results from a complex interplay between hard-wired genetics and epigenetic influences.

Scaling of morphology and ultrastructure of hearts among wild African antelope.

The hearts of smaller mammals tend to operate at higher mass-specific mechanical work rates than those of larger mammals. The ultrastructural characteristics of the heart that allow for such variation in work rate are still largely unknown. We have used perfusion-fixation, transmission electron microscopy and stereology to assess the morphology and anatomical aerobic power density of the heart as a function of body mass across six species of wild African antelope differing by approximately 20-fold in body mass. The survival of wild antelope, as prey animals, depends on competent cardiovascular performance. We found that relative heart mass (g kg-1 body mass) decreases with body mass according to a power equation with an exponent of -0.12±0.07 (±95% confidence interval). Likewise, capillary length density (km cm-3 of cardiomyocyte), mitochondrial volume density (fraction of cardiomyocyte) and mitochondrial inner membrane surface density (m2 cm-3 of mitochondria) also decrease with body mass with exponents of -0.17±0.16, -0.06±0.05 and -0.07±0.05, respectively, trends likely to be associated with the greater mass-specific mechanical work rate of the heart in smaller antelope. Finally, we found proportionality between quantitative characteristics of a structure responsible for the delivery of oxygen (total capillary length) and those of a structure that ultimately uses that oxygen (total mitochondrial inner membrane surface area), which provides support for the economic principle of symmorphosis at the cellular level of the oxygen cascade in an aerobic organ.

Revisiting concepts of thermal physiology: Predicting responses of mammals to climate change.

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.

Scaling of the ankle extensor muscle-tendon units and the biomechanical implications for bipedal hopping locomotion in the post-pouch kangaroo Macropus fuliginosus.

Bipedal hopping is used by macropods, including rat-kangaroos, wallabies and kangaroos (superfamily Macropodoidea). Interspecific scaling of the ankle extensor muscle-tendon units in the lower hindlimbs of these hopping bipeds shows that peak tendon stress increases disproportionately with body size. Consequently, large kangaroos store and recover more strain energy in their tendons, making hopping more efficient, but their tendons are at greater risk of rupture. This is the first intraspecific scaling analysis on the functional morphology of the ankle extensor muscle-tendon units (gastrocnemius, plantaris and flexor digitorum longus) in one of the largest extant species of hopping mammal, the western grey kangaroo Macropus fuliginosus (5.8-70.5 kg post-pouch body mass). The effective mechanical advantage of the ankle extensors does not vary with post-pouch body mass, scaling with an exponent not significantly different from 0.0. Therefore, larger kangaroos balance rotational moments around the ankle by generating muscle forces proportional to weight-related gravitational forces. Maximum force is dependent upon the physiological cross-sectional area of the muscle, which we found scales geometrically with a mean exponent of only 0.67, rather than 1.0. Therefore, larger kangaroos are limited in their capacity to oppose large external forces around the ankle, potentially compromising fast or accelerative hopping. The strain energy return capacity of the ankle extensor tendons increases with a mean exponent of ~1.0, which is much shallower than the exponent derived from interspecific analyses of hopping mammals (~1.4-1.9). Tendon safety factor (ratio of rupture stress to estimated peak hopping stress) is lowest in the gastrocnemius (< 2), and it decreases with body mass with an exponent of -0.15, extrapolating to a predicted rupture at 160 kg. Extinct giant kangaroos weighing 250 kg could therefore not have engaged in fast hopping using 'scaled-up' lower hindlimb morphology of extant western grey kangaroos.

Heterothermy is associated with reduced fitness in wild rabbits.

An increase in variation in the 24 h pattern of body temperature (heterothermy) in mammals can be induced by energy and water deficits. Since performance traits such as growth and reproduction also are impacted by energy and water balance, we investigated whether the characteristics of the body temperature rhythm provide an indication of the reproductive success of an individual. We show that the amplitude of the daily rhythm of body temperature in wild rabbits (Oryctolagus cuniculus) prior to breeding is inversely related to the number of pregnancies in the subsequent seven months, while the minimum daily body temperature is positively correlated to the number of pregnancies. Because reproductive output could be predicted from characteristics of the core body temperature rhythm prior to the breeding season, we propose that the pattern of the 24 h body temperature rhythm could provide an index of animal fitness in a given environment.

Thermal consequences of increased pelt loft infer an additional utilitarian function for grooming.

A strong case has been made that the primary function of grooming is hygienic. Nevertheless, its persistence in the absence of hygienic demand, and its obvious tactical importance to members of primate groups, underpins the view that grooming has become uncoupled from its utilitarian objectives and is now principally of social benefit. We identify improved thermoregulatory function as a previously unexplored benefit of grooming and so broaden our understanding of the utilitarian function of this behavior. Deriving the maximum thermal benefits from the pelt requires that it be kept clean and that the loft of the pelt is maintained (i.e., greater pelt depth), both of which can be achieved by grooming. In a series of wind-tunnel experiments, we measured the heat transfer characteristics of vervet monkey (Chlorocebus pygerythrus) pelts in the presence and absence of backcombing, which we used as a proxy for grooming. Our data indicate that backcombed pelts have improved thermal performance, offering significantly better insulation than flattened pelts and, hence, better protection from the cold. Backcombed pelts also had significantly lower radiant heat loads compared to flattened pelts, providing improved protection from radiant heat. Such thermal benefits, therefore, furnish grooming with an additional practical value to which its social use is anchored. Given the link between thermoregulatory ability and energy expenditure, our findings suggest that grooming for thermal benefits may be an important explanatory variable in the relationship between levels of sociability and individual fitness. Am. J. Primatol. 78:456-461, 2016. © 2015 Wiley Periodicals, Inc.

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.

Translating animal model research: does it matter that our rodents are cold?

Does it matter that rodents used as preclinical models of human biology are routinely housed below their thermoneutral zone? We compile evidence showing that such rodents are cold-stressed, hypermetabolic, hypertensive, sleep-deprived, obesity-resistant, fever-resistant, aging-resistant, and tumor-prone compared with mice housed at thermoneutrality. The same genotype of mouse has a very different phenotype and response to physiological or pharmacological intervention when raised below or at thermoneutrality.

Scaling of left ventricle cardiomyocyte ultrastructure across development in the kangaroo Macropus fuliginosus.

The heart and left ventricle of the marsupial western grey kangaroo Macropus fuliginosus exhibit biphasic allometric growth, whereby a negative shift in the trajectory of cardiac growth occurs at pouch exit. In this study, we used transmission electron microscopy to examine the scaling of left ventricle cardiomyocyte ultrastructure across development in the western grey kangaroo over a 190-fold body mass range (0.355-67.5 kg). The volume-density (%) of myofibrils, mitochondria, sarcoplasmic reticuli and T-tubules increase significantly during in-pouch growth, such that the absolute volume (ml) of these organelles scales with body mass (Mb; kg) with steep hyperallometry: 1.41Mb (1.38), 0.64Mb (1.29), 0.066Mb (1.45) and 0.035Mb (1.87), respectively. Maturation of the left ventricle ultrastructure coincides with pouch vacation, as organelle volume-densities scale independent of body mass across post-pouch development, such that absolute organelle volumes scale in parallel and with relatively shallow hypoallometry: 4.65Mb (0.79), 1.75Mb (0.77), 0.21Mb (0.79) and 0.35Mb (0.79), respectively. The steep hyperallometry of organelle volumes and volume-densities across in-pouch growth is consistent with the improved contractile performance of isolated cardiac muscle during fetal development in placental mammals, and is probably critical in augmenting cardiac output to levels necessary for endothermy and independent locomotion in the young kangaroo as it prepares for pouch exit. The shallow hypoallometry of organelle volumes during post-pouch growth suggests a decrease in relative cardiac requirements as body mass increases in free-roaming kangaroos, which is possibly because the energy required for hopping is independent of speed, and the capacity for energy storage during hopping could increase as the kangaroo grows.

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.

Special K: testing the potassium link between radioactive rubidium (86Rb) turnover and metabolic rate.

The measurement of (86)Rb turnover recently has been suggested as a useful method for measuring field metabolic rate in small animals. We investigated a proposed mechanism of (86)Rb turnover, its analogy to K(+), by comparing the turnover of (86)Rb in a model insect, the rhinoceros beetle Xylotrupes gideon, fed a diet of plum jam or plum jam enriched with K(+) or Rb(+). The turnover of (86)Rb in the beetles on the K(+) and the Rb(+) diets was higher than that for beetles on the jam diet (F2,311=32.4; P=1.58×10(-13)). We also exposed the beetles to different ambient temperatures to induce differences in metabolic rate ( ) while feeding them the jam and K(+) diets. was higher at higher ambient temperature (Ta) for both jam (F1,11=14.56; P=0.003) and K(+) (F1,8=15.39; P=0.004) dietary groups, and the turnover of (86)Rb was higher at higher Ta for both jam (F1,11=10.80; P=0.007) and K(+) (F1,8=12.34; P=0.008) dietary groups. There was a significant relationship between (86)Rb turnover and for both the jam (F1,11=35.00; P=1.0×10(-3)) and the K(+) (F1,8=64.33; P=4.3×10(-5)) diets, but the relationship differed between the diets (F1,19=14.07; P=0.001), with a higher (86)Rb turnover in beetles on the K(+)-enriched than on the jam diet at all Ta. We conclude that (86)Rb turnover is related to K(+) metabolism, and that this is the mechanism of the relationship between (86)Rb turnover and . Studies relating (86)Rb turnover to should maintain dietary [K] as close as possible to that of natural diets for the most accurate calibrations for free-ranging animals.

Blood flow for bone remodelling correlates with locomotion in living and extinct birds.

Nutrient arteries enter limb bones through discrete foramina on the shafts. They are required for bone remodelling in response to mechanical loading and dynamic forces imposed by locomotion. The cross-sectional area of the nutrient foramen of the femur represents an index of blood flow rate to the shaft and thus provides insight into the animal's level of activity. Morphometric data on femoral length, mass and foramen size from 100 extant bird species and eight extinct moa species were analysed allometrically and phylogenetically. The nutrient foramen blood flow index (Qi) and femur mass (Mf) increase with body mass (Mb). At 1 kg body mass, cursorial species have approximately 2.1 times higher Qi and 1.9 times heavier Mf than volant species. The scaling of Qi on Mf is independent of the primary mode of locomotion, but the ratio Qi/Mf decreases significantly in larger birds, although absolute Qi increases. The overall avian equation for Qi on Mb is not significantly different from previous data from mammals, but when differences in blood pressure are accounted for, estimated blood flow to the femur is approximately 1.9 times higher in cursorial birds than in mammals, possibly in relation to bipedalism and quadrupedalism, respectively. Femoral bone blood flow in both endothermic groups is estimated to be 50-100 times higher than in ectothermic reptiles.