Rest-phase Hypothermia Research Articles

Thermoregulatory costs of the innate immune response are modulated by winter food availability in a small passerine.

In winter, a challenge to the immune system could pose a major energetic trade-off for small endotherms, whereby increasing body temperature (Tb ; i.e. eliciting fever) may be beneficial to fight off invading pathogens yet incur a cost for vital energy-saving mechanisms. Having previously shown that the availability and acquisition of energy, through manipulation of food predictability, influences the depth of rest-phase hypothermia in a wild bird in winter, we expected that the nocturnal thermoregulatory component of the acute-phase immune response would also be modulated by food availability. By manipulating winter food availability in the wild for great tits Parus major, we created an area offering a "predictable" and constant supply of food at feeding stations, while an unmanipulated area was subject to naturally "unpredictable" food. Birds were subject to an immune challenge shortly after dusk, and the thermoregulatory response was quantified via continuous recording of nocturnal Tb , using subcutaneous thermo-sensitive transponders. In response to immune challenge, all birds increased Tb above the level maintained prior to immune challenge (i.e. baseline). However, birds experiencing a naturally unpredictable food supply elevated Tb more than birds subject to predictable food resources, during the period of expected peak response and for the duration of the night. Furthermore, "unpredictable-food" females took longer to return to their baseline Tb . Assuming baseline nocturnal Tb reflects an individual's optimum, based on their available energy budget, the metabolic cost of eliciting an acute-phase response for "unpredictable-food" birds was more than double that of "predictable-food" birds. The absence of differences in absolute Tb during the peak response could support the idea of an optimal Tb for immune system activation. Alternatively, "predictable-food" birds could have acquired tolerance to endotoxin as a result of using feeding stations, thus affording them reduced costs associated with a smaller Tb increase. These findings shed new light on the trade-offs associated with food acquisition, thermoregulation and immune function in small-bodied endotherms. This knowledge is of increasing importance, given the predicted elevated pathogen risks associated with changes in climate and anthropogenic activities.

Plasticity of mitochondrial function safeguards phosphorylating respiration during in vitro simulation of rest-phase hypothermia.

Many animals downregulate body temperature to save energy when resting (rest-phase hypothermia). Small birds that winter at high latitudes have comparatively limited capacity for hypothermia and so pay large energy costs for thermoregulation during cold nights. Available evidence suggests this process is fueled by adenosine triphosphate (ATP)-dependent mechanisms. Most ATP is produced by oxidative phosphorylation in the mitochondria, but mitochondrial respiration may be lower during hypothermia because of the temperature dependence of biological processes. This can create conflict between increased organismal ATP demand and a lower mitochondrial capacity to provide it. We studied this in blood cell mitochondria of wild great tits (Parus major) by simulating rest-phase hypothermia via a 6°C reduction in assay temperature in vitro. The birds had spent the night preceding the experiment in thermoneutrality or in temperatures representing mild or very cold winter nights, but night temperatures never affected mitochondrial respiration. However, across temperature groups, endogenous respiration was 14% lower in hypothermia. This did not reflect general thermal suppression of mitochondrial function because phosphorylating respiration was unaffected by thermal state. Instead, hypothermia was associated with a threefold reduction of leak respiration, from 17% in normothermia to 4% in hypothermia. Thus, the coupling of total respiration to ATP production was 96% in hypothermia, compared to 83% in normothermia. Our study shows that the thermal insensitivity of phosphorylation combined with short-term plasticity of leak respiration may safeguard ATP production when endogenous respiration is suppressed. This casts new light on the process by which small birds endure harsh winter cold and warrants future tests across tissues in vivo.

Predictability of food supply modulates nocturnal hypothermia in a small passerine : Food supply and nocturnal hypothermia

The combination of short days and long cold winter nights, in temperate regions, presents a major challenge for small diurnal birds. Small birds regularly employ heterothermy and enter rest-phase hypothermia during winter nights to conserve energy. However, we know little about how environmental conditions, such as food availability, shape these strategies. We experimentally manipulated food availability in winter to free-living great tits Parus major. A 'predictable' and constant food supply was provided to birds in one area of a forest, while birds in another area did not have access to a reliable supplementary food source. We found that predictability of food affected the extent of nocturnal hypothermia, but the response differed between the sexes. Whereas male nocturnal body temperature was similar regardless of food availability, females exposed to a naturally 'unpredictable' food supply entered deeper hypothermia at night, compared with females that had access to predictable food and compared with males in both treatment groups. We suggest that this response is likely a consequence of dominance, and subdominant females subject to unpredictable food resources cannot maintain sufficient energy intake, resulting in a higher demand for energy conservation at night. (Less)

Rest-Phase Hypothermia Reveals a Link Between Aging and Oxidative Stress: A Novel Hypothesis.

In endotherms, growth, reproduction, and survival are highly depended on energy metabolism. Maintenance of constant body temperature can be challenging for endotherms under continuously changing environmental conditions, such as low or high ambient temperatures or limited food. Thus, many birds may drop body temperature below normothermic values during the night, known as rest-phase hypothermia, presumably to decrease energy metabolism. Under the assumption of the positive link between aerobic metabolism and reactive oxygen species, it is reasonable to suggest that low body temperature, a proxy of energy metabolism, will affect oxidative stress of the birds. Aging may considerably affect behavior, performance and physiology in birds and still requires further investigation to understand age-specific changes along the lifespan of the organism. Until today, age-specific rest-phase hypothermic responses and their effect on oxidant-antioxidant status have never been investigated. We exposed 25 zebra finches (Taeniopygia guttata) of three age classes, 12 young birds (1.1–1.3 years old), 8 middle-aged (2.4–2.8 years old), and 5 old birds (4.2–7.5 years old) to day-long food deprivation or provided them normal access to food under thermoneutral conditions. We compared night-time body temperature, measured through implanted data loggers, and quantified plasma oxidative status (uric acid, antioxidant capacity, and d-ROM assay) the following morning. We found age-related differences in night-time body temperature following a day-long food deprivation while all three age groups remained normothermic in the night following a day with access to food. The lowest minimum body temperature (LSM ± SE: 36.6 ± 0.2°C) was observed in old individuals during rest-phase hypothermia. Surprisingly, these old birds also revealed the highest levels of plasma oxidative damage, while young and middle-aged birds maintained higher night-time body temperature and showed lower values of oxidative damage. These results lead us to propose a novel hypothesis on how aging may lead to an accumulation of oxidative damage; the impaired physiological capacity to thermoregulate with advancing age does increase the risk of oxidative stress under challenging conditions. When energy is limited, the risk to encounter oxidative stress is increasing via a compensation to defend normothermic body temperatures.

Predictability of food supply modulates nocturnal hypothermia in a small passerine.

The combination of short days and long cold winter nights, in temperate regions, presents a major challenge for small diurnal birds. Small birds regularly employ heterothermy and enter rest-phase hypothermia during winter nights to conserve energy. However, we know little about how environmental conditions, such as food availability, shape these strategies. We experimentally manipulated food availability in winter to free-living great tits Parus major. A ‘predictable' and constant food supply was provided to birds in one area of a forest, while birds in another area did not have access to a reliable supplementary food source. We found that predictability of food affected the extent of nocturnal hypothermia, but the response differed between the sexes. Whereas male nocturnal body temperature was similar regardless of food availability, females exposed to a naturally ‘unpredictable' food supply entered deeper hypothermia at night, compared with females that had access to predictable food and compared with males in both treatment groups. We suggest that this response is likely a consequence of dominance, and subdominant females subject to unpredictable food resources cannot maintain sufficient energy intake, resulting in a higher demand for energy conservation at night.

Nocturnal body temperature in wintering blue tits is affected by roost-site temperature and body reserves

Birds commonly use rest-phase hypothermia, a controlled reduction of body temperature (T(b)), to conserve energy during times of high metabolic demands. We assessed the flexibility of this heterothermic strategy by increasing roost-site temperature and recording the subsequent T(b) changes in wintering blue tits (Cyanistes caeruleus L.), assuming that blue tits would respond to treatment by increasing T(b). We found that birds increased T(b) when roost-site temperature was increased, but only at low ambient temperatures. Moreover, birds with larger fat reserves regulated T(b) at higher levels than birds carrying less fat. This result implies that a roosting blue tit maintains its T(b) at the highest affordable level, as determined by the interacting effect of ecophysiological costs associated with rest-phase hypothermia and energy reserves, in order to minimize potential fitness costs associated with a low T(b).

Patterns and dynamics of rest-phase hypothermia in wild and captive blue tits during winter

We evaluated biotic and abiotic predictors of rest-phase hypothermia in wintering blue tits (Cyanistes caeruleus) and also assessed how food availability influences nightly thermoregulation. On any given night, captive blue tits (with unrestricted access to food) remained largely homeothermic, whereas free-ranging birds decreased their body temperature (T(b)) by about 5 degrees C. This was not an effect of increased stress in the aviary as we found no difference in circulating corticosterone between groups. Nocturnal T(b) in free-ranging birds varied with ambient temperature, date and time. Conversely, T(b) in captive birds could not be explained by climatic or temporal factors, but differed slightly between the sexes. We argue that the degree of hypothermia is controlled predominantly by birds' ability to obtain sufficient energy reserves during the day. However, environmental factors became increasingly important for thermoregulation when resources were limited. Moreover, as birds did not enter hypothermia in captivity when food was abundant, we suggest that this strategy has associated costs and hence is avoided whenever resource levels permit.

Migrating blackcaps huddle at night at stopover sites

Small migratory birds employ a wide range of behavioral and physiological strategies to accelerate their fuel accumulation rate at migratory stopovers. Although they could potentially reduce the cost of night‐time rest by huddling with conspecifics, to date only anecdotal information exists about this behavior. We found that resting blackcaps (Sylvia atricapilla) regularly huddled in groups of two to six individuals in aviaries during migratory stopover. This occurred in spring migration in the Negev Desert and in autumn migration in central Poland. On some nights, huddling blackcaps used rest‐phase hypothermia, but on other nights, huddling birds maintained higher body temperatures at night than solitarily roosting individuals. Since migrating birds congregate at migratory stopovers, we anticipate huddling to be a common energy saving phenomenon among small migrating passerines.

Facultative Rest-Phase Hypothermia in Free-Ranging White-Throated Sparrows

Abstract Shallow facultative rest-phase hypothermia has been reported in a number of passerine families, but few published data exist about its use by free- ranging birds. We used temperature-sensitive radio- transmitters to determine whether White-throated Sparrows (Zonotrichia albicollis) employ nocturnal hypothermia during winter. We measured skin temperatures of 24 free-ranging sparrows between 13:00 and 14:00 and between 02:00 and 03:00 for each of three days and nights per subject. The average nightly skin- temperature reduction per individual was 3.4 ± 1.0°C (SD). Skin temperature reductions ranged from 0.2°C to 7.0°C among all individuals. There was a significant negative correlation between the magnitude of skin temperature decline and nighttime ambient temperature. Additionally, we found a negative trend between depth of hypothermia and a body density index. Fase de Reposo Hipotérmica Facultativa en Individuos de Zonotrichia albicollis que se Desplazan Libremente Resumen. La fase de reposo facultativa somera ha sido mencionada para un número de familias de paseriformes, pero existen pocos datos publicados sobre su uso por parte de aves que se desplazan libremente. Usamos radio transmisores sensibles a la temperatura para determinar si Zonotrichia albicollis emplea hipotermia nocturna durante el invierno. Medimos la temperatura de la piel de 24 individuos que se desplazan libremente entre las 13:00 y 14:00 y entre las 02:00 y 03:00 durante tres días y tres noches por individuo. La reducción nocturna promedio de la temperatura de la piel por individuo fue 3.4 ± 1.0°C (DE). Las reducciones de la temperatura de la piel variaron entre 0.2°C y 7.0°C considerando todos los individuos. Hubo una correlación negativa significativa entre la disminución de la magnitud de la temperatura de la piel y la temperatura ambiental nocturna. Adicionalmente, encontramos una tendencia negativa entre la profundidad de la hipotermia y el índice de densidad corporal.

FACULTATIVE REST-PHASE HYPOTHERMIA IN FREE-RANGING WHITE-THROATED SPARROWS

Abstract Shallow facultative rest-phase hypothermia has been reported in a number of passerine families, but few published data exist about its use by free- ranging birds. We used temperature-sensitive radio- transmitters to determine whether White-throated Sparrows (Zonotrichia albicollis) employ nocturnal hypothermia during winter. We measured skin temperatures of 24 free-ranging sparrows between 13:00 and 14:00 and between 02:00 and 03:00 for each of three days and nights per subject. The average nightly skin- temperature reduction per individual was 3.4 ± 1.0°C (SD). Skin temperature reductions ranged from 0.2°C to 7.0°C among all individuals. There was a significant negative correlation between the magnitude of skin temperature decline and nighttime ambient temperature. Additionally, we found a negative trend between depth of hypothermia and a body density index. Fase de Reposo Hipotermica Facultativa en Individuos de Zonotrichia albicollis que se Desplazan Libremente Resumen. La fase de reposo facul...

Facultative hypothermic responses in an Afrotropical arid-zone passerine, the red-headed finch (Amadina erythrocephala).

We investigated thermoregulation and facultative hypothermic responses to food deprivation in the red-headed finch (Amadina erythrocephala), a 22-g passerine endemic to the arid regions of southern Africa. We predicted that, like most other passerines investigated, A. erythrocephala exhibits shallow rest-phase hypothermia, but not torpor. We observed significant reductions in rest-phase energy expenditure and body temperature (Tb) in response to restricted feeding. The maximum extent of Tb reduction (ca. 5 degrees C) and energy savings (ca. 10%) were consistent with those reported for a number of other passerine species. The lowest Tb we observed in a bird able to arouse spontaneously was 34.8 degrees C. The parameters of facultative hypothermic responses in A. erythrocephala were indicative of shallow rest-phase hypothermia, but not torpor. The limited available data on hypothermic responses in passerines suggest that many species do not possess the capacity for torpor. In passerines, torpor appears to be restricted to a few nectarivores and aerial insectarivores, and may have evolved independently of the torpor observed in non-passerine taxa such as the Trochiliformes and Caprimulgidae. The basal metabolic rate (BMR) of A. erythrocephala was 30-46% lower than predicted by various allometric equations, but was similar to the predicted BMR for a 22-g desert bird.

AVIAN FACULTATIVE HYPOTHERMIC RESPONSES: A REVIEW

Abstract Recent evidence suggests that avian facultative hypothermic responses are more common, and occur in a wider variety of ecological contexts, than previously thought. The capacity for shallow hypothermia (rest-phase hypothermia) occurs throughout the avian phylogeny, but the capacity for pronounced hypothermia (torpor) appears to be restricted to certain taxa. Families in which torpor has been reported include the Todidae, Coliidae, Trochilidae, Apodidae, Caprimulgidae, and Columbidae. Facultative hypothermia occurs in species ranging in body mass (Mb) from <3 g to ca. 6500 g. Minimum body temperature (Tb) during hypothermia is continuously distributed from 4.3°C to ca. 38°C. The physiological distinction between torpor and rest-phase hypothermia is unclear. Whereas these two responses have traditionally been distinguished on the basis of Tb, we find little support for the biological reality of specific Tb limits. Instead, we argue that emphasis should be placed on understanding the relationship be...

Heterothermic responses in the speckled mousebird (Colius striatus).

We investigated normothermic thermoregulation and heterothermic responses to restricted food in the speckled mousebird Colius striatus, in the context of the widely accepted distinction between normothermia, rest-phase hypothermia, and torpor. Normothermic thermoregulation differed from typical endothermic patterns in that rest-phase body temperature (Tb) was not maintained with respect to a constant setpoint. Instead, Tb decreased during the course of the rest-phase, with the highest cooling rates observed at moderate ambient temperatures (Ta). Restricted food was associated with significant reductions in rest-phase Tb and metabolic rate. The lowest Tb recorded in a bird which was able to arouse spontaneously, was 18.2 degrees C. However, we were unable to clearly discern between normothermic, hypothermic and torpor Tb ranges. Furthermore, heterothermic responses did not accord with the patterns typically observed in birds and mammals. Metabolic suppression normally associated with entry into torpor and the defence of a torpor Tb setpoint was largely absent. The mousebirds significantly reduced their energy expenditure when heterothermic at moderate TaS only. We suggest that the observed patterns of thermoregulation in C. striatus, as well those previously reported in Colius colius, are associated with plesiomorphic clustering behaviour in the Coliiformes, and the tandem evolution of behavioural and metabolic thermoregulation.

Fever: Role of Pyrogens and Cryogens

The biology of cytokines is one of the most rapidly growing areas of biomedical research. It is understandable why the assumption was made several years ago that EP was equivalent to IL-1 (both alpha and beta) and subsequently to IL-1 alpha, IL-1 beta, and TNF. However, as more data have been obtained, it has become clearer that many cytokines and hormones are capable of participating in the febrile response. It is also becoming apparent that EPs and ECs might influence body temperature during nonpathological states, perhaps contributing to the elevation in temperature during or after exercise, the circadian variation in temperature, and others. Medical textbooks have begun to list IL-1 as the EP. As I attempted to make clear in this review, evidence that IL-1 alpha is a circulating EP is poor. The evidence is considerably stronger that IL-1 beta is an EP, at least during LPS-induced fever in rodents. The point I have tried to emphasize is that before any cytokine or hormone can be characterized as an EP or EC (or, for that matter, as being involved in any of the acute phase responses), clearly established rules must be followed, which are patterned after the traditional criteria used by Koch to distinguish a pathogenic microorganism from a benign one. As summarized in Tables 4 and 5, there are many candidates for EPs and ECs, but much more experimental evidence is essential before we gain a clear understanding of the relationship between contact with an exogenous pyrogen, the release of EPs and ECs, and the development of fever.

Gaseous Metabolism and Water Relations of the Zebra Finch, Taeniopygia castanotis

Gaseous Metabolism and Water Relations of the Zebra Finch, Taeniopygia castanotis