Thermoregulation In Birds Research Articles

Sleep and Thermoregulation in Birds: Cold Exposure Reduces Brain Temperature but Has Little Influence on Sleep Time and Sleep Architecture in Jackdaws (Coloeus monedula).

Birds have an electrophysiological sleep state that resembles mammalian rapid-eye-movement (REM) sleep. However, whether its regulation and function are similar is unclear. In the current experiment, we studied REM sleep regulation in jackdaws (Coloeus monedula) by exposing the birds to low ambient temperature, a procedure that selectively suppresses REM sleep in mammals. Eight jackdaws were equipped with electrodes to record brain activity and neck muscle activity and a thermistor to record cortical brain temperature. Recordings covered a three-day period starting with a 24 h baseline day at an ambient temperature of 21 °C, followed by a 12 h cold night at 4 °C, after which the ambient temperature was restored to 21 °C for the remaining recovery period. Cold exposure at night caused a significant drop in brain temperature of 1.4 °C compared to the baseline night. However, throughout the cold night, jackdaws expressed NREM sleep and REM sleep levels that were not significantly different from the baseline. Also, EEG spectral power during NREM sleep was unaffected by cold exposure. Thus, while cold exposure had a clear effect on brain temperature in jackdaws, it did not have the same REM sleep suppressing effect reported for mammals. These findings suggest that the REM-sleep-like state in birds, unlike REM sleep in mammals, is protected against the influence of low temperature.

Microhabitat characteristics related to seasonal roost switching: implications from a threatened and introduced cockatoo species in an urban landscape

BackgroundCommunal roosting is a common avian social behaviour, which potentially provides foraging benefits, predation avoidance or thermoregulation in birds. To identify the crucial environmental factors associated with roost site selection, most studies have focused on the comparison of physical characteristics between roosts and non-roosts. However, the differences among roosts have usually been neglected and the causes of roost switching have seldom been investigated.MethodsTo explore the variations among roost sites and assess the most influential environmental factors related to seasonal roost switching, we conducted a 105-day observation on an introduced population of critically endangered Yellow-crested Cockatoo (Cacatua sulphurea) in an urban environment in Hong Kong from 2014 to 2016. We identified seven roost sites that were occupied in different seasons and then measured their microhabitat characteristics in terms of land use types, human disturbance and microclimate temperature. To quantify these differences, we used Pearson’s chi-squared test, partial least squares determinant analysis (PLS-DA) and one-way repeated measures ANOVA, respectively.ResultsOur results distinguished roost sites occupied in three seasons, i.e. spring, summer and winter roosts, using several microhabitat characteristics. The land use types were significantly associated with roosts, where spring roosts were usually located in tree-dominated areas, which are the major feeding grounds. The discriminant analysis on human disturbance variables indicated that summer roosts were positively associated with night illumination. The microhabitat temperatures of winter roosts were significantly higher than those of most other roosts on cold nights.ConclusionsThe results highlighted significant variations among roosts, and seasonal roost switching was likely driven by specific microhabitat characteristics of each roost site, such as microclimate. It also helps us understand the behavioural adaptation of birds to urban environments.

Endocrinology of thermoregulation in birds in a changing climate

The ability to maintain a (relatively) stable body temperature in a wide range of thermal environments by use of endogenous heat production is a unique feature of endotherms such as birds. Endothermy is acquired and regulated via various endocrine and molecular pathways, and ultimately allows wide aerial, aquatic, and terrestrial distribution in variable environments. However, due to our changing climate, birds are faced with potential new challenges for thermoregulation, such as more frequent extreme weather events, lower predictability of climate, and increasing mean temperature. We provide an overview on thermoregulation in birds and its endocrine and molecular mechanisms, pinpointing gaps in current knowledge and recent developments, focusing especially on non-model species to understand the generality of, and variation in, mechanisms. We highlight plasticity of thermoregulation and underlying endocrine regulation, because thorough understanding of plasticity is key to predicting responses to changing environmental conditions. To this end, we discuss how changing climate is likely to affect avian thermoregulation and associated endocrine traits, and how the interplay between these physiological processes may play a role in facilitating or constraining adaptation to a changing climate. We conclude that while the general patterns of endocrine regulation of thermogenesis are quite well understood, at least in poultry, the molecular and endocrine mechanisms that regulate, e.g. mitochondrial function and plasticity of thermoregulation over different time scales (from transgenerational to daily variation), need to be unveiled. Plasticity may ameliorate climate change effects on thermoregulation to some extent, but the increased frequency of extreme weather events, and associated changes in resource availability, may be beyond the scope and/or speed for plastic responses. This could lead to selection for more tolerant phenotypes, if the underlying physiological traits harbour genetic and individual variation for selection to act on – a key question for future research.

Using a Thermal Camera to Measure Heat Loss Through Bird Feather Coats.

Feathers are essential to insulation, and therefore to the cost of thermoregulation,in birds. There is robust literature on the energetic cost of thermoregulation in birds across a variety of ecological circumstances. However, few studies characterize the contribution of the feathers alone to thermoregulation. Several previous studies have established methods for measuring the insulation value of animal pelts, but they require destructive sampling methods that are problematic for birds, whose feathers are not distributed evenly across the skin. More information is needed about 1) how the contribution of feathers to thermoregulation varies both across and within species and 2) how feather coats may change over space and time. Reported here is a method for rapidly and directly measuring the thermal performance of feather coats and the skin using dried whole skin specimens, without the need to destroy the skin specimen. This method isolates and measures the thermal gradient across a feather coat in a way that measurements of heat loss and metabolic cost in live birds, which use behavioral and physiological strategies to thermoregulate, cannot. The method employs a thermal camera, which allows the rapid collection of quantitative thermal data to measure heat loss from a stable source through the skin. This protocol can easily be applied to various research questions, is applicable to any avian taxa, and does not require destruction of the skin specimen. Finally, it will further the understanding of the importance of passive thermoregulation in birds by simplifying and accelerating the collection of quantitative data.

Lifelong Effects of Thermal Challenges During Development in Birds and Mammals.

Before they develop competent endothermy, mammals and birds are sensitive to fluctuating temperature. It follows that early life thermal environment can trigger changes to the ontogeny of thermoregulatory control. At the ecological level, we have incomplete knowledge of how such responses affect temperature tolerance later in life. In some cases, changes to pre- and postnatal temperature prime an organism’s capacity to meet a corresponding thermal environment in adulthood. However, in other cases, developmental temperature seems to constrain temperature tolerance later in life. The timing, duration, and severity of a thermal challenge will determine whether its impact is ameliorating or constraining. However, the effects influencing the transition between these states remain poorly understood, particularly in mammals and during the postnatal period. As climate change is predicted to bring more frequent spells of extreme temperature, it is relevant to ask under which circumstances developmental thermal conditions predispose or constrain animals’ capacity to deal with temperature variation. Increasingly stochastic weather also implies increasingly decoupled early- and late-life thermal environments. Hence, there is a pressing need to understand better how developmental temperature impacts thermoregulatory responses to matched and mismatched thermal challenges in subsequent life stages. Here, we summarize studies on how the thermal environment before, and shortly after, birth affects the ontogeny of thermoregulation in birds and mammals, and outline how this might carry over to temperature tolerance in adulthood. We also identify key points that need addressing to understand how effects of temperature variation during development may facilitate or constrain thermal adaptation over a lifetime.

Lower haematocrit, haemoglobin and red blood cell number in zebra finches acclimated to cold compared to thermoneutral temperature

Thermoregulation constitutes an important share of the energy budget of endotherms. Elevated thermoregulatory requirements must be met by oxygen supply through the blood, as heat is produced mainly via aerobic processes. In contrast to mammal studies, it remains unclear whether elevated thermoregulatory needs are followed by changes in haematological variables in birds. We investigated haematocrit (HCT), haemoglobin content per volume of blood (HGB), number of red blood cells (RBCcount), and size of the erythrocytes (RBCarea) in zebra finches Taeniopygia guttata acclimated to either cold or thermoneutral ambient temperatures under laboratory conditions. Seventy‐nine females were maintained for six weeks either in cold (T = +12°C) or thermoneutral (T = +32°C) ambient temperature prior to blood collection. On average, HGB, HCT and RBCcount were significantly lower by about 10% in cold acclimated compared to thermoneutral acclimated birds. Only RBCarea was not different between the two acclimation temperatures. Mean HCT, one of the most commonly measured haematological variable for example was 53 ± 0.9% (LSM ± SEM) in thermoneutral and 49 ± 0.8 % (LSM ± SEM) in cold acclimated zebra finches. On first sight, the observed lower values for three out of the four determined haematological variables in response to acclimation to cold question oxygen supply to be indeed a limiting factor for heat production. However, higher demands of oxygen supply due to increased thermoregulation in birds may instead require specific optimisation of blood viscosity and modulation by other cardiovascular properties. Nucleated red blood cells in birds may pose different strain on blood viscosity compared to non‐nucleated mammalian erythrocytes and explain the contrasting response in haematological variables to temperature acclimation between birds and mammals.

Pharmacokinetic Behavior of Marbofloxacin in Plasma from Chickens at Different Seasons

Abstract The purpose of this study was to evaluate the differences in the disposition and plasma pharmacokinetic behavior of marbofloxacin (MAR) in broiler chickens at different seasons. Chicken broilers (n = 345) were used, in lots of 5 individuals, divided into 6 groups depending on the way of administration, intravenous or oral (dose 2 mg/kg) and the test period. Post-administration plasma samples were obtained at different times, intravenously (0.08 to 24 hours) and orally (0.25 to 120 hours). A liquid-liquid extraction of MAR was performed by high-performance liquid chromatography (HPLC) with a fluorescent detector. The plasma concentrations obtained at the different sampling times of each season, were analyzed with ANOVA and pharmacokinetic analysis was conducted with the PK Solution 2.0 software. The concentration of marbofloxacin in plasma was significantly lower in winter and summer than in spring, with MAR being detected in winter up to 72 hours post-application, coinciding with the differences in MAR pharmacokinetics parameters with increase in the average residence time (MRT) is 9.4 hours in winter. Increased clearance MAR in summer (7.5 ml/min/kg) coincides with MRT 6.3 hours. Finally, the oral bioavailability of MAR is lower in summer and winter (86 ± 1.7% and 78 ± 3.1%) than in spring (94 ± 5.2 %). There are differences in the disposition and plasma pharmacokinetic behavior of MAR applied orally in broiler chickens, coinciding with the physiological changes in the thermoregulation of birds, considering its correct therapeutic management and contributing to provide safe food for human consumption.

Comment on an analysis of endotherm thermal tolerances: systematic errors in data compilation undermine its credibility.

Understanding the vulnerability of animal populations and communities to rapid climate warming is a critically important endeavour and has recently been informed by a variety of meta-analyses (e.g. [1]). One current area of interest is the synthesis of thermoregulatory data from mammals and birds to examine geographical variation in thermal limits, by comparing thermoregulatory parameters such as thermoneutral zone (TNZ) breadth and variation in the upper and lower critical temperatures that bound the TNZ [2–5]. Here, we report wide-ranging errors in the dataset that is the foundation of Khaliq et al .'s [2] analysis. Khaliq et al . [2] presented a large meta-analysis that extracted data on thermoregulation in birds (161 species) and mammals (297 species) from the physiological literature, with the goal of examining the relationships between physiological capacities and geographical variation in climate. From these individual studies, they compiled data on the lower (LCT) and upper (UCT) critical temperatures, which represent the upper and lower boundaries of the TNZ, the range of environmental temperatures over which resting metabolic rate is constant in endothermic homeotherms. Our discovery that many unsuitable or non-existent data had been included in the dataset compiled by Khaliq et al . [2] was initially triggered by our surprise at the large number of mammal UCT data ( N = 297). At the time, we were conducting a comprehensive review of mammalian thermoregulation in the heat and had found far fewer studies (approx. 100) that contained data permitting the determination of a UCT. We then examined the methods section in the electronic supplementary material, figure S1 and accompanying text, which indicated that Khaliq et al . had indeed used the appropriate definitions of LCT and UCT. Given this disparity, we reviewed the source data from …

The genomic landscape of evolutionary convergence in mammals, birds and reptiles.

Many lineage-defining (nodal) mutations possess high functionality. However, differentiating adaptive nodal mutations from those that are functionally compensated remains challenging. To address this challenge, we identified functional nodal mutations (fNMs) in ~3,400 nuclear DNA (nDNA) and 4 mitochondrial DNA (mtDNA) protein structures from 91 and 1,003 species, respectively, representing the entire mammalian, bird and reptile phylogeny. A screen for candidate compensatory mutations among co-occurring amino acid changes in close structural proximity revealed that such compensated fNMs encompass 37% and 27% of the mtDNA and nDNA datasets, respectively. Analysis of the remaining (non-compensated) mutations, which are enriched for adaptive mutations, showed that birds and mammals share most such recurrent fNMs (N = 51). Among the latter, we discovered mutations in thermoregulation-related genes. These represent the best candidates to explain the molecular basis of convergent body thermoregulation in birds and mammals. Our analysis reveals the landscape of possible mutational compensation and convergence in amniote phylogeny.

Bill size mediates behavioural thermoregulation in birds

Summary Bird bills have been the subject of classic evolutionary studies that demonstrate how morphological adaptations are driven by foraging ecology. As significant areas of heat loss, bills are also under selection with respect to thermoregulation, yet the ecological consequences of this function have been largely ignored until recently. Given the role of bills in thermoregulation is important, we predict that birds should behave to minimise heat loss through their bills at lower ambient temperatures by attempting to insulate their bill in their plumage. Our second prediction is that this thermoregulatory behaviour should be utilised more by species with relatively larger bills, because they will be more prone to heat loss. We demonstrate both these predictions to be correct using field observations and a comparative analysis of nine shorebird species. First, the placement of the bill within the back plumage while roosting (‘back rest’ behaviour), which insulates the bill, becomes more frequent at cooler temperatures. Second, species with large bills relative to their body size do indeed use back rest behaviour more frequently across a range of temperatures. Our findings show that behavioural thermoregulation can be mediated by bill size, and that bill morphology is not only relevant to foraging ecology but also influences behavioural adaptations to climate. A lay summary is available for this article.

Potential involvement of mammalian and avian uncoupling proteins in the thermogenic effect of thyroid hormones

Thyroid hormones (THs) have long been known to be involved in the control of thermoregulation in birds and mammals. In particular, they are reported to play a role in the regulation of heat production. The underlying mechanisms could be the stimulation of the nuclear and mitochondrial transcription of several genes involved in energy metabolism and/or a direct action on the activity of components of the mitochondrial respiratory chain. Attention has recently been focussed on a subfamily of mitochondrial anion carriers called uncoupling proteins (UCPs). These proteins are suspected to be involved in a partial dissipation of the mitochondrial proton electrochemical gradient that would uncouple phosphorylations from oxidations and hence produce heat. However, the involvement of uncoupling mechanisms in thermogenesis and particularly in the thermogenic effect of TH is still unclear. The thermogenic role of UCP1, specifically expressed in brown adipose tissue, and its regulation by TH in rodents is quite well recognised, but the involvement in heat production of its mammalian homologues UCP2, ubiquitously expressed, and UCP3, muscle and adipose tissue-specific, as well as the role of the muscular avian UCP (avUCP), are to be further investigated. The expression of the UCP2 and UCP3 genes was shown to be enhanced by TH in muscle of several rodent species, and to be increased in situations where thermogenesis is stimulated, whereas results are more contrasted in pig. There is now increasing evidence that the physiological role of the mammalian UCP3 and UCP2 is rather related to lipid oxidation and/or prevention of reactive oxygen species accumulation than to heat production by uncoupling. The expression of avUCP was also recently demonstrated to be strongly regulated by thyroid status in chicken, and overexpressed in experimental conditions favouring high triiodothyronine concentrations and thermogenesis. However, its real uncoupling activity and contribution to thermogenesis remain to be established.

Effects of methylene blue and α-lipoic acid on body temperature and fever in pigeons

The effects of oxygen radical scavenger methylene blue and thiol-reductant α-lipoic acid on diurnal core temperature (Tc) changes and on fever were assessed in pigeons (Columba livia) in an ambient temperature of 26±1°C, with lights on at 09:00 and off at 21:00. Intravenous (iv) injection of 10 μg/kg Escherichia coli lipopolysaccharide (LPS) at 13:00 evoked after a latency of 30 min first a variable decrease of Tc, followed by an increase starting 90 min later towards values which were 0.78±0.04°C higher than control between 18:00 and 20:00. Tc decreased in the dark phase parallel to the decline of Tc of afebrile pigeons but with a flatter slope to values which were 0.48±0.10°C higher than control between 05:00 and 06:00. The diurnal fever pattern of Tc was not altered when injections of LPS were applied to the same animals in intervals of 7 days. The iv infusion of 5 mg/kg/h methylene blue lasting from 12:00 to 18:00 did not alter the diurnal rise of Tc during the light phase, but attenuated the decrease of Tc during the dark phase. The initial decrease of Tc was not affected when LPS was injected during infusion of methylene blue; however, methylene blue completely prevented the febrile rise of Tc. Iv injections of 12.5, 25.0 and 37.5 mg/kg α-lipoic acid at 16:00 lowered Tc dose-dependently by 0.75±0.09°C, 1.47±0.14°C, and 1.90±0.18°C, respectively, the hypothermic effects lasting 50, 90 or 140 min, respectively. Treatment with the non-competitive glutamate N-methyl- d-aspartate (NMDA) receptor antagonist dizocilpine maleate (MK801) blocked the α-lipoic acid-induced hypothermia. Injection of 25 mg/kg α-lipoic acid 3 h after LPS caused a decrease of Tc by 1.05±0.20°C, lasting about 60 min. Tc then returned to levels not significantly different from the afebrile state between 18:00 and 20:00. The results suggest that an increased production of reactive oxygen species following LPS mediates the febrile rise of Tc because fever is prevented by the oxygen radical scavenger methylene blue. The hypothermic action of α-lipoic acid is assumed to be induced by reduction of vicinal thiol groups of the NMDA receptor, because the hypothermic effect is blocked by NMDA receptor antagonist MK801. The data support the hypothesis that the NMDA receptor is involved in thermoregulation of birds and that augmented oxidation of vicinal thiol groups attached to its ion channel leads to hyperthermia or causes fever.

Ontogenetic study of thermoregulation in birds

We reviewed our ontogenetic studies of thermoregulatory capacity in avian embryos in relation to metabolic responses to egg cooling.Basic understanding of abrupt egg cooling and quasi-equilibrium state of cooling was discussed together with egg's thermal conductance and heat production.Two cooling tests, which were designed to minimize the rate of heat loss during cooling, were conducted to investigate a feeble compensatory metabolic response to cooling in precocial and altricial embryos, and models for early development of homeothermy in birds were suggested.Instantaneous heart rate (IHR) response to cooling was measured in chick embryos. The baseline of IHR rised and became oscillating. HR oscillation may be a phenomenon related to thermoregulation, which needs to be studied.

The Early Development of Thermoregulation in Birds

There is evidence for incipient thermogenesis in the embryos of precocial species of birds during the later stages of incubation. In ovo, nascent thermoregulation is limited by (1) the high thermal conductance of the egg and embryonic tissues, (2) the rate at which oxygen can diffuse into the egg through the shell and the chorioallantoic membrane ("oxygen-conductance limited"), and (3) the degree of development of the thyroid gland and the metabolic capacity of the embryo ("power limited"). In birds with a semiprecocial mode of development, hatching appears to be a climactic event in the development of the thermoregulation. In contrast, altricial species are at the mercy of the ambient temperature ("Arrhenius limited") even after hatching, and they never experience an oxygen-conductance limitation. Thus, there is a great disparity in the thermoregulatory competence of hatchlings varying from the altricial poikilotherm to the precocial homeotherm. Consequently, the development of thermoregulation in altricial species is an entirely posthatching event, whereas in precocial species there is an embryonic component in the development of thermoregulation and the process is subject to several extraneous limitations, notably the functional pore structure of the eggshell, and the chorioallantoic membrane.

Metabolism and Thermoregulation in Hatchling Ring-Billed Gulls

The extensive efforts to analyze the size dependence of various parameters of thermoregulation in birds (King and Farner 1961, Lasiewski and Dawson 1967, Lasiewski et al. 1967, Herreid and Kessel 1967, Crawford and Lasiewski 1968, Aschoff and Pohl 1970) have been useful in defining certain physiological characteristics of these animals. However, the analyses have tended to obscure the fact that variation beyond that associated with general allometric relations can occur in these parameters within particular taxa. For example, House Sparrows (Passer domesticus) show geographic variation in heat resistance, thermal conductance, and metabolic responses to cold (Hudson and Kimzey 1966, Blem 1973, 1974, Kendeigh and Blem 1974). Horned Larks (Eremophila alpestris) in deserts surpass their counterparts from more mesic situations in thermoregulation in hot environments (Trost 1972). Basal metabolic rate of certain pigeons is inversely correlated with the degree of aridity of their respective environments (Dawson and Bennett 1973). Variation in thermoregulatory parameters is also evident among young of closely related species, judging by the results of Koskimies and Lahti (1964). These authors demonstrated that hatchling ducks of species breeding exclusively at arctic and subarctic latitudes tended to have better control of body temperature at cool ambient temperatures than those of species with wider and more southerly distributions. We feel that variation of this type within taxa may well reflect functionally significant adjustments. To evaluate the physiological role of these adjustments more precisely, we have studied the metabolism and thermoregulatory capacities of hatchling gulls in the genus Larus. This group is a particularly useful one for considerations of physiological variation, for it is represented by more than 30 species over a latitudinal span extending from the arctic to the sub-antarctic. Our initial study in this series (Dawson et al. 1972) concerned the Laughing Gull (Larus atricilla). We now report results obtained on the Ring-billed Gull (Larus delawarensis). This species nests predominantly on lakes at midlatitude in northern United States and southern Canada. It also breeds in maritime situations in Quebec and Newfoundland (A.O.U. Check-list 1957).

COMPARATIVE ASPECTS OF THE RESPIRATORY GAS EXCHANGE OF SEA URCHINS.

AbstractThe proportion of the total heat production of herons and gulls which at ambient temperatures ranging from—10° C to 35° C is dissipated to cold water or air surrounding their legs has been measured. At low ambient temperatures less than 10 % of the metabolic heat is lost from the legs. At higher ambient temperatures an increasing proportion of the metabolic heat is lost from the legs and at 35° C almost the entire heat production is dissipated through the legs. Heat loss to water was found to be about four times higher than to air of the same temperature. The degree of heat loss from the legs was shown to react within seconds to changes in ambient temperature. Likewise, panting stopped immediately when the legs were irregated by cold water. It is concluded that the naked legs of these birds serve as controlled heat conduits of great importance in thermoregulation.