Heat-acclimated Pigeons Research Articles

DEFENSE STRATEGIES AGAINST ENVIRONMENTAL HEAT STRESS IN BIRDS

ABSTRACT When heat-acclimated pigeons are exposed to ambient temperatures of 50–60°C, extremely high cutaneous evaporative cooling, together with a high insulative capacity of the feather coat, creates for the bird a microclimate within which physiological processes can be regulated normally. By skillfully using this cooling garment, pigeons maintain their resting metabolic rate and regulate low skin and body temperatures, employing neither panting nor gular fluttering. These physiological achievements parallel those of arctic animals. Hence, during animal evolution towards inhabiting extreme thermal environments, selection seems to have favored adaptations at the lowest energy cost in both the extreme cold arctic and the hottest deserts of the world.

The effect of α 2-adrenergic receptors on cutaneous water evaporation in the rock pigeon ( Columba livia)

The role of β-adrenergic receptors in regulating cutaneous water evaporation (CWE) in the rock pigeon ( Columba livia) is well documented. Here, we studied the involvement of the α 2-adrenergic receptors in this cooling mechanism of the heat-acclimated (HAc) pigeon. Systemic α 2-adrenergic activation [clonidine, 50 μg kg −1, intramuscular (i.m.)] was found to increase CWE in heat-acclimated pigeons at an ambient temperature ( T a) of 25 °C. Subcutaneous administration of the drug had no significant effect. Preinjection of an α 2-adrenergic antagonist (yohimbine, 10 mg kg −1, i.m.) completely prevented clonidine-induced CWE and attenuated propranolol-induced CWE by 53%. Pretreatment with a β-adrenergic agonist (isoproterenol, 4 mg kg −1, i.m.) abolished the effect of clonidine. None of the above treatments was found to elicit significant CWE in nonacclimated (NAc) pigeons. These findings, in addition to previously reported data, indicate a complex regulatory pathway of CWE in the heat-acclimated pigeon consisting of α 2- and β 2-adrenergic receptors. The possible hierarchical pattern of these receptors is discussed.

CUTANEOUS WATER EVAPORATION IN THE HEAT-ACCLIMATED ROCK PIGEON (COLUMBA LIVIA)--PHYSIOLOGICAL AND BIOCHEMICAL ASPECTS

The most conspicuous phenomenon in the process of heat acclimation of the rock pigeon (Columba livia) is the remarkable increase in its capacity to evaporate water from its skin. This cooling route becomes the chief thermoregulatory means in the heat-acclimated (HAc) pigeon and is responsible for its ability to maintain normal body temperatures even at extremely high ambient temperatures of 60 oC. Since the avian skin lacks sweat glands or any other homologous functional structure, cutaneous water evaporation (CWE) must occur along a different pathway than that known in mammals. The aim of this review is to characterize the CWE mechanism in the rock pigeon from three aspects: the regulatory pathway, the driving force, and the water passageway to the skin surface. CWE is controlled by the adrenergic system at various levels, both peripherally and at higher levels. It was found that nonspecific b-adrenergic inhibition (by propranolol) increases CWE in the HAc pigeon, but not in the non-acclimated (NAc) pige...

PLASTICITY IN AVIAN RESPONSES TO THERMAL CHALLENGES-- AN ESSAY IN HONOR OF JACOB MARDER

Birds show remarkable plasticity in their thermoregulatory responses, often enhancing heat or cold resistance seasonally or in response to experimentally applied thermal challenges. In regions with severe winters these animals commonly undergo substantial winter fattening, elevate their general metabolic level, and increase thermogenic capacity and endurance. Indications also exist that some species, at least, also increase their capacity for mobilizing energy substrates during cold challenges. Some of these responses also are induced by cold conditioning in the laboratory. The onset of warmer seasons or exposure to higher laboratory temperatures can lead to downregulation of general metabolic level, thereby reducing the thermal load with which birds must contend during the heat of summer days. However, the most spectacular phenotypic adjustment to heat thus far documented is that evident in the heat-acclimated rock pigeon (Columba livia), which achieves a remarkable resistance to high ambient temperature...

ACCUMULATION OF CALCIUM IN THE STRATUM CORNEUM OF THE ROCK PIGEON (COLUMBA LIVIA): STORAGE OR SECRETION?

In the pigeon (Columba livia), a different response of cutaneous water evaporation (CWE) is seen at different acclimation states. While in heat-acclimated pigeons the CWE at high ambient temperatures will be activated as expected, no such response to appropriate thermal stimuli is seen in cold-acclimated birds. This difference is also reflected in the function of the water barrier, which in the stratum corneum modulates the diffusion of water through the skin. In this respect, the skin of birds seems to be more dynamic than that of mammals. In mammals, the formation of this barrier by extracellular lipid lamellae derived from lamellar bodies of viable keratinocytes is a prerequisite for normal skin function. It is present in cold-acclimated pigeons, but is lacking in heat-acclimated birds. The ionic stimulus of extracellular calcium (Ca2+) has been claimed to mediate the formation of the mammalian-type barrier. In order to elucidate the role of Ca2+ in water barrier formation in avians, we studied winter-...

The role of β-adrenergic receptors in the cutaneous water evaporation mechanism in the heat-acclimated pigeon ( Columba livia)

The effects of selective and non-selective β-adrenergic agents on cutaneous water evaporation (CWE) were studied in hand-reared rock pigeons ( Columba livia). CWE was measured by the vapor diffusive resistance method, using a transient porometer. Intramuscular and subcutaneous injections of a non-selective β-adrenergic antagonist (propranolol) or a selective β 2-adrenergic antagonist (ICI-118 551) to heat-acclimated (HAc) pigeons at ambient temperature ( T a) of 24°C resulted in intensive CWE. The CWE values that were triggered by propranolol and ICI-118 551 (18.59±0.73 and 16.48±0.70 mg cm −2 h −1, respectively) were close to those induced by heat exposure (17.62±1.40 mg cm −2 h −1). Subcutaneous administration of propranolol produced local response. Intramuscular injection of salbutamol (selective β 2-adrenergic agonist) to HAc pigeons drastically diminished CWE induced by either propranolol, metoprolol or heat exposure. Such manipulations also enhanced panting at relatively low T as (42°C). The inhibition of β 1-adrenergic receptors by metoprolol increased CWE, while inhibition by atenolol produced no change from basal values. This difference may be attributed to their distinctive nature in penetrating the blood-brain barrier. Our findings indicate a regulatory pathway for CWE consisting of both β 1- and β 2-adrenergic receptors. We suggest that the β 1-adrenergic effect is restricted mainly to the CNS, while the β 2-adrenergic effect takes place at the effector level. We postulate this level to be either the cutaneous microvasculature or the epidermal layer.

Local cutaneous water barrier in cold- and heat-acclimated pigeons (Columba livia) in relation to cutaneous water evaporation.

The thermoregulatory function of the skin differs in adult cold-acclimated and heat-acclimated rock pigeons (Columba livia). In general, the cutaneous evaporative cooling mechanism is not activated by appropriate stimuli in cold-acclimated pigeons in contrast to heat-acclimated pigeons. We studied with electron microscopy whether the differences in the function of the skin are reflected in the structure of the epidermal water barrier of these two extreme acclimation states. The epidermis of cold-acclimated pigeons is attenuated, and the underlying dermis lacks any intimate vascularization. Both the extracellular and the intracellular domains in the stratum corneum contain organized lamellar lipids. At the stratum transitivum-stratum corneum interface, multigranular body secretion is indicated by the highly convoluted cell membranes and membraneous sacculae enclosing the multigranular bodies. Alternatively, multigranular bodies retain in the corneocytes, and the lipoid material originated from them is reprocessed to broad lamellae. The keratohyalin (KH) granules are spotlike and oriented as cortical bands beneath the plasma membrane. In heat-acclimated pigeons, the epidermis displays modified patches side by side with basic structural type of epidermis. The modified areas are characterized by hypertrophy and abundance of dermal capillaries adjacent to the hypertrophied patch. No lamellar lipids are discerned in the dilated extracellular space. The structure of multigranular bodies is abnormal, and the numbers of lipid droplets in the outer viable epidermis and stratum corneum are decreased. The transitional cells contain stellate KH granules, which form a network throughout the cell. It is concluded that cold-acclimated pigeons have a lamellar, extracellular water barrier, the cutaneous water evaporation is minimized, and heat is stored in the body core. Acclimation to heat leads to formation of structurally heterogeneous skin. The structurally modified skin patches show disruption of the barrier-forming machinery in the multigranular bodies and marked reorganization of fibrillar proteins and electron-dense KH masses in the transitional layer. Thus water barrier adjustments in cold- and heat-acclimated pigeons manifest the dynamic function of avian skin as a thermoregulatory organ.

Adaptive changes in the epidermal structure of the heat-acclimated rock pigeon (Columba livia): A comparative electron microscopy study.

The purpose of this study was to find out whether the microstructure of the highly permeable skin of heat-acclimated pigeons allowing increased evaporative cooling differs from the skin of pigeons in the non-acclimated or cold-acclimated state. In addition, the correlation between epidermal morphology and cutaneous water evaporation in heat-acclimated pigeons was elucidated. The epidermis of heat-acclimated pigeons differs in several respects from the epidermis of non-acclimated or cold-acclimated birds. Both the dorsal and the abdominal skin include modified areas, characterized by increased vascularization, epidermis with greater thickness, and changes in intracellular structures. Greater thickness results from hypertrophy of epidermal cells possibly due to greater fluid content of the sebokeratinocytes in the germinative layers. The stratum corneum includes corneocytes with thickened cornified envelopes and contains greater mass of keratin-complex material compared to non-acclimated and cold-acclimated pigeons. The extracellular space between the compactly piled corneocytes contains amorphous lipoid material. The multigranular bodies lack compact organization of lipid bilayers. The transitional layer in the heat-acclimated pigeon displays atypical keratohyalin granules, which are multilateral and dendritic in shape. It is concluded that the dorsal and abdominal skin of heat-acclimated pigeons contains areas that differ in structure from their counterparts in non-acclimated and cold-acclimated pigeons. The structural characteristics of these modified patches suggest a high rate of cutaneous evaporation and decreased skin resistance to transepidermal diffusion of water vapor. Thus, the skin of a heat-acclimated pigeon responds to the thermoregulatory requirements for increased cutaneous water evaporation by structural changes. J. Morphol. 235:17-29, 1998. © 1998 Wiley-Liss, Inc.

Adaptive changes in the epidermal structure of the heat‐acclimated rock pigeon (Columba livia): A comparative electron microscopy study

The purpose of this study was to find out whether the microstructure of the highly permeable skin of heat-acclimated pigeons allowing increased evaporative cooling differs from the skin of pigeons in the non-acclimated or cold-acclimated state. In addition, the correlation between epidermal morphology and cutaneous water evaporation in heat-acclimated pigeons was elucidated. The epidermis of heat-acclimated pigeons differs in several respects from the epidermis of non-acclimated or cold-acclimated birds. Both the dorsal and the abdominal skin include modified areas, characterized by increased vascularization, epidermis with greater thickness, and changes in intracellular structures. Greater thickness results from hypertrophy of epidermal cells possibly due to greater fluid content of the sebokeratinocytes in the germinative layers. The stratum corneum includes corneocytes with thickened cornified envelopes and contains greater mass of keratin-complex material compared to non-acclimated and cold-acclimated pigeons. The extracellular space between the compactly piled corneocytes contains amorphous lipoid material. The multigranular bodies lack compact organization of lipid bilayers. The transitional layer in the heat-acclimated pigeon displays atypical keratohyalin granules, which are multilateral and dendritic in shape. It is concluded that the dorsal and abdominal skin of heat-acclimated pigeons contains areas that differ in structure from their counterparts in non-acclimated and cold-acclimated pigeons. The structural characteristics of these modified patches suggest a high rate of cutaneous evaporation and decreased skin resistance to transepidermal diffusion of water vapor. Thus, the skin of a heat-acclimated pigeon responds to the thermoregulatory requirements for increased cutaneous water evaporation by structural changes. J. Morphol. 235:17–29, 1998. © 1998 Wiley-Liss, Inc.

Osmoregulation and body fluid compartmentalization in dehydrated heat-exposed pigeons.

Osmoregulatory and volume-regulatory responses of heat-acclimated pigeons (Columba livia) were studied during normal hydration and dehydration combined with heat exposure. Dehydrated heat-exposed pigeons (exposure to 50 degrees C following 48 h of water deprivation; 16-18% mass loss) could recover 97% of their initial body mass within 30 min of free drinking at the end of heat exposure. At the end of heat exposure, body temperature increased by 3 degrees C and hematocrit increased by 12.5%. Serum electrolyte and protein concentrations increased by 33-53% (P less than 0.001). Serum osmolality reached an outstanding mean value of 436.7 +/- 28.5 mosmol/kg (n = 11), 30.5% higher than the normal mean value. Serum glutamic-pyruvic transaminase and glutamic-oxaloacetic transaminase concentrations did not change during dehydration, suggesting no impairment in circulatory function. Blood urea nitrogen increased sixfold, indicating a total shutdown of the kidney. Relative plasma volume was maintained during dehydration at the expense of extravascular spaces and with a decreased vascular permeability as indicated by the increase in Evans blue-labeled albumin half-life (control, 104 +/- 53 min; dehydration, approaching infinity). Altogether, extracellular fluid volume and intracellular fluid volume contributed 53 and 47% of the evaporative water loss, respectively. It is concluded that plasma volume regulation may play an important role in the effective thermoregulatory responses of heat-exposed dehydrated pigeons. This regulation is achieved by preferential shifts of body water reserves among the various body water compartments coinciding with a remarkable tolerance to high osmotic pressures.

Adaptation of the Pigeon Egg to Incubation in Dry Hot Environments

Eggshell water vapor conductance (GH₂O), shell thickness (T), and effective pore area (Ap) of eggs from pigeons (Columba livia) nesting under extreme conditions (high ambient temperatures and low humidity) were compared with those of urban pigeons and pure rock doves breeding in mesic conditions. Heat-acclimated pigeons had eggshells characterized by ∼30%-40% lower than predicted GH₂O. A significantly reduced Ap and higher than predicted shell thickness accounted for the observed reduction in GH₂O. We conclude that these pigeons were physiologically adapted to successfully breed under extreme conditions prevailing in their original colony.

Effect of acute temperature stress on the plasma catecholamine, corticosterone and metabolite levels in the pigeon

1. Adult pigeons of both sexes were exposed to either +2°C or +32°C for 5, 15, 30 or 60 min. Furthermore, 2 groups of pigeons were housed at these temperatures for 3 weeks. 2. Acute cold or heat stress produced biphasic changes in the blood NA, A and corticosterone concentrations. Both at cold and heat an immediate rise in A level was seen, but corticosterone level increased only at cold, which was followed by a fall at 30 min. Thereafter the corticosterone levels were recovered and at 60 min even exceeded the initial values. In NA level an immediate and controversial fall both at cold and heat was seen. However, at cold, an unexpected and significant elevation above the pre-exposure level was seen at 30 min. 3. In FFA, glycerol and glucose levels an immediate fall at heat but a controversial elevation at cold was observed. 4. Our findings show that there are increased plasma glycerol, FFA, A and NA levels in cold-acclimated pigeon compared with heat-acclimated pigeon.