Yehuda Arieli

Heat balance of acclimated pigeons (Columba livia) exposed to temperatures up to 60°c ta

Abstract 1. 1. Hand-reared acclimated (Acc) and nonacclimated (NAcc) rock pigeons Columba livia were exposed to ambient temperatures (Ta) of 30–65°C and low relative humidities (RH) of 5–35%. 2. 2. Resting heat production of 3.6 ± 0.7 cal g −1 hr−1 (31.7 W/m2) and 4.9 ± 0.8 cal g −1 hr −1 (43.0 W/m2) were measured in Ace and NAcc pigeons, respectively. 3. 3. The total evaporative water loss (EWL) was significantly lower (P 4. 4. At 60°C Ta, acclimated pigeons dissipated 304% of heat production as latent heat. In Acc birds body temperature was regulated between 41.2 and 42.0°C within the thermoneutral zone (TNZ) (30–60°C). 5. 5. In NAcc pigeons the TNZ extends only between 30 and 42°C Ta. When Ta was increased from 35–45°C hyperthermia developed at 0.11°C/1°C increase in Ta. 6. 6. The heat acclimated pigeon effectively uses cutaneous evaporation instead of panting and gular fluttering for dissipation of both metabolic heat and ambient heat influx. 7. 7. The significance of the skin and the feather coat in the adaptation of birds to life in the hot deserts is discussed.

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.

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. J. Morphol. 246:118–130, 2000

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.

Heat stress induces ultrastructural changes in cutaneous capillary wall of heat-acclimated rock pigeon

In heat-acclimated rock pigeons, cutaneous water evaporation is the major cooling mechanism when exposed at rest to an extremely hot environment of 50-60 degrees C. This evaporative pathway is also activated in room temperature by a beta-adrenergic antagonist (propranolol) or an alpha-adrenergic agonist (clonidine) and inhibited by a beta-adrenergic agonist (isoproterenol). In contrast, neither heat exposure nor drug administration activates cutaneous evaporation in cold-acclimated pigeons. To elucidate the mechanisms underlying this phenomenon, we studied the role of the ultrastructure and permeability of the cutaneous vasculature. During both heat stress and the administration of propranolol and clonidine, we observed increased capillary fenestration and endothelial gaps. Similarly, propranolol increased the extravasation of Evans blue-labeled albumin in the skin tissue. We concluded that heat acclimation reinforces a mechanism by which the activation of adrenergic signal transduction pathways alters microvessel permeability during heat stress. Consequently the flux of plasma proteins and water into the interstitial space is accelerated, providing an interstitial source of water for sustained cutaneous evaporative cooling.In heat-acclimated rock pigeons, cutaneous water evaporation is the major cooling mechanism when exposed at rest to an extremely hot environment of 50-60°C. This evaporative pathway is also activated in room temperature by a β-adrenergic antagonist (propranolol) or an α-adrenergic agonist (clonidine) and inhibited by a β-adrenergic agonist (isoproterenol). In contrast, neither heat exposure nor drug administration activates cutaneous evaporation in cold-acclimated pigeons. To elucidate the mechanisms underlying this phenomenon, we studied the role of the ultrastructure and permeability of the cutaneous vasculature. During both heat stress and the administration of propranolol and clonidine, we observed increased capillary fenestration and endothelial gaps. Similarly, propranolol increased the extravasation of Evans blue-labeled albumin in the skin tissue. We concluded that heat acclimation reinforces a mechanism by which the activation of adrenergic signal transduction pathways alters microvessel permeability during heat stress. Consequently the flux of plasma proteins and water into the interstitial space is accelerated, providing an interstitial source of water for sustained cutaneous evaporative cooling.

Reproduction of rock pigeon exposed to extreme ambient temperatures

1. The breeding biology of rock pigeon (Columba livia) exposed to ambient temperatures (Ta) between 50 and 60 degrees C was investigated. 2. Four families accomplished three complete life cycles after long term daily exposure to extreme Ta, with about 100% success. 3. The steady state temperatures in the nest were 60, 58, 53 and 44.6 degrees C in the air, substrate surface, underwing, and in the eggs microenvironment, respectively. 4. At thermal conditions between 30 and 60 degrees C, egg temperature (Tegg) was regulated between 36.8 +/- 0.8 (S.D.) and 41.7 +/- 0.4 (S.D.). Tegg increases by 0.163 degrees C/1 degree C rise in Ta. 5. Mean Tb of the nonincubating parent exposed to 30-60 degrees C is 41.6 +/- 0.6 degrees C (S.D.). Under the same conditions the incubating parent regulated a significantly (P less than 0.01) lower Tb (38.8 degrees C) at 45 degrees C Ta and about 1 degree C lower Tb at 30 and 60 degrees C Ta, respectively. 6. By comparing the differences between fast (5 min) cooling of hot egg (44.8 degrees C) to slow heating (60-90 min), we could demonstrate the high sensitivity of the incubating parent to the danger of embryo overheating. 7. The significance of the adaptive behavioral and physiological mechanisms in breeding under extreme thermal conditions are discussed.

Cooling by cutaneous water evaporation in the heat-acclimated rock pigeon (Columba livia)

The present study provides an up-to-date overview of the cutaneous water-evaporation cooling mechanism in the rock pigeon. Cutaneous water evaporation fully replaces the classic respiratory cooling mechanism in the resting, heat-acclimated bird, and is more economical in terms of water conservation. It enables the pigeon to maintain homeostasis, and to breed successfully in harsh environments. Adrenergic signaling is involved in the initiation of this novel mechanism, either by deactivation of the beta-adrenergic receptors (ARs), or activation of the alpha-AR. The adrenergic signaling results in a marked increase in cutaneous blood flow and in the arterial-to-venous blood-flow ratio. This is associated with alterations in the cutaneous capillary wall ultrastructure, which increase its permeability to plasma proteins and water. The end result of this process might be an increase in water efflux from the capillary lumen. The properties of beta-ARs were measured in the cardiac muscle of thermal-acclimated pigeons. Significant down-regulation in the density of beta-ARs, associated with increased affinity of these receptors, was measured in the heat-acclimated pigeon. Concomitantly, changes in the skin ultrastructure and lipid composition were found in very well defined patches in the epidermis of heat-acclimated pigeons. These suppress the skin resistance to water transfer. We suggest that this cooling mechanism involves finely orchestrated adjustments in the ultrastructure of the skin and the cutaneous capillaries, and in skin blood flow. Adrenergic signals are among those factors that regulate this cooling mechanism during exposure to a hot environment.

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...

CNS thermosensitivity and control of latent heat dissipation in the pigeon

Abstract Thermoregulatory responses to heat exposure were studied in 12 hand-reared, acclimated pigeons (Columbia livia). Measurements of body temperature (Tcl), brain temperature (Tbr), cutaneous water evaporation (CWE) and respiratory frequency (fr) were carried out in intact conscious heat exposed birds. In a second group of lightly restrained birds, fr and CWE were taken when temperatures of the trunk, brain and air (Ta) were independently changed. Increasing Tbr to 43.5–43.8°C induced a pronounced polypnea (deep and fast, (300 breaths min −1 ) when Tcl regulated at 42.4°C. Moreover, when hyperthermia (Tcl = 43.0° C ) was combined with increased Tbr (43.0–43.8°C) shallow and fast panting (>500 breaths min −1 ) was evoked. CWE was probably elicited by inputs generated by the skin warm receptors as a result of increased Ta. Moreover it was demonstrated that warming the brain to 42.5°C elicits cutaneous water evaporation in birds exposed to 26°C. When a high Ta (60°C) is accompanied by a high relative humidity (17%), the combined effect generates inputs eliciting intensive panting. The integration of the present and earlier data allows us to generate a model demonstrating the distinguished significance of the trunk, skin and brain thermosensors in the regulation of both respiratory and cutaneous latent heat dissipation. The present model also emphasizes the fact that the highly thermosensitive pigeon brain responds in a similar pattern to that found in mammals

CHRONIC EXPOSURE TO DIFFERENT AMBIENT TEMPERATURES AFFECTS b-AR PROFILE AND HEART RESPONSIVENESS TO ISOPROTERENOL AND CALCIUM

The purpose of this investigation was to study the effect of thermal acclimation on the myocardium of rock pigeons. We determined the density and affinity of the b -adrenergic receptors in the left ventricle of cold-, heat-, and normothermic-acclimated pigeons by radioligand binding techniques. The mechanical performance of the left ventricle of the heart subjected to either isoproterenol or Ca2+ loading was measured using the Langendorff perfusion system. Heat- and cold-acclimated hearts demonstrated a significant downregulation of b - and b2 -adrenoreceptor density accompanied by an increase in their affinity when compared with normothermic-acclimated hearts. In agreement with these results, isoproterenol improved cardiac performance in cold- and heat-acclimated hearts. We also found that the heat-acclimated hearts were capable of functioning successfully when exposed to high Ca2+ loads, whereas cold-acclimated hearts were significantly less tolerant of Ca2+ loads and less efficient. Thermal acclimation...