William A. Buttemer

Interactions of corticosterone with feeding, activity and metabolism in passerine birds

Corticosterone (B) may play a direct role in the promotion of feeding behavior under conditions of nutritional stress. However, effects of exogenous B and nutritional stress in passerines indicate a complex relationship of fed state, perceived or anticipated nutritional stress, and previous history. In a series of investigations on caged White-crowned Zonotrichia leucophrys and Song Sparrows Z. melodia, foraging behaviors and feeding rates were unaffected by exogenous B in fed birds. When food was returned, birds implanted with B refed for longer and with greater intensity following the 24 hour fast. Additionally, B-implanted birds showed lower activity (perch hopping) than controls when fed ad libitum, but when fasted this trend reversed with B-implanted birds showing increased activity and apparent escape behavior. In a second study, small flocks of Pine Siskins Carduelis pinus and Darkeyed Juncos Junco hyemalis held in aviaries and fasted for 24 hours had higher plasma levels of B than similar flocks that had been allowed to refeed for 1 hour after fasting. However, the highest levels of B in fasted birds were still lower than in free-living conspecifics exposed to capture stress. This low amplitude modulation of plasma B levels in relation to fed state was corroborated by results from free-living Pine Siskins and Lapland Longspurs Calcarius lapponicus captured during snow storms. In spite of unusually high feeding intensities during the storm, individuals of only some Pine Siskins and no Lapland Longspurs had elevated circulating levels of B. In the latter species, serial samples revealed very high levels of B within 15 minutes of capture suggesting enhanced adrenal secretory activity as a result of the storm. Finally, in White-crowned Sparrows, exogenous B substantially reduced overnight metabolic expenditure by reducing the frequency and amplitude of arousal bouts during the night. This suggested a possible energy savings effect of B during the hours when foraging was impossible and, possibly, insurance that the individual will retain sufficient resources to seek food the following day. Taken together, our data suggest that B may be important for initiation of food-searching during periods of food deprivation. Only small increases in B secretion appear to be required thus facilitating a rapid return to homeostasis after food is located. Although under prolonged nutritional stress the basal levels of B remained low, adrenal potential to secrete B in response to further stress increased dramatically.

Dietary n-3 and n-6 fatty acids alter avian metabolism: metabolism and abdominal fat deposition

The effects of dietary saturated fatty acids and polyunsaturated fatty acids (PUFA) of the n-3 and n-6 series on weight gain, body composition and substrate oxidation were investigated in broiler chickens. At 3 weeks of age three groups of chickens (n 30; ten birds per group) were fed the fat-enriched experimental diets for 5 weeks. These diets were isonitrogenous, isoenergetic and contained 208 g protein/kg and 80 g edible tallow, fish oil or sunflower oil/kg; the dietary fatty acid profiles were thus dominated by saturated fatty acids, n-3 PUFA or n-6 PUFA respectively. Resting RQ was measured in five birds from each treatment group during weeks 4 and 5 of the experiment. There were no significant differences between treatments in total feed intake or final body mass. Birds fed the PUFA diets had lower RQ and significantly reduced abdominal fat pad weights (P<0.01) compared with those fed tallow. The dietary lipid profile changes resulted in significantly greater partitioning of energy into lean tissue than into fat tissue (calculated as breast lean tissue weight:abdominal fat mass) in the PUFA groups compared with the saturated fat group (P<0.01; with no difference between the n-3 and n-6 PUFA groups). In addition, the PUFA-rich diets lowered plasma concentrations of serum triacylglycerols and cholesterol. The findings indicate that dietary fatty acid profile influences nutrient partitioning in broiler chickens.

Frequency-dependent physiological trade-offs between competing colour morphs

Evolutionary theory suggests that alternative colour morphs (i.e. genetically controlled phenotypes) may derive similar fitness under frequency-dependent selection. Here we experimentally demonstrate opposing effects of frequency-dependent social environments on plasma hormone levels (testosterone and corticosterone) and immune function between red- and black-headed male morphs of the Gouldian finch (Erythrura gouldiae). Red-headed males are highly sensitive to changes in the social environment, especially towards the relative density of their own aggressive morph, exhibiting high stress responses and immunosuppression in socially competitive environments. In contrast, the non-aggressive black-headed males follow a more passive strategy that appears to buffer them against social stresses. The differential effect of hormones on aggressive behaviour and immune performance reinforces the contrasting behavioural strategies employed by these colour morphs, and highlights the importance of the social environment in determining the individual basis of behavioural and physiological responses.

Corticosterone treatment has no effect on reproductive hormones or aggressive behavior in free-living male tree sparrows, Spizella arborea

We examined the effect of corticosterone on plasma levels of reproductive hormones (testosterone, dihydrotestosterone, and luteinizing hormone) and territorial defense behavior in male tree sparrows, Spizella arborea. Birds receiving Silastic implants filled with corticosterone (B) had significantly higher plasma levels of B than control birds, which received empty implants, and exhibited pectoral muscle wastage and a decrease in body mass. We evaluated the hormonal and agonistic responses of the two implanted groups of birds using a simulated territorial intrusion (STI) 2 to 4 days after they were implanted. Corticosterone-treated and control birds did not differ in their circulating levels of reproductive hormones or in their behavioral responses to STI (latency to respond to intrusion, number of songs, and closest approach to a decoy and tape recording). Unlike previous studies of north temperate passerines, high physiological levels of exogenous B had no effect either on circulating levels of reproductive hormones or on territorial behaviors associated with breeding. Nonetheless, untreated tree sparrows do mount a robust adrenocortical response, having a two- to fourfold increase in plasma B levels during a 1-h period of capture. Thus, adrenocortical responsiveness is maintained in these birds, but elevated levels of glucocorticoids do not suppress reproductive hormones or associated behaviors. We believe that this hormonal and behavioral refractoriness to glucocorticoids-or uncoupling of the stress response from the reproductive axis-may be advantageous for species having extreme temporal constraints on their breeding schedules.

Ecophysiology of avian migration in the face of current global hazards

Long-distance migratory birds are often considered extreme athletes, possessing a range of traits that approach the physiological limits of vertebrate design. In addition, their movements must be carefully timed to ensure that they obtain resources of sufficient quantity and quality to satisfy their high-energy needs. Migratory birds may therefore be particularly vulnerable to global change processes that are projected to alter the quality and quantity of resource availability. Because long-distance flight requires high and sustained aerobic capacity, even minor decreases in vitality can have large negative consequences for migrants. In the light of this, we assess how current global change processes may affect the ability of birds to meet the physiological demands of migration, and suggest areas where avian physiologists may help to identify potential hazards. Predicting the consequences of global change scenarios on migrant species requires (i) reconciliation of empirical and theoretical studies of avian flight physiology; (ii) an understanding of the effects of food quality, toxicants and disease on migrant performance; and (iii) mechanistic models that integrate abiotic and biotic factors to predict migratory behaviour. Critically, a multi-dimensional concept of vitality would greatly facilitate evaluation of the impact of various global change processes on the population dynamics of migratory birds.

The long life of birds: the rat-pigeon comparison revisited.

The most studied comparison of aging and maximum lifespan potential (MLSP) among endotherms involves the 7-fold longevity difference between rats (MLSP 5y) and pigeons (MLSP 35y). A widely accepted theory explaining MLSP differences between species is the oxidative stress theory, which purports that reactive oxygen species (ROS) produced during mitochondrial respiration damage bio-molecules and eventually lead to the breakdown of regulatory systems and consequent death. Previous rat-pigeon studies compared only aspects of the oxidative stress theory and most concluded that the lower mitochondrial superoxide production of pigeons compared to rats was responsible for their much greater longevity. This conclusion is based mainly on data from one tissue (the heart) using one mitochondrial substrate (succinate). Studies on heart mitochondria using pyruvate as a mitochondrial substrate gave contradictory results. We believe the conclusion that birds produce less mitochondrial superoxide than mammals is unwarranted. We have revisited the rat-pigeon comparison in the most comprehensive manner to date. We have measured superoxide production (by heart, skeletal muscle and liver mitochondria), five different antioxidants in plasma, three tissues and mitochondria, membrane fatty acid composition (in seven tissues and three mitochondria), and biomarkers of oxidative damage. The only substantial and consistent difference that we have observed between rats and pigeons is their membrane fatty acid composition, with rats having membranes that are more susceptible to damage. This suggests that, although there was no difference in superoxide production, there is likely a much greater production of lipid-based ROS in the rat. We conclude that the differences in superoxide production reported previously were due to the arbitrary selection of heart muscle to source mitochondria and the provision of succinate. Had mitochondria been harvested from other tissues or other relevant mitochondrial metabolic substrates been used, then very different conclusions regarding differences in oxidative stress would have been reached.

The influence of testosterone on territorial defence and parental behavior in male free-living rufous whistlers, Pachycephala rufiventris.

We studied a population of rufous whistlers, Pachycephala rufiventris, throughout a single breeding season in central New South Wales, Australia. We evaluated the relation between plasma testosterone (T) and reproductive behaviors using both simulated territorial intrusions (STIs) and subcutaneous T implants. We compared circulating T values to aggression levels of males (using STI) during pair bond and territory establishment and again during incubation. Although plasma T levels were significantly lower in the latter period, male responsiveness to STI, in terms of proximity to decoy, call rate, and number of attacks on the decoy, was indistinguishable between the two breeding stages. T levels of males exposed to STI were not different from the levels of unexposed free-living males at the same breeding stage. The effect of exogenous T on parental behavior was examined by comparing duration of incubation bouts of males and their mates prior to and after T treatment. T males significantly reduced the amount of time they incubated following implantation, whereas Control males maintained their incubation effort. After cessation of breeding activities, T males displayed significantly higher call rates due to increased use of the primary intersexual advertisement call in this species. The reduction of incubation behavior following T implantation emphasises the functional significance of the rapid decline in T in free-living males during incubation. The results from both experiments suggest that intersexual advertisement, rather than territorial aggression, may be dependent on high T levels in this species.

Effect of Temperature on Evaporative Water Loss of the Australian Tree Frogs Litoria caerulea and Litoria chloris

The rate of evaporative water loss (EWL) of the Australian tree frogs Litoria caerulea and Litoria chloris was evaluated over the temperature intervals 25°–50° C and 25°–47° C, respectively. At 25° C, EWL of L. caerulea averaged 7.5 mg g⁻¹ h⁻¹ and that of L. chloris averaged 4.2 mg g⁻¹ h⁻¹. These values are much lower than those measured for similar-sized North American arboreal frogs. Consonant with these results, the cutaneous resistances to water vapor flux (ri) of these Australian frogs were much higher than those usually associated with amphibians, averaging 9 and 39 s cm⁻¹ for L. caerulea and L. chloris, respectively. At air temperatures above 40° C, the ri of L. chloris declined directly with temperature rise and averaged 2.5 s cm⁻¹ at 47° C. Body temperatures of L. chloris maintaining their water-conserving posture were stable and averaged 3 7.9° C at air temperatures from 43° through 47° C Such properties indicate a high degree of physiological thermoregulation by the canopy-dwelling L. chloris.

Fowl play and the price of petrel: long-living Procellariiformes have peroxidation-resistant membrane composition compared with short-living Galliformes

The membrane pacemaker hypothesis predicts that long-living species will have more peroxidation-resistant membrane lipids than shorter living species. We tested this hypothesis by comparing the fatty acid composition of heart phospholipids from long-living Procellariiformes (petrels and albatrosses) to those of shorter living Galliformes (fowl). The seabirds were obtained from by-catch of commercial fishing operations and the fowl values from published data. The 3.8-fold greater predicted longevity of the seabirds was associated with elevated content of peroxidation-resistant monounsaturates and reduced content of peroxidation-prone polyunsaturates and, consequently, a significantly reduced peroxidation index in heart membrane lipids, compared with fowl. Peroxidation-resistant membrane composition may be an important physiological trait for longevous species.

Effects of sublethal fenitrothion ingestion on cholinesterase inhibition, standard metabolism, thermal preference, and prey-capture ability in the Australian central bearded dragon (Pogona vitticeps, agamidae)

The central bearded dragon (Pogona vitticeps) is a medium-sized lizard that is common in semiarid habitats in Australia and that potentially is at risk of fenitrothion exposure from use of the chemical in plague locust control. We examined the effects of single sublethal doses of this organophosphate (OP; low dose = 2.0 mg/kg; high dose = 20 mg/kg; control = vehicle alone) on lizard thermal preference, standard metabolic rate, and prey-capture ability. We also measured activities of plasma total cholinesterase (ChE) and acetylcholinesterase before and at 0, 2, 8, 24, 120, and 504 h after OP dosing. Predose plasma total ChE activity differed significantly between sexes and averaged 0.66 +/- 0.06 and 0.45 +/- 0.06 micromol/min/ml for males and females, respectively. Approximately 75% of total ChE activity was attributable to butyrylcholinesterase. Peak ChE inhibition reached 19% 2 h after OP ingestion in the low-dose group, and 68% 8 h after ingestion in high-dose animals. Neither OP doses significantly affected diurnal body temperature, standard metabolic rate, or feeding rate. Plasma total ChE levels remained substantially depressed up to 21 d after dosing in the high-dose group, making this species a useful long-term biomonitor of OP exposure in its habitat.