Chemical composition and tissue energy density of the cuttlefish (Sepia apama) and its assimilation efficiency by Diomedea albatrosses.

The cuttlefish Sepia apama Gray (Mollusca: Cephalopoda) is a seasonally abundant food resource exploited annually by moulting albatrosses throughout winter and early spring in the coastal waters of New South Wales, Australia. To assess its nutritional value as albatross forage, we analysed S. apama for water, lipid protein, ash contents, energy density and amino acid composition. Because albatrosses consistently consume S. apama parts preferentially in the order of head, viscera and mantle, we analysed these sections separately, but did not identify any nutritional basis for this selective feeding behaviour. The gross energy value of S. apama bodies was 20.9 kJ/g dry mass, but their high water content (>83%; cf <70% for fish) results in a relatively low energy density of 3.53 kJ/g. This may contribute to a need to take large meals, which subsequently degrade flight performance. Protein content was typically >75% dry mass, whereas fat content was only about 1%. Albatrosses feed on many species of cephalopods and teleost fish, and we found the amino acid composition of S. apama to be comparable to a range of species within these taxa. We used S. apama exclusively in feeding trials to estimate the energy assimilation efficiency for Diomedea albatrosses. We estimated their nitrogen-corrected apparent energy assimilation efficiency for consuming this prey to be 81.82 ± 0.72% and nitrogen retention as 2.90 ± 0.11 g N kg(-1) d(-1). Although S. apama has a high water content and relatively low energy density, its protein composition is otherwise comparable to other albatross prey species. Consequently, the large size and seasonal abundance of this prey should ensure that albatrosses remain replete and adequately nourished on this forage while undergoing moult.

The effect of food temperature on postprandial metabolism in albatrosses.

Heat generated by the specific dynamic action (SDA) associated with feeding is known to substitute for the thermoregulatory costs of cold-exposed endotherms; however, the effectiveness of this depends on food temperature. When food is cooler than core body temperature, it is warmed by body heat and, consequently, imposes a thermoregulatory challenge to the animal. The degree to which this cost might be ;paid' by SDA depends on the relative timing of food heating and the SDA response. We investigated this phenomenon in two genera of endotherms, Diomedea and Thalassarche albatrosses, by measuring postprandial metabolic rate following ingestion of food at body temperature (40 degrees C) and cooler (0 and 20 degrees C). This permitted us to estimate potential contributions to food warming by SDA-derived heat, and to observe the effect of cold food on metabolic rate. For meal sizes that were approximately 20% of body mass, SDA was 4.22+/-0.37% of assimilated food energy, and potentially contributed 17.9+/-1.0% and 13.2+/-2.2% of the required heating energy of food at 0 degrees C for Diomedea and Thalassarche albatrosses, respectively, and proportionately greater quantities at higher food temperatures. Cold food increased the rate at which postprandial metabolic rate increased to 3.2-4.5 times that associated with food ingested at body temperature. We also found that albatrosses generated heat in excess by more than 50% of the estimated thermostatic heating demand of cold food, a probable consequence of time delays in physiological responses to afferent signals.

Diacetone alcohol, a dispersant solvent, contributes to acute toxicity of a fipronil-based insecticide in a passerine bird.

Fipronil, a phenyl pyrazole pesticide, is aerially applied in eastern Australia to control locust outbreaks, usually as "Adonis 3UL Insecticide" (BASF), an ultra low (UL) volume formulation containing 0.3% active pesticide. We tested the toxicities of technical-grade fipronil, the Adonis 3UL formulation and its components in zebra finch, a native bird at risk of exposure in locust control regions. We estimated oral-dose LD50 by the Up-and-Down method. Under laboratory conditions, we identified unexpectedly high toxicities due exclusively to diacetone alcohol (DAA), a solvent making up 12.5% of the Adonis 3UL formulation. In contrast, finches were asymptomatic when exposed to 0.3% technical grade fipronil dissolved in a minimum amount of acetone. Depending upon the behaviour and persistence of DAA under field conditions, this formulation of Adonis 3UL may pose a far greater threat to the health of small birds and possibly other vertebrates than expected for fipronil alone.

Testosterone effects on avian basal metabolic rate and aerobic performance: facts and artefacts.

We examined the effects of cage size and testosterone (T) levels on basal and peak metabolic rates (BMR and PMR, respectively) and on pectoral and leg muscle masses of male house sparrows (Passer domesticus). Birds were housed either in small birdcages or in flight aviaries for at least 2 weeks prior to the initial metabolic evaluations. They were then implanted with either empty or T-filled silastic capsules and remeasured 5-6 weeks later. Birds treated with single T implants achieved breeding levels (4-6 ng/mL) and one group given double implants reached 10 ng/mL. There was no effect of T on BMR or PMR in any group studied, but there was an effect of caging. Caged birds showed significant reductions in PMR over the course of captivity, whereas PMR in aviary-housed birds were indistinguishable from their free-living counterparts. Testosterone treatment significantly increased leg muscle mass in caged birds, but had no effect on muscle mass in aviary-housed sparrows. We conclude that testosterone has no direct effect on sparrow metabolic rate or muscle mass, but may interact with cage conditions to produce indirect changes to these variables.

Life and death: metabolic rate, membrane composition, and life span of animals.

Maximum life span differences among animal species exceed life span variation achieved by experimental manipulation by orders of magnitude. The differences in the characteristic maximum life span of species was initially proposed to be due to variation in mass-specific rate of metabolism. This is called the rate-of-living theory of aging and lies at the base of the oxidative-stress theory of aging, currently the most generally accepted explanation of aging. However, the rate-of-living theory of aging while helpful is not completely adequate in explaining the maximum life span. Recently, it has been discovered that the fatty acid composition of cell membranes varies systematically between species, and this underlies the variation in their metabolic rate. When combined with the fact that 1) the products of lipid peroxidation are powerful reactive molecular species, and 2) that fatty acids differ dramatically in their susceptibility to peroxidation, membrane fatty acid composition provides a mechanistic explanation of the variation in maximum life span among animal species. When the connection between metabolic rate and life span was first proposed a century ago, it was not known that membrane composition varies between species. Many of the exceptions to the rate-of-living theory appear explicable when the particular membrane fatty acid composition is considered for each case. Here we review the links between metabolic rate and maximum life span of mammals and birds as well as the linking role of membrane fatty acid composition in determining the maximum life span. The more limited information for ectothermic animals and treatments that extend life span (e.g., caloric restriction) are also reviewed.

Passive flow through an unstalked intertidal ascidian: orientation and morphology enhance suspension feeding in Pyura stolonifera.

Passive flow is believed to increase the gains and reduce the costs of active suspension feeding. We used a mixture of field and laboratory experiments to evaluate whether the unstalked intertidal ascidian Pyura stolonifera exploits passive flow. We predicted that its orientation to prevailing currents and the arrangement of its siphons would induce passive flow due to dynamic pressure at the inhalant siphon, as well as by the Bernoulli effect or viscous entrainment associated with different fluid velocities at each siphon, or by both mechanisms. The orientation of P. stolonifera at several locations along the Sydney-Illawarra coast (Australia) covering a wide range of wave exposures was nonrandom and revealed that the ascidians were consistently oriented with their inhalant siphons directed into the waves or backwash. Flume experiments using wax models demonstrated that the arrangement of the siphons could induce passive flow and that passive flow was greatest when the inhalant siphon was oriented into the flow. Field experiments using transplanted animals confirmed that such an orientation resulted in ascidians gaining food at greater rates, as measured by fecal production, than when oriented perpendicular to the wave direction. We conclude that P. stolonifera enhances suspension feeding by inducing passive flow and is, therefore, a facultatively active suspension feeder. Furthermore, we argue that it is likely that many other active suspension feeders utilize passive flow and, therefore, measurements of their clearance rates should be made under appropriate conditions of flow to gain ecologically relevant results.

Thermoenergetics of pre-moulting and moulting kookaburras (Dacelo novaeguineae): they're laughing.

We examined the effect of temperature on resting metabolic rate in seven field-captured laughing kookaburras (Dacelo novaeguineae) during late winter and early spring. Basal metabolic rate averaged 201+/-3.4 ml O(2) h(-1) (0.603 ml O(2) g(-1) h(-1)). Overall thermal conductance (K(o)) declined with ambient temperature ( T(a)) and averaged 0.026 ml O(2) g(-1) h(-1) degrees C(-1) at T(a)s<10 degrees C. Day-night differences in body temperatures (2.6 degrees C) and in alpha-phase versus rho-phase minimum metabolic rates were much greater (33%) than predicted for 340-g nonpasserine birds and suggest that these animals operate as low-metabolic intensity animals in their rest phase, but normal-metabolic intensity animals during their active phase. Metabolic rate was measured in four of the same birds undergoing moult. Thermal conductance increased to 60% above pre-moult values about 6 weeks after moult began. Basal metabolic rate of moulting birds showing peak thermal conductance readings averaged 17 ml O(2) h(-1) higher than pre-moult measurements. Although this increase was not statistically significant, we believe the moult costs of kookaburras are too low to overcome the inherent variability of BMR determination. We suggest that moult costs of kookaburras are only somewhat higher than the measured costs of protein synthesis of other endotherms.

Acyl composition of muscle membranes varies with body size in birds.

The acyl composition of phospholipids from pectoral muscle of eight species of birds, ranging in size from the 13 g zebra finch to the 34 kg emu, were measured and combined with recent published results for a 3 g hummingbird. This represents an approximately 11000-fold range in body mass. Muscle phospholipids, and thus muscle membrane bilayers, from birds had a relatively constant unsaturated acyl chain content of 62% but exhibited a significant allometric decline in unsaturation index (number of double bonds per 100 acyl chains) with increasing body mass. There was a significant allometric increase in the percentage of mono-unsaturates and a significant allometric decline in the percentage of n-3 polyunsaturates with increasing body mass, whilst there were no significant allometric trends in either percentage of n-6 or percentage of total polyunsaturates in bird muscle. The relative content of the highly polyunsaturated docosahexaenoic acid (22:6 n-3) showed the greatest scaling with body mass, having an allometric exponent of -0.28. The contribution of this n-3 polyunsaturate to the unsaturation index varied with body size, ranging from less than a 6% contribution in the emu to approximately 70% in the hummingbird. Such allometric variation in the acyl composition of bird muscle phospholipids is similar to that observed in mammals, although birds have fewer n-3 polyunsaturates and more n-6 polyunsaturates than do mammalian phospholipids. This allometric variation in phospholipid acyl composition is discussed with respect to both the metabolic intensity and lifespan of different sized bird species.

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.

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.

Seasonal and acute changes in adrenocortical responsiveness in an arctic-breeding bird.

The Lapland longspur, Calcarius lapponicus, times its breeding season so that chicks hatch coincident with the brief period of food abundance in the high arctic. This synchronization requires that all reproductive activities occur in over a much shorter period than at lower latitudes. Because of the known influence of stress hormones on delaying breeding in temperate-zone birds and the detrimental effects of such delays in the arctic, we expected the performance of the hypothalamic-pituitary-adrenal (HPA) axis of arctic-breeding birds to show less sensitivity to environmental stress than their mid-latitude counterparts. We found that adrenocortical responsiveness to the standardized stress of capture and handling, measured by taking five serial blood samples for corticosterone during the course of a 1-hr period, was similar to many temperate passerines and was also similar both between male and female longspurs and between the migratory and reproductive phases. However, the profile of plasma corticosterone during capture stress was significantly damped in longspurs sampled as they began their postnuptial molt. In addition, we had the opportunity to examine endocrine responses to a natural environmental stress in 1989 during a 3-day snowstorm which concealed available food resources. During this storm longspurs formed progressively larger flocks each day, with females abandoning incubation duties by the third day. Birds captured during the storm showed highly significant increases in both the rate of plasma corticosterone increase during capture and the peak postcapture level compared with birds sampled before the storm. This increased adrenal potential suggests increased activity of the HPA axis in response to severe conditions and is reminiscent of the response to fasting. Although the storm occurred during incubation, and reproductive hormone levels had begun to decline, we measured significant reductions in luteinizing hormone in both males and a subset of females captured during the storm.

Gender and seasonal differences in the adrenocortical response to ACTH challenge in an arctic passerine, Zonotrichia leucophrys gambelii.

We evaluated the adrenocortical response to acute stress in free-living Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii) using a standardized capture stress protocol in which five serial blood samples (70 microliters) were taken for measurement of plasma corticosterone (B) over the course of an hour of captivity (at 1, 5, 10, 30, and 60 min). In field-captured birds, male plasma B levels rose two to four times higher than those of females under capture stress during the breeding season, but were no different during winter (nonbreeding). We investigated the basis of this pattern by conducting dexamethasone (DEX) suppression tests on breeding and nonbreeding sparrows of both genders. This test involves pretreatment with subcutaneous DEX implants (a potent synthetic glucocorticoid) and challenge with intrajugular injections of either corticotropin (ACTH) or saline, followed by collection of a series of blood samples for evaluation of plasma B levels over a 2-hr period. ACTH injections in DEX-treated birds resulted in elevated B in both genders, with nonbreeding B profiles consistently lower than those of breeding birds. All DEX-treated, saline-injected birds, except breeding males, maintained low B levels for the entire 2-hr post-challenge period. This result indicates effective negative feedback by DEX on the hypothalamic-pituitary-adrenal axis, thus inhibiting endogenous B secretion. The apparent reduction in glucocorticoid feedback inhibition in breeding males may be related to an uncoupling of adrenal effects on reproductive behavior.

The effect of corticosterone on standard metabolic rates of small passerine birds.

Resting metabolic rates of Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii) and pine siskins (Carduelis pinus) were evaluated at thermoneutral temperatures before and after administration of corticosterone (B) at physiological doses. There was no effect of B on basal metabolic rate of either species, but nocturnal metabolic rate varied significantly less over the 3-h period of measurement in B-treated sparrows and siskins than in control birds. These results, coupled with observations of caged birds, suggest that corticosterone has no direct effect on avian resting metabolism but does reduce the responsiveness of birds to external stimuli and thus promotes nocturnal restfulness.

Avian eggs: thermoregulatory value of very high near-infrared reflectance.

Studies of the spectral reflectance of the eggs of 25 species of birds from nine families disclosed uniformly high reflectance (often above 90 percent) in the near infrared. This property is associated with the presence of the eggshell pigments protoporphyrin and the bilins. These pigments allow coloration for cryptic or other purposes with minimum solar heating, a combination not possible with the melanin pigments typical of vertebrates.