Persistent organic pollutants and organophosphate esters in feathers and blood plasma of adult kittiwakes (Rissa tridactyla) from Svalbard - associations with body condition and thyroid hormones.

Polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), organochlorine pesticides (OCPs) and organophosphate esters (OPEs) were assessed in blood plasma and feathers of 19 adult black-legged kittiwakes (Rissa tridactyla) breeding in two colonies (Blomstrandhalvøya and Krykkjefjellet) at the Arctic archipelago, Svalbard. Potential associations with body condition index (BCI) and thyroid hormones were investigated. All compound classes were detected in both blood plasma and feathers, but due to low sample size and volumes, OPEs could only be quantified in four individuals, warranting larger follow-up studies. Kittiwakes breeding at Blomstrandhalvøya had significantly higher concentrations of organic pollutants in blood plasma than kittiwakes breeding at Krykkjefjellet (p < 0.001). Concentrations in blood plasma and feathers did not significantly correlate for any of the investigated compounds, and feather concentrations did not differ significantly between the colonies. This suggests that pollutant levels in adult kittiwake feathers do not reflect local contamination at breeding sites and are as such not useful to monitor local contamination at Svalbard. Significant negative associations between BCI and most pollutants were found in both populations, whereas significant correlations between the BCI, the ratio of total triiodothyronine to free triiodothyronine (TT3:fT3), and several pollutants were only found for kittiwakes from Blomstrandhalvøya (all r ≥ -0.60 and p ≤ 0.05). This indicates that higher levels of circulating pollutants during the breeding period covary with the TT3: fT3 ratio, and may act as an additional stressor during this period.

No evidence for thermal transgenerational plasticity in metabolism when minimizing the potential for confounding effects.

Environmental change may cause phenotypic changes that are inherited across generations through transgenerational plasticity (TGP). If TGP is adaptive, offspring fitness increases with an increasing match between parent and offspring environment. Here we test for adaptive TGP in somatic growth and metabolic rate in response to temperature in the clonal zooplankton Daphnia pulex Animals of the first focal generation experienced thermal transgenerational 'mismatch' (parental and offspring temperatures differed), whereas conditions of the next two generations matched the (grand)maternal thermal conditions. Adjustments of metabolic rate occurred during the lifetime of the first generation (i.e. within-generation plasticity). However, no further change was observed during the subsequent two generations, as would be expected under TGP. Furthermore, we observed no tendency for increased juvenile somatic growth (a trait highly correlated with fitness in Daphnia) over the three generations when reared at new temperatures. These results are inconsistent with existing studies of thermal TGP, and we describe how previous experimental designs may have confounded TGP with within-generation plasticity and selective mortality. We suggest that the current evidence for thermal TGP is weak. To increase our understanding of the ecological and evolutionary role of TGP, future studies should more carefully identify possible confounding factors.

Differential reproductive responses to stress reveal the role of life-history strategies within a species.

Life-history strategies describe that 'slow'- in contrast to 'fast'-living species allocate resources cautiously towards reproduction to enhance survival. Recent evidence suggests that variation in strategies exists not only among species but also among populations of the same species. Here, we examined the effect of experimentally induced stress on resource allocation of breeding seabirds in two populations with contrasting life-history strategies: slow-living Pacific and fast-living Atlantic black-legged kittiwakes. We tested the hypothesis that reproductive responses in kittiwakes under stress reflect their life-history strategies. We predicted that in response to stress, Pacific kittiwakes reduce investment in reproduction compared with Atlantic kittiwakes. We exposed chick-rearing kittiwakes to a short-term (3-day) period of increased exogenous corticosterone (CORT), a hormone that is released during food shortages. We examined changes in baseline CORT levels, parental care and effects on offspring. We found that kittiwakes from the two populations invested differently in offspring when facing stress. In response to elevated CORT, Pacific kittiwakes reduced nest attendance and deserted offspring more readily than Atlantic kittiwakes. We observed lower chick growth, a higher stress response in offspring and lower reproductive success in response to CORT implantation in Pacific kittiwakes, whereas the opposite occurred in the Atlantic. Our findings support the hypothesis that life-history strategies predict short-term responses of individuals to stress within a species. We conclude that behaviour and physiology under stress are consistent with trade-off priorities as predicted by life-history theory. We encourage future studies to consider the pivotal role of life-history strategies when interpreting inter-population differences of animal responses to stressful environmental events.

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.

Basal metabolic rate: heritability and genetic correlations with morphological traits in the zebra finch.

Studies of genetic variation in metabolic traits have so far not focused on birds. In our study population of captive zebra finches we found evidence for a significant heritable genetic component in basal metabolic rate (BMR). Heritability of all morphological traits investigated (body mass, head length, tars length and wing length) was significantly larger than zero. All traits were positively phenotypically correlated. Eight of 10 genetic correlations presented in this study differed significantly from zero, all being positive, suggesting the possibility of correlated responses to any selection acting on the traits. When conditioned on the genetic variance in body mass, the heritability of BMR was reduced from 25% to 4%. Hence, our results indicate that genetic changes in BMR through directional selection are possible, but the potential for adaptation independent of body mass may be limited.

Does food shortage delay development of homeothermy in European shag nestlings (Phalacrocorax aristotelis)?

Nestlings seem to face a trade-off between reducing the basal level of energy metabolism, as an energy-saving response, and maintaining thermogenic capacity during temporal food shortage. In the present study we examined developmental responses to short-term diet restriction of 12-16 day old nestling European shags kept under laboratory conditions and tested whether temporal food shortage delay the development of homeothermy. During food shortage the European shag nestlings substantially reduced basal level of energy metabolism, resulting in significant energy savings. The reduction in basal level of energy metabolism corresponded with a reduction in peak metabolic rate. At the same time, the low peak metabolic rate of diet-restricted nestlings was offset by a lower mass-specific minimal thermal conductance, and an increased mass-specific absolute scope. Consequently, the insulation and the portion of peak metabolic rate available for regulatory thermogenesis seemed to develop normally, as expected from age, during the period of food shortage. Further, the degree of homeothermy, measured as the index of homeothermy, was not significantly lower in diet-restricted nestlings compared to controls at the same age. We conclude that temporal food shortage did not significantly delay the development of homeothermy in the European shag nestlings despite substantial reductions in basal level of energy metabolism and peak metabolic rate.

The energy economy of the arctic-breeding Kittiwake (Rissa tridactyla): a review.

The present paper reviews recent studies on changes in body mass, body composition and rates of energy expenditure during the breeding season in the black-legged Kittiwake (Rissa tridactyla) on Svalbard (79 degrees N). The main characteristic of the energy budget is a pronounced decrease in body mass as well as basal metabolic rate (BMR) after the eggs have hatched. While most internal organs lose mass in direct proportion to the general decrease in body mass, the liver and kidney masses decrease to a disproportionately greater extent. Since both the liver and the kidney have high intrinsic metabolic rates, these results support an earlier notion that the reduction in body mass is an adaptation to reduce maintenance costs. Alternatively, the reduced BMR is due to a decrease in energy uptake from the gastrointestinal tract, thereby ensuring that undigested food is ready to be regurgitated to the chicks. At the end of the chick-rearing period, the field metabolic rate (FMR) reaches its highest level, probably due to an increased workload associated with chick feeding. This occurs at a time of low body mass and BMR. A pronounced increase in the metabolic scope (FMR/BMR) during the latter part of the chick-rearing period demonstrates that BMR and FMR may change independently of each other and that the ratio FMR/BMR may not be a good measure of energy stress.

Individual variation in field metabolic rate of kittiwakes (Rissa tridactyla) during the chick-rearing period.

Field metabolic rate (FMR), using the doubly labelled water (DLW) method, was measured in free-ranging adult kittiwakes (Rissa tridactyla) early and late in the chick-rearing period at Svalbard, Norway. Individual variation in FMR was analysed by comparing FMR with body mass, sex, nest attendance, chick age, brood size, and basal metabolic rate (BMR). Mean FMR of kittiwakes during the chick-rearing period was 27.0+/-0.9 (SE) W kg(-1), while the individual variation (calculated as coefficient of variation [CV]) in FMR was 24%. Sex, time spent away from the nest, age of the chicks, and brood size contributed significantly to FMR and explained 65% of the variation in FMR. The FMR increased by 32% from early until late in the chick-rearing period. This occurred simultaneously with an increase in the time spent away from the nest. In 15 of 20 pairs, one of the mates had 15% or higher (mean of the 15 pairs, 22%+/-8%) FMR (W kg(-1)) than their partner, even though the mates spent equal amounts of time away from the nest. This indicates an intrapair conflict in FMR. The variation in total FMR of pairs was 40% less than the individual variation, and total FMR of pairs increased with age of the chicks. This indicates that the mates adjust their energy expenditure within a relatively constant FMR determined by the energy needs of the chicks. Individual variation in FMR could not be explained by variation in body mass or BMR. BMR measured late in the chick-rearing period was 26% lower than previous measurements of BMR from the prebreeding and incubation periods. The increase in FMR and simultaneous decrease in BMR caused a 40% increase in metabolic intensity (FMR/BMR) of kittiwakes during the chick-rearing period. It is suggested that the metabolic intensity is not a proper measure of the metabolic load in seabirds.

The relationship of central and peripheral organ masses to aerobic performance variation in house sparrows

We evaluated the relationship between organ mass and the limits to aerobic metabolism in house sparrows Passer domesticus. The results were used to test three models of performance limitation (the central limitation, peripheral limitation and symmorphosis concepts). Basal metabolic rate (BMR) was determined during the rest phase. The maximum rate of oxygen consumption during exercise ( v_dot (O2max)) was measured in an enclosed wheel that allowed limited hovering flight. Neither BMR nor v_dot (O2max) was affected by gender, but adults had significantly higher v_dot (O2max) and lower BMR than juveniles. The masses of most central organs (gut, gizzard, liver, heart, kidney and reproductive organs) differed significantly between ages. There were no gender differences in organ mass among juveniles, but liver mass differed between male and female adults. In the pooled data, BMR was positively correlated with the mass of three central organs (gut, liver and kidney) and with one peripheral effector (breast muscle); together, these explained more than half the variance in BMR (r(2)=0.57). In adults, BMR was positively correlated with the mass of reproductive tissue. The masses of one peripheral effector (breast muscle) and one central organ (the heart) were positively correlated with v_dot (O2max) (r(2)=0.17 for the pooled data set). These results are consistent with a symmorphosis model of aerobic capacity. We found a significant positive relationship between BMR and v_dot (O2max) in juveniles, but not in adults. Taken together, our data indicate that house sparrows can achieve elevated v_dot (O2max) without paying a 'penalty' (fitness trade-off) in the form of an increased BMR.

Yolk PCB and plasma retinol concentrations in shag (Phalacrocorax aristotelis) hatchlings.

To evaluate the possibilities of applying plasma retinol as a biomarker of response in seabirds exposed to chronic low levels of organochlorines, the relationship between yolk content of polychlorinated biphenyls (PCBs) and plasma retinol levels were studied in newly hatched shag chicks (Phalacrocorax aristotelis) from the coast of central Norway. The mean concentration of 29 PCB-congeners (SigmaPCB) in the yolk sac was 1.22 microgram/g ww (wet weight basis) (SD = 0.57, n = 10), or 17.99 ng/g lw (lipid weight basis) (SD = 6.26, n = 10). Expressed as TCDD-equivalents (SigmaTEQ), the exposure in the yolk sac was 43.9 pg/g ww (SD = 19.5, n = 10), or 637.1 pg/g lw (SD = 240.8, n = 10), considerably lower than the levels that have been associated with clear-cut lethal and sublethal effects such as egg mortality, hatchability, or live deformity in Phalacrocoracidae species. There were significant negative correlations between SigmaPCB ww and the variables egg volume, yolk mass, and hatchling mass. We suggest that these relationships are passive causes of a higher lipid concentration in small eggs, rather than the PCB affecting the variables. Analyses showed that there was a borderline significant positive correlation between SigmaPCB lw in yolk and plasma retinol concentration. Although the results indicate that plasma retinol level alone is a poor indicator of PCB exposure in shag hatchlings, the result may be related to the low level of contaminant exposure and the low sample size of the study.

Oxygen consumption and acid-base balance during shallow hypothermia in the pigeon.

In pigeons, during shallow nocturnal hypothermia induced by food deprivation, body temperature falls to values between 35 degrees C and 38 degrees C. Body temperature, oxygen consumption, and arterial blood pH and PCO2 were recorded during the entrance into such nocturnal hypothermic periods. In vivo pH was kept constant, while in vivo PCO2 increased slightly during hypothermia. This caused the temperature-corrected value of pH (pH*, measured at 40 degrees C) to fall by -0.014 units/degrees C, and the total CO2-content to rise by 3.2 mM, an increase of 16%. These changes in the acid-base balance represent, in effect, a respiratory acidosis that closely parallels the normal buffer line for pigeons. Q10 values, relating oxygen uptake to body temperature, were higher than 4.0 at the very beginning of the entrance into hypothermia, indicating that the metabolic rate was actively inhibited. However, the present results do not indicate any relationship between the acidosis and the inhibition of the metabolic rate.

Effect of high pressure on metabolic response to cold in rats.

The ability of rats to regulate body temperature in a cool helium-oxygen (heliox) atmosphere at high pressure was studied. Thermoregulatory ability in seven awake rats was assessed in a pressure chamber at 1.5, 21 and 41 ATA by monitoring body temperature and oxygen consumption during a gradual reduction of ambient temperature. Body temperature was measured by a radiotelemetry transmitter implanted into the intraperitoneal cavity. The thermal conductance of the rats increased from 0.37 to 0.75 W kg-1 degrees C-1 as air was substituted by heliox and increased further to 1.47 and 1.81 W kg-1 degrees C-1 as the pressure was increased to 21 and 41 ATA, respectively. At high pressure the rats were able to maintain body temperature until the metabolic rate reached a value of 21.9 +/- 2.0 W kg-1, which corresponds to peak metabolic rate. This occurred at an ambient temperature of approximately 21 degrees C. Below this ambient temperature the rats did not manage to maintain body temperature. The results show that the thermal effector mechanisms of rats respond adequately to a slowly decreasing ambient temperature in hyperbaric heliox environments.

Parabronchial oxygen extraction in ducks during selective cooling of the spinal cord.

Pekin ducks Anas platyrhynchos were chronically equipped with thermodes in the vertebral canal. Metabolic heat production, parabronchial oxygen extraction, vertebral canal temperature and body temperature were measured simultaneously before and during spinal cooling, at ambient temperatures ranging from 6 to 25 degrees C. Lowering vertebral canal temperature from 41.4 +/- 0.2 degrees C to 35.9 +/- 0.6 degrees C gave a mean increase in metabolic heat production of 1.54 +/- 0.26 W kg-1. Even though the spinal cooling had a clear metabolic effect, there was no concomitant change in parabronchial oxygen extraction. It is concluded that the thermosensitive structures residing in the spinal cord are not involved in the regulation of parabronchial gas exchange. The increase in parabronchial oxygen extraction, which is reported during cold exposure in birds, may therefore be induced by thermal inputs from peripheral thermoreceptors.

Gas exchange during high-frequency ventilation in the pigeon (Columba livia).

We studied the effect of high-frequency ventilation (HFV) on the gas exchange of tracheotomized pigeons. The pigeons were artificially ventilated using a piston pump, which alternately connected the pigeons' airways to a constant-flow source. Two-minute periods of HFV were interposed between long periods of normal ventilation. The effect of HFV was assessed by the recorded changes in the PO2, PCO2 and pH of arterial blood and from the changes in the composition of the gas in the interclavicular air sacs. The results showed that HFV can augment gas exchange when the tidal volume (VT) is less than the volume of the anatomical dead space (VD). However, normal arterial gas composition can only be maintained if respiratory frequency is high (greater than 20 Hz). At the normal panting frequency of pigeons (7.8 Hz), gas exchange can thus only be maintained if tidal volume is approximately 125% of the dead space. When panting the VT must be greater than the VD. This finding agrees with the results of recent work showing flush-out- or compound-panting in birds: i.e. if, during panting, VT approaches close to the VD, intermittent interruptions, by taking deeper breaths in order to ensure a supply of fresh air to the lungs, are necessary.

Ventilatory and circulatory changes during cold exposure in the Pekin duck Anas platyrhynchos.

Inspired ventilation (VI), O2 uptake (VO2), body temperature (TB), arterial blood pressure and arterio-venous differences in blood gases and pH were measured in ducks. Anas platyrhynchos, during exposure to variable ambient temperature (Ta) +20, 0 and -20 degrees C. A stable TB was maintained at all Ta's VO2 increased from 12.07 ml O2 (STPD) X kg-1 X min-1 at 20 degrees C to 28.95 ml O2 X kg-1 X min-1 at 20 degrees C. The ventilatory requirement (VI/VO2) changed from 0.468 L X mmol-1 at 20 degrees C to 0.322 L X mmol-1 at -20 degrees C corresponding to a change in overall O2-extraction from 28.5 to 41.4%. The increase in VI during cold exposure resulted from an increased tidal volume while breathing frequency was unchanged. This caused a smaller fraction of the total inspired air being dead space ventilation during cold exposure. The changed ventilatory requirement was largely the result of an increased parabronchial O2-extraction, whereas the altered ventilatory pattern accounted for a smaller part (21%) of the decreased ventilatory requirement. Arterial and venous O2 content and PaO2 changed little with cold exposure while PVO2 increased significantly. Calculated values for cardiac output increased from 173.7 ml X kg-1 X min-1 at +20 degrees C to 431.4 ml X kg-1 at -20 degrees C. From a thermoregulatory point of view it seems significant that the increased heat production during cold exposure is followed by an increased oxygen extraction in the lungs and in increased cardiac output, rather than by a further elevation of ventilation.

Cardiovascular changes associated with treadmill running in the Pekin duck.

Six adult white Pekin ducks were trained to run on a treadmill for 10 min at a speed of 1.43 km h-1. O2 consumption, CO2 production, breathing rate, blood gas tension and pH, sciatic and carotid blood flows and colonic and skin temperatures were measured in the experiments. A 2.6 times increase in oxygen consumption was observed when going from resting on the treadmill to exercise. The increased oxygen delivery was achieved by a 61% increase in cardiac output and a 51% increase in the arterio-venous oxygen content difference. Probably the reported resting oxygen consumption was higher than a true resting level causing the increment in oxygen consumption to be more correctly 3.6 times the resting level. Sciatic and carotid blood flow increased by 3.7 times and 2.3 times, respectively, during exercise. At cessation of exercise, the carotid blood flow decreased very rapidly, while the sciatic blood flow decreased more slowly. An increased web temperature above the exercise level was seen in the post-exercise period. The results suggest that the ducks prefer to use non-evaporative heat loss in the post-exercise period, respiratory evaporative cooling being of minor importance. this strategy may be correlated to the small internal heat load induced by the running (body temperature increased by only 0.3 degrees C.