Daily energy expenditure of singing great reed warblers Acrocephalus arundinaceus

According to honest signalling theory, signals must be costly to produce to retain information about the signaller's quality. The song produced by male birds during breeding is a vocal "ornament" used for intra- and inter-sexual purposes. The energetic cost of this vocal signal remains a contentious issue. We used the doubly labelled water method to measure field metabolic rate by estimating CO₂ production and then convert this to daily energy expenditure (DEE) in great reed warbler males singing under natural conditions (10 at low to moderate intensity and 7 at very high intensity from dawn to dusk). There was a significant positive relationship between singing intensity and DEE. From this relationship we extrapolated the average DEE for intensely singing males (i.e., males producing song sounds 50% of the time and hence sitting at their elevated song post in the top of a reed stem more or less continuously throughout the ∼20 h of daylight) to 3.3×BMR (basal metabolic rate) and for non-singing males to 2.2×BMR. The mean DEE measured for the seven males singing with very high intensity was 3.1×BMR. The maximum measured DEE for a single male was 3.9×BMR, i.e. close to the maximum sustainable DEE (4×BMR), and the minimum DEE was 2.1×BMR for a male singing at very low intensity. These results imply that producing intensive advertising song in birds may incur a substantial cost in terms of increased energy expenditure.     

Raised thermoregulatory costs at exposed song posts increase the energetic cost of singing for willow warblers Phylloscopus trochilus

Sexually selected displays, such as bird song, are expected to be costly. We examined a novel potential cost to bird song: whether a less favourable microclimate at exposed song posts would be predicted to raise metabolic rate. We measured the microclimate and height at which willow warblers Phylloscopus trochilus sang and foraged. Song posts were higher than foraging sites. The wind speed was 0.6±0.3 ms⁻¹ greater at song posts (mean±SD, N=12 birds). Song rate and song post selection were not influenced consistently by temperature or wind speed, but the birds sang from lower positions on one particularly windy day. This may have resulted from difficulty in holding on to exposed branches in windy conditions rather than a thermoregulatory constraint. The results suggest that the extra thermoregulatory costs at song posts would increase metabolic rate by an average of 10±4% and a maximum of 25±8% (N=12 birds) relative to birds singing at foraging sites. We estimated that metabolic rate would be 3–8% greater during singing than during quiet respiration because of heat and evaporative water loss in exhaled gases. The combined energy requirements for sound production, thermoregulation at exposed song posts and additional heat loss in exhaled air could increase the metabolic rate of willow warblers by an average of 14–23%, and a maximum of 42–63%, during singing. The energetic cost of singing may thus be much greater for birds in a cold, windy environment than for birds singing in laboratory conditions.     

Heat transfer and the energetic cost of singing by canaries <Emphasis Type="Italic">Serinus canaria</Emphasis>

Sexually selected displays, such as male passerine bird song, are predicted to be costly. However, most measurements calculated the rate of oxygen consumption during singing using respirometry have shown that bird song has a low energetic cost. Since birds are reluctant to sing when enclosed inside a respirometry chamber, the energetic cost of singing could differ from that under more normal circumstances. We used heat transfer modelling, based on thermal images, to estimate the energetic cost of singing by canaries (Serinus canaria) that were not enclosed in respirometry chambers. Metabolic rate calculated from heat transfer modelling was 0.70±0.02 W (N=10 birds) during singing, which was 14±5% greater than during standing (0.62±0.02 W). The energetic cost of singing did not differ significantly from that measured previously using respirometry when we took into account that birds sang for a greater proportion of the time during the current experiments. These conclusions were not sensitive to potential errors in the heat transfer model. Heat transfer modelling would be especially useful to obtain measurements of the energetic cost of activities that animals do not perform readily inside respirometry chambers, such as singing in birds.     

Flight modes in migrating European bee-eaters: heart rate may indicate low metabolic rate during soaring and gliding

Background

Many avian species soar and glide over land. Evidence from large birds (m _b>0.9 kg) suggests that soaring-gliding is considerably cheaper in terms of energy than flapping flight, and costs about two to three times the basal metabolic rate (BMR). Yet, soaring-gliding is considered unfavorable for small birds because migration speed in small birds during soaring-gliding is believed to be lower than that of flapping flight. Nevertheless, several small bird species routinely soar and glide.

Methodology/Principal Findings

To estimate the energetic cost of soaring-gliding flight in small birds, we measured heart beat frequencies of free-ranging migrating European bee-eaters (Merops apiaster, m _b∼55 g) using radio telemetry, and established the relationship between heart beat frequency and metabolic rate (by indirect calorimetry) in the laboratory. Heart beat frequency during sustained soaring-gliding was 2.2 to 2.5 times lower than during flapping flight, but similar to, and not significantly different from, that measured in resting birds. We estimated that soaring-gliding metabolic rate of European bee-eaters is about twice their basal metabolic rate (BMR), which is similar to the value estimated in the black-browed albatross Thalassarche (previously Diomedea) melanophrys, m _b∼4 kg). We found that soaring-gliding migration speed is not significantly different from flapping migration speed.

Conclusions/Significance

We found no evidence that soaring-gliding speed is slower than flapping flight in bee-eaters, contradicting earlier estimates that implied a migration speed penalty for using soaring-gliding rather than flapping flight. Moreover, we suggest that small birds soar and glide during migration, breeding, dispersal, and other stages in their annual cycle because it may entail a low energy cost of transport. We propose that the energy cost of soaring-gliding may be proportional to BMR regardless of bird size, as theoretically deduced by earlier studies.     

Metabolic costs of egg production in the European starling (Sturnus vulgaris)

The energy cost of egg production in passerine birds has typically been estimated to be 45%-60% of basal metabolic rate (BMR), but this is based on theoretical models using data on energy content of eggs and reproductive tissue; there are still very few empirical data on egg production costs. In this study, we directly measured resting metabolic rate (RMR) in egg-laying female European starlings (Sturnus vulgaris) over 3 yr. We compared these data with RMR of nonbreeding and chick-rearing birds and with estimated energy expenditure generated from a typical energy content model by using empirically derived data from body composition analysis for this species. We found marked variation in RMR between years and between reproductive stages, which complicates comparisons among breeding stages for the assessment of relative egg production costs. On the basis of this method, RMR during egg laying varied from +74% to -13% of nonbreeding RMR and from +20% to -7% of chick-rearing RMR. We therefore used an alternate approach: measuring changes in RMR through the complete cycle of follicle development and ovulation. The increase in RMR from the beginning of prelaying to the six-follicle stage (before first ovulation) when birds have a complete developing follicle hierarchy was 22.4%. This value is still much lower than that estimated from our energy content model. We discuss conceptual problems associated with the theoretical energy content approach but also suggest, on the basis of earlier work done in our lab, that the measured increase in RMR might still underestimate the actual cost of egg production if birds reallocate energy between different physiological systems.     

Energetic cost of foraging in free-diving emperor penguins.

Hypothesizing that emperor penguins (Aptenodytes forsteri) would have higher daily energy expenditures when foraging for their food than when being hand-fed and that the increased expenditure could represent their foraging cost, we measured field metabolic rates (FMR; using doubly labeled water) over 4-d periods when 10 penguins either foraged under sea ice or were not allowed to dive but were fed fish by hand. Surprisingly, penguins did not have higher rates of energy expenditure when they dove and captured their own food than when they did not forage but were given food. Analysis of time-activity and energy budgets indicated that FMR was about 1.7 x BMR (basal metabolic rate) during the 12 h d(-1) that penguins were lying on sea ice. During the remaining 12 h d(-1), which we termed their "foraging period" of the day, the birds were alert and active (standing, preening, walking, and either free diving or being hand-fed), and their FMR was about 4.1 x BMR. This is the lowest cost of foraging estimated to date among the eight penguin species studied. The calculated aerobic diving limit (ADL(C)), determined with the foraging period metabolic rate of 4.1 x BMR and known O(2) stores, was only 2.6 min, which is far less than the 6-min ADL previously measured with postdive lactate analyses in emperors diving under similar conditions. This indicates that calculating ADL(C) from an at-sea or foraging-period metabolic rate in penguins is not appropriate. The relatively low foraging cost for emperor penguins contributes to their relatively low total daily FMR (2.9 x BMR). The allometric relationship for FMR in eight penguin species, including the smallest and largest living representatives, is kJ d(-1)=1,185 kg(0.705).     

Metabolic adjustments in breeding female kittiwakes (<Emphasis Type="Italic">Rissa tridactyla</Emphasis>) include changes in kidney metabolic intensity

Black-legged kittiwakes (BLKIs) reduce self-maintenance cost through reductions in mass-specific basal metabolic rate (BMR), body mass and the size of visceral organs during the chick-rearing period. In the present study, we measured kidney in vitro oxygen consumption and plasma 3,3',5-triiodo-L: -thyronine (T3) levels of incubating and chick-rearing female BLKIs, to test whether the decrease in BMR is caused mainly by decreased metabolic intensity or simply by reductions in the size of organs with high metabolic intensity. Body mass and body condition were lower in chick-rearing birds compared with the incubating birds. In contrast to the previous findings, however, the kidney mass did not differ between the two breeding stages. Plasma T3 levels decreased substantially during the breeding season, indicating a reduction in BMR. Over the same period, kidney mass-specific oxygen consumption decreased (by 17.2%) from the incubating to the chick-rearing stage. Thus, the reduction in BMR found in breeding BLKIs seems partly explained by adjustments in metabolic intensity of visceral organs. Lowered metabolic intensity of visceral organs would permit increased allocation of energy to offspring at the expense of their own self-maintenance.     

The costs of singing in nightingales

The costs of singing in birds are poorly understood. One potential type of cost is a metabolic cost of singing. Previous studies have measured short-term changes in oxygen consumption associated with bouts of vocalizations, with equivocal results. In this study, I used an alternative approach to measuring the metabolic cost of singing, by measuring overnight loss of body mass, in male common nightingales, Luscinia megarhynchos, singing at night at different rates. Nightingales were shown not to forage at night. They reached a higher mass at dusk prior to singing more at night, and lost more mass overnight when dusk mass and overnight song rate were high. These results show that singing at night is associated with increased overnight consumption of body reserves, which represents a significant metabolic cost of singing at night. However, the correlation between dusk mass and overnight song rate makes it impossible to determine whether these costs arise from the energetic costs of the singing itself, or from the metabolic costs of the additional body reserves laid down at dusk on nights when song rate was high. There are also likely to be costs associated with accumulating and carrying these extra body reserves during daylight, as well as other potential costs of singing such as an increased risk of predation. These results are consistent with those models of signalling in biology that predict or assume that honest signals are costly. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Perch exposure and predation risk: a comparative study in passerines

Singing birds optimize signal transmission by perching in exposed locations. However, conspicuous singing may be risky, and previous research has found that individuals trade off singing performance with song perch exposure. We studied the relationship between predation risk (degree of concealment, height in tree or shrub, and distance to the forest edge) and time allocated to singing and vigilance in a group of 13 passerine species living in an East African savanna. Concealed birds sang more and were less vigilant. Vigilance increased as distance to the forested edge increased, but distance had no effect on time allocated to singing. Body size was significantly correlated with vigilance but not singing; larger passerines were more sensitive to both relative concealment and the distance to the forest edge, while song was influenced by neither of these factors. Perch height had no effect on either behavior. Our results suggest that birds modify vigilance and, to some extent, singing behavior to minimize their exposure to predators.     

Metabolic consequences of overlapping food restriction and cell‐mediated immune response in a long‐distance migratory shorebird,the little ringed plover Charadrius dubius

Investment in immunity is commonly viewed as an energetically costly activity in birds. Although several studies have focused on the energy cost of mounting an immune response and its concomitant physiological trade‐offs, nothing is known about the metabolic adjustments experienced by immunochallenged birds under resource limitation, or about the basal metabolism cost of mounting cell‐mediated immune (CMI) responses in bird species other than non‐migratory passerines. Here we measured the basal metabolic rate (BMR), inflammatory response, and body mass in ad libitum fed and food‐restricted little ringed plovers Charadrius dubius challenged with phytohemagglutinin (PHA) in order to assess the energy cost, the strength, and the time course of the CMI response in a long‐distance migratory bird in different nutritional states. We found that ad libitum birds injected with PHA significantly increased both mass‐independent BMR and inflammatory response, whereas birds with an induced food restriction‐immune response overlap experienced a mass‐independent BMR downregulation and decreased inflammatory response relative to ad libitum birds. We suggest that both the BMR downregulation and the diminished inflammatory response observed in birds facing such an overlap could be energy‐saving mechanisms to maintain the body mass above a critical level and maximize fitness.     

Energetics of fattening and starvation in the long-distance migratory garden warbler,Sylvia borin,during the migratory phase

Garden warblers (Sylvia borin) were subjected to starvation trials during their autumnal migratory phase in order to simulate a period of non-stop migration. Before, during and after this treatment the energy expenditure, activity, food intake and body mass of the subjects were monitored. Assimilation efficiency was constant throughout the experiments. The catabolized (during starvation) and deposited body tissue (during recovery) consisted of 73% fat. Basal metabolic rate was decreased during the starvation period and tended to a gradual increase during the recovery period. The reduced basal metabolic rate can possibly be attributed to a reduced size/function of the digestive system, which is consistent with the sub-maximal food intake immediately after resuming the supply of food to the experimental birds. The observed reductions in basal metabolic rate during starvation and activity during recovery can be viewed as adaptations contributing to a higher economization of energy supplies. The experimental birds were unable to eat large quantities of food directly after a period of starvation leading to a comparatively low, or no increase in body mass. Such a slow mass increase is in agreement with observations of migratory birds on arrival at stop-over sites.Abbreviations BM body mass - BMR basal metabolic rate - LBM lean body mass - RQ respiratory quotient     

Foraging energetics of Grey-headed Albatrosses Diotnedea chrysostoma at Bird Island,South Georgia

At-sea metabolism (CO₂ production) and water turnover of six breeding Grey-headed Albatrosses Diomedea chrysostoma were measured, using the doubly labelled water method, at Bird Island, South Georgia, Mean food consumption (estimated from a water influx rate of 1.01 1 d^-1 and data on dietary composition) was 1200gd^-1 or 50.4 W. At-sea metabolism (derived from a rate of CO₂ production of 3.98 1 h^-1) was 27.7 W, 2.5 times the estimated basal metabolic rate (BMR). On average the birds ingested nearly twice as much food energy as they expended to obtain it. The metabolic rate during flight (estimated from at-sea metabolism and activity budget data) was 36.3 W (range 34.7–39.0 W) or 3.2 (range 3.0–3.4) times the predicted BMR. This is the lowest cost of flight yet measured, but consistent with the highly developed adaptations for economic flight shown by albatrosses. These results are briefly compared with data for other polar vertebrates (penguins, fur seals) exploiting similar prey.     

树麻雀代谢率和器官重量在季节驯化中表型的可塑性变化

动物能量代谢的生理生态特征与物种的分布和丰富度密切相关,基础代谢率(BMR)是内温动物能量预算的重要组成部分。北温带的小型鸟类,通过增加产热来适应低温环境。增加BMR的基础之一是中心器官(代谢机器)发生明显的变化。本研究中我们测定了树麻雀(Passermontanus)的BMR、体重和各器官的重量,分析了麻雀各器官的季节性变化及与BMR的关系。方差分析表明:麻雀的BMR存在明显的季节性变化,在冬季和秋季较高。麻雀内部器官的变化同样有明显的季节性,冬季和秋季麻雀的肝脏、心脏、肌胃、小肠、直肠和整体消化道的重量,都有明显的增加。相关分析表明:麻雀的BMR与肝脏、心脏和消化道等内部器官存在明显的相关性。我们的结果验证了“中心限制假说”,即麻雀体内存在着与BMR相关的“代谢机器”,中心器官是提高麻雀BMR的基础之一。     

Seasonal variation in the metabolism-temperature relation of House Sparrows (Passer domesticus) in KwaZulu-Natal,South Africa

Many birds exhibit considerable phenotypic flexibility in metabolism to maintain thermoregulation or to conserve energy. This flexibility usually includes seasonal variation in metabolic rate. Seasonal changes in physiology and behavior of birds are considered to be a part of their adaptive strategy for survival and reproductive success. House Sparrows (Passer domesticus) are small passerines from Europe that have been successfully introduced to many parts of the world, and thus may be expected to exhibit high phenotypic flexibility in metabolic rate. Mass specific Resting Metabolic Rate (RMR) and Basal Metabolic Rate (BMR) were significantly higher in winter compared with summer, although there was no significant difference between body mass in summer and winter. A similar, narrow thermal neutral zone (25–28 °C) was observed in both seasons. Winter elevation of metabolic rate in House Sparrows was presumably related to metabolic or morphological adjustments to meet the extra energy demands of cold winters. Overall, House Sparrows showed seasonal metabolic acclimatization similar to other temperate wintering passerines. The improved cold tolerance was associated with a significant increase in VO₂ in winter relative to summer. In addition, some summer birds died at 5 °C, whereas winter birds did not, further showing seasonal variation in cold tolerance. The increase in BMR of 120% in winter, compared to summer, is by far the highest recorded seasonal change so far in birds.     

Thermal history can affect the short-term thermal acclimation of basal metabolic rate in the passerine Zonotrichia capensis

The obligatory cost of living for endotherms is measured by basal metabolic rate (BMR), a variable that is known to change after thermal acclimation. However, the relative timing between variation in ambient temperature and BMR is not well understood. In this study, we addressed this problem in the sparrow Zonotrichia capensis, studying whether previous thermal history affects the response of BMR to a new acclimation temperature. We found that after 4 weeks of acclimation either to 30 or 15 °C birds exhibited significant differences in BMR from pre-acclimation levels. Nevertheless, after a re-acclimation to the opposite treatment for six additional weeks, in the group previously acclimated to warm conditions the change in BMR was significantly greater than in the group previously acclimated to cold. We also found differences in the mass of the small intestine between groups but constancy in the mass of liver, kidney and heart masses at the end of the experiments. Our results indicate that the thermal history affects metabolic adjustments and highlights the importance of considering this when evaluating the plasticity of metabolic traits in small birds.     

The allometry of avian basal metabolic rate: good predictions need good data

Basal metabolic rate (BMR) is often predicted by allometric interpolation, but such predictions are critically dependent on the quality of the data used to derive allometric equations relating BMR to body mass (Mb). An examination of the metabolic rates used to produce conventional and phylogenetically independent allometries for avian BMR in a recent analysis revealed that only 67 of 248 data unambiguously met the criteria for BMR and had sample sizes with n>/=3. The metabolic rates that represented BMR were significantly lower than those that did not meet the criteria for BMR or were measured under unspecified conditions. Moreover, our conventional allometric estimates of BMR (W; logBMR=-1.461+0.669logMb) using a more constrained data set that met the conditions that define BMR and had n>/=3 were 10%-12% lower than those obtained in the earlier analysis. The inclusion of data that do not represent BMR results in the overestimation of predicted BMR and can potentially lead to incorrect conclusions concerning metabolic adaptation. Our analyses using a data set that included only BMR with n>/=3 were consistent with the conclusion that BMR does not differ between passerine and nonpasserine birds after taking phylogeny into account. With an increased focus on data mining and synthetic analyses, our study suggests that a thorough knowledge of how data sets are generated and the underlying constraints on their interpretation is a necessary prerequisite for such exercises.     

Is the Rate of Metabolic Ageing and Survival Determined by Basal Metabolic Rate in the Zebra Finch?

The relationship between energy metabolism and ageing is of great interest because aerobic metabolism is the primary source of reactive oxygen species which is believed to be of major importance in the ageing process. We conducted a longitudinal study on captive zebra finches where we tested the effect of age on basal metabolic rate (BMR), as well as the effect of BMR on the rate of metabolic ageing (decline in BMR with age) and survival. Basal metabolic rate declined with age in both sexes after controlling for the effect of body mass, indicating a loss of functionality with age. This loss of functionality could be due to accumulated oxidative damage, believed to increase with increasing metabolic rate, c.f. the free radical theory of ageing. If so, we would expect the rate of metabolic ageing to increase and survival to decrease with increasing BMR. However, we found no effect of BMR on the rate of metabolic ageing. Furthermore, survival was not affected by BMR in the males. In female zebra finches there was a tendency for survival to decrease with increasing BMR, but the effect did not reach significance (P<0.1). Thus, the effect of BMR on the rate of functional deterioration with age, if any, was not strong enough to influence neither the rate of metabolic ageing nor survival in the zebra finches.     

Plasma thyroid hormone concentrations in a wintering passerine bird: their relationship to geographic variation,environmental factors,metabolic rate,and body fat

Winter acclimatization among passerine birds involves metabolic adjustments that allow for high rates of thermogenesis. In previous studies, we observed geographic variation in the basal metabolic rate (BMR) of overwintering cardinals along a latitudinal gradient at two different longitudinal transects. Because thyroid hormones (THs) are important for metabolic adjustments in endotherms, we determined whether geographic variation in BMR can be explained by variation in thyroid status. We measured total plasma TH (thyroxine [T(4)] and 3,5,3'-triiodothyronine [T(3)]) concentrations by radioimmunoassay in birds from two latitudinal transects extending from approximately 31 degrees to 42 degrees. Birds from both transects had higher plasma THs in the late afternoon than in the early morning. Plasma T(3) increased with latitude, while plasma T(4) varied such that the southernmost birds and the northernmost birds had higher hormone concentrations than birds at the intermediate latitude. There was no correlation between plasma TH concentrations and BMR. To test whether thyroid status influences metabolic parameters in winter-acclimatized captive cardinals, we fed cardinals diets supplemented with T(4) (5 microg T(4) g(-1) food), the goitrogen methimazole (1 mg g(-1) food), or both. Plasma T(4) concentrations were altered by most of the treatments, but we observed no significant effects on any metabolic parameter. We conclude, therefore, that there is latitudinal variation in metabolic parameters in cardinals but that this variation is not explained by variation in plasma TH concentrations.     

Flight muscle catabolism during overnight fasting in a passerine bird,Eremophila alpestris

Summary Brood-rearing passerine birds often have sparse lipid reserves coupled with potentially high energy demands. This may necessitate increased fasting protein catabolism; however, the largest source of protein, flight muscle, must be maintained. This problem was examined in the horned lark (Eremophila alpestris), a 28-g passerine. Overnight fasting caused significant depletion of protein in flight muscle and liver, but not in other muscle groups. Proteolytic enzyme activity of the flight muscle doubled during fasting. Biochemical and ultrastructural studies revealed that protein was depleted disproportionately from the sarcoplasm of flight muscle cells. Fasting caused a reduction in the protein-specific glycolytic capacity of flight muscle tissue. Oxidative capacity of the flight muscle, as measured by both in vivo and in vitro assays, was not significantly affected. The disproportionate catabolism of flight muscle sarcoplasmic protein may be due to a greater susceptibility to proteolysis, and not necessarily because it represents a source of redundant storage protein.Abbreviations BMR basal metabolic rate - GPDH alpha-glycerophosphate dehydrogenase - mATPase myofibrillar adenosine triphosphatase - SDH succinate dehydrogenase - STPD standard temperature pressure dry     

The demands of incubation and avian clutch size

We reviewed information on the demands of incubation to examine whether these could influence the optimal clutch size of birds. The results indicate that appreciable metabolic costs of incubation commonly exist, and that the incubation of enlarged clutches can impose penalties on birds. In 23 studies on 19 species, incubation metabolic rate (IMR) was not elevated above the metabolic rate of resting non-incubating birds (RMR), but contrary to the physiological predictions of King and others, IMR was greater than RMR in 15 studies on 15 species. Across species, IMR was substantially above basal metabolic rate (BMR), averaging 1.606 × BMR. Of six studies on three species performed under thermo-neutral conditions, none found IMR to be in excess of RMR. IMRs measured exclusively within the thermo-neutral zone averaged only 1.08 × BMR contrasting with the significantly higher figure of 1.72 × BMR under wider conditions. 16 of 17 studies on procellariiforms found IMR below RMR, indicating a significant difference between this and other orders. We could find no other taxonomic, or ecological factors which had clear effects on IMR. Where clutch size was adjusted experimentally during incubation, larger clutches were associated with: significantly lower percentage hatching success in 11 of 19 studies; longer incubation periods in eight of ten studies; greater loss of adult body condition in two of five studies; and higher adult energy expenditure in eight of nine studies. Given that incubation does involve metabolic costs and given that the demands of incubation increase sufficiently with clutch size to affect breeding performance, we propose that the optimal clutch size of birds may in part by shaped by the number of eggs the parents can afford to incubate.