Basal metabolic rate, food intake, and body mass in cold- and warm-acclimated Garden Warblers

We address the question of whether physiological flexibility in relation to climate is a general feature of the metabolic properties of birds. We tested this hypothesis in hand-raised Garden Warblers (Sylvia borin), long-distance migrants, which normally do not experience great temperature differences between summer and winter. We maintained two groups of birds under cold and warm conditions for 5 months, during which their body mass and food intake were monitored. When relatedness (siblings vs. non-siblings) of the experimental birds was taken into account, body mass in cold-acclimated birds was higher than in warm-acclimated birds. BMR, measured at the end of the 5-month temperature treatment, was also higher in the cold- than the warm-acclimated group. Migrant birds thus seem to be capable of the same metabolic cold-acclimation response as has been reported in resident birds. The data support the hypothesis that physiological flexibility is a basic trait of the metabolic properties of birds.

Variation in energy intake and basal metabolic rate of a bird migrating in a wind tunnel

1. We studied the changes in body mass, metabolizable energy intake rate (ME) and basal metabolic rate (BMR) of a Thrush Nightingale, Luscinia luscinia, following repeated 12-h migratory flights in a wind tunnel. In total the bird flew for 176 h corresponding to 6300 km. This is the first study where the fuelling phase has been investigated in a bird migrating in captivity.

2. ME was very high, supporting earlier findings that migrating birds have among the highest intake rates known among homeotherms. ME was significantly higher the second day of fuelling, indicating a build-up of the capacity of the digestive tract during the first day of fuelling.

3. Further indications of an increase in size or activity level of metabolically active structures during fuelling come from the short-term variation in BMR, which increased over the 2-day fuelling period with more than 20%, and in almost direct proportion to body mass. However, mass-specific BMR decreased over the season.

4. The patterns of mass change, ME and BMR of our focal bird following two occasions of 12-h fasts were the same as after flights, indicating that fast and flight may involve similar physiological processes.

5. The relatively low ME the first day following a flight may be a contributing factor to the well-known pattern that migrating birds during stopover normally lose mass the first day of fuelling.

Metabolic rate and thermal conductance of lemmings from high-arctic Canada and Siberia

The arctic climate places high demands on the energy metabolism of its inhabitants. We measured resting (RMR) and basal metabolic rates (BMR), body temperatures, and dry and wet thermal conductances in summer morphs of the lemmings Dicrostonyx groenlandicus and Lemmus trimucronatus in arctic Canada, and the BMR of D. torquatus, D. groenlandicus, L. sibiricus, L. bungei and L. trimucronatus in Siberia. In contrast to previous studies the data were collected on animals that had spent only a limited time in captivity. All parameters were analysed in relation to the variations in body mass (20-90 g). Body temperature and BMR were lower in D. groenlandicus than L. trimucronatus, which coincides with greater longevity in the former species. Wet and dry thermal conductances of both species were similar and comparable with those of other Myomorpha (mouse-type rodents), indicating no evidence for a previously claimed lower thermal conductance in lemmings. BMR in lemmings appeared to be higher than in other Arvicolidae (voles, lemmings and muskrats), which could relate to their typically high-latitude distribution. However, the more southerly living Lemmus species had higher BMR than the more northerly living Dicrostonyx species, which may be explained by the former having a relatively low-quality diet.

Resting and peak metabolic rates of Arctic Tern nestlings and their relations to growth rate

We measured resting and peak metabolism in relation to growth rate in arctic tern Sterna paradisaea chicks over the first 10 d after hatching. For chicks with varying growth rate, body mass seems to be a better predictor of resting metabolic rate rather than age. The effect of changes in growth rate on resting metabolism of arctic terms is smaller than found interspecifically in hatchlings. It is possible that difference exist in the heat increment of feeding between fast and slow growers that would further reduce the effect of growth rate on resting metabolism. Chicks that had body masses lower than 75% of that expected for their age were metabolically inferior in withstanding a thermal challenge compared with chicks of the same age but normal mass. In contrast to resting metabolic rate, the extent of peak metabolic rate is related to both body mass and age. This, in part, the maturation of the thermoregulatory system proceeds steadily with time even when body mass lags behind.

Physiological response to extreme fasting in subantarctic fur seal (Arctocephalus tropicalis) pups : metabolic rates, energy reserve utilization, and water fluxes

Physiological response to extreme fasting in subantarctic fur seal (Arctocephalus tropicalis) pups: metabolic rates, energy reserve utilization, and water fluxes. Am J Physiol Regul Integr Comp Physiol 297: R1582–R1592, 2009. First published September 23, 2009; doi:10.1152/ajpregu.90857.2008.— Surviving prolonged fasting requires various metabolic adaptations, such as energy and protein sparing, notably when animals are simultaneously engaged in energy-demanding processes such as growth. Due to the intermittent pattern of maternal attendance, subantarctic fur seal pups have to repeatedly endure exceptionally long fasting episodes throughout the 10-mo rearing period while preparing for nutritional independence. Their metabolic responses to natural prolonged fasting (33.4 ± 3.3 days) were investigated at 7 mo of age. Within 4–6 fasting days, pups shifted into a stage of metabolic economy characterized by a minimal rate of body mass loss (0.7%/day) and decreased resting metabolic rate  (5.9 ± 0.1 ml O₂ ·kg^-1·day^-1) that was only 10% above the level predicted for adult terrestrial mammals. Field metabolic rate (289 ± 10 kJ·kg^-1 ·day^-1) and water influx (7.9 ± 0.9 ml·kg^-1 ·day^-1) were also among the lowest reported for any young otariid, suggesting minimized energy allocation to behavioral activity and thermoregulation. Furthermore, lean tissue degradation was dramatically reduced. High initial adiposity (>48%) and predominant reliance on lipid catabolism likely contributed to the exceptional degree of protein sparing attained. Blood chemistry supported these findings and suggested utilization of alternative fuels, such as β-hydroxybutyrate and de novo synthesized glucose from fat-released glycerol. Regardless of sex and body condition, pups tended to adopt a convergent strategy of extreme energy and lean body mass conservation that appears highly adaptive for it allows some tissue growth during the repeated episodes of prolonged fasting they experience throughout their development.

Phylogeny affects estimation of metabolic scaling in mammals

The relationship between body size and metabolic rate is a crucial issue in organismal biology and evolution. There has been considerable debate over whether the scaling exponent of the relationship is 0.75 (Kleiber’s Law) or 0.67. Here we show that determination of this exponent for mammals depends on both the evolutionary tree and the regression model used in the comparative analysis. For example, more recent molecular-based phylogenies tend to support a 0.67 exponent, whereas older phylogenies, mostly based on morphological data, suggest a 0.75 exponent. However, molecular phylogenies yield more variable results than morphological phylogenies and thus are not currently helping to resolve the issue.

Exploration strategies map along fast-slow metabolic and life-history continua in muroid rodents

1Personality is highly relevant to ecology and the evolution of fast–slow metabolic and life-history strategies. One of the most important personality traits is exploratory behaviour, usually measured on an animal introduced to a novel environment (e.g. open-field test).2Here, we use a unique comparative dataset on open-field exploratory behaviour of muroid rodents to test a key assumption of a recent evolutionary model, i.e. that exploration thoroughness is positively correlated to age at first reproduction (AFR). We then examine how AFR and exploratory behaviour are related to basal metabolic rate (BMR).3Inter-specific variation in exploratory behaviour was positively correlated with AFR. Both AFR and exploration behaviour were negatively correlated with BMR. These results remained significant when taking phylogeny into account.4We suggest that species occupying unproductive and unpredictable environments simultaneously benefit from high exploration, low BMR and delayed AFR because exploration increases the likelihood of finding scarce resources, whereas low BMR and delayed reproduction enhance survival during frequent resources shortages.5This study provides the first empirical evidence for a link between personality, life-history, phylogeny and energy metabolism at the inter-specific level. The superficial-thorough exploration continuum can be mapped along the fast–slow metabolic and life-history continua.

Testing dynamic variance-sensitive foraging using individual differences in basal metabolic rates of zebra finches

Social foragers can alternate between searching for food (producer tactic), and searching for other individuals that have located food in order to join them (scrounger tactic). Both tactics yield equal rewards on average, but the rewards generated by producer are more variable. A dynamic variance-sensitive foraging model predicts that social foragers should increase their use of scrounger with increasing energy requirements and/or decreased food availability early in the foraging period. We tested whether natural variation in minimum energy requirements (basal metabolic rate or BMR) is associated with differences in the use of producer–scrounger foraging tactics in female zebra finches Taeniopygia guttata. As predicted by the dynamic variance-sensitive model, high BMR individuals had significantly greater use of the scrounger tactic compared with low BMR individuals. However, we observed no effect of food availability on tactic use, indicating that female zebra finches were not variance-sensitive foragers under our experimental conditions. This study is the first to report that variation in BMR within a species is associated with differences in foraging behaviour. BMR-related differences in scrounger tactic use are consistent with phenotype-dependent tactic use decisions. We suggest that BMR is correlated with another phenotypic trait which itself influences tactic use decisions.

Individual and sex-specific differences in intrinsic growth rate covary with consistent individual differences in behaviour

1.The evolutionary causes of consistent individual differences in behavior are currently a source of debate. A recent hypothesis suggests that consistent individual differences in life-history productivity (growth and/or fecundity) may covary with behavioral traits that contribute to growth-mortality trade-offs, such as risk-proneness (boldness) and foraging activity (voraciousness). It remains unclear, however, to what extent individual behavioral and life-history profiles are set early in life, or are a more flexible result of specific environmental or developmental contexts that allow bold and active individuals to acquire more resources. 2.Longitudinal studies of individually housed animals under controlled conditions can shed light on this question. Since growth and behaviour can both vary within individuals (they are labile), studying between-individual correlations in behaviour and growth rate requires repeated scoring for both variables over an extended period of time. However, such a study has not yet been done. 3.Here, we repeatedly measured individual mass 7-times each, boldness 40-times each, and voracity 8-times each during the first four months of life on 90 individually-housed crayfish (Cherax destructor). Animals were fed ad-libitum, generating a context where individuals can express their intrinsic growth rate (i.e. growth capacity), but in which bold and voracious behaviour is not necessary for high resource acquisition (crayfish can and do hoard food back to their burrow). 4.We show that individuals that were consistently bold over time during the day were also bolder at night, were more voracious, and maintained higher growth rates over time than shy individuals. Independent of individual differences, we also observed that males were faster growing, bolder, and more voracious than females. 5.Our findings imply that associations between bold behaviour and fast growth can occur in unlimited food contexts where there is no necessary link between bold behaviour and resource acquisition - offering support for the 'personality- productivity' hypothesis. We suggest future research should study links between consistent individual differences in behaviour and life-history under a wider range of contexts, in order to shed light on the role of biotic and abiotic conditions in the strength, direction and stability of their covariance. This article is protected by copyright. All rights reserved.

Among- and within-individual correlations between basal and maximal metabolic rates in birds

The aerobic capacity model proposes that endothermy is a by-product of selection favouring high maximal metabolic rates (MMR) and its mechanistic coupling with basal metabolic rate (BMR). Attempts to validate this model in birds are equivocal and restricted to phenotypic correlations (rP), thus failing to distinguish among- and within-individual correlations (rind and re). We examined 300 paired measurements of BMR and MMR from 60 house sparrows before and after two levels of experimental manipulation - testosterone implants and immune challenge. Overall, repeatability was significant in both BMR (R=0.25±0.06) and MMR (R=0.52±0.06). Only the testosterone treatment altered the rP between BMR and MMR, which resulted from contrasting effects on rind and re. While rind was high and significant (0.62±0.22) in sham-implanted birds, re was negative and marginally non-significant (-0.15±0.09) in testosterone-treated birds. Thus, the expected mechanistic link between BMR and MMR was apparent, but only in birds with low testosterone levels.

Individual (co)variation in thermal reaction norms of standard and maximal metabolic rates in wild-caught slimy salamanders

Standard metabolic rate (SMR) and maximal metabolic rate (MMR) are fundamental measures in ecology and evolution because they set the scope within which animals can perform activities that directly affect fitness. In ectotherms, both SMR and MMR are repeatable over time when measured at a single ambient temperature (Ta). Many ectotherms encounter variable Ta from day to day and over their lifetime, yet it is currently unknown whether individual differences hold across an ecologically relevant range of Ta (i.e. thermal repeatability; RT). Moreover, it is possible that thermal sensitivity of SMR and MMR are important individual attributes, and correlated with one another, but virtually nothing is known about this at present. We measured SMR and MMR across an ecologically relevant Ta gradient (i.e. from 10 to 25 °C) in wild-caught salamanders (Plethodon albagula) and found that RT was significant in both traits. SMR and MMR were also positively correlated, resulting in a lower RT in absolute and factorial aerobic scopes (AAS and FAS). We found significant individual differences in thermal sensitivity for both SMR and MMR, but not for AAS and FAS. The intercept (at Ta = 0 °C) and the slope of the thermal reaction norms were negatively correlated; individuals with low MR at low Ta had a higher thermal sensitivity. Finally, individuals with a high thermal sensitivity for SMR also had high thermal sensitivity for MMR. Our results suggest that natural selection occurring over variable Ta may efficiently target the overall level of - and thermal sensitivity in - SMR and MMR. However, this may not be the case for metabolic scopes, as the positive correlation between SMR and MMR, in addition to their combined changes in response to Ta, yielded little individual variation in AAS and FAS. Our results support the idea that organisms with low metabolism at low Ta have a high metabolic thermal sensitivity as a compensatory mechanism to benefit in periods of warmer environmental conditions. Hence, our study reveals the importance of considering within-individual variation in metabolism, as it may represent additional sources of adaptive (co)variation.

High basal metabolic rates of shorebirds while in the Arctic: a circumpolar view

The basal metabolic rate (BMR) of Old World long-distance-migrant shorebirds has been found to vary along their migration route. On average, BMR is highest in the Arctic at the start of fall migration, intermediate at temperate latitudes, and lowest on the tropical wintering grounds. As a test of the generality of this pattern, we measured the BMR of one adult and 44 juvenile shorebirds of 10 species (1-18 individuals of each species, body-mass range 19-94 g) during the first part of their southward migration in the Canadian Arctic (68-76°N). The interspecific relationship between BMR and body mass was almost identical to that found for juvenile shorebirds in the Eurasian Arctic (5 species), although only one species appeared in both data sets. We conclude that high BMR of shorebirds in the Arctic is a circumpolar phenomenon. The most likely explanation is that the high BMR reflects physiological adaptations to low ambient temperatures. Whether the BMR of New World shorebirds drops during southward migration remains to be investigated.

A 'slow pace of life' in Australian old-endemic passerine birds is not accompanied by low basal metabolic rates

Life history theory suggests that species experiencing high extrinsic mortality rates allocate more resources toward reproduction relative to self-maintenance and reach maturity earlier ('fast pace of life') than those having greater life expectancy and reproducing at a lower rate ('slow pace of life'). Among birds, many studies have shown that tropical species have a slower pace of life than temperate-breeding species. The pace of life has been hypothesized to affect metabolism and, as predicted, tropical birds have lower basal metabolic rates (BMR) than temperate-breeding birds. However, many temperate-breeding Australian passerines belong to lineages that evolved in Australia and share 'slow' life-history traits that are typical of tropical birds. We obtained BMR from 30 of these 'old-endemics' and ten sympatric species of more recently arrived passerine lineages (derived from Afro-Asian origins or introduced by Europeans) with 'faster' life histories. The BMR of 'slow' temperate-breeding old-endemics was indistinguishable from that of new-arrivals and was not lower than the BMR of 'fast' temperate-breeding non-Australian passerines. Old-endemics had substantially smaller clutches and longer maximal life spans in the wild than new arrivals, but neither clutch size nor maximum life span was correlated with BMR. Our results suggest that low BMR in tropical birds is not functionally linked to their 'slow pace of life' and instead may be a consequence of differences in annual thermal conditions experienced by tropical versus temperate species.