Relative longevity and field metabolic rate in birds

Metabolism is a defining feature of all living organisms, with the metabolic process resulting in the production of free radicals that can cause permanent damage to DNA and other molecules. Surprisingly, birds, bats and other organisms with high metabolic rates have some of the slowest rates of senescence begging the question whether species with high metabolic rates also have evolved mechanisms to cope with damage induced by metabolism. To test whether species with the highest metabolic rates also lived the longest I determined the relationship between relative longevity (maximum lifespan), after adjusting for annual adult survival rate, body mass and sampling effort, and mass-specific field metabolic rate (FMR) in 35 species of birds. There was a strongly positive relationship between relative longevity and FMR, consistent with the hypothesis. This conclusion was robust to statistical control for effects of potentially confounding variables such as age at first reproduction, latitude and migration distance, and similarity in phenotype among species because of common phylogenetic descent. Therefore, species of birds with high metabolic rates senesce more slowly than species with low metabolic rates.     

Metabolic level and size scaling of rates of respiration and growth in unicellular organisms

1.  Metabolic rate is conventionally assumed to scale with body mass to the 3/4-power, independently of the metabolic level of the organisms being considered. However, recent analyses in a variety of animals and plants indicate that the power (log–log slope) of this relationship varies significantly with metabolic level, ranging from c . 2/3 to 1.
2.  Here I show that the scaling slopes of rates of respiration and growth are related to the metabolic level of a variety of unicellular organisms, as similarly occurs for respiration rates in multicellular organisms.
3.  The recently proposed 'metabolic-level boundaries hypothesis' provides insight into these effects of metabolic level. As predicted, the scaling slopes for resting (endogenous) respiration rate in prokaryotes, algae and protozoans are negatively related to metabolic level; and in protozoans, the scaling slope increases with starvation. Also as predicted, the scaling slopes of growth rate in algae and protozoans are negatively related to growth level. Unexpectedly, opposite effects of starvation on the metabolic scaling slopes of unicellular prokaryotes (compared to that of eukaryotes) may be a spurious result of respiration measurements that did not adequately consider the effects of rapid cell multiplication in prokaryotes with extremely short generation times.
4.  Analyses of both unicellular and multicellular organisms show that there is no universal metabolic scaling relationship, and that variation in metabolic scaling relationships is systematically and possibly universally related to metabolic level.     

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.     

Corticosterone, locomotor performance, and metabolism in side-blotched lizards (Uta stansburiana)

Elevated levels of circulating corticosterone commonly occur in response to stressors in wild vertebrates. A rise in corticosterone, usually in animals of subordinate rank, results in a variety of effects on behavior and physiology. Behavioral and physiological responses to short-term increases in corticosterone are well studied. In contrast, the effects of chronic elevated levels of corticosterone are poorly understood, particularly in lizards. Here, we examined the long-term effects of exogenous corticosterone on locomotor performance, resting and active metabolic rate, and hematocrit in male side-blotched lizards Uta stansburiana. Corticosterone implantation resulted in higher levels of stamina relative to sham-surgery controls. In addition, lizards with elevated corticosterone exhibited lower resting metabolic rates relative to controls. Corticosterone had no effect on peak activity metabolism but did result in faster recovery times following exhaustive exercise. We suggest that elevated levels of corticosterone in response to dominance interactions promote enhanced locomotor abilities, perhaps as a flight response to avoid agonistic interactions. Furthermore, stressed lizards are characterized by lower resting metabolic rates, which may serve as strategy to conserve energy stores and enhance survival.     

Seasonal variation in metabolic rate of a medium-sized frugivore, the Knysna Turaco (Tauraco corythaix)

Many seasonal thermoregulation studies have been conducted on Holarctic birds that live in predictable, highly seasonal climates with severe winters. However, relatively few studies have been conducted on their southern hemisphere Afrotropical counterparts that encounter less predictable climates with milder winters. These latter birds are expected to conserve energy in winter by downregulating their metabolic rates. Therefore in this study, metabolic rate was measured during summer and winter in Knysna Turaco, Tauraco corythaix (Musophagiformes, Musophagidae) (c. 310 g), a non-passerine, in order to test whether there is energy conservation in winter. No overall significant differences in resting metabolic rates over a range of ambient temperatures were observed between winter and summer. However, whole-organism basal metabolic rates were 18.5% higher (p=0.005) in winter than in summer (210.83±15.97 vs. 186.70±10.52 O₂ h⁻¹). Knysna Turacos had broad thermoneutral zones ranging from 20 to 28 °C in winter and 10 to 30 °C in summer. These results suggest that Knysna Turacos show seasonal thermoregulatory responses that represent cold defense rather than energy conservation, which is contrary to what was expected.     

Do the high energy lifestyles of shorebirds result in high maximal metabolic rates? Basal and maximal metabolic rates in least and pectoral sandpipers during migration

Shorebirds have high resting and field metabolic rates relative to many other bird groups, and this is posited to be related to their high‐energy lifestyle. Maximum metabolic outputs for cold or exercise are also often high for bird groups with energetically demanding lifestyles. Moreover, shorebirds demonstrate flexible basal and maximal metabolic rates, which vary with changing energy demands throughout the annual cycle. Consequently, shorebirds might be expected to have high maximum metabolic rates, especially during migration periods. We captured least Calidris minutilla and pectoral C. melanotos sandpipers during spring and fall migration in southeastern South Dakota and measured maximal exercise metabolic rate (MMR; least sandpipers only), summit metabolic rate (M_sum, maximal cold‐induced metabolic rate) and basal metabolic rate (BMR, minimum maintenance metabolic rate) with open‐circuit respirometry. BMR for both least and pectoral sandpipers exceeded allometric predictions by 3–14%, similar to other shorebirds, but M_sum and MMR for both species were either similar to or lower than allometric predictions, suggesting that the elevated BMR in shorebirds does not extend to maximal metabolic capacities. Old World shorebirds show the highest BMR during the annual cycle on the Arctic breeding grounds. Similarly, least sandpiper BMR during migration was lower than on the Arctic breeding grounds, but this was not the case for pectoral sandpipers, so our data only partially support the idea of similar seasonal patterns of BMR variation in New World and Old World shorebirds. We found no correlations of BMR with either M_sum or MMR for either raw or mass‐independent data, suggesting that basal and maximum aerobic metabolic rates are modulated independently in these species.     

Moult and basal metabolic costs in males of two subspecies of stonechats: the European Saxicola torquata rubicula and the East African S. t. axillaris

The circannual patterns in resting metabolic rate (RMR) of males of two subspecies of stonechats, the European Saxicola torquata rubicula and the East African S. t. axillaris, are compared. As the birds from the two subspecies were raised and kept under comparable laboratory conditions, differences in metabolic rate between the two subspecies had to be genetically determined. RMR peaked during moult in both subspecies. During the rest of the year RMR was fairly constant in both subspecies and assumed to reflect basal metabolic rate (BMR). African stonechats had a 22% lower mass specific BMR than European stonechats, which is thought to reflect a genetical physiological adaptation to the differences in environmental circumstances they experience in the field. A low BMR makes an animal more susceptible to cold. Hence, the relatively high plumage mass in the African compared to the European stonechat may be functionally linked to its relatively low BMR. Moult costs, calculated from the plumage masses and the differences in RMR inside and outside the moult period, tended to be higher in the European compared to the African stonechats. These data and an interspecific comparison of moult costs over various species of birds support the earlier notion by Lindström et al. (1993) that moult costs are more closely linked with BMR than with body mass or rate of moult. The relation between moult costs and BMR and the fact that the efficiency of moult is extremely low (3.8 and 6.4% for European and African stonechats, respectively) suggest that the maintenance of specific tissues necessary for moult is a large cost factor. Alternatively, impaired insulation during moult may necessitate an increased metabolic capacity which may be associated with an increased RMR.     

Is respirometry a standardized technique? A review of measurement of avian resting metabolic rates

A plethora of studies have been conducted since the 1920s on avian thermoregulatory physiology variables as measured using respirometry. In particular, many of these studies have determined basal metabolic rate in a wide array of avian taxa. Start time of experiment, duration of experiment, length and number of measurements to determine the resting metabolic rate at a particular temperature (RMR_Ta) were reviewed in avian metabolic studies prior to 2011. Although respirometry is considered a standard technique, it was evident that in avian studies there is a continuum of duration time used for measurements with a number of studies (30%) using only 1–2 h data collection while at the other end of the continuum a number of studies (22%) have used 9–15 h data collection (and some longer). Many studies are unclear in how many hours were used (22%) to collect data. We found that most avian studies (94%) were on postabsorptive birds and most were during the birds' rest phase (69.5%). The majority (62.6%) of studies only measured metabolic rate at one temperature per trial, while others (19.2%) have measured RMR_Ta at various temperatures within a single trial period. Recently, several studies have shown that for diurnal birds measurements need to be conducted during the scotophase, for the duration of the night (>9 h; except at extreme temperatures where evaporative water loss is high and may result in mortalities), and at one experimental temperature per night if reliable and precise data are to be obtained. In addition, repeated measures need to be stable for at least an hour to be considered as RMR_Ta. Consequently, given the variance in methods used in prior avian metabolic studies cognizance of this is required when designing and implementing avian thermoregulatory physiological measurements using respirometry, particularly if data are later used for comparative allometric studies.     

Lower body mass and higher metabolic rate enhance winter survival in root voles,Microtus oeconomus

Although the biological significance of individual variation in physiological traits is widely recognized, studies of their association with fitness in wild populations are surprisingly scarce. We investigated the effect of individual phenotypic variation in body mass, resting (RMR) and peak metabolic rates (PMR) on mortality of the root vole Microtus oeconomus. Body mass and metabolic rates varied significantly among consecutive years and were also age dependent, as individuals born in late summer and autumn were characterized by significantly lower body mass and metabolic rates than animals born earlier. At the beginning of winter voles born in spring and early summer exhibited reduced body mass and metabolic rates, whereas animals born later maintained lower body mass and RMR, which may be interpreted as phenotypic plasticity enhancing the probability of survival. Body mass had no significant effect on vole survival during summer. In contrast, smaller individuals were characterized by lower mortality during early winter, whereas higher body mass was positively associated with survival later in the season. High body‐mass‐corrected RMR positively affected survival in both summer and winter. The effect of PMR was apparent only during winter, though its direction (and correlation with RMR) varied among years. Deep snow cover negatively affected the survival of voles in both early and late winter. Ambient temperature was positively associated with winter survival, except for late winter, when rising temperature caused flooding of vole habitat. We conclude that the lack of consistency in the directionality and strength of the effects of body mass and metabolic rates on winter survival does not undermine their importance, but rather demonstrates the ability of individuals to adjust metabolic rate to changing environmental conditions. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 297–309.     

Inbreeding depression in the effects of body mass on energy use

Large organisms have higher metabolic rates than small organisms but, if we compare their relative metabolic rates (i.e. per gram of tissue), this relationship is very often reversed. The pervasiveness of this phenomenon, called metabolic scaling, has attracted several theoretical explanations, and also produced lingering debate over whether metabolic scaling is a physically constrained and universally constant phenomenon or a more variable and evolutionarily malleable trait. To bring novel insights to this debate, we manipulated male Gryllodes sigillatus crickets' coefficients of inbreeding to determine whether metabolic scaling is sensitive to the manipulation of genetic quality. Because inbreeding depression is inversely related to past selection, our results indicate that selection has favoured an overall lower metabolic rate and a less steep slope of metabolic scaling. Altered metabolic scaling as a result of inbreeding was found to be caused by increased variation in metabolic rate, suggesting the existence of balancing selection towards intermediate metabolic rates. Although we found effects of inbreeding on metabolic scaling, much of the relationship between body mass and metabolic rate remained unexplained, leaving plenty of room for speculation concerning the fixed constraints that might affect evolutionary trajectories. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 309–317.     

长爪沙鼠的代谢率与器官的关系

我们测定了野生长爪沙鼠（Meriones unguiculatus)的基础代谢率和冷诱导的最大代谢率,分析了动物体内11种器官或组织的大小与代谢率的关系。长爪沙鼠的基础代谢率为118.10mlO2/h,最大代谢率为659.83mlO2/h。经过残差分析表明,基础代谢率并不与任何一种器官或组织相关,而最大代谢率与小肠湿重（n=20,r=-0.478,P=0.033)和消化道全长（n=20,r=-0.487,P=0.030)显著相关,表明体内器官重量的差别并不是造成种内基础代谢率差别的原因;体内存在着与最大代谢率相关的“代谢机器”,消化系统（特别是小肠）是这一代谢机器的重要组成部分,但代谢机器的大小并不能通过基础代谢率反映出来。基础代谢率与最大代谢率不相关,因此不支持“较高的基础代谢率能够产生较高的非基础代谢率（最大代谢率等）”的假设。     

Energetic cost of calling: general constraints and species‐specific differences

The energetic cost of acoustic signalling varies tremendously among species. Understanding factors responsible for this heterogeneity is important for understanding the costs and benefits of signalling. Here, we present a general model, based on well‐established principles of bioenergetics, which predicts the energetic cost of call production across species. We test model predictions using an extensive database of resting and calling metabolic rates of insects, amphibians and birds. Results are largely supportive of model predictions. Calling metabolic rates scale predictably with body mass and temperature such that calling and resting metabolic rates are directly proportional to each other. The cost of acoustic signalling is ～8 times higher than resting metabolic rate in ectotherms, and ～2 times higher in birds. Differences in the increase in metabolic rate during calling are explained by the relative size of species’ sound‐producing muscles. Combined with published work, we quantify call efficiency and discuss model implications.     

Gene or Size: Metabolic Rate and Body Temperature in Obese Growth Hormone‐Deficient Dwarf Mice

Objective: SMA1 mice carry a missense mutation in the growth hormone gene that leads to semidominant dwarfism and obesity. In this study, the basic thermal and metabolic properties of SMA1 mice were examined to detect metabolic alterations that can support the accretion of excess fat. Research Methods and Procedures: Basal and resting metabolic rates (RMRs) in wild‐type and SMA1 (sma1/+ and sma1/sma1) mice were determined by indirect calorimetry. Body temperature (T_b) was recorded using intraperitoneally implanted temperature‐sensitive transmitters, and body composition was determined by DXA. Results: SMA1 mice have proportionally lower basal and resting metabolic rates, higher body mass (BM)‐specific RMRs, and a higher lower critical temperature, and display a decrease in T_b by 0.4 °C in sma1/+ and 0.9 °C in sma1/sma1. Discussion: The analysis of gene effects on BM and energy expenditure in mouse mutants must consider the appropriate allometric relationship between BM and metabolic rate. With the exception of T_b, all metabolic alterations observed in SMA1 reflect reduced size.     

Individual variation and repeatability of the aerobic performance in Brandt's voles (Lasiopodomys brandtii)

Metabolism is thought to play an important role in shaping behaviour, ecology and physiology in animals. To study the changes of metabolism among different ages or generations as well as the repeatability during the ontogeny, we carried out the research in Brandt's voles (Lasiopodomys brandtii), which covered two generations’ life. Meanwhile, we estimated the among-family variations to facilitate the heritability evaluation. Resting metabolic rate within the thermoneutral zone, resting metabolic rate at 5 °C, non-shivering thermogenesis and maximal metabolic rate during thermogenesis in both juveniles and adults were simultaneously measured. Population-average values of aerobic traits were generally consistent among different ages or generations; however, there was no repeatability at the level of individual variation during the ontogeny, which indicated that the aerobic traits of the young were not good indicators for that of later life. At the same time, the coefficient of intraclass correlation for full sibs failed to reach statistical significance, suggesting that heritability of aerobic traits in Brandt's voles was not high.     

温州地区4种雀形目鸟类基础代谢率与器官重量的相关性分析

动物代谢率存在差异的原因及其意义是进化牛理学上的一个核心问题.为了解代谢率的影响因素和功能意义,测定了红头长尾山雀Aegithalos concinnus、白头鹎Pycnonotus sinensis、丝光椋鸟Stumus sericeus和小鸦Emberi-za pusilla的基础代谢率,分析了动物体内的8种器官或者组织的大小与代谢率的关系.结果显示,基础代谢率与脑、肝脏,.肾脏、胃、小肠和总消化道干重(胃、小肠与直肠的干重之和)相关显著.     

Comparing a bioenergetics model with feeding rates of caged European starlings

We tested a bioenergetics model integrated within a mortality model that estimates numbers of European starlings (Sturnus vulgaris) poisoned with the avicide, Compound DRC-1339 Concentrate. The bioenergetics model predicted daily metabolic rate. Accuracy and reliability of this variable is critical because other algorithms (e.g., toxicity regressions, feeding behavior) in the mortality model depend on metabolic rate to calculate the amount of DRC-1339 ingested per bird. We tested the bioenergetics model by comparing its estimates of metabolic rate with those generated from measuring feeding rates of caged starlings during a feeding trial conducted outdoors during January 2008. Over the 12-day feeding trial, daily feeding rates of caged starlings indicated that metabolic rates ranged from 157 kJ/bird per day to 305 kJ/bird per day. The bioenergetics model predicted metabolic rates ranging from 208 kJ/bird per day to 274 kJ/bird per day. There was no difference between these 2 independently derived estimates of daily metabolic rate (paired t-test: t₍₁₁₎ = 1.4, P = 0.18). Using 95% confidence intervals calculated from variation of feeding rates among cages (n = 4, 6 birds/cage), the bioenergetics model's estimates were within 95% confidence intervals on 9 of 12 days and greater than the upper 95% confidence interval on 3 days. Daily estimates of metabolic rate were directly correlated between the bioenergetics model and the feeding-rate model (r₁₂ = 0.57, P = 0.05). A broad range of temperatures (−17°C to 14°C), wind speeds (0–40 km/hr), and percent cloud cover (0–100%) were encountered during the feeding trial. The bioenergetics model's predictions appeared robust to varying meteorological conditions typical of winters in middle latitudes of the interior United States. Compound DRC-1339 Concentrate is used by USDA Wildlife Services to manage chronic infestations of starlings at livestock facilities, which occur mainly during fall and winter. Compared to other methods used for estimating DRC-1339 mortality (e.g., counting birds pre- and posttreatment), bioenergetics modeling should improve the mortality model's overall accuracy and precision. © The Wildlife Society, 2011     

The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions

Summit metabolic rate ( M_sum , maximum cold-induced metabolic rate) is positively correlated with cold tolerance in birds, suggesting that high M_sum is important for residency in cold climates. However, the phylogenetic distribution of high M_sum among birds and the impact of its evolution on current distributions are not well understood. Two potential adaptive hypotheses might explain the phylogenetic distribution of high M_sum among birds. The cold adaptation hypothesis contends that species wintering in cold climates should have higher M_sum than species wintering in warmer climates. The flight adaptation hypothesis suggests that volant birds might be capable of generating high M_sum as a byproduct of their muscular capacity for flight; thus, variation in M_sum should be associated with capacity for sustained flight, one indicator of which is migration. We collected M_sum data from the literature for 44 bird species and conducted both conventional and phylogenetically informed statistical analyses to examine the predictors of M_sum variation. Significant phylogenetic signal was present for log body mass, log mass-adjusted M_sum , and average temperature in the winter range. In multiple regression models, log body mass, winter temperature, and clade were significant predictors of log M_sum . These results are consistent with a role for climate in determining M_sum in birds, but also indicate that phylogenetic signal remains even after accounting for associations indicative of adaptation to winter temperature. Migratory strategy was never a significant predictor of log M_sum in multiple regressions, a result that is not consistent with the flight adaptation hypothesis.     

Competitive ability is related to metabolic asymmetry in juvenile rainbow trout

Of 55 size–matched pairs of juvenile rainbow trout Oncorhynchus mykiss , each consisting of one high and one low relative metabolic rate fish (relative size difference <5%), the high relative metabolic rate fish was dominant in 36 pairs (65·5%), significantly more often than expected by chance. The probability of a fish winning was related to its relative metabolic rate (measured prior to introduction into the test arena); the higher the relative metabolic rate of a fish compared to its opponent, the greater its probability of being dominant. In the 36 pairs of fish where the low relative metabolic rate fish was the subordinate, its competitive ability was significantly correlated with how closely the two fish were matched in terms of their relative metabolic rates. The smaller the difference between the relative metabolic rates of the dominant high relative metabolic rate fish and subordinate low metabolic rate fish, the greater the competitive ability and feeding success of the low relative metabolic rate subordinate. However, no such relation was found in the 19 pairs of fish where the high relative metabolic rate fish was the subordinate. In these pairs, the competitive ability of the subordinate high relative metabolic rate fish was correlated with its size relative to its dyad partner. The larger the dominant low relative metabolic rate fish, the lower the competitive ability of the subordinate high relative metabolic rate fish.     

Role of the melanocortin-4 receptor in metabolic rate and food intake in mice

We evaluated the role of the melanocortin-4 receptor (MC-4R) in the control of metabolic rate and food intake in mice. Intraperitoneal administration of the non-selective MC-R agonist melanotan II (MT-II; a cyclic heptapeptide) increases metabolic rate in wildtype mice, while MC-4R knockout mice are insensitive to the effects of MT-II on metabolic rate. MC-4R knockout mice are also insensitive to the effects of MT-II on reducing food intake. We conclude that MC-4R can mediate control of both metabolic rate and food intake in mice. We infer that a role for MC-3R in mediating the acute effects of MT-II on basal metabolic rate and food intake in wildtype mice seems limited.     

Heritability of flight and resting metabolic rates in the Glanville fritillary butterfly

Dispersal capacity is a key life‐history trait especially in species inhabiting fragmented landscapes. Evolutionary models predict that, given sufficient heritable variation, dispersal rate responds to natural selection imposed by habitat loss and fragmentation. Here, we estimate phenotypic variance components and heritability of flight and resting metabolic rates (RMRs) in an ecological model species, the Glanville fritillary butterfly, in which flight metabolic rate (FMR) is known to correlate strongly with dispersal rate. We modelled a two‐generation pedigree with the animal model to distinguish additive genetic variance from maternal and common environmental effects. The results show that FMR is significantly heritable, with additive genetic variance accounting for about 40% of total phenotypic variance; thus, FMR has the potential to respond to selection on dispersal capacity. Maternal influences on flight metabolism were negligible. Heritability of flight metabolism was context dependent, as in stressful thermal conditions, environmentally induced variation dominated over additive genetic effects. There was no heritability in RMR, which was instead strongly influenced by maternal effects. This study contributes to a mechanistic understanding of the evolution of dispersal‐related traits, a pressing question in view of the challenges posed to many species by changing climate and fragmentation of natural habitats.