Resting energy metabolism of Goeldi's monkey (Callimico goeldii) is similar to that of other callitrichids

The resting metabolic rates (RMRs) of six adult Goeldi's monkeys (Callimico goeldii) were measured using standard methods of open circuit respirometry during both the active (daytime) and inactive (nighttime) circadian phases for this species. One subject was measured both while she was pregnant and after she delivered a full-term, stillborn infant. Inactive-phase RMR within thermal neutrality (above 27.5 degrees C) averaged 288.5 +/- 30.8 ml O2/hr; active-phase RMR within thermal neutrality averaged 416.3 +/- 60.9 ml O2/hr. These values are 74.6% and 107.6%, respectively, of the mammalian expected for animals of this body mass. During the inactive phase, metabolic rate increased an estimated 4.3% for every degree decline in temperature below 27.5 degrees C. The RMR in Goeldi's monkey is similar quantitatively and qualitatively to those of other captive callitrichids that have been studied, with active-phase RMR being at or slightly above the mammalian expected, and inactive-phase RMR being significantly reduced. We propose that this circadian pattern of RMR is a consequence of small body size, and is not a specific metabolic adaptation within the Callitrichidae. Thus we predict that metabolic studies measuring both circadian phases in other small primates will also find this pattern of reduced RMR during the inactive phase. The inactive-phase RMR within thermal neutrality of the pregnant female was not different from that measured after the stillbirth, despite an almost 15% difference in body mass. During pregnancy, however, the female was more metabolically responsive to temperature below thermal neutrality, and had a lower upper critical temperature (i.e., was less tolerant of heat).     

Energetics and life-history of bats in comparison to small mammals

Mammals can be aligned along a slow-fast life-history continuum and a low–high metabolic rate continuum based on their traits. Small non-volant mammals occupy the fast/high end in both continua with high reproductive rates and short life spans linked with high mass-specific metabolic rates. Bats occupy the high end of the metabolic continuum, but the slow end of the life-history continuum with low reproductive rates and long life spans. Typically, both continua are linked, and similar life-history traits of species are reflected in more similar metabolic rates. We therefore hypothesized that metabolic rates are similar in species with similar life-history traits. Resting metabolic rates (RMR) were measured for three ecologically and morphologically similar sympatric bat species (Myotis nattereri, M. bechsteinii, and Plecotus auritus; Vespertilionidae) and compared to data from other similar-sized, temperate insectivorous mammals with other life-history strategies. The bat species share similar life-histories and RMRs, both of which differ from the remaining mammals and therefore supporting our hypothesis. To verify that bats are similar in RMR, two energetically contrasting periods were compared. RMRs in post-lactating females did not differ between bat species. It was, however, positively correlated with parasite load in both Myotis species. However, RMRs differed during energy-demanding pregnancy where M. nattereri had the significantly lowest RMR, suggesting metabolic compensation as an energy-saving strategy. We conclude that the energy requirements of bat species with similar life-history traits resemble each other during periods of low energetic demands and are more similar to each other than to other small temperate mammals.     

Mitochondrial DNA variation in human metabolic rate and energy expenditure

The role of climate in driving selection of mtDNA as Homo sapiens migrated out of Africa into Eurasia remains controversial. We evaluated the role of mtDNA variation in resting metabolic rate (RMR) and total energy expenditure (TEE) among 294 older, community-dwelling African and European American adults from the Health, Aging and Body Composition Study. Common African haplogroups L0, L2 and L3 had significantly lower RMRs than European haplogroups H, JT and UK with haplogroup L1 RMR being intermediate to these groups. This study links mitochondrial haplogroups with ancestry-associated differences in metabolic rate and energy expenditure.     

Effects of environmental salinity and 17alpha-methyltestosterone on growth and oxygen consumption in the tilapia, Oreochromis mossambicus

Effects of environmental salinity and 17α-methyltestosterone (MT) on growth and oxygen consumption were examined in the tilapia, Oreochromis mossambicus. Yolk-sac fry were collected from brood stock in fresh water (FW). After yolk-sac absorption, they were assigned randomly to one of four groups: FW, MT treatment in FW, seawater (SW) and MT treatment in SW. All treatment groups were fed to satiation three times daily. The fish reared in SW (both control and MT-treated groups) grew significantly larger than either group in FW from day 43 throughout the experiment (195 days). The fish fed with MT added to their feed grew significantly larger than their respective controls from day 85 in FW and in SW until the end of the experiment. The routine metabolic rate (RMR) was determined monthly from month 2 (day 62) to month 5 (day 155). A significant negative correlation was seen between RMR and body mass in all treatment groups. Among fish of the same age, the SW-reared tilapia had significantly lower RMRs than the FW-reared fish. The MT-treated fish in SW showed significantly lower RMRs than the SW control group at months 3–5, whereas MT treatment in FW significantly increased the RMR at month 3. Comparison of regression lines between RMR and body mass indicates that MT treatment in FW caused a significant increase in oxygen consumption at a given mass of the fish, whereas MT treatment was without effect on RMR in SW-reared fish. These results clearly indicate that SW-rearing and MT treatment accelerate growth of tilapia, and that RMR decreases as fish size increased. It is also likely that the increased RMR and growth in MT-treated tilapia in FW may be due to the metabolic actions of MT, although the reason for the absence of MT treatment in SW is unclear.     

Metabolic and organ mass responses to selection for high growth rates in the domestic chicken (Gallus domesticus)

Evolutionary hypotheses suggest that higher rates of postembryonic development in birds should either lower the resting metabolic rate (RMR) in a trade-off between the costs of growth and maintenance or increase RMR because of a buildup of metabolic machinery. Furthermore, some suggest that higher rates of postembryonic development in birds should reduce peak metabolic rate (PMR) through delayed tissue maturation and/or an increased energy allocation to organ growth. We studied this by comparing metabolic rates and organ sizes of fast-growing meat-type chickens (broilers) with those of birds from a laying strain, which grow much slower. During the first week of life, despite growing six times faster, the RMR of the broiler chickens was lower than that of birds of the laying strain. The difference between strains in RMR disappeared thereafter, even though broilers continued to grow twice as fast as layers. The differences between strains in growth rate during the first week after hatching were not reflected in similar differences in the relative masses of the heart, liver, and small intestine. However, broilers had heavier intestines once they reached a body mass of 80 g. In contrast, broilers had relatively smaller brains than did layers. There was a positive correlation, over both strains, between RMR and the masses of leg muscles, intestine, and liver. Furthermore, despite delayed maturation of muscle tissue, broilers exhibited significantly higher PMR. We hypothesize that a balance between the larger relative muscle mass but lower muscle maturation level explains this high PMR. Another correlation, between leg muscle mass and PMR, partly explained the positive correlation between RMR and PMR.     

Relationships between bone growth rate, body mass and resting metabolic rate in growing amniotes: a phylogenetic approach

We explored the factors that explain the variation in resting metabolic rates (RMR) in growing amniotes by using the phylogenetic comparative method. For this, we measured raw RMR (mL O₂ h⁻¹), body mass, body mass growth rate, and periosteal bone growth rate in a sample of 44 growing individuals belonging to 13 species of amniotes. We performed variation partitioning analyses, which showed that phylogeny explains a significant fraction of the variation of mass-specific RMR (mL O₂ h⁻¹ g⁻¹), and that the cost of growth is much higher than the cost of maintenance. Moreover, we tested the hypothesis of the independence of energy allocation, and found that maintenance metabolism and growth rates are not significantly related. Finally, we calculated the statistical parameters of the relationship between geometry-corrected RMR (mL O₂ h⁻¹ g^−0.67) and bone growth rate. This relationship could potentially be used in palaeobiology to infer RMR from bone tissue samples of fossil species by assuming Amprino's rule (according to which bone tissue types reflect bone growth rates). These estimates would be especially interesting for Mesozoic non-avian theropod dinosaurs and Permian and Triassic therapsids to investigate, respectively, the origin of avian and mammalian endothermy.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 63–76.     

Does growth rate determine the rate of metabolism in shorebird chicks living in the Arctic?

We measured resting and peak metabolic rates (RMR and PMR, respectively) during development of chicks of seven species of shorebirds: least sandpiper (Calidris minutilla; adult mass 20-22 g), dunlin (Calidris alpina; 56-62 g), lesser yellowlegs (Tringa flavipes; 88-92 g), short-billed dowitcher (Limnodromus griseus; 85-112 g), lesser golden plover (Pluvialis dominicana; 150-156 g), Hudsonian godwit (Limosa haemastica; 205-274 g), and whimbrel (Numenius phaeopus; 380 g). We tested two opposing hypotheses: the growth rate-maturity hypothesis, which posits that growth rate in chicks is inversely related to functional maturity of tissues, and the fast growth rate-high metabolism hypothesis, which suggests that rapid growth is possible only with a concomitant increase in either RMR or PMR. We have found no evidence that chicks of shorebirds with fast growth rates have lower RMRs or lower PMRs, as would be predicted by the growth rate-maturity hypothesis, but our data suggested that faster-growing chest muscles resulted in increased thermogenic capacity, consistent with the fast growth-high metabolism hypothesis. The development of homeothermy in smaller species is a consequence primarily of greater metabolic intensities of heat-generating tissues. The maximum temperature gradient between a chick's body and environment that can be maintained in the absence of a net radiative load increased rapidly with body mass during development and was highest in least sandpipers and lowest among godwits. Chicks of smaller species could maintain a greater temperature gradient at a particular body mass because of their higher mass-specific maximum metabolic rates.     

Effects of body mass,temperature, and season on resting metabolism of the nocturnal gecko Hemidactylus flaviviridis

Abstract

The resting metabolic rate (RMR) of Hemidactylus flaviviridis was measured at different temperatures from 20 to 35°C during winter and summer acclimatization. The mass exponent b values ranged between 0.67 and 0.72. Winter-acclimatized geckos of various body masses had significantly lower RMRs than summer-acclimatized geckos only at 20°C. It seems that low thermal sensitivity for summer–acclimatized group may facilitate activity during its active seasons, and high thermal sensitivity between 20 and 25°C for winter–acclimatized group may conserve energy during inactivity in winter.     

Inter-sexual differences in resting metabolic rates in the Texas tarantula, Aphonopelma anax

Intra-specific variation in life history and mating strategies can lead to differences in energy allocation and expenditure in males and females. This may, in turn, explain large-scale evolutionary patterns. In this study, I investigated the effects of body mass, temperature and sex on resting metabolic rates (RMRs) in sexually mature male and female tarantulas (Aphonopelma anax (Chamberlin)), a species that exhibits extreme inter-sexual differences in life history after reaching sexual maturity. RMRs were measured as rates of CO(2) production in an open-flow respirometry system at 20, 25, 30 and 35 degrees C. These temperatures are typical to what this species experiences under natural conditions. In addition, a respiratory quotient (RQ) of 0.92 was calculated from rates of CO(2) production and O(2) consumption in a closed, constant-volume respirometry system. As expected, RMRs increased with increasing temperature and body mass. However, after adjusting for the influence of body mass, males had substantially higher metabolic rates than females at each temperature. This higher metabolic rate is proposed as an adaptive strategy to support higher energetic demands for males during their active, locomotory search for females during the mating season.     

The effects of norepinephrine and nutritional status on resting metabolic rates in the LA/N-cp rat

1. The effects of diet and norepinephrine (NE) on resting metabolic rate (RMR) were determined using indirect calorimetry in 6-month-old lean and corpulent LA/N-cp rats. RMRs of lean rats were greater than the corpulent. 2. Ingestion of carbohydrate (CHO) in the unfasted and fasted states increased the RMR of both groups, especially in the lean phenotype when compared to oil. 3. Serum T3 and glucose concentrations were similar in both phenotypes. 4. The effects of NE on RMR were maximal after a 200 micrograms NE/kg body weight injections.     

Is resting metabolic rate related to reproductive output in an orb-web spider,Argiope radon?

1. Resting metabolic rate (RMR) is a fundamental feature of animal biology that reflects the baseline level of energy expenditure. There are two main strategies that can address energy demands; animals can reallocate energy from maintenance by reducing RMR to meet energy demands (compensation model) or they can increase intake rate by increasing metabolic activities (performance model). 2. Orb-web spiders are sit-and-wait foragers that typically reside at the centre of their web waiting to intercept prey. Given their sedentary resource acquisition strategy, it is predicted that lower RMR is favoured to reduce self-maintenance energetic costs and to allow greater allocation to oogenesis (i.e., egg sac development). 3. In this study, we tested temporal variation in RMR of female Argiope radon (Araneae: Araneidae) spiders in response to mating status. Then we tested the degree to which between-individual variation in the parental RMR relates to reproductive output and spiderling early life-history traits. 4. Despite the notable between-individual variation, we found a temporal consistency of RMR in the female spiders at early adulthood. Mated females significantly reduced their RMR by around 35% compared to their unmated stage which supports compensation model. However, there was a significant correlation between female RMR and mass of the egg sac in these spiders which is an evidence for performance model. 5. Our findings suggest that energy management in this species is a complex phenomenon, both strategies are in effect simultaneously at within- and between-individual level shaping the individuals' phenotype.     

Fast molecular evolution associated with high active metabolic rates in poison frogs

Molecular evolution is simultaneously paced by mutation rate, genetic drift, and natural selection. Life history traits also affect the speed of accumulation of nucleotide changes. For instance, small body size, rapid generation time, production of reactive oxygen species (ROS), and high resting metabolic rate (RMR) are suggested to be associated with faster rates of molecular evolution. However, phylogenetic correlation analyses failed to support a relationship between RMR and molecular evolution in ectotherms. In addition, RMR might underestimate the metabolic budget (e.g., digestion, reproduction, or escaping predation). An alternative is to test other metabolic rates, such as active metabolic rate (AMR), and their association with molecular evolution. Here, I present comparative analyses of the associations between life history traits (i.e., AMR, RMR, body mass, and fecundity) with rates of molecular evolution of and mitochondrial loci from a large ectotherm clade, the poison frogs (Dendrobatidae). My results support a strong positive association between mass-specific AMR and rates of molecular evolution for both mitochondrial and nuclear loci. In addition, I found weaker and genome-specific covariates such as body mass and fecundity for mitochondrial and nuclear loci, respectively. No direct association was found between mass-specific RMR and rates of molecular evolution. Thus, I provide a mechanistic hypothesis of the link between AMRs and the rate of molecular evolution based on an increase in ROS within germ line cells during periodic bouts of hypoxia/hyperoxia related to aerobic exercise. Finally, I propose a multifactorial model that includes AMR as a predictor of the rate of molecular evolution in ectothermic lineages.     

Geographic variation in basal thermogenesis in little buntings: Relationship to cellular thermogenesis and thyroid hormone concentrations

Acclimatization to different ambient conditions is an essential prerequisite for survival of small passerine birds. Long-distance migration and winter acclimatization induce similar physiological and biochemical adjustments in passerines. To understand metabolic adaptations, the resting metabolic rate (RMR), the thermogenic properties of mitochondria in liver and muscle, and the activity of thyroid hormones were examined in field-captured little buntings (Emberiza pusilla) between Southeastern (Wenzhou) and Northeastern (Qiqihar) China from March to May in 2008 during their migration. Twelve birds were trapped from March to April in Wenzhou region, Zhejiang Province (27°29′N, 120°51′E) and eleven birds originated from April to May in Qiqihar region, Heilongjiang Province (47°29′N, 124°02′E). We found that RMRs of little buntings were significantly higher in Qiqihar than in Wenzhou. Consistently, mitochondrial state-4 respiration capacities and cytochrome c oxidase activities (COX) in liver and muscle, and circulating levels of plasma triiodothyronine (T₃) of little buntings were also significantly higher in Qiqihar than in Wenzhou. Variation in metabolic biochemical markers of liver and muscle, such as state-4 respiration and COX, and variation in thyroid hormone levels were correlated with variation in RMR. There was also a positive relationship between T₃ and metabolic biochemical markers. Little buntings mainly coped with a cold environment by enhancing thermogenic capacities through enhanced respiratory enzyme activities and plasma T₃. These results support the view that the primary means by which small birds meet energetic challenges of cold conditions is through metabolic adjustments.     

Limited mass‐independent individual variation in resting metabolic rate in a wild population of snow voles (Chionomys nivalis)

Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass‐independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long‐term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni‐ and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass‐dependent and mass‐independent components, while accounting for measurement error. RMR varies among individuals, that is, is repeatable (R = .46) and strongly co‐varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass‐independent RMR is reduced by 41% to R = .27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error and decompose the relative importance of mass‐dependent and mass‐independent physiological variation.     

Metabolic rate and food availability of the Antarctic amphipod <Emphasis Type="Italic">Gondogeneia antarctica</Emphasis> (Chevreux 1906): seasonal variation in allometric scaling and temperature dependence

Among the few existing works on seasonal variation in metabolic rate of polar species, most have been conducted during summer due to logistic constraints and have been focused on species that cease feeding during winter. In this work, we present the first extensive data set on the seasonal variation in metabolic rate of G. antarctica, an abundant amphipod that feeds throughout the year, and its relationship with body size, potential food availability and temperature. We measured the resting metabolic rate (RMR) of groups of individuals during 6 months from late summer through winter at 4 experimental temperatures and for a wide range of body size. RMR had a negative allometric scaling with body size and showed a tendency to increase with temperature as expected. However, temperature and body size effects on RMR showed a significant temporal variation, and an increase in temperature decreased scaling exponents. RMR at the mean seawater temperature throughout the study showed a strong seasonal variation following food availability: RMR decreased from the end of summer through winter, coinciding with a reduction in microphytobenthos stock, but recovered summer values in August, when an epontic algae boom occurred. The seasonal factorial aerobic scope (×2.37) is lower than benthic Antarctic invertebrates that cease feeding during winter, in agreement with what is expected based on theoretical grounds. Results suggest that seasonal variation of RMR would allow G. antarctica to achieve a high efficiency in energy utilization, while maintaining the ability to exploit sudden changes in food supply.     

Heritability of resting metabolic rate in a wild population of blue tits

We report the first study with the aim to estimate heritability in a wild population, a nest box breeding population of blue tits. We estimated heritability as well as genetic and phenotypic correlations of resting metabolic rate (RMR), body mass and tarsus length with an animal model based on data from a split cross‐fostering experiment with brood size manipulations. RMR and body mass, but not tarsus length, showed significant levels of explained variation but for different underlying reasons. In body mass, the contribution to the explained variation is mainly because of a strong brood effect, while in RMR it is mainly because of a high heritability. The additive variance in RMR was significant and the heritability was estimated to 0.59. The estimates of heritability of body mass (0.08) and tarsus length (0.00) were both low and based on nonsignificant additive variances. Thus, given the low heritability (and additive variances) in body mass and tarsus length the potential for direct selection on RMR independent of the two traits is high in this population. However, the strong phenotypic correlation between RMR and mass (0.643 ± 0.079) was partly accounted for by a potentially strong, although highly uncertain, genetic correlation (1.178 ± 0.456) between the two traits. This indicates that the additive variance of body mass, although low, might still somewhat constrain the independent evolvability of RMR.     

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.     

Ducklings exhibit substantial energy-saving mechanisms as a response to short-term food shortage

We investigated whether Pekin ducklings (Anas platyrhyncos domesticus) exhibited any energy-saving mechanisms that could lessen the detrimental effects of reduced food intake during early development. Further, we evaluated the role of body compositional changes behind such potential mechanisms and the consequences on thermoregulatory capacity. The ducklings exhibited substantial energy-saving mechanisms as a response to diet restriction. After 5 d of diet restriction, the resting metabolic rate (RMR) of 10- and 20-d-old ducklings was 16.4% and 32.1% lower, respectively, than predicted from body mass compared with ad lib. fed ducklings (controls). These reductions in RMR could have been adaptive responses in anticipation of a lasting food shortage, or they could have been consequences of the restricted diet and the lack of essential nutrients. We argue that the responses were adaptive. The low RMRs were not a consequence of depleted fuel stores because the diet-restricted ducklings exhibited substantial amounts of stored lipids at the end of the diet-restriction periods. Hypothermia accounted for approximately 50% of the reduction in RMR in the 10-d-old diet-restricted ducklings, but hypothermia did not occur in the 20-d-old diet-restricted ducklings. Diet restriction resulted in a reduced liver and intestine size and an unchanged size of the leg muscles and heart, while the length of the skull increased (compared with controls of a given body mass). However, changes in body composition were only minor predictors of the observed changes in RMR. Peak metabolic rate (PMR) was approximately 10% lower in the diet-restricted ducklings compared with the controls. We have interpreted the lower PMR as a consequence of the reductions in RMR rather than as a consequence of a decreased function of the thermoregulatory effector mechanisms.     

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.