The influence of foraging mode and arid adaptation on the basal metabolic rates of burrowing mammals

Two competing but nonexclusive hypotheses to explain the reduced basal metabolic rate (BMR) of mammals that live and forage underground (fossorial species) are examined by comparing this group with burrowing mammals that forage on the surface (semifossorial species). These hypotheses suggest that the low BMR of fossorial species either compensates for the enormous energetic demands of subterranean foraging (the cost-of-burrowing hypothesis) or prevents overheating in closed burrow systems (the thermal-stress hypothesis). Because phylogentically informed allometric analysis showed that arid burrowing mammals have a significantly lower BMR than mesic ones, fossorial and semifossorial species were compared within these groups. The BMRs of mesic fossorial and semifossorial mammals could not be reliably distinguished, nor could the BMRs of large (>77 g) arid fossorial and semifossorial mammals. This finding favours the thermal-stress hypothesis, because the groups appear to have similar BMRs despite differences in foraging costs. However, in support of the cost-of-burrowing hypothesis, small (<77 g) arid fossorial mammals were found to have a significantly lower BMR than semifossorial mammals of the similar size. Given the high mass-specific metabolic rates of small animals, they are expected to be under severe energy and water stress in arid environments. Under such conditions, the greatly reduced BMR of small fossorial species may compensate for the enormous energetic demands of subterranean foraging.     

Basal metabolic rate of birds is associated with habitat temperature and precipitation, not primary productivity

A classic example of ecophysiological adaptation is the observation that animals from hot arid environments have lower basal metabolic rates (BMRs, ml O2min-1) than those from non-arid (luxuriant) ones. However, the term 'arid' conceals within it a multitude of characteristics including extreme ambient temperatures (Ta, degrees C) and low annual net primary productivities (NPPs, gCm-2), both of which have been shown to correlate with BMR. To assess the relationship between environmental characteristics and metabolic rate in birds, we collated BMR measurements for 92 populations representing 90 wild-caught species and examined the relationships between BMR and NPP, Ta, annual temperature range (Tr), precipitation and intra-annual coefficient of variation of precipitation (PCV). Using conventional non-phylogenetic and phylogenetic generalized least-squares approaches, we found no support for a relationship between BMR and NPP, despite including species captured throughout the world in environments spanning a 35-fold range in NPP. Instead, BMR was negatively associated with Ta and Tr, and positively associated with PCV.     

Exploring individual quality: basal metabolic rate and reproductive performance in storm-petrels

Despite evidence that some individuals achieve both superiorreproductive performance and high survivorship, the factorsunderlying variation in individual quality are not well understood.The compensation and increased-intake hypotheses predict thatbasal metabolic rate (BMR) influences reproductive performance;if so, variation in BMR may be related to differences in individualquality. We evaluated whether BMR measured during the incubationperiod provides a proximate explanation for variation in individualquality by measuring the BMRs and reproductive performance ofLeach's storm-petrels (Oceanodroma leucorhoa) breeding on KentIsland, New Brunswick, Canada, during 2000 and 2001. We statisticallycontrolled for internal (body mass, breeding age, sex) and external(year, date, time of day) effects on BMR. We found that maleswith relatively low BMRs hatched their eggs earlier in the seasonand that their chicks' wing growth rates were faster comparedto males with relatively high BMRs. Conversely, BMR was notrelated to egg volume, hatching date, or chick growth rate forfemales or to lifetime (23 years) hatching success for eithersex. Thus, for males but not for females, our results supportthe compensation hypothesis. This hypothesis predicts that animalswith low BMRs will achieve better reproductive performance thananimals with high BMRs because they have lower self-maintenancecosts and therefore can apportion more energy to reproduction.These results provide evidence that intraspecific variationin reproductive performance is related to BMR and suggest thatBMR may influence individual quality in males.     

Ecological factors affect the level and scaling of avian BMR

The basal rate of metabolism (BMR) in 533 species of birds, when examined with ANCOVA, principally correlates with body mass, most of the residual variation correlating with food habits, climate, habitat, a volant or flightless condition, use or not of torpor, and a highland or lowland distribution. Avian BMR also correlates with migratory habits, if climate and a montane distribution is excluded from the analysis, and with an occurrence on small islands if a flightless condition and migration are excluded. Residual variation correlates with membership in avian orders and families principally because these groups are behaviorally and ecologically distinctive. However, the distinction between passerines and other birds remains a significant correlate of avian BMR, even after six ecological factors are included, with other birds having BMRs that averaged 74% of the passerine mean. This combination of factors accounts for 97.7% of the variation in avian BMR. Yet, migratory species that belong to Anseriformes, Charadriiformes, Pelecaniformes, and Procellariiformes and breed in temperate or polar environments have mass-independent basal rates equal to those found in passerines. In contrast, penguins belong to an order of polar, aquatic birds that have basal rates lower than passerines because their flightless condition depresses basal rate. Passerines dominate temperate, terrestrial environments and the four orders of aquatic birds dominate temperate and polar aquatic environments because their high BMRs facilitate reproduction and migration. The low BMRs of tropical passerines may reflect a sedentary lifestyle as much as a life in a tropical climate. Birds have BMRs that are 30-40% greater than mammals because of the commitment of birds to an expensive and expansive form of flight.     

Basal metabolic rate, body weight and diet in primates: an evaluation of the evidence.

The relationship between basal metabolic rate (BMR), body weight and diet is examined for primates. Contrary to the results reported in several recent works, there is no strong evidence that diet is directly linked to BMR, although a low BMR, relative to body weight, may be found in species with folivorous diets. There is some evidence that nocturnal haplorhine species have a relatively low BMR, but strepsirhines appear to have a uniformly low relative BMR regardless of their primary activity period. The evolution of BMR in primates is discussed in the light of these findings. Some predictions are made about the relative BMRs that should be found for other species whose BMR is, as yet, unknown.     

The allometry of parrot BMR: seasonal data for the Greater Vasa Parrot, <Emphasis Type="Italic">Coracopsis vasa</Emphasis>, from Madagascar

In this study we examined the allometry of basal metabolic rate (BMR) of 31 parrot species. Unlike previous reports, we show that parrots per se do not display BMRs that are any different to other captive-raised birds of their body size. An ordinary least squares regression fitted the data best and body mass explained 95% of the variation in BMR. There was no phylogenetic signal in the BMR data. We also provide new data for the Greater Vasa Parrot (Coracopsis vasa) of Madagascar. We tested the hypotheses that C. vasa may, because of its insular existence, display conservative energetic traits (low BMR, use of adaptive heterothermy) similar to those observed in several Malagasy mammals. However, this was not the case. C. vasa had a higher BMR than other parrots, especially during summer, when BMR was up-regulated by 50.5% and was 95.7% higher than predicted from an ordinary least squares (OLS) allometry of parrots (BMR = 0.042M _b^0.649, BMR in Watts, M _b in grammes). Compared with BMR data for 94 captive-raised bird species, the winter and summer BMRs were, respectively, 45.5 and 117.8% higher than predicted by a phylogenetic generalised least squares (PGLS) allometry (BMR = 0.030M _b^0.687, BMR in Watts, M _b in grammes). The summer up-regulation of BMR is the highest recorded for a bird of any size to date. We suggest that the costs of a high summer BMR may be met by the unusual cooperative breeding system of C. vasa in which groups of males feed the female and share paternity. The potential breeding benefits of a high summer BMR are unknown.     

Phylogenetic differences of mammalian basal metabolic rate are not explained by mitochondrial basal proton leak

Metabolic rates of mammals presumably increased during the evolution of endothermy, but molecular and cellular mechanisms underlying basal metabolic rate (BMR) are still not understood. It has been established that mitochondrial basal proton leak contributes significantly to BMR. Comparative studies among a diversity of eutherian mammals showed that BMR correlates with body mass and proton leak. Here, we studied BMR and mitochondrial basal proton leak in liver of various marsupial species. Surprisingly, we found that the mitochondrial proton leak was greater in marsupials than in eutherians, although marsupials have lower BMRs. To verify our finding, we kept similar-sized individuals of a marsupial opossum (Monodelphis domestica) and a eutherian rodent (Mesocricetus auratus) species under identical conditions, and directly compared BMR and basal proton leak. We confirmed an approximately 40 per cent lower mass specific BMR in the opossum although its proton leak was significantly higher (approx. 60%). We demonstrate that the increase in BMR during eutherian evolution is not based on a general increase in the mitochondrial proton leak, although there is a similar allometric relationship of proton leak and BMR within mammalian groups. The difference in proton leak between endothermic groups may assist in elucidating distinct metabolic and habitat requirements that have evolved during mammalian divergence.     

Field metabolic rates of black-browed albatrosses Thalassarche melanophrys during the incubation stage

Field metabolic rates (FMR) and activity patterns of black-browed albatrosses Thalassarche melanophrys were measured while at sea and on nest during the incubation stage at Kerguelen Island, southwestern Indian Ocean. Activity-specific metabolic rates of five albatrosses at sea (FMR_at-sea) were measured using doubly labeled water (DLW), and by equipping birds with wet-dry activity data loggers that determined when birds were in flight or on the water. The metabolic rates of four birds incubating their eggs (FMR_on-nest) were also measured using DLW. The mean±SD FMR_at-sea of albatrosses was 611±96 kJ kg⁻¹ d⁻¹ compared to FMR_on-nest of 196±52 kJ kg⁻¹ d⁻¹. While at sea, albatrosses spent 52.9±8.2% (N=3) of their time in flight and they landed on the water 41.2±13.9 times per day. The FMR of black-browed albatrosses appear to be intermediate to that of three other albatross species. Based on at-sea activity, the power requirement of flight was estimated to be 8.7 W kg⁻¹ (or 4.0×predicted BMR), which is high compared to other albatross species, but may be explained by the high activity levels of the birds when at sea. The FMR_at-sea of albatrosses, when scaled with body mass, are lower than other seabirds of similar body size, which probably reflects the economical nature of their soaring flight.     

The evolution of body armor in mammals: plantigrade constraints of large body size

Predictions associated with opposing selection generating minimum variance in basal metabolic rate (BMR) in mammals at a constrained body mass (CBM; 358 g) were tested. The CBM is presumed to be associated with energetic constraints linked to predation and variable resources at intermediate sizes on a logarithmic mass scale. Opposing selection is thought to occur in response to energetic constraints associated with predation and unpredictable resources. As body size approaches and exceeds the CBM, mammals face increasing risks of predation and daily energy requirements. Fast running speeds may require high BMRs, but unpredictable and low resources may select for low BMRs, which also reduce foraging time and distances and thus predation risks. If these two selection forces oppose each other persistently, minimum BMR variance may result. However, extreme BMR outliers at and close to the CBM should be indicative of unbalanced selection and predator avoidance alternatives (escapers vs. defenders), and may therefore provide indirect support for opposing selection. It was confirmed that body armor in defenders evolves at and above the CBM, and armored mammals had significantly lower BMRs than their nonarmored counterparts. However, analyses comparing the BMR of escapers--the fastest nonarmored runners (Lagomorpha)--with similar-sized counterparts were inconclusive and were confounded by limb morphology associated with speed optimization. These analyses suggest that the risks and costs of predation and the speed limitations of the plantigrade foot may constrain the evolution of large body sizes in plantigrade mammals.     

Basal metabolic rates in mammals: taxonomic differences in the allometry of BMR and body mass

No single equation adequately describes the allometric relation between body mass and BMR for mammals. Least squares regression of log-transformed data for 248 eutherian species results in a line with a slope (-0.30) significantly different from that of Kleiber's line (-0.25). Interordinal comparisons of least squares regressions of log-transformed BMR and mass suggest that the Insectivora have a significantly steeper slope to their allometric relationship than do most other orders, while the non-insectivore orders are statistically homogeneous with respect to slope. With respect to elevation, Edentata have the lowest BMRs; Marsupialia, Primates and Chiroptera are indistinguishable from each other but above the edentates; Primates, Chiroptera, Rodentia, Lagomorpha and Carnivora form the next highest homogeneous grouping; and Artiodactyla have the highest BMRs, significantly greater than all but Lagomorpha and Carnivora. Analysis of intraordinal variation within the Rodentia suggests significant heterogeneity among families in BMR-mass allometry.     

Repeatability of basal metabolism in breeding female kittiwakes Rissa tridactyla

We studied kittiwakes (Rissa tridactyla) breeding near Ny-Ålesund (79° N, 12° E) on Svalbard. In 1997, the basal metabolic rates (BMRs) of 17 breeding females were measured during the incubation and chick-rearing periods. The mean body mass of the kittiwakes decreased significantly (by 10%) between the incubation and chick-rearing periods. At the same time, both the whole-body and mass-specific BMRs decreased significantly. There was a positive and significant relationship between the BMR residuals from the incubation period and those from the chick-rearing period. Thus, the BMR of incubating female kittiwakes is a significant predictor of their BMR during the chick-rearing period. New BMR data were collected in 1998 from ten of these females, measured around the chick-hatching date. Repeatability values were calculated using either (i) the data for eight individuals for which three BMR measurements existed, or (ii) all the data from both years, yielding significant repeatabilities of 0.52 and 0.35, respectively. These values indicate that between 48 and 65% of the observed variation in BMR is due to intraindividual variability, while between-individual variability accounts for 35 to 52% of the variation in the BMR. This is the first report of a significant repeatability of the BMR of an endothermic organism across an elapsed time of more than one day.     

The Zoogeography of Mammalian Basal Metabolic Rate

Zoogeographical effects on the basal metabolic rate (BMR) of 487 mammal species were analyzed using conventional and phylogenetically independent ANCOVA. Minimal BMR variance occurred at a "constrained body mass" of 358 g, whereas maximum variance occurred at the smallest and largest body masses. Significant differences in BMR were identified for similar-sized mammals from the six terrestrial zoogeographical zones (Afrotropical, Australasian, Indomalayan, Nearctic, Neotropical, and Palearctic). Nearctic and Palearctic mammals had higher basal rates than their Afrotropical, Australasian, Indomalayan, and Neotropical counterparts. Desert mammals had lower basal rates than mesic mammals. The patterns were interpreted with a conceptual model describing geographical BMR variance in terms of the influence of latitudinal and zonal climate variability. Low and high basal rates were explained in unpredictable and predictable environments, respectively, especially in small mammals. The BMR of large mammals may be influenced in addition by mobility and predation constraints. Highly mobile mammals tend to have high BMRs that may somehow facilitate fast running speeds, whereas less mobile mammals are generally dietary specialists and are often armored. The model thus integrates physiological and ecological criteria and makes predictions concerning body size and life-history evolution, island effects, and locomotor energetics.     

Seasonal energetics of northern phocid seals

The metabolic rate of harp (Pagophilus groenlandicus), harbor (Phoca vitulina), and ringed seals (Pusa hispida) was measured at various temperatures in air and water to estimate basal metabolic rates (BMRs) in these species. The basal rate and body composition of three harp seals were also measured throughout the year to examine the extent to which they vary seasonally. Marine mammalian carnivores generally have BMRs that are over three times the rates expected from body mass in mammals generally, both as a response to a cold-water distribution and to carnivorous food habits with the basal rates of terrestrial carnivores averaging about 1.8 times the mean of mammals. Phocid seals, however, have basal rates of metabolism that are 30% lower than other marine carnivores. Captive seals undergo profound changes in body mass and food consumption throughout the year, and after accounting for changes in body mass, the lowest rate of food intake occurs in summer. Contrary to earlier observations, harp seals also have lower basal rates during summer than during winter, but the variation in BMR, relative to mass expectations, was not associated with changes in the size of fat deposits. The summer reduction in energy expenditure and food consumption correlated with a reduction in BMR. That is, changes in BMR account for a significant portion of the seasonal variation in energy expenditure in the harp seal. Changes in body mass of harp seals throughout the year were due not only to changes in the size of body fat deposits, but also to changes in lean body mass. These results suggest that bioenergetics models used to predict prey consumption by seals should include time-variant energy requirements.     

HOW DOES EVOLUTIONARY VARIATION IN BASAL METABOLIC RATES ARISE? A STATISTICAL ASSESSMENT AND A MECHANISTIC MODEL

Metabolic rates are related to the pace of life. Hence, research into their variability at global scales is of vital importance for several contemporary theories in physiology, ecology, and evolution. Here we evaluated the effect of latitude, climate, primary productivity, habitat aridity, and species trophic habits, on mass‐independent basal metabolic rates (BMRs) for 195 rodent species. The aims of this article were twofold. First, we evaluated the predictive power of different statistical models (via a model selection approach), using a dimensional reduction technique on the exogenous factor matrix to achieve a clear interpretation of the selected models. Second, we evaluated three specific predictions derived from a recently proposed hypothesis, herein called the “obligatory heat” model (OHM), for the evolution of BMR. Obtained results indicate that mean/minimum environmental temperature, rainfall/primary productivity and, finally, species trophic habits are, in this order, the major determinants of mass‐independent BMR. Concerning the mechanistic causes behind this variation, obtained data agree with the predictions of the OHM: (1) mean annual environmental temperature was the best single predictor of residual variation in BMR, (2) herbivorous species have greater mass‐independent metabolic rates, and tend to be present at high‐latitude cold environments, than species in other trophic categories.     

GENETIC CORRELATIONS IN A WILD RODENT: GRASS-EATERS AND FAST-GROWERS EVOLVE HIGH BASAL METABOLIC RATES

Basal metabolic rate (BMR), commonly used as a measure of the cost of living, is highly variable among species, and sources of the variation are subject to an enduring debate among comparative biologists. One of the hypotheses links the variation in BMR with diversity of food habits and life-history traits. We test this hypothesis by asking how BMR of a particular species, the bank vole Myodes (= Clethrionomys ) glareolus , would change under selection for high growth rate (measured as a postweaning body mass change; MD_PW ) and the ability to cope with a low-quality herbivorous diet (measured as body mass change during a four-day test; MD_LQD ). We show that both of the traits are heritable in the narrow sense ( MD_PW : h ²= 0.30; MD_LQD : h ²= 0.19), and are genetically correlated with mass-independent BMR (additive genetic correlation, r_A = 0.28 for MD_PW and 0.37 for MD_LQD ). Thus, both of the traits could change in response to a selection, and the selection would also result in a correlated evolution of the level of metabolism. The results are consistent with the hypothesis that a part of the interspecific variation in BMR evolved in response to selection for life-history and ecological traits such as food habits.     

An analysis of the factors that influence the level and scaling of mammalian BMR

The factors influencing the basal rate of metabolism (BMR) in 639 species of mammals include body mass, food habits, climate, habitat, substrate, a restriction to islands or highlands, use of torpor, and type of reproduction. They collectively account for 98.8% of the variation in mammalian BMR, but often interact in complex ways. The factor with the greatest impact on BMR, as always, is body mass (accounting for 96.8% of its variation), the extent of its impact reflecting the 10(6.17)-fold range of mass in measured species. The attempt to derive mathematically the power relationship of BMR in mammals is complicated by the necessity to include all of the factors that influence BMR that are themselves correlated with body mass. BMR also correlates with taxonomic affiliation because many taxa are distinguished by their ecological and behavioral characteristics. Phylogeny, reflecting previous commitments, may influence BMR either through a restriction on the realized range of behaviors or by opening new behavioral and ecological opportunities. A new opportunity resulted from the evolution by eutherians of a type of reproduction that permitted species feeding on high quality resources to have high BMRs. These rates facilitated high rates of gas, nutrient, and waste exchange between a pregnant eutherian and her placental offspring. This pattern led to high rates of reproduction in some eutherians, a response denied all monotremes and marsupials, thereby permitting eutherians to occupy cold-temperate and polar environments and to dominate other mammals in all environments to which ecologically equivalent eutherians had access.     

Does basal metabolic rate contain a useful signal? Mammalian BMR allometry and correlations with a selection of physiological, ecological, and life-history variables

Basal metabolic rate (BMR, mL O2 h(-1)) is a useful measurement only if standard conditions are realised. We present an analysis of the relationship between mammalian body mass (M, g) and BMR that accounts for variation associated with body temperature, digestive state, and phylogeny. In contrast to the established paradigm that BMR proportional to M3/4, data from 619 species, representing 19 mammalian orders and encompassing five orders of magnitude variation in M, show that BMR proportional to M2/3. If variation associated with body temperature and digestive state are removed, the BMRs of eutherians, marsupials, and birds do not differ, and no significant allometric exponent heterogeneity remains between orders. The usefulness of BMR as a general measurement is supported by the observation that after the removal of body mass effects, the residuals of BMR are significantly correlated with the residuals for a variety of physiological and ecological variables, including maximum metabolic rate, field metabolic rate, resting heart rate, life span, litter size, and population density.     

The intrinsic rate of natural increase and reproductive effort in primates

The intrinsic rate of natural increase (r_max) is calculated for 58 primate species. It is found that this parameter is negatively correlated with body weight, so that larger primate species consistently have a lower r_max than do smaller species. Although there is no apparent link between the raw value of r_max and environmental predictability, a relationship between a high r_max, relative to body weight, and an unpredictable environment is found to exist. However, there is no relationship between a predictable environment and either the raw value of r_max, or the relative r_max. After body size effects are removed, r_max is not correlated with basal metabolic rate (BMR). Pre-natal maternal investment (MI) is found to correlate highly with BMR, even after the removal of body weight effects. MI does not correlate either with r_max or with environmental predictability. Diet appears to have little influence either on r_max on MI, but there is some indication that folivores have both a high relative r_max and a high relative MI. These results are discussed in the light of theories of life-history strategy evolution.     

Between Metabolite Relationships: an essential aspect of metabolic change

Not only the levels of individual metabolites, but also the relations between the levels of different metabolites may indicate (experimentally induced) changes in a biological system. Component analysis methods in current 'standard' use for metabolomics, such as Principal Component Analysis (PCA), do not focus on changes in these relations. We therefore propose the concept of 'Between Metabolite Relationships' (BMRs): common changes in the covariance (or correlation) between all metabolites in an organism. Such structural changes may indicate metabolic change brought about by experimental manipulation but which are lost with standard data analysis methods. These BMRs can be analysed by the INdividual Differences SCALing (INDSCAL) method. First the BMR quantification is described and subsequently the INDSCAL method. Finally, two studies illustrate the power and the applicability of BMRs in metabolomics. The first study is about the induced plant response of cabbage to herbivory, of which BMRs are a considerable part. In the second study-a human nutritional intervention study of green tea extract-standard data analysis tools did not reveal any metabolic change, although the BMRs were considerably affected. The presented results show that BMRs can be easily implemented in a wide variety of metabolomic studies. They provide a new source of information to describe biological systems in a way that fits flawlessly into the next generation of systems biology questions, dealing with personalized responses. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s11306-011-0316-1) contains supplementary material, which is available to authorized users.     

On the intraspecific variability in basal metabolism and the food habits hypothesis in birds

The food habits hypothesis (FHH) stands as one of the most striking and often-cited interspecific patterns to emerge from comparative studies of endothermic energetics. The FHH identifies three components of diet that potentially produce variability in mass-independent BMR, i.e. food quality, food availability, and food predictability or environmental productivity. The hypothesis predicts that species with diets of low energy content and/or low digestibility should evolve low mass-independent BMRs. The effe...