Mass-independent Basal Metabolic Rate Research Articles

Basal metabolic rate in free-ranging tropical birds lacks long-term repeatability and is influenced by ambient temperature.

Tropical birds live longer, have smaller clutches and invest more resources into self-maintenance than temperate species. These "slow" life-histories in tropical birds are accompanied by low basal metabolic rate (BMR). It has recently been suggested that the low BMR of tropical species may be related not to their slow "pace of life" or high ambient temperatures (Ta ) in tropical latitudes, but to the stability of environmental conditions in tropics. Since the repeatability of metabolic traits is higher in stable environments, such as laboratory conditions, we predicted that long-term repeatability of BMR in a tropical climate should be higher than in a temperate one. Contrary to our predictions, the repeatability of mass-independent BMR in 64 individuals of free-living tropical birds from Vietnam was low and insignificant after the species affiliation was taken into account. It indicates that BMR cannot be used as an individual long-term characteristic of tropical birds. On the other hand, tropical birds showed consistent differences in their mass-independent BMR at the interspecific level. Using BMR measurements from 1543 individuals of 134 species, we also found that different characteristics of Ta within the week preceding BMR measurements had a significant impact on the mass-independent BMR of tropical birds. The most significant effect was the difference between the absolute maximum and minimum Ta within a single week. Our results indicate that the physiology of tropical birds is more subject to changes than would be expected based on the notion of the stability of climatic conditions in the tropics.

Effects of Selection for Mass-Independent Maximal Metabolic Rate on Food Consumption.

Metabolic rates potentially regulate the pace of important physiological and life-history traits. Natural selection has shaped the evolution of metabolic rates and the physiology that supports them, including digestibility and the rate of food consumption. Understanding the relationship between metabolic rates and energy internalization is central to understanding how resources are allocated among competing physiological functions. We investigated how artificial selection on mass-independent basal metabolic rate (BMR) and mass-independent aerobic maximal metabolic rate (MMR) affected food consumption and apparent digestibility in mice. Evolved changes in mass-corrected BMR-but not mass-corrected MMR-corresponded with changes in food consumption. This result is consistent with previous work showing that BMR constitutes a large portion of an animal's daily energy budget and thus that BMR might provide a better indicator of daily food requirements than MMR. In contrast, digestive efficiencies did not differ among selection treatments and did not evolve in these mice. This study provides insights into how evolution of metabolic rates may affect food consumption and overall energy use.

On the Interplay among Ambient Temperature, Basal Metabolic Rate, and Body Mass.

One of the most generalized conclusions arising from studies analyzing the ecological variation of energy metabolism in endotherms is the apparent negative correlation between ambient temperature and mass-independent basal metabolic rate (residual BMR). As a consequence, ambient temperature has been considered the most important external factor driving the evolution of residual BMR. It is not clear, however, whether this relationship is size dependent, and artifacts such as the biased sampling of body masses in physiological data sets could cause us to overstate the ubiquity of the relationship. Accordingly, here we used published data on body mass (mb), BMR, and annual mean temperature (Tmean) for 458 mammal species (and/or subspecies) to examine the size dependence of the relationship between temperature and BMR. We found a significant interaction between mb and Tmean as predictors of residual BMR, such that the effect of Tmean on residual BMR decreases as a function of mb. In line with this, the amount of residual variance in BMR explained by Tmean decreased with increasing mb, from 20%-30% at body sizes of less than 100 g to almost 0 at body sizes greater than 1,000 g. These data suggest that our current understanding of the importance of broad-scale variation in ambient temperature as a driver of metabolic evolution in endotherms probably is affected by the large number of small species in both nature and physiological data sets.

How low can you go? An adaptive energetic framework for interpreting basal metabolic rate variation in endotherms.

Adaptive explanations for both high and low body mass-independent basal metabolic rate (BMR) in endotherms are pervasive in evolutionary physiology, but arguments implying a direct adaptive benefit of high BMR are troublesome from an energetic standpoint. Here, we argue that conclusions about the adaptive benefit of BMR need to be interpreted, first and foremost, in terms of energetics, with particular attention to physiological traits on which natural selection is directly acting. We further argue from an energetic perspective that selection should always act to reduce BMR (i.e., maintenance costs) to the lowest level possible under prevailing environmental or ecological demands, so that high BMR per se is not directly adaptive. We emphasize the argument that high BMR arises as a correlated response to direct selection on other physiological traits associated with high ecological or environmental costs, such as daily energy expenditure (DEE) or capacities for activity or thermogenesis. High BMR thus represents elevated maintenance costs required to support energetically demanding lifestyles, including living in harsh environments. BMR is generally low under conditions of relaxed selection on energy demands for high metabolic capacities (e.g., thermoregulation, activity) or conditions promoting energy conservation. Under these conditions, we argue that selection can act directly to reduce BMR. We contend that, as a general rule, BMR should always be as low as environmental or ecological conditions permit, allowing energy to be allocated for other functions. Studies addressing relative reaction norms and response times to fluctuating environmental or ecological demands for BMR, DEE, and metabolic capacities and the fitness consequences of variation in BMR and other metabolic traits are needed to better delineate organismal metabolic responses to environmental or ecological selective forces.

Understanding evolutionary variation in basal metabolic rate: An analysis in subterranean rodents

Understanding how evolutionary variation in energetic metabolism arises is central to several theories in animal biology. Basal metabolic rate (BMR) –i.e., the minimum rate of energy necessary to maintain thermal homeostasis in endotherms– is a highly informative measure to increase our understanding, because it is determined under highly standardized conditions. In this study we evaluate the relationship between taxa- and mass-independent (residual) BMR and ten environmental factors for 34 subterranean rodent species. Both conventional and phylogenetically informed analyses indicate that ambient temperature is the major determinant of residual BMR, with both variables inversely correlated. By contrast, other environmental factors that have been shown to affect residual BMR in endotherms, such as habitat productivity and rainfall, were not significant predictors of residual BMR in this group of species. Then, the results for subterranean rodents appear to support a central prediction of the obligatory heat model (OHM), which is a mechanistic model aimed to explain the evolution of residual BMR. Specifically, OHM proposes that during the colonization of colder environments, individuals with greater masses of metabolically expensive tissues (and thus with greater BMR) are favored by natural selection due to the link between greater masses of metabolically expensive tissues and physiological capacities. This way, natural selection should establishes a negative correlation between ambient temperature and both internal organ size and residual BMR.

A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate.

Metabolic rates are correlated with many aspects of ecology, but how selection on different aspects of metabolic rates affects their mutual evolution is poorly understood. Using laboratory mice, we artificially selected for high maximal mass-independent metabolic rate (MMR) without direct selection on mass-independent basal metabolic rate (BMR). Then we tested for responses to selection in MMR and correlated responses to selection in BMR. In other lines, we antagonistically selected for mice with a combination of high mass-independent MMR and low mass-independent BMR. All selection protocols and data analyses included body mass as a covariate, so effects of selection on the metabolic rates are mass adjusted (that is, independent of effects of body mass). The selection lasted eight generations. Compared with controls, MMR was significantly higher (11.2%) in lines selected for increased MMR, and BMR was slightly, but not significantly, higher (2.5%). Compared with controls, MMR was significantly higher (5.3%) in antagonistically selected lines, and BMR was slightly, but not significantly, lower (4.2%). Analysis of breeding values revealed no positive genetic trend for elevated BMR in high-MMR lines. A weak positive genetic correlation was detected between MMR and BMR. That weak positive genetic correlation supports the aerobic capacity model for the evolution of endothermy in the sense that it fails to falsify a key model assumption. Overall, the results suggest that at least in these mice there is significant capacity for independent evolution of metabolic traits. Whether that is true in the ancestral animals that evolved endothermy remains an important but unanswered question.

Thyroid Hormones Correlate with Basal Metabolic Rate but Not Field Metabolic Rate in a Wild Bird Species

Thyroid hormones (TH) are known to stimulate in vitro oxygen consumption of tissues in mammals and birds. Hence, in many laboratory studies a positive relationship between TH concentrations and basal metabolic rate (BMR) has been demonstrated whereas evidence from species in the wild is scarce. Even though basal and field metabolic rates (FMR) are often thought to be intrinsically linked it is still unknown whether a relationship between TH and FMR exists. Here we determine the relationship between the primary thyroid hormone triiodothyronine (T3) with both BMR and FMR in a wild bird species, the black-legged kittiwake (Rissa tridactyla). As predicted we found a strong and positive relationship between plasma concentrations of T3 and both BMR and mass-independent BMR with coefficients of determination ranging from 0.36 to 0.60. In contrast there was no association of T3 levels with either whole-body or mass-independent FMR (R2 = 0.06 and 0.02, respectively). In accordance with in vitro studies our data suggests that TH play an important role in modulating BMR and may serve as a proxy for basal metabolism in wild birds. However, the lack of a relationship between TH and FMR indicates that levels of physical activity in kittiwakes are largely independent of TH concentrations and support recent studies that cast doubt on a direct linkage between BMR and FMR.

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

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

Skeletal muscle lipid metabolism changes in mice selected for high maximal metabolic rate

Exercise and fasting both increase free fatty acids, and elevated unsaturated free fatty acids are up‐regulators of lipid metabolism in skeletal muscles. We examined fatty acids in skeletal muscles in lines of Mus musculus artificially selected for high maximal metabolic rate (high‐MMR). These mice were not exercised and standard laboratory rat chow was available ad libitum. After 7 generations of directional selection for increased mass‐independent MMR, high‐MMR mice showed a 10.2% increase in mass‐independent MMR and a concomitant 2.8% increase in mass‐independent basal metabolic rate compared to control mice. Free fatty acids in the gastrocnemius muscle differed significantly between high‐MMR and control mice. For mice selected for high‐MMR, there was a significant increase in linoleic and oleic acids—consistent with elevated fatty acid oxidation in the skeletal muscle. There was no difference in muscle phospholipid fatty acid composition between high‐MMR and control mice. These findings suggest that selection for high‐MMR resulted in elevated fatty acid oxidation in the skeletal muscles. Most importantly, the results suggest that there is a genetic component to elevated unsaturated free fatty acids in skeletal muscles. Supported by NSF IOS 0344994.

Limited Access to Food and Physiological Trade‐Offs in a Long‐Distance Migrant Shorebird. I. Energy Metabolism, Behavior, and Body‐Mass Regulation

Previous experiments showed reduction of basal metabolic rate (BMR) in birds facing energetic challenges. We alternately exposed two groups of red knots (Calidris canutus) to either 6 h or 22 h of food availability for periods of 22 d. Six h of access to food led to a 6%-10% loss of body mass over the first 8 d, with nearly all of the birds' daily energy expenditures supported by body nutrient stores during the first 2 d. Birds responded by increasing feeding behavior and food intake, but the response was slow. There were no gains of mass before day 15, which suggests a digestive bottleneck and a period of physiological adjustment. Food-restricted birds exhibited decreases in pectoral-muscle thickness and BMR in association with a loss of body mass. Although a decrease in BMR saves energy, savings represented only 2%-7% of the daily energy spent in excess of that acquired during the deficit period. Red knots did not downregulate mass-independent BMR. On the bases of recent independent findings and the pattern of mass gain observed when food access was switched from 6 h to 22 h, we suggest that these birds routinely maintain nutrient stores as a buffer against periods of energy shortages, thereby precluding the need for downregulation of mass-independent BMR.

Genetic variances and covariances of aerobic metabolic rates in laboratory mice

The genetic variances and covariances of traits must be known to predict how they may respond to selection and how covariances among them might affect their evolutionary trajectories. We used the animal model to estimate the genetic variances and covariances of basal metabolic rate (BMR) and maximal metabolic rate (MMR) in a genetically heterogeneous stock of laboratory mice. Narrow-sense heritability (h(2)) was approximately 0.38 +/- 0.08 for body mass, 0.26 +/- 0.08 for whole-animal BMR, 0.24 +/- 0.07 for whole-animal MMR, 0.19 +/- 0.07 for mass-independent BMR, and 0.16 +/- 0.06 for mass-independent MMR. All h(2) estimates were significantly different from zero. The phenotypic correlation of whole animal BMR and MMR was 0.56 +/- 0.02, and the corresponding genetic correlation was 0.79 +/- 0.12. The phenotypic correlation of mass-independent BMR and MMR was 0.13 +/- 0.03, and the corresponding genetic correlation was 0.72 +/- 0.03. The genetic correlations of metabolic rates were significantly different from zero, but not significantly different from one. A key assumption of the aerobic capacity model for the evolution of endothermy is that BMR and MMR are linked. The estimated genetic correlation between BMR and MMR is consistent with that assumption, but the genetic correlation is not so high as to preclude independent evolution of BMR and MMR.

Hormonal Correlates and Thermoregulatory Consequences of Molting on Metabolic Rate in a Northerly Wintering Shorebird

Even though molt involves both endocrine and energetic changes in bird bodies, this study is among the first to combine assessments of energy costs together with thyroid hormone variations in molting birds. Individual shorebirds (red knots Calidris canutus islandica) were measured while in full summer and winter plumage as well as during peak of molt. Molt was associated with a 9.8% increase in average mass-independent basal metabolic rate (BMR) above nonmolting levels. Individual plasma levels of thyroxine (T(4)) were correlated with individual rate of body feather renewal, confirming that T(4) is related to body molt but also showing that it is potentially regulating its rate. Across seasons, mass-independent average heat loss measured as conductance gradually declined with conductance during molt falling between measured values for summer and winter. During the molting period, however, body molting rate was positively correlated with thermal conductance, indicating that for a given ambient temperature below thermoneutrality, the fastest molting birds were losing more body heat. Across seasons, triiodothyronine (T(3)), a hormone typically upregulated in response to a cold stimulus, was correlated with individual thermal conductance and BMR. We suggest that the increased heat loss of fast-molting birds leads to a cold-acclimatization response that may be partly responsible for the elevated BMR measured during molt. This could be mediated through a stimulatory effect of T(3) on BMR in response to increased heat loss. Our interpretation is supported by a positive relationship between the individual changes in conductance and the change in BMR from summer to the molting period.

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.

Basal metabolism is correlated with habitat productivity among populations of degus ( Octodon degus)

Several competing hypotheses attempt to explain how environmental conditions affect mass-independent basal metabolic rate (BMR) in mammals. One of the most inclusive is the hypothesis that associates BMR with food habits, including habitat productivity. The effects of food habits have been widely investigated at the interspecific level, and variation between individuals and populations has been largely ignored. Intraspecific analysis of physiological traits has the potential to compensate for many pitfalls associated with interspecific analyses and serve as a useful approach for evaluating hypotheses regarding metabolic adaptation. Here we tested the effects of climatic variables (mean annual rainfall = PP, mean annual temperature = T A), net primary productivity (NPP) and the de Martonne index (DMi) of aridity on mass-independent BMR among four populations of the caviomorph rodent Octodon degus along a geographic gradient in Chile. BMR was measured on animals maintained in a common garden acclimation set-up, thus kept under the same environment and diet quality for at least 6 months. Mass-independent BMR was significantly different among degu populations showing a large intraspecific spread in metabolic rates. A very large fraction of interpopulational variability in mass-independent BMR was explained by NPP, PP and DMi. Our results were conclusive about the effects of habitat productivity on setting the level of mass-independent BMR at the intraspecific–interpopulational level.

Intraspecific Variability in the Basal Metabolic Rate: Testing the Food Habits Hypothesis

Several competing hypotheses attempt to explain how environmental conditions affect mass-independent basal metabolic rate (BMR) in mammals. One of the most inclusive and yet debatable hypotheses is the one that associates BMR with food habits, including habitat productivity. These effects have been widely investigated at the interspecific level under the assumption that for any given species all traits are fixed. Consequently, the variation among individuals is largely ignored. Intraspecific analysis of physiological traits has the potential to compensate for many of the pitfalls associated with interspecific analyses and, thus, to be a useful approach for evaluating hypotheses regarding metabolic adaptation. In this study, we investigated the effects of food quality, availability, and predictability on the BMR of the leaf-eared mouse Phyllotis darwini. BMR was measured on freshly caught animals from the field, since they experience natural seasonal variations in environmental factors (and, hence, variations in habitat productivity) and diet quality. BMR was significantly correlated with the proportion of dietary plants and seeds. In addition, BMR was significantly correlated with monthly habitat productivity. Path analysis indicated that, in our study, habitat productivity was responsible for the observed changes in BMR, while diet per se had no effect on this variable.

Energetics, thermoregulation and torpor in the Chilean mouse-opossum Thylamys elegans (Didelphidae)

In this paper we studied the energetics and thermoregulation of the Chilean mouse-opossum Thylamys elegans (Dielphidae) a nocturnal small marsupial, endemic of southern South America. We studied their standard energetic and determined whether they exhibit shallow daily torpor or deep prolonged torpor as a function of ambient temperature and food availability. Thylamys elegans partially supports the hypothesis that Neotropical marsupials have somewhat a higher basal metabolic rate (BMR) and thermal conductance (Cm) than Australian ones. In fact, BMR was higher but Cm was lower than expected for their body mass. The higher mass-independent BMR of the Chilean mouse-opossum may be explained by its insectivorous food habits and its low Cm by its temperate habitats. Euthermic Chilean mouse-opossum showed daily fluctuations in body temperature being significantly higher during night time. In addition T. elegans entered in daily torpor and aroused spontaneously only was food was absent. That is, this species display a facultative type of daily torpor because propensity to enter in torpor was dependent of the combination of food absence and low ambient temperature. No torpor was observed when food was available. During torpor ambient temperature was slightly above ambient temperature between 0.3 to 0.5 °C. Torpor in this species as well as in marsupials in general, appears to be a flexible and an opportunistic response to unpredictable environmental conditions.

Nutrition and the energetic tactics of muskrats (Ondatra zibethicus): morphological and metabolic adjustments to seasonal shifts in diet quality

Basal metabolic rate (BMR), serum thyroxine (T4) concentration, lean organ mass, and body composition were measured in 94 captive, seasonally acclimatized muskrats (Ondatra zibethicus) between May 1991 and April 1992. Seasonal measurements of oxygen consumption, body water content, and mass were obtained from an additional 124 captive or free-ranging animals in 1994-1995. Mass-independent BMRs (kJ · kg-0.67· h-1) and serum T4concentrations (nmol · L-1) varied significantly over the year (P << 0.0001), with mean values in February exceeding July values by 31.1 and 77.2%, respectively. These variables tracked seasonal changes in the neutral detergent soluble (NDS) content of broadleaf cattails (Typha latifolia), the dominant food of muskrats in the study population. From July through February, alimentary tract, liver, spleen, and heart masses increased, while kidney mass declined. Body fat stores varied significantly over both years, with peak values measured in February. However, lean body and pelt masses exhibited little seasonal variation (P >> 0.05). Stepwise multiple regression and principal component analyses suggested that variation in BMR was associated most closely with changes in heart and alimentary tract masses. Annual variations in basal energy expenditure, serum T4concentration, and organ masses of wild muskrats appear to be linked to seasonal changes in forage NDS content and energy intake, and may be important factors relating to the annual pattern of fat accretion and mobilization in this semiaquatic rodent.

Individual Variation in Metabolism and Reproduction of Mus: Are Energetics and Life History Linked?

The possibility of functional relationships between energetics and life-history characteristics has been of considerable interest to evolutionary ecologists. Among species of mammals, life-history variables generally are not correlated with mass-independent basal metabolic rate, with the possible exceptions of maximal intrinsic rate of increase, litter size and reproductive effort during lactation. Whether this is generally true at the level of variation among individuals within a population (individual variation) is unclear. Therefore, we tested whether basal or maximal metabolic rates of random-bred female mice (Mus domesticus) were correlated with the size of their litters, litter mass, or mean offspring mass. The effects of variation in maternal mass, maternal age, experimental block and duration of fasting (for basal metabolic rate) were removed by calculating residuals from multiple regression equations. Basal and maximal metabolic rate were not significantly correlated with any of the life-history variables we studied. Thus, our results are generally consistent with those from interspecific comparisons of mammals: little evidence suggests necessary associations between metabolic rates and life history.

On the Relation Between Basal and Field Metabolic Rates in Birds and Mammals

Basal metabolic rate (BMR) is widely assumed to be an index of energy expenditure of free-living animals. However, few attempts have been made to check if the assumption is valid. In this study field metabolic rates (FMR) of 58 species of birds and mammals have been compared with their BMRs. FMR tends to increase with increasing body mass slower than BMR, but the difference was significant only in marsupials. A correlation between mass-independent FMR and BMR (residuals from regressions) is very high in eutherians (mainly rodents), but it is weak in birds and approaches zero in marsupials. The assumption of a proportionality between BMR and energy expenditure of animals does not have a sound experi-