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.     

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.     

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...     

The relationship between diet quality and basal metabolic rate in endotherms: insights from intraspecific analysis

In this article, we review intraspecific studies of basal metabolic rate (BMR) that address the correlation between diet quality and BMR. The "food-habit hypothesis" stands as one of the most striking and often-mentioned interspecific patterns to emerge from studies of endothermic energetics. Our main emphasis is the explicit empirical comparison of predictions derived from interspecific studies with data gathered from within-species studies in order to explore the mechanisms and functional significance of the putative adaptive responses encapsulated by the food-habit hypothesis. We suggest that, in addition to concentrating on the relationship among diet quality, internal morphology, and BMR, new studies should also attempt to unravel alternative mechanisms that shape the interaction between diet and BMR, such as enzymatic plasticity, and the use of energy-saving mechanisms, such as torpor. Another avenue for future study is the measurement of the effects of diet quality on other components of the energy budget, such as maximum thermogenic and sustainable metabolic rates. It is possible that the effects of diet quality operate on such components rather than directly on BMR, which might then push or pull along changes in these traits. Results from intraspecific studies suggest that the factors responsible for the association between diet and BMR at an ecological timescale might not be the same as those that promoted the evolution of this correlation. Further analyses should consider how much of a role the proximate and ultimate processes have played in the evolution of BMR.     

Intraspecific basal metabolic rate varies with trophic level in rufous-collared sparrows

One of the most controversial hypotheses that associate basal metabolic rate (BMR) with food habits and habitat productivity is the food habit hypothesis (FHH). Here we examined the relationship between BMR, diet, and climate among populations of the omnivorous passerine, Zonotrichia capensis (Emberizidae). We used nitrogen stable isotopes to estimate each individual's relative trophic level. To tease apart the effect of climatic variables and diet on BMR, we also used structural equation modeling. After the effect of body mass and climatic variables was taken into account, a significant effect of trophic level as estimated by δ¹⁵N on BMR was found. Our result seems to support the FHH at the intraspecific level, i.e., birds from the lower trophic levels – feeding on seeds and bud – had higher BMR than individuals from higher trophic levels.     

Phenotypic plasticity in the scaling of avian basal metabolic rate

Many birds exhibit short-term, reversible adjustments in basal metabolic rate (BMR), but the overall contribution of phenotypic plasticity to avian metabolic diversity remains unclear. The available BMR data include estimates from birds living in natural environments and captive-raised birds in more homogenous, artificial environments. All previous analyses of interspecific variation in BMR have pooled these data. We hypothesized that phenotypic plasticity is an important contributor to interspecific variation in avian BMR, and that captive-raised populations exhibit general differences in BMR compared to wild-caught populations. We tested this hypothesis by fitting general linear models to BMR data for 231 bird species, using the generalized least-squares approach to correct for phylogenetic relatedness when necessary. The scaling exponent relating BMR to body mass in captive-raised birds (0.670) was significantly shallower than in wild-caught birds (0.744). The differences in metabolic scaling between captive-raised and wild-caught birds persisted when migratory tendency and habitat aridity were controlled for. Our results reveal that phenotypic plasticity is a major contributor to avian interspecific metabolic variation. The finding that metabolic scaling in birds is partly determined by environmental factors provides further support for models that predict variation in scaling exponents, such as the allometric cascade model.     

Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents

Metabolic rate is a key aspect of organismal biology and the identification of selective factors that have led to species differences is a major goal of evolutionary physiology. We tested whether environmental characteristics and/or diet were significant predictors of interspecific variation in rodent metabolic rates. Mass-specific basal metabolic rates (BMR) and maximum metabolic rates (MMR, measured during cold exposure in a He-O2 atmosphere) were compiled from the literature. Maximum (Tmax) and minimum (Tmin) annual mean temperatures, latitude, altitude, and precipitation were obtained from field stations close to the capture sites reported for each population (N = 57). Diet and all continuous-valued traits showed statistically significant phylogenetic signal, with the exception of mass-corrected MMR and altitude. Therefore, results of phylogenetic analyses are emphasized. Body mass was not correlated with absolute latitude, but was positively correlated with precipitation in analyses with phylogenetically independent contrasts. Conventional multiple regressions that included body mass indicated that Tmax (best), Tmin, latitude, and diet were significant additional predictors of BMR. However, phylogenetic analyses indicated that latitude was the only significant predictor of mass-adjusted BMR (positive partial regression coefficient, one-tailed P = 0.0465). Conventional analyses indicated that Tmax, Tmin (best), and altitude explained significant amounts of the variation in mass-adjusted MMR. With body mass and Tmin in the model, no additional variables were significant predictors. Phylogenetic contrasts yielded similar results. Both conventional and phylogenetic analyses indicated a highly significant positive correlation between residual BMR and MMR (as has also been reported for birds), which is consistent with a key assumption of the aerobic capacity model for the evolution of vertebrate energetics (assuming that MMR and exercise-induced maximal oxygen consumption are positively functionally related). Our results support the hypothesis that variation in environmental factors leads to variation in the selective regime for metabolic rates of rodents. However, the causes of a positive association between BMR and latitude remain obscure. Moreover, an important area for future research will be experiments in all taxa are raised under common conditions to allow definitive tests of climatic adaptation in endotherm metabolic rates and to elucidate the extent of adaptive phenotypic plasticity.     

The effect of diet quality on physiological and life-history traits in the harvestman Pachylus paessleri

The balance between energy acquisition and expenditure is critical to the survival and reproductive success of animals. Here we investigate the long-term effects of diet quality on physiological and life-history flexibility in the harvestman, Pachylus paessleri. We used cow meal as a protein-rich diet and potatoes as a carbohydrate-rich diet in order to reproduce two extreme conditions regarding food quality in harvestmen natural habitat. As proxy variables of the energy expenditure process, we quantified standard metabolic rate (maintenance), changes in body mass (somatic condition), and fecundity (reproduction). We found that animals consuming the protein-rich diet were able to increase both their body condition and fecundity. However, the increment in these two life-history traits was correlated with higher maintenance costs. In contrast, the carbohydrate-rich diet did not provide enough specific nutrients for reproductive events, although it may have allowed animals to survive for a long time. Thus, according to the quality of the diet available in the environment, harvestman females can adopt different life-history strategies correlated with phenotypic adjustments at anatomical and physiological levels. In the Mediterranean region, spatial and temporal changes in food quality are typical, so greater phenotypic flexibility is expected to cope with this kind of environmental variation.     

Basal metabolic rate: heritability and genetic correlations with morphological traits in the zebra finch

Studies of genetic variation in metabolic traits have so far not focused on birds. In our study population of captive zebra finches we found evidence for a significant heritable genetic component in basal metabolic rate (BMR). Heritability of all morphological traits investigated (body mass, head length, tars length and wing length) was significantly larger than zero. All traits were positively phenotypically correlated. Eight of 10 genetic correlations presented in this study differed significantly from zero, all being positive, suggesting the possibility of correlated responses to any selection acting on the traits. When conditioned on the genetic variance in body mass, the heritability of BMR was reduced from 25% to 4%. Hence, our results indicate that genetic changes in BMR through directional selection are possible, but the potential for adaptation independent of body mass may be limited.     

内蒙古草原布氏田鼠代谢率与身体器官的关系

动物代谢率存在差异的原因及其意义是进化生理学的一个核心问题。为了解代谢率的影响因素和功能意义, 我们测定了不同驯化条件下布氏田鼠(Microtus brandti) 的基础代谢率(basal metabolic rate , BMR) 、日能量消耗(daily energy expenditure , DEE) 和冷诱导的最大代谢率(maximum metabolic rate , MMR) , 分析了动物体内11 种器官、组织的重量与代谢率的关系。结果显示, 排除温度、光照、食物质量和体重的影响后, BMR 与心脏、肝脏、肾脏、胃和盲肠相关; DEE与心脏、肾脏、胃和盲肠相关; MMR 与脑重显著负相关。这表明: 在布氏田鼠体内存在着代谢活性器官, 主要包括心脏、肝脏、肾脏、胃和盲肠, 这些器官对BMR 有较大的贡献。动物的能量周转水平与体内“代谢机器” (metabolic machinery) 的大小相关连, 主要受到心脏、肾脏、胃和盲肠的影响。最大代谢率受脑重的影响。BMR 与MMR 的相关性不显著, 而BMR 与DEE 的相关性显著, 说明较高的BMR 有助于维持较高的DEE , 但不能维持较高的MMR。     

Effects of dietary quality on basal metabolic rate and internal morphology of European starlings (Sturnus vulgaris)

European starlings (Sturnus vulgaris) were fed either a low- or high-quality diet to test the effects of dietary quality on basal metabolic rate (BMR) and internal morphology. Basal metabolic rate did not differ significantly between the two dietary groups, but internal morphology differed greatly. Starlings fed the low-quality diet had heavier gastrointestinal tracts, gizzards, and livers. Starlings fed the high-quality diet had heavier breast muscles. Starlings on the low-quality diet maintained mass, while starlings on the high-quality diet gained mass. Dry matter digestibility and energy digestibility were lower for starlings fed the low-quality diet, and their food and water intake were greater than starlings on the high-quality diet. The lack of dietary effect on BMR may be the result of increased energy expenditure of digestive organs paralleling a reduction of energy expenditure of organs and tissues not related to digestion (i.e., skeletal muscle). This trade-off in energy allocation among organs suggests a mechanism by which organisms may alter BMR in response to a change in seasonal variation in food availability.     

Determinants of inter-specific variation in basal metabolic rate

Basal metabolic rate (BMR) is the rate of metabolism of a resting, postabsorptive, non-reproductive, adult bird or mammal, measured during the inactive circadian phase at a thermoneutral temperature. BMR is one of the most widely measured physiological traits, and data are available for over 1,200 species. With data available for such a wide range of species, BMR is a benchmark measurement in ecological and evolutionary physiology, and is often used as a reference against which other levels of metabolism are compared. Implicit in such comparisons is the assumption that BMR is invariant for a given species and that it therefore represents a stable point of comparison. However, BMR shows substantial variation between individuals, populations and species. Investigation of the ultimate (evolutionary) explanations for these differences remains an active area of inquiry, and explanation of size-related trends remains a contentious area. Whereas explanations for the scaling of BMR are generally mechanistic and claim ties to the first principles of chemistry and physics, investigations of mass-independent variation typically take an evolutionary perspective and have demonstrated that BMR is ultimately linked with a range of extrinsic variables including diet, habitat temperature, and net primary productivity. Here we review explanations for size-related and mass-independent variation in the BMR of animals, and suggest ways that the various explanations can be evaluated and integrated.     

Diet, phylogeny, and basal metabolic rate in phyllostomid bats

Aside from the pervasive effects of body mass, much controversy exists as to what factors account for interspecific variation in basal metabolic rates (BMR) of mammals; however, both diet and phylogeny have been strongly implicated. We examined variation in BMR within the New World bat family Phyllostomidae, which shows the largest diversity of food habits among mammalian families, including frugivorous, nectarivorous, insectivorous, carnivorous and blood-eating species. For 27 species, diet was taken from the literature and BMR was either measured on animals captured in Brazil or extracted from the literature. Conventional (nonphylogenetic) analysis of covariance (ANCOVA), with body mass as the covariate, was first used to test the effects of diet on BMR. In this analysis, which assumes that all species evolved simultaneously from a single ancestor (i.e., a "star" phylogeny), diet exerted a strong effect on mass-independent BMR: nectarivorous bats showed higher mass-independent BMR than other bats feeding on fruits, insects or blood. In phylogenetic ANCOVAs via Monte Carlo computer simulation, which assume that species are part of a branching hierarchical phylogeny, no statistically significant effect of diet on BMR was observed. Hence, results of the nonphylogenetic analysis were misleading because the critical values for testing the effect of diet were underestimated. However, in this sample of bats, diet is perfectly confounded with phylogeny, because the four dietary categories represent four separate subclades, which greatly reduces statistical power to detect a diet (= subclade) effect. But even if diet did appear to exert an influence on BMR in this sample of bats, it would not be logically possible to separate this effect from the possibility that the dietary categories differ for some other reason (i.e., another synapomorphy of one or more of the subclades). Examples such as this highlight the importance of considering phylogenetic relationships when designing new comparative studies, as well as when analyzing existing data sets. We also discuss some possible reasons why BMR may not coadapt with diet.     

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.     

Responses of 'resistant' vertebrates to habitat loss and fragmentation: the importance of niche breadth and range boundaries

Abstract. An ability to predict species' sensitivities to habitat loss and fragmentation has important conservation implications, and numerous hypotheses have been proposed to explain interspecific differences observed in human-dominated landscapes. We used occupancy data collected on 32 species of vertebrates (16 mammals and 16 amphibians) in an agricultural landscape of Indiana, USA, to compare hypotheses that focus on different causal mechanisms underlying interspecific variation in responses to habitat alteration: (1) body size; (2) morphology and development; (3) behaviour; (4) niche breadth; (5) proximity to range boundary; and multiple-process models combining main effects and interactions of hypotheses (1)–(2) and (4)–(5). The majority of habitat alteration occurred over a century ago and coincided with extinction of several species; thus, our study dealt only with variation in responses of extant species that often are considered 'resistant' to human modifications of native habitat. Corrected Akaike scores and Akaike weights provided strongest support for models incorporating niche breadth and proximity to range boundary. Measures of dietary and habitat breadth obtained from the literature were negatively correlated with sensitivity to habitat alteration. Additionally, greater sensitivity was observed for species occurring at the periphery of their geographical ranges, especially at northern or western margins. Body size, morphological, developmental and behavioural traits were inferior predictors of tolerance to fragmentation for the species and landscape we examined. Our findings reinforce the importance of niche breadth as a predictor of species' responses to habitat alteration. They also highlight the importance of viewing the effects of habitat loss and fragmentation in a landscape within a biogeographical context that considers a species' level of adaptation to local environmental conditions.     

Phenotypic flexibility in basal metabolic rate is associated with rainfall variability among populations of rufous-collared sparrow

Phenotypic flexibility in metabolic rates allows organisms to reversibly adjust their energy flow to meet challenges imposed by a variable environment. In turn, the food habits hypothesis (FHH) predicts that species or populations adjust their basal metabolic rate (BMR) according to the diet attributes such as food abundance or predictability. Desert ecosystems represent a temporally heterogeneous environment because of low rain pulse predictability, which is also associated with temporal variation in food resources. In the present study, we investigated the relationship between the magnitude of BMR flexibility in response to dietary acclimation and the inter-annual rainfall variability in three populations of rufous-collared sparrows. Specifically we addressed the question of whether birds from a desert environment are more flexible in BMR than those from non-desert habitats. We found a positive trend between BMR flexibility and the inter-annual rainfall variability. In fact, dietary treatments had a significant effect only in desert birds, a result that also supported the FHH. Our study confirms the existence of phenotypic variation in response to environmental conditions among populations, and also highlights the importance of considering the circumstances in which phenotypic flexibility evolves and the specific environmental cues that induce their expression.     

黑线仓鼠的BMR个体差异及其应对高脂食物的能量学对策

为探讨高脂食物对小型哺乳动物能量代谢的影响及其与基础代谢率(Basal metabolic rate, BMR)的关系,将成年雌性黑线仓鼠(Cricetulus barabensis)分为高、低BMR组,每组再随机分为低脂、高脂食物组,驯化6周后,测定体重、摄入能和代谢率,以及消化酶活力、褐色脂肪组织(Brown adipose tissue, BAT)和主要内脏器官与肌肉的细胞色素c氧化酶(Cytochrome c oxidase, COX)活性、解偶联蛋白(Uncoupling protein, UCP) mRNA表达等。结果显示,高脂食物对高、低BMR组动物体重均无显著影响。与低脂食物组相比,高脂食物组的摄食量、摄入能和消化能显著下降,小肠脂肪酶活力显著增强,消化率明显增加,但高、低BMR组的组间差异不显著。夜间代谢水平显著高于昼间,高脂食物使高BMR组的夜间代谢率显著升高。BAT、肌肉和内脏器官COX活性不受高脂食物的影响,高、低BMR组的组间差异也不显著。高脂食物组仅肝脏UCP2表达显著上调。结果表明,能量摄入和消化系统形态及功能的可塑性调节是黑线仓鼠应对高脂食物的主要策略;黑线仓鼠的代谢率具有显著的昼夜节律,既受高脂食物的影响,也与动物自身的BMR水平有关,但UCP表达具有组织特异性,这可能不是导致BMR个体差异的因素。     

Environment, migratory tendency, phylogeny and basal metabolic rate in birds

Basal metabolic rate (BMR) represents the minimum maintenance energy requirement of an endotherm and has far-reaching consequences for interactions between animals and their environments. Avian BMR exhibits considerable variation that is independent of body mass. Some long-distance migrants have been found to exhibit particularly high BMR, traditionally interpreted as being related to the energetic demands of long-distance migration. Here we use a global dataset to evaluate differences in BMR between migrants and non-migrants, and to examine the effects of environmental variables. The BMR of migrant species is significantly higher than that of non-migrants. Intriguingly, while the elevated BMR of migrants on their breeding grounds may reflect the metabolic machinery required for long-distance movements, an alternative (and statistically stronger) explanation is their occupation of predominantly cold high-latitude breeding areas. Among several environmental predictors, average annual temperature has the strongest effect on BMR, with a 50% reduction associated with a 20 degrees C gradient. The negative effects of temperature variables on BMR hold separately for migrants and non-migrants and are not due their different climatic associations. BMR in migrants shows a much lower degree of phylogenetic inertia. Our findings indicate that migratory tendency need not necessarily be invoked to explain the higher BMR of migrants. A weaker phylogenetic signal observed in migrants supports the notion of strong phenotypic flexibility in this group which facilitates migration-related BMR adjustments that occur above and beyond environmental conditions. In contrast to the findings of previous analyses of mammalian BMR, primary productivity, aridity or precipitation variability do not appear to be important environmental correlates of avian BMR. The strong effects of temperature-related variables and varying phylogenetic effects reiterate the importance of addressing both broad-scale and individual-scale variation for understanding the determinants of BMR.     

Intraspecific correlations of basal and maximal metabolic rates in birds and the aerobic capacity model for the evolution of endothermy

The underlying assumption of the aerobic capacity model for the evolution of endothermy is that basal (BMR) and maximal aerobic metabolic rates are phenotypically linked. However, because BMR is largely a function of central organs whereas maximal metabolic output is largely a function of skeletal muscles, the mechanistic underpinnings for their linkage are not obvious. Interspecific studies in birds generally support a phenotypic correlation between BMR and maximal metabolic output. If the aerobic capacity model is valid, these phenotypic correlations should also extend to intraspecific comparisons. We measured BMR, M(sum) (maximum thermoregulatory metabolic rate) and MMR (maximum exercise metabolic rate in a hop-flutter chamber) in winter for dark-eyed juncos (Junco hyemalis), American goldfinches (Carduelis tristis; M(sum) and MMR only), and black-capped chickadees (Poecile atricapillus; BMR and M(sum) only) and examined correlations among these variables. We also measured BMR and M(sum) in individual house sparrows (Passer domesticus) in both summer, winter and spring. For both raw metabolic rates and residuals from allometric regressions, BMR was not significantly correlated with either M(sum) or MMR in juncos. Moreover, no significant correlation between M(sum) and MMR or their mass-independent residuals occurred for juncos or goldfinches. Raw BMR and M(sum) were significantly positively correlated for black-capped chickadees and house sparrows, but mass-independent residuals of BMR and M(sum) were not. These data suggest that central organ and exercise organ metabolic levels are not inextricably linked and that muscular capacities for exercise and shivering do not necessarily vary in tandem in individual birds. Why intraspecific and interspecific avian studies show differing results and the significance of these differences to the aerobic capacity model are unknown, and resolution of these questions will require additional studies of potential mechanistic links between minimal and maximal metabolic output.