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.     

Flightless rails endemic to islands have lower energy expenditures and clutch sizes than flighted rails on islands and continents

Data are presented on the standard energetics of six flighted and five flightless species of rails (Aves: Rallidae). The factors influencing these data and those from three additional species available from the literature, one of which was flightless, are examined. Basal rate of metabolism correlates with body mass, residency on islands or continents, volant condition, pectoral muscle mass, and food habits, but not with climate. The greatest capacity (96.2%) to account for the variation in basal rate of metabolism in 15 populations that belong to the 14 species occurs when body mass, volant condition, and food habits are combined. Then flighted species have basal rates that average 1.38 times those of flightless species and herbivorous rails have basal rates that are 1.37 times those of omnivorous species, which means that, independent of body mass, flighted gallinules have basal rates that are 1.9 times those of flightless, omnivorous rails. Distribution, pectoral muscle mass, and flight ability cannot be combined in the same analysis because they code for similar information. The evolution of a flightless condition in rails requires the absence of eutherian predators, but has occurred in the presence of marsupial predators. Each of the six studied flightless rails independently evolved a flightless condition and a low basal rate, whereas the evolution of herbivory and an associated high basal rate evolved at least twice in these species. Flightless rails on islands have clutch sizes that are only about one-half those of flighted rails living on continents, the reduction in clutch size correlating with a reduction in basal rate of metabolism. Thermal conductance in rails is correlated with body mass and food habits: herbivorous rails had conductances that were 1.43 times those of omnivores, i.e., conductances are highest in species with the highest basal rates.     

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.     

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.     

The comparative energetics of 'caviomorph' rodents.

The energetics of 11 species of New World hystricognath ('caviomorph') rodents are presented and compared with data from the literature on 19 additional species. Log(10) body mass alone accounts for 94% of the variation in the log(10) basal rate of metabolism in caviomorphs. The residual variation in basal rate is correlated with the stratum on which species live: arboreal species have low basal rates; terrestrial and fossorial species have intermediate basal rates; and aquatic species have high basal rates. When stratum is not included in the analysis, folivores, especially those that are arboreal, have lower basal rates than species with other food habits when combined with log(10) body mass. Small island endemics, all of which are folivores, have basal rates that are 61% of continental species. Log(10) basal rate correlates with family affiliation when combined with log(10) mass, but only if no other factor is included. Therefore, caviomorphs with low basal rates are arboreal, folivorous, live on small islands and belong to the Capromyidae, whereas other character combinations are associated with higher basal rates. These observations demonstrate that the basal rates of caviomorphs reflect many factor interactions. No differences in basal rate were found to reflect climate. Log(10) mass, the only factor to correlate with conductance, accounts for 82% of the variation in log(10) minimal thermal conductance. Mean interspecific body temperature was 36.9 degrees C; it was lowest in aquatic and fossorial species.     

The evolution of energetics in eutherian “insectivorans”: an alternate approach

An analysis of standard energetics in 57 species of “insectivorans”, small eutherians that preferentially feed on soil invertebrates, indicated that a combination of climate, the use of torpor, substrate, food habits, and log₁₀ body mass accounted for 92.5% of the variation in log10 basal rate of metabolism in insectivorans, whereas log₁₀ body mass alone accounted for 76.7% of the variation. With the addition of subfamily affiliation, this analysis accounted for 95.5% of the variation in log₁₀ basal rate, the most distinctive subfamilies being Soricinae and the Talpinae, which have equally high basal rates.Sorex species have basal rates that average 2.5 times those of tropical crocidurines, reflecting an approach bySorex to life in cold climates that does not include the use of torpor, a stratagem widely used by crocidurines in warm-temperate and tropical climates. The absence of torpor inSorex may facilitate a high reproductive rate through a high basal rate of metabolism, a combination that may be incompatible with a small mass, insectivorous food habits, and life in the lowland tropics, but required in cold-temperate environments. Insectivorans other than shrews, moles, and cold-temperature hedgehogs have low basal rates principally in association with tropical distributions and the use of torpor. Basal rate of metabolism in insectivorans also correlated with ordinal, familial, subfamilial, and tribal affiliations. The suggestion that phylogeny is an important determinant of performance characters like rate of metabolism ignores the requirement that performance must be compatible with conditions in the environment and with a species’ other characteristics. The principal reason why performance characters are correlated with taxonomic affiliation is that many clades consist of species that share a common approach to the environment. Thus, clades not only represent evolutionary histories, they also are crude measures of physiological and behavioral performances.     

哺乳动物基础代谢率的主要影响因素

综述了影响哺乳动物基础代谢率的主要因素, 包括体重、系统发育、食性、气候和栖息地、季节、生活习性和繁殖, 以及激素、器官、线粒体和质子漏的理化特征等, 并对这些因素可能的作用机理进行了简要的分析。     

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.     

影响食肉目动物能量学的生态因子

在食肉目的62种动物中,体重的变异可以解释基础代谢率86.8%的变化。当栖息基底、食性、生境和纬度等4个因素与体重合起来一起分析,则可以解释基础代谢率98.7%的变化,即这些生态和行为因子可以解释代谢率残差变异的81.1%。身体成分也是影响基础代谢率的另一个因素,可以解释一些大型树栖种类的较低的代谢率。除体重因素外,导致真兽类基础代谢率变异的主要原因是:当生态因素适合时,高水平的能量消耗可以促进动物的高繁殖输出,而动物的某些习性和生存环境则会要求低能量消耗,从而使繁殖率降低。当以科为单元进行分析时,对结果没有影响。生理参数与分类单元之间大多数的相关性反映了生态和行为因素与分类系统之间的一种粗略的相关关系。除非系统学可以反映动物的生态学和行为学,否则系统学不能决定动物适应性特征的状态     

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.     

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 metabolic rate and risk‐taking behaviour in birds

Basal metabolic rate (BMR) constitutes the minimal metabolic rate in the zone of thermo‐neutrality, where heat production is not elevated for temperature regulation. BMR thus constitutes the minimum metabolic rate that is required for maintenance. Interspecific variation in BMR in birds is correlated with food habits, climate, habitat, flight activity, torpor, altitude, and migration, although the selective forces involved in the evolution of these presumed adaptations are not always obvious. I suggest that BMR constitutes the minimum level required for maintenance, and that variation in this minimum level reflects the fitness costs and benefits in terms of ability to respond to selective agents like predators, implying that an elevated level of BMR is a cost of wariness towards predators. This hypothesis predicts a positive relationship between BMR and measures of risk taking such as flight initiation distance (FID) of individuals approached by a potential predator. Consistent with this suggestion, I show in a comparative analysis of 76 bird species that species with higher BMR for their body mass have longer FID when approached by a potential predator. This effect was independent of potentially confounding variables and similarity among species due to common phylogenetic descent. These results imply that BMR is positively related to risk‐taking behaviour, and that predation constitutes a neglected factor in the evolution of BMR.     

Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide

Thousands of plant species worldwide are dependent on birds for pollination. While the ecology and evolution of interactions between specialist nectarivorous birds and the plants they pollinate is relatively well understood, very little is known on pollination by generalist birds. The flower characters of this pollination syndrome are clearly defined but the geographical distribution patterns, habitat preferences and ecological factors driving the evolution of generalist‐bird‐pollinated plant species have never been analysed. Herein I provide an overview, compare the distribution of character states for plants growing on continents with those occurring on oceanic islands and discuss the environmental factors driving the evolution of both groups. The ecological niches of generalist‐bird‐pollinated plant species differ: on continents these plants mainly occur in habitats with pronounced climatic seasonality whereas on islands generalist‐bird‐pollinated plant species mainly occur in evergreen forests. Further, on continents generalist‐bird‐pollinated plant species are mostly shrubs and other large woody species producing numerous flowers with a self‐incompatible reproductive system, while on islands they are mostly small shrubs producing fewer flowers and are self‐compatible. This difference in character states indicates that diverging ecological factors are likely to have driven the evolution of these groups: on continents, plants that evolved generalist bird pollination escape from pollinator groups that tend to maintain self‐pollination by installing feeding territories in single flowering trees or shrubs, such as social bees or specialist nectarivorous birds. This pattern is more pronounced in the New compared to the Old World. By contrast, on islands, plants evolved generalist bird pollination as an adaptation to birds as a reliable pollinator group, a pattern previously known from plants pollinated by specialist nectarivorous birds in tropical mountain ranges. Additionally, I discuss the evolutionary origins of bird pollination systems in comparison to systems involving specialist nectarivorous birds and reconstruct the bird pollination system of Hawaii, which may represent an intermediate between a specialist and generalist bird pollination system. I also discuss the interesting case of Australia, where it is difficult to distinguish between specialist and generalist bird pollination systems.     

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.     

Adaptation of metabolism and evaporative water loss along an aridity gradient

Broad-scale comparisons of birds indicate the possibility of adaptive modification of basal metabolic rate (BMR) and total evaporative water loss (TEWL) in species from desert environments, but these might be confounded by phylogeny or phenotypic plasticity. This study relates variation in avian BMR and TEWL to a continuously varying measure of environment, aridity. We test the hypotheses that BMR and TEWL are reduced along an aridity gradient within the lark family (Alaudidae), and investigate the role of phylogenetic inertia. For 12 species of lark, BMR and TEWL decreased along a gradient of increasing aridity, a finding consistent with our proposals. We constructed a phylogeny for 22 species of lark based on sequences of two mitochondrial genes, and investigated whether phylogenetic affinity played a part in the correlation of phenotype and environment. A test for serial independence of the data for mass-corrected TEWL and aridity showed no influence of phylogeny on our findings. However, we did discover a significant phylogenetic effect in mass-corrected data for BMR, a result attributable to common phylogenetic history or to common ecological factors. A test of the relationship between BMR and aridity using phylogenetic independent constrasts was consistent with our previous analysis: BMR decreased with increasing aridity.     

Convergent, parallel and correlated evolution of trophic morphologies in the subfamily schizothoracinae from the Qinghai-Tibetan plateau

Schizothoracine fishes distributed in the water system of the Qinghai-Tibetan plateau (QTP) and adjacent areas are characterized by being highly adaptive to the cold and hypoxic environment of the plateau, as well as by a high degree of diversity in trophic morphology due to resource polymorphisms. Although convergent and parallel evolution are prevalent in the organisms of the QTP, it remains unknown whether similar evolutionary patterns have occurred in the schizothoracine fishes. Here, we constructed for the first time a tentative molecular phylogeny of the schizothoracine fishes based on the complete sequences of the cytochrome b gene. We employed this molecular phylogenetic framework to examine the evolution of trophic morphologies. We used Pagel's maximum likelihood method to estimate the evolutionary associations of trophic morphologies and food resource use. Our results showed that the molecular and published morphological phylogenies of Schizothoracinae are partially incongruent with respect to some intergeneric relationships. The phylogenetic results revealed that four character states of five trophic morphologies and of food resource use evolved at least twice during the diversification of the subfamily. State transitions are the result of evolutionary patterns including either convergence or parallelism or both. Furthermore, our analyses indicate that some characters of trophic morphologies in the Schizothoracinae have undergone correlated evolution, which are somewhat correlated with different food resource uses. Collectively, our results reveal new examples of convergent and parallel evolution in the organisms of the QTP. The adaptation to different trophic niches through the modification of trophic morphologies and feeding behaviour as found in the schizothoracine fishes may account for the formation and maintenance of the high degree of diversity and radiations in fish communities endemic to QTP.     

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.     

Insularity and the evolution of melanism,sexual dichromatism and body size in the worldwide‐distributed barn owl

Island biogeography has provided fundamental hypotheses in population genetics, ecology and evolutionary biology. Insular populations usually face different feeding conditions, predation pressure, intraspecific and interspecific competition than continental populations. This so‐called island syndrome can promote the evolution of specific phenotypes like a small (or large) body size and a light (or dark) colouration as well as influence the evolution of sexual dimorphism. To examine whether insularity leads to phenotypic differentiation in a consistent way in a worldwide‐distributed nonmigratory species, we compared body size, body shape and colouration between insular and continental barn owl (Tyto alba) populations by controlling indirectly for phylogeny. This species is suitable because it varies in pheomelanin‐based colouration from reddish‐brown to white, and it displays eumelanic black spots for which the number and size vary between individuals, populations and species. Females are on average darker pheomelanic and display more and larger eumelanic spots than males. Our results show that on islands barn owls exhibited smaller and fewer eumelanic spots and lighter pheomelanic colouration, and shorter wings than on continents. Sexual dimorphism in pheomelanin‐based colouration was less pronounced on islands than continents (i.e. on islands males tended to be as pheomelanic as females), and on small islands owls were redder pheomelanic and smaller in size than owls living on larger islands. Sexual dimorphism in the size of eumelanic spots was more pronounced (i.e. females displayed much larger spots than males) in barn owls living on islands located further away from a continent. Our study indicates that insular conditions drive the evolution towards a lower degree of eumelanism, smaller body size and affects the evolution of sexual dichromatism in melanin‐based colour traits. The effect of insularity was more pronounced on body size and shape than on melanic traits.     

Testing dynamic variance-sensitive foraging using individual differences in basal metabolic rates of zebra finches

Social foragers can alternate between searching for food (producer tactic), and searching for other individuals that have located food in order to join them (scrounger tactic). Both tactics yield equal rewards on average, but the rewards generated by producer are more variable. A dynamic variance-sensitive foraging model predicts that social foragers should increase their use of scrounger with increasing energy requirements and/or decreased food availability early in the foraging period. We tested whether natural variation in minimum energy requirements (basal metabolic rate or BMR) is associated with differences in the use of producer–scrounger foraging tactics in female zebra finches Taeniopygia guttata . As predicted by the dynamic variance-sensitive model, high BMR individuals had significantly greater use of the scrounger tactic compared with low BMR individuals. However, we observed no effect of food availability on tactic use, indicating that female zebra finches were not variance-sensitive foragers under our experimental conditions. This study is the first to report that variation in BMR within a species is associated with differences in foraging behaviour. BMR-related differences in scrounger tactic use are consistent with phenotype-dependent tactic use decisions. We suggest that BMR is correlated with another phenotypic trait which itself influences tactic use decisions.