Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals

Metabolic rate is commonly thought to scale with body mass (M) to the 3/4 power. However, the metabolic scaling exponent (b) may vary with activity state, as has been shown chiefly for interspecific relationships. Here I use a meta-analysis of literature data to test whether b changes with activity level within species of ectothermic animals. Data for 19 species show that b is usually higher during active exercise (mean ± 95% confidence limits = 0.918 ± 0.038) than during rest (0.768 ± 0.069). This significant upward shift in b to near 1 is consistent with the metabolic level boundaries hypothesis, which predicts that maximal metabolic rate during exercise should be chiefly influenced by volume-related muscular power production (scaling as M ¹). This dependence of b on activity level does not appear to be a simple temperature effect because body temperature in ectotherms changes very little during exercise.     

Testing metabolic ecology theory for allometric scaling of tree size, growth and mortality in tropical forests

The theory of metabolic ecology predicts specific relationships among tree stem diameter, biomass, height, growth and mortality. As demographic rates are important to estimates of carbon fluxes in forests, this theory might offer important insights into the global carbon budget, and deserves careful assessment. We assembled data from 10 old-growth tropical forests encompassing censuses of 367 ha and > 1.7 million trees to test the theory's predictions. We also developed a set of alternative predictions that retained some assumptions of metabolic ecology while also considering how availability of a key limiting resource, light, changes with tree size. Our results show that there are no universal scaling relationships of growth or mortality with size among trees in tropical forests. Observed patterns were consistent with our alternative model in the one site where we had the data necessary to evaluate it, and were inconsistent with the predictions of metabolic ecology in all forests.     

Testing the metabolic theory of ecology

The metabolic theory of ecology (MTE) predicts the effects of body size and temperature on metabolism through considerations of vascular distribution networks and biochemical kinetics. MTE has also been extended to characterise processes from cellular to global levels. MTE has generated both enthusiasm and controversy across a broad range of research areas. However, most efforts that claim to validate or invalidate MTE have focused on testing predictions. We argue that critical evaluation of MTE also requires strong tests of both its theoretical foundations and simplifying assumptions. To this end, we synthesise available information and find that MTE's original derivations require additional assumptions to obtain the full scope of attendant predictions. Moreover, although some of MTE's simplifying assumptions are well supported by data, others are inconsistent with empirical tests and even more remain untested. Further, although many predictions are empirically supported on average, work remains to explain the often large variability in data. We suggest that greater effort be focused on evaluating MTE's underlying theory and simplifying assumptions to help delineate the scope of MTE, generate new theory and shed light on fundamental aspects of biological form and function.     

Testing generalized allometries in allocation modeling within an individual-based simulation framework

The allocation of carbohydrates from photosynthesis to various plant compartments is a key process in ecophysiology and consequently an important element in process-based ecosystem modeling. In this study, we tested generalized empirical equations in a widely applied partitioning concept based on compartment-specific biomass allometries. For an 88-year chronosequence of European beech (Fagus sylvatica L.) in Austria, we used the individual-based hybrid forest model PICUS v1.4 to compare simulations employing foliage biomass functions at different levels of generalization against runs with site-specific parameterization and observations. Sensitivities of the individual tree model were generally in line with the original stand-level partitioning concept and ecological process understanding. While stand-level leaf area increased with increasing allocation to foliage, net primary productivity showed no significant response due to saturated radiation interception in the dense chronosequence stands. Strong sensitivities were revealed at the individual tree level, where favoring allocation to the foliage compartment resulted in increasing asymmetry of competition and height–diameter relationships. Applying a generalized parameterization based on data from the full range of continental species distribution resulted in a significant overestimation of mean tree height and subsequently standing volume stock at the chronosequence. At a lower hierarchical level of generality, however, simulations with a representative regional parameterization performed satisfactorily compared to model runs using the site-specific allometry. In relation to common accuracy demands, e.g., in forest management decision support, the study suggests the rejection of a generic parameterization while corroborating the use of regional generalizations in ecosystem models.     

Adaptive differences in plant physiology and ecosystem paradoxes: insights from metabolic scaling theory

The link between variation in species‐specific plant traits, larger scale patterns of productivity, and other ecosystem processes is an important focus for global change research. Understanding such linkages requires synthesis of evolutionary, biogeograpahic, and biogeochemical approaches to ecological research. Recent observations reveal several apparently paradoxical patterns across ecosystems. When compared with warmer low latitudes, ecosystems from cold northerly latitudes are described by (1) a greater temperature normalized instantaneous flux of CO₂ and energy; and (2) similar annual values of gross primary production (GPP), and possibly net primary production. Recently, several authors attributed constancy in GPP to historical and abiotic factors. Here, we show that metabolic scaling theory can be used to provide an alternative ‘biotically driven’ hypothesis. The model provides a baseline for understanding how potentially adaptive variation in plant size and traits associated with metabolism and biomass production in differing biomes can influence whole‐ecosystem processes. The implication is that one cannot extrapolate leaf/lab/forest level functional responses to the globe without considering evolutionary and geographic variation in traits associated with metabolism. We test one key implication of this model – that directional and adaptive changes in metabolic and stoichiometric traits of autotrophs may mediate patterns of plant growth across broad temperature gradients. In support of our model, on average, mass‐corrected whole‐plant growth rates are not related to differences in growing season temperature or latitude. Further, we show how these changes in autotrophic physiology and nutrient content across gradients may have important implications for understanding: (i) the origin of paradoxical ecosystem behavior; (ii) the potential efficiency of whole‐ecosystem carbon dynamics as measured by the quotient of system capacities for respiration, R, and assimilation, A; and (iii) the origin of several ‘ecosystem constants’– attributes of ecological systems that apparently do not vary with temperature (and thus with latitude). Together, these results highlight the potential critical importance of community ecology and functional evolutionary/physiological ecology for understanding the role of the biosphere within the integrated earth system.     

Ontogenetic scaling of metabolism, growth, and assimilation: testing metabolic scaling theory with Manduca sexta larvae

Metabolism, growth, and the assimilation of energy and materials are essential processes that are intricately related and depend heavily on animal size. However, models that relate the ontogenetic scaling of energy assimilation and metabolism to growth rely on assumptions that have yet to be rigorously tested. Based on detailed daily measurements of metabolism, growth, and assimilation in tobacco hornworms, Manduca sexta, we provide a first experimental test of the core assumptions of a metabolic scaling model of ontogenetic growth. Metabolic scaling parameters changed over development, in violation of the model assumptions. At the same time, the scaling of growth rate matches that of metabolic rate, with similar scaling exponents both across and within developmental instars. Rates of assimilation were much higher than expected during the first two instars and did not match the patterns of scaling of growth and metabolism, which suggests high costs of biosynthesis early in development. The rapid increase in size and discrete instars observed in larval insect development provide an ideal system for understanding how patterns of growth and metabolism emerge from fundamental cellular processes and the exchange of materials and energy between an organism and its environment.     

An analysis of epipubic bone function in mammals using scaling theory

Linear dimensions of epipubic bones in 61 species of metatherians and monotremes scale to mass differently in groups with or without marsupia, presumably reflecting emphasis on different but non-mutually exclusive functions. Sexual dimorphism of epipubic form exists. However, the allometric relationships of the epipubic bones of taxa that possess marsupia do not conform to the hypothesis that epipubic bones support the marsupium nearly as well as those without a marsupium. This observation renders a new hypothesis relating litter mass to epipubic form in taxa without marsupia. It appears that support of the marsupium is not the primary function or, at least, not the most proximate determinate of epipubic form in taxa with marsupia. The scaling of epipubic bone dimensions is consistent with the hypothesis that predicts epipubic bones serve to assist in locomotion by acting with the hypaxial muscles of the trunk and pectineus to protract the pelvic limbs. Epipubic length is shown to scale to maintain a mechanical advantage between these opposing muscle groups that approximates the rate that inertia of the hind limbs increases with total mass and speed of locomotion. This hypothesis provides an explanation for a skeletal element scaling significantly above geometric similarity. This observation has important theoretical significance as it suggests that skeletal architecture may, within limits, scale independently of mass-related stress.     

Organ-specific rates of cellular respiration in developing sunflower seedlings and their bearing on metabolic scaling theory

Fifty years ago Max Kleiber described what has become known as the "mouse-to-elephant" curve, i.e., a log-log plot of basal metabolic rate versus body mass. From these data, "Kleiber's 3/4 law" was deduced, which states that metabolic activity scales as the three fourths-power of body mass. However, for reasons unknown so far, no such "universal scaling law" has been discovered for land plants (embryophytes). Here, we report that the metabolic rates of four different organs (cotyledons, cotyledonary hook, hypocotyl, and roots) of developing sunflower (Helianthus annuus L.) seedlings grown in darkness (skotomorphogenesis) and in white light (photomorphogenesis) differ by a factor of 2 to 5 and are largely independent of light treatment. The organ-specific respiration rate (oxygen uptake per minute per gram of fresh mass) of the apical hook, which is composed of cells with densely packaged cytoplasm, is much higher than that of the hypocotyl, an organ that contains vacuolated cells. Data for cell length, cell density, and DNA content reveal that (1) hook opening in white light is caused by a stimulation of cell elongation on the inside of the curved organ, (2) respiration, cell density and DNA content are much higher in the hook than in the stem, and (3) organ-specific respiration rates and the DNA contents of tissues are statistically correlated. We conclude that, due to the heterogeneity of the plant body caused by the vacuolization of the cells, Kleiber's law, which was deduced using mammals as a model system, cannot be applied to embryophytes. In plants, this rule may reflect scaling phenomena at the level of the metabolically active protoplasmic contents of the cells.     

Phylogeny affects estimation of metabolic scaling in mammals

Abstract.— The relationship between body size and metabolic rate is a crucial issue in organismal biology and evolution. There has been considerable debate over whether the scaling exponent of the relationship is 0.75 (Kleiber's Law) or 0.67. Here we show that determination of this exponent for mammals depends on both the evolutionary tree and the regression model used in the comparative analysis. For example, more recent molecular-based phylogenies tend to support a 0.67 exponent, whereas older phylogenies, mostly based on morphological data, suggest a 0.75 exponent. However, molecular phylogenies yield more variable results than morphological phylogenies and thus are not currently helping to resolve the issue.     

Temporal metabolic rate variation in a continental Antarctic springtail

Terrestrial systems in Antarctica are characterized by substantial spatial and temporal variation. However, few studies have addressed the paucity of data on metabolic responses to the unpredictable Antarctic environment, particularly with regard to terrestrial biota. This study measured metabolic rate variation for individual springtails at a continental Antarctic site using a fiber-optic closed respirometry system incorporating a custom-made respiration chamber. Concurrent measures of (behavioural) activity were made via daily pitfall counts.Metabolic rate of Gomphiocephalus hodgsoni measured at constant temperature varied systematically with progression through the austral summer, and was greatest mid-season. This finding of clear intra-seasonal and temperature-independent variation in mass-specific metabolic rate in G. hodgsoni is one of very few such reports for a terrestrial invertebrate (and the only such study for Antarctica), and parallels physiological studies in the Antarctic marine environment linking metabolic rate elevation with biological function rather than temperature adaptation per se. However, response to temperature at relatively short time-scales is also likely to be an important part of the life history strategy of Antarctic terrestrial invertebrates such as G. hodgsoni, which appears capable of both physiologically and behaviourally ‘tuning’ in to short-term thermal variability to respond appropriately to the local unpredictable Antarctic habitat.     

Linking community size structure and ecosystem functioning using metabolic theory

Understanding how biogeochemical cycles relate to the structure of ecological communities is a central research question in ecology. Here we approach this problem by focusing on body size, which is an easily measured species trait that has a pervasive influence on multiple aspects of community structure and ecosystem functioning. We test the predictions of a model derived from metabolic theory using data on ecosystem metabolism and community size structure. These data were collected as part of an aquatic mesocosm experiment that was designed to simulate future environmental warming. Our analyses demonstrate significant linkages between community size structure and ecosystem functioning, and the effects of warming on these links. Specifically, we show that carbon fluxes were significantly influenced by seasonal variation in temperature, and yielded activation energies remarkably similar to those predicted based on the temperature dependencies of individual-level photosynthesis and respiration. We also show that community size structure significantly influenced fluxes of ecosystem respiration and gross primary production, particularly at the annual time-scale. Assessing size structure and the factors that control it, both empirically and theoretically, therefore promises to aid in understanding links between individual organisms and biogeochemical cycles, and in predicting the responses of key ecosystem functions to future environmental change.     

Influence of respirometry methods on intraspecific variation in standard metabolic rates in newts

Standard metabolic rate (SMR) is both a highly informative and variable trait. Variation in SMR stems not only from diverse intrinsic and extrinsic factors, but also from the use of diverse methods for metabolic measurements. We measured CO(2) production (VCO(2)) and oxygen consumption rates (VO(2)) using two flow-through respirometry modes, continuous and intermittent (stop-flow), to evaluate their potential contribution to SMR variation in Alpine newts, Ichthyosaura alpestris. Both respirometry modes yielded similar and repeatable VCO(2) values. Although VO(2) was highly repeatable, continuous respirometry produced lower VO(2) than the intermittent method. During intermittent measurements, the total number of activity bouts was higher than during continuous respirometry trials. Statistical correction for disparate activity levels minimized variation in oxygen consumption between respirometry modes. We conclude that use of either method of flow-through respirometry, if properly applied, introduced less noise to SMR estimates than a variation in activity levels.     

Joint multiple quantitative trait loci mapping for allometries of body compositions and metabolic traits to body weights in broiler

In order to map quantitative trait loci (QTLs) for allometries of body compositions and metabolic traits in chicken, we phenotypically characterize the allometric growths of multiple body components and metabolic traits relative to BWs using joint allometric scaling models and then establish random regression models (RRMs) to fit genetic effects of markers and minor polygenes derived from the pedigree on the allometric scalings. Prior to statistically inferring the QTLs for the allometric scalings by solving the RRMs, the LASSO technique is adopted to rapidly shrink most of marker genetic effects to zero. Computer simulation analysis confirms the reliability and adaptability of the so-called LASSO-RRM mapping method. In the F₂ population constructed by multiple families, we formulate two joint allometric scaling models of body compositions and metabolic traits, in which six of nine body compositions are tested as significant, while six of eight metabolic traits are as significant. For body compositions, a total of 14 QTLs, of which 9 dominant, were detected to be associated with the allometric scalings of drumstick, fat, heart, shank, liver and spleen to BWs; while for metabolic traits, a total of 19 QTLs also including 9 dominant be responsible for the allometries of T4, IGFI, IGFII, GLC, INS, IGR to BWs. The detectable QTLs or highly linked markers can be used to regulate relative growths of the body components and metabolic traits to BWs in marker-assisted breeding of chickens.     

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.     

Rensch's rule in large herbivorous mammals derived from metabolic scaling

Rensch's rule, which states that the magnitude of sexual size dimorphism tends to increase with increasing body size, has evolved independently in three lineages of large herbivorous mammals: bovids (antelopes), cervids (deer), and macropodids (kangaroos). This pattern can be explained by a model that combines allometry, life-history theory, and energetics. The key features are that female group size increases with increasing body size and that males have evolved under sexual selection to grow large enough to control these groups of females. The model predicts relationships among body size and female group size, male and female age at first breeding, death and growth rates, and energy allocation of males to produce body mass and weapons. Model predictions are well supported by data for these megaherbivores. The model suggests hypotheses for why some other sexually dimorphic taxa, such as primates and pinnipeds (seals and sea lions), do or do not conform to Rensh's rule.     

Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates

For more than a century, the scaling of animal metabolic rates with individual body masses and environmental temperature has predominantly been described by power-law and exponential relationships respectively. Many theories have been proposed to explain these scaling relationships, but were challenged by empirically documented curvatures on double-logarithmic scales. In the present study, we present a novel data set comprising 3661 terrestrial (mainly soil) invertebrate respiration rates from 192 independent sources across a wide range in body masses, environmental temperatures and phylogenetic groups. Although our analyses documented power-law and exponential scaling with body masses and temperature, respectively, polynomial models identified curved deviations. Interestingly, complex scaling models accounting for phylogenetic groups were able to remove curvatures except for a negative curvature at the highest temperatures (>30 °C) indicating metabolic down regulation. This might indicate that the tremendous differences in invertebrate body architectures, ecology and physiology may cause severely different metabolic scaling processes.     

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.