Interactive effects of intrinsic and extrinsic factors on metabolic rate.

Metabolism energizes all biological processes, and its tempo may importantly influence the ecological success and evolutionary fitness of organisms. Therefore, understanding the broad variation in metabolic rate that exists across the living world is a fundamental challenge in biology. To further the development of a more reliable and holistic picture of the causes of this variation, we review several examples of how various intrinsic (biological) and extrinsic (environmental) factors (including body size, cell size, activity level, temperature, predation and other diverse genetic, cellular, morphological, physiological, behavioural and ecological influences) can interactively affect metabolic rate in synergistic or antagonistic ways. Most of the interactive effects that have been documented involve body size, temperature or both, but future research may reveal additional 'hub factors'. Our review highlights the complex, intimate inter-relationships between physiology and ecology, knowledge of which can shed light on various problems in both disciplines, including variation in physiological adaptations, life histories, ecological niches and various organism-environment interactions in ecosystems. We also discuss theoretical and practical implications of interactive effects on metabolic rate and provide suggestions for future research, including holistic system analyses at various hierarchical levels of organization that focus on interactive proximate (functional) and ultimate (evolutionary) causal networks. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

The Relevance of Time in Biological Scaling.

Various phenotypic traits relate to the size of a living system in regular but often disproportionate (allometric) ways. These "biological scaling" relationships have been studied by biologists for over a century, but their causes remain hotly debated. Here, I focus on the patterns and possible causes of the body-mass scaling of the rates/durations of various biological processes and life-history events, i.e., the "pace of life". Many biologists have regarded the rate of metabolism or energy use as the master driver of the "pace of life" and its scaling with body size. Although this "energy perspective" has provided valuable insight, here I argue that a "time perspective" may be equally or even more important. I evaluate various major ways that time may be relevant in biological scaling, including as (1) an independent "fourth dimension" in biological dimensional analyses, (2) a universal "biological clock" that synchronizes various biological rates/durations, (3) a scaling method that uses various biological time periods (allochrony) as scaling metrics, rather than various measures of physical size (allometry), as traditionally performed, (4) an ultimate body-size-related constraint on the rates/timing of biological processes/events that is set by the inevitability of death, and (5) a geological "deep time" approach for viewing the evolution of biological scaling patterns. Although previously proposed universal four-dimensional space-time and "biological clock" views of biological scaling are problematic, novel approaches using allochronic analyses and time perspectives based on size-related rates of individual mortality and species origination/extinction may provide new valuable insights.

Variable metabolic scaling breaks the law: from 'Newtonian' to 'Darwinian' approaches.

Life's size and tempo are intimately linked. The rate of metabolism varies with body mass in remarkably regular ways that can often be described by a simple power function, where the scaling exponent (b, slope in a log-linear plot) is typically less than 1. Traditional theory based on physical constraints has assumed that b is 2/3 or 3/4, following natural law, but hundreds of studies have documented extensive, systematic variation in b. This overwhelming, law-breaking, empirical evidence is causing a paradigm shift in metabolic scaling theory and methodology from 'Newtonian' to 'Darwinian' approaches. A new wave of studies focuses on the adaptable regulation and evolution of metabolic scaling, as influenced by diverse intrinsic and extrinsic factors, according to multiple context-dependent mechanisms, and within boundary limits set by physical constraints.

Ontogenetic Changes in Body Shape and the Scaling of Metabolic Rate in the American Eel (Anguilla rostrata).

AbstractThe body mass (M) scaling of resting metabolic rate (RMR) may vary significantly throughout ontogeny for multiple reasons that are not perfectly understood. To compare two major geometric theories of metabolic scaling, surface area (SA) theory and resource transport network (RTN) theory, we tested whether ontogenetic shifts in metabolic scaling relate to changes in body shape in the American eel (Anguilla rostrata). To do so, we compared the log-linear scaling exponents of RMR to M (bR) and M to body length (bL) in juvenile and subadult eels (glass and yellow eel life stages, respectively). Glass eels exhibited a bL>3 and bR significantly <2/3, as predicted by SA theory. Yellow eels also had a bL>3, but their bR was not significantly different from 2/3 or 3/4. We hypothesize that two developmental changes contribute to bR being higher for yellow eels: (1) a greater reliance on branchial respiration than body-surface-dependent cutaneous respiration and (2) a lower rate of thickening during subadult growth. An ontogenetic decrease in the ratio of cutaneous to gill respiration may have increased the relative importance of the physical constraints of a single-pump, closed circulatory system on the body-size-dependent rate of resource supply to metabolizing tissues (as predicted by RTN theory) in subadult eels. Future research is needed to quantify these developmental changes and their potential mechanistic effects on metabolic scaling, especially in the elver, a critical life stage between the glass and yellow eel stages, that was not analyzed in this study.

How Metabolic Rate Relates to Cell Size.

Metabolic rate and its covariation with body mass vary substantially within and among species in little understood ways. Here, I critically review explanations (and supporting data) concerning how cell size and number and their establishment by cell expansion and multiplication may affect metabolic rate and its scaling with body mass. Cell size and growth may affect size-specific metabolic rate, as well as the vertical elevation (metabolic level) and slope (exponent) of metabolic scaling relationships. Mechanistic causes of negative correlations between cell size and metabolic rate may involve reduced resource supply and/or demand in larger cells, related to decreased surface area per volume, larger intracellular resource-transport distances, lower metabolic costs of ionic regulation, slower cell multiplication and somatic growth, and larger intracellular deposits of metabolically inert materials in some tissues. A cell-size perspective helps to explain some (but not all) variation in metabolic rate and its body-mass scaling and thus should be included in any multi-mechanistic theory attempting to explain the full diversity of metabolic scaling. A cell-size approach may also help conceptually integrate studies of the biological regulation of cellular growth and metabolism with those concerning major transitions in ontogenetic development and associated shifts in metabolic scaling.

Complications with body-size correction in comparative biology: possible solutions and an appeal for new approaches.

The magnitude of many kinds of biological traits relates strongly to body size. Therefore, a first step in comparative studies frequently involves correcting for effects of body size on the variation of a phenotypic trait, so that the effects of other biological and ecological factors can be clearly distinguished. However, commonly used traditional methods for making these body-size adjustments ignore or do not completely separate the causal interactive effects of body size and other factors on trait variation. Various intrinsic and extrinsic factors may affect not only the variation of a trait, but also its covariation with body size, thus making it difficult to remove completely the effect of body size in comparative studies. These complications are illustrated by several examples of how body size interacts with diverse developmental, physiological, behavioral and ecological factors to affect variation in metabolic rate both within and across species. Such causal interactions are revealed by significant effects of these factors on the body-mass scaling slope of metabolic rate. I discuss five possible major kinds of methods for removing body-size effects that attempt to overcome these complications, at least in part, but I hope that my Review will encourage the development of other, hopefully better methods for doing so.

A quantitative genetics perspective on the body-mass scaling of metabolic rate.

Widely observed allometric scaling (log-log slope<1) of metabolic rate (MR) with body mass (BM) in animals has been frequently explained using functional mechanisms, but rarely studied from the perspective of multivariate quantitative genetics. This is unfortunate, given that the additive genetic slope (bA) of the MR-BM relationship represents the orientation of the 'line of least genetic resistance' along which MR and BM may most likely evolve. Here, we calculated bA in eight species. Although most bA values were within the range of metabolic scaling exponents reported in the literature, uncertainty of each bA estimate was large (only one bA was significantly lower than 3/4 and none were significantly different from 2/3). Overall, the weighted average for bA (0.667±0.098 95% CI) is consistent with the frequent observation that metabolic scaling exponents are negatively allometric in animals (b<1). Although bA was significantly positively correlated with the phenotypic scaling exponent (bP) across the sampled species, bP was usually lower than bA, as reflected in a (non-significantly) lower weighted average for bP (0.596±0.100). This apparent discrepancy between bA and bP resulted from relatively shallow MR-BM scaling of the residuals [weighted average residual scaling exponent (be)=0.503±0.128], suggesting regression dilution (owing to measurement error and within-individual variance) causing a downward bias in bP. Our study shows how the quantification of the genetic scaling exponent informs us about potential constraints on the correlated evolution of MR and BM, and by doing so has the potential to bridge the gap between micro- and macro-evolutionary studies of scaling allometry.

Biological scaling analyses are more than statistical line fitting.

The magnitude of many biological traits relates strongly and regularly to body size. Consequently, a major goal of comparative biology is to understand and apply these 'size-scaling' relationships, traditionally quantified by using linear regression analyses based on log-transformed data. However, recently some investigators have questioned this traditional method, arguing that linear or non-linear regression based on untransformed arithmetic data may provide better statistical fits than log-linear analyses. Furthermore, they advocate the replacement of the traditional method by alternative specific methods on a case-by-case basis, based simply on best-fit criteria. Here, I argue that the use of logarithms in scaling analyses presents multiple valuable advantages, both statistical and conceptual. Most importantly, log-transformation allows biologically meaningful, properly scaled (scale-independent) comparisons of organisms of different size, whereas non-scaled (scale-dependent) analyses based on untransformed arithmetic data do not. Additionally, log-based analyses can readily reveal biologically and theoretically relevant discontinuities in scale invariance during developmental or evolutionary increases in body size that are not shown by linear or non-linear arithmetic analyses. In this way, log-transformation advances our understanding of biological scaling conceptually, not just statistically. I hope that my Commentary helps students, non-specialists and other interested readers to understand the general benefits of using log-transformed data in size-scaling analyses, and stimulates advocates of arithmetic analyses to show how they may improve our understanding of scaling conceptually, not just statistically.

Genome Size Covaries More Positively with Propagule Size than Adult Size: New Insights into an Old Problem.

The body size and (or) complexity of organisms is not uniformly related to the amount of genetic material (DNA) contained in each of their cell nuclei ('genome size'). This surprising mismatch between the physical structure of organisms and their underlying genetic information appears to relate to variable accumulation of repetitive DNA sequences, but why this variation has evolved is little understood. Here, I show that genome size correlates more positively with egg size than adult size in crustaceans. I explain this and comparable patterns observed in other kinds of animals and plants as resulting from genome size relating strongly to cell size in most organisms, which should also apply to single-celled eggs and other reproductive propagules with relatively few cells that are pivotal first steps in their lives. However, since body size results from growth in cell size or number or both, it relates to genome size in diverse ways. Relationships between genome size and body size should be especially weak in large organisms whose size relates more to cell multiplication than to cell enlargement, as is generally observed. The ubiquitous single-cell 'bottleneck' of life cycles may affect both genome size and composition, and via both informational (genotypic) and non-informational (nucleotypic) effects, many other properties of multicellular organisms (e.g., rates of growth and metabolism) that have both theoretical and practical significance.

Temperature effects on metabolic scaling of a keystone freshwater crustacean depend on fish-predation regime.

According to the metabolic theory of ecology, metabolic rate, an important indicator of the pace of life, varies with body mass and temperature as a result of internal physical constraints. However, various ecological factors may also affect metabolic rate and its scaling with body mass. Although reports of such effects on metabolic scaling usually focus on single factors, the possibility of significant interactive effects between multiple factors requires further study. In this study, we show that the effect of temperature on the ontogenetic scaling of resting metabolic rate of the freshwater amphipod Gammarus minus depends critically on habitat differences in predation regime. Increasing temperature tends to cause decreases in the metabolic scaling exponent (slope) in population samples from springs with fish predators, but increases in population samples from springs without fish. Accordingly, the temperature sensitivity of metabolic rate is not only size-specific, but also its relationship to body size shifts dramatically in response to fish predators. We hypothesize that the dampened effect of temperature on the metabolic rate of large adults in springs with fish, and of small juveniles in springs without fish are adaptive evolutionary responses to differences in the relative mortality risk of adults and juveniles in springs with versus without fish predators. Our results demonstrate a complex interaction among metabolic rate, body mass, temperature and predation regime. The intraspecific scaling of metabolic rate with body mass and temperature is not merely the result of physical constraints related to internal body design and biochemical kinetics, but rather is ecologically sensitive and evolutionarily malleable.

Effects of Fish Predators on the Mass-Related Energetics of a Keystone Freshwater Crustacean.

Little is known about how predators or their cues affect the acquisition and allocation of energy throughout the ontogeny of prey organisms. To address this question, we have been comparing the ontogenetic body-mass scaling of various traits related to energy intake and use between populations of a keystone amphipod crustacean inhabiting freshwater springs, with versus without fish predators. In this progress report, we analyze new and previously reported data to develop a synthetic picture of how the presence/absence of fish predators affects the scaling of food assimilation, fat content, metabolism, growth and reproduction in populations of Gammarus minus located in central Pennsylvania (USA). Our analysis reveals two major clusters of 'symmorphic allometry' (parallel scaling relationships) for traits related to somatic versus reproductive investment. In the presence of fish predators, the scaling exponents for somatic traits tend to decrease, whereas those for reproductive traits tend to increase. This divergence of scaling exponents reflects an intensified trade-off between somatic and reproductive investments resulting from low adult survival in the face of size-selective predation. Our results indicate the value of an integrated view of the ontogenetic size-specific energetics of organisms and its response to both top-down (predation) and bottom-up (resource supply) effects.

Ecological pressures and the contrasting scaling of metabolism and body shape in coexisting taxa: cephalopods versus teleost fish.

Metabolic rates are fundamental to many biological processes, and commonly scale with body size with an exponent ( bR) between 2/3 and 1 for reasons still debated. According to the 'metabolic-level boundaries hypothesis', bR depends on the metabolic level ( LR). We test this prediction and show that across cephalopod species intraspecific bR correlates positively with not only LR but also the scaling of body surface area with body mass. Cephalopod species with high LR maintain near constant mass-specific metabolic rates, growth and probably inner-mantle surface area for exchange of respiratory gases or wastes throughout their lives. By contrast, teleost fish show a negative correlation between bR and LR. We hypothesize that this striking taxonomic difference arises because both resource supply and demand scale differently in fish and cephalopods, as a result of contrasting mortality and energetic pressures, likely related to different locomotion costs and predation pressure. Cephalopods with high LR exhibit relatively steep scaling of growth, locomotion, and resource-exchange surface area, made possible by body-shape shifting. We suggest that differences in lifestyle, growth and body shape with changing water depth may be useful for predicting contrasting metabolic scaling for coexisting animals of similar sizes. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.

Ecology of ontogenetic body-mass scaling of gill surface area in a freshwater crustacean.

Several studies have documented ecological effects on intraspecific and interspecific body-size scaling of metabolic rate. However, little is known about how various ecological factors may affect the scaling of respiratory structures supporting oxygen uptake for metabolism. To our knowledge, our study is the first to provide evidence for ecological effects on the scaling of a respiratory structure among conspecific populations of any animal. We compared the body-mass scaling of gill surface area (SA) among eight spring-dwelling populations of the amphipod crustacean Gammarus minus Although gill SA scaling was not related to water temperature, conductivity or G. minus population density, it was significantly related to predation regime (and secondarily to pH). Body-mass scaling slopes for gill SA were significantly lower in four populations inhabiting springs with fish predators than for four populations in springs without fish (based on comparing means of the population slopes, or slopes calculated from pooled raw data for each comparison group). As a result, gill SA was proportionately smaller in adult amphipods from springs with versus without fish. This scaling difference paralleled similar differences in the scaling exponents for the rates of growth and resting metabolic rate. We hypothesized that gill SA scaling is shallower in fish-containing versus fishless spring populations of G. minus because of effects of size-selective predation on size-specific growth and activity that in turn affect the scaling of oxygen demand and concomitantly the gill capacity (SA) for oxygen uptake. Although influential theory claims that metabolic scaling is constrained by internal body design, our study builds on previous work to show that the scaling of both metabolism and the respiratory structures supporting it may be ecologically sensitive and evolutionarily malleable.

Ecological Influences and Morphological Correlates of Resting and Maximal Metabolic Rates across Teleost Fish Species.

Rates of aerobic metabolism vary considerably across evolutionary lineages, but little is known about the proximate and ultimate factors that generate and maintain this variability. Using data for 131 teleost fish species, we performed a large-scale phylogenetic comparative analysis of how interspecific variation in resting metabolic rates (RMRs) and maximum metabolic rates (MMRs) is related to several ecological and morphological variables. Mass- and temperature-adjusted RMR and MMR are highly correlated along a continuum spanning a 30- to 40-fold range. Phylogenetic generalized least squares models suggest that RMR and MMR are higher in pelagic species and that species with higher trophic levels exhibit elevated MMR. This variation is mirrored at various levels of structural organization: gill surface area, muscle protein content, and caudal fin aspect ratio (a proxy for activity) are positively related with aerobic capacity. Muscle protein content and caudal fin aspect ratio are also positively correlated with RMR. Hypoxia-tolerant lineages fall at the lower end of the metabolic continuum. Different ecological lifestyles are associated with contrasting levels of aerobic capacity, possibly reflecting the interplay between selection for increased locomotor performance on one hand and tolerance to low resource availability, particularly oxygen, on the other. These results support the aerobic capacity model of the evolution of endothermy, suggesting elevated body temperatures evolved as correlated responses to selection for high activity levels.

Body-Mass Scaling of Metabolic Rate: What are the Relative Roles of Cellular versus Systemic Effects?

The reason why metabolic rate often scales allometrically (disproportionately) with body mass has been debated for decades. A critical question concerns whether metabolic scaling is controlled intrinsically at the intracellular level or systemically at the organismal level. Recently, the relative importance of these effects has been tested by examining the metabolic rates of cultured dermal fibroblast and skeletal muscle cells in relation to donor body mass of a variety of birds and mammals. The lack of a relationship between in vitro cellular metabolic rates and body mass suggests that systemic effects, not intrinsic cellular effects are responsible for allometric metabolic scaling observed in whole organisms. Influential resource-transport network theory claims that the most important systemic effect involved is body-size related resource-supply limits to metabolizing cells. However, comparisons of in vitro cellular metabolic rates with scaling relationships for in vivo (basal) metabolic rates suggest that other systemic effects, such as body-size dependent biological regulation and tissue composition may also have major, perhaps more important effects. Furthermore, systemic effects must ultimately act at the cellular level, for example, by induced variation in the function, structure and intracellular densities of mitochondria. The mechanistic pathways involved require further study.

Shape shifting predicts ontogenetic changes in metabolic scaling in diverse aquatic invertebrates.

Metabolism fuels all biological activities, and thus understanding its variation is fundamentally important. Much of this variation is related to body size, which is commonly believed to follow a 3/4-power scaling law. However, during ontogeny, many kinds of animals and plants show marked shifts in metabolic scaling that deviate from 3/4-power scaling predicted by general models. Here, we show that in diverse aquatic invertebrates, ontogenetic shifts in the scaling of routine metabolic rate from near isometry (bR = scaling exponent approx. 1) to negative allometry (bR < 1), or the reverse, are associated with significant changes in body shape (indexed by bL = the scaling exponent of the relationship between body mass and body length). The observed inverse correlations between bR and bL are predicted by metabolic scaling theory that emphasizes resource/waste fluxes across external body surfaces, but contradict theory that emphasizes resource transport through internal networks. Geometric estimates of the scaling of surface area (SA) with body mass (bA) further show that ontogenetic shifts in bR and bA are positively correlated. These results support new metabolic scaling theory based on SA influences that may be applied to ontogenetic shifts in bR shown by many kinds of animals and plants.

Is metabolic rate a universal 'pacemaker' for biological processes?

A common, long-held belief is that metabolic rate drives the rates of various biological, ecological and evolutionary processes. Although this metabolic pacemaker view (as assumed by the recent, influential 'metabolic theory of ecology') may be true in at least some situations (e.g. those involving moderate temperature effects or physiological processes closely linked to metabolism, such as heartbeat and breathing rate), it suffers from several major limitations, including: (i) it is supported chiefly by indirect, correlational evidence (e.g. similarities between the body-size and temperature scaling of metabolic rate and that of other biological processes, which are not always observed) - direct, mechanistic or experimental support is scarce and much needed; (ii) it is contradicted by abundant evidence showing that various intrinsic and extrinsic factors (e.g. hormonal action and temperature changes) can dissociate the rates of metabolism, growth, development and other biological processes; (iii) there are many examples where metabolic rate appears to respond to, rather than drive the rates of various other biological processes (e.g. ontogenetic growth, food intake and locomotor activity); (iv) there are additional examples where metabolic rate appears to be unrelated to the rate of a biological process (e.g. ageing, circadian rhythms, and molecular evolution); and (v) the theoretical foundation for the metabolic pacemaker view focuses only on the energetic control of biological processes, while ignoring the importance of informational control, as mediated by various genetic, cellular, and neuroendocrine regulatory systems. I argue that a comprehensive understanding of the pace of life must include how biological activities depend on both energy and information and their environmentally sensitive interaction. This conclusion is supported by extensive evidence showing that hormones and other regulatory factors and signalling systems coordinate the processes of growth, metabolism and food intake in adaptive ways that are responsive to an organism's internal and external conditions. Metabolic rate does not merely dictate growth rate, but is coadjusted with it. Energy and information use are intimately intertwined in living systems: biological signalling pathways both control and respond to the energetic state of an organism. This review also reveals that we have much to learn about the temporal structure of the pace of life. Are its component processes highly integrated and synchronized, or are they loosely connected and often discordant? And what causes the level of coordination that we see? These questions are of great theoretical and practical importance.