Ontogenetic and interspecific scaling of consumption in insects

The uptake of resources from the environment is a basic feature of all life. Consumption rate has been found to scale with body size with an exponent close to unity across diverse organisms. However, past analyses have ignored the important distinction between ontogenetic and interspecific size comparisons. Using principles of dynamic energy budget theory, we present a mechanistic model for the body mass scaling of consumption, which separates interspecific size effects from ontogenetic size effects. Our model predicts uptake to scale with surface‐area (mass^2/3) during ontogenetic growth but more quickly (between mass^3/4 and mass¹) for interspecific comparisons. Available data for 41 insect species on consumption and assimilation during ontogeny provides strong empirical support for our theoretical predictions. Specifically, consumption rate scaled interspecifically with an exponent close to unity (0.89) but during ontogenetic growth scaled more slowly with an exponent of 0.70. Assimilation rate (consumption minus defecation) through ontogeny scaled more slowly than consumption due to a decrease in assimilation efficiency as insects grow. Our results highlight how body size imposes different constraints on metabolism depending on whether the size comparison is ontogenetic or inter‐specific. Synthesis One of the most robust patterns in biology is the effect of body size on metabolism – a relationship that underlies the rapidly emerging field of metabolic ecology. However, the precise energetic constraints imposed by body size have been notoriously difficult to entangle. Here we show that the constraints imposed on metabolism by body size are different depending on whether the size comparison is ontogenetic or interspecific. Using a single unifying theory of animal metabolism and a newly compiled data set on insect consumption and assimilation rates, we show that interspecific comparisons generally lead to the estimation of higher scaling exponents compared with ontogenetic comparisons. Our results help to explain large variation in estimated metabolic scaling exponents and will encourage future studies in metabolic ecology to make the important distinction between ontogenetic and evolutionary size changes.     

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 (b_R = scaling exponent approx. 1) to negative allometry (b_R < 1), or the reverse, are associated with significant changes in body shape (indexed by b_L = the scaling exponent of the relationship between body mass and body length). The observed inverse correlations between b_R and b_L 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 (b_A) further show that ontogenetic shifts in b_R and b_A are positively correlated. These results support new metabolic scaling theory based on SA influences that may be applied to ontogenetic shifts in b_R shown by many kinds of animals and plants.     

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.     

Scaling of metabolic rate in the lesser wax moth Achroia grisella does not fit the 3/4‐power law and shows significant sex differences

Allometric scaling of metabolic rates is commonly described as a power function and 0.75 is a widely accepted exponent. The universality of this exponent is in doubt and, particularly for insects, contradictory results have been obtained. Furthermore, sexual differences in scaling exponents are observed for several species that could lead to artefacts when they are not considered in intra‐ and interspecific scaling. Whether the metabolic scaling exponent in the lesser wax moth Achroia grisella differs significantly from 0.75 is tested, as well as whether it differs between the sexes. Adults of this moth neither feed nor drink, rendering them as suitable subjects for a study of metabolic rates. Neglecting sex differences, a metabolic scaling exponent of 0.8 is recorded. However, there are significant differences in metabolic scaling between the sexes. When considered separately, males scale with 0.96 and females with 0.67. Thus, in this species, a scaling exponent of 0.75 does not appear to exist either for males or females. The body size optimization model offers a potential explanation for the sex differences in metabolic scaling, although it remains to be tested in wax moths. With insects in particular, there is the need for more detailed studies on the scaling of metabolic rates that also take sexual differences into account.     

Intraspecific allometry of standard metabolic rate in green iguanas, Iguana iguana

To study the allometric relationship between standard metabolic rate and body mass (mass range 16-3627 g) in green iguanas, Iguana iguana (n=32), we measured rates of oxygen consumption (V(O(2))) at 30 degrees C during scotophase. The relationship could be described as: V(O(2))(ml h(-1))=0.478W(0.734). The resulting mass exponent was similar to the 3/4 power commonly used in interspecific curves (P>0.05), but differed from a proposed intraspecific value of 2/3 (P<0.05). The mass exponents of male (n=8) and female (n=11) iguanas did not differ (P>0.05). The mass adjusted V(O(2)) was higher than predicted from generalized squamate curves. The mean mass exponent of intra-individual allometric equations of iguanas (n=7) at varying masses during ontogeny did not differ from that of the pooled equation, indicating that scaling of V(O(2)) is similar for both between and within individuals. Thermal acclimation, compensatory changes in V(O(2)) with prolonged exposure to a constant temperature, was not observed in juvenile iguanas (n=11) between 1 and 5 weeks of acclimation at 30 degrees C.     

Beyond the '3/4-power law': variation in the intra- and interspecific scaling of metabolic rate in animals

In this review I show that the '3/4-power scaling law' of metabolic rate is not universal, either within or among animal species. Significant variation in the scaling of metabolic rate with body mass is described mainly for animals, but also for unicells and plants. Much of this variation, which can be related to taxonomic, physiological, and/or environmental differences, is not adequately explained by existing theoretical models, which are also reviewed. As a result, synthetic explanatory schemes based on multiple boundary constraints and on the scaling of multiple energy-using processes are advocated. It is also stressed that a complete understanding of metabolic scaling will require the identification of both proximate (functional) and ultimate (evolutionary) causes. Four major types of intraspecific metabolic scaling with body mass are recognized [based on the power function R=aMb, where R is respiration (metabolic) rate, a is a constant, M is body mass, and b is the scaling exponent]: Type I: linear, negatively allometric (b<1); Type II: linear, isometric (b=1); Type III: nonlinear, ontogenetic shift from isometric (b=1), or nearly isometric, to negatively allometric (b<1); and Type IV: nonlinear, ontogenetic shift from positively allometric (b>1) to one or two later phases of negative allometry (b<1). Ontogenetic changes in the metabolic intensity of four component processes (i.e. growth, reproduction, locomotion, and heat production) appear to be important in these different patterns of metabolic scaling. These changes may, in turn, be shaped by age (size)-specific patterns of mortality. In addition, major differences in interspecific metabolic scaling are described, especially with respect to mode of temperature regulation, body-size range, and activity level. A 'metabolic-level boundaries hypothesis' focusing on two major constraints (surface-area limits on resource/waste exchange processes and mass/volume limits on power production) can explain much, but not all of this variation. My analysis indicates that further empirical and theoretical work is needed to understand fully the physiological and ecological bases for the considerable variation in metabolic scaling that is observed both within and among species. Recommended approaches for doing this are discussed. I conclude that the scaling of metabolism is not the simple result of a physical law, but rather appears to be the more complex result of diverse adaptations evolved in the context of both physico-chemical and ecological constraints.     

Testing metabolic scaling theory using intraspecific allometries in Antarctic microarthropods

Quantitative scaling relationships among body mass, temperature and metabolic rate of organisms are still controversial, while resolution may be further complicated through the use of different and possibly inappropriate approaches to statistical analysis. We propose the application of a modelling strategy based on the theoretical approach of Akaike's information criteria and non‐linear model fitting (nlm). Accordingly, we collated and modelled available data at intraspecific level on the individual standard metabolic rate of Antarctic microarthropods as a function of body mass (M), temperature (T), species identity (S) and high rank taxa to which species belong (G) and tested predictions from metabolic scaling theory (mass‐metabolism allometric exponent b = 0.75, activation energy range 0.2–1.2 eV). We also performed allometric analysis based on logarithmic transformations (lm). Conclusions from lm and nlm approaches were different. Best‐supported models from lm incorporated T, M and S. The estimates of the allometric scaling exponent linking body mass and metabolic rate resulted in a value of 0.696 ± 0.105 (mean ± 95% CI). In contrast, the four best‐supported nlm models suggested that both the scaling exponent and activation energy significantly vary across the high rank taxa (Collembola, Cryptostigmata, Mesostigmata and Prostigmata) to which species belong, with mean values of b ranging from about 0.6 to 0.8. We therefore reached two conclusions: 1, published analyses of arthropod metabolism based on logarithmic data may be biased by data transformation; 2, non‐linear models applied to Antarctic microarthropod metabolic rate suggest that intraspecific scaling of standard metabolic rate in Antarctic microarthropods is highly variable and can be characterised by scaling exponents that greatly vary within taxa, which may have biased previous interspecific comparisons that neglected intraspecific variability.     

Intraspecific temperature dependence of the scaling of metabolic rate with body mass in fishes and its ecological implications

Metabolism constitutes a fundamental property of all organisms. Metabolic rate is commonly described to scale as a power function of body size and exponentially with temperature, thereby treating the effects of body size and temperature independently. Mounting evidence shows that the scaling of metabolic rate with body mass itself depends on temperature. Across‐species analyses in fishes suggest that the mass‐scaling exponent decreases with increasing temperature. However, whether this relationship holds at the within‐species level has rarely been tested. Here, we re‐analyse data on the metabolic rates of four freshwater fish species, two coregonids and two cyprinids, that cover wide ranges of body masses and their naturally experienced temperatures. We show that the standard metabolic rate of the coregonids is best fit when accounting for a linear temperature dependence of the scaling of metabolic rate with body mass, whereas a constant mass‐scaling exponent is supported in case of the cyprinids. Our study shows that phenotypic responses to temperature can result in temperature‐dependent scaling relationships at the species level and that these responses differ between taxa. Together with previous findings, these results indicate that evolutionarily adaptive and phenotypically plastic responses to temperature affect the scaling of metabolic rate with body mass in fishes.     

Allometric scaling of intraspecific space use

Allometric scaling relationships enable exploration of animal space-use patterns, yet interspecific studies cannot address many of the underlying mechanisms. We present the first intraspecific study of home range (HR) allometry relative to energetic requirements over several orders of magnitude of body mass, using as a model the predatory fish, pike Esox lucius. Analogous with interspecific studies, we show that space use increases more rapidly with mass (exponent = 1.08) than metabolic scaling theories predict. Our results support a theory that suggests increasing HR overlap with body mass explains many of these differences in allometric scaling of HR size. We conclude that, on a population scale, HR size and energetic requirement scale allometrically, but with different exponents.     

Effects of body mass and reproduction on the basal metabolic rate of brown long-eared bats (Plecotus auritus)

We measured basal metabolic rate (BMR) of nonreproductive and of breeding (pregnant and lactating) female brown long-eared bats (Plecotus auritus) to investigate the effects of intra- and interindividual variation in body mass and of reproduction on metabolism. The BMR of six nonreproductive females was measured between five and seven times at approximately 2-wk intervals over a period of 2.5 mo. There was a highly significant effect (P<0.001) of body mass on BMR of these nonreproductive females. The pooled within-individual scaling exponent (1.88) significantly exceeded the established mammalian interspecific exponent (0.75). In addition, we made single observations on 14 nonreproductive females to establish the effects of differences in mass between individuals. The mean BMR across all 14 individuals was 82 mW (+/-24 SD). There was a significant positive relationship between BMR and body mass across these individuals (r2=0.39), with a between-individual scaling exponent of 0.75. Inter- and intraindividual effects of mass on BMR were combined in a regression analysis that included mean body mass and deviation from mean mass on any given day as predictors. This regression model explained 55% of the variation in BMR. We made longitudinal measurements of BMR throughout reproduction and compared these with the predicted BMR of nonreproductive bats of the same body mass. Reproductive females exhibited temporal flexibility in BMR. BMR during pregnancy increased on a whole-animal basis but was significantly lower (by, on average, 15%) than BMR predicted for nonreproductive females of the same mass. Over a period of 1-75 d following birth, whole-animal BMR was greater than that during pregnancy, even though body mass declined after parturition. Hence, postbirth BMR was greater than the level predicted for nonreproductive females of the same mass. This study indicates that the scaling of BMR with body mass differs significantly within and between individuals and that there is a reduction of BMR in pregnancy and an elevation of BMR during lactation.     

Ontogenetic body-mass scaling of resting metabolic rate covaries with species-specific metabolic level and body size in spiders and snakes

According to common belief, metabolic rate usually scales with body mass to the 3/4-power, which is considered by some to be a universal law of nature. However, substantial variation in the metabolic scaling exponent (b) exists, much of which can be related to the overall metabolic level (L) of various taxonomic groups of organisms, as predicted by the recently proposed metabolic-level boundaries (MLB) hypothesis. Here the MLB hypothesis was tested using data for intraspecific (ontogenetic) body-mass scaling of resting metabolic rate in spiders and boid snakes. As predicted, in both animal groups b varies mostly between 2/3 and 1, and is significantly negatively related to L. L is, in turn, negatively related to species-specific body mass (M_m: estimated as the mass at the midpoint of a scaling relationship), and as a result, larger species tend to have steeper metabolic scaling slopes (b) than smaller species. After adjusting for the effects of M_m, b and L are still negatively related, though significantly only in the spiders, which exhibit a much wider range of L than the snakes. Therefore, in spiders and snakes the intraspecific scaling of metabolic rate with body mass itself scales with interspecific variation in both metabolic level and body mass.     

Scaling of the ballistic tongue apparatus in chameleons

Body dimensions of organisms can have a profound impact on their functional and structural properties. We examined the morphological proportions of the feeding apparatus of 105 chameleon specimens representing 23 species in seven genera, spanning a 1,000‐fold range in body mass to test whether the feeding apparatus conforms to the null hypotheses of geometric similarity that is based on the prevalence of geometric similarity in other ectothermic vertebrates. We used a phylogenetically corrected regression analysis based on a composite phylogenetic hypothesis to determine the interspecific scaling patterns of the feeding apparatus. We also determined the intraspecific (ontogenetic) scaling patterns for the feeding apparatus in three species. We found that both intraspecifically and interspecifically, the musculoskeletal components of the feeding apparatus scale isometrically among themselves, independent of body length. The feeding apparatus is thus of conserved proportions regardless of overall body length. In contrast, we found that the tongue apparatus as a whole and its musculoskeletal components scale with negative allometry with respect to snout‐vent length—smaller individuals have a proportionately larger feeding apparatus than larger individuals, both within and among species. Finally, the tongue apparatus as a whole scales with negative allometry with respect to body mass through ontogeny, but with isometry interspecifically. We suggest that the observed allometry may be maintained by natural selection because an enlarged feeding apparatus at small body size may maximize projection distance and the size of prey that smaller animals with higher mass‐specific metabolic rates can capture. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

A manipulative test of competing theories for metabolic scaling

The reasons why metabolic rate (B) scales allometrically with body mass (M) remain hotly debated. The field is dominated by correlational analyses of the relationship between B and M; these struggle to disentangle competing explanations because both B and M are confounded with ontogeny, life history, and ecology. Here, we overcome these problems by using an experimental approach to test among competing metabolic theories. We examined the scaling of B in size-manipulated and intact colonies of a bryozoan and show that B scales with M(0.5). To explain this, we apply a general model based on the dynamic energy budget theory for metabolic organization that predicts B on the basis of energy allocation to assimilation, maintenance, growth, and maturation. Uniquely, this model predicts the absolute value of B, emphasizes that there is no single scaling exponent of B, and demonstrates that a single model can explain the variation in B seen in nature.     

Ontogenic growth of the haemopoietic stem cell pool in humans

Recently, the size of the active stem cell pool has been predicted to scale allometrically with the adult mass of mammalian species with a 3/4 power exponent, similar to what has been found to occur for the resting metabolic rate across species. Here we investigate the allometric scaling of human haemopoietic stem cells (HSCs) during ontogenic growth and predict a linear scaling with body mass. We also investigate the allometric scaling of resting metabolic rate during growth in humans and find a linear scaling with mass similar to that of the haemopoietic stem cell pool. Our findings suggest a common underlying organizational principle determining the linear scaling of both the stem cell pool and resting metabolic rate with mass during ontogenic growth within the human species, combined with a 3/4 scaling with adult mass across mammalian species. It is possible that such common principles remain valid for haemopoiesis in other mammalian species.     

Ontogeny,function, and scaling of the mandibular symphysis in papionin primates

In vivo study of mastication in adult cercopithecine primates demonstrates a link between mandibular symphyseal form and resistance to “wishboning,” or lateral transverse bending. Mechanical consideration of wishboning at the symphysis indicates exponentially higher stresses along the lingual surface with increasing symphyseal curvature. Lengthening the anteroposterior width of the symphysis acts to resist these higher loads. Interspecific adult cercopithecine allometries show that both symphyseal curvature and symphyseal width exhibit positive allometry relative to body mass. The experimental and allometric data support an hypothesis that the cercopithecine mandibular symphysis is designed to maintain functional equivalence—in this case dynamic strain similarity—in wishboning stress and strain magnitudes across adult cercopithecines. We test the hypothesis that functional equivalence during masticatory wishboning is maintained throughout ontogeny by calculating relative stress estimates from morphometric dimensions of the mandibular symphysis in two cercopithecine primates, Macaca fascicularis and M. nemestrina. Results indicate no significant differences in relative stress estimates among the two macaque ontogenies and an interspecific sample of adult papionin primates. Further, relative stress estimates do not change significantly throughout ontogeny in either species. These results offer the first evidence for the maintenance of functional equivalence in stress and strain levels during postnatal growth in a habitually loaded cranial structure. Scaling analyses demonstrate significant slope differences for both symphyseal curvature and width between the ontogenetic and interspecific samples. The distinct interspecific cercopithecine slopes are realized by a series of ontogenetic transpositions in both symphyseal curvature and width. Throughout papionin ontogeny, symphyseal curvature increases with less negative allometry, while symphysis width increases with less positive allometry versus the interspecific pattern. As symphyseal curvature and width are inversely proportional to one another in estimating relative stresses, functionally equivalent stress levels are maintained both ontogenetically and interspecifically, because the relatively slower rate of allometric increase in symphyseal curvature during growth is compensated for by a slower rate of allometric increase in symphyseal width. These results indicate the primacy of maintaining functional equivalence during growth and the need for ontogenetic data in understanding the evolutionary processes that affect form–function relations as well as the interspecific patterning of adult form across a clade. J. Morphol. 235:157–175, 1998. © 1998 Wiley-Liss, Inc.     

Evolution of human growth prolongation

This investigation evaluates hypotheses that seek to explain temporal retardation or prolongation of human ontogeny. Current hypotheses that address this issue are poorly defined and conflate several distinct theoretical positions. A model that predicts homogeneity in the extension of human growth periods is evaluated. This model is contrasted with two alternatives. The first alternative predicts heterogeneity in the extension of human growth periods. The second anticipates that human growth prolongation is the result of the uniquely derived “insertion” of a human childhood period into an ancestral ontogenetic trajectory. Allometric analyses of body mass growth data from 21 species of anthropoid primates suggest that human female and male ontogenies often depart from patterns established by other primates, but these departures are not uniformly exceptional. Comparisons imply that derived changes in human growth are heterogeneous. Relative to interspecific expectations, early growth periods are much prolonged, but later growth periods are actually reduced. Moreover, the attributes of early growth periods, including growth rates, timing of growth events, and size-for-age, are highly variable across primates. Low correlations among growth periods suggest independence among growth phases. These analyses highlight minimal distinctions between competing models (heterogeneous extension and insertion hypotheses) that attempt to explain human growth prolongation. More important, the present study facilitates refinements of causal models that have been proposed to explain human growth prolongation. Specifically, human growth prolongation may be related to derived changes in patterns of brain development. Alternatively, metabolic factors may have exerted influences on human ontogeny. However, models that predict long growth periods as a byproduct of metabolic factors do not adequately explain temporal retardation of human ontogeny. Am J Phys Anthropol 107:331–350, 1998. © 1998 Wiley-Liss, Inc.     

Disparate Postnatal Ontogenies Do Not Add to the Shape Disparity of Infants

Integrating studies of ontogeny with analyses of disparity can reveal important and surprising insights into the origins of disparity and why it varies among groups. One such potentially surprising insight is that disparity could be constant over ontogeny even though species differ in both rates and timings of development and in their ontogenetic changes in shape. Several studies of both primates and rodents have concluded that disparity is generated prenatally although some have concluded that it arises postnatally. However, neither constancy nor an ontogenetic increase in disparity has been ever been rigorously documented for either primates or rodents. For a small sample of rodents, we show that species differ in their postnatal ontogenies but infants are neither more nor less disparate than adults and the major dimensions of disparity distinguishing the main clades also do not change. The constancy in both the level of disparity and its main dimensions does not result primarily from the subtlety of postnatal differences. Those differences are indeed subtle but the disparity in directions of ontogenetic shape change is nonetheless sufficient to increase shape disparity significantly. Disparity does not increase postnatally primarily because ontogenies are not strictly linear; disparity generated postnatally counteracts that produced earlier. What limits the progressive accumulation of disparity is the curvature of ontogenetic trajectories, a curvature presumably due to ontogenetic changes in the spatial distribution of rates of bone deposition and resorption.     

The routine metabolic rate of mulloway (Argyrosomus japonicus: Sciaenidae) and yellowtail kingfish (Seriola lalandi: Carangidae) acclimated to six different temperatures

This study compared the mass-specific routine metabolic rate (RMR) of similar sized mulloway (Argyrosomus japonicus), a sedentary species, and yellowtail kingfish (Seriola lalandi), a highly active species, acclimated at one of several temperatures ranging from 10–35 °C. Respirometry was carried out in an open-top static system and RMR corrected for seawater–atmosphere O₂ exchange using mass-balance equations. For both species RMR increased linearly with increasing temperature (T). RMR for mulloway was 5.78T − 29.0 mg O₂ kg^− 0.8 h^− 1 and for yellowtail kingfish was 12.11T − 39.40 mg O₂ kg^− 0.8 h^− 1. The factorial difference in RMR between mulloway and yellowtail kingfish ranged from 2.8 to 2.2 depending on temperature. The energetic cost of routine activity can be described as a function of temperature for mulloway as 1.93T − 9.68 kJ kg^− 0.8 day^− 1 and for yellowtail kingfish as 4.04T − 13.14 kJ kg^− 0.8 day^− 1. Over the full range of temperatures tested Q₁₀ values were approximately 2 for both species while Q₁₀ responses at each temperature increment varied considerably with mulloway and yellowtail kingfish displaying thermosensitivities indicative of each species respective niche habitat. RMR for mulloway was least thermally dependent at 28.5 °C and for yellowtail kingfish at 22.8 °C. Activation energies (E_a) calculated from Arrhenius plots were not significantly different between mulloway (47.6 kJ mol^− 1) and yellowtail kingfish (44.1 kJ mol^− 1).