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Understanding the effect of body size on flight costs is critical for the development of models of aerodynamics and animal energetics. Prior scaling studies that have shown that flight costs scale hypometrically have focused primarily on larger (>100 mg) insects and birds, but most flying species are smaller. We studied the flight physiology of 13 stingless bee species over a large range of body sizes (1–115 mg). Metabolic rate during hovering scaled hypermetrically (scaling slope = 2.11). Larger bees had warm thoraxes, while small bees were nearly ecothermic; however, even controlling for body temperature variation, flight metabolic rate scaled hypermetrically across this clade. Despite having a lower mass-specific metabolic rate during flight, smaller bees could carry the same proportional load. Wingbeat frequency did not vary with body size, in contrast to most studies that find wingbeat frequency increases as body size decreases. Smaller stingless bees have a greater relative forewing surface area, which may help them reduce the energy requirements needed to fly. Further, we hypothesize that the relatively larger heads of smaller species may change their body pitch in flight. Synthesizing across all flying insects, we demonstrate that the scaling of flight metabolic rate changes from hypermetric to hypometric at ∼58 mg body mass with hypermetic scaling below (slope = 1.2) and hypometric scaling (slope = 0.67) >58 mg in body mass. The reduced cost of flight likely provides selective advantages for the evolution of small body size in insects. The biphasic scaling of flight metabolic rates and wingbeat frequencies in insects supports the hypothesis that the scaling of metabolic rate is closely related to the power requirements of locomotion and cycle frequencies.

 

Metabolism, a metric of the energy cost of behavior, plays a significant role in social evolution. Body size and metabolic scaling are coupled, and a socioecological pattern of increased body size is associated with dietary change and the formation of larger and more complex groups. These consequences of the adaptive radiation of animal societies beg questions concerning energy expenses, a substantial portion of which may involve the metabolic rates of brains that process social information. Brain size scales with body size, but little is understood about brain metabolic scaling. Social insects such as ants show wide variation in worker body size and morphology that correlates with brain size, structure, and worker task performance, which is dependent on sensory inputs and information-processing ability to generate behavior. Elevated production and maintenance costs in workers may impose energetic constraints on body size and brain size that are reflected in patterns of metabolic scaling. Models of brain evolution do not clearly predict patterns of brain metabolic scaling, nor do they specify its relationship to task performance and worker ergonomic efficiency, two key elements of social evolution in ants. Brain metabolic rate is rarely recorded and, therefore, the conditions under which brain metabolism influences the evolution of brain size are unclear. We propose that studies of morphological evolution, colony social organization, and worker ergonomic efficiency should be integrated with analyses of species-specific patterns of brain metabolic scaling to advance our understanding of brain evolution in ants.

 

Metabolism is a fundamental attribute of all organisms that influences how species affect and are affected by their natural environment. Differences between sexes in ectothermic species may substantially alter metabolic scaling patterns, particularly in viviparous or live-bearing species where females must support their basal metabolic costs and that of their embryos. Indeed, if pregnancy is associated with marked increases in metabolic demand and alters scaling patterns between sexes, this could in turn interact with natural sex ratio variation in nature to affect population-level energy demand. Here, we aimed to understand how sex and pregnancy influence metabolic scaling and how differences between sexes affect energy demand in Gambusia affinis (Western mosquitofish). Using the same method, we measured routine metabolic rate in the field on reproductively active fish and in the laboratory on virgin fish. Our data suggest that changes in energy expenditure related to pregnancy may lead to steeper scaling coefficients in females (b = 0.750) compared to males (b = 0.595). In contrast, virgin females and males had similar scaling coefficients, suggesting negligible sex differences in metabolic costs in reproductively inactive fish. Further, our data suggest that incorporating sex differences in allometric scaling may alter population-level energy demand by as much as 20–28%, with the most pronounced changes apparent in male-biased populations due to the lower scaling coefficient of males. Overall, our data suggest that differences in energy investment in reproduction between sexes driven by pregnancy may alter allometric scaling and population-level energy demand.

 

Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g., basal, resting, field, and maximally active). The scaling of metabolism is usually highly correlated with the scaling of many life-history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to (a) lower contents of expensive tissues (brains, liver, and kidneys), and (b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. An additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include (1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries; (2) studies linking scaling to ecological or phylogenetic context; (3) studies that consider multiple, possibly interacting hypotheses; and (4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate, and reproduction.

 

Abstract Females and males can exhibit striking differences in body size, relative trait size, physiology, and behavior. As a consequence, the sexes can have very different rates of whole-body energy use, or converge on similar rates through different physiological mechanisms. Yet many studies that measure the relationship between metabolic rate and body size only pay attention to a single sex (more often males), or do not distinguish between sexes. We present four reasons why explicit attention to energy-use between the sexes can yield insight into the physiological mechanisms that shape broader patterns of metabolic scaling in nature. First, the sexes often differ considerably in their relative investment in reproduction, which shapes much of life-history and rates of energy use. Second, males and females share a majority of their genome but may experience different selective pressures. Sex-specific energy profiles can reveal how the energetic needs of individuals are met despite the challenge of within-species genetic constraints. Third, sexual selection often pushes growth and behavior to physiological extremes. Exaggerated sexually selected traits are often most prominent in one sex, can comprise up to 50% of body mass, and thus provide opportunities to uncover energetic constraints of trait growth and maintenance. Finally, sex-differences in behavior such as mating-displays, long-distance dispersal, and courtship can lead to drastically different energy allocation among the sexes; the physiology to support this behavior can shape patterns of metabolic scaling. The mechanisms underlying metabolic scaling in females, males, and hermaphroditic animals can provide opportunities to develop testable predictions that enhance our understanding of energetic scaling patterns in nature. 

Synopsis New biophysical theory and electronic databases raise the prospect of deriving fundamental rules of life, a conceptual framework for how the structures and functions of molecules, cells, and individual organisms give rise to emergent patterns and processes of ecology, evolution, and biodiversity. This framework is very general, applying across taxa of animals from 10–10 g protists to 108 g whales, and across environments from deserts and abyssal depths to rain forests and coral reefs. It has several hallmarks: (1) Energy is the ultimate limiting resource for organisms and the currency of biological fitness. (2) Most organisms are nearly equally fit, because in each generation at steady state they transfer an equal quantity of energy (˜22.4 kJ/g) and biomass (˜1 g/g) to surviving offspring. This is the equal fitness paradigm (EFP). (3) The enormous diversity of life histories is due largely to variation in metabolic rates (e.g., energy uptake and expenditure via assimilation, respiration, and production) and biological times (e.g., generation time). As in standard allometric and metabolic theory, most physiological and life history traits scale approximately as quarter-power functions of body mass, m (rates as ∼m–1/4 and times as ∼m1/4), and as exponential functions of temperature. (4) Time is the fourth dimension of life. Generation time is the pace of life. (5) There is, however, considerable variation not accounted for by the above scalings and existing theories. Much of this “unexplained” variation is due to natural selection on life history traits to adapt the biological times of generations to the clock times of geochronological environmental cycles. (6) Most work on biological scaling and metabolic ecology has focused on respiration rate. The emerging synthesis applies conceptual foundations of energetics and the EFP to shift the focus to production rate and generation time. 

Abstract Size at the start of life reflects the initial per offspring parental investment—including both the embryo and the nutrients supplied to it. Initial offspring size can vary substantially, both within and among species. Within species, increasing offspring size can enhance growth, reproduction, competitive ability, and reduce susceptibility to predation and starvation later in life, that can ultimately increase fitness. Previous work has suggested that the fitness benefits of larger offspring size may be driven by energy expenditure during development—or how offspring metabolic rate scales with offspring size. Despite the importance of early-life energy expenditure in shaping later life fitness trajectories, consideration of among-species scaling of metabolic rate at the time of birth as a potential source of general metabolic scaling patterns has been overlooked by theory. Here, we review the patterns and processes of energy expenditure at the start of life when mortality is often greatest. We compile existing data on metabolic rate and offspring size for 191 ectotherm species spanning eight phyla and use phylogenetically controlled methods to quantify among-species scaling patterns. Across a 109-fold mass range, we find that offspring metabolic rate scales hypometrically with size, with an overall scaling exponent of 0.66. This exponent varies across ontogenetic stage and feeding activity, but is consistently hypometric, including across environmental temperatures. Despite differences in parental investment, life history and habitat, large-offspring species use relatively less energy as a proportion of size, compared with small-offspring species. Greater residual energy can be used to fuel the next stages of life, particularly in low-resource environments. Based on available evidence, we conclude that, while large knowledge gaps remain, the evolution of offspring size is likely shaped by context-dependent selection acting on correlated traits, including metabolic rates maintaining hypometric scaling, which operates within broader physical constraints. 

Abstract Reinvasion of the oceans beginning 10–60 million years ago by ancient mammals instigated one of the most remarkable metabolic transitions across evolutionary time. A consequence of marine living, especially in colder waters, has been a 1.4–2.9-fold increase in resting metabolic rate (RMR) for otters, pinnipeds, and cetaceans over predicted levels for terrestrial mammals of similar body mass. Notably, the greatest metabolic elevation occurred in the smallest marine mammals, suggesting an underlying thermal causative mechanism. Superimposed on these resting costs are the metabolic demands of locomotion. Collectively termed the field metabolic rate (FMR), such active costs consistently approach three times the resting rates of individuals regardless of locomotor style, species, foraging patterns, habitat, or geographic location. In wild non-reproducing mammals, the FMR/RMR ratio averages 2.6–2.8 for both terrestrial and marine species, with the latter group maintaining larger absolute daily metabolic rates supported by comparatively higher food ingestion rates. Interestingly, the limit for habitual (multi-day), sustained maximal energy expenditure in human endurance athletes averages <3.0 times resting metabolic levels, with a notable exception in Tour de France cyclists. Importantly, both athletes and wild mammals seem similarly constrained; that is, by the ability to process enough calories in a day to support exceptional metabolic performance. 

Abstract Metabolic rate (MR) usually changes (scales) out of proportion to body mass (BM) as MR = aBMb, where a is a normalisation constant and b is the scaling exponent that reflects how steep this change is. This scaling relationship is fundamental to biology, but over a century of research has provided little consensus on the value of b, and why it appears to vary among taxa and taxonomic levels. By analysing published data on fish and taking an individual-based approach to metabolic scaling, I show that variation in growth of fish under naturally restricted food availability can explain variation in within-individual (ontogenetic) b for standard (maintenance) metabolic rate (SMR) of brown trout (Salmo trutta), with the fastest growers having the steepest metabolic scaling (b ≈ 1). Moreover, I show that within-individual b can vary much more widely than previously assumed from work on different individuals or different species, from –1 to 1 for SMR among individual brown trout. The negative scaling of SMR for some individuals was caused by reductions in metabolic rate in a food limited environment, likely to maintain positive growth. This resulted in a mean within-individual b for SMR that was significantly lower than the across-individual (“static”) b, a difference that also existed for another species, cunner (Tautogolabrus adspersus). Interestingly, the wide variation in ontogenetic b for SMR among individual brown trout did not exist for maximum (active) metabolic rate (MMR) of the same fish, showing that these two key metabolic traits (SMR and MMR) can scale independently of one another. I also show that across-species (“evolutionary”) b for SMR of 134 fishes is significantly steeper (b approaching 1) than the mean ontogenetic b for the brown trout and cunner. Based on these interesting findings, I hypothesise that evolutionary and static metabolic scaling can be systematically different from ontogenetic scaling, and that the steeper evolutionary than ontogenetic scaling for fishes arises as a by-product of natural selection for fast-growing individuals with steep metabolic scaling (b ≈ 1) early in life, where size-selective mortality is high for fishes. I support this by showing that b for SMR tends to increase with natural mortality rates of fish larvae within taxa.