Body mass scaling of passive oxygen diffusion in endotherms and ectotherms.

The area and thickness of respiratory surfaces, and the constraints they impose on passive oxygen diffusion, have been linked to differences in oxygen consumption rates and/or aerobic activity levels in vertebrates. However, it remains unclear how respiratory surfaces and associated diffusion rates vary with body mass across vertebrates, particularly in relation to the body mass scaling of oxygen consumption rates. Here we address these issues by first quantifying the body mass dependence of respiratory surface area and respiratory barrier thickness for a diversity of endotherms (birds and mammals) and ectotherms (fishes, amphibians, and reptiles). Based on these findings, we then use Fick's law to predict the body mass scaling of oxygen diffusion for each group. Finally, we compare the predicted body mass dependence of oxygen diffusion to that of oxygen consumption in endotherms and ectotherms. We find that the slopes and intercepts of the relationships describing the body mass dependence of passive oxygen diffusion in these two groups are statistically indistinguishable from those describing the body mass dependence of oxygen consumption. Thus, the area and thickness of respiratory surfaces combine to match oxygen diffusion capacity to oxygen consumption rates in both air- and water-breathing vertebrates. In particular, the substantially lower oxygen consumption rates of ectotherms of a given body mass relative to those of endotherms correspond to differences in oxygen diffusion capacity. These results provide insights into the long-standing effort to understand the structural attributes of organisms that underlie the body mass scaling of oxygen consumption.

A broad-scale comparison of aerobic activity levels in vertebrates: endotherms versus ectotherms.

Differences in the limits and range of aerobic activity levels between endotherms and ectotherms remain poorly understood, though such differences help explain basic differences in species' lifestyles (e.g. movement patterns, feeding modes, and interaction rates). We compare the limits and range of aerobic activity in endotherms (birds and mammals) and ectotherms (fishes, reptiles, and amphibians) by evaluating the body mass-dependence of VO2 max, aerobic scope, and heart mass in a phylogenetic context based on a newly constructed vertebrate supertree. Contrary to previous work, results show no significant differences in the body mass scaling of minimum and maximum oxygen consumption rates with body mass within endotherms or ectotherms. For a given body mass, resting rates and maximum rates were 24-fold and 30-fold lower, respectively, in ectotherms than endotherms. Factorial aerobic scope ranged from five to eight in both groups, with scope in endotherms showing a modest body mass-dependence. Finally, maximum consumption rates and aerobic scope were positively correlated with residual heart mass. Together, these results quantify similarities and differences in the potential for aerobic activity among ectotherms and endotherms from diverse environments. They provide insights into the models and mechanisms that may underlie the body mass-dependence of oxygen consumption.

Temperature effects on virion volume and genome length in dsDNA viruses.

Heterogeneity in rates of survival, growth and reproduction among viruses is related to virus particle (i.e. virion) size, but we have little understanding of the factors that govern the four to five orders of magnitude in virus size variation. Here, we analyse variation in virion size in 67 double-stranded DNA viruses (i.e. dsDNA) that span all major biomes, and infect organisms ranging from single-celled prokaryotes to multicellular eukaryotes. We find that two metrics of virion size (i.e. virion volume and genome length) decrease by about 55-fold as the temperature of occurrence increases from 0 to 40°C. We also find that gene overlap increases exponentially with temperature, such that smaller viruses have proportionally greater gene overlap at higher temperatures. These results indicate dsDNA virus size increases with environmental temperature in much the same way as the cell or genome size of many host species.

Energetics of stress: linking plasma cortisol levels to metabolic rate in mammals.

Physiological stress may result in short-term benefits to organismal performance, but also long-term costs to health or longevity. Yet, we lack an understanding of the variation in stress hormone levels (i.e. glucocorticoids) that exist within and across species. Here, we present comparative analyses that link the primary stress hormone in most mammals (i.e. cortisol) to metabolic rate. We show that baseline concentrations of plasma cortisol vary with mass-specific metabolic rate among cortisol-dominant mammals, and both baseline and elevated concentrations scale predictably with body mass. The results quantitatively link a classical measure of physiological stress to whole-organism energetics, providing a point of departure for cross-species comparisons of stress levels among mammals.

Telomeres and the Rate of Living: Linking Biological Clocks of Senescence.

AbstractTwo prominent theories of aging, one based on telomere dynamics and the other on mass-specific energy flux, propose biological time clocks of senescence. The relationship between these two theories, and the biological clocks proposed by each, remains unclear. Here, we examine the relationships between telomere shortening rate, mass-specific metabolic rate, and lifespan among vertebrates (mammals, birds, fishes). Results show that telomere shortening rate increases linearly with mass-specific metabolic rate and decreases nonlinearly with increasing body mass in the same way as mass-specific metabolic rate. Results also show that both telomere shortening rate and mass-specific metabolic rate are similarly related to lifespan and that both strongly predict differences in lifespan, although the slopes of the relationships are less than linear. On average, then, telomeres shorten a fixed amount per unit of mass-specific energy flux. So the mitotic clock of telomere shortening and the energetics-based clock described by metabolic rate can be viewed as alternative measures of the same biological clock. These two processes may be linked, we speculate, through the process of cell division.

Biological scaling: does the exception prove the rule?

Reich et al. report that the whole-plant respiration rate, R, in seedlings scales linearly with plant mass, M, so that R=C(R)M(theta) when theta approximately 1, in which c(R) is the scaling normalization and theta is the scaling exponent. They also state that because nitrogen concentration (N) is correlated with c(R), variation in N is a better predictor of R than M would be. Reich et al. and Hedin incorrectly claim that these "universal" findings question the central tenet of metabolic scaling theory, which they interpret as predicting theta = (3/4), irrespective of the size of the plant. Here we show that these conclusions misrepresent metabolic scaling theory and that their results are actually consistent with this theory.

Energetic basis of colonial living in social insects.

Understanding the ecology and evolution of insect societies requires greater knowledge of how sociality affects the performance of whole colonies. Metabolic scaling theory, based largely on the body mass scaling of metabolic rate, has successfully predicted many aspects of the physiology and life history of individual (or unitary) organisms. Here we show, using a diverse set of social insect species, that this same theory predicts the size dependence of basic features of the physiology (i.e., metabolic rate, reproductive allocation) and life history (i.e., survival, growth, and reproduction) of whole colonies. The similarity in the size dependence of these features in unitary organisms and whole colonies points to commonalities in functional organization. Thus, it raises an important question of how such evolutionary convergence could arise through the process of natural selection.

Energetic and biomechanical constraints on animal migration distance.

Animal migration is one of the great wonders of nature, but the factors that determine how far migrants travel remain poorly understood. We present a new quantitative model of animal migration and use it to describe the maximum migration distance of walking, swimming and flying migrants. The model combines biomechanics and metabolic scaling to show how maximum migration distance is constrained by body size for each mode of travel. The model also indicates that the number of body lengths travelled by walking and swimming migrants should be approximately invariant of body size. Data from over 200 species of migratory birds, mammals, fish, and invertebrates support the central conclusion of the model - that body size drives variation in maximum migration distance among species through its effects on metabolism and the cost of locomotion. The model provides a new tool to enhance general understanding of the ecology and evolution of migration.

Explaining differences in the lifespan and replicative capacity of cells: a general model and comparative analysis of vertebrates.

A better understanding of the factors that govern individual cell lifespan and the replicative capacity of cells (i.e. Hayflick's limit) is important for addressing disease progression and ageing. Estimates of cell lifespan in vivo and the replicative capacity of cell lines in culture vary substantially both within and across species, but the underlying reasons for this variability remain unclear. Here, we address this issue by presenting a quantitative model of cell lifespan and cell replicative capacity. The model is based on the relationship between cell mortality and metabolic rate, which is supported with data for different cell types from ectotherms and endotherms. These data indicate that much of the observed variation in cell lifespan and cell replicative capacity is explained by differences in cellular metabolic rate, and thus by the three primary factors that control metabolic rate: organism size, organism temperature and cell size. Individual cell lifespan increases as a power law with both body mass and cell mass, and decreases exponentially with increasing temperature. The replicative capacity of cells also increases with body mass, but is independent of temperature. These results provide a point of departure for future comparative studies of cell lifespan and replicative capacity in the laboratory and in the field.

Towards a general life-history model of the superorganism: predicting the survival, growth and reproduction of ant societies.

Social insect societies dominate many terrestrial ecosystems across the planet. Colony members cooperate to capture and use resources to maximize survival and reproduction. Yet, when compared with solitary organisms, we understand relatively little about the factors responsible for differences in the rates of survival, growth and reproduction among colonies. To explain these differences, we present a mathematical model that predicts these three rates for ant colonies based on the body sizes and metabolic rates of colony members. Specifically, the model predicts that smaller colonies tend to use more energy per gram of biomass, live faster and die younger. Model predictions are supported with data from whole colonies for a diversity of species, with much of the variation in colony-level life history explained based on physiological traits of individual ants. The theory and data presented here provide a first step towards a more general theory of colony life history that applies across species and environments.

Predators, prey, and transient states in the assembly of spatially structured communities.

Ecological theory suggests that both dispersal limitation and resource limitation can exert strong effects on community assembly. However, empirical studies of community assembly have focused almost exclusively on communities with a single trophic level. Thus, little is known about the combined effects of dispersal and resource limitation on assembly of communities with multiple trophic levels. We performed a landscape-scale experiment using spatially arranged mesocosms to study effects of dispersal and resource limitation on the assembly dynamics of aquatic invertebrate communities with two trophic levels. We found that interplay between dispersal and resource limitation regulated the assembly of predator and prey trophic levels in these pond communities. Early in assembly, predators and prey were strongly dispersal limited, and resource (i.e., prey) availability did not influence predator colonization. Later in assembly, after predators colonized, resource limitation was the strongest driver of predator abundance, and dispersal limitation played a negligible role. Thus, habitat isolation affected predators directly by reducing predator colonization rate, and indirectly through the effect of distance on prey availability. Dispersal and resource limitation of predators resulted in a transient period in which predators were absent or rare in isolated habitats. This period may be important for understanding population dynamics of vulnerable prey species. Our findings demonstrate that dispersal and resource limitation can jointly regulate assembly dynamics in multi-trophic systems. They also highlight the need to develop a temporal picture of the assembly process in multi-trophic communities because the availability and spatial distribution of limiting resources (i.e., prey) and the distribution of predators can shift radically over time.

Host cell volume explains differences in the size of DsDNA viruses.

The nearly 3 orders of magnitude variation in size observed among double-stranded DNA viruses (dsDNA) has important ecological consequences, but the factors responsible for this variation remain poorly understood. Here we first evaluate if a relationship exists between the genome size of diverse dsDNA viruses and their hosts in single-celled organisms (prokaryotes and eukaryotes). We find that dsDNA genome size increases systematically, though less than proportionally, with host genome size. We next evaluate possible relationships between virus size, host size and burst size in an analysis that includes both single-celled and multicellular hosts where genome size and cell volume are not as highly correlated. Here we find that virus volume increases sublinearly with host cell volume (but not genome size) across species, and that virus burst volume (burst size * virus volume) increases with host cell volume. These findings suggest that the size and number of dsDNA viruses produced by a particular host may be constrained by the volume of the infected host cell. This may be useful for better understanding virus-host population dynamics, and ultimately, a better understanding of which viruses may infect which hosts (i.e., host specificity) and the likelihood of cross-species transmission events (i.e., host jumping).

The energetic basis of acoustic communication.

Animals produce a tremendous diversity of sounds for communication to perform life's basic functions, from courtship and parental care to defence and foraging. Explaining this diversity in sound production is important for understanding the ecology, evolution and behaviour of species. Here, we present a theory of acoustic communication that shows that much of the heterogeneity in animal vocal signals can be explained based on the energetic constraints of sound production. The models presented here yield quantitative predictions on key features of acoustic signals, including the frequency, power and duration of signals. Predictions are supported with data from nearly 500 diverse species (e.g. insects, fishes, reptiles, amphibians, birds and mammals). These results indicate that, for all species, acoustic communication is primarily controlled by individual metabolism such that call features vary predictably with body size and temperature. These results also provide insights regarding the common energetic and neuromuscular constraints on sound production, and the ecological and evolutionary consequences of producing these sounds.

Characterizing the microbiomes of Antarctic sponges: a functional metagenomic approach.

Relatively little is known about the role of sponge microbiomes in the Antarctic marine environment, where sponges may dominate the benthic landscape. Specifically, we understand little about how taxonomic and functional diversity contributes to the symbiotic lifestyle and aids in nutrient cycling. Here we use functional metagenomics to investigate the community composition and metabolic potential of microbiomes from two abundant Antarctic sponges, Leucetta antarctica and Myxilla sp. Genomic and taxonomic analyses show that both sponges harbor a distinct microbial community with high fungal abundance, which differs from the surrounding seawater. Functional analyses reveal both sponge-associated microbial communities are enriched in functions related to the symbiotic lifestyle (e.g., CRISPR system, Eukaryotic-like proteins, and transposases), and in functions important for nutrient cycling. Both sponge microbiomes possessed genes necessary to perform processes important to nitrogen cycling (i.e., ammonia oxidation, nitrite oxidation, and denitrification), and carbon fixation. The latter indicates that Antarctic sponge microorganisms prefer light-independent pathways for CO2 fixation mediated by chemoautotrophic microorganisms. Together, these results show how the unique metabolic potential of two Antarctic sponge microbiomes help these sponge holobionts survive in these inhospitable environments, and contribute to major nutrient cycles of these ecosystems.

Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling.

Ecologists have long recognized that species are sustained by the flux, storage and turnover of two biological currencies: energy, which fuels biological metabolism and materials (i.e. chemical elements), which are used to construct biomass. Ecological theories often describe the dynamics of populations, communities and ecosystems in terms of either energy (e.g. population-dynamics theory) or materials (e.g. resource-competition theory). These two classes of theory have been formulated using different assumptions, and yield distinct, but often complementary predictions for the same or similar phenomena. For example, the energy-based equation of von Bertalanffy and the nutrient-based equation of Droop both describe growth. Yet, there is relatively little theoretical understanding of how these two distinct classes of theory, and the currencies they use, are interrelated. Here, we begin to address this issue by integrating models and concepts from two rapidly developing theories, the metabolic theory of ecology and ecological stoichiometry theory. We show how combining these theories, using recently published theory and data along with new theoretical formulations, leads to novel predictions on the flux, storage and turnover of energy and materials that apply to animals, plants and unicells. The theory and results presented here highlight the potential for developing a more general ecological theory that explicitly relates the energetics and stoichiometry of individuals, communities and ecosystems to subcellular structures and processes. We conclude by discussing the basic and applied implications of such a theory, and the prospects and challenges for further development.

Dinosaur fossils predict body temperatures.

Perhaps the greatest mystery surrounding dinosaurs concerns whether they were endotherms, ectotherms, or some unique intermediate form. Here we present a model that yields estimates of dinosaur body temperature based on ontogenetic growth trajectories obtained from fossil bones. The model predicts that dinosaur body temperatures increased with body mass from approximately 25 degrees C at 12 kg to approximately 41 degrees C at 13,000 kg. The model also successfully predicts observed increases in body temperature with body mass for extant crocodiles. These results provide direct evidence that dinosaurs were reptiles that exhibited inertial homeothermy.

Predicting natural mortality rates of plants and animals.

Understanding the factors that control the mortality rates of species in their natural environments is important for understanding the structure and dynamics of populations, communities and ecosystems. Here, we test a model of natural mortality that yields explicit, quantitative predictions based on the constraints of body size and temperature on individual metabolism. Extensive field data from plants, invertebrates, fish, birds and mammals indicate that much of the heterogeneity in rates of natural mortality can be predicted, despite the many extrinsic sources of mortality in natural systems. These results suggest that common 'rule(s)' govern mortality rates in ecological communities for organisms as diverse as plants and animals.

Assessing latitudinal gradients in speciation rates and biodiversity at the global scale.

The mechanisms responsible for latitudinal biodiversity gradients have fascinated and perplexed biologists since the time of Darwin. Ecological theory has yielded two general classes of mechanisms to account for variation in biodiversity: dispersal-assembly mechanisms that invoke differences in stochastic rates of speciation, extinction and dispersal; and niche-assembly mechanisms that invoke species differences, species interactions and environmental heterogeneity. Distinguishing between these two classes of mechanisms requires explicit consideration of macroevolutionary dynamics. Here, we assess the importance of dispersal-assembly mechanisms in the origin and maintenance of biodiversity using fossil data that encompass 30 million years of macroevolution for three distinct groups of ocean plankton: foraminifera, nannoplankton and radiolaria. Applying new methods of analysis to these fossil data, we show here for the first time that latitudinal biodiversity gradients exhibit strong positive correlations with speciation rates even after explicitly controlling for variation in sampling effort and for increases in habitat area towards the equator. These findings provide compelling evidence that geographical variation in macroevolutionary dynamics is a primary determinant of contemporary biodiversity gradients, as predicted by dispersal-assembly theory.

Temperature-dependence of biomass accumulation rates during secondary succession.

Rates of ecosystem recovery following disturbance affect many ecological processes, including carbon cycling in the biosphere. Here, we present a model that predicts the temperature dependence of the biomass accumulation rate following disturbances in forests. Model predictions are derived based on allometric and biochemical principles that govern plant energetics and are tested using a global database of 91 studies of secondary succession compiled from the literature. The rate of biomass accumulation during secondary succession increases with average growing season temperature as predicted based on the biochemical kinetics of photosynthesis in chloroplasts. In addition, the rate of biomass accumulation is greater in angiosperm-dominated communities than in gymnosperm-dominated ones and greater in plantations than in naturally regenerating stands. By linking the temperature-dependence of photosynthesis to the rate of whole-ecosystem biomass accumulation during secondary succession, our model and results provide one example of how emergent, ecosystem-level rate processes can be predicted based on the kinetics of individual metabolic rate.

Common metabolic constraints on dive duration in endothermic and ectothermic vertebrates.

Dive duration in air-breathing vertebrates is thought to be constrained by the volume of oxygen stored in the body and the rate at which it is consumed (i.e., "oxygen store/usage hypothesis"). The body mass-dependence of dive duration among endothermic vertebrates is largely supportive of this model, but previous analyses of ectothermic vertebrates show no such body mass-dependence. Here we show that dive duration in both endotherms and ectotherms largely support the oxygen store/usage hypothesis after accounting for the well-established effects of temperature on oxygen consumption rates. Analyses of the body mass and temperature dependence of dive duration in 181 species of endothermic vertebrates and 29 species of ectothermic vertebrates show that dive duration increases as a power law with body mass, and decreases exponentially with increasing temperature. Thus, in the case of ectothermic vertebrates, changes in environmental temperature will likely impact the foraging ecology of divers.