White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals.

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, 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, 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. A 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.

The Pace of Life: Metabolic Energy, Biological Time, and Life History.

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) of Brown et al. (2018). 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. 7) 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.

Universal rules of life: metabolic rates, biological times and the equal fitness paradigm.

Here we review and extend the equal fitness paradigm (EFP) as an important step in developing and testing a synthetic theory of ecology and evolution based on energy and metabolism. The EFP states that all organisms are equally fit at steady state, because they allocate the same quantity of energy, ~ 22.4 kJ/g/generation to the production of offspring. On the one hand, the EFP may seem tautological, because equal fitness is necessary for the origin and persistence of biodiversity. On the other hand, the EFP reflects universal laws of life: how biological metabolism - the uptake, transformation and allocation of energy - links ecological and evolutionary patterns and processes across levels of organisation from: (1) structure and function of individual organisms, (2) life history and dynamics of populations, and (3) interactions and coevolution of species in ecosystems. The physics and biology of metabolism have facilitated the evolution of millions of species with idiosyncratic anatomy, physiology, behaviour and ecology but also with many shared traits and tradeoffs that reflect the single origin and universal rules of life.

Toward a metabolic theory of life history.

The life histories of animals reflect the allocation of metabolic energy to traits that determine fitness and the pace of living. Here, we extend metabolic theories to address how demography and mass-energy balance constrain allocation of biomass to survival, growth, and reproduction over a life cycle of one generation. We first present data for diverse kinds of animals showing empirical patterns of variation in life-history traits. These patterns are predicted by theory that highlights the effects of 2 fundamental biophysical constraints: demography on number and mortality of offspring; and mass-energy balance on allocation of energy to growth and reproduction. These constraints impose 2 fundamental trade-offs on allocation of assimilated biomass energy to production: between number and size of offspring, and between parental investment and offspring growth. Evolution has generated enormous diversity of body sizes, morphologies, physiologies, ecologies, and life histories across the millions of animal, plant, and microbe species, yet simple rules specified by general equations highlight the underlying unity of life.

Metabolic asymmetry and the global diversity of marine predators.

Species richness of marine mammals and birds is highest in cold, temperate seas-a conspicuous exception to the general latitudinal gradient of decreasing diversity from the tropics to the poles. We compiled a comprehensive dataset for 998 species of sharks, fish, reptiles, mammals, and birds to identify and quantify inverse latitudinal gradients in diversity, and derived a theory to explain these patterns. We found that richness, phylogenetic diversity, and abundance of marine predators diverge systematically with thermoregulatory strategy and water temperature, reflecting metabolic differences between endotherms and ectotherms that drive trophic and competitive interactions. Spatial patterns of foraging support theoretical predictions, with total prey consumption by mammals increasing by a factor of 80 from the equator to the poles after controlling for productivity.

The shark-tuna dichotomy: why tuna lay tiny eggs but sharks produce large offspring.

Teleosts such as tunas and billfish lay millions of tiny eggs weighing on the order of 0.001 g, whereas chondrichthyes such as sharks and rays produce a few eggs or live offspring weighing about 2% of adult body mass, as much as 10 000 g in some species. Why are the strategies so extreme, and why are intermediate ones absent? Building on previous work, we show quantitatively how offspring size reflects the relationship between growth and death rates. We construct fitness contours as functions of offspring size and number, and show how these can be derived from juvenile growth and survivorship curves. Convex contours, corresponding to Pearl Type 1 and 2 survivorship curves, select for extremes, either miniscule or large offspring; concave contours select for offspring of intermediate size. Of particular interest are what we call critical straight-line fitness contours, corresponding to log-linear Pearl Type 3 survivorship curves, which separate regimes that select for opposite optimal offspring sizes.

BioTIME: A database of biodiversity time series for the Anthropocene.

MOTIVATION: The BioTIME database contains raw data on species identities and abundances in ecological assemblages through time. These data enable users to calculate temporal trends in biodiversity within and amongst assemblages using a broad range of metrics. BioTIME is being developed as a community-led open-source database of biodiversity time series. Our goal is to accelerate and facilitate quantitative analysis of temporal patterns of biodiversity in the Anthropocene. MAIN TYPES OF VARIABLES INCLUDED: The database contains 8,777,413 species abundance records, from assemblages consistently sampled for a minimum of 2 years, which need not necessarily be consecutive. In addition, the database contains metadata relating to sampling methodology and contextual information about each record. SPATIAL LOCATION AND GRAIN: BioTIME is a global database of 547,161 unique sampling locations spanning the marine, freshwater and terrestrial realms. Grain size varies across datasets from 0.0000000158 km2 (158 cm2) to 100 km2 (1,000,000,000,000 cm2). TIME PERIOD AND GRAIN: BioTIME records span from 1874 to 2016. The minimal temporal grain across all datasets in BioTIME is a year. MAJOR TAXA AND LEVEL OF MEASUREMENT: BioTIME includes data from 44,440 species across the plant and animal kingdoms, ranging from plants, plankton and terrestrial invertebrates to small and large vertebrates. SOFTWARE FORMAT: .csv and .SQL.

Equal fitness paradigm explained by a trade-off between generation time and energy production rate.

Most plant, animal and microbial species of widely varying body size and lifestyle are nearly equally fit as evidenced by their coexistence and persistence through millions of years. All organisms compete for a limited supply of organic chemical energy, derived mostly from photosynthesis, to invest in the two components of fitness: survival and production. All organisms are mortal because molecular and cellular damage accumulates over the lifetime; life persists only because parents produce offspring. We call this the equal fitness paradigm. The equal fitness paradigm occurs because: (1) there is a trade-off between generation time and productive power, which have equal-but-opposite scalings with body size and temperature; smaller and warmer organisms have shorter lifespans but produce biomass at higher rates than larger and colder organisms; (2) the energy content of biomass is essentially constant, ~22.4 kJ g-1 dry body weight; and (3) the fraction of biomass production incorporated into surviving offspring is also roughly constant, ~10-50%. As organisms transmit approximately the same quantity of energy per gram to offspring in the next generation, no species has an inherent lasting advantage in the struggle for existence. The equal fitness paradigm emphasizes the central importance of energy, biological scaling relations and power-time trade-offs in life history, ecology and evolution.

Who is and isn't having babies with Down syndrome in western Sydney: a ten year hospital cohort study.

BACKGROUND: Screening for Down syndrome (DS) is a key component of antenatal care, recommended to be universally offered to women irrespective of age or background. Despite this, the diagnosis of DS is often not made until the neonatal period. AIMS: To retrospectively describe and compare the differences in populations with an antenatal diagnosis (AD) and neonatal diagnosis (ND) of DS and to explore why an antenatal diagnosis was not made. MATERIALS AND METHODS: The cohorts were women cared for at Westmead Hospital whose pregnancy received a diagnosis of DS between 2006 and 2015. The demographic variables of the AD and ND cohorts were examined and reasons why an antenatal diagnosis was not made in the ND cohort were analysed. RESULTS: There were 127 diagnoses of DS in the 10-year period, of which 41% were in the ND cohort (n = 52) and 59% in the AD (n = 75). Declaring a religious affiliation rather than Nil Religion was significantly more common in the ND cohort (88.5%) and especially the ND sub-cohort who declined DS screening/testing (95.8%) than the AD cohort (72%, P < 0.05). Women who were not offered screening were significantly younger (P < 0.001) than those who were, with 69% and 20% being ≤30 years, respectively. CONCLUSIONS: The proportion of DS pregnancies diagnosed in the antenatal period in western Sydney could be increased by ensuring younger women are not falsely reassured that DS screening is unnecessary for them. While religious affiliation may be a factor when women decline screening, ensuring appropriate counselling remains important.

Temperature mediates continental-scale diversity of microbes in forest soils.

Climate warming is increasingly leading to marked changes in plant and animal biodiversity, but it remains unclear how temperatures affect microbial biodiversity, particularly in terrestrial soils. Here we show that, in accordance with metabolic theory of ecology, taxonomic and phylogenetic diversity of soil bacteria, fungi and nitrogen fixers are all better predicted by variation in environmental temperature than pH. However, the rates of diversity turnover across the global temperature gradients are substantially lower than those recorded for trees and animals, suggesting that the diversity of plant, animal and soil microbial communities show differential responses to climate change. To the best of our knowledge, this is the first study demonstrating that the diversity of different microbial groups has significantly lower rates of turnover across temperature gradients than other major taxa, which has important implications for assessing the effects of human-caused changes in climate, land use and other factors.

The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts.

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.

Biogeographic patterns of soil diazotrophic communities across six forests in North America.

Soil diazotrophs play important roles in ecosystem functioning by converting atmospheric N2 into biologically available ammonium. However, the diversity and distribution of soil diazotrophic communities in different forests and whether they follow biogeographic patterns similar to macroorganisms still remain unclear. By sequencing nifH gene amplicons, we surveyed the diversity, structure and biogeographic patterns of soil diazotrophic communities across six North American forests (126 nested samples). Our results showed that each forest harboured markedly different soil diazotrophic communities and that these communities followed traditional biogeographic patterns similar to plant and animal communities, including the taxa-area relationship (TAR) and latitudinal diversity gradient. Significantly higher community diversity and lower microbial spatial turnover rates (i.e. z-values) were found for rainforests (~0.06) than temperate forests (~0.1). The gradient pattern of TARs and community diversity was strongly correlated (r(2)  > 0.5) with latitude, annual mean temperature, plant species richness and precipitation, and weakly correlated (r(2)  < 0.25) with pH and soil moisture. This study suggests that even microbial subcommunities (e.g. soil diazotrophs) follow general biogeographic patterns (e.g. TAR, latitudinal diversity gradient), and indicates that the metabolic theory of ecology and habitat heterogeneity may be the major underlying ecological mechanisms shaping the biogeographic patterns of soil diazotrophic communities.

Long-term monitoring and experimental manipulation of a Chihuahuan desert ecosystem near Portal, Arizona (1977-2013).

Desert ecosystems have long served as model systems in the study of ecological concepts (e.g., competition, resource pulses, top-down/bottom-up dynamics). However, the inherent variability of resource availability in deserts, and hence consumer dynamics, can also make them challenging ecosystems to understand. Study of a Chihuahuan desert ecosystem near Portal, Arizona began in 1977. At this site, 24 experimental plots were established and divided among controls and experimental manipulations. Experimental manipulations over the years include removal of all or some rodent species, all or some ants, seed additions, and various alterations of the annual plant community. This dataset includes data previously available through an older data publication and adds 11 years of data. It also includes additional ant and weather data not previously available. These data have been used in a variety of publications documenting the effects of the experimental manipulations as well as the response of populations and communities to long-term changes in climate and habitat. Sampling is ongoing and additional data will be published in the future.

Metabolic heat production and thermal conductance are mass-independent adaptations to thermal environment in birds and mammals.

The extent to which different kinds of organisms have adapted to environmental temperature regimes is central to understanding how they respond to climate change. The Scholander-Irving (S-I) model of heat transfer lays the foundation for explaining how endothermic birds and mammals maintain their high, relatively constant body temperatures in the face of wide variation in environmental temperature. The S-I model shows how body temperature is regulated by balancing the rates of heat production and heat loss. Both rates scale with body size, suggesting that larger animals should be better adapted to cold environments than smaller animals, and vice versa. However, the global distributions of ∼9,000 species of terrestrial birds and mammals show that the entire range of body sizes occurs in nearly all climatic regimes. Using physiological and environmental temperature data for 211 bird and 178 mammal species, we test for mass-independent adaptive changes in two key parameters of the S-I model: basal metabolic rate (BMR) and thermal conductance. We derive an axis of thermal adaptation that is independent of body size, extends the S-I model, and highlights interactions among physiological and morphological traits that allow endotherms to persist in a wide range of temperatures. Our macrophysiological and macroecological analyses support our predictions that shifts in BMR and thermal conductance confer important adaptations to environmental temperature in both birds and mammals.

Fundamental insights into ontogenetic growth from theory and fish.

The fundamental features of growth may be universal, because growth trajectories of most animals are very similar, but a unified mechanistic theory of growth remains elusive. Still needed is a synthetic explanation for how and why growth rates vary as body size changes, both within individuals over their ontogeny and between populations and species over their evolution. Here, we use Bertalanffy growth equations to characterize growth of ray-finned fishes in terms of two parameters, the growth rate coefficient, K, and final body mass, m∞. We derive two alternative empirically testable hypotheses and test them by analyzing data from FishBase. Across 576 species, which vary in size at maturity by almost nine orders of magnitude, K scaled as [Formula: see text]. This supports our first hypothesis that growth rate scales as [Formula: see text] as predicted by metabolic scaling theory; it implies that species that grow to larger mature sizes grow faster as juveniles. Within fish species, however, K scaled as [Formula: see text]. This supports our second hypothesis, which predicts that growth rate scales as [Formula: see text] when all juveniles grow at the same rate. The unexpected disparity between across- and within-species scaling challenges existing theoretical interpretations. We suggest that the similar ontogenetic programs of closely related populations constrain growth to [Formula: see text] scaling, but as species diverge over evolutionary time they evolve the near-optimal [Formula: see text] scaling predicted by metabolic scaling theory. Our findings have important practical implications because fish supply essential protein in human diets, and sustainable yields from wild harvests and aquaculture depend on growth rates.

Human domination of the biosphere: Rapid discharge of the earth-space battery foretells the future of humankind.

Earth is a chemical battery where, over evolutionary time with a trickle-charge of photosynthesis using solar energy, billions of tons of living biomass were stored in forests and other ecosystems and in vast reserves of fossil fuels. In just the last few hundred years, humans extracted exploitable energy from these living and fossilized biomass fuels to build the modern industrial-technological-informational economy, to grow our population to more than 7 billion, and to transform the biogeochemical cycles and biodiversity of the earth. This rapid discharge of the earth's store of organic energy fuels the human domination of the biosphere, including conversion of natural habitats to agricultural fields and the resulting loss of native species, emission of carbon dioxide and the resulting climate and sea level change, and use of supplemental nuclear, hydro, wind, and solar energy sources. The laws of thermodynamics governing the trickle-charge and rapid discharge of the earth's battery are universal and absolute; the earth is only temporarily poised a quantifiable distance from the thermodynamic equilibrium of outer space. Although this distance from equilibrium is comprised of all energy types, most critical for humans is the store of living biomass. With the rapid depletion of this chemical energy, the earth is shifting back toward the inhospitable equilibrium of outer space with fundamental ramifications for the biosphere and humanity. Because there is no substitute or replacement energy for living biomass, the remaining distance from equilibrium that will be required to support human life is unknown.

Metabolic theory predicts whole-ecosystem properties.

Understanding the effects of individual organisms on material cycles and energy fluxes within ecosystems is central to predicting the impacts of human-caused changes on climate, land use, and biodiversity. Here we present a theory that integrates metabolic (organism-based bottom-up) and systems (ecosystem-based top-down) approaches to characterize how the metabolism of individuals affects the flows and stores of materials and energy in ecosystems. The theory predicts how the average residence time of carbon molecules, total system throughflow (TST), and amount of recycling vary with the body size and temperature of the organisms and with trophic organization. We evaluate the theory by comparing theoretical predictions with outputs of numerical models designed to simulate diverse ecosystem types and with empirical data for real ecosystems. Although residence times within different ecosystems vary by orders of magnitude-from weeks in warm pelagic oceans with minute phytoplankton producers to centuries in cold forests with large tree producers-as predicted, all ecosystems fall along a single line: residence time increases linearly with slope = 1.0 with the ratio of whole-ecosystem biomass to primary productivity (B/P). TST was affected predominantly by primary productivity and recycling by the transfer of energy from microbial decomposers to animal consumers. The theory provides a robust basis for estimating the flux and storage of energy, carbon, and other materials in terrestrial, marine, and freshwater ecosystems and for quantifying the roles of different kinds of organisms and environments at scales from local ecosystems to the biosphere.

Macroecology Meets Macroeconomics: Resource Scarcity and Global Sustainability.

The current economic paradigm, which is based on increasing human population, economic development, and standard of living, is no longer compatible with the biophysical limits of the finite Earth. Failure to recover from the economic crash of 2008 is not due just to inadequate fiscal and monetary policies. The continuing global crisis is also due to scarcity of critical resources. Our macroecological studies highlight the role in the economy of energy and natural resources: oil, gas, water, arable land, metals, rare earths, fertilizers, fisheries, and wood. As the modern industrial technological-informational economy expanded in recent decades, it grew by consuming the Earth's natural resources at unsustainable rates. Correlations between per capita GDP and per capita consumption of energy and other resources across nations and over time demonstrate how economic growth and development depend on "nature's capital". Decades-long trends of decreasing per capita consumption of multiple important commodities indicate that overexploitation has created an unsustainable bubble of population and economy.