RESUMEN
Within many species, and particularly fish, fecundity does not scale with mass linearly; instead, it scales disproportionately. Disproportionate intraspecific size-reproduction relationships contradict most theories of biological growth and present challenges for the management of biological systems. Yet the drivers of reproductive scaling remain obscure and systematic predictors of how and why reproduction scaling varies are lacking. Here, we parameterise life history optimisation model to predict global patterns in the life histories of marine fishes. Our model predict latitudinal trends in life histories: Polar fish should reproduce at a later age and show steeper reproductive scaling than tropical fish. We tested and confirmed these predictions using a new, global dataset of marine fish life histories, demonstrating that the risks of mortality shape maturation and reproductive scaling. Our model also predicts that global warming will profoundly reshape fish life histories, favouring earlier reproduction, smaller body sizes, and lower mass-specific reproductive outputs, with worrying consequences for population persistence.
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Peces , Reproducción , Animales , Peces/fisiología , Fertilidad , Calentamiento GlobalRESUMEN
Most explanations for the relationship between body size and metabolism invoke physical constraints; such explanations are evolutionarily inert, limiting their predictive capacity. Contemporary approaches to metabolic rate and life history lack the pluralism of foundational work. Here, we call for reforging of the lost links between optimization approaches and physiology.
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Metabolismo Energético , Modelos Biológicos , Humanos , Tamaño Corporal/fisiología , Metabolismo Energético/fisiologíaRESUMEN
Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.
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Tamaño Corporal , Vocalización Animal , Animales , Pájaros Cantores/fisiología , Pájaros Cantores/anatomía & histología , Ecosistema , Evolución BiológicaRESUMEN
Arctic birds and mammals are physiologically adapted to survive in cold environments but live in the fastest warming region on the planet. They should therefore be most threatened by climate change. We fitted a phylogenetic model of upper critical temperature (TUC) in 255 bird species and determined that TUC for dovekies (Alle alle; 22.4°C)-the most abundant seabird in the Arctic-is 8.8°C lower than predicted for a bird of its body mass (150 g) and habitat latitude. We combined our comparative analysis with in situ physiological measurements on 36 dovekies from East Greenland and forward-projections of dovekie energy and water expenditure under different climate scenarios. Based on our analyses, we demonstrate that cold adaptation in this small Arctic seabird does not handicap acute tolerance to air temperatures up to at least 15°C above their current maximum. We predict that climate warming will reduce the energetic costs of thermoregulation for dovekies, but their capacity to cope with rising temperatures will be constrained by water intake and salt balance. Dovekies evolved 15 million years ago, and their thermoregulatory physiology might also reflect adaptation to a wide range of palaeoclimates, both substantially warmer and colder than the present day.
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Charadriiformes , Ecosistema , Animales , Filogenia , Charadriiformes/fisiología , Aves , Cambio Climático , Mamíferos , Regiones ÁrticasRESUMEN
From bacteria to metazoans, higher density populations have lower per capita metabolic rates than lower density populations. The negative covariance between population density and metabolic rate is thought to represent a form of adaptive metabolic plasticity. A relationship between density and metabolism was actually first noted 100â years ago, and was focused on spermatozoa; even then, it was postulated that adaptive plasticity drove this pattern. Since then, contemporary studies of sperm metabolism specifically assume that sperm concentration has no effect on metabolism and that sperm metabolic rates show no adaptive plasticity. We did a systematic review to estimate the relationship between sperm aerobic metabolism and sperm concentration, for 198 estimates spanning 49 species, from protostomes to humans from 88 studies. We found strong evidence that per capita metabolic rates are concentration dependent: both within and among species, sperm have lower metabolisms in dense ejaculates, but increase their metabolism when diluted. On average, a 10-fold decrease in sperm concentration increased per capita metabolic rate by 35%. Metabolic plasticity in sperm appears to be an adaptive response, whereby sperm maximize their chances of encountering eggs.
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Espermatozoides , Masculino , Espermatozoides/metabolismo , Espermatozoides/fisiología , Animales , Humanos , Densidad de Población , Metabolismo Energético , Recuento de EspermatozoidesRESUMEN
Metabolism should drive demography by determining the rates of both biological work and resource demand. Long-standing "rules" for how metabolism should covary with demography permeate biology, from predicting the impacts of climate change to managing fisheries. Evidence for these rules is almost exclusively indirect and in the form of among-species comparisons, while direct evidence is exceptionally rare. In a manipulative field experiment on a sessile marine invertebrate, we created experimental populations that varied in population size (density) and metabolic rate, but not body size. We then tested key theoretical predictions regarding relationships between metabolism and demography by parameterizing population models with lifetime performance data from our field experiment. We found that populations with higher metabolisms had greater intrinsic rates of increase and lower carrying capacities, in qualitative accordance with classic theory. We also found important departures from theory-in particular, carrying capacity declined less steeply than predicted, such that energy use at equilibrium increased with metabolic rate, violating the long-standing axiom of energy equivalence. Theory holds that energy equivalence emerges because resource supply is assumed to be independent of metabolic rate. We find this assumption to be violated under real-world conditions, with potentially far-reaching consequences for the management of biological systems.
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Metabolismo Basal , Briozoos/fisiología , Conservación de los Recursos Naturales , Ecosistema , Metabolismo Energético , Modelos Biológicos , Migración Animal , Animales , Demografía , Densidad de PoblaciónRESUMEN
Respirometry is an important tool for understanding whole-animal energy and water balance in relation to the environment. Consequently, the growing number of studies using respirometry over the last decade warrants reliable reporting and data sharing for effective dissemination and research synthesis. We provide a checklist guideline on five key sections to facilitate the transparency, reproducibility, and replicability of respirometry studies: 1) materials, set up, plumbing, 2) subject conditions/maintenance, 3) measurement conditions, 4) data processing, and 5) data reporting and statistics, each with explanations and example studies. Transparency in reporting and data availability has benefits on multiple fronts. Authors can use this checklist to design and report on their study, and reviewers and editors can use the checklist to assess the reporting quality of the manuscripts they review. Improved standards for reporting will enhance the value of primary studies and will greatly facilitate the ability to carry out higher quality research syntheses to address ecological and evolutionary theories.
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Pérdida Insensible de Agua , Animales , Metabolismo Basal , Guías como Asunto , Reproducibilidad de los Resultados , Pérdida Insensible de Agua/fisiologíaRESUMEN
Constraint-based explanations have dominated theories of size-related patterns in nature for centuries. Explanations for metabolic scaling - the way in which metabolism changes with body mass - have been based on the geometry of circulatory networks through which resources are distributed, the need to dissipate heat produced as a by-product of metabolic processes, and surface-area-to-volume constraints on the flux of nutrients or waste. As an alternative to these constraint-based approaches, we recently developed a new theory that predicts that metabolic allometry arises as a consequence of the optimisation of growth and reproduction to maximise fitness within a finite life. Our theory is free of physical geometric constraints that limit the possibilities available to evolution, and we therefore argue that metabolic allometry can be explained without the need to invoke any of the assumed constraints traditionally imposed by metabolic theories. Our findings also suggest that metabolism, growth and reproduction have co-evolved to maximise fitness (i.e. lifetime reproduction) and that the observed patterns in these fundamental characteristics of life can similarly be explained by optimisation rather than constraint. In this Centenary Commentary, we present an overview of our approach and a critique of its limitations. We propose a suite of empirical tests that we hope will move the field forward, discuss the dangers of model overparameterisation and highlight the need to remain open to non-adaptive hypotheses for the origin of biological patterns.
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Metabolismo Energético , Reproducción , Modelos Biológicos , BiologíaRESUMEN
Climate has a key impact on animal physiology, which in turn can have a profound influence on geographic distributions. Yet, the mechanisms linking climate, physiology and distribution are not fully resolved. Using an integrative framework, we tested the predictions of the climatic variability hypothesis (CVH), which states that species with broader distributions have broader physiological tolerance than range-restricted species, in a group of Lampropholis skinks (8 species, 196 individuals) along a latitudinal gradient in eastern Australia. We investigated several physiological aspects including metabolism, water balance, thermal physiology, thermoregulatory behaviour and ecological performance. Additionally, to test whether organismal information (e.g. behaviour and physiology) can enhance distribution models, hence providing evidence that physiology and climate interact to shape range sizes, we tested whether species distribution models incorporating physiology better predict the range sizes than models using solely climatic layers. In agreement with the CVH, our results confirm that widespread species can tolerate and perform better at broader temperature ranges than range-restricted species. We also found differences in field body temperatures, but not thermal preference, between widespread and range-restricted species. However, metabolism and water balance did not correlate with range size. Biophysical modelling revealed that the incorporation of physiological and behavioural data improves predictions of Lampropholis distributions compared with models based solely on macroclimatic inputs, but mainly for range-restricted species. By integrating several aspects of the physiology and niche modelling of a group of ectothermic animals, our study provides evidence that physiology correlates with species distributions. Physiological responses to climate are central in establishing geographic ranges of skinks, and the incorporation of processes occurring at local scales (e.g. behaviour) can improve species distribution models.
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Regulación de la Temperatura Corporal , Agua , Humanos , Animales , Australia , Cambio Climático , TemperaturaRESUMEN
Alternative phenotypes allow individuals to pursue different adaptive pathways in response to the same selective challenge. Colour polymorphic species with geographically varying morph frequencies may reflect multiple adaptations to spatial variables such as temperature and climate. We examined whether thermal biology differed between colour morphs of an Australian lizard, the delicate skink, Lampropholis delicata. The delicate skink has two colour pattern morphs, with frequencies varying across latitude and sex: plain (darker, more common at temperate latitudes, more common in males) or striped (lighter, more common at lower latitudes, more common in females). We tested heating and cooling rate, sprint speed, thermal preference, field body temperature and metabolic rate in both morphs and sexes to determine any link between colour and morph frequency distribution. Plain individuals heated more quickly, but other thermal traits showed little variation among morphs. Lampropholis delicata colour influences rates of heat exchange, but the relationship does not appear to be adaptive, suggesting that behavioural thermoregulation homogenises body temperature in the field. While we find no substantial evidence of thermal differences between the two colour morphs, morph-specific behaviour may buffer against differences in heat exchange. Latitudinal variation in species colour may be driven by selection pressures other than temperature.
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Lagartos , Lagartos/anatomía & histología , Lagartos/clasificación , Lagartos/genética , Lagartos/fisiología , Animales , Pigmentación , Polimorfismo Genético , Masculino , Femenino , Calefacción , Pigmentación de la Piel , Fenómenos Fisiológicos de la PielRESUMEN
How the accelerating pace of global warming will affect animal populations depends on the effects of increasing temperature across the life cycle. Developing young are sensitive to environmental challenges, often with life-long consequences, but the risks of climate warming during this period are insufficiently understood. This may be due to limited insight into physiological sensitivity and the temperatures that represent a thermal challenge for young. Here we examined the physiological and behavioural effects of increasing temperatures by measuring metabolic rate, water loss, and heat dissipation behaviours between 25-45 °C in nestlings of a small free-living songbird of temperate SE-Australia, the superb fairy-wren. We found a high and relatively narrow thermoneutral zone from 33.1 to 42.3 °C, with metabolic rate increasing and all nestlings panting above this range. Evaporative water loss sharply increased above 33.5 °C; at the same temperature, nestlings changed their posture (extended their wings) to facilitate passive heat loss. However, at all temperatures measured, water loss was insufficient to dissipate metabolically produced heat, indicating poor cooling capabilities, which persisted even when individuals were panting. While nestlings are relatively tolerant to higher temperatures, with no evidence for hyperthermia at temperatures below 42 °C, they are at a high risk of dehydration even at lower temperatures, with limited ability to mitigate this. Thus, climate warming is likely to elevate the risk dehydration, which is concerning, since it is accompanied by drier conditions.
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Pájaros Cantores , Humanos , Animales , Pájaros Cantores/fisiología , Deshidratación , Regulación de la Temperatura Corporal/fisiología , Temperatura Corporal/fisiología , Calor , AguaRESUMEN
This meta-study uses phylogenetic scaling models across more than 30 species, spanning five orders of magnitude in body mass, to show that cardiac capillary numerical density and mitochondrial volume density decrease with body mass raised to the -0.07 ± 0.03 and -0.04 ± 0.01 exponents, respectively. Thus, while an average 10 g mammal has a cardiac capillary density of approximately 4150 mm-2 and a mitochondrial density of 33%, a 1 t mammal has considerably lower corresponding values of 1850 mm-2 and 21%. These similar scaling trajectories suggest quantitative matching for the primary oxygen supply and oxygen consuming structures of the heart, supporting economic design at the cellular level of the oxygen cascade in this aerobic organ. These scaling trajectories are nonetheless somewhat shallower than the exponent of -0.11 calculated for the maximum external mechanical power of the cardiac tissue, under conditions of heavy exercise, when oxygen flow between capillaries and mitochondria is probably fully exploited. This mismatch, if substantiated, implies a declining external mechanical efficiency of the heart with increasing body mass, whereby larger individuals put more energy in but get less energy out, a scenario with implications for cardiovascular design, aerobic capacity and limits of body size.
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Capilares , Elefantes , Animales , Humanos , Mitocondrias , Oxígeno , Consumo de Oxígeno , Filogenia , MusarañasRESUMEN
The distribution of disease vectors such as mosquitoes is changing. Climate change, invasions and vector control strategies all alter the distribution and abundance of mosquitoes. When disease vectors undergo a range shift, so do disease burdens. Predicting such shifts is a priority to adequately prepare for disease control. Accurate predictions of distributional changes depend on how factors such as temperature and competition affect mosquito life-history traits, particularly body size and reproduction. Direct estimates of both body size and reproduction in mosquitoes are logistically challenging and time-consuming, so the field has long relied upon linear (isometric) conversions between wing length (a convenient proxy of size) and reproductive output. These linear transformations underlie most models projecting species' distributions and competitive interactions between native and invasive disease vectors. Using a series of meta-analyses, we show that the relationship between wing length and fecundity are nonlinear (hyperallometric) for most mosquito species. We show that whilst most models ignore reproductive hyperallometry (with respect to wing length), doing so introduces systematic biases into estimates of population growth. In particular, failing to account for reproductive hyperallometry overestimates the effects of temperature and underestimates the effects of competition. Assuming isometry also increases the potential to misestimate the efficacy of vector control strategies by underestimating the contribution of larger females in population replenishment. Finally, failing to account for reproductive hyperallometry and variation in body size can lead to qualitative errors via the counter-intuitive effects of Jensen's inequality. For example, if mean sizes decrease, but variance increases, then reproductive outputs may actually increase. We suggest that future disease vector models incorporate hyperallometric relationships to more accurately predict changes in mosquito distribution in response to global change.
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Vectores de Enfermedades , Reproducción , Animales , Tamaño Corporal , Cambio Climático , Femenino , FertilidadRESUMEN
Environments, particularly developmental environments, can generate a considerable amount of phenotypic variation through phenotypic plasticity. Plasticity in response to incubation temperature is well characterised in egg-laying reptiles. However, traits do not always vary independently of one another, and studies encompassing a broad range of traits spanning multiple categories are relatively rare but crucial to better understand whole-organism responses to environmental change, particularly if covariation among traits may constrain plasticity. In this study, we investigated multivariate plasticity in response to incubation across three temperatures in the delicate skink, Lampropholis delicata, and whether this was affected by covariation among traits. At approximately 1 month of age, a suite of growth, locomotor performance, thermal physiology and behavioural traits were measured. Plasticity in the multivariate phenotype of delicate skinks was distinct for different incubation temperatures. Cool temperatures drove shifts in growth, locomotor performance and thermal physiology, while hot temperatures primarily caused changes in locomotor performance and behaviour. These differences are likely due to variation in thermal reaction norms, as there was little evidence that covariation among traits or phenotypic integration influenced plasticity, and there was no effect of incubation temperature on the direction or strength of covariation. While there were broad themes in terms of which trait categories were affected by different incubation treatments, traits appeared to be affected independently by developmental temperature. Comparing reaction norms of a greater range of traits and temperatures will enable better insight into these patterns among trait categories, as well as the impacts of environmental change.
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Lagartos , Animales , Lagartos/fisiología , Temperatura , Australia , Adaptación Fisiológica/fisiología , Frío , FenotipoRESUMEN
Glycogen is a critical store for locomotion. Depleted glycogen stores are associated with increased fatigue during exercise. The reduced effectiveness of low-carbohydrate diets for weight loss over longer time periods may arise because such diets reduce glycogen stores and thereby energy expenditure via physical activity. To explore the effect of a low-carbohydrate diet on activity and glycogen utilisation, we fed adult Drosophila melanogaster a standard or low-carbohydrate diet for 9 days and measured patterns of flight activity and rates of glycogen depletion. We hypothesised that flight activity and rates of glycogen depletion would be reduced on a low-carbohydrate diet. Flight activity was elevated in the low-carbohydrate group but glycogen depletion rates were unchanged. We conclude that increased activity is probably a foraging response to carbohydrate deficiency and speculate that the previously demonstrated metabolic depression that occurs on a low-carbohydrate diet in this species may allow for increased flight activity without increased glycogen depletion.
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Carbohidratos de la Dieta , Drosophila melanogaster , Glucógeno , Animales , Dieta , Dieta Baja en Carbohidratos , Drosophila melanogaster/metabolismo , Metabolismo Energético , Glucógeno/metabolismoRESUMEN
The oxygen and capacity-limited thermal tolerance (OCLTT) hypothesis proposes that the thermal tolerance of an animal is shaped by its capacity to deliver oxygen in relation to oxygen demand. Studies testing this hypothesis have largely focused on measuring short-term performance responses in animals under acute exposure to critical thermal maximums. The OCLTT hypothesis, however, emphasises the importance of sustained animal performance over acute tolerance. The present study tested the effect of chronic hypoxia and hyperoxia during development on moderate to long-term performance indicators at temperatures spanning the optimal temperature for growth in the speckled cockroach, Nauphoeta cinerea In contrast to the predictions of the OCLTT hypothesis, development under hypoxia did not significantly reduce growth rate or running performance, and development under hyperoxia did not significantly increase growth rate or running performance. The effects of developmental temperature and oxygen on tracheal morphology and metabolic rate were also not consistent with OCLTT predictions, suggesting that oxygen delivery capacity is not the primary driver shaping thermal tolerance in this species. Collectively, these findings suggest that the OCLTT hypothesis does not explain moderate to long-term thermal performance in N.cinerea, which raises further questions about the generality of the hypothesis.
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Cucarachas , Oxígeno , Animales , Hipoxia , Consumo de Oxígeno , TemperaturaRESUMEN
Dominance hierarchies confer benefits to group members by decreasing the incidences of physical conflict, but may result in certain lower ranked individuals consistently missing out on access to resources. Here, we report a linear dominance hierarchy remaining stable over time in a closed population of birds. We show that this stability can be disrupted, however, by the artificial mass loading of birds that typically comprise the bottom 50% of the hierarchy. Mass loading causes these low-ranked birds to immediately become more aggressive and rise-up the dominance hierarchy; however, this effect was only evident in males and was absent in females. Removal of the artificial mass causes the hierarchy to return to its previous structure. This interruption of a stable hierarchy implies a strong direct link between body mass and social behaviour and suggests that an individual's personality can be altered by the artificial manipulation of body mass.
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Columbidae , Predominio Social , Agresión , Animales , Femenino , Jerarquia Social , Humanos , Masculino , Conducta Social , Medio SocialRESUMEN
Temperature often affects maternal investment in offspring. Across and within species, mothers in colder environments generally produce larger offspring than mothers in warmer environments, but the underlying drivers of this relationship remain unresolved. We formally evaluated the ubiquity of the temperature-offspring size relationship and found strong support for a negative relationship across a wide variety of ectotherms. We then tested an explanation for this relationship that formally links life-history and metabolic theories. We estimated the costs of development across temperatures using a series of laboratory experiments on model organisms, and a meta-analysis across 72 species of ectotherms spanning five phyla. We found that both metabolic and developmental rates increase with temperature, but developmental rate is more temperature sensitive than metabolic rate, such that the overall costs of development decrease with temperature. Hence, within a species' natural temperature range, development at relatively cooler temperatures requires mothers to produce larger, better provisioned offspring.
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Tamaño Corporal , Madres , Temperatura , Adaptación Fisiológica , Animales , FemeninoRESUMEN
Amphibian skin is highly variable in structure and function across anurans, and plays an important role in physiological homeostasis and immune defence. For example, skin sloughing has been shown to reduce pathogen loads on the skin, such as the lethal fungus Batrachochytrium dendrobatidis ( Bd), but interspecific variation in sloughing frequency is largely unknown. Using phylogenetic linear mixed models, we assessed the relationship between skin turnover rate, skin morphology, ecological traits and overall evidence of Bd-driven declines. We examined skin sloughing rates in 21 frog species from three continents, as well as structural skin characteristics measured from preserved specimens. We found that sloughing rate varies significantly with phylogenetic group, but was not associated with evidence of Bd-driven declines, or other skin characteristics examined. This is the first comparison of sloughing rate across a wide range of amphibian species, and creates the first database of amphibian sloughing behaviour. Given the strong phylogenetic signal observed in sloughing rate, approximate sloughing rates of related species may be predicted based on phylogenetic position. While not related to available evidence of declines, understanding variation in sloughing rate may help explain differences in the severity of infection in genera with relatively slow skin turnover rates (e.g. Atelopus).
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Anuros , Quitridiomicetos/fisiología , Dermatomicosis/veterinaria , Piel/microbiología , Animales , Anuros/fisiología , Dermatomicosis/fisiopatología , FilogeniaRESUMEN
This meta-study investigated the relationships between blood flow rate (QÌ; cm3 s-1), wall shear stress (τw; dyn cm-2) and lumen radius (ri; cm) in 20 named systemic arteries of nine species of mammals, ranging in mass from 23â g mice to 652â kg cows, at rest. In the dataset, derived from 50 studies, lumen radius varied between 3.7â µm in a cremaster artery of a rat and 11.2â mm in the aorta of a human. The 92 logged data points of [Formula: see text] and ri are described by a single second-order polynomial curve with the equation: [Formula: see text] The slope of the curve increased from approximately 2 in the largest arteries to approximately 3 in the smallest ones. Thus, da Vinci's rule ([Formula: see text]) applies to the main arteries and Murray's law ([Formula: see text]) applies to the microcirculation. A subset of the data, comprising only cephalic arteries in which [Formula: see text] is fairly constant, yielded the allometric power equation: [Formula: see text] These empirical equations allow calculation of resting perfusion rates from arterial lumen size alone, without reliance on theoretical models or assumptions on the scaling of wall shear stress in relation to body mass. As expected, [Formula: see text] of individual named arteries is strongly affected by body mass; however, [Formula: see text] of the common carotid artery from six species (mouse to horse) is also sensitive to differences in whole-body basal metabolic rate, independent of the effect of body mass.