Vascular optimality dictates plant morphology away from Leonardo's rule.

Metabolic scaling theory (MST) provides an understanding of scaling in organismal morphology. Empirical data on the apparently universal pattern of tip-to-base conduit widening across vascular plants motivate a set of generalized MST (gMST) relationships allowing for variable rates of conduit coalescence and taper and a transition between transport and diffusive domains. Our model, with coalescence limited to the distalmost part of the conductive system, reconciles previous MST-based models and extends their applicability to the entire plant. We derive an inverse relationship between stem volume taper and conduit widening, which implies that plant morphology is dictated by vascular optimality and not the assumption of constant sapwood area across all branching levels, contradicting Leonardo's rule. Thus, energy efficiency controls conduit coalescence rate, lowering the carbon cost needed to sustain the vascular network. Our model shows that as a plant grows taller, it must increase conduit widening and coalescence, which may make it more vulnerable to drought. We calculated how our gMST model implies a lower carbon cost to sustain a similar network compared to previous MST-based models. We also show that gMST predicts the cross-sectional area of vessels and their frequency along the relative length better than previous MST models for a range of plant types. We encourage further research obtaining data that would allow testing other gMST predictions that remain unconfirmed empirically, such as conduit coalescence rate in stems. The premise of energy efficiency can potentially become instrumental to our understanding of plant carbon allocation.

Long-term experimental evolution decouples size and production costs in Escherichia coli.

Body size covaries with population dynamics across life's domains. Metabolism may impose fundamental constraints on the coevolution of size and demography, but experimental tests of the causal links remain elusive. We leverage a 60,000-generation experiment in which Escherichia coli populations evolved larger cells to examine intraspecific metabolic scaling and correlations with demographic parameters. Over the course of their evolution, the cells have roughly doubled in size relative to their ancestors. These larger cells have metabolic rates that are absolutely higher, but relative to their size, they are lower. Metabolic theory successfully predicted the relations between size, metabolism, and maximum population density, including support for Damuth's law of energy equivalence, such that populations of larger cells achieved lower maximum densities but higher maximum biomasses than populations of smaller cells. The scaling of metabolism with cell size thus predicted the scaling of size with maximum population density. In stark contrast to standard theory, however, populations of larger cells grew faster than those of smaller cells, contradicting the fundamental and intuitive assumption that the costs of building new individuals should scale directly with their size. The finding that the costs of production can be decoupled from size necessitates a reevaluation of the evolutionary drivers and ecological consequences of biological size more generally.

Hotter is not (always) better: Embracing unimodal scaling of biological rates with temperature.

Rate-temperature scaling relationships have fascinated biologists for nearly two centuries and are increasingly important in our era of global climate change. These relationships are hypothesized to originate from the temperature-dependent kinetics of rate-limiting biochemical reactions of metabolism. Several prominent theories have formalized this hypothesis using the Arrhenius model, which characterizes a monotonic temperature dependence using an activation energy E. However, the ubiquitous unimodal nature of biological temperature responses presents important theoretical, methodological, and conceptual challenges that restrict the promise for insight, prediction, and progress. Here we review the development of key hypotheses and methods for the temperature-scaling of biological rates. Using simulations, we examine the constraints of monotonic models, illustrating their sensitivity to data nuances such as temperature range and noise, and their tendency to yield variable and underestimated E, with critical consequences for climate change predictions. We also evaluate the behaviour of two prominent unimodal models when applied to incomplete and noisy datasets. We conclude with recommendations for resolving these challenges in future research, and advocate for a shift to unimodal models that better characterize the full range of biological temperature responses.

An allometry perspective on crops.

Understanding trait-trait coordination is essential for successful plant breeding and crop modeling. Notably, plant size drives variation in morphological, physiological, and performance-related traits, as described by allometric laws in ecology. Yet, as allometric relationships have been limitedly studied in crops, how they influence and possibly limit crop performance remains unknown. Here, we review how an allometry perspective on crops gains insights into the phenotypic evolution during crop domestication, the breeding of varieties adapted to novel conditions, and the prediction of crop yields. As allometry is an active field of research, modeling and manipulating crop allometric relationships can help to develop more resilient and productive agricultural systems to face future challenges.

Scaling of leaf area with biomass in trees reconsidered: constant metabolically active sapwood volume per unit leaf area with height growth.

Hypoallometric (slope<1) scaling between metabolic rate and body mass is often regarded as near-universal across organisms. However, there are compelling reasons to question hypoallometric scaling in woody plants, where metabolic rate is directly proportional to leaf area. This leaf area must provide carbon to the volume of the metabolically active sapwood (VMASW). Within populations of a species, variants in which VMASW increases per unit leaf area with height growth (e.g. ⅔ or ¾ scaling) would have proportionally less carbon for growth and reproduction as they grow taller. Therefore, selection should favor individuals in which, as they grow taller, leaf area scales isometrically with shoot VMASW (slope=1). Using tetrazolium staining, we measured total VMASW and total leaf area (LAtot) across 22 individuals of Ricinus communis and confirmed that leaf area scales isometrically with VMASW, and that VMASW is much smaller than total sapwood volume. With the potential of the LAtot-VMASW relationship to shape factors as diverse as the crown area-stem diameter relationship, conduit diameter scaling, reproductive output, and drought-induced mortality, our work indicates that the notion that sapwood increases per unit leaf area with height growth requires revision.

The scaling of metabolic traits differs among larvae and juvenile colonies of scleractinian corals.

Body size profoundly affects organism fitness and ecosystem dynamics through the scaling of physiological traits. This study tested for variation in metabolic scaling and its potential drivers among corals differing in life history strategies and taxonomic identity. Data were compiled from published sources and augmented with empirical measurements of corals in Moorea, French Polynesia. The data compilation revealed metabolic isometry in broadcasted larvae, but size-independent metabolism in brooded larvae; empirical measurements of Pocillopora acuta larvae also supported size-independent metabolism in brooded coral larvae. In contrast, for juvenile colonies (i.e. 1-4 cm diameter), metabolic scaling was isometric for Pocillopora spp., and negatively allometric for Porites spp. The scaling of biomass with surface area was isometric for Pocillopora spp., but positively allometric for Porites spp., suggesting the surface area to biomass ratio mediates metabolic scaling in these corals. The scaling of tissue biomass and metabolism were not affected by light treatment (i.e. either natural photoperiods or constant darkness) in either juvenile taxa. However, biomass was reduced by 9-15% in the juvenile corals from the light treatments and this coincided with higher metabolic scaling exponents, thus supporting the causal role of biomass in driving variation in scaling. This study shows that metabolic scaling is plastic in early life stages of corals, with intrinsic differences between life history strategy (i.e. brooded and broadcasted larvae) and taxa (i.e. Pocillopora spp. and Porites spp.), and acquired differences attributed to changes in area-normalized biomass.

Metabolic scaling of an invasive mussel depends on temperature and chemical cues from an invasive predator.

Metabolism drives various biological processes, potentially influencing the ecological success and evolutionary fitness of species. Understanding diverse metabolic rates is fundamental in biology. Mechanisms underlying adaptation to factors like temperature and predation pressure remain unclear. Our study explored the role of temperature and predation pressure in shaping the metabolic scaling of an invasive mussel species (Brachidontes pharaonis). Specifically, we performed laboratory-based experiments to assess the effects of phenotypic plasticity on the metabolic scaling by exposing the mussels to water conditions with and without predator cues from another invasive species (the blue crab, Callinectes sapidus) across various temperature regimes. We found that temperature effects on metabolic scaling of the invasive mussels are mediated by the presence of chemical cues of an invasive predator, the blue crab. Investigating temperature-predator interactions underscores the importance of studying the ecological effects of global warming. Our research advances our understanding of how environmental factors jointly impact physiological processes.

Growth, death, and resource competition in sessile organisms.

Population-level scaling in ecological systems arises from individual growth and death with competitive constraints. We build on a minimal dynamical model of metabolic growth where the tension between individual growth and mortality determines population size distribution. We then separately include resource competition based on shared capture area. By varying rates of growth, death, and competitive attrition, we connect regular and random spatial patterns across sessile organisms from forests to ants, termites, and fairy circles. Then, we consider transient temporal dynamics in the context of asymmetric competition, such as canopy shading or large colony dominance, whose effects primarily weaken the smaller of two competitors. When such competition couples slow timescales of growth to fast competitive death, it generates population shocks and demographic oscillations similar to those observed in forest data. Our minimal quantitative theory unifies spatiotemporal patterns across sessile organisms through local competition mediated by the laws of metabolic growth, which in turn, are the result of long-term evolutionary dynamics.

Supplemental oxygen does not improve growth but can enhance reproductive capacity of fish.

Fish tend to grow faster as the climate warms but attain a smaller adult body size following an earlier age at sexual maturation. Despite the apparent ubiquity of this phenomenon, termed the temperature-size rule (TSR), heated scientific debates have revealed a poor understanding of the underlying mechanisms. At the centre of these debates are prominent but marginally tested hypotheses which implicate some form of 'oxygen limitation' as the proximate cause. Here, we test the role of oxygen limitation in the TSR by rearing juvenile Galaxias maculatus for a full year in current-day (15°C) and forecasted (20°C) summer temperatures while providing half of each temperature group with supplemental oxygen (hyperoxia). True to the TSR, fish in the warm treatments grew faster and reached sexual maturation earlier than their cooler conspecifics. Yet, despite supplemental oxygen significantly increasing maximum oxygen uptake rate, our findings contradict leading hypotheses by showing that the average size at sexual maturation and the adult body size did not differ between normoxia and hyperoxia groups. We did, however, discover that hyperoxia extended the reproductive window, independent of fish size and temperature. We conclude that the intense resource investment in reproduction could expose a bottleneck where oxygen becomes a limiting factor.

What do molecular laws of life mean for species: absolute restrictions or mere suggestions?

Evolutionary biologists are interested in finding universal patterns of covariation between macroscopic and molecular traits. Knowledge of such laws of life can be essential for understanding the course of evolutionary processes. Molecular parameters are presumably close to fundamental limits set to all organisms by laws of physics and chemistry. Thus, laws of life that include such parameters are hypothesized to be similar at both wide interspecific levels of variation and narrower levels of intraspecific and intraindividual variation in different species. In this Commentary, I discuss examples where the significance or direction of such molecular laws of life can be compared at different levels of biological variation: (1) the membrane pacemaker theory of metabolism, (2) the correlation between variation in metabolic rate and mitochondrial efficiency and (3) the allometric scaling of metabolism. All three examples reveal that covariations within species or individuals that include molecular parameters do not always follow patterns observed between species. I conclude that limits set by molecular laws of life can be circumvented (at least to some degree) by changes in other traits, and thus, they usually do not impose strict limitations on minor within-species evolutionary changes (i.e. microevolution). I also briefly discuss some of the most promising perspectives for future studies on the universality of molecular laws of life.

Ontogenetic changes in root and shoot respiration, fresh mass and surface area of Fagus crenata.

BACKGROUND AND AIMS: To date, studies on terrestrial plant ecology and evolution have focused primarily on the trade-off patterns in the allocation of metabolic production to roots and shoots in individual plants and the scaling of whole-plant respiration. However, few empirical studies have investigated the root : shoot ratio by considering scaling whole-plant respiration at various sizes throughout ontogeny. METHODS: Here, using a whole-plant chamber system, we measured the respiration rates, fresh mass and surface area of entire roots and shoots from 377 Fagus crenata individuals, from germinating seeds to mature trees, collected from five different Japanese provenances. Non-linear regression analysis was performed for scaling of root and shoot respiration, fresh mass and surface area with body size. KEY RESULTS: Whole-plant respiration increased rapidly in germinating seeds. In the seedling to mature tree size range, the scaling of whole-plant respiration to whole-plant fresh mass was expressed as a linear trend on the log-log coordinates (exponent slightly greater than 0.75). In the same body size range, root and shoot respiration vs. whole-plant fresh mass were modelled by upward-convex (exponent decreased from 2.35 to 0.638) and downward-convex trends (exponent increased from -0.918 to 0.864), respectively. The root fraction in whole-plant respiration, fresh mass and surface area shifted continuously throughout ontogeny, increasing in smaller seedlings during early growth stages and decreasing in larger trees. CONCLUSIONS: Our results suggest a gradual shift in allocation priorities of metabolic energy from roots in seedlings to shoots in mature trees, providing insights into how roots contribute to shoot and whole-plant growth during ontogeny. The models of root : shoot ratio in relation to whole-plant physiology could be applied in tree growth modelling, and in linking the different levels of ecological phenomena, from individuals to ecosystems.

Oxygen limitation may affect the temperature and size dependence of metabolism in aquatic ectotherms.

Both oxygen and temperature are fundamental factors determining metabolic performance, fitness, ecological niches, and responses of many aquatic organisms to climate change. Despite the importance of physical and physiological constraints on oxygen supply affecting aerobic metabolism of aquatic ectotherms, ecological theories such as the metabolic theory of ecology have focused on the effects of temperature rather than oxygen. This gap currently impedes mechanistic models from accurately predicting metabolic rates (i.e., oxygen consumption rates) of aquatic organisms and restricts predictions to resting metabolism, which is less affected by oxygen limitation. Here, we expand on models of metabolic scaling by accounting for the role of oxygen availability and temperature on both resting and active metabolic rates. Our model predicts that oxygen limitation is more likely to constrain metabolism in larger, warmer, and active fish. Consequently, active metabolic rates are less responsive to temperature than are resting metabolic rates, and metabolism scales to body size with a smaller exponent whenever temperatures or activity levels are higher. Results from a metaanalysis of fish metabolic rates are consistent with our model predictions. The observed interactive effects of temperature, oxygen availability, and body size predict that global warming will limit the aerobic scope of aquatic ectotherms and may place a greater metabolic burden on larger individuals, impairing their physiological performance in the future. Our model reconciles the metabolic theory with empirical observations of oxygen limitation and provides a formal, quantitative framework for predicting both resting and active metabolic rate and hence aerobic scope of aquatic ectotherms.

Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature-dependent manner.

Aerobic metabolism generates 15-20 times more energy (ATP) than anaerobic metabolism, which is crucial in maintaining energy budgets in animals, fueling metabolism, activity, growth and reproduction. For ectothermic water-breathers such as fishes, low dissolved oxygen may limit oxygen uptake and hence aerobic metabolism. Here, we assess, within a phylogenetic context, how abiotic and biotic drivers explain the variation in hypoxia tolerance observed in fishes. To do so, we assembled a database of hypoxia tolerance, measured as critical oxygen tensions (Pcrit ) for 195 fish species. Overall, we found that hypoxia tolerance has a clear phylogenetic signal and is further modulated by temperature, body mass, cell size, salinity and metabolic rate. Marine fishes were more susceptible to hypoxia than freshwater fishes. This pattern is consistent with greater fluctuations in oxygen and temperature in freshwater habitats. Fishes with higher oxygen requirements (e.g. a high metabolic rate relative to body mass) also were more susceptible to hypoxia. We also found evidence that hypoxia and warming can act synergistically, as hypoxia tolerance was generally lower in warmer waters. However, we found significant interactions between temperature and the body and cell size of a fish. Constraints in oxygen uptake related to cellular surface area to volume ratios and effects of viscosity on the thickness of the boundary layers enveloping the gills could explain these thermal dependencies. The lower hypoxia tolerance in warmer waters was particularly pronounced for fishes with larger bodies and larger cell sizes. Previous studies have found a wide diversity in the direction and strength of relationships between Pcrit and body mass. By including interactions with temperature, our study may help resolve these divergent findings, explaining the size dependency of hypoxia tolerance in fish.

Solving the grand challenge of phenotypic integration: allometry across scales.

Phenotypic integration is a concept related to the cascade of trait relationships from the lowest organizational levels, i.e. genes, to the highest, i.e. whole-organism traits. However, the cause-and-effect linkages between traits are notoriously difficult to determine. In particular, we still lack a mathematical framework to model the relationships involved in the integration of phenotypic traits. Here, we argue that allometric models developed in ecology offer testable mathematical equations of trait relationships across scales. We first show that allometric relationships are pervasive in biology at different organizational scales and in different taxa. We then present mechanistic models that explain the origin of allometric relationships. In addition, we emphasized that recent studies showed that natural variation does exist for allometric parameters, suggesting a role for genetic variability, selection and evolution. Consequently, we advocate that it is time to examine the genetic determinism of allometries, as well as to question in more detail the role of genome size in subsequent scaling relationships. More broadly, a possible-but so far neglected-solution to understand phenotypic integration is to examine allometric relationships at different organizational levels (cell, tissue, organ, organism) and in contrasted species.

Metabolic rate and climate change across latitudes: evidence of mass-dependent responses in aquatic amphipods.

Predictions of individual responses to climate change are often based on the assumption that temperature affects the metabolism of individuals independently of their body mass. However, empirical evidence indicates that interactive effects exist. Here, we investigated the response of individual standard metabolic rate (SMR) to annual temperature range and forecasted temperature rises of 0.6-1.2°C above the current maxima, under the conservative climate change scenario IPCC RCP2.6. As a model organism, we used the amphipod Gammarus insensibilis, collected across latitudes along the western coast of the Adriatic Sea down to the southernmost limit of the species' distributional range, with individuals varying in body mass (0.4-13.57 mg). Overall, we found that the effect of temperature on SMR is mass dependent. Within the annual temperature range, the mass-specific SMR of small/young individuals increased with temperature at a greater rate (activation energy: E=0.48 eV) than large/old individuals (E=0.29 eV), with a higher metabolic level for high-latitude than low-latitude populations. However, under the forecasted climate conditions, the mass-specific SMR of large individuals responded differently across latitudes. Unlike the higher-latitude population, whose mass-specific SMR increased in response to the forecasted climate change across all size classes, in the lower-latitude populations, this increase was not seen in large individuals. The larger/older conspecifics at lower latitudes could therefore be the first to experience the negative impacts of warming on metabolism-related processes. Although the ecological collapse of such a basic trophic level (aquatic amphipods) owing to climate change would have profound consequences for population ecology, the risk is significantly mitigated by phenotypic and genotypic adaptation.

Larval nutrition impacts survival to adulthood, body size and the allometric scaling of metabolic rate in adult honeybees.

Resting metabolic rate (RMR) is a fundamental physiological measure linked to numerous aspects of organismal function, including lifespan. Although dietary restriction in insects during larval growth/development affects adult RMR, the impact of the nutritional composition of larval diets (i.e. diet quality) on adult RMR has not been studied. Using in vitro rearing to control larval diet quality, we determined the effect of dietary protein and carbohydrate on honeybee survival to adulthood, time to eclosion, body mass/size and adult RMR. High carbohydrate larval diets increased survival to adulthood and time to eclosion compared with both low carbohydrate and high protein diets. Upon emergence, bees reared on the high protein diet were smaller and lighter than those reared on other diets, whilst those raised on the high carbohydrate diet varied more in body mass. Newly emerged adult bees reared on the high carbohydrate diet showed a significantly steeper increase in allometric scaling of RMR compared with those reared on other diets. This suggests that the nutritional composition of larval diets influences survival to adulthood, time to eclosion and the allometric scaling of RMR. Given that agricultural intensification and increasing urbanisation have led to a decrease in both forage availability and dietary diversity for bees, our results are critical to improving understanding of the impacts of poor developmental nutrition on bee growth/development and physiology.

Variance in tree growth rates provides a key link for completing the theory of forest size structure formation.

In natural forests at a demographic equilibrium state, the size frequency distribution (SFD) of trees is linked with their size-dependent growth and mortality rates. While the mean growth rate (MGR) of each size class is generally used for determining the SFD, the variance in the growth rate (VGR) has always been ignored. Here, based on the analyses with Kolmogorov forward equation, we show that in general, the VGR can flatten the slope of the SFD and, in particular, can address the contradiction between the size-dependent MGR and the -2 power-law SFD in the metabolic scaling theory. We traced the origin of the VGR to the intrinsic stochasticity in the allometric growth coefficients of trees and deduced its functional form based on variance propagation. Using the forest censuses data from Barro Colorado Island, we verified the prediction of the VGR and indicated its indispensability in the theory of forest size-structure formation.

Consistent scaling of whole-shoot respiration between Moso bamboo (Phyllostachys pubescens) and trees.

Both Moso bamboo (Phyllostachys pubescens) and tree forests have a large biomass; they are considered to play an important role in ecosystem carbon budgets. The scaling relationship between individual whole-shoot (i.e., aboveground parts) respiration and whole-shoot mass provides a clue for comparing the carbon budgets of Moso bamboo and tree forests. However, nobody has empirically demonstrated whether there is a difference between these forest types in the whole-shoot scaling relationship. We developed whole-shoot chambers and measured the shoot respiration of 58 individual mature bamboo shoots from the smallest to the largest in a Moso bamboo forest, and then compared them with that of 254 tree shoots previously measured. For 30 bamboo shoots, we measured the respiration rate of leaves, branches, and culms. We found that the scaling exponent of whole-shoot respiration of bamboo fitted by a simple power function on a log-log scale was 0.843 (95 % CI 0.797-0.885), which was consistent with that of trees, 0.826 (95 % CI 0.799-0.851), but higher than 3/4, the value typifying the Kleiber's rule. The respiration rates of leaves, branches, and culms at the whole-shoot level were proportional to their mass, revealing a constant mean mass-specific respiration of 1.19, 0.224, and 0.0978 µmol CO2 kg- 1 s- 1, respectively. These constant values suggest common traits of organs among physiologically integrated ramets within a genet. Additionally, the larger the shoots, the smaller the allocation of organ mass to the metabolically active leaves, and the larger the allocation to the metabolically inactive culms. Therefore, these shifts in shoot-mass partitioning to leaves and culms caused a negative metabolic scaling of Moso bamboo shoots. The observed convergent metabolic scaling of Moso bamboo and trees may facilitate comparisons of the ecosystem carbon budgets of Moso bamboo and tree forests.

Adaptive diversification of growth allometry in the plant Arabidopsis thaliana.

Seed plants vary tremendously in size and morphology; however, variation and covariation in plant traits may be governed, at least in part, by universal biophysical laws and biological constants. Metabolic scaling theory (MST) posits that whole-organismal metabolism and growth rate are under stabilizing selection that minimizes the scaling of hydrodynamic resistance and maximizes the scaling of resource uptake. This constrains variation in physiological traits and in the rate of biomass accumulation, so that they can be expressed as mathematical functions of plant size with near-constant allometric scaling exponents across species. However, the observed variation in scaling exponents calls into question the evolutionary drivers and the universality of allometric equations. We have measured growth scaling and fitness traits of 451 Arabidopsis thaliana accessions with sequenced genomes. Variation among accessions around the scaling exponent predicted by MST was correlated with relative growth rate, seed production, and stress resistance. Genomic analyses indicate that growth allometry is affected by many genes associated with local climate and abiotic stress response. The gene with the strongest effect, PUB4, has molecular signatures of balancing selection, suggesting that intraspecific variation in growth scaling is maintained by opposing selection on the trade-off between seed production and abiotic stress resistance. Our findings suggest that variation in allometry contributes to local adaptation to contrasting environments. Our results help reconcile past debates on the origin of allometric scaling in biology and begin to link adaptive variation in allometric scaling to specific genes.

A General Model for Seed and Seedling Respiratory Metabolism.

The ontogeny of seed plants usually involves a dormant dehydrated state and the breaking of dormancy and germination, which distinguishes it from that of most organisms. Seed germination and seedling establishment are critical ontogenetic stages in the plant life cycle, and both are fueled by respiratory metabolism. However, the scaling of metabolic rate with respect to individual traits remains poorly understood. Here, we tested metabolic scaling theory during seed germination and early establishment growth using a recently developed model and empirical data collected from 41 species. The results show that (i) the mass-specific respiration rate (Rm) was weakly correlated with body mass, mass-specific N content, and mass-specific C content; (ii) Rm conformed to a single Michaelis-Menten curve as a function of tissue water content; and (iii) the central parameters in the model were highly correlated with DNA content and critical enzyme activities. The model offers new insights and a more integrative scaling theory that quantifies the combined effects of tissue water content and body mass on respiratory metabolism during early plant ontogeny.