Phylogeny and metabolic scaling in mammals

The scaling of metabolic rates to body size is widely considered to be of great biological and ecological importance, and much attention has been devoted to determining its theoretical and empirical value. Most debate centers on whether the underlying power law describing metabolic rates is 2/3 (as predicted by scaling of surface area/volume relationships) or 3/4 ("Kleiber's law"). Although recent evidence suggests that empirically derived exponents vary among clades with radically different metabolic strategies, such as ectotherms and endotherms, models, such as the metabolic theory of ecology, depend on the assumption that there is at least a predominant, if not universal, metabolic scaling exponent. Most analyses claimed to support the predictions of general models, however, failed to control for phylogeny. We used phylogenetic generalized least-squares models to estimate allometric slopes for both basal metabolic rate (BMR) and field metabolic rate (FMR) in mammals. Metabolic rate scaling conformed to no single theoretical prediction, but varied significantly among phylogenetic lineages. In some lineages we found a 3/4 exponent, in others a 2/3 exponent, and in yet others exponents differed significantly from both theoretical values. Analysis of the phylogenetic signal in the data indicated that the assumptions of neither species-level analysis nor independent contrasts were met. Analyses that assumed no phylogenetic signal in the data (species-level analysis) or a strong phylogenetic signal (independent contrasts), therefore, returned estimates of allometric slopes that were erroneous in 30% and 50% of cases, respectively. Hence, quantitative estimation of the phylogenetic signal is essential for determining scaling exponents. The lack of evidence for a predominant scaling exponent in these analyses suggests that general models of metabolic scaling, and macro-ecological theories that depend on them, have little explanatory power.     

Scaling mass and morphology in leaves: an extension of the WBE model

Recent advances in metabolic scaling theory have highlighted the importance of exchange surfaces and vascular network geometry in understanding the integration and scaling of whole-plant form and function. Additional work on leaf form and function has also highlighted general scaling relationships for many leaf traits. However, it is unclear if a common theoretical framework can reveal the general rules underlying much of the variation observed in scaling relationships at the whole-plant and leaf level. Here we present an extension of the general model introduced by G. B. West, J. H. Brown, and B. J. Enquist that has previously been applied to scaling phenomena for whole plants to predict scaling relationships in leaves. Specifically, the model shows how the exponents that describe the scaling of leaf surface area, length, and petiole diameter should change with increasing leaf mass (or with one another) and with variation in leaf dimensionality. The predictions of the model are tested and found to be in general agreement with a large data set of leaves collected from both temperate and arid sites. Our results demonstrate that a general model based on the scaling properties of biological distribution networks can also be successfully applied to understand the diversity of leaf form and function.     

Allometric exponents do not support a universal metabolic allometry

The debate about the value of the allometric scaling exponent (b) relating metabolic rate to body mass (metabolic rate = a x mass(b)) is ongoing, with published evidence both for and against a 3/4-power scaling law continuing to accumulate. However, this debate often revolves around a dichotomous distinction between the 3/4-power exponent predicted by recent models of nutrient distribution networks and a 2/3 exponent predicted by Euclidean surface-area-to-volume considerations. Such an approach does not allow for the possibility that there is no single "true" exponent. In the present study, we conduct a meta-analysis of 127 interspecific allometric exponents to determine whether there is a universal metabolic allometry or if there are systematic differences between taxa or between metabolic states. This analysis shows that the effect size of mass on metabolic rate is significantly heterogeneous and that, on average, the effect of mass on metabolic rate is stronger for endotherms than for ectotherms. Significant differences between scaling exponents were also identified between ectotherms and endotherms, as well as between metabolic states (e.g., rest, field, and exercise), a result that applies to b values estimated by ordinary least squares, reduced major axis, and phylogenetically correct regression models. The lack of support for a single exponent model suggests that there is no universal metabolic allometry and represents a significant challenge to any model that predicts only a single value of b.     

Deviations from predictions of the metabolic theory of ecology can be explained by violations of assumptions

The metabolic theory of ecology (MTE) is based on models derived from the first principles of thermodynamics and biochemical kinetics. The MTE predicts that the relationship between temperature and species richness of ectotherms should show a specific slope. Testing the validity of this model, however, depends on whether empirical data do not violate assumptions and are obtained within contour conditions. When dealing with richness gradients, the MTE must be empirically tested only for ectothermic organisms at high organization levels and when their body size as well as abundance does not vary with temperature gradients. Here we evaluate whether the magnitude of the deviations in slope expected from the MTE to empirical data for New World amphibians is due to the violations of model assumptions and to lack of generality due to restricting contour conditions. We found that the MTE correctly predicted biodiversity patterns only at higher levels of organization and when assumptions of the basic model were not violated. Approximately 60% of the deviations from the MTE-predicted slope across amphibian families were due to violations of the model assumptions. The hypothesis that richness patterns are a function of environmental temperature is too restrictive and does not take complex environmental and ecological processes into account. However, our results suggest that it may be possible to obtain multiple derivations of the MTE equation if idiosyncrasies in spatial and biological/ecological issues that are essential to understanding biodiversity patterns are considered.     

Allocation within a generic scaling framework

Barnes and Roderick [Barnes, B., Roderick, M.L., 2004. An ecological framework linking scales across space and time based on self-thinning. Theoret. Popul. Biol. 66, 113–128] developed a generic ecological framework for scaling from individuals to ecosystems. Their approach is general and can be applied to predict above-ground, or total (above- and below-ground), dry mass. In practice, the most common situation is to measure above-ground dry mass, and apply an allometric relationship to estimate the below-ground component. In this paper we develop a general theory for incorporating the dynamics of plant partitioning into the generic framework. We consider the inclusion of allometric relationships between components (such as between roots and shoots), as well as process driven relationships, and illustrate the application of each case. Through this approach, local scale measurements and individual-based dynamic relationships pertaining to plant partitioning can be applied to an understanding of partitioning at the patch (or ecosystem) scale. Moreover, we also demonstrate that the empirically based allometric relationships have, in some circumstances, a physical explanation, providing biological meaning to empirically established allometric constants.     

Energy use and animal abundance in litter and soil communities

Tools from metabolic scaling and food web theory were used to construct a general model of carbon flux by litter and soil invertebrates. The flux model was used to explore the energetic basis of invertebrate abundance and predicted that abundance should (1) scale linearly with net primary production; (2) be related to the body mass of animals as a power function, with an exponent between -0.65 and -0.85; (3) be related to the average body temperature of animals according to the Boltzmann factor, with an activation energy between 0.27 and 0.79 eV; and (4) decrease by a factor of 0.05 to 0.15 across trophic levels due to gross production efficiency of prey. Model predictions were generally supported by a global data set on invertebrate abundance that was amassed during the International Biological Programme, indicating that fundamental energetic principles explain a large degree of variation in invertebrate abundance across the globe.     

One size fits all: stability of metabolic scaling under warming and ocean acidification in echinoderms

Responses by marine species to ocean acidification (OA) have recently been shown to be modulated by external factors including temperature, food supply and salinity. However the role of a fundamental biological parameter relevant to all organisms, that of body size, in governing responses to multiple stressors has been almost entirely overlooked. Recent consensus suggests allometric scaling of metabolism with body size differs between species, the commonly cited ‘universal’ mass scaling exponent (b) of ¾ representing an average of exponents that naturally vary. One model, the Metabolic-Level Boundaries hypothesis, provides a testable prediction: that b will decrease within species under increasing temperature. However, no previous studies have examined how metabolic scaling may be directly affected by OA. We acclimated a wide body-mass range of three common NE Atlantic echinoderms (the sea star Asterias rubens, the brittlestars Ophiothrix fragilis and Amphiura filiformis) to two levels of pCO₂ and three temperatures, and metabolic rates were determined using closed-chamber respirometry. The results show that contrary to some models these echinoderm species possess a notable degree of stability in metabolic scaling under different abiotic conditions; the mass scaling exponent (b) varied in value between species, but not within species under different conditions. Additionally, we found no effect of OA on metabolic rates in any species. These data suggest responses to abiotic stressors are not modulated by body size in these species, as reflected in the stability of the metabolic scaling relationship. Such equivalence in response across ontogenetic size ranges has important implications for the stability of ecological food webs.     

Metabolic rates of epipelagic marine zooplankton as a function of body mass and temperature

The metabolic rates (oxygen uptake, ammonia excretion, phosphate excretion) of epipelagic marine zooplankton have been expressed as a function of body mass (dry, carbon, nitrogen and phosphorus weights) and habitat temperature, using the multiple-regression method. Zooplankton data used for this analysis are from phylogenetically mixed groups (56 to 143 species, representing 7 to 8 phyla, body mass range: 6 orders of magnitude) from various latitudes (habitat temperature range:-1.4° to 30°C). The results revealed that 84 to 96% of variation in metabolic rates is due to body mass and habitat temperature. Among the various body-mass units, the best correlation was provided by carbon and nitrogen units for all three metabolic rates. Oxygen uptake, ammonia excretion and phosphate excretion are all similar in terms of body-mass effect, but differ in terms of temperature effect. With carbon or nitrogen body-mass units, calculated Q₁₀ values are 1.82 to 1.89 for oxygen uptake, 1.91 to 1.93 for ammonia excretion and 1.55 for phosphate excretion. The effects of body mass and habitat temperature on the metabolic quotients (O:N, N:P, O:P) are insignificant. The present results for oxygen-uptake rate vs body mass do not differ significantly from those reported for general poikilotherms by Hemmingsen and for crustaceans by Ivleva at a comparable temperature (20°C). The importance of a body-mass measure for meaningful comparison is suggested by the evaluation of the habitat-temperature effect between mixed taxonomic groups and selected ones. Considering the dominant effects of body mass and temperature on zooplankton metabolic rates, the latitudinal gradient of community metabolic rate for net zooplankton in the ocean is estimated, emphasizing the non-parallelism between community metabolic rates and the standing stock of net zooplankton.     

Plant biomass allocation strategies of the dominant species in an alpine meadow of northwestern Sichuan,China北大核心CSCD

Plant biomass partitioning is an important driver of whole-plant net carbon gain, as biomass allocation could directly affect plant's future growth and reproduction. Alpine meadow in the northwestern Sichuan was impressed by the abundant community structure and species diversity. This study on biomass allocation pattern of different functional types and lifeforms might help understand plant life-history strategy of alpine meadow plants. We investigated 72 dominant herbaceous species for their compartments, biomass, and morphological traits during 2012-2014. These plants were sampled from natural grassland, disturbed grassland, and wintergreen grassland; they belonged to three functional types (grass, sedge, and forb) and two lifeforms (annual and perennial). The scaling relationships between functional traits of these plants were analyzed using Model type II regression method to estimate the parameters of the allometric equations. (1) Biomass allocation proportion of components significantly differed among grasses, sedges, and forbs owing to phylogeny: grasses had the highest stem biomass percentage, sedges had higher root biomass percentage, and forbs had higher leaf biomass percentage, but the scaling relationships were not significantly different, and isometric scaling was noted between biomass components for the three functional types. (2) Moreover, plant lifeforms affected the biomass allocation proportion of components, owing to the shorter or longer turnover rate and investment strategy between annual and perennial species. Annuals allocated more biomass to the stem and reproduction organs, but perennials invested more biomass to the leaves and roots. (3) In addition, plants from different grassland types differed in both biomass and morphology traits. Moreover, forbs from natural grassland and wintergreen grassland had higher leaf and reproductive biomass, but those from disturbed grasslands had higher stem biomass. Our results suggest that the functional type and lifeform decide the inherent scaling relationships between components of plants, but anthropogenic disturbance significantly impacted the quantity of component biomass. This study has important theoretical and practical significance to understand the response of alpine plants to climate change and anthropogenic disturbance as well as to help in the scientific management of alpine meadow. © 2018 Science Press. All rights reserved.     

The top-down mechanism for body-mass-abundance scaling

Scaling relationships between mean body masses and abundances of species in multitrophic communities continue to be a subject of intense research and debate. The top-down mechanism explored in this paper explains the frequently observed inverse linear relationship between body mass and abundance (i.e., constant biomass) in terms of a balancing of resource biomasses by behaviorally and evolutionarily adapting foragers, and the evolutionary response of resources to this foraging pressure. The mechanism is tested using an allometric, multitrophic community model with a complex food web structure. It is a statistical model describing the evolutionary and population dynamics of tens to hundreds of species in a uniform way. Particularities of the model are the detailed representation of the evolution and interaction of trophic traits to reproduce topological food web patterns, prey switching behavior modeled after experimental observations, and the evolutionary adaptation of attack rates. Model structure and design are discussed. For model states comparable to natural communities, we find that (1) the body-mass abundance scaling does not depend on the allometric scaling exponent of physiological rates in the form expected from the energetic equivalence rule or other bottom-up theories; (2) the scaling exponent of abundance as a function of body mass is approximately -1, independent of the allometric exponent for physiological rates assumed; (3) removal of top-down control destroys this pattern, and energetic equivalence is recovered. We conclude that the top-down mechanism is active in the model, and that it is a viable alternative to bottom-up mechanisms for controlling body-mass-abundance relations in natural communities.     

Metabolic rates of juvenile scalloped hammerhead sharks (Sphyrna lewini)

Oxygen consumption of juvenile scalloped hammerhead sharks, Sphyrna lewini, was measured in a Brett-type flume (volume=635 l) to quantify metabolic rates over a range of aerobic swimming speeds and water temperatures. Oxygen consumption (log transformed) increased at a linear rate with increases in tailbeat frequency and swimming speed. Estimates of standard metabolic rate ranged between 161 mg O₂ kg^-1 h^-1 at 21°C and 203 mg O₂ kg^-1 h^-1 at 29°C (mean-SD: 189ᆣ mg O₂ kg^-1 h^-1 at 26°C). Total metabolic rates ranged from 275 mg O₂ kg^-1 h^-1 at swimming speeds of 0.5 body lengths per second (L s^-1) to a maximum aerobic metabolic rate of 501 mg O₂ kg^-1 h^-1 at 1.4 L s^-1. Net cost of transport was highest at slower swimming speeds (0.5-0.6 L s^-1) and was lowest between 0.75 and 0.9 L s^-1. Therefore, these sharks are most energy efficient at swimming speeds between 0.75 and 0.9 L s^-1. These data indicate that tailbeat frequency and swimming speed can be used as predictors of metabolic rate of free-swimming juvenile hammerhead sharks.     

Linking patch-use behavior, resource density, and growth expectations in fish

Optimality theory rests on the assumptions that short-term foraging decisions are driven by variation in environmental quality, and that these decisions have important implications for long-term fitness. These assumptions, however, are rarely tested in a field setting. We linked behavioral foraging decisions in food patches with measures of environmental quality covering larger spatial (resource density) or temporal (growth parameters) scales. In 10 lakes, we measured the food density at which benthic fish give up foraging in experimental food patches (giving-up density, GUD), quantified the biomass of benthic invertebrates, and calculated the maximum individual size (L(infinity)) of bream (Abramis brama L.), a typical benthivore in these lakes. We found positive relationships between resource density and both GUD and L(infinity), and a positive relationship between L(infinity) and GUD. Prey characterized as vulnerable to predation contributed most to the relationships between resource density and either GUD or L(infinity). A path analysis showed that resource density and L(infinity) directly explained 54% and 28%, respectively, of the variation in GUD, whereas 86% of the variation in L(infinity) was explained by resource density, with mostly indirect contribution from GUD. We conclude that the short-term foraging behavior of benthivores matched our expectations based on optimality theory by being positively linked to variables on environmental quality operating at both a larger spatial scale and a longer temporal scale.     

Interspecific resource partitioning in sympatric ursids.

The fundamental niche of a species is rarely if ever realized because the presence of other species restricts it to a narrower range of ecological conditions. The effects of this narrower range of conditions define how resources are partitioned. Resource partitioning has been inferred but not demonstrated previously for sympatric ursids. We estimated assimilated diet in relation to body condition (body fat and lean and total body mass) and reproduction for sympatric brown bears (Ursus arctos) and American black bears (U. americanus) in south-central Alaska, 1998-2000. Based on isotopic analysis of blood and keratin in claws, salmon (Oncorhynchus spp.) predominated in brown bear diets (> 53% annually) whereas black bears assimilated 0-25% salmon annually. Black bears did not exploit salmon during a year with below average spawning numbers, probably because brown bears deterred black bear access to salmon. Proportion of salmon in assimilated diet was consistent across years for brown bears and represented the major portion of their diet. Body size of brown bears in the study area approached mean body size of several coastal brown bear populations, demonstrating the importance of salmon availability to body condition. Black bears occurred at a comparable density (mass:mass), but body condition varied and was related directly to the amount of salmon assimilated in their diet. Both species gained most lean body mass during spring and all body fat during summer when salmon were present. Improved body condition (i.e., increased percentage body fat) from salmon consumption reduced catabolism of lean body mass during hibernation, resulting in better body condition the following spring. Further, black bear reproduction was directly related to body condition; reproductive rates were reduced when body condition was lower. High body fat content across years for brown bears was reflected in consistently high reproductive levels. We suggest that the fundamental niche of black bears was constrained by brown bears through partitioning of food resources, which varied among years. Reduced exploitation of salmon caused black bears to rely more extensively on less reliable or nutritious food sources (e.g., moose [Alces alces], berries) resulting in lowered body condition and subsequent reproduction.     

Metabolic rates of epipelagic marine copepods as a function of body mass and temperature

Metabolic rates (oxygen consumption, ammonia excretion, phosphate excretion) have been calculated as a function of body mass (dry, carbon, nitrogen and phosphorus weights) and habitat temperature, using multiple regression. The metabolic data used for this analysis were species structured, collected from Arctic to Antarctic seas (temperature range: -1.7°C to 29.0°C). The data were further divided into geographical and/or seasonal groups (35 species and 43 data sets for oxygen consumption; 38 species and 58 data sets for ammonia excretion; 22 species and 31 data sets for phosphate excretion). The results revealed that the variance attributed to body mass and temperature was highest (93-96%) for oxygen consumption rates, followed by ammonia excretion rates (74-80%) and phosphate excretion rates (46-56%). Among the various body mass units, the best correlation was provided by the nitrogen unit, followed by the dry weight unit. The calculated Q₁₀ values varied slightly according to the choice of body mass units; overall ranges were 1.8-2.1 for oxygen consumption rates, 1.8-2.0 for ammonia excretion rates and 1.6-1.9 for phosphate excretion rates. The effects of body mass and temperature on the metabolic quotients (O:N, N:P, O:P) were insignificant in most cases. Although the copepod metabolic data used in the present analysis were for adult and pre-adult stages, possible applications of the resultant regression equations to predict the metabolic rates of naupliar and early copepodite stages are discussed. Finally, global patterns of net growth efficiency [growth (growth+metabolism)^-1] of copepods were deduced by combining the present metabolic equation with Hirst and Lampitt's global growth equation for epipelagic marine copepods.     

Life history traits predict relative abundance in an assemblage of forest caterpillars

Species in a given trophic level occur in vastly unequal abundance, a pattern commonly documented but poorly explained for most taxa. Theoretical predictions of species density such as those arising from the metabolic theory of ecology hold well at large spatial and temporal scales but are not supported in many communities sampled at a relatively small scale. At these scales ecological factors may be more important than the inherent limits to energy use set by allometric scaling of mass. These factors include the amount of resources available, and the ability of individuals to convert these resources successfully into population growth. While previous studies have demonstrated the limits of macroecological theory in explaining local abundance, few studies have tested alternative generalized mechanisms determining abundance at the community scale. Using an assemblage of forest moth species found co-occurring as caterpillars on a single host plant species, we tested whether species abundance on that plant could be explained by mass allometry, intrinsic population growth, diet breadth, or some combination of these traits. We parameterized life history traits of the caterpillars in association with the host plant in both field and laboratory settings, so that the population growth estimate was specific to the plant on which abundance was measured. Using a generalized least-squares regression method incorporating phylogenetic relatedness, we found no relationship between abundance and mass but found that abundance was best explained by both intrinsic population growth rate and diet breadth. Species population growth potential was most affected by survivorship and larval development time on the host plant. Metabolic constraints may determine upper limits to local abundance levels for species, but local community abundance is strongly predicted by the potential for population increase and the resources available to that species in the environment.     

Allocation in reproduction is not tailored to the probable number of matings in common toad (<Emphasis Type="Italic">Bufo bufo</Emphasis>) males

The theory of life history evolution assumes trade-offs between competing fitness traits such as reproduction, somatic growth, and maintenance. One prediction of this theory is that if large individuals have a higher reproductive success, small/young individuals should invest less in reproduction and allocate more resources in growth than large/old individuals. We tested this prediction using the common toad (Bufo bufo), a species where mating success of males is positively related to their body size. We measured testes mass, soma mass, and sperm stock size in males of varying sizes that were either (1) re-hibernated at the start of the breeding season, (2) kept without females throughout the breeding season, or (3) repeatedly provided with gravid females. In the latter group, we also estimated fertilization success and readiness to re-mate. Contrary to our predictions, the relationship between testes mass and soma mass was isometric, sperm stock size relative to testes mass was unrelated to male size, fertilization success was not higher in matings with larger males, and smaller males were not less likely to engage in repeated matings than larger males. These results consistently suggest that smaller males did not invest less in reproduction to be able to allocate more in growth than larger males. Causes for this unexpected result may include relatively low year-to-year survival, unpredictable between-year variation in the strength of sexual selection and low return rates of lowered reproductive investment.     

The allometry of plant spacing that regulates food intake rate in mammalian herbivores

The distance that mammalian herbivores can travel without interrupting food processing corresponds to a distance threshold (d*) in plant spacing where change occurs in the mechanisms regulating the functional response. The instantaneous rate of food consumption is controlled by food encounter rate when plant spacing exceeds d*. Below this threshold, food processing in the mouth controls instantaneous intake rate. The distance threshold provides a mechanistic definition of the scale of heterogeneity of the food resource. Recent work indicates that d* should scale positively with the body mass of mammalian herbivores. Here I evaluated the empirical evidence for this positive scaling by investigating (1) herbivores consuming only alfalfa (Medicago sativa), (2) grazers, and (3) herbivores consuming any kind of vegetation. Overall, I found greater evidence for a negative than for a positive scaling of d*. Out of the three groups, only herbivores consuming alfalfa could yield a positive covariation between d* and body mass. However, even this positive scaling became negative when herbivores consumed bites of alfalfa that were only a fraction of their maximum size. Finally, d* also scaled negatively among herbivores foraging in similar food patches. Overall, differences in foraging decisions among mammalian herbivores seem more likely to have been shaped by a negative than a positive scaling of d*.     

Effect of butyl benzyl phthalate on life table-demography of two successive generations of cladoceran Moina macrocopa Straus

In this study, the acute toxicity of butyl benzyl phthalate (BBP) to freshwater cladoceran Moina macrocopa was tested, and its chronic effects on survival and reproduction of two successive generations of the cladoceran were studied using life-table demographic method. The results showed that the 48-hr LC50 of BBP for M. macrocopa was 3.69 mg l(-1). Compared to the blank controls, BBP at 125, 500, 1000 and 2000 microg l(-1) significantly shortened the life expectancy at birth, BBP at 125-2000 microg l(-1) decreased the net reproductive rate, and BBP at 500 and 1000 microg I(-1) shortened the generation time but increased the intrinsic rate of population increase of the parental M. macrocopa. BBP at 62.5,125, 500,1000 and 2000 microg l(-1) increased the intrinsic rate of population increase of the F1 generation. A significant dose-effect relationship existed between BBP concentration and life expectancy at birth, net reproductive rate as well as intrinsic rate of population increase of the parental M. macrocopa. The parental M. macrocopa were more sensitive in survival, development and reproduction to BBP than the F1 generation, but the reverse was also true in the population growth. Extending chronic toxicity tests to the second generation of M. macrocopa increased the cost-effectiveness of the assays.     

Thermal and energetic constraints on ectotherm abundance: a global test using lizards

Population densities of birds and mammals have been shown to decrease with body mass at approximately the same rate as metabolic rates increase, indicating that energetic needs constrain endotherm population densities. In ectotherms, the exponential increase of metabolic rate with body temperature suggests that environmental temperature may additionally constrain population densities. Here we test simple bioenergetic models for an ecologically important group of ectothermic vertebrates by examining 483 lizard populations. We find that lizard population densities decrease as a power law of body mass with a slope approximately inverse to the slope of the relationship between metabolic rates and body mass. Energy availability should limit population densities. As predicted, environmental productivity has a positive effect on lizard density, strengthening the relationship between lizard density and body mass. In contrast, the effect of environmental temperature is at most weak due to behavioral thermoregulation, thermal evolution, or the temperature dependence of ectotherm performance. Our results provide initial insights into how energy needs and availability differentially constrain ectotherm and endotherm density across broad spatial scales.