Variation in scorpion metabolic rate and rate-temperature relationships: implications for the fundamental equation of the metabolic theory of ecology

The fundamental equation of the metabolic theory of ecology (MTE) indicates that most of the variation in metabolic rate are a consequence of variation in organismal size and environmental temperature. Although evolution is thought to minimize energy costs of nutrient transport, its effects on metabolic rate via adaptation, acclimatization or acclimation are considered small, and restricted mostly to variation in the scaling constant, b(0). This contrasts strongly with many conclusions of evolutionary physiology and life-history theory, making closer examination of the fundamental equation an important task for evolutionary biologists. Here we do so using scorpions as model organisms. First, we investigate the implications for the fundamental equation of metabolic rate variation and its temperature dependence in the scorpion Uroplectes carinatus following laboratory acclimation. During 22 days of acclimation at 25 degrees C metabolic rates declined significantly (from 127.4 to 78.2 microW; P = 0.0001) whereas mean body mass remained constant (367.9-369.1 mg; P = 0.999). In field-fresh scorpions, metabolic rate-temperature (MRT) relationships varied substantially within and among individuals, and therefore had low repeatability values (tau = 0.02) and no significant among-individual variation (P = 0.181). However, acclimation resulted in a decline in within-individual variation of MRT slopes which subsequently revealed significant differences among individuals (P = 0.0031) and resulted in a fourfold increase in repeatability values (tau = 0.08). These results highlight the fact that MRT relationships can show substantial, directional variation within individuals over time. Using a randomization model we demonstrate that the reduction in metabolic rate with acclimation while body mass remains constant causes a decline both in the value of the mass-scaling exponent and the coefficient of determination. Furthermore, interspecific comparisons of activation energy, E, demonstrated significant variation in scorpions (0.09-1.14 eV), with a mean value of 0.77 eV, significantly higher than the 0.6-0.7 eV predicted by the fundamental equation. Our results add to a growing body of work questioning both the theoretical basis and empirical support for the MTE, and suggest that alternative models of metabolic rate variation incorporating explicit consideration of life history evolution deserve further scrutiny.     

WBE 模型及其在生态学中的应用：研究概述

介绍了WBE模型,综述了该模型在生态学中的应用进展。WBE模型,以及以该模型为基础的MTE模型,假设生物体为自相似分形网络结构,提出代谢速率和个体大小之间存在3/4指数关系,分别预测了从个体到生物圈多个尺度上的生物属性之间的异速生长关系,而且部分得到了验证。WBE模型的应用涵盖了个体组织生物量、年生长率,种群密度和生态系统单位面积产量、能量流动率等多个方面;即使在生物圈大尺度上,WBE模型也可用来预测试验中无法直接测量的特征变量的属性,如全球碳储量的估算等。至今,关于WBE和MTE模型仍然存在各种褒贬争论,讨论焦点主要集中于模型建立的前提假设以及权度指数的预测。今后的研究工作应规范试验技术和方法,考虑物种多样性和环境等因素的影响,提出符合各类生物的模型结构体系,使其具有更广泛的应用性和预测性。     

Testing the metabolic theory of ecology

The metabolic theory of ecology (MTE) predicts the effects of body size and temperature on metabolism through considerations of vascular distribution networks and biochemical kinetics. MTE has also been extended to characterise processes from cellular to global levels. MTE has generated both enthusiasm and controversy across a broad range of research areas. However, most efforts that claim to validate or invalidate MTE have focused on testing predictions. We argue that critical evaluation of MTE also requires strong tests of both its theoretical foundations and simplifying assumptions. To this end, we synthesise available information and find that MTE's original derivations require additional assumptions to obtain the full scope of attendant predictions. Moreover, although some of MTE's simplifying assumptions are well supported by data, others are inconsistent with empirical tests and even more remain untested. Further, although many predictions are empirically supported on average, work remains to explain the often large variability in data. We suggest that greater effort be focused on evaluating MTE's underlying theory and simplifying assumptions to help delineate the scope of MTE, generate new theory and shed light on fundamental aspects of biological form and function.     

Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems

Plant-herbivore interactions mediate the trophic structure of ecosystems. We use a comprehensive data set extracted from the literature to test the relative explanatory power of two contrasting bodies of ecological theory, the metabolic theory of ecology (MTE) and ecological stoichiometry (ES), for per-capita and population-level rates of herbivory across ecosystems. We found that ambient temperature and herbivore body size (MTE) as well as stoichiometric mismatch (ES) both constrained herbivory, but at different scales of biological organization. Herbivore body size, which varied over 11 orders of magnitude, was the primary factor explaining variation in per-capita rates of herbivory. Stoichiometric mismatch explained more variation in population-level herbivory rates and also in per-capita rates when we examined data from within functionally similar trophic groups (e.g. zooplankton). Thus, predictions from metabolic and stoichiometric theories offer complementary explanations for patterns of herbivory that operate at different scales of biological organization.     

Metabolic theory or metabolic models?

The metabolic theory of ecology (MTE) claims to derive ecological relationships from the structure of resource distribution networks, which is assumed to determine the scaling of metabolism with body mass, and from the effect of temperature on the rate of biological processes. MTE is controversial. I propose that some of the controversy stems from the implicit adoption of different views of science by the proponents and critics of MTE. The perspective of proponents is consistent with the theory-centric view of science called the received view, whereas many of the critics implicitly adopt an alternative view consistent with a model-centric view of science. I propose that adopting the model-centric view can help to settle some of the differences among proponents and critics of MTE.     

A test of the metabolic theory of ecology with two longevity data sets reveals no common cause of scaling in biological times

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Large‐scale patterns of tree species richness and the metabolic theory of ecology

The metabolic theory of ecology (MTE) endeavours to explain ecosystem structure and function in terms of the effects of temperature and body size on metabolic rate. In a recent paper (Wang et al., 2009, Proceedings of the National Academy of Sciences USA, 106 , 13388), we tested the MTE predictions of species richness using tree distributions in eastern Asia and North America. Our results supported the linear relationship between log‐transformed species richness and the inverse of absolute temperature predicted by the MTE, but the slope strongly depends on spatial scale. The results also indicate that there are more tree species in cold climate at high latitudes in North America than in eastern Asia, but the reverse is true in warm climate at low latitudes. Qian & Ricklefs (2011, Global Ecology and Biogeography, 20 , 362–365) recently questioned our data and some of the analyses. Here we reply to them, and provide further analyses to show that their critiques are primarily based on unsuitable data and subjective conjecture.     

A metabolic theory of ecology applied to temperature and mass dependence of N and P excretion by common carp

Our study used a metabolic theory of ecology (MTE) to explore scaling of metabolic rates by body size and temperature, and to predict nutrient excretion by common carp (Cyprinus carpio). At high biomasses, common carp have negative impacts on water quality, and one mechanism is excretion of the nutrients N and P. We measured whole-body and mass-specific excretion rates during summer and winter for fish of different sizes (wet mass range 28–1,196 g) to produce an allometric scaling model capable of predicting excretion at different temperatures. We found positive relationships between both dissolved and total nutrient concentrations and fish wet mass in summer and winter, with greater excretion rates in summer (mean water temperature 24.2°C) than in winter (mean water temperature 9.2°C). Mass-specific excretion rates decreased with increasing fish size, consistent with the MTE, and the temperature-adjusted model explained more variation for N excretion than for P. The proportion of dissolved nutrients (NH₄ and PO₄) to total nutrients increased with increasing fish size. The significance of these models is that they can be used to predict population-based nutrient excretion by common carp when thermal history, fish density and size distribution in a water body are known.     

Climate change effects on macrofaunal litter decomposition: the interplay of temperature,body masses and stoichiometry

Macrofauna invertebrates of forest floors provide important functions in the decomposition process of soil organic matter, which is affected by the nutrient stoichiometry of the leaf litter. Climate change effects on forest ecosystems include warming and decreasing litter quality (e.g. higher C : nutrient ratios) induced by higher atmospheric CO₂ concentrations. While litter-bag experiments unravelled separate effects, a mechanistic understanding of how interactions between temperature and litter stoichiometry are driving decomposition rates is lacking. In a laboratory experiment, we filled this void by quantifying decomposer consumption rates analogous to predator–prey functional responses that include the mechanistic parameters handling time and attack rate. Systematically, we varied the body masses of isopods, the environmental temperature and the resource between poor (hornbeam) and good quality (ash). We found that attack rates increased and handling times decreased (i) with body masses and (ii) temperature. Interestingly, these relationships interacted with litter quality: small isopods possibly avoided the poorer resource, whereas large isopods exhibited increased, compensatory feeding of the poorer resource, which may be explained by their higher metabolic demands. The combination of metabolic theory and ecological stoichiometry provided critically important mechanistic insights into how warming and varying litter quality may modify macrofaunal decomposition rates.     

The offspring-development-time/offspring-number trade-off

The metabolic theory of ecology (MTE) states that metabolic rate, ruled mainly by individual mass and temperature, determines many other biological rates. This view of ecology as ruled by the laws of physics and thermodynamics contrasts with life-history-optimization (LHO) theories, where traits are shaped by evolutionary processes. Integrating the MTE and LHO can lead, however, to a synthetic theory of ecology. In this work, we link the two theories to show that offspring development time is the result of both maternal investment in offspring and the metabolic constraints on offspring growth. We formulate a model that captures how offspring development time is the consequence of both offspring growth rate, determined by temperature and allometric scaling in accordance with the MTE, and the size reached by offspring at the end of the developmental period, determined mainly by LHO and reproductive strategies. We first extend the trade-off between offspring size and offspring number to ectotherms, showing that increased body temperatures result in increased resources available for reproduction. We then combine this trade-off with the general ontogenetic growth model to show that there is a trade-off between the number of offspring produced and offspring development time. The model predicts a shorter developmental time in organisms producing larger numbers of offspring.     

Evidence that gestation duration and lactation duration are coupled traits in primates

Gestation duration and lactation duration are usually treated as independently evolving traits in primates, but the metabolic theory of ecology (MTE) suggests both durations should be determined by metabolic rate. We used phylogenetic generalized least-squares linear regression to test these different perspectives. We found that the allometries of the durations are divergent from each other and different from the scaling exponent predicted by the MTE (0.25). Gestation duration increases much more slowly (0.06 < m < 0.12), and lactation duration much more quickly (0.36 < m < 0.52) with body mass than the MTE predicts. By contrast, we found that the combined duration of gestation and lactation is consistent with the MTE''s predictions (0.22 < m < 0.35). These results suggest that gestation duration and lactation duration might best be viewed as distinct but coupled adaptations. When transferring energy to their offspring, primate mothers must meet metabolically dictated physiological requirements while optimizing the timing of the switch from gestation to lactation in relation to some as-yet-unidentified body-size-related factor.     

When growth models are not universal: evidence from marine invertebrates

The accumulation of body mass, as growth, is fundamental to all organisms. Being able to understand which model(s) best describe this growth trajectory, both empirically and ultimately mechanistically, is an important challenge. A variety of equations have been proposed to describe growth during ontogeny. Recently, the West Brown Enquist (WBE) equation, formulated as part of the metabolic theory of ecology, has been proposed as a universal model of growth. This equation has the advantage of having a biological basis, but its ability to describe invertebrate growth patterns has not been well tested against other, more simple models. In this study, we collected data for 58 species of marine invertebrate from 15 different taxa. The data were fitted to three growth models (power, exponential and WBE), and their abilities were examined using an information theoretic approach. Using Akaike information criteria, we found changes in mass through time to fit an exponential equation form best (in approx. 73% of cases). The WBE model predominantly overestimates body size in early ontogeny and underestimates it in later ontogeny; it was the best fit in approximately 14% of cases. The exponential model described growth well in nine taxa, whereas the WBE described growth well in one of the 15 taxa, the Amphipoda. Although the WBE has the advantage of being developed with an underlying proximate mechanism, it provides a poor fit to the majority of marine invertebrates examined here, including species with determinate and indeterminate growth types. In the original formulation of the WBE model, it was tested almost exclusively against vertebrates, to which it fitted well; the model does not however appear to be universal given its poor ability to describe growth in benthic or pelagic marine invertebrates.     

Body condition helps to explain metabolic rate variation in wolf spiders

1. Metabolism is the fundamental process that powers life. Understanding what drives metabolism is therefore critical to our understanding of the ecology and behaviour of organisms in nature. 2. Metabolic rate generally scales with body size according to a power law. However, considerable unexplained variation in metabolic rate remains after accounting for body mass with scaling functions. 3. We measured resting metabolic rates (oxygen consumption) of 227 field‐caught wolf spiders. Then, we tested for effects of body mass, species, and body condition on metabolic rate. 4. Metabolic rate scales with body mass to the 0.85 power in these wolf spiders, and there are metabolic rate differences between species. After accounting for these factors, residual variation in metabolic rate is related to spider body condition (abdomen:cephalothorax ratio). Spiders with better body condition consume more oxygen. 5. These results indicate that recent foraging history is an important determinant of metabolic rate, suggesting that although body mass and taxonomic identity are important, other factors can provide helpful insights into metabolic rate variation in ecological communities.     

Summer acclimatization in the short-tailed field vole,Microtus agrestis

We investigated the changes that occurred in basal and noradrenaline-induced metabolic rate, body temperature and body mass in short-tailed field voles,Microtus agrestis, during exposure to naturally increasing photoperiod and ambient temperature. These parameters were first measured in winter-acclimatized voles (n=8) and then in the same voles which had been allowed to seasonally acclimatize to photoperiod and ambient temperature (6 months later). Noradrenaline induced metabolic rate, basal metabolic rate and nonshivering thermogenesis were significantly higher in winter-acclimatized compared to summer-acclimatized voles. There was a significant positive relationship between basal metabolic rate and noradrenaline-induced metabolic rate. Body mass was significantly higher in summer-acclimatized compared to winter-acclimatized voles. There was a significant positive relationship between body mass and noradrenaline-induced metabolic rate in both winter-acclimalized and summer-acclimatized voles; however, there was no relationship between basal metabolic rate and body mass in either seasonal group of voles. Body temperature after measurements of basal metabolic rate was not significantly different in the seasonal cohorts of voles. However, body temperature was significantly higher in winter-acclimatized compared to summer-acclimatized voles after injection of noradrenaline. Previously we have found that a long photoperiod was not a sufficient stimulus to reduce thermogenic capacity in winter-acclimatized voles during cold exposure, since basal metabolic rate increased to compensate for a reduction in regulatory nonshivering thermogenesis. Here we found that a combination of increased ambient temperature and photoperiod did significantly reduce thermogenic capacity in winter-acclimatized voles. This provided evidence that the two aspects of non-shivering thermogenesis, obligatory and regulatory, are stimulated by different exogenous cues. Summer acclimatization in the shorttailed field vole is manifest as a significant decrease in both basal and noradrenaline-induced metabolic rate, combined with a significant increase in body mass.Abbreviations ANCOV A analysis of covariance - BAT brown adipose tissue - BM body mass - BMR basal metabolic rate - NST non-shivering thermogenesis - NA noradrenaline - V the maximum V recorded following mass specific injection of noradrenaline - V the maximum V recorded following mass specific injection of saline - T _a ambient temperature - T _b rectal body temperature - T _1c lower critical temperature - UCP uncoupling protein - V oxygen consumption     

Dynamics of the active site architecture in plant-type ferredoxin-NADP reductases catalytic complexes

Kinetic isotope effects in reactions involving hydride transfer and their temperature dependence are powerful tools to explore dynamics of enzyme catalytic sites. In plant-type ferredoxin-NADP⁺ reductases the FAD cofactor exchanges a hydride with the NADP(H) coenzyme. Rates for these processes are considerably faster for the plastidic members (FNR) of the family than for those belonging to the bacterial class (FPR). Hydride transfer (HT) and deuteride transfer (DT) rates for the NADP⁺ coenzyme reduction of four plant-type FNRs (two representatives of the plastidic type FNRs and the other two from the bacterial class), and their temperature dependences are here examined applying a full tunnelling model with coupled environmental fluctuations. Parameters for the two plastidic FNRs confirm a tunnelling reaction with active dynamics contributions, but isotope effects on Arrhenius factors indicate a larger contribution for donor–acceptor distance (DAD) dynamics in the Pisum sativum FNR reaction than in the Anabaena FNR reaction. On the other hand, parameters for bacterial FPRs are consistent with passive environmental reorganisation movements dominating the HT coordinate and no contribution of DAD sampling or gating fluctuations. This indicates that active sites of FPRs are more organised and rigid than those of FNRs. These differences must be due to adaptation of the active sites and catalytic mechanisms to fulfil their particular metabolic roles, establishing a compromise between protein flexibility and functional optimisation. Analysis of site-directed mutants in plastidic enzymes additionally indicates the requirement of a minimal optimal architecture in the catalytic complex to provide a favourable gating contribution.     

代谢异速生长理论及其在微生物生态学领域的应用

新陈代谢是生物的基本生理过程,影响生物在不同环境中参与物质循环和能量转化的过程.代谢速率作为生物体重要的生命过程指标,几乎影响所有的生物活性速率,且在很多研究中均表现出异速生长现象.所谓代谢异速是指生物体代谢速率与其个体大小(或质量)之间存在的幂函数关系.代谢异速生长理论的提出,从机制模型角度解释了代谢异速关系这一普遍存在的生命现象.该理论利用分形几何学及流体动力学等原理,从生物能量学角度阐释了异速生长规律的机理,证实了3/4权度指数的存在;但同时有研究表明,权度指数因环境因素等影响处于2/3-1范围之间而非定值.随着研究工作的深入,代谢异速生长理论研究从起初的宏观动植物领域拓展到了微生物领域,在研究微生物的代谢异速生长理论时,可将微生物的可操作分类单元(Operational taxonomic unit,OTU)或具有特定功能的功能群视为一个微生物个体,基于其遗传多样性和功能多样性特征进行表征,以便于将微生物群落多样性与其生态功能性联系起来,使该理论在微生物生态学领域得到有效的补充和完善.尽管细菌具有独特的生物学特性,但与宏观生物系统中观测到的现象表现出明显的一致性.有研究表明,3个农田土壤细菌基于遗传多样性的OTU数的平均周转率分别为0.71、0.80和0.84,介于2/3与1之间,可能与生物代谢异速指数有一定关联,为微生物代谢异速指数的研究提出了一个参考解决方案.鉴于微生物个体特征和生物学特性,在分析代谢速率与个体大小关系中,从微生物单位个体的定义、个体大小表征到计量单位的统一,仍需更多的理论支持.分析了代谢异速生长理论在微生物与生态系统功能关系研究中的可能应用,延伸了该理论的应用范围,并对尚待加强的研究问题进行了评述和展望.     

Rate of egg maturation in marine turtles exhibits 'universal temperature dependence'

1. The metabolic theory of ecology (MTE) predicts that, after correcting for body mass variation among organisms, the rates of most biological processes will vary as a universal function of temperature. However, empirical support for 'universal temperature dependence' (UTD) is currently equivocal and based on studies of a limited number of traits. 2. In many ectothermic animals, the rate at which females produce mature eggs is temperature dependent and may be an important factor in determining the costs of reproduction. 3. We tested whether the rate of egg maturation in marine turtles varies with environmental temperature as predicted by MTE, using the time separating successive clutches of individual females to estimate the rate at which eggs are formed. We also assessed the phenotypic contribution to this rate, by using radio telemetry to make repeated measurements of interclutch intervals for individual green turtles (Chelonia mydas). 4. Rates of egg maturation increased with seasonally increasing water temperatures in radio-tracked green turtles, but were not repeatable for individual females, and did not vary according to maternal body size or reproductive investment (number and size of eggs produced). 5. Using a collated data set from several different populations and species of marine turtles, we then show that a single relationship with water temperature explains most of the variation in egg maturation rates, with a slope that is statistically indistinguishable from the UTD predicted by MTE. However, several alternative statistical models also described the relationship between temperature and egg maturation rates equally parsimoniously. 6. Our results offer novel support for the MTE's predicted UTD of biological rates, although the underlying mechanisms require further study. The strong temperature dependence of egg maturation combined with the apparently weak phenotypic contribution to this rate has interesting behavioural implications in ectothermic animals. We suggest that maternal thermoregulatory behaviour in marine turtles, and many other reptiles, is consistent with a strategy of adaptively increasing body temperatures to accelerate egg maturation.     

Thermoregulation in male temperate bats depends on habitat characteristics

Several energy-saving strategies have evolved in animals, one example being the short-term reduction of metabolism and body temperature (torpor) in endotherms. For bats, pronounced torpor behaviour has been described. The aim of this study was to assess individual variation in torpor expression of male Myotis daubentonii, and to analyse whether this variation is related to habitat characteristics. For that we measured skin temperatures of bats from different habitats using radio transmitters and also recorded ambient temperature. Skin temperature was corrected for ambient temperature and individual body mass. Cluster analysis of residuals revealed two different thermoregulatory strategies. Males in cluster 1 were more often encountered torpid and reached lower minimum skin temperatures than males in cluster 2. The differences in behaviour were related to environmental variables (water surface area near the roost, roost altitude, precipitation, ambient temperature in the warmest quarter of the year). Males from cluster 1 occupied less favourable habitats (less water surface, higher altitudes, wetter and colder climate) than males from cluster 2. Our data suggest a linkage between torpor behaviour and habitat characteristics. These characteristics could be used to identify favourable and marginal habitats for M. daubentonii.