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.     

生态学代谢理论研究进展

代谢理论是近年来生态学领域的重要进展,不仅有效地解释了生物的新陈代谢率随个体大小和温度的变化规律,还通过代谢率将个体、种群、群落、生态系统水平上的生物学模式联系起来。介绍了代谢理论的研究历史和主要内容,并通过几个例子说明该理论的应用。     

Marine copepod diversity patterns and the metabolic theory of ecology

The ongoing climate change has improved our understanding of how climate affects the reproduction of animals. However, the interaction between food availability and climate on breeding has rarely been examined. While it has been shown that breeding of boreal birds of prey is first and foremost determined by prey abundance, little information exists on how climatic conditions influence this relationship. We studied the joint effects of main prey abundance and ambient weather on timing of breeding and reproductive success of two smaller (pygmy owl Glaucidium passerinum and Tengmalm’s owl Aegolius funereus) and two larger (tawny owl Strix aluco and Ural owl Strix uralensis) avian predator species using long-term nation-wide datasets during 1973–2004. We found no temporal trend either in vole abundance or in hatching date and brood size of any studied owl species. In the larger species, increasing late winter or early spring temperature advanced breeding at least as much as did high autumn abundance of prey (voles). Furthermore, increasing snow depth delayed breeding of the largest species (Ural owl), presumably by reducing the availability of voles. Brood size was strongly determined by spring vole abundance in all four owl species. These results show that climate directly affects the breeding performance of vole-eating boreal avian predators much more than previously thought. According to earlier studies, small-sized species should advance their breeding more than larger species in response to increasing temperature. However, we found an opposite pattern, with larger species being more sensitive to temperature. We argue that this pattern is caused by a difference in the breeding tactics of larger mostly capital breeding and smaller mostly income breeding owl species.     

Latitude,tree species diversity and the metabolic theory of ecology

The latitudinal diversity gradient (LDG) has been known for over a century, but its origin remains poorly understood. Because both latitude and species richness are broadly related to temperature, environmental temperature has been proposed as a driver of the LDG. Recently, Wang et al. (2009, Proceedings of the National Academy of Sciences USA, 106 ,13388–13392) used datasets compiled from tree distributions in eastern Asia and North America to compare the species richness?temperature relationship between the two regions at several spatial scales and framed their analyses in the context of the metabolic theory of ecology. Here, we show that their datasets lack comparability between eastern Asia and North America and that some aspects of their analyses probably biased their results, casting doubt on some of their conclusions.     

Behavioral implications of mechanistic ecology

Summary Mechanistic principles from engineering, meteorology, and soil physics are integrated with ecology and physiology to develop models for prediction of animal behavior. The Mojave Desert biome and the desert iguana are used to illustrate these principles.A transient energy balance model for animals in an outdoor environment is presented. The concepts and relationships have been tested in a wind tunnel, in a simulated desert, and in the field. The animal model requires anatomical information and knowledge of the thermoregulatory responses of the animal. The micrometeorological model requires only basic meteorological parameters and two soil physical properties as inputs. Tests of the model in the field show agreement between predicted and measured temperatures above and below the surface of about 2 to 3°C.The animal and micrometeorological models are combined to predict daily and seasonal activity patterns, available times for predator-prey interaction, and daily, seasonal and annual requirements for food and water. It is shown that food, water and the thermal environment can limit animal activity, and furthermore, the controlling limit changes with season. Actual observations of activity patterns and our predictions show close agreement, in many cases, and pose intriguing questions in those situations where agreement does not exist. This type of modeling can be used to further study predator-prey interactions, to study how changes in the environment might affect animal behavior, and to answer other important ecological and physiological questions.     

The metabolism of lake plankton does not support the metabolic theory of ecology

We tested if the metabolic theory of ecology (MTE) correctly predicts plankton metabolism in a temperate lake, based on a long-term (about 15 years), high-frequency dataset of body size, abundance and production, using two different techniques: least squares regression and maximum likelihood. For phytoplankton, the general fit was relatively poor (r²=0.53). The assumption of the MTE on temperature dependence of metabolism was not supported, and the assumed value of ¾ of the allometric exponent was barely within 95% confidence limits. For some of the models, the value of b was significantly higher than ¾. When radiation was included as an additional predictor, it improved the model considerably (r²=0.67). Including grazing by zooplankton reduced the model residuals during the summer period, when grazing is a dominant factor. The allometric exponent had virtually no effect for phytoplankton, due to little variability in average individual size. Zooplankton production, on the other hand, was better predicted by MTE, showing stronger effects of temperature and body size, the average of which varied by a factor of more than a hundred. However, the best-fitting value of the allometric exponent for zooplankton was 0.85, and significantly higher than the ¾ predicted by the theory. The ratio of observed production to biomass for the entire plankton community declined linearly with the body size (in log-log) with a slope corresponding to a value of b=0.85. We conclude that the MTE has little predictive power for the metabolism of lacustrine plankton, in particular for phytoplankton, and especially at the scale of variability of this study, and that this could be improved by incorporating radiation into the model.     

Elucidating the global elapid (Squamata) richness pattern under metabolic theory of ecology

Environmental determinants of global patterns in species richness are still uncertain. The Metabolic Theory of Ecology (MTE) proposes that species richness patterns can be explained by environmental temperature acting on the metabolism of ectothermic organisms. However, the generality of this theory has been questioned due to its low fit to the geographic variation in species richness of different taxonomic groups. Here, we investigated whether the MTE drives elapid richness, testing the non-stationarity of the relationship between the natural logarithm of species richness (ln S) and the inverse function of temperature (1/kT) using a geographically weighted regression (GWR). The relationship between ln S and 1/kT varied systematically over space and showed non-stationarity. Few tropical locations were consistent with MTE predictions, whereas other regions fitted differently. Although the slope of the GWR model ranged from low to high, the temperature did not predict species richness strongly on average and did not limit the upper values of richness. The response of richness to temperature in some areas might reflect a recent history of colonization and diversification of species across tropical and subtropical regions. In regions not affected by temperature, species richness should be structured by other biotic and abiotic interactions. This scenario reveals that the non-stationarity of the relationship would be linked to idiosyncrasies in the sample sites, which can drift the magnitude or change the relationship between species richness and temperature throughout space.     

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.     

Warming reduces metabolic rate in marine snails: adaptation to fluctuating high temperatures challenges the metabolic theory of ecology

The universal temperature-dependence model (UTD) of the metabolic theory of ecology (MTE) proposes that temperature controls mass-scaled, whole-animal resting metabolic rate according to the first principles of physics (Boltzmann kinetics). Controversy surrounds the model''s implication of a mechanistic basis for metabolism that excludes the effects of adaptive regulation, and it is unclear how this would apply to organisms that live in fringe environments and typically show considerable metabolic adaptation. We explored thermal scaling of metabolism in a rocky-shore eulittoral-fringe snail (Echinolittorina malaccana) that experiences constrained energy gain and fluctuating high temperatures (between 25°C and approximately 50°C) during prolonged emersion (weeks). In contrast to the prediction of the UTD model, metabolic rate was often negatively related to temperature over a benign range (30–40°C), the relationship depending on (i) the temperature range, (ii) the degree of metabolic depression (related to the quiescent period), and (iii) whether snails were isolated within their shells. Apparent activation energies (E) varied between 0.05 and −0.43 eV, deviating excessively from the UTD''s predicted range of between 0.6 and 0.7 eV. The lowering of metabolism when heated should improve energy conservation in a high-temperature environment and challenges both the theory''s generality and its mechanistic basis.     

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.     

Reconsidering what enclosure and exclosure mean in restoration ecology

There is ambiguity in the use of the terms “enclosure” and “exclosure” in describing the passive method used for the restoration of degraded ecosystems. We argue that in the context of ecological restoration, the term enclosure is generally more appropriate to use than exclosure. Unlike exclosure, the term enclosure focuses on the degraded area to be restored, does not exclude selective permeability of external factors, and potentially accommodates local people's livelihood needs. However, the term exclosure is appropriate to use in the case of experimental exclosures or management of restoration sites which explicitly exclude specific disturbance factors.     

Biotelemetry: a mechanistic approach to ecology

Remote measurement of the physiology, behaviour and energetic status of free-living animals is made possible by a variety of techniques that we refer to collectively as 'biotelemetry'. This set of tools ranges from transmitters that send their signals to receivers up to a few kilometers away to those that send data to orbiting satellites and, more frequently, to devices that log data. They enable researchers to document, for long uninterrupted periods, how undisturbed organisms interact with each other and their environment in real time. In spite of advances enabling the monitoring of many physiological and behavioural variables across a range of taxa of various sizes, these devices have yet to be embraced widely by the ecological community. Our review suggests that this technology has immense potential for research in basic and applied animal ecology. Efforts to incorporate biotelemetry into broader ecological research programs should yield novel information that has been challenging to collect historically from free-ranging animals in their natural environments. Examples of research that would benefit from biotelemetry include the assessment of animal responses to different anthropogenic perturbations and the development of life-time energy budgets.     

Spatial patterns of species richness in New World coral snakes and the metabolic theory of ecology

The metabolic theory of ecology (MTE) has attracted great interest because it proposes an explanation for species diversity gradients based on temperature-metabolism relationships of organisms. Here we analyse the spatial richness pattern of 73 coral snake species from the New World in the context of MTE. We first analysed the association between ln-transformed richness and environmental variables, including the inverse transformation of annual temperature (1/kT). We used eigenvector-based spatial filtering to remove the residual spatial autocorrelation in the data and geographically weighted regression to account for non-stationarity in data. In a model I regression (OLS), the observed slope between ln-richness and 1/kT was ?0.626 (r² = 0.413), but a model II regression generated a much steeper slope (?0.975). When we added additional environmental correlates and the spatial filters in the OLS model, the R² increased to 0.863 and the partial regression coefficient of 1/kT was ?0.676. The GWR detected highly significant non-stationarity, in data, and the median of local slopes of ln-richness against 1/kT was ?0.38. Our results expose several problems regarding the assumptions needed to test MTE: although the slope of OLS fell within that predicted by the theory and the dataset complied with the assumption of temperature-independence of average body size, the fact that coral snakes consist of a restricted taxonomic group and the non-stationarity of slopes across geographical space makes MTE invalid to explain richness in this case. Also, it is clear that other ecological and historical factors are important drivers of species richness patterns and must be taken into account both in theoretical modeling and data analysis.     

Some metabolic aspects of ecology

Summary

Due to the similarity of the major metabolic pathways in all living organisms it might be thought unlikely that the study of metabolic variation would add to an understanding of ecological differences. However, a quantitative study of the regulation of metabolism and its end-products indicates a link between cell biochemistry and the capability of certain species to succeed in particular environments. A study of anaerobic metabolism in animals and plants shows a number of similarities in those species able to survive in oxygen-poor environments. These include the production of nontoxic end-products and the avoidance of a large oxygen debt. As a large variety of organisms is examined, these comparisons suggest that the metabolic solutions to a given environmental stress, whether in plants or animals, can be strikingly similar. Therefore, although the main metabolic pathways in most living organism are the same, the regulation of metabolism varies with the ecology of the species. Examples are discussed in which a knowledge of metabolism in relation to ecology could have practical applications in forestry and agriculture.     

Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling

Ecologists have long recognized that species are sustained by the flux, storage and turnover of two biological currencies: energy, which fuels biological metabolism and materials (i.e. chemical elements), which are used to construct biomass. Ecological theories often describe the dynamics of populations, communities and ecosystems in terms of either energy (e.g. population-dynamics theory) or materials (e.g. resource-competition theory). These two classes of theory have been formulated using different assumptions, and yield distinct, but often complementary predictions for the same or similar phenomena. For example, the energy-based equation of von Bertalanffy and the nutrient-based equation of Droop both describe growth. Yet, there is relatively little theoretical understanding of how these two distinct classes of theory, and the currencies they use, are interrelated. Here, we begin to address this issue by integrating models and concepts from two rapidly developing theories, the metabolic theory of ecology and ecological stoichiometry theory. We show how combining these theories, using recently published theory and data along with new theoretical formulations, leads to novel predictions on the flux, storage and turnover of energy and materials that apply to animals, plants and unicells. The theory and results presented here highlight the potential for developing a more general ecological theory that explicitly relates the energetics and stoichiometry of individuals, communities and ecosystems to subcellular structures and processes. We conclude by discussing the basic and applied implications of such a theory, and the prospects and challenges for further development.     

Land-plant ecology on the basis of functional traits

The tissue traits and architectures of plant species are important for land-plant ecology in two ways. First, they control ecosystem processes and define habitat and resources for other taxa; thus, they are a high priority for understanding the ecosystem at a site. Second, knowledge of trait costs and benefits offers the most promising path to understanding how vegetation properties change along physical geography gradients. There exists an informal shortlist of plant traits that are thought to be most informative. Here, we summarize recent research on correlations and tradeoffs surrounding some traits that are prospects for the shortlist. By extending the list and by developing better models for how traits influence species distributions and interactions, a strong foundation of basic ecology can be established, with many practical applications.