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.     

Bottom-up regulation of plant community structure in an aridland ecosystem

We conducted a long-term rodent exclosure experiment in native grass- and shrub-dominated vegetation to evaluate the importance of top-down and bottom-up controls on plant community structure in a low-productivity aridland ecosystem. Using multiple regressions and analysis of covariance, we assessed how bottom-up precipitation pulses cascade through vegetation to affect rodent populations, how rodent populations affect plant community structure, and how rodents alter rates of plant community change over time. Our findings showed that bottom-up pulses cascade through the system, increasing the abundances of plants and rodents, and that rodents exerted no control on plant community structure and rate of change in grass-dominated vegetation, and only limited control in shrub-dominated vegetation. These results were discussed in the context of top-down effects on plant communities across broad gradients of primary productivity. We conclude that bottom-up regulation maintains this ecosystem in a state of low primary productivity that constrains the abundance of consumers such that they exert limited influence on plant community structure and dynamics.     

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.     

Diversity–stability relationships revisited: scaling rules for biological communities near equilibrium

The debate on diversity–stability relationships has a long history of theoretical interest and plays a central role in development of modern ecology. But such debate has recently re-opened under critical scrutiny both in theoretical and empirical studies. In this paper we use allometric (or energetic) scaling and statistical physics approaches to this problem. On the basis of local Damuth symmetry, a Markov model of transfer of energy between different species, and the fluctuation–dissipation theorem, scaling rules of species number and population variability of biological communities near equilibrium are derived. These scaling rules indicate that the diversity–stability relationship may be an energetic and thermodynamic consequence of ecological systems near equilibrium, not a simple statistical consequence as derived by other recent theoretical work.     

Habitat provisioning for aboveground predators decreases detritivores

Although provisioning of habitat by ecosystem engineers is one of the most common biological interactions, previous studies have mostly focused on facilitative or bottom-up processes. Here we show that engineering effects can indirectly strengthen top-down effects mediated by predator abundance. We conducted a small-scale manipulative field experiment and broad-scale field observations of the plant, web spider, and detrital insect system in forest understory habitats. In the field experiment, artificially increasing architectural elements enhanced the abundance of spiders by providing physical support for web building. Moreover, aerial insects derived from the detrital food web decreased in response to increased spider abundance. As artificial architecture per se did not affect aerial detritivores, these results indicate that ecosystem engineering indirectly strengthens top-down effects mediated by predators. In field observations conducted in 12 cedar forests, path analyses supported the importance of an indirect pathway originating from understory vegetation complexity to spider abundance and to aerial detritivores. The effect size of spiders on detrital insects was similar in the field experiment and in the observations. These results indicate that the engineering effects of plants cascade to detrital insects through web spiders across different scales.     

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.     

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.     

Scaling toxicity data across species

The response of various species to doses of chemicals can often give the impression that some (such as cattle in the case of molybdenum) are much more susceptible than others to these chemicals. These impressions usually rely on an underlying assumption that equivalent doses are based on mg of the chemical per kg body weight of the animal. That is, that doses scale as the first power of body weight. This assumption is more often wrong than right. When viewed in a more general way, where the scaling is proportional to a power of the body weight and the exponent determined empirically, it is often found that equivalent doses scale with an exponent in the range of 0.6 to 0.8. As a result, larger animals are indeed more susceptible to toxicity on a mg kg^–1 body weight basis, but this is not because of unique differences in the species, but only because of different body sizes. This method of scaling is called allometry or allometric scaling. An early version of this approach was based on body surface area where the exponent is 2/3. More recently, pharmacokinetics has revealed that the reason for the different response of larger animals is related to the slower metabolic and clearance rates for larger animals which give rise to larger biological half-lives for chemicals in the body and to higher tissue concentrations per given dose.     

Turning up the heat: temperature influences the relative importance of top-down and bottom-up effects

Understanding how communities respond to changes in temperature is a major challenge for community ecology. Temperature influences the relative degree to which top-down and bottom-up forces structure ecological communities. In greenhouse experiments using the aquatic community found in pitcher plants (Sarracenia purpurea), I tested how temperature affected the relative importance of top-down (mosquito predation) and bottom-up (ant carcasses) forces on protozoa and bacteria populations. While bottom-up effects did not vary consistently with temperature, the top-down effects of predators on protozoa increased at higher temperatures. These results suggest that temperature could change the relative importance of top-down and bottom-up effects in ecological communities. Specifically, higher temperature may increase the strength of top-down effects by raising predator metabolic rate and concomitant processes (e.g., activity, foraging, digestion, growth) relative to cooler temperatures. These findings apply broadly to an understanding of trophic interactions in a variable environment and are especially relevant in the context of ongoing climate change.     

Individual- and population-level responses of a keystone predator to geographic variation in prey

Investigating how food supply regulates the behavior and population structure of predators remains a central focus of population and community ecology. These responses will determine the strength of bottom-up processes through the food web, which can potentially lead to coupled top-down regulation of local communities. However, characterizing the bottom-up effects of prey is difficult in the case of generalist predators and particularly with predators that have large dispersal scales, attributes that characterize most marine top predators. Here we use long-term data on mussel, barnacle, limpet, and other adult prey abundance and recruitment at sites spread over 970 km to investigate individual- and population-level responses of the keystone intertidal sunstar Heliaster helianthus on the coast of Chile. Our results show that this generalist predator responds to changes in the supply of an apparently preferred prey, the competitively dominant mussel Perumytilus purpuratus. Individual-level parameters (diet composition, per capita prey consumption, predator size) positively responded to increased mussel abundance and recruitment, whereas population-level parameters (density, biomass, size structure) did not respond to bottom-up prey variation among sites separated by a few kilometers. No other intertidal prey elicited positive individual predator responses in this species, even though a large number of other prey species was always included in the diet. Moreover, examining predator-prey correlations at approximately 80, 160, and 200 km did not change this pattern, suggesting that positive prey feedback could occur over even larger spatial scales or as a geographically unstructured process. Thus individual-level responses were not transferred to population changes over the range of spatial scales examined here, highlighting the need to examine community regulation processes over multiple spatial scales.     

Testing the metabolic theory of ecology: allometric scaling exponents in mammals

Many fundamental traits of species measured at different levels of biological organization appear to scale as a power law to body mass (M) with exponents that are multiples of 1/4. Recent work has united these relationships in a "metabolic theory of ecology" (MTE) that explains the pervasiveness of quarter-power scaling by its dependence on basal metabolic rate (B), which scales as M(0.75). Central to the MTE is theory linking the observed -0.25 scaling of maximum population growth rate (rm) and body mass to the 0.75 scaling of metabolic rate and body mass via relationships with age at first reproduction (alpha) derived from a general growth model and demographic theory. We used this theory to derive two further predictions: that age at first reproduction should scale inversely to mass-corrected basal metabolic rate alpha infinity (B/M)(-l) such that rm infinity (B/M)1. We then used phylogenetic generalized least squares and model selection methods to test the predicted scaling relationships using data from 1197 mammalian species. There was a strong phylogenetic signal in these data, highlighting the need to account for phylogeny in allometric studies. The 95% confidence intervals included, or almost included, the scaling exponent predicted by MTE for B infinity M(0.75), rm infinity M(-0.25), and rm infinity alpha(-1), but not for alpha infinity M(0.25) or the two predictions that we generated. Our results highlight a mismatch between theory and observation and imply that the observed -0.25 scaling of maximum population growth rate and body mass does not arise via the mechanism proposed in the MTE.     

Long-term change in benthopelagic fish abundance in the abyssal northeast Pacific Ocean

Food web structure, particularly the relative importance of bottom-up and top-down control of animal abundances, is poorly known for the Earth's largest habitats: the abyssal plains. A unique 15-yr time series of climate, productivity, particulate flux, and abundance of primary consumers (primarily echinoderms) and secondary consumers (fish) was examined to elucidate the response of trophic levels to temporal variation in one another. Towed camera sled deployments in the abyssal northeast Pacific (4100 m water depth) showed that annual mean numbers of the dominant fish genus (Coryphaenoides spp.) more than doubled over the period 1989-2004. Coryphaenoides spp. abundance was significantly correlated with total abundance of mobile epibenthic megafauna (echinoderms), with changes in fish abundance lagging behind changes in the echinoderms. Direct correlations between surface climate and fish abundances, and particulate organic carbon (POC) flux and fish abundances, were insignificant, which may be related to the varied response of the potential prey taxa to climate and POC flux. This study provides a rare opportunity to study the long-term dynamics of an unexploited marine fish population and suggests a dominant role for bottom-up control in this system.     

Crown ratio influences allometric scaling in trees

Allometric theories suggest that the size and shape of organisms follow universal rules, with a tendency toward quarter-power scaling. In woody plants, however, structure is influenced by branch death and shedding, which leads to decreasing crown ratios, accumulation of heartwood, and stem and branch tapering. This paper examines the impacts on allometric scaling of these aspects, which so far have been largely ignored in the scaling theory. Tree structure is described in terms of active and disused pipes arranged as an infinite branching network in the crown, and as a tapering bundle of pipes below the crown. Importantly, crown ratio is allowed to vary independently of crown size, the size of the trunk relative to the crown deriving from empirical results that relate crown base diameter to breast height diameter through crown ratio. The model implies a scaling relationship in the crown which reduces to quarter-power scaling under restrictive assumptions but would generally yield a scaling exponent somewhat less than three-quarters. For the whole tree, the model predicts that scaling between woody mass and foliage depends on crown ratio. Measurements on three boreal tree species are consistent with the model predictions.     

Two-way coupling versus one-way forcing of plankton and fish models to predict ecosystem changes in the Benguela

‘End-to-end’ models have been adopted in an attempt to capture more of the processes that influence the ecology of marine ecosystems and to make system wide predictions of the effects of fishing and climate change. Here, we develop an end-to-end model by coupling existing models that describe the dynamics of low (ROMS–N₂P₂Z₂D₂) and high trophic levels (OSMOSE). ROMS–N₂P₂Z₂D₂ is a biogeochemical model representing phytoplankton and zooplankton seasonal dynamics forced by hydrodynamics in the Benguela upwelling ecosystem. OSMOSE is an individual-based model representing the dynamics of several species of fish, linked through opportunistic and size-based trophic interactions. The models are coupled through a two-way size-based predation process. Plankton provides prey for fish, and the effects of predation by fish on the plankton are described by a plankton mortality term that is variable in space and time. Using the end-to-end model, we compare the effects of two-way coupling versus one-way forcing of the fish model with the plankton biomass field. The fish-induced mortality on plankton is temporally variable, in part explained by seasonal changes in fish biomass. Inclusion of two-way feedback affects the seasonal dynamics of plankton groups and usually reduces the amplitude of variation in abundance (top-down effect). Forcing and coupling lead to different predicted food web structures owing to changes in the dominant food chain which is supported by plankton (bottom-up effect). Our comparisons of one-way forcing and two-way coupling show how feedbacks may affect abundance, food web structure and food web function and emphasise the need to critically examine the consequences of different model architectures when seeking to predict the effects of fishing and climate change.     

Herbivore vs. nutrient control of marine primary producers: context-dependent effects

Pervasive overharvesting of consumers and anthropogenic nutrient loading are changing the strengths of top-down and bottom-up forces in ecosystems worldwide. Thus, identifying the relative and synergistic roles of these forces and how they differ across habitats, ecosystems, or primary-producer types is increasingly important for understanding how communities are structured. We used factorial meta-analysis of 54 field experiments that orthogonally manipulated herbivore pressure and nutrient loading to quantify consumer and nutrient effects on primary producers in benthic marine habitats. Across all experiments and producer types, herbivory and nutrient enrichment both significantly affected primary-producer abundance. They also interacted to create greater nutrient enrichment effects in the absence of herbivores, suggesting that loss of herbivores produces more dramatic effects of nutrient loading. Herbivores consistently had stronger effects than did nutrient enrichment for both tropical macroalgae and seagrasses. The strong effects of herbivory but limited effects of nutrient enrichment on tropical macroalgae suggest that suppression of herbivore populations has played a larger role than eutrophication in driving the phase shift from coral- to macroalgal-dominated reefs in many areas, especially the Caribbean. For temperate macroalgae and benthic microalgae, the effects of top-down and bottom-up forces varied as a function of the inherent productivity of the ecosystem. For these algal groups, nutrient enrichment appeared to have stronger effects in high- vs. low-productivity systems, while herbivores exerted a stronger top-down effect in low-productivity systems. Effects of herbivores vs. nutrients also varied among algal functional groups (crustose algae, upright macroalgae, and filamentous algae), within a functional group between temperate and tropical systems, and according to the metric used to measure producer abundance. These analyses suggest that human alteration of food webs and nutrient availability have significant effects on primary producers but that the effects vary among latitudes and primary producers, and with the inherent productivity of ecosystems.     

Bottom-up and top-down effects on insect herbivores do not vary among sites of different salinity

It has been suggested, but rarely tested, that the relative strength of top-down and bottom-up factors in communities varies along an environmental stress gradient. We compared the strength of bottom-up and top-down effects on the densities of insect herbivores along a range of sites of different salinities in west-central Florida. We used a 2 x 2 factorial design with plots divided into four treatments: (1) bottom-up manipulation, where fertilizer was applied to increase plant quality; (2) top-down manipulation, where sticky traps were used to reduce the effects of natural enemies (parasitoids); (3) bottom-up and top-down manipulation, where fertilizer was applied and sticky traps were used; and (4) control plots. These plots were established along a range of salinities among seven different sites containing the salt marsh plant Borrichia frutescens. In each plot, we determined the parasitism levels and abundances of the sap sucker Pissonotus quadripustulatus, the gall maker Asphondylia borrichiae, and the lepidopteran stem borer Argyresthia spp. Gall density, Pissonotus density, and stem borer density were significantly higher in lower salinity sites, suggesting a strong effect of environmental stress. There was a significant increase of galls and Pissonotus and a marginally significant increase of bored stems on fertilized plots but not on trapped plots. There was a significant interaction of site and fertilizer on gall parasitism. There were no interactions of either treatment with salinity on herbivore densities. The general lack of interaction between salinity level and other treatments on herbivore densities contrasts with our previous result where treatment effects did vary with salinity level on a large experimentally generated salinity gradient at one site. Thus, the results of the present paper suggest that, while environmental stress can modify top-down and bottom-up effects on herbivores at single sites, variation in site-to-site factors, possibly including clonal identity of plant, affects herbivore densities so much as to swamp out any observable interaction between environmental stress and top-down or bottom-up factors.     

Interacting trophic forcing and the population dynamics of herring

Small pelagic fish occupy a central position in marine ecosystems worldwide, largely by determining the energy transfer from lower trophic levels to predators at the top of the food web, including humans. Population dynamics of small pelagic fish may therefore be regulated neither strictly bottom-up nor top-down, but rather through multiple external and internal drivers. While in many studies single drivers have been identified, potential synergies of multiple factors, as well as their relative importance in regulating population dynamics of small pelagic fish, is a largely unresolved issue. Using a statistical, age-structured modeling approach, we demonstrate the relative importance and influence of bottom-up (e.g., climate, zooplankton availability) and top-down (i.e., fishing and predation) factors on the population dynamics of Bothnian Sea herring (Clupea harengus) throughout its life cycle. Our results indicate significant bottom-up effects of zooplankton and interspecific competition from sprat (Sprattus sprattus), particularly on younger age classes of herring. Although top-down forcing through fishing and predation by grey seals (Halichoerus grypus) and Atlantic cod (Gadus morhua) also was evident, these factors were less important than resource availability and interspecific competition. Understanding key ecological processes and interactions is fundamental to ecosystem-based management practices necessary to promote sustainable exploitation of small pelagic fish.     

Biodiversity mediates productivity through different mechanisms at adjacent trophic levels

Biodiversity may enhance productivity either because diverse communities more often contain productive species (selection effects) or because they show greater complementarity in resource use. Our understanding of how these effects influence community production comes almost entirely from studies of plants. To test whether previous results apply to higher trophic levels, we first used simulations to derive expected contributions of selection and complementarity to production in competitive assemblages defined by either neutral interactions, dominance, or a trade-off between growth and competitive ability. The three types of simulated assemblages exhibited distinct interaction signatures when diversity effects were partitioned into selection and complementarity components. We then compared these signatures to those of experimental marine communities. Diversity influenced production in fundamentally different ways in assemblages of macroalgae, characterized by growth-competition trade-offs, vs. in herbivores, characterized by dominance. Forecasting the effects of changing biodiversity in multitrophic ecosystems will require recognizing that the mechanism by which diversity influences functioning can vary among trophic levels in the same food web.     

A universal approach to estimate biomass and carbon stock in tropical forests using generic allometric models

Allometric equations allow aboveground tree biomass and carbon stock to be estimated from tree size. The allometric scaling theory suggests the existence of a universal power-law relationship between tree biomass and tree diameter with a fixed scaling exponent close to 8/3. In addition, generic empirical models, like Chave's or Brown's models, have been proposed for tropical forests in America and Asia. These generic models have been used to estimate forest biomass and carbon worldwide. However, tree allometry depends on environmental and genetic factors that vary from region to region. Consequently, theoretical models that include too few ecological explicative variables or empirical generic models that have been calibrated at particular sites are unlikely to yield accurate tree biomass estimates at other sites. In this study, we based our analysis on a destructive sample of 481 trees in Madagascar spiny dry and moist forests characterized by a high rate of endemism (> 95%). We show that, among the available generic allometric models, Chave's model including diameter, height, and wood specific gravity as explicative variables for a particular forest type (dry, moist, or wet tropical forest) was the only one that gave accurate tree biomass estimates for Madagascar (R2 > 83%, bias < 6%), with estimates comparable to those obtained with regional allometric models. When biomass allometric models are not available for a given forest site, this result shows that a simple height-diameter allometry is needed to accurately estimate biomass and carbon stock from plot inventories.     

Asymmetry in community regulation: effects of predators and productivity

Eutrophication and predator additions and extinctions are occurring in ecosystems worldwide. Although theory predicts that both will strongly alter the distribution of biomass in whole communities, empirical evidence has not been consolidated to quantitatively determine whether these theoretical predictions are generally borne out in real ecosystems. Here we analyze data from two types of trophic cascade studies, predator removals in factorial combination with fertilization and observed productivity gradients, to assess the role of top-down and bottom-up forces in structuring multi-trophic communities and compare results from these analyses to those from an extensive database of trophic cascade studies. We find that herbivore biomass declines and plant biomass increases in the presence of predators, regardless of system productivity. In contrast, while plants are increased by fertilization, this effect does not significantly increase herbivores in either the presence or absence of predators. These patterns are consistent among marine, freshwater, and terrestrial ecosystems and are largely independent of study size and duration. Thus, top-down effects of predation are transferred through more trophic levels than are bottom-up effects of eutrophication, showing strong asymmetry in the direction of control of biomass distribution in communities.