A Consumer-Resource Approach to Community Structure

Because all species are consumers and all, eventually, are consumedby other species, consumer-resource interaction is one of themost fundamental processes of ecology. Simple models that includethe direct mechanisms of consumer-resource interactions maythus be the fundamental building-block for models of communitystructure. These models are easily extended to include suchcomplexity as the effects of physical limiting factors, spatialheterogeneity in resource supply, fluctuating resource supply,and multiple trophic levels. Each such modification places constraintson the traits of species that can persist. Consumer-resourcemodels make predictions about many aspects of community structure,including species richness, species composition, species dominance,population dynamics, morphological or physiological traits ofspecies, and patterns of phenotypic variation within species.Thus, each model affords numerous opportunities to test andmodify or reject it. A review of a variety of communities suggeststhat much of the structure of each community can be explainedby a relatively simple consumer-resource model, but that differentelements of complexity may be important in different communities.     

Resource-dependent dispersal and the speed of biological invasions

Many mobile organisms exhibit resource-dependent movement in which movement rates adjust to changes in local resource densities through changes in either the probability of moving or the distance moved. Such changes may have important consequences for invasions because reductions in resources behind an invasion front may cause higher dispersal while simultaneously reducing population growth behind the front and thus lowering the number of dispersers. Intuiting how the interplay between population growth and dispersal affects invasions is difficult without mathematical models, yet most models assume dispersal rates are constant. Here we present spatial-spread models that allow for consumer-resource interactions and resource-dependent dispersal. Our results show that when resources affect the probability of dispersal, then the invasion dynamics are no different than if resources did not affect dispersal. When resources instead affect the distance dispersed, however, the invasion dynamics are strongly affected by the strength of the consumer-resource interaction, and population cycles behind the wave front lead to fluctuating rates of spread. Our results suggest that for actively dispersing invaders, invasion dynamics can be determined by species interactions. More practically, our work suggests that reducing invader densities behind the front may be a useful method of slowing an invader's rate of spread.     

Spatial scaling of consumer-resource interactions in advection-dominated systems

Ecologists studying consumer-resource interactions in advection-dominated systems such as streams and rivers frequently seek to link the results of small-scale experiments with larger-scale patterns of distribution and abundance. Accomplishing this goal requires determining the characteristic scale, termed the response length, at which there is a shift from local dynamics dominated by advective dispersal to larger-scale dynamics dominated by births and deaths. Here, we model the dynamics of consumer-resource systems in a spatially variable, advective environment and show how consumer-resource interactions alter the response length relative to its single-species value. For one case involving a grazer that emigrates in response to high predator density, we quantify the changes using published data from small-scale experiments on aquatic invertebrates. Using Fourier analysis, we describe the responses of advection-dominated consumer-resource systems to spatially extended environmental variability in a way that involves explicit consideration of the response length. The patterns we derive for different consumer-resource systems exhibit important similarities in how component populations respond to spatial environmental variability affecting dispersal as opposed to demographic parameters.     

Adaptive plasticity in ontogenetic niche shifts stabilizes consumer-resource dynamics

Ontogenetic niche shifts, changes in the diet or habitats of organisms during their ontogeny, are widespread among various animal taxa. Ontogenetic niche shifts introduce stage structure in a population with different stages interacting with different communities and can substantially affect their dynamics. In this article, I use mathematical models to test the hypothesis that adaptive plasticity in the timing of ontogenetic niche shifts has a stabilizing effect on consumer-resource dynamics. Adaptive plasticity allows consumers in one ontogenetic niche to perform an early shift to the next ontogenetic niche if the resource density of the first niche is low. The early shift will reduce predation by the consumer on the scarce resource. On the other hand, adaptive plasticity allows consumers to delay their shift to the next niche if the resource density of the first niche is high. The delayed shift will increase the predation on the abundant resource. As a result, the scarce resource will tend to increase, and the abundant resource will tend to decrease. This causes density-dependent negative feedback in the resource dynamics, which stabilizes the consumer-resource dynamics. To test this hypothesis, I compare three consumer-resource models differing in terms of mechanisms controlling the timing of the ontogenetic niche shift: the fixed-age model assumes that the age at which the ontogenetic niche shift occurs is fixed; the fixed-size model assumes that the size at the shift is fixed; and the adaptive plasticity model assumes that the timing of the shift is such that the individual fitness of the consumer is maximized. I show that only the adaptive plasticity model has a locally stable equilibrium and that the stabilizing effect is due to the density-dependent negative feedback in the resource dynamics. I discuss the ontogenetic niche shifts of lake fish in light of the obtained result.     

Behavioral interference and facilitation in the foraging cycle shape the functional response

Individual forager behaviors should affect per capita intakerates and thereby population and consumer-resource properties.We consider and incorporate conspecific facilitation and interferenceduring the separate foraging-cycle stages in a functional responsemodel that links individual behavioral interactions with consumer-resourceprocesses. Our analyses suggest that failing to properly considerand include all effects of behavioral interactions on foraging-cyclestage performances may either over- or underestimate effectsof interactions on the shape of both functional responses andpredator zero-growth isoclines. Incorporation of prey- and predator-dependentinteractions among foragers in the model produces predator isoclineswith potentials for highly complex consumer-resource dynamics.Facilitation and interference during the foraging cycle aretherefore suggested as potent behavioral mechanisms to causepatterns of community dynamics. We emphasize that correct estimationsof interaction-mediated foraging-cycle efficiencies should beconsidered in empirical and theoretical attempts to furtherour understanding of the mechanistic link between social behaviorsand higher order processes.     

Resource competition in stage-structured populations

Two models are made to account for the dynamics of a consumer-resource system in which the consumers are divided into juveniles and adults. The resource grows logistically and a type II functional response is assumed for consumers. Resource levels determine fecundity and maturation rates in one model, and mortality rates in the other. The analysis of the models shows that the condition for establishment of consumers is that the product of per capita fecundity rate and maturation rates is higher than the product of juvenile and adult per capita decay rates at a resource level equal to its carrying capacity. This result imposes a minimal abundance of resource able to maintain the consumers. A second result shows an equilibrium stage structure, with a small instability when juveniles and adults mean saturation constants are different. The implications of these results for community dynamics are discussed.     

Consumer-resource dynamics: quantity, quality, and allocation

Background

The dominant paradigm for modeling the complexities of interacting populations and food webs is a system of coupled ordinary differential equations in which the state of each species, population, or functional trophic group is represented by an aggregated numbers-density or biomass-density variable. Here, using the metaphysiological approach to model consumer-resource interactions, we formulate a two-state paradigm that represents each population or group in a food web in terms of both its quantity and quality.

Methodology and Principal Findings

The formulation includes an allocation function controlling the relative proportion of extracted resources to increasing quantity versus elevating quality. Since lower quality individuals senesce more rapidly than higher quality individuals, an optimal allocation proportion exists and we derive an expression for how this proportion depends on population parameters that determine the senescence rate, the per-capita mortality rate, and the effects of these rates on the dynamics of the quality variable. We demonstrate that oscillations do not arise in our model from quantity-quality interactions alone, but require consumer-resource interactions across trophic levels that can be stabilized through judicious resource allocation strategies. Analysis and simulations provide compelling arguments for the necessity of populations to evolve quality-related dynamics in the form of maternal effects, storage or other appropriate structures. They also indicate that resource allocation switching between investments in abundance versus quality provide a powerful mechanism for promoting the stability of consumer-resource interactions in seasonally forcing environments.

Conclusions/Significance

Our simulations show that physiological inefficiencies associated with this switching can be favored by selection due to the diminished exposure of inefficient consumers to strong oscillations associated with the well-known paradox of enrichment. Also our results demonstrate how allocation switching can explain observed growth patterns in experimental microbial cultures and discuss how our formulation can address questions that cannot be answered using the quantity-only paradigms that currently predominate.     

Synapse adhesion: a dynamic equilibrium conferring stability and flexibility

Cell adhesion molecules (CAMs) linked to cytoskeleton generate stable cell-cell junctions. Cadherins provide a canonical example, but paradoxically, they participate in a multitude of transient and regulatable interactions. Their extracellular binding generates weak adhesion that is modified by clustering; interactions with F-actin are regulated, can be transient, and can alter F-actin dynamics. Additionally, cadherin recycling from the cell surface can modify the size and location of junctions and strength of adhesion. In epithelial cells, this ongoing dynamic behavior is important for maintaining stable junctions. Recent work supports that cadherins act similarly at synapses where their actions are likely to be shared by integrins and other actin-linked CAMs. Together the collaborative activities of such CAMs provide a stable, but flexible structure that can promote and support changes in synapse shape and size while maintaining stable junctions to permit information flow.     

When individual life history matters: conditions for juvenile-adult stage structure effects on population dynamics

Ecological theory about the dynamics of interacting populations is mainly based on unstructured models that account for species abundances only. In turn, these models constitute the basis for our understanding of the functioning of ecological communities and ecosystems and their responses to environmental change, natural disturbances and human impacts. Structured models that take into account differences between individuals in age, stage or size have been shown to sometimes make predictions that run counter to the predictions of unstructured analogues. It is however unclear which biological mechanisms that are accounted for in the structured models give rise to these contrasting predictions. Focusing on two particular rules-of-thumb that generally hold in unstructured consumer-resource models, one relating to the relationship between mortality and equilibrium density of the consumer and the other relating to the stability of the equilibrium, I investigate the necessary conditions under which accounting for juvenile-adult stage structure can lead to qualitatively different model predictions. In particular, juvenile-adult stage structure is shown to overturn the two rules-of-thumb in case the model also accounts for the energetic requirements for basic metabolic maintenance. Given the fundamental nature of both juvenile-adult stage structure as well as metabolic maintenance requirements, these results call into question the generality of the predictions derived from unstructured models.     

Phenologically-Structured Predator-Prey Dynamics with Temperature Dependence

Studies document the fact that temperature changes strongly affect interactions in many consumer-resource systems through altered, or shifted, phenologies. The mistiming of events, such as migration or emergence times, or the contraction or expansion of development times can upset the normal synchronization and lead to increased or decreased predation events. In this paper, we formulate a continuous time, phenologically-structured model of predator-prey interactions that is driven by temperature variations. It is particularly applicable to arthropod interactions because their development rates are so strongly temperature related. The model takes the form of a system of partial differential-integral equations for the species’ population densities in development-time variables. In special cases, the model is analytically tractable and we find a closed-form solution. By calculating density variations under different temperature regimes, the model gives a quantitative method for assessing the effects of global temperature change on consumer-resource interactions.     

Mechanistic theory and modelling of complex food-web dynamics in Lake Constance

Mechanistic understanding of consumer-resource dynamics is critical to predicting the effects of global change on ecosystem structure, function and services. Such understanding is severely limited by mechanistic models' inability to reproduce the dynamics of multiple populations interacting in the field. We surpass this limitation here by extending general consumer-resource network theory to the complex dynamics of a specific ecosystem comprised by the seasonal biomass and production patterns in a pelagic food web of a large, well-studied lake. We parameterised our allometric trophic network model of 24 guilds and 107 feeding relationships using the lake's food web structure, initial spring biomasses and body-masses. Adding activity respiration, the detrital loop, minimal abiotic forcing, prey resistance and several empirically observed rates substantially increased the model's fit to the observed seasonal dynamics and the size-abundance distribution. This process illuminates a promising approach towards improving food-web theory and dynamic models of specific habitats.     

Dynamical Transitions in a Pollination–Herbivory Interaction: A Conflict between Mutualism and Antagonism

Plant-pollinator associations are often seen as purely mutualistic, while in reality they can be more complex. Indeed they may also display a diverse array of antagonistic interactions, such as competition and victim–exploiter interactions. In some cases mutualistic and antagonistic interactions are carried-out by the same species but at different life-stages. As a consequence, population structure affects the balance of inter-specific associations, a topic that is receiving increased attention. In this paper, we developed a model that captures the basic features of the interaction between a flowering plant and an insect with a larval stage that feeds on the plant’s vegetative tissues (e.g. leaves) and an adult pollinator stage. Our model is able to display a rich set of dynamics, the most remarkable of which involves victim–exploiter oscillations that allow plants to attain abundances above their carrying capacities and the periodic alternation between states dominated by mutualism or antagonism. Our study indicates that changes in the insect’s life cycle can modify the balance between mutualism and antagonism, causing important qualitative changes in the interaction dynamics. These changes in the life cycle could be caused by a variety of external drivers, such as temperature, plant nutrients, pesticides and changes in the diet of adult pollinators.     

Interaction strength and stability in stage‐structured food web modules

There has been a long‐standing debate on what creates stability in food webs. One major finding is that weak interactions can mute the destabilizing potential of strong interactions. Considering that stage structure is common in nature, that existing studies on stability that include population stage structure point in different directions, and the recent theoretical developments in the area of stage structure, there is a need to address the effects of population stage structure in this context. Using simple food web modules, with stage structure in an intermediate consumer, we here begin to theoretically investigate the effects of stage structure on food web stability. We found a general correspondence to previous results such that strong interactions had destabilizing effects and weak interactions that result in decreased energy flux had stabilizing effects. However, we also found a number of novel results connected to stage structure. Interestingly, weak interactions can be destabilizing when they excite other interactions. We also found that cohort cycles and predator–prey cycles did not respond in the same way to increasing interactions strength. We found that the combined effects of two predators feeding on the same prey can strongly destabilize a system. Consistent with previous studies, we also found that stage‐specific feeding can create a refuge effect that leads to a lack of strong destabilization at high interaction strength. Overall, stage structure had both stabilizing and destabilizing aspects. Some effects could be explained by our current understanding of energetic processes; others need additional consideration. Additional aspects such as shunting of energy between stages, control of biomass fluxes, and interactions between lags and energy flux, should be considered.     

Measles metapopulation dynamics: a gravity model for epidemiological coupling and dynamics

Infectious diseases provide a particularly clear illustration of the spatiotemporal underpinnings of consumer-resource dynamics. The paradigm is provided by extremely contagious, acute, immunizing childhood infections. Partially synchronized, unstable oscillations are punctuated by local extinctions. This, in turn, can result in spatial differentiation in the timing of epidemics and, depending on the nature of spatial contagion, may result in traveling waves. Measles epidemics are one of a few systems documented well enough to reveal all of these properties and how they are affected by spatiotemporal variations in population structure and demography. On the basis of a gravity coupling model and a time series susceptible-infected-recovered (TSIR) model for local dynamics, we propose a metapopulation model for regional measles dynamics. The model can capture all the major spatiotemporal properties in prevaccination epidemics of measles in England and Wales.     

Do Food Web Models Reproduce the Structure of Mutualistic Networks?

Background

Simple models inspired by processes shaping consumer-resource interactions have helped to establish the primary processes underlying the organization of food webs, networks of trophic interactions among species. Because other ecological interactions such as mutualisms between plants and their pollinators and seed dispersers are inherently based in consumer-resource relationships we hypothesize that processes shaping food webs should organize mutualistic relationships as well.

Methodology/Principal Findings

We used a likelihood-based model selection approach to compare the performance of food web models and that of a model designed for mutualisms, in reproducing the structure of networks depicting mutualistic relationships. Our results show that these food web models are able to reproduce the structure of most of the mutualistic networks and even the simplest among the food web models, the cascade model, often reproduce overall structural properties of real mutualistic networks.

Conclusions/Significance

Based on our results we hypothesize that processes leading to feeding hierarchy, which is a characteristic shared by all food web models, might be a fundamental aspect in the assembly of mutualisms. These findings suggest that similar underlying ecological processes might be important in organizing different types of interactions.     

McComedy: A user-friendly tool for next-generation individual-based modeling of microbial consumer-resource systems

Individual-based modeling is widely applied to investigate the ecological mechanisms driving microbial community dynamics. In such models, the population or community dynamics emerge from the behavior and interplay of individual entities, which are simulated according to a predefined set of rules. If the rules that govern the behavior of individuals are based on generic and mechanistically sound principles, the models are referred to as next-generation individual-based models. These models perform particularly well in recapitulating actual ecological dynamics. However, implementation of such models is time-consuming and requires proficiency in programming or in using specific software, which likely hinders a broader application of this powerful method. Here we present McComedy, a modeling tool designed to facilitate the development of next-generation individual-based models of microbial consumer-resource systems. This tool allows flexibly combining pre-implemented building blocks that represent physical and biological processes. The ability of McComedy to capture the essential dynamics of microbial consumer-resource systems is demonstrated by reproducing and furthermore adding to the results of two distinct studies from the literature. With this article, we provide a versatile tool for developing next-generation individual-based models that can foster understanding of microbial ecology in both research and education.     

Integrated population model reveals that kestrels breeding in nest boxes operate as a source population

The identification of the source–sink status of a population is critical for the establishment of conservation plans and enacting smart management decisions. We developed an integrated population model to formally assess the source status of a kestrel Falco tinnunculus population breeding in nest boxes in Switzerland. We estimated juvenile and adult survival, reproduction and net dispersal (emigration/immigration) by jointly analyzing capture–recapture, dead recovery, breeding monitoring and population survey data. We also investigated the role of nest boxes on kestrel demography and assessed the contributions of vital rates to realized population growth rates. The results indicate that the kestrel population breeding in nest boxes has acted as a source over the 15 years of the study duration. A quantitative approach suggests that a substantial number of individuals have emigrated annually from this population likely affecting the population dynamics outside the management area. Variation in fecundity explained 34% of the temporal variability of the population growth rate. Moreover, a literature review suggests that kestrel pairs produce on average 1.4 chicks more per breeding attempt in nest boxes compared to natural open nests. Together, these findings suggest that fecundity was an important driver for the dynamics of this population and that nest boxes have contributed to its raise. Nest boxes are regularly used as an efficient tool for conservation management. We suggest that such a conservation action can result in the establishment of a source population being beneficial for populations both inside and outside the managed area.     

Constrained proteome allocation affects coexistence in models of competitive microbial communities

Microbial communities are ubiquitous and play crucial roles in many natural processes. Despite their importance for the environment, industry and human health, there are still many aspects of microbial community dynamics that we do not understand quantitatively. Recent experiments have shown that the structure and composition of microbial communities are intertwined with the metabolism of the species that inhabit them, suggesting that properties at the intracellular level such as the allocation of cellular proteomic resources must be taken into account when describing microbial communities with a population dynamics approach. In this work, we reconsider one of the theoretical frameworks most commonly used to model population dynamics in competitive ecosystems, MacArthur’s consumer-resource model, in light of experimental evidence showing how proteome allocation affects microbial growth. This new framework allows us to describe community dynamics at an intermediate level of complexity between classical consumer-resource models and biochemical models of microbial metabolism, accounting for temporally-varying proteome allocation subject to constraints on growth and protein synthesis in the presence of multiple resources, while preserving analytical insight into the dynamics of the system. We first show with a simple experiment that proteome allocation needs to be accounted for to properly understand the dynamics of even the simplest microbial community, i.e. two bacterial strains competing for one common resource. Then, we study our consumer-proteome-resource model analytically and numerically to determine the conditions that allow multiple species to coexist in systems with arbitrary numbers of species and resources.Subject terms: Biodiversity, Microbial ecology, Microbial ecology, Bacterial physiology