Biodiversity in model ecosystems, II: species assembly and food web structure

This is the second of two papers dedicated to the relationship between population models of competition and biodiversity. Here, we consider species assembly models where the population dynamics is kept far from fixed points through the continuous introduction of new species, and generalize to such models the coexistence condition derived for systems at the fixed point. The ecological overlap between species and shared preys, that we define here, provides a quantitative measure of the effective interspecies competition and of the trophic network topology. We obtain distributions of the overlap from simulations of a new model based both on immigration and speciation, and show that they are in good agreement with those measured for three large natural food webs. As discussed in the first paper, rapid environmental fluctuations, interacting with the condition for coexistence of competing species, limit the maximal biodiversity that a trophic level can host. This horizontal limitation to biodiversity is here combined with either dissipation of energy or growth of fluctuations, which in our model limit the length of food webs in the vertical direction. These ingredients yield an effective model of food webs that produce a biodiversity profile with a maximum at an intermediate trophic level, in agreement with field studies.     

Benthos as the basis for arctic lake food webs

Plankton have traditionally been viewed as the basis for limnetic food webs, with zooplankton acting as a gateway for energy passing between phytoplanktonic primary producers and fish. Often, benthic production has been considered to be important primarily in shallow systems or as a subsidy to planktonic food web pathways. Stable isotope food web analyses of two arctic lakes (NE14 and I minus) in the Toolik Lake region of Alaska indicate that benthos are the primary source of carbon for adults of all species of benthic and pelagic fish present. We found no effect of turbidity, which may suppress benthic algae by shading, on food web structure. Even though Secchi transparency varied from 10.2 m in NE14 to 0.55–2.6 m in I minus, food webs in both lakes were based upon benthos, had four trophic levels, and culminated with omnivorous lake trout. We suggest that the importance of benthos in the food webs of these lakes is due to their extreme oligotrophy, resulting in planktonic resources that are insufficient for the support of planktivorous consumers.     

Biodiversity maintenance in food webs with regulatory environmental feedbacks

Although the food web is one of the most fundamental and oldest concepts in ecology, elucidating the strategies and structures by which natural communities of species persist remains a challenge to empirical and theoretical ecologists. We show that simple regulatory feedbacks between autotrophs and their environment when embedded within complex and realistic food-web models enhance biodiversity. The food webs are generated through the niche-model algorithm and coupled with predator-prey dynamics, with and without environmental feedbacks at the autotroph level. With high probability and especially at lower, more realistic connectance levels, regulatory environmental feedbacks result in fewer species extinctions, that is, in increased species persistence. These same feedback couplings, however, also sensitize food webs to environmental stresses leading to abrupt collapses in biodiversity with increased forcing. Feedback interactions between species and their material environments anchor food-web persistence, adding another dimension to biodiversity conservation. We suggest that the regulatory features of two natural systems, deep-sea tubeworms with their microbial consortia and a soil ecosystem manifesting adaptive homeostatic changes, can be embedded within niche-model food-web dynamics.     

Emergence of non-random structure in local food webs generated from randomly structured regional webs

Previous studies have shown that high-resolution, empirical food webs possess a non-random network structure, typically characterized by uniform or exponential degree distributions. However, the empirical food webs that have been investigated for their structural properties represent local communities that are only a subset of a larger pool of regionally coexisting species. Here, we use a simple model to investigate the effects of regional food web structure on local food webs that are assembled by two simple processes: random immigration of species from a source web (regional food web), and random extinction of species within the local web. The model shows that local webs with non-random degree distributions can arise from randomly structured source webs. A comparison of local webs assembled from randomly structured source webs with local webs assembled from source webs generated by the niche model shows that the former have higher species richness at equilibrium, but have a nonlinear response to changing extinction rates. These results imply that the network structure of regional food webs can play a significant role in the assembly and dynamics of local webs in natural ecosystems. With natural landscapes becoming increasingly fragmented, understanding such structure may be a necessary key to understanding the maintenance and stability of local species diversity.     

Omnivory and the stability of food webs

The ecological concept of omnivory, feeding at more than a single trophic level, is formulated as an intermediate stage between any two of three classical three-dimensional species interaction systems-tritrophic chain, competition, and polyphagy. It is shown that omnivory may be either stabilizing or destabilizing, depending, in part, on the conditions of the parent systems from which it derives. It is further conjectured that the tritrophic to competition gradient cannot be entirely stable, that there must be an instability at some level of intermediate omnivory.     

Food webs: experts consuming families of experts

Food webs of habitats as diverse as lakes or desert valleys are known to exhibit common "food-web patterns", but the detailed mechanisms generating these structures have remained unclear. By employing a stochastic, dynamical model, we show that many aspects of the structure of predatory food webs can be understood as the traces of an evolutionary history where newly evolving species avoid direct competition with their relatives. The tendency to avoid sharing natural enemies (apparent competition) with related species is considerably weaker. Thus, "experts consuming families of experts" can be identified as the main underlying food-web pattern. We report the results of a systematic, quantitative model validation showing that the model is surprisingly accurate.     

Adaptive omnivory and species coexistence in tri-trophic food webs

The commonness of omnivory in natural communities is puzzling, because simple dynamic models of tri-trophic systems with omnivory are prone to species extinction. In particular, the intermediate consumer is frequently excluded by the omnivore at high levels of enrichment. It has been suggested that adaptive foraging by the omnivore may facilitate coexistence, because the intermediate consumer should persist more easily if it is occasionally dropped from the omnivore's diet. We explore theoretically how species permanence in tri-trophic systems is affected if the omnivore forages adaptively according to the "diet rule", i.e., feeds on the less profitable of its two prey species only if the more profitable one is sufficiently rare. We show that, compared to systems where omnivory is fixed, adaptive omnivory may indeed facilitate 3-species persistence. Counter to intuition, however, facilitation of 3-species coexistence requires that the intermediate consumer is a more profitable prey than the basal resource. Consequently, adaptive omnivory does not facilitate persistence of the intermediate consumer but enlarges the persistence region of the omnivore towards parameter space where a fixed omnivore would be excluded by the intermediate consumer. Overall, the positive effect of adaptive omnivory on 3-species persistence is, however, small. Generally, whether omnivory is fixed or adaptive, 3-species permanence is most likely when profitability (=conversion efficiency into omnivores) is low for basal resources and high for intermediate consumers.     

Effects of network and dynamical model structure on species persistence in large model food webs

Four models of network structure are combined with models of bioenergetic dynamics to study the role of food web topology and nonlinear dynamics on species coexistence in complex ecological networks. Network models range from the highly structured niche model to loosely constrained energetically feasible random networks. Bioenergetic models differ in how they represent primary production, functional responses, and consumption by generalists. Network structure weakly influenced the ability of species to coexist. Species persistence is strongly affected by functional responses and generalists’ consumption rates but weakly affected by models and amounts of primary production. Despite these generalities, specific mechanisms that determine persistence under one dynamical regime, such as top-down control by consumers, may play an insignificant role under different dynamical conditions. Future research is needed to strengthen the weak empirical basis for various functional forms and parameter values that strongly influence whether species can coexist in complex food webs. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Highly resolved early Eocene food webs show development of modern trophic structure after the end-Cretaceous extinction

Generalities of food web structure have been identified for extant ecosystems. However, the trophic organization of ancient ecosystems is unresolved, as prior studies of fossil webs have been limited by low-resolution, high-uncertainty data. We compiled highly resolved, well-documented feeding interaction data for 700 taxa from the 48 million-year-old latest early Eocene Messel Shale, which contains a species assemblage that developed after an interval of protracted environmental and biotal change during and following the end-Cretaceous extinction. We compared the network structure of Messel lake and forest food webs to extant webs using analyses that account for scale dependence of structure with diversity and complexity. The Messel lake web, with 94 taxa, displays unambiguous similarities in structure to extant webs. While the Messel forest web, with 630 taxa, displays differences compared to extant webs, they appear to result from high diversity and resolution of insect–plant interactions, rather than substantive differences in structure. The evidence presented here suggests that modern trophic organization developed along with the modern Messel biota during an 18 Myr interval of dramatic post-extinction change. Our study also has methodological implications, as the Messel forest web analysis highlights limitations of current food web data and models.     

The effects of mixotrophy on the stability and dynamics of a simple planktonic food web model

Recognition of the microbial loop as an important part of aquatic ecosystems disrupted the notion of simple linear food chains. However, current research suggests that even the microbial loop paradigm is a gross simplification of microbial interactions due to the presence of mixotrophs-organisms that both photosynthesize and graze. We present a simple food web model with four trophic species, three of them arranged in a food chain (nutrients-autotrophs-herbivores) and the fourth as a mixotroph with links to both the nutrients and the autotrophs. This model is used to study the general implications of inclusion of the mixotrophic link in microbial food webs and the specific predictions for a parameterization that describes open ocean mixed layer plankton dynamics. The analysis indicates that the system parameters reside in a region of the parameter space where the dynamics converge to a stable equilibrium rather than displaying periodic or chaotic solutions. However, convergence requires weeks to months, suggesting that the system would never reach equilibrium in the ocean due to alteration of the physical forcing regime. Most importantly, the mixotrophic grazing link seems to stabilize the system in this region of the parameter space, particularly when nutrient recycling feedback loops are included.     

The impact of climate change on the structure of Pleistocene food webs across the mammoth steppe

Species interactions form food webs, impacting community structure and, potentially, ecological dynamics. It is likely that global climatic perturbations that occur over long periods of time have a significant influence on species interaction patterns. Here, we integrate stable isotope analysis and network theory to reconstruct patterns of trophic interactions for six independent mammalian communities that inhabited mammoth steppe environments spanning western Europe to eastern Alaska (Beringia) during the Late Pleistocene. We use a Bayesian mixing model to quantify the contribution of prey to the diets of local predators, and assess how the structure of trophic interactions changed across space and the Last Glacial Maximum (LGM), a global climatic event that severely impacted mammoth steppe communities. We find that large felids had diets that were more constrained than those of co-occurring predators, and largely influenced by an increase in Rangifer abundance after the LGM. Moreover, the structural organization of Beringian and European communities strongly differed: compared with Europe, species interactions in Beringian communities before—and possibly after—the LGM were highly modular. We suggest that this difference in modularity may have been driven by the geographical insularity of Beringian communities.     

The impact of nonlinear functional responses on the long-term evolution of food web structure

We investigate the long-term web structure emerging in evolutionary food web models when different types of functional responses are used. We find that large and complex webs with several trophic layers arise only if the population dynamics is such that it allows predators to focus on their best prey species. This can be achieved using modified Lotka-Volterra or Holling/Beddington functional responses with effective couplings that depend on the predator's efficiency at exploiting the prey, or a ratio-dependent functional response with adaptive foraging. In contrast, if standard Lotka-Volterra or Holling/Beddington functional responses are used, long-term evolution generates webs with almost all species being basal, and with additionally many links between these species. Interestingly, in all cases studied, a large proportion of weak links result naturally from the evolution of the food webs.     

Food webs robustness to biodiversity loss: the roles of connectance, expansibility and degree distribution

We analyse the robustness of food webs against species loss by considering the influence of several structural factors of the networks, such as connectance, degree distribution and expansibility. The last concept refers to the absence of structural bottlenecks in the food web, whose removal separate the network into large isolate clusters. In theory networks with identical connectance can display different expansibility characteristics. Using the spectral scaling method we studied 17 food networks and classified them as good expansion (GE) and not-GE networks. The combination of GE properties and degree distribution of species permitted the classification of food webs into six different classes. These classes characterize the differences in robustness of food webs to species loss. While the webs having uniform degree distributions and displaying GE properties are the most robust to species loss, the presence of bottlenecks and skewed distribution of the number of links per species make food webs very vulnerable to primary removal of species.     

Evidence for the existence of a robust pattern of prey selection in food webs

Food webs aim to provide a thorough representation of the trophic interactions found in an ecosystem. The complexity of empirical food webs, however, is leading many ecologists to focus dynamic ecosystem studies on smaller microcosm or mesocosm studies based upon community modules, which comprise three to five species and the interactions likely to have ecological relevance. We provide here a structural counterpart to community modules. We investigate food-web 'motifs' which are n-species connected subgraphs found within the food web. Remarkably, we find that the over- and under-representation of three-species motifs in empirical food webs can be understood through comparison to a static food-web model, the niche model. Our result conclusively demonstrates that predation upon species with some 'characteristic' niche value is the prey selection mechanism consistent with the structural properties of empirical food webs.     

Quantifying the interaction structure and the topological importance of species in food webs: A signed digraph approach

Due to the structural complexity of nature, it is not always easy to identify topologically importance species in an ecosystem. In the past decade, several studies in ecology have developed methods for measuring species importance basing on direct and indirect inter-specific interactions. Here, by extending a previously developed methodology, we present an approach that can quantify the interaction structure of a food web and consequently the topological importance of species when the food web is viewed as a signed digraph. The basic principle behind our approach is to determine the sign and strength of direct and indirect interactions for all pathways up to a predefined number of steps. Our approach mainly differs from the previous methodology in that we are able to quantify the strength of inter-specific interaction as well as in what way species interact with each other, as it can explicitly quantify a wide range of ecological interactions such as cascading effect, indirect food supply effect, apparent and exploitive competitions in the same framework. This then allows us to quantify the topological importance of a species and examine whether it is a predominately positive or negative interactor in a food web. Furthermore, our analysis reveals that positive and negative effects from one species on others eventually cancel each other out for longer pathways resulting in stable interaction structure. Applications of our methodology include providing a more informative index for conservation biologists, and the potential use of interaction structure derived from our approach in food web robustness studies is also discussed.     

Emergence of complexity in evolving niche-model food webs

We have analysed mechanisms that promote the emergence of complex structures in evolving model food webs. The niche model is used to determine predator-prey relationships. Complexity is measured by species richness as well as trophic level structure and link density. Adaptive dynamics that allow predators to concentrate on the prey species they are best adapted to lead to a strong increase in species number but have only a small effect on the number and relative occupancy of trophic levels. The density of active links also remains small but a high number of potential links allows the network to adjust to changes in the species composition (emergence and extinction of species). Incorporating effects of body size on individual metabolism leads to a more complex trophic level structure: both the maximum and the average trophic level increase. So does the density of active links. Taking body size effects into consideration does not have a measurable influence on species richness. If species are allowed to adjust their foraging behaviour, the complexity of the evolving networks can also be influenced by the size of the external resources. The larger the resources, the larger and more complex is the food web it can sustain. Body size effects and increasing resources do not change size and the simple structure of the evolving networks if adaptive foraging is prohibited. This leads to the conclusion that in the framework of the niche model adaptive foraging is a necessary but not sufficient condition for the emergence of complex networks. It is found that despite the stabilising effect of foraging adaptation the system displays elements of self-organised critical behaviour.     

Bioenergetic food webs as a means of linking toxicological effects across scales of ecological organization

Although significant progress has been made in ourability to predict population-level consequences oftoxic effects on individuals, extending thispredictive ability to communities, functional guilds,and ecosystems will require more integration ofecological theory into environmental science. Bioenergetics and food webs have long been centralthemes in ecology and greatly expanded ourunderstanding of nature. Although numerousenergetic-based toxicological endpoints have beendeveloped, few have extended this framework beyond theindividual level. Most energetic endpoints includeindividual growth, and only occasionally is thisintegrated with population dynamics. However,population-level energetic analyses (e.g., secondaryproduction) integrate individual and populationprocesses, and provide two key parameters: consumptionand energy flow. Within a food web framework,estimates of consumption and energy flow throughpopulations facilitate linking population-levelcontaminant effects to ecosystem-level effects. Several examples are given to illustrate the utilityof this approach.     

Bottom-up effects of species diversity on the functioning and stability of food webs

1. The importance of species diversity for the stability of populations, communities and ecosystem functions is a central question in ecology. 2. Biodiversity experiments have shown that diversity can impact both the average and variability of stocks and rates at these levels of ecological organization in single trophic-level ecosystems. Whether these impacts hold in food webs and across trophic levels is still unclear. 3. We asked whether resource species diversity, community composition and consumer feeding selectivity in planktonic food webs impact the stability of resource or consumer populations, community biomass and ecosystem functions. We also tested the relative importance of resource diversity and community composition. 4. We found that resource diversity negatively affected resource population stability, but had no effect on consumer population stability, regardless of the consumer's feeding selectivity. Resource diversity had positive effects on most ecosystem functions and their stability, including primary production, resource biomass and particulate carbon, nitrogen and phosphorus concentrations. 5. Community composition, however, generally explained more variance in population, community and ecosystem properties than species diversity per se. This result points to the importance of the outcomes of particular species interactions and individual species' effect traits in determining food web properties and stability. 6. Among the stabilizing mechanisms tested, an increase in the average resource community biomass with increasing resource diversity had the greatest positive impact on stability. 7. Our results indicate that resource diversity and composition are generally important for the functioning and stability of whole food webs, but do not have straightforward impacts on consumer populations.     

Global change alters the stability of food webs

Recent research has generally shown that a small change in the number of species in a food web can have consequences both for community structure and ecosystem processes. However ‘change’ is not limited to just the number of species in a community, but might include an alteration to such properties as precipitation, nutrient cycling and temperature. How such changes might affect species interactions is important, not just through the presence or absence of interactions, but also because the patterning of interaction strengths among species is intimately associated with community stability. Interaction strengths encompass such properties as feeding rates and assimilation efficiencies, and encapsulate functionally important information with regard to ecosystem processes. Interaction strengths represent the pathways and transfer of energy through an ecosystem. We review the best empirical data available detailing the frequency distribution of interaction strengths in communities. We present the underlying (but consistent) pattern of species interactions and discuss the implications of this patterning. We then examine how such a basic pattern might be affected given various scenarios of ‘change’ and discuss the consequences for community stability and ecosystem functioning.