Does evolution design robust food webs?

Theoretical works that use a dynamical approach to study the ability of ecological communities to resist perturbations are largely based on randomly generated ecosystem structures. By contrast, we ask here whether the evolutionary history of food webs matters for their robustness. Using a community evolution model, we first generate trophic networks by varying the level of energy supply (richness) of the environment in which species adapt and diversify. After placing our simulation outputs in perspective with present-day food webs empirical data, we highlight the complex, structuring role of this environmental condition during the evolutionary setting up of trophic networks. We then assess the robustness of food webs by studying their short-term ecological responses to swift changes in their customary environmental richness. We reveal that the past conditions have a crucial effect on the robustness of current food webs. Moreover, directly focusing on connectance of evolved food webs, it turns out that the most connected ones appear to be the least robust to sharp depletion in the environmental energy supply. Finally, we appraise the 'adaptation' of food webs themselves: generally poor, except in relation to a diversity of flux property.

Modelling, singular perturbation and bifurcation analyses of bitrophic food chains.

Two predator-prey model formulations are studied: the classical Rosenzweig-MacArthur (RM) model and the Mass Balance (MB) chemostat model. When the growth and loss rate of the predator is much smaller than that of the prey these models are slow-fast systems leading mathematically to a singular perturbation problem. In contradiction to the RM-model, the resource for the prey is modelled explicitly in the MB-model but this comes with additional parameters. These parameter values are chosen such that the two models become easy to compare. In both models the transcritical bifurcation, a threshold above which invasion of predator into prey-only system occurs, and the Hopf bifurcation where the interior equilibrium becomes unstable leading to a stable limit cycle occur. The slow-fast limit cycles are called relaxation oscillations which for increasing differences in time scales leads to the well known degenerated trajectories being concatenations of slow parts of the trajectory and fast parts of the trajectory. In the fast-slow version of the RM-model a canard explosion of the stable limit cycles occurs in the oscillatory region of the parameter space. To our knowledge this type of dynamics has not been observed for the RM-model and not even for more complex ecosystem models. When a bifurcation parameter crosses the Hopf bifurcation point the amplitude of the emerging stable limit cycles increases. However, depending of the perturbation parameter the shape of this limit cycle changes abruptly from one consisting of two concatenated slow and fast episodes with small amplitude of the limit cycle, to a shape with large amplitude of which the shape is similar to the relaxation oscillation, the well known degenerated phase trajectories consisting of four episodes (concatenation of two slow and two fast). The canard explosion point is accurately predicted by using an extended asymptotic expansion technique in the perturbation and bifurcation parameter simultaneously where the small amplitude stable limit cycles exist. The predicted dynamics of the MB-model is in a large part of the parameter space similar to that of the RM-model. However, the fast-slow version of MB-model does not predict a canard explosion phenomenon.

Towards a simplification of models using regression trees.

Over-parametrization in modelling is a well-known issue that makes it hard to identify which part of a model is responsible for a given behaviour. In line with that ascertainment, this work presents the outline of an empirical method to simplify models by decreasing the number of parameters. By using regression trees to classify outputs according to related input parameters, the method provides the modeller with an objective tool to reduce the range of the used parameters and, under certain conditions, to establish relations between them. Thereby, the complexity of the model is reduced on the basis of mathematical arguments. As an example, a dynamic energy budget-based model of a mesopelagic bacterial ecosystem is simplified using the presented method. The main benefits of such a method are thus highlighted: (i) more robust parameter estimations; (ii) less complex formulations; and (iii) fewer modelling assumptions. To conclude, the difficulties encountered are discussed, and several solutions are proposed to deal with them.

Dynamic energy budget theory restores coherence in biology.

We present the state of the art of the development of dynamic energy budget theory, and its expected developments in the near future within the molecular, physiological and ecological domains. The degree of formalization in the set-up of the theory, with its roots in chemistry, physics, thermodynamics, evolution and the consistent application of Occam's razor, is discussed. We place the various contributions in the theme issue within this theoretical setting, and sketch the scope of actual and potential applications.

How far details are important in ecosystem modelling: the case of multi-limiting nutrients in phytoplankton-zooplankton interactions.

We try to answer the question of to what extent details in nutrient uptake and phytoplankton physiology matter for population and community dynamics. To this end, we study how two nutrients interact in limiting phytoplankton growth. A popular formulation uses a product-rule for nutrient uptake, which we compare with that on the basis of synthesizing units. We first fit different nutrient uptake models to a dataset and conclude that the quantitative differences between the models are small. Then we study the sensitivity of phytoplankton growth and zooplankton-phytoplankton interactions (ZPi) models to uptake formulations. Two population models are compared; they are based on different assumptions on the relation between nutrient uptake and phytoplankton growth. We find that the population and community models are sensitive to uptake formulations. According to the uptake formulation used in the ZPi models, qualitative differences can be observed. Indeed, although two models based on functions with similar shapes have close equilibria, these can differ in stability properties. Since stability involves the derivatives of formulas, even if two formulas provide close values, large numerical differences in the stability criterion may occur after derivation. We conclude that mechanistic details can be of importance for community modelling.

Study of a virus-bacteria interaction model in a chemostat: application of geometrical singular perturbation theory.

This paper provides a mathematical analysis of a virus-marine bacteria interaction model. The model is a simplified case of the model published and used by Middelboe (Middelboe, M. 2000 Microb. Ecol. 40, 114-124). It takes account of the virus, the susceptible bacteria, the infected bacteria and the substrate in a chemostat. We show that the numerical values of the parameters given by Middelboe allow two different time scales to be considered. We then use the geometrical singular perturbation theory to study the model. We show that there are two invariant submanifolds of dimension two in the four-dimensional phase space and that these manifolds cross themselves on the boundary of the domain of biological relevance. We then perform a rescaling to understand the dynamics in the vicinity of the intersection of the manifolds. Our results are discussed in the marine ecological context.

Imaging oxygen distribution in marine sediments. The importance of bioturbation and sediment heterogeneity.

The influence of sediment oxygen heterogeneity, due to bioturbation, on diffusive oxygen flux was investigated. Laboratory experiments were carried out with 3 macrobenthic species presenting different bioturbation behaviour patterns: the polychaetes Nereis diversicolor and Nereis virens, both constructing ventilated galleries in the sediment column, and the gastropod Cyclope neritea, a burrowing species which does not build any structure. Oxygen two-dimensional distribution in sediments was quantified by means of the optical planar optode technique. Diffusive oxygen fluxes (mean and integrated) and a variability index were calculated on the captured oxygen images. All species increased sediment oxygen heterogeneity compared to the controls without animals. This was particularly noticeable with the polychaetes because of the construction of more or less complex burrows. Integrated diffusive oxygen flux increased with oxygen heterogeneity due to the production of interface available for solute exchanges between overlying water and sediments. This work shows that sediment heterogeneity is an important feature of the control of oxygen exchanges at the sediment-water interface.

Global production increased by spatial heterogeneity in a population dynamics model.

Spatial and temporal heterogeneity are often described as important factors having a strong impact on biodiversity. The effect of heterogeneity is in most cases analyzed by the response of biotic interactions such as competition of predation. It may also modify intrinsic population properties such as growth rate. Most of the studies are theoretic since it is often difficult to manipulate spatial heterogeneity in practice. Despite the large number of studies dealing with this topics, it is still difficult to understand how the heterogeneity affects populations dynamics. On the basis of a very simple model, this paper aims to explicitly provide a simple mechanism which can explain why spatial heterogeneity may be a favorable factor for production. We consider a two patch model and a logistic growth is assumed on each patch. A general condition on the migration rates and the local subpopulation growth rates is provided under which the total carrying capacity is higher than the sum of the local carrying capacities, which is not intuitive. As we illustrate, this result is robust under stochastic perturbations.

Relations between bacterial biomass and carbon cycle in marine sediments: an early diagenetic model.

A new model for early diagenetic processes has been developed through a new formula explicitly accounting for microbial population dynamics. Following a mechanistic approach based on enzymatic reactions, a new model has been proposed for oxic mineralisation and denitrification. It incorporates the dynamics of bacterial metabolism. We find a general formula for inhibition processes of which some other mathematical expressions are particular cases. Moreover a fast numerical algorithm has been developed. It allows us to perform simulations of different diagenetic models in non-steady states. We use this algorithm to compare our model to a classical one (Soetaert et al., 1996). Dynamical evolutions of a perturbation of particulate organic carbon (POC) input are studied for both models. The results are very similar for stationary cases. But with variable inputs, the bacterial biomass dynamics brings about noticeable differences, and these are discussed.

Quantitative steps in symbiogenesis and the evolution of homeostasis.

The merging of two independent populations of heterotrophs and autotrophs into a single population of mixotrophs has occurred frequently in evolutionary history. It is an example of a wide class of related phenomena, known as symbiogenesis. The physiological basis is almost always (reciprocal) syntrophy, where each species uses the products of the other species. Symbiogenesis can repeat itself after specialization on particular assimilatory substrates. We discuss quantitative aspects and delineate eight steps from two free-living interacting populations to a single fully integrated endosymbiotic one. The whole process of gradual interlocking of the two populations could be mimicked by incremental changes of particular parameter values. The role of products gradually changes from an ecological to a physiological one. We found conditions where the free-living, epibiotic and endobiotic populations of symbionts can co-exist, as well as conditions where the endobiotic symbionts outcompete other symbionts. Our population dynamical analyses give new insights into the evolution of cellular homeostasis. We show how structural biomass with a constant chemical composition can evolve in a chemically varying environment if the parameters for the formation of products satisfy simple constraints. No additional regulation mechanisms are required for homeostasis within the context of the dynamic energy budget (DEB) theory for the uptake and use of substrates by organisms. The DEB model appears to be dosed under endosymbiosis. This means that when each free-living partner follows DEB rules for substrate uptake and use, and they become engaged in an endosymbiotic relationship, a gradual transition to a single fully integrated system is possible that again follows DEB rules for substrate uptake and use.

Alteration and release of aliphatic compounds by the polychaete Nereis virens (Sars) experimentally fed with hydrocarbons.

In the laboratory, marine worms were fed with a mixture of algae and several aliphatic hydrocarbons for 15 days. After ingestion by the worms, 34.9% of hydrocarbons are found in the faeces and only 3.1% accumulated in the gut. The comparison between the initial mixture and the faeces shows that the worm's digestive process lead to changes in the distribution of the n-alkane mixture. These changes are different from those only due to physical processes in the experimental conditions. In our experiment, no variation in the distribution of hydrocarbons in faeces with time and no microbial hydrocarbon biodegradation were evidenced. Our results suggest that marine worm feeding can substantially affect the fate of hydrocarbons in the sedimentary marine ecosystem by predominantly stimulating dissolution processes.

Emergence of individual behaviour at the population level. Effects of density-dependent migration on population dynamics.

The aim of this work is to study the effects of different individual behaviours on the overall growth of a spatially distributed population. The population can grow on two spatial patches, a source and a sink, that are connected by migrations. Two time scales are involved in the dynamics, a fast one corresponding to migrations and a slow one associated with the local growth on each patch. Different scenarios of density-dependent migration are proposed and their effects on the population growth are investigated. A general discussion on the use of aggregation methods for the study of integration of different ecological levels is proposed.

Emergence of population growth models: fast migration and slow growth.

We present aggregation and emergence methods in large-scale dynamical systems with different timescales. Aggregation corresponds to the reduction of the dimension of a dynamical system which is replaced by a smaller model for a small number of global variables at a slow timescale. We study the couplings between fast and slow dynamics leading to the emergence of global properties in the aggregated model. First, we study the case of a single population in a patchy environment. Growth rates are assumed to be linear on each patch. Individuals can migrate from one patch to another at a fast timescale. We choose different density dependent migration processes. In each case, we use aggregation methods to obtain the corresponding growth equation for the total density of the population at a slow timescale. We look for particular density dependent migration processes leading to an aggregated logistic-like equation. Second, we study the case of two interacting populations. A particular choice of density dependent migrations leads to an aggregated competition model.