Successful strategies in size structured mixotrophic food webs

This study investigates how food web structures in aquatic microbial communities emerge based on different mixotrophic life strategies. Unicellular mixotrophic organisms that combine osmotrophy and primary production with phagotrophy account for significant amounts of primary production and bacterivory in marine environments, yet mixotrophs are still usually absent in large-scale biogeochemical models. We here present for the first time a thorough analysis of a food web model with a finely resolved structure in both cell size and foraging mode, where foraging mode is a strategy ranging from pure osmotrophy to pure phagotrophy. A trade-off for maximum uptake rates of mixotrophs is incorporated. We study how different factors determine the food web structure, here represented by the topology of the distribution of given amounts of total phosphorous over the cell size-foraging mode plane. We find that mixotrophs successfully coexist with foraging specialists (pure osmo- and phagotrophs) for a wide range of conditions, a result consistent with the observed prevalence of mixotrophs in recent oceanographic surveys. Mixotrophy trade-off and size-dependent parameters have a strong effect on the emerging community structure, stressing the importance of foraging mode and size considerations when working with microbial diversity and food web dynamics. The proposed model may be used to develop timely representations of mixotrophic strategies in larger biogeochemical ocean models.     

The Protozooplankton–Ichthyoplankton Trophic Link: An Overlooked Aspect of Aquatic Food Webs1

ABSTRACT. Since the introduction of the microbial loop concept, awareness of the role played by protozooplankton in marine food webs has grown. By consuming bacteria, and then being consumed by metazooplankton, protozoa form a trophic link that channels dissolved organic material into the “classic” marine food chain. Beyond enhancing energy transfer to higher trophic levels, protozoa play a key role in improving the food quality of metazooplankton. Here, we consider a third role played by protozoa, but one that has received comparatively little attention: that as prey items for ichthyoplankton. For >100 years it has been known that fish larvae consume protozoa. Despite this, fisheries scientists and biological oceanographers still largely ignore protozoa when assessing the foodweb dynamics that regulate the growth and survival of larval fish. We review evidence supporting the importance of the protozooplankton–ichthyoplankton link, including examples from the amateur aquarium trade, the commercial aquaculture industry, and contemporary studies of larval fish. We then consider why this potentially important link continues to receive very little attention. We conclude by offering suggestions for quantifying the importance of the protozooplankton–ichthyoplankton trophic link, using both existing methods and new technologies.     

Does structural sensitivity alter complexity–stability relationships?

Structural sensitivity, namely the sensitivity of a model dynamics to slight changes in its mathematical formulation, has already been studied in some models with a small number of state variables. The aim of this study is to investigate the impact of structural sensitivity in a food web model. Especially, the importance of structural sensitivity is compared to that of trophic complexity (number of species, connectance), which is known to strongly influence food web dynamics. Food web structures are built using the niche model. Then food web dynamics are modeled using several type II functional responses parameterized to fit the same predation fluxes. Food web persistence was found to be mostly determined by trophic complexity. At the opposite, even if food web connectance promotes equilibrium dynamics, their occurrence is mainly driven by the choice of the functional response. These conclusions are robust to changes in some parameter values, the fitting method and some model assumptions. In a one-prey/one-predator system, it was shown that the possibility that multiple stable states coexist can be highly structural sensitive. Quantifying this type of uncertainty at the scale of ecosystem models will be both a natural extension to this work and a challenging issue.     

Antagonistic and Synergistic Interactions Among Predators

The structure and dynamics of food webs are largely dependent upon interactions among consumers and their resources. However, interspecific interactions such as intraguild predation and interference competition can also play a significant role in the stability of communities. The role of antagonistic/synergistic interactions among predators has been largely ignored in food web theory. These mechanisms influence predation rates, which is one of the key factors regulating food web structure and dynamics, thus ignoring them can potentially limit understanding of food webs. Using nonlinear models, it is shown that critical aspects of multiple predator food web dynamics are antagonistic/synergistic interactions among predators. The influence of antagonistic/synergistic interactions on coexistence of predators depended largely upon the parameter set used and the degree of feeding niche differentiation. In all cases when there was no effect of antagonism or synergism (a _ij =1.00), the predators coexisted. Using the stable parameter set, coexistence occurred across the range of antagonism/synergism used. However, using the chaotic parameter strong antagonism resulted in the extinction of one or both species, while strong synergism tended to coexistence. Whereas using the limit cycle parameter set, coexistence was strongly dependent on the degree of feeding niche overlap. Additionally increasing the degree of feeding specialization of the predators on the two prey species increased the amount of parameter space in which coexistence of the two predators occurred. Bifurcation analyses supported the general pattern of increased stability when the predator interaction was synergistic and decreased stability when it was antagonistic. Thus, synergistic interactions should be more common than antagonistic interactions in ecological systems.     

The dynamics of spatially coupled food webs

The dynamics of ecological systems include a bewildering number of biotic interactions that unfold over a vast range of spatial scales. Here, employing simple and general empirical arguments concerning the nature of movement, trophic position and behaviour we outline a general theory concerning the role of space and food web structure on food web stability. We argue that consumers link food webs in space and that this spatial structure combined with relatively rapid behavioural responses by consumers can strongly influence the dynamics of food webs. Employing simple spatially implicit food web models, we show that large mobile consumers are inordinately important in determining the stability, or lack of it, in ecosystems. More specifically, this theory suggests that mobile higher order organisms are potent stabilizers when embedded in a variable, and expansive spatial structure. However, when space is compressed and higher order consumers strongly couple local habitats then mobile consumers can have an inordinate destabilizing effect. Preliminary empirical arguments show consistency with this general theory.     

Seasonal microbial processes in a high-latitude fjord (Kongsfjorden, Svalbard): I. Heterotrophic bacteria, picoplankton and nanoflagellates

Temporal dynamics of the microbial food web in the Barents Sea and adjacent water masses in the European Arctic are to a large extent unknown. Seasonal variation in stocks and production rates of heterotrophic bacteria and phototrophic and heterotrophic picoplankton and nanoflagellates was investigated in the upper 50 m of the high-latitude Kongsfjorden, Svalbard, during six field campaigns between March and December 2006. Heterotrophic bacteria, picoplankton and nanoflagellates contributed to ecosystem structure and function in all seasons. Activity within the microbial food web peaked during spring bloom in April, parallel to low abundances of mesozooplankton. In the nutrient-limited post-bloom scenario, an efficient microbial loop, fuelled by dissolved organic carbon from abundant mesozooplankton feeding on phytoplankton and protozooplankton, facilitated maximum integrated primary production rates. A tight microbial food web consisting of heterotrophic bacteria and phototrophic and heterotrophic picoplankton and nanoflagellates was found in the stratified water masses encountered in July and September. Microbial stocks and rates were low but persistent under winter conditions. Seasonal comparisons of microbial biomass and production revealed that structure and function of the microbial food web were fundamentally different during the spring bloom when compared with other seasons. While the microbial food web was in a regenerative mode most of the time, during the spring bloom, a microbial transfer mode represented a trophic link for organic carbon in time and space. The microbial food web’s ability to fill different functional roles in periods dominated by new and regenerated production may enhance the ecological flexibility of pelagic ecosystems in the present era of climate change.     

Contrasting Mixotrophic Lifestyles Reveal Different Ecological Niches in Two Closely Related Marine Protists

Many marine microbial eukaryotes combine photosynthetic with phagotrophic nutrition, but incomplete understanding of such mixotrophic protists, their functional diversity, and underlying physiological mechanisms limits the assessment and modeling of their roles in present and future ocean ecosystems. We developed an experimental system to study responses of mixotrophic protists to availability of living prey and light, and used it to characterize contrasting physiological strategies in two stramenopiles in the genus Ochromonas. We show that oceanic isolate CCMP1393 is an obligate mixotroph, requiring both light and prey as complementary resources. Interdependence of photosynthesis and heterotrophy in CCMP1393 comprises a significant role of mitochondrial respiration in photosynthetic electron transport. In contrast, coastal isolate CCMP2951 is a facultative mixotroph that can substitute photosynthesis by phagotrophy and hence grow purely heterotrophically in darkness. In contrast to CCMP1393, CCMP2951 also exhibits a marked photoprotection response that integrates non-photochemical quenching and mitochondrial respiration as electron sink for photosynthetically produced reducing equivalents. Facultative mixotrophs similar to CCMP2951 might be well adapted to variable environments, while obligate mixotrophs similar to CCMP1393 appear capable of resource efficient growth in oligotrophic ocean environments. Thus, the responses of these phylogenetically close protists to the availability of different resources reveals niche differentiation that influences impacts in food webs and leads to opposing carbon cycle roles.     

Food Web Structure in the Recently Flooded Sep Reservoir as Inferred From Phytoplankton Population Dynamics and Living Microbial Biomass

Phytoplankton dynamics, bacterial standing stocks and living microbial biomass (derived from ATP measurements, 0.7-200 mm size class) were examined in 1996 in the newly flooded (1995) Sep Reservoir ('Massif Central,' France), for evidence of the importance of the microbial food web relative to the traditional food chain. Phosphate concentrations were low, N:P ratios were high, and phosphate losses converted into carbon accounted for <50% of phytoplankton biomass and production, indicating that P was limiting phytoplankton development during the study. The observed low availability of P contrasts with the high release of "directly" assimilable P often reported in newly flooded reservoirs, suggesting that factors determining nutrient dynamics in such ecosystems are complex. The phosphate availability, but also the water column stability, seemed to be among the major factors determining phytoplankton dynamics, as (i) large-size phytoplankton species were prominent during the period of increasing water column stability, whereas small-size species dominated phytoplankton assemblages during the period of decreasing stability, and (ii) a Dinobryon divergens bloom occurred during a period when inorganic P was undetectable, coinciding with the lowest values of bacterial standing stocks. Indication of grazing limitation of bacterial populations by the mixotrophic chrysophyte D. divergens (in late spring) and by other potential grazers (mainly rotifers in summer) seemed to be confirmed by the Model II or functional slopes of the bacterial vs phytoplankton regressions, which were always <0.63. Phytoplankton biomass was not correlated with phosphorus sources and its contribution was remarkably low relative to the living microbial biomass which, in contrast, was positively correlated with total phosphorus in summer. We conclude that planktonic microheterotrophs are strongly implicated in the phosphorus dynamics in the Sep Reservoir, and thus support the idea that an important amount of matter and energy flows through the "microbial loop" and food web, shortly after the flooding of a reservoir.     

Importance of mixotrophic bacterivory can be predicted by light and loss rates

Recent observational studies form oligotrophic waters provide ample evidence that mixotrophic flagellates often account for the bulk of bacterivory. However, we lack a general framework that allows a mechanistic understanding of success of mixotrophs in the competition with heterotrophic bacterivores. This is especially needed for integrating mixotrophy in models of the microbial loop. Based on general tradeoffs linked to the combined resource use in mixotrophs (generalist versus specialist), we propose a concept where mixotrophs are favored by conditions of high light – low losses, corresponding to the situation found in the surface waters of oligotrophic oceans. Under such conditions, they can achieve positive net growth at very low resource levels, allowing simultaneous competition with specialized protists. Conversely, heterotrophic bacterivores and photoautotrophs should be especially favored in more productive and low‐light conditions. We show experimentally that the combined effect of light and loss rates (dilution) predicts the success of mixotrophic bacterivorous flagellates. Moreover, our results suggest that total bacterivory, contrary as seen in the traditional microbial loop concept, has a more intricate coupling to light.     

Re-evaluating the omnivory–stability relationship in food webs

Under equilibrium conditions, previous theory has shown that the presence of omnivory destabilizes food webs. Correspondingly, omnivory ought to be rare in real food webs. Although, early food web data appeared to verify this, recently many ecologists have found omnivory to be ubiquitous in food web data gathered at a high taxonomic resolution. In this paper, we re-investigate the role of omnivory in food webs using a non-equilibrium perspective. We find that the addition of omnivory to a simple food chain model (thus a simple food web) locally stabilizes the food web in a very complete way. First, non-equilibrium dynamics (e.g. chaos) tend to be eliminated or bounded further away from zero via period-doubling reversals invoked by the omnivorous trophic link. Second, food chains without interior attractors tend to gain a stable interior attractor with moderate amounts of omnivory.     

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.     

Synergism between research and simulation models of estuarine microbial food webs

Construction of mathematical simulation models helps to organize current information and extend inferences from available data. During the past two decades, microbial ecology has undergone rapid developments in both quantity and quality of available data. In particular, considerable advances have been made in our knowledge of microbial food web dynamics in the Duplin River watershed at Sapelo Island, Georgia. Here we provide examples of how modeling and microbial ecology have interfaced. In the early 1970s, construction of a 14-compartment model of carbon flow through a salt marsh ecosystem aided in directing method development and field experiments on the sediment microbial community. In turn, the results of field experiments corroborated the model's postulated controls on the community. Also, during the past 12 years we have developed a series of simulation models reflecting the growing information on the aquatic microbial food web. Early models provided evidence for the microbial loop but illustrated the paucity of knowledge concerning controls for bacterial growth on detritus. Results from newer methods in microbial ecology and studies from the Duplin River have allowed us to construct a model which provides realistic simulations but is also highly sensitive to certain parameter value changes (e.g., in organic matter availability and grazing by protozoans). Thus improvements in model structure and corroboration of the models with extant data have been closely tied to methodological and conceptual advances in microbial ecology. The relationship is viewed as synergistic, as needs for model parameter values and equation forms have directed further development of methods, experimentation, and field observations.     

Roles of food web and heterotrophic microbial processes in upper ocean biogeochemistry: Global patterns and processes

The growth and dynamics of plankton in the ocean vary with natural cycles, global climate change and the long-term evolution of ecosystems. The ocean is a large reservoir for CO₂ and the food webs in the upper ocean play critical roles in regulating the global carbon cycle, changes in atmospheric CO₂ and associated global warming. Microheterotrophs are a key component of the upper ocean food webs. Here, we report on the results of an analysis of the distribution of bacteria and related properties in the World Ocean. We found that, for the data set as a whole, there is a significant latitudinal gradient in all field-measured and computed bacterial properties, except growth rate. Gradients were, for the most part, driven by an equator-ward increase in the Southern Hemisphere. The biomass, rates of production and respiration and dissolved organic carbon concentrations were significantly higher in the Northern than the Southern hemispheres. In contrast, growth rates were the same in the two hemispheres. We conclude that the lower biomass and production in the Southern Hemisphere reflects greater top-down control by microbial grazers, which would be due to a lower abundance or activity of omnivorous zooplankton in the Southern than Northern Hemispheres. These large spatial differences in dynamics, structure and activity of the bacterial community and the microbial food web will be reflected in different patterns of carbon cycling, export and air–sea exchange of CO₂ and the potential ability of the ocean to sequester carbon.     

The impact of climate warming on the diurnal dynamics of the microbial loop: Ice cover vs. lack of ice cover on dystrophic lakes

One of the effects of warming is earlier retreat of the ice cover or a complete lack of ice cover on water bodies in the winter. However, there is still no information on how climate warming affects the 24-hour dynamics of the planktonic microbial loop in winter. The aim of this investigation was to assess the diurnal dynamics of the taxonomic composition and abundance of microbial communities in experimentally reproduced conditions (samples from under the ice, +2, +4 and +8 °C) and to analyse the relationships between components of the microbial loop in relation to physical and chemical parameters. Samples were taken in winter from three dystrophic reservoir. The biological and physicochemical parameters in the water were analysed at the start (day 0), 15 and end of the experiment (day 30) over a 24-hour cycle. The increase in temperature caused an increase in the numbers of predators (particularly testate amoebae and ciliates) and a reduction in the body size of individual populations. During the period with ice cover, marked dominance of mixotrophic testate amoeba (Hyalosphenia papilio) and ciliates (Paramecium bursaria) was observed, while the increase in temperature caused an increase in the proportion of bacterivorous ciliates (Cinetochilum margaritaceum).     

Mathematical identification of critical reactions in the interlocked feedback model

Dynamic simulations are necessary for understanding the mechanism of how biochemical networks generate robust properties to environmental stresses or genetic changes. Sensitivity analysis allows the linking of robustness to network structure. However, it yields only local properties regarding a particular choice of plausible parameter values, because it is hard to know the exact parameter values in vivo. Global and firm results are needed that do not depend on particular parameter values. We propose mathematical analysis for robustness (MAR) that consists of the novel evolutionary search that explores all possible solution vectors of kinetic parameters satisfying the target dynamics and robustness analysis. New criteria, parameter spectrum width and the variability of solution vectors for parameters, are introduced to determine whether the search is exhaustive. In robustness analysis, in addition to single parameter sensitivity analysis, robustness to multiple parameter perturbation is defined. Combining the sensitivity analysis and the robustness analysis to multiple parameter perturbation enables identifying critical reactions. Use of MAR clearly identified the critical reactions responsible for determining the circadian cycle in the Drosophila interlocked circadian clock model. In highly robust models, while the parameter vectors are greatly varied, the critical reactions with a high sensitivity are uniquely determined. Interestingly, not only the per-tim loop but also the dclk-cyc loop strongly affect the period of PER, although the dclk-cyc loop hardly changes its amplitude and it is not potentially influential. In conclusion, MAR is a powerful method to explore wide parameter space without human-biases and to link a robust property to network architectures without knowing the exact parameter values. MAR identifies the reactions critically responsible for determining the period and amplitude in the interlocked feedback model and suggests that the circadian clock intensively evolves or designs the kinetic parameters so that it creates a highly robust cycle.     

Periodic metabolic systems: Oscillations in multiple-loop negative feedback biochemical control networks

Summary For a general multiple loop feedback inhibition system in which the end product can inhibit any or all of the intermediate reactions it is shown that biologically significant behaviour is always confined to a bounded region of reaction space containing a unique equilibrium. By explicit construction of a Liapunov function for the general n dimensional differential equation it is shown that some values of reaction parameters cause the concentration vector to approach the equilibrium asymptotically for all physically realizable initial conditions. As the parameter values change, periodic solutions can appear within the bounded region. Some information about these periodic solutions can be obtained from the Hopf bifurcation theorem. Alternatively, if specific parameter values are known a numerical method can be used to find periodic solutions and determine their stability by locating a zero of the displacement map. The single loop Goodwin oscillator is analysed in detail. The methods are then used to treat an oscillator with two feedback loops and it is found that oscillations are possible even if both Hill coefficients are equal to one.     

Systematic search for the rate constants that control the exocytotic process from chromaffin cells by a genetic algorithm

We have recently created a kinetic model that reproduces the dynamics of exocytosis with high accuracy. The reconstruction necessitated a search, in a multi-dimensional parameter space, for 37 parameters that described the system, with no assurance that the parameters, which reconstructed the observations, are a unique set. In the present study, a Genetic Algorithm (GA) was used for a thorough search in the unknown parameter space, using a strategy of gradual increase of the complexity of the analyzed input data. Upon systematic incorporation of one to four measurable parameters, used as input signals for the analysis, the constraint set on the GA search imposed the convergence of the free parameters into a single narrow range. The mean values for each adjustable parameter represent a minimum for the fitness function in the multi-dimensional parameter space. The GA search demonstrates that the parameters that control the kinetics of exocytosis are the rate constants of the steps downstream to synaptotagmin binding, and that the equilibrium constant of the binding of calcium to Munc13 controls the calcium-dependent priming process. Thus, the systematic use of the GA creates a link between specific reactions in the process of exocytosis and experimental phenotypes.     

Bursting Regimes in a Reaction-Diffusion System with Action Potential-Dependent Equilibrium

The equilibrium Nernst potential plays a critical role in neural cell dynamics. A common approximation used in studying electrical dynamics of excitable cells is that the ionic concentrations inside and outside the cell membranes act as charge reservoirs and remain effectively constant during excitation events. Research into brain electrical activity suggests that relaxing this assumption may provide a better understanding of normal and pathophysiological functioning of the brain. In this paper we explore time-dependent ionic concentrations by allowing the ion-specific Nernst potentials to vary with developing transmembrane potential. As a specific implementation, we incorporate the potential-dependent Nernst shift into a one-dimensional Morris-Lecar reaction-diffusion model. Our main findings result from a region in parameter space where self-sustaining oscillations occur without external forcing. Studying the system close to the bifurcation boundary, we explore the vulnerability of the system with respect to external stimulations which disrupt these oscillations and send the system to a stable equilibrium. We also present results for an extended, one-dimensional cable of excitable tissue tuned to this parameter regime and stimulated, giving rise to complex spatiotemporal pattern formation. Potential applications to the emergence of neuronal bursting in similar two-variable systems and to pathophysiological seizure-like activity are discussed.     

Significance of predation by protists in aquatic microbial food webs

Predation in aquatic microbial food webs is dominated by phagotrophic protists, yet these microorganisms are still understudied compared to bacteria and phytoplankton. In pelagic ecosystems, predaceous protists are ubiquitous, range in size from 2 μm flagellates to >100 μm ciliates and dinoflagellates, and exhibit a wide array of feeding strategies. Their trophic states run the gamut from strictly phagotrophic, to mixotrophic: partly autotrophic and partly phagotrophic, to primarily autotrophic but capable of phagotrophy. Protists are a major source of mortality for both heterotrophic and autotrophic bacteria. They compete with herbivorous meso- and macro-zooplankton for all size classes of phytoplankton. Protist grazing may affect the rate of organic sinking flux from the euphotic zone. Protist excretions are an important source of remineralized nutrients, and of colloidal and dissolved trace metals such as iron, in aquatic systems. Work on predation by protists is being facilitated by methodological advances, e.g., molecular genetic analysis of protistan diversity and application of flow cytometry to study population growth and feeding rates. Examples of new research areas are studies of impact of protistan predation on the community structure of prey assemblages and of chemical communication between predator and prey in microbial food webs. This revised version was published online in August 2006 with corrections to the Cover Date.