Community convergence in a simple microbial food web

Previous studies of communities implicate many potential mechanisms that can create alternate stable states. These include density-dependent foraging behavior, size refuges reached by early colonists, environmental feedback following disturbance, and different initial densities of intraguild predators. Previous work shows that alternate states of varying stability can occur in food webs containing the intraguild predators Blepharisma americanum and Tetrahymena vorax. Differences in colonization history could create the alternate states, consisting of dominance by either Blepharisma or Tetrahymena, but it was unclear whether results depended on effects of initial density or only on changes in the resource base. We manipulated initial densities of both species to determine if density effects alone could create alternate stable states. Convergence of these communities over time indicated that differences in initial density did not create alternate stable states. By default, other factors influenced by colonization history, such as resource availability, may produce alternate states. Models of alternate stable-state phenomena should incorporate differences in resource availability in addition to direct competitive and predatory interactions to provide a more complete depiction of the causes of differences in community composition in otherwise similar habitats.     

Modeling the microbial food web

Models of the microbial food web have their origin in the debate over the importance of bacteria as an energetic subsidy for higher trophic levels leading to harvestable fisheries. Conceptualization of the microbial food web preceded numerical models by 10–15 years. Pomeroy's work was central to both efforts. Elements necessary for informative and comprehensive models of microbial loops in plankton communities include coupled carbon and nitrogen flows utilizing a size-based approach to structuring and parameterizing the food web. Realistic formulation of nitrogen flows requires recognition that both nitrogenous and nonnitrogenous organic matter are important substrates for bacteria. Nitrogen regeneration driven by simple mass-specific excretion constants seems to overestimate the role of bacteria in the regeneration process. Quantitative assessment of the link-sink question, in which the original loop models are grounded, requires sophisticated analysis of size-based trophic structures. The effects of recycling complicate calculation of the link between bacteria or dissolved organic matter and mesozooplankton, and indirect effects show that the link might be much stronger than simple analyses have suggested. Examples drawn from a series of oceanic mixed layer plankton models are used to illustrate some of these points. Single-size class models related to traditional P-Z-N approaches are incapable of simulating bacterial biomass cycles in some locations (e.g., Bermuda) but appear to be adequate for more strongly seasonal regimes at higher latitudes.     

Trophic coupling within the microbial food web: a study with fine temporal resolution in a eutrophic freshwater ecosystem

• 1 The major components of the microbial food web (dissolved organic carbon, bacteria, protozoa, rotifers and algae) of Priest Pot, a small freshwater pond, were investigated over a period of 5 months. Water samples were collected from the epilimnion every 1–3 days.
• 2 Time series analysis helped identify the trophic relationships within the planktonic community. There were strong predator—prey relationships between both ciliates and large rotifers and the total nanoplankton, between rotifers and small ciliates and between the total microzooplankton community and phytoplankton. Small rotifers and small ciliates probably share the same food resources. The major bacterivores in the system could not be identified with our methods. However, our previous results point to a dominating role of nanoplanktonic (2–20 μm) heterotrophic protists as the main grazers of bacteria.
• 3 Rotifers are the major type of metazoan zooplankton in Priest Pot; crustacean zooplankton are absent from the community. Bacterial production probably reaches rotifers via a variety of pathways: there may be a three-step link from bacteria to bacterivorous nanoplankton, to ciliates and then to rotifers. Furthermore, a strong correlation between the nanoplankton and rotifers suggests a direct link between these components, implying a much shorter pathway. Some of the rotifers in the pond can graze directly on bacteria, and many of the larger planktonic organisms (large ciliates and rotifers) are algivores. The latter two predator—prey relationships suggest an efficient transfer of bacterial and primary production to higher trophic levels.

     

Relating planktonic microbial food web structure in lentic freshwater ecosystems to water quality and land use

Relationships among picoplankton, protozoa, phytoplankton, plantnutrients, lake type, drainage basin morphology and land coverwere studied in 45 water bodies in South Island, New Zealandthat ranged from large, deep, ultra-oligotrophic lakes to shallow,macrophyte-dominated ponds and swamps. The biomasses of mostheterotrophic components of the pelagic microbial food webswere positively related to phytoplankton and features of thedrainage basin that enhanced nutrient input, and imply strongresource-driven structuring of pelagic microbial food webs.Prokaryotic picophytoplankton biomass was negatively relatedto indices of eutrophication, and the picoautotroph contributionto total microbial food web biomass declined with increasingtotal phosphorus concentration from 16.5% in deep lakes to <0.02%in swamps and ponds. Biomass ratios of (picoplankton plus protozoa):phytoplanktonranged from 40:60 in swamps and ponds to >70:30 in deep lakes,and indicate the potential importance of microbial food websin carbon transfer to higher trophic levels in deep, less productivelakes. Strong relationships exist between land use in the catchmentand pelagic microbial food web structure and biomass acrossa wide range in size and trophic state of water bodies in heterogeneouslandscapes.     

A methane-driven microbial food web in a wetland rice soil

Methane oxidation is a key process controlling methane emission from anoxic habitats into the atmosphere. Methanotrophs, responsible for aerobic methane oxidation, do not only oxidize but also assimilate methane. Once assimilated, methane carbon may be utilized by other organisms. Here we report on a microbial food web in a rice field soil driven by methane. A thin layer of water-saturated rice field soil was incubated under opposing gradients of oxygen and (13)C-labelled methane. Bacterial and eukaryotic communities incorporating methane carbon were analysed by RNA-stable isotope probing (SIP). Terminal restriction fragment length polymorphism (T-RFLP) and cloning showed that methanotrophs were the most prominent group of bacteria incorporating methane carbon. In addition, a few Myxobacteria-related sequences were obtained from the 'heavy' rRNA fraction. Denaturing gradient gel electrophoresis (DGGE) targeting 18S rRNA detected various groups of protists in the 'heavy' rRNA fraction including naked amoeba (Lobosea and Heterolobosea), ciliates (Colpodea) and flagellates (Cercozoa). Incubation of soil under different methane concentrations in air resulted in the development of distinct protozoan communities. These results suggest that methane carbon is incorporated into non-methanotrophic pro- and microeukaryotes probably via grazing, and that methane oxidation is a shaping force of the microeukaryotic community depending on methane availability.     

The microbial food web along salinity gradients

The microbial food web was studied along a gradient of salinity in two solar salterns used for the commercial production of salt. The different ponds in the salterns provide a wide range of ecosystems with food webs of different complexities. Abundance of prokaryotes, cell volume, prokaryotic heterotrophic production, chlorophyll a, abundance of heterotrophic flagellates, ciliates and phytoplankton were determined in several ponds in each saltern. Increases in salinity resulted in a progressive reduction in the abundance and number of different groups of eukaryotic microorganisms present, but an increase in biomass of prokaryotes. Maximal activity of both phyto- and bacterioplankton was found at a salinity of around 100 per thousand, where there was also a maximum in chlorophyll a concentration. Growth rates of heterotrophic prokaryotes decreased with increasing salinity. Bacterivory disappeared above 250 per thousand salinity, whereas other loss factors such as viral lysis appeared to be of minor importance throughout the gradient [Guixa-Boixereu et al. (1996) Aquat. Microb. Ecol. 11, 215-227].     

Habitat structural complexity mediates food web dynamics in a freshwater macrophyte community

A considerable amount of research has investigated the influence of habitat structure on predator success, yet few studies have explored the implications for community structure and food-web dynamics. The relative importance of macrophyte structure and fish predation on the composition of the macroinvertebrate and periphyton communities in a lowland river was investigated using a multifactorial caging experiment. We hypothesised that: (1) fish predators are less effective in a more structurally complex macrophyte analogue; (2) strong direct and indirect effects of fish predators (e.g. trophic cascades) are less likely to occur in a structurally complex habitat; and (3) the strength of these patterns is influenced by the composition of the prevailing community assemblage. We measured the abundance and composition of the macroinvertebrate and periphyton communities associated with three different-shaped macrophyte analogues, under different fish predator treatments and at different times. Macrophyte analogue architecture had strong, consistent effects on both the macroinvertebrate and periphyton communities; both were most abundant and diverse on the most structurally complex plant analogue. In contrast, the fish predators affected only a subset of the macroinvertebrate community and there was a suggestion of minor indirect effects on periphyton community composition. Contrary to expectations, the fish predators had their strongest effects in the most structurally complex macrophyte analogue. We conclude that in this system, macrophyte shape strongly regulates the associated freshwater assemblage, resulting in a diverse community structure less likely to exhibit strong effects of fish predation.     

Rapid evolution buffers ecosystem impacts of viruses in a microbial food web

Predation and parasitism often regulate population dynamics, community interactions, and ecosystem functioning. The strength of these top-down pressures is variable, however, and may be influenced by both ecological and evolutionary processes. We conducted a chemostat experiment to assess the direct and indirect effects of viruses on a marine microbial food web comprised of an autotrophic host (Synechococcus) and non-target heterotrophic bacteria. Viruses dramatically altered the host population dynamics, which in turn influenced phosphorus resource availability and the stoichiometric allocation of nutrients into microbial biomass. These virus effects diminished with time, but could not be attributed to changes in the abundance or composition of heterotrophic bacteria. Instead, attenuation of the virus effects coincided with the detection of resistant host phenotypes, suggesting that rapid evolution buffered the effect of viruses on nutrient cycling. Our results demonstrate that evolutionary processes are important for community dynamics and ecosystem processes on ecologically relevant time scales.     

Identification of bacterial micropredators distinctively active in a soil microbial food web

The understanding of microbial interactions and trophic networks is a prerequisite for the elucidation of the turnover and transformation of organic materials in soils. To elucidate the incorporation of biomass carbon into a soil microbial food web, we added 13C-labeled Escherichia coli biomass to an agricultural soil and identified those indigenous microbes that were specifically active in its mineralization and carbon sequestration. rRNA stable isotope probing (SIP) revealed that uncultivated relatives of distinct groups of gliding bacterial micropredators (Lysobacter spp., Myxococcales, and the Bacteroidetes) lead carbon sequestration and mineralization from the added biomass. In addition, fungal populations within the Microascaceae were shown to respond to the added biomass after only 1 h of incubation and were thus surprisingly reactive to degradable labile carbon. This RNA-SIP study identifies indigenous microbes specifically active in the transformation of a nondefined complex carbon source, bacterial biomass, directly in a soil ecosystem.     

Structure of planktonic microbial food web in a brackish stratified Siberian lake

The distribution of primary components of the microbial community (autotrophic pico- and nanoplankton, phototrophic bacteria, heterotrophic bacteria, microscopic fungi, heterotrophic flagellates, ciliates and heliozoa) in the water column of Lake Shira, a steppe brackish-water, stratified lake in Khakasia, Siberia (Russia), were assessed in midsummer. Bacterioplankton was the main component of the planktonic microbial community, accounting for 65.3 to 75.7% of the total microbial biomass. The maximum concentration of heterotrophic bacteria were recorded in the monimolimnion of the lake. Autotrophic microorganisms contributed more significantly to the total microbial biomass in the pelagic zone (20.2–26.5%) than in the littoral zone of the lake (8.7–14.9%). First of all, it is caused by development of phototrophic sulphur bacteria at the oxic-anoxic boundary. The concentrations of most aerobic phototrophic and heterotrophic microorganisms were maximal in the upper mixolimnion. Heterotrophic flagellates dominated the protozoan populations. Ciliates were minor component of the planktonic microbial community of the lake. Heterotrophic flagellates were the most diverse group of planktonic eucaryotes in the lake, which represented by 36 species. Facultative and obligate anaerobic flagellates were revealed in the monimolimnion. There were four species of Heliozoa and only three of ciliates in the lake.     

Direct and indirect responses of a freshwater food web to a potent synthetic oestrogen

Endocrine-disrupting chemicals (EDCs) in municipal effluents directly affect the sexual development and reproductive success of fishes, but indirect effects on invertebrate prey or fish predators through reduced predation or prey availability, respectively, are unknown. At the Experimental Lakes Area in northwestern Ontario, Canada, a long-term, whole-lake experiment was conducted using a before-after-control-impact design to determine both direct and indirect effects of the synthetic oestrogen used in the birth control pill, 17α-ethynyloestradiol (EE2). Algal, microbial, zooplankton and benthic invertebrate communities showed no declines in abundance during three summers of EE2 additions (5–6 ng l⁻¹), indicating no direct toxic effects. Recruitment of fathead minnow (Pimephales promelas) failed, leading to a near-extirpation of this species both 2 years during (young-of-year, YOY) and 2 years following (adults and YOY) EE2 additions. Body condition of male lake trout (Salvelinus namaycush) and male and female white sucker (Catostomus commersonii) declined before changes in prey abundance, suggesting direct effects of EE2 on this endpoint. Evidence of indirect effects of EE2 was also observed. Increases in zooplankton, Chaoborus, and emerging insects were observed after 2 or 3 years of EE2 additions, strongly suggesting indirect effects mediated through the reduced abundance of several small-bodied fishes. Biomass of top predator lake trout declined by 23–42% during and after EE2 additions, most probably an indirect effect from the loss of its prey species, the fathead minnow and slimy sculpin (Cottus cognatus). Our results demonstrate that small-scale studies focusing solely on direct effects are likely to underestimate the true environmental impacts of oestrogens in municipal wastewaters and provide further evidence of the value of whole-ecosystem experiments for understanding indirect effects of EDCs and other aquatic stressors.     

Effects of temperature variability on community structure in a natural microbial food web

Climate change research has demonstrated that changing temperatures will have an effect on community‐level dynamics by altering species survival rates, shifting species distributions, and ultimately, creating mismatches in community interactions. However, most of this work has focused on increasing temperature, and still little is known about how the variation in temperature extremes will affect community dynamics. We used the model aquatic community held within the leaves of the carnivorous plant, Sarracenia purpurea, to test how food web dynamics will be affected by high temperature variation. We tested the community response of the first (bacterial density), second (protist diversity and composition), and third trophic level (predator mortality), and measured community respiration. We collected early and late successional stage inquiline communities from S. purpurea from two North American and two European sites with similar average July temperature. We then created a common garden experiment in which replicates of these communities underwent either high or normal daily temperature variation, with the average temperature equal among treatments. We found an impact of temperature variation on the first two, but not on the third trophic level. For bacteria in the high‐variation treatment, density experienced an initial boost in growth but then decreased quickly through time. For protists in the high‐variation treatment, alpha‐diversity decreased faster than in the normal‐variation treatment, beta‐diversity increased only in the European sites, and protist community composition tended to diverge more in the late successional stage. The mortality of the predatory mosquito larvae was unaffected by temperature variation. Community respiration was lower in the high‐variation treatment, indicating a lower ecosystem functioning. Our results highlight clear impacts of temperature variation. A more mechanistic understanding of the effects that temperature, and especially temperature variation, will have on community dynamics is still greatly needed.     

Major contribution of sulfide-derived sulfur to the benthic food web in a large freshwater lake

In freshwater systems, contributions of chemosynthetic products by sulfur-oxidizing bacteria in sediments as nutritional resources in benthic food webs remain unclear, even though chemosynthetic products might be an important nutritional resource for benthic food webs in deep-sea hydrothermal vents and shallow marine systems. To study geochemical aspects of this trophic pathway, we sampled sediment cores and benthic animals at two sites (90 and 50 m water depths) in the largest freshwater (mesotrophic) lake in Japan: Lake Biwa. Stable carbon, nitrogen, and sulfur isotopes of the sediments and animals were measured to elucidate the sulfur nutritional resources for the benthic food web precisely by calculating the contributions of the incorporation of sulfide-derived sulfur to the biomass and of the biogeochemical sulfur cycle supporting the sulfur nutritional resource. The recovered sediment cores showed increases in ³⁴S-depleted sulfide at 5 cm sediment depth and showed low sulfide concentration with high δ³⁴S in deeper layers, suggesting an association of microbial activities with sulfate reduction and sulfide oxidation in the sediments. The sulfur-oxidizing bacteria may contribute to benthic animal biomass. Calculations based on the biomass, sulfur content, and contribution to sulfide-derived sulfur of each animal comprising the benthic food web revealed that 58%–67% of the total biomass sulfur in the benthic food web of Lake Biwa is occupied by sulfide-derived sulfur. Such a large contribution implies that the chemosynthetic products of sulfur-oxidizing bacteria are important nutritional resources supporting benthic food webs in the lake ecosystems, at least in terms of sulfur. The results present a new trophic pathway for sulfur that has been overlooked in lake ecosystems with low-sulfate concentrations.     

Changes in the pelagic microbial food web due to artificial eutrophication

The effect of nutrient enrichment on the structure and carbon flow in the pelagic microbial food web was studied in mesocosm experiments using seawater from the northern Baltic Sea. The experiments included food webs of at least four trophic levels; (1) phytoplankton–bacteria, (2) flagellates, (3) ciliates and (4) mesozooplankton. In the enriched treatments high autotrophic growth rates were observed, followed by increased heterotrophic production. The largest growth increase was due to heterotrophic bacteria, indicating that the heterotrophic microbial food web was promoted. This was further supported by increased growth of heterotrophic flagellates and ciliates in the high nutrient treatments. The phytoplankton peak in the middle of the experiments was mainly due to an autotrophic nanoflagellate, Pyramimonas sp. At the end of the experiment, the proportion of heterotrophic organisms was higher in the nutrient enriched than in the nutrient-poor treatment, indicating increased predation control of primary producers. The proportion of potentially mixotrophic plankton, prymnesiophyceans, chrysophyceans and dinophyceans, were significantly higher in the nutrient-poor treatment. Furthermore, the results indicated that the food web efficiency, defined as mesozooplankton production per basal production (primary production + bacterial production − sedimentation), decreased with increasing nutrient status, possibly due to increasing loss processes in the food web. This could be explained by promotion of the heterotrophic microbial food web, causing more trophic levels and respiration steps in the food web.     

Dynamics of evolutionary patterns of clades in a food web system model

The evolutionary patterns of animal species clades in an evolving food web system were examined by computer simulation. In this system, each animal species fed on other species according to feeding preference. The food web system evolved via the appearance and extinction of species. The model succeeded in reproducing evolutionary patterns of diversity similar to those seen in the fossil record. This result indicates that the model reproduced the temporal changes of the rates of colonization and extinction of species in the system, which have been decided a priori in the previous stochastic models. In the food web system, the numbers of both predatory and prey species influenced the temporal diversity patterns in each clade in the system. The number of prey species fluctuated strongly, whereas the number of predatory species gradually increased with time. Therefore, temporal diversity patterns were influenced mainly by the number of predatory species. As a result of the gradual increase of the number of predatory species, it was difficult for each clade to maintain its species diversity for a long time. Slight changes of interspecific interaction can sometimes decide the destiny of a clade. When a clade is faced with extinction, if one predatory species of the clade becomes extinct and one or two prey species of the clade appear, the species diversity in the clade increases again. This result indicates that slight changes of interspecific interaction sometimes decide the destiny of a clade.     

The carbohydrates of Phaeocystis and their degradation in the microbial food web

The ubiquity and high productivity associated with blooms of colonial Phaeocystis makes it an important contributor to the global carbon cycle. During blooms organic matter that is rich in carbohydrates is produced. We distinguish five different pools of carbohydrates produced by Phaeocystis. Like all plants and algal cells, both solitary and colonial cells produce (1) structural carbohydrates, (hetero) polysaccharides that are mainly part of the cell wall, (2) mono- and oligosaccharides, which are present as intermediates in the synthesis and catabolism of cell components, and (3) intracellular storage glucan. Colonial cells of Phaeocystis excrete (4) mucopolysaccharides, heteropolysaccharides that are the main constituent of the mucous colony matrix and (5) dissolved organic matter (DOM) rich in carbohydrates, which is mainly excreted by colonial cells. In this review the characteristics of these pools are discussed and quantitative data are summarized. During the exponential growth phase, the ratio of carbohydrate-carbon (C) to particulate organic carbon (POC) is approximately 0.1. When nutrients are limited, Phaeocystis blooms reach a stationary growth phase, during which excess energy is stored as carbohydrates. This so-called overflow metabolism increases the ratio of carbohydrate-C to POC to 0.4–0.6 during the stationary phase, leading to an increase in the C/N and C/P ratios of Phaeocystis organic matter. Overflow metabolism can be channeled towards both glucan and mucopolysaccharides. Summarizing the available data reveals that during the stationary phase of a bloom glucan contributes 0–51% to POC, whereas mucopolysaccharides contribute 5–60%. At the end of a bloom, lysis of Phaeocystis cells and deterioration of colonies leads to a massive release of DOM rich in glucan and mucopolysaccharides. Laboratory studies have revealed that this organic matter is potentially readily degradable by heterotrophic bacteria. However, observations in the field of accumulation of DOM and foam indicate that microbial degradation is hampered. The high C/N and C/P ratios of Phaeocystis organic matter may lead to nutrient limitation of microbial degradation, thereby prolonging degradation times. Over time polysaccharides tend to self-assemble into hydrogels. This may have a profound effect on carbon cycling, since hydrogels provide a vehicle to move DOM up the size spectrum to sizes subject to sedimentation. In addition, it changes the physical nature and microscale structure of the organic matter encountered by bacteria which may affect the degradation potential of the Phaeocystis organic matter.     

Direct and indirect food web regulation of microbial decomposers in headwater streams

The direct and indirect regulation of primary productivity has been well established in autotrophic‐based ecosystems; however, less is known about the processes affecting decomposers in detrital‐based ecosystems. Because, small headwater, woodland streams are a dominate feature in most ecosystems and are tightly linked to terrestrial detritus, understanding decomposer‐mediated functions in these systems is critical for understanding carbon processes across the landscape. In this light, we conducted a microcosm and mesocosm experiment to test the direct and indirect food web effects on decomposers in small stream ecosystems. The results from the microcosm experiment supported an existing literature, demonstrating that nutrients directly stimulate decomposers and that microbivores directly reduce decomposers. Based on well‐founded food web theory in autotrophic systems, we predicted that fishes from different trophic‐functional guilds would indirectly stimulate decomposers by enhancing dissolved nutrients and by reducing microbivore densities. Our mesocosm experiment partially supported these predictions. Specifically, we found that fishes that consumed mostly terrestrial foods increased decomposers from the bottom–up by enhancing allochthonous nutrient loading into the stream ecosystems. Contrary to our predictions, however, predatory fishes that consume microbivores did not increase decomposers from the top–down. Rather, in streams with the predatory fish species, microbivores increased (rather than decreased) on leaf litter. This may have resulted from an experimental artifact associated with refuge provided by leaf packs. In conclusion, our data demonstrate that decomposers are regulated by similar direct and indirect processes important in autotrophic‐based ecosystems. This provides further evidence that food web processes can regulate leaf decomposition and flux of detrital carbon through ecosystems.     

Global change effects on a mechanistic decomposer food web model

Global change may affect the structure and functioning of decomposer food webs through qualitative changes in freshly fallen litter. We analyzed the predicted effects of a changing environment on a dynamic model of a donor‐controlled natural decomposer ecosystem near Wekerom, the Netherlands. This system consists of fungi, bacteria, fungivores, bacterivores and omnivores feeding on microbiota and litter as well. The model concentrates on carbon and nitrogen flows through the trophic niches that define this decomposer system, and is designed to predict litter masses and abundances of soil biota. For modeling purposes, the quality of freshly fallen leaf litter is defined in terms of nitrogenous and non‐nitrogenous components, of which refractory and labile forms are present. The environmental impacts of elevated CO₂, enhanced UV‐B and eutrophication, each with their own influence on leaf litter quality, are studied. The model predicts steady‐state dynamics exclusively, for all three scenarios. Environmental changes impact most demonstratively on the highest trophic niches, and affect microbiotic abundances and litter decomposition rates to a lesser extent. We conclude that the absence of trophic cascade effects may be attributed to weak trophic links, and that non‐equilibrium dynamics occurring in the system are generally because of encounter rates based on fractional substrate densities in the litter. We set out a number of experimentally testable hypotheses that may improve understanding of ecosystem dynamics.     

Predicting the species abundance distribution using a model food web

A large number of models of the species abundance distribution (SAD) have been proposed, many of which are generically similar to the log-normal distribution, from which they are often indistinguishable when describing a given data set. Ecological data sets are necessarily incomplete samples of an ecosystem, subject to statistical noise, and cannot readily be combined to yield a closer approximation to the underlying distribution. In this paper, we adopt the Webworld ecosystem model to study the predicted SAD in detail. The Webworld model is complex, and does not allow analytic examination of such features; rather, we use simulation data and an approach similar to that of ecologists analysing empirical data. By examining large sets of fully described data we are able to resolve features which can distinguish between models but which have not been investigated in detail in field data. We find that the power-law normal distribution is superior to both the log-normal and logit-normal distributions, and that the data can improve on even this at the high-population cut-off.