Deriving microbial food web structure by maximizing entropy production over variable timescales

Although microorganisms are the primary drivers of biogeochemical cycles, the structure and functioning of microbial food webs are poorly studied. This is the case in Sphagnum peatlands, where microbial communities play a key role in the global carbon cycle. Here, we explored the structure of the microbial food web from a Sphagnum peatland by analyzing (1) the density and biomass of different microbial functional groups, (2) the natural stable isotope (δ(13)C and δ(15)N) signatures of key microbial consumers (testate amoebae), and (3) the digestive vacuole contents of Hyalosphenia papilio, the dominant testate amoeba species in our system. Our results showed that the feeding type of testate amoeba species (bacterivory, algivory, or both) translates into their trophic position as assessed by isotopic signatures. Our study further demonstrates, for H. papilio, the energetic benefits of mixotrophy when the density of its preferential prey is low. Overall, our results show that testate amoebae occupy different trophic levels within the microbial food web, depending on their feeding behavior, the density of their food resources, and their metabolism (i.e., mixotrophy vs. heterotrophy). Combined analyses of predation, community structure, and stable isotopes now allow the structure of microbial food webs to be more completely described, which should lead to improved models of microbial community function.

Microbial food web organisms are at the base of the functioning of pelagic ecosystems and support the whole marine food web. They are very reactive to environmental changes and their interactions are modified in response to different productive periods such as phytoplankton bloom and non-bloom as well as contrasted climatic years. To study ecological associations, identify potential interactions between microorganisms and study the structure of the microbial food web in coastal waters, a weekly monitoring was carried out in the Thau Lagoon on the French Mediterranean coast. The monitoring lasted from winter to late spring during two contrasting climatic years, a typical Mediterranean (2015) and a year with an extreme warm winter (2016). Correlation networks comprising 110 groups/taxa/species were constructed to characterize potential possible interactions between the microorganisms during bloom and non-bloom periods. Complex correlation networks during the bloom and dominated by negative intraguild correlations and positive correlations of phytoplankton with bacteria. Such pattern can be interpreted as a dominance of competition and mutualism. In contrast, correlation networks during the non-bloom period were less complex and mostly dominated by tintinnids associations with bacteria mostly referring to potential feeding on bacteria, which suggests a shift of biomass transfer from phytoplankton-dominated food webs during bloom to more bacterioplankton-based food webs during non-bloom. Inter-annual climatic conditions significantly modified the structure of microbial food webs. The warmer year favored relationships among smaller group/taxa/species at the expense of large phytoplankton and ciliates, possibly due to an intensification of the trophic cascade with a potential shift in energy circulation through microbial food web. Our study compares a typical Mediterranean spring with another mimicking the prospected intensification of global warming; if such consideration holds true, the dominance of future coastal marine ecosystems will be shifted from the highly productive herbivorous food web to the less productive microbial food web.

Using hierarchical stable isotope to reveal microbial food web structure and trophic transfer efficiency differences during lake melt season

Determining how microbial communities organize and function at the ecosystem level is essential to understanding and predicting how they will respond to environmental change. Mathematical models can be used to describe these communities, but properly representing all the biological interactions in extremely diverse natural microbial ecosystems in a mathematical model is challenging. We examine a complementary approach based on the maximum entropy production (MEP) principle, which proposes that systems with many degrees of freedom will likely organize to maximize the rate of free energy dissipation. In this study, we develop an MEP model to describe biogeochemistry observed in Siders Pond, a phosphate limited meromictic system located in Falmouth, MA that exhibits steep chemical gradients due to density-driven stratification that supports anaerobic photosynthesis as well as microbial communities that catalyze redox cycles involving O, N, S, Fe and Mn. The MEP model uses a metabolic network to represent microbial redox reactions, where biomass allocation and reaction rates are determined by solving an optimization problem that maximizes entropy production over time, and a 1D vertical profile constrained by an advection-dispersion-reaction model. We introduce a new approach for modeling phototrophy and explicitly represent oxygenic photoautotrophs, photoheterotrophs and anoxygenic photoautotrophs. The metabolic network also includes reactions for aerobic organoheterotrophic bacteria, sulfate reducing bacteria, sulfide oxidizing bacteria and aerobic and anaerobic grazers. Model results were compared to observations of biogeochemical constituents collected over a 24 hour period at 8 depths at a single 15 m deep station in Siders Pond. Maximizing entropy production over long (3 day) intervals produced results more similar to field observations than short (0.25 day) interval optimizations, which support the importance of temporal strategies for maximizing entropy production over time. Furthermore, we found that entropy production must be maximized locally instead of globally where energy potentials are degraded quickly by abiotic processes, such as light absorption by water. This combination of field observations and modeling results indicate that natural microbial systems can be modeled by using the maximum entropy production principle applied over time and space using many fewer parameters than conventional models.

Food web structure and energy flux dynamics, but not taxonomic richness, influence microbial ecosystem functions in a Sphagnum-dominated peatland

Natural ecosystems comprise an innumerable amount of different organisms. These organisms are not separated, they interact and depend on each other. Today’s ecosystems are facing an enormous decline in biodiversity due to human impacts with thus far unknown consequences. One key objective of ecological research is to understand the mechanisms generating and maintaining this incredible amount of diversity. However, comprehensive analyses of natural ecosystems are impeded by their complexity and diversity. Food webs, therefore, provide an excellent tool to analyze the complexity of ecosystems. They depict the system‘s diversity and species interactions in a condensed form. Furthermore, food-web structure can help to predict the interaction strengths between species and the energy pathways through the system. In my thesis, I use food web structure to analyze structural properties which separate food webs from other network types and furthermore I investigate generalities and differences of food-web structure across different ecosystems. 
\nOne of the most important ecosystems is the soil ecosystem, as it provides the base for aboveground productivity. However, detailed soil food webs are scarce. In chapter 2, I assembled the complex food webs of 48 forest soil communities and analyzed if soil food webs differ in their topological parameters from those of other ecosystems. I found that soil food webs are characterized by a higher number of omnivorous and cannibalistic species. Moreover, they comprise more trophic chains and intraguild-predation motifs than food webs from other ecosystems. Finally, soil food webs showed high average and maximum trophic levels. These differences in network structure to other ecosystem types may be a result of ecosystem-specific constraints on hunting and feeding characteristics of the species that emerge as network parameters at the food-web level. Despite these differences, soil food webs showed the same scaling of their properties with connectance and size. In a second analysis of land-use effects, I found significant but only small differences of soil food web structure between different beech and coniferous forest types, which may be explained by generally strong selection effects of the soil that are independent of human land use. This study has unravelled systematic structures of soil food-webs, extending our mechanistic understanding how their environmental characteristics determine patterns at the community level. Additionally, I have shown that the general scaling laws also apply for soil food webs.
\nIn addition to purely topological properties, I analyzed another important aspect of food webs. The distributions of body masses and degrees across species are key determinants of food-web structure and dynamics. In chapter 3, I analyzed body masses of species and their systematic distributions across food-web structure. In particular, allometric degree distributions combine both aspects in the relationship between degrees and body masses. They are of critical importance for the stability of complex ecological networks. I used an entirely novel global body-mass database including food-web structures of four different ecosystem types to analyze body-mass distributions, cumulative degree distributions, and allometric degree distributions regarding differences among ecosystem types. My results demonstrate some general patterns across ecosystems: the body masses are either roughly log-normally (terrestrial and stream ecosystems) or multimodally (lake and marine ecosystems) distributed, and most networks exhibit exponential cumulative degree distributions except stream networks that most often possess uniform degree distributions. Additionally, with increasing species body masses we found significant decreases in vulnerability in 70% of the food webs and significant increases in generality in 80% of the food webs. Overall, these analyses document striking generalities in the body-mass and degree structure across ecosystem types as well as surprising exceptions (uniform degree distributions in stream ecosystems). This suggests general constraints of body masses on the link structure of natural food webs irrespective of ecosystem characteristics. 
\nWhile I revealed general patterns of food-web topology in chapter 2 and 3, I investigated the drivers of these general patterns in chapter 4. Therefore, I analyzed the influence of different external factors on community (beta diversity) and food-web structure. Two main theoretical bodies explain β-diversity, the niche theory and neutral theory. However, neutral theory predicts only distributions for trophically identical species, whereas influences of local niches or neutral effects on food-web structure as a crucial part of the multitrophic structure of ecosystems are not taken into account. In chapter 4, I therefore analyzed the effects of spatial distance and environmental dissimilarity on the species dissimilarity (beta diversity) and food web dissimilarity (structural dissimilarity) of multitrophic forest communities. I showed that the mechanisms proposed by neutral theory can adequately predict the beta diversity of multitrophic species communities. Furthermore, food-web structure was robust and affected neither by spatial distance (random dispersal, neutral theory) nor by environmental filtering (niche theory). I additionally analyzed model food webs (random and niche topology) and compared their dissimilarities to empirical food webs. The highest dissimilarity was reached by random food webs whereas niche model food webs were in between and the lowest distances were expressed by empirical food webs. Further, random food webs displayed the highest mean trophic level (115), while niche model food webs showed lower (5) and empirical food webs the lowest (4) mean trophic level values. Hence, food-web structure appears to be energetically optimized with local species adapted to energetic niches within the food web while species identity within these niches remains random. This suggests that different species could be adapted to the same energetic niches and, while following random drift, still assemble into similar food web structures.
\nAltogether, the results of this thesis demonstrate the practicality of food-web structure in unravelling generalities across different ecosystems. Furthermore, food-web structure explains species distributions across the environment and provides additional important information on the ecosystem. 
\nThe observed generalities indicate constraints on food-web structure. The allometric degree distributions demonsrate such constraints on food-web structure by distributing the links in dependence of the species body masses. Finally, my results from chapter 4 indicate that, additionally to global topological constraints, local communities have to meet certain energetic constraints to explain the similarity found across food webs.

Relationships among picoplankton, protozoa, phytoplankton, plant nutrients, lake type, drainage basin morphology and land cover were studied in 45 water bodies in South Island, New Zealand that ranged from large, deep, ultra-oligotrophic lakes to shallow, macrophyte-dominated ponds and swamps. The biomasses of most heterotrophic components of the pelagic microbial food webs were positively related to phytoplankton and features of the drainage basin that enhanced nutrient input, and imply strong resource-driven structuring of pelagic microbial food webs. Prokaryotic picophytoplankton biomass was negatively related to indices of eutrophication, and the picoautotroph contribution to total microbial food web biomass declined with increasing total phosphorus concentration from 16.5% in deep lakes to <0.02% in swamps and ponds. Biomass ratios of (picoplankton plus protozoa):phytoplankton ranged from 40:60 in swamps and ponds to >70:30 in deep lakes, and indicate the potential importance of microbial food webs in carbon transfer to higher trophic levels in deep, less productive lakes. Strong relationships exist between land use in the catchment and pelagic microbial food web structure and biomass across a wide range in size and trophic state of water bodies in heterogeneous landscapes.

Microbial food web (MFW) in the seawater encompasses the smallest organisms: viruses, autotrophic prokaryotes and heterotrophic prokaryotes (HP), nanoflagellates, eukaryotic phytoplankton and ciliates. For many years, scientists investigated the MFW structure differences in distinct water masses. However, the MFW structure seasonal variation in coastal areas remains poorly documented. In this study, we report on the seasonal and spatial variations of the MFW structure in the temperate Sanggou Bay in four successive seasons, from spring to winter. With a temperature increase from 1.90 to 24.20C, HP biomass increased from 3.77 to 135.77 μg C dm-3, almost covering the whole variation range for the global ocean. The autotrophic (AUTO) components, including Synechococcus (SYN), phototrophic picoeukaryotes (PEUK) and pigmented nanoflagellates (PNF), exhibited biomass variation ranges as large as previously reported. The MFW structure seasonal variation was driven by MFW relative biomasses (biomass ratios of MFW components to HP). With the increase of HP biomass, PNF and PEUK relative biomasses increased more rapidly than those of other groups while that of ciliates slightly decreased. The HETE:AUTO (biomass ratio of heterotroph to autotroph organisms) decreased with temperature, it was 1 in other seasons. Cluster analyses distinguished Inside Bay and Outside Bay on the basis of hydrological characteristics. Consistently, the two subdivisions of Sanggou Bay exhibited different MFW structures as well as distinct tintinnid communities. The main MFW structure difference between Inside and Outside Bay was the biomass ratios of AUTO components to HP. Our results showed that the variations of autotrophic component biomass ratios relative to HP were the main factor responsible for the MFW structure seasonal variation. The spatial difference in MFW structure as well as in tintinnid taxonomic composition between Inside and Outside Bay was linked to the semienclosed nature of the Bay that does not favour efficient mixing with outside Yellow Sea waters.

Metabolism Predicts Ecological Response to Warming

Shallow, hypertrophic Lake Sobygard is characterized by strong fluctuations in the plankton community structure over short time scales, and cascading predation effects from higher to lower trophic levels. We examined the coupling between the classical and microbial food web for a 1 month period, during which the typical zooplankton summer succession from rotifers (mainly Brachionus spp.) to cyclopoid copepods and daphnids occurred. In addition to the analysis of the plankton succes- sion, we performed mesocosm experiments, comparing the microbial community structure in treat- ments with and without metazooplankton. We focused on the development of different functional groups within the microbial food web: total heterotrophic bacteria, filamentous bacteria (as grazing- resistant forms), prokaryotic and eukaryotic, autotrophic picoplankton (pAPP and eAPP), hetero- trophic nanoflagellates (HNF) and ciliates. During the first experiment, the metazooplankton was dominated by rotifers which exerted only moderate top-down control on small ciliates, HNF and APP. Cascading predation effects were visible after the collapse of the rotifer population; enhanced protozoan grazing resulted in a decrease in single-celled bacteria and an increase in filamentous bacteria. During the second experiment, characterized by dominance of Cyclops vicinus, strong alter- ations in the microbial food web structure occurred. The most obvious effects were an efficient predation control of planktonic ciliates by copepods and a shift of the picoplankton towards fila- mentous bacteria and a very high biomass of pAPP, which we interpret as a result of enhanced protozoan grazing pressure on bacterioplankton. After the peak in cyclopoids, Daphnia spp. became the dominant zooplankton taxa which resulted in the well known strong predation effects on all microbial components. The two experiments confirm that metazooplankton species composition is an important structuring factor for the microbial food web. Two functional groups deserve special attention: filamentous bacteria and pAPP. Filamentous bacteria, which attained nearly 50% of total heterotrophic bacterial biomass during the second period, seem to be a sensitive indicator of the overall planktonic food web structure and showed significant responses in the enclosures. With a special staining procedure, we analysed the abundance of filamentous bacteria in Lugol-fixed samples collected since 1984 during periods when either daphnids, cyclopoids or rotifers dominated the meta- zooplankton community. On average, high abundance of filaments was always associated with Cyclops-dominated situations, low numbers with Daphnia dominance and high, but rather variable numbers with rotifer dominance. A general close correlation of pAPP with filamentous bacteria might indicate that pAPP also possess a reduced edibility for protozoans.

Nonpoint source pollution entering rivers will pollute water quality, degrading the health of aquatic ecosystems. However, owing to the lack of quantitative research on the effects of nonpoint source pollution on the structure of aquatic food webs, there is a lack of quantitative basis for river management. Nonpoint source pollution is not only difficult to control effectively, but also the success rate of water ecological restoration projects is low. With the increasing proportion of nonpoint source pollution in water environmental problems, it is urgent to quantitatively assess and predict the impact of nonpoint source pollution on the structure of food webs. Therefore, this thesis presents a method for quantitatively assessing and predicting the impact of nonpoint source pollution on the structure of food webs through using fuzzy clustering to screen the typical points of the impact of nonpoint source pollution, then using canonical correspondence analysis (CCA) and partial least squares regression analysis to comprehensively filtrate the driving factors affect food web that results in nonpoint source pollution, and then determining the impact of each driving factor on the structure of food webs. Finally, the change trend of food web structure is predicted. The results show that (1) the driving factors that the nonpoint source pollution that affects the food web structure is NH3‐N and chemical oxygen demand (COD). The increase in NH3‐N and COD promotes the growth of phytoplankton, causing the change of the primary productivity of the ecosystem, and ultimately changes the entire food web structure; (2) NH3‐N and COD affect the stability, maturity, connectivity and complexity of the aquatic food web structure. The increase of NH3‐N increases the connectivity and maturity of the food web structure but reduces complexity and stability; the increase of COD increases the connection of the food web structure, while reducing the other three indicators; (3) in some areas with good water quality, aquatic species diversity is high, the relationship of interspecies dietary is complex, food web structure level index is high and the structure of food web is stable. The food web structure in the rainy season will be better than that in the dry season. In some areas with severe water pollution and poor food web structure, the ability of the food web to resist external interference is weak. The food web structure in the rainy season will be worse than that in the dry season owing to rainfall into the river. The methods and conclusions in this treatise can provide a reliable and quantitative scientific basis for river ecosystem management and ecosystem restoration and can improve the success rate of ecological restoration projects.

Spatio-temporal reproducibility of the microbial food web structure associated with the change in temperature: Long-term observations in the Adriatic Sea

Microbial food web structure in the Arabian Sea: a US JGOFS study

Simple SummaryIn terrestrial natural ecosystems, more complex and diverse networks of plant–insect primary consumers and their predators are often more productive, stable, and resilient. Plant diversity often positively correlates to the diversity of phytophagous insects and their natural enemies generating multitrophic interactions with changing outcomes (bottom-up effects). The use of cover crops can promote natural enemy populations and their temporal synchronization with a target pest, resulting in greater pest control. Therefore, changes in the habitat conditions can alter food webs. In agroecosystems, characteristics of the food trophic webs, as connectance, measured as the proportion of realized links in the network, could be linked to the efficiency of pest control. In this study, we evaluated how the use of oat cover crops affects composition and structure in the aphid–parasitoid–hyperparasitoid food webs of plum orchards with different habitat management contexts: plums with inter-rows of oats as a cover crop (OCC) and plums with inter-rows with spontaneous vegetation (SV). Quantitative food web metrics differed significantly among treatments showing a higher generality, vulnerability, interaction evenness, and linkage density in SV, while OCC presented a higher degree of specialization.By increasing plant diversity in agroecosystems, it has been proposed that one can enhance and stabilize ecosystem functioning by increasing natural enemies’ diversity. Food web structure determines ecosystem functioning as species at different trophic levels are linked in interacting networks. We compared the food web structure and composition of the aphid– parasitoid and aphid-hyperparasitoid networks in two differentially managed plum orchards: plums with inter-rows of oats as a cover crop (OCC) and plums with inter-rows of spontaneous vegetation (SV). We hypothesized that food web composition and structure vary between OCC and SV, with network specialization being higher in OCC and a more complex food web composition in SV treatment. We found a more complex food web composition with a higher species richness in SV compared to OCC. Quantitative food web metrics differed significantly among treatments showing a higher generality, vulnerability, interaction evenness, and linkage density in SV, while OCC presented a higher degree of specialization. Our results suggest that plant diversification can greatly influence the food web structure and composition, with bottom-up effects induced by plant and aphid hosts that might benefit parasitoids and provide a better understanding of the activity, abundance, and interactions between aphids, parasitoids, and hyperparasitoids in plum orchards.

Predicting the effects of dissolved organic matter (DOM) on pelagic food webs can be difficult because DOM modifies water column optics and can have contrasting effects on species across trophic levels. We combined large mesocosm, smaller‐scale experiments and autoregressive modeling driven bu DOC concentration or DOM optical quality (colored DOM, or CDOM, measured as DOC‐specific absorbance at 320 nm, SUVA320) to assess how heterotrophic and phototrophic microbial populations were altered in a temperate oligotrophic lake. DOM additions yielded DOC concentrations of 1.6 mg L−1 (control) 2.5 mg L−1, 3.0 mg L−1, and 4.3 mg L−1. Primary (PP) and bacterial (BP) production as well as heterotrophic and autotrophic protist abundances were stimulated in the higher DOM additions. BP responded rapidly to DOM additions, but unlike PP, returned to the level of controls within 2–7 d. A bioassay showed that the DOM was a nitrogen source for phytoplankton. The two models revealed that BP and edible phytoplankton were stimulated by CDOM (SUVA320), but only BP was stimulated by DOC concentration. Ultraviolet radiation (UV) inhibited protists in both models, but stimulated edible phytoplankton only in the SUVA320 model runs. These results suggest that in transparent oligotrophic lakes large influxes of terrestrial (high SUVA320) DOM will stimulate the microbial food web by providing a nutrient subsidy to bacteria and reducing exposure of protists to damaging UV. Nutrients associated with moderate DOM input may also stimulate PP relative to BP, as was observed in these and other experiments, rather than causing an overall system shift toward heterotrophy.