Acute resource pulses from periodical cicadas propagate to belowground food webs but do not affect tree performance.

Soil food webs are complex networks that consist of several trophic levels and taxonomic groups including soil microorganisms, protists, nematodes, annelids and soil arthropods. Interactions between and within trophic levels and taxonomic groups regulate important ecosystem functions such as the cycling of carbon (C) and nutrients, with soil microorganisms channeling resources from the base of the food web to higher trophic levels of meso- and macrofauna decomposers and predators. Root exudates and decomposing plant residues are the major basal resources of C, and recent research highlighted the dominant role of root C for forest soil food webs. However, despite the large importance of agroecosystems for the global energy budget, channeling of C and nutrients in arable systems still is little understood. The present thesis focused on the flux of shoot residue- and root-derived C within arable soil food webs. In three field experiments I investigated soil animal community responses and the incorporation of shoot residue- and root-derived C into soil meso- and macrofauna at the species level. In the experiment presented in Chapter 2 I investigated the effects of aboveground resources on abundances and community composition of the soil animal food web of two arable fields planted with wheat and maize, respectively, by adding hackled maize shoot residues to the fields. Addition of shoot residue-derived resources did not affect the soil animal food web, suggesting that aboveground resources are of minor importance for soil animal communities. However, independent of shoot residue addition, the abundance and diversity were much higher and more fluctuating in wheat as compared to maize fields, due to more favourable habitat conditions and more pronounced pulses of root-derived resources in form of root exudates and decomposing root residues in wheat. Taking advantage of the differences in natural 13C/12C signatures of wheat and maize I tracked the incorporation of shoot residue- and root-derived resources into the body tissue of soil animals (Chapter 3). In general, one year after the start of the experiment incorporation of root-derived resources exceeded that of shoot residue-derived resources by a factor of two, highlighting the importance of root-derived resources for arable soil food webs. Furthermore, at higher taxonomic resolution only few soil animal taxa predominantly relied on shoot residue-derived resources, while approximately 30% preferred root-derived resources, and half of the taxa were generalist feeders incorporating both shoot residue- and root-derived resources. In a pulse labelling experiment (Chapter 4) I investigated the short-term incorporation of root-derived C and fertilizer N into the soil animal food web using 13CO2 and K15NO3. Ratios of 13C/12C and 15N/14N were measured in bulk soil, maize shoots, roots and meso- and macrofauna, plus 13C/12C in nematodes and microbial phospholipid fatty acids over a period of 25 days. Both 13C and 15N were incorporated into all compartments of the soil food web, with saprotrophic fungi incorporating by far the highest amounts of 13C, while higher trophic levels, i.e. nematodes and meso- and macrofauna, were less enriched. This suggests a prominent role of saprotrophic fungi in C and nutrient cycling in arable fields, but also that the majority of root-derived C remains locked up at the base of the food web. Further, higher amounts of 13C in predators than decomposers of meso- and macrofauna indicate a prominent role of nematodes for transferring resources to higher trophic levels. Overall, the present thesis highlights the importance of root-derived as compared to shoot residue-derived resources for arable soil food webs, thereby contributing to a better understanding of C and nutrient fluxes in agroecosystems.

Many freshwater ecosystems receive allochthonous resource subsidies from adjacent terrestrial environments. In eastern North American forests, geographic broods of periodical cicadas emerge every 13 to 17 y to breed, and local abundances can sometimes be >300 individuals/m2. Most individuals avoid predation, senesce after breeding, and become a resource pulse for forest ecosystems; some cicada carcasses enter freshwater ecosystems where they represent a detrital resource pulse. Here, we present a 2-part study in which we examined the deposition of cicada detritus into woodland ponds and low-order streams in southwestern Ohio during the emergence of Brood X periodical cicadas. We compared the deposition of nutrients associated with periodical cicada detritus and terrestrial leaf litter into small woodland ponds and low-order streams. We used a laboratory experiment to compare patterns of decomposition and nutrient release of adult periodical cicada carcasses and sycamore leaf litter. Input of periodical cicada detritus to woodland streams and ponds was a function of local cicada emergence densities. Organic C loading to woodland aquatic ecosystems from cicada detritus was substantially less than that from terrestrial leaf litter; however, the higher mass-specific N and P content of cicada material made cicada detritus a relatively important nutrient input. N and P deposited in cicada detritus represented 0.2 to 61% of the N and 0.3 to 50% of the P deposited into woodland aquatic ecosystems via terrestrial leaf litter. Decomposition experiments indicated that cicada detritus was of much higher quality than was sycamore leaf litter; female and male cicada carcasses lost mass at significantly faster rates than sycamore leaves (female k = −0.05/d, male k = −0.04/d, sycamore leaf k = −0.002/d). Release rates of C, N, and P from cicada carcasses were 4, 39, and 150× greater, respectively, than release rates from sycamore leaves. Our study indicates that periodical cicada detritus can represent a substantial allochthonous resource pulse to forested aquatic ecosystems and that cicada detritus is of substantially higher quality than is terrestrial leaf litter. These results suggest that deposition and decomposition of periodical cicada detritus can affect the productivity and dynamics of woodland aquatic ecosystems and that the role of animal-derived resource pulses to ecosystems requires further exploration.

Trophic shifts of generalist consumers can have broad food-web and biodiversity consequences through altered trophic flows and vertical diversity. Previous studies have used trophic shifts as indicators of food-web responses to perturbations, such as species invasion, and spatial or temporal subsidies. Resource pulses, as a form of temporal subsidies, have been found to be quite common among various ecosystems, affecting organisms at multiple trophic levels. Although diet switching of generalist consumers in response to resource pulses is well documented, few studies have examined if the switch involves trophic shifts, and if so, the directions and magnitudes of the shifts. In this study, we used stable carbon and nitrogen isotopes with a Bayesian multi-source mixing model to estimate proportional contributions of three trophic groups (i.e. producer, consumer, and fungus-detritivore) to the diets of the White-footed mouse (Peromyscus leucopus) receiving an artificial seed pulse or a naturally-occurring cicadas pulse. Our results demonstrated that resource pulses can drive trophic shifts in the mice. Specifically, the producer contribution to the mouse diets was increased by 32% with the seed pulse at both sites examined. The consumer contribution to the mouse diets was also increased by 29% with the cicadas pulse in one of the two grids examined. However, the pattern was reversed in the second grid, with a 13% decrease in the consumer contribution with the cicadas pulse. These findings suggest that generalist consumers may play different functional roles in food webs under perturbations of resource pulses. This study provides one of the few highly quantitative descriptions on dietary and trophic shifts of a key consumer in forest food webs, which may help future studies to form specific predictions on changes in trophic interactions following resource pulses.

Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and processes in response to interacting global change factors

Resource pulses affect productivity and dynamics in a diversity of ecosystems, including islands, forests, streams, and lakes. Terrestrial and aquatic systems differ in food web structure and biogeochemistry; thus they may also differ in their responses to resource pulses. However, there has been a limited attempt to compare responses across ecosystem types. Here, we identify similarities and differences in the causes and consequences of resource pulses in terrestrial and aquatic systems. We propose that different patterns of food web and ecosystem structure in terrestrial and aquatic systems lead to different responses to resource pulses. Two predictions emerge from a comparison of resource pulses in the literature: (1) the bottom-up effects of resource pulses should transmit through aquatic food webs faster because of differences in the growth rates, life history, and stoichiometry of organisms in aquatic vs. terrestrial systems, and (2) the impacts of resource pulses should also persist longer in terrestrial systems because of longer generation times, the long-lived nature of many terrestrial resource pulses, and reduced top-down effects of consumers in terrestrial systems compared to aquatic systems. To examine these predictions, we use a case study of a resource pulse that affects both terrestrial and aquatic systems: the synchronous emergence of periodical cicadas (Magicicada spp.) in eastern North American forests. In general, studies that have examined the effects of periodical cicadas on terrestrial and aquatic systems support the prediction that resource pulses transmit more rapidly in aquatic systems; however, support for the prediction that resource pulse effects persist longer in terrestrial systems is equivocal. We conclude that there is a need to elucidate the indirect effects and long-term implications of resource pulses in both terrestrial and aquatic ecosystems.

Although belowground food webs have received much attention, studies concerning microarthropods in nondetrital food webs are scarce. Because adult oribatid mites often number between 250,000–500,000/m2 in coniferous forests, microarthropods are a potential food resource for macroarthropod and vertebrate predators of the forest floor. Although the contribution of microarthropods to aboveground food webs has received little attention, sufficient data concerning macroarthropods and vertebrate predators were available at the Savannah River Site (SRS, Aiken, South Carolina) to construct a food web model of the various trophic interactions. To supplement this analysis, literature of microarthropod predation by arthropods and vertebrates was reviewed. This information was incorporated with the existing data to produce a model for taxa occurring in coniferous forests at the SRS. Because of the diversity and natural history of microarthropod predators, both vertebrate and invertebrate, the resulting web is quite connected and includes transfers to many trophic levels. The diets of arthropods and vertebrates are variable; yet feeding patterns reflect the relative abundance of prey at a place and time. Also, many predators feed on members of their own group. These factors suggest that belowground transfers are deserved of more attention in these and other forest food webs where substantial numbers of detritus feeding invertebrates inhabit the soil/litter interface and are available as prey items. Moreover, this model can be generalized to describe the dynamics of arthropod and vertebrate communities in other coniferous forests. The functioning of terrestrial ecosystems is dependent upon the interrelationships between aboveground and belowground food webs, and transfers of biotic components of the decomposer subsystem to aboveground consumers connect the two subsystems. It is hoped that those consumers traditionally associated with foliage-based food webs be reconsidered, as they may be gaining a proportion of their nutrition from organisms in the detrital pathway.

Temporal and spatial variations of soil nematode assemblages across distinct forest ecosystems

Food web topologies depict the community structure as distributions of feeding interactions across populations. Although the soil ecosystem provides important functions for aboveground ecosystems, data on complex soil food webs is notoriously scarce, most likely due to the difficulty of sampling and characterizing the system. To fill this gap we assembled the complex food webs of 48 forest soil communities. The food webs comprise 89 to 168 taxa and 729 to 3344 feeding interactions. The feeding links were established by combining several molecular methods (stable isotope, fatty acid and molecular gut content analyses) with feeding trials and literature data. First, we addressed whether soil food webs (n = 48) differ significantly from those of other ecosystem types (aquatic and terrestrial aboveground, n = 77) by comparing 22 food web parameters. We found that our soil food webs are characterized by many omnivorous and cannibalistic species, more trophic chains and intraguild‐predation motifs than other food webs and high average and maximum trophic levels. Despite this, we also found that soil food webs have a similar connectance as other ecosystems, but interestingly a higher link density and clustering coefficient. 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. In a second analysis of land‐use effects, we 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. Overall, our study has unravelled some systematic structures of soil food‐webs, which extends our mechanistic understanding how environmental characteristics of the soil ecosystem determine patterns at the community level.

Soil food webs were long considered an ecosystem sink for primary production and a black box of reticulated interactions. Quantification of multiple and changing interactions among consumers and resources within and beyond soil food webs stands up as a major challenge. In this mini-review/opinion paper, I present development of ideas on soil food-web structure focusing on resource omnivory – a central characteristic that is linked to food-web structure and stability. There is plenty of empirical evidence for trophic differentiation among soil invertebrates along different food-web dimensions (food resources, trophic levels, microhabitats, time). This comes along with the pervasive idea of widespread omnivory in soil food webs. I argue that we need to quantitatively assess multiple-resource feeding by soil consumers and related drivers across various taxa and different ecosystem types to come closer to predictions of soil food-web structure and dynamics. At the meta-ecosystem level, cross-ecosystem omnivory (i.e. feeding across energy fluxes from different ecosystems) plays an important role in connecting soil with aboveground and aquatic food webs. Aboveground-belowground studies have been focusing on the interfaces such as the rhizosphere and litter surface. Broader cascading impacts of the energy and organismic fluxes across these interfaces within the recipient ecosystem are, however, less understood. Of particular interest here are connections of vertebrate communities to soil food webs and the central role of soil-borne insects in cross-ecosystem energy exchange. Interactions between soil and aquatic food webs span for dozens to hundreds of meters from the terrestrial-aquatic interface, transferring significant amount of energy and matter between these ecosystems. Consequent changes of the structure and functioning in the recipient ecosystem requires more attention, especially how biodiversity-ecosystem functioning relationships manifest across ecosystems. Continuously developing methods, such as compound-specific isotopic analyses, can facilitate quantification of cross-ecosystem omnivory, helping to understand effects of food-web changes across the ecosystem borders. Overall, I present soil food webs as an open and dynamic pool with multiple cross-ecosystem connections and call for quantitative studies in this direction.

Long-term vegetation restoration promotes the stability of the soil micro-food web in the Loess Plateau in North-west China

Trophic cascades are increasingly being regarded as important features of aboveground and belowground food webs, but the effects of aboveground cascades on soil food webs, and vice versa, remains essentially unexplored. We conducted an experiment consisting of model synthesised communities containing grassland plant and invertebrate species, in which treatments included soil only, soil+plants, soil+plants+aphids, and soil+plants+aphids+predators; predator treatments consisted of the lacewing Micromus tasmaniae and ladybird beetle Coccinella undecimpunctata added either singly or in combination. Addition of Micromus largely reversed the negative effects of aphids on plant biomass, while both of the predator species caused large changes in the relative abundances of dominant plant species. Predators of aphids also affected several components of the belowground subsystem. Micromus had positive indirect effects on the primary consumer of the soil decomposer food web (microflora), probably through promoting greater input of basal resources to the decomposer subsystem. Predator treatments also influenced densities of the tertiary consumers of the soil food web (top predatory nematodes), most likely through inducing changes in plant community composition and therefore the quality of resource input to the soil. The secondary consumers of the soil food web (microbe‐feeding nematodes) were, however, unresponsive. The fact that some trophic levels of the soil food web but not others responded to aboveground manipulations is explicable in terms of top‐down and bottom‐up forces differentially regulating different belowground trophic levels. Addition of aphids also influenced microbial community structure, promoted soil bacteria at the expense of fungi, and enhanced the diversity of herbivorous nematodes; in all cases these effects were at least partially reversed by addition of Micromus. These results in tandem point to upper level consumers in aboveground food webs as a potential driver of the belowground subsystem, and provide evidence that predator‐induced trophic cascades aboveground can have effects that trickle through soil food webs.

Resource pulses provide short-duration, large-magnitude resources that influence ecosystem productivity, structure, and function. However, little empirical evidence is available evaluating how lake ecosystems respond to varying resource pulse magnitudes. We used mesocosms inoculated with primary producers and consumers to compare resource pulses of 0, 25, 50, 100, and 250 kg/ha of common carp Cyprinus carpio to simulate post-winterkill fish biomass in shallow lakes. Ecosystem responses to a gradient of resource pulse magnitudes typically had the greatest effects on nutrient availability and primary producers with fewer detectable effects for consumers. Total phosphorus, total Kjeldahl nitrogen, nitrate, phytoplankton, and periphyton productions increased as a result of the resource pulse, whereas copepods were the only consumer observed to elicit a positive response. In contrast, pulse magnitude had little effect on ecosystem stability, trophic position, or energy flow, potentially due to the low biomass of pulse magnitudes introduced. Resource pulses of moderate or large size generally increased nutrient availability and primary productivity while decreasing water clarity, suggesting that resource pulses can be an important factor influencing shallow eutrophic lakes but that effects may not be proportional to pulse size.

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.

Energetics and Stability in Belowground Food Webs

Abiotic soil properties, plant community composition, and herbivory all have been reported as important factors influencing the composition of soil communities. However, most studies thus far have considered these factors in isolation, whereas they strongly interact in the field. Here, we study how grazing by vertebrate herbivores influences the soil nematode community composition of a floodplain grassland while we account for effects of grazing on plant community composition and abiotic soil properties. Nematodes are the most ubiquitous invertebrates in the soil. They include a variety of feeding types, ranging from microbial feeders to herbivores and carnivores, and they perform key functions in soil food webs. Our hypothesis was that grazing affects nematode community structure and composition through altering plant community structure and composition. Alternatively, we tested whether the effects of grazing may, directly or indirectly, run via changes in soil abiotic properties. We used a long-term field experiment containing plots with and without vertebrate grazers (cattle and rabbits). We compared plant and nematode community structure and composition, as well as a number of key soil abiotic properties, and we applied structural equation modeling to investigate four possible pathways by which grazing may change nematode community composition. Aboveground grazing increased plant species richness and reduced both plant and nematode community heterogeneity. There was a positive relationship between plant and nematode diversity indices. Grazing decreased the number of bacterial-feeding nematodes, indicating that in these grasslands, top-down control of plant production by grazing leads to bottom-up control in the basal part of the bacterial channel of the soil food web. According to the structural equation model, grazing had a strong effect on soil abiotic properties and plant community composition, whereas plant community composition was the main determinant of nematode community composition. Other pathways, which assumed that grazing influenced nematode community composition by inducing changes in soil abiotic properties, did not significantly explain variation in nematode community composition. We conclude that grazing-induced changes in nematode community composition mainly operated via changes in plant community composition. Influences of vertebrate grazers on soil nematodes through modification of abiotic soil properties were of less importance.