The Contribution of Microarthropods to Aboveground Food Webs: A Review and Model of Belowground Transfer in a Coniferous Forest

Acute resource pulses can have dramatic legacies for organismal growth, but the legacy effects of resource pulses on broader aspects of community structure and ecosystem processes are less understood. Mass emergence of periodical cicadas (Magicicada spp.) provides an excellent opportunity to shed light on the influence of resource pulses on community and ecosystem dynamics: the adults emerge every 13 or 17 years in vast numbers over much of eastern North America, with a smaller but still significant number becoming incorporated into forest food webs. To study the potential effects of such arthropod resource pulse on primary production and belowground food webs, we added adult cicada bodies to the soil surface surrounding sycamore trees and assessed soil carbon and nitrogen concentrations, plant-available nutrients, abundance and community composition of soil fauna occupying various trophic levels, decomposition rate of plant litter after 50 and 100 days, and tree performance for 4 years. Contrary to previous studies, we did not find significant cicada effects on tree performance despite observing higher plant-available nutrient levels on cicada addition plots. Cicada addition did change the community composition of soil nematodes and increased the abundance of bacterial- and fungal-feeding nematodes, while plant feeders, omnivores, and predators were not influenced. Altogether, acute resource pulses from decomposing cicadas propagated belowground to soil microbial-feeding invertebrates and stimulated nutrient mineralization in the soil, but these effects did not transfer up to affect tree performance. We conclude that, despite their influence on soil food web and processes they carry out, even massive resource pulses from arthropods do not necessarily translate to NPP, supporting the view that ephemeral nutrient pulses can be attenuated relatively quickly despite being relatively large in magnitude.

Size-structured food webs form integrated trophic systems where energy is channeled from small to large consumers. Empirical evidence suggests that size structure prevails in aquatic ecosystems, whereas in terrestrial food webs trophic position is largely independent of body size. Compartmentalization of energy channeling according to size classes of consumers was suggested as a mechanism that underpins functioning and stability of terrestrial food webs including those belowground, but their structure has not been empirically assessed across the whole size spectrum. Here we used stable isotope analysis and metabolic regressions to describe size structure and energy use in eight belowground communities with consumers spanning 12 orders of magnitude in living body mass, from protists to earthworms. We showed a negative correlation between trophic position and body mass in invertebrate communities and a remarkable nonlinearity in community metabolism and trophic positions across all size classes. Specifically, we found that the correlation between body mass and trophic level is positive in the small-sized (protists, nematodes, arthropods below 1 μg in body mass), neutral in the medium-sized (arthropods of 1 μg to 1 mg), and negative in the large-sized consumers (large arthropods, earthworms), suggesting that these groups form compartments with different trophic organization. Based on this pattern, we propose a concept of belowground food webs being composed of (1) size-structured micro-food web driving fast energy channeling and nutrient release, for example in microbial loop; (2) arthropod macro-food web with no clear correlation between body size and trophic level, hosting soil arthropod diversity and subsidizing aboveground predators; and (3) "trophic whales," sequestering energy in their large bodies and restricting its propagation to higher trophic levels in belowground food webs. The three size compartments are based on a similar set of basal resources, but contribute to different ecosystem-level functions and respond differently to variations in climate, soil characteristics and land use. We suggest that the widely used vision of resource-based energy channeling in belowground food webs can be complemented with size-based energy channeling, where ecosystem multifunctionality, biodiversity, and stability are supported by a balance across individual size compartments.

Food webs

Temporal and spatial heterogeneity of trophic interactions within below-ground food webs

Some ecological ideas developed gradually and only gained coherence and details after they had become commonplace. The history of two interrelated ideas, food chains and food webs, is an example of a gradual, cumulative history. Here is a brief survey of these concepts from about 1700 to 1970 (Fig. 1). The earliest identified food chains seem to have concerned hyper-parasitism (Egerton 2005, 2006a), which students of insects discovered in the later 1600s. But it was entrepreneurial naturalist Richard Bradley (Egerton 2006b) who generalized the concept (Bradley 1718, part 3:60–61): …Insects which prey upon others are not without some others of lesser Rank to feed upon them likewise, and so to Infinity; for that there are Beings subsisting, which are not commonly visible may be easily demonstrated…in a Microscope. This was turned into verse by Jonathan Swift (Fig. 2) in 1733 (lines 341–344). So, Nat'ralists observe, a Flea Hath smaller Fleas that on him prey, And these have smaller yet to bite 'em, And so proceed ad infinitum. In Bradley's account, food chains illustrated the balance of nature (Egerton 1973:333–335). Swift was a prominent literary figure who had a general interest in science, but his lines on fleas were meant as a swipe at lesser poets. Neither Bradley nor Swift provided an illustration, so we can help them out with this one from Alfred Elliott's 1957 Zoology textbook (Fig. 3), though Elliott borrowed the idea for the central figures of fleas from Robert Hegner's 1938 book, Big Fleas Have Little Fleas, or Who's Who Among the Protozoa. Carl Linnaeus, in an ecologically important essay, "The Economy of Nature" (Linnaeus [Latin] 1749; [English] 1775:114, 1977), briefly itemized the stages of two food chains, one terrestrial, one aquatic (Egerton 2007a). There are likely other naturalists between Linnaeus and Darwin who reported on food chains, but attracted little notice. Darwin may be the first to report a food web, occasioned by the Beagle's stopover at the rather barren island of St. Paul on 16 February 1832. He gave its location as 0° 58′ north latitude and 29° 15' west longitude, and 540 miles from America. He found only two species of birds, the booby (a gannet) and the Noddy Tern. The latter built a simple nest with seaweed. Then follows his food web (Darwin 1839:10): By the side of many of these nests a small flying-fish was placed; which, I suppose, had been brought by the male bird for its partner…quickly a large and active crab (Craspus), which inhabits the crevices of the rock, stole the fish from the side of the nest, as soon as we had disturbed the birds. Not a single plant, not even a lichen, grows on this island; yet it is inhabited by several insects and spiders. The following list completes, I believe, the terrestrial fauna: a species of Feronia and an acarus, which must have come here as parasites on the birds; a small brown moth, belonging to a genus that feeds on feathers; a staphylinus (Quedius) and a woodlouse from beneath the dung; and lastly, numerous spiders, which I suppose prey on these small attendants on, and scavengers of the waterfowl. After reading this account, Rear-Admiral William Symonds told Darwin that he had seen at St. Paul crabs drag young birds from nests and eat them. Darwin added his information to this passage in the second edition (1845) of his book on the voyage of the Beagle (Edwards 1985:34). In The Origin of Species (1859:73–74), Darwin reported the most famous example of a food chain in the scientific literature (Fig. 4). It is in chapter 3 on the "Struggle for existence," and involves humble bees (called "bumble bees" in America) pollinating red clover; though some bees were eaten by field mice, the mice, in turn, were kept in check by domestic cats. Darwin speculated that if it were not for the cats, the mice would decimate the bees, and the clover would go unpollinated, since only humble bees pollinate clover. A later, unknown commentator extended this chain further (Milne and Milne 1966:6) by suggesting that old maids commonly kept cats, that clover-fed cattle were eaten by British seamen who protected the British Empire, and that if it were not for old maids, the British Empire would fall! In other words, Darwin's food chain became a biological version of Englishman George Herbert's well-known admonition (1640): For want of a nail the shoe is lost, For want of a shoe the horse is lost, For want of a horse the rider is lost. In America, this admonition is attributed to Ben Franklin, who borrowed it without acknowledgement for Poor Richard's Almanac (1757). But getting back to Darwin's food chain, in 1947 W. L. McAtee pointed out that Darwin's food chain dynamic lacks full validity, since we now know that honey bees also pollinate red clover and that humble bees often appropriate mouse holes, so humble bees and mice have an ambiguous relationship. In Darwin's defense, he heavily depended on H. W. Newman's 1850–1851 study "On the habits of the Bombinatrices" (Darwin 1975:183). The next discussion of note for our purposes is from a remarkable German zoologist, Karl Semper. In 1877, he gave 12 lectures at the Lowell Institute in Boston, published simultaneously in English and German editions in 1881. The English title is Animal Life as Affected by the Natural Conditions of Existence. This book was the first detailed synthesis of animal ecology. In a discussion of the food of herbivores and carnivores (Semper 1881:51–52), he pointed out that when herbivores transform vegetation into flesh, there is a loss of mass due to oxidation of organic material, and that the same is true when carnivores transform the flesh of their prey into their own flesh. To illustrate this, he arbitrarily assumed a 10 to 1 ratio of food to flesh. One thousand units of plant food could only support 100 units of a herbivore, and those 100 units of herbivore could only support 10 units of a carnivore. Although his book has 106 illustrations, this generalized food chain was not illustrated. However W. E. Pequegnat's diagram (Fig. 5) from Scientific American (1958:86) captures Semper's concept, even to the point of using a 10 to 1 ratio. Semper wrote at a time when there was little quantified thinking in natural history. He had first trained as an engineer and then as a physiologist (Mayr 1975), and that background came to the fore in this discussion. Although his book was widely read, apparently no one carried this line of quantitative thinking any further in the 1880s or 1890s. We are used to seeing food chains or webs diagrammed. The advantages are obvious: they provide a visual panorama of detailed information. The early history of such diagrams is elusive. The bibliography on food chains and webs that Allee, Emerson, Park, Park, and Schmidt compiled (1949:514) can assist in the search. However, they did not discover the earliest ones now known, published in 1880 by Lorenzo Camerano, which are reprinted in an English translation of his article (1994:377–378). Since Camerano's two diagrams do not resemble any known from later zoologists, it seems likely that he did not have much, if any, influence on later diagrams. Joel Cohen (1994:353–355) suggests that Camerano was influenced by diagrams for other purposes in books by Darwin and by Hermann Helmholtz, though Camerano's diagrams do not resemble theirs. Like Semper's, Camerano's food webs are generalized rather than specific. The earliest specific food web I have found (Fig. 6) is on "The boll weevil complex," published in 1912 by Pierce, Cushman, and Hood in a USDA Bulletin. Their motive was to promote bowl weevil eradication—by encouraging its predators and parasites. Theirs may not have been the first specific diagram published, because others appeared about the same time in different biological specializations, where it is unlikely that the members of one specialization were reading the literature of other specializations. The following year, University of Illinois animal ecologist Victor E. Shelford (Fig. 7; photo, Croker 1991) published Animal Communities in Temperate America as Illustrated in the Chicago Region, which contained diagrams of both aquatic (Fig. 8) and land food webs (Fig. 9). There is no reason to suspect that he was influenced by the boll weevil diagram of 1912. Shelford used both of his diagrams to show how the community tends toward equilibrium, although the terrestrial community was more complex than the aquatic community, and consequently its equilibrium was more precarious. Shelford became a leading American animal ecologist (Croker 1991); his book was reprinted in 1937 and 1977. The earliest known food web diagram for a marine community was drawn by Danish fishery biologist Johannes Petersen (Fig. 10) in "A preliminary result of the investigations on the valuation of the sea"1915. He studied the Kattegat region of shallow water between eastern Denmark and Sweden (Fig. 11), an area with maximum length of 150 miles and maximum width of 90 miles. Significantly, he attempted to establish the annual productivity for this region, and his diagram indicates the thousands of tons of each group of organisms, with both a number and a proportioned rectangle (Fig. 12). In the text he stated that the eel-grass (Zostera marina) figure of 24,000,000 tons represents only the amount produced in the summer, and that the annual production is twice that. Presumably, all the other figures are annual production and not just summer production. The tons of plaice and cod are the actual commercial catch of those fish from International Fishery Statistics for 1910, and that was possibly true also for the tons of herring given, though he did not say so. The numbers given for other animals seem to be estimates. Although he indicated on his diagram that herring fed on plankton, he thought plankton was much less important than Zostera as a foundation for this food web. He concluded that the Kattegat had a "very unfavourable proportion between producers and consumers"(Petersen 1915:32). What he meant by this seems to be indicated by the following sentence in which he stated that carp ponds have "even without artificial feeding, given a yield of fish per hectare several times greater than that of the Kattegat." Petersen reproduced the same diagram with minor alterations in his final report, "The sea bottom and its production of fish-food" (1918:23). His colleague, H. Blegvad, also used rectangles in his diagram of "Food of fish and principal animals in Nyborg Fjord" (1916:24) (Fig. 13) but without attempting to represent precise quantities. However, he did give quantitative data in the text of his article, which provided some sense of the quantities of organisms involved at each level. In the same year as Blegvad, the American zoologist Harold Sellers Colton published what Jonathan A. D. Fisher calls (2005:145) "possibly the first intertidal marine food web ever illustrated." It is in Colton's article on a carnivorous snail, Thais lapillus (now Nucella lapillus), and shows both which animals the snail eats and which animals eat the snail (Fig. 14). Colton did not indicate what inspired his diagram, but his brief bibliography does include Shelford's book (1913). Fisher did not find references in the later relevant literature to Colton's two articles on this snail (probably due in part to Colton's leaving marine biology for archeology [Miller 1991]), so we do not know of any influence that his diagram exerted. Charles Elton (Fig. 15) helped make such diagrams commonplace. He went on an Oxford University Arctic expedition in 1921 to Spitsbergen and took along Shelford's book as a possible model for his own study (Elton 1966:33). However, Elton soon realized that the community he studied had a different dynamic than Shelford's aquatic and terrestrial ones. Elton was impressed by the transfer of food from sea to land, which is reflected in his diagram (Fig. 16) published in 1923. Although V. S. Summerhayes is listed as the senior author of their joint study, since he was a botanist, we can assume that Elton developed this diagram, in which plants are not emphasized. Two years later, in 1925, Elton published this much simpler Canadian food web (Fig. 17), which includes information on the lengths of animals. In 1924, English fishery biologist A. C. Hardy published a diagram (Fig. 18) on food consumed by herring at different stages of development. It bears no similarity to any diagrams previously shown, and it seems likely that he either was inspired by some unidentified example from the fisheries literature, or that he independently developed his diagram. Be that as it may, in 1927 Elton published his classic textbook, Animal Ecology, which reprinted and explained these last three diagrams by himself and Hardy. In that book Elton also introduced (1927:55) the terms "food chain" and "food cycle." Widespread use of his book popularized the use of food web diagrams. In both Hardy's diagram and in Elton's for 1925, more information was conveyed than merely which animal ate which food. Hardy's additional information was on the age of herring in relation to food, and Elton's was on the size of the consumer in relation to food. Elton also popularized the idea of a food pyramid (1927:68–70), which concept had been implied by Semper. In 1926 Germany's leading limnologist, August Thienemann (Fig. 19) published this unique food web of lakes (Fig. 20). His 50-page article on nutrient cycles in lakes introduced into limnology the terms "producers," "consumers," (though Petersen [1915], quoted above, had used both terms in marine biology) and "reducers." Thienemann's 1926 paper and two of his other papers influenced an American postdoctoral student, Raymond Lindeman, who produced one of the most influential diagrams in the history of ecology (Fig. 21), though few if any ecologists have published similar diagrams. It appeared in his posthumous paper, "The trophic–dynamic aspect of ecology" (1942). Like Thienemann's diagram, Lindeman's is a generalized food web, but both men had hard specific data backing up their concepts. In that respect theirs were similar to diagrams by Shelford, Elton, and Hardy, which illustrated specific food webs, and unlike Semper's generalized food web, which was an educated guess. In the caption to his diagram Lindeman indicated that it was similar to one he had published the previous year. A comparison of his two diagrams indicates what he learned in his year at Yale University working under Evelyn Hutchinson (Cook 1977). The 1941 diagram is identical to the 1942 diagram except it lacks the symbols for trophic levels along the side. Lindeman (1942:159) used Thienemann's terms "producers" and "consumers," but suggested substituting the term "decomposers" for Thienemann's term, "reducers," to signify that the indicated process was not just chemical, but also biological. In 1943, a year after Lindeman's 1942 diagram appeared in the journal Ecology, Harvard marine ecologist George Clarke published this conventional food web (Fig. 22), but three years later, after he had studied Lindeman's diagram and its explanation, Clarke published his diagram (Fig. 23) in Ecological Monographs, of a marine food web that emphasizes productivity and human removal of material. It also shows Clarke's concern for the rate of production at each trophic level. The Odum brothers, Eugene and Howard Thomas, carried Lindeman's thinking further. The Atomic Energy Committee became interested in radiation ecology (Kwa 1989:48), and Eugene Odum (Fig. 24; photo, Craige 2001) developed a program at the University of Georgia to study food chains at the Savannah River Research Facility to trace radioactive pollution (Craige 2001). By injecting plant stems with radioactive phosphorus-32, he and his colleagues traced it up the food chain to leafhoppers, beetles, and spiders (Kwa 1989:58). About 1957 the programs at Oak Ridge and Savannah River converged, with both programs using radioactive tracers to measure the flow of materials up the food chain (Kwa 1989:66). In the second edition of Eugene Odum's famous textbook, Fundamentals of Ecology (1959:47), there is a 1949 diagram of a food chain (Fig. 25). When I saw it, I assumed that Lindeman's influence had flowed across the Atlantic in just a few years, but when I compared it with British ecologist Erichsen Jones' own diagram, I discovered what Odum meant when he wrote that his diagram was "redrawn" from the one by Jones: Odum added the labels to the left of the diagram as a pedagogical aid. Howard Thomas Odum (Fig. 26; photo from Katherine Ewel) received his graduate training under Hutchinson at Yale. (In 1954 he taught me freshman zoology at Duke.) In 1956, he produced a diagram (Fig. 27) of matter and energy flow, in steady-state flowing-water communities in Florida. At that point, the reader could still understand the diagram without special training. However, H. T. Odum continued developing his thinking along the lines of systems ecology and used symbols from electrical engineering. By 1971 he published esoteric diagrams (Fig. 28) that integrate humans into the biotic community. This was an important step towards founding several applied ecological sciences (Mitsch 1994, Hall 1995, Egerton 2007b). Other ecologists developed food chain and food web concepts in another direction. In 1948, D. E. Howell reported finding DDT in human fat, and by 1949 biologists were reporting that fish feeding on insects killed by DDT were also being killed (Hoffmann and Surber 1949, Langford 1949). Rachel Carson (Fig. 29) publicized the discovery of insecticides traveling up the food chain in ever-increasing concentrations in her best-selling book, Silent Spring (1962:110–111), as did Robert Rudd in his less-read book, Pesticides and the Living Landscape 1964. Carson did not provide diagrams, and the ones Rudd used were quite simple. Here are four (Fig. 30) of the seven diagrams in his book. DDT was the most notorious insecticide, and in 1967 George Woodwell published a diagram (Fig. 31) in Scientific American showing increased concentrations of DDT as it progressed up the food chain. By 1970, Clive Edwards constructed a much more detailed food web (Fig. 32), showing DDT pathway and concentrations from the time of spraying DDT into the air, all the way up the food chain until it became concentrated in predatory birds, mammals, and humans. From simple narratives around 1700, food chain and food web concepts have been developed into progressively more sophisticated vehicles for conveying ecological ideas (Polis et al. 2004, de Ruiter et al. 2005). Lorenzo Camerano's two 1880 diagrams of food webs had no known influence, but after the visual stimulus of diagrams became established in the early 1900s, many ecologists found creative ways to express visually their discoveries concerning food chains and webs. This is a revised version of a talk given at the ESA Annual Meeting in August 2006 in Memphis, Tennessee. For comments preceding the talk, I thank Robert P. McIntosh, Professor Emeritus of Biology, University of Notre Dame (now in Florida). For several references used in the revision, I thank Jonathan A. D. Fisher, Department of Biology, University of Pennsylvania, Philadelphia.

Energetics and Stability in Belowground Food Webs

Worldwide tree diversity loss raises concerns about functional and energetic declines across trophic levels. In this study, we coupled 160 above- and belowground food webs, quantifying energy fluxes to microorganisms and invertebrates in a tree-mycorrhiza diversity experiment, to test how tree diversity affects fluxes of energy above and below the ground. The experiment differentiates three mycorrhizal type treatments: only AM tree species (with arbuscular mycorrhizae), only EcM tree species (with ectomycorrhizae; one, two, and four tree species), or mixtures of both AM and EcM tree species (AM+EcM; two and four tree species). Our results indicate that most energy initially flowed through belowground communities, with soil microorganisms contributing 97.7% of total energy and belowground fauna accounting for 60.9% of energy to animals. Consequently, belowground fauna fueled surface (62.3% of predation) and aboveground (30.5% of predation) predators. Tree diversity increased ecosystem multifunctionality (indicated by total and averaged energy fluxes) by ∼30% and energy across most trophic levels in EcM tree communities, while it shifted food webs from fast (such as bacterial-dominated) to slow (such as fungal-dominated) channels in AM tree communities. Tree diversity primarily impacted energy fluxes through belowground communities and strengthened the coupling of above- and belowground food webs, with increasing importance of belowground prey for predators at the soil surface and above the ground. These findings highlight that tree diversity and mycorrhizal types drive above- and belowground ecosystem functioning via belowground energy fluxes.

Diverse populations of invertebrates constitute the food web in detritus layers of a forest floor. Heterogeneity in trophic interactions within such a species‐rich community food web may affect the dynamic properties of biological communities such as stability. To examine the vertical heterogeneity in trophic interactions among invertebrates in litter and humus layers, we studied differences in species composition and variations in carbon and nitrogen stable‐isotope ratios (δ 13 C and δ 15 N) using community‐wide metrics of the forest floors of temperate broadleaf forests in Japan. The species composition differed between the two layers, and the invertebrates in the litter layer were generally larger than those in the humus layer, suggesting that these layers harbored separate food webs based on different basal resources. However, the δ 13 C of invertebrates, an indicator of differences in the basal resources of community food webs, did not provide evidence for separate food webs between layers even though plant‐derived organic matter showed differences in stable‐isotope ratios according to decomposition state. The minimum δ 15 N of invertebrates also did not differ between layers, suggesting sharing of food by detritivores from the two layers at lower trophic levels. The maximum and range of δ 15 N were greater in the humus layer, suggesting more trophic transfers (probably involving microorganisms) than in the litter layer and providing circumstantial evidence for weak trophic interactions between layers at higher trophic levels. Thus, the invertebrate community food web was not clearly compartmentalized between the detrital layers but still showed a conspicuous spatial (vertical) heterogeneity in trophic interactions.

BackgroundUnderstanding feedback between above- and below-ground processes of biological communities is a key to the effective management of natural and agricultural ecosystems. However, as above- and below-ground food webs are often studied separately, our knowledge of material flow and community dynamics in terrestrial ecosystems remains limited.ResultsWe developed a high-throughput sequencing method for examining how spiders link above- and below-ground food webs as generalist predators. To overcome problems related to DNA-barcoding-based analyses of arthropod–arthropod interactions, we designed spider-specific blocking primers and Hexapoda-specific primers for the selective PCR amplification of Hexapoda prey sequences from spider samples. By applying the new DNA metabarcoding framework to spider samples collected in a temperate secondary forest in Japan, we explored the structure of a food web involving 15 spider species and various taxonomic groups of Hexapoda prey. These results support the hypothesis that multiple spider species in a community can prey on both above- and below-ground prey species, potentially coupling above- and below-ground food-web dynamics.ConclusionsThe PCR primers and metabarcoding pipeline described in this study are expected to accelerate nuclear marker-based analyses of food webs, illuminating poorly understood trophic interactions in ecosystems.

1. Stable nitrogen (N) isotope has been widely used to disentangle food webs and to infer trophic positions of organisms based on an assumption that the stepwise enrichment occurs along trophic levels. The enrichment of N-15 in soil organisms with diet humification has also been reported, but the underlying mechanism has not been fully examined. 2. To examine the effect of diet humification on N-15, we estimated the stable N isotope ratios and diet ages of earthworms and termites. These organisms feed on organic matter with various degrees of humification, ranging from undecomposed plant materials to humified organic matter (soil organic matter), in a gallery forest and a savanna in the Ivory Coast. We defined diet age as the time elapsed since carbon (C) in the diet of earthworms and termites was fixed from atmospheric CO2 by photosynthesis; it was estimated by comparing the radiocarbon (C-14) content of these organisms to atmospheric (CO2)-C-14 records. 3. Stable N isotope ratios increased along the humification gradient of diets, and values for earthworms and termites varied from 1.8 parts per thousand to 9.9 parts per thousand and from -1.5 parts per thousand to 15.9 parts per thousand, respectively. Epigeic (litter-feeding) earthworms had younger diet ages (2-4 years), whereas endogeic (soil-feeding) earthworms generally exhibited older diet ages (5-9 years). Grass-feeding termites had young diet ages (2 years), and wood/soil-feeding termites had the oldest diet ages (c. 50 years). Soil-feeding termites were similar in diet age (7-12 years) to wood feeders (8-11 years), with the exception of one species (18-21 years) that consumes large-diameter wood. 4. A significant positive relationship was found between diet ages and stable N isotope ratios of the two groups in the savanna. This relationship held in the gallery forest when termites feeding on woody tissues were not considered. These results show that the stable N isotope ratios of organisms can increase with diet age, unless C in the diet has been stored as organic matter, such as woody tissue, that is able to age without being subject to humification processes. 5. Given that above-ground food webs are often sustained directly by material and energy flow from below-ground food webs, in addition to trophic interactions, gradual enrichment of N-15 with the humification of below-ground diets should be considered when interpreting stable N isotope ratios of terrestrial food webs.

Human impact on structure and functioning of ecosystems is rapidly increasing. Virtually all European forests are managed with major implications for diversity and structure of food webs. Centipedes (Chilopoda: Lithobiidae) are abundant arthropod predators in European temperate forest soils with a generalistic feeding behaviour. However, little is known on the variability in the prey spectrum of centipedes with land use and the responsible factors. Combining fatty acid (FA) analysis, which allows determination of the relative contribution of different prey to predator nutrition, and stable isotope analysis, providing insight into the trophic structure of decomposer food webs, we investigated variations in trophic niches of two dominant centipede species, Lithobius mutabilis and Lithobius crassipes , in differently aged beech and spruce forests. FA composition of the two centipede species differed significantly with bacterial marker FAs being more abundant in L. crassipes as compared to L. mutabilis . Differences were most pronounced in spruce as compared to beech forests. The results suggest that dense needle litter in coniferous forests may restrict prey availability to the larger L. mutabilis and confine foraging to the litter surface whereas the smaller L. crassipes is able to also exploit prey of deeper litter layers. Lithobius crassipes was significantly more enriched in 15 N and 13 C compared to L. mutabilis suggesting that, compared to L. mutabilis , the smaller L. crassipes occupies higher trophic levels and relies more on root derived carbon. The results indicate that trophic niches of centipedes vary in a species specific way between forest types with body size and habitat structure being major determinants of the variations in the prey spectrum. Combining techniques for delineating predator–prey interactions allowed insights into variations in trophic interrelationships and their driving forces in temperate forest soil food webs.

The prevailing paradigm in subterranean ecology is that below-ground food webs are simple, limited to one or two trophic levels, and composed of generalist species because of spatio-temporally patchy food resources and pervasive energy limitation. This paradigm is based on relatively few studies of easily accessible, air-filled caves. However, in some subterranean ecosystems, chemolithoautotrophy can subsidize or replace surface-based allochthonous inputs of photosynthetically derived organic matter (OM) as a basal food resource and promote niche specialization and evolution of higher trophic levels. Consequently, the current subterranean trophic paradigm fails to account for variation in resources, trophic specialization, and food chain length in some subterranean ecosystems. We reevaluated the subterranean food web paradigm by examining spatial variation in the isotopic composition of basal food resources and consumers, food web structure, stygobiont species diversity, and chromophoric organic matter (CDOM), across a geochemical gradient in a large and complex groundwater system, the Edwards Aquifer in Central Texas (USA). Mean δ13C values of stygobiont communities become increasingly more negative along the gradient of photosynthetic OM sources near the aquifer recharge zone to chemolithoautotrophic OM sources closer to the freshwater-saline water interface (FWSWI) between oxygenated freshwater and anoxic, sulfide-rich saline water. Stygobiont community species richness declined with increasing distance from the FWSWI. Bayesian mixing models were used to estimate the relative importance of photosynthetic OM and chemolithoautorophic OM for stygobiont communities at three biogeochemically distinct sites. The contribution of chemolithoautotrophic OM to consumers at these sites ranged between 25% and 69% of total OM utilized and comprised as much as 88% of the diet for one species. In addition, the food web adjacent to the FWSWI had greater trophic diversity when compared to the other two sites. Our results suggest that diverse OM sources and in situ, chemolithoautotrophic OM production can support complex groundwater food webs and increase species richness. Chemolithoautotrophy has been fundamental for the long-term maintenance of species diversity, trophic complexity, and community stability in this subterranean ecosystem, especially during periods of decreased photosynthetic production and groundwater recharge that have occurred over geologic time scales.

Viruses are present in any cellular organism and are numerous in the environment. Though they influence nutrient cycles, interactions and energy flows in food webs, viral diversity distribution and assembly in ecosystems are still understudied [1].In our project “Viral hotspots and fluxes across above- and belowground food webs (ViralWeb)” we aim to clarify mechanisms of distribution of viruses and their diversity forming across above- and belowground ecosystem compartments and food webs. We focus on plants, fungi, and invertebrate animals as model potential hosts. We also concentrate on RNA viruses, as they dominate eukaryotic viromes [2].We hypothesize that the diversity and distribution of viruses in ecosystems depend on the diversity of hosts and flows of matter and biomass among ecosystem compartments and food-web nodes. We have three specific hypotheses:1) the RNA viral diversity of the ecosystem is positively correlated with the diversity of potential viral hosts in this ecosystem;2) there are local hotspots of viral diversity in systems, such as “cumulative” substrates (e.g., leaf litter) and hosts (top predators);3) patterns of viral distribution in food webs are correlated with flows of matter and energy among food-web nodes and ecosystem compartments. We expect to detect a positive correlation between the similarity of viral community and connectedness of two nodes in a food web.We plan to conduct our investigation based on biodiversity manipulation experiments in central Germany (the Jena Experiment and MyDiv). Our sampling design is based on plots with different diversity levels of hosts (plants, fungi, and invertebrates).Green parts of plants, fungi, litter, soil, and invertebrate consumers by ecological groups [3] will be sampled. The diversity of hosts will be accessed using DNA analysis and morphological identification. The presence of viruses and replication evidences will be detected via high-throughput sequencing and strand-specific RT-PCR [4].For both study sites food webs will be reconstructed and energy fluxes across above- and belowground compartments will be calculated [5]. Invertebrate hosts’ classification and body size measurement will be facilitated using image analysis approach [6]. Based on obtained average consumer sizes the biomass of food web nodes will be calculated [7]. Energy fluxes will be estimated from metabolic rates of invertebrates accounting for temperature and assimilation efficiency [8].We expect the results of ViralWeb project to help us better understand the mechanisms of spread of viruses and clarify and predict the roles of viruses in ecosystems.The project was supported by the Flexpool funding mechanism of the German Centre for Integrative Biodiversity Research (iDiv). Refernces[1] Williamson KE et al. (2017). Annual review of virology, 4:201-219. https://doi.org/10.1146/annurev-virology-101416-041639[2] Wolf YI et al. (2018). MBio, 9(6):10-1128. https://doi.org/10.1128/mbio.02329-18[3] Potapov AM et al. (2022). Biological Reviews 97:1057–1117. doi:https://doi.org/10.1111/brv.12832[4] Baty JW et al. (2020). Myrmecol. News 30:213-228. https://doi.org/10.25849/myrmecol.news_030:213[5] Potapov AM et al. (2024). Nature, 1-7. https://doi.org/10.1038/s41586-024-07083-y[6] Sys S et al. (2022). Methods in Ecology and Evolution 2041–210X.14001. doi:10.1111/2041-210X.14001[7] Sohlström EH et al. (2018). Ecology and Evolution 8:12737–12749. doi:10.1002/ece3.4702[8] Potapov AM (2022). Biological Reviews, 97(4):1691-1711. https://doi.org/10.1111/brv.12857

Predator diversity and abundance are under strong human pressure in all types of ecosystems. Whereas predator potentially control standing biomass and species interactions in food webs, their effects on prey biomass and especially prey biodiversity have not yet been systematically quantified. Here, we test the effects of predation in a cross‐system meta‐analysis of prey diversity and biomass responses to local manipulation of predator presence. We found 291 predator removal experiments from 87 studies assessing both diversity and biomass responses. Across ecosystem types, predator presence significantly decreased both biomass and diversity of prey across ecosystems. Predation effects were highly similar between ecosystem types, whereas previous studies had shown that herbivory or decomposition effects differed fundamentally between terrestrial and aquatic systems based on different stoichiometry of plant material. Such stoichiometric differences between systems are unlikely for carnivorous predators, where effect sizes on species richness strongly correlated to effect sizes on biomass. However, the negative predation effect on prey biomass was ameliorated significantly with increasing prey richness and increasing species richness of the manipulated predator assemblage. Moreover, with increasing richness of the predator assemblage present, the overall negative effects of predation on prey richness switched to positive effects. Our meta‐analysis revealed strong general relationships between predator diversity, prey diversity and the interaction strength between trophic levels in terms of biomass. This study indicates that anthropogenic changes in predator abundance and diversity will potentially have strong effects on trophic interactions across ecosystems.SynthesisThe past centuries we have experienced a dramatic loss of top–predator abundance and diversity in most types of ecosystems. To understand the direct consequences of predator loss on a global scale, we quantitatively summarized experiments testing predation effects on prey communities in a cross‐system meta‐analysis. Across ecosystem types, predator presence significantly decreased both biomass and diversity of prey, and predation effects were highly similar. However, with increasing predator richness, the overall negative effects of predation on prey richness switched to positive ones. Anthropogenic changes in predator communities will potentially have strong effects on prey diversity, biomass, and trophic interactions across ecosystems.

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.