ABSTRACT
Soil organisms drive major ecosystem functions by mineralising carbon and releasing nutrients during decomposition processes, which supports plant growth, aboveground biodiversity and, ...ultimately, human nutrition. Soil ecologists often operate with functional groups to infer the effects of individual taxa on ecosystem functions and services. Simultaneous assessment of the functional roles of multiple taxa is possible using food‐web reconstructions, but our knowledge of the feeding habits of many taxa is insufficient and often based on limited evidence. Over the last two decades, molecular, biochemical and isotopic tools have improved our understanding of the feeding habits of various soil organisms, yet this knowledge is still to be synthesised into a common functional framework. Here, we provide a comprehensive review of the feeding habits of consumers in soil, including protists, micro‐, meso‐ and macrofauna (invertebrates), and soil‐associated vertebrates. We have integrated existing functional group classifications with findings gained with novel methods and compiled an overarching classification across taxa focusing on key universal traits such as food resource preferences, body masses, microhabitat specialisation, protection and hunting mechanisms. Our summary highlights various strands of evidence that many functional groups commonly used in soil ecology and food‐web models are feeding on multiple types of food resources. In many cases, omnivory is observed down to the species level of taxonomic resolution, challenging realism of traditional soil food‐web models based on distinct resource‐based energy channels. Novel methods, such as stable isotope, fatty acid and DNA gut content analyses, have revealed previously hidden facets of trophic relationships of soil consumers, such as food assimilation, multichannel feeding across trophic levels, hidden trophic niche differentiation and the importance of alternative food/prey, as well as energy transfers across ecosystem compartments. Wider adoption of such tools and the development of open interoperable platforms that assemble morphological, ecological and trophic data as traits of soil taxa will enable the refinement and expansion of the multifunctional classification of consumers in soil. The compiled multifunctional classification of soil‐associated consumers will serve as a reference for ecologists working with biodiversity changes and biodiversity–ecosystem functioning relationships, making soil food‐web research more accessible and reproducible.
A large number of predatory mesostigmatid mite species populate forest soils in high densities. The present study investigates the trophic structure of the Mesostigmata community of old growth beech ...stands in Central Germany and identifies potential prey groups using natural variations in stable isotope ratios (13C/12C and 15N/14N). Data on relative abundances and body mass were included for each of the 40 species studied to analyze functional aspects in Mesostigmata feeding ecology. The results indicate that Mesostigmata predominantly feed on secondary decomposers, whereas primary decomposer and intra-guild prey are of minor importance. Dominant species featured high δ13C signatures suggesting that they predominantly feed on species relying on root derived resources such as bacterial feeding nematodes. Less abundant species where characterized by lower δ13C values suggesting that they predominantly feed on prey relying on litter derived resources such as fungal feeding Collembola. Related taxa often had distinctively different isotope ratios suggesting that trophic niche partitioning facilitates coexistence of morphologically similar species. Unexpectedly, the trophic position of Mesostigmata species was not related to body size reflecting the varying trophic position of their main prey, nematodes and Collembola, suggesting that body size is a poor predictor of trophic position in soil food webs.
► We analyzed variations in stable isotope ratios in 40 Mesostigmata species of beech forests. ► The majority of species occupy distinct trophic niches including closely related species. ► The most important prey comprises secondary decomposers presumably in particular nematodes. ► Trophic level in Mesostigmata correlates little with body size.
Forest soil and litter is inhabited by a diverse community of animals, which directly and indirectly rely on dead organic matter as habitat and food resource. However, community composition may be ...driven by biotic or abiotic forces, and these vary with changes in habitat structure and resource supply associated with forest land use. To evaluate these changes, we compiled comprehensive data on the species composition of soil animal communities and environmental factors in forest types varying in land-use intensity in each of three regions in Germany, i.e., coniferous, young managed, old managed, and unmanaged beech forests. Coniferous forests featured high amounts of leaf litter and low microbial biomass concentrations contrasting in particular unmanaged beech forests. However, soil animal diversity and functional community composition differed little between forest types, indicating resilience against disturbance and forest land use. Structural equation modelling suggested that despite a significant influence of forest management on resource abundance and quality, the biomass of most soil fauna functional groups was not directly affected by forest management or resource abundance/quality, potentially because microorganisms hamper the propagation of nutrients to higher trophic levels. Instead, detritivore biomass depended heavily on soil pH. Macrofauna decomposers thrived at high pH, whereas mesofauna decomposers benefitted from low soil pH, but also from low biomass of macrofauna decomposers, potentially due to habitat modification by macrofauna decomposers. The strong influence of soil pH shows that decomposer communities are structured predominantly by regional abiotic factors exceeding the role of local biotic factors such as forest type.
Conversion of tropical rainforests into plantations fundamentally alters ecological niches of animal species. Generalist predators such as centipedes (Chilopoda) may be able to persist in converted ...ecosystems due to their ability to adapt and switch to alternative prey populations. We investigated variations in community composition and trophic niches of soil and litter living centipedes in a range of ecosystems including rainforests, jungle rubber agroforests, and rubber and oil palm monocultures in two landscapes in Sumatra, Indonesia. Including information on environmental factors in the soil and litter habitat, we explored drivers shaping ecological niches of soil living invertebrate predators in one of the world's hotspots of rainforest conversion. Conversion of rainforests into agroforests and plantations was associated with a marked change in the composition of centipede communities. However, irrespective of major differences in habitat characteristics, changes in total abundances were small and the overall diversity and biomass of centipedes was similar in each of the systems investigated, suggesting that the number of ecological niches for this group of predators remains unchanged. By using stable isotope analysis (15N and 13C), we investigated trophic niche shifts of the centipede community; lower δ13C values of centipedes in oil palm plantations as compared to other ecosystems suggests that centipedes switch from decomposer prey to other prey, presumably understory associated herbivores, due to reduced availability of litter associated prey species. The results suggest that the ability to utilize alternative prey is a key feature enabling invertebrate predators to persist in ecosystems undergoing major structural changes due to anthropogenic land use change.
Large areas of tropical rainforest are being converted to agricultural and plantation land uses, but little is known of biodiversity and ecological functioning under these replacement land uses. We ...investigated the effects of conversion of rainforest into jungle rubber, intensive rubber and oil palm plantations on testate amoebae, diverse and functionally important protists in litter and soil. Living testate amoebae species richness, density and biomass were all lower in replacement land uses than in rainforest, with the impact being more pronounced in litter than in soil. Similar abundances of species of high and low trophic level in rainforest suggest that trophic interactions are more balanced, with a high number of functionally redundant species, than in rubber and oil palm. In contrast, plantations had a low density of high trophic level species indicating losses of functions. This was particularly so in oil palm plantations. In addition, the relative density of species with siliceous shells was >50% lower in the litter layer of oil palm and rubber compared to rainforest and jungle rubber. This difference suggests that rainforest conversion changes biogenic silicon pools and increases silicon losses. Overall, the lower species richness, density and biomass in plantations than in rainforest, and the changes in the functional composition of the testate amoebae community, indicate detrimental effects of rainforest conversion on the structure and functioning of microbial food webs.
Mesofauna taxa fill key trophic positions in soil food webs, even in terrestrial-marine boundary habitats characterized by frequent natural disturbances. Salt marshes represent such boundary ...habitats, characterized by frequent inundations increasing from the terrestrial upper to the marine pioneer zone. Despite the high abundance of soil mesofauna in salt marshes and their important function by facilitating energy and carbon flows, the structure, trophic ecology and habitat-related diet shifts of mesofauna species in natural salt marsh habitats is virtually unknown. Therefore, we investigated the effects of natural disturbance (inundation frequency) on community structure, food web complexity and resource use of soil mesofauna using stable isotope analysis (15N, 13C) in three salt marsh zones. In this intertidal habitat, the pioneer zone is exposed to inundations twice a day, but lower and upper salt marshes are less frequently inundated based on shore height. The mesofauna comprised 86 species / taxa dominated by Collembola, Oribatida and Mesostigmata. Shifts in environmental disturbances influenced the structure of food webs, diversity and density declined strongly from the land to the sea pointing to the importance of increasing levels of inundation frequency. Accordingly, the reduced diversity and density was associated by a simplification of the food web in the pioneer zone as compared to the less inundated lower and upper salt marsh with a higher number of trophic levels. Strong variations in δ15N signatures demonstrated that mesofauna species are feeding at multiple trophic levels. Primary decomposers were low and most mesofauna species functioned as secondary decomposers or predators including second order predators or scavengers. The results document that major decomposer taxa, such as Collembola and Oribatida, are more diverse than previously assumed and predominantly dwell on autochthonous resources of the respective salt marsh zone. The results further suggest that Mesostigmata mostly adopt an intraguild predation lifestyle. The high trophic position of a large number of predators suggests that intraguild predation is of significant importance in salt marsh food webs. Presumably, intraguild predation contributes to stabilizing the salt marsh food web against disturbances.
Anthropogenic pressures alter the biodiversity, structure and organization of biological communities with severe consequences for ecosystem processes. Species invasion is such a human‐induced ...ecosystem change with pronounced impacts on recipient ecosystems. Around the globe, earthworms invade habitats and impact abiotic soil conditions and a wide range of above‐ and belowground organisms. In northern North America, where earthworms have been largely absent since the last glaciation period and most earthworm species present today have only been (re‐)introduced a few hundred years ago, invasion impacts have been intensively studied. However, despite several studies assessing impacts of invasive earthworms on soil fauna, studies have rarely investigated the simultaneous responses of different soil‐fauna size groups and biodiversity facets which might respond differently to earthworm invasion and independently affect ecosystem processes. Our study goes beyond previously‐established knowledge on earthworm‐invasion effects by simultaneously assessing differences in four biodiversity facets, namely the abundance, biomass, richness and Shannon index of soil invertebrate macro‐, meso‐ and microfauna communities between high‐ and low‐invasion status plots (n = 80) and in relation to invasion intensity measured as earthworm biomass across four northern North American forests sampled between 2016 and 2017. Across forests and soil‐fauna groups, we found reduced abundance (−33 to −45%) and richness (−18 to −25%) in high compared to low‐invasion status areas. Additionally, meso‐ (−14%) and microfauna biomass (−38%) and macro‐ (−7%) and microfauna Shannon index (−8%) were reduced. Higher invasion intensity (earthworm biomass) was additionally related to reduced soil‐fauna biodiversity. While the studied biodiversity facet was important for the soil fauna response, soil‐fauna size group was comparably unimportant. Given the global ubiquity of earthworm invasion and the importance of soil fauna for key ecosystem processes, our observational results help to assess future impacts of this invasion and the consequences for anthropogenically‐altered ecosystem functioning.
To maintain constant chemical composition, i.e. elemental homeostasis, organisms have to consume resources of sufficient quality to meet their own specific stoichiometric demand. Therefore, ...concentrations of elements indicate resource quality, and rare elements in the environment may act as limiting factors for individual organisms scaling up to constrain population densities. We investigated how the biomass densities of invertebrate populations of temperate forest soil communities depend on 1) the stoichiometry of the basal litter according to ecological stoichiometry concepts and 2) the population average body mass as predicted by metabolic theory. We used a large data set on biomass densities of 4959 populations across 48 forests in three regions of Germany. Following various ecological stoichiometry hypotheses, we tested for effects of the carbon‐to‐element ratios of 10 elements. Additionally, we included the abiotic litter characteristics habitat size (represented by litter depth), litter diversity and pH, as well as forest type as an indicator for human management. Across 12 species groups, we found that the biomass densities scaled significantly with population‐averaged body masses thus supporting metabolic theory. Additionally, 10 of these allometric scaling relationships exhibited interactions with stoichiometric and abiotic co‐variables. The four most frequent co‐variables were 1) forest type, 2) the carbon‐to‐phosphorus ratio (C:P), 3) the carbon‐to‐sodium ratio (C:Na), and the carbon‐to‐nitrogen ratio (C:N). Hence, our analyses support the sodium shortage hypothesis for microbi‐detritivores, the structural elements hypothesis for some predator groups (concerning N), and the secondary productivity hypothesis (concerning P) across all trophic groups in our data. In contrast, the ecosystem size hypothesis was only supported for some meso‐ and macrofauna detritivores. Our study is thus providing a comprehensive analysis how the elemental stoichiometry of the litter as the basal resource constrain population densities across multiple trophic levels of soil communities.
One of the most significant consequences of contemporary global change is the rapid decline of biodiversity in many ecosystems. Knowledge of the consequences of biodiversity loss in terrestrial ...ecosystems is largely restricted to single ecosystem functions. Impacts of key plant functional groups on soil biota are considered to be more important than those of plant diversity; however, current knowledge mainly relies on short-term experiments.
We studied changes in the impacts of plant diversity and presence of key functional groups on soil biota by investigating the performance of soil microorganisms and soil fauna two, four and six years after the establishment of model grasslands. The results indicate that temporal changes of plant community effects depend on the trophic affiliation of soil animals: plant diversity effects on decomposers only occurred after six years, changed little in herbivores, but occurred in predators after two years. The results suggest that plant diversity, in terms of species and functional group richness, is the most important plant community property affecting soil biota, exceeding the relevance of plant above- and belowground productivity and the presence of key plant functional groups, i.e. grasses and legumes, with the relevance of the latter decreasing in time.
Plant diversity effects on biota are not only due to the presence of key plant functional groups or plant productivity highlighting the importance of diverse and high-quality plant derived resources, and supporting the validity of the singular hypothesis for soil biota. Our results demonstrate that in the long term plant diversity essentially drives the performance of soil biota questioning the paradigm that belowground communities are not affected by plant diversity and reinforcing the importance of biodiversity for ecosystem functioning.
Ecological communities consist of small abundant and large non-abundant species. The energetic equivalence rule is an often-observed pattern that could be explained by equal energy usage among ...abundant small organisms and non-abundant large organisms. To generate this pattern, metabolism (as an indicator of individual energy use) and abundance have to scale inversely with body mass, and cancel each other out. In contrast, the pattern referred to as biomass equivalence states that the biomass of all species in an area should be constant across the body-mass range. In this study, we investigated forest soil communities with respect to metabolism, abundance, population energy use, and biomass. We focused on four land-use types in three different landscape blocks (Biodiversity Exploratories). The soil samples contained 870 species across 12 phylogenetic groups. Our results indicated positive sublinear metabolic scaling and negative sublinear abundance scaling with species body mass. The relationships varied mainly due to differences among phylogenetic groups or feeding types, and only marginally due to land-use type. However, these scaling relationships were not exactly inverse to each other, resulting in increasing population energy use and biomass with increasing body mass for most combinations of phylogenetic group or feeding type with land-use type. Thus, our results are mostly inconsistent with the classic perception of energetic equivalence, and reject the biomass equivalence hypothesis while documenting a specific and nonrandom pattern of how abundance, energy use, and biomass are distributed across size classes. However, these patterns are consistent with two alternative predictions: the resource-thinning hypothesis, which states that abundance decreases with trophic level, and the allometric degree hypothesis, which states that population energy use should increase with population average body mass, due to correlations with the number of links of consumers and resources. Overall, our results suggest that a synthesis of food web structures with metabolic theory may be most promising for predicting natural patterns of abundance, biomass, and energy use.
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