Rainforest transformation reallocates energy from green to brown food webs.

Terrestrial animal biodiversity is increasingly being lost because of land-use change1,2. However, functional and energetic consequences aboveground and belowground and across trophic levels in megadiverse tropical ecosystems remain largely unknown. To fill this gap, we assessed changes in energy fluxes across 'green' aboveground (canopy arthropods and birds) and 'brown' belowground (soil arthropods and earthworms) animal food webs in tropical rainforests and plantations in Sumatra, Indonesia. Our results showed that most of the energy in rainforests is channelled to the belowground animal food web. Oil palm and rubber plantations had similar or, in the case of rubber agroforest, higher total animal energy fluxes compared to rainforest but the key energetic nodes were distinctly different: in rainforest more than 90% of the total animal energy flux was channelled by arthropods in soil and canopy, whereas in plantations more than 50% of the energy was allocated to annelids (earthworms). Land-use change led to a consistent decline in multitrophic energy flux aboveground, whereas belowground food webs responded with reduced energy flux to higher trophic levels, down to -90%, and with shifts from slow (fungal) to fast (bacterial) energy channels and from faeces production towards consumption of soil organic matter. This coincides with previously reported soil carbon stock depletion3. Here we show that well-documented animal biodiversity declines with tropical land-use change4-6 are associated with vast energetic and functional restructuring in food webs across aboveground and belowground ecosystem compartments.

Feeding habits and multifunctional classification of soil-associated consumers from protists to vertebrates.

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.

Multidimensional trophic niche revealed by complementary approaches: Gut content, digestive enzymes, fatty acids and stable isotopes in Collembola.

Trophic niche differentiation may explain coexistence and shape functional roles of species. In complex natural food webs, however, trophic niche parameters depicted by single and isolated methods may simplify the multidimensional nature of consumer trophic niches, which includes feeding processes such as food choice, ingestion, digestion, assimilation and retention. Here we explore the correlation and complementarity of trophic niche parameters tackled by four complementary methodological approaches, that is, visual gut content, digestive enzyme, fatty acid and stable isotope analyses-each assessing one or few feeding processes, and demonstrate the power of method combination. Focusing on soil ecosystems, where many omnivore species with cryptic feeding habits coexist, we chose Collembola as an example. We compiled 15 key trophic niche parameters for 125 species from 40 studies. We assessed correlations among trophic niche parameters and described variation of these parameters in different Collembola species, families and across life-forms, which represent microhabitat specialisation. Correlation between trophic niche parameters was weak in 45 out of 64 pairwise comparisons, pointing at complementarity of the four methods. Jointly, the results indicated that fungal- and plant-feeding Collembola assimilate storage, rather than structural polysaccharides, and suggested bacterial feeding as a potential alternative feeding strategy. Gut content and fatty acid analyses suggested alignment between ingestion and assimilation/retention processes in fungal- and plant-feeding Collembola. From the 15 trophic niche parameters, six were related to Collembola family identity, suggesting that not all trophic niche dimensions are phylogenetically structured. Only three parameters were related to the life-forms, suggesting that species use various feeding strategies when living in the same microenvironments. Consumers can meet their nutritional needs by varying their food choices, ingestion and digestion strategies, with the connection among different feeding processes being dependent on the consumed resource and consumer adaptations. Multiple methods reveal different dimensions, together drawing a comprehensive picture of the trophic niche. Future studies applying the multidimensional trophic niche approach will allow us to trace trophic complexity and reveal niche partitioning of omnivorous species and their functional roles, especially in cryptic environments such as soils, caves, deep ocean or benthic ecosystems.

Diversity and functional structure of soil animal communities suggest soil animal food webs to be buffered against changes in forest land use.

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.

Variation in trophic niches of oribatid mites in temperate forest ecosystems as indicated by neutral lipid fatty acid patterns.

Shifting of trophic niches of soil microarthropods may allow them to adapt to changing resource conditions as induced by global change processes. However, the capability of microarthropods to shift their trophic niches is little studied. Whereas some studies based on stable isotopes (15N/13C) point to distinct and narrow trophic niches, others indicate that trophic niches are plastic. Here, we investigated shifts in trophic niches of oribatid mites (Oribatida, Acari), a major soil detritivore microarthropod group, due to forest management, i.e., plantation of beech and spruce forests in Central Europe, using neutral lipid fatty acid (NLFA) markers. Due to differential microbial communities, we expected a fungi-based diet of oribatid mites in beech forest, but more bacterial contributions to the diet in spruce forest. Supporting these hypotheses, NLFA markers indicated that the trophic niches of each of the studied oribatid mite species differed between beech and spruce forests and shifted from feeding predominantly on litter and fungi in beech forest to more intensively feeding on bacteria in spruce forest. Oribatid mite species with the most pronounced differences in trophic niches included Achipteria coleoptrata, Eupelops hirtus, Eupelops plicatus and Liacarus xylariae, which had been classified as primary or secondary decomposers in previous studies. Overall, the results indicate that the ability of oribatid mite species to colonize different habitats and ecosystems is due to their ability to adjust their diet, i.e., to trophic plasticity. Changes in trophic niches in each of the studied oribatid mite species suggest that detritivores in soil may better cope with future changes in environmental conditions and associated changes in resource composition than species above the ground.

Conversion of rainforest to oil palm and rubber plantations alters energy channels in soil food webs.

In the last decades, lowland tropical rainforest has been converted in large into plantation systems. Despite the evident changes above ground, the effect of rainforest conversion on the channeling of energy in soil food webs was not studied. Here, we investigated community-level neutral lipid fatty acid profiles in dominant soil fauna to track energy channels in rainforest, rubber, and oil palm plantations in Sumatra, Indonesia. Abundant macrofauna including Araneae, Chilopoda, and Diplopoda contained high amounts of plant and fungal biomarker fatty acids (FAs). Lumbricina had the lowest amount of plant, but the highest amount of animal-synthesized C20 polyunsaturated FAs as compared to other soil taxa. Mesofauna detritivores (Collembola and Oribatida) contained high amounts of algal biomarker FAs. The differences in FA profiles between taxa were evident if data were analyzed across land-use systems, suggesting that soil fauna of different size (macro- and mesofauna) are associated with different energy channels. Despite that, rainforest conversion changed the biomarker FA composition of soil fauna at the community level. Conversion of rainforest into oil palm plantations enhanced the plant energy channel in soil food webs and reduced the bacterial energy channel; conversion into rubber plantations reduced the AMF-based energy channel. The changes in energy distribution within soil food webs may have significant implications for the functioning of tropical ecosystems and their response to environmental changes. At present, these responses are hard to predict considering the poor knowledge on structure and functioning of tropical soil food webs.

Combining bulk and amino acid stable isotope analyses to quantify trophic level and basal resources of detritivores: a case study on earthworms.

Quantification of the bacterial, fungal, and plant energy channels to the nutrition of detritivores is methodologically challenging. This is especially true for earthworms that ingest large amounts of litter and soil mixed with microorganisms. Novel methods such as compound-specific stable isotope analysis (CSIA) of C and N of individual amino acids promise major progress in this field in comparison with bulk stable isotope analysis (bulk SIA). Here, we combine CSIA and bulk SIA of carbon and nitrogen to quantify the linkage of epigeic and endogeic earthworm species to different energy channels across boreal and temperate forest ecosystems. The results showed pronounced flux of energy directly from plants to earthworms (33-50% of essential amino acids, EAA) refining the position of earthworms in soil food webs as both competitors and consumers of microorganisms. Epigeic earthworm species primarily relied on plant litter and endogeic species primarily relied on bacteria and soil organic matter. The linkage of both groups to plant or microbial energy channel was likely driven by the quality of detritus. Both bulk 15N and 13C enrichments were related to the trophic level of earthworms. Furthermore, 15N enrichment was related to the proportions of bacterial and plant EAA in the diet. Strong negative correlation between trophic level (CSIA of nitrogen) and the proportion of plant EAA (CSIA of carbon) suggests that both novel methods can indicate the degree of microbivory in detritivores. CSIA of amino acids provide detailed and baseline-independent information on basal resources and trophic levels of detritivores.

Driving factors and temporal fluctuation of Collembola communities and reproductive mode across forest types and regions.

Despite the major role of Collembola in forest soil animal food webs, ecological and evolutionary determinants of their community composition are not well understood. We investigated abundance, community structure, life forms, and reproductive mode of Collembola in four different forest types (coniferous, young managed beech, old managed beech, and unmanaged beech forests) representing different management intensities. Forest types were replicated within three regions across Germany: the Schorfheide-Chorin, the Hainich, and the Swabian Alb, differing in geology, altitude, and climate. To account for temporal variation, samples were taken twice with an interval of 3 years. To identify driving factors of Collembola community structure, we applied structural equation modeling, including an index of forest management intensity, abiotic and biotic factors such as pH, C-to-N ratio of leaf litter, microbial biomass, and fungal-to-bacterial ratio. Collembola abundance, biomass, and community composition differed markedly between years, with most pronounced differences in the Schorfheide, the region with the harshest climatic conditions. There, temporal fluctuations of parthenogenetic Collembola were significantly higher than in the other regions. In the year with the more favorable conditions, parthenogenetic species flourished, with their abundance depending mainly on abiotic, density-independent factors. This is in line with the "Structured Resource Theory of Sexual Reproduction," stating that parthenogenetic species are favored if density-independent factors, such as desiccation, frost or flooding, prevail. In contrast, sexual species in the same year were mainly influenced by resource quality-related factors such as the fungal-to-bacterial ratio and the C-to-N ratio of leaf litter. The influence of forest management intensity on abundances was low, indicating that disturbance through forest management plays a minor role. Accordingly, differences in community composition were more pronounced between regions than between different forest types, pointing to the importance of regional factors.

Lack of energetic equivalence in forest soil invertebrates.

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.

General relationships between abiotic soil properties and soil biota across spatial scales and different land-use types.

Very few principles have been unraveled that explain the relationship between soil properties and soil biota across large spatial scales and different land-use types. Here, we seek these general relationships using data from 52 differently managed grassland and forest soils in three study regions spanning a latitudinal gradient in Germany. We hypothesize that, after extraction of variation that is explained by location and land-use type, soil properties still explain significant proportions of variation in the abundance and diversity of soil biota. If the relationships between predictors and soil organisms were analyzed individually for each predictor group, soil properties explained the highest amount of variation in soil biota abundance and diversity, followed by land-use type and sampling location. After extraction of variation that originated from location or land-use, abiotic soil properties explained significant amounts of variation in fungal, meso- and macrofauna, but not in yeast or bacterial biomass or diversity. Nitrate or nitrogen concentration and fungal biomass were positively related, but nitrate concentration was negatively related to the abundances of Collembola and mites and to the myriapod species richness across a range of forest and grassland soils. The species richness of earthworms was positively correlated with clay content of soils independent of sample location and land-use type. Our study indicates that after accounting for heterogeneity resulting from large scale differences among sampling locations and land-use types, soil properties still explain significant proportions of variation in fungal and soil fauna abundance or diversity. However, soil biota was also related to processes that act at larger spatial scales and bacteria or soil yeasts only showed weak relationships to soil properties. We therefore argue that more general relationships between soil properties and soil biota can only be derived from future studies that consider larger spatial scales and different land-use types.

The underestimated importance of belowground carbon input for forest soil animal food webs.

The present study investigated the relative importance of leaf and root carbon input for soil invertebrates. Experimental plots were established at the Swiss Canopy Crane (SCC) site where the forest canopy was enriched with (13)C depleted CO(2) at a target CO(2) concentration of c. 540 p.p.m. We exchanged litter between labelled and unlabelled areas resulting in four treatments: (i) leaf litter and roots labelled, (ii) only leaf litter labelled, (iii) only roots labelled and (iv) unlabelled controls. In plots with only (13)C-labelled roots most of the soil invertebrates studied were significantly depleted in (13)C, e.g. earthworms, chilopods, gastropods, diplurans, collembolans, mites and isopods, indicating that these taxa predominantly obtain their carbon from belowground input. In plots with only (13)C-labelled leaf litter only three taxa, including, e.g. juvenile Glomeris spp. (Diplopoda), were significantly depleted in (13)C suggesting that the majority of soil invertebrates obtain its carbon from roots. This is in stark contrast to the view that decomposer food webs are based on litter input from aboveground.