ABSTRACT
The belowground compartment of terrestrial ecosystems drives nutrient cycling, the decomposition and stabilisation of organic matter, and supports aboveground life. Belowground consumers ...create complex food webs that regulate functioning, ensure stability and support biodiversity both below and above ground. However, existing soil food‐web reconstructions do not match recently accumulated empirical evidence and there is no comprehensive reproducible approach that accounts for the complex resource, size and spatial structure of food webs in soil. Here I build on generic food‐web organisation principles and use multifunctional classification of soil protists, invertebrates and vertebrates, to reconstruct a ‘multichannel’ food web across size classes of soil‐associated consumers. I infer weighted trophic interactions among trophic guilds using feeding preferences and prey protection traits (evolutionarily inherited traits), size and spatial distributions (niche overlaps), and biomass‐dependent feeding. I then use food‐web reconstruction, together with assimilation efficiencies, to calculate energy fluxes assuming a steady‐state energetic system. Based on energy fluxes, I propose a number of indicators, related to stability, biodiversity and multiple ecosystem‐level functions such as herbivory, top‐down control, translocation and transformation of organic matter. I illustrate this approach with an empirical example, comparing it with traditional resource‐focused soil food‐web reconstruction. The multichannel reconstruction can be used to assess ‘trophic multifunctionality’ (analogous to ecosystem multifunctionality), i.e. simultaneous support of multiple trophic functions by the food web, and compare it across communities and ecosystems spanning beyond the soil. With further empirical validation of the proposed functional indicators, this multichannel reconstruction approach could provide an effective tool for understanding animal diversity–ecosystem functioning relationships in soil. This tool hopefully will inspire more researchers to describe soil communities and belowground–aboveground interactions comprehensively. Such studies will provide informative indicators for including consumers as active agents in biogeochemical models, not only locally but also on regional and global scales.
ABSTRACT
Despite the major importance of soil biota in nutrient and energy fluxes, interactions in soil food webs are poorly understood. Here we provide an overview of recent advances in uncovering ...the trophic structure of soil food webs using natural variations in stable isotope ratios. We discuss approaches of application, normalization and interpretation of stable isotope ratios along with methodological pitfalls. Analysis of published data from temperate forest ecosystems is used to outline emerging concepts and perspectives in soil food web research.
In contrast to aboveground and aquatic food webs, trophic fractionation at the basal level of detrital food webs is large for carbon and small for nitrogen stable isotopes. Virtually all soil animals are enriched in 13C as compared to plant litter. This ‘detrital shift’ likely reflects preferential uptake of 13C‐enriched microbial biomass and underlines the importance of microorganisms, in contrast to dead plant material, as a major food resource for the soil animal community.
Soil organic matter is enriched in 15N and 13C relative to leaf litter. Decomposers inhabiting mineral soil layers therefore might be enriched in 15N resulting in overlap in isotope ratios between soil‐dwelling detritivores and litter‐dwelling predators. By contrast, 13C content varies little between detritivores in upper litter and in mineral soil, suggesting that they rely on similar basal resources, i.e. little decomposed organic matter. Comparing vertical isotope gradients in animals and in basal resources can be a valuable tool to assess trophic interactions and dynamics of organic matter in soil.
As indicated by stable isotope composition, direct feeding on living plant material as well as on mycorrhizal fungi is likely rare among soil invertebrates. Plant carbon is taken up predominantly by saprotrophic microorganisms and channelled to higher trophic levels of the soil food web. However, feeding on photoautotrophic microorganisms and non‐vascular plants may play an important role in fuelling soil food webs.
The trophic niche of most high‐rank animal taxa spans at least two trophic levels, implying the use of a wide range of resources. Therefore, to identify trophic species and links in food webs, low‐rank taxonomic identification is required. Despite overlap in feeding strategies, stable isotope composition of the high‐rank taxonomic groups reflects differences in trophic level and in the use of basal resources. Different taxonomic groups of predators and decomposers are likely linked to different pools of organic matter in soil, suggesting different functional roles and indicating that trophic niches in soil animal communities are phylogenetically structured.
During last two decades studies using stable isotope analysis have elucidated the trophic structure of soil communities, clarified basal food resources of the soil food web and revealed links between above‐ and belowground ecosystem compartments. Extending the use of stable isotope analysis to a wider range of soil‐dwelling organisms, including microfauna, and a larger array of ecosystems provides the perspective of a comprehensive understanding of the structure and functioning of soil food webs.
Do large organisms occupy higher trophic levels? Predators are often larger than their prey in food chains, but empirical evidence for positive body mass–trophic level scaling for entire food webs ...mostly comes from marine communities on the basis of unicellular producers. Using published data on stable isotope compositions of 1,093 consumer species, we explored how trophic level scales with body size, food web type (green vs. brown), and phylogenetic group across biomes. In contrast to widespread assumptions, the relationship between body size and trophic level of consumers—from protists to large vertebrates—was not significant per se but varied among ecosystem types and animal groups. The correlation between body size and trophic level was strong in marine consumers, weak in freshwater consumers, and absent in terrestrial consumers, which was also observed at the scale of local food webs. Vertebrates occupied higher trophic positions than invertebrates, and green trophic chains were longer than brown ones in aquatic (primarily marine) but not in terrestrial food webs. Variations in body size of top predators suggest that terrestrial and many freshwater food webs are size compartmentalized, implying different trophic dynamics and responses to perturbations than in size-structured marine food webs.
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.
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.
The authors revealed the information provided by four complementary methods in trophic ecology, including visual gut content‐, digestive enzyme‐, fatty acid‐ and stable isotope analyses, thereby to demonstrate multidimensional nature of trophic niches in Collembola—one of the functionally diverse taxa with cryptic feeding habits in soil.
Many ecosystem functions depend on the structure of food webs, which heavily relies on the body size spectrum of the community. Despite that, little is known on how the size spectrum of soil animals ...responds to agricultural practices in tropical land‐use systems and how these responses affect ecosystem functioning.
We studied land‐use‐induced changes in below‐ground communities in tropical lowland ecosystems in Sumatra (Jambi province, Indonesia), a hot spot of tropical rainforest conversion into rubber and oil palm plantations. The study included ca. 30,000 measured individuals from 33 high‐order taxa of meso‐ and macrofauna spanning eight orders of magnitude in body mass. Using individual body masses, we calculated the metabolism of trophic guilds and used food web models to calculate energy fluxes and infer ecosystem functions, such as decomposition, herbivory, primary and intraguild predation.
Land‐use change was associated with reduced abundance and taxonomic diversity of soil invertebrates, but strong increase in total biomass and moderate changes in total energy flux. These changes were due to increased biomass of large‐sized decomposers in soil, in particular earthworms, with their share in community metabolism increasing from 11% in rainforest to 59%–76% in jungle rubber, and rubber and oil palm plantations. Decomposition, that is the energy flux to decomposers, stayed unchanged, but herbivory, primary and intraguild predation decreased by an order of magnitude in plantation systems. Intraguild predation was very important, being responsible for 38% of the energy flux in rainforest according to our model.
Conversion of rainforest into monoculture plantations is associated by an uneven loss of size classes and trophic levels of soil invertebrates resulting in sequestration of energy in large‐sized primary consumers and restricted flux of energy to higher trophic levels. Pronounced differences between rainforest and jungle rubber reflect sensitivity of rainforest soil animal communities to moderate land‐use changes. Soil communities in plantation systems sustained high total energy flux despite reduced biodiversity. The high energy flux into large decomposers but low energy fluxes into other trophic guilds suggests that trophic multifunctionality of below‐ground communities is compromised in plantation systems.
The study links size spectrum, energy fluxes and diversity of soil invertebrate communities under the massive land‐use change in Indonesia. Energy in soil food webs of plantations is sequestered in large decomposers and does not reach high trophic levels, which may compromise stability and multifunctionality of these systems.
Animals that have similar morphological traits are expected to share similar ecological niches. This statement applies to individual animals within a species and thus species often serve as the ...functional units in ecological studies. Species are further grouped into higher‐ranked taxonomic units based on their morphological similarity and thus are also expected to be ecologically similar. On the other hand, theory predicts that strong competition between closely related species may result in differentiation of ecological niches. Due to high diversity and limited taxonomic expertise, soil food webs are often resolved using supraspecific taxa such as families, orders or even classes as functional units.
Here, we tested the trophic differentiation and consistency of supraspecific taxa across major lineages of temperate forest soil invertebrates: Annelida, Chelicerata, Myriapoda, Crustacea and Hexapoda. Published data on stable isotope compositions of carbon and nitrogen were used to infer basal resources and trophic level, and explore the relationship between taxonomic and trophic dissimilarity of local populations.
Genera and families had normal and unimodal distributions of isotopic niches, suggesting that supraspecific taxa are trophically consistent. The isotopic niche of local populations varied considerably resulting in large overlap of niches among species. Within the same genus, the effect of species identity on stable isotope composition of populations was not significant in 92% of cases. More than 50% of the variability in Δ15N values (trophic level) across lineages was explained by classes and orders, while the variability in Δ13C values (basal resources) was explained mostly by families and genera. The variability in stable isotope composition in Chelicerata and Hexapoda was explained by lower taxonomic ranks than in Myriapoda.
We compiled a comprehensive list of mean Δ13C and Δ15N values of invertebrate taxa from temperate forest soils allowing to refine soil food web models when measurements of trophic niches of local populations are not feasible. Supraspecific taxa are meaningful as trophic nodes in food web studies, but the consistency varies among taxa and the choice of taxonomic resolution depends on the research question; generally, identification of taxa should be more detailed in more diverse taxonomic groups.
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Plain Language Summary
Agricultural expansion is among the main threats to biodiversity and functions of tropical ecosystems. It has been shown that conversion of rainforest into plantations erodes biodiversity, but ...further consequences for food-web structure and energetics of belowground communities remains little explored. We used a unique combination of stable isotope analysis and food-web energetics to analyze in a comprehensive way consequences of the conversion of rainforest into oil palm and rubber plantations on the structure of and channeling of energy through soil animal food webs in Sumatra, Indonesia. Across the animal groups studied, most of the taxa had lower litter-calibrated Δ
C values in plantations than in rainforests, suggesting that they switched to freshly-fixed plant carbon ('fast' energy channeling) in plantations from the detrital C pathway ('slow' energy channeling) in rainforests. These shifts led to changes in isotopic divergence, dispersion, evenness, and uniqueness. However, earthworms as major detritivores stayed unchanged in their trophic niche and monopolized the detrital pathway in plantations, resulting in similar energetic metrics across land-use systems. Functional diversity metrics of soil food webs were associated with reduced amount of litter, tree density, and species richness in plantations, providing guidelines on how to improve the complexity of the structure of and channeling of energy through soil food webs. Our results highlight the strong restructuring of soil food webs with the conversion of rainforest into plantations threatening soil functioning and ecosystem stability in the long term.
Deforestation and land-use change in tropical regions result in habitat loss and extinction of species that are unable to adapt to the conditions in agricultural landscapes. If the associated loss of ...functional diversity is not compensated by species colonizing the converted habitats, extinctions might be followed by a reduction or loss of ecosystem functions including biological control. To date, little is known about how land-use change in the tropics alters the functional diversity of invertebrate predators and which key environmental factors may mitigate the decline in functional diversity and predation in litter and soil communities. We applied litter sieving and heat extraction to study ground spider communities and assessed structural characteristics of vegetation and parameters of litter in rainforest and agricultural land-use systems (jungle rubber, rubber, and oil palm monocultures) in a Southeast Asian hotspot of rainforest conversion: Sumatra, Indonesia. We found that (1) spider density, species richness, functional diversity, and community predation (energy flux to spiders) were reduced by 57–98% from rainforest to oil palm monoculture; (2) jungle rubber and rubber monoculture sustained relatively high diversity and predation in ground spiders, but small cryptic spider species strongly declined; (3) high species turnover compensated losses of some functional trait combinations, but did not compensate for the overall loss of functional diversity and predation per unit area; (4) spider diversity was related to habitat structure such as amount of litter, understory density, and understory height, while spider predation was better explained by plant diversity. Management practices that increase habitat-structural complexity and plant diversity such as mulching, reduced weeding, and intercropping monocultures with other plants may contribute to maintaining functional diversity of and predation services provided by ground invertebrate communities in plantations.
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.
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