Uncovering trophic positions and food resources of soil animals using bulk natural stable isotope composition

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 C as compared to plant litter. This 'detrital shift' likely reflects preferential uptake of C-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 N and C relative to leaf litter. Decomposers inhabiting mineral soil layers therefore might be enriched in N resulting in overlap in isotope ratios between soil-dwelling detritivores and litter-dwelling predators. By contrast, C 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 mi...

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

“…This is in line with previous studies reporting that Diplopoda typically function as primary decomposers by feeding on plant litter (Bonkow, Scheu, & Schaefer, Scheu & Schaefer, 1998;Cárcamo, Abe, Prescott, Holl, & Chanway, 2000). High 13 C and low 15 N enrichment indicates that litter-dwelling Diplopoda likely assimilate plant material colonized by saprotrophic fungi (Potapov, Semenina, Kurakov, & Tiunov, 2013;Potapov, Tiunov, & Scheu, 2018;Semenyuk, Tiunov, & Golovatch, 2011). High 13 C and low 15 N enrichment indicates that litter-dwelling Diplopoda likely assimilate plant material colonized by saprotrophic fungi (Potapov, Semenina, Kurakov, & Tiunov, 2013;Potapov, Tiunov, & Scheu, 2018;Semenyuk, Tiunov, & Golovatch, 2011).…”

Trophic consistency of supraspecific taxa in below‐ground invertebrate communities: Comparison across lineages and taxonomic ranks

“…This distinction explained more than 70% of all variability in trophic levels within the subphylum, while low‐rank classifications explained only a small part. Arachnida in our dataset comprised Oribatida, predominantly living as detritivores and fungal feeders, and Mesostigmata and Araneae living as predators (but the latter two orders were distinct in Δ 13 C values, suggesting the use of different basal resources; Potapov, Tiunov, et al, ). In Hexapoda, the trophic niche varied between classes (Insecta vs. Collembola) and also between orders.…”

“…Since we analysed a taxonomic rather than a phylogenetic tree, our conclusions about evolutionary aspects of trophic‐niche conservatism are limited. However, similar Δ 13 C values across different taxa suggest that different types of organic compounds, such as plant tissues or microbially processed detritus (Potapov, Tiunov, et al, ), are utilized by an array of different lineages of consumers resulting in functional redundancy of high‐rank taxa. Resource specialization such as feeding on different organic matter compounds therefore is unlikely to drive principal evolutionary adaptations in soil invertebrates, suggesting that it is relatively easy to switch between herbivory and detritivory or between preying on herbivores and decomposers.…”

“…The analysis was based on a large compilation of published data on stable isotope composition of soil invertebrates from temperate forests (Potapov, Tiunov, et al, ). In the dataset, only records identified to species or genus level were included resulting in 415 species from 21 orders and five high‐rank taxa: Annelida, Chelicerata, Myriapoda, Crustacea and Hexapoda (Supporting Information Table S1).…”

“…Although natural variations in stable isotope ratios of carbon ( 13 C/ 12 C) and nitrogen ( 15 N/ 14 /N) cannot identify the exact trophic interactions between species, they indicate species that are similar or different in their trophic position and use of basal resources, thus representing key trophic‐niche dimensions (Martinez del Rio, Wolf, Carleton, & Gannes, ; Newsome, Martinez del Rio, Bearhop, & Phillips, ; Rodríguez & Herrera, ). In particular in soil food webs, 13 C concentrations increase with decomposition of plant material, while 15 N concentrations increase with trophic level (Potapov, Tiunov, & Scheu, ). Based on this methodological framework, we analysed published data on stable isotope composition of carbon and nitrogen to explore the trophic niches (i.e., trophic links to plant material of different stages of decomposition and trophic level) of major below‐ground arthropod lineages at different taxonomic levels.…”