The flux of root-derived carbon via fungi and bacteria into soil microarthropods (Collembola) differs markedly between cropping systems
Introduction
A considerable amount of plant photosynthates is transferred to roots shortly after being fixed from the atmosphere and is released into the soil as rhizodeposits (Dennis et al., 2010; Pausch and Kuzyakov, 2018). This root-derived carbon (C), mainly comprising low molecular substances such as sugars, amino acids, and organic acids, is the major C source for soil microorganisms (Anderson et al., 1993; Buée et al., 2009). Root-derived C fluxes thereby regulate a wide range of soil ecological processes and accelerate the cycling of virtually all elements (Kuzyakov, 2002). Although soil microorganisms are the primary consumers of rhizodeposits, their activity and biomass, and thereby C fluxes to higher trophic levels, are significantly influenced by microbial grazers, such as nematodes and springtails (Collembola) (Maboreke et al., 2017; Ngosong et al., 2014). However, as soil food webs are highly complex with considerable proportions of generalist consumers (Digel et al., 2014; Scheu, 2002), trophic links between microorganisms and higher trophic levels in food webs are difficult to disentangle.
Collembola are important members of soil food webs, contributing to C transport at the litter-soil interface (Ruf et al., 2006), and channeling C and nutrients from basal resources, including bacteria, fungi, and plants, to higher trophic levels (Liu et al., 2016; Oelbermann et al., 2008). Collembola heavily rely on root-derived C (Garrett et al., 2001; Larsen et al., 2007; Pollierer et al., 2007; Scheunemann et al., 2015), potentially due to their high preference for root-associated microorganisms (Maboreke et al., 2017; Ostle et al., 2007). Collembola incorporate root-derived C from different channels based on bacteria, fungi, and plants (Crotty et al., 2011; Pollierer et al., 2012), and change diet according to resource availability (Eerpina et al., 2017; Endlweber et al., 2009; Scheunemann et al., 2015). However, determinants of the variation in dietary composition of Collembola between cropping systems and its dependence on differences in microbial resources, especially those utilizing root-derived C, are not well studied.
The incorporation of root-derived C into microbial groups varies between cropping systems, due to differences in plant species, and soil chemical and physical conditions (Sechi et al., 2014; Zieger et al., 2017). Therefore, the channeling of root-derived C into Collembola and higher trophic levels of soil food webs likely also varies between cropping systems. For instance, trees and grasses allocate high amounts of C to roots and rhizodeposits, which are used by mycorrhizal and saprotrophic fungi (De Deyn et al., 2011; Denef et al., 2007; Zieger et al., 2017). By contrast, bacteria are likely to be important in channeling root-derived C to higher trophic levels in more intensively managed systems, with their relative importance affected by crop species and management practices (Elfstrand et al., 2008; Pausch et al., 2016a, b). For instance, some crop species, such as oilseed rape, do not form mycorrhizal associations and accumulate secondary compounds that are toxic to saprotrophic fungi in their rhizosphere (Kirkegaard and Sarwar, 1998; Okubo et al., 2016), which may facilitate the utilization of root-derived C by bacteria.
Collembola species with different functional traits dwell in different soil depth, likely resulting in differential incorporation of root-derived C from bacterial and fungal channels. Epedaphic Collembola are surface-dwelling species inhabiting the upper litter layer, where they may incorporate root-derived C from the fungal channel since fungal hyphae transfer root-derived C from rhizosphere to bulk soil and litter (Klironomos and Kendrick, 1995). By contrast, hemiedaphic and euedaphic Collembola inhabiting the lower litter layer and mineral soil (Potapov et al., 2016) are more likely to access microbial resources in the rhizosphere, and to incorporate root C from both bacterial and fungal channels.
Fatty acid (FA) analysis provides biomarkers for basal resources such as bacteria, fungi, and plants, allowing to detail the trophic links between Collembola and basal resources (Chamberlain et al., 2004; Ruess et al., 2007; Ruess and Müller-Navarra, 2019). The principle of FA analysis is based on “dietary routing”; to save energy, consumers incorporate FAs from the diet, such as microbial phospholipid fatty acids (PLFAs), into storage lipids, i.e. neutral lipid fatty acids (NLFAs), without major modification (Blem, 1976). Therefore, trophic links of consumers to basal resources can be traced by measuring the proportion of specific biomarkers in NLFAs of consumers. In labeling experiments, or when resources differ in isotopic composition (Ngosong et al., 2014; Pollierer et al., 2012; Scheunemann et al., 2016), stable isotope ratios of C within these biomarkers can provide information on the flux of C through specific energy channels or compartments of soil food webs. Previous studies have shown that Collembola gain plant C via consumption of bacteria, fungi, and roots (Ferlian et al., 2015; Haubert et al., 2009; Ngosong et al., 2011; Pollierer et al., 2012; Sechi et al., 2014). However, most studies analyzing natural abundance isotope ratios or long-term labeling experiments did not separate the flux of C from rhizodeposits from that of C from leaf or root litter. In pulse labeling studies, Collembola rapidly incorporated root-derived C, with peaks of label after three days (Garrett et al., 2001; Högberg et al., 2010; Zieger et al., 2017). Therefore, combining FA analysis with short-term oriented methods, such as 13C pulse labeling, may allow to separate the role of different basal resources in channeling root-derived C into soil food webs (Maboreke et al., 2017).
To investigate the relative importance of bacterial and fungal channels for the incorporation of root-derived C into Collembola, we pulse labeled three cropping systems in an agroforestry field with 13CO2 and traced the incorporation of root-derived C into biomarker NLFAs of five Collembola species belonging to epedaphic, hemiedaphic, and euedaphic groups. The three cropping systems included a herbaceous crop monoculture (oilseed rape, Brassica napus L.), a mixed-grass community (grassland dominated by Lolium perenne L. mixed with clover Trifolium repens L.), and a tree plantation (willow, Salix schwerinii E.L. Wolf and Salix viminalis L.). To investigate the incorporation of root-derived C from different basal resources into Collembola NLFAs, we employed 13C pulse labeling and compound-specific PLFA and NLFA analysis.
We tested the following hypotheses:
- i)
The relative importance of energy channels for the incorporation of root-derived C into Collembola differs among cropping systems, with higher incorporation of root-derived C from the bacterial channel in rape than in grass and willow, where fungi are the primary root-derived C source.
- ii)
Within the same cropping system, relative fluxes of root-derived C via the bacterial and fungal energy channels differ between Collembola functional groups, with higher relevance of the fungal channel for epedaphic Collembola, whereas hemiedaphic and euedaphic Collembola are more closely associated with bacterial resources.
Section snippets
Site description
The study sites were located in Reiffenhausen, south of Göttingen in central Germany (51°39′83″ N/9°98′75″ E a.s.l.). The mean annual precipitation is 635 mm and average annual temperature is 9.1 °C (Richter et al., 2015). The soil at the study sites is characterized by sedimentary deposits of Middle and Upper Triassic Sandstone material, partly mixed with claystone material and covered by loess sediments. The main soil types present are Stagnic Cambisol and Haplic Stagnosol. The texture of the
Incorporation of 13C
The 13C incorporation into NLFAs differed between biomarkers, cropping systems, and functional groups of Collembola (epedaphic: significant biomarker × cropping system interaction, F4,64 = 3.28, P = 0.017; hemi-/euedaphic: significant biomarker × cropping system × functional group interaction, F2,94 = 3.176, P = 0.046; Table S3). The incorporation of 13C into the bacterial biomarker NLFAs of Collembola differed significantly between cropping systems, with similar trends among functional groups
Incorporation of root-derived C into Collembola NLFAs
Despite Collembola are among the major microbivores in soil food webs, it is unknown to what extent trophic relationships between Collembola and microorganisms differ among cropping systems. Supporting our first hypothesis, the incorporation of root-derived C from bacterial and fungal channels into Collembola differed markedly between cropping systems, with more root-derived C channeled into the bacterial biomarker NLFAs in rape compared to grass and willow, where relatively more root-derived C
Conclusions
Results of the present study demonstrate that the flux of root C into soil microbivores via the bacterial and fungal energy channel strongly varies between cropping systems, with higher incorporation of root-derived C from the bacterial channel in rape than in the grass and willow systems, where the fungal channel dominates. The differences in dietary composition of Collembola among cropping systems mainly reflect the change of microorganisms in the rhizosphere but not in bulk soil, suggesting
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We gratefully acknowledge the China Scholarship Council (CSC) (201604910550) for supporting Z.L. M.M.P. has been funded by the DFG (MA 7145/1-1). Thanks to the support from the project “SIGNAL – sustainable intensification of agriculture through agroforestry”. Thanks to Nicole Scheunemann for help with the field sampling and guidance in Collembola identification, to Guido Humpert for guidance in NLFA extraction and measurement, to Jens Dyckmans and the team of the Centre for Stable Isotope
References (88)
- et al.
Changes in root-associated microbial communities are determined by species-specific plant growth responses to stress and disturbance
European Journal of Soil Biology
(2012) - et al.
Arbuscular mycorrhizal fungi and their associated microbial community modulated by Collembola grazers in host plant free substrate
Soil Biology and Biochemistry
(2014) - et al.
Understanding the legacy effect of previous forage crop and tillage management on soil biology, after conversion to an arable crop rotation
Soil Biology and Biochemistry
(2016) - et al.
Microbial community composition and rhizodeposit-carbon assimilation in differently managed temperate grassland soils
Soil Biology and Biochemistry
(2009) - et al.
The legacy effect of cover crops on soil fungal populations in a cereal rotation. Agriculture,
Ecosystems and Environment
(2016) - et al.
Carbon routes from decomposing plant residues and living roots into soil food webs assessed with 13C labelling
Soil Biology and Biochemistry
(2008) - et al.
Functional differences in the microbial processing of recent assimilates under two contrasting perennial bioenergy plantations
Soil Biology and Biochemistry
(2017) - et al.
Collembola switch diet in presence of plant roots thereby functioning as herbivores
Soil Biology and Biochemistry
(2009) - et al.
Trophic niche differentiation and utilisation of food resources in collembolans based on complementary analyses of fatty acids and stable isotopes
Soil Biology and Biochemistry
(2015) The role of Collembola in carbon and nitrogen cycling in soil
Pedobiologia
(2002)