SSS4.2

Soil fauna is a key control of the decomposition rate of leaf litter, yet its interactions with litter quality and the soil environment remain elusive. We conducted a litter decomposition experiment across different topographic levels within the landscape replicated in two rainforest sites providing natural gradients in soil fertility to test the hypothesis that low nutrient availability in litter and soil increases the strength of fauna control over litter decomposition. We crossed these data with a large dataset of 44 variables characterizing the biotic and abiotic microenvironment of each sampling point and found that microbe-driven Carbon (C) and Nitrogen (N) losses from leaf litter were 10.1 and 17.9 % lower, respectively, in the nutrient-poorest site but this among-site difference was equalized when meso- and macrofauna had access to the litterbags. Further, on average soil fauna enhanced the rate of litter decomposition by 22.6%, and this contribution consistently increased as nutrient availability in the microenvironment declined. Our results indicate that nutrient scarcity increases the importance of soil fauna on C and N cycling in tropical rainforests. Further, soil fauna is able to equalize differences in microbial decomposition potential thus buffering to a remarkable extent nutrient shortages at an ecosystem level.

How to cite: Peguero, G., Sardans, J., Richter, A., Janssens, I., and Peñuelas, J.: Nutrient scarcity strengthens soil fauna control over leaf litter decomposition in tropical rainforests, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-747, https://doi.org/10.5194/egusphere-egu22-747, 2022.

Millipedes, one of the most important detritivores in nature, host a community of microorganisms in their guts that may contribute to their nutrition and overall fitness. However, it remains unclear to what extent do millipedes depend on their microbiome. We evaluated the degree of dependence of methane and non-methane releasing millipedes on their gut microbiome using an experimental approach combining chemical inhibitors, microscopy, stable-isotope probing and meta-omics. First, we used either antibiotics or the methanogenesis inhibitor 2-bromoethanesulphate (BES) on juvenile Epibolus pulchripes (topical; methane releasing) and Glomeris connexa (European; non-methane releasing) to suppress microbial activity. Antibiotics had a large and significant effect on the number of faecal pellets and bacterial plate counts but did not achieve sterilization. It also reduced the weight and CH₄ output in E. pulchripes but did not stop it. BES completely inhibited CH₄ production, but recovery was observed after 14-days of feeding on untreated leaves. BES also reduced the abundance of the functional gene for methanogenesis in the faeces—mcrA—but did not affect their weight or faecal pellet production. While the hindguts of antibiotic-treated E. pulcripes and G. connexa were dominated by Bacteroidota and Proteobacteria, the faeces were dominated by Proteobacteria according to the 16S rRNA amplicon sequencing analysis. Light microscopy and catalysed reporter deposition fluorescence in situ hybridization (CARD-FISH) showed that E. pulchripes harbour a multitude of ciliates with ecto- and endo-symbiotic methanogens belonging to Methanobacteriales and Methanomassilicoccales. Surprisingly, these methanogens were still detectable at similar numbers even when methanogenesis was entirely suppressed. We also used RNA stable isotope probing (RNA-SIP) in conjunction with metagenomics to identify key microbial players in the hindguts and distinguish the microbial metabolic potentials of the two millipede species. RNA-SIP results indicated slow labelling of the bacteria over several weeks, with only a few phyla labelled during the first week of feeding on ¹³C-labelled poplar leaves. We recovered 305 high-quality MAGs (E. pulchripes - 282 and G. connexa - 33) with ≥ 50% completeness using metagenomics, comprising 18 prokaryotic phyla (E. pulchripes - 18 and G. connexa - 5). In addition, the MAGs contained some novel bacteria along with some known members of the termite gut microbiota. The results from reconstructed metabolic pathways indicate that the potential role of hindgut bacteria is carbohydrate metabolism, followed by energy metabolism, lipid metabolism, nucleotide metabolism and amino acid metabolism. Analysis of the metatranscriptome is currently ongoing. Overall, we conclude that while the microbiome is beneficial for the millipede and its composition reflects the prevailing conditions in the gut, it is not essential. Instead, it seems that unlike other methane-releasing animals like termites or ruminants, the millipedes are not dependent on the fermentation products of microorganisms for their nutrition. Together, these results contribute to our understanding of the millipede microbiota and represent the largest genomic resource available to date. 

How to cite: Eyiuche Nweze, J., Gupta, S., Horváthová, T., Šustr, V., and Angel, R.: Do methane and non-methane releasing millipedes depend on their gut microbiome to digest leaf litter?, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-1603, https://doi.org/10.5194/egusphere-egu22-1603, 2022.

Microbial necromass is regarded as a central pool of soil organic carbon, whose management is critical in efforts to reduce atmospheric CO₂ concentrations and mitigate climate change. However, recent concepts on soil organic matter formation have ignored one of the most important factors for the formation and stabilization of microbial necromass in many soils: earthworms. Based on recent evidence, we conceptualize how the ingestion and mixing of mineral particles and organic matter by earthworms temporarily convert the egested soil to a hotspot of quick and efficient microbial growth and turnover, in which increased amounts of necromass tightly bind to mineral surfaces and stabilize within aggregates. We further stress the low dependence of this process on the quality of pre-existing soil organic matter (in contrast to the assumptions of recent concepts) and its high relevance to the resilience of soil carbon to external disturbances in extensive regions of the soil remote from classical hotspots of microbial necromass formation. We finally provide suggestions on how to close remaining research gaps.

How to cite: Angst, G., Frouz, J., van Groenigen, J. W., Scheu, S., Kögel-Knabner, I., and Eisenhauer, N.: Aligning earthworm activity and microbial necromass formation in mineral soil, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-13493, https://doi.org/10.5194/egusphere-egu22-13493, 2022.

Negative Emission Technologies (NETs) are urgently needed if we want to keep global temperature increase below 1.5 °C. Enhanced Silicate Weathering (ESW) is a NET with as yet unknown potential to mitigate climate change. There are indications that ESW rates can be amplified by biotic activity, including that of earthworms. Earlier studies have suggested various pathways through which earthworms might enhance weathering rates, including the grinding of minerals in their gizzard, the stimulation of microbial communities in their gut, as well as the production of mucus rich in organic acids and digestive enzymes. Within this research, we aim to unravel the mechanisms through which earthworms increase mineral weathering rates, and ultimately to develop a bio-reactor in which these processes are optimized. As a first step, we carried out two experiments to determine the suitability of two earthworm species and to establish the optimal conditions for earthworms and mineral weathering in a small bio-reactor. The first study tested the potential of two endogeic earthworm species, Aporrectodea caliginosa and Allolobophora chlorotica, in a system with two types of rock flours (dunite and basalt) and three organic sources (hay, straw and co-digestate solid). The results showed that both earthworm species can thrive and remain active in the bio-reactor in the presence of basalt mixed with either co-digestate or straw. In the second study we tested the tolerance of the same two earthworm species to two temperatures exceeding earthworms ambient levels (20°C and 25°C) and two flow rates (50 ml/day and 80 ml/day) in a system with basalt and straw. The results showed that both earthworm species can survive and remain active at the highest temperature level and the highest flow rate. Our findings demonstrate that earthworms are suitable for use in a bio-reactor and can tolerate physical conditions which are known to stimulate weathering. Future studies will elucidate to what extent earthworms can enhance weathering.

How to cite: Calogiuri, T., Garamszegi, P., Vidal, A., van Groenigen, J. W., and Hagens, M.: Can earthworms enhance mineral weathering and thereby increase carbon sequestration? , EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-5706, https://doi.org/10.5194/egusphere-egu22-5706, 2022.

Earthworms are newcomers to South-Eastern Canada, as they were unable to survive the last glaciation period that ended about 11,000 years ago. Since their introduction by Europeans over recent centuries, these exotic earthworm species have substantially affected pedological processes and soil functions. For example, a recent study in the province of Quebec found that earthworms invading native sugar maple (Acer saccharum Marsh.) forests could potentially increase soil nitrous oxide (N₂O) emissions by increasing denitrification rates. However, the underlying microbial mechanisms driving the production of this greenhouse gas via denitrification remain unclear. This led us to conduct field and laboratory studies in order to explore whether earthworms preferentially promote bacterial and/or fungal denitrification pathways. We measured earthworm abundance and collected surface mineral soil samples from 38 sugar maple forests, half of which were earthworm-free. In each soil sample, we measured fungal, bacterial and total microbial biomass by substrate-induced respiration, we measured fungal, bacterial and total denitrification by acetylene inhibition, and we quantified the abundance bacterial (nirK, nirS and nosZ) and fungal (P450nor) denitrifying genes by qPCR. Earthworm abundance correlated positively with bacterial as well as fungal biomass, but did not affect the bacterial-to-fungal biomass ratio. Accordingly, bacterial-mediated and fungal-mediated denitrification rates both increased with the abundance of earthworms. However, earthworm abundance correlated positively with the specific bacterial denitrification rate (SBDR = (bacterial-mediated denitrification rate) ÷ (bacterial biomass)), but not with the specific fungal denitrification rate (SFDR = (fungal-mediated denitrification rate) ÷ (fungal biomass)). Moreover, qPCR analyses showed a positive correlation between earthworm abundance and the proportion of all bacterial denitrifying genes in the microbial population, but no such effect on fungal denitrifying genes. Taken collectively, our results suggest that earthworms may increase N₂O emissions in sugar maple forest soils by preferentially promoting the bacterial-mediated denitrification pathway.

How to cite: Villeneuve, C., Bradley, R., and Beauregard, P. B.: Evidence that invasive earthworms promote bacterial-mediated nitrous oxide emissions in forest ecosystems, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-6069, https://doi.org/10.5194/egusphere-egu22-6069, 2022.

The arthropod family Scarabaeidae is estimated to consist of over 30,000 species worldwide, including important pests. Their larvae – commonly known as white grubs – are often part of the soil decomposer community feeding on living plant roots, plant residues as well as faeces. As a result, scarab beetle larvae have the potential to directly and indirectly affect the spatial and temporal variability of soil greenhouse gas (GHG) fluxes, especially through their capability to emit significant amounts of CH₄. However, due to a lack of field data (Görres & Kammann 2020), little is known about their quantitative impact on soil GHG budgets. We conducted a mesocosm experiment with common cockchafer larvae (Melolontha melolontha) with the twofold aim to better understand their effect on soil CO₂, CH₄ and N₂O fluxes as well as the methodological challenges associated with studying this soil fauna group under field conditions. The experiment was conducted in Germany (temperate zone) over an entire vegetation period in mesocosms with three different vegetation types (grassland, grassland + carrots, and carrots, respectively) and three different larval infestation rates (0, 8, and 16 larvae m^-2, respectively). Greenhouse gas flux measurements were conducted with the static chamber method on a monthly basis, including the use of isotopic labels to focus especially on gross soil CH₄ fluxes. In this presentation, we will focus on the methodological difficulties encountered during the experiment and the potential of field-based isotope pool dilution techniques for non-invasive studies of scarab beetle larval CH₄ emissions.

This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 703107.

Reference

Görres, C.-M., Kammann, C. (2020). First field estimation of greenhouse gas release from European soil-dwelling Scarabaeidae larvae targeting the genus Melolontha. PLoS ONE 15(8): e0238057, doi 10.1371/journal.pone.0238057.

How to cite: Görres, C.-M. and Kammann, C.: Studying the effect of scarab beetle larvae on soil greenhouse gas fluxes in a mesocosm experiment, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-10525, https://doi.org/10.5194/egusphere-egu22-10525, 2022.

Summer droughts strongly affect soil organic carbon (SOC) cycling, but net effects on SOC storage are unclear as drought affects both C inputs and outputs from soils. Here, we explored the overlooked role of soil fauna on SOC storage in forests, hypothesizing that soil fauna is particularly drought-sensitive, thereby reducing litter incorporation into the mineral soil and, eventually, long-term SOC storage.

In a drought-prone pine forest (Switzerland), we performed a large-scale irrigation experiment for 17 years and assessed its impact on vertical SOC distribution and composition. We also examined litter decomposition of dominant tree species using litterbags of different mesh sizes and determined soil fauna abundance and community composition.

Long-term irrigation resulted in a C loss in the organic layers (-1.0 kg C m^-2) and a comparable C gain in the mineral soil (+0.8 kg C m^-2) in the first decade of irrigation, and thus did not affect total SOC stocks. Irrigation increased the mass loss of Quercus pubescens and Viburnum lantana leaf litter more strongly when meso- and macrofauna were included (+215%) compared to excluded (+44%). The enhanced faunal-mediated litter decomposition was paralleled by a many-fold increase in the abundance of meso- and macrofauna during irrigation. Moreover, irrigation led to a shift in Acari and Collembola community composition, with irrigation characterized by the presence of drought-sensitive species. In comparison, microbial SOC mineralization was less responsive to lower soil moisture. Our results suggest that the vertical redistribution of SOC with irrigation was mainly driven by litter incorporation through meso- and macrofauna, here accelerated by irrigation and suppressed by naturally occurring summer droughts.

Our study shows that soil fauna is highly sensitive to natural drought reducing the incorporation of C from organic layers to the mineral soil. In the longer term, this potentially affects SOC storage, decreasing the C stored in mineral soil. Therefore, soil fauna plays a key but so far largely overlooked role in shaping SOC responses to drought.

How to cite: Guidi, C., Frey, B., Brunner, I., Meusburger, K., Vogel, M., Chen, X., Stucky, T., Gwiazdowicz, D. J., Skubała, P., Schaub, M., Rigling, A., and Hagedorn, F.: Soil fauna drives vertical redistribution of soil organic carbon by long-term irrigation in a dry pine forest, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-4828, https://doi.org/10.5194/egusphere-egu22-4828, 2022.

In the search for a more sustainable form of agriculture, a better recycling of major nutrients is essential. For phosphorus (P), one of the most limiting factors to better recycling is chemical adsorption to reactive soil particles, which seriously restricts P supply to plants in many soils. It has been known for some time that earthworms can temporarily increase soil P availability in their casts. However, the exact pathways behind this effect are unclear, making it difficult to infer under which conditions earthworms may significantly contribute to P recycling. In two greenhouse experiments, we studied the occurrence of earthworm-induced increased P availability (i) across a range of common earthworm species; and (ii) across four soils with different physico-chemical characteristics. In the first experiment we analyzed casts of eight common Dutch earthworm species for P pools and related soil properties. For all species, pH in casts was higher than in the bulk soil (up to 1.6 pH unit). Dissolved Organic Carbon (DOC) concentrations were an order of magnitude higher in the casts, and directly available P (defined as water-soluble ortho-phosphate) up to two orders of magnitude. Although these effects were significant for all earthworm species, significant changes were found between the species that could not be explained by conventional earthworm feeding guilds. In the second experiment, we tested effects of three different earthworm species across four soils differing in texture, metal oxide composition, P availabilty and pH. We found a significant effect of earthworms on P availability in all soils, but the extent of this effect varied. Using surface complexation modeling we evaluated the relative importance of the various possible mechanisms. We concluded that the effect of pH on P desorption was relatively small. Increased mineralization of organic P did play an important role; as did competitive desorption of DOC to metal oxides. However, our study also showed a new important pathway: a reduction in reactive surface area of soil metal (hydr)oxides during earthworm gut passage. As this decrease was important in iron (hydr)oxide-dominated soils but not in aluminum (hydr)oxide-dominated soils, we suggest that earthworms have the largest potential to affect soil P availability in the former soils.

How to cite: Van Groenigen, J. W., Vos, H. M. J., Hiemstra, T., and Koopsman, G. F.: Through which pathways can earthworms increase soil phosphorus availability?, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-13417, https://doi.org/10.5194/egusphere-egu22-13417, 2022.

The role of earthworms on biogeochemical carbon cycling is a major knowledge gap resulting from the difficulty of isolating and exploring the effects provided by the diversity of organisms. In this study, we investigated the effect of six earthworm species belonging to three ecological categories on soil organic carbon (SOC) mineralisation. To this end, we produced casts with the six species using subsoil material with low SOC content and miscanthus litter. Cast were subjected to laboratory ageing for 140 days. During this process, we monitored physicochemical parameters, CO₂ emissions and determined the micro-scale organisation of the casts’ particulate organic matter and pores using X-ray tomography.

Our results showed contrasting properties of fresh casts from the 3 main ecological categories, in accordance with the earthworm species’ morphological or behavioral strategies, indicating that those were maintained in artificial environments. However, species-specific changes in cast properties throughout ageing increased intragroup variability among ecological categories. As a result we observed earthworm species-specific evolution of CO₂ mineralisation rates during casts ageing. We found that at least half of the variability in CO₂ emissions was explained by cast microstructural changes, related to the spatial arrangement between particulate organic matter, porosity, and mineral particles. We conclude that earthworm species-specific traits may play a role in organic carbon protection through their impact on microstructural cast properties.

How to cite: Le Mer, G., Bottinelli, N., Dignac, M.-F., Capowiez, Y., Jouquet, P., Mazurier, A., Baudin, F., Caner, L., and Rumpel, C.: Exploring the control of earthworm cast macro- and micro-scale features on soil organic carbon mineralisation across species and ecological categories, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-5216, https://doi.org/10.5194/egusphere-egu22-5216, 2022.

Earthworm activities in soil generate biogenic aggregates (casts), the mass of which can reach up to 30 - 50t/ha. The dynamics of organic matter (OM) is strongly constrained (accessibility, O₂ content, etc.) within these structures and they tend to have high OM contents. As a result of their large mass and high OM contents, these aggregates can have significant effects on OM dynamics and protection over distinct time scales: (i) over the short term, earthworms increase OM mineralization through their own metabolic processes and by stimulating soil microbial activity, the so-called priming effect; (ii) over longer terms, during cast ageing, a new equilibrium may be reached, leading to the protection of the incorporated OM. However few incubation studies have been conducted for more than three months. Consequently, the net influence of earthworm’s casts on the OM dynamics is still poorly understood and remains to be determined.

Our objective was to estimate whether the incorporation of fresh OM into casts leads to its protection or to an enhanced degradation during the period of cast ageing. To do so, we compared the fate of ¹³C labeled fresh OM added to bulk soil to the fate of fresh OM ingested by earthworms (L. Terrestris) in mesocosms, and monitored OM mineralization during one year. The incorporation of fresh OM into casts was also determined as were the microbial communities involved in the consumption of labelled OM (via ¹³C-phospholipid fatty acid analysis). In addition, the OM stability was estimated as the proportion of mineral associated.

The results showed that fresh OM was largely incorporated into casts, with significant differences in the mineralization rates obtained for the OM incorporated into the soil, compared with that incorporated into the casts. This difference decreased over time, as the casts aged. Fungal activity was lower when OM was incorporated in casts. In conclusion, earthworms influence the fate of fresh OM in soil by delaying its mineralization but do not lead to long-term stabilization.

How to cite: Quenea, K., Nunan, N., Lerch, T., Chenu, C., Aubry, E., Pouteau, V., Plessis, C., and Leloup, J.: Distinct patterns of change of organic matter in bulk soil or in earthworm casts during ageing, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-13352, https://doi.org/10.5194/egusphere-egu22-13352, 2022.

Earthworms have a positive effect on plant growth; this is typically attributed to increased N availability. Earthworms can also increase Si availability; plant Si plays a role in drought tolerance. Finally, earthworms effect microfaunal diversity. We conducted a glasshouse experiment to investigate interactions between these factors. Wheat varieties (Skyfall and four ancient strains) were grown in a greenhouse under presence / absence of adult Allolobophora chlorotica and no-drought / drought watering regimes (39 days watering then a further 17 days of watering or no watering).

Despite earthworm aestivation in drought treatments, plant growth was greater in both the no-drought and drought treatments.

Plant %N was greater in the watered treatments; for the drought treatments, it was greater in the earthworm-present treatments. Plant %C was greater in the earthworm-present treatments. In the earthworm-absent treatments Plant %P and %Si was greater in the watered treatments. In the watered treatments %P and %Si was greater in the absence of earthworms.

Soil pH (c. 8.1) was slightly decreased in the earthworm-present and in the watered treatments. The watered treatments contained more extractable nitrate. Extractable P showed no difference across treatments. The droughted earthworm-present treatments contained more extractable Si than both the earthworm-present watered treatments and earthworm-absent drought treatments.

Different wheat strains behaved similarly with Skyfall showing greater biomass and, sometimes, elemental concentrations.

Bacterial and fungal beta-diversity varied with both watering and earthworm treatments; fungal diversity also varied between wheat strains.

Plants showed significant differences in RNA expression between both watering and earthworm treatments including for genes linked to N uptake.

Earthworms promoted plant growth under both watered and drought conditions. Under drought conditions this does not appear to be related to Si availability or uptake. Similarly we observed no simple relationship between earthworm-presence, N (or P) and plant growth though under drought conditions the presence of earthworms promoted growth and %N in the plants despite lower extractable nitrate. The RNA response of plants suggests a N-related effect perhaps mediated by changes in microbial diversity.

How to cite: Hodson, M., Brailey-Jones, P., Burns, W., Harper, A., Hartley, S., Helgason, T., and Walker, H.: Earthworm-plant-microbiota interactions, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-2974, https://doi.org/10.5194/egusphere-egu22-2974, 2022.

Soil fauna can support soil organic matter storage. Important mechanisms facilitation this effect is connected with bioturbation and mixing of organic matter with clay particles which can stimulate accumulation of microbial necromass on mineral surfaces as shown in earthworms. However it has been show that also litter feeding fauna which do not ingest mineral soil may slow down organic matter decomposition and support carbon storage. In this contribution we bring overview of potential mechanisms that may be responsible for this phenomena. Decreased decomposition rate in fauna excrements might result from the removal of easily available polysaccharides, the increase in aliphatic components, an increase in the resistant components of lignin, the accumulation of microbial cell walls (microbial necromass) by increasing of microbial turnover, by binding of nitrogen into complexes with aromatic components, which reduce N availability an finally by higher availability of nitrogen in leachate coming from fauna excrements which may cause negative priming effect and slow down decomposition. These mechanisms will be illustrated on examples and their implication of carbon sequestration will be discussed.

How to cite: Frouz, J.: How litter feeding arthropods can promote carbon sequestration, EGU General Assembly 2022, Vienna, Austria, 23–27 May 2022, EGU22-11026, https://doi.org/10.5194/egusphere-egu22-11026, 2022.