Soil Collembola Research Articles

Effects of mycotoxin-producing fungi on the fitness and gut bacterial community of the soil springtail Folsomia candida.

Mycotoxin-producing fungi are widespread in nature and raise concerns for human and livestock health. Although they share the same ecosystem, interactions between mycotoxin-producing fungi and soil arthropods are not well understood. In this study, we report an unexpected finding that the soil arthropod Folsomia candida is rather tolerant to these mycotoxin-producing fungi. F. candida can survive solely on mycotoxin-producing fungi as a food source with reduced physiological parameters. Moreover, the gut microbial community is disturbed by mycotoxin-producing fungi, and some of the bacteria isolated from F. candida's gut can inhibit the growth of corresponding fungi. Notably, the altered physiological parameters and gut microbiota are restored when a normal diet is reintroduced, suggesting F. candida's resilience to mycotoxin-producing fungi. These findings clarify the impact of toxin-producing diets on F. candida, shedding light on how organisms can build resilience to environmental stimuli.

Microarthropod responses to fire: vegetation cover modulates impacts on Collembola and Acari assemblages in Mediterranean area

BackgroundIn the Mediterranean region, fire is a recurring disturbance that impacts both surface and underground organisms. While the effects on plants and surface animals are well-studied, the consequences for soil microarthropods are often overlooked. This research addresses the microarthropod responses to fire by comparing post-fire Collembola and Acari assemblages in soils with different vegetation covers. Three years post-fire, surface soils were sampled within the Vesuvius National Park (Southern Italy) from a total of 24 sites, comprising 6 sites each under holm oak (HO), pine (P), black locust (BL), and herbaceous (H) vegetation. Within each vegetation cover, sites were further categorized into three unburnt (NB) and three burnt (B) sites for comprehensive analysis. Collembola and Acari were extracted, identified at the family and suborder level, respectively and analyzed for density and taxa richness.ResultsThe results highlighted that fire alone did not impact microarthropod communities, but its effects varied according to the vegetation covers. Microarthropod abundance declined in burnt soils under P, and increased in burnt soils under BL. Furthermore, eu-edaphic organisms (Onychiuridae, Oribatida), typical of stable environments, decreased in soils under P, and increased in soils under black locust.ConclusionsFire impact on microarthropod communities changed according to the vegetation covers, highlighting the importance of considering vegetation type when managing post-fire landscapes. The rapid recovery of microarthropod communities under some vegetation covers suggests that fire may not universally impair soil biodiversity in Mediterranean environments.

Warming decreased plant litter decomposition by modulating soil fauna interactions in a Tibetan alpine meadow

Litter decomposition is a vital process for maintaining ecosystem carbon cycling. It is affected by soil fauna which are predators and decomposers of litter. However, how the interactions of soil fauna communities affect litter decomposition remains unclear under warming. Here, we conducted a five-year in-situ manipulative warming experiment by Open-Top Chamber (OTC) in an alpine meadow on the Tibetan Plateau to reveal how warming affects litter decomposition. The results demonstrated that warming decreased the litter decomposition rate by 29 %, the soil collembola abundance by 25 %, and the nematode abundance by 27 %. Nematode ecological indices remain stable but a shift in the decomposition of litter to the fungivores pathway under warming. The piecewise structural equation modelling result revealed that the combined reduction in soil collembola and nematodes synergistically leads to a massive decline in litter decomposition rate under warming. Our results highlight that the interactions of soil fauna can regulate litter decomposition under warming, and collembola abundance as the “speed-limiter” of litter decomposition. Therefore, the response of changes in soil fauna relationships to warming should be completely considered in future climate change modelling of the grassland carbon cycle.

Collembola and ants: Influence of trails of red wood ants (Formica lugubris) on the community of soil springtails

Red wood ants are keystone species in forest ecosystems. Because ants are active polyphagous predators, they control the abundance of other arthropods. In addition to direct effects on other species, there are a number of indirect effects caused by ants. In our study, we investigated the influence of ants on springtails, which they rarely come into contact with. Springtails have been set as a model group to assess the state of soil animals, since they are one of the most numerous and widespread groups of soil microarthropods. They are characterized by high sensitivity to environmental changes. The basic characteristics (abundance, species richness, and species diversity) of the springtail community and the response of certain species to the presence of ant trails have been studied. The total abundance and species richness of springtails decreased along ant trails. Among occurred species Parisotoma ParIsotoma notabilis, Lepidacyrtus lignorum, Isotomiella minor, Desoria tigrina, and Pseudasinella alba are the most numerous species both along ant trails and in control samples. There are no significant changes in species diversity (assessed by the Shannon-Weaver index). Species structure of springtail communities along ant trails and in control is different. Two groups of common Collembola species are identified: (1) increasing their numbers in the presence of ants, (2) on the contrary, decreasing. The presence of ants in a forest ecosystem influences the soil springtail community, although ant-Collembola interactions are indirect.

Karst landforms as microrefugia for soil Collembola: Open versus forested dolines

Enclosed surficial karst dolines are geomorphologically diverse habitats with the potential to strongly shape community structure and the distribution of functional groups of organisms. Forest habitats in karst landscapes are characterized by lower soil temperatures and microclimatic fluctuations compared to open habitats; therefore, they may provide favorable conditions for cold-adapted/psychrophilic species, which are highly vulnerable to climate warming. We compared the diversity and structure of soil Collembola communities at sites along microclimatic gradients in open and forested karst dolines. The effect of topography and related environmental conditions on the distribution of ecological groups of soil Collembola was analyzed, and the function of the dolines as potential climate refugia for psychrophilic arthropods was assessed. The karst dolines revealed significant habitat heterogeneity, including warm plateaus and S-facing slopes and colder and wetter bottoms and N-facing slopes. The inner sites of the dolines had an overall higher abundance and species richness compared to the plateau sites. Nonmetric multidimensional scaling ordination revealed a clear delimitation of Collembola communities in terms of warmer and cooler sites in the open dolines, while the forested dolines did not reveal such a clear pattern. The studied dolines showed a potential to serve as microrefugia in the context of global climate change. Dolines could support the long-term persistence of at least some species such as cold-adapted species. Karst dolines in the temperate zone play a key role in maintaining biodiversity; therefore, they should be central in biodiversity conservation programs.

Cadmium toxicity to and accumulation in a soil collembolan (Folsomia candida): major factors and prediction using a back-propagation neural network model.

Accurate prediction of cadmium (Cd) ecotoxicity to and accumulation in soil biota is important in soil health. However, very limited information on Cd ecotoxicity on naturally contaminated soils. Herein, we investigated soil Cd ecotoxicity using Folsomia candida, a standard single-species test animal, in 28 naturally Cd-contaminated soils, and the back-propagation neural network (BPNN) model was used to predict Cd ecotoxicity to and accumulation in F. candida. Soil total Cd and pH were the primary soil properties affecting Cd toxicity. However, soil pH was the main factor when the total Cd concentration was < 3mgkg-1. Interestingly, correlation analysis and the K-spiked test confirmed nutrient potassium (K) was essential for Cd accumulation, highlighting the significance of studying K in Cd accumulation. The BPNN model showed greater prediction accuracy of collembolan survival rate (R2 = 0.797), reproduction inhibitory rate (R2 = 0.827), body Cd concentration (R2 = 0.961), and Cd bioaccumulation factor (R2 = 0.964) than multiple linear regression models. Then the developed BPNN model was used to predict Cd ecological risks in 57 soils in southern China. Compared to multiple linear regression models, the BPNN models can better identify high-risk regions. This study highlights the potential of BPNN as a novel and rapid tool for the evaluation and monitoring of Cd ecotoxicity in naturally contaminated soils.

Molecular level toxicity effects of As(V) on Folsomia candida: Integrated transcriptomics and metabolomics analyses

Arsenic (As) is a widespread metalloid with well-known toxicity. To date, numerous studies have focused on individual level toxicity (e.g., growth and reproduction) of As to typical invertebrate springtails in soils, however, the molecular level toxicity and mechanism was poorly understood. Here, an integrated transcriptomics and metabolomics approach was used to reveal responses of Folsomia candida exposed to As(V) of 10 and 60 mg kg−1 at which the individual level endpoints were influenced. Transcriptomics identified 5349 and 4020 differentially expressed genes (DEGs) in low and high concentration groups, respectively, and the most DEGs were down-regulated. Enrichment analysis showed that low and high concentrations of As(V) significantly inhibited chromatin/chromosome-related biological processes (chromatin/chromosome organization, nucleosome assembly and organization, etc.) in springtails. At high concentration treatment, structural constituent of cuticle, chitin metabolic process and peptidase activity (serine-type peptidase activity, endopeptidase activity, etc.) were inhibited or disturbed. Moreover, the apoptosis pathway was significantly induced. Metabolomics analysis identified 271 differential changed metabolites (DCMs) in springtails exposed to high concentration of As. Steroid hormone biosynthesis was the most significantly affected pathway. Several DCMs that related to chitin metabolism could further support above transcriptomic results. These findings further extended the knowledge of As toxic mechanisms to soil fauna and offer important information for the environmental risk assessment.

Effects of common artificial sweeteners at environmentally relevant concentrations on soil springtails and their gut microbiota

Artificial sweeteners (AS) are extensively utilized as sugar substitutes and have been recognized as emerging environmental contaminants. While the effect of AS on aquatic organisms has garnered recent attention, their effects on soil invertebrates and gut microbial communities remain unclear. To address this knowledge gap, we exposed springtails (Folsomia candida) to both single and combined treatments of four typical AS (sucralose [SUC], saccharin [SAC], cyclamate [CYC], and acesulfame [ACE]) at environmentally relevant concentrations of 0.01, 0.1 and 1 mg kg−1 in soil. Following the first-generational exposure, the reproduction of juveniles showed a significant increase under all the AS treatments of 0.1 mg kg−1. The transcriptomic analysis revealed significant enrichment of several Kyoto Encyclopedia of Gene and Genome pathways (e.g., glycolysis/gluconeogenesis, pentose and glucuronate interconversions, amino sugar, and nucleotide sugar metabolism, ribosome, and lysosome) in springtails under all AS treatments. Analysis of gut bacterial microbiota indicated that three AS (SUC, CYC, and ACE) significantly decreased alpha diversity, and all AS treatments increased the abundance of the genus Achromobacter. After the sixth-generational exposure to CYC, weight increased, but reproduction was inhibited. The pathways that changed significantly (e.g., extracellular matrix-receptor interaction, amino sugar and nucleotide sugar metabolism, lysosome) were generally similar to those altered in first-generational exposure, but with opposite regulation directions. Furthermore, the effect on the alpha diversity of gut microbiota was contrary to that after first-generational exposure, and more noticeable disturbances in microbiota composition were observed. These findings underscore the ecological risk of AS in soils and improve our understanding of the toxicity effects of AS on living organisms.

Ecological functions of fungal sesquiterpenes in the food preference and fitness of soil Collembola.

Volatile organic compounds (VOCs) emitted by fungi play a key role in locating and selecting hosts for fungivorous arthropods. However, the ecological functions of many common VOC classes, such as sesquiterpenes, remain unknown. Mutants of Trichoderma virens, defective in the emission of most sesquiterpenes owing to the deletion of the terpene cyclase vir4, were used to evaluate the role of this compound class in the food preference and fitness of the soil Collembola Folsomia candida. Choice experiments with and without direct contact with fungal mycelium revealed that Collembola were preferentially attracted to Δvir4 mutants impaired in sesquiterpene synthesis compared to wild-type T. virens. Grazing by F. candida on the sesquiterpene deficient T. virens strain had no effect on Collembola survival, reproduction and growth compared to wild-type T. virens. The results suggest that sesquiterpenes play an important role in fungal defence as repellents, but not as deterrents or toxins, against fungivorous Collembola. Our research contributes to the understanding of ecological interactions between fungi and fungivorous arthropods, providing insights into the specific ecological functions of sesquiterpenes. The study has implications for chemical ecology and the dynamics of multitrophic interactions in soil ecosystems.

Glyphosate-Based Herbicide Formulations and Their Relevant Active Ingredients Affect Soil Springtails Even Five Months after Application

Glyphosate is the most widely used active ingredient (AI) in glyphosate-based herbicides (GBHs) worldwide and is also known to affect a variety of soil organisms. However, we know little about how the effects of glyphosate AIs differ from those of GBHs that also contain so-called inert co-formulants. We conducted a greenhouse experiment using the model cover crop white mustard (Sinapis alba) to investigate the effects of three GBHs (Roundup PowerFlex, Roundup LB Plus, and Touchdown Quattro) and their respective glyphosate AIs (glyphosate potassium, isopropylamine, and diammonium salt) on epedaphic springtails (Sminthurinus niger; Collembola) activity in soils with low (3.0%) or high (4.1%) organic matter content (SOM). Springtail activity was assessed using pitfall traps. Most GBHs and AIs reduced springtail activity compared to mechanical removal of mustard in the short-term and even up to 5 months after application. GBHs and AIs differed considerably in their effects on springtail activity, and effects were modified by SOM content. Our results highlight the need to (i) distinguish between the effects of glyphosate AIs and commercial GBH formulations, (ii) disclose all ingredients of GBHs, as co-formulants also affect non-target organisms, and (iii) include soil properties in ecotoxicological risk assessments for soil organisms to better characterize the situation in the field.

Root trenching and stable isotope analysis uncover trophic links of euedaphic collembola species to mycorrhizal mycelium in pine forests

Ectomycorrhizal fungi are a prominent component of the soil biota of boreal forests, but the role of mycorrhizal mycelium as a food source for soil Collembola remains controversial. We addressed this question in a trenching experiment in young (70 years old) and old (180 years old) stands of Scotch pine, combined with stable isotope analysis. Trenching halved the biomass of ectomycorrhizal mycelium, estimated using in-growth mesh bags. In the young forest, the abundance of two euedaphic Collembola species, Mesaphorura yosiii and Willemia anophthalma, decreased after trenching by 99 and 97% respectively, while in the old forest the abundance of Collembola was not affected. In both forests, trenching reduced δ15N values of the dominant euedaphic species Isotomiella minor and W. anophthalma, indicating a shift in trophic niches. Thus, we obtained convincing evidence of species-specific trophic links of euedaphic Collembola species to the mycelium of mycorrhizal fungi.

Soil Springtail Communities Are Resilient to Forest Tent Caterpillar Defoliation in Quebec Mixed Hardwood Forests

Outbreaks of defoliator insects are important natural disturbances in boreal forests, but their increasing frequency under warming climate conditions is of concern. Outbreak events can shape ecosystem dynamics with cascading effects through trophic networks. Caterpillar defoliation can alter tree physiology, increase sunlight to the understory, and result in the deposition of large amounts of leaf litter and caterpillar frass to the forest floor. These modifications can thus affect soil organisms through direct (e.g., changes in soil temperature or moisture) or indirect (e.g., changes in detrital and root food webs) mechanisms. We assessed whether a recent (2015 to 2017) outbreak of the forest tent caterpillar (Malacosoma disstria) at the Lake Duparquet Teaching and Research Forest (Abitibi, QC, Canada) affected soil springtail communities, abundant microarthropods in forest soils. In 2018 and 2019, we sampled litter and soil (0–10 cm depth) at eight sites each in aspen-dominated (Populus tremuloides Michx) stands that were undefoliated or had a recent defoliation history. We found no significant difference in springtail abundance (specimens cm−2) or alpha diversity indices between undefoliated sites and those with defoliation history. However, we observed a transient change in springtail community composition 1 year after the outbreak (2018) with the absence of Folsomia nivalis, Anurophorus sp1, and Xenylla christianseni in sites with defoliation history, but no compositional differences were observed in 2019. Certain soil nutrients (P, C, Mg, Mn) were significant predictors of springtail community composition, but soil microbial biomass was not, despite its significant decrease in sites with defoliation history. Our results show that soil springtail communities respond in the short-term to the forest tent caterpillar outbreak with compositional shifts, but seem ultimately resilient to these events.

The interaction effects of biodegradable microplastics and Cd on Folsomia candida soil collembolan.

In real-field soil conditions, multiple chemicals exposure may be the real scenario for soil biota. The co-occurrence of microplastics (MPs) and cadmium (Cd) is common in soils, which may pose a potential risk to soil ecosystems. Degradable microplastics are producing more MPs, and the potential effects on soil ecosystems are unknown. Therefore, a standard soil animal collembolan Folsomia candida was used to evaluate the single and interaction effects of biodegradable MPs (PLA) and Cd. The results showed that single and co-biodegradable PLA and Cd all had negative influences on the survival, reproduction, and growth of F. candida, and the effects intensified with PLA concentrations. The survival rate, reproduction rate, adult body length, and juvenile body length decreased by 20.0%, 24.2%, 22.9%, and 32.2% at MPs-100 treatment. But combined PLA and Cd alleviated the toxicity of single Cd on F. candida at lower PLA concentrations. The number of juveniles increased by 29.3%, the survival rate increased by 7.52%, the adult body length increased by 11.7%, and the juvenile body length increased by 19.0% at MPs-1 + Cd than single Cd treatment. Biochemical assays on antioxidant enzymes had the same results. Antioxidant enzymes CAT and POD were more sensitive than SOD. CAT and POD activities were induced quickly at shorter exposure periods, and MP treatment thus may be promising biomarkers on soil collembolan for soil MP exposure. PLA is degraded with time in soils; therefore, the long-term effects of co-MPs and Cd in soils are suggested to be further studied.

Responses of Soil Collembolans to Land Degradation in a Black Soil Region in China

Land degradation in black soil regions has a significant effect on belowground systems, and Collembolans can adequately indicate environmental changes in the soil. However, there is currently a knowledge gap in the literature regarding the responses of soil Collembolans to land degradation. In order to better understand this issue, in this study, a total of 180 soil Collembolan samples were collected from four habitats with varying degrees of land degradation in the Songnen Plain, namely a no land-degradation habitat (NLD), light land-degradation habitat (LLD), moderate land-degradation habitat (MLD) and severe land-degradation habitat (SLD). The results reveal that the different degrees of land degradation caused some differences in the taxonomic composition of the Collembolans; however, the majority of the Collembolan species are distributed relatively evenly. Proisotoma minima are always a dominant species during the study period. Seasonal variations are observed in the abundance, richness and diversity levels. In the severe land-degradation habitats (SLD), the abundance, richness, diversity and community complexity of the Collembolans are aways at the lowest levels. In addition, Proisotoma minima is negatively correlated with a majority of the species of Collembolans in the low levels of the land-degradation habitats, whereas they are positively correlated with most of the other species in the high levels. Epedaphic and euedaphic Collembolans responded to land degradation more obviously. The structural equation model (SEM) displays that soil Collembolan communities respond negatively to land degradation. Overall, our results provide implications that soil Collembolan communities are affected by land degradation, and that different taxa of soil Collembolans respond to degradation in numerous ways.

Ecotoxicological studies of selected agrochemicals on the moulting stages of Cyphoderus javanus under laboratory conditions

Indiscriminate use of toxic pesticides in agriculture has raised serious concerns worldwide, which led to a steady destruction of soil biota as well as the overall health of ecosystem. The present study was designed to evaluate the effects of selected agrochemicals such as cyfluthrin (insecticide), fytran (fungicide) and oxadiargyl (herbicide) on the moulting stages of soil springtail Cyphoderus javnaus. Laboratory analysis results indicated that the agrochemical treated organisms showed prolonged moulting intervals and need more days than normal to become a complete adult having sexual maturity. On treatment with the sub lethal concentration of oxadiargyl, first moult noticed after12th day, second moult after24 th day, third moult after 36 th day of egg hatching. The effect of herbicide oxadiargyl on Cyphoderus javanus was found to be comparatively higher than that of other two pesticides. The changes noticed in developmental stages, moulting period and egg laying pattern in Cyphoderus javanus when exposed to agrochemicals indicated that this soil collembolan is a potential biomarker of ecotoxicology investigations.

Three new species of Collembola from Sicily with first record of the genus Superodontella Stach, 1949 from Italy

Three new species of soil Collembola from both agricultural lands (vineyards and olive orchards) and a natural habitat (beech forest) located in Sicily (Italy) are described: Superodontella eleonorae sp. nov., first record of this genus for Italy, Lepidocyrtus rapitalai sp. nov. and Pseudosinella francae sp. nov..

A new insight into the potential drivers of antibiotic resistance gene enrichment in the collembolan gut association with antibiotic and non-antibiotic agents

Effects of non-antibiotic pharmaceuticals on antibiotic resistance genes (ARGs) in soil ecosystem are still unclear. In this study, we explored the microbial community and ARGs variations in the gut of the model soil collembolan Folsomia candida following soil antiepileptic drug carbamazepine (CBZ) contamination, while comparing with antibiotic erythromycin (ETM) exposure. Results showed that, CBZ and ETM all significantly influenced ARGs diversity and composition in the soil and collembolan gut, increasing the relative abundance of ARGs. However, unlike ETM, which influences ARGs via bacterial communities, exposure to CBZ may have primarily facilitated enrichment of ARGs in gut through mobile genetic elements (MGEs). Although soil CBZ contamination did not pose an effect on the gut fungal community of collembolans, it increased the relative abundance of animal fungal pathogens contained therein. Soil ETM and CBZ exposure both significantly increased the relative abundance of Gammaproteobacteria in the collembolan gut, which may be used to indicate soil contamination. Together, our results provide a fresh perspective for the potential drivers of non-antibiotic drugs on ARG changes based on the actual soil environment, revealing the potential ecological risk of CBZ on soil ecosystems involving ARGs dissemination and pathogens enrichment.

Globally invariant metabolism but density-diversity mismatch in springtails

Soil life supports the functioning and biodiversity of terrestrial ecosystems. Springtails (Collembola) are among the most abundant soil arthropods regulating soil fertility and flow of energy through above- and belowground food webs. However, the global distribution of springtail diversity and density, and how these relate to energy fluxes remains unknown. Here, using a global dataset representing 2470 sites, we estimate the total soil springtail biomass at 27.5 megatons carbon, which is threefold higher than wild terrestrial vertebrates, and record peak densities up to 2 million individuals per square meter in the tundra. Despite a 20-fold biomass difference between the tundra and the tropics, springtail energy use (community metabolism) remains similar across the latitudinal gradient, owing to the changes in temperature with latitude. Neither springtail density nor community metabolism is predicted by local species richness, which is high in the tropics, but comparably high in some temperate forests and even tundra. Changes in springtail activity may emerge from latitudinal gradients in temperature, predation and resource limitation in soil communities. Contrasting relationships of biomass, diversity and activity of springtail communities with temperature suggest that climate warming will alter fundamental soil biodiversity metrics in different directions, potentially restructuring terrestrial food webs and affecting soil functioning.

Adverse effects of the cyfluthrin on Cyphoderus javanus Borner (Collembola) in soil

Soil collembolans are key model organisms for ecotoxicological studies and play an inevitable role in litter degradation, nutrient cycling, energy flow and various ecosystem functioning. The detritivore collembolan, yphoderus javanus, was used to determine the toxicity of insecticide formulation cyfluthrin under laboratory conditions. The impacts of insecticide cyfluthrin on life history parameters of C. javanus revealed that mortality rates increased with increasing concentration. The fecundity rates, the number of eggs laid, the number of juveniles’ emergence and longevity were found to be decreased drastically with insecticidal exposure. The high mortality of soil collembolans deducts the decomposition rate of organic matter and leaf litter, thereby reducing the fertility of soil.

Karst Dolines Support Highly Diversified Soil Collembola Communities—Possible Refugia in a Warming Climate?

Karst dolines, as geomorphologically diverse natural landforms, usually exhibit more or less steep microclimatic gradients that provide a mosaic of diverse microhabitat conditions, resulting in a high diversity of soil biota with numerous rare endemic and/or relict species occupying these habitats. In this study, we investigated the spatial patterns of Collembola abundance, species richness, community structure and distribution of functional groups at topographically and microclimatically different sites across three open (unforested) karst dolines in a north-south direction in the Slovak Karst, Slovakia. We also assessed the refugial capacity of dolines for collembolan communities. The Friedman ANOVA test confirmed the significant differences in soil mean temperatures between the sites of all the dolines selected. The diverse soil microclimatic conditions within the dolines supported higher Collembola diversity (species numbers, diversity indices) compared with sites on the karst plateau and showed a potential to facilitate the persistence of some species that are absent or very rare in the surrounding landscape. In dolines with circular morphology and comparable size, the topography and soil microclimate had a stronger effect on community composition and structure than soil organic carbon. Shallow solution dolines provided microhabitats for various functional groups of soil Collembola in relation to the microclimatic character of the individual sites. It was observed that such landforms can also function as microclimatic refugia for cold-adapted species through the accumulation of colder air and the buffering of the local microclimate against the ambient mesoclimate, thus underlying the necessity of adequate attention in terms of the conservation of the karst natural phenomena.