Global fine-resolution data on springtail abundance and community structure.

Springtails (Collembola) inhabit soils from the Arctic to the Antarctic and comprise an estimated ~32% of all terrestrial arthropods on Earth. Here, we present a global, spatially-explicit database on springtail communities that includes 249,912 occurrences from 44,999 samples and 2,990 sites. These data are mainly raw sample-level records at the species level collected predominantly from private archives of the authors that were quality-controlled and taxonomically-standardised. Despite covering all continents, most of the sample-level data come from the European continent (82.5% of all samples) and represent four habitats: woodlands (57.4%), grasslands (14.0%), agrosystems (13.7%) and scrublands (9.0%). We included sampling by soil layers, and across seasons and years, representing temporal and spatial within-site variation in springtail communities. We also provided data use and sharing guidelines and R code to facilitate the use of the database by other researchers. This data paper describes a static version of the database at the publication date, but the database will be further expanded to include underrepresented regions and linked with trait data.

Phoretic behavior of the pseudoscorpion Megachernes ryugadensis on the Japanese wood mouse Apodemus speciosus.

Phoresy is a passive transportation behavior where one organism (phoront) disperses to a new location by attaching to another organism. Pseudoscorpions are arthropod predators that mainly live in soil, subterranean habitats, and under tree bark. Some species also live in animal nests and engage in phoresy on small mammals, suggesting close associations with these animals. However, the relationship between phoretic pseudoscorpions and hosts as well as the ecological significance of phoresy remain largely unexplored. Here, to understand the function of phoresy of Megachernes ryugadensis, phoretic on small mammals, their phoretic behavior was investigated in a deciduous forest in northern Japan; individual-level dynamics of phoresy were examined by over 3-year mark-recapture surveys that concurrently marked the host and phoront; and host characteristics, such as sex and age class, were analyzed based on a 2-year small mammal trapping survey. The primary host species was the abundant Japanese wood mouse Apodemus speciosus. Out of 132 pseudoscorpions marked, 5 were recaptured approximately 1 month later. No pseudoscorpions were recaptured within the same census period (3-4 days) when they were marked, indicating that phoresy events last less than one night, and pseudoscorpions are unlikely to engage in phoresy again within a few weeks of their initial engagement. Furthermore, analysis of host characteristics revealed a tendency for female mice and adult individuals to have a higher probability of being hosts compared with males and subadults, respectively. Based on the findings in this and previous studies, the function of phoresy in this species is discussed.

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.

Contrasting patterns of nitrogen release from fine roots and leaves driven by microbial communities during decomposition.

Leachate from decaying root and leaf litter plays crucial roles in soil biogeochemical processes in forest ecosystems. Unlike for leaf litter, however, the chemical composition and microbial community of root litter leachate are poorly understood. We hypothesized that both leachate nitrogen (N) composition and microbial communities differ between plant organs and decomposition stages and that leachate composition affects microbial community composition. We conducted a 2.5-year laboratory incubation using root and leaf substrate from Cryptomeria japonica and Chamaecyparis obtusa. We monitored the N forms released and used metabarcoding to characterize the microbial communities. Leachate N accounted for 40 % and 30 % of net N losses from C. japonica and C. obtusa roots, respectively; the remainder was probably lost in gaseous forms. In contrast, leaves absorbed N during the incubation regardless of tree species. The predominant N form in root leachate was nitrate (NO3-); cumulative NO3- quantity was 22.6 and 25.5 times greater in root than in leaf leachate for C. japonica and C. obtusa, respectively. A nitrifying bacterium was selected as the indicator taxon in root substrates, whereas many families of N-fixing bacteria were selected in leaf substrates. At the end of the incubation period, bacterial taxonomic diversity was high in both organs from both tree species, ranging from 177 to 339 taxa and increasing with time. However, fungal diversity was low for both organs (72 to 155 taxa). Shifts in bacterial community structure were related to NO3- concentration and leachate pH, whereas shifts in fungal community structure were related to leachate pH. These results suggest that the contrasting N dynamics of root and leaf substrates are strongly affected by the characteristics of and the microbes recruited by their leachates. Understanding organ-specific litter N dynamics is indispensable for predicting N cycling for optimal management of forest ecosystems in a changing world.

Radiocarbon signature reveals that most springtails depend on carbon from living plants.

Terrestrial carbon cycling is largely mediated by soil food webs. Identifying the carbon source for soil animals has been desired to distinguish their roles in carbon cycling, but it is challenging for small invertebrates at low trophic levels because of methodological limitations. Here, we combined radiocarbon (14C) analysis with stable isotope analyses (13C and 15N) to understand feeding habits of soil microarthropods, especially focusing on springtail (Collembola). Most Collembola species exhibited lower Δ14C values than litter regardless of their δ13C and δ15N signatures, indicating their dependence on young carbon. In contrast with general patterns across all taxonomic groups, we found a significant negative correlation between δ15N and Δ14C values among the edaphic Collembola. This means that the species with higher δ15N values depend on C from more recent photosynthate, which suggests that soil-dwelling species generally feed on mycorrhizae to obtain root-derived C. Many predatory taxa exhibited higher Δ14C values than Collembola but lower than litter, indicating non-negligible effects of collembolan feeding habits on the soil food web. Our study demonstrated the usefulness of radiocarbon analysis, which can untangle the confounding factors that change collembolan δ15N values, clarify animal feeding habits and define the roles of organisms in soil food webs.

A meta-analysis on decomposition quantifies afterlife effects of plant diversity as a global change driver.

Biodiversity loss can alter ecosystem functioning; however, it remains unclear how it alters decomposition-a critical component of biogeochemical cycles in the biosphere. Here, we provide a global-scale meta-analysis to quantify how changes in the diversity of organic matter derived from plants (i.e. litter) affect rates of decomposition. We find that the after-life effects of diversity were significant, and of substantial magnitude, in forests, grasslands, and wetlands. Changes in plant diversity could alter decomposition rates by as much as climate change is projected to alter them. Specifically, diversifying plant litter from mono- to mixed-species increases decomposition rate by 34.7% in forests worldwide, which is comparable in magnitude to the 13.6-26.4% increase in decomposition rates that is projected to occur over the next 50 years in response to climate warming. Thus, biodiversity changes cannot be solely viewed as a response to human influence, such as climate change, but could also be a non-negligible driver of future changes in biogeochemical cycles and climate feedbacks on Earth.

Living Litter: Dynamic Trait Spectra Predict Fauna Composition.

Understanding what drives soil fauna species composition through space and time is crucial because we should preserve soil fauna biodiversity and its key role in ecosystem functioning in this era of fast environmental change. As plant leaf litter provides both food and habitat for soil fauna, a focus on litter traits that relate to these two functions will help in understanding soil invertebrate community structure and dynamics comprehensively. To advance this agenda, we propose a conceptual framework to explicitly link the invertebrate community composition to the temporal dynamics of the litter trait space defined by two axes: a food-quality axis related to plant resource economics and chemistry and a habitat-quality axis related to litter particle size and shape.

Taxi drivers: the role of animals in transporting mycorrhizal fungi.

Dispersal of mycorrhizal fungi via animals and the importance for the interacting partners' life history as well as for ecosystems is an understudied topic. In this review, we describe the available evidence and the most important knowledge gaps and finally suggest ways to gain the missing information. So far, 33 articles have been published proving a successful transfer of mycorrhizal propagules by animals. The vast majority of research on invertebrates was focused on arbuscular mycorrhizal (AM) fungi, whereas papers on vertebrates (mainly rodents and artiodactyls) equally addressed ectomycorrhizal (ECM) and AM fungi. Effective dispersal has been mostly shown by the successful inoculation of bait plants and less commonly by spore staining or germination tests. Based on the available data and general knowledge on animal lifestyles, collembolans and oribatid mites may be important in transporting ECM fungal propagules by ectozoochory, whereas earthworms, isopods, and millipedes could mainly transfer AM fungal spores in their gut systems. ECM fungal distribution may be affected by mycophagous dipterans and their hymenopteran parasitoids, while slugs, snails, and beetles could transport both mycorrhizal groups. Vertebrates feeding on fruit bodies were shown to disperse mainly ECM fungi, while AM fungi are transported mostly accidentally by herbivores. The important knowledge gaps include insufficient information on dispersal of fungal propagules other than spores, the role of invertebrates in the dispersal of mycorrhizal fungi, the way in which propagules pass through food webs, and the spatial distances reached by different dispersal mechanisms both horizontally and vertically.

Leachate from fine root litter is more acidic than leaf litter leachate: A 2.5-year laboratory incubation.

Some tree species increase fine root production under soil acidification, thus changing the balance of litter input from leaves and roots. Litter leaches a significant amount of acidic materials during its decomposition, which might facilitate soil acidification. In this context, we focused on dissolved organic matter (DOM) as the major component of acidic materials. We hypothesized that both the quality and quantity of DOM, which control its function (i.e., proton supply), differ between leaf and root litter. To test this hypothesis, we conducted a 2.5-year laboratory incubation experiment using fresh fine roots and fresh green leaves as litter of two coniferous species (Cryptomeria japonica and Chamaecyparis obtusa) and investigated the leachate pH and DOM composition based on the optical properties. After the early stage of decomposition when flash leaching of DOM converged, the amount of dissolved organic carbon (DOC) leached from roots increased again and leachate pH declined. In contrast, DOC concentrations continued to decrease in leaf leachates during the incubation period, and the pH decrease was not as striking as that of root leachates. Optical properties (ultraviolet visible absorption and fluorescence) of DOM revealed that humic-like substances in DOM played a central role in the acidic pH of root leachates. The total amount of protons released from roots of C. japonica and C. obtusa is about 13 and 18 times higher, respectively, than that from leaves. These results imply that the increase of fine root biomass may induce a positive plant-soil feedback in acidic soils, affecting soil biogeochemical functions of terrestrial ecosystems.

A quantitative protocol for DNA metabarcoding of springtails (Collembola).

We developed a novel protocol with superior quantitative analysis results for DNA metabarcoding of Collembola, a major soil microarthropod order. Degenerate PCR primers were designed for conserved regions in the mitochondrial cytochrome c oxidase subunit I (mtCOI) and 16S ribosomal RNA (mt16S) genes based on published collembolan mitogenomes. The best primer pair was selected based on its ability to amplify each gene, irrespective of the species. DNA was extracted from 10 natural communities sampled in a temperate forest (with typically 25-30 collembolan species per 10 soil samples) and 10 mock communities (with seven cultured collembolan species). The two gene regions were then amplified using the selected primers, ligated with adapters for 454 technology, and sequenced. Examination of the natural community samples showed that 32 and 36 operational taxonomic units (defined at a 90% sequence similarity threshold) were recovered from the mtCOI and mt16S data, respectively, which were comparable to the results of the microscopic identification of 25 morphospecies. Further, sequence abundances for each collembolan species from the mtCOI and mt16S data of the mock communities, after normalization by using a species as the internal control, showed good correlation with the number of individuals in the samples (R = 0.91-0.99), although relative species abundances within a mock community sample estimated from sequences were skewed from community composition in terms of the number of individuals or biomass of the species. Thus, this protocol enables the comparison of collembolan communities in a quantitative manner by metabarcoding.

Low multifunctional redundancy of soil fungal diversity at multiple scales.

Theory suggests that biodiversity might help sustain multiple ecosystem functions. To evaluate possible biodiversity-multifunctionality relationships in a natural setting, we considered different spatial scales of diversity metrics for soil fungi in the northern forests of Japan. We found that multifunctionality increased with increasing local species richness, suggesting a limited degree of multifunctional redundancy. This diversity-multifunctionality relationship was independent of the compositional uniqueness of each community. However, we still found the importance of community composition, because there was a positive correlation between community dissimilarity and multifunctional dissimilarity across the landscape. This result suggests that functional redundancy can further decrease when spatial variations in identities of both species and functions are simultaneously considered at larger spatial scales. We speculate that different scales of diversity could provide multiple levels of insurance against the loss of functioning if high-levels of local species diversity and compositional variation across locations are both maintained. Alternatively, making species assemblages depauperate may result in the loss of multifunctionality.

Concordance and discordance between taxonomic and functional homogenization: responses of soil mite assemblages to forest conversion.

The compositional characteristics of ecological assemblages are often simplified; this process is termed "biotic homogenization." This process of biological reorganization occurs not only taxonomically but also functionally. Testing both aspects of homogenization is essential if ecosystem functioning supported by a diverse mosaic of functional traits in the landscape is concerned. Here, we aimed to infer the underlying processes of taxonomic/functional homogenization at the local scale, which is a scale that is meaningful for this research question. We recorded species of litter-dwelling oribatid mites along a gradient of forest conversion from a natural forest to a monoculture larch plantation in Japan (in total 11 stands), and collected data on the functional traits of the recorded species to quantify functional diversity. We calculated the taxonomic and functional ß-diversity, an index of biotic homogenization. We found that both the taxonomic and functional ß-diversity decreased with larch dominance (stand homogenization). After further deconstructing ß-diversity into the components of turnover and nestedness, which reflect different processes of community organization, a significant decrease in the response to larch dominance was observed only for the functional turnover. As a result, there was a steeper decline in the functional ß-diversity than the taxonomic ß-diversity. This discordance between the taxonomic and functional response suggests that species replacement occurs between species that are functionally redundant under environmental homogenization, ultimately leading to the stronger homogenization of functional diversity. The insights gained from community organization of oribatid mites suggest that the functional characteristics of local assemblages, which support the functionality of ecosystems, are of more concern in human-dominated forest landscapes.

Biotic homogenization and differentiation of soil faunal communities in the production forest landscape: taxonomic and functional perspectives.

Biotic homogenization has been reported worldwide. Although simplification of communities across space is often significant at larger scales, it could also occur at the local scale by changing biotic interactions. This study aimed to elucidate local community processes driving biotic homogenization of soil faunal communities, and the possibility of biotic re-differentiation. We recorded species of oribatid mites in litter and soil layers along a gradient of forest conversion from monoculture larch plantation to primary forests in central Japan. We collected data for functional traits of the recorded species to quantify functional diversity. Then we quantified their taxonomic/functional turnover. Litter diversity was reduced in the larch-dominated stands, leading to habitat homogenization. Consequently, litter communities were biologically homogenized and differentiated in the plantations and in the natural forest, respectively. Turnover of functional traits for litter communities was lower and higher than expected by chance in the plantations and in the natural stand, respectively. This result suggests that the dominant assembly process shifts from limiting similarity to habitat filtering along the forest restoration gradient. However, support for such niche-based explanations was not observed for communities in the soil layer. In the monocultures, functional diversity expected from a given regional species pool significantly decreased for litter communities but not for those in the soil layer. Such discrepancy between communities in different layers suggests that communities more exposed to anthropogenic stresses are more vulnerable to the loss of their functional roles. Our study explains possible community processes behind the observed patterns of biological organization, which can be potentially useful in guiding approaches for restoring biodiversity.

Null model approaches to evaluating the relative role of different assembly processes in shaping ecological communities.

Various local processes simultaneously shape ecological assemblages. ß-diversity is a useful metric for inferring the underlying mechanisms of community assembly. However, ß-diversity is not independent of γ-diversity, which may mask the local mechanisms that govern community processes across regions. Recent approaches that rely on an abundance-based null model could solve this sampling issue. However, if abundance varies widely across a region, the relative roles of deterministic and stochastic processes may be substantially misestimated. Furthermore, there is additional uncertainty as to whether null models used to correct γ-dependence in ß-diversity should be independent of the observed patterns of species abundance distributions or whether the models should reflect these patterns. Here, we aim to test what null models with various constraints imply about the underlying processes shaping ß-diversity. First, we found that an abundance-driven sampling effect could substantially influence the calculation of γ-corrected ß-diversity. Second, we found that the null models that preserve the species abundance patterns could better reflect empirical patterns of spatial organization of individuals. The different implications generated from different applications of the null model approach therefore suggest that there are still frontiers regarding how local processes that shape species assemblages should be quantified. Carefully exploring each facet within different assembly processes is important.

Seasonal ozone uptake by a warm-temperate mixed deciduous and evergreen broadleaf forest in western Japan estimated by the Penman-Monteith approach combined with a photosynthesis-dependent stomatal model.

Canopy-level stomatal conductance over a warm-temperate mixed deciduous and evergreen broadleaf forest in Japan was estimated by the Penman-Monteith approach, as compensated by a semi-empirical photosynthesis-dependent stomatal model, where photosynthesis, relative humidity, and CO2 concentration were assumed to regulate stomatal conductance. This approach, using eddy covariance data and routine meteorological observations at a flux tower site, permits the continuous estimation of canopy-level O3 uptake, even when the Penman-Monteith approach is unavailable (i.e. in case of direct evaporation from soil or wet leaves). Distortion was observed between the AOT40 exposure index and O3 uptake through stomata, as AOT40 peaked in April, but with O3 uptake occurring in July. Thus, leaf pre-maturation in the predominant deciduous broadleaf tree species (Quercus serrata) might suppress O3 uptake in springtime, even when the highest O3 concentrations were observed.