Effects of climate on the distribution and conservation of commonly observed European earthworms.

Belowground biodiversity distribution does not necessarily reflect aboveground biodiversity patterns, but maps of soil biodiversity remain scarce because of limited data availability. Earthworms belong to the most thoroughly studied soil organisms and-in their role as ecosystem engineers-have a significant impact on ecosystem functioning. We used species distribution modeling (SDMs) and available data sets to map the spatial distribution of commonly observed (i.e., frequently recorded) earthworm species (Annelida, Oligochaeta) across Europe under current and future climate conditions. First, we predicted potential species distributions with commonly used models (i.e., MaxEnt and Biomod) and estimated total species richness (i.e., number of species in a 5 × 5 km grid cell). Second, we determined how much the different types of protected areas covered predicted earthworm richness and species ranges (i.e., distributions) by estimating the respective proportion of the range area. Earthworm species richness was high in central western Europe and low in northeastern Europe. This pattern was mainly associated with annual mean temperature and precipitation seasonality, but the importance of predictor variables to species occurrences varied among species. The geographical ranges of the majority of the earthworm species were predicted to shift to eastern Europe and partly decrease under future climate scenarios. Predicted current and future ranges were only poorly covered by protected areas, such as national parks. More than 80% of future earthworm ranges were on average not protected at all (mean [SD] = 82.6% [0.04]). Overall, our results emphasize the urgency of considering especially vulnerable earthworm species, as well as other soil organisms, in the design of nature conservation measures.

Efectos del clima sobre la distribución y conservación de la lombriz de tierra europea Resumen La distribución de la biodiversidad del subsuelo no refleja necesariamente los patrones de biodiversidad, pero los mapas de la biodiversidad del suelo aún son escasos debido a la disponibilidad limitada de datos. Las lombrices son uno de los organismos del suelo más estudiados a detalle­en su papel de ingenieros del ecosistema­y tienen un impacto significativo sobre el funcionamiento de ecosistema. Usamos modelos de distribución de especies (MDE) y conjuntos de datos disponibles para mapear la distribución espacial de las especies (Annelida, Oligochaeta) de lombrices más observadas (es decir, registradas con frecuencia) en toda Europa bajo el clima actual y el futuro. Primero pronosticamos la distribución potencial de las especies con modelos de uso común (MaxEnt y Biomod) y estimamos la riqueza total de especies (número de especies en una cuadrícula de 5 × 5 km). Después determinamos cuánto pronosticaban los diferentes tipos de áreas protegidas contempladas la riqueza de lombrices y la distribución de las especies mediante la estimación de la proporción respectiva del rango del área. La riqueza de especies fue alta en el occidente central y baja en el noreste de Europa. Este patrón estuvo asociado principalmente con la temperatura media anual y la estacionalidad de la precipitación, aunque la importancia de las variables de pronóstico para la presencia de la especie varió entre especies. Se pronosticó que la distribución geográfica de la mayoría de las especies cambiaría al este de Europa y disminuiría parcialmente bajo los escenarios climáticos futuros. El pronóstico de la distribución actual y futura contaba con una cobertura deficiente de las áreas protegidas, como los parques nacionales. En promedio, más del 80% de la distribución futura de las lombrices no estaba protegido (promedio [SD] = 82.6% [0.04]). En general, nuestros resultados destacan la urgencia por considerar a las especies vulnerables de lombrices, así como a otros organismos del suelo, en el diseño de las medidas de conservación.

Ecosystem type drives soil eukaryotic diversity and composition in Europe.

Soil eukaryotes play a crucial role in maintaining ecosystem functions and services, yet the factors driving their diversity and distribution remain poorly understood. While many studies focus on some eukaryotic groups (mostly fungi), they are limited in their spatial scale. Here, we analyzed an unprecedented amount of observational data of soil eukaryomes at continental scale (787 sites across Europe) to gain further insights into the impact of a wide range of environmental conditions (climatic and edaphic) on their community composition and structure. We found that the diversity of fungi, protists, rotifers, tardigrades, nematodes, arthropods, and annelids was predominantly shaped by ecosystem type (annual and permanent croplands, managed and unmanaged grasslands, coniferous and broadleaved woodlands), and higher diversity of fungi, protists, nematodes, arthropods, and annelids was observed in croplands than in less intensively managed systems, such as coniferous and broadleaved woodlands. Also in croplands, we found more specialized eukaryotes, while the composition between croplands was more homogeneous compared to the composition of other ecosystems. The observed high proportion of overlapping taxa between ecosystems also indicates that DNA has accumulated from previous land uses, hence mimicking the land transformations occurring in Europe in the last decades. This strong ecosystem-type influence was linked to soil properties, and particularly, soil pH was driving the richness of fungi, rotifers, and annelids, while plant-available phosphorus drove the richness of protists, tardigrades, and nematodes. Furthermore, the soil organic carbon to total nitrogen ratio crucially explained the richness of fungi, protists, nematodes, and arthropods, possibly linked to decades of agricultural inputs. Our results highlighted the importance of long-term environmental variables rather than variables measured at the time of the sampling in shaping soil eukaryotic communities, which reinforces the need to include those variables in addition to ecosystem type in future monitoring programs and conservation efforts.

Earthworm-Driven Changes in Soil Chemico-Physical Properties, Soil Bacterial Microbiota, Tree/Tea Litter Decomposition, and Plant Growth in a Mesocosm Experiment with Two Plant Species.

Earthworms and soil microorganisms contribute to soil health, quality, and fertility, but their importance in agricultural soils is often underestimated. This study aims at examining whether and to what extent the presence of earthworms (Eisenia sp.) affected the (a) soil bacterial community composition, (b) litter decomposition, and (c) plant growth (Brassica oleracea L., broccoli; Vicia faba L., faba bean). We performed a mesocosm experiment in which plants were grown outdoors for four months with or without earthworms. Soil bacterial community structure was evaluated by a 16S rRNA-based metabarcoding approach. Litter decomposition rates were determined by using the tea bag index (TBI) and litter bags (olive residues). Earthworm numbers almost doubled throughout the experimental period. Independently of the plant species, earthworm presence had a significant impact on the structure of soil bacterial community, in terms of enhanced α- and ß-diversity (especially that of Proteobacteria, Bacteroidota, Myxococcota, and Verrucomicrobia) and increased 16S rRNA gene abundance (+89% in broccoli and +223% in faba bean). Microbial decomposition (TBI) was enhanced in the treatments with earthworms, and showed a significantly higher decomposition rate constant (kTBI) and a lower stabilization factor (STBI), whereas decomposition in the litter bags (dlitter) increased by about 6% in broccoli and 5% in faba bean. Earthworms significantly enhanced root growth (in terms of total length and fresh weight) of both plant species. Our results show the strong influence of earthworms and crop identity in shaping soil chemico-physical properties, soil bacterial community, litter decomposition and plant growth. These findings could be used for developing nature-based solutions that ensure the long-term biological sustainability of soil agro- and natural ecosystems.

Global data on earthworm abundance, biomass, diversity and corresponding environmental properties.

Earthworms are an important soil taxon as ecosystem engineers, providing a variety of crucial ecosystem functions and services. Little is known about their diversity and distribution at large spatial scales, despite the availability of considerable amounts of local-scale data. Earthworm diversity data, obtained from the primary literature or provided directly by authors, were collated with information on site locations, including coordinates, habitat cover, and soil properties. Datasets were required, at a minimum, to include abundance or biomass of earthworms at a site. Where possible, site-level species lists were included, as well as the abundance and biomass of individual species and ecological groups. This global dataset contains 10,840 sites, with 184 species, from 60 countries and all continents except Antarctica. The data were obtained from 182 published articles, published between 1973 and 2017, and 17 unpublished datasets. Amalgamating data into a single global database will assist researchers in investigating and answering a wide variety of pressing questions, for example, jointly assessing aboveground and belowground biodiversity distributions and drivers of biodiversity change.

No evidence for increased loss of old carbon in a temperate organic soil after 13 years of simulated climatic warming despite increased CO2 emissions.

Determining the temperature sensitivity of terrestrial carbon (C) stores is an urgent priority for predicting future climate feedbacks. A key aspect to solve this long-standing research gap is to determine whether warmer temperatures will increase autotrophic activities leading to greater C storage or promote heterotrophic activities that will drive these systems to become C sources. We experimentally addressed this critical question by subjecting intact plant-soil systems in a UK upland ecosystem to simulated climate warming under natural field conditions. We report the results of a 13-year field-based climate manipulation experiment combining in situ respiration measurements with radiocarbon (14 C) analyses of respired CO2 , dissolved organic carbon (DOC), soil and the tissue contents of the dominant soil fauna (enchytraeids). We found that warming during the growing season produced the largely expected increases in ecosystem respiration (63%) and leaching of DOC (19%) with no evidence for thermal acclimation or substrate exhaustion over the whole 13-year experimental period. Contrary to expectations, we found no evidence to support an increased release of old soil C after more than a decade of simulated climatic change, and indeed, 14 C analyses indicated that warming caused a significant shift towards mineralisation of more recent plant-derived C inputs. Further support came from the radiocarbon analyses of the enchytraeid tissues, which showed a greater assimilation of the more recent (plant-derived) C sources following warming. Therefore, in contrast to subarctic ecosystems, our results suggest that changes in C storage in this UK upland soil are strongly coupled to plant activities and that increasing temperatures will drive the turnover of organic material fixed only within recent years, without resulting in the loss of existing old carbon stores.

Response to Comment on "Global distribution of earthworm diversity".

James et al claim that there are areas of concern in our work. We believe that they have misunderstood the methods behind our paper and that differences in scale have been overlooked. Once those misunderstandings have been resolved, their remaining criticisms are either not sustained or agree with our statements. To advance the field, we recommend additional sampling using comparable methodologies in underrepresented areas.

Integrative taxonomy of some Iranian peregrine earthworm species using morphology and barcoding (Annelida: Megadrili).

Despite the biological and economic importance of earthworms, the taxonomic status and evolutionary relationships of most lumbricid genera are still under debate. Further complications arise from the recognition that earthworms also show a high cryptic diversity. Past and current field studies of Iranian earthworm fauna have resulted in the identification of a total number of 28 earthworm species. However, many specimens do not fully fit into their original descriptions, making the species assignation very difficult. In this study, we evaluated the genetic diversity using mitochondrial markers as a tool to assess the species occurrence of some problematic species in Iran. Four species with high morphological variation were selected: Aporrectodea caliginosa (Savigny, 1826), Aporrectodea trapezoides (Dugès, 1828), Dendrobaena byblica (Rosa, 1893) and Dendrobaena veneta (Rosa, 1886). Morphological identification was contrasted with the molecular information generated through COI and 16S barcoding and the COI and 16S sequences stored in the Genbank. The results of this first integrative taxonomic analysis revealed that D. veneta consisted of two separated clades and that a number of species assigned to D. byblica showed very close relationships with those belonging to the genus Philomontanus. The lack of taxonomic expertise and identification characters providing a clear and unambiguous identification of earthworms highlights the urgent need of new tools to identify species unequivocally. Therefore, it is concluded that more taxonomical studies are needed to clarify the diagnostic characters and taxonomic status of the species belonging to two genera, Aporrectodea and Dendrobaena (Lumbricidae), in Iran.

KEYLINK: towards a more integrative soil representation for inclusion in ecosystem scale models. I. review and model concept.

The relatively poor simulation of the below-ground processes is a severe drawback for many ecosystem models, especially when predicting responses to climate change and management. For a meaningful estimation of ecosystem production and the cycling of water, energy, nutrients and carbon, the integration of soil processes and the exchanges at the surface is crucial. It is increasingly recognized that soil biota play an important role in soil organic carbon and nutrient cycling, shaping soil structure and hydrological properties through their activity, and in water and nutrient uptake by plants through mycorrhizal processes. In this article, we review the main soil biological actors (microbiota, fauna and roots) and their effects on soil functioning. We review to what extent they have been included in soil models and propose which of them could be included in ecosystem models. We show that the model representation of the soil food web, the impact of soil ecosystem engineers on soil structure and the related effects on hydrology and soil organic matter (SOM) stabilization are key issues in improving ecosystem-scale soil representation in models. Finally, we describe a new core model concept (KEYLINK) that integrates insights from SOM models, structural models and food web models to simulate the living soil at an ecosystem scale.

Towards an integrative understanding of soil biodiversity.

Soil is one of the most biodiverse terrestrial habitats. Yet, we lack an integrative conceptual framework for understanding the patterns and mechanisms driving soil biodiversity. One of the underlying reasons for our poor understanding of soil biodiversity patterns relates to whether key biodiversity theories (historically developed for aboveground and aquatic organisms) are applicable to patterns of soil biodiversity. Here, we present a systematic literature review to investigate whether and how key biodiversity theories (species-energy relationship, theory of island biogeography, metacommunity theory, niche theory and neutral theory) can explain observed patterns of soil biodiversity. We then discuss two spatial compartments nested within soil at which biodiversity theories can be applied to acknowledge the scale-dependent nature of soil biodiversity.

Global distribution of earthworm diversity.

Soil organisms, including earthworms, are a key component of terrestrial ecosystems. However, little is known about their diversity, their distribution, and the threats affecting them. We compiled a global dataset of sampled earthworm communities from 6928 sites in 57 countries as a basis for predicting patterns in earthworm diversity, abundance, and biomass. We found that local species richness and abundance typically peaked at higher latitudes, displaying patterns opposite to those observed in aboveground organisms. However, high species dissimilarity across tropical locations may cause diversity across the entirety of the tropics to be higher than elsewhere. Climate variables were found to be more important in shaping earthworm communities than soil properties or habitat cover. These findings suggest that climate change may have serious implications for earthworm communities and for the functions they provide.

Intensive Cultivation of Kiwifruit Alters the Detrital Foodweb and Accelerates Soil C and N Losses.

The detrital food web plays an important role in the functioning of agro-ecosystems due to their positive effect on organic matter transformations and nutrient supply to the growing crops, however, the activities of the organisms involved are strongly influenced by agricultural practices. In NW Spain, commercial Hayward kiwifruit (Actinidia chinensis var. deliciosa) is intensively produced using conventional techniques (CONV), however, more sustainable methods, such as integrated (INT) and organic (ORG), have been increasingly adopted to decrease the negative impacts on the environment. We investigated the effects of these agricultural managements on earthworm abundance and functional diversity as well as microbial biomass and enzyme activity and evaluated the potential implications for nutrient retention and runoff in kiwifruit orchards. Our results showed that the CONV soils significantly contained fewer earthworms (ca. 80% less individuals than the INT and ORG systems), with their communities being mainly dominated by small epigeics, but a higher microbial biomass (0.53 ± 0.06 mg C g-1 dw soil compared to <0.25 mg C g-1 dw soil in INT and ORG), and 20% more activity of the enzymes involved in C (ß-glucosidase) and N mineralization (urease). Consequently, more C and N was lost from these soils (on average, >37% more CO2, and five times more DIN) than from the less intensively managed soils. In contrast, the INT and ORG systems sustained a more complex and functionally diverse soil food web that lead to higher soil C and N retention. Therefore, agriculture management (i.e., intensive vs. less intensive) and its effects on the structure of the below-ground communities (i.e., microorganisms plus surface detritivores vs. deep burrowers plus geophagous forms) determine the nutrient sink/source function of these agro-ecosystems. These findings highlight the importance of including the contribution of soil biota to soil processes when optimizing fertilization loads and mitigating environmental impacts of agricultural practices.

Stable-isotope labeling and probing of recent photosynthates into respired CO2, soil microbes and soil mesofauna using a xylem and phloem stem-injection technique on Sitka spruce (Picea sitchensis).

RATIONALE: Here we report on the successful application of a novel stem-injection stable-isotope-labeling and probing technique in mature trees to trace the spatial and temporal distribution of rhizosphere carbon belowground. METHODS: Three 22-year-old Sitka spruce trees were injected with 6.66 g of (13)C-labeled aspartic acid. Over the succeeding 30 days, soil CO(2) efflux, phospholipid fatty-acid (PLFA) microbial biomarkers and soil invertebrates (mites, collembolans and enchytraeids) were analyzed along a 50 m transect from each tree to determine the temporal and spatial patterns in the translocation of recently fixed photosynthates belowground. RESULTS: Soil δ(13)CO(2) values peaked 13-23 days after injection, up to 5 m from the base of the injected tree and was, on average, 3.5‰ enriched in (13)C relative to the baseline. Fungal PLFA biomarkers peaked 2-4 days after stem-injection, up to 20 m from the base of the injected tree and were (13)C-enriched by up to 50‰. Significant (13)C enrichment in mites and enchytraeids occurred 4-6 days after injection (by, on average, 1.5‰). CONCLUSIONS: Stem injection of large trees with (13)C-enriched compounds is a successful tool to trace C-translocation belowground. In particular, the significant (13)C enrichment of CO(2) and enchytraeids near the base of the tree and the significant (13)C enrichment of PLFAs up to 20 m away indicate that mature Sitka spruce (Picea sitchensis) have the capacity to support soil communities over large distances.

Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest.

SUMMARY: *The flux of carbon from tree photosynthesis through roots to ectomycorrhizal (ECM) fungi and other soil organisms is assumed to vary with season and with edaphic factors such as nitrogen availability, but these effects have not been quantified directly in the field. *To address this deficiency, we conducted high temporal-resolution tracing of (13)C from canopy photosynthesis to different groups of soil organisms in a young boreal Pinus sylvestris forest. *There was a 500% higher below-ground allocation of plant C in the late (August) season compared with the early season (June). Labelled C was primarily found in fungal fatty acid biomarkers (and rarely in bacterial biomarkers), and in Collembola, but not in Acari and Enchytraeidae. The production of sporocarps of ECM fungi was totally dependent on allocation of recent photosynthate in the late season. There was no short-term (2 wk) effect of additions of N to the soil, but after 1 yr, there was a 60% reduction of below-ground C allocation to soil biota. *Thus, organisms in forest soils, and their roles in ecosystem functions, appear highly sensitive to plant physiological responses to two major aspects of global change: changes in seasonal weather patterns and N eutrophication.

Revealing the uncultivated majority: combining DNA stable-isotope probing, multiple displacement amplification and metagenomic analyses of uncultivated Methylocystis in acidic peatlands.

Peatlands represent an enormous carbon reservoir and have a potential impact on the global climate because of the active methanogenesis and methanotrophy in these soils. Uncultivated methanotrophs from seven European peatlands were studied using a combination of molecular methods. Screening for methanotroph diversity using a particulate methane monooxygenase-based diagnostic gene array revealed that Methylocystis-related species were dominant in six of the seven peatlands studied. The abundance and methane oxidation activity of Methylocystis spp. were further confirmed by DNA stable-isotope probing analysis of a sample taken from the Moor House peatland (England). After ultracentrifugation, (13)C-labelled DNA, containing genomic DNA of these Methylocystis spp., was separated from (12)C DNA and subjected to multiple displacement amplification (MDA) to generate sufficient DNA for the preparation of a fosmid metagenomic library. Potential bias of MDA was detected by fingerprint analysis of 16S rRNA using denaturing gradient gel electrophoresis for low-template amplification (0.01 ng template). Sufficient template (1-5 ng) was used in MDA to circumvent this bias and chimeric artefacts were minimized by using an enzymatic treatment of MDA-generated DNA with S1 nuclease and DNA polymerase I. Screening of the metagenomic library revealed one fosmid containing methanol dehydrogenase and two fosmids containing 16S rRNA genes from these Methylocystis-related species as well as one fosmid containing a 16S rRNA gene related to that of Methylocella/Methylocapsa. Sequencing of the 14 kb methanol dehydrogenase-containing fosmid allowed the assembly of a gene cluster encoding polypeptides involved in bacterial methanol utilization (mxaFJGIRSAC). This combination of DNA stable-isotope probing, MDA and metagenomics provided access to genomic information of a relatively large DNA fragment of these thus far uncultivated, predominant and active methanotrophs in peatland soil.

Enhancing the understanding of earthworm feeding behaviour via the use of fatty acid delta13C values determined by gas chromatography-combustion-isotope ratio mass spectrometry.

Litter-dwelling (epigeic) Lumbricus rubellus and soil-dwelling (endogeic) Allolobophora chlorotica earthworms were observed aggregating under C(3) (delta(13)C = -31.3 per thousand; delta(15)N = 10.7 per thousand) and C(4) (delta(13)C = -12.6 per thousand; delta(15)N = 7.5 per thousand) synthetic dung pats applied to a temperate grassland (delta(13)C = -30.3 per thousand; delta(15)N = 5.7 per thousand) in an experiment carried out for 372 days. Bulk delta(13)C values of earthworms collected from beneath either C(3) or C(4) dung after 28, 56, 112 and 372 days demonstrated that (i) L. rubellus beneath C(4) dung were significantly (13)C-enriched after 56 days (delta(13)C = -23.8 per thousand) and 112 days (delta(13)C = -22.4 per thousand) compared with those from C(3) dung treatments (56 days, delta(13)C = -26.5 per thousand; 112 days, delta(13)C = -27.0 per thousand), and (ii) A. chlorotica were 2.1 per thousand (13)C-enriched (delta(13)C = -24.2 per thousand) relative to those from C(3) dung (delta(13)C = -26.3 per thousand) treatments after 372 days. Bulk delta(15)N values did not suggest significant uptake of dung N by either species beneath C(3) or C(4) dung, but showed that the endogeic species (total mean delta(15)N = 3.3 per thousand) had higher delta(15)N values than the epigeic species (total mean delta(15)N = 5.4 per thousand). Although the two species exhibited similar fatty acid profiles, individual fatty acid delta(13)C values revealed extensive routing of dietary C into body tissue of L. rubellus, but minor incorporation into A. chlorotica. In particular, the direct incorporation of microbial biomarker fatty acids (iC(17:0), aC(17:0)) from (13)C-labelled dung in situ, the routing of dung C into de novo synthesised compounds (iC(20:4)(omega)(6),C(20:5)(omega)(3), and the assimilation of essential fatty acids ((C(18:1)(omega)(9), C(18:1)(omega(7), C(18:2)(omega(6), C(18:3)(omega)(3)) derived from dung, were determined.

Earthworm resources of Benghazi, Libya.

This study presents the first survey of earthworm species (Oligochaeta) from Benghazi, a Mediterranean coastal city in Libya. A total of three peregrine species were recorded: Allolobophora caliginosa trapezoides, Allolobophora rosea (Family: Lumbricidae), Microscolex dubius (Family: Microscolecidae). Their distribution and density in six habitats (vegetable garden, flower garden, green house, farmland, grassland, plain barren landscape) are discussed in relation to some of the physico-chemical parameters and composition of the soil.