Mickaël Hedde

Pesticides and earthworms. A review

Earthworms provide key soil functions that favour many positive ecosystem services. These services are important for agroecosystem sustainability but can be degraded by intensive cultural practices such as use of pesticides. Many literature reports have investigated the effect of pesticides on earthworms. Here, we review those reports to assess the relevance of the indicators of earthworm response to pesticides, to assess their sensitivity to pesticides, and to highlight the remaining knowledge gaps. We focus on European earthworm species and products authorised in Europe, excluding natural compounds and metals. We consider different organisation levels: the infra-individual level (gene expression and physiology), the individual and population levels (life-history traits, population density and behaviour) and the community level: community biomass and density. Our analysis shows that earthworms are impacted by pesticides at all organisation levels. For example, pesticides disrupt enzymatic activities, increase individual mortality, decrease fecundity and growth, change individual behaviour such as feeding rate and decrease the overall community biomass and density. Insecticides and fungicides are the most toxic pesticides impacting survival and reproduction, respectively.

Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits

Summary 1. Trait-based approaches are increasingly being used to test mechanisms underlying species assemblages and biotic interactions across a wide range of organisms including terrestrial arthropods and to investigate consequences for ecosystem processes. Such an approach relies on the standardized measurement of functional traits that can be applied across taxa and regions. Currently, however, unified methods of trait measurements are lacking for terrestrial arthropods and related macroinvertebrates (terrestrial invertebrates hereafter). 2. Here, we present a comprehensive review and detailed protocol for a set of 29 traits known to be sensitive to global stressors and to affect ecosystem processes and services. We give rec- ommendations how to measure these traits under standardized conditions across various ter- restrial invertebrate taxonomic groups. 3. We provide considerations and approaches that apply to almost all traits described, such as the selection of species and individuals needed for the measurements, the importance of intraspecific trait variability, how many populations or communities to sample and over which spatial scales. 4. The approaches outlined here provide a means to improve the reliability and predictive power of functional traits to explain community assembly, species diversity patterns and ecosystem processes and services within and across taxa and trophic levels, allowing compar- ison of studies and running meta-analyses across regions and ecosystems. 5. This handbook is a crucial first step towards standardizing trait methodology across the most studied terrestrial invertebrate groups, and the protocols are aimed to balance general applicability and requirements for special cases or particular taxa. Therefore, we envision this handbook as a common platform to which researchers can further provide methodological input for additional special cases.

Effects of tree canopy composition on earthworms and other macro-invertebrates in beech forests of Upper Normandy (France)

Summary The effect of canopy composition on soil macro-invertebrate communities in two deciduous temperate forests: a pure beech (Fagus sylvatica L.) and a mixed beech-hornbeam (Carpinus betulus L.) stand was investigated. The initial hypothesis was that heterogeneity of trophic resources within the mixed stand might increase diversity and heterogeneity of soil macro-invertebrate communities at stand level. The macrofauna was sampled in autumn and spring by hand sorting 121 (25 × 25 × 30 cm) soil monoliths regularly distributed within each stand. Earthworms were identified to species level while the remaining macro-invertebrates were identified to family level. Results were analysed by univariate and multivariate (PCA) statistical tools as well as a geostatistical tool. Few differences were observed when comparing the total macro-invertebrate density between sites and dates. In contrast, significant patterns were found for several taxonomic or trophic groups taken separately (e.g. Lumbricidae, detritivore and predator densities were significantly higher in the pure beech stand (PS). The first and the third PCA axes respectively revealed a site and a season effect while the second axis revealed a spatial segregation within the detritivore group as it distinguished high densities of Lumbricidae from those of Isopoda and Diplopoda. The variance of record scores on this axis measured for each site and date revealed that spatial variability of soil macrofauna communities was greater for PS on both dates than for MS. Semi-variance analysis performed on record coordinates on the second axis of the PCA revealed that only macro-invertebrate communities sampled under the pure stand in autumn were spatially structured (autocorrelation range about 32 m). These results do not support the general agreement that resource diversity and patchiness increases soil fauna biodiversity and heterogeneity.

Functional traits of soil invertebrates as indicators for exposure to soil disturbance.

We tested a trait-based approach to link a soil disturbance to changes in invertebrate communities. Soils and macro-invertebrates were sampled in sandy soils contaminated by long-term wastewater irrigation, adding notably organic matter and trace metals (TM). We hypothesized that functional traits of invertebrates depict ways of exposure and that exposure routes relate to specific TM pools. Geophages and soft-body invertebrates were chosen to inform on exposure by ingestion or contact, respectively. Trait-based indices depicted more accurately effects of pollution than community density and diversity did. Exposure by ingestion had more deleterious effects than by contact. Both types of exposed invertebrates were influenced by TM, but geophages mainly responded to changes in soil organic matter contents. The trait-based approach requires to be applied in various conditions to uncorrelate specific TM impacts from those of other environmental factors.

Earthworm cast production as a new behavioural biomarker for toxicity testing

There is currently a lack of ecotoxicity tests adapted to earthworm species of higher ecological relevance and whose endpoints could be directly related to their ecological role in the soil. We propose a new and relatively simple ecotoxicity test based on the estimation of cast production (CP) by Lumbricus terrestris under laboratory conditions. CP was found to be linearly correlated to earthworm biomass and to be greatly influenced by soil water content. Azinphos-methyl had no effect on CP at all the concentrations tested. Significant decreases were observed at the normal application rate for other pesticides with (imidacloprid, carbaryl, methomyl) or without (ethyl-parathion and chlorpyrifos-ethyl) a clear concentration-effect response. For the highest concentration tested, reduction in CP varied between 35 and 67%. CP is straightforward and rapidly measured and ecologically meaningful. We thus believe it to be of great use as an endpoint in ecotoxicity testing.

Increasing soil carbon storage: mechanisms, effects of agricultural practices and proxies. A review

The international 4 per 1000 initiative aims at supporting states and non-governmental stakeholders in their efforts towards a better management of soil carbon (C) stocks. These stocks depend on soil C inputs and outputs. They are the result of fine spatial scale interconnected mechanisms, which stabilise/destabilise organic matter-borne C. Since 2016, the CarboSMS consortium federates French researchers working on these mechanisms and their effects on C stocks in a local and global change setting (land use, agricultural practices, climatic and soil conditions, etc.). This article is a synthesis of this consortium’s first seminar. In the first part, we present recent advances in the understanding of soil C stabilisation mechanisms comprising biotic and abiotic processes, which occur concomitantly and interact. Soil organic C stocks are altered by biotic activities of plants (the main source of C through litter and root systems), microorganisms (fungi and bacteria) and ‘ecosystem engineers’ (earthworms, termites, ants). In the meantime, abiotic processes related to the soil-physical structure, porosity and mineral fraction also modify these stocks. In the second part, we show how agricultural practices affect soil C stocks. By acting on both biotic and abiotic mechanisms, land use and management practices (choice of plant species and density, plant residue exports, amendments, fertilisation, tillage, etc.) drive soil spatiotemporal organic inputs and organic matter sensitivity to mineralisation. Interaction between the different mechanisms and their effects on C stocks are revealed by meta-analyses and long-term field studies. The third part addresses upscaling issues. This is a cause for major concern since soil organic C stabilisation mechanisms are most often studied at fine spatial scales (mm–μm) under controlled conditions, while agricultural practices are implemented at the plot scale. We discuss some proxies and models describing specific mechanisms and their action in different soil and climatic contexts and show how they should be taken into account in large scale models, to improve change predictions in soil C stocks. Finally, this literature review highlights some future research prospects geared towards preserving or even increasing C stocks, our focus being put on the mechanisms, the effects of agricultural practices on them and C stock prediction models.

Soil detritivore macro-invertebrate assemblages throughout a managed beech rotation

This work addresses the driving factors responsible for patterns in the detritivore macrofaunal communities of a managed beechwood chronosequence (28 to 197 years old, Normandy, France). We investigated the variation patterns of density, biomass and diversities of detritivore macrofauna throughout this rotation. Multivariate analyses were carried out to identify the main covariation patterns between species and some properties of their physical environment, and to describe the main ecological gradients constraining the macro-invertebrate community assembly. A total of 6 earthworm, 6 woodlouse and 7 millipede species were found in the whole data set. Density, biomass and diversity were profoundly influenced by forest ageing, mainly because of variation in humic epipedon spatial variability. Three groups of species were identified according to their environmental requirements. Some hypotheses regarding the external (related to management practices) or internal (related to inter-specific interactions) assembly rules behind species assemblages are proposed, an approach which has rarely been used in soil ecology. Finally, the impact of forestry practices on soil functioning through their impact on detritivore macro-invertebrate communities is discussed.RésuméCe travail a pour but d’identifier les facteurs responsables des schémas de variation des communautés de la macrofaune detritivore d’une chronoséquence (28 à 197 ans) de futaie régulière de hêtre (Normandie, France). Les modèles de variation de la densité, la biomasse et la diversité ont été recherchés. Les modèles de covariation entre les espèces et certaines propriétés physiques du milieu ainsi que les gradients écologiques qui contraignent les assemblages de macro-détritivores ont été décrits à l’aide d’analyses multivariées. En tout, 6 espèces de vers de terre, 6 espèces d’isopodes et 7 espèces de diplopodes ont été identifiées. La maturation du peuplement de hêtre, principalement par les modifications de l’épisolum humifère, influence fortement les densité, biomasse et diversité. Trois groupes d’espèces sont identifiés sur la base de leurs exigences environnementales. Quelques hypothèses sont proposées quant aux règles externes (liées aux pratiques sylvicoles) et internes (liées aux relations interspéciques) qui contraignent la composition des assemblages d’espèces, cette approche ayant jusqu’à présent été peu utilisée en écologie du sol. Enfin, l’impact des pratiques sylvicoles sur le fonctionnement du sol, au travers de leur impact sur les communautés de macro-détritivores, est discuté.

A Thesaurus for Soil Invertebrate Trait-Based Approaches

Soil invertebrates are known to be much involved in soil behaviour and therefore in the provision of ecosystem services. Functional trait-based approaches are methodologies which can be used to understand soil invertebrates’ responses to their environment. They (i) improve the predictions and (ii) are less dependent on space and time. The way traits have been used recently has led to misunderstandings in the integration and interpretation of data. Trait semantics are especially concerned. The aim of this paper is to propose a thesaurus for soil invertebrate trait-based approaches. T-SITA, an Internet platform, is the first initiative to deal with the semantics of traits and ecological preferences for soil invertebrates. It reflects the agreement of a scientific expert community to fix semantic properties (e.g. definition) of approximately 100 traits and ecological preferences. In addition, T-SITA has been successfully linked with a fully operational database of soil invertebrate traits. Such a link enhances data integration and improves the scientific integrity of data.

Is there a relationship between earthworm energy reserves and metal availability after exposure to field-contaminated soils?

Generic biomarkers are needed to assess environmental risks in metal polluted soils. We assessed the strength of the relationship between earthworm energy reserves and metal availability under conditions of cocktail of metals at low doses and large range of soil parameters. Aporrectodea caliginosa was exposed in laboratory to a panel of soils differing in Cd, Pb and Zn total and available (CaCl2 and EDTA-extractable) concentrations, and in soil texture, pH, CEC and organic-C. Glycogen, protein and lipid contents were recorded in exposed worms. Glycogen contents were not linked to the explaining variables considered. Variable selection identified CaCl2 extractable metals concentrations and soil texture as the main factors affecting protein and lipid contents. The results showed opposite effects of Pb and Zn, high inter-individual variability of biomarkers and weak relationships with easily extractable metals. Our results support the lack of genericity of energy reserves in earthworms exposed to field-contaminated soils.

A structural equation model of soil metal bioavailability to earthworms: confronting causal theory and observations using a laboratory exposure to field-contaminated soils

Structural equation models (SEM) are increasingly used in ecology as multivariate analysis that can represent theoretical variables and address complex sets of hypotheses. Here we demonstrate the interest of SEM in ecotoxicology, more precisely to test the three-step concept of metal bioavailability to earthworms. The SEM modeled the three-step causal chain between environmental availability, environmental bioavailability and toxicological bioavailability. In the model, each step is an unmeasured (latent) variable reflected by several observed variables. In an exposure experiment designed specifically to test this SEM for Cd, Pb and Zn, Aporrectodea caliginosa was exposed to 31 agricultural field-contaminated soils. Chemical and biological measurements used included CaC12-extractable metal concentrations in soils, free ion concentration in soil solution as predicted by a geochemical model, dissolved metal concentration as predicted by a semi-mechanistic model, internal metal concentrations in total earthworms and in subcellular fractions, and several biomarkers. The observations verified the causal definition of Cd and Pb bioavailability in the SEM, but not for Zn. Several indicators consistently reflected the hypothetical causal definition and could thus be pertinent measurements of Cd and Pb bioavailability to earthworm in field-contaminated soils. SEM highlights that the metals present in the soil solution and easily extractable are not the main source of available metals for earthworms. This study further highlights SEM as a powerful tool that can handle natural ecosystem complexity, thus participating to the paradigm change in ecotoxicology from a bottom-up to a top-down approach.