Effects of soil pollutants, biogeochemistry and microbiology on the distribution and composition of enchytraeid communities in urban and suburban holm oak stands

Highlights

• We examined the enchytraeid assemblages of urban holm oak stands in relation to pollution gradients.

• Only the co-variation between pollution and other soil chemico-physical factors showed significant effects.

• Thermophilous species in Fridericia and Achaeta are mainly affected by Ca bioavailability.

Abstract

Holm oaks form typical urban woodlands in the Mediterranean region. We aimed at characterizing the enchytraeid communities in these environments and searching for possible correlations with soil parameters, including the traffic contamination. Samples of litter and topsoil were collected at different spatial scales and seasons in Naples and Siena cities and in two suburban stands. Only the co-variation between pollution and other soil chemico-physical factors showed significant effects, whereas no direct effect of soil microbiology was detected. Some thermophilous Fridericia and Achaeta tolerate high concentrations of heavy metals and PAHs and their abundance was mainly determined by Ca bioavailability. Central-European mesophilous species increased significantly under more temperate environmental conditions. Different combinations of soil cohesiveness, grain size composition and moisture regime seem to select species of certain body sizes.

Introduction

Terrestrial annelids play key ecological roles in a wide range of ecosystems and are directly exposed to soil gaseous, liquid and solid phases. They are sensitive to environmental stress factors (e.g. Capowiez et al., 2010; Fründ et al., 2010; Pereira et al., 2010) and standard bioassay methods using earthworms (e.g. ISO, 1998, 2008) and enchytraeids (ISO, 2004) are among the most broadly accepted in soil toxicity testing. Changes in oligochaete species richness and composition are used in German and Dutch biological soil classification networks for the characterization of soil properties and disturbances (see Jänsch et al., 2005; Beylich and Graefe, 2009). However, in natural settings, faunal communities are modulated by complex interactions with a range of physical, chemical and biotic factors and it is difficult to single out what conditions are really crucial for the occurrence and abundance of each species. Some laboratory studies indicate the negative effects of heavy metals, PAHs, pesticides and pharmaceuticals on enchytraeid survival (e.g. Römbke, 2003; Jarratt and Thompson, 2009), but in central and northern Europe the number of species in this family can be very high in urban environments, reaching 24–27 for a single lawn in Hamburg (Graefe et al., unpubl. in Schlaghamerský and Pižl, 2009), Berlin (Heck et al., 1999) and Potsdam (Möller, 1971). Population densities and species number at urban greens appear to vary according to the type and management of soil and vegetation (higher densities and biomass in forests, higher number of species in grassland sites) rather than to levels of environmental pollution (Kasprzak, 1986). However, the assessment of the effects of pollutants on soil communities is often biased by the many confounding effects that one has to take into account in observational studies (e.g. Legendre and Legendre, 1998). A fundamental issue is the spatial scale at which gradients in pollutant concentrations are likely to affect the specific soil fauna assemblage (Ettema and Wardle, 2002; Caruso et al., 2009). Soil animal assemblages display a multitude of spatial patterns at multiple scales, which are caused by processes acting at scales ranging from few cm to regional (Ettema and Wardle, 2002), and correlations between spatial patterns of pollutants and the soil fauna distribution might be invalidated if spatial autocorrelation is not taken into account (Caruso et al., 2009). This can be solved by adopting a strategy based on a spatial replication of pollution gradients, coupled with partial correlation and partial regression analyses that control for the effects of spatial autocorrelation and the other factors influencing soil animal assemblages (e.g. water content, organic matter). Under these circumstances, the more the analysed group is diverse in terms of species spatial turnover, the more this group is likely to “detect” an effect of the pollution gradient, all the rest being taken into account statistically (e.g. environmental covariates such as soil moisture, organic matter or vegetation type).

Very little information is available on enchytraeid communities in Mediterranean ecosystems, although in some typical habitats such as evergreen oak forests they are always present, often with rich species assemblages (see Rota, 1995). In such habitats, enchytraeids often play a more important role than earthworms, because the high content of tannin (2.1% d.w. in holm oak leaves; Sadaka-Laulan and Ponge, 2000) reduces the litter palatability for most earthworm species, limiting the latter to few specialized forms. Since the 16th century holm oak (Quercus ilex L.) trees have been used in the landscaping of many Italian urban parks and gardens; their leaves are efficient interceptors of airborne contaminants and are one of the most used matrices for passive biomonitoring of atmospheric deposition of persistent contaminants in urban environments (e.g. Monaci et al., 2000; De Nicola et al., 2008; Gratani et al., 2008).

With the aim of contributing to the knowledge of enchytraeid assemblages in Mediterranean urban ecosystems and evaluating the role of environmental parameters (including pollutants) in structuring their communities, we investigated community patterns in urban and suburban holm oak stands in a small (Siena) and a large (Naples) city. A number of soil variables (pH, texture, fungal and bacterial biomass, moisture, organic matter, trace metals and PAHs concentrations) were determined. By taking into account the effects of several covariates such as soil variables and spatial autocorrelation in species distribution at multiple scales, we tested the main hypothesis that changes in level of soil pollutants significantly correlate with changes in enchytraeid species distribution.