Tancredi Caruso

Choosing and using diversity indices: Insights for ecological applications from the German Biodiversity Exploratories

Biodiversity, a multidimensional property of natural systems, is difficult to quantify partly because of the multitude of indices proposed for this purpose. Indices aim to describe general properties of communities that allow us to compare different regions, taxa, and trophic levels. Therefore, they are of fundamental importance for environmental monitoring and conservation, although there is no consensus about which indices are more appropriate and informative. We tested several common diversity indices in a range of simple to complex statistical analyses in order to determine whether some were better suited for certain analyses than others. We used data collected around the focal plant Plantago lanceolata on 60 temperate grassland plots embedded in an agricultural landscape to explore relationships between the common diversity indices of species richness (S), Shannon’s diversity (H’), Simpson’s diversity (D1), Simpson’s dominance (D2), Simpson’s evenness (E), and Berger–Parker dominance (BP). We calculated each of these indices for herbaceous plants, arbuscular mycorrhizal fungi, aboveground arthropods, belowground insect larvae, and P. lanceolata molecular and chemical diversity. Including these trait-based measures of diversity allowed us to test whether or not they behaved similarly to the better studied species diversity. We used path analysis to determine whether compound indices detected more relationships between diversities of different organisms and traits than more basic indices. In the path models, more paths were significant when using H’, even though all models except that with E were equally reliable. This demonstrates that while common diversity indices may appear interchangeable in simple analyses, when considering complex interactions, the choice of index can profoundly alter the interpretation of results. Data mining in order to identify the index producing the most significant results should be avoided, but simultaneously considering analyses using multiple indices can provide greater insight into the interactions in a system.

Relative role of deterministic and stochastic determinants of soil animal community: a spatially explicit analysis of oribatid mites

1. Ecologists are debating the relative role of deterministic and stochastic determinants of community structure. Although the high diversity and strong spatial structure of soil animal assemblages could provide ecologists with an ideal ecological scenario, surprisingly little information is available on these assemblages. 2. We studied species-rich soil oribatid mite assemblages from a Mediterranean beech forest and a grassland. We applied multivariate regression approaches and analysed spatial autocorrelation at multiple spatial scales using Morans eigenvectors. Results were used to partition community variance in terms of the amount of variation uniquely accounted for by environmental correlates (e.g. organic matter) and geographical position. Estimated neutral diversity and immigration parameters were also applied to a soil animal group for the first time to simulate patterns of community dissimilarity expected under neutrality, thereby testing neutral predictions. 3. After accounting for spatial autocorrelation, the correlation between community structure and key environmental parameters disappeared: about 40% of community variation consisted of spatial patterns independent of measured environmental variables such as organic matter. Environmentally independent spatial patterns encompassed the entire range of scales accounted for by the sampling design (from tens of cm to 100 m). This spatial variation could be due to either unmeasured but spatially structured variables or stochastic drift mediated by dispersal. Observed levels of community dissimilarity were significantly different from those predicted by neutral models. 4. Oribatid mite assemblages are dominated by processes involving both deterministic and stochastic components and operating at multiple scales. Spatial patterns independent of the measured environmental variables are a prominent feature of the targeted assemblages, but patterns of community dissimilarity do not match neutral predictions. This suggests that either niche-mediated competition or environmental filtering or both are contributing to the core structure of the community. This study indicates new lines of investigation for understanding the mechanisms that determine the signature of the deterministic component of animal community assembly.

Arbuscular mycorrhizal fungal communities are phylogenetically clustered at small scales

Next-generation sequencing technologies with markers covering the full Glomeromycota phylum were used to uncover phylogenetic community structure of arbuscular mycorrhizal fungi (AMF) associated with Festuca brevipila. The study system was a semi-arid grassland with high plant diversity and a steep environmental gradient in pH, C, N, P and soil water content. The AMF community in roots and rhizosphere soil were analyzed separately and consisted of 74 distinct operational taxonomic units (OTUs) in total. Community-level variance partitioning showed that the role of environmental factors in determining AM species composition was marginal when controlling for spatial autocorrelation at multiple scales. Instead, phylogenetic distance and spatial distance were major correlates of AMF communities: OTUs that were more closely related (and which therefore may have similar traits) were more likely to co-occur. This pattern was insensitive to phylogenetic sampling breadth. Given the minor effects of the environment, we propose that at small scales closely related AMF positively associate through biotic factors such as plant-AMF filtering and interactions within the soil biota.

Compositional divergence and convergence in arbuscular mycorrhizal fungal communities.

In spite of the controversy that they have generated, neutral models provide ecologists with powerful tools for creating dynamic predictions about beta-diversity in ecological communities. Ecologists can achieve an understanding of the assembly rules operating in nature by noting when and how these predictions are met or not met. This is particularly valuable for those groups of organisms that are challenging to study under natural conditions (e.g., bacteria and fungi). Here, we focused on arbuscular mycorrhizal fungal (AMF) communities and performed an extensive literature search that allowed us to synthesize the information in 19 data sets with the minimal requisites for creating a null hypothesis in terms of community dissimilarity expected under neutral dynamics. In order to achieve this task, we calculated the first estimates of neutral parameters for several AMF communities from different ecosystems. Communities were shown either to be consistent with neutrality or to diverge or converge with respect to the levels of compositional dissimilarity expected under neutrality. These data support the hypothesis that divergence occurs in systems where the effect of limited dispersal is overwhelmed by anthropogenic disturbance or extreme biological and environmental heterogeneity, whereas communities converge when systems have the potential for niche divergence within a relatively homogeneous set of environmental conditions. Regarding the study cases that were consistent with neutrality, the sampling designs employed may have covered relatively homogeneous environments in which the effects of dispersal limitation overwhelmed minor differences among AMF taxa that would lead to environmental filtering. Using neutral models we showed for the first time for a soil microbial group the conditions under which different assembly processes may determine different patterns of beta-diversity. Our synthesis is an important step showing how the application of general ecological theories to a model microbial taxon has the potential to shed light on the assembly and ecological dynamics of communities.

Primary assembly of soil communities: disentangling the effect of dispersal and local environment

It has long been recognised that dispersal abilities and environmental factors are important in shaping invertebrate communities, but their relative importance for primary soil community assembly has not yet been disentangled. By studying soil communities along chronosequences on four recently emerged nunataks (ice-free land in glacial areas) in Iceland, we replicated environmental conditions spatially at various geographical distances. This allowed us to determine the underlying factors of primary community assembly with the help of metacommunity theories that predict different levels of dispersal constraints and effects of the local environment. Comparing community assembly of the nunataks with that of non-isolated deglaciated areas indicated that isolation of a few kilometres did not affect the colonisation of the soil invertebrates. When accounting for effects of geographical distances, soil age and plant richness explained a significant part of the variance observed in the distribution of the oribatid mites and collembola communities, respectively. Furthermore, null model analyses revealed less co-occurrence than expected by chance and also convergence in the body size ratio of co-occurring oribatids, which is consistent with species sorting. Geographical distances influenced species composition, indicating that the community is also assembled by dispersal, e.g. mass effect. When all the results are linked together, they demonstrate that local environmental factors are important in structuring the soil community assembly, but are accompanied with effects of dispersal that may “override” the visible effect of the local environment.

The Berger–Parker index as an effective tool for monitoring the biodiversity of disturbed soils: a case study on Mediterranean oribatid (Acari: Oribatida) assemblages

Recent data on oribatid mites (Acari: Oribatida) indicates that Mediterranean soil communities tend to show uneven patterns of species abundance distribution (SAD) that are well fitted by a simple model such as the geometric series. In the case of linear distributions, the fraction of total sampled individuals that is contributed by the most abundant species, known as the Berger–Parker index, synthetically describes the SAD of disturbed communities. This study assessed the bioindicator potential of the Berger–Parker index by comparing its variations among Mediterranean oribatid assemblages under different types of soil disturbance. The index significantly changes between undisturbed and disturbed soils reaching the highest values in areas with strong physical disturbance due to agricultural management. The Berger–Parker index is therefore a practical and effective tool for monitoring biodiversity impairment linked to human disturbance in soil ecosystems.

Arbuscular mycorrhizal fungi – short‐term liability but long‐term benefits for soil carbon storage?

The interaction between plants and mycorrhizal fungi represents a major link between atmospheric and soil-contained carbon (C). In order to estimate the fate of atmospheric CO2 under the projected increases in the upcoming century, ranging from an increase of 20% to > 200% compared with current concentrations (Pachauri & Reisinger, 2007), it is crucial to understand how plants and mycorrhizal fungi either buffer or exacerbate atmospheric CO2 rises through their effects on soil C sequestration. Indirect evidence suggests that arbuscular mycorrhizal fungi (AMF) generally stimulate soil carbon pools (Wilson et al., 2009), and experience enhanced growth under elevated CO2 (eCO2) (Antoninka et al., 2011), leading to the assumption that they will buffer atmospheric CO2 increases. However, long-term experiments under eCO2 show both increased carbon storage (Iversen et al., 2012) and accelerated decomposition (negating the effect of the increase of soil carbon inputs; Phillips et al., 2012), leaving the question as to whether soils will buffer against CO2 increases wide open.While there is a dearth of direct empirical evidence regarding the involvement of AMF in soil C storage processes under conditions of global change, there is uncertainty about how component processes leading to soil C storage will be affected. Recently, Cheng et al. (2012) presented a compelling body of evidence to suggest that AMF may diminish rather than enhance soil C pools in the topsoil. Their findings are based on the observation that, in the presence of AMF, fresh above-ground plant litter decomposes faster, in particular at eCO2 and increased nitrogen (N) concentrations (Cheng et al., 2012). This observation suggests that AMF can accelerate decomposition and can even lead to a loss of soil C pools, at least in the short term. However, we feel that other parts of the soil C equation will need to be resolved in order to fully understand how AMF affect long-term soil C-sequestration potential. This is because short-term experiments do not account for potential increases in organic matter (OM) of plant or microbial origin triggered by increased decomposition; long-term (decadal scale) effects of soil biota such as AMF can be qualitatively different from short-term effects; and pulse increases of CO2 and N affect soils in a way that may not represent a system where CO2 and N are at consistently higher concentrations. Soil C sequestration is the net build-up of C in the entire soil profile through accumulation ofOM from plant, fungal (and other microbial) and animal origins. Decomposition of OM is an ongoing process, and snapshot rate assessments must therefore be interpreted with caution. If a particular nutrient (e.g. C or N) is elevated, this may lead to accelerated decomposition, but conclusions about soil C gain or loss can only be drawn if the effect of biomass increases of all biota is also incorporated into the equation (Fig. 1a). This becomes apparent in a simplemodel where AMF are allowed to produce recalcitrant compounds (such as various polysaccharides (K€ogel-Knabner, 2002) and glomalin, in line with experimental observations; Rillig, 2004) that contribute to the future OM fraction (see Fig. 1b). In the short term, an AMFmediated increase in decomposition of labile plant littermay lead to a reduction of soil C. However, the C balance is offset by a longterm gain in recalcitrant compounds (Fig. 1a). Contributions of AMF are likely to be further amplified through physically protecting OM from decomposition by means of soil aggregation (Rillig, 2004) and via a general increase in plant productivity and hence significantly higher litter input (Hoeksema et al., 2010). The principal mechanism by which AMF are proposed to stimulate soil C efflux is through priming of decomposers, which is a commonly observed soil-biotic response to increased (labile) OM deposition (de Graaff et al., 2010). However, whether this stimulation of soil saprobes is a permanent effect will require further study: C pulses and the resulting soil fungal community responses are a well-appreciated side-effect of sudden-onset CO2 exposure designs, which disappearwhenCO2 is gradually increased (Klironomos et al., 2005). Such sudden increases in atmospheric CO2 concentration are unlikely to happen in the near future. By contrast, other parameters will likely change under permanently altered amounts of resources, for instance litter quality. Decomposability of plant litter is known to decrease following plant exposure to eCO2 (Norby et al., 2001), and has the potential to buffer soil C concentrations against effects predicted from shortterm experiments. Thus the magnitude of priming effects through AMF under permanent eCO2 (as opposed to pulse elevation) must be scaled against indirect effects on litter quality to fully appreciate the contribution of AMF to plant-derived soil C concentrations. A way in which short-term experimental studies could control for some of these effects is to include additional treatments where soil and OM (thus controlling for factors such as soil aggregation and quantity and quality of litter) have been preconditioned, to the extent feasible, according to experimental treatments of interest (e.g. ambient vs eCO2; low vs high N; + vs AMF) in a factorial manner. Another highly useful addition might be a treatment where plant roots but not AMF can access plant litter generated under ambient vs eCO2 concentrations (a true nonAMF treatment). Even though these approaches do not resolve all fundamental issues arising from predicting long-term processes with short-term experiments, decomposition in the eCO2 and AMF treatments can be compared between ‘uniform’ and ‘preconditioned’ (according to treatment) plant and soil material. This way

Interactive effects of root endophytes and arbuscular mycorrhizal fungi on an experimental plant community.

Plant-soil microbial interactions have moved into focus as an important mechanism for understanding plant coexistence and composition of communities. Both arbuscular mycorrhizal (AM) as well as other root endophytic fungi co-occur in plant roots, and therefore have the potential to influence relative abundances of plant species in local assemblages. However, no study has experimentally examined how these key root endosymbiont groups might interact and affect plant community composition. Here, using an assemblage of five plant species in mesocosms in a fully factorial experiment, we added an assemblage of AM fungi and/or a mixture of root endophytic fungal isolates, all obtained from the same grassland field site. The results demonstrate that the AM fungi and root endophytes interact to affect plant community composition by changing relative species abundance, and consequently aboveground productivity. Our study highlights the need to explicitly consider interactions of root-inhabiting fungal groups in studies of plant assemblages.

Indigenous Arbuscular Mycorrhizal Fungal Assemblages Protect Grassland Host Plants from Pathogens

Plant roots can establish associations with neutral, beneficial and pathogenic groups of soil organisms. Although it has been recognized from the study of individual isolates that these associations are individually important for plant growth, little is known about interactions of whole assemblages of beneficial and pathogenic microorganisms associating with plants. We investigated the influence of an interaction between local arbuscular mycorrhizal (AM) fungal and pathogenic/saprobic microbial assemblages on the growth of two different plant species from semi-arid grasslands in NE Germany (Mallnow near Berlin). In a greenhouse experiment each plant species was grown for six months in either sterile soil or in sterile soil with one of three different treatments: 1) an AM fungal spore fraction isolated from field soil from Mallnow; 2) a soil pathogen/saprobe fraction consisting of a microbial community prepared with field soil from Mallnow and; 3) the combined AM fungal and pathogen/saprobe fractions. While both plant species grew significantly larger in the presence of AM fungi, they responded negatively to the pathogen/saprobe treatment. For both plant species, we found evidence of pathogen protection effects provided by the AM fungal assemblages. These results indicate that interactions between assemblages of beneficial and pathogenic microorganisms can influence the growth of host plants, but that the magnitude of these effects is plant species-specific.

Spatial patterns and autocorrelation in the response of microarthropods to soil pollutants: The example of oribatid mites in an abandoned mining and smelting area

Although exogenous factors such as pollutants can act on endogenous drivers (e.g. dispersion) of populations and create spatially autocorrelated distributions, most statistical techniques assume independence of error terms. As there are no studies on metal soil pollutants and microarthropods that explicitly analyse this key issue, we completed a field study of the correlation between Oribatida and metal concentrations in litter, organic matter and soil in an attempt to account for spatial patterns of both metals and mites. The 50-m wide study area had homogenous macroscopic features, steep Pb and Cu gradients and high levels of Zn and Cd. Spatial models failed to detect metal-oribatid relationships because the observed latitudinal and longitudinal gradients in oribatid assemblages were independent of the collinear gradients in the concentration of metals. It is therefore hypothesised that other spatially variable factors (e.g. fungi, reduced macrofauna) affect oribatid assemblages, which may be influenced by metals only indirectly.