Land-use and land-management change: relationships with earthworm and fungi communities and soil structural properties

National monitoring programmes have often identified that soils under different land use and land management regimes harbour differing soil communities [1, 2]. In a limited number of cases the primary drivers of this variation have been identified, such as the strong influence of soil pH on bacterial communities [3]. When augmented by the results of smaller scale experimental and monitoring studies, which have frequently shown similar effects, these observations suggest a strong forcing effect of incumbent land use on overall soil community size and composition. Such community changes can have implications for soil functioning. In particular, the activities of specific groups of the soil biota (e.g. microorganisms, ecosystem engineers) are considered important to many soil functions that underpin the provision of ecosystem goods and services. These functionally relevant groups have become, therefore, an established focus for soil community and ecosystem process research [4–8].

With a relative wealth of data available describing patterns of land use associated change in overall abundance (at least for well-studied taxa) and also studies that link soil community characteristics to ecological metrics e.g. [3, 6, 9–11], quantifying these community effects and establishing their functional links to soil processes is potentially achievable. Here we have sought to summarise how some of the best-studied changes in land use and management affect community metrics for two key functional components of the soil biota, namely earthworms and soil fungi. We focus on transitions of extensification in land use that may benefit these taxa. Further, we relate community size changes for these two groups to influences on soil structural properties, thereby attempting to quantify implications of land use changes to functional linkages in the soil ecosystem.

The approach we have chosen for the assessment was based on a systematic review and meta-analysis of the published literature. For earthworms, the analysis focussed on assessing the effects of land use and land management changes on overall community size. This focus on total abundance was chosen because in published studies, detailed community characteristics, such as species identity, were often not reported; and this would have limited the size of the available data-set. For soil fungi, both overall abundance measures and community structural indicators were considered. This reflects the wider variety of metrics reported in the literature for this group. For both taxa, we sought to quantify the magnitude of community change occurring when land management practices or land use convert from more intensive to less intensive conditions. Three such scenarios were considered 1) implementation of reduced tillage regimes to previously intensively tilled lands; 2) conversion of managed arable land to natural or managed grassland; 3) successional conversion or afforestation of grassland to woodland.

To extend our review, we also considered the implications of earthworm and fungal community changes for soil properties in two further literature analyses. For earthworms, because the multiple roles of this group on greenhouse gas emissions and carbon sequestration have recently been comprehensively appraised [12], we focussed instead on the effects of community size and functional group (epigeic, endogeic, anecic) composition on soil porosity. This recognises the role of earthworms as ‘ecosystems engineers’ , capable of altering their physical environment through their casting and burrowing activities [13, 14]. For soil fungi, the association of community measures with soil microaggregate stability was determined to investigate the potentially important role of this group in the formation of soil aggregates, via hyphal growth and the production of coagulating substances like glomalin [15, 16]. These two analyses, thus, both consider how changes in community metrics for these two groups can translate through to effects on soil structure.

Our meta-analyses for land-use transition effects on community metrics highlighted a consistent trend across the two studied taxa. This pattern relates declining land use intensity with positive effects on community parameters, especially in agricultural lands. This trend is consistent with a number of studies that have examined earthworm and fungal communities under different land uses at independent sites over larger spatial scales [10, 20–24]. The value of our meta-analysis is that it provides a robust assessment of the effect sizes that are associated with steps in this transition. In the meta-analysis and in almost all individual studies, community metrics for both earthworms and fungi showed lowest values under intensive arable use. This is likely to be because soils under such management are subject to a combination of physical (e.g. tillage) and chemical (e.g. mineral fertiliser and pesticides) perturbations. When introduced, reduced or no-till management practices resulted in a generally significant positive effect on a range of community metrics for soil fungi. A similar significant positive effect of reducing tillage was also shown in a meta-analysis of primarily German data on tillage regime effects on earthworm abundance [25]. This latter study, however, also suggested that reduced tillage does not universally favour an increased density of all taxa, since Collembola numbers showed a trend for decrease under minimal management regimes.

The conversion of arable land to grassland represents a further reduction in land use intensity over reduced tillage, since soils under grassland are left to establish a normal depth profile. Further, the use of pesticides in such areas is often greatly reduced (compared to arable field) and organic inputs (dung, manures) can be greater. Conversion to pasture was found to be significantly beneficial for earthworm abundance and several fungal metrics. Analysis of density change with conversion time indicated a rapid accrual of earthworm numbers. Given the dominance of short-range dispersal in earthworms, the rapid change in earthworm densities following conversion, suggests that population increases are driven primarily by the recruitment of new progeny from the standing arable crop community. Since endogeic species may often be dominant in arable systems, it is such species that may be first to increase in number in response to grassland conversion. Later on as suitable food sources become available (especially surface litter) and recolonisation occurs, a more diverse community of epigeic, anecic and endogeic species can develop which can support or enhance ecosystem functions including water infiltration [26].

For fungi, a significant temporal trend in effect size of change in community metrics was seen following arable conversion to grassland. That effect sizes were positive across all major metric types, suggests an effect that is driven by abundance increases in a range of species from different fungal taxa. The general increase in fungal metrics seen is consistent with a series of studies that have reported such temporal effects. Thus in USA prairie lands, Bach et al. [27] found an asymptotic increase in arbuscular mycorrhizal fungal biomass between 0 and 18 years of restoration, while Van Der Wal et al. [22] found increases in fungal biomass and ergosterol across a chronosequence of abandoned arable land in the Netherlands. Such progressive changes in fungal community responses to grassland conversion suggest that colonisation rates may act to restrict the speed of fungal community change. However, there is also the potential for local controls on competition associated with the development of different organic substrates to regulate fungal community structure [28].

On grassland conversion to woodland, earthworm communities are generally maintained at previous grassland densities. For deciduous woodlands, identification of a consistent trend was challenging because of the high variation associated with effect size metrics. This variation probably reflects the strong effect of tree species composition on earthworm community development as observed in previous common garden experiments [29–31]. Only on conversion to coniferous woodland is there a suggestion of a negative impact on earthworm numbers (Figure 3). The relatively poor quality of coniferous needles as a food source [32], provides one explanation for this decline. Further, the chemistry and physical structure of soils associated with different woodlands may also affect soil habitat suitability for earthworms. For example, both earthworm survival and reproduction have been shown to be compromised in acidic soils [33, 34]. However, a direct effect of pH change on effect size was not statistically supported by the meta-analysis.

For fungi, over time Rao et al. [35] found ectomycorrhizal infection and diversity to increase in a chronosequence of pine stands from 2 to 17 years old. In contrast, our analysis suggests an overall negative relationship with fungal measures and time since conversion, although in contrast to Rao et al. [35] this was for deciduous woodland (the only woodland type for which sufficient studies were available for a reliable analysis). Different patterns of response were noticeable between major metric types following woodland conversion providing insights into the nature of community change. Significant reductions in Biomass measures associated with increases in Colonisation measures suggests a shift to a community containing a greater proportion of mycorrhizal species, as would be expected in ecosystems dominated by trees. Further analysis of areas subject to afforestation are needed to fill gaps in knowledge concerning land use effects on fungi especially in non-deciduous systems and the resulting impacts for their ecological functioning.

An explicit aim of the current study was to go beyond providing quantitative information on the effects of land use change on earthworm abundance and fungal community metrics to assess also the potential effect of such change on the contribution to soil structure of the two studied taxa. Soil structure is dependent on features including the nature and stability of microaggregates and the development and maintenance of macropores that result from the burrowing activities of earthworms [36]. To date, however, the precise relationships between earthworm and fungal community metrics and soil structural properties have not been analysed systematically. For earthworms, constructions of regression models in this study to link relevant drivers to soil porosity using the data available mainly from field studies identified that earthworm abundance, tillage system and habitat type each had a significant effect on water infiltration rate.

More detailed analyses identified that the effects of individual earthworm ecological groups on infiltration differed. Anecic and epigeic earthworms increased water infiltration significantly, but this effect was not seen for endogeic worms. A positive effect was anticipated for the deep burrowing anecics, as they maintain vertical burrows for feeding and casting at the soil surface [26, 37]. For this reason anecic earthworms have to date been the main ecological group considered in soil hydrological models [36]. Unlike anecics, epigeics are primarily surface dwellers living at the litter boundary or within this surface layer. Epigeics do not make vertical burrows, although shallow horizontal burrows can be maintained by some species [24, 38, 39]. Three factors relating to their lifestyle may explain the positive effect of epigeic species on water infiltration rates. Firstly, surface activity may prevent the formation of a soil surface crust of low water permeability. Secondly, the production and degradation of earthworm casts to form stable microaggregates can be important for soil moisture regulation and thus for water affinity and conductivity [40]. Finally, when exposed to adverse conditions (frost, drought), epigeic species may burrow deeper into the soil. At these times, epigeic earthworms can form temporary vertical burrows that may act as conduits for water flow.

The positive effects of anecic and epigeic species on water infiltration are important aspects for soil hydrology modelling. Bardgett et al. [41] outlined an approach that could be used to link earthworm community characteristics to soil hydrological processes. Both anecic and epigeic earthworms positively affect water transport to the deeper soil layer and ultimately to groundwater. This insight provides a challenge for land-management, since it is known that cultivation (disturbance) has a positive effect on soil hydraulic properties, yet such management is shown here to result in an average two to three fold reduction in earthworm abundance and negative effects on multiple soil fungal community metrics. Research to identify optimal strategies that exploit both the benefits of cultivation, while maintaining earthworm and fungal communities, is therefore needed to devise an approach that maximises hydrological processes to prevent run-off in managed lands.

Fungi too are known to contribute to soil structural development through hyphal growth and the production of coagulating substances like glomalin which may act as a ‘glue’ for soil microaggregates [15, 16]. In this study, the positive relationship between the responses of fungi and soil microaggregate stability, which was generally consistent across studies and transitions, demonstrates a strong functional link between these microbes and soil structure properties. This reinforces similar positive relationships found between glomalin and aggregate stability at individual locations e.g. [16, 42, 43]. That glomalin levels in common with a number of other fungal community metrics respond positively to extensification as land-use transition from arable to pasture to woodland, suggests that measurement of this protein may be a useful integrative indicator of changes in the fungal community and associated soil functional metrics.

The wealth of species that are present in soils has long been recognised to contribute to many important ecological processes [44–46]. Quantifying precisely how land use and land management practices influence important soil taxa can provide practitioners with essential information that can be used to identify best practices for sustainable soil management. For example, in unmanaged systems understanding the contribution of earthworm and fungal communities to soil porosity and structure can provide useful information that can help to assess vulnerability to surface run-off and water logging. In managed systems, this detailed information can be used to identify best practice in relation to tillage levels and resulting effects on earthworms and fungi. The wider up-scaling of this knowledge through modelling to the landscape level can then be used to enhance the scientific basis for environmental economic modelling, providing a basis for sound decision making that optimises environmental benefits and enhance farmers’ income security [47].

To provide quantitative data on the impact of land management and land use change on earthworm and fungal community metrics, an established systematic literature review optimised for the available project resources was followed [48, 49]. Three clearly defined land management and land use transitions were considered. First, paired experiments in which fields within the same region were subjected to conventional tillage versus reduced/no till management (herein referred to as the “Tillage comparison”). No detailed results were presented here for earthworms because independent reviews of the effect of tillage on earthworm communities have recently been published [25, 50], and also because a separate detailed meta-analysis of different tillage practices, soil type and sampling method effects on earthworm community size and diversity aspects is forthcoming (Schmidt et al., unpublished). Second, studies in which separate fields in a region have been kept under conventional arable use or converted to natural grassland or grazing pasture, or alternatively have been kept under arable versus grassland use for a known period (herein referred to as “Arable to grassland conversion”). Third, studies in which separate areas in a region have been kept as grassland or have undergone natural succession to tropical, deciduous or coniferous woodland or have been actively planted with trees for later agroforestry cropping (herein referred to as the “Grassland to woodland conversion”).