The negative effect of wood ants (Formica rufa) on microarthropod density and soil biological quality in a semi-arid pine forest

Abstract

Wood ants (Formica rufa group) are widely distributed in the northern hemisphere and have an important effect on ecosystem processes. The objectives of this study were to evaluate the relationship between F. rufa and the soil biological quality and microarthropod diversity in a semi-arid black pine forest. Microarthropod sampling was conducted for 2 years, from October 2014 to September 2016, at four ant nest mounds of similar size. A total of 288 soil cores were sampled bimonthly, near the nests (designated as the adjacent zone) and at a distance of 10 m away from the nests (designated as the distant zone) during the study period. The results were evaluated by the mean density, QBS-ar index, and Shannon diversity index scores. The mean density of the microarthropods in the adjacent zone (32,797 ind m^–2) was lower than the mean density observed in the distant zone (44,462 ind m^–2). The Shannon diversity index values were insensitive to differences in microarthropod density, as affected by wood ants, between the adjacent and distant zones, but the QBS-ar values were significantly different between the zones. This suggested that the QBS-ar index may be advantageous in monitoring the impact of wood ants on soil microarthropods in a semi-arid pine forest. Overall, this study reveals that F. rufa may have a significant impact on soil microarthropods in semi-arid forest ecosystems.

Introduction

Ants are ecosystem engineers (Bottinelli et al., 2015; Jones et al., 1994; Jouquet et al., 2006; Lavelle, 1997) and are important contributors to soil bioturbation, organic matter decomposition, and nutrient mineralization (Domisch et al., 2008; Jouquet et al., 2006); the biotic defence of plants (Rosumek et al., 2009); and the regulation of herbivores (Whittaker and Warrington, 1985); they are widely regarded as keystone taxa. Ant species are considered to be good bioindicators for environmental and land-use changes and soil-based ecosystem services (Majer, 1983; Sanabria et al., 2014; Tiede et al., 2017). Thus, ants may be worthy of more attention as studies of soil biology continue.

Wood ants (Formica rufa group) are found in many areas in the northern hemisphere (Stockan and Robinson, 2016). Wood ant nests have above-ground mounds and below-ground areas that are generally similar in volume (Jurgensen et al., 2008). The above-ground mounds are made of needles, leaves, twigs, and bark, materials that affect the nest pH directly or indirectly (Jílková et al., 2011, 2012). Wood ants build corridors and chambers in their nests, and these structures affect the porosity and aeration of soils near the nests (Frouz and Jilkova, 2008). Consequently, as wood ants design and build their nests, they modify the properties of the surrounding soils and generate certain conditions within their nests. The interiors of the nests have a high moisture content (Frouz, 2000), which creates an appropriate microclimate for microorganisms; it allows for greater microbial activity and higher rates of decomposition and nutrient cycling inside the nests than in adjacent soils (Cerda and Jurgensen, 2008; Jilkova et al., 2013; Laakso and Setälä, 1997). Depending on the density of wood ant nests in a given area, the total amount of litter decomposition that occurs inside the nests can have a significant overall impact on the area (Jílková et al., 2012).

Ants may alter soil conditions outside the nest through their foraging activities (Frouz and Jilkova, 2008). Wood ants actively prey on above-ground and tree-level invertebrates. Because wood ants mainly forage in the tree canopy and litter layer, their effects on soil fauna are regarded as minimal (Skinner, 1980). In a number of studies, including those using ant removal experiments, the impact of wood ants on soil invertebrates was found to be only slightly significant or nonsignificant, especially where plenty of tree-crown invertebrates were available as a food resource (Laakso and Setälä, 2000; Lenoir et al., 2003; Robinson et al., 2016). In other circumstances, however, as when wood ants were forced to forage on the forest floor, the ants did have some effects on the soil fauna (Lenoir, 2003). Results from a study by Robinson et al. (2016) indicated that the foraging activity of F. rufa may influence the soil fauna, either directly (by suppressing competing predators) or indirectly (by reducing the numbers of herbaceous plants, which caused the litter quality to deteriorate). Wood ants collected needle litter for building their nests, decreasing the amount of litter and affecting the nutrient cycle in the area of their influence. They affected the arthropod decomposer community by their activities in foraging, decomposition, and nutrient cycling (Domisch et al., 2008; Stadler et al., 2006). Besides their effects on nutrient cycling and plant productivity, the predation pressure was probably different in wood ant nests and in soils adjacent to the nests (Johansson and Gibb, 2016; Savolainen and Vepsäläinen, 1988). The ants were able to compete more aggressively than other predators, such as Coleoptera, Araneae, Chilopoda, and predatory mites; this influenced the decomposers, especially the microarthropod decomposers (Laakso et al., 1995; Moore et al., 1988).

Numerous microarthropods (e.g., Collembola, Acarina, Protura) dwell in different types of soils and litter layers (Coleman et al., 2004). Soil microarthropods have body widths from 100 μm to 2 mm (Swift et al., 1979) and have significant effects on ecosystem processes (Cole et al., 2006; Cragg and Bardgett, 2001) such as litter decomposition, nutrient turnover on the forest floor, and primary production; they also have a crucial role in the context of soil biodiversity in forest ecosystems (Birkhofer et al., 2011; Wagg et al., 2014). The density of microarthropods can be influenced by wood ants via a number of mechanisms such as changes to pH and aeration (Frouz and Jilkova, 2008), decomposition rates (Domisch et al., 2008) and soil nutrient dynamics (Finér et al., 2013). These effects may arise from the building of nests, the breaking up of organic material, and foraging by ants in the litter layer.

The literature on the impact of wood ants on soil microarthropods is limited, and, therefore, research is needed to address their relationship to diversity levels of soil microarthropods and to soil biological quality. Microarthropods are well-described members of the soil biota, and several alternative methods are available to assess the impact on them of a wide range of factors. For example, the Soil Biological Quality index based on arthropods (QBS-ar), introduced by Parisi et al. (2005), determines the soil biological quality by evaluating how well soil microarthropods can adapt to changing soil habitats. Because the QBS-ar index assesses both the biodiversity and vulnerability of soil microarthropods (Menta et al., 2018), it potentially can link the soil quality to any disturbances that alter its score. So far, the index has been used mainly to determine the impact of anthropogenic disturbances on soil quality (Parisi et al., 2005). In the future, it may be used to evaluate the impact of natural disturbances, such as those caused by wood ants, on soil microarthropods.

A literature search showed that information on the role of wood ants in the soil microarthropod community, especially in semi-arid regions, is quite minimal. Studies conducted in boreal regions have shown that there is no significant impact of wood ants on soil microarthropods (Laakso and Setälä, 2000; Lenoir et al., 2003; Punttila et al., 2004). However, these results may not be generalized to temperate regions, where food is often limited for wood ants, forcing them to prey on soil invertebrates as alternative food resources (Duma, 2003; Lenoir et al., 2003). Additionally, although the QBS-ar index has been used in many ways, it has not been used to evaluate the impact of wood ants on soil microarthropods. It does seem to have the potential for such a use because it accounts for their existence in soil.

The aim of this study was to evaluate ecological relationships between wood ants and soil microarthropods in a typical semi-arid pine forest ecosystem. In addition, it assessed the potential of the QBS-ar index for evaluating the effect of wood ants on soil microarthropods in such an ecosystem.