Ant and Earthworm Bioturbation in Cold-Temperate Ecosystems

Ecosystems https://doi.org/10.1007/s10021-018-0317-2  2018 The Author(s) Ant and Earthworm Bioturbation in Cold-Temperate Ecosystems A. R. Taylor,1* L. Lenoir,1 B. Vegerfors,2 and T. Persson1 1 Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, 750 07 Uppsala, Sweden; 2Department of Energy and Technology, Swedish University of Agricultural Sciences, Box 7032, 750 07 Uppsala, Sweden ABSTRACT In temperate ecosystems, earthworms and ants are the most important organisms for bioturbation. Little is known about how these groups contribute to bioturbation in different environments and to what extent overall bioturbation depends on their diversity. We developed a formula that allows quantification of annual earthworm bioturbation, thereby taking differences between earthworm ecotypes into account. With this formula, we calculated earthworm bioturbation at three sites, each with vegetation types typically found in Northern Europe. Earthworm bioturbation was low (1 Mg dry soil ha-1 y-1) in Scots pine and Norway spruce forests with acidic soil (pH 3.9–4.4) and high (between 15 and 34 Mg dry soil ha-1 y-1) in broadleaf forests, grasslands, alder carr and spruce forests on calcareous soil. Burrowing (endogeic and anecic) earthworms accounted for most of the earthworm bioturbation, and these worms had the highest population densities at moderate-to-high soil pH (pH 5–7.2). Estimates of ant bioturbation at the same sites were based on nest abundance, size and residence time. Mean ant bioturbation varied between 0.2 and 1 Mg dry soil ha-1 y-1, but individual plots had up to 2.4 Mg dry soil ha-1 y-1. In soils with pH higher than 5, the relative contribution of ants to total bioturbation was only 1–5%. Ant bioturbation was higher than earthworm bioturbation only in some forest soils with pH 3.9–4.4. Thus, earthworms appear to be the dominant cause of bioturbation in most types of terrestrial ecosystems in the cold-temperate areas of Europe and when information on local earthworm communities and monthly soil temperatures is available, bioturbation can be quantified using the presented ‘earthworm bioturbation formula’. Key words: Aporrectodea caliginosa; egestion; Lumbricidae; Myrmica; nest density; pH; soil turnover; temperature dependence. HIGHLIGHTS Received 20 January 2018; accepted 29 September 2018 Author Contribution: T. Persson conceived the funding, designed the study and performed the research together with L. Lenoir and A.R. Taylor. T. Persson developed the model to estimate earthworm bioturbation, L. Lenoir estimated ant bioturbation and A.R. Taylor contributed with new methods for the underlying baseline research. B. Vegerfors analysed the data. A.R. Taylor and T. Persson wrote the paper and L. Lenoir commented on the manuscript. *Corresponding author; e-mail:  We present a method to calculate earthworm and ant bioturbation  Earthworm and ant bioturbation depended on the species composition  Earthworm bioturbation was larger than ant bioturbation at soil pH > 4.3 INTRODUCTION In cold-temperate regions, earthworms and ants are the most important ‘ecosystem engineers’ (Lavelle and others 1997; Jones and Gutiérrez 2007) A.R. Taylor and others that significantly affect the structure and function of the ecosystems they inhabit (Folgarait 1998; Le Bayon and others 2017) via their bioturbation activity. Bioturbation, that is, the biological reworking of soils and sediments (Meysman and others 2006), takes place when earthworms and ants transport soil and organic matter from one place to the other. Earthworms translocate and mix soil when feeding/egesting, while ants bioturbate via their nest-building activities. Earthworm and ant bioturbation contributes to a range of ecosystem services, like decomposition, nutrient cycling, soil structuring/formation and the regulation of water and gas exchange (Lavelle and others 2006; Wall and others 2012). However, the impact of bioturbation on individual services and the temporal and spatial dynamics of their bioturbation activity differ significantly between both groups (Folgarait 1998; Wilkinson and others 2009; Blouin and others 2013; Turbé and others 2010). This is, on the one hand, due to earthworms and ants having different spatial aggregation patterns, dispersal distances and life spans. On the other hand, the longevity and physical and chemical properties of the biotic structures created by both groups above-ground (for example, mounds, nests, casts, middens) and below-ground (for example, galleries, chambers, burrows, casts) are distinctly different (Hedde and others 2005). Earthworm casts and burrows differ from ant artefacts by the origin of their organic matter (OM) and the gut transit experienced before structure building. Thus, the resource quality for microorganisms in these biostructures differs depending on engineer foraging specificity leading to differences in the OM humification rates (Hedde and others 2005). There are only few studies that directly link the functioning of biological soil components like that of soil ecosystem engineers to ecosystem services (Adhikari and Hartemink 2016) because it is inherently difficulty to measure their impact on a particular ecosystem service under field conditions (Barrios 2007). To assess the full impact of environmental engineering by earthworms and ants in cold-temperate regions, it is important to consider the cumulative effects of bioturbation by both groups and to relate the rate of material transport to their community characteristics, that is, species composition and abundance, in the particular environment investigated (Wilkinson and others 2009). Differences in the bioturbation activity of earthworm species are reflected in the common division into three ecological types (sensu Bouché 1977)—epigeic (surface living), endogeic (shallow burrowing) and anecic (deep burrowing) species—which separates species according to their life history strategies and behaviour. The latter has an impact on the nutritional quality of the food resources consumed which in turn strongly affects species egestion rates and thus bioturbation. Ant bioturbation and its effect on the environment are also largely dependent on the respective ant species and their nestbuilding characteristics (Frouz and Jilková 2008). Although most ants live in below-ground galleries and chambers (Dostál and others 2005), a small group of ants—the majority of which are in the genus Formica—build most of their nest aboveground using needles, twigs, resin and bark collected from the surrounding forest floor (Laakso and Setälä 1998; Jurgensen and others 2008). Nest density, that is, the number of ant nests per area, has been suggested as the most important factor explaining variation in soil turnover by ants between different habitats (Lobry de Bruyn and Conacher 1994). The goal of the present study was to assess and compare environmental engineering activities of ants and (...truncated)