Ant and Earthworm Bioturbation in Cold-Temperate Ecosystems
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Ecosystems https://doi.org/10.1007/s10021-018-0317-2 Ó 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 1Department 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 soil pH (pH 5–7.2). Estimates of ant bioturbation at the most important organisms for bioturbation. Little is same sites were based on nest abundance, size and known about how these groups contribute to biotur- residence time. Mean ant bioturbation varied between bation in different environments and to what extent 0.2and1Mgdrysoilha-1 y-1, but individual plots overall bioturbation depends on their diversity. We hadupto2.4Mgdrysoilha-1 y-1. In soils with pH developed a formula that allows quantification of an- higher than 5, the relative contribution of ants to total nual earthworm bioturbation, thereby taking differ- bioturbation was only 1–5%. Ant bioturbation was ences between earthworm ecotypes into account. higher than earthworm bioturbation only in some With this formula, we calculated earthworm biotur- forest soils with pH 3.9–4.4. Thus, earthworms appear bation at three sites, each with vegetation types typi- to be the dominant cause of bioturbation in most types cally found in Northern Europe. Earthworm of terrestrial ecosystems in the cold-temperate areas of bioturbation was low (1 Mg dry soil ha-1 y-1)in Europe and when information on local earthworm Scots pine and Norway spruce forests with acidic soil communities and monthly soil temperatures is avail- (pH 3.9–4.4) and high (between 15 and 34 Mg dry able, bioturbation can be quantified using the pre- soil ha-1 y-1) in broadleaf forests, grasslands, alder sented ‘earthworm bioturbation formula’. carr and spruce forests on calcareous soil. Burrowing (endogeic and anecic) earthworms accounted for most Key words: Aporrectodea caliginosa; egestion; of the earthworm bioturbation, and these worms had Lumbricidae; Myrmica; nest density; pH; soil turn- the highest population densities at moderate-to-high over; temperature dependence. HIGHLIGHTS We present a method to calculate earthworm and ant bioturbation Earthworm and ant bioturbation depended on the species composition Received 20 January 2018; accepted 29 September 2018 Earthworm bioturbation was larger than ant bioturbation at soil pH > 4.3 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 biotur- INTRODUCTION bation, L. Lenoir estimated ant bioturbation and A.R. Taylor contributed with new methods for the underlying baseline research. B. Vegerfors In cold-temperate regions, earthworms and ants analysed the data. A.R. Taylor and T. Persson wrote the paper and L. are the most important ‘ecosystem engineers’ (La- Lenoir commented on the manuscript. ´ *Corresponding author; e-mail: [email protected] velle and others 1997; Jones and Gutierrez 2007) A.R. Taylor and others that significantly affect the structure and function anecic (deep burrowing) species—which separates of the ecosystems they inhabit (Folgarait 1998;Le species according to their life history strategies and Bayon and others 2017) via their bioturbation behaviour. The latter has an impact on the nutri- activity. Bioturbation, that is, the biological tional quality of the food resources consumed reworking of soils and sediments (Meysman and which in turn strongly affects species egestion rates others 2006), takes place when earthworms and and thus bioturbation. Ant bioturbation and its ants transport soil and organic matter from one effect on the environment are also largely depen- place to the other. Earthworms translocate and mix dent on the respective ant species and their nest- soil when feeding/egesting, while ants bioturbate building characteristics (Frouz and Jilkova´ 2008). via their nest-building activities. Although most ants live in below-ground galleries Earthworm and ant bioturbation contributes to a and chambers (Dosta´l and others 2005), a small range of ecosystem services, like decomposition, group of ants—the majority of which are in the nutrient cycling, soil structuring/formation and the genus Formica—build most of their nest above- regulation of water and gas exchange (Lavelle and ground using needles, twigs, resin and bark col- others 2006; Wall and others 2012). However, the lected from the surrounding forest floor (Laakso impact of bioturbation on individual services and and Seta¨la¨ 1998; Jurgensen and others 2008). Nest the temporal and spatial dynamics of their biotur- density, that is, the number of ant nests per area, bation activity differ significantly between both has been suggested as the most important factor groups (Folgarait 1998; Wilkinson and others 2009; explaining variation in soil turnover by ants be- Blouin and others 2013; Turbe´ and others 2010). tween different habitats (Lobry de Bruyn and This is, on the one hand, due to earthworms and Conacher 1994). ants having different spatial aggregation patterns, The goal of the present study was to assess and dispersal distances and life spans. On the other compare environmental engineering activities of hand, the longevity and physical and chemical ants and earthworms—using bioturbation as a properties of the biotic structures created by both proxy—in a range of vegetation types shared by groups above-ground (for example, mounds, nests, both groups. We used an indirect approach to place casts, middens) and below-ground (for example, earthworm and ant bioturbation in a quantitative galleries, chambers, burrows, casts) are distinctly framework via estimating the amount of soil and different (Hedde and others 2005). Earthworm OM moved over time by each group. We see this as casts and burrows differ from ant artefacts by the a first step towards linking empirical data on origin of their organic matter (OM) and the gut abundance and composition of soil ecosystem transit experienced before structure building. Thus, engineer communities with their function in a the resource quality for microorganisms in these specific environment and their impact on ecosys- biostructures differs depending on engineer forag- tem services (Meysman and others 2006). For ing specificity leading to differences in the OM earthworms, we developed a formula that allows humification rates (Hedde and others 2005). There quantifying annual earthworm bioturbation; it is are only few studies that directly link the func- based, amongst other parameters, on the egestion tioning of biological soil components like that of rates of the most common European earthworm soil ecosystem engineers to ecosystem services species. For ants, calculations of annual bioturba- (Adhikari and Hartemink 2016) because it is tion are based on ant nest density, volume and inherently difficulty to measure their impact on a residence time. For both groups, we distinguish particular ecosystem service under field conditions between the contributions of different ant species (Barrios 2007). and earthworm ecotypes. To assess the full impact of environmental engi- The present study focusses on the bioturbation of neering by earthworms and ants in cold-temperate ecosystem engineers in grasslands and cold-tem- regions, it is important to consider the cumulative perate forests in Sweden. However, the results will effects of bioturbation by both groups and to relate be significant for a much wider region because the the rate of material transport to their community vegetation types investigated are typically found all characteristics, that is, species composition and over Scandinavia and even Northern Europe. Par- abundance, in the particular environment investi- ticularly in Finland and Sweden, forests account for gated (Wilkinson and others 2009). Differences in around 70% of the land area. In these Scandinavian the bioturbation activity of earthworm species are forests and woodlands, especially those dominated reflected in the common division into three eco- by pine and oak, ants are recognized as important logical types (sensu Bouche´ 1977)—epigeic (sur- ecosystem engineers (Douwes and others 2012) face living), endogeic (shallow burrowing) and which may to a certain extent be due to their visual Ant and Earthworm Bioturbation presence, for example the large, visible ant mounds SKB, Swedish Nuclear Fuel and Waste Manage- often constructed by ants of the genus Formica. ment Company, which needed soil biological data Earthworms are assumed to be of lesser importance, on these two sites for selection of a repository of particularly in pine- and spruce-dominated forests, radioactive waste from nuclear plants. The third because, in contrast to ants, they are negatively af- site consisted of a number of sub-sites in the Upp- fected by low soil pH (Lofs-Holmin 1983; Edwards sala region, Spikbole, Andersby a¨ngsbackar, Fex- and Bohlen 1996), which is very common in Scan- boda and O¨ sterbybruk (Table 1). The climate at all dinavian coniferous forests. Therefore, traditionally sites is characterized by semi-arid conditions during far more research focusses on the functional role of the growing season (daily mean > +5°C) that earthworms in agricultural fields and grasslands (for extends over 180 days (May–September) at Fors- example, Scheu 2003)