Elsevier

Geoderma

Volume 404, 15 December 2021, 115262
Geoderma

Invasive earthworms affect soil morphological features and carbon stocks in boreal forests

https://doi.org/10.1016/j.geoderma.2021.115262Get rights and content

Highlights

  • Earthworm impacts on morphological features varied among studied soil types.

  • Development of a carbon-rich top mineral horizon and vermimull humus forms.

  • Forest floor carbon stocks decreased for Luvisols and Brunisols.

  • Surface mineral soil carbon stocks increased for Brunisols only.

  • Minor effects on carbon stocks for Podzols.

Abstract

Non-native earthworms have been invading North America since European settlement. Compared to temperate forests, their presence in the boreal forest is much more recent and thus remains understudied, despite the potential threat they represent for soil carbon (C) stocks. Here we compared earthworm-invaded and earthworm-free zones in soil types representative of the boreal forest, including Luvisols, Podzols, and Brunisols (Cambisols). We observed that the forest floor (surface organic layer, or LFH) decreased in thickness after invasion in most cases and developed into a Vermimull, with the loss of the most humified layer (humic or H horizon). Simultaneously, the surface mineral horizon was reworked by earthworms into a novel Ahu horizon, characterized by higher organic matter and enriched in earthworm casts. Forest floor C stocks decreased by 94% and 59% for Luvisols and Brunisols respectively, while those of Podzols remained apparently unaffected. Mineral soil C stocks in Brunisols increased after invasion, while no changes were observed in Luvisols and Podzols. Our results demonstrated the substantial impact that invading earthworms are having on soil morphological features and C stocks in boreal forests. Effects were similar to what has been reported for temperate forests, although the degree of impact depended on soil type. While C stocks were less affected in the mineral soil compared to the forest floor, the development of a novel surface horizon reworked by earthworms could alter microbial dynamics and impact mineral C persistence. Further research is needed to quantify long-term implications of earthworm presence for boreal soil C stocks.

Introduction

The Wisconsin glaciation, which ended about 12,000 years BP, completely extirpated native earthworms from most of North America (Hendrix, 2006). As a result, northern ecosystems, including their soils, vegetation and carbon (C) pools, have developed in the absence of earthworms (Addison, 2009). Since European settlement, exotic earthworms have been introduced and have been invading North America (Scheu and McLean, 1993). Despite limiting factors such as long cold winters and acidic soil conditions, earthworms have been observed in boreal forests (Addison, 2009), where the rapid growth of recreational and industrial activities is facilitating their invasion (Cameron et al., 2007). The boreal forest is the largest terrestrial C reservoir on Earth, and any change in its C dynamics can potentially have major implications for global C pools (Frelich et al., 2019, Kurz et al., 2013). With an expected 4–5 °C increase in temperature by the end of the 21st century (Boulanger et al., 2017), a greater part of the boreal forest will become hospitable to earthworms (Booysen et al., 2018). Moreover, liming has been commonly used to restore sugar maple forests in Eastern Canada, alleviating the acidic conditions found in those soils (Moore et al., 2013). Earthworms have already been observed in boreal forests of Alaska (Saltmarsh et al., 2016), Western Canada (Cameron et al., 2007) and Eastern Canada (Moore and Reynolds, 2003). The concerns about this ongoing invasion are not limited to North America, as the presence of European geoengineering (endogeic and anecic, see below) earthworm species have been recorded in various parts of the Arctic biome such as Russia and Fennoscandia, where they are considered exotic and invasive (Blume-Werry et al., 2020, Wackett et al., 2018).

Although mostly seen as beneficial in agricultural soils and for post-mining reclamation, earthworms may not be desirable in forest soils since they mainly feed on organic matter (OM) found in the forest floor or mineral soil (Blouin et al., 2013, Frouz et al., 2009). Some exotic earthworm species can fundamentally change soil properties in a few years for temperate forests, even more so in soils devoid of endemic species by occupying a vacant ecological niche (Hendrix and Bohlen, 2002, Langmaid, 1964). In temperate forests of North America, earthworms have been shown to substantially increase C losses from the forest floor, which even disappeared in extreme cases, thereby decreasing overall soil C stocks and increasing CO2 emissions, at least transitionally (Blouin et al., 2013, Bohlen et al., 2004a, Hale et al., 2005b). However, some of the C lost from the forest floor is transferred to the upper mineral horizon by bioturbation and is potentially stabilized in aggregates formed by earthworms (Bossuyt et al., 2004). The loss of forest floor C following earthworm invasion is probably also occurring in boreal forests, albeit at a slower pace, but there are insufficient data and understanding of net effects (Kurz et al., 2013). When compared to agroecosystems, earthworm effects on net CO2 emissions in natural ecosystems such as temperate forests are smaller because of larger C pools, as was reviewed by Lubbers et al. (2013). Boreal forests are characterized by lower decomposition rates and thicker forest floors compared to temperate forests (DeLuca and Boisvenue, 2012). For these reasons, the conclusion of Lubbers et al. (2013) for temperate forests may not hold true for the boreal biome. Although a few studies showed that litter decomposition rate was increased in the presence of earthworms in some boreal forest soils (Laganière et al., 2010), it is still unclear whether these organisms can affect the vertical distribution of C and the overall C balance in these soils.

It is challenging to study long term effects of earthworms on soil properties (Clements et al., 1991). Under laboratory conditions, studies span from 21 days to 2.4 years (Bossuyt et al., 2005, Frouz et al., 2014, Hale et al., 2008). Under field conditions, studies also typically focus on quantifying short term effects of earthworms over a maximum of 3 years (Bohlen et al., 2004a, Fisk et al., 2004, Groffman et al., 2004). As an alternative, simultaneously studying earthworm-invaded and earthworm-free zones in otherwise similar ecosystems can be considered as a long term experiment, where non-invaded zones act as control sites (Blouin et al., 2013, Lubbers et al., 2013). This ‘space-for-time’ approach is commonly used in community ecology (Damgaard, 2019, Sax et al., 2005, Thomaz et al., 2012) and has been applied in southern Alberta to compare soil chemistry and microbial activity along a transect corresponding to different invasion stages (Eisenhauer et al., 2007). Although for many sites it is nearly impossible to determine when the invasion started, historical knowledge of road construction, fishing activities and/or agriculture should give valuable hints for potential invasion vectors (Cameron et al., 2007).

Most invasions involve multiple earthworm species, with different ecological behaviours. Bouché (1977) defined three categories based on their feeding behaviour and habitat: epigeic, endogeic and anecic earthworms. By feeding on plant litter, epigeic and anecic species accelerate litter disappearance from the soil surface, the latter having the strongest effect because of higher body mass (Hale et al., 2005a, Huang et al., 2020). As endogeic species inhabit the mineral soil and do not feed on plant litter, they have little impact on the litter layer but have the strongest effect on the structure and aggregation of the underlying mineral horizons (Bossuyt et al., 2006, Knowles et al., 2016). The association of at least two functional groups can yield to a greater cumulative effect on litter decomposition and soil organic carbon (SOC) stabilization and/or persistence (Huang et al., 2020). In temperate forests, Hale et al. (2005a) described a succession of earthworm species along the leading edge of invasion, which was defined as the point where forest floor thickness had decreased to zero. Epigeic species were observed 20 m or more in advance of the leading edge, endogeic species were found right behind the leading edge, and anecic species thrived 20–30 m behind. This gradient found at the stand scale by Hale et al. (2005a) was also described along a 125 km north–south transect in temperate forests of south-central Ontario by Choi et al. (2017), with the most northern site being the least invaded. At a global scale, Phillips et al. (2019) showed that earthworm diversity increases with latitude, and is mostly correlated with climate variables. But in these invaded regions, the reported earthworm density is higher than for most of the globe, as those exotic species access a large, otherwise unused pool of resources.

Understanding the factors and processes of soil formation is a prerequisite for the description of soil horizons and morphological features (Jenny, 1941). In addition, the use of a soil classification system – such as the Canadian System for Soil Classification in the case of the present study – is fundamental to organize knowledge in a defined frame, allowing for comparisons among soil types (Soil Classification Working Group, 1998). In temperate forests, effects of invasive earthworms on soil morphology have been described in Podzols (Langmaid, 1964, Nielsen and Hole, 1964) and Luvisols (Alban and Berry, 1994, Eisenhauer et al., 2007). In all cases, authors described development of an organic-rich A horizon mainly comprised of earthworm casts. In boreal forests, the main soil types potentially hospitable to earthworms are Podzols, Brunisols (corresponding to Cambisols in the World Reference Base classification by FAO (2014)) and Luvisols (DeLuca and Boisvenue, 2012). Podzolic and Luvisolic soils, respectively covering 14.3 and 8.8% of Canada’s land area, develop on drastically different parent materials: acidic coarse-textured for the former and calcareous fine-textured for the latter (Lavkulich and Arocena, 2011, Maynard et al., 2014, Sanborn et al., 2011). As for Brunisolic soils, covering about 14% of land surface in Canada, they typically co-exist with both Podzolic and Luvisolic soils but lack the same level of horizon development (Smith et al., 2011).

This study aimed to describe soil morphological features and estimate organic C stocks for the forest floor and top mineral soil in earthworm-invaded and earthworm-free zones for contrasting soil types and boreal ecozones present within the Canadian boreal forest: Luvisolic soils typical of the Boreal Plains in Western Canada and Podzolic and Brunisolic soils found in the Boreal Shield of Eastern Canada. We hypothesized that effects of invasive earthworms in the boreal forest would be similar to those in temperate forests, with zones invaded by earthworms associated with thinner forest floors and cast-rich uppermost mineral soils, and that more pronounced changes would be evident in the presence of at least two earthworm functional groups. In terms of C stocks, we expected a decrease in the forest floor and an increase in the mineral soil resulting from a transfer of organic matter from the forest floor to the mineral soil after earthworm invasion. Furthermore, we expected to see a variable degree of earthworm effects related to soil type, considering the fundamental differences between the three studied soil types. Luvisols under trembling aspen (Populus tremuloides Michx.) canopy would show the largest changes after earthworm invasion, while acidic Podzols would be the least affected. Brunisols would be intermediate as they developed on acidic parent material but under deciduous canopy.

Section snippets

Study sites

The study was conducted in the Boreal Plains and the Boreal Shield ecozones of Canada, respectively in Alberta and Quebec (Table 1; Fig. 1). The different sites were selected based on existing research data as well as the likelihood to find both earthworm-invaded and earthworm-free zones within the same site or in similar environmental conditions. The selected sites represent some of the most common scenarios in the boreal: Podzols (WRB: Podzols; USDA: Spodosols) under coniferous canopy,

Earthworm biomass and functional groups

The epigeic species Dendrobaena octaedra has been shown to be the most abundant and first invader in North American forests (Cameron et al., 2007, Hale et al., 2005a). Our results match this observation as the species was found in all sites except Grands Jardins, and was at its highest density at EMEND and Wolf Lake, considered to be the earlier stages of invasion (Table 3). However, the density of D. octaedra (432 ind.m−2; Supplementary Table 3) observed at EMEND was drastically lower than

Conclusion

This study highlights changes occurring in boreal soils following earthworm invasion. Luvisols, Brunisols and Podzols invaded by at least two functional groups of earthworms developed a similar dark A horizon enriched in TOC and earthworm casts associated with a Vermimull. As hypothesized, we observed changes linked to earthworm invasion similar to what has been observed in temperate forests, namely a decrease in forest floor thickness and the development of a reworked surface mineral horizon.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

The Natural Sciences and Engineering Research Council of Canada (NSERC) provided overall financial support through a Discovery Grant (RGPIN-2014-04693) to Sylvie Quideau. This work was also funded by the Forest and Climate Change Program of the Canadian Forest Service, an Alberta Conservation Association grant for biodiversity and a University of Alberta Northern Research Award.

We would like to thank Jean-David Moore and Rock Ouimet from Ministère des Forêts, de la Faune et des Parcs (MFFP) du

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