Arctic worming: Human-facilitated earthworm invasion transforms soil organic matter budgets and pools in Fennoscandian forests

Abstract

Earth’s high latitude ecosystems are already under dire threat from climate warming, permafrost thaw, and intensifying natural resource exploitation. In addition to these ongoing concerns, accelerating urbanization, agricultural expansion, and greater opportunities for recreation in high-latitude regions are likely to introduce a less conspicuous but potentially potent threat: non-native geoengineeing earthworms. Earthworms were eradicated from northern N. America (including Minnesota) during the last glaciation, and it is now established that humans are (re-) introducing exotic earthworm species into these forests with dramatic consequences on soil and ecosystem functioning. However, their invasiveness and capacity to modify high-latitude boreal and arctic forests like those in Fennoscandia remains largely unknown. Here I explore two inter-related hypotheses concerning earthworms and soils in Fennoscandian forests: H1) despite their different human history and proximity to the native range of Lumbricidae earthworms (Southern and Central Europe), I predicted that Pleistocene glaciations also extirpated earthworms from Fennoscandia, suggesting that European earthworms (if present) are also non-native and invasive in these landscapes; and H2) if introduced by humans, the invasive earthworms transform Fennoscandian forest soil morphologies and soil organic matter (SOM) dynamics by removing thick organic layers at the forest floor and forming A-horizon (mineral topsoil) in their wake. To address H1, I tested a series of sub-hypotheses stating that: 1) earthworms did not colonize the Fennoscandian landscape via dispersal by brackish seawater, nor were they introduced by early indigenous peoples (Sami) who followed the retreating glaciers into northern Fennoscandia; and 2) earthworms are spreading into Fennoscandian forests from ‘worm point sources’ created by modern human-mediated dispersal vectors such as farming, fishing, gardening, and logging (among others). Although I could not dispel the possibility that small epigeic-type earthworms may have entered the Fennoscandian landscape considerably earlier via water-mediated dispersal and/or by ‘hitch-hiking’ along with Sami settlers, I found that more impactful ‘geoengineering’ species are only present in arctic landscapes associated with more modern (i.e. last two centuries) human disturbance (supporting H1) and are radiating outward from these anthropogenic point sources into virgin arctic and boreal forests. Furthermore, in line with H2, expansion of these geoengineers into adjacent forests consistently induced changes to forest soil morphologies and nutrient cycling regimes, including rapid reduction of the SOM pool in organic horizons and re-allocation of this SOM into mineral horizons: wherein it is sorbed onto mineral surfaces and/or occluded within aggregates. This belowground transformation likely has significant aboveground consequences as well as implications for the long-term carbon balance of boreal and arctic ecosystems, which store more than half (~ 53%) of earth’s soil carbon. Furthermore, based on results from N. America, this ‘unseen’ invasion may also have cascading effects on fungal and microbial associations, plant communities, and overall ecosystem functioning. Considering that the arctic is already being disproportionately affected by climate change and that human activities in these regions are likely to accelerate as these regions warm, additional research assessing the ecological impacts of arctic worming is urgently needed.