A review of exotic earthworm observations in the Canadian boreal forest and taiga zones

In the last decades, concerns have emerged that boreal forests could convert from a carbon sink to a carbon source, thus accentuating climate change. Although forest fire is generally mentioned as the main factor that could cause the boreal forest to transition to a carbon source, other factors, such as exotic earthworm activity, could also play an important role. Invasive exotic earthworms can also affect nutrient cycling, biodiversity and forest dynamics. In this context, a better knowledge of the distribution of exotic earthworms can help understand the likely changes in the ecosystems that they have colonized. Here we report the results of an exhaustive literature review of the presence of exotic earthworms in the Canadian boreal forest and taiga zones. We identified 230 sectors containing 14 earthworm species (11 exotic, 2 native and 1 putative native) in 6 provinces and 3 territories across Canada’s boreal forest and taiga zone. We also report 23 as-yet unpublished observations from the province of Quebec. We note the presence of earthworms in environments (acid soils, harsh climate) that were historically considered inadequate for their survival. This suggests that the portion of Canada’s boreal forests suitable for their presence or colonization is larger than what was previously believed. This study represents the first compilation of exotic earthworm presence in this large northern area. Factors that could affect their distribution and potential effects on boreal ecosystems are also discussed. Globally, several earthworm species seem to be overcoming the previously assumed limitation by temperature and pH.

Invasive Earthworms Alter Forest Soil Microbiomes and Nitrogen Cycling

Northern hardwood forests in formerly glaciated areas had been free of earthworms until exotic European earthworms were introduced by human activities. The invasion of exotic earthworms is known to dramatically alter soil physical, geochemical, and biological properties, but its impacts on soil microbiomes are still unclear. Here we show that the invasive earthworms alter soil microbiomes and ecosystem functioning, especially for nitrogen cycling. We collected soil samples at different depths from three sites across an active earthworm invasion chronosequence in a hardwood forest in Minnesota, USA. We analyzed the structures and the functional potentials of the soil microbiomes by using amplicon sequencing, high-throughput nitrogen cycle gene quantification (NiCE chip), and shotgun metagenomics. Both the levels of earthworm invasion and soil depth influenced the microbiome structures. In the most recently and minimally invaded soils, Nitrososphaera and Nitrospira as well as the genes related to nitrification were more abundant than in the heavily invaded soils. By contrast, genes related to denitrification and nitrogen fixation were more abundant in the heavily invaded than the minimally invaded soils. Our results suggest that the N cycling in forest soils is mostly nitrification driven before earthworm invasion, whereas it becomes denitrification driven after earthworm invasion.

Molecular evidence reveals introduced populations of Eiseniella tetraedra (Savigny, 1826) (Annelida, Lumbricidae) with European origins from protected freshwater ecosystems of the southern Alborz Mountains

The presence of exotic earthworms has recently become a major concern and drawn significant attention to their potential effects on ecosystems and native invertebrate fauna. Although the occurrence of invasive annelids has been well recorded, their settlement in Iran is poorly documented. To investigate the biodiversity of aquatic Oligochaeta and to assess the presence of possible exotic species, DNA barcoding using the mitochondrial cytochrome c oxidase subunit 1 (COI) gene was conducted in two major protected rivers (Jajroud, Karaj) of the southern Alborz Mountains. As a result, new lineages of Tubifex, Haplotaxis and Lumbriculus were identified from Iran. Moreover, a semiaquatic lumbricid species, Eiseniella tetraedra, was unexpectedly found to be the most abundant species. The analyses showed the presence of six divergent lineages of E. tetraedra occurring in individual rivers. The presence of identical haplotypes shared between European, North American, Australian and Iranian localities, the sympatric accumulation of several distinct intraspecific lineages in the same rivers and the lack of a phylogeographic pattern reinforce the hypothesis of a possible inadvertent anthropogenic introduction. The relative abundance of lineages indicates a significant decline in the abundance of native oligochaetes, which may be linked to the preponderance of recently introduced European populations of E. tetraedra, probably mediated through human activities.

Ecosystem responses to exotic earthworm invasion in northern North American forests

Earth is experiencing a substantial loss of biodiversity at the global scale, while both species gains and losses are occurring at local and regional scales. The influence of these nonrandom changes in species distributions could profoundly affect the functioning of ecosystems and the essential services that they provide. However, few experimental tests have been conducted examining the influence of species invasions on ecosystem functioning. Even fewer have been conducted using invasive ecosystem engineers, which can have disproportionately strong influence on native ecosystems relative to their own biomass. The invasion of exotic earthworms is a prime example of an ecosystem engineer that is influencing many ecosystems around the world. In particular, European earthworm invasions of northern North American forests cause simultaneous species gains and losses with significant consequences for essential ecosystem processes like nutrient cycling and crucial services to humanity like soil erosion control and carbon sequestration. Exotic earthworms are expected to select for specific traits in communities of soil microorganisms (fast-growing bacteria species), soil fauna (promoting the bacterial energy channel), and plants (graminoids) through direct and indirect effects. This will accelerate some ecosystem processes and decelerate others, fundamentally altering how invaded forests function. This project aims to investigate ecosystem responses of northern North American forests to earthworm invasion. Using a novel, synthetic combination of field observations, field experiments, lab experiments, and meta-analyses, the proposed work will be the first systematic examination of earthworm effects on (1) plant communities and (2) soil food webs and processes. Further, (3) effects of a changing climate (warming and reduced summer precipitation) on earthworm performance will be investigated in a unique field experiment designed to predict the future spread and consequences of earthworm invasion in North America. By assessing the soil chemical and physical properties as well as the taxonomic (e.g., by the latest next-generation sequencing techniques) and functional composition of plant, soil microbial and animal communities and the processes they drive in four forests, work packages I-III take complementary approaches to derive a comprehensive and generalizable picture of how ecosystems change in response to earthworm invasion. Finally, in work package IV, meta-analyses will be used to integrate the information from work packages I-III and existing literature to investigate if earthworms cause invasion waves, invasion meltdowns, habitat homogenization, and ecosystem state shifts. Global data will be synthesized to test if the relative magnitude of effects differs from place to place depending on the functional dissimilarity between native soil fauna and exotic earthworms. Moving from local to global scale, the present proposal examines the influence of earthworm invasions on biodiversity–ecosystem functioning relationships from an aboveground–belowground perspective in natural settings. This approach is highly innovative as it utilizes the invasion by exotic earthworms as an exciting model system that links invasion biology with trait-based community ecology, global change research, and ecosystem ecology, pioneering a new generation of biodiversity–ecosystem functioning research.