Contrasting protist communities (Cercozoa: Rhizaria) in pristine and earthworm-invaded North American deciduous forests

Earthworms are considered ecosystem engineers due to their fundamental impact on soil structure, soil processes and on other soil biota. An invasion of non-native earthworm species has altered soils of North America since European settlement, a process currently expanding into still earthworm-free forest ecosystems due to continuous spread and increasing soil temperatures owing to climate change. Although earthworms are known to modify soil microbial diversity and activity, it is as yet unclear how eukaryote consumers in soil microbial food webs will be affected. Here, we investigated how earthworm invasion affects the diversity of Cercozoa, one of the most dominant protist taxa in soils. Although the composition of the native cercozoan community clearly shifted in response to earthworm invasion, the communities of the different forests showed distinct responses. We identified 39 operational taxonomic units (OTUs) exclusively indicating earthworm invasion, hinting at an earthworm-associated community of Cercozoa. In particular, Woronina pythii, a hyper-parasite of plant-parasitic Oomycota in American forests, increased strongly in the presence of invasive earthworms, indicating an influence of invasive earthworms on oomycete communities and potentially on forest health, which requires further research.

Aboveground impacts of a belowground invader: how invasive earthworms alter aboveground arthropod communities in a northern North American forest

Declining arthropod communities have recently gained a lot of attention with climate and land-use change among the most-frequently discussed drivers. Here, we focus on a seemingly underrepresented driver of arthropod-community decline: biological invasions. For ∼12,000 years, earthworms have been absent from wide parts of northern North America, but they have been re-introduced with dramatic consequences. Most studies investigating earthworm-invasion impacts focus on the belowground world, resulting in limited knowledge on aboveground-community changes. We present observational data on earthworm, plant, and aboveground-arthropod communities in 60 plots, distributed across areas with increasing invasion status (low, medium, high) in a Canadian forest. We analyzed how earthworm-invasion status and biomass impact aboveground arthropod community abundance, biomass, and species richness, and how earthworm impacts cascade across trophic levels. We sampled ∼13,000 arthropods, dominated by Hemiptera, Diptera, Araneae, Thysanoptera, and Hymenoptera. Total arthropod abundance, biomass, and species richness declined significantly from areas of low to those with high invasion status with reductions of 61, 27, and 18%, respectively. Structural Equation Models unraveled that earthworms directly and indirectly impact arthropods across trophic levels. We show that earthworm invasion can alter aboveground multitrophic arthropod communities and suggest that belowground invasions can be important drivers of aboveground-arthropod decline.

The Long-Term Effects of Invasive Earthworms on Plant Community Composition and Diversity in a Hardwood Forest in Northern Minnesota

Non-native European earthworms are invading hardwood forests in the Chippewa National Forest, MN. We applied a model using historic O-horizon soil thickness to classify 41 hardwood sites in the Chippewa National Forest as “long-term wormed” (wormed during the 1989-1996 and 2017 sampling period), “short-term wormed” (unwormed during the 1989-1996 sampling period and wormed in the 2017 sampling period), or “unwormed” (unwormed during the 1989-1996 and 2017 sampling period). We found that graminoids, especially Carex pensylvanica , had the greatest abundance in sites that had been wormed for over two decades. The families with the greatest negative change in percent cover after over two decades of earthworm invasion were Asteraceae, Violaceae, and Sapindaceae (specifically Acer species). Across all diversity metrics measured, long-term wormed sites had the lowest understory plant species diversity, short-term wormed sites had intermediate diversity, and unwormed sites exhibited the highest diversity. Long-term wormed sites had the lowest species richness at both small and large scales (1 to 1024m 2 ). The greatest within-group compositional dissimilarity occurred at sites that had been wormed for over two decades, indicating that compositional changes in plant communities are still occurring more than two decades since invasion. Sites that had been wormed for over two decades did not appear to have reached a compositionally similar end-state “wormed” community type. If results of this study are indicative of future trends as earthworms become established, it can be expected that understory diversity will decrease as hardwood forest stands become wormed over time.

Oil palm and rubber expansion facilitates earthworm invasion in Indonesia

Deforestation, plantation expansion and other human activities in tropical ecosystems are often associated with biological invasions. These processes have been studied for above-ground organisms, but associated changes below the ground have received little attention. We surveyed rainforest and plantation systems in Jambi province, Sumatra, Indonesia, to investigate effects of land-use change on the diversity and abundance of earthworms—a major group of soil-ecosystem engineers that often is associated with human activities. Density and biomass of earthworms increased 4—30-fold in oil palm and rubber monoculture plantations compared to rainforest. Despite much higher abundance, earthworm communities in plantations were less diverse and dominated by the peregrine morphospecies Pontoscolex corethrurus, often recorded as invasive. Considering the high deforestation rate in Indonesia, invasive earthworms are expected to dominate soil communities across the region in the near future, in lieu of native soil biodiversity. Ecologically-friendly management approaches, increasing structural habitat complexity and plant diversity, may foster beneficial effects of invasive earthworms on plant growth while mitigating negative effects on below-ground biodiversity and the functioning of the native soil animal community.

Do Invasive Earthworms Affect the Functional Traits of Native Plants?

As ecosystem engineers, invasive earthworms are one of the main drivers of plant community changes in North American forests previously devoid of earthworms. One explanation for these community changes is the effects of earthworms on the reproduction, recruitment, and development of plant species. However, few studies have investigated functional trait responses of native plants to earthworm invasion to explain the mechanisms underlying community changes. In a mesocosm (Ecotron) experiment, we set up a plant community composed of two herb and two grass species commonly found in northern North American forests under two earthworm treatments (presence vs. absence). We measured earthworm effects on above- and belowground plant biomass and functional traits after 3 months of experiment. Our results showed that earthworm presence did not significantly affect plant community biomass and cover. Furthermore, only four out of the fifteen above- and belowground traits measured were affected by earthworm presence. While some traits, such as the production of ramets, the carbon and nitrogen content of leaves, responded similarly between and within functional groups in the presence or absence of earthworms, we observed opposite responses for other traits, such as height, specific leaf area, and root length within some functional groups in the presence of earthworms. Plant trait responses were thus species-specific, although the two grass species showed a more pronounced response to earthworm presence with changes in their leaf traits than herb species. Overall, earthworms affected some functional traits related to resource uptake abilities of plants and thus could change plant competition outcomes over time, which could be an explanation of plant community changes observed in invaded ecosystems.

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.

How Introduced Earthworms Alter Ecosystems

We all know earthworms as important friends in our garden: they help plants to grow better by providing nutrients, water, and air in the soil. However, in some cases, earthworms have more negative effects. This is because other organisms need to be used to the activities of earthworms to benefit from their presence. Some regions of the world have developed without earthworms for over thousands of years. For example, in northern North America, earthworms have been absent for more than 10,000 years and have only been re-introduced over the past ~400 years. In many cases, introduced earthworms find a perfect environment, because no other organisms have been able to use the resources that these earthworms now consume. As so-called ecosystem engineers, earthworms dramatically alter many ecosystem characteristics. In this article, we summarize the known consequences of earthworm invasion, report on how scientists study these, and highlight remaining knowledge gaps that you might help solving should you decide to become an ecologist.