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ECOSYSTEM RESPONSES TO EXOTIC EARTHWORM INVASION IN NORTHERN NORTH AMERICAN FORESTS

Periodic Reporting for period 4 - ECOWORM (ECOSYSTEM RESPONSES TO EXOTIC EARTHWORM INVASION IN NORTHERN NORTH AMERICAN FORESTS)

Reporting period: 2020-09-01 to 2021-02-28

Earth is experiencing substantial biodiversity losses at the global scale, while both species gains and losses are occurring locally and regionally. Changes in the biodiversity and composition of ecological communities could profoundly influence ecosystem functions and services. However, few experimental tests have examined the influences of invasive ecosystem engineers, which can have disproportionally strong impacts on native ecosystems. Invasive earthworms are a prime example of ecosystem engineers that influence many ecosystems around the world. In particular, European earthworms invading northern North American forests may cause simultaneous species gains and losses with significant consequences for essential ecosystem processes like nutrient cycling and crucial services like carbon sequestration. Moreover, there is limited knowledge of the global distribution of soil biodiversity, including native and exotic earthworms, their drivers and threats, as well as ecosystem consequences of biodiversity change. Using a synthetic combination of field observations, field experiments, lab experiments, macro-ecological analyses, and meta-analyses, the present project is the first systematic examination of earthworm effects on relationships between plant communities, soil communities, and ecosystem processes. Further, effects of a changing climate on the spread and consequences of earthworm invasion as well as the global distribution of soil biodiversity, including earthworms, were investigated. Results of this research project highlight the pervasive effects of soil biodiversity (particularly invasive earthworms) on relationships between plant communities, soil communities, and ecosystem processes. Invasive earthworms cause substantial reductions of the diversity of soil animals, facilitate the invasion of exotic plants at the expense of native plants, and alter soil physical and chemical properties as well as nutrient cycling. Moreover, it revealed the global environmental drivers of earthworm diversity as well as other soil taxa, highlighting the significant role of climate (precipitation and temperature) determining the distribution of soil organisms at the local to global scale. These findings contributed to the development of a global soil biodiversity monitoring program. The combination of data on (soil) biodiversity and ecosystem functions showed that anthropogenic changes in environmental conditions that affect biodiversity will alter the services provided by ecosystems.
After staffing all positions, kick-off meetings with collaborators were organized to finalize the planning of the field observation campaign and the field experiment. In WP1 and WP2, plant, soil microbial, and animal communities were sampled in four different forests in the USA and Canada according to the proposed plan. The field sampling design had to be slightly modified by sampling areas with and without earthworms as other invasion states were impossible to standardize across forests. Four major field campaigns were performed (one each in 2016, 2017, 2018, and 2019). The planned field experiment was successfully established in August of 2017, sampled in 2018 and 2019, and dismantled in 2020. Moreover, in WP2 we studied phytometers (two aspen species) for herbivory rates and leaf chemical analyses. A complementary mesocosm experiment was performed to explore invasive earthworm effects on tree leaf chemistry under controlled environmental conditions. We performed the planned samplings in the B4WarmED experiment and already published the respective papers (WP3). In WP4, we conducted several workshops for synthesis and meta-analysis work on (1) invasive earthworm effects on soil food webs and biodiversity, (2) invasive earthworm effects on soil chemical properties, (3) global analyses of earthworm and soil biodiversity distribution, and (4) global soil biodiversity distribution and future monitoring.
Altogether, this project has been highly successful with more than 50 scientific papers in international, peer-reviewed journals. I expect that at least 10 more papers will be published by 2022. These results have also already been presented at dozens of scientific meetings, conferences, and workshops. Moreover, my group does a lot of public outreach. Since the start of ECOWORM, a total of over 350 mass media reports covered our research and outreach activities in print, radio, television, and online (social media not included). An ECOWORM exhibit will be shown in the German Pavilion at the EXPO 2020 in Dubai (now planned for 2021/2022). Four further complementary proposals received additional third-party funding that build on the present project and will help to further advance its contents.
Our first meta-analyses of invasive earthworm effects on plant and soil biodiversity go well beyond the state of the art by showing that earthworm effects increase with the functional richness (i.e. complexity) of the earthworm community. Earthworms facilitate the invasion of non-native plants and change soil communities by favoring fungal- over bacterial-dominated food webs. Our field observation study further shows for the first time that negative effects of invasive earthworms on soil animals are similarly pronounced across size classes (soil micro-, meso-, and macrofauna). Meta-analysis results on invasive earthworm effects on soil chemical properties indicate that earthworms enhance nitrogen and carbon leaching from the soil, decrease soil water content, and increase soil pH. A unique combination of field observations and a controlled Ecotron experiment allowed us to study for the first time the effects of invasive earthworms on leaf defense traits, herbivore damage and pathogen infection in two poplar tree species native to North American boreal forests.
Moreover, my postdocs and I led multiple perspectives and opinion papers on (1) the pervasive effects of exotic earthworms on multiple ecosystem functions, (2) the role of mycorrhizae for the functioning of terrestrial ecosystems, (3) important topics of future soil ecological research, (4) the future of biodiversity-ecosystem functioning research, (5) scaling-issues in soil biodiversity research, (6) gaps in global soil biodiversity data as well as the need and features of future soil biodiversity monitoring, and (7) the essential soil biodiversity variables and related soil health indicators for decision makers. We compiled a global dataset of earthworm communities from >9,000 sites in 57 countries to predict earthworm diversity patterns. In perspectives papers, we outlined that any soil biodiversity assessment needs to consider the different spatial and temporal scales. An important novel insight generated from our work is that climate variables are exceptionally important in driving soil organisms and functions, suggesting that climate change may have serious implications for soil communities. Work in ECOWORM stimulated the initiation of an international soil monitoring program based on essential soil biodiversity variables and holistic soil indicators. In addition to these significant novel findings, we are still expecting to publish papers on invasive earthworm effects on (1) soil ecosystem multifunctionality, (2) the structure and energy fluxes of above-belowground food webs, (3) and the biotic homogenization of ecological communities.
Global effects of exotic earthworm invasion