Co-invasion of three Asian earthworms, Metaphire hilgendorfi, Amynthas agrestis and Amynthas tokioensis in the USA

Earthworm invasions are one of the most serious causes of ecological deterioration in the temperate deciduous forests of North America. Non-native earthworms impact understory vegetation, leaf litter layer, carbon dynamics, nutrient availability, and the associated food webs. Here we report a significant status change and confirm expansion of known range of Amynthas agrestis, one of the most serious invasive species in North America, and two of its close relatives, A. tokioensis and Metaphire hilgendorfi. The three species have never been confirmed to co-occur in North American ecosystems. We examined 1760 earthworms collected from 30 sites across northeastern USA, and identified them using a new morphological key. Our data show that sympatric occurrence of at least two, and often all three, species is more common than having only one species. In addition, A. tokioensis was dominant in many of these earthworm communities. The status change in species composition from only one species to two or three and the shift in dominance are most likely caused by previous incorrect species identification. Our results support expansion of known range of A. tokioensis and M. hilgendorfi northward and westward into states with colder winters. This range expansion may have taken place alongside that of A. agrestis in the last 10-20 years, but has long been overlooked. Altogether, results highlight an urgent need for correct species identification. The recognition of an expanding multi-species system represents a unique opportunity to further evaluate complex interactions among co-invading and resident species, and to investigate whether interspecific interactions have unexpected non-additive impacts on ecological processes.