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Multiple invasion routes have led to the pervasive introduction of earthworms in North America

Nature Ecology & Evolution volume 8, pages 489–499 (2024)Cite this article

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Abstract

Soil-dwelling organisms play a key role in ecosystem functioning and the delivery of ecosystem services. As a consequence, soil taxa such as earthworms are iconic in good land management practices. However, their introduction in places where species did not co-evolve with them can trigger catastrophic changes. This issue has been largely ignored so far in nature management policies because of the positive image of soil taxa and the lack of knowledge of the magnitude of soil fauna introductions outside their native range. Here we address this gap with a large spatio-temporal database of introduced alien earthworms. We show that 70 alien earthworm species have colonized the North American continent. They have larger geographical ranges than native species and novel ecological functions, representing a serious threat to the biodiversity and functioning of native ecosystems. The probably continuous introduction of alien earthworms, from a variety of sources and introduction pathways, into many distant and often empty niches, contrasts with the classical patterns of invasions in most aboveground taxa. This suggests that earthworms, and probably other soil organisms, constitute a major but overlooked pool of invasive species that are not adequately managed by existing control and mitigation strategies.

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Fig. 1: Estimated relative alien earthworm species richness in North America.
Fig. 2: Spatio-temporal dynamics of earthworm alien species richness across North America.
Fig. 3: Correlations between the species richness of alien earthworms and the species richness of aboveground alien taxa.
Fig. 4: Historical dynamics of North America’s colonization by alien earthworm species.
Fig. 5: Introduction pathways of alien earthworm species in the United States between 1945 and 1975.
Fig. 6: Functional niche of earthworm species in North America and functional enrichment brought by aliens.

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Data availability

Earthworm native and alien species richness in North America at the two spatial resolutions, together with the aboveground alien species richness in TDWG4 units, is available in the EWINA_RICH99 database at https://doi.org/10.5281/zenodo.6421014. EWINA_IPATHS100, the database of intercepted earthworm introduction pathways from 1945 to 1975 is available at https://doi.org/10.5281/zenodo.6408609. EWINA_SP101, the tabular data of Ecological profile of earthworm species found in North America, including geographical origin, alien status, functional role and reproduction mode is available at https://doi.org/10.5281/zenodo.6462831. EWINA_1st_RECORDS102, the list of first year of observation of each earthworm species in North America can be found at https://zenodo.org/record/6759725. The sources of the environmental data are given in Supplementary Table 1. The list of data sources is provided in Supplementary Information.

Code availability

R scripts used for the analyses are available at https://github.com/JeromeMathieuEcology/GlobalWorming.

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Acknowledgements

We thank the people who helped with digitizing information on the distribution of native and alien earthworm species, particularly E. Pedarros, S. Dandrifosse, C. Mathieu, J. Nabias and T. Allain. We highly appreciate the comments and suggestions of N. Eisenhauer, I. Gounand, G. Lacroix and O. Moine, and the help of W. Dawson and R. Early regarding the use of their databases, as well as the help of M. Wright regarding the use of the package ranger. Finally, we thank the Animal Plant Health Inspection Service from the United States Department of Agriculture and the Invasive Alien Species & Domestic Programs Section from the Canadian Food Inspection Agency for their help regarding the import-export regulation laws. Funding was provided by the France-Stanford Center for Interdisciplinary Studies.

Author information

Authors and Affiliations

  1. Institut d’Ecologie et des Sciences de l’Environnement de Paris, Sorbonne Université, CNRS, UPEC, INRAE, IRD, Paris, France

    Jérôme Mathieu

  2. Oligochaetology Laboratory, Kitchener, Ontario, Canada

    John W. Reynolds

  3. New Brunswick Museum, Saint John, New Brunswick, Canada

    John W. Reynolds

  4. Red de Biodiversidad y Sistemática, Instituto de Ecología A.C., Xalapa, Mexico

    Carlos Fragoso

  5. Department of Biology, Stanford University, Stanford, CA, USA

    Elizabeth Hadly

  6. Department of Earth System Science, Stanford University, Stanford, CA, USA

    Elizabeth Hadly

  7. Stanford Woods Institute for the Environment, Stanford University, Stanford, CA, USA

    Elizabeth Hadly

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  1. Jérôme Mathieu
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Contributions

J.M. and E.H. conceived the original idea and secured the principal funding. J.M. curated the data and ran the analyses. J.M., J.W.R. and C.F. searched for data, J.M. wrote the first draft, and all authors reviewed and edited the manuscript.

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Correspondence to Jérôme Mathieu.

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Extended data

Extended Data Fig. 1 Critical patterns and mechanisms that needs to be documented to manage earthworm invasive species, and corresponding figures in this article.

Five aspects of earthworm invasions in North America are covered here: a) Which and how many earthworm species are alien? What are their functional niches? b) When, where and how introductions occurred? c) What is the distribution of alien species and the drivers of their habitat? d) How similar, or particular, are alien earthworm species richness compared with other above-ground taxa? e) Where do alien earthworm species have the maximal potential ecological impact?.

Extended Data Fig. 2 Geographical coverage of the EWINA database.

Data that are available in the EWINA database are indicated in dark grey, while geographical units with no data are indicated in light grey. A/ Complete coverage. B/ Coverage for the period 2000-2021. Only the data from 2000-2021 were used to model RASR (Relative Alien Species Richness).

Extended Data Fig. 3 Geographical range of Native and Alien species across North America.

Each horizontal bar represents the geographical range of a species. The range is expressed as the proportion of geographic units where the species occur. The color of the bars indicates the origin of the species. The 15 most widespread species are listed in the box, by decreasing order of geographical range. * B. rubidus is a synonym of Dendrodrilus rubidus, m: species considered as alien in Mexico, c species considered as alien in Canada, cm species considered as alien in Canada and Mexico.

Extended Data Fig. 4 Reproduction type of native and alien earthworm species in North America.

A: Amphimictic : reproduction sexual and biparenthal, AP : generaly amphimictic with parthenogenesis in some morphs, P : parthenogenetic, reproduction uniparental, PF : parthenogenesis facultative (χ2 = 42.8, p = 1.15 10−8).

Extended Data Fig. 5 Temporal dynamics of the known geographical range of native and alien earthworm species across North America.

Each line represents the geographical range of a species over time. Geographical range is expressed as the percentage of geographical units (county level, Extended Data Fig. 2) that are occupied by a species.

Extended Data Fig. 6 Variable importance in the random forest model of earthworms’ RASR.

Variable importance represents the magnitude of accuracy loss of the predictions across all trees when randomizing the considered variable. The procedure is repeated for all variables of interest.

Extended Data Fig. 7 C-ICE plots: influence of the covariates on predicted RASR.

The thick yellow line indicates the effect of the covariate for an average environmental condition (All other covariates being at their average value). The blue lines indicate the effect of the covariate for the individual conditions across the training dataset. The heterogeneity of the individual blue lines indicates the variability of the predictor across individual conditions.

Extended Data Fig. 8 Earthworm species richness in the TDWG-level 4 geographical units.

Maps of the species richness of earthworm across the TDWG-level 4 regions. The TDWG regions are standardized geographical units defined to compare species richness across taxa at large scale. The maps detail the Alien, Native, and Total species richness of earthworm respectively. These data were used for the comparison with above ground taxa (Fig. 3).

Extended Data Fig. 9 Model performance.

This plot shows the predicted value of each observation, using a model in which the observation was not used to train the model (OOB test data), against the observed RASR. The closer the data are from the line, the best the model performs. We can see that the model tends to slightly underestimate RASR in actual high values RASR and slightly overestimate RASR values in actual low values of RASR. OOB r2 is 0.6.

Extended Data Fig. 10 Map of predictions’ uncertainty.

This map shows the uncertainty of the predictions made by the model. This is useful to interpret the predicted values mapped in Fig. 1. We see that the uncertainty is overall relatively low.

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Mathieu, J., Reynolds, J.W., Fragoso, C. et al. Multiple invasion routes have led to the pervasive introduction of earthworms in North America. Nat Ecol Evol 8, 489–499 (2024). https://doi.org/10.1038/s41559-023-02310-7

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