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Invading plants remain undetected in a lag phase while they explore suitable climates

Nature Ecology & Evolution volume 8, pages 477–488 (2024)Cite this article

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Abstract

Successful alien species may experience a period of quiescence, known as the lag phase, before becoming invasive and widespread. The existence of lags introduces severe uncertainty in risk analyses of aliens as the present state of species is a poor predictor of future distributions, invasion success and impact. Predicting a species’ ability to invade and pose negative impacts requires a quantitative understanding of the commonality and magnitude of lags, environmental factors and mechanisms likely to terminate lag. Using herbarium and climate data, we analysed over 5,700 time series (species × regions) in 3,505 naturalized plant species from nine regions in temperate and tropical climates to quantify lags and test whether there have been shifts in the species’ climatic space during the transition from the lag phase to the expansion phase. Lags were identified in 35% of the assessed invasion events. We detected phylogenetic signals for lag phases in temperate climate regions and that annual self-fertilizing species were less likely to experience lags. Where lags existed, they had an average length of 40 years and a maximum of 320 years. Lengthy lags (>100 years) were more likely to occur in perennial plants and less frequent in self-pollinating species. For 98% of the species with a lag phase, the climate spaces sampled during the lag period differed from those in the expansion phase based on the assessment of centroid shifts or degree of climate space overlap. Our results highlight the importance of functional traits for the onset of the expansion phase and suggest that climate discovery may play a role in terminating the lag phase. However, other possibilities, such as sampling issues and climate niche shifts, cannot be ruled out.

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Fig. 1: Potential scenarios for differences between the climate envelopes of lag and post-lag phases.
Fig. 2: Biphasic temporal trends.
Fig. 3: The comparison of lag and post-lag periods for climate variables identified as the most influential in causing a climate niche shift between the two invasion phases based on multivariate analysis.
Fig. 4: Probability and length of lag phase.

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Data availability

For Australia, a list of naturalized alien plants was acquired from the compendium of the introduced flora of Australia65 and the corresponding occurrence records were extracted from Australia’s Virtual Herbarium (https://www.ala.org.au)67. New Zealand’s data were obtained from literature41,47,68. The GloNAF database is available in the literature69,101 and was queried to extract species lists for the remaining six regions. Georeferenced occurrence records were extracted from the Global Biodiversity Informatics Facility (https://www.gbif.org)70. Trait data were extracted from TRYDB (https://www.try-db.org). Climate data were downloaded from the second version of the WorldClim dataset (https://www.worldclim.org/data/worldclim21.html). All data are available online and in the literature.

The minimum dataset comprises the naturalized species lists sourced from the GloNaf database, the compendium of the introduced flora of Australia65 and previous studies41,47 and is available under the CC BY 4.0 licence (https://doi.org/10.26188/24782898).

Code availability

The analysis has been implemented using existing packages referenced in the text. Implementation scripts are available on request.

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Acknowledgements

M.V.K. was supported by the German Research Foundation DFG (grant number 264740629). P.P. and J.P. were supported by EXPRO grant number 19-28807X (Czech Science Foundation) and long-term research development project RVO 67985939 (Czech Academy of Sciences). F.E. received funding through the 2017–2018 Belmont Forum and BiodivERsA joint call for research proposals under the BiodivScen ERA-Net COFUND programme and the funding organization FWF (‘AlienScenarios’ project number I 4011-B32).

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Authors and Affiliations

  1. School of BioSciences, Faculty of Science, University of Melbourne, Parkville, Victoria, Australia

    Philipp Robeck

  2. Division of BioInvasions, Global Change & Macroecology, Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria

    Franz Essl

  3. Centre for Invasion Biology, Department of Botany & Zoology, Stellenbosch University, Matieland, South Africa

    Franz Essl

  4. Ecology, Department of Biology, University of Konstanz, Konstanz, Germany

    Mark van Kleunen

  5. Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, China

    Mark van Kleunen

  6. Department of Invasion Ecology, Institute of Botany, Czech Academy of Sciences, Průhonice, Czech Republic

    Petr Pyšek & Jan Pergl

  7. Department of Ecology, Faculty of Science, Charles University, Prague, Czech Republic

    Petr Pyšek

  8. Department of Biodiversity, Macroecology & Biogeography, University of Göttingen, Göttingen, Germany

    Patrick Weigelt

  9. Centre of Biodiversity and Sustainable Land Use, University of Göttingen, Göttingen, Germany

    Patrick Weigelt

  10. Campus Institute Data Science, Göttingen, Germany

    Patrick Weigelt

  11. Department of Plant Sciences, University of California, Davis, Davis, CA, USA

    Mohsen B. Mesgaran

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M.B.M. conceived the idea; M.B.M. and P.R. designed the research, performed the analysis and wrote the first draft of the paper; F.E., M.V.K., P.P., J.P. and P.W. provided data, edited the paper and provided comments.

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Robeck, P., Essl, F., van Kleunen, M. et al. Invading plants remain undetected in a lag phase while they explore suitable climates. Nat Ecol Evol 8, 477–488 (2024). https://doi.org/10.1038/s41559-023-02313-4

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  • DOI: https://doi.org/10.1038/s41559-023-02313-4

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