Skip to main content
Log in

Stage dependence of Elton’s biotic resistance hypothesis of biological invasions

  • Article
  • Published:

From Nature Plants

View current issue Submit your manuscript

Abstract

Elton’s biotic resistance hypothesis posits that species-rich communities are more resistant to invasion. However, it remains unknown how species, phylogenetic and functional richness, along with environmental and human-impact factors, collectively affect plant invasion as alien species progress along the introduction–naturalization–invasion continuum. Using data from 12,056 local plant communities of the Czech Republic, this study reveals varying effects of these factors on the presence and richness of alien species at different invasion stages, highlighting the complexity of the invasion process. Specifically, we demonstrate that although species richness and functional richness of resident communities had mostly negative effects on alien species presence and richness, the strength and sometimes also direction of these effects varied along the continuum. Our study not only underscores that evidence for or against Elton’s biotic resistance hypothesis may be stage-dependent but also suggests that other invasion hypotheses should be carefully revisited given their potential stage-dependent nature.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1: Geographical distribution of the non-invaded and invaded plots in the Czech Republic.
Fig. 2: Summary results from models linking alien species presence and richness to explanatory variables.

Similar content being viewed by others

Data availability

The data used in this study were obtained from these sources: the data on vegetation plots were from the Czech National Phytosociological Database54 (https://botzool.cz/vegsci/phytosociologicalDb/); species’ statuses along the invasion continuum were extracted from Pyšek et al.55; the three leaf traits required for CSR calculation were collected from the Pladias Database of the Czech Flora and Vegetation58 and other publications61,62,63,64,65,66; species CSR scores were calculated using the StrateFy tool60; climatic variables were extracted from Tolasz73; soil pH was collected from the Land Use/Land Cover Area Frame Survey74; and the human population density of the cadastral area where each plot located was obtained from the Digital Vector Database of Czech Republic ArcČR v.4.0 (ref. 75). The data that support the findings of this study are available via GitHub at https://github.com/kun-ecology/BioticResistance_InvasionContinuum and via Zenodo at https://doi.org/10.5281/zenodo.12818669 (ref. 79).

Code availability

R functions for the computation of phylogenetic and functional metrics have been deposited on GitHub (https://github.com/kun-ecology/ecoloop). R scripts for reproducing the analyses and figures are available via GitHub at https://github.com/kun-ecology/BioticResistance_InvasionContinuum and via Zenodo at https://doi.org/10.5281/zenodo.12818669 (ref. 79).

References

  1. Roy, H. E. et al. (eds) Summary for Policymakers of the Thematic Assessment Report on Invasive Alien Species and Their Control of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES Secretariat, 2023).

  2. Spatz, D. R. et al. Globally threatened vertebrates on islands with invasive species. Sci. Adv. 3, e1603080 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Walsh, J. R., Carpenter, S. R. & Vander Zanden, M. J. Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc. Natl Acad. Sci. USA 113, 4081–4085 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Liu, C. et al. Economic costs of biological invasions in Asia. NeoBiota 67, 53–78 (2021).

    Article  Google Scholar 

  5. Capinha, C., Essl, F., Porto, M. & Seebens, H. The worldwide networks of spread of recorded alien species. Proc. Natl Acad. Sci. USA 120, e2201911120 (2023).

    Article  CAS  PubMed  Google Scholar 

  6. Seebens, H. et al. Projecting the continental accumulation of alien species through to 2050. Glob. Change Biol. 27, 970–982 (2021).

    Article  CAS  Google Scholar 

  7. Richardson, D. M. & Pyšek, P. Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog. Phys. Geogr. 30, 409–431 (2006).

    Article  Google Scholar 

  8. Elton, C. S. The Ecology of Invasions by Animals and Plants (Univ. Chicago Press, 1958).

  9. Bach, W. et al. Phylogenetic composition of native island floras influences naturalized alien species richness. Ecography 2022, e06227 (2022).

    Article  Google Scholar 

  10. Beaury, E. M., Finn, J. T., Corbin, J. D., Barr, V. & Bradley, B. A. Biotic resistance to invasion is ubiquitous across ecosystems of the United States. Ecol. Lett. 23, 476–482 (2020).

    Article  PubMed  Google Scholar 

  11. Lefebvre, S., Segar, J. & Staude, I. R. Non-natives are linked to higher plant diversity across spatial scales. J. Biogeogr. 51, 1290–1298 (2024).

    Article  Google Scholar 

  12. Fridley, J. D. et al. The invasion paradox: reconciling pattern and process in species invasion. Ecology 88, 3–17 (2007).

    Article  CAS  PubMed  Google Scholar 

  13. Herben, T., Mandák, B., Bímová, K. & Münzbergová, Z. Invasibility and species richness of a community: a neutral model and a survey of published data. Ecology 85, 3223–3233 (2004).

    Article  Google Scholar 

  14. Jeschke, J. M. et al. Taxonomic bias and lack of cross-taxonomic studies in invasion biology. Front. Ecol. Environ. 10, 349–350 (2012).

    Article  Google Scholar 

  15. Jeschke, J. M. General hypotheses in invasion ecology. Divers. Distrib. 20, 1229–1234 (2014).

    Article  Google Scholar 

  16. Stohlgren, T. J., Barnett, D. T. & Kartesz, J. T. The rich get richer: patterns of plant invasions in the United States. Front. Ecol. Environ. 1, 11–14 (2003).

    Article  Google Scholar 

  17. Shea, K. & Chesson, P. Community ecology theory as a framework for biological invasions. Trends Ecol. Evol. 17, 170–176 (2002).

    Article  Google Scholar 

  18. Delavaux, C. S. et al. Native diversity buffers against severity of non-native tree invasions. Nature 621, 773–781 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339 (2011).

    Article  PubMed  Google Scholar 

  20. Pyšek, P. & Richardson, D. M. Invasive species, environmental change and management, and health. Annu. Rev. Environ. Resour. 35, 25–55 (2010).

    Article  Google Scholar 

  21. Daly, E. Z. et al. A synthesis of biological invasion hypotheses associated with the introduction–naturalisation–invasion continuum. Oikos 2023, e09645 (2023).

    Article  Google Scholar 

  22. Guo, K. et al. Ruderals naturalize, competitors invade: varying roles of plant adaptive strategies along the invasion continuum. Funct. Ecol. 36, 2469–2479 (2022).

    Article  CAS  Google Scholar 

  23. Pyšek, P. et al. Small genome size and variation in ploidy levels support the naturalization of vascular plants but constrain their invasive spread. N. Phytol. 239, 2389–2403 (2023).

    Article  Google Scholar 

  24. Omer, A. et al. The role of phylogenetic relatedness on alien plant success depends on the stage of invasion. Nat. Plants 8, 906–914 (2022).

    Article  PubMed  Google Scholar 

  25. Guo, K. et al. Plant invasion and naturalization are influenced by genome size, ecology and economic use globally. Nat. Commun. 15, 1330 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Richardson, D. M. & Pyšek, P. Naturalization of introduced plants: ecological drivers of biogeographical patterns. N. Phytol. 196, 383–396 (2012).

    Article  Google Scholar 

  27. Byun, C., De Blois, S. & Brisson, J. Plant functional group identity and diversity determine biotic resistance to invasion by an exotic grass. J. Ecol. 101, 128–139 (2013).

    Article  Google Scholar 

  28. Banerjee, A. K. et al. Not just with the natives, but phylogenetic relationship between stages of the invasion process determines invasion success of alien plant species. Preprint at https://doi.org/10.1101/2022.10.12.512006 (2022).

  29. Cubino, J. P., Těšitel, J., Fibich, P., Lepš, J. & Chytrý, M. Alien plants tend to occur in species-poor communities. NeoBiota 73, 39–56 (2022).

    Article  Google Scholar 

  30. Lannes, L. S. et al. Species richness both impedes and promotes alien plant invasions in the Brazilian Cerrado. Sci. Rep. 10, 11365 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Stohlgren, T. J. et al. Exotic plant species invade hot spots of native plant diversity. Ecol. Monogr. 69, 25–46 (1999).

    Article  Google Scholar 

  32. Davidson, A. M., Jennions, M. & Nicotra, A. B. Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol. Lett. 14, 419–431 (2011).

    Article  PubMed  Google Scholar 

  33. Lau, J. A. & Funk, J. L. How ecological and evolutionary theory expanded the ‘ideal weed’ concept. Oecologia 203, 251–266 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Prentis, P. J., Wilson, J. R. U., Dormontt, E. E., Richardson, D. M. & Lowe, A. J. Adaptive evolution in invasive species. Trends Plant Sci. 13, 288–294 (2008).

    Article  CAS  PubMed  Google Scholar 

  35. Stohlgren, T., Jarnevich, C. S., Chong, G. W. & Evangelista, P. Scale and plant invasions: a theory of biotic acceptance. Preslia 78, 405–426 (2006).

    Google Scholar 

  36. Cavieres, L. A. Facilitation and the invasibility of plant communities. J. Ecol. 109, 2019–2028 (2021).

    Article  Google Scholar 

  37. Catford, J. A., Vesk, P. A., Richardson, D. M. & Pyšek, P. Quantifying levels of biological invasion: towards the objective classification of invaded and invasible ecosystems. Glob. Change Biol. 18, 44–62 (2012).

    Article  Google Scholar 

  38. Su, G., Mertel, A., Brosse, S. & Calabrese, J. M. Species invasiveness and community invasibility of North American freshwater fish fauna revealed via trait-based analysis. Nat. Commun. 14, 2332 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Parker, J. D. et al. Do invasive species perform better in their new ranges? Ecology 94, 985–994 (2013).

    Article  PubMed  Google Scholar 

  40. Iseli, E. et al. Rapid upwards spread of non-native plants in mountains across continents. Nat. Ecol. Evol. 7, 405–413 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Pauchard, A. et al. Ain’t no mountain high enough: plant invasions reaching new elevations. Front. Ecol. Environ. 7, 479–486 (2009).

    Article  Google Scholar 

  42. Zheng, M.-M., Pyšek, P., Guo, K., Hasigerili, H. & Guo, W.-Y. Clonal alien plants in the mountains spread upward more extensively and faster than non-clonal. Neobiota 91, 29–48 (2024).

    Article  Google Scholar 

  43. Zu, K. et al. Elevational shift in seed plant distributions in China’s mountains over the last 70 years. Glob. Ecol. Biogeogr. 32, 1098–1112 (2023).

    Article  Google Scholar 

  44. Reeve, S. et al. Rare, common, alien and native species follow different rules in an understory plant community. Ecol. Evol. 12, e8734 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Hartemink, A. E. & Barrow, N. J. Soil pH–nutrient relationships: the diagram. Plant Soil 486, 209–215 (2023).

    Article  CAS  Google Scholar 

  46. Dawson, W., Rohr, R. P., van Kleunen, M. & Fischer, M. Alien plant species with a wider global distribution are better able to capitalize on increased resource availability. N. Phytol. 194, 859–867 (2012).

    Article  Google Scholar 

  47. Dawson, W. et al. Global hotspots and correlates of alien species richness across taxonomic groups. Nat. Ecol. Evol. 1, 0186 (2017).

    Article  Google Scholar 

  48. Pyšek, P. et al. Disentangling the role of environmental and human pressures on biological invasions across Europe. Proc. Natl Acad. Sci. USA 107, 12157–12162 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Damgaard, C. A critique of the space-for-time substitution practice in community ecology. Trends Ecol. Evol. 34, 416–421 (2019).

    Article  PubMed  Google Scholar 

  50. Hejda, M., Pyšek, P. & Jarošík, V. Impact of invasive plants on the species richness, diversity and composition of invaded communities. J. Ecol. 97, 393–403 (2009).

    Article  Google Scholar 

  51. Lovell, R. S. L., Collins, S., Martin, S. H., Pigot, A. L. & Phillimore, A. B. Space-for-time substitutions in climate change ecology and evolution. Biol. Rev. 98, 2243–2270 (2023).

    Article  PubMed  Google Scholar 

  52. Thomaz, S. M. et al. Using space-for-time substitution and time sequence approaches in invasion ecology. Freshw. Biol. 57, 2401–2410 (2012).

    Article  Google Scholar 

  53. Wogan, G. O. U. & Wang, I. J. The value of space‐for‐time substitution for studying fine‐scale microevolutionary processes. Ecography 41, 1456–1468 (2018).

    Article  Google Scholar 

  54. Chytrý, M. & Rafajová, M. Czech National Phytosociological Database: basic statistics of the available vegetation-plot data. Preslia 75, 1–15 (2003).

    Google Scholar 

  55. Pyšek, P. et al. Catalogue of alien plants of the Czech Republic (3rd edition): species richness, status, distributions, habitats, regional invasion levels, introduction pathways and impacts. Preslia 94, 447–577 (2022).

    Article  Google Scholar 

  56. Divíšek, J. et al. Similarity of introduced plant species to native ones facilitates naturalization, but differences enhance invasion success. Nat. Commun. 9, 4631 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Raunkiaer, C. The Life Forms of Plants and Statistical Plant Geography (Clarendon, 1934).

  58. Chytrý, M. et al. Pladias Database of the Czech flora and vegetation. Preslia 93, 1–87 (2021).

    Article  Google Scholar 

  59. Li, D. rtrees: an R package to assemble phylogenetic trees from megatrees. Ecography 2023, e06643 (2023).

    Article  Google Scholar 

  60. Pierce, S. et al. A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Funct. Ecol. 31, 444–457 (2017).

    Article  Google Scholar 

  61. Díaz, S. et al. The global spectrum of plant form and function: enhanced species-level trait dataset. Sci. Data 9, 755 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Guo, W.-Y. et al. The role of adaptive strategies in plant naturalization. Ecol. Lett. 21, 1380–1389 (2018).

    Article  PubMed  Google Scholar 

  63. Guo, W.-Y. et al. Domestic gardens play a dominant role in selecting alien species with adaptive strategies that facilitate naturalization. Glob. Ecol. Biogeogr. 28, 628–639 (2019).

    Article  Google Scholar 

  64. Tavşanoǧlu, Ç. & Pausas, J. G. A functional trait database for Mediterranean Basin plants. Sci. Data 51, 180135 (2018).

    Article  Google Scholar 

  65. Bjorkman, A. D. et al. Tundra Trait Team: a database of plant traits spanning the tundra biome. Glob. Ecol. Biogeogr. 27, 1402–1411 (2018).

    Article  Google Scholar 

  66. Kattge, J. et al. TRY plant trait database—enhanced coverage and open access. Glob. Change Biol. 26, 119–188 (2020).

    Article  Google Scholar 

  67. Goolsby, E. W., Bruggeman, J. & Ané, C. Rphylopars: fast multivariate phylogenetic comparative methods for missing data and within-species variation. Methods Ecol. Evol. 8, 22–27 (2017).

    Article  Google Scholar 

  68. Matthews, T. J. et al. A global analysis of avian island diversity–area relationships in the Anthropocene. Ecol. Lett. 26, 965–982 (2023).

    Article  PubMed  Google Scholar 

  69. Cardoso, P. et al. Calculating functional diversity metrics using neighbor-joining trees. Ecography https://doi.org/10.1101/2022.11.27.518065 (2022).

  70. Cardoso, P., Rigal, F. & Carvalho, J. C. BAT—Biodiversity Assessment Tools, an R package for the measurement and estimation of alpha and beta taxon, phylogenetic and functional diversity. Methods Ecol. Evol. 6, 232–236 (2015).

    Article  Google Scholar 

  71. Swenson, N. G. Functional and Phylogenetic Ecology in R (Springer, 2014).

  72. Loiola, P. P. et al. Invaders among locals: alien species decrease phylogenetic and functional diversity while increasing dissimilarity among native community members. J. Ecol. 106, 2230–2241 (2018).

    Article  Google Scholar 

  73. Tolasz, R. et al. Atlas Podnebí Česka—Climate Atlas of Czechia (Czech Hydrometeorological Institute and Palacký Univ., 2007).

  74. Ballabio, C. et al. Mapping LUCAS topsoil chemical properties at European scale using Gaussian process regression. Geoderma 355, 113912 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Digital Vector Database of Czech Republic ArcČR v.4.0 (ČÚZK, ČSÚ and ArcDATA Prague, 2021).

  76. Lindgren, F. & Rue, H. Bayesian spatial modelling with R-INLA. J. Stat. Softw. 63, 1–25 (2015).

    Article  Google Scholar 

  77. Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010).

    Article  Google Scholar 

  78. R Core Team. R: A Language and Environment for Statistical Computing http://www.R-project.org/ (R Foundation for Statistical Computing, 2023).

  79. Guo, K. et al. Stage dependence of Elton’s biotic resistance hypothesis of biological invasions. Zenodo https://doi.org/10.5281/zenodo.12818669 (2024).

Download references

Acknowledgements

K.G. and W.-Y.G. were supported by the Natural Science Foundation of China (grant no. 32171588, awarded to W.-Y.G.) and the Shanghai Pujiang Program (grant no. 21PJ1402700, awarded to W.-Y.G.). K.G. was also supported by the Shanghai Sailing Program (grant no. 22YF1411700) and the Natural Science Foundation of China (grant no. 32301386). P.P. was supported by the Czech Science Foundation (EXPRO grant no. 19-28807X) and the Czech Academy of Sciences (long-term research development project RVO 67985939). M.C. and Z.L. were supported by the Czech Science Foundation (EXPRO grant no. 19-28491X). J.D. was supported by the Technology Agency of the Czech Republic (grant no. SS02030018). M.S. was funded by the project GEOSANT with the funding organization Masaryk University (MUNI/A/1469/2023).

Author information

Authors and Affiliations

Authors

Contributions

K.G., P.P. and W.-Y.G. conceptualized the research. P.P., M.C., J.D., M.S. and W.-Y.G. provided the data. K.G. analysed the data and drafted the paper, with substantial contributions from all authors.

Corresponding author

Correspondence to Wen-Yong Guo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Plants thanks Martha Hoopes and Johannes Kollmann for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, K., Pyšek, P., Chytrý, M. et al. Stage dependence of Elton’s biotic resistance hypothesis of biological invasions. Nat. Plants (2024). https://doi.org/10.1038/s41477-024-01790-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41477-024-01790-0

  • Springer Nature Limited

Navigation