Plant invasion and naturalization are influenced by genome size, ecology and economic use globally

. 2024 Feb 13 ; 15 (1) : 1330. [epub] 20240213

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38351066

Grantová podpora
32171588 National Natural Science Foundation of China (National Science Foundation of China)

Odkazy

PubMed 38351066
PubMed Central PMC10864296
DOI 10.1038/s41467-024-45667-4
PII: 10.1038/s41467-024-45667-4
Knihovny.cz E-zdroje

Human factors and plant characteristics are important drivers of plant invasions, which threaten ecosystem integrity, biodiversity and human well-being. However, while previous studies often examined a limited number of factors or focused on a specific invasion stage (e.g., naturalization) for specific regions, a multi-factor and multi-stage analysis at the global scale is lacking. Here, we employ a multi-level framework to investigate the interplay between plant characteristics (genome size, Grime's adaptive CSR-strategies and native range size) and economic use and how these factors collectively affect plant naturalization and invasion success worldwide. While our findings derived from structural equation models highlight the substantial contribution of human assistance in both the naturalization and spread of invasive plants, we also uncovered the pivotal role of species' adaptive strategies among the factors studied, and the significantly varying influence of these factors across invasion stages. We further revealed that the effects of genome size on plant invasions were partially mediated by species adaptive strategies and native range size. Our study provides insights into the complex and dynamic process of plant invasions and identifies its key drivers worldwide.

Biodiversity Macroecology and Biogeography University of Goettingen Göttingen Germany

Campus Institute Data Science Göttingen Germany

Centre of Biodiversity and Sustainable Land Use University of Goettingen Göttingen Germany

Czech Academy of Sciences Institute of Botany Department of Evolutionary Plant Biology Průhonice CZ 25243 Czech Republic

Czech Academy of Sciences Institute of Botany Department of Invasion Ecology Průhonice CZ 25243 Czech Republic

Department of Agricultural and Environmental Sciences University of Milan Via G Celoria 2 1 20133 Milan Italy

Department of Biosciences Durham University Durham UK

Department of Botany Faculty of Science University of South Bohemia Branišovská 1760 České Budějovice CZ 370 05 Czech Republic

Department of Ecology Faculty of Science Charles University Viničná 7 Prague CZ 12844 Czech Republic

Department of Evolution Ecology and Behaviour Institute of Infection Veterinary and Ecological Sciences University of Liverpool Liverpool UK

Division of BioInvasions Global Change and Macroecology Department of Botany and Biodiversity Research University of Vienna Vienna Austria

Ecology Department of Biology University of Konstanz Universitätsstrasse 10 D 78457 Konstanz Germany

Research Center for Global Change and Complex Ecosystems School of Ecological and Environmental Sciences East China Normal University 200241 Shanghai P R China

Royal Botanic Gardens Kew Richmond Surrey TW9 3AB UK

Shanghai Key Lab for Urban Ecological Processes and Eco Restoration School of Ecological and Environmental Sciences East China Normal University 200241 Shanghai P R China

Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation Taizhou University Taizhou 318000 P R China

Zhejiang Tiantong Forest Ecosystem National Observation and Research Station School of Ecological and Environmental Sciences East China Normal University 200241 Shanghai P R China

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Bellard C, Cassey P, Blackburn TM. Alien species as a driver of recent extinctions. Biol. Lett. 2016;12:20150623. doi: 10.1098/rsbl.2015.0623. PubMed DOI PMC

Blackburn TM, Bellard C, Ricciardi A. Alien versus native species as drivers of recent extinctions. Front. Ecol. Environ. 2019;17:203–207. doi: 10.1002/fee.2020. DOI

Sax DF, Gaines SD. Species invasions and extinction: The future of native biodiversity on islands. Proc. Natl Acad. Sci. USA. 2008;105:11490–11497. doi: 10.1073/pnas.0802290105. PubMed DOI PMC

Capinha C, Essl F, Seebens H, Moser D, Pereira HM. The dispersal of alien species redefines biogeography in the Anthropocene. Science. 2015;348:1248–1251. doi: 10.1126/science.aaa8913. PubMed DOI

Yang Q, et al. The global loss of floristic uniqueness. Nat. Commun. 2021;12:7290. doi: 10.1038/s41467-021-27603-y. PubMed DOI PMC

Diagne C, et al. High and rising economic costs of biological invasions worldwide. Nature. 2021;592:571–576. doi: 10.1038/s41586-021-03405-6. PubMed DOI

IPBES. 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. In (eds. Roy, H. E. et al.) 10.5281/zenodo.7430692 (IPBES Secretariat, 2023).

Novoa A, et al. Global costs of plant invasions must not be underestimated. NeoBiota. 2021;69:75–78. doi: 10.3897/neobiota.69.74121. DOI

Seebens H, et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 2017;8:14435. doi: 10.1038/ncomms14435. PubMed DOI PMC

Seebens H, et al. Projecting the continental accumulation of alien species through to 2050. Glob. Change Biol. 2021;27:970–982. doi: 10.1111/gcb.15333. PubMed DOI

van Kleunen M, et al. Economic use of plants is key to their naturalization success. Nat. Commun. 2020;11:3201. doi: 10.1038/s41467-020-16982-3. PubMed DOI PMC

Balestri E, Vallerini F, Menicagli V, Barnaba S, Lardicci C. Biotic resistance and vegetative propagule pressure co-regulate the invasion success of a marine clonal macrophyte. Sci. Rep. 2018;8:16621. doi: 10.1038/s41598-018-35015-0. PubMed DOI PMC

Lockwood JL, Cassey P, Blackburn TM. The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Divers. Distrib. 2009;15:904–910. doi: 10.1111/j.1472-4642.2009.00594.x. DOI

Kubešová M, Moravcová L, Suda J, Jarošík V, Pyšek P. Naturalized plants have smaller genomes than their non-invading relatives: A flow cytometric analysis of the Czech alien flora. Preslia. 2010;82:81–96.

Lopes S, et al. Genome size variation in Cactaceae and its relationship with invasiveness and seed traits. Biol. Invasions. 2021;23:3047–3062. doi: 10.1007/s10530-021-02557-w. DOI

Pyšek P, et al. Small genome separates native and invasive populations in an ecologically important cosmopolitan grass. Ecology. 2018;99:79–90. doi: 10.1002/ecy.2068. PubMed DOI

Pyšek P, et al. Small genome size and variation in ploidy levels support the naturalization of vascular plants but constrain their invasive spread. New Phytol. 2023;239:2389–2403. doi: 10.1111/nph.19135. PubMed DOI

Knight CA, Molinari NA, Petrov DA. The large genome constraint hypothesis: Evolution, ecology and phenotype. Ann. Bot. 2005;95:177–190. doi: 10.1093/aob/mci011. PubMed DOI PMC

Simonin KA, Roddy AB. Genome downsizing, physiological novelty, and the global dominance of flowering plants. PLOS Biol. 2018;16:e2003706. doi: 10.1371/journal.pbio.2003706. PubMed DOI PMC

Beaulieu JM, et al. Correlated evolution of genome size and seed mass. New Phytol. 2007;173:422–437. doi: 10.1111/j.1469-8137.2006.01919.x. PubMed DOI

Carta A, Mattana E, Dickie J, Vandelook F. Correlated evolution of seed mass and genome size varies among life forms in flowering plants. Seed Sci. Res. 2022;32:46–52. doi: 10.1017/S0960258522000071. DOI

Bennett MD. Nuclear DNA content and minimum generation time in herbaceous plants. Proc. R. Soc. Lond. B Biol. Sci. 1972;181:109–135. doi: 10.1098/rspb.1972.0042. PubMed DOI

Sinjushin AA. The duration of the life cycle is associated with C-value and affects reproductive features in the Fabeae, the tribe with largest genomes in Fabaceae. Flora. 2021;285:151954. doi: 10.1016/j.flora.2021.151954. DOI

Pellicer J, Hidalgo O, Dodsworth S, Leitch IJ. Genome size diversity and its impact on the evolution of land plants. Genes. 2018;9:88. doi: 10.3390/genes9020088. PubMed DOI PMC

Suda J, Meyerson LA, Leitch IJ, Pyšek P. The hidden side of plant invasions: The role of genome size. New Phytol. 2015;205:994–1007. doi: 10.1111/nph.13107. PubMed DOI

te Beest M, et al. The more the better? the role of polyploidy in facilitating plant invasions. Ann. Bot. 2012;109:19–45. doi: 10.1093/aob/mcr277. PubMed DOI PMC

Parker JD. Do invasive species perform better in their new ranges? Ecology. 2013;94:985–994. doi: 10.1890/12-1810.1. PubMed DOI

van Kleunen M, Weber E, Fischer M. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol. Lett. 2010;13:235–245. doi: 10.1111/j.1461-0248.2009.01418.x. PubMed DOI

Jenkins C, Keller SR. A phylogenetic comparative study of preadaptation for invasiveness in the genus Silene (Caryophyllaceae) Biol. Invasions. 2011;13:1471–1486. doi: 10.1007/s10530-010-9907-4. DOI

Fristoe TS, et al. Dimensions of invasiveness: Links between local abundance, geographic range size, and habitat breadth in Europe’s alien and native floras. Proc. Natl Acad. Sci. USA. 2021;118:1–11. doi: 10.1073/pnas.2021173118. PubMed DOI PMC

Pierce S, et al. A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Funct. Ecol. 2017;31:444–457. doi: 10.1111/1365-2435.12722. DOI

Pierce S, Maffi D, Faoro F, Cerabolini BEL, Spada A. The leaf anatomical trade-offs associated with plant ecological strategy variation. Plant Ecol. 2022;223:1233–1246. doi: 10.1007/s11258-022-01270-5. DOI

Díaz S, et al. The global spectrum of plant form and function. Nature. 2016;529:167–171. doi: 10.1038/nature16489. PubMed DOI

Guo W-Y, et al. Domestic gardens play a dominant role in selecting alien species with adaptive strategies that facilitate naturalization. Glob. Ecol. Biogeogr. 2019;28:628–639. doi: 10.1111/geb.12882. DOI

Guo W, et al. The role of adaptive strategies in plant naturalization. Ecol. Lett. 2018;21:1380–1389. doi: 10.1111/ele.13104. PubMed DOI

Freckleton RP, Watkinson AR. Asymmetric competition between plant species. Funct. Ecol. 2001;15:615–623. doi: 10.1046/j.0269-8463.2001.00558.x. DOI

Grime, J. P. & Pierce, S. The Evolutionary Strategies that Shape Ecosystems. 10.1002/9781118223246 (John Wiley & Sons, Ltd, 2012).

Wingler A, Sandel B. Relationships of the competitor, stress tolerator, ruderal functional strategies of grass species with lifespan, photosynthetic type, naturalization and climate. AoB PLANTS. 2023;15:1–10. doi: 10.1093/aobpla/plad021. PubMed DOI PMC

Pyšek P, Křivánek M, Jarošík V. Planting intensity, residence time, and species traits determine invasion success of alien woody species. Ecology. 2009;90:2734–2744. doi: 10.1890/08-0857.1. PubMed DOI

Pyšek P, et al. Naturalization of central European plants in North America: Species traits, habitats, propagule pressure, residence time. Ecology. 2015;96:762–774. doi: 10.1890/14-1005.1. PubMed DOI

Rejmánek M. A theory of seed plant invasiveness: The first sketch. Biol. Conserv. 1996;78:171–181. doi: 10.1016/0006-3207(96)00026-2. DOI

Liao H, et al. The role of functional strategies in global plant distribution. Ecography. 2021;44:493–503. doi: 10.1111/ecog.05476. DOI

van Kleunen M, Johnson SD, Fischer M. Predicting naturalization of southern African Iridaceae in other regions. J. Appl. Ecol. 2007;44:594–603. doi: 10.1111/j.1365-2664.2007.01304.x. DOI

Dawson W, Burslem DFRP, Hulme PE. Factors explaining alien plant invasion success in a tropical ecosystem differ at each stage of invasion. J. Ecol. 2009;97:657–665. doi: 10.1111/j.1365-2745.2009.01519.x. DOI

Divíšek J, et al. Similarity of introduced plant species to native ones facilitates naturalization, but differences enhance invasion success. Nat. Commun. 2018;9:4631. doi: 10.1038/s41467-018-06995-4. PubMed DOI PMC

Essl F, et al. Drivers of the relative richness of naturalized and invasive plant species on Earth. AoB PLANTS. 2019;11:1–13. doi: 10.1093/aobpla/plz051. PubMed DOI PMC

Omer A, et al. The role of phylogenetic relatedness on alien plant success depends on the stage of invasion. Nat. Plants. 2022;8:906–914. doi: 10.1038/s41477-022-01216-9. PubMed DOI

Blackburn TM, et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 2011;26:333–339. doi: 10.1016/j.tree.2011.03.023. PubMed DOI

Pyšek P, et al. Catalogue of alien plants of the Czech Republic (2nd edition): Checklist update, taxonomic diversity and invasion patterns. Preslia. 2012;84:155–255.

Richardson, D. M., Pyšek, P. & Carlton, J. T. A Compendium of Essential Concepts and Terminology in Invasion Ecology. In Fifty Years of Invasion Ecology: The Legacy of Charles Elton 409–420 10.1002/9781444329988.ch30 (Wiley-Blackwell, 2010).

Richardson DM, Pyšek P. Naturalization of introduced plants: Ecological drivers of biogeographical patterns. New Phytol. 2012;196:383–396. doi: 10.1111/j.1469-8137.2012.04292.x. PubMed DOI

Pyšek P, et al. MAcroecological Framework for Invasive Aliens (MAFIA): disentangling large-scale context dependence in biological invasions. NeoBiota. 2020;62:407–461. doi: 10.3897/neobiota.62.52787. DOI

van Kleunen M, Dawson W, Maurel N. Characteristics of successful alien plants. Mol. Ecol. 2015;24:1954–1968. doi: 10.1111/mec.13013. PubMed DOI

Palma E, Vesk PA, White M, Baumgartner JB, Catford JA. Plant functional traits reflect different dimensions of species invasiveness. Ecology. 2021;102:1–14. doi: 10.1002/ecy.3317. PubMed DOI

Banerjee AK, Prajapati J, Bhowmick AR, Huang Y, Mukherjee A. Different factors influence naturalization and invasion processes – A case study of Indian alien flora provides management insights. J. Environ. Manag. 2021;294:113054. doi: 10.1016/j.jenvman.2021.113054. PubMed DOI

Guo K, et al. Ruderals naturalize, competitors invade: Varying roles of plant adaptive strategies along the invasion continuum. Funct. Ecol. 2022;36:2469–2479. doi: 10.1111/1365-2435.14145. DOI

Moodley D, Geerts S, Richardson DM, Wilson JRU. Different traits determine introduction, naturalization and invasion success in woody plants: Proteaceae as a Test Case. PLoS ONE. 2013;8:e75078. doi: 10.1371/journal.pone.0075078. PubMed DOI PMC

Bürkner, P. C. brms: An R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).

Grace JB, et al. Guidelines for a graph-theoretic implementation of structural equation modeling. Ecosphere. 2012;3:art73. doi: 10.1890/ES12-00048.1. DOI

Gioria M, et al. Persistent soil seed banks promote naturalisation and invasiveness in flowering plants. Ecol. Lett. 2021;24:1655–1667. doi: 10.1111/ele.13783. PubMed DOI PMC

Razanajatovo M, et al. Plants capable of selfing are more likely to become naturalized. Nat. Commun. 2016;7:1–9. doi: 10.1038/ncomms13313. PubMed DOI PMC

The Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical J. Linn. Soc.181, 1–20 (2016).

Pandit MK, White SM, Pocock MJO. The contrasting effects of genome size, chromosome number and ploidy level on plant invasiveness: a global analysis. New Phytol. 2014;203:697–703. doi: 10.1111/nph.12799. PubMed DOI

Dong B. et al. Naturalization of introduced plants is driven by life‐form‐dependent cultivation biases. Divers. Distrib. 30, 55–70 (2023).

Bradley BA, et al. Global change, global trade, and the next wave of plant invasions. Front. Ecol. Environ. 2012;10:20–28. doi: 10.1890/110145. DOI

Essl F, et al. Socioeconomic legacy yields an invasion debt. Proc. Natl Acad. Sci. USA. 2011;108:203–207. doi: 10.1073/pnas.1011728108. PubMed DOI PMC

Seebens H, et al. Global trade will accelerate plant invasions in emerging economies under climate change. Glob. Change Biol. 2015;21:4128–4140. doi: 10.1111/gcb.13021. PubMed DOI

Bjorkman AD, et al. Tundra Trait Team: A database of plant traits spanning the tundra biome. Glob. Ecol. Biogeogr. 2018;27:1402–1411. doi: 10.1111/geb.12821. DOI

Brym ZT, Lake JK, Allen D, Ostling A. Plant functional traits suggest novel ecological strategy for an invasive shrub in an understorey woody plant community. J. Appl. Ecol. 2011;48:1098–1106. doi: 10.1111/j.1365-2664.2011.02049.x. DOI

Dayrell RLC, et al. Ontogenetic shifts in plant ecological strategies. Funct. Ecol. 2018;32:2730–2741. doi: 10.1111/1365-2435.13221. DOI

Tavşanoǧlu Ç, Pausas JG. A functional trait database for Mediterranean Basin plants. Sci. Data. 2018;5:1–18. doi: 10.1038/sdata.2018.135. PubMed DOI PMC

Wang H, et al. The China Plant Trait Database: toward a comprehensive regional compilation of functional traits for land plants. Ecology. 2018;99:500. doi: 10.1002/ecy.2091. PubMed DOI

Cayuela L, Granzow-de la Cerda Í, Albuquerque FS, Golicher DJ. taxonstand: An r package for species names standardisation in vegetation databases. Methods Ecol. Evol. 2012;3:1078–1083. doi: 10.1111/j.2041-210X.2012.00232.x. DOI

Pellicer J, Leitch IJ. The Plant DNA C-values database (release 7.1): an updated online repository of plant genome size data for comparative studies. New Phytol. 2020;226:301–305. doi: 10.1111/nph.16261. PubMed DOI

Greilhuber J, Doležel J, Lysák MA, Bennett MD. The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Ann. Bot. 2005;95:255–260. doi: 10.1093/aob/mci019. PubMed DOI PMC

Diazgranados, M. et al. World Checklist of Useful Plant Species. Knowl. Netw. Biocomplexity10.5063/F1CV4G34 (2020).

POWO. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Published on the Internet; http://www.plantsoftheworldonline.org/ (2023).

Govaerts R, Nic Lughadha E, Black N, Turner R, Paton A. The World Checklist of Vascular Plants, a continuously updated resource for exploring global plant diversity. Sci. Data. 2021;8:215. doi: 10.1038/s41597-021-00997-6. PubMed DOI PMC

Compositae Working Group. Global Compositae Database. https://www.compositae.org (2023).

GRIN. Germplasm resource information network. https://www.ars-grin.gov/ (2023).

IUCN. The IUCN Red List of Threatened Species. https://www.iucnredlist.org/ (2023).

Richardson DM, et al. Naturalization and invasion of alien plants: concepts and definitions. Divers. Distrib. 2000;6:93–107. doi: 10.1046/j.1472-4642.2000.00083.x. DOI

van Kleunen M, et al. The Global Naturalized Alien Flora (GloNAF) database. Ecology. 2019;100:e02542. doi: 10.1002/ecy.2542. PubMed DOI

CBD. Alien species that threaten ecosystems, habitats or species. https://www.cbd.int/kb/record/decision/7197?RecordType=decisionSubject=IAS (2000).

IUCN Species Survival Commission (SSC), Invasive Species Specialist Group. Guidelines for the prevention of biodiversity loss caused by alien invasive species. (2000).

CABI. CABI Compendium. CABI Compendium. Wallingford, UK:CAB International. www.cabi.org/isc (2023).

Global Invasive Species Database. GISD. The Global Invasive Species Databasehttp://www.iucngisd.org/gisd/ (2015).

Weber, E. Invasive Plant Species of the World: A Reference Guide to Environmental Weeds(2nd edition)10.1108/rr-06-2017-0133 (2017).

Smith SA, Brown JW. Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot. 2018;105:302–314. doi: 10.1002/ajb2.1019. PubMed DOI

Zanne AE, et al. Three keys to the radiation of angiosperms into freezing environments. Nature. 2014;506:89–92. doi: 10.1038/nature12872. PubMed DOI

Jin Y, Qian H. V.PhyloMaker: an R package that can generate very large phylogenies for vascular plants. Ecography. 2019;42:1353–1359. doi: 10.1111/ecog.04434. PubMed DOI PMC

Yu, G. Data integration, manipulation and visualization of phylogenetic trees. (Chapman and Hall/CRC, 2022).

R Core Team. R: A language and environment for statistical computing. (2022).

Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35:526–528. doi: 10.1093/bioinformatics/bty633. PubMed DOI

Bürkner, P. Estimating Phylogenetic Multilevel Models with BRMS. https://cran.r-project.org/web/packages/brms/vignettes/brms_phylogenetics.html (2021).

Byrnes J. Structural Equation Modeling for Ecology and Evolutionary Biology. https://jebyrnes.github.io/semclass/ (2019).

Guo, K. et al. Plant invasion and naturalization are influenced by genome size, ecology and economic use globally. 10.5281/zenodo.10113291 (2023). PubMed PMC

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