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Limiting similarity and Darwin’s naturalization hypothesis: understanding the drivers of biotic resistance against invasive plant species

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Abstract

Several hypotheses have been proposed to explain biotic resistance of a recipient plant community based on reduced niche opportunities for invasive alien plant species. The limiting similarity hypothesis predicts that invasive species are less likely to establish in communities of species holding similar functional traits. Likewise, Darwin’s naturalization hypothesis states that invasive species closely related to the native community would be less successful. We tested both using the invasive alien Ambrosia artemisiifolia L. and Solidago gigantea Aiton, and grassland species used for ecological restoration in central Europe. We classified all plant species into groups based on functional traits obtained from trait databases and calculated the phylogenetic distance among them. In a greenhouse experiment, we submitted the two invasive species at two propagule pressures to competition with communities of ten native species from the same functional group. In another experiment, they were submitted to pairwise competition with native species selected from each functional group. At the community level, highest suppression for both invasive species was observed at low propagule pressure and not explained by similarity in functional traits. Moreover, suppression decreased asymptotically with increasing phylogenetic distance to species of the native community. When submitted to pairwise competition, suppression for both invasive species was also better explained by phylogenetic distance. Overall, our results support Darwin’s naturalization hypothesis but not the limiting similarity hypothesis based on the selected traits. Biotic resistance of native communities against invasive species at an early stage of establishment is enhanced by competitive traits and phylogenetic relatedness.

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References

  • Abouheif E (1999) A method for testing the assumption of phylogenetic independence in comparative data. Evol Ecol Res 1:895–909

    Google Scholar 

  • Barney JN, Ho MW, Atwater DZ (2016) Propagule pressure cannot always overcome biotic resistance: the role of density-dependent establishment in four invasive species. Weed Res 56:208–218. doi:10.1111/wre.12204

    Article  Google Scholar 

  • Bates DM, Watts DG (1988) Nonlinear regression analysis and its applications. Wiley, New York

    Book  Google Scholar 

  • Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15:899–910. doi:10.1046/j.1420-9101.2002.00472.x

    Article  Google Scholar 

  • Byun C, de Blois S, Brisson J (2013) Plant functional group identity and diversity determine biotic resistance to invasion by an exotic grass. J Ecol 101:128–139. doi:10.1111/1365-2745.12016

    Article  Google Scholar 

  • Byun C, de Blois S, Brisson J (2015) Interactions between abiotic constraint, propagule pressure, and biotic resistance regulate plant invasion. Oecologia 178:285–296. doi:10.1007/s00442-014-3188-z

    Article  PubMed  Google Scholar 

  • Cahill JFJ, Kembel SW, Lamb EG, Keddy PA (2008) Does phylogenetic relatedness influence the strength of competition among vascular plants? Perspect Plant Ecol Evol Syst 10:41–50. doi:10.1016/j.ppees.2007.10.001

    Article  Google Scholar 

  • Conradi T, Kollmann J (2016) Species pools and environmental sorting control different aspects of plant diversity and functional trait composition in recovering grasslands. J Ecol 104:1314–1325. doi:10.1111/1365-2745.12617

    Article  Google Scholar 

  • Daehler C (2001) Darwin’s naturalization hypothesis revisited. Am Nat 158:324–330. doi:10.1086/321316

    Article  CAS  PubMed  Google Scholar 

  • Darwin C (1859) The origin of species. J Murray, London

    Google Scholar 

  • Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. doi:10.1016/s0169-5347(01)02283-2

    Article  Google Scholar 

  • Di Rienzo J, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo C (2013) InfoStat Version 2013. Universidad Nacional de Córdoba, Argentina, InfoStat Group

    Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London

    Book  Google Scholar 

  • Emery SM (2007) Limiting similarity between invaders and dominant species in herbaceous plant communities? J Ecol 95:1027–1035. doi:10.1111/j.1365-2745.2007.01274.x

    Article  Google Scholar 

  • Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. P Natl Acad Sci 100:8916–8920. doi:10.1073/pnas.1033107100

    Article  CAS  Google Scholar 

  • Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081. doi:10.1038/nature05719

    Article  CAS  PubMed  Google Scholar 

  • Funk JL, Cleland EE, Suding KN, Zavaleta ES (2008) Restoration through reassembly: plant traits and invasion resistance. Trends Ecol Evol 23:695–703. doi:10.1016/j.tree.2008.07.013

    Article  PubMed  Google Scholar 

  • Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC, Harris CJ, Licari D (2005) Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett 8:1066–1074. doi:10.1111/j.1461-0248.2005.00809.x

    Article  Google Scholar 

  • Herben T, Goldberg DE (2014) Community assembly by limiting similarity vs. competitive hierarchies: testing the consequences of dispersion of individual traits. J Ecol 102:156–166. doi:10.1111/1365-2745.12181

    Article  Google Scholar 

  • Hooper DU, Dukes JS (2010) Functional composition controls invasion success in a California serpentine grassland. J Ecol 98:764–777. doi:10.1111/j.1365-2745.2010.01673.x

    Article  Google Scholar 

  • Keddy PA, Shipley B (1989) Competitive hierarchies in herbaceous plant communities. Oikos 54:234–241. doi:10.2307/3565272

    Article  Google Scholar 

  • Kiehl K, Kirmer A, Donath TW, Rasran L, Hölzel N (2010) Species introduction in restoration projects—evaluation of different techniques for the establishment of semi-natural grasslands in Central and Northwestern Europe. Basic Appl Ecol 11:285–299. doi:10.1016/j.baae.2009.12.004

    Article  Google Scholar 

  • Kleyer M, Bekker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M, Poschlod P, Van Groenendael JM, Klimeš L, Klimešová J, Klotz S, Rusch GM, Hermy M, Adriaens D, Boedeltje G, Bossuyt B, Dannemann A, Endels P, Götzenberger L, Hodgson JG, Jackel AK, Kühn I, Kunzmann D, Ozinga WA, Römermann C, Stadler M, Schlegelmilch J, Steendam HJ, Tackenberg O, Wilmann B, Cornelissen JHC, Eriksson O, Garnier E, Peco B (2008) The LEDA Traitbase: a database of life-history traits of the Northwest European flora. J Ecol 96:1266–1274. doi:10.1111/j.1365-2745.2008.01430.x

    Article  Google Scholar 

  • Klotz S, Kühn I, Durka W (2002) BIOLFLOR—Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. Bundesamt für Naturschutz, Bonn

    Google Scholar 

  • Kowarik I (2003) Biologische Invasionen. Neophyten und Neozoen in Mitteleuropa. Ulmer, Stuttgart

    Google Scholar 

  • Kraft NJB, Valencia R, Ackerly DD (2008) Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322:580–582. doi:10.1126/science.1160662

    Article  CAS  PubMed  Google Scholar 

  • Kunstler G et al (2012) Competitive interactions between forest trees are driven by species’ trait hierarchy, not phylogenetic or functional similarity: implications for forest community assembly. Ecol Lett 15:831–840. doi:10.1111/j.1461-0248.2012.01803.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Lepŝ J, Doleẑal J, Bezemer TM, Brown VK, Hedlund K, Igual Arroyo M, Jörgensen HB, Lawson CS, Mortimer SR, PeixGeldart A, Rodríguez Barrueco C, Santa Regina I, Ŝmilauer P, van der Putten WH (2007) Long-term effectiveness of sowing high and low diversity seed mixtures to enhance plant community development on ex-arable fields. Appl Veg Sci 10:97–110. doi:10.1111/j.1654-109X.2007.tb00508.x

    Article  Google Scholar 

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. doi:10.1111/j.1461-0248.2004.00657.x

    Article  Google Scholar 

  • Li S-P, Cadotte MW, Meiners SJ, Z-s Hua, H-y Shu, J-t Li, W-s Shu (2015a) The effects of phylogenetic relatedness on invasion success and impact: deconstructing Darwin’s naturalisation conundrum. Ecol Lett 18:1285–1292. doi:10.1111/ele.12522

    Article  PubMed  Google Scholar 

  • Li S-P, Guo T, Cadotte MW, Y-j Chen, J-l Kuang, Z-s Hua, Zeng Y, Song Y, Liu Z, Shu W-S, J-t Li (2015b) Contrasting effects of phylogenetic relatedness on plant invader success in experimental grassland communities. J Appl Ecol 52:89–99. doi:10.1111/1365-2664.12365

    Article  CAS  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. doi:10.1016/j.tree.2005.02.004

    Article  PubMed  Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion Ecology, 2nd edn. Wiley-Blackwell, Oxford

    Google Scholar 

  • Longo G, Seidler TG, Garibaldi LA, Tognetti PM, Chaneton EJ (2013) Functional group dominance and identity effects influence the magnitude of grassland invasion. J Ecol 101:1114–1124. doi:10.1111/1365-2745.12128

    Article  Google Scholar 

  • Lulow ME (2006) Invasion by non-native annual grasses: the importance of species biomass, composition, and time among California native grasses of the Central Valley. Restor Ecol 14:616–626. doi:10.1111/j.1526-100X.2006.00173.x

    Article  Google Scholar 

  • Ma C, Pu Z, Li S-P, Tan J, Liu M, Zhou J, Li H, Jiang L (2016) Different effects of invader—native phylogenetic relatedness on invasion success and impact: a meta-analysis of Darwin’s naturalization hypothesis. Proc R Soc Lond [Biol]. doi:10.1098/rspb.2016.0663

    Google Scholar 

  • MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385. doi:10.2307/2459090

    Article  Google Scholar 

  • Maron J, Marler M (2007) Native plant diversity resists invasion at both low and high resource levels. Ecology 88:2651–2661. doi:10.2307/27651410

    Article  PubMed  Google Scholar 

  • Middleton EL, Bever JD, Schultz PA (2010) The effect of restoration methods on the quality of the restoration and resistance to invasion by exotics. Restor Ecol 18:181–187. doi:10.1111/j.1526-100X.2008.00501.x

    Article  Google Scholar 

  • Miller AL, Diez JM, Sullivan JJ, Wangen SR, Wiser SK, Meffin R, Duncan RP (2013) Quantifying invasion resistance: the use of recruitment functions to control for propagule pressure. Ecology 95:920–929. doi:10.1890/13-0655.1

    Article  Google Scholar 

  • Ordonez A (2014) Functional and phylogenetic similarity of alien plants to co-occurring natives. Ecology 95:1191–1202. doi:10.1890/13-1002.1

    Article  PubMed  Google Scholar 

  • Pearse WD, Purvis A (2013) phyloGenerator: an automated phylogeny generation tool for ecologists. Meth Ecol Evol 4:692–698. doi:10.1111/2041-210X.12055

    Article  Google Scholar 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Price JN, Pärtel M (2013) Can limiting similarity increase invasion resistance? A meta-analysis of experimental studies. Oikos 122:649–656. doi:10.1111/j.1600-0706.2012.00121.x

    Article  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing—R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/. Accessed 23 Nov 2016

  • Rothrock PE, Squiers ER, Sheeley S (1993) Heterogeneity and size of a persistent seedbank of Ambrosia artemisiifolia L. and Setaria faberi Herrm. B Torrey Bot Club 120:417–422. doi:10.2307/2996745

    Article  Google Scholar 

  • Snaydon RW (1991) Replacement or additive designs for competition studies? J Appl Ecol 28:930–946. doi:10.2307/2404218

    Article  Google Scholar 

  • Strauss SY, Webb CO, Salamin N (2006) Exotic taxa less related to native species are more invasive. P Natl Acad Sci 103:5841–5845. doi:10.1073/pnas.0508073103

    Article  CAS  Google Scholar 

  • Symstad AJ (2000) A test of the effects of functional group richness and composition on grassland invasibility. Ecology 81:99–109. doi:10.1890/0012-9658(2000)081[0099:atoteo]2.0.co;2

  • Thuiller W, Gallien L, Boulangeat I, De Bello F, Münkemüller T, Roquet C, Lavergne S (2010) Resolving Darwin’s naturalization conundrum: a quest for evidence. Divers Distrib 16:461–475. doi:10.1111/j.1472-4642.2010.00645.x

    Article  Google Scholar 

  • Török P, Deák B, Vida E, Valkó O, Lengyel S, Tóthmérész B (2010) Restoring grassland biodiversity: sowing low-diversity seed mixtures can lead to rapid favourable changes. Biol Conserv 143:806–812. doi:10.1016/j.biocon.2009.12.024

    Article  Google Scholar 

  • Von Holle B, Simberloff D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86:3212–3218. doi:10.1890/05-0427

    Article  Google Scholar 

  • Weigelt A, Jolliffe P (2003) Indices of plant competition. J Ecol 91:707–720. doi:10.1046/j.1365-2745.2003.00805.x

    Article  Google Scholar 

  • Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159. doi:10.1146/annurev.ecolsys.33.010802.150452

    Article  Google Scholar 

  • Wilsey BJ, Daneshgar PP, Polley HW (2011) Biodiversity, phenology and temporal niche differences between native- and novel exotic-dominated grasslands. Perspect Plant Ecol Evol Syst 13:265–276. doi:10.1016/j.ppees.2011.07.002

    Article  Google Scholar 

  • Wißkirchen R, Haeupler H (1998) Standardliste der Farn- und Blütenpflanzen Deutschlands. Verlag Eugen Ulmer, Stuttgart

    Google Scholar 

  • Young SL, Barney JN, Kyser GB, Jones TS, DiTomaso JM (2009) Functionally similar species confer greater resistance to invasion: implications for grassland restoration. Restor Ecol 17:884–892. doi:10.1111/j.1526-100X.2008.00448.x

    Article  Google Scholar 

  • Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O’Meara BC, Moles AT, Reich PB, Royer DL, Soltis DE, Stevens PF, Westoby M, Wright IJ, Aarssen L, Bertin RI, Calaminus A, Govaerts R, Hemmings F, Leishman MR, Oleksyn J, Soltis PS, Swenson NG, Warman L, Beaulieu JM (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92. doi:10.1038/nature12872

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

F.A.Y. was supported by a scholarship financed by the European Commission through the Erasmus Mundus Arcoiris program, a grant from Dr.-Ing. Leonhard-Lorenz-Foundation, and the Laura Bassi stipend awarded by Technical University of Munich. C.K. received support by the Evangelisches Studienwerk Villigst e.V., and J.M.J. and J.K. were supported by the Deutsche Forschungsgemeinschaft (DFG; JE 288/9-1, KO 1741/3-1). We are grateful to Johann Krimmer and Gerhard Karrer for providing the seed material, Tiffany Knight for her advice on the phylogenetic analysis, and Ingolf Kühn for very helpful comments he made at a conference regarding this study. We acknowledge two anonymous referees for helpful comments on the manuscript. We also thank Timo Conradi, Zoe Palmes, Esteban Aliverti, Patrícia Sperotto, Katie Wolcott, and the representatives of the staff at Greenhouse Laboratory Center Dürnast, Robert Hansel, and Ivonne Jüttner for technical help.

Author contribution statement

FAY and CK conceived and designed the experiments, while JK contributed with suggestions to improve them. FAY and CK collected the data, and FAY performed the statistical analysis and drafted the manuscript after discussions with CK, JMJ, and JK. CK, JMJ, and JK improved the manuscript.

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Correspondence to F. A. Yannelli.

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Communicated by EA Gross.

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Yannelli, F.A., Koch, C., Jeschke, J.M. et al. Limiting similarity and Darwin’s naturalization hypothesis: understanding the drivers of biotic resistance against invasive plant species. Oecologia 183, 775–784 (2017). https://doi.org/10.1007/s00442-016-3798-8

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