Oecologia

, Volume 183, Issue 3, pp 775–784 | Cite as

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

  • F. A. Yannelli
  • C. Koch
  • J. M. Jeschke
  • J. Kollmann
Community ecology – original research

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.

Keywords

Ambrosia artemisiifolia Functional traits Priority effect Propagule pressure Solidago gigantea 

Supplementary material

442_2016_3798_MOESM1_ESM.xlsx (15 kb)
Supplementary material 1 (XLSX 14 kb)
442_2016_3798_MOESM2_ESM.xlsx (18 kb)
Supplementary material 2 (XLSX 18 kb)
442_2016_3798_MOESM3_ESM.docx (96 kb)
The datasets generated during this study are available in the supporting information as supplementary information files. (DOCX 96 kb)

References

  1. Abouheif E (1999) A method for testing the assumption of phylogenetic independence in comparative data. Evol Ecol Res 1:895–909Google Scholar
  2. 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 CrossRefGoogle Scholar
  3. Bates DM, Watts DG (1988) Nonlinear regression analysis and its applications. Wiley, New YorkCrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. Daehler C (2001) Darwin’s naturalization hypothesis revisited. Am Nat 158:324–330. doi:10.1086/321316 CrossRefPubMedGoogle Scholar
  10. Darwin C (1859) The origin of species. J Murray, LondonGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. Di Rienzo J, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo C (2013) InfoStat Version 2013. Universidad Nacional de Córdoba, Argentina, InfoStat GroupGoogle Scholar
  13. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonCrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081. doi:10.1038/nature05719 CrossRefPubMedGoogle Scholar
  17. 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 CrossRefPubMedGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. Keddy PA, Shipley B (1989) Competitive hierarchies in herbaceous plant communities. Oikos 54:234–241. doi:10.2307/3565272 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. Klotz S, Kühn I, Durka W (2002) BIOLFLOR—Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. Bundesamt für Naturschutz, BonnGoogle Scholar
  25. Kowarik I (2003) Biologische Invasionen. Neophyten und Neozoen in Mitteleuropa. Ulmer, StuttgartGoogle Scholar
  26. 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 CrossRefPubMedGoogle Scholar
  27. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefPubMedGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion Ecology, 2nd edn. Wiley-Blackwell, OxfordGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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
  37. MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385. doi:10.2307/2459090 CrossRefGoogle Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. Ordonez A (2014) Functional and phylogenetic similarity of alien plants to co-occurring natives. Ecology 95:1191–1202. doi:10.1890/13-1002.1 CrossRefPubMedGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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
  46. 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 CrossRefGoogle Scholar
  47. Snaydon RW (1991) Replacement or additive designs for competition studies? J Appl Ecol 28:930–946. doi:10.2307/2404218 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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;2Google Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. Von Holle B, Simberloff D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86:3212–3218. doi:10.1890/05-0427 CrossRefGoogle Scholar
  53. Weigelt A, Jolliffe P (2003) Indices of plant competition. J Ecol 91:707–720. doi:10.1046/j.1365-2745.2003.00805.x CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. 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 CrossRefGoogle Scholar
  56. Wißkirchen R, Haeupler H (1998) Standardliste der Farn- und Blütenpflanzen Deutschlands. Verlag Eugen Ulmer, StuttgartGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Chair of Restoration Ecology, Department Ecology and Ecosystem ManagementTechnical University of MunichFreisingGermany
  2. 2.Department of Botany and Zoology, Centre for Invasion BiologyStellenbosch UniversityMatielandSouth Africa
  3. 3.Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB)BerlinGermany
  4. 4.Institute of Biology, Department of Biology, Chemistry, PharmacyFreie Universität BerlinBerlinGermany
  5. 5.Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB)BerlinGermany
  6. 6.Norwegian Institute of Bioeconomy Research (NIBIO)ÅsNorway

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