Biological Invasions

, Volume 12, Issue 7, pp 2117–2130 | Cite as

Weak effects of the exotic invasive Carpobrotus edulis on the structure and composition of Portuguese sand-dune communities

  • Sara Maltez-Mouro
  • Fernando T. Maestre
  • Helena Freitas
Original Paper


Sand dune ecosystems have a high conservation value worldwide, but they are highly threatened by exotic plant invasion. We investigated the impacts of the exotic invasive species Carpobrotus edulis on the composition and structure (spatial pattern, total cover, species diversity and species co-occurrence) of native sand dune communities in the western coast of Portugal. We studied eight sites following a north-south gradient; in each site we established 8–10 transects of 25 contiguous quadrats of one square meter. C. edulis had a significantly clumped pattern in five of the study sites, which, however, was not related to the spatial pattern of native species. The effects of climate on the community structure variables were on average three times stronger than those of C. edulis. This species also had small effects on the floristic composition of native species. Our results indicate that the success and impacts of C. edulis are habitat-dependent and context-specific. They also provide evidence of a strong resilience to the impacts of invasion in the studied sand dune ecosystems: C. edulis did not reach large abundances or exert negative impacts on native communities to the extent expected. These ecosystems provide a unique opportunity to increase our understanding on the origin of impacts by invasive species, and on how particular communities resist the impacts of an invader.


Abiotic gradients Ecosystem structure Species composition Invasion impacts 



Structural equation modeling


Standardized effect sizes



“We thank Ana Mouro and João Mouro for their help with the field-work, and we thank Matthew A. Bowker and Adrián Escudero for their help with the statistical analyses. We also thank to anonymous referees who helped improve the paper. SMM was supported by grant SFRH/BPD/39744/2007, given by the European Social Funds of the Portuguese Foundation for Science and Technology, Ministry of Sciences and High Education. FTM was supported by a Ramón y Cajal contract from the Spanish Ministerio de Ciencia e Innovación (MCINN), co-funded by the European Social Fund, by the Fundación BBVA (BIOCON06/105 project), by the British Ecological Society (Studentship 231/1975), by the Comunidad de Madrid (grant S-0505/AMB/0335), and by the MCINN (grant CGL2008-00986-E/BOS).”


  1. Albert ME (1995) Portrait of an invader II: the ecology and management of Carpobrotus edulis. CalEPPC News. Spring 1995Google Scholar
  2. Albert ME, D’Antonio CM, Schierenbeck KA (1997) Hybridization and introgression in Carpobrotus spp. (Aizoaceae) in California. I. Morphological evidence. Am J Bot 84(7):896–904CrossRefGoogle Scholar
  3. Almeida JD, Freitas H (2001) The exotic and invasive flora of Portugal. Bot Compl 25:317–327Google Scholar
  4. Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspect Plant Ecol 3:52–66CrossRefGoogle Scholar
  5. Alvarez ME, Cushman JH (2002) Community-level consequences of a plant invasion: effects on three habitats in coastal California. Ecol Appl 12:1434–1444CrossRefGoogle Scholar
  6. Amos (2003) Amos Version 5.0.1. James L. Arbuckle. SmallWaters Corp., ChicagoGoogle Scholar
  7. Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  8. Borcard D, Legendre P (2004) SpaceMaker2—user’s guide. Département de sciences biologiques. Université de Montréal, CanadaGoogle Scholar
  9. Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73(3):1045–1055CrossRefGoogle Scholar
  10. Burke MJW, Grime JP (1996) An experimental study of plant community invisibility. Ecology 77:776–790CrossRefGoogle Scholar
  11. Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasions. Oecologia 130:146–156Google Scholar
  12. Campelo F, Marchante H, Freitas H (1999) Ecology and population dynamics of the invasive exotic species Carpobrotus edulis in the Portugese sandy coast. Proceedings 5th international conference on the ecology of invasive alien plants. 13–16 October 1999. La Maddalena, Sardinia, ItalyGoogle Scholar
  13. Coleman HM, Levine JM (2007) Mechanisms underlying the impacts of exotic annual grasses in a coastal California meadow. Biol Inv 9:65–71CrossRefGoogle Scholar
  14. Collins B, Wein GR (1993) Competition between native and immigrant Polygonum congeners. Can J Bot 71:939–945Google Scholar
  15. Colwell RK (1994–2004) EstimateS: statistical estimation of species richness and shared species from samples. http://,
  16. Conser C, Connor EF (2009) Assessing the residual effects of Carpobrotus edulis invasion, implications for restoration. Biol Inv 11:349–358CrossRefGoogle Scholar
  17. D’Antonio CM (1993) Mechanisms controlling invasion of coastal plant communities by the alien succulent Carpobrotus edulis. Ecology 74:83–95CrossRefGoogle Scholar
  18. D’Antonio CM (2006) Global invasive species database ( National Biological Information Infrastructure (NBII) & IUCN/SSC Invasive Species Specialist Group (ISSG)
  19. D’Antonio CM, Haubensak K (1998) Community and ecosystem impacts of introduced species. Fremontia 26:13–18Google Scholar
  20. D’Antonio CM, Mahall BE (1991) Root profiles and competition between the invasive, nonindigenous perennial, Carpobrotus edulis (Aizoaceae), in coastal strand communities of central California. J Appl Ecol 27:693–702Google Scholar
  21. D’Antonio CM, Vitousek PM (1992) Biological invasions by nonindigenous grasses, the grass/fire cycle, and global change. Ann Rev Ecol Syst 23:63–87Google Scholar
  22. D’Antonio CM, Dudley TL, Mack M (1999) Disturbance and biological invasions: direct effects and feedbacks. Submitted for ecosystems of disturbed ground. Walker L (ed) Elsevier PressGoogle Scholar
  23. Dullinger S, Kleinbauer I, Pauli H, Gottfried M, Brooker R, Nagy L, Theurillat J-P, Holten JI, Abdaladze O, Benito J-L, Borel J-L, Coldea G, Ghosn D, Kanka R, Merzouki A, Klettner C, Moiseev P, Molau U, Reiter K, Rossi G, Stanisci A, Tomaselli M, Unterlugauer P, Vittoz P, Grabherr G (2007) Weak and variable relationships between environmental severity and small-scale co occurrence in alpine plant communities. J Ecol 95:1284–1295CrossRefGoogle Scholar
  24. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  25. Franco JA (1971–1984) Nova Flora de Portugal (Continente e Açores). Vol. I–II. Franco JA (ed) Escolar Editora, LisboaGoogle Scholar
  26. Franco JA, Afonso MLR (1994) Nova Flora de Portugal (Continente e Açores). Vol. III (Fascículos I-II). Escolar Editora, LisboaGoogle Scholar
  27. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081CrossRefPubMedGoogle Scholar
  28. Going BM, Hillerislambers J, Levine JM (2009) Abiotic and biotic resistance to grass invasion in serpentine annual plant communities. Oecologia 159:839–847Google Scholar
  29. Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621CrossRefGoogle Scholar
  30. Gotelli NJ, Entsminger GL (2003) Swap algorithms in null model analysis. Ecology 84:532–535CrossRefGoogle Scholar
  31. Gould AMA, Gorchov DL (2000) Effects of the exotic invasive shrub Lonicera maackii on the survival and fecundity of three species of native annuals. Am Midl Nat 144:36–50CrossRefGoogle Scholar
  32. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  33. Gritti ES, Smith B, Sykes MT (2006) Vulnerability of Mediterranean Basin ecosystems to climate change and invasion by exotic plant species. J Biogeogr 33:145–157CrossRefGoogle Scholar
  34. Hager HA (2004) Competitive effect versus competitive response of invasive and native wetland plant species. Oecologia 139:140–149CrossRefPubMedGoogle Scholar
  35. Hamilton JG, Holzapfel C, Mahall BE (1999) Coexistence and interference between native perennial grass and non-native annual grasses in California. Oecologia 121:518–526CrossRefGoogle Scholar
  36. Henriques RPB, Hay JD (1992) Nutrient content, correlation with ecological factors and the structure of plant communities in a tropical beach-dune system. Acta Oecol Int J Ecol 13:101–117Google Scholar
  37. Hobbs RJ, Hobbs LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337CrossRefGoogle Scholar
  38. Hutchinson TF, Vankat JL (1997) Invasibility and effects of Amur honeysuckle in southwestern Ohio forests. Conserv Biol 11:1117–1124CrossRefGoogle Scholar
  39. Iriondo JM, Albert MJ, Escudero A (2003) Structural equation modelling: an alternative for assessing causal relationships in threatened plant populations. Biol Conserv 113:367–377CrossRefGoogle Scholar
  40. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  41. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989CrossRefGoogle Scholar
  42. Lortie CJ, Cushman H (2007) Effects of a directional abiotic gradient on plant community dynamics and invasion in a coastal dune system. J Ecol 95:468–481CrossRefGoogle Scholar
  43. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710Google Scholar
  44. Maestre FT, Martínez I, Escolar C, Escudero A (2009) On the relationship between abiotic stress and co-occurrence patterns: an assessment at the community level using soil lichen communities and multiple stress gradients. Oikos 118:1015–1022CrossRefGoogle Scholar
  45. Meiners SJ (2007) Apparent competition: an impact of exotic shrub invasion on tree regeneration. Biol Inv 9:849–855CrossRefGoogle Scholar
  46. Ninyerola M, Pons X, Roure JM (2005) Atlas climático digital de la Península Ibérica. Metodología y aplicaciones enbioclimatología y geobotánica. Universidad Autónoma de Barcelona, Barcelona. Maps available online:
  47. Økland RH, Eilertsen O (1994) Canonical correspondence analysis with variation partitioning: some comments and an application. J Veg Sci 5:117–126CrossRefGoogle Scholar
  48. Perry JN (1998) Measures of spatial patterns for counts. Ecology 79:1008–1017CrossRefGoogle Scholar
  49. Perry JN, Dixon PM (2002) A new method to measure spatial association for ecological count data. Ecoscience 9:133–141Google Scholar
  50. Perry JN, Winder L, Holland JM, Alston RD (1999) Red-blue plots for detecting clusters in count data. Ecol Lett 2:106–113CrossRefGoogle Scholar
  51. Perry JN, Liebhold AM, Rosenberg MS, Dungan J, Miriti M, Jakomulska A, Citron-Pousty S (2002) Illustrations and guidelines for selecting statistical methods for quantifying spatial pattern in ecological data. Ecography 25:578–600CrossRefGoogle Scholar
  52. Prieur-Richard A-H, Lavorel S, Linhart YB, Santos A (2002) Plant diversity, herbivory, and resistance of a plant community to invasion in Mediterranean annual communities. Oecologia 130:96–104Google Scholar
  53. Reichard SH (1997) Predicting invasions of woody plants introduced into North America. Conserv Biol 11:193–202CrossRefGoogle Scholar
  54. Reinhart KO, Maestre FT, Callaway RM (2006) Facilitation and inhibition of seedlings of an invasive tree (Acer platanoides) by different tree species in a mountain ecosystem. Biol Inv 8:231–240CrossRefGoogle Scholar
  55. SADIE (2001) SADIEShell Version 1.22. Kelvin F. Conrad and IACR-Rothamsted.
  56. Sax DF, Gaines SD (2008) Species invasions and extinction: the future of native biodiversity on islands. Proc Natl Acad Sci USA 105:11490–11497Google Scholar
  57. Schork MA, Remington RD (2000) Statistics with applications to the biological and health sciences. Prentice-Hall Inc., USAGoogle Scholar
  58. Shipley B (2002) Cause and correlation in biology: a user’s guide to path analysis. structural equations and causal inference. Cambridge University Press, CambridgeGoogle Scholar
  59. Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Front Ecol Envir 3:12–20CrossRefGoogle Scholar
  60. StatSoft, Inc. (2001) STATISTICA (data analysis software system), version 6.
  61. Suehs CM, Affre L, Medail F (2004) Invasion dynamics of two alien Carpobrotus (Aizoaceae) taxa on a Mediterranean island: I. Genetic diversity and introgression. Heredity 92:31–40CrossRefPubMedGoogle Scholar
  62. ter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167–1179CrossRefGoogle Scholar
  63. ter Braak C, Smilauer P (2002) Canoco for Windows, v.4.5. Center for Biometry, WageningenGoogle Scholar
  64. Thomson D (2005) Measuring the effects of invasive species on the demography of a rare endemic plant. Biol Inv 7:615–624CrossRefGoogle Scholar
  65. Thuiller W, Lavorel S, Araújo MB, Sykes MT, Prentice C (2005) Climate change threats to plant diversity in Europe. Proc Natl Acad Sci USA 102:8245–8250CrossRefPubMedGoogle Scholar
  66. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630CrossRefPubMedGoogle Scholar
  67. Traveset A, Moragues E, Valladares F (2008) Spreading of the invasive Carpobrotus spp. in Mediterranean ecosystems: the advantage of performing well in different light environments. Appl Veg Sci 11:45–54CrossRefGoogle Scholar
  68. Vilà M, D’Antonio CM (1998) Fruit choice and seed dispersal of invasive vs. noninvasive Carpobrotus (Aizoaceae) in coastal California. Ecology 79:1053–1060Google Scholar
  69. Vilà M, Tessier M, Suehs CM, Brundu G, Carta L, Galanidis A, Lambdon P, Manca M, Médail F, Moragues E, Traveset A, Troumbis AY, Hulme PE (2006) Local and regional assessments of the impacts of plant invaders on vegetation structure and soil properties of Mediterranean islands. J Biogeogr 33:853–861CrossRefGoogle Scholar
  70. Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Weswtbrooks R (1997) Introduced species: a significant component of human-caused global change. NZ J Ecol 21:1–16Google Scholar
  71. Vivrette NJ, Muller CH (1977) Mechanism of invasion and dominanace of coastalgrassland by Mesembyranthemum crystallinum. Ecol Monogr 47:301–318CrossRefGoogle Scholar
  72. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefPubMedGoogle Scholar
  73. Williamson M (1999) Invasions. Ecography 22:5–12CrossRefGoogle Scholar
  74. Winder L, Alexander CJ, Holland JM, Woolley C, Perry JN (2001) Modelling the dynamic spatio-temporal response of predators to transient prey patches in the field. Ecol Lett 4:568–576CrossRefGoogle Scholar
  75. Wiser SK, Allen RB, Clinton PW, Platt KH (1998) Community structure and forest invasion by an exotic herb over 23 years. Ecology 79:2071–2081CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Sara Maltez-Mouro
    • 1
  • Fernando T. Maestre
    • 2
  • Helena Freitas
    • 1
  1. 1.Centre for Functional Ecology, Departamento de Botânica, Faculdade de Ciências e TecnologiaUniversidade de CoimbraCoimbraPortugal
  2. 2.Área de Biodiversidad y Conservación, Departamento de Biología y GeologíaUniversidad Rey Juan CarlosMóstolesSpain

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