Biological Invasions

, Volume 19, Issue 12, pp 3601–3611 | Cite as

Understanding the influence of urbanization on invasibility: Carpobrotus edulis as an exemplar

  • Yaiza Lechuga-Lago
  • Ana Novoa
  • Johannes J. Le Roux
  • Luís González


Coastal dune areas are valuable ecosystems, generally impacted by habitat destruction and invasive alien species. In this study, we assessed how human disturbance and invasion by Carpobrotus edulis impact the soils and the establishment of native flora in the north-western coastal regions of Spain. We compared soil characteristics (pH, conductivity, water content, nutrients and enzymatic activities) and native plant as well as C. edulis fitness correlates (germination and early growth) between uninvaded and invaded soils from urban and natural coastal dune areas. We found that human disturbance impacts coastal soils by increasing organic matter and water content, modifying soil nutrients and cycles, and reducing the pH in urban soils. The presence of invasive C. edulis further increases these impacts. These changes in soil characteristics allow for the establishment of the native, but ruderal, Scolymus hispanicus and non-native C. edulis, both of which are not adapted to the typically limiting conditions of coastal dunes. In some instances, the coastal dune endemic, Malcolmia littorea, showed no fitness effects in response to urbanization or the presence of C. edulis. These results suggest that human disturbed coastal areas might be more easily invaded than natural areas. More broadly, our findings of differential responses of different native species to disturbance and invasion, illustrate the need for multi-taxon approaches when assessing the impacts of invasive species.


Enzymatic activities Ecological impacts Germination Invasive species Nutrients Urban areas 



This research was carried out within the frame of the project ‘‘Retos en la gestión de la planta invasora C. edulis. Variabilidad fenotípica y cambios en la relación suelo-planta durante el proceso de invasión’’ (in Spanish), reference CGL2013-48885-C2-1-R, founded by the Ministry of Economy and Competence (Spanish Government). A.N. and J.J.L.R. acknowledge funding from Stellenbosch University’s DST-NRF Centre of Excellence for Invasion Biology. JLR acknowledges funding from South Africa’s National Research Foundation (NRF Grant No. 91117). AN acknowledge funding from the Working for Water Programme of the South African Department of Environmental Affairs, through the South African National Biodiversity Institute Invasive Species Programme and from Centre of Excellence PLADIAS (Czech Science Foundation Project No. 14-36079G) and the long-term research development project (The Czech Academy of Sciences, Project No. RVO 67985939).We also thank Alejandra Guisande Collazo, Alba Ferreiro Martinez for assistance and Flora Alonso Vega and Manoel Lago Vila for valuable insights provided on the extraction of soil nutrients.


  1. Akasaka M, Osawa T, Ikegami M (2015) The role of roads and urban area in occurrence of an ornamental invasive weed: a case of Rudbeckia laciniata L. Urban Ecosyst. doi: 10.1007/s11252-015-0466-4 Google Scholar
  2. Albert ME (1995) Portrait of an invader II: the ecology and management of Carpobrotus edulis. CalEPPC News Spring 95:4–6Google Scholar
  3. Allen SE (1989) Chemical analysis of ecological materials. Blackwell Scientific Publications, HobokenGoogle Scholar
  4. Allison SD, Vitousek PM (2004) Extracellular enzyme activities and carbon chemistry as drivers of tropical plant litter decomposition. Biotropica 36:285–296. doi: 10.1111/j.1744-7429.2004.tb00321.x Google Scholar
  5. Ariza E, Jimenez JA, Sarda R, Villares M, Pinto J, Fraguell R et al (2010) Proposal for an integral quality index for urban and urbanized beaches. Environ Manage 45(5):998–1013Google Scholar
  6. Badalamenti E, Luciano G, Armando LV et al (2016) The impact of Carpobrotus cfr. acinaciformis (L.) L. Bolus on soil nutrients, microbial communities structure and native plant communities in Mediterranean ecosystems. Plant Soil. doi: 10.1007/s11104-016-2924-z Google Scholar
  7. Berendse AF, Lammerts EJ, Olff H, Ecology SP (1998) Soil organic matter accumulation and its implications for nitrogen mineralization and plant species composition during succession in coastal dune slacks reviewed work (s): soil organic matter accumulation and its implications for nitrogen and plant spec. Plant Ecol 137:71–78CrossRefGoogle Scholar
  8. Bot A, Benites J (2005) The importance of soil organic matter: key to drought-resistant soil and sustained food production (No. 80). Food and Agriculture OrganizationGoogle Scholar
  9. Cao C, Jiang S, Ying Z et al (2011) Spatial variability of soil nutrients and microbiological properties after the establishment of leguminous shrub Caragana microphylla lam. plantation on sand dune in the horqin sandy land of northeast china. Ecol Eng 37:1467–1475. doi: 10.1016/j.ecoleng.2011.03.012 CrossRefGoogle Scholar
  10. Carboni M, Carranza ML, Acosta A (2009) Assessing conservation status on coastal dunes: a multiscale approach. Landsc Urban Plan 91:17–25. doi: 10.1016/j.landurbplan.2008.11.004 CrossRefGoogle Scholar
  11. Chiapusio G, Sanchez M, Reigosa MJ et al (1997) Do germination indices adequately reflect allelochemical effects on the germination process? J Chem Ecol 23:2445–2453. doi: 10.1023/B:JOEC.0000006658.27633.15 CrossRefGoogle Scholar
  12. Conser C, Connor EF (2009) Assessing the residual effects of Carpobrotus edulis invasion, implications for restoration. Biol Invasions 11:349–358. doi: 10.1007/s10530-008-9252-z CrossRefGoogle Scholar
  13. D’Antonio CM (2006) Global invasive species database. National Biological Information Infrastructure and Invasive Species Specialist GroupGoogle Scholar
  14. D’Antonio CM, Haubensak K (1998) Community and ecosystem impacts of introduced species. Fremontia 26:13–18Google Scholar
  15. D’Antonio CM, Mahall B (1991) Root profiles and competition between the invasive, exotic perennial, Carpobrotus edulis, and two native shrub species in California coastal scrub. Am J Bot 78:885–894CrossRefGoogle Scholar
  16. D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87CrossRefGoogle Scholar
  17. de la Peña E, de Clercq N, Bonte D et al (2010) Plant-soil feedback as a mechanism of invasion by Carpobrotus edulis. Biol Invasions 12:3637–3648. doi: 10.1007/s10530-010-9756-1 CrossRefGoogle Scholar
  18. Dehnen-Schmutz K, Touza J, Perrings C, Williamson M (2007) A century of the ornamental plant trade and its impact on invasion success. Divers Distrib 13:527–534. doi: 10.1111/j.1472-4642.2007.00359.x CrossRefGoogle Scholar
  19. Everard M, Jones L, Watts B (2010) Have we neglected the societal importance of sand dunes? An ecosystem services perspective. Aquat Conserv Mar Freshw Ecosyst 20:476–487. doi: 10.1002/aqc.1114 CrossRefGoogle Scholar
  20. Feng MH, Shan XQ, Zhang SZ, Wen B (2005) Comparison of a rhizosphere-based method with other one-step extraction methods for assessing the bioavailability of soil metals to wheat. Chemosphere 59:939–949. doi: 10.1016/j.chemosphere.2004.11.056 CrossRefPubMedGoogle Scholar
  21. Foxcroft LC, Richardson DM, Wilson JRU (2008) Ornamental plants as invasive aliens: problems and solutions in Kruger National Park, South Africa. Environ Manag 41:32–51. doi: 10.1007/s00267-007-9027-9 CrossRefGoogle Scholar
  22. Gaertner M, Larson BMH, Irlich UM et al (2016) Managing invasive species in cities: a framework from Cape Town, South Africa? Landsc Urban Plan 151:1–9. doi: 10.1016/j.landurbplan.2016.03.010 CrossRefGoogle Scholar
  23. Gallagher KG, Schierenbeck KA, D’Antonio CM (1997) Hybridization and introgression in Carpobrotus spp. (Aizoaceae) in California, II. Allozyme evidence. Am J Bot 84:905–911CrossRefPubMedGoogle Scholar
  24. García-Mora MR, Gallego-Fernández JB, Williams AT, García-Novo F (2001) A coastal Dune Vulnerability classification: a case study of the SW Iberian Peninsula. J Coast Res 17:802–811Google Scholar
  25. GEIB (2006) TOP 20: Las 20 especies exóticas invasoras más dañinas presentes en EspañaGoogle Scholar
  26. German DP, Chacon SS, Allison SD (2011) Substrate concentration and enzyme allocation can affect rates of microbial decomposition. Ecology 92:1471–1480. doi: 10.1890/10-2028.1 CrossRefPubMedGoogle Scholar
  27. Grime JP (1997) Ecology: biodiversity and ecosystem function: the Debate Deepens. Science (80-) 277:1260–1261CrossRefGoogle Scholar
  28. Grootjans AP, Adema EB, Bekker RM, Lammerts EJ (2004) Why coastal dune slacks sustain a high biodiversity. In: Martínez ML, Psuty NP (eds) Coastal dunes: ecology and conservation (Ecological Studies 171). Springer, Berlin, pp 85–101Google Scholar
  29. Guitián F, Carballas T (1976) Ténicas de análisis de suelos. Pico Sacro, Santiago de compostelaGoogle Scholar
  30. Jiménez JA, Gracia V, Valdemoro HI et al (2011) Managing erosion-induced problems in NW Mediterranean urban beaches. Ocean Coast Manag 54:907–918. doi: 10.1016/j.ocecoaman.2011.05.003 CrossRefGoogle Scholar
  31. Kachi N, Hiros T (1983) Limiting nutrients for plant growth in coastal sand dune soils. J Ecol 71:937–944CrossRefGoogle Scholar
  32. Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72. doi: 10.1007/BF00257924 CrossRefGoogle Scholar
  33. Klotz S, Kühn I (2010) Urbanisation and alien invasion. In: Gaston KJ (ed) Urban ecology. Cambridge University Press, Cambridge, pp 120–133CrossRefGoogle Scholar
  34. Kowarik I (2011) Novel urban ecosystems, biodiversity, and conservation. Environ Pollut 159:1974–1983. doi: 10.1016/j.envpol.2011.02.022 CrossRefPubMedGoogle Scholar
  35. Lechuga-Lago Y, Sixto-Ruiz M, Roiloa SR, González L (2016) Clonal integration facilitates the colonization of drought environments by plant invaders. AoB Plant 8:1–11. doi: 10.1093/aobpla/plw023 CrossRefGoogle Scholar
  36. Martínez ML, Maun AM, Psuty NP (2004a) The fragility and conservation of the world’s coastal dunes: geomorphological, ecological, and socioeconomic perspectives. In: Martínez ML, Psuty N (eds) Coastal dunes: ecology and conservation. Springer, Berlin, pp 355–370Google Scholar
  37. Martínez ML, Psuty NP, Lubke RA (2004b) A perspective on coastal dunes. In: Coast dunes, ecology and conservation. Ecolog, vol 171, 3–10. doi:  10.1007/978-3-540-74002-5_1
  38. Maun MA (1994) Adaptations enhancing survival and establishment of seedlings on coastal dune systems. Vegetatio 111:59–70. doi: 10.2307/20046398 Google Scholar
  39. Maun MA (2009) The biology of coastal sand dunes. Oxford University Press, OxfordGoogle Scholar
  40. Millenium Ecosystem Assessment (2005) Ecosystems and human well-being. Synthesis. Island Press, WashingtonGoogle Scholar
  41. Nobis MP, Jaeger JAG, Zimmermann NE (2009) Neophyte species richness at the landscape scale under urban sprawl and climate warming. Divers Distrib 15:928–936CrossRefGoogle Scholar
  42. Novoa A, González L (2014) Impacts of Carpobrotus edulis (L.) N.E.Br. on the germination, establishment and survival of native plants: a clue for assessing its competitive strength. PLoS ONE 9:e107557. doi: 10.1371/journal.pone.0107557 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Novoa A, González L, Moravcová L, Pyšek P (2012) Effects of soil characteristics, allelopathy and frugivory on establishment of the invasive plant Carpobrotus edulis and a co-occuring native, Malcolmia littorea. PLoS ONE. doi: 10.1371/journal.pone.0053166 Google Scholar
  44. Novoa A, González L, Moravcová L, Pyšek P (2013a) Constraints to native plant species establishment in coastal dune communities invaded by Carpobrotus edulis: Implications for restoration. Biol Conserv 164:1–9. doi: 10.1016/j.biocon.2013.04.008 CrossRefGoogle Scholar
  45. Novoa A, Rodríguez R, Richardson D, González L (2013b) Soil quality: a key factor in understanding plant invasion? The case of Carpobrotus edulis (L.) N.E.Br. Biol Invasions 16:429–443. doi: 10.1007/s10530-013-0531-y CrossRefGoogle Scholar
  46. Olff H, Huisman J, Van Tooren B (1993) Species dynamics and nutrient accumulation during early primary succession in coastal sand dunes. J Ecol 81:693–706. doi: 10.2307/2261667 CrossRefGoogle Scholar
  47. Posmyk MM, Bałabusta M, Wieczorek M et al (2009) Melatonin applied to cucumber (Cucumis sativus L.) seeds improves germination during chilling stress. J Pineal Res 46:214–223. doi: 10.1111/j.1600-079X.2008.00652.x CrossRefPubMedGoogle Scholar
  48. Pyšek P, Richardson DM, Pergl J et al (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23:237–244. doi: 10.1016/j.tree.2008.02.002 CrossRefPubMedGoogle Scholar
  49. Richardson DM, Pyšek P (2004) What is an invasive species ? Crop Prot Compend. doi: 10.1111/j.1366-9516.2004.00096.x Google Scholar
  50. Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species—a global review. Divers Distrib 17:788–809. doi: 10.1111/j.1472-4642.2011.00782.x CrossRefGoogle Scholar
  51. Rousset O, Lepart J (2000) Positive and negative interactions at different life stages of a colonizing species (Quercus humilis). J Ecol 88:401–412. doi: 10.1046/j.1365-2745.2000.00457.x CrossRefGoogle Scholar
  52. Santoro R, Jucker T, Carboni M, Acosta ATR (2012) Patterns of plant community assembly in invaded and non-invaded communities along a natural environmental gradient. J Veg Sci 23:483–494. doi: 10.1111/j.1654-1103.2011.01372.x CrossRefGoogle Scholar
  53. Schemske DW, Husband BC, Ruckelshaus MH et al (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75:584–606CrossRefGoogle Scholar
  54. Staudhammer CL, Escobedo FJ, Holt N et al (2015) Predictors, spatial distribution, and occurrence of woody invasive plants in subtropical urban ecosystems. J Environ Manag 155:97–105. doi: 10.1016/j.jenvman.2015.03.012 CrossRefGoogle Scholar
  55. Sullivan J, Timmins S, Williams PA (2005) Movement of exotic plants into coastal native forests from gardens in northern New Zealand. N Z J Ecol 29:1–10Google Scholar
  56. Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307. doi: 10.1016/0038-0717(69)90012-1 CrossRefGoogle Scholar
  57. Thuiller W, Richardson DM, Py Ek P et al (2005) Niche-based modelling as a tool for predicting the risk of alien plant invasions at a global scale. Glob Change Biol 11:2234–2250. doi: 10.1111/J.1365-2486.2005.01018.X CrossRefGoogle Scholar
  58. Tutin T, Heywood V, Burges N et al (1993) Flora Europaea. Cambridge Univ Press, CambridgeGoogle Scholar
  59. Ungar IA (1978) Halophyte seed germination. Bot Rev 44:233–264CrossRefGoogle Scholar
  60. Van der Watt E, Pretorius JC (2001) Purification and identification of active antibacterial components in Carpobrotus edulis L. J Ethnopharmacol 76:87–91. doi: 10.1016/S0378-8741(01)00197-0 CrossRefPubMedGoogle Scholar
  61. Wang WS, Shan XQ, Wen B, Zhang SZ (2003) Relationship between the extractable metals from soils and metals taken up by maize roots and shoots. Chemosphere 53:523–530. doi: 10.1016/S0045-6535(03)00518-6 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Yaiza Lechuga-Lago
    • 1
  • Ana Novoa
    • 2
    • 3
    • 4
  • Johannes J. Le Roux
    • 2
  • Luís González
    • 1
  1. 1.Laboratorio de investigación nº 21, Ecofisioloxia, Departamento de Bioloxía Vexetal e Ciencias do Solo, Edificio de Ciencias ExperimentaisUniversity of VigoVigo, PontevedraSpain
  2. 2.Department of Botany and Zoology, Centre for Invasion BiologyStellenbosch UniversityMatielandSouth Africa
  3. 3.Invasive Species Programme, South African National Biodiversity InstituteKirstenbosch Research CentreClaremontSouth Africa
  4. 4.Department of Invasion Ecology, Institute of BotanyThe Czech Academy of SciencesPrůhoniceCzech Republic

Personalised recommendations