, Volume 16, Issue 4, pp 678–693 | Cite as

Using Life Strategies to Explore the Vulnerability of Ecosystem Services to Invasion by Alien Plants

  • Joana R. VicenteEmail author
  • Ana T. Pinto
  • Miguel B. Araújo
  • Peter H. Verburg
  • Angela Lomba
  • Christophe F. Randin
  • Antoine Guisan
  • João P. Honrado


Invasive plants can have different effects on ecosystem functioning and on the provision of ecosystem services, with the direction and magnitude of such effects depending on the service and ecosystem being considered, but also on the life strategies of the invaders. Strategies can influence invasiveness, but also key processes of host ecosystems. To address the combined effects of these various factors, we developed a methodological framework to identify areas of possible conflict between ecosystem services and alien invasive plants, considering interactions between landscape invasibility and species invasiveness. Our framework combines multi-model inference, efficient techniques to map ecosystem services, and life strategies. The latter provides a functional link between invasion, functional changes, and potential provision of services by invaded ecosystems. The framework was applied to a region in Portugal, for which we could successfully predict current patterns of plant invasion, of ecosystem service provision, and of potential conflict between alien species richness and the potential provision of selected services. Potential conflicts were identified for all combinations of plant strategy and ecosystem service, with an emphasis on carbon sequestration, water regulation, and wood production. Lower levels of conflict were obtained between invasive plant strategies and the habitat for biodiversity supporting service. The value of the proposed framework for landscape management and planning is discussed with emphasis on anticipation of conflicts, mitigation of negative impacts, and facilitation of positive effects of plant invasions on ecosystems and their services.

Key words

ecosystem services life strategies CSR Grime alien invasive plants multi-model inference ecosystem services mapping spatial conflict 



The authors would like to express their gratitude to Henrique Miguel Pereira for his valuable contribution throughout the development of this research. This study was financially supported by the Portuguese Foundation for Science and Technology through PhD Grant SFRH/BD/40668/2007 to J. R. Vicente. A. Lomba benefited support by the Portuguese Foundation for Science and Technology through Post-Doctoral Grant SFRH/BPD/80747/2011. J. P. Honrado benefited support from FCT through Project PTDC/AGR-AAM/104819/2008 (ECOSENSING). C. F. Randin benefitted support from the European Research Council (ERC) through project TREELIM. A. Guisan received support from the Swiss National Centre of Competence in Research “Plant Survival”. M. B. Araújo acknowledges support from the ‘Rui Nabeiro’ Chair on Biodiversity, the Spanish Research Council, and the Danish NSF for support of his research.

Supplementary material

10021_2013_9640_MOESM1_ESM.docx (75 kb)
Supplementary material 1 (DOCX 74 kb)


  1. AFN. 2010. Inventário Florestal Nacional, Portugal continental, 2005–2006. Lisboa: Autoridade Florestal Nacional.Google Scholar
  2. Alagador D, João Martins M, Cerdeira JO, Cabeza M, Araújo MB. 2011. A probabilistic-based approach to match species with reserves when data are at different resolutions. Biol Conserv 144:811–20.CrossRefGoogle Scholar
  3. Alpert P, Bone E, Holzapfel C. 2000. Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspectives in Plant Ecology Evolution and Systematics 3:52–66.CrossRefGoogle Scholar
  4. Araújo MB, Guisan A. 2006. Five (or so) challenges for species distribution modelling. J Biogeogr 33:1677–88.CrossRefGoogle Scholar
  5. Araújo MB, Alagador D, Cabeza M, Nogués Bravo D, Thuiller W. 2011. Climate change threatens European conservation areas. Ecol Lett 14:484–92.PubMedCrossRefGoogle Scholar
  6. Arévalo JR, Delgado JD, Otto R, Naranjo A, Salas M, Fernandez-Palacios JM. 2005. Distribution of alien vs. native plant species in roadside communities along an altitudinal gradient in Tenerife and Gran Canaria (Canary Islands). Perspectives in Plant Ecology Evolution and Systematics 7:185–202.CrossRefGoogle Scholar
  7. Baselga A, Araújo MB. 2009. Individualistic vs. community modelling of species distributions under climate change. Ecography 32:55–65.CrossRefGoogle Scholar
  8. Bennett EM, Peterson GD, Gordon LJ. 2009. Understanding relationships among multiple ecosystem services. Ecol Lett 12:1394–404.PubMedCrossRefGoogle Scholar
  9. Brauman KA, Daily GC, Duarte TK, Mooney HA. 2007. The nature and value of ecosystem services: an overview highlighting hydrologic services. Annu Rev Environ Resour 32:67–98.CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR. 2002. Model selection and multi model inference: a practical information-theoretic approach. New York: Springer.Google Scholar
  11. Charles H, Dukes JS. 2007. Impacts of invasive species on ecosystem services biological invasions. In: Nentwig W, Caldwell MM, Heldmaier G, Jackson RB, Lange OL, Mooney HA, Schulze ED, Sommer U, Eds. Impacts of invasive species on ecosystem services biological invasions. Berlin: Springer. p 217–37.Google Scholar
  12. Chytrý M, Maskell L, Pino J, Pyšek P, Vilà M, Font X, Smart S. 2008. Habitat invasions by alien plants: a quantitative comparison among Mediterranean, subcontinental and oceanic regions of Europe. J Appl Ecol 45:448–58.CrossRefGoogle Scholar
  13. Civantos E, Thuiller W, Luigi M, Guisan A, Araújo MB. 2012. Potential impacts of climate change on ecosystem services in Europe: the case of pest control. Bioscience 62:658–66.CrossRefGoogle Scholar
  14. Coomes DA, Allen RB. 2007. Effects of size, competition and altitude on tree growth. J Ecol 95:1084–97.CrossRefGoogle Scholar
  15. Crowl TA, Crist TO, Parmenter RR, Belovsky G, Lugo AE. 2008. The spread of invasive species and infectious disease as drivers of ecosystem change. Front Ecol Environ 6:238–46.CrossRefGoogle Scholar
  16. DGSFA. 1969. Tabelas de Volume. Lisboa: Direcção-Geral dos Serviços Florestais e Aquícolas.Google Scholar
  17. Duarte C, Ribeiro E, Cosme J. 1991. Yield tables for pinheiro bravo (Pinus pinaster). DGF Informação 2:23–5.Google Scholar
  18. Dufour A, Gadallah F, Wagner HH, Guisan A, Buttler A. 2006. Plant species richness and environmental heterogeneity in a mountain landscape: effects of variability and spatial configuration. Ecography 29:573–84.CrossRefGoogle Scholar
  19. Dukes JS. 2011. Responses of invasive species to a changing climate and atmosphere. In: Richardson DM, Ed. Fifty years of invasion ecology: the legacy of Charles Elton. Oxford: Blackwell Publishing. p 345–57.Google Scholar
  20. Dukes JS, Mooney HA. 2004. Disruption of ecosystem processes in western North America by invasive species. Revista chilena de historia natural 77:411–37.CrossRefGoogle Scholar
  21. Dye P, Jarmain C. 2004. Water use by black wattle (Acacia mearnsii): implications for the link between removal of invading trees and catchment streamflow response. S Afr J Sci 100:40–4.Google Scholar
  22. Ehrenfeld JG. 2003. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–23.CrossRefGoogle Scholar
  23. Ehrenfeld JG. 2010. Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80.CrossRefGoogle Scholar
  24. Euliss NH Jr, Smith LM, Liu S, Duffy WG, Faulkner SP, Gleason RA, Eckles SD. 2011. Integrating estimates of ecosystem services from conservation programs and practices into models for decision makers. Ecol Appl 21:128–34.CrossRefGoogle Scholar
  25. Gebremichael M, Barros AP. 2006. Evaluation of MODIS gross primary productivity (GPP) in tropical monsoon regions. Remote Sens Environ 100:150–66.CrossRefGoogle Scholar
  26. Gerlach JDG Jr. 2004. The impacts of serial land-use changes and biological invasions on soil water resources in California, USA. J Arid Environ 57:365–79.CrossRefGoogle Scholar
  27. Godoy O, Richardson DM, Valladares F, Castro-Díez P. 2009. Flowering phenology of invasive alien plant species compared with native species in three Mediterranean-type ecosystems. Ann Bot 103:485–94.PubMedCrossRefGoogle Scholar
  28. Goodwin BJ, McAllister AJ, Fahrig L. 1999. Predicting invasiveness of plant species based on biological information. Conserv Biol 13:422–6.CrossRefGoogle Scholar
  29. Gorgens AHM, Van Wilgen BW. 2004. Invasive alien plants and water resources in South Africa: current understanding, predictive ability and research challenges. S Afr J Sci 100:27–33.Google Scholar
  30. Grime JP. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–94.CrossRefGoogle Scholar
  31. Grotkopp E, Rejmanek M, Rost TL. 2002. Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. Amer Nat 159:396–419.Google Scholar
  32. Guisan A, Zimmermann N. 2000. Predictive habitat distribution models in ecology. Ecol Model 135:147–86.CrossRefGoogle Scholar
  33. Hirzel A, Guisan A. 2002. Which is the optimal sampling strategy for habitat suitability modelling. Ecol Model 157:331–41.CrossRefGoogle Scholar
  34. Holmes PM, Richardson DM, Esler KJ, Witkowski ETF, Fourie S. 2005. A decision-making framework for restoring riparian zones degraded by invasive alien plants in South Africa. S Afr J Bot 101:553–64.Google Scholar
  35. Honrado J, Vicente J, Lomba A, Alves P, Macedo JA, Henriques R, Granja H, Caldas FB. 2010. Fine-scale patterns of vegetation assembly in the monitoring of changes in coastal sand-dune landscapes. Web Ecol 9:82–95.Google Scholar
  36. Keeley JE, Baer-Keeley M, Fotheringham CJ. 2005. Alien plant dynamics following fire in Mediterranean-climate California shrublands. Ecol Appl 15:2109–25.CrossRefGoogle Scholar
  37. Le Maitre DC, Richardson DM, Chapman RA. 2004. Alien plant invasions in South Africa: driving forces and the human dimension. S Afr J Sci 100:103–12.Google Scholar
  38. Levine JM, Vilà M, Antonio CMD, Dukes JS, Grigulis K, Lavorel S. 2003. Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond Ser B 270:775–81.CrossRefGoogle Scholar
  39. Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B. 2008. Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–14.PubMedCrossRefGoogle Scholar
  40. Lomba A, Pellissier L, Randi C, Vicente J, Moreira F, Honrado J, Guisan A. 2010. Overcoming the rare species modelling paradox: a novel hierarchical framework applied to an Iberian endemic plant. Biol Conserv 143:2647–57.CrossRefGoogle Scholar
  41. Marco DE, Montemurro MA, Cannas SA. 2011. Comparing short and long-distance dispersal: modelling and field case studies. Ecography 34:671–82.CrossRefGoogle Scholar
  42. Metzger MJ, Rounsevell MDA, Acosta-Michlik L, Leemands R, Schöter D. 2006. The vulnerability of ecosystem services to land use change. Agric Ecosyst Environ 114:69–85.CrossRefGoogle Scholar
  43. Meyerson LA, Baron J, Melillo JM, Naiman RJ, O’Malley RI, Orians G, Palmer MA, Pfaff ASP, Running SW, Sala OE. 2005. Aggregate measures of ecosystem services: can we take the pulse of nature? Front Ecol Environ 3:56–9.CrossRefGoogle Scholar
  44. Millennium Ecosystem Assessment (MA). 2005. Ecosystems and human well-being: synthesis. Washington, DC: Island Press.Google Scholar
  45. Nelson E, Mendoza G, Regetz J, Polasky S, Tallis H, Cameron CR, Chan KMA, Daily GC, Goldstein J, Kareiva PM. 2009. Modeling multiple ecosystem services, biodiversity conservation, commodity production, and tradeoffs at landscape scales. Front Ecol Environ 7:4–11.CrossRefGoogle Scholar
  46. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W. 1983. Applied linear regression models. Burr Ridge (IL): Irwin.Google Scholar
  47. Páscoa F. 2001. Pbravo v.2.0. Modelo de produção para o pinheiro bravo. PAMAF Medida 4, Acção 3 (Divulgação). Federação dos Produtores Florestais de Portugal. Aplicação Informática e Manual do Utilizador. 47 pp.Google Scholar
  48. Pauchard A, Shea K. 2006. Integrating the study of non-native plant invasions across spatial scales. Biol Invasions 8:399–413.CrossRefGoogle Scholar
  49. Pejchar L, Mooney HA. 2009. Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504.PubMedCrossRefGoogle Scholar
  50. Peng Y, Gitelson AA. 2012. Remote estimation of gross primary productivity in soybean and maize based on total crop chlorophyll content. Remote Sens Environ 117:440–8.CrossRefGoogle Scholar
  51. Pino J, Font X, Carbo J, Jove M, Pallares L. 2005. Large-scale correlates of alien plant invasion in Catalonia (NE of Spain). Biol Conserv 122:339–50.CrossRefGoogle Scholar
  52. Pyke CR, Thomas R, Porter RD, Hellmann JJ, Dukes JS, Lodge DM, Chavarria G. 2008. Current practices and future opportunities for policy on climate change and invasive species. Conserv Biol 22:585–92.Google Scholar
  53. Ricciardi A, Cohen J. 2007. The invasiveness of an introduced species does not predict its impact. Biol Invasions 9:309–15.Google Scholar
  54. Rose M, Hermanutz L. 2004. Are boreal ecosystems susceptible to alien plant invasion? Evidence from protected areas. Oecologia 139:467–77.PubMedCrossRefGoogle Scholar
  55. Säumel I, Kowarik I. 2010. Urban rivers as dispersal corridors for primarily wind-dispersed invasive tree species. Landsc Urban Plann 94:244–9.CrossRefGoogle Scholar
  56. Shafroth PB, Cleverly JR, Dudley TL, Taylor JP, Van Riper C, Weeks EP, Stuart JN. 2005. Control of Tamarix in the western United States: implications for water salvage, wildlife use, and riparian restoration. Environ Manage 35:231–46.PubMedCrossRefGoogle Scholar
  57. Shono H. 2000. Efficiency of the finite correction of Akaike’s information criteria. Fish Sci 66:608–10.CrossRefGoogle Scholar
  58. Steinitz O, Heller J, Tsoar A, Rotem D, Kadmon R. 2006. Environment, dispersal and patterns of species similarity. J Biogeogr 33:1044–54.CrossRefGoogle Scholar
  59. Steinmann K, Linder HP, Zimmermann NE. 2009. Modelling plant species richness using functional groups. Ecol Model 220:962–7.Google Scholar
  60. Thuiller W, Richardson DM, Midgley GF. 2007. Will climate change promote alien plant invasions? In: Nentwig W, Ed. Biological invasions. Berlin: Springer. p 197–211.CrossRefGoogle Scholar
  61. Tomé M, Ribeiro F, Soares P. 2001. O modelo GLOBULUS 2.1. Grupo de Inventariação e Modelação de Recursos Florestais, Relatórios técnicos do GIMREF, no 2001. Lisboa: Instituto Superior de Agronomia, Universidade Técnica de Lisboa. 93 pp.Google Scholar
  62. Vicente J, Alves P, Randin C, Guisan A, Honrado J. 2010. What drives invasibility? A multi-model inference test and spatial modelling of alien plant species richness patterns in Northern Portugal. Ecography 33:1081–92.CrossRefGoogle Scholar
  63. Vicente J, Randin C, Gonçalves J, Metzger M, Lomba A, Honrado J, Guisan A. 2011. Where will conflicts between alien and rare species occur after climate and land-use change? A test with a novel combined modelling approach. Biol Invasions 13:1209–27.CrossRefGoogle Scholar
  64. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P. 2011. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–8.PubMedCrossRefGoogle Scholar
  65. Vincent PJ, Haworth JM. 1983. Poisson regression models of species abundance. J Biogeogr 10:153–60.CrossRefGoogle Scholar
  66. Walther GR. 2002. Weakening of climatic constraints with global warming and its consequences for evergreen broad-leaved species. Folia Geobot 37:129–39.CrossRefGoogle Scholar
  67. Walther GR, Gritti ES, Berger S, Hickler T, Tang ZY, Sykes MT. 2007. Palms tracking climate change. Glob Ecol Biogeogr 16:801–9.CrossRefGoogle Scholar
  68. Williams JW, Seabloom EW, Slayback D, Stoms DM, Viers JH. 2005. Anthropogenic impacts upon plant species richness and net primary productivity in California. Ecol Lett 8:127–37.CrossRefGoogle Scholar
  69. Wu C, Niu Z, Tang Q, Huang W, Rivard B, Feng J. 2009. Remote estimation of gross primary production in wheat using chlorophyll-related vegetation indices. Agric For Meteorol 149:1015–21.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Joana R. Vicente
    • 1
    • 2
    Email author
  • Ana T. Pinto
    • 1
  • Miguel B. Araújo
    • 3
    • 4
    • 5
  • Peter H. Verburg
    • 6
  • Angela Lomba
    • 1
    • 7
  • Christophe F. Randin
    • 8
  • Antoine Guisan
    • 7
  • João P. Honrado
    • 1
    • 2
  1. 1.Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO)Faculdade de Ciências da Universidade do PortoVairãoPortugal
  2. 2.Departamento de BiologiaFaculdade de Ciências da Universidade do PortoPortoPortugal
  3. 3.Department of Biodiversity and Evolutionary BiologyNational Museum of Natural Sciences, CSICMadridSpain
  4. 4.Cátedra Rui Nabeiro-BiodiversidadeUniversidade de Évora, CIBIOÉvoraPortugal
  5. 5.Center for Macroecology, Evolution and Climate, Department of BiologyUniversity of CopenhagenCopenhagenDenmark
  6. 6.Institute for Environmental Studies (IVM)VU University AmsterdamAmsterdamThe Netherlands
  7. 7.Département d’Ecologie et d’Evolution (DEE)Université de Lausanne LausanneSwitzerland
  8. 8.Institute of Botany University of BaselBaselSwitzerland

Personalised recommendations