Plant Ecology

, Volume 206, Issue 1, pp 83–96 | Cite as

High competitiveness of a resource demanding invasive acacia under low resource supply

  • Christiane Werner
  • Ulrich Zumkier
  • Wolfram Beyschlag
  • Cristina Máguas
Article

Abstract

Mechanisms controlling the successful invasion of resource demanding species into low-resource environments are still poorly understood. Well-adapted native species are often considered superior competitors under stressful conditions. Here we investigate the competitive ability of the resource demanding alien Acacia longifolia, which invades nutrient-poor Mediterranean sand dunes such as in coastal areas of Portugal. We explore the hypothesis that drought may limit invasion in a factorial competition experiment of the alien invasive versus two native species of different functional groups (Halimium halimifolium, Pinus pinea), under well-watered and drought conditions. Changes in biomass, allocation pattern, and N-uptake-efficiency (via 15N-labeling) indicated a marked drought sensitivity of the invader. However, highly efficient drought adaptations of the native species did not provide a competitive advantage under water limiting conditions. The competitive strength of H.halimifolium towards the alien invader under well-watered conditions turned into a positive interaction between both species under drought. Further, low resource utilization by native species benefited A. longifolia by permitting continued high nitrogen uptake under drought. Hence, the N-fixing invader expresses low plasticity by continuous high resource utilization, even under low resource conditions. The introduction of novel traits into a community like N-fixation and high resource use may promote A. longifolia invasiveness through changes in the physical environment, i.e., the water and nutrient cycle of the invaded sand dune system, thereby potentially disrupting the co-evolved interactions within the native plant community.

Keywords

Progressive drought Mediterranean Invasive species 15N stable isotope labeling Competition Biomass 

References

  1. Bartelheimer M, Steinlein T, Beyschlag W (2008) 15N-Nitrate-labelling demonstrates a size symmetric competitive effect on belowground resource uptake. Plant Ecol 199:243–253CrossRefGoogle Scholar
  2. Baruch Z (1996) Ecophysiological aspects of the invasion by African grasses and their impact on biodiversity and function of neotropical savannas. Ecol Stud 121:79–93Google Scholar
  3. Beyschlag W, Hanisch S, Friedrich S, Jentsch A, Werner C (2009) 15N natural abundances during early and late succession in a middle-European dry acidic grassland. Plant Biol. doi:10.1111/j.1438-8677.2008.00173.x
  4. Blumenthal D (2005) Interrelated causes of plant invasion. Science 310:243–244CrossRefPubMedGoogle Scholar
  5. Booth MS, Caldwell MM, Stark JM (2003) Overlapping resource use in three Great Basin species: implications for community invasibility and vegetation dynamics. J Ecol 91:36–48CrossRefGoogle Scholar
  6. Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tielborger K, Travis JM, Anthelme F (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34CrossRefGoogle Scholar
  7. Call LJ, Nilsen ET (2005) Analysis of interactions between the invasive tree-of-heaven (Alianthus altissima) and the native black locust (Robinia pseudoacacia). Plant Ecol 176:272–285CrossRefGoogle Scholar
  8. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–522CrossRefPubMedGoogle Scholar
  9. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848CrossRefPubMedGoogle Scholar
  10. Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  11. Chapin FSI, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Díaz S (2000) Consequences of changing biodiversity. Nature 405:234–242CrossRefPubMedGoogle Scholar
  12. Chesson P (2000) Mechanisms of maintenance of species diversity. Ann Rev Ecol Syst 31:343–366CrossRefGoogle Scholar
  13. Corbin JD, D’ Antonio CM (2004) Effects of exotic species on soil nitrogen cycling: implications for restoration. Weed Technol 18:1464–1467CrossRefGoogle Scholar
  14. Correia O, Martins AC, Catarino F (1992) Comparative phenology and seasonal nitrogen variation in Mediterranean species of Portugal. Ecol Mediterr XVIII:7–18Google Scholar
  15. Crawley MJ (1990) The population dynamics of plants. Philos Trans Biol Sci 330:125–140CrossRefGoogle Scholar
  16. Cronk QB, Fuller JL (1995) Plant invaders. Chapman and Hall, LondonGoogle Scholar
  17. D’ Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87Google Scholar
  18. Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Syst 34:183–212CrossRefGoogle Scholar
  19. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534CrossRefGoogle Scholar
  20. Dietz H, Steinlein T (2004) Recent advances in understanding plant invasions. Prog Bot 65:539–573Google Scholar
  21. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139CrossRefPubMedGoogle Scholar
  22. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  23. Escudero A, Mediavilla S, Heilmeier H (2008) Leaf longevity and drought: avoidance of the costs and risks of early leaf abscission as inferred from the leaf carbon isotopic composition. Funct Plant Biol 35:705–713CrossRefGoogle Scholar
  24. Evans RD, Rimer R, Sperry L (2001) Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11:1301–1310CrossRefGoogle Scholar
  25. Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. Proc Natl Acad Sci 100:8916–8920PubMedGoogle Scholar
  26. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1108CrossRefPubMedGoogle Scholar
  27. Grime JP, Hodgson JG (1987) Botanical contributions to contemporary ecological theory. New Phytol 106:283–295Google Scholar
  28. Große-Stoltenberg A (2009) Impacts of an “invasive engeneer”on the structure of Mediterranean-Atlantic dune and forest phytocoenoses. Diploma-Thesis, University MünsterGoogle Scholar
  29. Grund K, Conedera M, Schröder H, Walther GR (2005) The role of fire in the invasion process of evergreen broad-leaved species. Basic Appl Ecol 6:47–56CrossRefGoogle Scholar
  30. Harris MR, Facelli JM (2003) Competition and resource availability in an annual plant community dominated by an invasive species, Carrichtera annua (L. Aschers.), in South Australia. Plant Ecol 167:19–29CrossRefGoogle Scholar
  31. Hellmann C, Sutter R (2008) Spatial influences of the N2-fixing invasive Acacia longifolia (Andrews) Willd. on leaf nitrogen traits of three indigenous species and on light interception regimes in a Portuguese dune ecosystem. Bachelor-Thesis, University BielefeldGoogle Scholar
  32. Hoagland DR, Arnon I (1950) The water culture method for growing plants without soil. (California Agriculture Experiment Station: Berkeley) Circular No. 347Google Scholar
  33. Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for Conservation. Conserv Biol 6:324–337CrossRefGoogle Scholar
  34. Högberg P (1997) 15N natural abundance in soil–plant systems. New Phytol 137:179–203CrossRefGoogle Scholar
  35. Kowarik I (2003) Biologische Invasionen-Neophyten und Neozoen in Mitteleuropa. Ulmer, StuttgartGoogle Scholar
  36. Kramer R (2005) Influence of chilling stress and competition on an alien invasive and native mediterranean species. Staatsexamensarbeit, University BielefeldGoogle Scholar
  37. Lambdon PW, Lloret F, Hume PE (2008) Do alien plants on Mediterranean islands tend to invade different niches from native species? Biol Invasion 10:703–716CrossRefGoogle Scholar
  38. 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 177:706–714CrossRefPubMedGoogle Scholar
  39. MacArthur RH (1972) Geographical ecology: patterns in the distribution of species. Princeton University Press, Princeton, NJGoogle Scholar
  40. Marchante H, Marchante E, Freitas H (2003) Invasion of the Portuguese dune ecosystems by the exotic species Acacia longifolia (Andrews) Willd.: effects at the community level. In: Child LE, Brock JH, Brundu G, Prach K, Pyšek P, Wade PM, Williamson M (eds) Plant invasions: ecological threats and management solutions. Backhuys Publishers, The Netherlands, Leiden, pp 75–85Google Scholar
  41. Marchante H, Marchante E, Buscardo E, Maia J, Freitas H (2004) Recovery potential of dune ecosystems invaded by an exotic acacia species (Acacia longifolia). Weed Technol 18:1427–1433CrossRefGoogle Scholar
  42. Marchante E, Kjoller A, Struwe S, Freitas H (2008a) Short- and long-term impacts of Acacia longifolia invasion on the belowground processes of a Mediterranean coastal dune ecosystem. Appl Soil Ecol 40:210–217CrossRefGoogle Scholar
  43. Marchante E, Kjoller A, Struwe S, Freitas H (2008b) Invasive Acacia longifolia induce changes in the microbial catabolic diversity of sand dunes. Soil Biol Biochem 40:2563–2568CrossRefGoogle Scholar
  44. Marchante E, Kjoller A, Struwe S, Freitas H (2009) Soil recovery after the removal of the N2-fixing invasive Acacia longifolia: consequences for ecosystem restoration. Biol Invasion. doi:10.1007/s10530-008-9295-1
  45. Maron JL, Jefferies RL (1999) Bush lupine mortality, altered resource availability, and alternative vegetation states. Ecology 80:443–454CrossRefGoogle Scholar
  46. McKane RB, Johnson LC, Shaver GR et al (2002) Resource-based niches provide a basis for plant species diversity and dominance in Arctic Tundra. Nature 6867:68–70CrossRefGoogle Scholar
  47. McKenney JL, Cripps MG, Price WJ, Hinz HL, Schwarzländer M (2007) No difference in competitive ability between invasive North American and native European Lepidium draba populations. Plant Ecol 193:292–303CrossRefGoogle Scholar
  48. Miller TE, Burns JH, Munguia P, Walters EL et al (2005) A critical review of twenty years’ use of the resource-ratio theory. Am Nat 186:439–448CrossRefGoogle Scholar
  49. Mooney HA, Hobbs RJ (eds) (2000) Invasive species in a changing world. Island Press, Washington, DCGoogle Scholar
  50. Naeem S, Knops JM, Tilman D, Howe KM, Kenndy T, Gale S (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91:97–108CrossRefGoogle Scholar
  51. Ortmeier K (2007) Importance of nursery plants for invasive process of Acacia longifolia in Portuguese dune ecosystems. Diploma Thesis, University BielefeldGoogle Scholar
  52. Peperkorn R (2005) Key factors of invasiveness of Acacia longifolia—experimental comparison with native species from Mediterranean sand ecosystems. PhD thesisGoogle Scholar
  53. Peperkorn R, Werner C, Beyschlag W (2005) Phenotypic plasticity of an invasive acacia versus two native Mediterranean species. Funct Plant Biol 32:933–944CrossRefGoogle Scholar
  54. Pereira AJ, Evangelista H, Marchante H, Marchante E, Schreck C, Freitas H, Ramos M, Correia O, Máguas C (2004). Water use in dune ecosystems: native versus invasive species (Acacia longifolia). In: Procedings: VII Simposio Luso-espanhol de Relações Hidricas em plantas, pp 163–166Google Scholar
  55. Rascher KG, Máguas C, Correia O, Werner C (2009) Tracing seasonal changes in water use of an invasive Acacia and a native Pine in Southern Portugal by measurement of sap flow. Acta Horticulturae (in press)Google Scholar
  56. Richardson DM, Pyšek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr 30:409–431CrossRefGoogle Scholar
  57. Rodriguez-Echeverría S, Crisóstomo JA, Nabais C, Freitas H (2009) Belowground mutualists and the invasive ability of Acacia longifolia in coastal dunes of Portugal. Biol Invasions 11(3):651–661CrossRefGoogle Scholar
  58. Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25:251–263CrossRefPubMedGoogle Scholar
  59. Stock WD, Wienand KT, Baker AC (1995) Impacts of invading Nitrogen-fixing acacia species on patterns of nutrient cycling in two cape ecosystems: evidence from soil incubation studies and 15N natural abundance values. Oecologia 101:375–383CrossRefGoogle Scholar
  60. Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273CrossRefPubMedGoogle Scholar
  61. Tilman D (1980) Resources: a graphical-mechanistic approach to competition and predation. Am Nat 116:362–393CrossRefGoogle Scholar
  62. Tilman D (1985) The resource-ratio of plant succession. Am Nat 125:827–852CrossRefGoogle Scholar
  63. Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861CrossRefPubMedGoogle Scholar
  64. Vila M, Weiner J (2004) Are invasive plant species better competitors than native plant species?—evidence from pair-wise experiments. Oikos 105:229–238CrossRefGoogle Scholar
  65. Vitousek PM (1994) Beyond global warming: ecology and global change. Ecology 75:1861–1876CrossRefGoogle Scholar
  66. Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawaii: plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59:247–265CrossRefGoogle Scholar
  67. Werner C, Correia O (1996) Photoinhibition in cork-oak leaves under stress: influence of the bark-stripping on the chlorophyll fluorescence emission in Quercus suber L. Trees 10:288–292Google Scholar
  68. Werner C, Correia O, Beyschlag W (1999) Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought. Acta Oecol 20:15–23CrossRefGoogle Scholar
  69. Werner C, Ryel RJ, Correia O, Beyschlag W (2001) Structural and functional variability within the canopy and its relevance for carbon gain and stress avoidance. Acta Oecol 22:1–10CrossRefGoogle Scholar
  70. Werner C, Correia O, Beyschlag W (2002) Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem. Funct Plant Biol 29:999–1011CrossRefGoogle Scholar
  71. Werner C, Peperkorn R, Máguas C, Beyschlag W (2008) Competitive balance between the alien invasive Acacia longifolia and native Mediterranean species. In: Tokarska-Guzik B, Brock JH, Brundu G, Child L, Daehler CC, Pyšek P (eds) Plant invasions: human perception, ecological impacts and management. Backhuys Publishers, Leiden, The Netherlands, pp 261–275Google Scholar
  72. Witkowski ETF (1991a) Effects of invasive alien Acacias on nutrient cycling in the coastal lowlands of the Cape Fynbos. J Appl Ecol 28:1–15CrossRefGoogle Scholar
  73. Witkowski ETF (1991b) Growth and competition between seedlings of Protea repens L. and the alien invasive, Acacia saligna (Labill.) Wendl. in relation to nutrient availability. Funct Ecol 5:101–110CrossRefGoogle Scholar
  74. Yelenik SG, Stock WD, Richardson DM (2004) Ecosystem level impacts of invasive Acacia saligna in the South African Fynbos. Rest Ecol 12:44–51CrossRefGoogle Scholar
  75. Zunzunegui M, Díaz Barradas MC, García Novo F (2000) Different phenotypic response of Halimium halimifolium in relation to groundwater availability. Plant Ecol 148:165–174CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Christiane Werner
    • 1
  • Ulrich Zumkier
    • 1
  • Wolfram Beyschlag
    • 1
  • Cristina Máguas
    • 2
  1. 1.Department of Experimental and Systems EcologyUniversity BielefeldBielefeldGermany
  2. 2.Centro de Biologia Ambiental, Faculdade de CiênciasUniversidade LisboaLisbonPortugal

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