Abstract
Clonal growth seems to be a common trait for many of the most aggressive invasive plant species. However, little research has been conducted to determine the role of clonality in the successful invasion of new areas by exotic species. Carpobrotus edulis (L.) N.E. Br. is a mat-forming succulent plant, native to South Africa that is invasive in coastal dunes of Australia, New Zealand, USA and Southern Europe. Although Carpobrotus edulis is a clonal plant, there is no information on the role of clonality for the invasion by this species, therefore the objective of this study was to test whether or not physiological integration improves the performance of C. edulis invading coastal sand dunes. To do that, a 6-month field experiment was designed in which the stolon connections between the apical ramets and the C. edulis mats were severed to prevent physiological integration. This treatment was applied to ramets growing under high and low competition with the native species. Apical ramets with intact stolon connections were used as control. Integration improved the survivorship and growth of apical ramets, both in high and low competition. Connected ramets showed a more pronounced increase of clonal growth (estimated as stolon length) during the experimental period and a higher total biomass and number of ramets at the completion of the experiment. In terms of survivorship, the benefit of integration was greater under high competition. Physiological integration can therefore be considered an important factor in the invasiveness of C. edulis, both in open space and in direct competition with the native plants.
Similar content being viewed by others
References
Almeida JD, Freitas H (2001) The exotic and invasive flora of Portugal. Botanica Complutensis 25:317–327
Almeida JD, Marchante E, Marchante H, Freitas H (2003) A brief report on the invasive flora of Portugal. Aliens 18:16–18
Alpert P (1991) Nitrogen sharing among ramets increases clonal growth in Fragaria chiloensis. Ecology 72:69–80
Alpert P (1999) Clonal integration in Fragaria chiloensis differs between populations: ramets from grassland are selfish. Oecologia 120:69–76
Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility, and the role of environmental stress in preventing the spread of non-native plants. Perspect Plant Ecol Evol Syst 3:52–66
Amsberry L, Baker MA, Ewanchuk PJ, Bertness MD (2000) Clonal integration and the expansion of Phragmites australis. Ecol Appl 10:1110–1118
Baker HG (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24
Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants–an economic analogy. Annu Rev Ecol Syst 16:363–392
Costa JC, Aguiar C, Capelo J, Lousã M, Neto C (1998) Biogeografia de Portugal continental. Quercetea 0:5–56
Costa JC, Lousã M, Capelo J, Espírito Santo MD, Izco Sevillano J, Arsénio P (2000) The coastal vegetation of the Portuguese divisory sector: dunes cliffs and low-scrub communities. Finisterra XXXV 69:69–93
D’Antonio CM (1993) Mechanisms controlling invasion of coastal plant communities by the alien succulent Carpobrotus edulis. Ecology 74:83–95
D’Antonio CM, Mahall BE (1991) Root profiles and competition between the invasive, exotic perennial, Carpobrotus edulis, and two native shrub species in California coastal scrub. Am J Bot 78:885–894
Evans JP (1992) The effect of local resource availability and clonal integration on ramet functional morphology in Hydrocotyle bonariensis. Oecologia 89:265–276
Gleeson SK, Tilman D (1992) Plant allocation and the multiple limitation hypothesis. Am Nat 139:1322–1343
Gonçalves ML (1990) Carpobrotus. In: Castroviejo S (ed) Flora Iberica. Plantas vasculares de la Península Ibérica e Islas Baleares. Vol. II Platanaceae–Plumbaginaceae (partim). Real Jardín Botánico-CSIC, Madrid, pp 82–84
Grime JP, Mackey JML (2002) The role of plasticity in resource capture by plants. Evol Ecol 16:299–307
Groves RH, di Castri F (1991) Biogeography of Mediterranean invasions. Cambridge University Press, Cambridge
Hartnett DC, Bazzaz FA (1983) Physiological integration among intraclonal ramets in Solidago canadensis. Ecology 64:779–788
Hutchings MJ, Bradbury IK (1986) Ecological perspectives on clonal perennial herbs. Bioscience 36:178–182
Johnson IR, Thornley JHM (1987) A model of root:shoot partitioning and optimal growth. Ann Bot 60:133–142
Jónsdóttir IS, Watson MA (1997) Extensive physiological integration: an adaptive trait in resource-poor environments? In: de Kroon H, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 109–136
Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457–481
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204
Levine JM, Vilà M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc B 270:775–781
Liu J, Dong M, Miao S, Li Z, Song M, Wang R (2006) Invasive alien plants in China: role of clonality and geographical origin. Biol Invasions 8:1461–1470
Liu J, He WM, Zhang SM, Liu FH, Dong M, Wang RQ (2008) Effect of clonal integration on photosynthesis of the invasive clonal plant Alternanthera philoxeroides. Photosynthetica 46:299–302
Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Maurer DA, Zedler JB (2002) Differential invasion of a wetland grass explained by tests of nutrients and light availability on establishment and clonal growth. Oecologia 131:279–288
Otfinowski R, Kenkel NC (2008) Clonal integration facilitates the proliferation of smooth brome clones invading northern fescue prairies. Plant Ecol 199:235–242
Peltzer DA (2002) Does clonal integration improve competitive ability? A test using aspen (Populus tremuloides [Salicaceae]) invasion into prairie. Am J Bot 89:494–499
Pennings SC, Callaway RM (2000) The advantages of clonal integration under different ecological conditions: a community-wide test. Ecology 81:709–716
Peperkorn R, Werner C, Beyschlag W (2005) Phenotypic plasticity of an invasive acacia versus two native Mediterranean species. Funct Plant Biol 32:933–944
Pitelka LF, Ashmun JW (1985) Physiology and integration of ramets in clonal plants. In: Jackson JBC, Buss LW, Cook RE (eds) Population biology and evolution of clonal organisms. Yale University Press, New Haven, pp 399–435
Price EAC, Marshall C (1999) Clonal plants and environmental heterogeneity. Plant Ecol 141:3–7
Pyšek P (1997) Clonality and plant invasion: can a trait make a difference? In: de Kroon H, van Groenendal J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 405–427
Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661
Rodríguez-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 11:651–661
Roiloa SR, Retuerto R (2005) Presence of developing ramets of Fragaria vesca L. increases photochemical efficiency in parent ramets. Int J Plant Sci 166:795–803
Roiloa SR, Retuerto R (2006a) Small-scale heterogeneity in soil quality influences photosynthetic efficiency and habitat selection in a clonal plant. Ann Bot 98:1043–1052
Roiloa SR, Retuerto R (2006b) Physiological integration amiliorates effects of serpentine soils in the clonal herb Fragaria vesca. Physiol Plantarum 128:662–676
Roy J (1990) In search of characteristics of plant invaders. In: di Castri AJ, Hansen AJ, Debushe M (eds) Biological invasions in Europe and the Mediterranean Basin. Kluwer, Dordrecht, pp 335–352
Saitoh T, Seiwa K, Nishiwaki A (2002) Importance of physiological integration of dwarf bamboo to persistence in forest understorey: a field experiment. J Ecol 90:78–85
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332
Salzman AG, Parker MA (1985) Neighbors ameliorate local salinity stress for a rhizomatous plant in a heterogeneous environment. Oecologia 65:273–277
Shumway SW (1995) Physiological integration among clonal ramets during invasion of disturbance patches in a New England salt marsh. Ann Bot 76:225–233
Silander JA Jr (1985) Microevolution in clonal plants. In: Jackson JBC, Buss LW, Cook RE (eds) Population biology and evolution of clonal organisms. Yale University Press, New Haven, pp 107–152
Sintes T, Moragues E, Traveset A, Rita J (2007) Clonal growth dynamics of the invasive Carpobrotus affine acinaciformis in Mediterranean coastal systems: a non-linear model. Ecol Model 206:110–118
Slade AJ, Hutchings MJ (1987) An analysis of the costs and benefits of physiological integration between ramets in the clonal perennial herb Glechoma hederacea. Oecologia 73:425–431
Stuefer JF, de Kroon H, During HJ (1996) Exploitation of environmental heterogeneity by spatial division of labour in a clonal plant. Funct Ecol 10:328–334
Traveset A, Brundu G, Carta L, Mprezetou I, Lambdon P, Manca M, Médail F, Moragues E, Rodríguez-Pérez J, Siamantziouras AKD, Suehs CM, Troumbis A, Vilà M, Hulme PE (2008a) Consistent performance of invasive plant species within and among islands of the Mediterranean basin. Biol Invasions 10:847–858
Traveset A, Moragues E, Valladares F (2008b) Spreading of the invasive Carpobrotus aff. acinaciformis in Mediterranean ecosystems: the advantage of performing in different light environments. Appl Veg Sci 11:45–54
Vilà M, Siamantziouras AKD, Brundu G, Camarda I, Lambdon P, Médail F, Moragues E, Suehs CM, Traveset A, Troumbis AY, Hulme PE (2008) Widespread resistance of Mediterranean island ecosystems to the establishment of three alien species. Divers Distrib 14:839–851
Wang N, Yu FH, Li PX, He WM, Liu FH, Liu JM, Dong M (2008) Clonal integration affects growth, photosynthetic efficiency and biomass allocation, but not the competitive ability, of the alien invasive Alternanthera philoxeroides under severe stress. Ann Bot 101:671–678
Wijesinghe DK, Handel SN (1994) Advantages of clonal growth in heterogeneous habitats: an experiment with Potentilla simplex. J Ecol 82:495–502
Williamson MH (1996) Biological invasions. Chapman & Hall, London
Wisura W, Glen HF (1993) The South African species of Carpobrotus (Mesembryanthema–Aizoaceae). Contrib Bolus Herbarium 15:76–107
Yu F, Dong M, Krüsi B (2004) Clonal integration helps Psammochloa villosa survive sand burial in an inland dune. New Phytol 162:697–704
Acknowledgments
We thank D. Bachmann for field assistance, J. Sanchez-Vilas for statistics comments and Kerrin Forster for English correction. We are grateful to an anonymous referee and to Editor Daniel Simberloff for their valuable comments on an earlier version of this paper. S. R. Roiloa was supported by an “Ángeles Alvariño” research grant awarded by the Autonomous Government of Galicia, Spain.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Roiloa, S.R., Rodríguez-Echeverría, S., de la Peña, E. et al. Physiological integration increases the survival and growth of the clonal invader Carpobrotus edulis . Biol Invasions 12, 1815–1823 (2010). https://doi.org/10.1007/s10530-009-9592-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-009-9592-3