Abstract
Invasive success of many fleshy-fruited plants has been linked to opportunistic interactions with generalist frugivores. Prunus mahaleb is a small tree, producing large quantities of little, bright black, sugary drupes that are consumed by vertebrates. It is native to the Mediterranean region but has become invasive in several countries. This study was carried out at a nature reserve including remnant mountain grasslands of high conservation value in the southern Argentine Pampas. Our aim is to reconstruct the colonization history of invading populations proposing a generalized model to describe the invasion process: colonization events result in the establishment of a founder tree followed by a lag phase until it reaches massive seed production and enables an increase in local recruitment and plant density. To test this hypothesis, we analyzed population age structures and contrasted them with those predicted using a Leslie matrix growth model. We found that matrix model predictions fit well to actual age structures. Our results reveal the existence of an 8–18-year lag period between the establishment of the founder tree and local effective recruitment. The end of this lag coincides with an abrupt increase in individual fruit production that may have a strong effect on bird attraction and successful seed dispersal. This lag phase represents an opportunity for preventing further spread of P. mahaleb. Early detection and rapid eradication of new invasion focuses should be targeted as a principal aim of an effective control strategy.
Similar content being viewed by others
References
Abrahamson WG (ed) (1989) Plant-animal interactions. McGraw-Hill Book Company, New York
Archer S, Boutton TW, Hibbard KA (2001) Trees in grasslands: biogeochemical consequences of woody plant expansion. In: Schulze ED, Heimann M, Harrison S et al (eds) Global biogeochemical cycles in the climate system. Elsevier, San Diego, pp 115–138
Barger NN, Archer SR, Campbell JL, Huang C, Morton JA, Knapp AK (2011) Woody plant proliferation in North American drylands: a synthesis of impacts on ecosystem carbon balance. J Geophys Res Biogeosci 116(G4):G00K07. doi:10.1029/2010jg001506
Bass D, Crossman N, Lawrie S, Lethbridge M (2006) The importance of population growth, seed dispersal and habitat suitability in determining plant invasiveness. Euphytica 148(1):97–109
Bilenca DN, Miñarro FO (2004) Áreas valiosas de pastizal em las pampas y campos de Argentina, Uruguay y sur de Brasil. Uruguay y sur de Brasil, Buenos Aires
Brouillet L, Coursol F, Meades SJ, Favreau M, Anions M, Bélisle P, Desmet P (2010) VASCAN, the database of vascular plants of Canada. http://data.canadensys.net/vascan/. Accessed 27 Aug 2012
Browning DM, Archer SR, Asner GP, McClaran MP, Wessman CA (2008) Woody plants in grasslands: post-encroachment stand dynamics. Ecol Appl 18(4):928–944. doi:10.1890/07-1559.1
Buckley YM, Anderson S, Catterall CP, Corlett RT, Engel T, Gosper CR, Nathan R, Richardson DM, Setter M, Spiegel O, Vivian-Smith G, Voigt FA, Weir JES, Westcott DA (2006) Management of plant invasions mediated by frugivore interactions. J Appl Ecol 43(5):848–857. doi:10.1111/j.1365-2664.2006.01210.x
Burgos J (1968) El clima de la provincial de Buenos Aires en relación con la vegetación natural y el suelo. In: Cabrera A (ed) Flora de la provincia de Buenos Aires, vol 4., 1Colección científica INTA, Buenos Aires, pp 33–100
Debussche M, Lepart J (1992) Establishment of woody plants in Mediterranean old fields: opportunity in space and time. Landsc Ecol 6(3):133–145. doi:10.1007/bf00130026
Deckers B, Verheyen K, Hermy M, Muys B (2005) Effects of landscape structure on the invasive spread of black cherry Prunus serotina in an agricultural landscape in Flanders, Belgium. Ecography 28(1):99–109
Deckers B, Verheyen K, Vanhellemont M, Maddens E, Muys B, Hermy M (2008) Impact of avian frugivores on dispersal and recruitment of the invasive Prunus serotina in an agricultural landscape. Biol Invasions 10(5):717–727
Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) (2007) Seed dispersal: theory and its application in a changing world. CAB International, Columns Design Ltd., Reading
García C, Arroyo JM, Godoy JA, Jordano P (2005) Mating patterns, pollen dispersal, and the ecological maternal neighbourhood in a Prunus mahaleb L. population. Mol Ecol 14(6):1821–1830. doi:10.1111/j.1365-294X.2005.02542.x
García C, Jordano P, Godoy JA (2007) Contemporary pollen and seed dispersal in a Prunus mahaleb population: patterns in distance and direction. Mol Ecol 16(9):1947–1955
Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers Distrib 11(6):549–558. doi:10.1111/j.1366-9516.2005.00195.x
Grisez TJ, Barbour JR, Karrfalt RP (2008) Prunus L. Cherry, peach and plum. In: Bonner FT, Karrfalt RP (eds) The woody plant seed manual. Agriculture handbook 727. Agriculture handbook 727. Forest Service, Department of Agriculture, USA, pp 875–890
Guitián J, Sánchez JM, Guitián P (1992) Niveles de fructificación en Crataegus monogyna Jacq., Prunus mahaleb L., Prunus spinosa L. (Rosaceae). Anales Jardín Botánico de Madrid 50:239–245
Halpern CB, Antos JA, Rice JM, Haugo RD, Lang NL (2010) Tree invasion of a montane meadow complex: temporal trends, spatial patterns, and biotic interactions. J Veg Sci 21(4):717–732. doi:10.1111/j.1654-1103.2010.01183.x
Harper JL (1977) Population biology of plants. Academic, London
Herrera CM (1989) Frugivory and seed dispersal by carnivorous mammals, and associated fruit characteristics, in undisturbed Mediterranean habitats. Oikos 55:250–262
Herrera CM, Jordano P (1981) Prunus mahaleb and Birds: the High-Efficiency Seed Dispersal System of a Temperate Fruiting Tree. Ecol Monogr 51(2):203–218
Hintze JL, Nelson RD (1998) Violin plots: a box plot-density trace synergism. Am Stat 52(2):181–184. doi:10.1080/00031305.1998.10480559
Jordano P (1987) Avian fruit removal: effects of fruit variation, crop size and insect damage. Ecology 68(6):1711–1723
Jordano P (1993) Pollination biology of Prunus mahaleb L.: deferred consequences of gender variation for fecuntdity and seed size. Biol J Linn Soc 50:65–84
Jordano P (1994) Spatial and temporal variation in the avian-frugivore assemblage of Prunus mahaleb: patterns and consequences. Oikos 71(3):479–491
Jordano P (1995) Frugivore-mediated selection on fruit and seed size: birds and St. Lucie’s cherry, Prunus Mahaleb. Ecology 76(8):2627–2639
Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in natural plant communities, 2nd edn. Commonwealth Agricultural Bureau International, Wallingford, pp 105–156
Jordano P, Schupp EW (2000) Seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecol Monogr 70(4):591–615
Jurena PN, Archer S (2003) Woody plant establishment and spatial heterogeneity in grasslands. Ecology 84(4):907–919. doi:10.1674/0003-0031(2002)147[0256:EOPDOT]2.0.CO;2
Kollmann J, Pflugshaupt K (2001) Flower and fruit characteristics in small and isolated populations of a fleshy-fruited shrub. Plant Biol 3(1):62–71
Kollmann J, Pflugshaupt K (2005) Population structure of a fleshy-fruited species at its range edge—the case of Prunus mahaleb L. in northern Switzerland. Bot Helv 115(1):49–61
Meekins JF, McCarthy BC (2002) Effect of population density on the demography of an invasive plant (Alliaria petiolata, Brassicaceae) population in a southeastern Ohio forest. Am Midl Nat 147(2):256–278. doi:10.1890/0012-9658(2003)084[0907:WPEASH]2.0.CO;2
Mooney HA, Mack RN, McNeely JA, Neville LE, Schei PJ, Waage JK (2005) Invasive alien species: a new synthesis. Scientific Committee on Problems of the Environment (SCOPE), Paris
Pflugshaupt K, Kollmann J, Fischer M, Roy B (2002) Pollen quantity and quality affect fruit abortion in small populations of a rare fleshy-fruited shrub. Basic Appl Ecol 3(4):319–327
R-Core-Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rice J, Halpern C, Antos J, Jones J (2012) Spatio-temporal patterns of tree establishment are indicative of biotic interactions during early invasion of a montane meadow. Plant Ecol 213(4):555–568. doi:10.1007/s11258-012-0021-9
Sallabanks R (1992) Fruit fate, frugivory, and fruit characteristics: a study of the hawthorn, Crataegus monogyna (Rosaceae). Oecologia 91(2):296–304. doi:10.1007/bf00317800
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102
Swearingen J (2008) WeedUS: database of plants invading natural areas in the United States. Plant Conservation Alliance, Alien Plant Working Group. http://www.invasive.org/weedus/index.html. Accessed 11 May 2009
Van Auken OW (2000) Shrub invasions of north American semiarid grasslands. Annu Rev Ecol Syst 31(1):197–215. doi:10.1146/annurev.ecolsys.31.1.197
Van Auken OW (2009) Causes and consequences of woody plant encroachment into western north American grasslands. J Environ Manag 90(10):2931–2942. doi:10.1016/j.jenvman.2009.04.023
Webb CJ, Sykes WR, Garnock-Jones PJ (1988) Flora of New Zealand. Manaaki Whenua, Landcare Research. http://FloraSeries.LandcareResearch.co.nz. Accessed 09 May 2008
Wickham H (2009) ggplot2: elegant graphics for data analysis, 0.9.2.1 edn. Springer, New York
Zalba SM (2001) Efectos de la forestación con especies exóticas sobre comunidades de aves de pastizal pampeano. Doctoral Thesis, Universidad Nacional del Sur, Bahía Blanca
Zalba SM, Villamil CB (2002) Woody plant invasion in relictual grasslands. Biol Invasions 4(1):55–72
Acknowledgments
This work was funded by CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina), CIC (Comisión de Investigaciones Científicas de la Provincia de Buenos Aires, Argentina) and Universidad Nacional del Sur, Bahía Blanca, Argentina. We are grateful to Ernesto Tornquist Provincial Park rangers who helped in field work and two anonymous referees that provided helpful comments on earlier versions of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Amodeo, M.R., Zalba, S.M. Wild cherries invading natural grasslands: unraveling colonization history from population structure and spatial patterns. Plant Ecol 214, 1299–1307 (2013). https://doi.org/10.1007/s11258-013-0252-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-013-0252-4