Skip to main content
Log in

Differences in phenology and fruit characteristic between invasive and native woody species favor exotic species invasiveness

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

This study evaluates the idea that differences in reproductive phenology and traits between coexisting exotic and native species may promote exotic invasiveness. Reproductive phenology, proportions of flowers setting unripe fruits and ripe fruits (fruit set), abundance and morphology of fruits, and seed viability were compared between two invasive (Crataegus monogyna and Sorbus aucuparia) and six native woody fleshy-fruited species at three sites in temperate forests of northwestern Patagonia, Argentina. Flowering and the onset of fruit ripening occurred later in the exotic species than in most of the native species. The exotic species differed between them in some aspects of the reproductive process: C. monogyna had a higher fruit set, whereas S. aucuparia produced more flowers which offset its low values of fruit set. In both the exotic species and one simultaneously fruiting native species (Schinus patagonicus), high numbers of ripe fruits with a high proportion of viable seeds remained on the plants at a time when fruits of other native species were either scarce or absent (autumn–winter period). Compared to the fruits of S. patagonicus, those of both the exotic species are larger and fleshier. Therefore, the fruits of both the exotic species offer the dispersers, especially birds which were the most important frugivores in these studied temperate forests, a resource that would not be provided by the native plants. The success of these exotic species in Patagonian forests appears to be attributable in part to differences in their reproductive attributes such as fruit phenology and fruit traits such as size and fleshiness.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:396–403

    Article  CAS  Google Scholar 

  • Amico GC, Aizen MA (2005) Dispersión de semillas por aves en un bosque templado de Sudamérica austral: ¿quién dispersa a quién? Ecol Austral 15:89–100

    Google Scholar 

  • Armesto JJ, Rozzi R, Miranda P, Sabag C (1987) Plant/frugivore interactions in South American temperate forests. Rev Chil Hist Nat 60:321–336

    Google Scholar 

  • Aslan C, Rejmánek M (2012) Native fruit traits may mediate dispersal competition between native and non-native plants. NeoBiota 12:1–24

    Article  Google Scholar 

  • Bass DA, Neville DC, Lawriel SL, Lethbridge MR (2006) The importance of population growth, seed dispersal and habitat suitability in determining plant invasiveness. Euphytica 148:97–109

    Article  Google Scholar 

  • Bates D, Maechler M, Bolcker B (2009) Package lme4: linear mixed-effects models using S4 classes. URL http://lme4.r-forge.r-project.org/. Accessed 12 june 2011

  • Brown BJ, Randall RJ, Graham SA (2002) Competition for pollination between an invasive species (Purple Loosestrife) and a native congener. Ecol 83(8):2328–2336

    Article  Google Scholar 

  • 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 43:848–857

    Article  Google Scholar 

  • Cavallero L, Raffaele E (2010) Fire enhances the “competition-free” space of an invader shrub: Rosa rubiginosa in northwestern Patagonia. Biol Invasions 12:3395–3404

    Article  Google Scholar 

  • Correa MN (1984) Flora Patagónica IVb: Dicotyledones dialipétalas. INTA, Buenos Aires

    Google Scholar 

  • Cronk QC, Fuller JL (1995) Plant invaders. Chapman & Hall, London

    Google Scholar 

  • Daehler CC (2003) Performance comparisons of co–occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211

    Article  Google Scholar 

  • Damascos MA (2005) Especies nativas posibles facilitadoras de la recuperación del bosque de Austrocedrus chilensis. Ecociprés: Reunión sobre ecología, conservación y uso de los bosques de ciprés de la cordillera. CIEFAP, Esquel, pp 67–71

    Google Scholar 

  • Delouche JC, Wayne Still TW, Raspet M, Lienhard M (1971) Prueba de viabilidad de la semilla con Tetrazol. Centro Regional de Ayuda Técnica. Agencia para el desarrollo Internacional (AID), México

    Google Scholar 

  • Dickson TL, Hopwood J, Wilsey BJ (2012) Do priority effects benefit invasive plants more than native plants? An experiment with six grassland species. Biol Invasions 14:2617–2624

    Article  Google Scholar 

  • Erfmeier A, Bruelheide H (2004) Comparison of native and invasive Rododendron ponticum population: growth, reproduction and morphology under field conditions. Flora 199:120–133

    Article  Google Scholar 

  • Ezcurra C, Brion C (2005) Plantas del Nahuel Huapi. Catálogo de la flora vascular del Parque Nacional Nahuel Huapi, Argentina. Universidad Nacional del Comahue. Red Latinoamericana de Botánica, San Carlos de Bariloche

  • Fernández N (2007) Plantas exóticas invasoras de los Parques Nacionales de Patagonia. http://www.scribd.com/doc/3910028/LasplantasexoticasinvasorasdelosParquesNacionalesde-Patagonia. Accessed 16 july 2013

  • Funes MC, Sanguinetti P, Laclau P, Maresca L, García L, Mazzieri F, Chazarreta L, Bocos D, Diana Lavalle F, Espósito P, González A, Gallardo A (2006) Diagnóstico del estado de conservación de la biodiversidad en el Parque Nacional Lanín: su viabilidad de protección en el largo plazo. Informe final, Parque Nacional Lanín, San Martín de los Andes

    Google Scholar 

  • García D, Chacoff NP (2007) Scale-dependent effects of habitat fragmentation on hawthorn pollination, frugivory and seed predation. Conserv Biol 21(2):400–411

    Article  PubMed  Google Scholar 

  • García D, Obeso JR, Martínez I (2005) Rodent seed predation promotes differential recruitment among bird-dispersed trees in temperate secondary forests. Oecologia 144:435–446

    Article  PubMed  Google Scholar 

  • Gibson MR, Richardson DM, Marchante E, Marchante H, Rodger JG, Stone GN, Byrne M, Fuentes-Ramírez A, George N, Harris C, Johnson SD, Le Roux JJ, Miller JT, Murphy DJ, Pauw A, Prescott MN, Wandrag EM, Wilson JRU (2011) Reproductive biology of Australasian acacias: important mediator of invasiveness? Divers Distrib 17:911–933

    Article  Google Scholar 

  • Godoy O, Castro-Díez P, Valladares F, Costa-Tenorio M (2009a) Different flowering phenology of alien invasive species in Spain: evidence for the use of an empty temporal niche? Plant Biol 11:803–811

    Article  CAS  PubMed  Google Scholar 

  • Godoy O, Richardson DM, Valladares F, Castro-Díez P (2009b) Flowering phenology of invasive alien plant species compared with native species in three Mediterranean-type ecosystems. Ann Bot 103:485–494

    Article  PubMed Central  PubMed  Google Scholar 

  • Gosper CR (2004) Fruit characteristic of invasive bitou bush, Chrysanthemoides monilifera (Asteraceae), and a comparison with co-occurring native plant species. Aust J Bot 52(2):223–230

    Article  Google Scholar 

  • Gosper CR, Vivian-Smith G (2010) Fruit traits of vertebrate-dispersed alien plants: smaller seeds and more pulp sugar than indigenous species. Biol Invasions 12:2153–2163

    Article  Google Scholar 

  • Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers Distrib 11:549–558

    Article  Google Scholar 

  • Greenberg CH, Scott WT (2010) Fleshy fruit removal and nutritional composition of winter-fruiting plants: a comparison of non-native invasive and native species. Nat Areas J 30(3):312–321

    Article  Google Scholar 

  • Guitián J (1993) Why Prunus mahaleb (Rosaceae) produce more flowers than fruits. Am J Bot 80(11):1305–1309

    Article  Google Scholar 

  • Guitián J, Fuentes M (1992) Reproductive biology of Crataegus monogyna in northwestern Spain. Acta Oecol 13(1):3–11

    Google Scholar 

  • Guitián J, Munilla I, Guitián P, Guitián J, Bermejo T, Navarro L, Larrinaga AR, López B (2000) Zorzales, espinos y serbales: un estudio sobre el consumo de frutos silvestres de las aves migratorias en la costa occidental europea. Santiago de Compostela University Press, Santiago de Compostela

    Google Scholar 

  • Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC, Harris CJ, Licari D (2005) Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett 8:1066–1074

    Article  Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: Predicting invaders. Trends Ecol Evol 16(4):199–204

    Article  PubMed  Google Scholar 

  • Lake JC, Leishman MR (2004) Invasion success of exotic plants in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biol Conserv 117:215–216

    Article  Google Scholar 

  • Lloret F, Médail F, Brundu G, Camarda I, Moragues E, Rita J, Lambdon P, Hulme PE (2005) Species attributes and invasion success by alien plants on Mediterranean islands. J Ecol 93:512–520

    Article  Google Scholar 

  • Lodge DM (1993) Biological Invasions: Lessons for Ecology. Tree 8(4):133–136

    CAS  Google Scholar 

  • Mandon-Dalger I, Clergeau P, Tassin J, Revière JN, Gatti S (2004) Relationships between alien plants and an alien bird species on Reunion Island. J Trop Ecol 20:635–642

    Article  Google Scholar 

  • McAlpine KG, Jesson LK, Kubien DS (2008) Photosynthesis and water-use efficiency: a comparison between invasive (exotic) and non-invasive (native) species. Austral Ecol 33:10–19

    Article  Google Scholar 

  • Morales CL, Traveset A (2009) A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Lett 12:716–728

    Article  PubMed  Google Scholar 

  • Moroney JR, Rundel PW (2013) Abundance and dispersion of the invasive Mediterranean annual, Centaurea melitensis in its native and non-native range. Biol Invasions 15:495–507

    Article  Google Scholar 

  • Muller-Dombois D, Ellemberg H (1974) Aims and methods of vegetation ecology. John Wiley press, New York

    Google Scholar 

  • Munoz AA, Cavieres LA (2008) The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities. J Ecol 96:459–467

    Article  Google Scholar 

  • Pairon M, Chabrerie O, Casado CM, Jacquemart AL (2006) Sexual regeneration traits linked to black cherry (Prunus serotina Ehrh.) invasiveness. Acta Oecol 30:238–247

    Article  Google Scholar 

  • Pattison RR, Goldstein G, Ares A (1998) Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117:449–459

    Article  Google Scholar 

  • Pereyra FX (2007) Geomorfología urbana de San Carlos de Bariloche y su influencia en los peligros naturales, Río Negro. Revista de la Asociación Geológica Argentina 62:309–320

    Google Scholar 

  • Pías B, Salvande M, Guitián P (2007) Variation in predispersal losses in reproductive potential in rowan (Sorbus aucuparia L. Rosaceae) in the NW Iberian Peninsula. Plant Ecol 188:191–203

    Article  Google Scholar 

  • Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Biol invasions, Springer, Berlin, pp 97–125

  • Raspé O, Findlay C, Jacquemart AL (2000) Sorbus aucuparia L. J Ecol 88(5):910–930

    Article  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/. Accessed 3 Apr 2011

  • Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecol 77(6):1655–1661

    Article  Google Scholar 

  • Rejmánek M, Richardson DM, Pyšek P (2005) Plant invasions and invisibility of plant communities. In: van der Maarel E (ed) Vegetation ecology. Blackwell, Oxford, pp 332–355

    Google Scholar 

  • Richardson DM, Allsopp N, DʼAntonio CM, Milton SJ, Rejmánek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93

    Article  CAS  PubMed  Google Scholar 

  • Rovere AE, Molares S, Ladio AH (2013) Plantas utilizadas en cercos vivos de ciudades patagónicas: aportes de la etnobotánica para la conservación. Ecol Austral 23:165–173

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Sallabanks R (1993a) Hierarchical mechanisms of fruits selection by an avian frugivore. Ecol 74(5):1326–1336

    Article  Google Scholar 

  • Sallabanks R (1993b) Fruiting plants attractiveness to avian seed dispersers: native vs invasive Crataegus in western Oregon. Madroño 40(2):108–116

    Google Scholar 

  • Simberloff D, Relva MA, Nuñez M (2002) Gringos en el bosque: introduced tree invasion in a native Nothofagus/Austrocedrus forest. Biol Invasions 4:35–53

    Article  Google Scholar 

  • Sobral M, Larrinaga AR, Guitián J (2010) Do seed-dispersing birds exert selection on optimal plant trait combination? Correlated phenotypic selection on the fruit and seed size of hawthorn (Crataegus monogyna). Evol Ecol 24:1277–1290

    Article  Google Scholar 

  • Tierney GL, Fahey TJ (1998) Soil seed bank dynamics of pin cherry in a northern hardwood forest, New Hampshire, USA. Can J For Res 28:1471–1480

    Article  Google Scholar 

  • Van Kleunen M, Weber E, Fischer M (2010a) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245

    Article  PubMed  Google Scholar 

  • Van Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M (2010b) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13:947–958

    PubMed  Google Scholar 

  • Vila M, D’Antonio CM (1998) Fruit choice and seed dispersal of invasive vs. noninvasive Carpobrotus (Aizoaceae) in Coastal California. Ecol 79(3):1053–1060

    Article  Google Scholar 

  • Webb CJ, Sykes WR, Garnock Jones PJ (1988) Flora of New Zealand. Volume IV. Naturalised pteridophytes, gymnosperms, dicotyledons. Botany Division, D. S. I. R., Christchurch

  • Williams PA (2006) The role of blackbird (Turdus merula) in weed invasion in New Zealand. New Zeal J Ecol 30(2):285–291

    Google Scholar 

  • Wolkovich EM, Cleland EE (2011) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9(5):294–297

    Article  Google Scholar 

  • Wolkovich EM, Cleland EE (2014) Phenological niches and the future of invaded ecosystems with climate change. AoB Plants 6:0–16

    Article  Google Scholar 

Download references

Acknowledgments

We thank D. Lediuk and L. Quevedo for helping with field work, L. Graham and M. Zuliani for their assistance in lab work, P. Alarcón for helping in data analyses, C. Rezzano for facilitating the photographic equipment, and two anonymous reviewers whose comments and suggestion contributed to improve the manuscript. This work was funded by the projects B135 and B164 Universidad Nacional del Comahue. Karen Lediuk acknowledges a PhD. fellowship from CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karen D. Lediuk.

Additional information

Communicated by W. E. Rogers.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lediuk, K.D., Damascos, M.A., Puntieri, J.G. et al. Differences in phenology and fruit characteristic between invasive and native woody species favor exotic species invasiveness. Plant Ecol 215, 1455–1467 (2014). https://doi.org/10.1007/s11258-014-0402-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-014-0402-3

Keywords

Navigation