, Volume 167, Issue 2, pp 469–479 | Cite as

Relative abundance of an invasive alien plant affects native pollination processes

  • Anke Christiane DietzschEmail author
  • Dara Anne Stanley
  • Jane Catherine Stout
Plant-Animal interactions - Original Paper


One major characteristic of invasive alien species is their occurrence at high abundances in their new habitat. Flowering invasive plant species that are visited by native insects and overlap with native plant species in their pollinators may facilitate or disrupt native flower visitation and fertilisation by forming large, dense populations with high numbers of flowers and copious rewards. We investigated the direction of such a proposed effect for the alien invasive Rhododendron ponticum in Irish habitats. Flower visitation, conspecific and alien pollen deposition, fruit and seed set were measured in a self-compatible native focal plant, Digitalis purpurea, and compared between field sites that contained different relative abundances of R. ponticum. Flower visitation was significantly lower at higher alien relative plant abundances than at lower abundances or in the absence of the alien. Native flowers experienced a significant decrease in conspecific pollen deposition with increasing alien abundance. Heterospecific pollen transfer was very low in all field sites but increased significantly with increasing relative R. ponticum abundance. However, lower flower visitation and lower conspecific pollen transfer did not alter reproductive success of D. purpurea. Our study shows that indirect interactions between alien and native plants for pollination can be modified by population characteristics (such as relative abundance) in a similar way as interactions among native plant species. In D. purpurea, only certain aspects of pollination and reproduction were affected by high alien abundances which is probably a result of high resilience due to a self-compatible breeding system. Native species that are more susceptible to pollen limitation are more likely to experience fitness disadvantages in habitats with high relative alien plant abundances.


Rhododendron ponticum Pollinator visitation Pollen deposition Reproductive output Plant diversity 



Thanks to Karl Duffy for field assistance and to Steven Waldren and the members of staff of the Trinity Botanic Gardens for technical support. We thank Coillte Ireland for access to field sites and usage permission, and Bill Kunin for helpful comments on the manuscript. This study was funded by Science Foundation Ireland as part of a Basic Research Grant (04/BR/B0637) and a UREKA Phytotechnology Ireland Summer School Grant, both awarded to J.C.S. This research complies with current Irish laws.


  1. Agresti A (1996) An introduction to categorical data analysis. Wiley, New YorkGoogle Scholar
  2. Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281PubMedCrossRefGoogle Scholar
  3. Ashman T-L, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421CrossRefGoogle Scholar
  4. Bartomeus I, Bosch J, Vilà M (2008a) High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community. Ann Bot 102:417–424PubMedCrossRefGoogle Scholar
  5. Bartomeus I, Vilà M, Santamaría L (2008b) Contrasting effects of invasive plants in plant–pollinator networks. Oecologia 155:761–770PubMedCrossRefGoogle Scholar
  6. Bjerknes A-L, Totland Ø, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12CrossRefGoogle Scholar
  7. Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328–2336CrossRefGoogle Scholar
  8. Buxton BH, Darlington CD (1932) Crosses between Digitalis purpurea and Digitalis ambigua. New Phytol 31:225–240CrossRefGoogle Scholar
  9. Caruso CM (1999) Pollination of Ipomopsis aggregata (Polemoniaceae): effects of intra- vs. interspecific competition. Am J Bot 86:663–668PubMedCrossRefGoogle Scholar
  10. Caruso CM (2002) Influence of plant abundance on pollination and selection on floral traits of Ipomopsis aggregata. Ecology 83:241–254Google Scholar
  11. Chittka L, Schürkens S (2001) Successful invasion of a floral market—an exotic Asian plant has moved in on Europe’s river-banks by bribing pollinators. Nature 411:653PubMedCrossRefGoogle Scholar
  12. Chittka L, Gumbert A, Kunze J (1997) Foraging dynamics of bumble bees: correlates of movements within and between plant species. Behav Ecol 8:239–249CrossRefGoogle Scholar
  13. Cross JR (1975) Rhododendron ponticum L. J Ecol 63:345–364CrossRefGoogle Scholar
  14. Erfmeier A, Bruelheide B (2004) Comparsion of native and invasive Rhododendron ponticum populations: growth, reproduction and morphology under field conditions. Flora 199:120–133Google Scholar
  15. Feinsinger P, Murray KG, Kinsman S, Busby WH (1986) Floral neighborhood and pollination success in four hummingbird-pollinated cloud forest plant species. Ecology 67:449–464CrossRefGoogle Scholar
  16. Feinsinger P, Tiebout HM III, Young BE (1991) Do tropical bird-pollinated plants exhibit density-dependent interactions? Field experiments. Ecology 72:1953–1963CrossRefGoogle Scholar
  17. Feldman TS (2008) The plot thickens: does low density affect visitation and reproductive success in a perennial herb, and are these effects altered in the presence of a co-flowering species? Oecologia 156:807–817PubMedCrossRefGoogle Scholar
  18. Fossitt JA (2000) A guide to habitats in Ireland, 1st edn. The Heritage Council, DublinGoogle Scholar
  19. Ghazoul J (2002) Flowers at the front line of invasion? Ecol Entomol 27:638–640CrossRefGoogle Scholar
  20. Ghazoul J (2004) Alien abduction: disruption of native plant–pollinator interactions by invasive species. Biotropica 36:156–164Google Scholar
  21. Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304CrossRefGoogle Scholar
  22. Gómez JM, Abdelaziz M, Lorite J, Jesús Muñoz-Pajares A, Perfectti F (2010) Changes in pollinator fauna cause spatial variation in pollen limitation. J Ecol 98:1243–1252CrossRefGoogle Scholar
  23. Goulson D, Wright NP (1998) Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae). Behav Ecol 9:213–219CrossRefGoogle Scholar
  24. Grabas GP, Laverty TM (1999) The effect of purple loosestrife (Lythrum salicaria L.; Lythraceae) on the pollination and reproductive success of sympatric co-flowering wetland plants. Ecoscience 6:230–242Google Scholar
  25. Grant V (1994) Modes and origins of mechanical and ethological isolation in angiosperms. Proc Natl Acad Sci USA 91:3–10PubMedCrossRefGoogle Scholar
  26. Harder LD (1990) Pollen removal by bumble bees and its implications for pollen dispersal. Ecology 71:1110–1125CrossRefGoogle Scholar
  27. Harder LD, Wilson WG (1998) Theoretical consequences of heterogeneous transport conditions for pollen dispersal by animals. Ecology 79:2789–2807CrossRefGoogle Scholar
  28. Hegland SJ, Boeke L (2006) Relationships between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecol Entomol 31:532–538CrossRefGoogle Scholar
  29. Hill PSM, Hollis J, Wells H (2001) Foraging decisions in nectarivores: unexpected interactions between flower constancy and energetic rewards. Anim Behav 62:729–737CrossRefGoogle Scholar
  30. Jakobsson A, Padrón B, Traveset A (2008) Pollen transfer from invasive Carpobrotus spp. to natives—a study of pollinator behaviour and reproduction success. Biol Conserv 141:136–145CrossRefGoogle Scholar
  31. Johnson SD, Peter CI, Nilsson LA, Ågren J (2003) Pollination success in a deceptive orchid is enhanced by co-occurring rewarding magnet plants. Ecology 84:2919–2927CrossRefGoogle Scholar
  32. Kalisz S, Vogler DW (2003) Benefits of autonomous selfing under unpredictable pollinator environments. Ecology 84:2928–2942CrossRefGoogle Scholar
  33. King MJ, Buchmann SL (1995) Bumble bee-initiated vibration release mechanism of Rhododendron pollen. Am J Bot 82:1407–1411CrossRefGoogle Scholar
  34. Kirchner F, Luijten SH, Imbert E, Riba M, Mayol M, González-Martínez SC, Mignot A, Colas B (2005) Effects of local density on insect visitation and fertilization success in the narrow-endemic Centaurea corymbosa (Asteraceae). Oikos 111:130–142CrossRefGoogle Scholar
  35. Knight ME, Martin AP, Bishop S, Osborne JL, Hale RJ, Sanderson RA, Goulson D (2005) An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species. Mol Ecol 14:1811–1820PubMedCrossRefGoogle Scholar
  36. Kunin WE (1997) Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. J Ecol 85:225–234CrossRefGoogle Scholar
  37. Larson DL, Royer RA, Royer MR (2006) Insect visitation and pollen deposition in an invaded prairie plant community. Biol Conserv 130:148–159CrossRefGoogle Scholar
  38. Levin DA, Anderson WW (1970) Competition for pollinators between simultaneously flowering species. Am Nat 104:455–467CrossRefGoogle Scholar
  39. 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 Lond B 270:775–781CrossRefGoogle Scholar
  40. Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant–pollinator network: an experimental approach. Ecol Lett 10:539–550PubMedCrossRefGoogle Scholar
  41. Mejías JA, Arroyo J, Ojeda F (2002) Reproductive ecology of Rhododendron ponticum (Ericaceae) in relict Mediterranean populations. Bot J Linn Soc 140:297–311CrossRefGoogle Scholar
  42. Moeller DA (2004) Facilitative interactions among plants via shared pollinators. Ecology 85:3289–3301CrossRefGoogle Scholar
  43. Morales CL, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Crit Rev Plant Sci 27:221–238CrossRefGoogle Scholar
  44. 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 12:716–728PubMedCrossRefGoogle Scholar
  45. Moroń D, Lenda M, Skórka P, Szentgyörgyi H, Settele J, Woyciechowski M (2009) Wild pollinator communities are negatively affected by invasion of alien goldenrods in grassland landscapes. Biol Conserv 142:1322–1332CrossRefGoogle Scholar
  46. Muñoz 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 96:459–467CrossRefGoogle Scholar
  47. Nazir R, Reshi Z, Wafai BA (2008) Reproductive ecology of medicinally important Kashmir Himalayan species of Digitalis L. Plant Species Biol 23:59–70CrossRefGoogle Scholar
  48. Nienhuis CM (2009) The interactions between native bees and alien plants. PhD dissertation, Trinity College Dublin, IrelandGoogle Scholar
  49. Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME, Goulson D, Hale RJ, Sanderson RA (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77:406–415PubMedCrossRefGoogle Scholar
  50. Palmer TM, Stanton ML, Young TP (2003) Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. Am Nat 162:S63–S79PubMedCrossRefGoogle Scholar
  51. Pappers SM, de Jong TJ, Klinkhamer PGL, Meelis E (1999) Effects of nectar content on the number of bumblebee approaches and the length of visitation sequences in Echium vulgare (Boraginaceae). Oikos 87:580–586CrossRefGoogle Scholar
  52. Parker IM, Haubensak KA (2002) Comparative pollinator limitation of two non-native shrubs: do mutualisms influence invasions? Oecologia 130:250–258Google Scholar
  53. Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle B, Moyle PB, Byers JE, Goldwasser L (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19CrossRefGoogle Scholar
  54. Percival M, Morgan P (1965) Observations on the floral biology of Digitalis species. New Phytol 64:1–22CrossRefGoogle Scholar
  55. Petanidou T, Ellis WN (1996) Interdependence of native bee faunas and floras in changing Mediterranean communities. In: Matheson A, Buchmann SL, O’Toole C, Westrich P, Williams IH (eds) The conservation of bees. Academic, London, pp 210–226Google Scholar
  56. Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol Syst 4:53–74CrossRefGoogle Scholar
  57. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists, 1st edn. Cambridge University Press, CambridgeGoogle Scholar
  58. Rathcke BJ (1983) Competition and facilitation among plants for pollination. In: Real LA (ed) Pollination biology. Academic, Orlando, pp 305–329Google Scholar
  59. Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107CrossRefGoogle Scholar
  60. 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 32:305–332CrossRefGoogle Scholar
  61. Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, Holt RD, Mayfield MM, O’Connor MI, Rice WR (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471PubMedCrossRefGoogle Scholar
  62. Somanathan H, Borges RM, Chakravarthy VS (2004) Does neighborhood floral display matter? Fruit set in carpenter bee-pollinated Heterophragma quadriloculare and beetle-pollinated Lasiosiphon eriocephalus. Biotropica 36:139–147Google Scholar
  63. Stang M, Klinkhamer PGL, van der Meijden E (2006) Size constraints and flower abundance determine the number of interactions in a plant–flower visitor web. Oikos 112:111–121CrossRefGoogle Scholar
  64. Stout JC (2007) Pollination of invasive Rhododendron ponticum (Ericaceae) in Ireland. Apidologie 38:198–206CrossRefGoogle Scholar
  65. Stout JC, Allen JA, Goulson D (1998) The influence of relative plant density and floral morphological complexity on the behaviour of bumblebees. Oecologia 117:543–550CrossRefGoogle Scholar
  66. Stout JC, Parnell JAN, Arroyo J, Crowe TP (2006) Pollination ecology and seed production of Rhododendron ponticum in native and exotic habitats. Biodivers Conserv 15:755–777CrossRefGoogle Scholar
  67. Thomson JD (1978) Effect of stand composition on insect visitation in two-species mixtures of Hieracium. Am Midl Nat 100:431–440CrossRefGoogle Scholar
  68. Totland Ø, Nielsen A, Bjerknes A-L, Ohlson M (2006) Effects of an exotic plant and habitat disturbance on pollinator visitation and reproduction in a boreal forest herb. Am J Bot 93:868–873PubMedCrossRefGoogle Scholar
  69. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216PubMedCrossRefGoogle Scholar
  70. Usher MB (1986) Invasibility and wildlife conservation: invasive species on nature reserves. Philos Trans R Soc Lond B 314:695–710CrossRefGoogle Scholar
  71. Vilà M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I, Stout JC, Tscheulin T (2009) Invasive plant integration into native plant–pollinator networks across Europe. Proc R Soc Lond B 276:3887–3893CrossRefGoogle Scholar
  72. Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. NZ J Ecol 21:1–16Google Scholar
  73. Waites AR, Ågren J (2004) Pollinator visitation, stigmatic pollen loads and among-population variation in seed set in Lythrum salicaria. J Ecol 92:512–526CrossRefGoogle Scholar
  74. Weidenhamer JD, Callaway RM (2010) Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J Chem Ecol 36:59–69PubMedCrossRefGoogle Scholar
  75. Westphal C, Steffan-Dewenter I, Tscharntke T (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol Lett 6:961–965CrossRefGoogle Scholar
  76. Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends Plant Sci 7:270–277PubMedCrossRefGoogle Scholar
  77. Wolf S, Moritz RFA (2008) Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae). Apidologie 39:419–427CrossRefGoogle Scholar
  78. Yurkonis KA, Meiners SJ (2004) Invasion impacts local species turnover in a successional system. Ecol Lett 7:764–769CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Anke Christiane Dietzsch
    • 1
    Email author
  • Dara Anne Stanley
    • 1
  • Jane Catherine Stout
    • 1
  1. 1.School of Natural Sciences, Botany BuildingTrinity CollegeDublin 2Ireland

Personalised recommendations