Biological Invasions

, Volume 12, Issue 8, pp 2751–2763 | Cite as

Shading by invasive shrub reduces seed production and pollinator services in a native herb

Original Paper


Plant invasions disrupt native plant reproduction directly via competition for light and other resources and indirectly via competition for pollination. Furthermore, shading by an invasive plant may reduce pollinator visitation and therefore reproduction in native plants. Our study quantifies and identifies mechanisms of these direct and indirect effects of an invasive shrub on pollination and reproductive success of a native herb. We measured pollinator visitation rate, pollen deposition, and female reproductive success in potted arrays of native Geranium maculatum in deciduous forest plots invaded by the non-native shrub Lonicera maackii and in two removal treatments: removal of aboveground L. maackii biomass and removal of flowers. We compared fruit and seed production between open-pollinated and pollen-supplemented plants to test for pollen and light limitation of reproduction. Plots with L. maackii had significantly lower light, pollinator visitation rate, and conspecific pollen deposition to G. maculatum than biomass removal plots. Loniceramaackii flower removal did not increase pollinator visitation or pollen deposition compared to unmanipulated invaded plots, refuting the hypothesis of competition for pollinators. Thus, pollinator-mediated impacts of invasive plants are not limited to periods of co-flowering or pollinator sharing between potential competitors. Geranium maculatum plants produced significantly fewer seeds in plots containing L. maackii than in plant removal plots. Seed set was similar between pollen-supplemented and open-pollinated plants, but pollen-supplemented plants exhibited higher seed set in plant removal plots compared to invaded plots. Therefore, we conclude that the mechanism of impact of L. maackii on G. maculatum reproduction was increased understory shade.


Competition Ecosystem service Lonicera maackii Pollinator visitation Pollen limitation 


  1. Agren A, Willson MF (1991) Gender variation and sexual differences in reproductive characters and seed production in gynodioecious Geranium maculatum. Am J Bot 78:470–480CrossRefGoogle Scholar
  2. Agren A, Willson MF (1992) Determinants of seed production in Geranium maculatum. Oecologia 92:177–182CrossRefGoogle Scholar
  3. Bartomeus I, Bosch J, Vila M (2008a) High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community. Ann Bot 102:417–424CrossRefPubMedGoogle Scholar
  4. Bartomeus I, Vila M, Santamaria L (2008b) Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155:761–770CrossRefPubMedGoogle Scholar
  5. Bertin RI, Sholes ODV (1993) Weather, pollination, and the phenology of Geranium maculatum. Am Midl Nat 129:52–66CrossRefGoogle Scholar
  6. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemuller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354CrossRefPubMedGoogle Scholar
  7. Bjerknes AL, Totland O, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12CrossRefGoogle Scholar
  8. Braithwaite RW, Lonsdale WM, Estbergs JA (1989) Alien vegetation and native biota in tropical Australia—the impact of Mimosa—Pigra. Biol Conserv 48:189–210CrossRefGoogle Scholar
  9. Brown BJ, Mitchell RJ (2001) Competition for pollination: effects of pollen of an invasive plant on seed set of a native congener. Oecologia 129:43–49CrossRefGoogle Scholar
  10. 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
  11. Campbell DR (1985) Pollinator sharing and seed set of Stellaria pubera: competition for pollination. Ecology 66:544–553CrossRefGoogle Scholar
  12. Cariveau DP, Norton AP (2009) Spatially contingent interactions between an exotic and native plant mediated through flower visitors. Oikos 118:107–114CrossRefGoogle Scholar
  13. 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 411:653–653CrossRefPubMedGoogle Scholar
  14. Cipollini KA, McClain GY, Cipollini D (2008) Separating above- and belowground effects of Alliaria petiolata and Lonicera maackii on the performance of Impatiens capensis. Am Midl Nat 160:117–128CrossRefGoogle Scholar
  15. Collier MH, Vankat JL, Hughes MR (2002) Diminished plant richness and abundance below Lonicera maackii, an invasive shrub. Am Midl Nat 147:60–71CrossRefGoogle Scholar
  16. Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296CrossRefGoogle Scholar
  17. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  18. Eickwort GC, Ginsberg HS (1980) Foraging and mating behavior in Apoidea. Annu Rev Entomol 25:421–446CrossRefGoogle Scholar
  19. Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71:757–764CrossRefGoogle Scholar
  20. Ghazoul J (2002) Flowers at the front line of invasion? Ecol Entomol 27:638–640CrossRefGoogle Scholar
  21. Ghazoul J (2004) Alien abduction: disruption of native plant-pollinator interactions by invasive species. Biotropica 36:156–164Google Scholar
  22. Goodell K (2008) Invasive exotic plant-bee interactions. In: James RR, Pitts-Singer TL (eds) Bee Pollination in Agroecosystems. Oxford University Press, Oxford, pp 166–183CrossRefGoogle Scholar
  23. Goodell K, Iler AM (2007) Reproduction and habitat-dependent pollinator services in the invasive shrub Lonicera maackii. Ohio Invasive Plants Research Conference, The Ohio Biological Survey, Delaware, OHGoogle Scholar
  24. Gorchov DL, Trisel DE (2003) Competitive effects of the invasive shrub Lonicera maackii (Rupr.) Herder (Caprifoliaceae), on the growth and survival of native tree seedlings. Plant Ecol 166:13–24CrossRefGoogle Scholar
  25. Gould AMA, Gorchov DL (2000) Effects of the exotic invasive shrub Lonicera maackii, amur honeysuckle, on survival and fecundity of native forest annual herbs. Am Midl Nat 144:36–50CrossRefGoogle Scholar
  26. 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
  27. Herrera CM (1995a) Floral biology, microclimate, and pollination by ectothermic bees in an early-blooming herb. Ecology 76:218–228CrossRefGoogle Scholar
  28. Herrera CM (1995b) Microclimate and individual variation in pollinators: flowering plants are more than their flowers. Ecology 76:1516–1524CrossRefGoogle Scholar
  29. Herrera CM (1997) Thermal biology and foraging responses of insect pollinators to the forest floor irradiance mosaic. Oikos 78:601–611CrossRefGoogle Scholar
  30. Herrera CM, Pellmyr O (2002) Plant-animal interactions an evolutionary approach. Blackwell Science, OxfordGoogle Scholar
  31. Hutchinson TF, Vankat JL (1997) Invasibility and effects of Amur honeysuckle in southwestern Ohio forests. Conserv Biol 11:1117–1124CrossRefGoogle Scholar
  32. Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, NiwotGoogle Scholar
  33. Knight TM, Steets JA, Ashman TL (2006) A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation. Am J Bot 93:271–277CrossRefGoogle Scholar
  34. Kudo G, Ida TY, Tani T (2008) Linkages between phenology, pollination, photosynthesis, and reproduction in deciduous forest understory plants. Ecology 89:321–331CrossRefPubMedGoogle Scholar
  35. Larson DL, Royer RA, Royer MR (2006) Insect visitation and pollen deposition in an invaded prairie plant community. Biol Conserv 130:148–159CrossRefGoogle Scholar
  36. Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B Biol Sci 270:775–781CrossRefGoogle Scholar
  37. Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from grace. Bioscience 46:18–24CrossRefGoogle Scholar
  38. Luken JO, Kuddes LM, Tholemeier TC (1997) Response of understory species to gap formation and soil disturbance in Lonicera maackii thickets. Restor Ecol 5:229–235CrossRefGoogle Scholar
  39. Martin MC (1965) An ecological life history of Geranium maculatum. Am Midl Nat 73:111–149CrossRefGoogle Scholar
  40. Martin PH, Canham CD, Marks PL (2009) Why forests appear resistant to exotic plant invasions: intentional introductions, stand dynamics, and the role of shade tolerance. Front Ecol Environ 7:142–149CrossRefGoogle Scholar
  41. Mazer SJ (2007) Status of pollinators in North America. Nature 450:1162–1163CrossRefGoogle Scholar
  42. McCall C, Primack RB (1987) Resources limit the fecundity of three woodland herbs. Oecologia 71:431–435CrossRefGoogle Scholar
  43. Miller KE, Gorchov GL (2004) The invasive shrub, Lonicera maackii, reduces growth and fecundity of perennial forest herbs. Oecologia 139:359–375CrossRefPubMedGoogle Scholar
  44. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vazquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740CrossRefPubMedGoogle Scholar
  45. Moragues E, Traveset A (2005) Effect of Carpobrotus spp. on the pollination success of native plant species of the Balearic Islands. Biol Conserv 122:611–619CrossRefGoogle Scholar
  46. Morales CL, Traveset A (2009) A meta-analysis of alien vs native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Lett 12:716–728CrossRefPubMedGoogle Scholar
  47. Mulcahy DL, Curtis PS, Snow AA (1983) Pollen competition in a natural population. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Academic Press, New York, pp 330–337Google Scholar
  48. 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 96:459–467CrossRefGoogle Scholar
  49. Nielsen C, Heimes C, Kollmann J (2008) Little evidence for negative effects of an invasive alien plant on pollinator services. Biol Invasions 10:1353–1363CrossRefGoogle Scholar
  50. Robertson C (1928) Flowers and insects. Privately published, Carlinville, p 221Google Scholar
  51. Schmidt KA, Whelan CJ (1999) Effects of exotic Lonicera and Rhamnus on songbird nest predation. Conserv Biol 13:1502–1506CrossRefGoogle Scholar
  52. Totland O (2001) Environment-dependent pollen limitation and selection on floral traits in an alpine species. Ecology 82:2233–2244CrossRefGoogle Scholar
  53. Totland O, Nielsen A, Bjerknes AL, Ohlson M (2006) Effects of an exotic plant and habitat disturbance on pollinator visitation and reproduction in a boreal forest herb. Am J Bot 93:868–873CrossRefGoogle Scholar
  54. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216CrossRefPubMedGoogle Scholar
  55. Trisel DE, Gorchov DL (1994) Regional distribution, ecological impact, and leaf phenology of the invasive shrub Lonicera maackii. Bull Ecol Soc Am 75:231Google Scholar
  56. Vitousek PM (1990) Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies. Oikos 57:7–13CrossRefGoogle Scholar
  57. Waser NM (1983) Competition for pollination and floral character differences among sympatric plant species: a review of the evidence. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Academic Press, New York, pp 277–293Google Scholar
  58. Willson MF, Miller LJ, Rathcke BJ (1979) Floral display in Phlox and Geranium: adaptive aspects. Evolution 33:52–63CrossRefGoogle Scholar
  59. Woods KD (1993) Effects of invasion by Lonicera tatarica L. on herbs and tree seedlings in four New England forests. Am Midl Nat 130:62–74CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Evolution, Ecology, and Organismal BiologyThe Ohio State UniversityColumbusUSA
  2. 2.Department of Evolution, Ecology, and Organismal BiologyThe Ohio State UniversityNewarkUSA

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