, Volume 174, Issue 1, pp 217–226 | Cite as

Does the invasive Lupinus polyphyllus increase pollinator visitation to a native herb through effects on pollinator population sizes?

  • Anna JakobssonEmail author
  • Benigno Padrón
Plant-microbe-animal interactions - Original research


Invasive plants may compete with native species for abiotic factors as light, space and nutrients, and have also been shown to affect native pollination interactions. Studies have mainly focused on how invasive plants affect pollinator behaviour, i.e. attraction of pollinators to or away from native flowers. However, when an invasive plant provides resources utilized by native pollinators this could increase pollinator population sizes and thereby pollination success in natives. Effects mediated through changes in pollinator population sizes have been largely ignored in previous studies, and the dominance of negative interactions suggested by meta-analyses may therefore be biased. We investigated the impact of the invasive Lupinus polyphyllus on pollination in the native Lotus corniculatus using a study design comparing invaded and uninvaded sites before and after the flowering period of the invasive. We monitored wild bee abundance in transects, and visit rate and seed production of potted Lotus plants. Bumblebee abundance increased 3.9 times in invaded sites during the study period, whereas it was unaltered in uninvaded sites. Total visit rate per Lotus plant increased 2.1 times in invaded sites and decreased 4.4 times in uninvaded sites. No corresponding change in seed production of Lotus was found. The increase in visit rate to Lotus was driven by an increase in solitary bee visitation, whereas mainly bumblebees were observed to visit the invasive Lupinus. The mechanism by which the invasive increases pollinator visit rates to Lotus could be increased availability of other flower resources for solitary bees when bumblebees forage on Lupinus.


Pollination Wild bees Flower resources Seed production Agricultural landscape 



We are grateful for many constructive comments on the text from professor J. Ågren and two anonymous reviewers. We also thank P. Börjesson for statistical advice. The study was financed by grants to A. Jakobsson from the foundation Oscar and Lilli Lamms Minne and the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning. The experiments comply with the current laws of Sweden in which the experiments were performed.


  1. Anonymous (2005) Blomsterlupinen och dess bekämpning. The Finnish Environment Institute
  2. 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
  3. Bartomeus I, Vilà M, Santamaría L (2008b) Contrasting effects of invasive plants in plant–pollinator networks. Oecologia 155:761–770PubMedCrossRefGoogle Scholar
  4. 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
  5. Brown BJ, Randall JM, Graham SA (2002) Competition for pollination between an invasive species (Purple loosestrife) and a native congener. Ecology 83:2328–2336CrossRefGoogle Scholar
  6. Carvell C, Roya DB, Smart SM, Pywella RF, Prestona CD, Goulson C (2006) Declines in forage availability for bumblebees at a national scale. Biol Conserv 132:481–489CrossRefGoogle Scholar
  7. Chittka L, Schürkens S (2001) Successful invasion of a floral market. Nature 411:653PubMedCrossRefGoogle Scholar
  8. Corbet SA et al (2001) Native or exotic? Double or single? Evaluating plants for pollinator-friendly gardens. Ann Bot 87:219–232CrossRefGoogle Scholar
  9. Dietzsch AC, Stanley DA, Stout JC (2011) Relative abundance of an invasive alien plant affects native pollination processes. Oecologia 167:469–479PubMedCrossRefGoogle Scholar
  10. Frisborg A (2009) Främmande arter i Västra Götalands län. In. Länsstyrelsen i Västra Götalands län Naturvårdsenheten.
  11. Goulson D, Hughes W, Derwent L, Stout JC (2002) Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130:267–273Google Scholar
  12. Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208PubMedCrossRefGoogle Scholar
  13. 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
  14. Herrmann F, Westphal C, Moritz RFA, Steffan-Dewenter I (2007) Genetic diversity and mass resources promote colony size and forager densities of a social bee (Bombus pascuorum) in agricultural landscapes. Mol Ecol 16:1167–1178PubMedCrossRefGoogle Scholar
  15. 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
  16. Jakobsson A, Padrón B, Traveset A (2009) Competition for pollinators between invasive and native plants: effects of spatial scale of investigation (Note). Ecoscience 16:138–141CrossRefGoogle Scholar
  17. Kandori I, Hirao T, Matsunaga S, Kurosaki T (2009) An invasive dandelion unilaterally reduces the reproduction of a native congener through competition for pollination. Oecologia 159:559–569PubMedCrossRefGoogle Scholar
  18. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Sys 29:83–112CrossRefGoogle Scholar
  19. Kowarik I (2003) Human agency in biological invasions: secondary releases foster naturalisation and population expansion of alien plant species. Biol Invasions 5:293–312Google Scholar
  20. Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816PubMedCrossRefGoogle Scholar
  21. Lambdon P et al (2008) Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia 80:101–149Google Scholar
  22. Larson DL, Royer RA, Royer MR (2006) Insect visitation and pollen deposition in an invaded prairie plant community. Biol Conserv 130:148–159Google Scholar
  23. Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on native plant-pollinator network: and experimental approach. Ecol Lett 10:539–550PubMedCrossRefGoogle Scholar
  24. McGregor S (1976) Insect pollination of cultivated crop plantsGoogle Scholar
  25. Memmott J, Waser NM (2002) Integration of alien plants into a native flower–pollinator visitation web. Proc R Soc Lond B 269:2395–2399CrossRefGoogle Scholar
  26. Mitchell RJ, Flanagan R, Brown B, Waser N, Karron J (2009) New frontiers in competition for pollination. Ann Bot 103:1403–1413PubMedCrossRefGoogle Scholar
  27. Montero-Castaño A, Vilà M (2012) Impact of landscape alteration and invasions on pollinators: a meta-analysis. J Ecol 100:884–893CrossRefGoogle Scholar
  28. 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
  29. 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
  30. Moron 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
  31. 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
  32. Nielsen C, Heimes C, Kollmann J (2008) Little evidence for negative effects of an invasive alien plant on pollinator services. Biol Invasions. doi: 10.1007/s10530-007-9210-1 Google Scholar
  33. Nienhuis CM, Dietzsch AC, Stout JC (2009) The impacts of an invasive alien plant and its removal on native bees. Apidologie 40:450–463CrossRefGoogle Scholar
  34. Öckinger E, Smith HG (2007) Semi-natural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59CrossRefGoogle Scholar
  35. Osborne JL et al (2008) Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. J Appl Ecol 45:784–792CrossRefGoogle Scholar
  36. Padrón B, Traveset A, Biedenweg T, Díaz D, Nogales M, Olesen J (2009) Impact of alien plant invaders on pollination networks in two archipelagos. PLoS ONE 4:e6275. doi: 6210.1371/journal.pone.0006275 PubMedCentralPubMedCrossRefGoogle Scholar
  37. Pettersson MW, Cederberg B, Nilsson LA (2004) Grödor och vildbin i Sverige: Kunskapssammanställning för hållbar utveckling av insektspollinerad matproduktion och biologisk mångfald i jordbrukslandskapet. In: ArtDatabanken, SLU and Department of Plant Ecology Uppsala UniversityGoogle Scholar
  38. Potts S, Biesmeijer J, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353PubMedCrossRefGoogle Scholar
  39. Ramula S, Pihlaja K (2012) Plant communities and the reproductive success of native plants after the invasion of an ornamental herb. Biol Invasions 14:2079–2090CrossRefGoogle Scholar
  40. Ricketts TH et al (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515PubMedCrossRefGoogle Scholar
  41. Sakai AK et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  42. Samnegård U, Persson AS, Smith HG (2011) Gardens benefit bees and enhance pollination in intensively managed farmland. Biol Conserv 144:2602–2606CrossRefGoogle Scholar
  43. Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440CrossRefGoogle Scholar
  44. Stout JC, Morales C (2009) Ecological impacts of invasive alien species on bees. Apidologie 40:388–409CrossRefGoogle Scholar
  45. Tepedino VJ, Bradley BA, Griswold TL (2008) Might flowers of invasive plants increase native bee carrying capacity? Intimations from Capitol Reef National Park, Utah. Nat Areas J 28:44–50CrossRefGoogle Scholar
  46. Totland Ø, Nielsen A, Bjerknes A-L, Ohlsob 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
  47. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216PubMedCrossRefGoogle Scholar
  48. Valdovinos FS, Ramos-Jiliberto R, Flores JD, Espinoza C, López G (2009) Structure and dynamics of pollination networks: the role of alien plants. Oikos 118:1190–1200CrossRefGoogle Scholar
  49. Valtonen A, Jantunen J, Saarinen K (2006) Flora and lepidoptera fauna adversely affected by invasive Lupinus polyphyllus along road verges. Biol Conserv 133:389–396CrossRefGoogle Scholar
  50. Vilà M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I (2009) Invasive plant integration into native plant-pollinator networks across Europe. Proc R Soc Lond B 276:3887–3893CrossRefGoogle Scholar
  51. Waser NM, Real LA (1979) Effective mutualism between sequentially flowering plant species. Nature 281:670–672CrossRefGoogle Scholar
  52. Westphal C, Steffan-Dewenter I, Tscharntke T (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol Lett 6:961–965CrossRefGoogle Scholar
  53. Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149:289–300PubMedCrossRefGoogle Scholar
  54. Westphal C, Steffan-Dewenter I, Tscharntke T (2009) Mass flowering oilseed rape improves early colony growth but not sexual reproduction of bumblebees. J Appl Ecol 46:187–193CrossRefGoogle Scholar
  55. Williams NM, Cariveau D, Winfree R, Kremen C (2011) Bees in disturbed habitats use, but do not prefer, alien plants. Basic Appl Ecol 12:332–341CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Plant Ecology and Evolution, Department of Ecology and Genetics, EBCUppsala UniversityUppsalaSweden
  2. 2.Frontera-El Hierro, Santa Cruz de TenerifeSpain

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