Effectiveness of native bumblebees as pollinators of the alien invasive plant Impatiens glandulifera (Balsaminaceae) in Ireland

Authors

  • Caroline Nienhuis
  • Jane Stout

DOI:

https://doi.org/10.26786/1920-7603(2009)1

Keywords:

Alien plant, <I>Bombus pascuorum</I>, pollen deposition, pollen removal, morphological matching

Abstract

Flowers of alien invasive plants can be pollen limited due to a lack of effective pollinators. The alien Impatiens glandulifera is predominantly visited by bumblebees in its invaded range. There bumblebees pollinate I. glandulifera, but it remains unclear whether foraging behaviour or bumblebee or flower morphology affects effectiveness. We investigated the effectiveness of native bumblebee (Bombus pascuorum) pollinators in Ireland by quantifying pollen deposition and removal, and seed production after a single bumblebee visit. Morphological characteristics of flowers and bumblebee body parts were measured to determine their influence on pollen deposition and removal. B. pascuorum is a highly effective pollinator of the alien due to its high visitation frequency, the morphological fit with flowers and individuals removing large pollen quantities and inducing maximum seed set after a single visit. The impact of native bumblebees on I. glandulifera pollination and the implications of the pollination mechanism of the alien for its successful spread are discussed.

References

Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (ed) The Genetics of Colonizing Species, Academic Press, New York, pp 147-168.

Barrow DA, Pickard RS (1984) Size-related selection of food plants by bumblebees. Ecological Entomology 9: 369-373. DOI: https://doi.org/10.1111/j.1365-2311.1984.tb00832.x

Beerling DJ, Perrins JM (1993) Impatiens glandulifera Royle (Impatiens roylei Walp.). Journal of Ecology 81: 367-382. DOI: https://doi.org/10.2307/2261507

Bell G, Lefebvre L, Giraldeau L-A, Weary D (1984) Partial preference of insects for male flowers of an annual herb. Oecologia 64: 287-294. DOI: https://doi.org/10.1007/BF00379123

Chittka L, Schürkens S (2001) Successful invasion of a floral market. Nature 411: 653. DOI: https://doi.org/10.1038/35079676

Crawley MJ (1993) GLIM for Ecologists. Blackwell, Oxford.

Faegri K, Van der Pijl L (1966) The Principles of Pollination Ecology. Pergamon, Oxford.

Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35: 375-403. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Fukuda Y, Suzuki F, Murata J (2001) The function of each sepal in pollinator behaviour and effective pollination in Aconitum japonicum var. montanum. Plant Species Biology 16: 151-157. DOI: https://doi.org/10.1046/j.1442-1984.2001.00059.x

Fumero-Cabán JJ, Meléndez-Ackerman EJ (2007) Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). American Journal of Botany 94: 419-424. DOI: https://doi.org/10.3732/ajb.94.3.419

Fussell M, Corbet SA (1992) Flower usage by bumblebees - a basis for forage plant management. Journal of Applied Ecology 29: 451-465. DOI: https://doi.org/10.2307/2404513

Harder LD, Thomson JD (1989) Evolutionary options for maximising pollen dispersal of animal-pollinated plants. The American Naturalist 133: 323-344. DOI: https://doi.org/10.1086/284922

Herrera CM (1987) Components of pollinator "quality": comparative analysis of a diverse insect assemblage. Oikos 50: 79-90. DOI: https://doi.org/10.2307/3565403

Hiei K, Suzuki F (2001) Visitation frequency of Melampyrum roseum var. japonicum (Scrophulariaceae) by three bumblebee species and its relation to pollination efficiency. Canadian Journal of Botany 79: 1167-1174. DOI: https://doi.org/10.1139/b01-095

Hodges D (1964) Pollen Grain Drawings from 'The Pollen Loads of the Honeybee'. Bee Research Association, London.

Hollander M, Wolfe DA (1999) Nonparametric Statistical Methods. John Wiley & Sons, New York.

Hurlbert AH, Hosoi SA, Temeles EJ, Ewald PJ (1996) Mobility of Impatiens capensis flowers: effect on pollen deposition and hummingbird foraging. Oecologia 105: 243-246. DOI: https://doi.org/10.1007/BF00328553

Könies H, Glavač V (1979) Über die Konkurrenzfähigkeit des Indischen Springkrautes (Impatiens glandulifera ROYLE) am Fuldaufer bei Kassel. Philippia 4: 47-59.

Larson KC, Fowler SP, Walker JC (2002) Lack of pollinators limits fruit set in the exotic Lonicera japonica. American Midland Naturalist 148: 54-60. DOI: https://doi.org/10.1674/0003-0031(2002)148[0054:LOPLFS]2.0.CO;2

Levine JM, Vilà M, D'Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proceedings of the Royal Society B-Biological Sciences 270: 775-781. DOI: https://doi.org/10.1098/rspb.2003.2327

Lopezaraiza-Mikel ME (2006) The impact of alien species on native pollination systems. PhD, University of Bristol, Bristol.

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. Ecology Letters 10: 539-550. DOI: https://doi.org/10.1111/j.1461-0248.2007.01055.x

Mack RN, Simberloff D, Lonsdale MW, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10: 689-710. DOI: https://doi.org/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2

Manchester SJ, Bullock JM (2000) The impacts of non-native species on UK biodiversity and the effectiveness of control. Journal of Applied Ecology 37: 845-864. DOI: https://doi.org/10.1046/j.1365-2664.2000.00538.x

Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proceedings of the Royal Society B-Biological Sciences 269: 2395-2399. DOI: https://doi.org/10.1098/rspb.2002.2174

Milbau A, Stout JC (2008) Factors associated with alien plants transitioning from casual, to naturalized, to invasive. Conservation Biology 22: 308-317. DOI: https://doi.org/10.1111/j.1523-1739.2007.00877.x

Minitab (2000) MINITABTM Statistical Software for Windows. Release 13.30, State College, Pensylvania.

Moore PD, Webb JA, Collinson ME (1999) Pollen Analysis. Blackwell Scientific, Oxford.

Morales CL, Aizen MA (2002) Does invasion of exotic plants promote invasion of exotic flower visitors? A case study from the temperate forests of the southern Andes. Biological Invasions 4: 87-100. DOI: https://doi.org/10.1023/A:1020513012689

Parker IM (1997) Pollinator limitation of Cytisus scoparius (Scotch Broom), an invasive exotic shrub. Ecology 78: 1457-1470. DOI: https://doi.org/10.1890/0012-9658(1997)078[1457:PLOCSS]2.0.CO;2

Parker IM, Haubensak KA (2002) Comparative pollinator limitation of two non-native shrubs: do mutualisms influence invasions? Oecologia 130: 250-258. DOI: https://doi.org/10.1007/s004420100799

Perrins J, Fitter A, Williamson M (1993) Population biology and rates of invasion of three introduced Impatiens species in the British Isles. Journal of Biogeography 20: 33-44. DOI: https://doi.org/10.2307/2845737

Prowse A, Goodridge F (2000) Pollinator visitation rates of Impatiens glandulifera and other native riparian vegetation. Aspects of Applied Biology 58: 249-254.

Pyšek P, Prach K (1995) Invasion dynamics of Impatiens glandulifera: a century of spreading reconstructed. Biological Conservation 74: 41-48. DOI: https://doi.org/10.1016/0006-3207(95)00013-T

Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge. DOI: https://doi.org/10.1017/CBO9780511806384

Richardson DM (2004) Plant invasion ecology - dispatches from the front line. Diversity and Distributions 10: 315-319. DOI: https://doi.org/10.1111/j.1366-9516.2004.00129.x

Richardson DM, Allsopp N, D'Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions - the role of mutualisms. Biological Reviews 75: 65-93. DOI: https://doi.org/10.1111/j.1469-185X.1999.tb00041.x

Saini MS, Ghattor HS (2007) Taxonomy and food plants of some bumble bee species of Lahaul and Spiti valley of Himachal Pradesh. Zoos' Print Journal 22: 2648-2657. DOI: https://doi.org/10.11609/JoTT.ZPJ.1434.2648-57

Sawyer R, Pickard RS (1981) Pollen Identification for Beekeepers. University College Cardiff Press, Cardiff.

Schemske DW (1978) Evolution of reproductive characteristics in Impatiens (Balsaminaceae): the significance of cleistogamy and chasmogamy. Ecology 59: 596-613. DOI: https://doi.org/10.2307/1936588

Schemske DW, Horvitz CC (1984) Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225: 519-521. DOI: https://doi.org/10.1126/science.225.4661.519

Showler K (1989) The Himalayan balsam in Britain: an undervalued source of nectar. Bee World 70: 130-131.

Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1: 21-32. DOI: https://doi.org/10.1023/A:1010086329619

Sowig P (1989) Effects of flowering plants patch size on species composition of pollinator communities, foraging strategies, and resource partitioning in bumblebees (Hymenoptera, Apidae). Oecologia 78: 550-558. DOI: https://doi.org/10.1007/BF00378747

SPSS (2006) SPSS for Windows. SPSS Inc., Chicago.

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: 111-121. DOI: https://doi.org/10.1111/j.0030-1299.2006.14199.x

Starý P, Tkalců B (1998) Bumble-bees (Hym., Bombidae) associated with the expansive touch-me-not, Impatiens glandulifera in wetland bio-corridors. Anzeiger für Schädlingskunde, Pflanzenschutz, Umweltschutz 71: 85-87. DOI: https://doi.org/10.1007/BF02770639

Stout JC (2007a) Pollination of invasive Rhododendron ponticum (Ericaceae) in Ireland. Apidologie 38: 1-9. DOI: https://doi.org/10.1051/apido:2006071

Stout JC (2007b) Reproductive biology of the invasive exotic shrub, Rhododendron ponticum L. (Ericaceae). Botanical Journal of the Linnean Society 155: 373-381. DOI: https://doi.org/10.1111/j.1095-8339.2007.00719.x

Stout JC, Kells AR, Goulson D (2002) Pollination of the invasive exotic shrub Lupinus arboreus (Fabaceae) by introduced bees in Tasmania. Biological Conservation 106: 425-434. DOI: https://doi.org/10.1016/S0006-3207(02)00046-0

Stout JC, Parnell JAN, Arroyo J, Crowe TP (2006) Pollination ecology and seed production of Rhododendron ponticum in native and exotic habitats. Biodiversity and Conservation 15: 755-777. DOI: https://doi.org/10.1007/s10531-004-1065-5

Suzuki F, Dohzono I, Hiei K, Fukudas Y (2002) Pollination effectiveness of three bumblebee species on flowers of Hosta sieboldiana (Liliaceae) and its relation to floral structure and pollinator size. Plant Species Biology 17: 139-146. DOI: https://doi.org/10.1046/j.1442-1984.2002.00076.x

Thomson JD (1986) Pollen transport and deposition by bumble bees in Erythronium: influences of floral nectar and bee grooming. Journal of Ecology 74: 329-341. DOI: https://doi.org/10.2307/2260258

Titze A (2000) The efficiency of insect pollination of the neophyte Impatiens glandulifera (Balsaminaceae). Nordic Journal of Botany 20: 33-42. DOI: https://doi.org/10.1111/j.1756-1051.2000.tb00729.x

Traveset A, Willson MF, Sabag C (1998) Effect of nectar-robbing birds on fruit set of Fuchsia magellanica in Tierra Del Fuego: a disrupted mutualism. Functional Ecology 12: 459-464. DOI: https://doi.org/10.1046/j.1365-2435.1998.00212.x

Traynor L (1981) Use of a fast and accurate method for evaluating pollen production of Alfalfa and Almond flowers. American Bee Journal 121: 23-25.

Valentine DH (1978) The pollination of introduced species, with special reference to the British Isles and the genus Impatiens. In: Richards AJ (ed) The Pollination of Flowers by Insects, Academic Press, London, pp 117-123.

Willis SG, Hulme PE (2002) Does temperature limit the invasion of Impatiens glandulifera and Heracleum mantegazzianum in the UK? Functional Ecology 16: 530-539. DOI: https://doi.org/10.1046/j.1365-2435.2002.00653.x

Willis SG, Hulme PE (2004) Environmental severity and variation in the reproductive traits of Impatiens glandulifera. Functional Ecology 18: 887-898. DOI: https://doi.org/10.1111/j.0269-8463.2004.00907.x

Wilson P (1995) Selection for pollination success and the mechanical fit of Impatiens flowers around bumblebee bodies. Biological Journal of the Linnean Society 55: 355-383. DOI: https://doi.org/10.1006/bijl.1995.0047

Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72: 1503-1507. DOI: https://doi.org/10.2307/1941124

Wilson P, Thomson JD (1996) How do flowers diverge? In: Lloyd DG, Barrett SCH (ed) Floral Biology: Studies on Floral Evolution in Animal-Pollinated Systems, Chapman and Hall, New York, pp 88-111. DOI: https://doi.org/10.1007/978-1-4613-1165-2_4

Young HJ, Dunning DW, von Hasseln KW (2007) Foraging behaviour affects pollen removal and deposition in Impatiens capensis (Balsaminaceae). American Journal of Botany 94: 1267-1271. DOI: https://doi.org/10.3732/ajb.94.7.1267

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Published

2009-11-13

How to Cite

Nienhuis, C., & Stout, J. (2009). Effectiveness of native bumblebees as pollinators of the alien invasive plant Impatiens glandulifera (Balsaminaceae) in Ireland. Journal of Pollination Ecology, 1, 1–11. https://doi.org/10.26786/1920-7603(2009)1

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