, Volume 156, Issue 4, pp 835–845 | Cite as

Displacement of a native by an alien bumblebee: lower pollinator efficiency overcome by overwhelmingly higher visitation frequency

  • Josefin A. Madjidian
  • Carolina L. Morales
  • Henrik G. Smith
Plant-Animal Interactions - Original Paper


Biological invasions might constitute a major threat to mutualisms. Introduced pollinators might competitively displace their native counterparts, which in turn affects the pollination of native plants, if native and alien visitors differ in pollinator effectiveness. Since its invasion in 1994 into south-west Argentina, the introduced European bumblebee Bombus ruderatus has continuously increased in abundance, along with a simultaneous decrease in the abundance of the native Bombus dahlbomii. The latter is the only native bumblebee species of the temperate forests of southern South America, and the main pollinator of the endemic herb Alstroemeria aurea. In order to evaluate the impact of the ongoing displacement of the native by the alien bumblebee, we compared the pollinator effectiveness (i.e., the combination of pollinator efficiency per visit and visitation frequency) between both bumblebee species, as well as related pollinator traits that might account for potential differences in pollinator efficiency. Native Bombus dahlbomii, which has a larger body and spent more time per flower, was the more efficient pollinator compared to Bombus ruderatus, both in terms of quantity and quality of pollen deposited per visit. However, Bombus ruderatus was a much more frequent flower visitor than Bombus dahlbomii. As a consequence, Bombus ruderatus is nowadays a more effective pollinator of A. aurea than its native congener. Despite the lack of evidence of an increase in seed set at the population level, comparisons with historical records of Bombus dahlbomii abundances prior to Bombus ruderatus’ invasion suggest that the overall pollination intensity of A. aurea might in fact have risen as a consequence of this invasion. Field experiments like these, that incorporate the natural variation in abundance of native and alien species, are powerful means to demonstrate that the consequences of invasions are more complex than previous manipulated and controlled experiments have suggested.


Alstroemeria aurea Bombus dahlbomii Bombus ruderatus Introduced species Pollinator effectiveness 



We thank M. Arbetman for field and laboratory assistance, the Adminstración de Parques Nacionales, Delegación Regional Patagonia (Argentina), for research permits, and the staff of Refugio Neumeyer for logistic support. Jane Stout and Marcelo Aizen provided valuable comments on a previous draft. We thank Marcelo Aizen for encouraging discussion and sharing ideas. J. A. M. was supported by the Exchange Program for Students and Teachers between the Universidad Nacional del Comahue (Argentina) and the Plant Ecology Department of Lund (Sweden), funded by Linnaeus-Palme. C. L. M. was supported by The Canon National Parks Science Scholars Program and the National Research Council of Argentina (CONICET). H. G. S was supported by a grant from the Swedish Research Council Formas. The experiments performed within this study comply with the current laws of Argentina.


  1. Abrahamovich A, Diaz NB (2001) Distribución geográfica de las especies del género Bombus Latreille (Hymenoptera, Apidae) en Argentina. Rev Bras Entomol 45:23–36Google Scholar
  2. Aizen MA (1997) Influence of local floral density and sex ratio on pollen receipt and seed output: empirical and experimental results in dichogamous Alstroemeria aurea (Alstroemeriaceae). Oecologia 111:404–412CrossRefGoogle Scholar
  3. Aizen MA (2001) Flower sex ratio, pollinator abundance, and the seasonal pollination dynamics of a protandrous plant. Ecology 82:127–144CrossRefGoogle Scholar
  4. Aizen MA, Basilio A (1995) Within and among flower sex-phase distribution in Alstroemeria aurea (Alstroemeriaceae). Can J Bot 73:1986–1994CrossRefGoogle Scholar
  5. Aizen MA, Basilio A (1998) Sex differential nectar secretion in protandrous Alstroemeria aurea (Alstroemeriaceae): is production altered by pollen removal and receipt? Am J Bot 85:245–252CrossRefGoogle Scholar
  6. Aizen MA, Feinsinger P (2003) Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation. In: Bradshaw G, Marquet P, Mooney HA (eds) How landscapes change: human disturbance and ecosystem disruptions in the Americas. Springer, New York, pp 112–119Google Scholar
  7. Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281PubMedCrossRefGoogle Scholar
  8. Aizen MA, Raffaele E (1996) Nectar production and pollination in Alstroemeria aurea: responses to level and pattern of flowering shoot defoliation. Oikos 76:312–322CrossRefGoogle Scholar
  9. Aizen MA, Raffaele E (1998) Flowering-shoot defoliation affects pollen grain size and post pollination performance in Alstroemeria aurea. Ecology 79:2133–2142Google Scholar
  10. Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PloS Biol 6:396–403CrossRefGoogle Scholar
  11. Aizen MA, Vázquez DP, Smith-Ramirez C (2002) Historia natural y conservacíon de los mutualismos planta-animal del bosque templade de Sudamérica austral. Rev Chil Hist Nat 75:79–97CrossRefGoogle Scholar
  12. Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122PubMedGoogle Scholar
  13. Arretz PV, Macfarlane RP (1986) The introduction of Bombus ruderatus to Chile for red clover pollination. Bee World 67:15–22Google Scholar
  14. Barthell JF, Randall JM, Thorp RW, Wenner AM (2001) Promotion of seed set in yellow star-thistle by honey bees: evidence of an invasive mutualism. Ecol Appl 11:1870–1883CrossRefGoogle Scholar
  15. Christian CE (2001) Consequences of biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639PubMedCrossRefGoogle Scholar
  16. Dick CW (2001) Genetic rescue of a remnant tropical tree by an alien pollinator. Proc Roy Soc Lond B 268:2391–2397CrossRefGoogle Scholar
  17. Feinsinger P, Tiebout HM (1991) Competition among plants sharing hummingbird pollinators: Laboratory experiments on a mechanism. Ecology 72:1946–1952CrossRefGoogle Scholar
  18. Fumero-Cabán JJ, Meléndez-Ackerman EJ (2007) Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). Am J Bot 94:419–424CrossRefGoogle Scholar
  19. Goulson D (2003a) Bumblebees. Their behaviour and ecology. Oxford University Press, OxfordGoogle Scholar
  20. Goulson D (2003b) Effects of introduced bees on native ecosystems. Annu Rev Ecol Syst 34:1–26CrossRefGoogle Scholar
  21. Goulson D, Stout JC, Langley J, Hughes WOH (2000) Identity and function of scent marks deposited by foraging bumblebees. J Chem Ecol 26:2897–2911CrossRefGoogle Scholar
  22. Gross CL, Mackay D (1998) Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae). Biol Cons 86:169–178CrossRefGoogle Scholar
  23. Harder LD, Aizen MA (2004) The functional significance of synchronous protandry in Alstroemeria aurea. Funct Ecol 18:467–474CrossRefGoogle Scholar
  24. Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am Nat 133:323–344CrossRefGoogle Scholar
  25. Herrera CM (1987) Components of pollinator “quality”: comparative analysis of a diverse insect assemblage. Oikos 50:79–90CrossRefGoogle Scholar
  26. Hingston AB, Potts BM, McQuillan PB (2004) The swift parrot, Lathamus discolour, (Psittacidae), social bees (Apidae) and native insects as pollinators of Eucalyptus globules ssp. Globules (Myrtaceae). Aust J Bot 52:371–379CrossRefGoogle Scholar
  27. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233CrossRefGoogle Scholar
  28. Inari N, Nagamitsu T, Kenta T, Goka K, Hiura T (2005) Spatial and temporal pattern of introduced Bombus terrestris abundance in Hokkaido, Japan, and its potential impact on native bumblebees. Popul Ecol 47:77–82CrossRefGoogle Scholar
  29. Inouye DW (1980) The effect of proboscis and corolla tube lengths on pattern and rates of flower visitation by bumblebees. Oecologia 45:197–201CrossRefGoogle Scholar
  30. Ivey CT, Martines P, Wyatt R (2003) Variation in pollinator effectiveness in swamp milkweed Asclepias incarnata (Apocynaceae). Am J Bot 90:214–255CrossRefGoogle Scholar
  31. Kenta T, Inari N, Nagamitsu T, Goka K, Hiura T (2007) Commercialized European bumblebee can cause pollination disturbance: An experiment on seven native plant species in Japan. Biol Cons 134:298–309CrossRefGoogle Scholar
  32. Macfarlane RP, Gurr L (1995) Distribution of bumblebees in New Zealand. New Zeal Entomol 18:29–36Google Scholar
  33. Mendes do Carmo R, Villaron Franceschinelli E (2004) Introduced honeybees (Apis mellifera) reduce pollination success without affecting the floral resource taken by pollinators. Biotropica 36:371–376Google Scholar
  34. Michener CD (2000) The bees of the world. John Hopkins University Press, BaltimoreGoogle Scholar
  35. Morales CL (2006) Alteración del hábitat e interacciones entre especies nativas y exóticas a través de la polinización en Bosques Templados de Sudamérica Austral. Dissertation. Universidad Nacional del Comahue, BarilocheGoogle Scholar
  36. Morales CL (2007) Introducción de abejorros (Bombus) no nativas: causas, consecuencias ecológicas y perspectivas. Ecol Austral 17:51–65Google Scholar
  37. Morales CL, Aizen MA (2002) Does the invasion of alien plants promote invasion of alien flower visitors? A case study from the temperate forests of southern Andes. Biol Invasions 4:87–100CrossRefGoogle Scholar
  38. Morales CL, Aizen MA (2004) Potential displacement of the native bumblebee Bombus dahlbomii by the invasive Bombus ruderatus in NW Patagonia. In: Hartfelder K, De Jong D (eds) Proceedings of the 8th International Conference on Tropical Bees and VI Encontro sobre Abelhas. Riverao Preto, Brazil, pp 70–76Google Scholar
  39. Morales CL, Aizen MA (2006) Invasive mutualism and the structure of plant-pollinator interactions in the temperate forests of north-west Patagonia, Argentina. J Ecol 94:171–180CrossRefGoogle Scholar
  40. Premoli A, Aizen MA, Kitzberger TD, Raffaele E (2006) Situación ambiental de los bosques Andion-Patagónicos. In: Brown AD, Martínez Ortiz U, Acerbi M, Corchera J (eds) La Situación Ambiental Argentina 2005. Fundacion Vida Silvestre Argentina, Buenos Aires, pp 281–291Google Scholar
  41. Rebolledo RR, Martinez PH, Palma MR, Aguilera PA, Klein KC (2004) Actividad de visita de Bombus dahlbomii (Guérin) y Bombus ruderatus (F.) (Himenoptera: Apidae) sobre trébol rosado (Trifolium pratense L.) en la IX región de la Araucanía, Chile. Agric Téc (Chile) 64:245–250Google Scholar
  42. Roig-Alsina A, Aizen MA (1996) Bombus ruderatus Fabricius, un nuevo Bombus para la Argentina (Hymenoptera: Apidea). Physis 5:49–50Google Scholar
  43. Ruz L (2002) Bee pollinators introduced to Chile: a review. In: Kevan PG, Imperatriz-Fonseca VL (eds) Pollinating bees. The conservation link between agriculture and nature. Proceedings of the workshop on the conservation and sustainable use of pollinators in agriculture, with emphasis on bees. Ministry of Environment, Brasilia, pp 115–167Google Scholar
  44. Semmens TD, Turner E, Buttermore R (1993) Bombus terrestris (L.) (Hymenoptera: apidae) now established in Tasmania. Aust J Entomol 32:346CrossRefGoogle Scholar
  45. Souto CP, Aizen MA, Premoli AC (2002) Effects of crossing distance and genetic relatedness on pollen performance in Alstroemeria aurea (Alstroemeriaceae). Am J Bot 89:427–432CrossRefGoogle Scholar
  46. Stout JC, Goulson D (2001) The use of conspecific and interspecific scent marks by foraging bumblebees (Bombus spp.). Behav Ecol Sociobiol 43:317–326CrossRefGoogle Scholar
  47. Stout JC, Goulson D (2002) The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers. Behav Ecol Sociobiol 52:239–246CrossRefGoogle Scholar
  48. Torreta JP, Medan D, Abrahamovich AH (2006) First record of the invasive bumblebee Bombus terrestris (L.) (Hymenoptera, Apidae) in Argentina. Trans Am Entomol Soc 132:285–289Google Scholar
  49. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualism. Trends Ecol Evol 21:208–216PubMedCrossRefGoogle Scholar
  50. Vázquez DP, Simberloff D (2002) Ecological specialization and susceptibility to disturbance: conjectures and refutations. Am Nat 159:606–623CrossRefPubMedGoogle Scholar
  51. Vázquez DP, Morris W, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett 8:1088–1094CrossRefGoogle Scholar
  52. Wittenberg R, Cock JWM (2001) Invasive Alien species: a toolkit of best prevention and management practices. CAB International, OxfordshireGoogle Scholar
  53. Zamora R (2001) Functional equivalence in plant-animal interactions: ecological and evolutionary consequences. Oikos 88:442–447CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Josefin A. Madjidian
    • 1
    • 3
  • Carolina L. Morales
    • 2
  • Henrik G. Smith
    • 1
  1. 1.Department of Ecology, Plant Ecology and SystematicsLund UniversityLundSweden
  2. 2.Laboratorio EcotonoUniversidad Nacional del ComahueBarilocheArgentina
  3. 3.Plant Ecology and SystematicsLundSweden

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