Biological Invasions

, Volume 15, Issue 3, pp 489–494 | Cite as

Alien parasite hitchhikes to Patagonia on invasive bumblebee

  • Marina P. ArbetmanEmail author
  • Ivan Meeus
  • Carolina L. Morales
  • Marcelo A. Aizen
  • Guy Smagghe
Invasion Note


The worldwide trade in bumblebees can lead to the spread of diseases, which in turn has been claimed as a factor in bumblebee decline. Populations of the introduced Bombus terrestris, which invaded NW Patagonia, Argentina, in 2006, harbor the highly pathogenic protozoan Apicystis bombi. We asked whether A. bombi had been co-introduced with B. terrestris, and if so, whether spillover occurred to the two resident bumblebee species in the region: the introduced European Bombus ruderatus and the native Bombus dahlbomii. We searched for A. bombi by means of PCR in samples of B. ruderatus and B. dahlbomii collected before and after the invasion of B. terrestris and in samples of the latter. We found no A. bombi in samples of B. ruderatus and B. dahlbomii collected before B. terrestris invasion, whereas post invasion, A. bombi was present in all 3 species. The identity of the parasite was established by sequencing the 18S region, which was identical for the three bumblebee species and also matched the European sequence, confirming it to be A. bombi. This is the first report of A. bombi in B. ruderatus and B. dahlbomii. Moreover, our results suggest that Patagonia had been free of A. bombi until this parasite was co-introduced with B. terrestris, and spilled over in situ to these two previously resident species. Finally, our findings provide indirect circumstantial evidence of a potential link between the population collapse and geographic retraction of B. dahlbomii and the introduction of this novel parasite.


Apicystis bombi Bombus dahlbomii Bombus ruderatus Mattesia bombi Bumblebee parasites Bombus terrestris 



We thank the National Parks Administration of Argentina (APN) staff for sampling permits and Felix Vidoz and Andres Novaro for logistics during field work. H. Lestani, M. Zorzoli, M. Sabatino, Y. Sassal, A. Saez, G. Amico and J. Paritsis kindly provided bumblebee samples. This study was partially financed by Rufford Small Grant and the Canon National Parks Science Scholars Program to CLM, and the Research Council of Ghent University (BOF-UGent), the Fund for Scientific Research-Flanders (FWO-Vlaanderen, Belgium) and the Flemish agency for Innovation by Science and Technology (IWT-Vlaanderen, Brussels). CLM and MAA are researchers at the National Research Council of Argentina (CONICET). We specially thank to D. Goulson, M. Nuñez, an anonymous reviewer and to the Editor-in-Chief D. Simberloff whose constructive comments and suggestions helped to clarify and improve this paper.

Supplementary material

10530_2012_311_MOESM1_ESM.doc (66 kb)
Supplementary material 1 (DOC 66 kb)


  1. Abrahamovich AH, Tellería MC, Díaz NB (2001) Bombus species and their associated flora in Argentina. Bee World 82(2):76–87Google Scholar
  2. Allen GR, Seeman OD, Schmid-Hempel P, Buttermore RE (2007) Low parasite loads accompany the invading population of the bumblebee, Bombus terrestris in Tasmania. Insectes Soc 54(1):56–63CrossRefGoogle Scholar
  3. Arretz P, Macfarlane R (1986) The introduction of Bombus ruderatus to Chile for red clover pollination. Bee World 67:15–22Google Scholar
  4. Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee Bombus terrestris. Evolution 55(8):1639–1643PubMedGoogle Scholar
  5. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL (2011) Patterns of widespread decline in North American bumble bees. In: Proceedings of the national academy of sciences of the United States of AmericaGoogle Scholar
  6. Cankaya NE, Kaftanoglu O (2006) An investigation on some diseases and parasites of bumblebee queens (Bombus terrestris L.) in Turkey. Pak J Biol Sci 9(7):1282–1286CrossRefGoogle Scholar
  7. Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129(4):461–467CrossRefGoogle Scholar
  8. Frampton M, Droege S, Conrad T, Prager S, Richards MH (2008) Evaluation of specimen preservatives for DNA analyses of bees. J Hymenopt Res 17(2):195–200Google Scholar
  9. Goka K, Okabe K, Yoneda M (2006) Worldwide migration of parasitic mites as a result of bumblebee commercialization. Popul Ecol 48(4):285–291CrossRefGoogle Scholar
  10. Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53(1):191–208PubMedCrossRefGoogle Scholar
  11. Hayo HWV, van Adriaan D (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37(4):421–451CrossRefGoogle Scholar
  12. Junqueira ACM, Lessinger AC, Azeredo-Espin AML (2002) Methods for the recovery of mitochondrial DNA sequences from museum specimens of myiasis-causing flies. Med Vet Entomol 16(1):39–45PubMedCrossRefGoogle Scholar
  13. Liersch S, Schmid-Hempel P (1998) Genetic variation within social insect colonies reduces parasite load. Proc R Soc Lond B Biol Sci 265(1392):221–225CrossRefGoogle Scholar
  14. Lipa JJ, Triggiani O (1996) Apicystis gen nov and Apicystis bombi (Liu, Macfarlane & Pengelly) comb nov (Protozoa: Neogregarinida), a cosmopolitan parasite of Bombus and Apis (Hymenoptera: Apidae). Apidologie 27(1):29–34CrossRefGoogle Scholar
  15. Macfarlane RP (2005) Mites associated with bumble bees (Bombus: Apidae) in New Zealand. Rec Canterb Mus 19:29–34Google Scholar
  16. Macfarlane RP, Lipa JJ, Liu HJ (1995) Bumble bee pathogens and internal enemies. Bee World 76(3):130–148Google Scholar
  17. Madjidian JA, Morales CL, Smith HG (2008) Displacement of a native by an alien bumblebee: Lower pollinator efficiency overcome by overwhelmingly higher visitation frequency. Oecologia 156(4):835–845PubMedCrossRefGoogle Scholar
  18. Meeus I, de Graaf DC, Jans K, Smagghe G (2010) Multiplex PCR detection of slowly-evolving trypanosomatids and neogregarines in bumblebees using broad-range primers. J Appl Microbiol 109:107–115PubMedGoogle Scholar
  19. Meeus I, Brown MJF, De Graaf DC, Smagghe G (2011) Effects of invasive parasites on bumble bee declines. Conserv Biol 25(4):662–671PubMedCrossRefGoogle Scholar
  20. Montalva J, Dudley L, Kalin Arroyo M, Retamales H, Abrahamovich AH (2011) Geographic distribution and associated flora of native and introduced bumble bees (Bombus spp.) in Chile. J Apic Res 50(1):11–21CrossRefGoogle Scholar
  21. Morales CL (2007) Introducción de abejorros (Bombus) no nativos: causas, consecuencias ecológicas y perspectivas. Ecol austral 17:51–65Google Scholar
  22. Phillips AJ, Simon C (1995) Simple, efficient, and nondestructive DNA extraction protocol for arthropods. Ann Entomol Soc Am 88(3):281–283Google Scholar
  23. Plischuk S, Lange CE (2009) Invasive Bombus terrestris (Hymenoptera: Apidae) parasitized by a flagellate (Euglenozoa: Kinetoplastea) and a neogregarine (Apicomplexa: Neogregarinorida). J Invertebr Pathol 102(3):263–265PubMedCrossRefGoogle Scholar
  24. Plischuk S, Martín-Hernández R, Prieto L, Lucía M, Botías C, Meana A, Abrahamovich AH, Lange C, Higes M (2009) South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera). Environ Microbiol Rep 1(2):131–135CrossRefGoogle Scholar
  25. Plischuk S, Meeus I, Smagghe G, Lange CE (2011) Apicystis bombi (Apicomplexa: Neogregarinorida) parasitizing Apis mellifera and Bombus terrestris (Hymenoptera: Apidae) in Argentina. Environ Microbiol Rep 3(5):565–568Google Scholar
  26. Roig-Alsina A, Aizen MA (1996) Bombus ruderatus Fabricius, un nuevo Bombus para la Argentina (Hymenoptera: Apidea). Physis 5:49–50Google Scholar
  27. Rutrecht ST, Brown MJF (2008) The life-history impact and implications of multiple parasites for bumble bee queens. Int J Parasitol 38(7):799–808PubMedCrossRefGoogle Scholar
  28. Ruz L (2002) Bee pollinators introduced to chile: a Review. In: VL KPIF (ed) Pollinating bees—the conservation link between agriculture and nature. Ministry of Environment/Brasília, pp 155–167Google Scholar
  29. Schmid-Hempel P (2001) On the evolutionary ecology of host–parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–158PubMedCrossRefGoogle Scholar
  30. Torretta JP, Medan D, Abrahamovich AH (2006) First record of the invasive bumblebee Bombus terrestris (L.) (Hymenoptera, Apidae) in Argentina. Trans Am Entomol Soc 132(3 & 4):285–289Google Scholar
  31. Williams PH, Osborne JL (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40(3):367–387CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Marina P. Arbetman
    • 1
    • 2
    Email author
  • Ivan Meeus
    • 3
  • Carolina L. Morales
    • 2
  • Marcelo A. Aizen
    • 2
  • Guy Smagghe
    • 3
  1. 1.Universidad Nacional de Río NegroBarilocheArgentina
  2. 2.Laboratorio Ecotono, Centro Regional Universitario BarilocheUniversidad Nacional del Comahue—INIBIOMA (Conicet)BarilocheArgentina
  3. 3.Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium

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