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Alien parasite hitchhikes to Patagonia on invasive bumblebee

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Abstract

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.

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References

  • Abrahamovich AH, Tellería MC, Díaz NB (2001) Bombus species and their associated flora in Argentina. Bee World 82(2):76–87

    Google Scholar 

  • 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):56–63

    Article  Google Scholar 

  • Arretz P, Macfarlane R (1986) The introduction of Bombus ruderatus to Chile for red clover pollination. Bee World 67:15–22

    Google Scholar 

  • Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee Bombus terrestris. Evolution 55(8):1639–1643

    PubMed  CAS  Google Scholar 

  • 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 America

  • 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):1282–1286

    Article  Google Scholar 

  • 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):461–467

    Article  Google Scholar 

  • 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):195–200

    Google Scholar 

  • Goka K, Okabe K, Yoneda M (2006) Worldwide migration of parasitic mites as a result of bumblebee commercialization. Popul Ecol 48(4):285–291

    Article  Google Scholar 

  • Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53(1):191–208

    Article  PubMed  CAS  Google Scholar 

  • 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):421–451

    Article  Google Scholar 

  • 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):39–45

    Article  PubMed  CAS  Google Scholar 

  • Liersch S, Schmid-Hempel P (1998) Genetic variation within social insect colonies reduces parasite load. Proc R Soc Lond B Biol Sci 265(1392):221–225

    Article  Google Scholar 

  • 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):29–34

    Article  Google Scholar 

  • Macfarlane RP (2005) Mites associated with bumble bees (Bombus: Apidae) in New Zealand. Rec Canterb Mus 19:29–34

    Google Scholar 

  • Macfarlane RP, Lipa JJ, Liu HJ (1995) Bumble bee pathogens and internal enemies. Bee World 76(3):130–148

    Google Scholar 

  • 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):835–845

    Article  PubMed  Google Scholar 

  • 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 109:107–115

    PubMed  CAS  Google Scholar 

  • Meeus I, Brown MJF, De Graaf DC, Smagghe G (2011) Effects of invasive parasites on bumble bee declines. Conserv Biol 25(4):662–671

    Article  PubMed  Google Scholar 

  • 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):11–21

    Article  Google Scholar 

  • Morales CL (2007) Introducción de abejorros (Bombus) no nativos: causas, consecuencias ecológicas y perspectivas. Ecol austral 17:51–65

    Google Scholar 

  • Phillips AJ, Simon C (1995) Simple, efficient, and nondestructive DNA extraction protocol for arthropods. Ann Entomol Soc Am 88(3):281–283

    CAS  Google Scholar 

  • 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):263–265

    Article  PubMed  Google Scholar 

  • 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):131–135

    Article  Google Scholar 

  • 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):565–568

  • Roig-Alsina A, Aizen MA (1996) Bombus ruderatus Fabricius, un nuevo Bombus para la Argentina (Hymenoptera: Apidea). Physis 5:49–50

    Google Scholar 

  • Rutrecht ST, Brown MJF (2008) The life-history impact and implications of multiple parasites for bumble bee queens. Int J Parasitol 38(7):799–808

    Article  PubMed  Google Scholar 

  • 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 155–167

  • Schmid-Hempel P (2001) On the evolutionary ecology of host–parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–158

    Article  PubMed  CAS  Google Scholar 

  • 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):285–289

    Google Scholar 

  • Williams PH, Osborne JL (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40(3):367–387

    Article  Google Scholar 

Download references

Acknowledgments

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.

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Correspondence to Marina P. Arbetman.

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Arbetman, M.P., Meeus, I., Morales, C.L. et al. Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biol Invasions 15, 489–494 (2013). https://doi.org/10.1007/s10530-012-0311-0

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