Abstract
The European bumblebee, Bombus terrestris, is an invasive eusocial species whose distribution is expanding greatly beyond its native range because numerous colonies are imported to or locally produced in non-native countries for pollination of agricultural crops. Closely related species exist in Japan where the unrestricted import and use of B. terrestris has resulted in the establishment of wild colonies. Laboratory studies previously showed that B. terrestris and Japanese native species can copulate and produce fertilized eggs. Although these eggs do not hatch, the interspecific mating can cause a serious reproductive disturbance to native bumblebees. In this study, we determined the frequencies of interspecies mating between B. terrestris males and native bumblebee queens in the wild on the islands of Hokkaido and Honshu by analyzing the DNA sequences of spermatozoa stored in spermathecae of native queens. We found that 20.2% of B. hypocrita hypocrita queens and 30.2% of B. hypocrita sapporoensis queens had spermatozoa of B. terrestris males in their spermathecae. Given that a Bombus queen generally mates only once in her life, such high frequencies of interspecific mating with B. terrestris pose serious threats to the populations of native bumblebees in Japan.
Similar content being viewed by others
References
Abernethy K (1994) The establishment of a hybrid zone between red and sika deer (genus Cervus). Mo Ecol 3:551–562
Australian Hydroponics and Greenhouse Association (2005) Report on the terms of reference for assessing the suitability for live import into mainland Australia of the large earth bumblebee (Bombus terrestris L., 1758). In: The Australian Government Minister for the Environment and Heritage. http://www.environment.gov.au/biodiversity/trade-use/invitecomment/bombus-terrestris.html. Accessed 23 July 2008
Ayasse M, Paxton RJ, Tengo J (2001) Mating behavior and chemical communication in the order Hymenoptera. Annu Rev Entomol 46:31–78
Barlow ND, Goldson SL (2002) Alien invertebrates in New Zealand. In: Pimentel D (ed) Biological invasions: economic and environmental costs of alien plant, animal, and microbe species. CRC, Boca Raton, pp 195–216
Buttermore RE (1997) Observations of successful Bombus terrestris (L.) (Hymenoptera: Apidae) colonies in Southern Tasmania. Aust J Entomol 36:251–254
Dafni A (1998) The threat of Bombus terrestris spread. Bee World 79:113–114
Dafni A, Shmida A (1996) The possible ecological implications of the invasion of Bombus terrestris (L.) (Apidae) at Mt. Carmel, Israel. In: Matheson A, Buchmann SL, O’Toole CH, Westrich P, Williams IH (eds) The conservation of bees. Academic, London, pp 183–200
Dohzono IK, Kunitake KY, Yokoyama J, Goka K (2008) Alien bumble bee affects native plant reproduction through interactions with native bumble bees. Ecology 89:3082–3092
Duvoisin N, Baer B, Schmid-Hempel P (1999) Sperm transfer and male competition in a bumblebee. Anim Behav 58:743–749
Estoup A, Scholl A, Pouvreau A, Solignac M (1995) Monoandry and polyandry in bumble bees (Hymenoptera: Bombidae) as evidenced by highly variable microsatellites. Mol Ecol 4:89–93
Estoup A, Solignac M, Cornuet J-M, Goudet J, Scholl A (1996) Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol Ecol 5:19–31
Goka K, Okabe K, Yoneda M, Niwa S (2001) Bumblebee commercialization will cause worldwide migration of parasitic mites. Mol Ecol 10:2095–2099
Goka K, Okabe K, Yoneda M (2006) Worldwide migration of parasitic mites as a result of bumblebee commercialization. Pop Ecol 48:285–291
Goulson D (2003a) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34:1–26
Goulson D (2003b) Bumblebees: their behaviour and ecology. Oxford University Press, Oxford
Hingston AB, McQuillan PB (1998) Does the recently introduced bumblebee Bombus terrestris (Apidae) threaten Australian ecosystems? Aust J Ecol 23:539–549
Hingston AB, McQuillan PB (1999) Desplacement of Tasmanian native megachilid bees by the recently introduced bumblebee Bombus terrestris (Linnaeus, 1758) (Hymenoptera: Apidae). Aust J Zool 47:59–65
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. Pop Ecol 47:77–82
Ings TC, Raine NE, Chittka L (2005) Mating preference of commercially imported bumblebees (Bombus terrestris) in Britain (Hymenoptera: Apidae). Entomol Gener 28:233–238
Ings TC, Ward NL, Chittka L (2006) Can commercially imported bumble bees out-compete their native conspecifics? J Appl Ecol 43:940–948
Inoue MN, Yokoyama J, Washitani I (2008) Displacement of Japanese native bumblebees by the recently introduced Bombus terrestris (L.) (Hymenoptera: Apidae). J Insect Conserv 12:135–146
Ishii HS, Kadoya T, Kikuchi R, Suda S, Washitani I (2008) Habitat and flower resource partitioning by an exotic and three native bumble bees in central Hokkaido, Japan. Biol. Conserv. 141:2597–2607
Ito M (1991) Taxonomy, ecology and distribution of Japanese bumblebees. In: Heinrich B (ed) Bumblebee economics (Japanese version translated by Inoue T). Bun-ichi Sogo Shuppan, Tokyo, pp 258–292 (in Japanese)
Kanbe Y, Okada I, Yoneda M, Goka K, Tsuchida K (2008) Interspecific mating of the introduced bumblebee Bombus terrestris and the native Japanese bumblebee Bombus hypocrita sapporoensis results in inviable hybrids. Naturwissenschaften 95:1003–1008
Katayama E (1964) Observation on the later stage colonies of Bombus ardens Smith (Hymenoptera, Apidae). Kontyu 32:393–402 (in Japanese with English summary)
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 Conserv 134:298–309
Koyama J, Kakinohana H, Miyatake T (2004) Eradication of the melon fly from Japan: importance of behavior, ecology, genetics, and evolution. Annu Rev Entomol 49:331–349
Krieger GM, Duchateau M-J, van Doorn A, Ibarrra F, Francke W, Ayasse M (2006) Identification of queen sex pheromone components of the bumblebee Bombus terrestris. J Chem Ecol 32:453–471
Kunitake Y, Goka K (2006) A new aspect of alien species problem—ecological risks caused by commercialization of the native bumblebee, Bombus ignitus. Nature and Insects 41:37–40 (in Japanese)
Matsumura C, Yokoyama J, Washitani I (2004) Invasion status and potential ecological impacts of an invasive alien bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) naturalized in southern Hokkaido, Japan. Glob Environ Res 8:51–66
Mooney HA, Cleadland EE (2001) The evolutionary impact of invasive species. PNAS 98:5446–5451
Ono M (1998) Why is now the bumblebees? Nature and Insects 33:2–3 (in Japanese)
Payne CM, Laverty TM, Lachance MA (2003) The frequency of multiple paternity in bumble bee (Bombus) colonies based on microsatellite DNA at the B10 locus. Insect Soc 50:375–378
Perry WL, Feder JE, Dwyer G, Lodge DM (2001a) Hybrid zone dynamics and species replacement between Orconectes crayfish in a northern Wisconsin lake. Evolution 55:1153–1166
Perry WL, Feder JE, Lodge DM (2001b) Implications of hybridization between introduced and resident Orconectes crayfishes. Conserv Biol 15:1656–1666
Peters JM, Queller DC, Strassmann JE, Solis CR (1995) Maternity assignment and queen replacement in a social wasp. Proc R Soc Lond B 260:7–12
Rasmont P, Coppee A, Michez D, De Meulemeester T (2008) An overview of the Bombus terrestris (L. 1758) subspecies (Hymenoptera: Apidae). Ann Soc Entomol Fr (ns) 44:243–250
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Evol Syst 27:83–109
Ruz L (2002) Bee pollinators introduced to Chile: a review. In: Kevan P, Imperatriz Fonseca VL (eds) Pollinating bees—the conservation link between agriculture and nature. Ministry of Environment, Brasilia, pp 155–167
Schmid-Hempel R, Schmid-Hempel P (2000) Female mating frequencies in Bombus spp. from Central Europe. Insectes Soc 47:36–41
Semmens TD, Turner E, Buttermore R (1993) Bombus terrestris (L.) (Hymenoptera: Apidae) now established in Tasmania. J Aust Entomol 32:346
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York
Takahashi J, Itoh M, Shimizu I, Ono M (2008) Male parentage and queen mating frequency in the bumblebee Bombus ignitus (Hymenoptera: Bombinae). Ecol Res 23:937–942
Taniguchi S (1955) Biological studies on the Japanese bees II. Study on the nesting behavior of Bombus ardens Smith. Sc Rep Hyogo Univ Agric Ser Agr 2:89–96
Terzo M, Valterova I, Rasmont P (2007) Atypical secretions of the male cephalic labial glands in bumblebees: the case of Bombus (Rhodobombus) mesomelas Gerstaecker (Hymenoptera: Apidae). Chem Biodivers 4:1466–1471
Velthuibs HHW, van Doorn A (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37:421–445
Widmer A, Schmid-Hempel P, Estoup A, Scholl A (1998) Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary islands and Madeira. Heredity 81:563–572
Wilson KA, Magnuson JJ, Lodge DM, Hill AM, Kratz TK, Perry WL, Willis TV (2004) A long-term rusty crayfish (Orconectes rusticus) invasion: dispersal patterns and community change in a north temperate lake. Can J Fish Aquat Sci 61:2255–2266
Winston ML (1992) The biology and management of Africanized honey bees. Annu Rev Entomol 37:173–193
Yoneda M, Tsuchida K, Goka K (2008) Ecological risks of commercialized bumblebee and the Invasive Alien Species Act. Jpn J Appl Entomol Zool 52:47–62 (in Japanese)
Acknowledgments
We thank J. Yokoyama, T. Koide, M. Mitsuhata, Y. Saito, Y. Kida, I. Dohzono, M. N. Inoue, and L. Kawaguchi for kindly providing insect specimens, and K. Suzuki, N. Yoshiuchi, A. Nakane, and M. Kaieda for technical and secretarial support. We also thank the editor and anonymous reviewers for their valuable comments on this manuscript. This research was part of the Research Project for Sophistication of Study for Agriculture, Forestry and Fisheries supported by the Ministry of Agriculture, Forestry and Fisheries of Japan, entitled “Development of Control Methods against Ecological Risks of Commercial Bumblebee for Pollination” (2005–2007, no. 1701, chief K.G.).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kondo, N.I., Yamanaka, D., Kanbe, Y. et al. Reproductive disturbance of Japanese bumblebees by the introduced European bumblebee Bombus terrestris . Naturwissenschaften 96, 467–475 (2009). https://doi.org/10.1007/s00114-008-0495-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-008-0495-4