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Ecological impacts of invasive alien species on bees

Impacts écologiques d’espèces invasives étrangères sur les abeilles

Ökologische Folgen invasiver fremder Arten auf Bienen

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Abstract

We review direct and indirect impacts of invasive alien species (focussing on plants and insects) on native bees worldwide. Although there is a rapidly growing body of research into the effects of invasive alien plants on native plant pollination via disruption of native mutualisms, there has been little research on the impacts of invasive alien plants directly on bees. Such impacts are likely to vary according to the taxon of plant, the functional specificity of the native bees, and ecosystem context. Conversely, there have been more attempts to document impacts of invasive alien social bees on native bees. Most of these studies only indirectly evaluate competition for resources, have focused on a few native species and findings are sometimes contradictory. However, some studies showed strong negative impacts, suggesting that effects might be species-specific. Additionally, pathogen spillover and reproductive disruption due to interspecific mating has been demonstrated among some closely related taxa. Where we lack unequivocal evidence for impacts however, this should not be interpreted as lack of effect. We recommend that future studies are robustly designed and consider impacts on genetic, species (particularly solitary bees) and ecosystem biodiversity.

Zusammenfassung

Invasive fremde Arten sind wichtige Antreiber globaler Umweltveränderungen, indem sie direkt oder indirekt auf die einheimische Biodiversität und die Ökosystemprozesse Einfluss nehmen. Die durch einheimische Bienen erbrachten Bestäubungsleistungen werden allgemein durch einen weiten Bereich menschlicher Aktivitäten als gefährdet angesehen, im Blickpunkt dieser zusammenfassenden Untersuchung stehen potentielle Gefährdungen durch invasive Arten. Ziel des Artikels ist, den möglichen Einfluss invasiver fremder Arten auf die einheimischen Bienen abzuschätzen, um Gefährdungen bestimmen und Forschungsprioritäten in diesem Gebiet festlegen zu können. Wir berücksichtigten die Auswirkungen invasiver fremder Pflanzen, Bienen und Parasiten auf das Verhalten, die Populationen und Gesellschaften einheimischer Bienen und die Leistungen, die sie für das Ökosystem erbringen.

Invasive fremde Pflanzen können direkt oder indirekt auf die einheimischen Bienen Einfluss nehmen (Abb. 1). Direkter Einfluss beinhaltet die Bereitstellung von Blütenressourcen, wobei deren Wert entsprechend ihrer morphologischen Zugänglichkeit, Nährwert und der zeitlichen und räumlichen Verfügbarkeit der Belohnungen variiert. Ein indirekter Einfluss liegt vor, wenn invasive fremde Pflanzen die einheimische Pflanzengemeinschaft beeinflussen (entweder durch Wettbewerb um abiotische Ressourcen oder um biotische Ressourcen einschließlich der Bestäubung) (Tab. I). Insgesamt können Beeinflussungen des individuellen Verhaltens und Überlebens relativ leicht bestimmt werden, während dagegen Einflüsse auf Populationen oder Gesellschaften wesentlich schwerer vorauszusehen sind und bislang nur wenig untersucht wurden.

Der überwiegende Teil der Forschungen über die Auswirkung fremder invasiver Insekten auf die einheimischen Bienen hat sich auf die Auswirkungen von eingeführten sozialen Arten von Honigbienen oder Hummeln bezogen, die um Ressourcen oder Nistplätze in Konkurrenz stehen, die Verbreitung von Pathogenen und Krankheiten verursachen oder die Populationsstruktur durch Hybridisation oder Introgression beeinflussen. Trotz erheblicher Aufmerksamkeit der Forschung gibt es wenig schlüssige Nachweise für eine Kompetition zwischen fremden und einheimischen Bienen um Futterres-sourcen, hauptsächlich weil Untersuchungen zur Kompetition schwierig durchzuführen und zu interpretieren sind. Allerdings haben einige Untersuchungen eine Verminderung der Fitness einheimischer Bienen bei Anwesenheit invasiver fremder Bienen nachgewiesen. Es gibt allerdings so gut wie keine Untersuchungen zur Kompetition um andere Ressourcen als Futterressourcen, dies schließt Nistplätze trotz ihres offensichtlichen kompetitiven Potentials ein. Kürzlich wurde offensichtlich, dass insbesondere in Nordamerika eine der größten von eingeführten Bestäubern ausgehenden Gefährdungen ist, dass sie möglicherweise neuartige Pathogene und Krankheiten auf die einheimischen Bienen übertragen (Tab. II). Die Fähigkeit eingeführter Arten mit einheimischen Arten zu hybridisieren ist gut bekannt, und mit der Entwicklung molekularere Marker zur Erkennung einer Introgression dürfte das Ausmaß des Problems klarer werden.

Wir schlagen verschiedene Forschungsschwerpunkte vor, nämlich dass (1) Untersuchungen des Ausmaßes der Auswirkungen sollten sowohl in zeitliches als auch räumlicher Hinsicht erweitert werden, in einem robusten Versuchsdesign strukturiert sein und repliziert werden, (2) besondere Aufmerksamkeit sollte den Auswirkungen auf solitäre und spezialisierte Bienenarten zukommen, (3) eine schnelle Erfassung potentieller Auswirkungen neuer Eindringlinge sollte zu einer raschen Entscheidungsfindung, Überwachung und Entschärfung des Problems führen, (4) die Pathologie, Virulenz und Kreuzinfektiösität von Pathogenen und Parasiten muss besser verstanden werden, und (5) die Auswirkungen weiterer Umweltänderungen auf Grund des Klimawandels müssen wegen der potentiellen räumlichen und zeitlichen Verlagerungen bei invasiven und einheimischen Pflanzen und Bestäubern sowie ihrer Interaktionen in Betracht gezogen werden. Wir empfehlen, dass Erhaltungsmaßnahmen einheimischer Bestäuber eine hohe Priorität zukommen sollte und dass diese Angelegenheit auf der Ebene des gesamten Ökosystems betrachtet werden sollte und nicht anhand eines nur artbasierten Ansatzes.

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References

  • Aigner P.A. (2004) Ecological and genetic effects on demographic processes: pollination, clonality and seed production in Dithyrea maritima, Biol. Conserv. 116, 27–34.

    Article  Google Scholar 

  • Aizen M.A., Feinsinger P. (1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine ‘Chaco Serrano’, Ecol. Appl. 4, 378–392.

    Article  Google Scholar 

  • Aizen M.A., Feinsinger P. (2003) Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation, in: Bradshaw G., Marquet P. (Eds.), How landscapes change: Human disturbance and ecosystem disruptions in the Americas, Springer-Verlag, Berlin, pp. 111–129.

    Google Scholar 

  • Aizen M.A., Morales C.L., Morales J.M. (2008) Invasive mutualists erode native pollination webs, PLoS Biol. 6, e31.

    Article  PubMed  CAS  Google Scholar 

  • Akratanakul P., Burgett M. (1975) Varroa jacobsoni: a prospective pest of honeybees in many parts of the world, Bee World 56, 119–120.

    Google Scholar 

  • Altshuler D.L. (1999) Novel interactions of nonpollinating ants with pollinators and fruit consumers in a tropical forest, Oecologia 119, 600–606.

    Article  Google Scholar 

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

    Google Scholar 

  • Ashworth L., Aguilar R., Galetto L., Aizen M.A. (2004) Why do pollination generalist and specialist plant species show similar reproductive susceptibility to habitat fragmentation? J. Ecol. 92, 717–719.

    Article  Google Scholar 

  • Barthell J.F., Frankie G.W., Thorp R.W. (1998) Invader effects in a community of cavity nesting megachilid bees (Hymenoptera: Megachilidae), Environ. Entomol. 27, 240–247.

    Google Scholar 

  • Barthell J.F., Randall J.M., Thorp R.W., Wenner A.M. (2001) Promotion of seed set in yellow star-thistle by honey bees: evidence of an invasive mutualism, Ecol. Appl. 11, 1870–1883.

    Article  Google Scholar 

  • Bartomeus I., Bosch J., Vila M. (2008a) High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community, Ann. Bot. 102, 417–424.

    Article  PubMed  Google Scholar 

  • Bartomeus I., Vilà M., Santamaría L. (2008b) Contrasting effects of invasive plants in plant— pollinator networks, Oecologia 155, 761–770.

    Article  PubMed  Google Scholar 

  • Beekman M., Ratnieks F.L.W. (2000) Long-range foraging by the honey-bee, Apis mellifera L., Funct. Ecol. 14, 490–496.

    Article  Google Scholar 

  • Biesmeijer J.C., Roberts S.P.M., Reemer M., Ohlemüller R., Edwards M., Peeters T., Schaffers A.P., Potts S.G., Kleukers R., Thomas C.D., Settele J., Kunin W.E. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands, Science 313, 351–354.

    Article  PubMed  CAS  Google Scholar 

  • Bjerknes A.-L., Totland Ø., Hegland S.J., Nielsen A. (2007) Do alien plant invasions really affect pollination success in native plant species? Biol. Conserv. 138, 1–12.

    Article  Google Scholar 

  • Bronstein J.L. (1995) The plant-pollinator landscape, in: Hansson L., Fahrig L., Merriam G. (Eds.), Mosaic landscapes and ecological processes, Chapman and Hall, London, pp. 256–288.

    Google Scholar 

  • Brosi B.J., Daily G.C., Shih T.M., Oviedo F., Duran G. (2008) The effects of forest fragmentation on bee communities in tropical countryside, J. Appl. Ecol. 45, 773–783.

    Article  Google Scholar 

  • Brown B.J., Mitchell R.J., Graham S.A. (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener, Ecology 83, 2328–2336.

    Article  Google Scholar 

  • Brown M.J.F., Loosli R., Schmid-Hempel P. (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees, Oikos 91, 421–427.

    Article  Google Scholar 

  • Brown M.J.F., Schmid-Hempel R., Schmid-Hempel P. (2003) Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory, J. Anim. Ecol. 72, 994–1002.

    Article  Google Scholar 

  • Bull J.J. (1994) Virulence, Evolution 48, 1423–1437.

    Article  Google Scholar 

  • Buttermore R.E., Pomeroy N., Hobson W., Semmens T., Hart R. (1998) Assessment of the genetic base of Tasmaninan bumble bees (Bombus terrestris) for development as pollination agents, J. Apic. Res. 37, 23–25.

    Google Scholar 

  • Butz Huryn V. (1997) Ecological impacts of introduced honey bees, Q. Rev. Biol. 72, 275–97.

    Article  Google Scholar 

  • Butz Huryn V.M., Moller H. (1995) An assessment of the contribution of honey bees (Apis mellifera) to weed reproduction in New Zealand protected natural areas, N. Z. J. Ecol. 19, 111–122.

    Google Scholar 

  • Carey F., Lewis J., MacGregor J., Martin-Smith M. (1959) Pharmacological and chemical observations on some toxic nectars, J. Pharm. Pharmacol. 11, 269T-274T.

    Article  Google Scholar 

  • Chapman R.E., Bourke A.F.G. (2001) The influence of sociality on the conservation biology of social insects, Ecol. Lett. 4, 650–662.

    Article  Google Scholar 

  • Chittka L., Schurkens S. (2001) Successful invasion of a floral market, Nature 411, 653.

    Article  PubMed  CAS  Google Scholar 

  • Colla S.R., Otterstatter M.C., Gegear R.J., Thomson J.D. (2006) Plight of the bumble bee: Pathogen spillover from commercial to wild populations, Biol. Conserv. 129, 461–467.

    Article  Google Scholar 

  • Committee on the Status of Pollinators in North America, National Research Council (2007) Status of Pollinators in North America. The National Academies Press, Washington, D.C. [online] http://books.nap.edu/openbook.php?isbn=0309102898 (accessed on 03 March 2009).

    Google Scholar 

  • Cook S.M., Awmack C.S., Murray D.A., Williams I.H. (2003) Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol. Entomol. 28, 622–627.

    Article  Google Scholar 

  • Corbet S.A., Bee J., Dasmahapatra K., Gale S., Gorringe E., La Ferla B., Moorhouse T., Trevail A., Van Bergen Y., Vorontsova M. (2001) Native or exotic? Double or single? Evaluating plants for pollinator-friendly gardens, Ann. Bot. 87, 219–232.

    Article  Google Scholar 

  • Cresswell J.E., Osborne J.L., Goulson D. (2000) An economic model of the limits to foraging range in central place foragers with numerical solutions for bumblebees, Ecol. Entomol. 25, 249–255.

    Article  Google Scholar 

  • Darvill B., Knight M.E., Goulson D. (2004) Use of genetic markers to quantify bumblebee foraging range and nest density, Oikos 107, 471–478.

    Article  Google Scholar 

  • de Jong D.D., Morse R.A., Eickwort G.C. (1982) Mite pests of honey bees, Annu. Rev. Entomol. 27, 229–252.

    Article  Google Scholar 

  • De La Rúa P., Serrano J., Galián J. (2002) Biodiversity of Apis mellifera populations from Tenerife (Canary Islands) and hybridisation with East European races, Biodiv. Conserv. 11, 59–67.

    Article  Google Scholar 

  • De La Rúa P., Jaffé R., Dall’Olio R., Muñoz I., Serrano J. (2009) Biodiversity, conservation and current threats to European honeybees, Apidologie 40, 263–284.

    Article  Google Scholar 

  • Dehnen-Schmutz K., Williamson M. (2006) Rhododendron ponticum in Britain and Ireland: Social, economic and ecological factors in its successful invasion, Environ. Hist. 12, 325–350.

    Article  Google Scholar 

  • Donovan B.J. (1980) Interactions between native and introduced bees in New Zealand. N. Z. J. Ecol. 3, 104–116.

    Google Scholar 

  • Dornhaus A., Chittka L. (1999) Evolutionary origins of bee dances, Nature 401, 38–38.

    Article  CAS  Google Scholar 

  • Dornhaus A., Chittka L. (2001) Food alert in bumblebees (Bombus terrestris): possible mechanisms and evolutionary implications, Behav. Ecol. Sociobiol. 50, 570–576.

    Article  Google Scholar 

  • Dupont Y.L., Hansen D.M., Valido A., Olesen J.M. (2004) Impact of introduced honey bees on native pollination interactions of the endemic Echium wildpretii (Boraginaceae) on Tenerife, Canary Islands, Biol. Conserv. 118, 301–311.

    Article  Google Scholar 

  • Durrer S., Schmid-Hempel P. (1994) Shared use of flowers leads to horizontal pathogen transmission, Phil. Trans. R. Soc. Lond. 258, 299–302.

    Google Scholar 

  • Edwards M., Jenner M. (2005) Field guide to the bumblebees of Great Britain and Ireland, Ocelli Limited, United Kingdom.

    Google Scholar 

  • Estay P. (2007) Bombus en Chile: Especies, Biologia y Manejo, Colección de Libros INIA 22, Instituto de Investigaciones Agropecuarias, Centro Regional de Investigacion La Platina, Santiago, Chile.

    Google Scholar 

  • Fitzpatrick U., Murray T.E., Paxton R.J., Breen J., Cotton D., Santorum V., Brown M.J.F. (2007) Rarity and decline in bumblebees — A test of causes and correlates in the Irish fauna, Biol. Conserv. 136, 185–194.

    Article  Google Scholar 

  • Genersch E., Yue C., Fries I., de Miranda J.R. (2006) Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities, J. Invertebr. Pathol. 91, 61–63.

    Article  PubMed  Google Scholar 

  • Ghazoul J. (2002) Flowers at the front line of invasion? Ecol. Entomol. 27, 639–640.

    Article  Google Scholar 

  • Ghazoul J. (2004) Alien abduction: disruption of native plant-pollinator interactions by invasive species, Biotropica 36, 156–164.

    Google Scholar 

  • Ghazoul J. (2005) Buzziness as usual? Questioning the global pollination crisis, Trends Ecol. Evol. 20, 367–373.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Goka K., Okabe K., Yoneda M., Niwa S. (2001) Bumblebee commercialization will cause worldwide migration of parasitic mites, Mol. Ecol. 10, 2095–2099.

    Article  PubMed  CAS  Google Scholar 

  • Goodell K. (2000) The impact of honey bees on native solitary bees: competition and indirect effects, PhD Dissertation, State University of New York, New York.

    Google Scholar 

  • Goulson D. (2003) Effects of introduced bees on native ecosystems, Annu. Rev. Ecol. Evol. System. 34, 1–26.

    Article  Google Scholar 

  • Goulson D., Stout J.C. (2001) Homing ability of the bumblebee, Bombus terrestris, Apidologie 32, 105–112.

    Article  Google Scholar 

  • Goulson D., Stout J., Kells A. (2002) Do alien bumblebees compete with native flower-visiting insects in Tasmania? J. Insect Conserv. 6, 179–189.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grabas G.P., Laverty T.M. (1999) The effect of purple loosestrife (Lythrum salicaria L.; Lythraceae) on the pollination and reproductive success of sympatric co-flowering wetland plants, Ecoscience 6, 230–242.

    Google Scholar 

  • Gross C.L. (2001) The effect of introduced honeybees on native bee visitation and fruit-set in Dillwynia juniperina (Fabaceae) in a fragmented ecosystem, Biol. Conserv. 102, 89–95.

    Article  Google Scholar 

  • Gross C.L., Mackay D. (1998) Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae), Biol. Conserv. 86, 169–178.

    Article  Google Scholar 

  • Groves R.H. (1998) Recent incursions of weeds to Australia 1971–1995, CRC for Weed Management Systems Technical Series 3, 1–74.

    Google Scholar 

  • Herrmann F., Westphal C., Moritz R.F.A., Steffan-Dewenter I. (2007) Genetic diversity and mass resources promote colony size and forager densities of a social bee (Bombus pascuorum) in agricultural landscapes, Mol. Ecol. 16, 1167–1178.

    Article  PubMed  CAS  Google Scholar 

  • Higes M., Martín R., Meana A. (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe, J. Invertebr. Pathol. 92, 93–95.

    Article  PubMed  CAS  Google Scholar 

  • Hoehn P., Tscharntke T., Tylianakis J.M., Steffan-Dewenter I. (2008) Functional group diversity of bee pollinators increases crop yield, Proc. R. Soc. B: Biol. Sci. 275, 2283–2291.

    Article  Google Scholar 

  • Hoffmann D., Pettis J., Neumann P. (2008) Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens), Insectes Soc. 55, 153–162.

    Article  Google Scholar 

  • Holzschuh A., Steffan-Dewenter I., Kleijn D., Tscharntke T. (2007) Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context, J. Appl. Ecol. 44, 41–49.

    Article  Google Scholar 

  • Horskins K., Turner V. (1999) Resource use and foraging patterns of honeybees, Apis mellifera, and native insects on flowers of Eucalyptus costata, Aust. J. Ecol. 24, 221–227.

    Article  Google Scholar 

  • Huang W.-F., Jiang J.-H., Chen Y.-W., Wang C.-H. (2007) A Nosema ceranae isolate from the honeybee Apis mellifera, Apidologie 38, 30–37.

    Article  Google Scholar 

  • 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, 77–82.

    Article  Google Scholar 

  • Ings T.C., Raine N.E., Chittka L. (2005a) Mating preference of commercially imported bumblebees (Bombus terrestris) in Britain (Hymenoptera: Apidae), Entomol. Gen. 28, 233–238.

    Google Scholar 

  • Ings T.C., Schikora J., Chittka L. (2005b) Bumblebees, humble pollinators or assiduous invaders? A population comparison of foraging performance in Bombus terrestris, Oecologia 144, 508–516.

    Article  PubMed  Google Scholar 

  • Ings T.C., Ward N.L., Chittka L. (2006) Can commercially imported bumble bees out-compete their native conspecifics? J. Appl. Ecol. 43, 940–948.

    Article  Google Scholar 

  • Inouye D. (1977) Species structure of bumblebee communities in North America and Europe, in: Mattson W.J. (Ed.), The role of arthropods in forest ecosystems, Springer-Verlag, New York, pp. 35–40.

    Google Scholar 

  • Inouye D.W. (1980) The terminology of floral larceny, Ecology 61, 1251–1253.

    Article  Google Scholar 

  • Jakobsson A., Padrón B., Traveset A. (2007) Pollen transfer from invasive Carpobrotus spp. to natives — A study of pollinator behaviour and reproduction success, Biol. Conserv. 141, 136–145.

    Article  Google Scholar 

  • Jensen A.B., Palmer K.A., Boomsma J.J., Pedersen (2005) Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe, Molec. Ecol. 14, 93–106.

    Article  Google Scholar 

  • Jesse L.C., Moloney K.A., Obrycki J.J. (2006) Insect pollinators of the invasive plant, Rosa multiflora (Rosaceae), in Iowa, USA, Weed Biol. Manage. 6, 235–240.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kato M., Shibata A., Yasui T., Nagamasu H. (1999) Impact of introduced honeybee, Apis mellifera, upon native bee communities in the Bonin (Ogasawara) Islands, Res. Popul. Ecol. 41, 217–228.

    Article  Google Scholar 

  • Kearns C.A., Inouye D.W., Waser N.M. (1998) Endangered mutualisms: the conservation of plant-pollinator interactions, Annu. Rev. Ecol. System. 29, 83–112.

    Article  Google Scholar 

  • Keller I., Fluri P., Imdorf A. (2005) Pollen nutrition and colony development in honey bees: part I, Bee World 86, 3–10.

    Google Scholar 

  • Kenis M., Auger-Rozenberg M., Roques A., Timms L., Péré C., Cock M., Settele J., Augustin S., Lopez-Vaamonde C. (2009) Ecological effects of invasive alien insects, Biol. Invasions 11, 21–45.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Klein A.M., Vaissière B.E., Cane J.H., Steffan-Dewenter I., Cunningham S.A., Kremen C., Tscharntke T. (2007) Importance of pollinators in changing landscapes for world crops, Proc. R. Soc. B Biol. Sci. 274, 303–313.

    Article  Google Scholar 

  • Knight M.E., Martin A.P., Bishop S., Osborne J.L., Hale R.J., Sanderson R.A., Goulson D. (2005) An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species, Mol. Ecol. 14, 1811–1820.

    Article  PubMed  CAS  Google Scholar 

  • Koca I., Koca A.F. (2007) Poisoning by mad honey: A brief review, Food Chem. Toxicol. 45, 1315–1318.

    Article  PubMed  CAS  Google Scholar 

  • Kremen C., Williams N.M., Thorp R.W. (2002) Crop pollination from native bees at risk from agricultural intensification, Proc. Natl. Acad. Sci. USA 99, 16812–16816.

    Article  PubMed  CAS  Google Scholar 

  • Lach L. (2008) Argentine ants displace floral arthropods in a biodiversity hotspot, Diver. Distrib. 14, 281–290.

    Article  Google Scholar 

  • Lambdon P.W., Pyšek P., Basnou C., Hejda M., Arianoutsou M., Essl F., Jarošík V., Pergl J., Winter M., Anastasiu P., Andriopoulos P., Bazos I., Brundu G., Celesti-Grapow L., Chassot P., Delipetrou P., Josefsson M., Kark S., Klotz S., Kokkoris Y., Kühn I., Marchante H., Perglová I., Pino J., Vilà M., Zikos A., Roy D., Hulme P.E. (2008) Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs, Preslia 80, 101–149.

    Google Scholar 

  • Larson D.L., Royer R.A., Royer M.R. (2006) Insect visitation and pollen deposition in an invaded prairie plant community, Biol. Conserv. 130, 148–159.

    Article  Google Scholar 

  • Levine J.M., D’Antonio C.M. (2003) Forecasting biological invasions with increasing international trade, Conserv. Biol. 17, 322–326.

    Article  Google Scholar 

  • Levine J.M., Vila M., D’Antonio C.M., Dukes J.S., Grigulis K., Lavorel S. (2003) Mechanisms underlying the impacts of exotic plant invasions, Proc. R. Soc. Lond. B Biol. Sci. 270, 775–781.

    Article  Google Scholar 

  • Liu H., Pemberton R.W. (2008) Solitary invasive orchid bee outperforms co-occurring native bees to promote fruit set of an invasive Solanum, Oecologia DOI 10.1007/s00442-008-1232-6.

  • Lockwood J., Hoopes M., Marchetti M. (2007) Invasion Ecology, Wiley-Blackwell.

  • Lodge D. (1993) Biological invasions: lessons for ecology, Trends Ecol. Evol. 8, 133–137.

    Article  PubMed  CAS  Google Scholar 

  • Lopezaraiza Mikel M. (2006) The impact of alien species on native pollination systems, PhD Thesis, University of Bristol, Bristol.

    Google Scholar 

  • Lopezaraiza-Mikel M.E., Hayes R.B., Whalley M.R., Memmott J. (2007) The impact of an alien plant on a native plant-pollinator network: an experimental approach, Ecol. Lett. 10, 539–550.

    Article  PubMed  Google Scholar 

  • Losey J.E., Vaughan M. (2006) The economic value of ecological services provided by insects, Bioscience 56, 311–323.

    Article  Google Scholar 

  • MacFarlane R.P., Gurr B.L. (1995) Distribution of bumble bees in New Zealand, N. Z. Entomol. 18, 29–36.

    Google Scholar 

  • Macfarlane R.P., Lipa J.J., Liu H.J. (1995) Bumble bee pathogens and internal enemies, Bee World 76, 130–148.

    Google Scholar 

  • Martin P.H. (1999) Norway maple (Acer platanoides) invasion of a natural forest stand: understory consequence and regeneration pattern, Biol. Invasions 1, 215–222.

    Article  Google Scholar 

  • Memmott J., Waser N.M. (2002) Integration of alien plants into a native flower pollinator visitation web, Proc. R. Soc. B Biol. Sci. 269, 2395–2399.

    Article  Google Scholar 

  • Memmott J., Waser N.M., Price M.V. (2004) Tolerance of pollination networks to species extinctions, Proc. R. Soc. B Biol. Sci. 271, 2605–2611.

    Article  Google Scholar 

  • Mendes do Carmo R., Franceschinelli E.V., Silveira F.A. (2004) Introduced honeybees (Apis mellifera) reduce pollination success without affecting the floral resource taken by native pollinators, Biotropica 36, 371–376.

    Google Scholar 

  • Milbau A., Stout J.C. (2008) Factors associated with alien plants transitioning from casual, to naturalized, to invasive, Conserv. Biol. 22, 308–317.

    Article  PubMed  Google Scholar 

  • Moller H. (1996) Lessons for invasion theory from social insects, Biol. Conserv. 78, 125–142.

    Article  Google Scholar 

  • Mooney H.A., Cleland E.E. (2001) The evolutionary impact of invasive species, Proc. Natl. Acad. Sci. USA 98, 5446–5451.

    Article  PubMed  CAS  Google Scholar 

  • Moragues E., Traveset A. (2005) Effects of Carpobrotus spp. on the pollination success of native plant species of the Balearic Islands, Biol. Conserv. 122, 611–619.

    Article  Google Scholar 

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

    Google Scholar 

  • Morales C.L., Aizen M.A. (2002) Does invasion of exotic plants promote invasion of exotic flower visitors? A case study from the temperate forests of the southern Andes, Biol. Invasions 4, 87–100.

    Article  Google Scholar 

  • Morales C.L., Aizen M.A. (2006) Invasive mutualisms and the structure of plant—pollinator interactions in the temperate forests of north-west Patagonia, Argentina, J. Ecol. 94, 171–180.

    Article  Google Scholar 

  • Moritz R.F.A., Härtel S., Neumann P. (2005) Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity, Ecoscience 12, 289–301.

    Article  Google Scholar 

  • Muñoz A.A., Cavieres L.A. (2008) The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities, J. Ecol. 96, 459–467.

    Article  Google Scholar 

  • Murray T.E., Kuhlmann M., Potts S.G. (2009) Conservation ecology of bees: populations species and communities, Apidologie 40, 211–236.

    Article  Google Scholar 

  • Nagamitsu T., Kenta T., Inari N., Kato E., Hiura T. (2007) Abundance, body size, and morphology of bumblebees in an area where an exotic species, Bombus terrestris, has colonized in Japan, Ecol. Res. 22, 331–341.

    Article  Google Scholar 

  • Nielsen C., Heimes C., Kollmann J. (2008) Little evidence for negative effects of an invasive alien plant on pollinator services, Biol. Invasions 10, 1353–1363.

    Article  Google Scholar 

  • Ono M. (1997) Ecological implications of introducing Bombus terrestris and significance of domestication of Japanese native bumblebee (Bombus spp.), in: Proc. Int. Workshop on Biological Invasions of Ecosystem by Pests and Beneficial Organisms, NIAES, Ministry of Agriculture, Forestry and Fisheries, Japan, Tsukuba, pp. 244–252.

    Google Scholar 

  • Osborne J.L., Martin A.P., Carreck N.L., Swain J.L., Knight M.E., Goulson D., Hale R.J., Sanderson R.A. (2008) Bumblebee flight distances in relation to the forage landscape, J. Anim. Ecol. 77, 406–415.

    Article  PubMed  Google Scholar 

  • Otterstatter M.C., Thomson J.D. (2008) Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS Biol. 3, 1–9.

    Google Scholar 

  • Otti O., Schmid-Hempel P. (2007) Nosema bombi: A pollinator parasite with detrimental fitness effects, J. Invertebr. Pathol. 96, 118–124.

    Article  PubMed  Google Scholar 

  • Paini D.R. (2004) Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: A review, Aust. Ecol. 29, 399–407.

    Article  Google Scholar 

  • Paini D.R., Roberts J.D. (2005) Commercial honey bees (Apis mellifera) reduce the fecundity of an Australian native bee (Hylaeus alcyoneus), Biol. Conserv. 123, 103–112.

    Article  Google Scholar 

  • Paini D.R., Williams M.R., Roberts J.D. (2005) No short-term impact of honey bees on the reproductive success of an Australian native bee, Apidologie 36, 613–621.

    Article  Google Scholar 

  • Parker I.M. (1997) Pollinator limitation of Cytisus scoparius (Scotch broom), an invasive exotic shrub, Ecology 78, 1457–1470.

    Google Scholar 

  • Parker I.M., Simberloff D., Lonsdale W.M., Goodell K., Wonham M., Kareiva P.M., Williamson M.H., Von Holle B., Moyle P.B., Byers J.E., Goldwasser L. (1999) Impact: Toward a framework for understanding the ecological effects of invaders, Biol. Invasions 1, 3–19.

    Article  Google Scholar 

  • Pimentel D., Zuniga R., Morrison D. (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States, Ecol. Econ. 52, 273–288.

    Article  Google Scholar 

  • Pleasants J. (1981) Bumblebee response to variation in nectar availability, Ecology 62, 1648–1661.

    Article  Google Scholar 

  • Ponchau O., Iserbyt S., Verhaeghe J.C., Rasmont P. (2006) Is the caste-ratio of the oligolectic bumblebee Bombus gerstaeckeri Morawitz (Hymenoptera: Apidae) biased to queens? Ann. Soc. Entomol. Fr. 42, 207–214.

    Google Scholar 

  • Pyšek P., Pyšek A. (1995) Invasion by Heracleum mantegazzianum in different habitats in the Czech Republic, J. Veg. Sci. 6, 711–718.

    Article  Google Scholar 

  • Pyšek P., Jarošík V., Kučera T. (2003) Inclusion of native and alien species in temperate nature reserves: an historical study from Central Europe, Conserv. Biol. 17, 1414–1424.

    Article  Google Scholar 

  • Reichard S.H., White P. (2001) Horticulture as a pathway of invasive plant introductions in the United States, BioScience 51, 103–113.

    Article  Google Scholar 

  • Richardson D.M., Allsopp N., D’Antonio C.M., Milton S.J., Rejmánek M. (2000) Plant invasions — the role of mutualisms, Biol. Rev. 75, 65–93.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Roubik D. (1978) Competitive interactions between neotropical pollinators and Africanized honey bees, Science 201, 2030–1032.

    Article  Google Scholar 

  • Roubik D. (1982) Ecological impact of Africanized honeybees on native neotropical pollinators, in: Jaisson P. (Ed.), Social Insects in the Tropics 1, Univ. Paris-Nord, pp. 233–247.

  • Roubik D. (1983) Experimental community studies: time-series tests of competition between African and Neotropical bees, Ecology 64, 971–978.

    Article  Google Scholar 

  • Roubik D. (1991) Aspects of Africanized honey bee ecology in tropical America, in: Spirak M., Fletcher D.J.C., Breed M.D. (Eds.), The “African” honeybee, Westview Press, Boulder, Colorado, pp. 259–281.

    Google Scholar 

  • Roubik D. (1996) African honey bees as exotic pollinators in French Guiana, in: Matheson A., Buchmann S.L., O’Toole C., Westrich P., Williams I.D. (Eds.), The Conservation of Bees, Lin Soc Symp Series 18, Academic Press, London, pp. 73–182.

    Google Scholar 

  • Roubik D. (2001) Ups and downs in pollinator populations: when is there a decline? Conserv. Ecol. 5, 2.

    Google Scholar 

  • Roubik D.W., Wolda H. (2001) Do competing honey bees matter? Dynamics and abundance of native bees before and after honey bee invasion, Popul. Ecol. 43, 53–62.

    Article  Google Scholar 

  • Roulston T.H., Cane J.H., Buchmann S.L. (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecol. Monogr. 70, 617–643.

    Google Scholar 

  • Ruz L. (2002) Bee pollinators introduced to Chile: a review, in: Kevan P., Imperatriz Fonseca V. (Eds.), Pollinating bees — the conservation link between agriculture and nature, Ministry of Environment Brasília, pp. 155–167.

  • Ruz L., Herrera R. (2001) Preliminary observations on foraging activities if Bombus dahlbomii and Bombus terrestris (Hym: Apidae) on native and non-native vegetation in Chile, Acta Hortic. 561, 165–169.

    Google Scholar 

  • Sakagami S. (1976) Specific differences in the bionomic characters of bumblebees: a comparative review, J. Fac. Sci., Hokkaido University Series VI, Zoology 20, 390–447.

    Google Scholar 

  • Sala O.E., Chapin III F.S., Armesto J.J., Berlow E., Bloomfield J., Dirzo R., Huber-Sanwald E., Huenneke L.F., Jackson R.B., Kinzig A., Leemans R., Lodge D.M., Mooney H.A., Oesterheld M., Poff N.L., Sykes M., Walker B.H., Walker M., Wall D.H. (2000) Global biodiversity scenarios for the year 2100, Science 287, 1770–1774.

    Article  PubMed  CAS  Google Scholar 

  • Schaffer W.M., Zeh D.W., Buchmann S.L., Kleinhans S., Schaffer M.V., Antrim J. (1983) Competition for nectar between introduced honey bees and native North American bees and ants, Ecology 64, 564–577.

    Article  Google Scholar 

  • Schmid-Hempel P. (1998) Parasites in social insects, Princeton University Press.

  • Schmid Hempel P., Loosli R. (1998) A contribution to the knowledge of Nosema infections in bumble bees, Bombus spp., Apidologie 29, 525–535.

    Article  Google Scholar 

  • Schneider S.S., Hoffman G.D., Smith D.R. (2004) The African honey bee: Factors contributing to a successful biological invasion, Annu. Rev. Entomol. 49, 351–376.

    Article  CAS  Google Scholar 

  • Semmens T., Turner E., Buttermore R. (1993) Bombus terrestris (L.) (Hymenoptera, Apidae) now established in Tasmania, J. Aust. Entomol. Soc. 32.

  • Simberloff D. (1991) Keystone species and community effects of biological introductions, in: Ginzburg L. (Ed.), Assessing Ecological Risks of Biotechnology, Butterworth-Heinemann, Boston, MA, pp. 1–19.

    Google Scholar 

  • Spiewok S., Neumann P. (2006) Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida), Ecol. Entomol. 31, 623–628.

    Article  Google Scholar 

  • Steffan-Dewenter I., Kuhn A. (2003) Honeybee foraging in differentially structured landscapes, Proc. R. Soc. B Biol. Sci. 270, 569–575.

    Article  Google Scholar 

  • Steffan-Dewenter I., Westphal C. (2008) The interplay of pollinator diversity, pollination services and landscape change, J. Appl. Ecol. 45, 737–741.

    Article  Google Scholar 

  • Stokes K.E., Buckley Y.M., Sheppard A.W. (2006) A modelling approach to estimate the effect of exotic pollinators on exotic weed population dynamics: bumblebees and broom in Australia, Div. Distrib. 12, 593–600.

    Article  Google Scholar 

  • Stout J.C. (2007) Pollination of invasive Rhododendron ponticum (Ericaceae) in Ireland, Apidologie 38, 198–206.

    Article  Google Scholar 

  • Stout J., Goulson D. (2000) Bumblebees in Tasmania: their distribution and potential impact on Australian flora and fauna, Bee World 81, 80–86.

    Google Scholar 

  • Stout J., Kells A., Goulson D. (2002) Pollination of the invasive exotic shrub Lupinus arboreus (Fabaceae) by introduced bees in Tasmania, Biol. Conserv. 106, 425–434.

    Article  Google Scholar 

  • Stout J.C., Parnell J.A.N., Arroyo J., Crowe T.P. (2006) Pollination ecology and seed production of Rhododendron ponticum in native and exotic habitats, Biodiv. Conserv. 15, 755–777.

    Article  Google Scholar 

  • Sugden E.A., Pyke G.H. (1991) Effects of honey bees on colonies of Exoneura asimillima, an Australian native bee, Aust. Ecol. 16, 171–181.

    Article  Google Scholar 

  • Sudgen E.A., Thorp R.W., Buchmann S.L. (1996) Honey bee, native bee competition: focal point for environmental change and apicultural response in Australia, Bee World 77, 26–44.

    Google Scholar 

  • Tepedino V., Alston D., Bradley B., Toler T., Griswold T. (2007) Orchard pollination in Capitol Reef National Park, Utah, USA. Honey bees or native bees? Biodiv. Conserv. 16, 3083–3094.

    Article  Google Scholar 

  • Tepedino V.J., Bradley B.A., Griswold T.L. (2008) Might flowers of invasive plants increase native bee carrying capacity? Intimations from Capitol Reef National Park, Utah, Nat. Areas J. 28, 44–50.

    Article  Google Scholar 

  • Thomson D.M. (2004) Detecting the effects of introduced species: a case study of competition between Apis and Bombus, Oikos 114, 407–418.

    Article  Google Scholar 

  • Thomson D.M. (2006) Competitive interactions between the invasive European honey bee and native bumble bees, Ecology 85, 458–470.

    Article  Google Scholar 

  • Thorp R.W. (2003) Bumble bees (Hymenoptea: Apidae): commercial use and environmental concerns, in: Strickler K., Cane J.H. (Eds.), For non native crops, whence pollinators of the future? Thomas Say Publications in Entomology: Proceedings, Entomological Society of America, Lanham, MD, pp. 21–40.

    Google Scholar 

  • Thorp R., Shepherd M. (2005) Species profile: Subgenus Bombus, in: Shepherd M., Vaughan M., Black S. (Eds.), Red List of Pollinator Insects of North America, Xerces Society for Invertebrate Conservation, CD-ROM Version 1, Portland, OR.

    Google Scholar 

  • Totland O., Nielsen A., Bjerknes A.-L., Ohlson M. (2006) Effects of an exotic plant and habitat disturbance on pollinator visitation and reproduction in a boreal forest herb, Am. J. Bot. 93, 868–873.

    Article  PubMed  Google Scholar 

  • Traveset A., Richardson D.M. (2006) Biological invasions as disruptors of plant reproductive mutualisms, Trends Ecol. Evol. 21, 208–216.

    Article  PubMed  Google Scholar 

  • Tscharntke T., Klein A.M., Kruess A., Steffan-Dewenter I., Thies C. (2005) Landscape perspectives on agricultural intensification and biodiversity — ecosystem service management, Ecol. Lett. 8, 857–874.

    Article  Google Scholar 

  • Valentine D.H. (1978) The pollination of introduced species, with special reference to the British Isles and the genus Impatiens, in: Richards A.J. (Ed.), The pollination of flowers by insects, Academic Press, London, pp. 117–123.

    Google Scholar 

  • Vázquez D.P., Aizen M.A. (2004) Asymmetric specialization: a pervasive feature of plant-pollinator interactions, Ecology 85, 1251–1257.

    Article  Google Scholar 

  • Velthuis H.H., van Doorn A. (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination, Apidologie 37, 421–451.

    Article  Google Scholar 

  • Vergara C. (2008) Environmental impact of exotic bees introduced for crop pollination, in: James R., Pitts-Singer T.L. (Eds.), Bee pollination in agricultural ecosystems, Oxford University Press, pp. 145–166.

  • Vilà M., Weiner J. (2004) Are invasive plant species better competitors than native plant species? — evidence from pair-wise experiments, Oikos 105, 229–238.

    Article  Google Scholar 

  • Walther-Hellwig K., Fokul G., Frankl R., Büchler R., Ekschmitt K., Wolters V. (2006) Increased density of honeybee colonies affects foraging bumblebees, Apidologie 37, 517–532

    Article  Google Scholar 

  • Waser N.M., Chittka L., Price M.V., Williams N.M., Ollerton J. (1996) Generalization in pollination systems, and why it matters, Ecology 77, 1043–1060.

    Article  Google Scholar 

  • Westphal C., Steffan-Dewenter I., Tscharntke T. (2003) Mass flowering crops enhance pollinator densities at a landscape scale, Ecol. Lett. 6, 961–965.

    Article  Google Scholar 

  • Westphal C., Steffan-Dewenter I., Tscharntke T. (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence, Oecologia 149, 289–300.

    Article  PubMed  Google Scholar 

  • White E.M., Wilson J.C., Clarke A.R. (2006) Biotic indirect effects: a neglected concept in invasion biology, Diver. Distrib. 12, 443–455.

    Article  Google Scholar 

  • Williams P.H., Osborne J. (2009) Bumblebee conservation and vulnerability world-wide, Apidologie 40, 367–387.

    Article  Google Scholar 

  • Williamson M. (1996) Biological Invasions. Chapman & Hall, London.

    Google Scholar 

  • Windle P.N., Chavarría G. (2005) The tragedy of the commons revisited: invasive species (Forum), Front. Ecol. Environ. 3, 109–115.

    Article  Google Scholar 

  • Winfree R., Williams N.M., Dushoff J., Kremen C. (2007) Native bees provide insurance against ongoing honey bee losses, Ecol. Lett. 10.

  • Winter K., Adams L., Thorp R.W., Inouye D.S., Day L., Ascher J., Buchmann S.L. (2006) Importation of non-native Bumble bees into North America: Potential consequences of using Bombus terrestris and other non-native bumblebees for Greenhouse Crop Pollination in Canada, Mexico, and the United States, White Paper of the North American Pollinator Protection Campaign.

  • Wolda H., Roubik D. (1986) Nocturnal bee abundance and seasonal bee activity in a Panamanian forest, Ecology 76, 426–433.

    Article  Google Scholar 

  • Yang G. (2005) Harm of introducing the western honeybee Apis mellifera L. to the Chinese honeybee Apis cerana F. and its ecological impact, Acta Entomol. Sin. 48, 401–406.

    Google Scholar 

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Stout, J.C., Morales, C.L. Ecological impacts of invasive alien species on bees. Apidologie 40, 388–409 (2009). https://doi.org/10.1051/apido/2009023

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