Skip to main content
SpringerLink
Log in

Africanized honey bees pollinate and preempt the pollen of Spondias mombin (Anacardiaceae) flowers

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

The invasion of generalist Africanized honey bees may change certain plant–pollinator interactions. We evaluated the preemption by honey bees and the exploitative competition with native bees on a tree with nocturnally dehiscent small flowers. Our main objectives were to quantify pollen production and harvesting, to verify whether honey bees exploitatively compete with native bees and to identify the effective pollinators of Spondias mombin. The nocturnally dehiscent flowers were pollen depleted by honey bees and attracted various nocturnal and diurnal bee species. A threefold increase in native bee abundance was produced by delaying pollen availability and by preventing the preemption of pollen by honey bees. The results suggest that honey bees reduce the foraging benefit of late-arriving native bees. Honey bees and Scaptotrigona aff. tubiba were regarded as the main effective pollinators of S. mombin due to their abundance, behavior, and ability to visit a large number of flowers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.

Similar content being viewed by others

References

  • Absy, M.L., Camargo, J.M.F., Kerr, W.E., Miranda, I.P.A. (1984) Espécies de plantas visitadas por Meliponinae (Hymenoptera; Apoidea) para coleta de pólen na região do médio Amazonas. Rev. Bras. Biol. 44, 227–237

    Google Scholar 

  • Adler, G.H., Kielpinski, K.A. (2000) Reproductive phenology of a tropical canopy tree, Spondias mombin. Biotropica 32, 686–692

    Article  Google Scholar 

  • Bawa, K., Opler, P.A. (1975) Dioecism in tropical forest trees. Evolution 29, 167–179

    Article  Google Scholar 

  • Biesmeijer, J.C., Slaa, E.J. (2006) The structure of eusocial bee assemblages in Brazil. Apidologie 37, 240–258

    Article  Google Scholar 

  • Biesmeijer, J.C., van Marwilk, B., van Deursen, K., Punt, W., Sommeijer, M.J. (1992) Pollen sources for Apis mellifera L. (Hym, Apidae) in Surinam, based on pollen grain volume estimates. Apidologie 23, 245–256

    Article  Google Scholar 

  • Butz-Huryn, V.N. (1997) Ecological impacts of introduced honeybees. Q. Rev. Biol. 72, 275–297

    Article  Google Scholar 

  • Castro M.S., Barreto L.S. (2008) Polinização e conservação do umbuzeiro (Spondias tuberosa Arr. Câm.) e de seus polinizadores, in: Spondias no Brasil: umbú, cajá e espécies afins, UFRPE, Recife, pp. 40–44.

  • Croat, T.B. (1978) Flora of Barro Colorado Island. Stanford University Press, Stanford

    Google Scholar 

  • Dyer, F.C. (2002) The biology of the dance language. Annu. Rev. Entomol. 47, 917–949

    Article  PubMed  CAS  Google Scholar 

  • Feliciano, M.L.M., Melo, R.B. (2003) Atlas Geográfico da Paraíba. SEPLAN/IDEME, João Pessoa

    Google Scholar 

  • Freitas, B.M., Paxton, R.J. (1998) A comparison of two pollinators: the introduced honey bee Apis mellifera and an indigenous bee Centris tarsata on cashew Anacardium occidentale in its native range of NE Brazil. J. Appl. Ecol. 35, 109–121

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Holanda-Neto, J.P., Freitas, B.M., Bueno, D.M., Araújo, Z.B. (2002) Low seed/nut productivity in cashew (Anacardium occidentale L.): effects of self-incompatibility and honey bee (Apis mellifera) foraging behavior. J. Hortic. Sci. Biotech. 77, 226–231

    Google Scholar 

  • Horskins, K., Turner, V.B. (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 

  • Lozano, N.B. (1986) Contribucion al estúdio de la anatomia floral y de la polinizacion del jobo (Spondias mombin L.). Caldasia 15, 369–380

    Google Scholar 

  • Marques-Souza, A.C., Absy, M.L., Kerr, W.E. (2007) Pollen harvest features of the Central Amazonian bee Scaptotrigona fulvicutis Moure 1964 (Apidae: Meliponinae), in Brazil. Acta Bot. Bras. 21, 11–20

    Article  Google Scholar 

  • Martins, C.F., Moura, A.C.A., Barbosa, M.R.V. (2003) Bee plants and relative abundance of corbiculate Apidae species in a brazilian caatinga area. Rev. Nordest. Biol. 17, 63–74

    Google Scholar 

  • Menezes, C., Silva, C.I., Singer, R.B., Kerr, W.E. (2007) Competição entre abelhas durante forrageamento em Schefflera arboricola (Hayata) Merr. Biosci. J. 23, 63–69

    Google Scholar 

  • Mitchell J.D. (1997) Flora of the Guianas 129. Anacardiaceae. Series A: phanerogams fascicle 19. Görts-van Rijn A.R.A., Jansen-Jacobs M.J. (eds) pp. 79. Royal Botanic Gardens, Kew

  • Nadia, T.L., Machado, I.C., Lopes, A.V. (2007) Polinização de Spondias tuberosa Arruda (Anacardiaceae) e análise da partilha de polinizadores com Ziziphus joazeiro Mart. (Rhamnaceae), espécies frutíferas e endêmicas da caatinga. Rev. Bras. Bot. 30, 89–100

    Article  Google Scholar 

  • Nason, J.D., Hamrick, J.L. (1997) Reproductive and genetics consequences of forest fragmentation: two case studies of Neotropical canopy trees. J. Hered. 88, 264–276

    Article  Google Scholar 

  • Nieh, J.C. (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35, 159–182

    Article  Google Scholar 

  • Pedro, S.R., Camargo, J.M.F. (1991) Interactions on floral resources between the Africanized honey bee Apis mellifera L. and the native bee community (Hymenoptera: Apoidea) in a natural “cerrado” ecosystem in southeast Brazil. Apidologie 22, 397–415

    Article  Google Scholar 

  • Pennington, T.D., Sarukhan, J. (2005) Arboles tropicales de Mexico. Instituto Nacional de Investigaciones Forestales, Mexico

    Google Scholar 

  • Ramalho, M. (2004) Stingless bees and mass flowering trees in the canopy of Atlantic Forest: a tight relationship. Acta Bot. Bras. 18, 37–47

    Article  Google Scholar 

  • Ramalho, M., Kleinert-Giovannini, A., Imperatriz-Fonseca, V.L. (1990) Important bee plants for stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical habitats: a review. Apidologie 21, 469–488

    Article  Google Scholar 

  • Roubik, D.W. (1978) Competitive interactions between Neotropical pollinators and Africanized honey bees. Science 201, 1030–1032

    Article  PubMed  CAS  Google Scholar 

  • Roubik, D.W. (1980) Foraging behavior of commercial Africanized honeybees and stingless bees. Ecology 61, 836–845

    Article  Google Scholar 

  • Roubik, D.W. (1988) An overview of Africanized honeybee populations: reproduction, diet and competition. In: Needham, G., Page Jr., R.E., Delfinado-Baker, M. (eds.) Africanized honeybees and bee mites, pp. 45–54. E. Horwood, Chichester

    Google Scholar 

  • Roubik, D.W. (1989) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Roubik, D.W. (1995) Pollination of cultivated plants in the tropic. Food and Agriculture Organization, p. 118. FAO Agricultural Services Bulletin, Rome

    Google Scholar 

  • Roubik, D.W. (1996) African honey bees as exotic pollinators in French Guiana. In: Matheson, A., Buchmann, S.L., O’Toole, C., Westrich, P., Williams, I.H. (eds.) The conservation of bees, pp. 173–182. Academic, London

    Google Scholar 

  • Roubik, D.W. (2009) Ecological impact on native bees by the invasive Africanized honey bee. Acta biol. Colomb. 14, 115–124

    Google Scholar 

  • Roubik, D.W., Villanueva-Gutiérrez, R. (2009) Invasive Africanized honey bee impact on native solitary bees: a pollen resource and trap nest analysis. Biol. J. Linn. Soc. 98, 152–160

    Article  Google Scholar 

  • Roubik, D.W., Moreno, J.E., Vergara, C., Wittmann, D. (1986) Sporadic food competition with the African honey bee: projected impact on neotropical social bees. J. Trop. Ecol. 2, 97–111

    Article  Google Scholar 

  • Schaffer, W.M., Jensen, D.B., Hobbs, D.E., Gurevitch, J., Todd, J.R., Schaffer, M.V. (1979) Competition, foraging energetics, and the cost of sociality in three species of bees. Ecology 60, 976–987

    Article  Google Scholar 

  • Siqueira, K.M.M., Kiill, L.H.P., Martins, C.F., Lemos, I.B., Monteiro, S.P., Feitoza, E.A. (2008) Estudo comparativo da polinização de Mangifera indica L. em cultivo convencional e o orgânico na região do vale do submédio do São Francisco. Rev. Bras. Frutic. 30, 303–310

    Article  Google Scholar 

  • Sommeijer, M.J., De Rooy, G.A., Punt, W., De Bruijn, L.L.M. (1983) A comparative study of foraging behavior and pollen resources of various stingless bees (Hym., Meliponinae) and honeybees (Hym., Apinae) in Trinidad, West-Indies. Apidologie 14, 205–224

    Article  Google Scholar 

  • Stacy, E.A., Hamrick, J.L., Nason, J.D., Hubbell, S.P., Foster, R.B., Condit, R. (1996) Pollen dispersal in low-density populations of three neotropical tree species. Am. Nat. 148, 275–298

    Article  Google Scholar 

  • Teixeira, A.F.R., Oliveira, F.F., Viana, B.F. (2007) Utilization of floral resources by bees of the genus Frieseomelitta von Iheriing (Hymenoptera: Apidae). Neotrop. Entomol. 36, 675–684

    Article  PubMed  Google Scholar 

  • Wcislo, W.T., Gonzalez, V.H., Engel, M.S. (2003) Nesting and social behavior of a wood-dwelling neotropical bee, Augochlora isthmii (Schwarz), and notes on a new species, A. alexanderi Engel (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 74, 588–602

    Google Scholar 

  • Wcislo, W.T., Arneson, L., Roesch, K., Gonzalez, V., Smith, A., Fernandez, H. (2004) The evolution of nocturnal behavior in sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae): an escape from competitors and enemies? Biol. J. Linn. Soc. 83, 377–387

    Article  Google Scholar 

  • Wilms, W., Imperatriz-Fonseca, V.L., Engels, W. (1996) Resource partitioning between highly eusocial bees and possible impact of the introduced Africanized honey bee on native stingless bees in the Brazilian Atlantic Rainforest. Stud. Neotropical Fauna Environ. 31, 137–151

    Article  Google Scholar 

Download references

Acknowledgments

We thank the EMEPA staff for permission to work in the Experimental Station. We would also like to thank Renata Marinho Cruz and Maria Luiza de Melo Cruz for help in field work for this study and Clemens Schlindwein for reading the manuscript and for constructive criticism. We would like to thank CAPES and the Brazilian Research Council (CNPq) for their financial support.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Universidade Federal da Paraíba-UFPB, 58051-900, João Pessoa, PB, Brazil

    Liedson Tavares Carneiro

  2. Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba-UFPB, 58051-900, João Pessoa, PB, Brazil

    Celso Feitosa Martins

Authors
  1. Liedson Tavares Carneiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Celso Feitosa Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Celso Feitosa Martins.

Additional information

Manuscript editor: James Nieh

Les abeilles africanisées pollinisent et collectent prioritairement à toute autre espèce d’abeilles le pollen des fleurs de Spondias mombin (Anacardiaceae).

Apis mellifera / réduction du pollen disponible / abeille sans aiguillon / abeille nocturne / pollinisation / Brésil

Afrikanisierte Bienen bestäuben die Blüten von Spondias mombin L. (Anacardiaceae) und kommen dabei anderen Bienen zuvor.

Apis mellifera / Pollenreduzierung / Stechellose Bienen / nachtaktive Bienen / Bestäubung / Brasilien

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carneiro, L.T., Martins, C.F. Africanized honey bees pollinate and preempt the pollen of Spondias mombin (Anacardiaceae) flowers. Apidologie 43, 474–486 (2012). https://doi.org/10.1007/s13592-011-0116-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-011-0116-7

Keywords

Search

Navigation