Improved Pollination Efficiency and Reduced Honey Bee Colony Decline in Greenhouses by Allowing Access to the Outside During Part of the Day

Authors

  • Daniel Nicodemo UNESP http://orcid.org/0000-0001-6594-5791
  • Euclides Braga Malheiros Universidade Estadual de São Paulo
  • David De Jong Universidade de São Paulo
  • Regina Helena Nogueira Couto Universidade Estadual Paulista

DOI:

https://doi.org/10.13102/sociobiology.v65i4.3455

Keywords:

Apis mellifera, brood, cucumber, Cucumis sativus, fruit set, honey

Abstract

Although honey bees are efficient pollinators of many crops cultivated in greenhouses, it is difficult to maintain colony strength and consequently pollination efficiency. Many bees die under greenhouse conditions and the colonies rapidly weaken. We examined the effect of adaptations to the hive entrance that allowed control of whether and when bees had access to the outside environment to see how it would affect pollination efficiency and colony condition in greenhouses with flowering cucumber (Cucumis sativus) plants in comparison with colonies that remained constantly inside the greenhouse, previously left in a dark environment or not. We recorded the type and period of visitation to the cucumber flowers, numbers of honey bees entering and leaving the two entrance hives and the effect of this type of management on the quantity of brood and food. Fiveframe Langstroth “nucleus” colonies were equipped with two 30 square centimeter entrances and two 3.0 cm diameter circular openings. Allowing the bees to make visits outside the greenhouse in early morning with redirection of bees into the greenhouse at 8.30 a.m. did not reduce visitation to cucumber flowers in the greenhouse. Maintaining colonies in the greenhouse reduced brood area and food stores. These losses were significantly reduced in colonies that had access outside the greenhouse during the early morning. Another advantage of alternating access to the inside and the outside of the greenhouse was that there was less possibility of interactions between bees and people working on the crop, and also pesticides application could be made without directly affecting foraging bees.

Downloads

Download data is not yet available.

References

Abou-Shaara, H.F. (2014) . The foraging behaviour of honey bees, Apis mellifera: a review. Veterinarni Medicina, 59: 1-10. doi:10.17221/7240-VETMED

Abrol, D.P. (2012). Pollination biology: biodiversity conservation and agricultural production. New York: Springer, 792 p

Al-Tikrity, W.S., Hillmann, R.C., Benton, A.W. & Clarke, W.W. (1971). A new instrument for brood measurement in a honeybee colony. American Bee Journal, 111: 20-26.

Bartomeus, I., Potts, S.G., Steffan-Dewenter, I., Vaissière, B.E. Woyciechowski,M., Krewenka, K.M., Tscheulin, T., Roberts, S.P.M., Szentgyörgyi, H., Westphal, C., Bommarco, R. (2014). Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. PeerJ, 2:e328. doi:10.7717/peerj.328.

Beekman, M. & Ratnieks, F.L.W. (2000). Long-range foraging by the honey-bee, Apis mellifera L., Functional Ecology, 14: 490-496. doi: 10.1046/j.1365-2435.2000.00443.x

Bomfim, I.G.A., Bezerra, A.D.M., Nunes, A.C., Aragão, F.A.S. & Freitas, B.M. (2014). Adaptive and foraging behavior of two stingless bee species (Apidae: Meliponini) in greenhouse mini watermelon pollination. Sociobiology, 61: 502-509. doi: 10.13102/sociobiology.v61i4.502-509

Brodschneider, R. & Crailsheim, K. (2010). Nutrition and health in honey bees. Apidologie, 41: 278-294. doi.org/10.1051/apido/2010012.

Cermeño, Z.S. (1979). Cultivo de plantas hortícolas em estufa. Lisboa : Litexa, 368p.

Couto, R.H.N.; Couto, L.A. (2006). Apicultura: manejo e produtos. 3.ed. Jaboticabal: Funep, 193p.

Crailsheim, K., Schneider, L.H.W., Hrassnigg, N., Buhlmann, G., Brosch, U., Gmeinbauer, R. & Schoffmann, B. (1992). Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): dependence on individual age and function. Journal of Insect Physiology, 38: 409-410.

Dafni, A., Kevan, P., Gross, C.L. & Goka, K. (2010). Bombus terrestris, pollinator, invasive and pest: an assessment of problems associated with its widespread introductions for commercial purposes. Applied Entomology and Zoology, 45: 101-113. doi:10.1303/aez.2010.101

Dag, A. & Eisikowitch, D. (1995). The influence of hive location on honeybee foraging activity and fruit set in melons grown in plastic greenhouses. Apidologie, 26: 511-519. doi:10.1051/apido:19950608

Del Sarto, M.C., Peruquetti, R.C. & Campos, L.A. (2005). Evaluation of the neotropical stingless bee Melipona quadrifasciata (Hymenoptera: Apidae) as pollinator of greenhouse tomatoes. Journal of Economic Entomology, 98: 260-266.

Diaz, B.M. & Fereres, A. (2007). Ultraviolet-blocking materials as a physical barrier to control insect pests and plant pathogens in protected crops. Pest Technology 1:85-95.

Dustmann, J.H. & von der Ohe, W. (1988). Effect of cold snaps on the build up of honeybee colonies (Apis mellifera L.) in spring time. Apidologie, 19: 245-254.

Edrich, W., Neumeyer, N. & von Heiversen, O. (1979). “Anti-sun orientation” of bees with regard to a field of ultraviolet light. Journal of comparative physiology, 134: 151–157. doi:10.1007/BF00610473

Free, J.B. Insect pollination of crops. London: Academic Press, 1993. 544 p

Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., Cunningham, S.A., Kremen, C., Carvalheiro, L.G., Harder, L.D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N.P., Dudenhöffer, J.H., Freitas, B.M., Ghazoul, J., Greenleaf, S., Hipólito, J., Holzschuh, A., Howlett, B., Isaacs, R., Javorek, S.K., Kennedy, C.M., Krewenka, K.M., Krishnan, S., Mandelik, Y., Mayfield, M.M., Motzke, I., Munyuli, T., Nault, B.A., Otieno, M., Petersen, J., Pisanty, G., Potts, S.G., Rader, R., Ricketts, T.H., Rundlöf, M., Seymour, C.L., Schüepp, C., Szentgyörgyi, H., Taki, H., Tscharntke, T., Vergara, C.H., Viana, B.F., Wanger, T.C., Westphal, C., Williams, N. & Klein, A.M. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339: 1608–1611. doi:10.1126/ science.1230200

Guerra-Sanz, J.M. (2008). Crop pollination in greenhouses. In R.R. James & T.L. Pitts-Singer (Eds.), Bee pollination in agricultural ecosystems (pp.27-47). Oxford: Oxford University Press.

Herbert Jr. , E.W., Shimanuki, H. & Caron, D. (1977). Optimum protein levels required by honey bees (Hymenoptera, Apidae) to initiate and maintain brood rearing. Apidologie, 8: 141-146.

Katayama, E. (1987) Utilization of honeybees as pollinators for strawberries in plastic greenhouses, Honeybee Science, 8: 147-150.

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, Proceedings of the Royal Society B, 274: 303-313. doi:10.1098/rspb.2006.3721

Malagodi-Braga & K.S., Kleinert, A.M.P. (2004). Could Tetragonisca angustula Latreille (Apinae, Meliponini) be effective as strawberry pollinator in greenhouses? Australian Journal of Agricultural Research, 55: 771-773. doi:10.1071/AR03240

Ministério da Agricultura, Pecuária e Abastecimento [MAPA]. 2018. Sistema Agrofi t. http://www.agricultura.gov.br/servicos-e-sistemas/sistemas/agrofi t. (accessed date: 13 July, 2018).

McGregor, S. E. (1976). Insect pollination of cultivated crop plants. Washington: USDA, 411 p

Muijzenberg, E.W.B. van den (1980). A history of greenhouses. Wageningen: Institute of Agricultural Engineering, 435 p

Naug, D. (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation, 142: 2369–2372.

Nicodemo, D., Couto, R.H.N., Malheiros, E.B. & De Jong, D. (2009). Honey bee as an effective pollinating agent of pumpkin. Scientia Agricola, 66: 476-480. doi: 10.1590/S0103-90162009000400007

Nicodemo, D., Malheiros, E.B., De Jong, D. & Couto, R.H.N. Biologia floral de pepino (Cucumis sativus L.) tipo Aodai cultivado em estufa. Científica, 40: 41–46.

Nicodemo, D., Malheiros, E.B., De Jong, D. & Couto, R.H.N. (2013). Enhanced production of parthenocarpic cucumbers pollinated with stingless bees and Africanized honey bees in greenhouses. Semina: Ciências Agrárias, 34: 3625-3634. doi:10.5433/1679-0359.2013v34n6Supl1p3625

Nogueira-Couto, R.H.N. & Calmona, R.C. (1993). Polinização entomófila em pepino (Cucumis sativus L. var. Aodai melhorada). Naturalia, 18: 77-82.

Nye, W.P. (1962). Management of honeybee colonies for pollination in cages. Bee World, 43: 37-40.

Raij, B.V., Cantarella, H., Quaggio, J.A. & Furlani, A.M.C. (1997). Recomendações de adubação e calagem para o Estado de São Paulo. Campinas: IAC, 285 p

Reyes-Carrillo, J.L., Eischen, F.A., Cano-Rios, P., Rodriguez-Martinez, R. & Camberos, U.N. (2007). Pollen collection and honey bee forager distribution in Cantaloupe. Acta Zoológica Mexicana, 23: 29-36.

Sabara H.A. & Winston M.L. (2003). Managing honey bees (Hymenoptera: Apidae) for greenhouse tomato pollination. Journal of Economic Entomology, 96: 547-54.

Santos, S.A.B., Roselino, A.C. & Bego, L.R. (2008). Pollination of cucumber, Cucumis sativus L. (Cucurbitales: Cucurbitaceae), by the stingless bees Scaptotrigona aff. depilis Moure and Nannotrigona testaceicornis Lepeletier (Hymenoptera: Meliponini) in greenhouses. Neotropical Entomology, 37: 506-512. doi:10.1590/S1519-566X2008000500002

SAS Institute. (2003). SAS user’s guide. (Version 9.1 ed.). Cary, NC: SAS Inst. Inc.

Sganzerla, E. (1997). Nova agricultura: a fascinante arte de cultivar com os plásticos. Guaíba: Agropecuária, 347 p

Slaaa, E.J., Chaves, L.A.S., Malagodi-Braga, K.S. & Hofsteded, F.E. (2006). Stingless bees in applied pollination: practice and perspectives. Apidologie, 37: 293-315, doi:10.1051/apido:2006022

Southwick, E.E. & Southwick, L. (1992). estimating the economic value of honey bees (Hymenoptera: Apidae) as agricultural pollinators in the united states. Journal of Economic Entomology, 85: 621–633, doi:10.1093/jee/85.3.621

Van Straten, G., Van Willigenburg, L.G., Van Henten, E.J. & Van Ooteghem, R.J.C. (2010). Optimal control of greenhouse cultivation, Boca Raton: CRC Press, 296 p

Velthuis, H.H.W. & 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. doi:10.1051/apido:2006019

Winston, M.L. (1987). The biology of the honey bee. Cambridge: Harvard University Press. 281p

Downloads

Published

2018-10-11

How to Cite

Nicodemo, D., Malheiros, E. B., Jong, D. D., & Couto, R. H. N. (2018). Improved Pollination Efficiency and Reduced Honey Bee Colony Decline in Greenhouses by Allowing Access to the Outside During Part of the Day. Sociobiology, 65(4), 714–721. https://doi.org/10.13102/sociobiology.v65i4.3455

Issue

Section

Research Article - Bees

Most read articles by the same author(s)