The use of different stingless bee species to pollinate cherry tomatoes under protected cultivation
DOI:
https://doi.org/10.13102/sociobiology.v68i1.5227Keywords:
buzzing, scraping, Melipona, Nannotrigona, protected cultivation, Solanum lycopersicum.Abstract
Under standard greenhouse conditions, the tomato fruits of spontaneous self-pollination are expected to be of lower quality than those of bee pollination, as well as that simultaneously use different bee species which can complement pollination services. To test these hypotheses, we evaluated the complementarity of pollination services from the use of three native stingless bee species that have distinct foraging behaviors, Melipona bicolor Lepeletier 1836, Nannotrigona testaceicornis (Lepeletier 1836) and Partamona helleri (Friese 1900) during flowering of cherry tomatoes in greenhouses. Fruit quality parameters resulted from pollination experiments were measured and the acclimatization of the analyzed bee species was evaluated. Visits of M. bicolor and N. testaceicornis to the tomato flowers contributed significantly to the increase in the average weight, seed number, and thickness of the pericarp (only for N. testaceicornis) of the fruits, compared to the spontaneous self-pollination treatment. Partamona helleri, however, did not show any pollen collection behavior in the experimental conditions. Although N. testaceicornis do not perform the buzzing behavior, fruits from its pollination were equivalent to those fruits from pollination by M. bicolor. The simultaneous use of bee species with different flower-visiting behaviors can optimize tomato pollination in greenhouses, contributing significantly to the quality of the fruits and the increase of productivity and consequently the commercial value.
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Ahmad, M., Bodlah, I., Mehmood, K., Sheikh, U.A.A, & M.A. Aziz. (2015). Pollination and Foraging Potential of European Bumblebee, Bombus terrestris (Hymenoptera: Apidae) on Tomato Crop under Greenhouse System. Pakistan Journal of Zoology, 47: 1279-1285.
Banda, H.J., & R.J. Paxton. (1991). Pollination of greenhouse tomatoes by bees. Acta Horticulturae, 288: 194-198. doi: 10.17660 / ActaHortic.1991.288.28
Bartelli, B.F., & F.H. Nogueira-Ferreira. (2014). Pollination Services Provided by Melipona quadrifasciata Lepeletier (Hymenoptera: Meliponini) in Greenhouses with Solanum lycopersicum L. (Solanaceae). Sociobiology, 61: 510-516. doi: 10.13102/sociobiology.v61i4.510-516
Bartelli, B.F., Santos, A.O.R., & F.H. Nogueira-Ferreira. (2014). Colony performance of Melipona quadrifasciata (Hymenoptera, Meliponina) in a Greenhouse of Lycopersicon esculentum (Solanaceae). Sociobiology, 61: 60-67. doi: 10.13102/sociobiology.v61i1.60-67
Bell, M.C., Spooner-Hart, R.N., & A.M. Haigh. (2006). Pollination of greenhouse tomatoes by the Australian bluebanded bee Amegilla (Zonamegilla) holmesi (Hymenoptera: Apidae). Journal of Economic Entomology, 99: 437-442. doi: 10.1603/0022-0493-99.2.437
Bispo dos Santos, A.S., Roselino, A.C., Hrncir, M., & L.R. Bego. (2009). Pollination of tomatoes by the stingless bee Melipona quadrifasciata and the honey bee Apis mellifera (Hymenoptera, Apidae). Genetics and Molecular Research, 8: 751-757. doi: 10.4238 / vol8-2kerr015
Bomfim, I.G.A., Bezerra, A.D.M., Nunes, A.C., Aragão, F.A.S., & B.M. Freitas. (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
Brand, H. (2005). Geoprópolis em colméias de Mandaçaia (Melipona quadrifasciata Lepeletier): um modelo de herança poligênica. Acta Biológica Paranaense, 4: 139-141. doi: http://dx.doi.org/10.5380/abpr.v34i0.960
Buchmann, S.L., & J.H. Cane. (1989). Bees assess pollen returns while sonicating Solanum flowers. Oecologia, 81: 289-294. doi: 10.1007 / BF00377073
Buchmann, S.L. (1983). Buzz pollination in angiosperms. Handbook of Experimental Pollination Biology, New York: Van Nostrand Reinhold Company, 73-113 p.
Camargo, J.M.F. (1972). Manual de apicultura. Ed. Agronômica Ceres, São Paulo.
Cauich, O., Quezada-Euán, J.J.G., Macias-Macias, J.O., Reyes-Oregel, V., Medina-Peralta, S., & V. Parra-Tabla. (2004). Behavior and pollination efficiency of Nannotrigona perilampoides (Hymenoptera: Meliponini) on greenhouse tomatoes (Lycopersicon esculentum) in subtropical México. Journal of Economic Entomology, 97: 172-179. doi: 10.1093 / jee / 97.2.475
Cruz, D.O., & L.A.O. Campos. (2009). Polinização por abelhas em cultivos protegidos. Revista Brasileira de Agrociência, 15: 5-10. doi: HTTP://DX.DOI.ORG/10.18539/CAST.V15I1-4.1979
Cruz, D.O., Freitas, B.M., Silva, L.A., Silva, E.M.S., & G.A. Bomfim. (2004). Adaptação e comportamento de pastejo da abelha jandaíra (Melipona subnitida Ducke) em ambiente protegido. Acta Scientiarum Animal Sciences, 26: 293-298. doi: https://doi.org/10.4025/actascianimsci.v26i3.1777
Da Silva, M.A., Oliveira, F.A., & M. Hrncir. (2016). Efeito de diferentes tratamentos de polinização em berinjela em casa de vegetação. Revista Verde de Agroecologia e Desenvolvimento Sustentável, 11: 30-36. doi: https://doi.org/10.18378/rvads.v11i1.3771
De Luca, P.A., & M. Vallejo-Marín. (2013). What’s the “buzz” about? The ecology and evolutionary significance of buzz-pollination. Current Opinion in Plant Biology, 16: 429–435. doi: 10.1016 / j.pbi.2013.05.002
Del Sarto, M.C.L., Peruquetti, R.C., & L.A.O. Campos. (2005). Evaluation of the Neotropical stingless bee Melipona quadrifasciata (Hymenoptera: Apidae) as pollinator of greenhouse tomatoes. Journal of Economic Entomology, 98: 260-266. doi: https://doi.org/10.1093/jee/98.2.260
Dogterom, M.H., Matteoni, J.A., & R.C. Powright. (1998). Pollination of greenhouse tomatoes by the North American Bombus vosnesenskii (Hymenoptera: Apidae). Journal of Economic Entomology, 91: 71-75. doi: https://doi.org/10.1093/jee/91.1.71
Dos Santos, S.A.B., Roselino, A.C., & L. Bego. (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: https://doi.org/10.1590/S1519-566X2008000500002
Free, J.B. (1993). Insect pollination of crops. University of Wales, Cardiff, UK.
Giurfa, M., & M. Lehrer. (2001). Honeybee vision and floral displays: from detection to close-up recognition, pp 61–82. In: Cognitive ecology of pollination (Chittka L, Thomson J Eds.), Cambridge University Press, Cambridge. doi: https://doi.org/10.1017/CBO9780511542268.005
Hammer, Ø., Harper, D.A.T., & Ryan, P.D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 9pp.
Higuti, A.R.O., Godoy, A.R., Salata, A.C., & A.I.I. Cardoso. (2010). Produção de tomate em função da “vibração” das plantas. Bragantia, 69: 87-92. doi: https://doi.org/10.1590/S0006-87052010000100012
Hikawa, M., & R. Miyanaga. (2009). Effects of pollination by Melipona quadrifasciata (Hymenoptera: Apidae) on tomatoes in protected culture. Applied Entomology and Zoology, 44: 301-307. doi: 10.1303 / aez.2009.301
Hogendoorn K., Gross C.L., Sedgley M., & Keller M. (2006). Increased tomato yield through pollination by native Australian Amegilla chlorocyanea (Hymenoptera: Anthophoridae). Journal of Economic Entomology, 99: 829-833. doi: https://doi.org/10.1093/jee/99.3.828
Hogendoorn, K., Steen, Z., & M.P. Schwarz. (2000). Native Australian carpenter bees as a potential alternative to introducing bumble bees for tomato pollination in greenhouses. Journal of Apicultural Research, 39: 67-74. doi: https://doi.org/10.1080/00218839.2000.11101023
Kearns, C.A., & D.W. Inouye. (1993). Techniques for pollinations biologists. Niwot, Colorado, University press of Colorado.
Kevan, P.G., Sraver, W.A., Offer, M., & T.M. Laverty. (1991). Pollination of greenhouse tomatoes by bumble bees in Ontario. Proceedings of The Entomological Society of Ontario, 122: 15-19.
Kiss, J. (2006). Casa aquecida: Um sistema de colméias com calefação mantém a temperature em 28 graus e permite a criação de abelhas nordestinas no Sul do país. Revista Globo Rural, 245: 32-37.
Mann, L.K. (1943). Fruit shape of watermelons as affected by placement of pollen on the stigma. Botanical Gazette, 105: 257-262.
McGregor, S.E. (1976). Insect pollination of cultivated plants. Washington: USDA.
Michener, C.D. (1974). The social behavior of the bees. A comparative study. Cambridge, The Belkanp Press.
Morandin, L.A., Laverty, T.M., & P.G. Kevan. (2001a). Bumble bee (Hymenoptera: Apidae) activity and pollination levels in commercial tomato greenhouses. Journal of Economic Entomology, 94: 462-467. doi: https://doi.org/10.1603/0022-0493-94.2.462
Morandin, L.A., Laverty, T.M., & P.G. Kevan. (2001b). Effect of bumble bee (Hymenoptera: Apidae) pollination intensity on the quality of greenhouse tomatoes. Journal of Economic Entomology, 94: 172-179. doi: 10.1603 / 0022-0493-94.1.172
Nunes-Silva, P., Hrncir, M., Silva, C.I., Roldão, Y.S., & V.L. Imperatriz-Fonseca. (2013). Stingless bees, Melipona fasciculata, as eficiente pollinators of eggplant (Solanum melongena) in greenhouses, Apidologie, 44: 537-546. doi: 10.1007/s13592-013-0204-y
Palma, G., Quezada-Euán, J.J.G., Reyes-Oregel, V., Meléndez, V., & H. Moo-Valle. (2008). Production of greenhouse tomatoes (Lycopersicon esculentum) using Nannotrigona perilampoides, Bombus impatiens and mechanical vibration (Hym.: Apoidea). Journal of Applied Entomology, 132: 79-85. doi: https://doi.org/10.1111/j.1439-0418.2007.01246.x
Picken, A.J.F. (1984). A review of pollination and fruit set in the tomato (Lycopersicon esculentum Mill.). Journal of Horticultural Science, 59: 1-13. doi: https://doi.org/10.1080/00221589.1984.11515163
Portman, Z.M., Orr M.C., & T. Griswold. (2019). A review and updated classification of pollen gathering behavior in bees (Hymenoptera, Apoidea). Journal of Hymenoptera Research, 71: 171-208. doi: 10.3897/jhr.71.32671
Pressman, E., Shaked, R., Rosenfeld, K., & A. Hefetz. (1999). A comparative study of the efficiency of bumble bees and an electric bee in pollinating unheated greenhouse tomatoes. Journal of Horticultural Science & Biotechnology, 74: 101-104. doi: https://doi.org/10.1080/14620316.1999.11511080
Roselino, A.C., Santos, S.B., Hrncir, M., & L.R. Bego. (2009). Differences between the quality of strawberries (Fragaria x ananassa) pollinated by the stingless bees Scaptotrigona aff. depilis and Nannotrigona testaceicornis. Genetics and Molecular Research, 8: 539-545. doi: 10,4238 / vol8-2kerr005
Shelly, T.E., Villalobos, E., & OTS-USAP. (2000). Buzzing bees (Hymenoptera: Apidae, Halictidae) on Solanum (Solanaceae): floral choice and handling time track pollen availability. Florida Entomologist, 83: 180-187. doi: 10.2307 / 3496153
Silva-Neto, C.M., Ribeiro, A.C.C., Gomes, F.L., Melo, A.P.C., Oliveira, G.M., Faquinello, P., Franceschinelli, E.V., & A.R. Nascimento. (2018). The stingless bee mandaçaia (Melipona quadrifasciata Lepeletier) increases the quality of greenhouse tomatoes. Journal of Apicultural Research. doi: 10.1080/00218839.2018.1494913
Srinivasan, M.V., Zhang, S.W., & K. Witney. (1994). Visual discrimination of pattern orientation in honeybees: Performance and implications for “cortical” processing. Philosophical Transactions: Biological Sciences, 343: 199-210. doi: 10.1098 / rstb.1994.0021
Teixeira, L., & F.D.N.M. Campos. (2005). Início da atividade de vôo em abelhas sem ferrão (Hymenoptera, Apidae): influência do tamanho da abelha e da temperatura ambiente. Revista Brasileira de Zoociências, 7: 195-202.
Thorp, R.W. (2000). The collection of pollen by bees. Plant Systematics and Evolution, 222: 211-223.
Westerkamp, C., & Gottsberger. G. (2000). Diversity pays in crop pollination. Crop Science, 40: 1209-1222. doi: https://doi.org/10.2135/cropsci2000.4051209x
Whittington, R., & M. Winston. (2004). Comparison and Examination of Bombus occidentalis and Bombus impatiens (Hymenoptera: Apidae) in Tomato Greenhouses. Horticultural Entomology, 97: 1384-1389. doi: https://doi.org/10.1093/jee/97.4.1384
Wille, A. (1963). Behavioral adaptions of bees for pollen collecting from Cassia flowers. Revista de Biologia Tropical, 11: 205-210.
Zar, J.H. (1999). Biostatistical analysis. Fourth edition, pp 208-214. USA: Prentice Hall.
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