Acta Univ. Agric. Silvic. Mendelianae Brun. 2022, 70(3), 215-226 | DOI: 10.11118/actaun.2022.016

The Foraging Activity and Pollination Services of Three Stingless Bee Species to Enhance Fruit Quality and Quantity of Okra (Abelmoschus Esculentus L.)

Kartika Marta Djakaria1, Tri Atmowidi2, Windra Priawandiputra2
1 Animal Bioscience Study Program, Graduate School, IPB University Campus Darmaga, Bogor 16680, West Java, Indonesia
2 Department of Biology, Faculty of Mathematics and Natural Sciences, IPB University Campus Darmaga, Bogor 16680, West Java, Indonesia

Insect pollination has been reported to have a better yield quality and quantity than artificial pollination. Wild bees, including stingless bees contribute to effective and efficient pollination on okra (Abelmoschus esculentus L.: Malvaceae). However, previously no report about okra pollination by native Indonesian stingless bees, which can be potential as pollinators. Therefore, this research aims to compare foraging activities of three species of stingless bees (Heterotrigona itama, Tetragonula laeviceps, and T. clypearis) on okra plants and fruits quality and quantity parameters among four pollination treatments (three stingless bee species and without pollinator). Four cages with 50 okra plants were used for pollination treatments. The foraging observation of different stingless bee species on okra was conducted in the cages, and the okra yield from each treatment was compared. Our results showed the foraging activities of three stingless bee species were higher in the morning than those in the afternoon. In the morning, the number of visits of T. clypearis and T. laeviceps were negatively correlated with visit duration. The current study also showed that size and weight of pod, the number of seeds, and the percentage of fruit set of okra were enhanced by pollination of three stingless bee species. Unfortunately, the pollination of stingless bee species did not affect the seed germination and flavonoid content of fruits. The native of Indonesian stingless bees are good pollinators to improve pod quality and quantity.

Keywords: flavonoid, fruits, Heterotrigona itama, pollinator, Tetragonula laeviceps, Tetragonula clypearis

Received: November 22, 2021; Revised: March 24, 2022; Accepted: May 23, 2022; Published: July 1, 2022  Show citation

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Djakaria, K.M., Atmowidi, T., & Priawandiputra, W. (2022). The Foraging Activity and Pollination Services of Three Stingless Bee Species to Enhance Fruit Quality and Quantity of Okra (Abelmoschus Esculentus L.). Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 70(3), 215-226. doi: 10.11118/actaun.2022.016
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    References

    1. A'YUNIN, Q., RAUF, A. and HARAHAP, I. S. 2019. Foraging behaviour and pollination efficiency of Heterotrigona itama (Cockerell) and Tetragonula laeviceps (Smith) (Hymenoptera: Apidae) on chayote. Jurnal Ilmu Pertanian Indonesia, 24(3): 247-257. Go to original source...
    2. ANGBANYERE, M. A. and BAIDOO, P. K. 2014. The effect of pollinators and pollination on fruit set and fruit yield of okra (Abelmoschus esculentus (L.) Moench) in the forest region of Ghana. Am. J. Exp. Agri., 4(9): 985-995. Go to original source...
    3. ASMA, S. S., ADAM, N. A., NAJWA, S. M. Y., ASILAH, N., SYUKRI, T. S. and ASIAH, W. N. 2019. Foraging behavior of stingless bee (Geniotrigona thoracica and Heterotrigona itama) on star fruit trees (Averrhoa carambola L.). IOP Conference Series: Earth and Environmental Science, 383: 012011. Go to original source...
    4. ATMOWIDI, T., BUCHORI, D., MANUWOTO, S., SURYOBROTO, B. and HIDAYAT, P. 2007. Diversity of pollinator insects in relation to seed set of mustard (Brassica rapa L.: Cruciferae). HAYATI J. Biosci., 14(4): 155-161. Go to original source...
    5. ATMOWIDI, T., PRAWASTI, T. S., and RAFFIUDIN, R. 2018. Flight activities and pollen load of three species of stingless bees (Apidae: Melliponinae). IOP Conference Series: Earth and Environmental Science, 197: 012025. Go to original source...
    6. AZMI, W. A., ZULQURNAIN, N. S. and GHAZI, R. 2015. Melissopalynology and foraging activity of stingless bees, Lepidotrigona terminata (Hymenoptera: Apidae) from an apiary in Besut, Terengganu. Journal of Sustainability Science and Management, 10(1): 27-35.
    7. AZO'O, M. E., FOHOUO, F. N. T. and MESSI, J. 2011. Influence of the foraging activity of the entomofauna on okra (Abelmoschus esculentus) seed yield. Int. J. Agri. Biol., 13(5): 761-765.
    8. BELLUSCI, F., PELLEGRINO, G., and MUSACCHIO, A. 2009. Different levels of inbreeding depression between outcrossing and selfing Serapias species. Biologia Plantarum, 53(1): 175-178. Go to original source...
    9. BENCHASRI, S. 2012. Okra (Abelmoschus esculentus (L.) Moench) as a valuable vegetable of the world. Ratarstvo i povrtarstvo, 49(1): 105-112. Go to original source...
    10. BOMMARCO, R., MARINI, L. and VAISSIERE, B. E. 2012. Insect pollination enhances seed yield, quality, and market value in oilseed rape. Oecologia, 169(4): 1025-1032. Go to original source...
    11. BRITTAIN, C., KREMEN, C., GARBER, A. and KLEIN, A. M. 2014. Pollination and plant resources change the nutritional quality of almonds for human health. PLoS ONE, 9(2): e90082. Go to original source...
    12. BUCHORI, D., RIZALI, A., PRIAWANDIPUTRA, W., SARTIAMI, D. and JOHANNIS, M. 2020. Population growth and insecticide residues of honey bees in tropical agricultural landscapes. Diversity, 12(1): 1. Go to original source...
    13. CHAUTA-MELLIZO, A., CAMPBELL, S. A., BONILLA, M. A., THALER, J. S. and POVEDA, K. 2012. Effects of natural and artificial pollination on fruit and offspring quality. Basic and Applied Ecology, 13(6): 524-532. Go to original source...
    14. CHOLIS, M. N., ALPIONITA, R., PRAWASTI, T. S. and ATMOWIDI, T. 2020. Pollen load and flower constancy of stingless bees Tetragonula laeviceps (Smith) and Heterotrigona itama (Cockerell) (Apidae: Meliponinae). In: Proceedings of the International Conference and the 10th Congress of the Entomological Society of Indonesia (ICCESI 2019), pp. 285-289. Go to original source...
    15. DE BRUIJN , L. L. M. and SOMMEIJER, M. J. 1997. Colony foraging in different species of stingless bees (Apidae, Meliponinae) and the regulation of individual nectar foraging. Insectes Sociaux, 44(1): 35-47. Go to original source...
    16. ERDTMAN , G. 1960. The acetolysis method. Svensk Bot Tidskr, 54: 561-564.
    17. FIDALGO, A. de O., CECEL, A. T., MAZZI, J. F. de O. and BARBEDO, C. J. 2019. Pollination and quality of seeds and plantlets of Eugenia uniflora L.. Hoehnea, 46(1): e05218. Go to original source...
    18. GADHIYA, V. C. and PASTAGIA, J. J. 2019. Time spent by stingless bees, Tetragonula laeviceps for nectar and pollen collection from musk melon flower. J. Entomol. Zool. Studies, 7(2): 498-500.
    19. GARRATT, M. P. D., BREEZE, T. D., JENNER, N., POLCE, C., BIESMEIJER, J. C. and POTTS, S. G. 2014. Avoiding a bad apple: Insect pollination enhances fruit quality and economic value. Agriculture, Ecosystems and Environment, 184(100): 34-40. Go to original source...
    20. GOTTLIEB, D., KEASAR, T., SHMIDA, A. and MOTRO, U. 2005. Possible foraging benefits of bimodal daily activity in Proxylocopa olivieri (Lepeletier) (Hymenoptera: Anthophoridae). Environ. Entomol., 34(2): 417-424. Go to original source...
    21. HEARD, T. A. 1994. Behaviour and pollinator efficiency of stingless bees and honey bees on macadamia flowers. Journal of Apicultural Research, 33(4): 191-198. Go to original source...
    22. KUMAR, H. R., REDDY, S. K. M., SHISHIRA, D. and ESHWARAPPA, G. 2020. Stingless bees in sunflower pollination. Journal of Entomology and Zoology Studies, 8(1): 299-302.
    23. HERRERA, C. M. 1990. Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability in a summer-flowering mediterranean shrub. Oikos, 58(3): 277-288. Go to original source...
    24. HUNICKEN, P. L., MORALES, C. L., GARCIA, N. and GARIBALDI, L. A. 2020. Insect pollination, more than plant nutrition, determines yield quantity and quality in apple and pear. Neotropical Entomology, 49(4): 525-532. Go to original source...
    25. KAHONO, S., PANUWAN, C. and ENGEL, M. S. 2018. Social Bees and the Current Status of Beekeeping in Indonesia. In: Asian Beekeeping in the 21st Century. Springer Singapore, pp. 287-306. Go to original source...
    26. KAJOBE, R. and ECHAZARRETA, C. M. 2005. Temporal resource partitioning and climatological influences on colony flight and foraging of stingless bees (Apidae; Meliponini) in Ugandan tropical forests. African Journal of Ecology, 43(3): 267-275. Go to original source...
    27. KAKUTANI, T., INOUE, T., TEZUKA, T. and MAETA, Y. 1993. Pollination of strawberry by the stingless bee, Trigona minangkabau, and the honey bee, Apis mellifera: An experimental study of fertilization efficiency. Res. Popul. Ecol., 35: 95-111. Go to original source...
    28. KISHAN, T. M., SRINIVASAN, M. R., RAJASHREE, V. and THAKUR, R. K. 2017. Stingless bee Tetragonula iridipennis Smith for pollination of greenhouse cucumber. Journal of Entomology and Zoology studies, 5(4): 1729-1733.
    29. KLATT, B. K., HOLZSCHUH, A., WESTPHAL, C., CLOUGH, Y., SMIT, I., PAWELZIK, E. and TSCHARNTKE, T. 2014. Bee pollination improves crop quality, shelf life and commercial value. Proceedings of the Royal Society B: Biological Sciences, 281(1775): 20132440. Go to original source...
    30. KWAPONG, P., AIDOO, K., COMBEY, R., and KARIKARI, A. 2010. Stingless Bees: Importance, Management and Utilisation: A Training Manual for Stingless Bee Keeping. Stingless Bee Project, Ghana. Unimax Macmillan.
    31. LIU, Y., QI, J., LUO, J., QIN, W., LUO, Q., ZHANG, Q., WU, D., LIN, D., LI, S., DONG, H., CHEN, D., and CHEN, H. 2021. Okra in food field: nutritional value, health benefits and effects of processing methods on quality. Food Reviews International, 37(1): 67-90. Go to original source...
    32. LUNAU, K., PIOREK, V., KROHN, O. and PACINI, E. 2015. Just spines-mechanical defense of malvaceous pollen against collection by corbiculate bees. Apidologie, 46(2): 144-149. Go to original source...
    33. MARTIN, P. and BATESON, P. 1986. Measuring Behaviour: An Introductory Guide. Cambridge: Cambridge University Press.
    34. MUDRI-STOJNIC, S., ANDRIC, A., JOZAN, Z. and VUJIC, A. 2012. Pollinator diversity (Hymenoptera and Diptera) in semi-natural habitats in Serbia during summer. Archives of Biological Sciences, 64(2): 777-786. Go to original source...
    35. MURRELL, D. C. and NASH, W. T. 1981. Nectar secretion by toria (Brassica campestris L. V. Toria) and foraging behaviour of three Apis species on toria in Bangladesh. Journal of Apicultural Research, 20(1): 34-38. Go to original source...
    36. NAVATHA, L. and SREEDEVI, K. 2012. Insect pollinator diversity and abundance in castor, Ricinus communis L. Current Biotica, 6(2): 251-253.
    37. NICODEMO, D., MALHEIROS, E. B., JONG, D. De and COUTO, R. H. N. 2013. Incremento da produção de pepino partenocárpico com abelhas sem ferrão e Africanizadas em casas de vegetação. Semina:Ciencias Agrarias, 34(6 SUPPL. 1): 3625-3634. Go to original source...
    38. NUNES-SILVA, P., HRNCIR, M., DA SILVA, C. I., ROLDAO, Y. S. and IMPERATRIZ-FONSECA, V. L. 2013. Stingless bees, Melipona fasciculata, as efficient pollinators of eggplant (Solanum melongena) in greenhouses. Apidologie, 44(5): 537-546. Go to original source...
    39. NYE, W. P. and ANDERSON, J. L. 1974. Insect pollinators frequenting strawberry blossoms and the effect of honey bees on yield and fruit quality. Journal of the American Society for Horticultural Science, 99(1): 40-44. Go to original source...
    40. PANGESTIKA, N. W., ATMOWIDI, T. and KAHONO, S. 2017. Pollen load and flower constancy of three species of stingless bees (Hymenoptera, Apidae, Meliponinae). Tropical Life Sciences Research, 28(2): 179 -187. Go to original source...
    41. PERERA, S. and KARUNARATNE, I. 2019. Floral visits of the wild bee, Lithurgus atratus, impact yield and seed germinability of okra, Abelmoschus esculentus, in Sri Lanka. Journal of Pollination Ecology, 25(1): 1-6. Go to original source...
    42. PLEASANTS, J. M. 1983. Nectar production patterns in Ipomopsis aggregata (Polemoniaceae). American Journal of Botany, 70(10): 1468-1475. Go to original source...
    43. PRIAWANDIPUTRA, W., AZIZI, M. G., RISMAYANTI, DJAKARIA, K. M., WICAKSONO, A. RAFFIUDIN, R., ATMOWIDI, T. and BUCHORI, D. 2020. Stingless Bees: Guide to Farming of Stingless Bees in Forest Border Village [in Indonesian: Lebah Tanpa Sengat (Stingless Bees): Panduan Budidaya Lebah Tanpa Sengat (Stingless Bees) di Desa Perbatasan Hutan]. ZSL Indonesia.
    44. PUTRA, D. P., DAHELMI, SALMAH, S. and SWASTI, E. 2016. Pollination in chili pepper (Capsicum annuum L.) by Trigona laeviceps and T. minangkabau. Journal of Entomology and Zoology Studies, 4(4): 191-194.
    45. PUTRA, D. P., MURNITA, and JASMI. 2020. Effect of inorganic fertilizers and stingless bee pollination on increasing productivity of corn (Zea mays L.). Indian Journal of Agricultural Research, 54(6): 811-814.
    46. PUTRA, R. E., PERMANA, A. D. and KINASIH, I. 2014. Application of asiatic honey bees (Apis cerana) and stingless bees (Trigona laeviceps) as pollinator agents of hot pepper (Capsicum annuum L.) at local Indonesia farm system. Psyche: A Journal of Entomology, 2014: 687979. Go to original source...
    47. R CORE TEAM. 2014. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.R-project.org/ [Accessed: 2021, November 8].
    48. SAEZ, A., NEGRI, P., VIEL, M. and AIZEN, M. A. 2019. Pollination efficiency of artificial and bee pollination practices in kiwifruit. Scientia Horticulturae, 246: 1017-1021. Go to original source...
    49. SANCHEZ, L. A., SLAA, E. J., SANDI, M. and SALAZAR, W. 2001. Use of stingless bees for commercial pollination in enclousers: A promise for the future. Acta Horticulturae, 561: 219-223. Go to original source...
    50. SANTOS, A. O. R., BARTELLI, B. F. and NOGUEIRA-FERREIRA, F. H. 2014. Potential pollinators of tomato, Lycopersicon esculentum (Solanaceae), in open crops and the effect of a solitary bee in fruit set and quality. Journal of Economic Entomology, 107(3): 987-994. Go to original source...
    51. SHIN, Y. S., PARK, S. D. and KIM, J. H. 2007. Influence of pollination methods on fruit development and sugar contents of oriental melon (Cucumis melo L. cv. Sagyejeol-Ggul). Scientia Horticulturae, 112(4): 388-392. Go to original source...
    52. SIHAG, R. C. 1986. Insect pollination increases seed production in cruciferous and umbelliferous crops. Journal of Apicultural Research, 25(2): 121-126. Go to original source...
    53. SURIAWANTO, N., ATMOWIDI, T. and KAHONO, S. 2017. Nesting sites characteristics of stingless bees (Hymenoptera: Apidae) in Central Sulawesi, Indonesia. Journal of Insect Biodiversity, 5(10): 1-9. Go to original source...
    54. THOMSON, J. D. 1986. Pollen transport and deposition by bumble bees in Erythronium: influences of floral nectar and bee grooming. British Ecological Society, 74(2): 329-341. Go to original source...
    55. TRAVERO, J. T., NUEZ, I. L. and SAGLIBA, W. S. 2012. Pollination of Apis mellifera and Trigona biroi on the productivity of solanaceous crops. International Journal of Environmental and Rural Development, 3(2): 99-102.
    56. VEIGA, J. C., MENEZES, C., VENTURIERI, G. C. and CONTRERA, F. A. L. 2013. The bigger, the smaller: relationship between body size and food stores in the stingless bee Melipona flavolineata. Apidologie, 44(3): 324-333. Go to original source...
    57. WALTERS, S. A. and TAYLOR, B. H. 2006. Efects of honey bee pollination on pumpkin fruit and seed yield. HortScience, 41(2): 370-373. Go to original source...
    58. WANG, Q., ZHENG, Y., YU, Y., GAO, H., LAI, C., LUO, X. and HUANG, X. 2019. Effects of cross-pollination by 'Murcott' tangor on the physicochemical properties, bioactive compounds and antioxidant capacities of 'Qicheng 52' navel orange. Food Chemistry, 270: 476-480. Go to original source...
    59. WICAKSONO, A., ATMOWIDI, T. and PRIAWANDIPUTRA, W. 2020. Flight activities and pollen load of Lepidotrigona terminata Smith (Apidae: Meliponinae). HAYATI J. Biosci. 27(2): 97-106. Go to original source...
    60. WIETZKE, A., WESTPHAL, C., GRAS, P., KRAFT, M., PFOHL, K., KARLOVSKY, P., PAWELZIK, E., TSCHARNTKE, T. and SMIT, I. 2018. Insect pollination as a key factor for strawberry physiology and marketable fruit quality. Agriculture, Ecosystems and Environment, 258: 197-204. Go to original source...
    61. WOODCOCK, T. S., LARSON, B. M. H., KEVAN, P. G., INOUYE, D. W. and LUNAU, K. 2014. Flies and flowers II: Floral attractants and rewards. Journal of Pollination Ecology, 12(8): 63-94. Go to original source...

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