The Beneficial Effects of Honey Bees (Apis mellifera L.) as a Potential Pollinator on Quantitative and Qualitative Yield Parameters of Sunflower (Helianthus annuus L.)

Öz

A field study was conducted at the experimental station of the Bee Research Department, Naqada region, Qena Governorate, Egypt, during the 2024 sunflower (Helianthus annuus L.) flowering season. This research aimed to identify the insect pollinator community associated with sunflower plants, particularly honey bees (Apis mellifera L.), to evaluate their foraging ecology and quantify their effects on H. annuus yield parameters. The study implemented three pollination scenarios: open pollination (OP), allowing full insect pollinator access; managed honey bee-only (MHO), providing exclusive A. mellifera pollination within an isolated netted plot containing one colony; and non-pollinated (NP) plants, where pollinators were excluded using insect-proof mesh cages. Hymenoptera included the main pollinators (90%) especially A. mellifera, which recorded the most abundant pollinator (78%). The peak foraging activity of A. mellifera on sunflowers recorded at 9 am (excluding January 18), declined by midday (12 pm), and was lowest in the afternoon (3 pm). A. mellifera foragers exhibited significantly longer mean visitation durations (seconds capitulum) during mid-February compared to late February under OP conditions. Sunflowers under OP condition yielded the most seeds per plant head (565.67 head⁻¹), surpassing MHO (450.67 head⁻¹) and NP (241.33 head⁻¹). The NP group had statistically significant lower yield parameters (head weight per plant, number of seeds per head, 100-seed weight (g.), seed yield (t ha-1), seed set, oil content % and seed germination %) than the OP and/or MHO. The difference in seed yield, weight, oil content% and germination% between OP and MHO pollination conditions was statistically non-significant (p > 0.05). However, MHO exhibited superior seed setting compared to OP and NP, recording 93.78%, 89.00 and 26%, respectively. Our results concluded that MHO plays a significant role in sunflower pollination, leading to substantial improvements in yield parameters compared to NP. However, they might not fully compensate for the absence of other pollinators in terms of the number of seeds per head and head weight.

Anahtar Kelimeler

• Sunflower
• Pollination
• Foraging behavior
• Seed set
• Oil content

Kaynakça

1. Abbasi, K. H., Jamal, M., Ahmad, S., Ghramh, H. A., Khanum, S., Khan, K. A., Ullah, M. A., Aljedani, D. M. and Zulfiqar, B. (2021). Standardization of managed honey bee (Apis mellifera) hives for pollination of Sunflower (Helianthus annuus) crop. Journal of King Saud University-Science, 33(8): 101608.
2. Abdel-Rahman, M. O. and Moustafa, A. D. (2012). An estimate of honeybee colony losses and their perceived reasons during two years in Qena and Luxor Governorates, Upper Egypt. Assiut Journal of Agricultural Sciences, 43(2): 91-104.
3. Abdelsatar, M. A., Ahmed, A. A. E. H. and Ibrahim, S. E. L. K. (2020). Genetic variability and selection criteria of some sunflower genotypes under different pollination methods. Acta agriculturae Slovenica, 116(1): 35-47.
4. Al Naggar, Y., Codling, G., Giesy, J. P. and Safer, A. (2018). Beekeeping and the need for pollination from an agricultural perspective in Egypt. Bee World, 95(4): 107-112.
5. Ali, H, Randhawa, S. A. and Yousaf, M. (2004). Quantitative and qualitative traits of sunflower (Helianthus annus L.) as influenced by planting dates and nitrogen application. International Journal of Agriculture and Biology, 6: 410-412.
6. Ali, Q., Ali, M., Khan, F. Z. A. and Awan, T. H. (2024). Comparing the Efficacy of Single and Multiple Visits by Honey and Solitary Bees on Sunflower Seed Production. Sociobiology, 71(4): 10425.
7. Altayeb, O. A. E. and Nagi, S. K. E. (2015). Efficacy of honeybees (Apis mellifera) on the production of sunflower (Helianthus annus L.) seeds in the Sudan. Journal of Experimental Biology and Agricultural Sciences, 3(2): 191-195.
8. American Oil Chemists Society – AOCS (1985). Official methods and recommended practices of the American Oil Chemists’ Society. American Oil Chemists’ Society, Champaign.

9. Amro, A. M. (2021). Pollinators and pollination effects on three canola (Brassica napus L.) cultivars: A case study in Upper Egypt. Journal of King Saud University-Science, 33(1): 101240.
10. Borror, D., Triplehorn, C. and Johnson, N. (1989). An Introduction to the Study of Insects. 6th edition, Saunders College Publishing, Philadelphia, U. S. A.
11. Charrière, J. D., Imdorf, A., Koenig, C., Gallmann, S. and Kuhn, R. (2010). Do sunflowers influence the development of honey bee, Apis mellifera, colonies in areas with diversified crop farming. Journal of Apicultural Research, 49(3): 227-235.
12. Debaeke, P., Casadebaig, P., Flenet, F. and Langlade, N. (2017). Sunflower crop and climate change: vulnerability, adaptation, and mitigation potential from case-studies in Europe. OCL Oilseeds and fats crops and lipids, 24(1): 15-25.
13. DeGrandi-Hoffman, G. and Watkins, J. C. (2000). The foraging activity of honey bees Apis mellifera and non-Apis bees on hybrid sunflowers (Helianthus annuus) and its influence on cross-pollination and seed set. Journal of Apicultural Research, 39(1-2): 37-45.
14. Facylate, K. K. (1971). Field Studies of Soil Invertebrate. 2nd ed. Vishia Shkoola Press, Moscow, USSR. Ferguson, B., Prasifka, J. R., Carroll, M. J., Corby-Harris, V. and DeGrandi-Hoffman, G. (2024). Honey bee (Apis mellifera L.) foraging rewards in sunflowers: effect of floral traits on visitation and variation in pollen quality over two consecutive years. Journal of Apicultural Research, 63(4): 622-630.
15. Goras, G., Tananaki, C., Dimou, M., Tscheulin, T., Petanidou, T. and Thrasyvoulou, A. (2016). Impact of honeybee (Apis mellifera L.) density on wild bee foraging behaviour. Journal of Apicultural Science, 60: 49-62.
16. Greenleaf, S. S. and Kremen, C. (2006). Wild bees enhance honey bees’ pollination of hybrid sunflower. Proceedings of the National Academy of Sciences, 103(37): 13890-13895.
17. Gürkan, H. (2023). Evaluation of the impacts of climate change on sunflower with aquacrop model. Journal of Tekirdag Agricultural Faculty, 20(4): 933-947.
18. Hussein, M. H. and Abdel-Aal, S. A. (1982). Wild and honeybees as pollinators of 10 plant species in Assiut area, Egypt. Assiut journal of Agricultural, 93: 342-346.
19. Idrees, A., Qadir, Z. A., Hasnat, A. U., Afzal, A., Ahmad, S., Aqueel, M. A., Li, Z., Rady, A., Ali, S. and Li, J. (2023). Effectiveness of honeybee (Apis mellifera) visit on the pollination of different sunflower cultivars. Journal of King Saud University-Science, 35(7): 102837.
20. Jilo, K. R., Edeo, M. A., Hunde, T. A. and Aboye, B. M. (2025). Fatty acid composition, oil yield, and oil content of sunflower (Helianthus annuus L.) across different pollination treatments. Journal of Biosciences, 50(2): 1-8.
21. Karso, B. A., Dabash, A. H. and Bas, S. M. A. (2023). The Effect of Honeybee for Increasing of Sunflower Productivity. 4th International Agricultural Conference (IAC-2023), 10-11 January, Mosul, Iraq.
22. Kendarini, N., Herwati, A., Novansyah, R. A., and Ardiarini, N.R. (2025). Determining the Relationship Between Yield and Yield Components in Sunflower (Helianthus annuus L.). Journal of Agriprecision and Social Impact, 2(1): 140-152.
23. Kevan P. G. (2001) Pollination: Plinth, Pedestal, and Pillar for Terrestrial Productivity. The Why, How, and Where of Pollination Protection, Conservation, and Promotion. In: Bees and Crop Pollination Crisis, Crossroads, Conservation. Ed(s): Stubbs, C. S. and Drummond, F. A., Thomas Say Publications in Entomology. Entomological Society of America, Lanham, Maryland, U. S. A.
24. Kevan, P. and Eisikowitch, D. (1990). The effects of insect pollination on canola (Brassica napus L. cv. OAC Triton) seed germination. Euphytica, 45(1): 39-41.
25. Kevan, P. G. and Viana, B. F. (2003). The global decline of pollination services. Biodiversity, 4(4): 3-8.
26. Mallinger, R. E. and Prasifka, J. R. (2017). Bee visitation rates to cultivated sunflowers increase with the amount and accessibility of nectar sugars. Journal of Applied Entomology, 141(7): 561-573.
27. Mallinger, R. E., Bradshaw, J., Varenhorst, A. J. and Prasifka, J. R. (2019). Native solitary bees provide economically significant pollination services to confection sunflowers (Helianthus annuus L.) (Asterales: Asteraceae) grown across the Northern Great Plains. Journal of Economic Entomology, 112(1): 40-48.
28. McCabe, L. M. and Cobb, N. S. (2021). From bees to flies: global shift in pollinator communities along elevation gradients. Frontiers in Ecology and Evolution, 8: 626124.
29. Mota, L., Loureiro, J., González, J. A., Hevia, V., Ortega-Marcos, J. J., Rad, C., Marks, E. A. and Castro, S. (2024). Optimizing sunflower yield: Understanding pollinator contribution to inform agri-environmental strategies. Field Crops Research, 319: 109651.
30. Moustafa, A. M., M Khodairy, M. and Aly, A. M. (2008). Role of the insect pollinators, especially honey bee on productivity of sunflower seed yield and its relation to some other factors. Assiut Journal of Agricultural Sciences, 39(2): 149-164.
31. Muhammad, W., Saeed, S., Ahmad, A., Ishfaq, M. Y. and Anjum, M. M. (2021). Pollinator community of sunflower (Helianthus annus L.) and its role in crop reproductive success. Asian Journal of Agricultural and Biology, 2: 1-6.
32. Nene, W. A., Manoko, M. L. and Muruke, M. H. (2024). Pollination potential of African honey bees, Apis mellifera (litorea):(Hymenoptera: Apidae) in sunflower, Helianthus annuus production in South-Eastern Tanzania. Journal of Apicultural Research, 63(5): 868-874.
33. Önemli, F. and Önemli, G. (2023). Evaluation of Wild Annual Sunflower Species for Some Morphological, Phenological, and Agronomic Characters under Field Conditions. Journal of Tekirdag Agricultural Faculty, 20(4): 857-870.
34. Perrot, T., Gaba, S., Roncoroni, M., Gautier, J. L., Saintilan, A. and Bretagnolle, V. (2019). Experimental quantification of insect pollination on sunflower yield, reconciling plant and field scale estimates. Basic and Applied Ecology, 34: 75-84.
35. Roath, W. W. and Miller, J. F. (1982). Environmental effects on seed set in oilseed Sunflower (Helianthus annuus L.). Canadian Journal of Plant Sciences, 62: 867-873.
36. Roch, J. C., Malfi, R., Van Wyk, J. I., Muñoz Agudelo, D. C., Milam, J. and Adler, L. S. (2023). The intersection of bee and flower sexes: pollen presence shapes sex-specific bee foraging associations in sunflower. Environmental Entomology, 52(3): 480-490.
37. Said, F., Inayatullah, M. and Hussain, A. (2017). Studies on visitation pattern of honeybee (Hymenoptera: Apidae) and its impact on the yield and oil contents of sunflower (Helianthus annuus L.) seed in Peshawar valley, Pakistan. Pakistan Journal of Zoology, 49(3): 943-949.
38. Shapiro, S. S. and Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52(3-4): 591-611.