Main Article Content
Abstract
An experiment was conducted to investigate the effect of seasonal changes on the morphological (corbicula, proboscis, forewing, and hindwing) and physiological (hypopharyngeal glands and differential haemocyte count) characters of Apis mellifera L. workers during autumn, winter, spring, and summer seasons in year 2021 and 2022. The study found that the maximum values for morphological parameters i.e., proboscis length, corbicula length, length and width of forewing and hindwing, and physiological parameters i.e., hypopharyngeal gland acini size (length, width and surface area) and counts of plasmatocytes and granulocytes were consistently obtained during spring season. Notably, the most substantial reduction in immune cell count occurred during winter. Furthermore, a constant pattern observed across all seasons, indicating a significant increase in the size of all morphological characteristics as bees transitioned from nurses to foragers. In contrast, nurse bees always have larger hypopharyngeal gland acini sizes compared to foragers in all seasons. The differential haemocyte counts indicated a prevalence of plasmatocytes in the adult bee haemolymph. However, as bees shifted from nursing to foraging, the percentage of plasmatocytes and granulocytes decreased, accompanied by an increase in pycnotic cells, which signify programmed cell death. Consequently, the spring season emerged as the most favorable period for the growth and development of worker honey bees. This season consistently showcased optimal morphological and physiological characteristics, underscoring its importance in the life cycle of Apis mellifera colonies.
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References
- Abou-Shaara, H. F., & Ahmed, M. E. (2015). Characterization and tracking changes of morphological characteristics in honey bee, Apis mellifera, colonies. Journal of Entomological and Acarological Research, 47(3), 103-108.
- Ajao, A. M., Oladimeji, Y. U., Idowu, A. B., Babatunde, S. K., & Obembe, A. (2014). Morphological characteristics of Apis mellifera L. (Hymenoptera: Apidae) in Kwara State, Nigeria. International Journal of Agriculture Sciences, 4(4), 171-175.
- Al-Kahtani, S. N., & Taha, E. K. A. (2014). Morphometric studies on dwarf honeybee Apis florea F. workers in Saudi Arabia. Journal of Apicultural Science, 58(1), 127–134.
- Al-Kahtani, S. N., & Taha, E. K. A. (2021). Morphometric study of Yemeni (Apis mellifera jemenitica) and Carniolan (A. m. carnica) honeybee workers in Saudi Arabia. Plos one, 16(2), e0247262.
- Al-Ghamdi, A. A., Al-Khaibari, A. M., & Mohamed, O. O. (2011). Consumption rate of some proteinic diets affecting hypopharyngeal glands development in honeybee workers. Saudi Journal of Biological Sciences, 18(1), 73–77.
- Ali, H., Abdulaziz, S. A., Javaid, I., Ayman, A. O., Hael, S. R., & Brian, H. S. (2019). Effect of season and behavioral activity on the hypopharyngeal glands of three honey bee, Apis mellifera L., races under stressful climatic conditions of central Saudi Arabia. Journal of Hymenoptera Research, 68, 85-101.
- Amdam, G. V., Simões, Z. L. P., Hagen, A., Norberg, K., Schrøder, K., Mikkelsen, Ø., Kirkwood, T. B. L., & Omholt, S. W. (2004). Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Experimental Gerontology, 39(5), 767–773.
- Antontseva, P. V. (1975). Seasonal changes in external characters of local bees in Dzhungarskii Alatau (mountains). Tert. Sborn. Nauch. Trud. Alma-Atin I Semipal, Zoovet, Institov, 36, 31-32.
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- Brouwers, E. V. M. (1982). Measurement of hypopharyngeal gland activity in the honey bees. Journal of Apicultural Research, 21(4), 193-198.
- Deseyn, J., & Billen, J. (2005). Age-dependent morphology and ultrastructure of the hypopharyngeal gland on Apis mellifera workers (Hymenoptera: Apidae). Apidologie, 36(1), 49-57.
- Diab, A. M., Shehata, I. A. A., Nafea, E. A., & Abdallah, M. L. (2018). Influence of different diets on honey bee workers (Apis mellifera L.) hemocytes. Egyptian Journal of Agricultural Research, 96(4), 1405-1411.
- Döke, M. A., Frazium, M., & Grozinger, C. (2015). Overwintering Honey Bees: Biology and Management. Current Opinion in Insect Science, 10, 185-193.
- Edriss, M. A., Mostajeran, M., & Ebadi, R. (2002). Correlation between honey yield and morphological traits of honey bee in Isfahan. Journal of Science and Technology of Agriculture and Natural Resource, 6(2), 91-103.
- Free, J. B. (1993). Insect pollination of crops. Academic press, London and New York.
- Gupta, R. K. (2014). Taxonomy and distribution of different honeybee species. In Beekeeping for poverty alleviation and livelihood security, pp. 63-103. Springer: Dordrecht.
- Herbert, E. W. Jr., Sylvester, H. A., Vandenberg, J. D., & Shimanuki, H. (1988). Influence of nutritional stress and the age of adults on the morphometrics of honey bees (Apis mellifera L.). Apidologie, 19(3), 221-230.
- Hystad, E. M., Salmela, H., Amdam, G. V., & Münch, D. (2017). Hemocyte mediated phagocytosis differs between honeybee (Apis mellifera) worker castes. PLoS ONE, 12(9), e018418.
- Jedruszuk, A. (1998). Total hemocytes count in hemolymph of adult worker honey bees (Apis mellifera L.) from spring-summer and autumn-winter generations. Pszczelnicze Zsezyty Naukowe, 42(2), 43-44.
- Johnson, B. R. (2008). Within-nest temporal polyethism in the honey bee. Behavioral Ecology and Sociobiology, 62, 777-784.
- Johnson, B. R. (2010). Division of labor in honey bees: form, function, and proximate mechanisms. Behavioral Ecology and Sociobiology, 64, 305-316.
- Kaur, G., Sharma, R., Chaudhary, A., & Singh, R. (2021). Factors affecting immune responses in honey bees: an insight. Journal of Apiculture Science, 65(1), 25-47.
- Le Conte, Y., & Navajas, M. (2008). Climate change: impact on honey bee population and diseases. Revue scientifique et technique/office international does epizooties, 27(2), 499-510.
- Mattu, V. K., & Verma, L.R. (1983). Comparative morphometric studies on the Indian honey bee of the North West Himalayas. 1. Tongue and antenna. Journal of Apiculture Science, 22, 79-85.
- Mattu, V. K., & Verma, L.R. (1984). Comparative morphometric studies on the Indian honey bee Apis cerana indica F., effect of seasonal variations. Apidologie, 15, 63-74.
- Maurizio, A. (1954). Pollenernährung und Lebensvorgänge bei der Honigbiene (Apis mellifica L.). Landw. Jb. Schweiz. 68(2),115-182.
- Millar, D. A., & Ratcliffe, N. A. (1994). Invertebrates, pp. 29–68. In: Turner, R.J. (Ed.), Immunology: A Comparative Approach. John Wiley & Son, West Sussex.
- Mostajeran, M., Edriss, M. A., & Basiri, M. R. (2006). Analysis of colony and morphological characters in honey bees (Apis mellifera meda). Pakistan Journal of Biological Sciences, 9(14), 2685-2688.
- Musila, J., & Přidal, A. (2024). Seasonal Changes in Hemolymph Protein Level and Hypopharyngeal Gland Size Depending on Age and In-Nest Location of Honeybee Workers. Animals, 14(3), 512.
- Papa, G., Maier, R., Durazzo, A., Lucarini, M., Karabagias, I. K., Plutino, M., Bianchetto, E., Aromolo, R., Pignatti, G., Ambrogio, A., & Pellecchia, M. (2022). The honey bee Apis mellifera: An insect at the interface between human and ecosystem health. Biology, 11(2), 233.
- Richardson, R. T., Ballinger, M. N., Qian, F., Christman, J. W., & Johnson, R. M. (2018). Morphological and functional characterization of honey bee, Apis mellifera, hemocyte cell communities. Apidologie, 49, 397–410. http://
- Shakeel, M., Ahmad, S., Ali, H., Al-Kahtani, S., Ghramh, H., & Khan, Kh. (2020). Seasonal impact and comparative analysis of hypopharyngeal glands in worker and forager honey bees of two different species: Apis mellifera and A. cerana. Fresenius Environmental Bulletin, 29(10), 9024–9030.
- Shawer, M. B., Taha, E. K. A., Mousa, K. M., Khan, K. A., Ibrahim, S., Hassan, S., & Elnabawy, E. S. M. (2021). Seasonal variations of colony activities linked to morphometric and glands characterizations of hybrid Carniolan honey bee (Apis mellifera carnica Pollmann) workers. Journal of King Saud University-Science, 33(6), 101543.
- Siddiqui, M. I., & Al-Khalifa, M. S. (2014). Review of hemocyte count, response to chemicals, phagocytosis, encapsulation and metamorphosis in insects. Italian Journal of Zoology, 81(1), 2-15.
- Steinmann, N., Corona, M., Neumann, P., & Dainat, B. (2015). Overwintering is associated with reduced expression of immune genes and higher susceptibility to virus infection in honey bees. PLoS ONE, 10(6), e0129956.
- Tuell, J. K., & Isaacs, R. (2010). Weather during bloom affects pollination and yield of highbush blueberry. Journal of Economic Entomology, 103(3), 557–562.
- Xu, X., Du, X., Zhou, S., Zhou, B., Lai, K., Wang, Q., Li, H., Zhu, C., Xu, H., Zhang, X. & Zhu, X. (2023). Impacts of high temperature during early capped brood on pupal development and the size of appendages in adult workers Apis cerana. Frontiers in Ecology and Evolution, 11, 1144216.
References
Abou-Shaara, H. F., & Ahmed, M. E. (2015). Characterization and tracking changes of morphological characteristics in honey bee, Apis mellifera, colonies. Journal of Entomological and Acarological Research, 47(3), 103-108.
Ajao, A. M., Oladimeji, Y. U., Idowu, A. B., Babatunde, S. K., & Obembe, A. (2014). Morphological characteristics of Apis mellifera L. (Hymenoptera: Apidae) in Kwara State, Nigeria. International Journal of Agriculture Sciences, 4(4), 171-175.
Al-Kahtani, S. N., & Taha, E. K. A. (2014). Morphometric studies on dwarf honeybee Apis florea F. workers in Saudi Arabia. Journal of Apicultural Science, 58(1), 127–134.
Al-Kahtani, S. N., & Taha, E. K. A. (2021). Morphometric study of Yemeni (Apis mellifera jemenitica) and Carniolan (A. m. carnica) honeybee workers in Saudi Arabia. Plos one, 16(2), e0247262.
Al-Ghamdi, A. A., Al-Khaibari, A. M., & Mohamed, O. O. (2011). Consumption rate of some proteinic diets affecting hypopharyngeal glands development in honeybee workers. Saudi Journal of Biological Sciences, 18(1), 73–77.
Ali, H., Abdulaziz, S. A., Javaid, I., Ayman, A. O., Hael, S. R., & Brian, H. S. (2019). Effect of season and behavioral activity on the hypopharyngeal glands of three honey bee, Apis mellifera L., races under stressful climatic conditions of central Saudi Arabia. Journal of Hymenoptera Research, 68, 85-101.
Amdam, G. V., Simões, Z. L. P., Hagen, A., Norberg, K., Schrøder, K., Mikkelsen, Ø., Kirkwood, T. B. L., & Omholt, S. W. (2004). Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Experimental Gerontology, 39(5), 767–773.
Antontseva, P. V. (1975). Seasonal changes in external characters of local bees in Dzhungarskii Alatau (mountains). Tert. Sborn. Nauch. Trud. Alma-Atin I Semipal, Zoovet, Institov, 36, 31-32.
Bamidele, J. A., Idowu, A. B., Ademolu, K. O., Osipitan, A. A., & Ajao, A. M. (2023). Seasonal variation in some morphological characters of Apis mellifera adansonii workers from three ecological zones of Nigeria. 1899-1911.
Brouwers, E. V. M. (1982). Measurement of hypopharyngeal gland activity in the honey bees. Journal of Apicultural Research, 21(4), 193-198.
Deseyn, J., & Billen, J. (2005). Age-dependent morphology and ultrastructure of the hypopharyngeal gland on Apis mellifera workers (Hymenoptera: Apidae). Apidologie, 36(1), 49-57.
Diab, A. M., Shehata, I. A. A., Nafea, E. A., & Abdallah, M. L. (2018). Influence of different diets on honey bee workers (Apis mellifera L.) hemocytes. Egyptian Journal of Agricultural Research, 96(4), 1405-1411.
Döke, M. A., Frazium, M., & Grozinger, C. (2015). Overwintering Honey Bees: Biology and Management. Current Opinion in Insect Science, 10, 185-193.
Edriss, M. A., Mostajeran, M., & Ebadi, R. (2002). Correlation between honey yield and morphological traits of honey bee in Isfahan. Journal of Science and Technology of Agriculture and Natural Resource, 6(2), 91-103.
Free, J. B. (1993). Insect pollination of crops. Academic press, London and New York.
Gupta, R. K. (2014). Taxonomy and distribution of different honeybee species. In Beekeeping for poverty alleviation and livelihood security, pp. 63-103. Springer: Dordrecht.
Herbert, E. W. Jr., Sylvester, H. A., Vandenberg, J. D., & Shimanuki, H. (1988). Influence of nutritional stress and the age of adults on the morphometrics of honey bees (Apis mellifera L.). Apidologie, 19(3), 221-230.
Hystad, E. M., Salmela, H., Amdam, G. V., & Münch, D. (2017). Hemocyte mediated phagocytosis differs between honeybee (Apis mellifera) worker castes. PLoS ONE, 12(9), e018418.
Jedruszuk, A. (1998). Total hemocytes count in hemolymph of adult worker honey bees (Apis mellifera L.) from spring-summer and autumn-winter generations. Pszczelnicze Zsezyty Naukowe, 42(2), 43-44.
Johnson, B. R. (2008). Within-nest temporal polyethism in the honey bee. Behavioral Ecology and Sociobiology, 62, 777-784.
Johnson, B. R. (2010). Division of labor in honey bees: form, function, and proximate mechanisms. Behavioral Ecology and Sociobiology, 64, 305-316.
Kaur, G., Sharma, R., Chaudhary, A., & Singh, R. (2021). Factors affecting immune responses in honey bees: an insight. Journal of Apiculture Science, 65(1), 25-47.
Le Conte, Y., & Navajas, M. (2008). Climate change: impact on honey bee population and diseases. Revue scientifique et technique/office international does epizooties, 27(2), 499-510.
Mattu, V. K., & Verma, L.R. (1983). Comparative morphometric studies on the Indian honey bee of the North West Himalayas. 1. Tongue and antenna. Journal of Apiculture Science, 22, 79-85.
Mattu, V. K., & Verma, L.R. (1984). Comparative morphometric studies on the Indian honey bee Apis cerana indica F., effect of seasonal variations. Apidologie, 15, 63-74.
Maurizio, A. (1954). Pollenernährung und Lebensvorgänge bei der Honigbiene (Apis mellifica L.). Landw. Jb. Schweiz. 68(2),115-182.
Millar, D. A., & Ratcliffe, N. A. (1994). Invertebrates, pp. 29–68. In: Turner, R.J. (Ed.), Immunology: A Comparative Approach. John Wiley & Son, West Sussex.
Mostajeran, M., Edriss, M. A., & Basiri, M. R. (2006). Analysis of colony and morphological characters in honey bees (Apis mellifera meda). Pakistan Journal of Biological Sciences, 9(14), 2685-2688.
Musila, J., & Přidal, A. (2024). Seasonal Changes in Hemolymph Protein Level and Hypopharyngeal Gland Size Depending on Age and In-Nest Location of Honeybee Workers. Animals, 14(3), 512.
Papa, G., Maier, R., Durazzo, A., Lucarini, M., Karabagias, I. K., Plutino, M., Bianchetto, E., Aromolo, R., Pignatti, G., Ambrogio, A., & Pellecchia, M. (2022). The honey bee Apis mellifera: An insect at the interface between human and ecosystem health. Biology, 11(2), 233.
Richardson, R. T., Ballinger, M. N., Qian, F., Christman, J. W., & Johnson, R. M. (2018). Morphological and functional characterization of honey bee, Apis mellifera, hemocyte cell communities. Apidologie, 49, 397–410. http://
Shakeel, M., Ahmad, S., Ali, H., Al-Kahtani, S., Ghramh, H., & Khan, Kh. (2020). Seasonal impact and comparative analysis of hypopharyngeal glands in worker and forager honey bees of two different species: Apis mellifera and A. cerana. Fresenius Environmental Bulletin, 29(10), 9024–9030.
Shawer, M. B., Taha, E. K. A., Mousa, K. M., Khan, K. A., Ibrahim, S., Hassan, S., & Elnabawy, E. S. M. (2021). Seasonal variations of colony activities linked to morphometric and glands characterizations of hybrid Carniolan honey bee (Apis mellifera carnica Pollmann) workers. Journal of King Saud University-Science, 33(6), 101543.
Siddiqui, M. I., & Al-Khalifa, M. S. (2014). Review of hemocyte count, response to chemicals, phagocytosis, encapsulation and metamorphosis in insects. Italian Journal of Zoology, 81(1), 2-15.
Steinmann, N., Corona, M., Neumann, P., & Dainat, B. (2015). Overwintering is associated with reduced expression of immune genes and higher susceptibility to virus infection in honey bees. PLoS ONE, 10(6), e0129956.
Tuell, J. K., & Isaacs, R. (2010). Weather during bloom affects pollination and yield of highbush blueberry. Journal of Economic Entomology, 103(3), 557–562.
Xu, X., Du, X., Zhou, S., Zhou, B., Lai, K., Wang, Q., Li, H., Zhu, C., Xu, H., Zhang, X. & Zhu, X. (2023). Impacts of high temperature during early capped brood on pupal development and the size of appendages in adult workers Apis cerana. Frontiers in Ecology and Evolution, 11, 1144216.