Palynological Diversity of Melliferous flora around Apiaries from District Mardan Khyber Pakhtunkhwa-Pakistan

The Botanical Review - Tập 88 - Trang 299-332 - 2021
Nabila1, Mushtaq Ahmad1,2, Muhammad Ali2,3, Muhammad Zafar1, Shazia Sultana1, Salman Majeed4, Ghulam Yaseen1, Shabir Ahmad4
1Department of Plant Sciences, Quaid-I-Azam University, Islamabad, Pakistan
2Quaid-I-Azam University, Islamabad, Pakistan
3Pakistan Academy of Sciences, Islamabad, Pakistan
4Department of Plant Sciences, Quaid- i- Azam University, Islamabad, Pakistan

Tóm tắt

The guiding principles for raising beekeeping products in developing countries provide support for commercializing honey production in order to generate income for beekeepers through the exploration of melliferous flora. The main objective of this study was to conduct a preliminary investigation into the pollen morphology of selected melliferous species that are frequently visited by honeybees in the vicinity of apiaries in the district of Mardan, Khyber Pakhtunkhwa. In this study, an updated overview was provided by reviewing the literature regarding palynological investigation of melliferous flora. The morpho-palynological features, dominant plant families visited by honeybees, and life forms of melliferous species were also discussed. The Acetolysis method was used to prepare the microscopic slides of pollen, measure and describe the qualitative and quantitative features using LM and SEM. Results showed maximum pollen polar and equatorial diameter in M. azadirachta (37.9 μm) and (40.9 μm) respectively. The polar to equatorial diameter ratio (P/E) was observed to be the highest in M. domestica (1.14). Colpi length was calculated to be the highest in the P. granatum (13.8 μm). The highest percentage of pollen fertility was calculated in V. tricolor (92.5%), whereas the lowest was in O. rosea (64.28%). Studied characters under LM and SEM have appeared as a useful tool for the delimitation of melliferous flora, which may lead to the correct identification of the potential and valuable bee floral resources for beekeepers. The outcomes of this study aid in the assessment of melliferous flora and help in providing conservation measures for the sustainable development of beekeeping and the honeybee flora of the region.

Tài liệu tham khảo

Agwu, C.O.C., Essien, B.C., & Badmus, S.A. (2013). Melissopalynological study of honey samples from four localities in Dekina local government area of Kogi state, Nigeria. Journal of Biological and Chemical Research, 30(2), 921-928. Ahmad, M., Khan, M.A., Hasan, A., Zafar, M., & Sultana, S. (2008). Chemotaxonomic standardization of herbal drugs milk thistle and globe thistle. Asian Journal of Chemistry, 20(6), 4443. Ahmad, M., Bano, A., Zafar, M., Khan, M. A., Chaudhry, M. J. I., & Sultana, S. (2013). Pollen morphology of some species of the family asteraceae from the alpine zone, Deosai Plateau, northern Pakistan. Palynology, 37(2), 189-195. Ahmad, M., Ozdimir, F., Zafar, M., Ahmad, S., & Sultana, S. (2019a). Bee flora of Himalayan region (Pakistan) for sustainable rural development using SEM techniques for pollen identification. uluslararasi aricilik arastirmalari ve surdurulebilir kirsal kalkinma stratijileri kongresi ekimbingul, 11-13. Ahmad, S., Zafar, M., Ahmad, M., Ozdemir, F.A., Yaseen, G., Sultana, S. & Kutlu, M.A. (2020). Palynological Studies of Winter Weeds Melliferous Flora of District Bannu, Khyber Pakhtunkhwa, Pakistan. Annali di Botanica, 10. doi: https://doi.org/10.13133/2239-3129/14863. Ahmad, S., Zafar, M., Ahmad, M., Yaseen, G. & Sultana, S. (2019b). Microscopic investigation of palyno-morphological features of melliferous flora of Lakki Marwat district, Khyber Pakhtunkhwa, Pakistan. Microscopy research and technique, 82(6), 720-730. https://doi.org/10.1002/jemt.23218 Al-Ghamdi, A., Al-Abbadi, A.A., Khan, K.A., Ghramh, H.A., Ahmed, A.M., & Ansari, M.J. (2020a). In vitro antagonistic potential of gut bacteria isolated from indigenous honey bee race of Saudi Arabia against Paenibacillus larvae. Journal of Apicultural Research, 59(5), 825-833. https://doi.org/10.1080/00218839.2019.1706912 Al-Ghamdi, A.A., Al-Khulaidi, A., Al-Sagheer, N.A., Nuru, A. & Tadesse, Y. (2020b). Identification, characterization and mapping of honeybee flora of Al-Baha region of Saudi Arabia. Journal of Environmental Biology, 41(3), 613-622. https://doi.org/10.22438/jeb/41/3/MRN-1208 Amina, H., Ahmad, M., Bhatti, G. R., Zafar, M., Sultana, S., Butt, M. A., Bahadur, S., Haq, I. U., Ghufran, M. A., & Ahmad, S. (2020). Microscopic investigation of pollen morphology of Brassicaceae from Central Punjab-Pakistan. Microscopy Research and Technique, 83(4), 446-454. https://doi.org/10.1002/jemt.23432 Asmat, T., Khan, M. A., Ahmed, M., Zafar, M., Manzoor, F., Munir, M., Akhtar, K., Bashir, S., Mukhtar, T., & Ambreen, M. (2011). Pollen morphology of selected species of Scrophulariaceae of District Dir Upper, Pakistan. Journal of Medicinal Plants Research, 5(28), 6423-6428. Bahadur, S., Ahmad, M., Mir, S., Zafar, M., Sultana, S., Ashfaq, S., & Arfan, M. (2018). Identification of monocot flora using pollen features through scanning electron microscopy. Microscopy Research and Technique, 81(6), 599-613. https://doi.org/10.1002/jemt.23015 Begum, H.A., Iqbal, J., & Aziz, A., 2021. Characterization of pollen profile of Apis mellifera L. in arid region of Pakistan. Saudi Journal of Biological Sciences, 28(5), 2964-2974. https://doi.org/10.1016/j.sjbs.2021.02.035 Bhalchandra, W., Baviskar, R., & Nikam, T. (2014). Diversity of nectariferous and polleniferous bee flora at Anjaneri and Dugarwadi hills of Western Ghats of Nasik district (MS) India. Journal of Entomology and Zoology Studies, 2(4), 244-249. Bohart, G.E. (1960). Insect pollination of forage legumes. Bee World, 41(4), 85-97. Camargo, S.C., Garcia, R.C., Feiden, A., Vasconcelos, E.S., Pires, B.G., Hartleben, A.M., Moraes, F.J., Oliveira, L.D., Giasson, J., Mittanck, E.S. & Gremaschi, J.R. (2014). Implementation of a geographic information system (GIS) for the planning of beekeeping in the west region of Paraná. Anais da Academia Brasileira de Ciências, 86(2), 955-971. https://doi.org/10.1590/0001-3765201420130278 Çeter, T., Pinar, N. M., İnceer, H., Hayirlioğlu-Ayaz, S., & Yaprak, A. E. (2013). The comparative pollen morphology of genera Matricaria L. and Tripleurospemum Sch. Bip.(Asteraceae) in Turkey. Plant systematics and evolution, 299(5), 959-977. https://doi.org/10.1007/s00606-013-0776-z Chauhan, M.S., Farooqui, A. & Trivedi, A. (2017). Plants foraged by bees for honey production in northern India: The diverse flora of India and its implications for apiculture. Acta palaeobotanica, 57(1), 119-132. DOI: https://doi.org/10.1515/acpa-2017-0003 Chaubal, R., Zanella, C., Trimnell, M.R., Fox, T.W., Albertsen, M.C., & Bedinger, P. (2000). Two male-sterile mutants of Zea mays (Poaceae) with an extra cell division in the anther wall. American journal of botany, 87(8), 1193-1201. Coh-Martínez, M.E., Cetzal-Ix, W., Martínez-Puc, J.F., Basu, S.K., Noguera-Savelli, E., & Cuevas, M.J. (2019). Perceptions of the local beekeepers on the diversity and flowering phenology of the melliferous flora in the community of Xmabén, Hopelchén, Campeche, Mexico. Journal of ethnobiology and ethnomedicine, 15(1), pp.1-16. https://doi.org/10.1186/s13002-019-0296-1 Crane, E. (1973). Honey sources in some tropical and subtropical countries. Bee world, 54(4), 177-186. de Oliveira Souza, S., Souza de Oliveira, R., Aona, L.Y.S., Souza, F.V.D., Soares, T.L., Rossi, M.L., & de Souza, E.H. (2020). Pollen morphology and viability of Tillandsia (Bromeliaceae) species by light microscopy and scanning electron microscopy. Microscopy Research and Technique, 84(3), 441-459. https://doi.org/10.1002/jemt.23601 Dimou, M., & Thrasyvoulou, A. (2007). Seasonal variation in vegetation and pollen collected by honeybees in Thessaloniki, Greece. Grana, 46(4), 292-299. https://doi.org/10.1080/00173130701760718 González-Suárez, M., Mora-Olivo, A., Villanueva-Gutiérrez, R., Lara-Villalón, M., Vanoye-Eligio, V. & Guerra-Pérez, A. (2020). Diversity of melliferous flora in the State of Tamaulipas, Mexico. Revista Mexicana De Ciencias Pecuarias, 11(3), 914-932. https://doi.org/10.22319/rmcp.v11i3.4717 Ibrahim, M., Khan, M.N., Ali, S., Razzaq, A., Zaman, A., Iqbal, M., & Jan, F. (2019). Floristic composition and species diversity of plant resources of rural area “Takht Bhai” district Mardan, Khyber Pakhtunkhwa, Pakistan. Medicinal and aromatic Plants (Los Angeles), 8(338), 2167-0412. Jones, G.D., & Bryant, V.M. (2007). A comparison of pollen counts: Light versus scanning electron microscopy. Grana, 46(1), 20-33. https://doi.org/10.1080/00173130601173897 Kaul, M.L. (2012). Male sterility in higher plants (Vol. 10). Springer Science & Business Media. Khan, H. U., Anjum, S. I., Sultana, N., & Khattak, B. (2016). Honey production potential of the honey bee (Apis mellifera) in Karak and Kohat, Pakistan. Journal of Entomology and Zoology Studies, 4(6), 559-564 Khan, I., Akhtar, N., & Khan, S. A. (2020). Palynological investigation of some selected species of family Fabaceae from Pakistan, using light and scanning electron microscopy techniques. Microscopy Research and Technique, 83(3), 223-231. https://doi.org/10.1002/jemt.23405 Khan, R. (2005). Studies on the pollen morphology of the genus Sisymbrium and monotypic genera Atelanthera and Arcyosperma (Brassicaceae) from Pakistan. Pakistan Journal of Botany, 37(1), 15-22. Laxmikant, B., & Devendra, M. (2017). Melittopalynological Investigation of Winter Honeys Collected From Apisdorsata Hives of Nagbhidtahsil of Chandrapur District of Maharashtra State (India). International Refereed Journal of Engineering and Science, 6(9), 36-44. Liu, F.L., Zhang, X.W., Chai, J.P., & Yang, D.R. (2006). Pollen phenolics and regulation of pollen foraging in honeybee colony. Behavioral ecology and sociobiology, 59(4), 582-588. https://doi.org/10.1007/s00265-005-0084-x Lortie, C.J., & Aarssen, L.W., 1999. The advantage of being tall: higher flowers receive more pollen in Verbascum thapsus L.(Scrophulariaceae). Ecoscience, 6(1), 68-71. https://doi.org/10.1080/11956860.1999.11952207 Majeed, S., Zafar, M., Ahmad, M., Kilic, O., Sultana, S., Raza, J., Yaseen, G., Gul, H., Mir, S. & Jabeen, M. (2020). Pollen morphological investigations of family Cactaceae and its taxonomic implication by light microscopy and scanning electron microscopy. Microscopy research and technique, 83(7), 767-777. https://doi.org/10.1002/jemt.23467 Mallick, P.K. (2020). Pollen Grains Morphology of Angiosperms. International Journal of Applied Sciences and Biotechnology, 8(2), 205-210. https://doi.org/10.3126/ijasbt.v8i2.28520 Mangi, J., Tahir, S.S., Tahir, M., & Rajput, M. (2018). Pollen Analysis of Natural Honey Collected from District Dadu, Sindh Pakistan. Sindh University Research Journal-SURJ (Science Series), 50(2), 327-334. Maw, K.H., Than, K.N. & Yee, N.N. (2020). Pollen Morphology of Some Ornamental Plants in Yadanabon University Campus, Mandalay. 3rd Myanmar Korea Conference Research Journal, 3(1), 203-210. Mesfin, T., Crawford, D. J., & Smith, E. B. (1995). Pollen morphology of North American Coreopsis (Compositae—Heliantheae). Grana, 34(1), 21-27. https://doi.org/10.1080/00173139509429029 Modro, A.F.H., Luz, C.F.P.D. & Meira Neto, J.A.A. (2007). Nutritional composition and quality of bee pollen collected in Minas Gerais, Brazil. Pesquisa Agropecuária Brasileira, 42(8), 1057-1065. https://doi.org/10.1590/S0100-204X2007000800001 Nascimento, A.S., Marchini, L.C., Carvalho, C.A.L., Araújo, D.F.D., & Silveira, T.A. (2015). Pollen spectrum of stingless bees honey (Hymenoptera: Apidae), Paraná State, Brazil. Journal of Entomology and Zoology Studies, 3(2), 290-296. Nazeri, J.V. (2008). Pollen morphology of the genus Malus (Rosaceae). Iranian Journal of Science And Technology Transaction A- Science, 32, 89-97. Nazish, M., Zafar, M., Ahmad, M., Sultana, S., Ullah, R., Alqahtani, A.S., Ullah, F., Ahmad, S., Ashfaq, S., & Ullah, F. (2019). Palyno-morphological investigations of halophytic taxa of Amaranthaceae through SEM from Salt range of Northern Punjab, Pakistan. Microscopy research and technique, 82(3), 304-316. https://doi.org/10.1002/jemt.23173 Noor, M. J., Ahmad, M., Zafar, M., & Ashraf, M.A. (2017). Palynological studies of melliferous and allergenic flora of Pakistan: A key to pollen and spore identification. Journal of Apicultural Research, 56(3), 300-309. https://doi.org/10.1080/00218839.2017.1306373 Noor, M.J. & Ahmad, M. (2021). Scanning electron imaging of mellitophilous and allergenic pollen grain of arid and northern irrigated agroecological zones of Pakistan. Microscopy Research and Technique, 1-28. https://doi.org/10.1002/jemt.23742 Pashayan, S.A. (2019). August. Ecological state of honey plants in apiaries of the Tyumen region. In: IOP Conference Series: Earth and Environmental Science, 315(7), 072001. IOP Publishing. doi:https://doi.org/10.1088/1755-1315/315/7/072001 Perveen, A., & Qaiser, M. (2005). Pollen flora of Pakistan-XLIV. Rhamnaceae. Pakistan Journal of Botany, 37(2), 195-202. Qureshi, M.N., Talha, N., Ahmad, M., Zafar, M. & Ashfaq, S. (2019). Morpho-palynological investigations of natural resources: A case study of Surghar mountain district Mianwali Punjab, Pakistan. Microscopy research and technique, 82(7), 1047-1056. https://doi.org/10.1002/jemt.23252 Rao, K.S., & Chinnappa, C.C. (1983). Pericolporate pollen in Gentianaceae. Canadian Journal of Botany , 61 (1), 174-178. Rasoloarijao, T.M., Ramavovololona, P., Ramamonjisoa, R., Clemencet, J., Lebreton, G. & Delatte, H. (2019). Pollen morphology of melliferous plants for Apis mellifera unicolor in the tropical rainforest of Ranomafana National Park, Madagascar. Palynology, 43(2), 292-320. https://doi.org/10.1080/01916122.2018.1443980 Rodríguez, Y.J.C., Vázquez-Sánchez, M., Cruz-Cárdenas, G. & Villaseñor, J.L. (2019). Use of ecological niche models of plant species to optimize placement of apiaries. Journal of Apicultural Science, 63(2), 243-265. https://doi.org/10.2478/jas-2019-0017 Saavedra-Carhuatacto, D.M., Aguinago-Castro, F., RojasIndrogo, C., & Delgado-Paredes, G.E. (2014). Analysis of pollen loads collected by honey bees (Apis mellifera L.) from Lambayeque Province (Peru): botanical origin and protein content. Journal of Global Biosciences, 3(1), 285-298. Saklani, S., & Mattu, V.K. (2020). Scanning Electron Microscopic Study on Pollens of 8 Bee Floral Resources from Kangra Hills, Himachal Pradesh, India. International Journal of Biotech Trends and Technology, 10(1), 67-71. Santos, A., Nascimento, A., Santos, J., Silva, S., Lucas, C., & Carvalho, C. (2019). Pollen spectrum of the honey of Apis mellifera L. collected in the period of honey production. Scientific Electronic Archives, 12(6), 69-76. https://doi.org/10.36560/1262019893 Seijo, M. C., Escuredo, O., & Rodríguez-Flores, M. S. (2019). Physicochemical properties and pollen profile of Oak honeydew and Evergreen Oak honeydew honeys from Spain: A comparative study. Foods, 8(4), 126. https://doi.org/10.3390/foods8040126 Sekina, M.A., & Moore, P.D. (1995). Morphological studies of the pollen grains of the semi-arid region of Egypt. Flora, 190(2), 115-133. https://doi.org/10.1016/S0367-2530(17)30641-2 Shaheen, F.A., Khan, K.A., Husain, M., Mahmood, R., & Rafique, M.K. (2017). Role of honey bees (Apis mellifera L.) foraging activities in increased fruit setting and production of apples (Malus domestica). Pakistan Journal of Agricultural Research, 30(1), 29-34. Shrestha, K. K., Paudyal, K. N., & Ferguson, D. K. (2005). Pollen Morphology of Himalayan Viola (Violaceae). Nepal Journal of Science and Technology, 6(1). Shubharani, R., Roopa, P. & Sivaram, V. (2013). Pollen morphology of selected bee forage plants. Global Journal of Bio-Science and Biotechnology, 2(1), pp.82-90. Siede, R., Eickhoff, B., Freyer, C., Windpassinger, S., & Büchler, R. (2021). The bioenergy crop Sorghum bicolor is a relevant pollen source for honey bees (Apis mellifera). GCB Bioenergy, 13(7), 1149-1161. https://doi.org/10.1111/gcbb.12835 Singh, M., & Mall, P. (2017). Palynological studies of pollen grains of some apiculture importance bee flora in Tarai region of Uttarakhand. Journal of Pharmacognosy and Phytochemistry, 6(6), 352-356. Sufyan, M., Badshah, I., Ahmad, M., Zafar, M., Bahadur, S., & Rashid, N. (2018). Identification of medicinally used Flora using pollen features imaged in the scanning electron microscopy in the lower Margalla Hills Islamabad Pakistan. Microscopy and Microanalysis, 24(3), 292-299. https://doi.org/10.1017/S1431927618000326 Sunita, S., Jamwal, R. & Mattu, V.K. (2018). Scanning Electron Microscopic study on pollens of eight bee floral resources from Hamirpur hills, Himachal Pradesh, India. Journal of Experimental Biology and Agricultural Sciences, 6(6), 1004-1009. DOI: https://doi.org/10.18006/2018.6(6).1004.1009 Tiwari, P., Tiwari, J.K., & Ballabha, R. (2010). Studies on sources of bee-forage for rock bee (Apis dorsata F.) from Garhwal Himalaya, India: a melisso-palynologaical approach. Nature and Science, 8(6), 5-15. Ullah, F., Zafar, M., Ahmad, M., Dilbar, S., Shah, S. N., Sohail, A., Zaman, W., Iqbal, M., Bahadur, S., & Tariq, A. (2018). Pollen morphology of subfamily Caryophylloideae (Caryophyllaceae) and its taxonomic significance. Microscopy Research and Technique, 81(7), 704-715. https://doi.org/10.1002/jemt.23026 Ullah, S.A., Zafar, M., Ahmad, M., Ghufran, M.A., Bursal, E., Kilic, O., Sultana, S., Yaseen, G., Khan, S. & Majeed, S. (2021). Microscopic implication and evaluation of herbaceous melliferous plants of southern Khyber Pakhtunkhwa-Pakistan using light and scanning electron microscope. Microscopy Research and Technique, 1-15. https://doi.org/10.1002/jemt.23732 Waykar, B., & Baviskar, R.K. (2015). Diversity of bee foraging flora and floral calendar of Paithan taluka of Aurangabad district (Maharashtra), India. Journal of Applied Horticulture, 17(2), 155-159. Wen, H.Z., & Wang, R.J. (2012). Ligustrum guangdongense (Oleaceae), a New Species from China. Novon: A Journal for Botanical Nomenclature, 22(1), 114-117. https://doi.org/10.3417/2010104 Yang, S., Yuan, Z., Yin, Y., Zhao, X., Feng, L., Han, L., & Zhu, F. (2015). Pollen morphology of pomegranate (Punica granatum L.) from different eco-geographical populations in China. Acta Horticulturae, (1089), 269-277. https://doi.org/10.17660/ActaHortic.2015.1089.35 Zoratti, M.L, Barbattini, R., & Frill, F. (1995). Bee flora in the Codroipo area (Italy). L'ape Nostra Amica, 17(4), 5- 14.