Pollen source variation between agricultural areas and forest edges: a case study of the red dwarf honeybee (Apis florea Fabricius) in the Rarh region, West Bengal, India

Document Type : Paper, English

Authors

1 Department of Botany & Forestry, Vidyasagar University, Midnapore-721102, India

2 Department of Botany, Rampurhat College, Rampurhat-731224, India

3 Department of Botany & Forestry, Vidyasagar University, Midnapore, India

10.22034/jesi.46.3.2

Abstract

Conserving native honeybees is vital for ecosystem stability and food security, yet the impact of changing landscapes on the pollen foraging of the red dwarf honeybee (Apis florea) remains poorly understood. The study investigated how landscape variation influences pollen foraging by Apis florea in West Bengal, examining its pollen resources and collection patterns across agricultural areas and forest edges. We conducted palynological analyses of corbicular pollen loads. The honeybee species exhibited floral constancy and polylecty, collecting a wide variety of pollen types (57 in total). The composition and predominant pollen sources varied between the two landscapes. In agricultural areas, predominant pollen sources were Coriandrum sativum, Cucumis sativus, Cucurbita maxima, Luffa aegyptiaca, and Rhamphospermum nigrum. In contrast, at forest edges, several tree species such as Acacia auriculiformis, Eucalyptus tereticornis, and Terminalia arjuna were dominant, along with some crop species, including Coriandrum sativum and Rhamphospermum nigrum. However, the monthly number and diversity of pollen types did not differ significantly between the two landscapes. Based on diverse characteristics of bee-visited flowers, the honeybee species was considered a generalist forager. In conclusion, the red dwarf honeybee was adapted to diverse habitats. Agricultural land use influenced the botanical composition of pollen collected by honeybees, but did not appear to restrict overall pollen flow to colonies.

Graphical Abstract

Pollen source variation between agricultural areas and forest edges: a case study of the red dwarf honeybee (Apis florea Fabricius) in the Rarh region, West Bengal, India

Keywords

Main Subjects


Article Title [Persian]

تنوع منابع گرده در مناطق کشاورزی و حاشیه جنگل‌ها: مطالعه موردی زنبور عسل کوتوله قرمز (Apis florea Fabricius) در منطقه رار بنگال غربی، هند

Authors [Persian]

  • سومان دی 1
  • اوجوال لیک 2
  • پراکاش کارامکار 3
1 گروه گیاه‌شناسی و جنگل‌داری، دانشگاه ویدیاساگار، میدناپور-۷۲۱۰۲، هند
2 گروه گیاه‌شناسی، دانشکده سالدیها، سالدیها-۷۲۲۱۷۳، هند
3 گروه گیاه‌شناسی، دانشکده رامپورها‌ت، رامپورها‌ت-۷۳۱۲۲۴، هند
Abstract [Persian]

حفاظت از جمعیت زنبورهای عسل بومی، نقشی حیاتی در پایداری اکوسیستم و امنیت غذایی دارد، با این حال اثر تغییرات چشم‌اندازهای طبیعی بر رفتار گرده‌جویی زنبور عسل کوتوله‌ی قرمز (Apis florea) هنوز به‌خوبی شناخته نشده است. این پژوهش، نشان داد که چگونه تفاوت بین چشم‌اندازهای طبیعی روی گرده‌جویی این گونه در بنگال غربی تأثیر می‌گذارد. تحقیق با هدف مطالعه منابع گرده و الگوهای جمع‌آوری آن در مناطق کشاورزی و حاشیه‌های جنگلی طراحی شد. برای این منظور، ارزیابی گرده‌شناسی بر روی بارهای گرده ی جمع‌آوری‌شده در سبد گرده‌ی پاهای زنبور انجام شد. این گونه زنبور عسل، پایداری گل‌گزینی و رفتار چندگل‌پسندی (Polylecty) از خود نشان داد و طیف گسترده‌ای از انواع گرده‌ها (در مجموع ۵۷ نوع) را جمع‌آوری کرد. ترکیب و منابع غالب گرده میان دو نوع چشم‌انداز متفاوت بود. در مناطق کشاورزی، منابع اصلی گرده شامل: گشنیز (Coriandrum sativum)، خیار (Cucumis sativus)، کدو تنبل (Cucurbita maxima)، لوفا یا کدوی اسفنجی (Luffa aegyptiaca) و خردل سیاه (Rhamphospermum nigrum) بودند. در مقابل، در حاشیه‌های جنگلی چندین گونه درختی مانند: آکاسیا (Acacia auriculiformis)، اوکالیپتوس (Eucalyptus tereticornis) و ارجونا (Terminalia arjuna) به همراه برخی گیاهان زراعی مانند گشنیز و خردل سیاه، منابع غالب گرده محسوب می‌شدند. با این حال، تعداد گرده ها (در طول ماه) و تنوع انواع گرده‌ها بین دو چشم‌انداز، تفاوت معنی‌داری نشان نداد. بر اساس ویژگی‌های متنوع گل‌هایی که زنبورها از آن‌ها بازدید می‌کردند، این گونه زنبور عسل به‌عنوان یک گرده‌جوی عمومی (Generalist forager) در نظر گرفته شد. در نتیجه، زنبور عسل کوتوله‌ی قرمز یک گرده‌جوی عمومی است که توانایی سازگاری با زیستگاه‌های متنوع را دارد. توسعه کشاورزی بر ترکیب گیاهی گرده‌های جمع‌آوری‌شده توسط زنبورها تأثیر می‌گذارد، اما به نظر می‌رسد که روی جریان کلی گرده به سوی کلنی‌ها، تاثیری نمیگذارد.

Keywords [Persian]

  • generalist forager
  • floral constancy
  • pollen load
  • pollen type
  • polylectic forager

© 2026 by Author(s), Published by the Entomological Society of Iran

This Work is Licensed under Creative Commons Attribution-Non-Commercial 4.0 International Public License.

Abrol, D. P. (2010) Foraging behaviour of Apis florea F., an important pollinator of Allium cepa L. Journal of Apicultural Research 49(4), 318–325. https://doi.org/10.3896/IBRA.1.49.4.04.
Aguiar, C. M. L., Santos, G. M., Martins, C. F. & Presley, S. J. (2013) Trophic niche breadth and niche overlap in a guild of flower-visiting bees in a Brazilian dry forest. Apidologie 44, 153–162. https://doi.org/10.1007/s13592-012-0167-4.
Alshallash, K. S., Abolaban, G., Elhamamsy, S. M., Zaghlool, A., Nasr, A., Nagib, A., et al. (2023) Bee pollen as a functional product–chemical constituents and nutritional properties. Journal of Ecological Engineering 24(2), 173–183. https://doi.org/10.12911/22998993/156611.
Alves, R. F., Santos, F. A. R. (2017) Arecaceae potential for production of monofloral bee pollen. Grana 56(4), 294–303. https://doi.org/10.1080/00173134.2016.1239760.
Andrada, A. C. & Tellería, M. C. (2005) Pollen collected by honey bees (Apis mellifera L.) from south of Caldén district (Argentina): botanical origin and protein content. Grana 44(2), 115–122. https://doi.org/10.1080/00173130510010459.
Barth, O. M., Freitas, A. S., Oliveira, É. S., Silva, R. A., Maester, F. M., Andrella, R. R. & Cardozo, G. M. (2010) Evaluation of the botanical origin of commercial dry bee pollen load batches using pollen analysis: a proposal for technical standardization. Anais da Academia Brasileira de Ciências, 82(4), 893–902. https://doi.org/10.1590/S0001-37652010000400011.
Brosi, B. J., Armsworth, P. R. & Daily, G. C. (2008) Optimal design of agricultural landscapes for pollination services. Conservation Letters 1, 27–36. https://doi.org/10.1111%2Fj.1755-263X.2008.00004.x.
Campos, M. G., Bogdanov, S., de Almeida-Muradian, L. B., Szczesna, T., Mancebo, Y., Frigerio, C. & Ferreira, F. (2008) Pollen composition and standardisation of analytical methods. Journal of Apicultural Research 47(2), 154–161. https://doi.org/10.1080/00218839.2021.1948240.
Carroll, M. J., Brown, N., Goodall, C., Downs, A. M., Sheenan, T. H. & Anderson, K. E. (2017) Honey bees preferentially consume freshly-stored pollen. PloS One 12(4), e0175933. https://doi.org/10.1371/journal.pone.0249458.
Dafni, A. (1992) Pollination Ecology- A Practical Approach. Oxford University Press, USA.
Danner, N., Molitor, A. M., Schiele, S., Härtel, S. & Steffan‐Dewenter, I. (2016) Season and landscape composition affect pollen foraging distances and habitat use of honey bees. Ecological Applications 26(6), 1920–1929. https://doi.org/10.1890/15-1840.1.
El Shafie, H. A. F., Mogga, J. B. B. & Basedow, T. H. (2002) Studies on the possible competition for pollen between the honey bee, Apis mellifera sudanensis, and the imported dwarf honey bee Apis florea (Hym., Apidae) in North‐Khartoum (Sudan). Journal of Applied Entomology 126(10), 557–562. https://doi.org/10.1046/j.1439-0418.2002.00711.x.
Erdtman, E. (1960) The acetolysis method: A revised description. Svensk Botanisk Tidskrift 54, 561–564.
Garibaldi, L. A., Steffan-Dewenter, I., Kremen, C., Morales, J. M., Bommarco, R., Cunningham, S. A., et al. (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecology Letters 14(10), 1062–1072. https://doi.org/10.1111/j.1461-0248.2011.01669.x.
Gupta, D. K., Shukla, A. K., Mohamed, M. N. & Jangid, B. L. (2020) Influence of annual ornamental flowers (Asteraceae) Joseph on the relative abundance of honey bee species in the hot semi-arid environment. Annals of Arid Zone 59, 1–7. https://doi.org/10.56093/aaz.v59i1%20&%202.103046.
Grüter, C., Moore, H., Firmin, N., Helanterä, H. & Ratnieks, F. L. (2011) Flower constancy in honey bee workers (Apis mellifera) depends on ecologically realistic rewards. Journal of Experimental Biology 214(8), 1397–1402. https://doi.org/10.1242/jeb.050583.
Joosten, H. & De Klerk, P. (2002) What’s in a name? Some thoughts on pollen classification, identification, and nomenclature in Quaternary palynology. Review of Palaeobotany and Palynology 122, 29–45. https://doi.org/10.1016/S0034-6667(02)00090-8.
Joseph, J., Santibáñez, F., Laguna, M. F., Abramson, G., Kuperman, M. N. & Garibaldi, L. A. (2020) A spatially extended model to assess the role of landscape structure on the pollination service of Apis mellifera. Ecological Modelling 431, 109201. https://doi.org/10.1016/j.ecolmodel.2020.109201.
Kalpana, T. P., Fatima, K. & Ramanujam, C. G. K. (1990) Pollen analysis of Apis cerana and Apis florea honeys from Adikmet area, Hyderabad. Proceedings of the Indian Academy of Sciences 100(3), 183–193. https://doi.org/10.1007/BF03053448.
Kaluza, B. F., Wallace, H., Keller, A., Heard, T. A., Jeffers, B., Drescher, N., et al. (2017) Generalist social bees maximize diversity intake in plant species‐rich and resource‐abundant environments. Ecosphere 8(3), e01758. https://doi.org/10.1002/ecs2.1758.
Lan, J., Ding, G., Ma, W., Jiang, Y. & Huang, J. (2021) Pollen source affects development and behavioral preferences in honey bees. Insects 12(2), 130. https://doi.org/10.3390/insects12020130.
Laxmikant, B. & Devendra, M. (2014) Summer pollen sources to Apis dorsata honeybees collected from Bramhapuri forest area of Chandrapur district of Maharashtra state (India). International Journal of Life Sciences 2, 160–164.
Layek, U., Bhakat, R. K., & Karmakar P. (2015a) Foraging behaviour of Apis florea Fabricius during winter and spring-summer in Bankura and Paschim Medinipur districts, West Bengal. Global Journal of Bio-Science and Biotechnology 4, 255–263.
Layek, U., Bhakat, R. K., & Karmakar, P. (2026) Foraging niche overlap among exotic honeybees (Apis mellifera) and native honeybees (Apis cerana, Apis dorsata and Apis florea), considering pollen sources in the Rarh regions of West Bengal, India. Ecologies 7(1), 15. https://doi.org/10.3390/ecologies7010015.
Layek, U., Bisui, S., Mondal, R., Das, N., De, S. K. & Karmakar, P. (2021) Floral traits and chemical cues associated with rock bee (Apis dorsata Fabricius) for the host selection in West Bengal, India. Grana 60(4), 310–323. https://doi.org/10.1080/00173134.2020.1823466.
Layek, U., Das, N., Mondal, R. & Karmakar, P. (2023) Distribution, nesting biology, and floral preference of giant honeybee (Apis dorsata Fabricius) in Southern West Bengal, India. In: Role of giant honeybees in natural and agricultural systems, Abrol, D.P. (Ed.), CRC Press, Boca Raton, USA, pp. 305–323. https://doi.org/10.1201/9781003294078-21.
Layek. U. & Karmakar, P. (2020) Distribution, Nesting biology, and floral resources of red dwarf honey bee (Apis florea Fabricius) in West Bengal, India. In: The future role of dwarf honeybees in natural and agricultural systems, Abrol, D.P. (Ed.), CRC Press, Boca Raton, USA, pp. 301–309. https://doi.org/10.1201/9781003033936-23.
Layek, U., Karmakar, P. & Pal, P. K. (2015b) Significance of Trianthema portulacastrum L. in sustenance of Apis florea colonies during dearth period. International Journal of Biosciences 7(1), 22–29. http://dx.doi.org/10.12692/ijb/7.1.22-29.
Layek, U., Kundu, A., Chatterjee, P. & Karmakar, P. (2025) Pollen collecting behaviour of stingless bees (Tetragonula iridipennis Smith) on corn (Zea mays L.): an important pollen source. Grana 64(1), 44–56. https://doi.org/10.1080/00173134.2025.2490484.
Layek, U., Manna, S. S. & Karmakar, P. (2020) Pollen foraging behaviour of honey bee (Apis mellifera L.) in southern West Bengal, India. Palynology 44(1): 114–126. https://doi.org/10.1080/01916122.2018.1533898.
Layek, U., Nandi, T. & Karmakar, P. (2016) Pollen forage and storage pattern of Apis dorsata Fabricius in Bankura and Paschim Medinipur districts, West Bengal. International Journal of Pure and Applied Bioscience 4(5), 59–71. https://doi.org/10.18782/2320-7051.2384.
Liolios, V., Tananaki, C., Dimou, M., Kanelis, D., Goras, G., Karazafiris, E. & Thrasyvoulou, A. (2015) Ranking pollen from bee plants according to their protein contribution to honey bees. Journal of Apicultural Research 54(5), 582–592. https://doi.org/10.1080/00218839.2016.1173353
Mărgăoan, R. & Cornea-Cipcigan, M. (2024) Carotenoids and vitamins of pollen. In: Pollen chemistry & biotechnology, Ecem Bayram, N., Ž. Kostic, A., Can Gercek, Y. (Eds.), Springer International Publishing, Cham, Switzerland, pp. 147–177. https://doi.org/10.1007/978-3-031-47563-4_8.
Melin, A., Rouget, M., Colville, J. F., Midgley, J. J. & Donaldson, J. S. (2018) Assessing the role of dispe/rsed floral resources for managed bees in providing supporting ecosystem services for crop pollination. PeerJ 6, e5654. https://doi.org/10.7717/peerj.5654.
Mondal, R., Das, N., Layek, U., De, S. K. & Karmakar, P. (2023) Pollen sources of Asian honeybee (Apis cerana Fabricius) in Paschim Medinipur district of West Bengal, India. Grana 62(5-6), 369–381. https://doi.org/10.1080/00173134.2023.2263452.
Moreira, E. F., Boscolo, D. & Viana, B. F. (2015) Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PloS One 10(4), e0123628. https://doi.org/10.1371/journal.pone.0123628.
Nates-Parra, G. & Rodríguez, Á. (2011) Forrajeo en colonias de Melipona eburnea (Hymenoptera: Apidae) en el piedemonte llanero (Meta, Colombia). Revista Colombiana de Entomología 37(1): 121–127.
Novais, J. S. D., Absy, M. L. & Santos, F. A. R. (2013) Pollen grains in honeys produced by Tetragonisca angustula (Latreille, 1811) (Hymenoptera: Apidae) in tropical semi-arid areas of north-eastern Brazil. Arthropod-Plant Interactions 7(6), 619–632. https://doi.org/10.1007/s11829-013-9276-x.
Obregon, D. & Nates-Parra, G. (2014) Floral preference of Melipona eburnea Friese (Hymenoptera: Apidae) in a Colombian Andean region. Neotropical Entomology 43(1), 53–60. https://doi.org/10.1007/s13744-013-0172-y
Pang, C., Dong, K., Guo, Y., Ding, G., Lu, Y., Guo, Z., et al. (2022) Effects of three types of pollen on the growth and development of honey bee larvae (Hymenoptera, Apidae). Frontiers in Ecology and Evolution 10, 870081. https://doi.org/10.3389/fevo.2022.870081
Pernal, S. F. & Currie, R. W. (2001) The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.). Behavioral Ecology and Sociobiology 51: 53–68. https://doi.org/10.1007/s002650100412
Pielou, E. C. (1977) Mathematical Ecology (2nd edition). New York: Willey-Interscience Publishing, John Wiley & Sons.
Raj, D., Rana, V. K. &, Devi, N. (1993) Comparative studies on pollen loads and pollen constancy of Apis mellifera L. and Apis cerana indica F. on rapeseed. Journal of Entomological Research 17, 43–43.
Requier, F., Odoux, J. F., Henry, M. & Bretagnolle, V. (2017) The carry‐over effects of pollen shortage decrease the survival of honeybee colonies in farmlands. Journal of Applied Ecology 54(4), 1161–1170. https://doi.org/10.1111/1365-2664.12836.
Rzepecka-Stojko, A., Stojko, J., Kurek-Górecka, A., Górecki, M., Kabała-Dzik, A., Kubina, R., Moździerz, A., & Buszman, E. (2015). Polyphenols from Bee Pollen: Structure, absorption, metabolism and biological activity. Molecules, 20(12), 21732–21749. https://doi.org/10.3390/molecules201219800
Shannon, C. E. & Weaver, W. (1949) The mathematical theory of communication. Urbano: University of Illinois Press.
Sosa-Nájera, M. S., Martínez-Hernández, E., del Socorro Lozano-García, M. & Cuadriello-Aguilar, J. I. (1994) Nectaropolliniferous sources used by Trigona (Tetragonisca) angustula in Chiapas, southern México. Grana 33(4-5), 225–230. https://doi.org/10.1080/00173139409429003.
Steffan-Dewenter, I. & Kuhn, A. (2003) Honeybee foraging in differentially structured landscapes. Proceedings of the Royal Society of London. Series B: Biological Sciences 270(1515), 569–575. https://doi.org/10.1098/rspb.2002.2292.
Suwannapong, G., Maksong, S., Yemor, T., Junsuri, N. & Benbow, M. E. (2013) Three species of native Thai honey bees exploit overlapping pollen resources: identification of bee flora from pollen loads and midguts from Apis cerana, A. dorsata and A. florea. Journal of Apicultural Research 52(5), 196–201. https://doi.org/10.3896/IBRA.1.52.5.05.
Van der Sluijs, J. P. & Vaage, N. S. (2016) Pollinators and global food security: the need for holistic global stewardship. Food Ethics 1(1), 75–91. https://doi.org/10.1007/s41055-016-0003-z.
Vossler, F. G. (2012) Flower visits, nesting and nest defence behaviour of stingless bees (Apidae: Meliponini): suitability of the bee species for meliponiculture in the Argentinean Chaco region. Apidologie 43(2), 139–161. https://doi.org/10.1007/s13592-011-0097-6.
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