Pollen foraging preference based on floral resource distance in Tetragonula biroi
Article Sidebar
Abstract Views: 373
File Views: 10
Main Article Content
Abstract
Abstract. Nuraeni S, Tiwi AA, Prastiyo A. 2025. Pollen foraging preference based on floral resource distance in Tetragonula biroi. Asian J Agric 9: 423-432. The stingless bee Tetragonula biroi plays a vital role as a pollinator and depends primarily on pollen and nectar for nutrition. Understanding its foraging behavior is essential for optimizing floral resource management in meliponiculture systems. This study investigates the foraging preferences of T. biroi based on the distance of floral resources in Awani Bee Garden, Makassar, South Sulawesi, Indonesia. Pollen identification was conducted using light microscopy on bee bread samples collected from three hives, and the spatial distribution of flowering plants around the hives was documented. This research was conducted from November 2023 to February 2025, using descriptive analysis of pollen types and plant distance from the hive. A Spearman’s correlation analysis was also conducted to examine the relationship between the distance of floral sources and the percentage of pollen collected. Foraging preference was operationally defined as the percentage of pollen collected from each plant species relative to its distance from the hive. Results revealed that T. biroi collected pollen from 18 plant species located at distances ranging from 2 to 498 m. The most dominant pollen sources were Clerodendrum paniculatum (16.87%), Macaranga tanarius (15.20%), and Carica papaya (13.97%). Over 70% of the total pollen came from plant species located within 10 m of the hive, such as Capsicum annuum (2 m, 6.93%), Mangifera indica (2 m, 7.49%). However, the bees also utilized distant sources such as Turnera subulata (485 m, 0.56%) and Antigonon leptopus (498 m, 2.12%), demonstrating flexible foraging behavior within their ecological range. Spearman's correlation showed a weak negative relationship between plant distance and pollen percentage (? = -0.387) with p>0.05, indicating that the preference for nearby floral sources was not statistically significant but ecologically observable. These findings suggest that while proximity plays a role in foraging, T. biroi exhibits adaptable behavior based on resource distribution.
Article Details
Issue
Section
How to Cite
References
Adgaba N, Al-Ghamdi A, Tadesse Y, Getachew A, Awad AM, Ansari MJ, Owayss AA, Mohammed SEA, Alqarni AS. 2017. Nectar secretion dynamics and honey production potentials of some major honey plants in Saudi Arabia. Saudi J Biol Sci 24 (1): 180-191. DOI: 10.1016/j.sjbs.2016.05.002.
Agussalim A, Agus A, Umami N, Budisatria IGS. 2017. Variation of honey bees forages as source of nectar and pollen based on altitude in Yogyakarta. Bull Anim Sci 41 (4): 448-460. DOI: 10.21059/buletinpeternak.v41i4.13593.
Anderson KE, Mott BM. 2023. Ecology of pollen storage in honey bees: Sugar tolerant yeast and the aerobic social microbiota. Insects 14 (3): 265. DOI: 10.3390/insects14030265.
Bänsch S, Tscharntke T, Ratnieks FL, Härtel S, Westphal C. 2020. Foraging of honey bees in agricultural landscapes with changing patterns of flower resources. Agric Ecosyst Environ 291: 106792. DOI: 10.1016/j.agee.2019.106792.
Beckwith BR, Johansson EM, Huff VJ. 2022. Connecting people, plants and place: A native plant society's journey towards a community of practice. People Nat 4 (6): 1414-1425. DOI: 10.1002/pan3.10368.
Begna T, Ulziibayar D, Noor-ul-Ane M, Shin JH, Jung C. 2020. Offering pollen as reward enhances foraging activity of honey bee, Apis mellifera on strawberry greenhouse during winter season. J Apic 35 (2): 111-118. DOI: 10.17519/apiculture.2020.06.35.2.111.
Breda LS, de Melo Nascimento JE, de Toledo VDAA, de Lima VA, Felsner ML. 2024. Characterizing the use of botanical resources from pollen loads from Apis mellifera, and stingless bees’ pot-pollen palynology: An approach using network analysis and generalized linear models. Sociobiology 71: e8800. DOI: 10.13102/sociobiology.v71i2.8800.
Budiaman B, Rahman AF, Nurhayati N, Jumadi NH, Khatima K, Prastiyo A. 2025. Analysis of productivity from four stingless bees (Apidae: Meliponini) and forages in urban forest, South Sulawesi, Indonesia. Asian J For 9: 144-151. DOI: 10.13057/asianjfor/r090115.
Conchou L, Lucas P, Meslin C, Proffit M, Staudt M, Renou M. 2019. Insect odorscapes: From plant volatiles to natural olfactory scenes. Front Physiol 10: 972. DOI: 10.3389/fphys.2019.00972.
Crone MK, Biddinger DJ, Grozinger CM. 2022. Wild bee nutritional ecology: Integrative strategies to assess foraging preferences and nutritional requirements. Front Sustain Food Syst 6: 847003. DOI: 10.3389/fsufs.2022.847003.
Delgado T, Leal LC, El Ottra JHL, Brito VLG, Nogueira A. 2023. Flower size affects bee species visitation pattern on flowers with poricidal anthers across pollination studies. Flora 299: 152198. DOI: 10.1016/j.flora.2022.152198.
Erdtman G. 1953. Pollen Morphology and Plant Taxonomy: Angiosperms (An Introduction to Palynology). Brill, Leiden.
Farfan SJA, Celentano D, Silva Junior CHL, de Freitas Silveira MV, Serra RTA, Gutierrez JAM, Barros HC, Ribeiro MHM, Barth OM, Alves RMO, García LMH, Rousseau GX. 2023. The effect of landscape composition on stingless bee (Melipona fasciculata) honey productivity in a wetland ecosystem of Eastern Amazon, Brazil. J Apic Res 62 (5): 1102-1114. DOI: 00218839.2022.2137307.
Forster CY, Middleton EJT, Gloag R, Hochuli DF, White TE, Latty T. 2023. Impact of empty flowers on foraging choice and movement within floral patches by the honey bee, Apis mellifera. Insectes Sociaux 70 (4): 413-422. DOI: 10.1007/s00040-023-00934-3.
Fowler RE, Rotheray EL, Goulson D. 2016. Floral abundance and resource quality influence pollinator choice. Insect Conserv Divers 9 (6): 481-494. DOI: 10.1111/icad.12197.
Giuliani C, Giovanetti M, Lupi D, Mesiano MP, Barilli R, Ascrizzi R, Flamini G, Fico G. 2020. Tools to tie: Flower characteristics, VOC emission profile, and glandular trichomes of two Mexican Salvia species to attract bees. Plants 9: 1645. DOI: 10.3390/plants9121645.
Gresty CE, Clare E, Devey DS, Cowan RS, Csiba L, Malakasi P, Lewis OT, Willis KJ. 2018. Flower preferences and pollen transport networks for cavity?nesting solitary bees: Implications for the design of agri?environment schemes. Ecol Evol 8 (15): 7574-7587. DOI: 10.1002/ece3.4234.
Gruter C, Segers FH, Hayes L. 2024. Extensive loss of forage diversity in social bees owing to flower constancy in simulated environments. Proc R Soc B: Biol Sci 291: 20241036. DOI: 10.1098/rspb.2024.1036.
Hrncir M, Maia-Silva C, da Silva Teixeira-Souza VH, Imperatriz-Fonseca VL. 2019. Stingless bees and their adaptations to extreme environments. J Comp Physiol A 205: 415-426. DOI: 10.1007/s00359-019-01327-3.
Jayadi LZ, Susandarini R. 2020. Melissopalynological analysis of honey produced by two species of stingless bees in Lombok Island, Indonesia. Nusantara Biosci 12: 97-108. DOI: 10.13057/nusbiosci/n120203.
Kaehler TG, Halinski R, Contrera FA, Silveira A, Blochtein B. 2024. Flight distance and foraging of Tetragonisca fiebrigi (Apidae: Meliponini) in response to different concentrations of sugar in food resources and abiotic factors. J Apic Res 63 (3): 387-399. DOI: 10.1080/00218839.2021.2005872.
Koethe S, Fischbach V, Banysch S, Reinartz L, Hrncir M, Lunau K. 2020. A comparative study of food source selection in stingless bees and honeybees: Scent marks, location, or color. Front Plant Sci 11: 516. DOI: 10.3389/fpls.2020.00516.
Kumar A, Malik S, Chaudhary P, Kumar N. 2017. Studies on the growth and flowering of different mango (Mangifera indica L.) cultivars under Western Uttar Pradesh conditions. J Pharmacogn Phytochem 6 (6): 439-442.
Layek U, Bisui S, Karmakar P. 2024. Flight range and resource loading-unloading behavior of stingless bee Tetragonula iridipennis (Smith). J Apic Res 63 (3): 400-411. DOI: 10.1080/00218839.2021.1994259.
Lemanski NJ, Williams NM, Winfree R. 2022. Greater bee diversity is needed to maintain crop pollination over time. Nature Ecol Evol 6 (10): 1516-1523. DOI: 10.1038/s41559-022-01847-3.
Lichtenberg EM, Mendenhall CD, Brosi B. 2017. Foraging traits modulate stingless bee community disassembly under forest loss. J Anim Ecol 86 (6): 1404-1416. DOI: 10.1111/1365-2656.12747.
Louveaux J, Maurizio A, Vorwohl G. 1978. Methods of melissopalynology. Bee World 59: 139-157. DOI: 10.1080/0005772X.1978.11097714.
Machado T, Viana BF, da Silva CI, Boscolo D. 2020. How landscape composition affects pollen collection by stingless bees? Landsc Ecol 35 (3): 747-759. DOI: 10.1007/s10980-020-00977-y.
Maia-Silva C, Hrncir M, Giannini TC, Toledo-Hernández M, Imperatriz-Fonseca VL. 2024. Small Amazonian stingless bees: An opportunity for targeted cocoa pollination. Front Bee Sci 2: 1357811. DOI: 10.3389/frbee.2024.1357811.
Maia-Silva C, Limão AAC, Silva CI, Imperatriz-Fonseca VL, Hrncir M. 2020. Stingless bees (Melipona subnitida) overcome severe drought events in the Brazilian tropical dry forest by opting for high-profit food sources. Neotrop Entomol 49 (4): 595-603. DOI: 10.1007/s13744-019-00756-8.
Marazzi B, Gonzalez AM, Delgado-Salinas A, Luckow MA, Ringelberg JJ, Hughes CE. 2019. Extrafloral nectaries in Leguminosae: Phylogenetic distribution, morphological diversity and evolution. Aust Syst Bot 32 (6): 409-458. DOI: 10.1071/SB19012.
M?rg?oan R, Stran? M, Varadi A, Topal E, Yücel B, Cornea-Cipcigan M, Campos MG, Vodnar DC. 2019. Bee collected pollen and bee bread: Bioactive constituents and health benefits. Antioxidants 8 (12): 568. DOI: 10.3390/antiox8120568.
Mohammad SM, Mahmud-Ab-Rashid NK, Zawawi N. 2021. Stingless bee-collected pollen (bee bread): Chemical and microbiology properties and health benefits. Molecules 26 (4): 957. DOI: 10.3390/molecules26040957.
Nagamitsu T, Inoue T. 2005. Floral resource utilization by stingless bees (Apidae, Meliponini). In: Roubik DW, Sakai S, Karim AAH (eds). Pollination Ecology and the Rain Forest Sarawak Studies. Springer, New York. DOI: 10.1007/0-387-27161-9_7.
Newis R, Nichols J, Farrar MB, Fuller C, Hosseini Bai S, Wilson RS, Wallace HM. 2023. Stingless bee (Tetragonula carbonaria) foragers prioritise resin and reduce pollen foraging after hive splitting. Apidologie 54 (4): 1-13. DOI: 10.1007/s13592-023-01018-8.
Newman RJS, Marchant R, Enns C, Capitani C. 2021. Assessing the impacts of land use and climate interactions on beekeeping livelihoods in the Taita Hills, Kenya. Dev Pract 31 (4): 446-461. DOI: 10.1080/09614524.2020.1854689.
Nuraeni S, Mahmudah R, Sadapotto A. 2024. Identify the source of pollen feed in honey and bee bread of Tetragonula biroi. IOP Conf Ser Earth Environ Sci 1315: 012064. DOI: 10.1088/1755-1315/1315/1/012064.
Nurnberger F, Härtel S, Steffan-Dewenter I. 2019. Seasonal timing in honey bee colonies: Phenology shifts affect honey stores and varroa infestation levels. Oecologia 189: 1121-1131. DOI: 10.1007/s00442-019-04377-1.
Pardee GL, Ballare KM, Neff JL, Do LQ, Ojeda D, Bienenstock EJ, Brosi BJ, Grubesic TH, Miller JA, Tong D, Jha S. 2023. Local and landscape factors influence plant-pollinator networks and bee foraging behavior across an urban corridor. Land 12: 362. DOI: 10.3390/land12020362.
Paul P, Chowdhury M. 2020. Pollen of selected Indian species from subfamily Polygonoideae (Polygonaceae). Biologia 75: 1083-1095. DOI: 10.2478/s11756-020-00449-3.
Pereira DC, Monkolski A, Tenutti E, de Oliveira G, de Souza-Franco GM. 2025. Stingless bees and urban spaces: An investigation of the conditions for adaptation to city buildings and landscaping. Rev Ibero-Am Humanid Cienc Educ 11 (1): 1196-1221. DOI: 10.51891/rease.v11i1.17882.
Poorter L, van Der Sande MT, Amissah L, Bongers F, Hordijk I, Kok J, Laurance SGW, Martínez-Ramos M, Matsuo T, Meave JA, Muñoz R, Peña-Claros M, van Breugel M, Herault B, Jakovac CC, Lebrija-Trejos E, Norden N, Lohbeck M. 2024. A comprehensive framework for vegetation succession. Ecosphere 15: e4794. DOI: 10.1002/ecs2.4794.
Prado MA, Urrego LE, Durán LI, Hernández J. 2021. Effect of climate seasonality and vegetation cover on floral resource selection by two stingless bee species. Apidologie 52 (5): 974-989. DOI: 10.1007/s13592-021-00881-7.
Prastiyo A, Nuraeni S, Budiaman B. 2024. Morphology and morphometric of Tetragonula biroi bees at three different altitudes in South Sulawesi, Indonesia. Biodiversitas 25 (5): 1993-2002. DOI: 10.13057/biodiv/d250516.
Priyambodo P, Rustiati EL, Permatasari N, Sidik M, Lestari IA, Yani AA, Sa'uddah LD. 2023. Optimizing honey production in stingless bee farming. J Community Serv Empower 4 (2): 360-367. DOI: 10.22219/jcse.v4i2.26431.
Pushpakumara G, Sokolow J, Sthapit B, Sujarwo W, Hunter D. 2020. Keeping it close to home: Home gardens and biodiversity conservation. In: Dissanayake DHG, Maredia KM (eds). Home Gardens for Improved Food Security and Livelihoods Routledge, London. DOI: 10.4324/9781315471778-3.
Raffiudin R, Dyahastuti M, Nugraha R, Sayusti T, Djuita NR, Suwananda E, Allvioningrum V, Mardhony R, Biagioni S, Setyaningsih CA, Prasetyo LB, Priawandiputra W, Atmowidi T, Saad A, Behling H. 2024. The effect of land cover on the foraging behavior and pollen in the honey of the giant bee Apis dorsata in Sumatra. Front Bee Sci 2: 1366287. DOI: 10.3389/frbee.2024.1366287.
Rahmad B, Damiri N, Hanafiah Z, Adriani D, Hanum L. 2024. Food source diversity and honey production in stingless bee meliponiculture, Ogan Komering Ulu Timur, South Sumatra, Indonesia. Biodiversitas 25 (6): 2747-2756. DOI: 10.13057/biodiv/d250645.
Roselino AC, Rodrigues AV, Hrncir M. 2016. Stingless bees (Melipona scutellaris) learn to associate footprint cues at food sources with a specific reward context. J Comp Physiol A 202: 657-666. DOI: 10.1007/s00359-016-1104-1.
Roubik DW. 2023. Stingless bee (Apidae: Apinae: Meliponini) ecology. Annu Rev Entomol 68 (1): 231-256. DOI: 10.1146/annurev-ento-120120-103938.
Salatnaya H, Fuah AM, Engel MS, Sumantri C, Widiatmaka W, Kahono S. 2021. Diversity, nest preferences, and forage plants of stingless bees (Hymenoptera: Apidae: Meliponini) from West Halmahera, North Moluccas, Indonesia. Jurnal Ilmu Ternak dan Veteteriner 26 (4): 167-178. DOI: 10.14334/jitv.v26i4.2896.
Schulze-Albuquerque I, Costa ACGD, Milet-Pinheiro P, Navarro DMDAF, Thomas WW, Machado IC. 2020. Visual and olfactory floral cues related to ambophilous pollination systems in Poaceae. Bot J Linn Soc 192 (1): 242-257. DOI: 10.1093/botlinnean/boz082.
Sreekumar S, Kelber A, Somanathan H. 2025. Influence of floral traits on visitation patterns in a miniature tropical stingless bee, Tetragonula iridipennis. Sci Nat 112: 1-13. DOI: 10.1007/s00114-025-01994-0.
Tobajas E, Domínguez?García V, Molina FP, Bartomeus I. 2024. Pollinator asynchrony drives the temporal stability of flower visitation rates, but not of plant reproductive success. J Ecol 112 (1): 4-13. DOI: 10.1111/1365-2745.14216.
Villanueva-Gutiérrez R, Roubik DW, Porter-Bolland L. 2015. Bee-plant interactions: Competition and phenology of flowers visited by bees. In: Islebe GA, Calmé S, León-Cortés JL, Schmook B (eds). Biodiversity and Conservation of the Yucatán Peninsula. Springer, Cham. DOI: 10.1007/978-3-319-06529-8_6.
Wayo K, Sritongchuay T, Chuttong B, Attasopa K, Bumrungsri S. 2020. Local and landscape compositions influence stingless bee communities and pollination networks in tropical mixed fruit orchards, Thailand. Diversity 12 (12): 482. DOI: 10.3390/d12120482.
Zhou HX, Cheng MH, Pan JL, Cui P, Song YQ, Yu Y, Cao J, Zha HG. 2023. Residues of sulfoxaflor and its metabolites in floral and extrafloral nectar from Hibiscus rosa-sinensis L. (Malvaceae) with or without co-application of tebuconazole. Pest Biochem Physiol 196: 105587. DOI: 10.1016/j.pestbp.2023.105587.
Zortéa KÉM, Rossi AAB, Cordeiro AGM, Sander NL, dos Santos Cardoso E, da Silva CJ. 2022. Pollen morphology, meiotic index and pollen viability in individuals of Vochysia divergens Pohl native to the Amazon and the Pantanal. Res Soc Dev 11 (4): e51511427540. DOI: 10.33448/rsd-v11i4.27540.