Refuge as a Tool for Pollinator Conservation: Enhancing Biodiversity in RGL (Rimau Gerga Lebong) Citrus Orchards

Yunita Fera Rahmawati, Yuris Setyadin, Budi Purwantiningsih

Abstract


The RGL (Rimau Gerga Lebong) citrus orchard in Malang Regency, East Java (7°55'12“ S; 112°33'45” E) was the location for this study, which focused on the problem of declining pollinator populations in fruit cultivation areas. The study aimed to analyze pollinator diversity in three types of flowering plants sunflowers (Helianthus annuus), marigolds (Tagetes erecta), and wild cosmos (Cosmos caudatus) grown around citrus orchards, while evaluating their contribution to agroecosystem stability within the framework of Integrated Pest Management (IPM). Field observations were conducted from June to December 2024 using a combination of visual censuses and sweep net methods along 100 m × 2 m transects. From the observation results, 29 pollinator species from 10 families were identified, with Apidae as the dominant group that was consistently present in all treatments. These findings indicate that planting flowering plants around RGL orange orchards could support the recovery of pollinator communities while strengthening ecosystem services in integrated agricultural systems.Refuge planting increased species richness (R = 3.87 vs. 3.40 in controls) and total pollinator abundance, although the Shannon-Wiener Index (H’) in refuge areas (1.696) was lower than in controls (2.075), attributable to the disproportionate dominance of Amata huebneri. Sunflower refuge supported the highest pollinator diversity and abundance, marigold effectively attracted Syrphidae and Meliponini stingless bees, while wild cosmos enriched Lepidoptera and solitary bee composition. Bray-Curtis cluster analysis and PCA ordination confirmed that each refuge type produced distinct qualitative shifts in pollinator community structure. This study recommends implementing multispecies refuge systems combining all three plant species proportionally to prevent single-species dominance, broaden pollinator guild diversity, and optimize integrated pollination and biological control services in RGL citrus agroecosystems.

Keywords


Apidae; citrus agroecosystem; integrated pest management; pollinator diversity; refuge

Full Text:

PDF

References


Aguiar, L. M. S., Diniz, U. M., Bueno?Rocha, I. D., Filomeno, L. R. A., Aguiar?Machado, L. S., Gomes, P. A., & Togni, P. H. B. (2024). Untangling biodiversity interactions: A meta network on pollination in Earth’s most diverse tropical savanna. Ecology and Evolution, 14(3). https://doi.org/10.1002/ece3.11094

Alignier, A., Lenestour, N., Jeavons, E., van Baaren, J., Aviron, S., Uroy, L., Ricono, C., & Le Lann, C. (2023). Floral resource maps: a tool to explain flower-visiting insect abundance at multiple spatial scales. Landscape Ecology, 38(6), 1511–1525. https://doi.org/10.1007/s10980-023-01643-9

Aminah, S. N., Nasruddin, A., Annisaa, N. W., Abdullah, T., & Fatahuddin. (2021). The presence of refugia and population of insect pest in rice field. IOP Conference Series: Earth and Environmental Science, 807(2), 022093. https://doi.org/10.1088/1755-1315/807/2/022093

Aminatun, T., Budiwati, B., Rahmawati, Y. F., Widiyanti, D. N. A., & Fahdah, L. A. (2023). The effects of flowering trap crops on diversity and longevity of pollinator insect visitation on chili plants. Biodiversitas Journal of Biological Diversity, 24(2). https://doi.org/10.13057/biodiv/d240226

Asmini, A., Atmowidi, T., & Kahono, S. (2022). Pollination by Three Species of Stingless Bees (Hymenoptera: Meliponini) Increase Seed Set of Mustard (Brassica rapa L.: Brassicaceae). Hayati Journal of Biosciences, 29(5), 712–719. https://doi.org/10.4308/hjb.29.5.712-719

Bednaršek, N., Pelletier, G., Beck, M. W., Feely, R. A., Siegrist, Z., Kiefer, D., Davis, J., & Peabody, B. (2024). Predictable patterns within the kelp forest can indirectly create temporary refugia from ocean acidification. Science of The Total Environment, 945, 174065. https://doi.org/10.1016/j.scitotenv.2024.174065

Boon, J. S., Keith, S. A., Exton, D. A., & Field, R. (2023). The role of refuges in biological invasions: A systematic review. Global Ecology and Biogeography, 32(8), 1244–1271. https://doi.org/10.1111/geb.13701

Borror, D. J. , T. C. A. , & J. N. F. (1992). An introduction to the study of insects (6th ed.). Saunders College Publishing.

Bottero, I., Dominik, C., Schweiger, O., Albrecht, M., Attridge, E., Brown, M. J. F., Cini, E., Costa, C., De la Rúa, P., de Miranda, J. R., Di Prisco, G., Dzul Uuh, D., Hodge, S., Ivarsson, K., Knauer, A. C., Klein, A.-M., Mänd, M., Martínez-López, V., Medrzycki, P., … Stout, J. C. (2023). Impact of landscape configuration and composition on pollinator communities across different European biogeographic regions. Frontiers in Ecology and Evolution, 11. https://doi.org/10.3389/fevo.2023.1128228

Burgio, G., Dindo, M. L., Pape, T., Whitmore, D., & Sommaggio, D. (2025). Diptera as predators in biological control: applications and future perspectives. BioControl, 70(1), 1–17. https://doi.org/10.1007/s10526-024-10281-2

Callaway, B., Goodman-Bacon, A., & Sant’Anna, P. H. (2024). Difference-in-differences with a Continuous Treatment. https://doi.org/10.3386/w32117

Chellam, S., Bai, D. G., Rani, D. V., Sindhu, M., Pushpalatha, V., JS, R., & Manoosha, G. (2024). Agro-ecological approaches to pest management: The role of crop diversification and habitat manipulation. International Journal of Advanced Biochemistry Research, 8(9S), 154–157. https://doi.org/10.33545/26174693.2024.v8.i9Sb.2077

Cohen, H., Philpott, S. M., Liere, H., Lin, B. B., & Jha, S. (2021). The relationship between pollinator community and pollination services is mediated by floral abundance in urban landscapes. Urban Ecosystems, 24(2), 275–290. https://doi.org/10.1007/s11252-020-01024-z

David, M. A., Yommi, A., Sánchez, E., Martinez, A., Murillo, N., Marcellán, O., Atela, O., & Palacio, M. A. (2022). Strategic use of honey bees (Apis mellifera L.) to increase the number and size of fruits in kiwifruit (Actinidia chinensis var. deliciosa). European Journal of Agronomy, 133, 126420. https://doi.org/10.1016/j.eja.2021.126420

Fried, G., Le Corre, V., Rakotoson, T., Buchmann, J., Germain, T., Gounon, R., Royer, H., Biju?Duval, L., Felten, E., Vieren, E., & Chauvel, B. (2022). Impact of new management practices on arable and field margin plant communities in sunflower, with an emphasis on the abundance of Ambrosia artemisiifolia (Asteraceae). Weed Research, 62(2), 134–148. https://doi.org/10.1111/wre.12522

Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., Kremen, C., Carvalheiro, L. G., Harder, L. D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N. P., Dudenhöffer, J. H., Freitas, B. M., Ghazoul, J., Greenleaf, S., … Klein, A. M. (2013). Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance. Science, 339(6127), 1608–1611. https://doi.org/10.1126/science.1230200

Goulson, D., Nicholls, E., Botías, C., & Rotheray, E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229). https://doi.org/10.1126/science.1255957

Guignard, Q., Spaethe, J., Slippers, B., Strube-Bloss, M., & Allison, J. D. (2021). Evidence for UV-green dichromacy in the basal hymenopteran Sirex noctilio (Siricidae). Scientific Reports, 11(1), 15601. https://doi.org/10.1038/s41598-021-95107-2

Hagen, M., & Kraemer, M. (2010). Agricultural surroundings support flower–visitor networks in an Afrotropical rain forest. Biological Conservation, 143(7), 1654–1663. https://doi.org/10.1016/j.biocon.2010.03.036

Hasriyanty, Yunus, M., Rosmini, Adelia, & Suriani. (2023). Arthropoda Diversity in Paddy Field with Refugia Plants (pp. 34–39). https://doi.org/10.2991/978-94-6463-334-4_7

Hederström, V., Ekroos, J., Friberg, M., Krausl, T., Opedal, Ø. H., Persson, A. S., Petrén, H., Quan, Y., Smith, H. G., & Clough, Y. (2024). Pollinator?mediated effects of landscape?scale land use on grassland plant community composition and ecosystem functioning – seven hypotheses. Biological Reviews, 99(3), 675–698. https://doi.org/10.1111/brv.13040

Hou, Z., Liu, J., Cai, M., Liu, Y., Zhang, M., Wang, L., Yang, W., & Huang, B. (2023). The volatile organic compounds and palatability of mixed ensilage of marigold (Tagetes erecta L.) crop residues. Scientific Reports, 13(1), 2080. https://doi.org/10.1038/s41598-023-28511-5

Jiang, S., Li, H., & Wu, K. (2023). Predation and Control Effect of Eupeodes corollae Fabricius (Diptera: Syrphidae) on Leguminous Plant Aphids. Agronomy, 13(7), 1739. https://doi.org/10.3390/agronomy13071739

Jordan, A., Patch, H. M., Grozinger, C. M., & Khanna, V. (2021). Economic Dependence and Vulnerability of United States Agricultural Sector on Insect-Mediated Pollination Service. Environmental Science & Technology, 55(4), 2243–2253. https://doi.org/10.1021/acs.est.0c04786

Jordão, J. P., da Silva, A. P., Nana, H. R. T., da Costa Pereira, R. R., & Fávaro, C. F. (2024). Ecology of entomological communities in cocoa flowers (Theobroma cacao L.) in the shade-grown system: harmonic interactions in pollination. Agroforestry Systems, 98(8), 3179–3194. https://doi.org/10.1007/s10457-024-01082-8

Josephrajkumar, A., Mani, M., Anes, K. M., & Mohan, C. (2022). Ecological Engineering in Pest Management in Horticultural and Agricultural Crops. In Trends in Horticultural Entomology (pp. 123–155). Springer Nature Singapore. https://doi.org/10.1007/978-981-19-0343-4_4

Kumar, R., Hajam, Y. A., Kumar, I., & Neelam. (2024). Insect Pollinators’s Diversity in the Himalayan Region: Their Role in Agriculture and Sustainable Development. In Role of Science and Technology for Sustainable Future (pp. 243–276). Springer Nature Singapore. https://doi.org/10.1007/978-981-97-0710-2_16

Kuppler, J., & Kotowska, M. M. (2021). A meta?analysis of responses in floral traits and flower–visitor interactions to water deficit. Global Change Biology, 27(13), 3095–3108. https://doi.org/10.1111/gcb.15621

Lowe, E. B., Groves, R., & Gratton, C. (2021). Impacts of field-edge flower plantings on pollinator conservation and ecosystem service delivery – A meta-analysis. Agriculture, Ecosystems & Environment, 310, 107290. https://doi.org/10.1016/j.agee.2020.107290

Loy, X., & Brosi, B. J. (2022). The effects of pollinator diversity on pollination function. Ecology, 103(4). https://doi.org/10.1002/ecy.3631

Magurran AE. (2004). Measuring Biological Diversity. Blackwell Scientific Oxford, UK.

Maia-Silva, C., Hrncir, M., Giannini, T. C., Toledo-Hernández, M., & Imperatriz-Fonseca, V. L. (2024). Small Amazonian stingless bees: an opportunity for targeted cocoa pollination. Frontiers in Bee Science, 2. https://doi.org/10.3389/frbee.2024.1357811

Michener, C. D. (2007). . The bees of the world, 2nd edn. – Johns Hopkins University Press.

Nath, R., Singh, H., & Mukherjee, S. (2023). Insect pollinators decline: an emerging concern of Anthropocene epoch. Journal of Apicultural Research, 62(1), 23–38. https://doi.org/10.1080/00218839.2022.2088931

Noss, R. F., Cartwright, J. M., Estes, D., Witsell, T., Elliott, K. G., Adams, D. S., Albrecht, M. A., Boyles, R., Comer, P. J., Doffitt, C., Faber-Langendoen, D., Hill, J. G., Hunter, W. C., Knapp, W. M., Marshall, M., Pyne, M., Singhurst, J. R., Tracey, C., Walck, J. L., & Weakley, A. (2021). Science needs of southeastern grassland species of conservation concern: A framework for species status assessments. https://doi.org/10.3133/ofr20211047

Phan, N. T., Biddinger, D. J., Rajotte, E. G., Smagghe, G., Reddy, G. V., Ren, Z., & Joshi, N. K. (2025). Pesticide use in integrated pest and pollinator management framework to protect pollinator health. Pest Management Science, 81(4), 1691–1696. https://doi.org/10.1002/ps.8582

Pioltelli, E., Guzzetti, L., Biella, P., Sala, D., Copetta, A., Mussano, P., Galimberti, A., & Labra, M. (2024). Animal pollination shapes fruits market features, seeds functional traits and modulates their chemistry. Scientific Reports, 14(1), 22734. https://doi.org/10.1038/s41598-024-73647-7

Puttha, R., Venkatachalam, K., Hanpakdeesakul, S., Wongsa, J., Parametthanuwat, T., Srean, P., Pakeechai, K., & Charoenphun, N. (2023). Exploring the Potential of Sunflowers: Agronomy, Applications, and Opportunities within Bio-Circular-Green Economy. Horticulturae, 9(10), 1079. https://doi.org/10.3390/horticulturae9101079

Rahmawati, Y. F. , & A. L. N. F. (n.d.). Effectiveness of Predator Diversity in Refuge Plants in Reducing Bactrocera sp. Population on Batu 55 Tangerines. LenteraBio: Berkala Ilmiah Biologi, 15(1), 1–8.

Rahmawati, Y. F., Leksono, A. S., Gama, Z. P., & Rizali, A. (2025). The impact of refuges on Citrus orchards associated with arthropods in different agroecosystem in Malang, Indonesia. Cogent Food & Agriculture, 11(1). https://doi.org/10.1080/23311932.2024.2448599

Rahmawati, Y. F., Leksono, A. S., Rizali, A., & Gama, Z. P. (2024). Population dynamics of Bactrocera spp., and parasitization efficacy of Opius sp. (Hymenoptera: Braconidae) in citrus varieties. Biodiversitas Journal of Biological Diversity, 25(11). https://doi.org/10.13057/biodiv/d251134

Serralta-Batun, L. P. , J.-O. J. J. , M.-R. V. , & M.-R. M. A. (2024). Taxonomic and functional diversity of bees in traditional agroecosystems and tropical forest patches on the Yucatan Peninsula. Tropical Conservation Science, 17(19400829231225428).

Setyadin, Y., Leksono, A. S., & Tarno, H. (2025). Diversity and bioindicators of natural enemies in organic paddy fields implementing habitat modification. BIO Web of Conferences, 154, 01004. https://doi.org/10.1051/bioconf/202515401004

Shpak, Y. V., Leheta, U. V., & Sosnovskyi, K. S. (2023). Importance of pollinator diversity for sunflower seed production. Agrology, 6(4), 79–85. https://doi.org/10.32819/021113

Singh, G., Cook, J. M., Spooner?Hart, R. N., & Makinson, J. C. (2025). Insect floral visitors vary spatiotemporally and influence fruit production in mango orchards. Ecological Entomology, 50(6), 1121–1136. https://doi.org/10.1111/een.70005

Sladonja, B., Tlak Gajger, I., Uzelac, M., Poljuha, D., Garau, C., Landeka, N., Barták, M., & Bacaro, G. (2023). The Impact of Beehive Proximity, Human Activity and Agricultural Intensity on Diptera Diversity in a Mediterranean Mosaic of Agroecosystems, with a Focus on Pest Species. Animals, 13(6), 1024. https://doi.org/10.3390/ani13061024

Sponsler, D., Iverson, A., & Steffan?Dewenter, I. (2023). Pollinator competition and the structure of floral resources. Ecography, 2023(9). https://doi.org/10.1111/ecog.06651

Torezan-Silingardi, H. M., Silberbauer-Gottsberger, I., & Gottsberger, G. (2021). Pollination Ecology: Natural History, Perspectives and Future Directions. In Plant-Animal Interactions (pp. 119–174). Springer International Publishing. https://doi.org/10.1007/978-3-030-66877-8_6

Traut, W., Sahara, K., & ffrench-Constant, R. H. (2023). Lepidopteran Synteny Units reveal deep chromosomal conservation in butterflies and moths. G3: Genes, Genomes, Genetics, 13(8). https://doi.org/10.1093/g3journal/jkad134

Ulyshen, M., Urban?Mead, K. R., Dorey, J. B., & Rivers, J. W. (2023). Forests are critically important to global pollinator diversity and enhance pollination in adjacent crops. Biological Reviews, 98(4), 1118–1141. https://doi.org/10.1111/brv.12947

Vanlalhmangaiha, R., Singh, H. K., Boopathi, T., Lalhruaitluangi, S., & Sangma, T. T. (2023). Impact of insect pollination on the quantitative and qualitative characteristics of sweet orange, Citrus sinensis (L.) Osbeck. Journal of Apicultural Research, 62(4), 767–776. https://doi.org/10.1080/00218839.2021.2013401

Villagómez, G. N., Spaethe, J., & Leonhardt, S. D. (2024). The stingless bee Trigona fulviventris prefers sweet and salty over savory nectar. Apidologie, 55(4), 39. https://doi.org/10.1007/s13592-024-01081-9

Windriyanti, W., Rahmadhini, N., Fernando, I., & Kusuma, R. M. (2023). Arthropods discovered on refugio flowering plants in Mangifera indica plantation. Biodiversitas Journal of Biological Diversity, 24(9). https://doi.org/10.13057/biodiv/d240915

Xerces Society for Invertebrate Conservation. (2021). Farming with native beneficial insects: Ecological pest control solutions. Storey Publishing.




DOI: https://doi.org/10.14421/biomedich.2026.151.833-843

Refbacks

  • There are currently no refbacks.


Bookmark and Share


Copyright (c) 2026 Yunita Fera Rahmawati, Yuris Setyadin, Budi Purwantiningsih



Biology, Medicine, & Natural Product Chemistry
ISSN 2089-6514 (paper) - ISSN 2540-9328 (online)
Published by Sunan Kalijaga State Islamic University & Society for Indonesian Biodiversity.

CC BY NC
This work is licensed under a CC BY-NC