Attractiveness of Tetragonula laeviceps (Hymenoptera: Apidae) to Citrus Volatile Compounds and Flower Colors in Indoor Microclimate Conditions

Authors

  • Muhamad Aldi Nurdiansyah Doctoral Program of Biology, School of Life Sciences and Technology, Institut Teknologi Bandung, Bandung, West Java, Indonesia
  • Muhammad Yusuf Abduh School of Life Sciences and Technology, Institut Teknologi Bandung, Bandung, West Java, Indonesia
  • Hajime Ono Laboratory of Chemical Ecology, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
  • Agus Dana Permana Laboratory of Chemical Ecology, Graduate School of Agriculture, Kyoto University, Kyoto, Japan

DOI:

https://doi.org/10.13102/sociobiology.v71i3.10395

Keywords:

Attractant, behavior, GC-MS, olfactory, visual cues

Abstract

Tetragonula laeviceps plays a vital role as a primary pollinator of citrus flowers for successful pollination. However, there is still a lack of understanding about how T. laeviceps can find citrus flowers. This study aimed to elucidate the factors influencing the attraction of T. laeviceps to citrus flowers, focusing on microclimate conditions, and visual and olfactory factors. For this, we conducted six-choice assays in a stingless bee house using artificial flowers as visual cues and citrus essential oils as olfactory stimuli. Three pairs of red or white artificial flowers were displayed to adult workers, with each pair placed in glass vials filled with diluted orange (Citrus reticulata) essential oil, lemon (Citrus limon) essential oil, or solvent. Simultaneously, microclimate conditions were measured, including temperature, relative humidity, and light intensity. We observed that the highest number of T. laeviceps visited the artificial flowers at 11:00, irrespective of visual and olfactory factors. We also found a positive correlation between the number of visits and both temperature and light intensity, whereas there was a negative correlation with humidity. The number of visits did not exhibit a significant difference between flower colors. In contrast, we observed the highest visitation to the orange essential oil, followed by the lemon essential oil and solvent. Gas Chromatograph – Mass Spectrometry (GC-MS) analysis revealed common terpenes in orange and lemon essential oils, while linalool and α-citral were predominantly detected in the orange essential oil. These characteristic terpenes could potentially be the attractants for T. laeviceps.

Downloads

Download data is not yet available.

References

Abduh, M.Y., Ramdhani, F., Setiawan, A., Rifqialdi, G., Rahmawati, A. & Zainudin, I.M. (2023). Determination of productivity, yield and bioactivity of propolis extract produced by Tetragonula spp. Cultivated in Modular Tetragonula hives. Heliyon, 9: e17304. https://doi.org/10.1016/j.heliyon.2023.e17304

Aizen, M.A., Aguiar, S., Biesmeijer, J.C., Garibaldi, L.A., Inouye, D.W., Jung, C., Martins, D.J., Medel, R., Morales, C.L., Ngo, H., Pauw, A., Paxton, R.J., Sáez, A. & Seymour, C.L. (2019). Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification. Global Change Biology, 25: 3516-3527. https://doi.org/10.1111/gcb.14736

Azam, M., Song, M., Fan, F., Zhang, B., Xu, Y., Xu, C. & Chen, K. (2013). Comparative analysis of flower volatiles from nine citrus at three blooming stages. International Journal of Molecular Sciences, 14: 22346-22367. https://doi.org/10.3390/ijms141122346

Azmi, W.A., Wan Sembok, W.Z., Yusuf, N., Mohd Hatta, M.F., Salleh, A.F., Hamzah, M.A.H. & Ramli, S.N. (2019). Effects of pollination by the indo-malaya stingless bee (Hymenoptera: Apidae) on the quality of greenhouse-produced rockmelon. Journal of Economic Entomology, 112: 20-24. https://doi.org/10.1093/jee/toy290

Balamurali, G.S., Nicholls, E., Somanathan, H. & Hempel de Ibarra, N. (2018). A comparative analysis of colour preferences in temperate and tropical social bees. Science of Nature, 105: 1-10. https://doi.org/10.1007/s00114-017-1531-z

Barbosa, A.B., Meneses, H.M., Rosa, F.L. & Freitas, B.M. (2020). Flight activity of the stingless bee Plebeia aff. flavocincta in tropical conditions as an indicator of the general health of the colony. Sociobiology, 67: 545-553. https://doi.org/10.13102/sociobiology.v67i4.4926

Beck, J.J., Torto, B. & Vannette, R.L. (2017). Eavesdropping on plant-insect-microbe chemical communications in agricultural ecology: A virtual issue on semiochemicals. Journal of Agricultural and Food Chemistry, 65: 5101-5103. https://doi.org/10.1021/acs.jafc.7b02741

Buchori, D., Rizali, A., Priawandiputra, W., Raffiudin, R., Sartiami, D., Pujiastuti, Y., Jauharlina, Pradana, M.G., Meilin, A., Leatemia, J.A., Sudiarta, I.P., Rustam, R., Nelly, N., Lestari, P., Syahputra, E., Hasriyanti, Watung, J.F., Daud, I.D.A., Hariani, N., … Johannis, M. (2022). Beekeeping and managed bee diversity in Indonesia: Perspective and preference of beekeepers. Diversity, 14: 1-14. https://doi.org/10.3390/d14010052

Cholis, M.N., Atmowidi, T. & Kahono, S. (2020). The diversity and abundance of visitor insects on pummelo (Citrus maxima (burm) Merr ) cv . nambangan. Journal of Entomology and Zoology Studies, 8: 344-351.

dos Santos, S. A. B., Roselino, A. C., Hrncir, M., & Bego, L. R. (2009). Pollination of tomatoes by the stingless bee Melipona quadrifasciata and the honey bee Apis mellifera (Hymenoptera, Apidae). Genetics and Molecular Research, 8: 751-757. https://doi.org/10.4238/vol8-2kerr015

Dyer, A.G., Boyd-Gerny, S., Shrestha, M., Garcia, J.E., van der Kooi, C.J. & Wong, B.B.M. (2019). Colour preferences of Tetragonula carbonaria Sm. stingless bees for colour morphs of the Australian native orchid Caladenia carnea. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 205: 347-361. https://doi.org/10.1007/s00359-019-01346-0

Feng, Y.X., Lu, X.X., Du, Y.S., Zheng, Y., Zeng, D. & Du, S.S. (2022). Sesquiterpenoid-rich essential oils from two magnolia plants: Contact and repellent activity to three stored-product Insects. Journal of Oleo Science, 71: 435-443. https://doi.org/10.5650/jos.ess21241

Gallagher, M.K. & Campbell, D.R. (2020). Pollinator visitation rate and effectiveness vary with flowering phenology. American Journal of Botany, 107: 445-455. https://doi.org/10.1002/ajb2.1439

Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C., Morales, J.M., Bommarco, R., Cunningham, S.A., Carvalheiro, L.G., Chacoff, N.P., Dudenhöffer, J.H., Greenleaf, S.S., Holzschuh, A., Isaacs, R., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L.A., Potts, S.G., Ricketts, T.H., Szentgyörgyi, H., … Klein, A.M. (2011). Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecology Letters, 14: 1062-1072. https://doi.org/10.1111/j.1461-0248.2011.01669.x

Grajales-Conesa, J., Meléndez Ramírez, V., Cruz López, L. & Sánchez, D. (2013). Native bees in blooming orange (Citrus Sinensis) and lemon (Citrus Limon) orchards in Yucatán, México. Acta Zoológica Mexicana, 29: 437-440.

Grajales-Conesa, J., Ramírez, V.M., Cruz-López, L. & Guillén, D.S. (2012). Effect of citrus floral extracts on the foraging behavior of the stingless bee Scaptotrigona pectoralis (Dalla Torre). Revista Brasileira de Entomologia, 56: 76-80. https://doi.org/10.1590/S0085-56262012000100012

Grüter, C. (2020). Stingless Bees. Springer International Publishing. https://doi.org/10.1007/978-3-030-60090-7

Hall, M.A., Jones, J., Rocchetti, M., Wright, D. & Rader, R. (2020). Bee visitation and fruit quality in berries under protected cropping vary along the length of polytunnels. Journal of Economic Entomology, 113: 1337-1346. https://doi.org/10.1093/jee/toaa037

Kantsa, A., Raguso, R.A., Dyer, A.G., Sgardelis, S.P., Olesen, J.M. & Petanidou, T. (2017). Community-wide integration of floral colour and scent in a Mediterranean scrubland. Nature Ecology and Evolution, 1: 1502-1510. https://doi.org/10.1038/s41559-017-0298-0

Kishan Tej, M., Srinivasan, M.R., Rajashree, V. & Thakur, R.K. (2017). Stingless bee Tetragonula iridipennis Smith for pollination of greenhouse cucumber. Journal of Entomology and Zoology Studies, 5: 1729-1733.

Klatt, B.K., Burmeister, C., Westphal, C., Tscharntke, T. & von Fragstein, M. (2013). Flower volatiles, crop varieties and bee responses. PLoS ONE, 8. https://doi.org/10.1371/journal.pone.0072724

Koethe, S., Banysch, S., Alves-Dos-Santos, I. & Lunau, K. (2018). Spectral purity, intensity and dominant wavelength: Disparate colour preferences of two Brazilian stingless bee species. PLoS ONE, 13: 1-13.

https://doi.org/10.1371/journal.pone.0204663

Koh, I., Lonsdorf, E.V., Williams, N.M., Brittain, C., Isaacs, R., Gibbs, J. & Ricketts, T.H. (2016). Modeling the status, trends, and impacts of wild bee abundance in the United States. Proceedings of the National Academy of Sciences of the United States of America, 113: 140-145. https://doi.org/10.1073/pnas.1517685113

Layek, U., Kundu, A. & Karmakar, P. (2020). Floral ecology, floral visitors and breeding system of Gandharaj lemon (Citrus × limon L. Osbeck). Botanica Pacifica, 9: 1-7. https://doi.org/10.17581/bp.2020.09208

MacInnis, G., Normandin, E. & Ziter, C.D. (2023). Decline in wild bee species richness associated with honey bee (Apis mellifera L.) abundance in an urban ecosystem. PeerJ, 11: e14699. https://doi.org/10.7717/peerj.14699

Malerbo-Souza, D.T., Nogueira-Couto, R.H. & Couto, L.A. (2004). Honey bee attractants and pollination in sweet orange, Citrus sinensis (L.) Osbeck, var. Pera-Rio. Journal of Venomous Animals and Toxins Including Tropical Diseases, 10: 144-153. https://doi.org/10.1590/s1678-91992004000200004

Mc Cabe, S.I.M. & Farina, W.M. (2010). Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini). Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 196: 481-490. https://doi.org/10.1007/s00359-010-0536-2

Nurdiansyah, M.A., Abduh, M.Y. & Permana, A.D. (2023). Effects of meliponiculture Tetragonula laeviceps on pollinator diversity and visitation rate and citrus productivity in West Java, Indonesia. Biodiversitas, 24: 5757-5763. https://doi.org/10.13057/biodiv/d241058

Panziera, D., Requier, F., Chantawannakul, P., Pirk, C. W.W. & Blacquière, T. (2022). The Diversity decline in wild and managed honey bee populations urges for an integrated conservation approach. Frontiers in Ecology and Evolution, 10: 1-7. https://doi.org/10.3389/fevo.2022.767950

Polatto, L.P., Chaud-Netto, J. & Alves-Junior, V.V. (2014). Influence of abiotic factors and floral resource availability on daily foraging activity of bees. Journal of Insect Behavior, 27: 593-612. https://doi.org/10.1007/s10905-014-9452-6

Potts, S.G., Roberts, S.P.M., Dean, R., Marris, G., Brown, M.A., Jones, R., Neumann, P. & Settele, J. (2010). Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research, 49: 15-22. https://doi.org/10.3896/IBRA.1.49.1.02

Putra, R.E., Permana, A.D. & Kinasih, I. (2014). Application of Asiatic honey bees (Apis cerana) and stingless bees (Trigona laeviceps) as pollinator agents of hot pepper (Capsicum annuum L.) at local Indonesia farm system. Psyche. https://doi.org/10.1155/2014/687979

R Core Development Team (2023). A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/

Rachersberger, M., Cordeiro, G.D., Schäffler, I. & Dötterl, S. (2019). Honeybee pollinators use visual and floral scent cues to find apple (Malus domestica) flowers. Journal of Agricultural and Food Chemistry, 67: 13221-13227. https://doi.org/10.1021/acs.jafc.9b06446

Raguso, R.A. (2008). Wake up and smell the roses: The ecology and evolution of floral scent. Annual Review of Ecology, Evolution, and Systematics, 39: 549-569. https://doi.org/10.1146/annurev.ecolsys.38.091206.095601

Rhodes, C.J. (2018). Pollinator decline – An ecological calamity in the making? Science Progress, 101: 121-160. https://doi.org/10.3184/003685018x15202512854527

Roselino, A.C., Santos, S.B., Hrncir, M. & Bego, L.R. (2009). Differences between the quality of strawberries. Genetic and Molecular Research, 8: 539-545.

Sathiyaseelan, M., Jayaraj, J., Shanthi, M. & Sujatha, K. (2023). Behavioural response of stored product insects to light and bait sources in paddy storage godown. Indian Journal of Entomology, 85: 451-454. https://doi.org/10.55446/IJE.2021.150

Taha, E.K.A., Al-Abdulsalam, M. & Al-Kahtani, S. (2016). Insect pollinators and foraging behavior of honey bees on alfalfa (Medicago sativa L.) in Saudi Arabia. Journal of the Kansas Entomological Society, 89: 92-99. https://doi.org/10.2317/150402.1

Trianto, M. & Purwanto, H. (2022). Diversity, abundance, and distribution patterns of stingless bees (Hymenoptera: Meliponini) in Yogyakarta, Indonesia. Biodiversitas, 23: 695-702. https://doi.org/10.13057/biodiv/d230214

van Engelsdorp, D., Hayes, J., Underwood, R.M. & Pettis, J. (2008). A survey of honey bee colony losses in the U.S., Fall 2007 to Spring 2008. PLoS ONE, 3: 8-13. https://doi.org/10.1371/journal.pone.0004071

Zhang, L., Su, Q.F., Wang, L.S., Lv, M.W., Hou, Y.X. & Li, S.S. (2023). Linalool: A ubiquitous floral volatile mediating the communication between plants and insects. Journal of Systematics and Evolution, 61: 538-549. https://doi.org/10.1111/jse.12930

Downloads

Published

2024-07-25

How to Cite

Nurdiansyah, M. A., Abduh, M. Y., Ono, H., & Permana, A. D. (2024). Attractiveness of Tetragonula laeviceps (Hymenoptera: Apidae) to Citrus Volatile Compounds and Flower Colors in Indoor Microclimate Conditions. Sociobiology, 71(3), e10395. https://doi.org/10.13102/sociobiology.v71i3.10395

Issue

Vol. 71 No. 3 (2024)

Section

Research Article - Bees

License

Copyright (c) 2024 Muhamad Aldi Nurdiansyah, Muhammad Yusuf Abduh, Hajime Ono, Agus Dana Permana

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.

Authors who publish with this journal agree to the following terms:

 

    1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

 

    1. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

 

  1. Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).