A review of plant protection against the olive fly (Bactrocera oleae (Rossi, 1790) Gmelin) and molecular methods to monitor the insecticide resistance alleles


  • Matjaž Hladnik University of Primorska, Faculty of Mathematics, Natural Sciences and Information Technologies, Glagoljaška 8, SI-6000 Koper, Slovenia




organophosphates, ace gene, resistance alleles, plant protection methods, alternative methods, spinosad, biological control


Olive fly (Bactrocera oleae (Rossi, 1790) Gmelin) is one of the most important olive pests worldwide. Most plant protection measures are based on insecticides, especially organophosphates, pyrethroids, and recently a spinosad. Insecticides are used as cover sprays or in more environmentally friendly methods in which insecticides are used in combination with attractants and pheromones as bait sprays or for mass trapping. However, due to negative impacts of insecticides to environment, new plant protection methods are constantly developing with the aim to lower the consumption of insecticides or even to eliminate them by biological control with entomopathogenic organisms, sterile insect technique (SIT), or transgenic method RIDL (release of insects carrying a dominant lethal). However, these methods need to be improved in order to guarantee adequate protection. Alternative methods than those traditionally used are required due to long term usage causing the development of resistance to the insecticides, ultimately lowering their effectiveness. Molecular methods for monitoring the frequencies of resistant alleles and the current status of resistance alleles in olive growing countries are reviewed here.


Akmoutsou, P., Mademtzoglou, D., Nakou, I., Onoufriadis, A., Papadopoulou, X., Kounatidis, I., ... Mavragani-Tsipidou, P. (2011). Evaluation of toxicity and genotoxic effects of spinosad and deltamethrin in Drosophila melanogaster and Bactrocera oleae. Pest Management Science, 67(12), 1534-1540. doi:10.1002/ps.2208

Ant, T., Koukidou, M., Rempoulakis, P., Gong, H.-F., Economopoulos, A., Vontas, J., Alphey, L. (2012). Control of the olive fruit fly using genetics-enhanced sterile insect technique. BMC Biology, 10(1), 1-8. doi:10.1186/1741-7007-10-51

Apostolaki, A., Livadaras, I., Saridaki, A., Chrysargyris, A., Savakis, C., Bourtzis, K. (2011). Transinfection of the olive fruit fly Bactrocera oleae with Wolbachia: towards a symbiont‐based population control strategy. Journal of Applied Entomology, 135(7), 546-553. doi:10.1111/j.1439-0418.2011.01614.x

Bengochea, P., Budia, F., Viñuela, E., Medina, P. (2014). Are kaolin and copper treatments safe to the olive fruit fly parasitoid Psyttalia concolor? Journal of Pest Science, 87(2), 351-359. doi:10.1007/s10340-013-0543-5

Bueno, A. M., Jones, O. (2002). Alternative methods for controlling the olive fly, Bactrocera oleae, involving semiochemicals. IOBC wprs Bulletin, 25(9), 147-156.

Burrack, H. J., Connell, J. H., Zalom, F. G. (2008). Comparison of olive fruit fly (Bactrocera oleae (Gmelin)) (Diptera: Tephritidae) captures in several commercial traps in California. International Journal of Pest Management, 54(3), 227-234. doi:10.1080/09670870801975174

Daane, K. M., Johnson, M. W. (2010). Olive Fruit Fly: Managing an Ancient Pest in Modern Times. Annual review of entomology, 55(1), 151-169. doi:10.1146/annurev.ento.54.110807.090553

Daane, K. M., Wang, X., Nieto, D. J., Pickett, C. H., Hoelmer, K. A., Blanchet, A., Johnson, M. W. (2015). Classic biological control of olive fruit fly in California, USA: release and recovery of introduced parasitoids. BioControl, 60(3), 317-330. doi:10.1007/s10526-015-9652-9

Doğaç, E., Kandemir, İ., Taşkın, V. (2015). Geographical distribution and frequencies of organophosphate-resistant Ace alleles and morphometric variations in olive fruit fly populations. Pest Management Science, 71(11), 1529-1539. doi:10.1002/ps.3958

Efthimia, S., Martin, R., Maria-Eleni, G., Konstantina T, T., Nikolaos E, Z., Klelia D, S., ... Kostas D, M. (2014). Olive fly transcriptomics analysis implicates energy metabolism genes in spinosad resistance. 15, 714. doi:10.1186/1471-2164-15-714

Fabbri, A., Lambardi, M., Ozden-Tokatli, Y. (2009). Olive Breeding. In S. M. Jain & P. M. Priyadarshan (Eds.), Breeding Plantation Tree Crops: Tropical Species (pp. 423-465). New York, NY: Springer New York. doi: 10.1007/978-0-387-71201-7_12

Garantonakis, N., Varikou, K., Markakis, E., Birouraki, A., Sergentani, C., Psarras, G., Koubouris, G. C. (2016). Interaction between Bactrocera oleae (Diptera: Tephritidae) infestation and fruit mineral element content in Olea europaea (Lamiales: Oleaceae) cultivars of global interest. Applied Entomology and Zoology, 51(2), 257-265. doi:10.1007/s13355-016-0397-4

Genç, H., Schetelig, M. F., Nirmala, X., Handler, A. M. (2016). Germline transformation of the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), with a piggyBac transposon vector. Turkish Journal of Biology, 40(4), 845-855. doi:10.3906/biy-1510-55

Gil-Ortiz, R. (2015). Development of new ecological long-lasting dispensers of semiochemicals for the control of Bactrocera oleae (Rossi). Pest Management Science, 71(12), 1694-1694. doi:10.1002/ps.4156

Gonçalves, M. F., Santos, S. A. P., Torres, L. M. (2012). Efficacy of spinosad bait sprays to control Bactrocera oleae and impact on non-target arthropods. Phytoparasitica, 40(1), 17-28. doi:10.1007/s12600-011-0195-z

Hagen, K. S., Finney, G. L. (1950). A Food Supplement for Effectively Increasing the Fecundity of Certain Tephritid Species. Journal of Economic Entomology, 43(5), 735. doi: 10.1093/jee/43.5.735

Hanife, G. (2016). Screening of Organophosphate Resistance in the Acetycholinesterase Gene of Field Collected Olive Fruit Fly, Bactrocera Oleae Rossi (Diptera: Tephritidae). Romanian Biotechnological Letters, 21(1), 11209-11216.

Haniotakis, G. E. (2005). Olive pest control: present status and prospects. Bulletin OILB/SROP, 28(9), 1-9.

Hawkes, N. J., Janes, R. W., Hemingway, J., Vontas, J. (2005). Detection of resistance-associated point mutations of organophosphate-insensitive acetylcholinesterase in the olive fruit fly, Bactrocera oleae (Gmelin). Pesticide Biochemistry and Physiology, 81(3), 154-163. doi:10.1016/j.pestbp.2004.11.003

Herz, A., Hassan, S. A., Hegazi, E., Nasr, F. N., Youssef, A. A., Khafagi, W. E., ... Pereira, J. A. (2005). Towards sustainable control of Lepidopterous pests in olive cultivation. Gesunde Pflanzen, 57(5), 117-128. doi:10.1007/s10343-005-0076-9

Jardak, T., Ali Triki, M., Rhouma, A., Ksantini, M. (2007). Plant health protection. Production techniques in olive growing. Madrid, MD: International Olive Council.

Kakani, E. G., Bon, S., Massoulié, J., Mathiopoulos, K. D. (2011). Altered GPI modification of insect AChE improves tolerance to organophosphate insecticides. Insect Biochemistry and Molecular Biology, 41(3), 150-158. doi:10.1016/j.ibmb.2010.11.005

Kakani, E. G., Ioannides, I. M., Margaritopoulos, J. T., Seraphides, N. A., Skouras, P. J., Tsitsipis, J. A., Mathiopoulos, K. D. (2008). A small deletion in the olive fly acetylcholinesterase gene associated with high levels of organophosphate resistance. Insect Biochemistry and Molecular Biology, 38(8), 781-787. doi:10.1016/j.ibmb.2008.05.004

Kakani, E. G., Mathiopoulos, K. D. (2008). Organophosphosphate resistance-related mutations in the acetylcholinesterase gene of Tephritidae. Journal of Applied Entomology, 132(9-10), 762-771. doi:10.1111/j.1439-0418.2008.01373.x

Kakani, E. G., Sagri, E., Omirou, M., Ioannides, I. M., Mathiopoulos, K. D. (2013). Detection and geographical distribution of the organophosphate resistance-associated Δ3Qace mutation in the olive fruit fly, Bactrocera oleae (Rossi). Pest Management Science, 70(5), 743-750. doi:10.1002/ps.3564

Kakani, E. G., Zygouridis, N. E., Tsoumani, K. T., Seraphides, N., Zalom, F. G., Mathiopoulos, K. D. (2010). Spinosad resistance development in wild olive fruit fly Bactrocera oleae (Diptera: Tephritidae) populations in California. Pest Management Science, 66(4), 447-453. doi:10.1002/ps.1921

Knap, T., Bandelj, D. (2016). Microsatellite analysis revealed a different approach of control of olive fly population (Bactrocera oleae) in Slovenia. Journal of Applied Entomology. doi:10.1111/jen.12333

Leftwich, P. T., Bolton, M., Chapman, T. (2016). Evolutionary biology and genetic techniques for insect control. Evolutionary Applications, 9(1), 212-230. doi:10.1111/eva.12280

Malacrinò, A., Schena, L., Campolo, O., Laudani, F., Palmeri, V. (2015). Molecular analysis of the fungal microbiome associated with the olive fruit fly Bactrocera oleae. Fungal Ecology, 18, 67-74. doi:10.1016/j.funeco.2015.08.006

Malheiro, R., Casal, S., Baptista, P., Pereira, J. A. (2015a). A review of Bactrocera oleae (Rossi) impact in olive products: From the tree to the table. Trends in Food Science & Technology, 44(2), 226-242. doi:10.1016/j.tifs.2015.04.009

Malheiro, R., Casal, S., Cunha, S. C., Baptista, P., Pereira, J. A. (2015b). Olive Volatiles from Portuguese Cultivars Cobrançosa, Madural and Verdeal Transmontana: Role in Oviposition Preference of Bactrocera oleae (Rossi) (Diptera: Tephritidae). PLoS ONE, 10(5), e0125070. doi:10.1371/journal.pone.0125070

Malheiro, R., Casal, S., Cunha, S. C., Baptista, P., Pereira, J. A. (2016). Identification of leaf volatiles from olive (Olea europaea) and their possible role in the ovipositional preferences of olive fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae). Phytochemistry, 121, 11-19. doi:10.1016/j.phytochem.2015.10.005

Margaritopoulos, J. T., Skavdis, G., Kalogiannis, N., Nikou, D., Morou, E., Skouras, P. J., ... Vontas, J. (2008). Efficacy of the pyrethroid alpha-cypermethrin against Bactrocera oleae populations from Greece, and improved diagnostic for an iAChE mutation. Pest Management Science, 64(9), 900-908. doi:10.1002/ps.1580

Mutero, A., Pralavorio, M., Bride, J. M., Fournier, D. (1994). Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proceedings of the National Academy of Sciences of the United States of America, 91(13), 5922-5926. doi: 10.1073/pnas.91.13.5922

Nardi, F., Carapelli, A., Vontas, J. G., Dallai, R., Roderick, G. K., Frati, F. (2006). Geographical distribution and evolutionary history of organophosphate-resistant Ace alleles in the olive fly (Bactrocera oleae). Insect Biochemistry and Molecular Biology, 36(7), 593-602. doi:10.1016/j.ibmb.2006.05.002

Ochando, M. D., Reyes, A. (2000). Genetic population structure in olive fly Bactrocera oleae (Gmelin): gene flow and patterns of geographic differentiation. Journal of Applied Entomology, 124(3-4), 177-183. doi:10.1046/j.1439-0418.2000.00460.x

Ortega, M., Pascual, S. (2014). Spatio-temporal analysis of the relationship between landscape structure and the olive fruit fly Bactrocera oleae (Diptera: Tephritidae). Agricultural and Forest Entomology, 16(1), 14-23. doi:10.1111/afe.12030

Pascual, S., Cobos, G., Seris, E., González-Núñez, M. (2010). Effects of processed kaolin on pests and non-target arthropods in a Spanish olive grove. Journal of Pest Science, 83(2), 121-133. doi:10.1007/s10340-009-0278-5

Pascual, S., Cobos, G., Seris, E., Sánchez-Ramos, I., González-Núñez, M. (2014). Spinosad bait sprays against the olive fruit fly (Bactrocera oleae (Rossi)): effect on the canopy non-target arthropod fauna. International Journal of Pest Management, 60(4), 258-268. doi:10.1080/09670874.2014.966171

Pavlidi, N., Dermauw, W., Rombauts, S., Chrisargiris, A., Van Leeuwen, T., Vontas, J. (2013). Analysis of the Olive Fruit Fly Bactrocera oleae Transcriptome and Phylogenetic Classification of the Major Detoxification Gene Families. PLoS ONE, 8(6), e66533. doi:10.1371/journal.pone.0066533

Pereira-Castro, I., Van Asch, B., Trindade Rei, F., Teixeira da Costa, L. (2015). Bactrocera oleae (Diptera: Tephritidae) organophosphate resistance alleles in Iberia: Recent expansion and variable frequencies. European Journal of Entomology, 112(1), 20-26. doi:10.14411/eje.2015.019

Piñero, J. C., Mau, R. F. L., Vargas, R. I. (2010). Comparison of Rain-Fast Bait Stations Versus Foliar Bait Sprays for Control of Oriental Fruit Fly, Bactrocera dorsalis, in Papaya Orchards in Hawaii. Journal of Insect Science, 10, 157. doi:10.1673/031.010.14117

Podgornik, M., Vuk, I., Arbeiter, A., Hladnik, M., Bandelj, D. (2013). Population Fluctuation of Adult Males of the Olive Fruit Fly Bactrocera oleae (Rossi) Analysis in Olive Orchards in Relation to Abiotic Factors. Entomological News, 123(1), 15-25. doi:10.3157/021.123.0106

Potamitis, I., Rigakis, I., Fysarakis, K. (2014). The Electronic McPhail Trap. Sensors, 14(12), 22285-22299. doi:10.3390/s141222285

Rejili, M., Fernandes, T., Dinis, A. M., Pereira, J. A., Baptista, P., Santos, S. A. P., Lino-Neto, T. (2016). A PCR-based diagnostic assay for detecting DNA of the olive fruit fly, Bactrocera oleae, in the gut of soil-living arthropods. Bulletin of Entomological Research, 106(5), 695-699. doi:10.1017/S000748531600050X

Rojnić, I. D., Bažok, R., Barčić, J. I. (2015). Reduction of olive fruit fly damage by early harvesting and impact on oil quality parameters. European Journal of Lipid Science and Technology, 117(1), 103-111. doi:10.1002/ejlt.201400150

Saour, G., Makee, H. (2004). A kaolin‐based particle film for suppression of the olive fruit fly Bactrocera oleae Gmelin (Dip., Tephritidae) in olive groves. Journal of Applied Entomology, 128(1), 28-31. doi:10.1046/j.1439-0418.2003.00803.x

Skouras, P. J., Margaritopoulos, J. T., Seraphides, N. A., Ioannides, I. M., Kakani, E. G., Mathiopoulos, K. D., Tsitsipis, J. A. (2007). Organophosphate resistance in olive fruit fly, Bactrocera oleae, populations in Greece and Cyprus. Pest Management Science, 63(1), 42-48. doi:10.1002/ps.1306

Tsakas, S. C. (1977). Genetics of Dacus oleae. VIII. Selection for the Amount of Acetylcholinesterase after Organophosphate Treatment. Evolution, 31(4), 901-904. doi:10.2307/2407454

Tzanakakis, M. E. (2003). Seasonal development and dormancy of insects and mites feeding on olive: A review. Netherlands Journal of Zoology, 52(2), 87-224. doi:10.1163/156854203764817670

Varikou, K., Alexandrakis, V., Gika, V., Birouraki, A., Marnelakis, C., Sergentani, C. (2013). Estimation of fly population density of Bactrocera oleae in olive groves of Crete. Phytoparasitica, 41(1), 105-111. doi:10.1007/s12600-012-0270-0

Varikou, K., Garantonakis, N., Birouraki, A. (2014). Response of olive fruit fly Bactrocera oleae to various attractant combinations, in orchards of Crete. Bulletin of Insectology, 67(1), 109-114. doi: 10.1016/j.cropro.2015.11.007

Varikou, K., Garantonakis, N., Birouraki, A. (2015). Residual attractiveness of various bait spray solutions to Bactrocera oleae. Crop Protection, 68, 60-66. doi:10.1016/j.cropro.2014.11.009

Varikou, K., Garantonakis, N., Birouraki, A., Ioannou, A., Kapogia, E. (2016). Improvement of bait sprays for the control of Bactrocera oleae (Diptera: Tephritidae). Crop Protection, 81, 1-8. doi:10.1016/j.cropro.2015.11.007

Vontas, J. G., Cosmidis, N., Loukas, M., Tsakas, S., Hejazi, M. J., Ayoutanti, A., Hemingway, J. (2001). Altered Acetylcholinesterase Confers Organophosphate Resistance in the Olive Fruit Fly Bactrocera oleae. Pesticide Biochemistry and Physiology, 71(2), 124-132. doi:10.1006/pest.2001.2568

Vontas, J. G., Hejazi, M. J., Hawkes, N. J., Cosmidis, N., Loukas, M., Hemingway, J. (2002). Resistance-associated point mutations of organophosphate insensitive acetylcholinesterase, in the olive fruit fly Bactrocera oleae. Insect Molecular Biology, 11(4), 329-336. doi:10.1046/j.1365-2583.2002.00343.x

Yokoyama, V. Y. (2014a). Olive fruit fly adult response to attract-and-kill bait stations in greenhouse cages with weathered bait spray and a commercial table olive orchard. Journal of Asia-Pacific Entomology, 17(4), 717-721. doi:10.1016/j.aspen.2014.07.004

Yokoyama, V. Y. (2014b). Response of Olive Fruit Fly (Diptera: Tephritidae) to an Attract-and-Kill Trap in Greenhouse Cage Tests. 14(250). doi:10.1093/jisesa/ieu112

Yousef, M., Garrido-Jurado, I., Ruíz-Torres, M., Quesada-Moraga, E. (2016). Reduction of adult olive fruit fly populations by targeting preimaginals in the soil with the entomopathogenic fungus Metarhizium brunneum. Journal of Pest Science, 1-10. doi:10.1007/s10340-016-0779-y

Zygouridis, N. E., Argov, Y., Nemny-Lavy, E., Augustinos, A. A., Nestel, D., Mathiopoulos, K. D. (2014). Genetic changes during laboratory domestication of an olive fly SIT strain. Journal of Applied Entomology, 138(6), 423-432. doi:10.1111/jen.12042



24. 01. 2017



Agronomy section

How to Cite

Hladnik, M. (2017). A review of plant protection against the olive fly (Bactrocera oleae (Rossi, 1790) Gmelin) and molecular methods to monitor the insecticide resistance alleles. Acta Agriculturae Slovenica, 109(1), 135-146. https://doi.org/10.14720/aas.2017.109.1.13

Similar Articles

1-10 of 971

You may also start an advanced similarity search for this article.