Research Article

Contact effects of sulfoxaflor, spirotetramat and flonicamid on key natural enemies in citrus orchards

Volume: 10 Number: 3 September 25, 2026

Contact effects of sulfoxaflor, spirotetramat and flonicamid on key natural enemies in citrus orchards

Abstract

Türkiye is one of the most important citrus producers, where red scale, Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae), and citrus mealybug, Planococcus citri Risso (Hemiptera: Pseudococcidae), cause significant quality and yield losses. This study evaluated the contact effects of sulfoxaflor 240 g/L (15 and 20 ml/da), spirotetramat 100 g/L (75 and 100 ml/da) and flonicamid 500 g/kg (15 g/da) on the larvae, pupae, adults and eggs of the predator Chilocorus bipustulatus (L.) (Coleoptera: Coccinellidae), and on the adults of the parasitoids Leptomastix dactylopii Howard and Anagyrus pseudococci Girault (Hymenoptera: Encyrtidae), key natural enemies of P. citri, and Aphytis melinus DeBach (Hymenoptera: Aphelinidae), a key parasitoid of A. aurantii. Laboratory bioassays followed the IOBC dry-film method in a randomized complete block design with six treatments (including an untreated control) and four independent replications at 25 ± 1 °C, 65 ± 5% relative humidity and a 16/8 h light/dark photoperiod, and were complemented by semi-field cage experiments on potted orange seedlings in an uncultivated greenhouse. Corrected mortality was classified according to the rating scale of the International Organisation for Biological Control (IOBC), the laboratory scale being applied to the laboratory bioassays and the separate semi-field scale to the cage experiments. All products tested were harmless (class 1) or only slightly harmful (class 2) to the different biological stages of C. bipustulatus, with mean corrected mortality never exceeding 71%. In contrast, both doses of sulfoxaflor caused 100% mortality of all three parasitoid species under laboratory conditions and were rated harmful (class 4), whereas the lower dose of spirotetramat was harmless (class 1) to A. pseudococci adults and flonicamid was harmless (class 1) to L. dactylopii adults. Flonicamid was moderately harmful (class 3) to A. pseudococci adults in the laboratory and harmful (class 4) under semi-field conditions. Selectivity was therefore species-, dose- and exposure-dependent: sulfoxaflor was of low toxicity to C. bipustulatus but harmful to all three parasitoids in the laboratory; spirotetramat, particularly at the lower dose, was harmless or slightly harmful to A. pseudococci but slightly to moderately harmful to L. dactylopii; and flonicamid differed sharply between the two parasitoids of P. citri. Recommendations for the use of these insecticides in integrated pest management should therefore take account of the natural enemy species present. 

Keywords

Biological control, Citrus, Integrated pest management, IOBC, Natural enemies, Pesticide selectivity

Thanks

The authors thank the Western Mediterranean Agricultural Research Institute (BATEM) and Koppert Biyolojik Mücadele ve Polinasyon Sistemleri Ltd. Şti. for supplying the parasitoid material, and the Department of Plant Protection, Faculty of Agriculture, Süleyman Demirel University, for providing the starter culture of Chilocorus bipustulatus.

References

  1. Akgün, C. (2006). Turunçgiller sektör profili [Citrus sector profile]. İstanbul Chamber of Commerce, Foreign Trade Branch. http://www.ito.org.tr/Dokuman/Sektor/1-97.pdf
  2. Amano, H., & Haseeb, M. (2001). Recently-proposed methods and concepts of testing the effects of pesticides on the beneficial mite and insect species: Study limitations and implications in IPM. Applied Entomology and Zoology, 36(1), 1–11. https://doi.org/10.1303/aez.2001.1
  3. Battaglia, D., & Viggiani, G. (1982). Osservazioni sulla distribuzione e sulla fenologia di Aonidiella aurantii (Mask.) (Homoptera: Diaspididae) e dei suoi nemici naturali in Campania. Annali della Facoltà di Scienze Agrarie della Università degli Studi di Napoli, Portici, Serie 4, 16, 125–132.
  4. Ben-Dov, Y., & Rosen, D. (1969). Efficacy of natural enemies of the California red scale on citrus in Israel. Journal of Economic Entomology, 62(5), 1057–1060. https://doi.org/10.1093/jee/62.5.1057
  5. Bernardo, U., & Viggiani, G. (2000). Effects of spinosad, a new naturally derived insect control agent, on the mealybug parasitoid Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae). IOBC/WPRS Bulletin, 23, 81–84.
  6. Cloyd, R. A., & Dickinson, A. (2006). Effect of insecticides on mealybug destroyer (Coleoptera: Coccinellidae) and parasitoid Leptomastix dactylopii (Hymenoptera: Encyrtidae), natural enemies of citrus mealybug (Homoptera: Pseudococcidae). Journal of Economic Entomology, 99(5), 1596–1604. https://doi.org/10.1093/jee/99.5.1596
  7. DeBach, P. (1969). Biological control of diaspine scale insects on citrus in California. Proceedings of the First International Citrus Symposium, 2, 801–815.
  8. DeBach, P., & White, E. B. (1960). Commercial mass culture of the California red scale parasite Aphytis lingnanensis (Bulletin No. 770). California Agricultural Experiment Station.
  9. El Ammari, M., Ziri, R., El Bahja, F., Hamrani, M., Boukita, H., Brhadda, N., Bouzakraoui, S., & Fahad, K. (2024). Biological control of citrus pests: A systematic bibliometric analysis 2000–2023. Journal of Agriculture and Food Research, 18, 101492. https://doi.org/10.1016/j.jafr.2024.101492
  10. Erkılıç, L., Uygun, N., Aytaş, M., Tekeli, N., & Karaca, İ. (1994). Bazı tarımsal savaş ilaçlarının Chilocorus bipustulatus L. (Coleoptera: Coccinellidae) ve Cybocephalus fodori minor (Coleoptera: Coccinellidae)'a etkileri üzerinde araştırmalar [Studies on the effects of some pesticides on Chilocorus bipustulatus L. and Cybocephalus fodori minor]. In Proceedings of the 3rd Turkish Biological Control Congress, 25–28 January 1994, İzmir, Türkiye (pp. 471–480).
APA
Maral, H., Civelek, H. S., & Ulusoy, M. R. (2026). Contact effects of sulfoxaflor, spirotetramat and flonicamid on key natural enemies in citrus orchards. International Journal of Agriculture Environment and Food Sciences, 10(3), 791-801. https://doi.org/10.31015/jaefs.2026.3.27
AMA
1.Maral H, Civelek HS, Ulusoy MR. Contact effects of sulfoxaflor, spirotetramat and flonicamid on key natural enemies in citrus orchards. int. j. agric. environ. food sci. 2026;10(3):791-801. doi:10.31015/jaefs.2026.3.27
Chicago
Maral, Hasan, Hasan Sungur Civelek, and Mehmet Rifat Ulusoy. 2026. “Contact Effects of Sulfoxaflor, Spirotetramat and Flonicamid on Key Natural Enemies in Citrus Orchards”. International Journal of Agriculture Environment and Food Sciences 10 (3): 791-801. https://doi.org/10.31015/jaefs.2026.3.27.
EndNote
Maral H, Civelek HS, Ulusoy MR (September 1, 2026) Contact effects of sulfoxaflor, spirotetramat and flonicamid on key natural enemies in citrus orchards. International Journal of Agriculture Environment and Food Sciences 10 3 791–801.
IEEE
[1]H. Maral, H. S. Civelek, and M. R. Ulusoy, “Contact effects of sulfoxaflor, spirotetramat and flonicamid on key natural enemies in citrus orchards”, int. j. agric. environ. food sci., vol. 10, no. 3, pp. 791–801, Sept. 2026, doi: 10.31015/jaefs.2026.3.27.
ISNAD
Maral, Hasan - Civelek, Hasan Sungur - Ulusoy, Mehmet Rifat. “Contact Effects of Sulfoxaflor, Spirotetramat and Flonicamid on Key Natural Enemies in Citrus Orchards”. International Journal of Agriculture Environment and Food Sciences 10/3 (September 1, 2026): 791-801. https://doi.org/10.31015/jaefs.2026.3.27.
JAMA
1.Maral H, Civelek HS, Ulusoy MR. Contact effects of sulfoxaflor, spirotetramat and flonicamid on key natural enemies in citrus orchards. int. j. agric. environ. food sci. 2026;10:791–801.
MLA
Maral, Hasan, et al. “Contact Effects of Sulfoxaflor, Spirotetramat and Flonicamid on Key Natural Enemies in Citrus Orchards”. International Journal of Agriculture Environment and Food Sciences, vol. 10, no. 3, Sept. 2026, pp. 791-0, doi:10.31015/jaefs.2026.3.27.
Vancouver
1.Hasan Maral, Hasan Sungur Civelek, Mehmet Rifat Ulusoy. Contact effects of sulfoxaflor, spirotetramat and flonicamid on key natural enemies in citrus orchards. int. j. agric. environ. food sci. 2026 Sep. 1;10(3):791-80. doi:10.31015/jaefs.2026.3.27