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Moroccan entomopathogenic nematodes for sustainable control of Dactylopius opuntiae
Nematodos entomopatógenos marroquíes para el control sostenible de Dactylopius opuntiae
DOI:
https://doi.org/10.15446/abc.v31n2.122217Palabras clave:
Biopesticides, Cactaceae, Host–pathogen interactions, Infective juveniles, Integrated pest management (en)Bioplaguicidas, Cactáceas, Interacciones huésped–patógeno, Juveniles infectivos, Manejo integrado de plagas (es)
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Dactylopius opuntiae (carmine cochineal) is an invasive insect that damages cactus pear crops in Morocco. This study evaluated the laboratory pathogenicity of Moroccan strains of two entomopathogenic nematodes (Steinernema feltiae SF-MA1 and Heterorhabditis bacteriophora HB-MA2) against adult females of D. opuntiae. The experiments included five concentrations of infective juveniles (100, 200, 400, 600, and 800 juveniles per milliliter) and three temperatures (20, 25, and 30 °C). Mortality was assessed from 24 to 120 h and corrected using Abbott’s formula. The data were analyzed using two-way analysis of variance, probit regression, and response surface analysis. Mortality varied with nematode species, concentration, exposure time, and temperature. Overall, mortality increased with concentration and exposure time, and the dose–temperature interaction additionally determined nematode efficacy. H. bacteriophora achieved its highest mortality and lowest median lethal concentration at 25 °C, whereas S. feltiae was most effective at 20 °C. Response surface analysis identified combinations of moderate temperatures and high doses that maximized mortality. These findings indicated that locally adapted entomopathogenic nematodes may be promising candidates for D. opuntiae control. However, semi-field and field experiments are required to validate their use in cactus pear orchards.
La cochinilla carmín, Dactylopius opuntiae, es una plaga invasora que afecta la producción de nopal en Marruecos. Este estudio evaluó, en condiciones de laboratorio, la patogenicidad de dos cepas marroquíes de nematodos entomopatógenos, Steinernema feltiae SF-MA1 y Heterorhabditis bacteriophora HB-MA2, contra hembras adultas de D. opuntiae. Los bioensayos combinaron cinco concentraciones de juveniles infectivos (100, 200, 400, 600 y 800 juveniles por mililitro) con tres temperaturas (20, 25 y 30 °C), y la mortalidad se registró entre 24 y 120 h. Los datos se analizaron mediante análisis de varianza de dos vías, regresión probit y análisis de superficie de respuesta. La mortalidad varió según la especie de nematodo, la concentración, el tiempo de exposición y la temperatura. H. bacteriophora alcanzó su mayor mortalidad y su menor concentración letal media a 25 °C, mientras que S. feltiae fue más eficaz a 20 °C. El análisis de superficie de respuesta identificó combinaciones de temperaturas moderadas y dosis elevadas que maximizaron la mortalidad. Estos resultados indicaron que los nematodos adaptados localmente pueden ser candidatos prometedores contra D. opuntiae. Sin embargo, se requieren ensayos semicontrolados y de campo antes de proponer recomendaciones agronómicas definitivas.
Referencias
Abbott, W. S. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18(2), 265–267. https://doi.org/10.1093/jee/18.2.265a
Bouharroud, R., Amarraque, A. and Qessaoui, R. (2016). First report of the Opuntia cochineal scale Dactylopius opuntiae (Hemiptera: Dactylopiidae) in Morocco. EPPO Bulletin, 46(2), 308–310. https://doi.org/10.1111/epp.12298
Bouharroud, R., Sbaghi, M., Boujghagh, M. and El Bouhssini, M. (2018). Biological control of the prickly pear cochineal Dactylopius opuntiae Cockerell (Hemiptera: Dactylopiidae). EPPO Bulletin, 48(2), 300–306. https://doi.org/10.1111/epp.12471
Bouharroud, R., El Aalaoui, M., Boujghagh, M., Hilali, L., El Bouhssini, M. and Sbaghi, M. (2019). New record and predatory activity of Hyperaspis campestris (Herbst 1783) (Coleoptera: Coccinellidae) on Dactylopius opuntiae (Cockerell) in Morocco. Entomological News, 128(2), 156–160. https://doi.org/10.3157/021.128.0202
Bouharroud, R., Chafiki, S., Qessaoui, R., Imlil, Y., Bargach, J., Derhem, A. and Elaini, R. (2025). Differential impact of temperature, release rate, prey density, and pesticides on Hyperaspis trifurcata (Coleoptera: Coccinellidae) to optimize integrated management of Dactylopius opuntiae (Hemiptera: Dactylopiidae). Plants, 14(7), 1129. https://doi.org/10.3390/plants14071129
CABI. (2021). Dactylopius opuntiae (prickly pear cochineal). CABI Compendium. https://doi.org/10.1079/cabicompendium.17659
Campos-Herrera, R. (Ed.). (2015). Nematode pathogenesis of insects and other pests: Ecology and applied technologies for sustainable plant and crop protection. Springer. https://doi.org/10.1007/978-3-319-18266-7
Dillman, A. R. and Sternberg, P. W. (2012). Entomopathogenic nematodes. Current Biology, 22(11), R430–R431. https://doi.org/10.1016/j.cub.2012.03.047
El Aalaoui, M., Bouharroud, R., Sbaghi, M., Boujghagh, M. and El Bouhssini, M. (2019). Natural enemies associated with Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae) in Morocco and their population fluctuations. Revue Marocaine des Sciences Agronomiques et Vétérinaires, 7(3), 391–396.
El Aalaoui, M., Bouharroud, R., Sbaghi, M., El Bouhssini, M. and Hilali, L. (2020). Seasonal biology of Dactylopius opuntiae (Hemiptera: Dactylopiidae) on Opuntia ficus-indica (Caryophyllales: Cactaceae) under field and semi-field conditions. Ponte, 76(1/1), 259–271. https://doi.org/10.21506/j.ponte.2020.1.17
El Aalaoui, M., Mokrini, F., Dababat, A. A., Lahlali, R. and Sbaghi, M. (2022). Moroccan entomopathogenic nematodes as potential biocontrol agents against Dactylopius opuntiae (Hemiptera: Dactylopiidae). Scientific Reports, 12, 7590. https://doi.org/10.1038/s41598-022-11709-4
El Aalaoui, M., Rammali, S. and Sbaghi, M. (2024). Biological control of Dactylopius opuntiae (Cockerell) using entomopathogenic fungi in Morocco. Biocontrol Science and Technology, 34(11), 1068–1089. https://doi.org/10.1080/09583157.2024.2405154
El Aalaoui, M., Rammali, S., Kamal, F. Z., Ciobica, A., Albert, C., Burlui, V., Novac, B., Bencharki, B. and Sbaghi, M. (2025). Integrated field control of Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae) in Opuntia spp. using biorational methods. Frontiers in Microbiology, 16, 1714087. https://doi.org/10.3389/fmicb.2025.1714087
El Fakhouri, K., Ramdani, C., Aasfar, A., Boulamtat, R., Sijilmassi, B., El Bouhssini, M. and Kadmiri, I. M. (2023). Isolation, identification and pathogenicity of local entomopathogenic bacteria as biological control agents against the wild cochineal Dactylopius opuntiae (Cockerell) on cactus pear in Morocco. Scientific Reports, 13, 21647. https://doi.org/10.1038/s41598-023-48976-8
El Fakhouri, K., Ramdani, C., Boulamtat, R., Sobeh, M., Taarji, N., Kadmiri, I. M. and El Bouhssini, M. (2025). Natural product-based biopesticides for sustainable control of the wild cochineal Dactylopius opuntiae (Hemiptera: Dactylopiidae) in Morocco. Acta Horticulturae, 1422, 371–382. https://doi.org/10.17660/ActaHortic.2025.1422.45
Fallet, P., Bazagwira, D., Ruzzante, L., Ingabire, G., Levivier, S., Bustos-Segura, C., Kajuga, J., Toepfer, S. and Turlings, T. C. J. (2024). Entomopathogenic nematodes as an effective and sustainable alternative to control the fall armyworm in Africa. PNAS Nexus, 3(4), pgae122. https://doi.org/10.1093/pnasnexus/pgae122
Finney, D. J. (1971). Probit analysis (3rd ed.). Cambridge University Press.
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5), 294–299.
Glazer, I. and Lewis, E. E. (2000). Bioassays for entomopathogenic nematodes. In A. Navon and K. R. S. Ascher (Eds.), Bioassays of entomopathogenic microbes and nematodes (pp. 229–247). CABI Publishing. https://doi.org/10.1079/9780851994222.0229
Grewal, P. S., Ehlers, R. U. and Shapiro-Ilan, D. I. (Eds.). (2005). Nematodes as biocontrol agents. CABI Publishing. https://doi.org/10.1079/9780851990170.0000
Hazir, S., Kaya, H. K., Stock, S. P. and Keskin, N. (2003). Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turkish Journal of Biology, 27, 181–202.
Kaya, H. K. and Gaugler, R. (1993). Entomopathogenic nematodes. Annual Review of Entomology, 38, 181–206. https://doi.org/10.1146/annurev.en.38.010193.001145
Kaya, H. K. and Stock, S. P. (1997). Techniques in insect nematology. In L. A. Lacey (Ed.), Manual of techniques in insect pathology (pp. 281–324). Academic Press. https://doi.org/10.1016/B978-012432555-5/50016-6
Kim, J., Hiltpold, I., Jaffuel, G., Sbaiti, I., Hibbard, B. E. and Turlings, T. C. J. (2021). Calcium-alginate beads as a formulation for the application of entomopathogenic nematodes to control rootworms. Journal of Pest Science, 94, 1197–1208. https://doi.org/10.1007/s10340-021-01349-4
Labaude, S. and Griffin, C. T. (2018). Transmission success of entomopathogenic nematodes used in pest control. Insects, 9(2), 72. https://doi.org/10.3390/insects9020072
Lacey, L. A. and Georgis, R. (2012). Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology, 44(2), 218–225.
Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M. and Goettel, M. S. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132, 1–41. https://doi.org/10.1016/j.jip.2015.07.009
Lu, D., Baiocchi, T. and Dillman, A. R. (2016). Genomics of entomopathogenic nematodes and implications for pest control. Trends in Parasitology, 32(8), 588–598. https://doi.org/10.1016/j.pt.2016.04.008
Mazzeo, G., Nucifora, S., Russo, A. and Suma, P. (2019). Dactylopius opuntiae, a new prickly pear cactus pest in the Mediterranean: An overview. Entomologia Experimentalis et Applicata, 167(1), 59–72. https://doi.org/10.1111/eea.12756
Mendel, Z., Protasov, A., Golan, O., Bensimon, D., Kolodny, O. and Suma, P. (2024). Navigating challenges in the management of Dactylopius opuntiae (Cockerell): Transitioning from introduction biological control to a preemptive strategy of artificial seeding of a natural enemy. Biological Control, 196, 105582. https://doi.org/10.1016/j.biocontrol.2024.105582
Myers, R. H., Montgomery, D. C. and Anderson-Cook, C. M. (2016). Response surface methodology: Process and product optimization using designed experiments (4th ed.). Wiley.
Palafox-Luna, J. A., Rodríguez-Leyva, E., Lomeli-Flores, J. R., Vigueras-Guzmán, A. L. and Vanegas-Rico, J. M. (2018). Life cycle and fecundity of Dactylopius opuntiae (Hemiptera: Dactylopiidae) in Opuntia ficus-indica (Caryophyllales: Cactaceae). Agrociencia, 52(1), 103–114.
Peterson, R. K. D. (2025). Insect pest management and environmental risk. Annual Review of Entomology, 70, 103–121. https://doi.org/10.1146/annurev-ento-121123-021252
Ramakuwela, T., Tarasco, E., Chavarría-Hernández, N. and Toepfer, S. (2025). Entomopathogenic nematodes: Commercial use and future perspectives. Journal of Invertebrate Pathology, 212, 108388. https://doi.org/10.1016/j.jip.2025.108388
Ramdani, C., Bouharroud, R., Sbaghi, M., Mesfioui, A. and El Bouhssini, M. (2021). Field and laboratory evaluations of different botanical insecticides for the control of Dactylopius opuntiae (Cockerell) on cactus pear in Morocco. International Journal of Tropical Insect Science, 41, 1623–1632. https://doi.org/10.1007/s42690-020-00363-w
Ramdani, C., El-Fakhouri, K., Boulamtat, R., Bouharroud, R., Mesfioui, A., Al-Jboory, I. and El Bouhssini, M. (2022). Entomopathogenic fungi as biological control agents of Dactylopius opuntiae (Hemiptera: Dactylopiidae) under laboratory and greenhouse conditions. Frontiers in Sustainable Food Systems, 6, 997254. https://doi.org/10.3389/fsufs.2022.997254
Rasmann, S., Köllner, T. G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J. and Turlings, T. C. J. (2005). Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature, 434, 732–737. https://doi.org/10.1038/nature03451
Sabbahi, R. and Hock, V. (2022). Control of the prickly pear cochineal, Dactylopius opuntiae (Cockerell), in Morocco: An overview. Journal of Plant Diseases and Protection, 129, 1323–1330. https://doi.org/10.1007/s41348-022-00655-y
Shapiro-Ilan, D. I., Gouge, D. H., Piggott, S. J. and Fife, J. P. (2006). Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biological Control, 38(1), 124–133. https://doi.org/10.1016/j.biocontrol.2005.09.005
White, G. F. (1927). A method for obtaining infective nematode larvae from cultures. Science, 66(1709), 302–303. https://doi.org/10.1126/science.66.1709.302-a
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