Akdeniz meyve sineği Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae)’yı kontrol etmek için yerel entomopatojen nematodların uygulanması

Öz

Akdeniz meyve sineği, Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae), dünyanın en tahripkar meyve zararlılarından biridir. Ceratitis capitata toprakta pupa olur ve bu durum onu entomopatojen nematodlar (EPN) gibi toprak kökenli birçok patojenin hedefi haline getirir. Entomopatojen nematodlar birçok önemli zararlı için oldukça öldürücü, hedef dışı organizmalar içinse güvenlidir ve C. capitata’yı kontrol etmek için iyi bir alternatif olabilirler. Bu çalışmada, dört yerel EPN türü; Steinernema affine Bovien, 1937, Steinernema carpocapsae Weiser, 1955, Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae) ve Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae)’nın C. capitata’nın üçüncü dönem larvalarına ve pupalarına karşı etkinlikleri değerlendirilmiştir. Çalışma 2019-2020 yıllarında hem laboratuvarda (plastik kaplarda) hem de iklim odasında (plastik saksılarda ahşap kafeslerde) sırası ile 100 ve 200 IJs/larva-pupa ile 7.650 ve 15.300 IJs/saksı dozunda yürütülmüştür. Çalışmada EPN’lere karşı C. capitata’nın larvalarının pupalarından daha duyarlı olduğu bulunmuştur. Zararlı larva ve pupalara karşı en yüksek etkinliği S. feltiae 113 ve H. bacteriophora 12 izolatları gösterirken, S. affine 47 izolatı en düşük etkinliği göstermiştir. Entomopatojen nematodlar tarafından C. capitata popülasyonunun baskılanması, bu EPN’lerin zararlının kontrolü için potansiyel olarak faydalı biyolojik mücadele etmenleri olarak kabul edilebileceğini göstermektedir. İleride yapılacak arazi çalışmaları ile desteklendikten sonra bu iki yerel EPN izolatı, C. capitata’ya karşı ümit var çevre dostu biyolojik etmenler olarak kullanılabilir.

Anahtar Kelimeler

• Biyolojik kontrol
• Ceratitis capitata
• etkinlik
• entomopatojen nematodlar
• yerel izolatlar

Implementing local entomopathogenic nematodes to control Mediterranean fruit fly Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae)

Öz

The Mediterranean fruit fly, Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae), is one of the world’s most destructive fruit pests. Ceratitis capitata pupates in the soil, making it a target of many soilborne pathogens like entomopathogenic nematodes (EPNs). Entomopathogenic nematodes are highly lethal to many important pests, safe to non-target organisms and they might be good alternatives for control of C. capitata. In this study, the efficacy of four local EPN species; Steinernema affine Bovien, 1937, Steinernema carpocapsae Weiser, 1955, Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae) and Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) against the third instar larvae and pupae of C. capitata were evaluated. The study was conducted in 2019-2020 both in the laboratory (in plastic cups) and in a climate room (in wooden cages with plastic pots) at doses of 100 and 200 IJs/larva-pupa and 7,650 and 15,300 IJs/pot, respectively. Larvae of C. capitata were found more susceptible to EPNs than pupae in the study. Steinernema feltiae isolate 113 and H. bacteriophora isolate 12 showed the highest efficacy while S. affine isolate 47 showed the least efficacy against the pest larvae and pupae. Suppression of C. capitata population by EPNs indicates that these EPNs can be considered as a biological control agent potentially useful for the control of this pest. After further support by field studies, these two local EPN isolates could be used as promising eco-friendly biological agents against C. capitata.

Anahtar Kelimeler

• Biological control
• Ceratitis capitata
• efficacy
• entomopathogenic nematodes
• local isolates

Kaynakça

1. Abbott, W. S., 1925. Method of computing the effectiveness of insecticides. Journal of Economic Entomology, 18 (2): 265-267.
2. Anonymous, 2013. Bitki Pasaportu İçin Bitki Sağlığı Rehberi. Gıda ve Kontrol Genel Müdürlüğü, Bitki Sağlığı ve Karantina Daire Başkanlığı, Ankara, 260 s. (in Turkish).
3. Belair, G., Y. Fournier & N. Dauphinais, 2003. Efficacy of steinernematid nematodes against three insect pests of crucifers in Quebec. The Journal of Nematology, 35 (3): 259-265.
4. Bode, H. B. 2009. Entomopathogenic bacteria as a source of secondary metabolites. Current Opinion in Chemical Biology, 13 (2): 224-230.
5. Boemare, N., 2002. “Biology, taxonomy and systematics of Photorhabdus and Xenorhabdus, 35-57”. In: Entomopathogenic Nematology (Ed. R. Gaugler). CABI Publishing, Wallingford, 372 pp.
6. Chergui, S., A. Benzehra, K. Boudjemaa, H. Barkou & I. Karaca, 2019. Efficacy of Turkish isolate of Steinernema feltiae (Rhabditida: Steinernematidae) in controlling the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), under laboratory conditions. Egyptian Journal of Biological Pest Control, 29 (60): 1-7.
7. Dillman, A. R., J. M. Chaston, B. J. Adams, T. A. Ciche, H. Goodrich-Blair, S. P. Stock & P. W. Sternberg, 2012. An entomopathogenic nematode by any other name. PLoS Pathogens, 8 (3): e1002527.
8. Forschler, B. T., J. N. All & W. A. Gardner, 1990. Steinernema feltiae activity and infectivity in response to herbicide exposure in aqueous and soil environments. Journal of Invertebrate Pathology, 55 (3): 375-379.

9. Gazit, Y., Y. Rossler & I. Glazer, 2000. Evaluation of entomopathogenic nematodes for the control of Mediterranean fruit fly (Diptera: Tephritidae). Biocontrol Science and Technology, 10 (2): 157-164.
10. Genc, H., 2008. Modified agar-based diet for laboratory rearing of Olive fruit fly Bactrocera oleae Gmelin (Diptera: Tephritidae). Florida Entomologist, 9 (4): 651-656.
11. Genc, H. & S. Yücel, 2017. Determination of host preferences of Medfly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), in the laboratory. Turkish Journal of Agricultural and Natural Sciences, 4 (3): 292-301.
12. Georgis, R. 1990. “Formulation and application technology, 173-191”. In: Entomopathogenic nematodes in biological control (Eds. R. Gaugler & H. K. Kaya) Boca Raton, CRC Press, 381 pp.
13. Glazer, I., 1992. Survival and efficacy of Steinernema carpocapsae in an exposed environment. Biocontrol Science and Technology, 2 (2): 101-107.
14. Gözel, C. & U. Gözel, 2019. The efficacy of native entomopathogenic nematodes against the pine processionary moth, Thaumetopoea pityocampa Den. & Schiff. (Lepidoptera: Thaumetopoeidae). Turkish Journal of Biological Control, 10 (2): 118-126.
15. Gözel, C. & İ. Kasap, 2015. Efficacy of entomopathogenic nematodes against the Tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato field. Turkish Journal of Entomology, 39 (3): 229-237.
16. Grewal, P. S., R. U. Ehlers & D. I. Shapiro-Ilan, 2005. Nematodes as Biological Control Agents. CABI Publishing, Wallingford, England, UK, 505 pp.
17. Griffin, C. T., N. E. Boemare & E. E. Lewis, 2005. “Biology and Behaviour, 47-64”. In: Nematodes as Biocontrol Agents (Eds. P. S. Greval, U. R. Ehlers & D.I. Shapiro-Ilan). CABI Publishing, Wallingford, 505 pp.
18. Harbi, A., B. Sabater-Muñoz, F. Beitia & B. Chermiti, 2018. Biological control of Ceratitis capitata (Diptera: Tephritidae) in Tunisia: Introduction and potential establishment of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) in Tunisian citrus orchards. Integrated Control in Citrus Fruit Crops IOBC-WPRS Bulletin, 132 : 142-149.
19. Head, J., A. J. Lawrence & K. F. A. Walters, 2004. Efficacy of the entomopathogenic nematode, Steinernema feltiae, against Bemisia tabaci in relation to plant species. Journal of Applied Entomology, 128 (8): 543-547.
20. Hendrichs, J., A. S. Robinson, J. P. Cayol & W. Enkerlin, 2002. Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: The importance of mating behavior studies. Florida Entomologist, 85 (1): 1-13.
21. Karagöz, M., B. Gülcü, C. Hazır, H. K. Kaya & S. Hazır, 2009. Biological control potential of Turkish entomopathogenic nematodes against the Mediterranean fruit fly Ceratitis capitata. Phytoparasitica, 37 (2): 153-159.
22. Katsoyannos, B. I., R. R. Heath, N. T. Papadopoulos, N. D. Epsky & J. Hendrichs, 1999. Field evaluation of Mediterranean fruit fly (Diptera: Tephritidae) female selective attractants for use in monitoring programs. Journal of Economic Entomology, 92 (3): 583-589.
23. Kaya, H. K. & R. Gaugler, 1993. Entomopathogenic nematodes. Annual Review of Entomology, 38 (1): 181-206.
24. Kaya, H. K. & S. P. Stock, 1997. “Techniques in Insect Nematology, 281-324”. In: Manual of Techniques in Insect Pathology (Eds. L. A. Lacey). Biological Techniques Series, Academic Press, San Diego, California, 409 pp.
25. Kepenekçi, I. & A. Susurluk, 2006. Infectivity of two Turkish isolates of Steinernema feltiae (Rhabditida: Steinernematidae) against Rhagoletis cerasi and Ceratitis capitata. Nematologia Mediterranea, 34 (1): 95-97.
26. Koppenhöfer, A. M., 2007. “Nematodes 249-264”. In: Field Manual of Techniques in Invertebrate Pathology Application and Evaluation of Pathogens for Control of Insects and Other Invertebrate Pests (Eds. L. A. Lacey & H. K. Kaya). New York City, Springer, 868.
27. Laborda, R., L. Bargues, C. Navarro, O. Barajas, M. Arroyo, E. M. Garcia, E. Montoro, E. Lopis, A. Martinez & J. M. Sayagues, 2003. Susceptibility of the mediterranean fruit Ceratitis capitata) to entomopathogenic nematode Steinernema spp. ("Biorend C"). Bulletin OILB/SROP 26 (6): 95-97.
28. Lacey, L. A., D. Grzywacz, D. I. Shapiro-Ilan, R. Frutos, M. Brownbridge & M. S. Goettel, 2015. Insect pathogens as biological control agents: Back to the future Journal of Invertebrate Pathology, 132 : 1-41.
29. Lacey, L. A., D. I. Shapiro-Ilan & G. M. Glenn, 2010. Post application of antidesiccant agents improves efficacy of entomopathogenic nematodes in formulated host cadavers or aqueous suspension against diapausing codling moth larvae (Lepidoptera: Tortricidae). Biocontrol Science and Technology, 20 (9): 909-921.
30. Lindengren, J. E., 1990. “Field suppression of three fruit fly species (Diptera: Tephritidae) with Steinernema carpocapsae”. Vth International Colloquium on Invertebrate Pathology and Microbial Control (20-24 August 1990, Adelaide, Australia), 223 pp.
31. Liquido, N. J., L. A. Shinoda & R. T. Cunningham, 1991. Host Plants of the Mediterranean Fruit Fly (Diptera: Tephritidae) an Annotated World Review. Entomological Society of America, Miscellaneous Publications, 52 pp.
32. Lu, D., M. Macchietto, D. Chang, M. M. Barros, J. Baldwin & A. Mortazavi, 2017. Activated entomopathogenic nematode infective juveniles release lethal venom proteins. PLoS Pathogens, 13 (4): e1006302.
33. Magaña, C., P. Hernandez-Crespo, F. Ortego & P. Castañera, 2007. Resistance to malathion in field populations of Ceratitis capitata. Journal of Economic Entomology, 100 (6): 1836-1843.
34. Malan, A. P. & A. Manrakhan, 2009. Susceptibility of the Mediterranean fruit fly (Ceratitis capitata) and the natal fruit fly (Ceratitis rosa) to entomopathogenic nematodes. Journal of Invertebrate Pathology, 100 (1): 47-49.
35. Minas, R. S., R. M. Souza, C. Dolinski, R. S. Carvalho & R. S. Burla, 2016. Potential of entomopathogenic nematodes (Rhabditida: Heterorhabditidae) to control Mediterranean fruit fly (Diptera: Tephritidae) soil stages. Nematoda, 2016 (3): e02016.
36. Mokrini, F., S. E. Laasli, Y. Benseddik, A. B. Joutei, A. Blenzar, H. Lakhal, M. Sbaghi, M. Imren, G. Özer, T. Paulitz, R. Lahlali & A. A. Dababat, 2020. Potential of Moroccan entomopathogenic nematodes for the control of the Mediterranean fruit fly Ceratitis capitata Wiedemann (Diptera: Tephritidae). Scientific Reports, 10 (1): 19204.
37. Montoya, P., J. Cancino, M. Zenil, E. Gómez & A. Villaseñor, 2005. Parasitoid releases in the control of Ceratitis capitata (Diptera: Tephritidae) outbreaks, in coffee growing zones of Chiapas, Mexico. Vedalia, 12 (1): 85-89.
38. Navarro-Llopis, V., F. Alfaro, J. Dominguez, J. Sanchis & J. Primo, 2008. Evaluation of traps and lures for mass trapping of Mediterranean fruit fly in citrus groves. Journal of Economic Entomology, 101 (1): 126-131.
39. Nouh, G. M. & M. A. Hussein, 2014. The role of entomopathogenic nematodes as biocontrol agents against some tephritid flies. Advances in Biological Research, 8 (6): 301-306.
40. Papadopoulos, N. T., B. I. Katsoyannos, J. R. Carey, 1998. Temporal changes in the composition of the overwintering larval population of the Mediterranean fruit flies (Dipt., Tephritidae) in Northern Greece. Entomological Society of America, 91 (4): 430-434.
41. Rohde, C., A. M. Junior, F. D. Carvalho, M. A. T. da Silva, 2012. Selection of entomopathogenic nematodes for the control of the fruit fly Ceratitis capitata (Diptera: Tephritidae). Revista Brasileira de Ciências Agrárias, 7 : 797-802.
42. Rohde, C., A. M. Junior, M. A. T. Silva, F. D. Carvalho & C. S. Ferreira, 2010. Influence of soil temperature and moisture on the infectivity of entomopathogenic nematodes (Rhabditida: Heterorhabiditidae e Steinernematidae) against larvae of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Neotropical Entomology, 39 (4): 608611.
43. Rovesti, L. & K. V. Deseo 1991. Compatibility of pesticides with the entomopathogenic nematode, Heterorhabditis heliothidis. Nematologica, 37 (1): 113-116.
44. Satar, S., G. Tiring, D. İşpınar & A. R. Algan, 2016. Population fluctuation of Ceratitis capitata Wied. (Diptera: Tephritidae) in grapefruit orchards and effect of temperature on its development. Plant Protection Bulletin, 56 (4): 429-440.
45. Shapiro-Ilan, D. I., T. E. Cottrell, R. F. Mizell, D. L. Horton, B. Behle & C. Dunlap, 2010. Efficacy of Steinernema carpocapsae for control of the lesser peach tree borer, Synanthedon pictipes: Improved aboveground suppression with a novel gel application. Biological Control, 54 (1): 23-28.
46. Smart, Jr. G. C., 1995. Entomopathogenic nematodes for the biological control of insects. Journal of Nematology, 27 (4S): 529-534.
47. Toledo, J., J. E. Ibarra, P. Liedo, A. Gómez, M. A. Rasgado & T. Willians, 2005. Infection of Anastrepha ludens (Diptera: Tephritidae) larvae by Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) under laboratory and field conditions. Biocontrol Science and Technology, 15 (6): 627-634.
48. Tsitsipis, J. A. & A. Kontos, 1983. Improved solid adult diet for the olive fruit fly Dacus oleae. Entomologia Hellenica, 1: 24-29.
49. Tzanakakis, M. E., 1989. “Small Scale Rearing, 105-118”. In: Fruit Flies: Their Biology, Natural Enemies and Control (Eds. A. S. Robinson & G. Hooper). Vol 3B. Amsterdam, the Netherlands: Elsevier, 447 pp.
50. White, G. F., 1927. A method for obtaining infective nematode larvae from culture. Science, 66 (1709): 302-303.
51. Yee, W. L. & L. A. Lacey, 2003. Stage-specific mortality of Rhagoletis indifferens (Diptera: Tephritidae) exposed to three species of Steinernema nematodes. Biological Control, 27 (3): 349-356.
52. Zucchi, R. A., 2001. “Mosca-do-mediterrâneo, Ceratitis capitata (Diptera: Tephritidae), 15-22”. In: Historico e Impacto das Pragas Introdusidaz no Brasil (Eds. E. F. Vilela, R. A. Zucchi & F. Cantor). Ribeirão Preto, 173 pp.