Rhyzopertha dominica erginlerinin Beauveria bassiana konidisporları uygulanan buğday tanelerine davranışsal tepkisi ve ölüm oranı

Öz

Bu çalışma, zararlı hareketi ve ölüm oranı belirlenerek Rhyzopertha dominica erginlerinin Beauveria bassiana sporu uygulanmış buğday tanelerine olan tepkisini incelemek amacıyla yürütülmüştür. Zararlının inaktive edilmiş B. bassiana sporlarına tepkileri de ayrıca test edilmiştir. Her deney ünitesi R. dominica erginlerinin bölmeler arasında geçişinin kısıtlanmadığı iki eşit bölmeden oluşmuştur. Bölmelere spor uygulanmış veya spor uygulanmamış buğday taneleri doldurularak farklı düzenekler oluşturulmuştur. Fungus uygulamalarında aktif veya inaktive edilmiş B. bassiana konidileri kullanılmıştır. R. dominica ergin salımlarının sadece bir bölmeye veya her iki bölmeye yapıldığı iki deneme kurulmuştur. Deneme sonunda böceklerin dağılımı ve ölüm oranları kaydedilmiştir. R. dominica erginleri, B. bassiana sporlarının varlığına karşı belirgin bir kaçınma davranışı sergilemiş ve toplam ölüm oranı %95,00'ten %68,75'e düşmüştür. R. dominica erginleri inaktive edilmiş B. bassiana sporlarına da aynı tepkiyi göstermiş olup aktif ve inaktif sporlar arasında ayrım yapmamışlardır. B. bassiana uygulamasının başarısına zararlı davranışının etkisi kullanım stratejisine bağlı olarak değişebilir: temiz alanlarda toplanma nedeniyle homojen olmayan dağılımlar etkinlikte düşüşe neden olabilecekken, fungusun repellent özelliği zararlının bulaşmasını engelleme açısından avantaj sağlayabilecektir.

Anahtar Kelimeler

• Böcek davranışı
• Kaçınma
• Biyolojik mücadele
• Entomopatojen fungus

Behavioral response of Rhyzopertha dominica adults to wheat kernels treated with Beauveria bassiana conidia and mortality rate

Öz

This study was conducted to investigate the reaction of Rhyzopertha dominica adults to treated-wheat kernels with Beauveria bassiana spores considering pest movement and mortality. The pest’s reaction to inactivated B. bassiana spores was also tested. Each experimental unit had two equal-sized of compartments without restriction of R. dominica adult movements to both sites. By filling each compartment with wheat kernels treated or untreated, different layouts were created using two compartments. Treatments included either active or inactivated B. bassiana conidia. In setup of two experiments, R. dominica adults were released in either one or both compartments. The distribution of insects and mortalities were recorded at the end of the experiments. R. dominica adults exhibited a marked avoidance behavior towards the presence of B. bassiana spores, reducing the total mortality from 95.00% to 68.75%. R. dominica adults showed the same response to inactivated B. bassiana spores, and could not differentiate between active and inactive spores. The effect of this behavior on the success of B. bassiana treatments depends on the application strategy: while non-homogeneous distribution may lead to reduced efficacy due to insects aggregating in untreated areas, the fungus's inherent repellency offers a strategic advantage for preventing initial infestations.

Anahtar Kelimeler

• Insect behavior
• Avoidance
• Biological control
• Entomopathogenic fungi

Kaynakça

1. Abdel-Raheem, M. A., Ismail, I. A., Abdel Rahman, R. S., Farag, N. A., & Abdel Rahman, I. E. (2015). Entomopathogenic fungi, *Beauveria bassiana* (Bals.) and *Metarhizium anisopliae* (Metsch.) as biological control agents on some stored product insects. *Journal of Entomology and Zoology Studies, 3*(6), 316–320.
2. Athanassiou, C. G., & Palyvos, N. E. (2006). Laboratory evaluation of two diatomaceous earth formulations against *Blattisocius keegani* Fox (Mesostigmata, Ascidae) and *Cheyletus malaccensis* Oudemans (Prostigmata: Cheyletidae). *Biological Control, 38*, 350–355. https://doi.org/10.1016/j.biocontrol.2006.04.007
3. Barış, C. (2026). Investigation of mass production performance and virulence of some entomopathogenic fungal isolates and their single-spore strains against *Rhyzopertha dominica*. *Turkish Journal of Agricultural and Natural Sciences, 13*(1), 1–9. https://doi.org/10.30910/turkjans.1713146
4. Barış, C., & Er, M. K. (2025). Mortality effect of wettable powder formulations containing entomopathogenic fungal spores against some stored-product pests. *Turkish Journal of Entomology, 49*(2), 103–115. https://doi.org/10.16970/entoted.1599102
5. Baverstock, J., Alderson, P. G., & Pell, J. K. (2005). *Pandora neoaphidis* transmission and aphid foraging behaviour. *Journal of Invertebrate Pathology, 90*(1), 73–76. https://doi.org/10.1016/j.jip.2005.05.009
6. Baverstock, J., Roy, H. E., & Pell, J. K. (2010). Entomopathogenic fungi and insect behaviour: From unsuspecting hosts to targeted vectors. *BioControl, 55*(1), 89–102. https://doi.org/10.1007/s10526-009-9238-5
7. Bruetsch, T., Felden, A., Reber, A., & Chapuisat, M. (2014). Ant queens (Hymenoptera: Formicidae) are attracted to fungal pathogens during the initial stage of colony founding. *Myrmecological News, 20*, 71–76. https://iris.unil.ch/handle/iris/46136
8. Cotes, B., Thöming, G., Amaya-Gómez, C. V., Novák, O., & Nansen, C. (2020). Root-associated entomopathogenic fungi manipulate host plants to attract herbivorous insects. *Scientific Reports, 10*(1), Article 22424. https://doi.org/10.1038/s41598-020-80123-5

9. Couceiro, J. C., Wood, M. J., Papadopoulos, A., Silva, J. J., Vontas, J., & Dimopoulos, G. (2025). Development of mycoinsecticides: Advances in formulation, regulatory challenges and market trends for entomopathogenic fungi. *Journal of Fungi, 12*(1), Article 7. https://doi.org/10.3390/jof12010007
10. El Khoury, Y., Bari, G., Salvemini, C., Altieri, G. M., Karimi, J., Poliseno, M., & Tarasco, E. (2022). Susceptibility of four stored-product insect pests to *Beauveria bassiana* and *Metarhizium anisopliae* strains. *Redia, 105*, 175–182. https://hdl.handle.net/11586/454706
11. Er, M. K., Işıkber, A. A., & Tunaz, H. (2019). Effects of *Beauveria bassiana* on quantity of F1 larvae and larval mortality of *Tribolium confusum* (Coleoptera: Tenebrionidae). *Tarım ve Doğa Dergisi, 22*(6), 916. https://doi.org/10.18016/ksutarimdoga.vi.541840
12. Er, M. K., Tunaz, H., Ücük, C., Barış, C., & Işıkber, A. A. (2016). Occurrence of entomopathogenic fungi on insect pests of stored wheat and maize in Central and South Anatolia in Turkey. *Turkish Journal of Entomology, 40*(3), 249–263. https://izlik.org/JA99SP89EH
13. Ferizli, A. G., Beris, G., & Baspinar, E. (2005). Mortality and F1 production of *Rhyzopertha dominica* (F.) on wheat treated with diatomaceous earth: Impact of biological and environmental parameters on efficacy. *Journal of Pest Science, 78*, 231–238. https://doi.org/10.1007/s10340-005-0099-0
14. Geedi, R., Canas, L., Reding, M. E., & Ranger, C. M. (2023). Attraction of *Myzus persicae* (Hemiptera: Aphididae) to volatiles emitted from the entomopathogenic fungus *Beauveria bassiana*. *Environmental Entomology, 52*(1), 31–38. https://doi.org/10.1093/ee/nvac100
15. Golzan, S. R., Talaei-Hassanloui, R., Homayoonzadeh, M., & Safavi, S. A. (2023). Role of cuticle-degrading enzymes of *Beauveria bassiana* and *Metarhizium anisopliae* in virulence on *Plodia interpunctella* (Lepidoptera, Pyralidae) larvae. *Journal of Asia-Pacific Entomology, 26*(2), Article 102038. https://doi.org/10.1016/j.aspen.2023.102038
16. Haq, T., Usmani, N. F., & Abbas, T. (2005). Screeening of plant leaves as grain protectants against *Tribolium castaneum* during storage. *Journal of Botany, 37*, 149–153.
17. Janmaat, A., Fung, V., Rempel, C., Quik, R., Kabaluk, T., & Cory, J. (2022). Lack of avoidance of the fungal entomopathogen, *Metarhizium brunneum*, by male *Agriotes obscurus* beetles. *Journal of Invertebrate Pathology, 194*, Article 107824. https://doi.org/10.1016/j.jip.2022.107824
18. Kaya, K., Sertkaya, E., Üremiş, İ., & Soylu, S. (2018). Determination of chemical composition and fumigant insecticidal activities of essential oils of some medicinal plants against the adults of cowpea weevil, *Callosobruchus maculatus*. *Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 21*(5), 708–714. https://doi.org/10.18016/ksudobil.386176
19. Korkmaz, H. Y., & Er, M. K. (2022). Persistence of *Beauveria bassiana* efficacy on wheat grains to protect stored-grains from post-treatment pest infestations. *Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 25*(Ek Sayı 1), 143–148. https://doi.org/10.18016/ksutarimdoga.vi.1018408
20. Kumar, D., & Kalita, P. (2017). Reducing postharvest losses during storage of grain crops to strengthen food security in developing countries. *Foods, 6*(1), Article 8. https://doi.org/10.3390/foods6010008
21. Long, D. W., Groden, E., & Drummond, F. A. (2000). Horizontal transmission of *Beauveria bassiana* (Bals.) Vuill. *Agricultural and Forest Entomology, 2*(1), 11–17.
22. Ludwig, S. W., & Oetting, R. D. (2002). Efficacy of *Beauveria bassiana* plus insect attractants for enhanced control of *Frankliniella occidentalis* (Thysanoptera: Thripidae). *Florida Entomologist, 85*(1), 270–272. https://doi.org/10.1653/0015-4040(2002)085[0270:EOBBPI]2.0.CO;2
23. Mantzoukas, S., Lagogiannis, I., Kitsiou, F., & Eliopoulos, P. A. (2023). Entomopathogenic action of wild fungal strains against stored product beetle pests. *Insects, 14*(1), Article 91. https://doi.org/10.3390/insects14010091
24. Mburu, D. M., Maniania, N. K., & Hassanali, A. (2013). Comparison of volatile blends and nucleotide sequences of two *Beauveria bassiana* isolates of different virulence and repellency towards the termite *Macrotermes michealseni*. *Journal of Chemical Ecology, 39*(1), 101–108. https://doi.org/10.1007/s10886-012-0207-6
25. Mburu, D. M., Ndung'u, M. W., Maniania, N. K., & Hassanali, A. (2011). Comparison of volatile blends and gene sequences of two isolates of *Metarhizium anisopliae* of different virulence and repellency toward the termite *Macrotermes michaelseni*. *Journal of Experimental Biology, 214*(6), 956–962. https://doi.org/10.1242/jeb.050419
26. Mburu, D. M., Ochola, L., Maniania, N. K., Njagi, P. G. N., Gitonga, L. M., Ndung’u, M. W., & Hassanali, A. (2009). Relationship between virulence and repellency of entomopathogenic isolates of *Metarhizium anisopliae* and *Beauveria bassiana* to the termite *Macrotermes michaelseni*. *Journal of Insect Physiology, 55*(9), 774–780. https://doi.org/10.1016/j.jinsphys.2009.04.015
27. Meyling, N. V., & Pell, J. K. (2006). Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. *Ecological Entomology, 31*(2), 162–171. https://doi.org/10.1111/j.0307-6946.2006.00781.x
28. Michalaki, M. P., Athanassiou, C. G., Teenberg, T., & Buchelos, C. Th. (2007). Effect of *Paecilomyces fumosoroseus* (Wise) Brown and Smith (Ascomycota: Hypocreales) alone or in combination with diatomaceous earth against *Tribolium confusum* Jacquelin du Val (Coleoptera: Tenebrionidae) and *Ephestia kuehniella* Zeller (Lepidoptera: Pyralidae). *Biological Control, 40*, 280–286. https://doi.org/10.1016/j.biocontrol.2006.09.003
29. Mitina, G. V., Stepanycheva, E. A., & Choglokova, A. A. (2024). New approaches to evaluating the effectiveness of entomopathogenic fungi in microbiological plant protection against the western flower thrips *Frankliniella occidentalis* (Pergande) (Thysanoptera, Thripidae). *Entomological Review, 104*(2), 110–115. https://doi.org/10.1134/S0013873824020027
30. Mitina, G. V., Stepanycheva, E. A., Choglokova, A. A., & Cherepanova, M. A. (2023). Effect of volatile organic compounds of entomopathogenic fungi of the genus *Lecanicillium* and their component, acetic acid, on female behavior in the western flower thrips *Frankliniella occidentalis* (Pergande) (Thysanoptera, Thripidae). *Entomological Review, 103*(2), 144–151. https://doi.org/10.1134/S0013873823020033
31. Moino, A., Alves, S. B., & Pereira, R. M. (1998). Efficacy of *Beauveria bassiana* (Balsamo) Vuillemin isolates for control of stored-grain pests. *Journal of Applied Entomology, 122*(1–5), 301–305. https://doi.org/10.1111/j.1439-0418.1998.tb01501.x
32. Moran, M. N., Aguero, C. M., Eyer, P. A., & Vargo, E. L. (2022). Rescue strategy in a termite: Workers exposed to a fungal pathogen are reintegrated into the colony. *Frontiers in Ecology and Evolution, 10*, Article 840223. https://doi.org/10.3389/fevo.2022.840223
33. Musso, A., Marcondes Almeida, J. E., Padín, S. B., Ordoqui, E., & Lopez Lastra, C. C. (2020). Efficacy of entomopathogenic fungi against *Rhyzopertha dominica* (Fabricius) (Coleoptera: Bostrichidae) under laboratory conditions.
34. Mutlu, Ç., Öğreten, A., Kaya, C., & Mamay, M. (2019). Influence of different grain storage types on Khapra beetle, *Trogoderma granarium* Everts, 1898 (Coleoptera: Dermestidae), infestation in southeastern Anatolia (Turkey) and its resistance to malathion and deltamethrin. *Turkish Journal of Entomology, 43*(2), 131–142. https://doi.org/10.16970/entoted.528623
35. Myles, T. G. (2002). Alarm, aggregation, and defense by *Reticulitermes flavipes* in response to a naturally occurring isolate of *Metarhizium anisopliae*. *Sociobiology, 40*(2), 243–256.
36. Nayak, M. K., Daglish, G. J., Phillips, T. W., & Ebert, P. R. (2020). Resistance to the fumigant phosphine and its management in insect pests of stored products: A global perspective. *Annual Review of Entomology, 65*(1), 333–350. https://doi.org/10.1146/annurev-ento-011019-025047
37. Ormond, E. L., Thomas, A. P., Pell, J. K., Freeman, S. N., & Roy, H. E. (2011). Avoidance of a generalist entomopathogenic fungus by the ladybird, *Coccinella septempunctata*. *FEMS Microbiology Ecology, 77*(2), 229–237. https://doi.org/10.1111/j.1574-6941.2011.01100.x
38. Ozdemir, I. O., Tuncer, C., Erper, I., & Kushiyev, R. (2020). Efficacy of the entomopathogenic fungi *Beauveria bassiana* and *Metarhizium anisopliae* against the cowpea weevil, *Callosobruchus maculatus* F. (Coleoptera: Chrysomelidae: Bruchinae). *Egyptian Journal of Biological Pest Control, 30*(1), Article 24. https://doi.org/10.1186/s41938-020-00219-y
39. Pereira, H., Willeput, R., & Detrain, C. (2021). A fungus infected environment does not alter the behaviour of foraging ants. *Scientific Reports, 11*(1), Article 23573. https://doi.org/10.1038/s41598-021-02817-8
40. Seiedy, M., Heydari, S., & Tork, M. (2015). Orientation of *Hippodamia variegata* (Coleoptera: Coccinellidae) to healthy and *Beauveria bassiana*-infected *Aphis fabae* (Hemiptera: Aphididae) in an olfactometer system. *Turkish Journal of Zoology, 39*(1), 53–58. https://doi.org/10.3906/zoo-1310-18
41. Sertkaya, E., Kaya, K., & Soylu, S. (2010a). Acaricidal activities of the essential oils from several medicinal plants against the carmine spider mite (*Tetranychus cinnabarinus* Boisd.) (Acarina: Tetranychidae). *Industrial Crops and Products, 31*(1), 107–112. https://doi.org/10.1016/j.indcrop.2009.09.009
42. Sertkaya, E., Kaya, K., & Soylu, S. (2010b). Chemical compositions and insecticidal activities of the essential oils from several medicinal plants against the cotton whitefly, *Bemisia tabaci*. *Asian Journal of Chemistry, 22*(4), 2982–2990.
43. Staples, J. A., & Milner, R. J. (2000). A laboratory evaluation of the repellency of *Metarhizium anisopliae* conidia to *Coptotermes lacteus* (Isoptera: Rhinotermitidae).
44. Stejskal, J. (2015). Polymers of phenylenediamines. *Progress in Polymer Science, 41*, 1–31. https://doi.org/10.1016/j.progpolymsci.2014.10.007
45. Telli, Ö., & Yiğit, A. (2020). Hatay ili turunçgillerinde zararlı Turunçgil ipek beyazsineği, *Paraleyrodes minei* Iaccarino (Hemiptera: Aleyrodidae)’nin konukçuları, popülasyon değişimi ve biyolojisi. *Mustafa Kemal Üniversitesi Tarım Bilimleri Dergisi, 25*(1), 36–45. https://doi.org/10.37908/mkutbd.599235
46. Thompson, S. R., & Brandenburg, R. L. (2005). Tunneling responses of mole crickets (Orthoptera: Gryllotalpidae) to the entomopathogenic fungus, *Beauveria bassiana*. *Environmental Entomology, 34*(1), 140–147. https://doi.org/10.1603/0046-225X-34.1.140
47. Vianna, F., Russo, L., Troncozo, I., Ferreri, N., Abajo, J. M. D., Scorsetti, A. C., & Pelizza, S. (2023). Susceptibilidad de *Rhyzopertha dominica* (Coleoptera: Bostrichidae) y *Sitophilus oryzae* (Coleoptera: Curculionidae) al hongo entomopatógeno *Beauveria bassiana* (Balsamo-Crivelli) Vuillemin sl (Hypocreales: Clavicipitaceae). *Revista de la Facultad de Ciencias Agrarias. Universidad Nacional de Cuyo, 55*(2), 76–84.
48. Villani, M. G., Krueger, S. R., Schroeder, P. C., Consolie, F., Consolie, N. H., Preston-Wilsey, L. M., & Roberts, D. W. (1994). Soil application effects of *Metarhizium anisopliae* on Japanese beetle (Coleoptera: Scarabaeidae) behavior and survival in turfgrass microcosms. *Environmental Entomology, 23*(2), 502–513. https://doi.org/10.1093/ee/23.2.502
49. Wakil, W., Kavallieratos, N. G., Ghazanfar, M. U., Usman, M., Habib, A., & El-Shafie, H. A. (2021). Efficacy of different entomopathogenic fungal isolates against four key stored-grain beetle species. *Journal of Stored Products Research, 93*, Article 101845. https://doi.org/10.1016/j.jspr.2021.101845
50. Yanagawa, A., Imai, T., Akino, T., Toh, Y., & Yoshimura, T. (2015). Olfactory cues from pathogenic fungus affect the direction of motion of termites, *Coptotermes formosanus*. *Journal of Chemical Ecology, 41*(12), 1118–1126. https://doi.org/10.1007/s10886-015-0649-8
51. Yıldırım, E., Özbek, H., & Aslan, İ. (2001). *Depolanmış ürün zararlıları*. Atatürk Üniversitesi Ziraat Fakültesi Yayınları.
52. Zhang, W., Xie, M., Eleftherianos, I., Mohamed, A., Cao, Y., Song, B., & Xia, Y. (2023). An odorant binding protein is involved in counteracting detection-avoidance and Toll-pathway innate immunity. *Journal of Advanced Research, 48*, 1–16. https://doi.org/10.1016/j.jare.2022.08.013
53. Zobar, D., & Kıvan, M. (2022). Bazı entomopatojen fungus türlerinin *Capnodis tenebrionis* Linnaeus, 1758 (Coleoptera: Buprestidae)’in belirli dönemleri üzerinde patojeniteleri. *Mustafa Kemal Üniversitesi Tarım Bilimleri Dergisi, 27*(3), 469–476. https://doi.org/10.37908/mkutbd.1071813