Environmental persistence of the conidia of native entomopathogenic fungi and their efficiency on Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae)

Year 2024, Volume: 48 Issue: 3, 327 - 342, 16.10.2024

Mehmet Sedat Sevinç , İsmail Karaca

https://doi.org/10.16970/entoted.1498947

Abstract

This study aimed to investigate the effects of local Beauveria bassiana (Balsamo) Vuillemin and Cordyceps fumosorosea (Wize) (Hypocreales: Cordycipitaceae) isolates on Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae) prepupae, during 2020 and 2021 in the Mediterranean Region of Türkiye. In petri dishes, mortality rates varied with doses: for LD.2016 (B. bassiana), between 30 and 60%, for M6-4 (B. bassiana), 30-46%, of IFR (C. fumosorosea), 65-100%. Additionally, differences were detected between the prepupa and pupa periods of the larvae depending on the isolate. In sterile soil studies, the IFR caused mortality rates of 53-93%, while those for the LD.2016 isolate were 20-55%, depending on the doses. In conidial survival studies, the IFR caused mortality rates of 70-93% at 0 months and 44-60% in the 12th month. The LD.2016 mortality was among 37-55% at 0 months, while mortality rates decreased to 2% in the 12th month. The reproductive capacity of adult individuals that emerged alive after infection was negatively affected depending on time and fungal isolate. In semi-controlled field conditions, the IFR isolate had mortality rates varied between 40 and 65%, and LD.2016 mortality rates varied between 34 and 62%, depending on doses. It was observed that the fungi used in the study had potential in biological control of C. capitata.

Keywords

Beauveria bassiana, Cordyceps fumosorosea, reproductive capacity, soil surface application, sublethal effects

Supporting Institution

Ministry of Agriculture and Forestry of the Republic of Turkey, General Directorate of Agricultural Research and Policies

Project Number

TAGEM/BSAD/A/21/A2/P5/2404

Thanks

This study was funded by the Ministry of Agriculture and Forestry of the Republic of Turkey, General Directorate of Agricultural Research and Policies, (with the project number TAGEM/BSAD/A/21/A2/P5/2404), and the manuscript was produced from a part of data from first author’s PhD. dissertation. Petri dishes bioassay results and the first application results of conidial persistence studies (0th month on sterile soil bioassays), which form a part of this study, were presented as an oral presentation at the 8th International Entomopathogens and Microbial Control Congress held in Antalya-Turkey on 6-8 October 2022, and the summary was included in the congress summary book.

Yerel entomopatojen fungus konidialarının çevresel kalıcılığı ve Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae) üzerindeki etkinliği

Abstract

Bu çalışmada, 2020-2021 yıllarında Türkiye Akdeniz Bölgesi'nde yerel Beauveria bassiana (Balsamo) Vuillemin ve Cordyceps fumosorosea (Wize) (Hypocreales: Cordycipitaceae) izolatlarının Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae) prepupaları üzerindeki etkilerinin araştırılması amaçlanmıştır. Petri kaplarında ölüm oranları dozlara göre; LD.2016 (B. bassiana) için %30-60 arasında, M6-4 (B. bassiana) için %30-46 arasında, IFR (C. fumosorosea) için %65-100 arasında değişmiştir. Ayrıca, izolatlara bağlı olarak larvaların prepupa ve pupa dönemleri arasında farklılıklar tespit edilmiştir. Steril toprak çalışmalarında IFR %53-93 arasında mortaliteye neden olurken, LD.2016 izolatı için bu oran doza bağlı olarak %20-55 olmuştur. Konidial hayatta kalma çalışmalarında IFR 0. ayda %70-93, 12. ayda ise %44-60 arasında mortaliteye neden olmuştur. LD.2016 mortalitesi 0. ayda %37-55 arasında iken, 12. ayda mortalite oranları %2'ye düşmüştür. Enfeksiyondan sonra canlı çıkan ergin bireylerin üreme kapasitesi zamana ve fungal izolata bağlı olarak olumsuz etkilenmiştir. Yarı kontrollü arazi koşullarında IFR izolatında mortalite oranları doza bağlı olarak %40-65 arasında, LD.2016 mortalite oranları ise %34-62 arasında değişmiştir. Çalışmada kullanılan fungusların C. capitata'nın biyolojik mücadelesinde potansiyel taşıdığı görülmüştür.

Keywords

Beauveria bassiana, Cordyceps fumosorosea, üreme kapasitesi, toprak yüzey uygulaması, ölümcül olmayan etkiler

Project Number

TAGEM/BSAD/A/21/A2/P5/2404

References

• Abbott, W. S., 1925. A method of computing the effectiveness of an Insecticide. Journal of Economic Entomology, 18 (2): 265-267.
• Baydar, R., Ö. Güven & İ. Karaca, 2016. Occurrence of entomopathogenic fungi in agricultural soils from Isparta Province in Turkey and their pathogenicity to Galleria mellonella (L.) (Lepidoptera: Pyralidae) larvae. Egyptian Journal of Biological Pest Control, 26 (2): 323-327.
• Behie, S. W., S. J. Jones & M. J. Bidochka, 2015. Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria, Fungal Ecology, 13 (1): 112-119.
• Beris, I. E., D. P. Papachristos, A. Fytrou, S. A. Antonatos & D. C. Kontodimas, 2013. Pathogenicity of three entomopathogenic fungi on pupae and adults of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Journal of Pest Science, 86 (1): 275-284.
• Bernardo, M. A. & M. S. Singer, 2017. Parasite-altered feeding behavior in insects: Integrating functional and mechanistic research frontiers. The Journal of Experimental Biology, 220 (16): 2848-2857.
• Castrillo, M. A., P. Moya, E. Hernández & E. Primo-Yufera, 2000. Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to entomopathogenic fungi and their extracts. Biological Control, 19 (3): 274-282.
• Chergui, S., K. Boudjemaa, A. Benzehra & İ. Karaca, 2020. Pathogenicity of indigenous Beauveria bassiana (Balsamo) against Ceratitis capitata Wiedemann (Diptera: Tephritidae) under laboratory conditions. Egyptian Journal of Biological Pest Control, 30 (1): 1-7.
• Dash, C. K., B. S. Bamisile, R. Keppanan, M. Qasim, Y. Lin, S. U. Islam, M. Hussain & L. Wang, 2018. Endophytic entomopathogenic fungi enhance the growth of Phaseolus vulgaris L. (Fabaceae) and negatively affect the development and reproduction of Tetranychus urticae Koch (Acari: tetranychidae), Microbial Pathogenesis, 125 (1): 385-392.
• Dias, N. P., M. J. Zotti, P. Montoya, I. R. Carvalho & D. E. Nava, 2018. Fruit fly management research: A systematic review of monitoring and control tactics in the world. Crop Protection, 112 (1): 187-200.
• Dimbi, S., N. K. Maniania & S. Ekesi, 2009. Effect of Metarhizium anisopliae inoculation on the mating behavior of three species of African Tephritid fruit flies, Ceratitis capitata, Ceratitis cosyra and Ceratitis fasciventris. Biological Control, 50 (2): 111-116.
• Dimbi, S., N. K., Maniania, S. A. Lux, S. Ekesi & J. K. Mueke, 2003. Pathogenicity of Metarhizium anisopliae (Metsch.) Sorokin and Beauveria bassiana (Balsamo) Vuillemin, to three adult fruit fly species: Ceratitis capitata (Weidemann), C. rosa var. fasciventris Karsch and C. cosyra (Walker) (Diptera: Tephritidae). Mycopathologia, 156 (4): 375-382.
• Ding, J. L., H. Y. Lin, J. Hou, M. G. Feng & S. H. Ying, 2023. The entomopathogenic fungus Beauveria bassiana employs autophagy as a persistence and recovery mechanism during conidial dormancy. Mbio, 14 (2): e03049-22.
• Ekesi, S., K. Maniania & S. A. Lux, 2010. Mortality in three African Tephritid fruit fly puparia and adults caused by the entomopathogenic fungi, Metarhizium anisopliae and Beauveria bassiana. Biocontrol Science and Technology, 12 (1): 7-17.
• Feng, M. G., T. J. Poprawski & G. G. Khachatourians, 1994. Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control: current status, Biocontrol Science and Technology, 4 (1): 3-34.
• Gava, C. A. T., P. F. D. S. Tavares, J. S. Gonçalves & B. A. J. Paranhos, 2020. Applying local entomopathogenic fungi strains to the soil can control Ceratitis capitata (Diptera: Tephritidae) Wiedemann adults. Biocontrol Science and Technology, 30 (2): 103-115.
• Hallouti, A., H. Benjlil, A. El Hamdaoui, R. A. Hammou, M. A. Hamza, A. Zahidi, A. A. B. Aoumar & H. Boubaker, 2021. Evaluation of native entomopathogenic fungi isolates for microbial control of the Mediterranean fruit fly (Ceratitis capitata (Diptera: Tephritidae)) pupae and adults. Sumerianz Journal of Biotechnology, 4 (4): 153-164.
• Hussain, A., M. Y. Tian, Y. R. He & S. Ahmed, 2009. Entomopathogenic fungi disturbed the larval growth and feeding performance of Ocinara varians (Lepidoptera: Bombycidae) larvae. Insect Science, 16 (6): 511-517. IBM SPSS, 2015. Statistics for Windows, 2015 Version 23.0. Armonk, NY: IBM Corporation.
• Islam, W., M. Adnan, A. Shabbir, H. Naveed, Y. S. Abubakar, M. Qasim, M. Tayyab, A. Noman, M. S. Nisar, K. A. Khan & H. Ali, 2021. Insect-fungal-interactions: A detailed review on entomopathogenic fungi pathogenicity to combat insect pests. Microbial Pathogenesis, 159 (1): 105-122.
• Jackson, T. A., S. B. Alves & R. M. Pereira, 2000. “Success in Biological Control of Soil-Dwelling İnsects by Pathogens and Nematodes, 271-296”. In: Biological Control: Measures of Success (Eds. G. Gurr & S. Wratten). Kluver Academics Publishers: New York, USA, 429 pp.
• Jaronski, S. T., 2007. “Soil Ecology of The Entomopathogenic Ascomycetes: A Critical Examination of What We (think) We Know, 1-53”. In: Use of Entomopathogenic Fungi in Biological Pest Management (Eds. S. Ekesi & N. K. Maniania). Research Signpost: Kerala, 321 pp.
• Keller, S. & G. Zimmerman, 1989. “Mycopathogens of Soil Insects, 240-270”. In: Insect-Fungus Interactions (Eds. N. Wilding, N. M. Collins, P. M. Hammond & J. F. Webber). Academic Press, London, 343 pp.
• Lu, H. L. & R. J. St Leger, 2016. Insect immunity to entomopathogenic fungi. Advances in Genetics, 94 (1): 251-285.
• Meyling, N. V. & J. Eilenberg, 2007. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: Potential for conservation biological control. Biological Control, 43 (2): 145-155.
• O'Callaghan, M., R. A. Ballard & D. Wright, 2022. Soil microbial inoculants for sustainable agriculture: Limitations and opportunities. Soil Use and Management, 38 (3): 1340-1369.
• Ortiz-Urquiza, A. & N. O. Keyhani, 2013. Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects, 4 (3): 357-374.
• Qazzaz, F. O., M. I. Al-Masri & R. M. Barakat, 2015. Effectiveness of Beauveria bassiana Native Isolates in the Biological Control of the Mediterranean Fruit Fly (Ceratitis capitata). Advances in Entomology, 3 (2): 44-55.
• Quesada-Moraga, E., A. Ruiz-García & C. Santiago-Álvarez, 2006. Laboratory evaluation of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae against puparia and adults of Ceratitis capitata (Diptera: Tephritidae). Journal of Economic Entomology, 99 (6): 1955-1966.
• Quesada-Moraga, E., I. Garrido-Jurado, M. Yousef-Yousef & N. González-Mas, 2022. Multitrophic interactions of entomopathogenic fungi in BioControl. BioControl, 67 (5): 457-472.
• Rehner, S. A. & E. Buckley, 2005. A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia, 97 (1): 84-98.
• Roberts, D. W. & R. J. St. Leger, 2004. Metarhizium spp., cosmopolitan insect-pathogenic fungi: Mycological aspects. Advances in Applied Microbiology, 54 (1): 1-70.
• Samson, R. A., H. C. Evans & J. P. Latge, 1988. Atlas of Entomopathogenic Fungi. Springer-Verlag: New York, USA, 187 pp.
• Scholte, E. J., B. G. J. Knols, R. A. Samson & W. Takken, 2004. Entomopathogenic fungi for mosquito control: a review, Journal of Insect Science, 4 (1): 1-24.
• Sevinç, M. S. & İ. Karaca, 2024. Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) popülasyonunda ana yaşının biyolojik parametrelere etkisi. Meyve Bilimi, 11 (1): 35-42 (in Turkish with abstract in English).
• Shah, P. A. & J. K. Pell, 2003. Entomopathogenic fungi as biological control agents, Applied Microbiology and Biotechnology, 61 (5): 413-423.
• Sheldrake, M., 2020. Saklı Dünya (Turkish version of “Entangled Life: How Fungi Make Our Worlds, Change Our Minds & Shape Our Futuresbook”), First Edition, August 2022, Domingo: İstanbul, 368 pp (in Turkish).
• Soliman, N. A., S. M. Al-amin, A. E. Mesbah, A. Ibrahim & A. Mahmoud, 2020. Pathogenicity of three entomopathogenic fungi against the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Egyptian Journal of Biological Pest Control, 30 (1): 1-8.
• Solter, L. F., A. E. Hajek & L. A. Lacey, 2017. “Exploration for Entomopathogens, 13-23”. In: Microbial Control of Insect and Mite Pests (Eds. L. A. Lacey). Academic Press: London, 482 pp.
• Thomas, M. B., S. Blanford & C. Lomer, 1997. Reduction of feeding by the variegated grasshopper, Zonocerus variegatus, following infection by the fungal pathogen, Metarhizium flavoviride. Biocontrol Science and Technology, 7 (3): 327-334.
• Tscharntke, T. & B. A. Hawking, 2000. “Multitrophic Level Interactions: An Introduction, 1-7”. In: Multitrophic Level Interactions (Eds. T. Tscharntke & B. A. Hawking). Cambridge University Press: Cambridge. 284 pp. Tukey, J. W., 1949. Comparing individual means in the analysis of variance. Biometrics, 5 (2): 99-114.
• Ullah, M. S. & U. T. Lim, 2017. Laboratory evaluation of the effect of Beauveria bassiana on the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae). Journal of Invertebrate Pathology, 148 (1):102-109.
• Vega, F. E., M. S. Goettel, M. Blackwell, D. Chandler, M. A. Jackson, S. Keller, M. Koike, N. K. Maniania, A. Monz´on, B. H. Ownley, J. K. Pell, D. E. N. Rangel & H. E. Roy, 2009. Fungal entomopathogens: new insights on their ecology. Fungal Ecology, 2 (4): 149-159.
• Vidal, S & L. R. Jaber, 2015. Entomopathogenic fungi as endophytes: plant-endophyteherbivore interactions and prospects for use in biological control. Current Science, 109 (1): 46-54.
• Villaseñor, A., S. Flores, S. E. Campos, J. Toledo, P. Montoya, P. Liedo & W. Enkerlin, 2019. Use of entomopathogenic fungi for fruit fly control in area-wide SIT programmes. (Website: https://www.iaea.org/sites/default/files/21/05/2019_ipc_use_of_entomopathogenic_fungi_eng.pdf), (Access date: 25.09.2024).
• Yeşilırmak, M., M. S. Sevinç, & B. Yaman, 2024. Elma bahçelerinde elma içkurdu ve kırmızı örümceklere karşı kullanılan bazı insektisit ve akarisitlerin Akdeniz meyve sineği, Ceratitis capitata (Diptera: Tephritidae) üzerinde etkileri. ANADOLU Ege Tarımsal Araştırma Enstitüsü Dergisi, 34 (1): 33-37 (in Turkish with abstract in English).
• Zimmermann, G., 2007. Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Science and Technology, 17 (6): 553-596.
• Zimmermann, G., 2008. The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): Biology, ecology and use in biological control. Biocontrol Science and Technology, 18 (9): 865-901.