Characterization of entomopathogenic fungi as a natural biological control of American cockroaches (Periplaneta americana)
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Abstract. Rosa E, Ekowati CN, Handayani TT, Ikhsanudin A, Apriliani F, Arifiyanto A. 2020. Characterization of entomopathogenic fungi as a natural biological control of American cockroaches (Periplaneta americana). Biodiversitas 21: 5276-5282. Eradicating cockroaches using chemical insecticides produces residues that contaminate the environment and promote insect resistance. Biological control has become an option for controlling cockroaches. The use of entomopathogenic fungi is one of them. The aim of this study was to obtain a fungal isolate that was effective at killing cockroaches. The result of entomopathogenic fungi isolation from cockroaches obtained 4 isolates, IK1, IK2, IK3 isolates were included in the Aspergillus genus while IK4 was Penicillium. Extracellular enzymes serve as screening materials for biocontrol candidates. IK1 and IK3 isolates showed higher chitinase activity than the other two isolates. The highest mortality of Periplaneta americana at nymphs stage was 60% achieved by the treatment of Aspergillus sp. IK3 with a concentration of 109 conidia/ mL. In adult stage cockroach the mortality was increased to 86%.
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References
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Atiokeng Tatang, R. J., Tsila, H. G., & Wabo Poné, J. 2017. Medically Important Parasites Carried by Cockroaches in Melong Subdivision, Littoral, Cameroon. Journal of Parasitology Research, 2017. https://doi.org/10.1155/2017/7967325
Barnet, H. L., & Hunter, B. 1998. Ilustrated Genera of Imperfect Fungi (4th ed.). Macmillian Publishing Company.
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Brzezinska, M. S., Jankiewicz, U., Burkowska, A., & Walczak, M. 2014. Chitinolytic microorganisms and their possible application in environmental protection. Current Microbiology, 68(1), 71–81. https://doi.org/10.1007/s00284-013-0440-4
Dhawan, M., & Joshi, N. 2017. Enzymatic comparison and mortality of Beauveria bassiana against cabbage caterpillar Pieris brassicae LINN. Brazilian Journal of Microbiology, 48(3), 522–529. https://doi.org/10.1016/j.bjm.2016.08.004
Gutierrez, A. C., Go??biowski, M., Pennisi, M., Peterson, G., García, J. J., Manfrino, R. G., & López Lastra, C. C. 2015. Cuticle Fatty Acid Composition and Differential Susceptibility of Three Species of Cockroaches to the Entomopathogenic Fungi Metarhizium anisopliae (Ascomycota, Hypocreales). Journal of Economic Entomology, 108(2), 752–760. https://doi.org/10.1093/jee/tou096
Jain, A., Jain, R., & Jain, S. 2020. Isolation of Coprophilous Fungi (Moist Chamber Method). In: Basic Techniques in Biochemistry, Microbiology and Molecular Biology. Springer Protocols Handbooks. https://doi.org/10.1007/978-1-4939-9861-6_32
Lechuga, E. G. O., Zapata, I. Q., & Niño, K. A. 2016. Detection of extracellular enzymatic activity in microorganisms isolated from waste vegetable oil contaminated soil using plate methodologies. African Journal of Biotechnology, 15(11), 408–416. https://doi.org/10.5897/ajb2015.14991
Litwin, A., Nowak, M., & Ró?alska, S. 2020. Entomopathogenic fungi: unconventional applications. Reviews in Environmental Science and Biotechnology, 19(1), 23–42. https://doi.org/10.1007/s11157-020-09525-1
Lopes, R. B., Martins, I., Souza, D. A., & Faria, M. 2013. Influence of some parameters on the germination assessment of mycopesticides. In Journal of Invertebrate Pathology (Vol. 112, Issue 3). https://doi.org/10.1016/j.jip.2012.12.010
Mantzoukas, S., & Eliopoulos, P. A. 2020. Endophytic entomopathogenic fungi: A valuable biological control tool against plant pests. Applied Sciences (Switzerland), 10(1). https://doi.org/10.3390/app10010360
Martindah, E., & Bahri, S. 2016. Kontaminasi Mikotoksin pada Rantai Makanan. Wartazoa, 26(3), 115–124. http://linkinghub.elsevier.com/retrieve/pii/S2211601X15001431
Moges, F., Eshetie, S., Endris, M., Huruy, K., Muluye, D., Feleke, T., Silassie, F. G., Ayalew, G., & Nagappan, R. 2016. Cockroaches as a Source of High Bacterial Pathogens with Multidrug Resistant Strains in Gondar Town, Ethiopia. BioMed Research International, 2016. https://doi.org/10.1155/2016/2825056
Mongeau, J. M., Demir, A., Dallmann, C. J., Jayaram, K., Cowan, N. J., & Full, R. J. 2014. Mechanical processing via passive dynamic properties of the cockroach antenna can facilitate control during rapid running. Journal of Experimental Biology, 217(18), 3333–3345. https://doi.org/10.1242/jeb.101501
Nelly, N., Syahrawati, M., Hamid, H., Habazar, T., & Gusnia, D. N. 2019. Diversity and characterization of entomopathogenic fungi from rhizosphere of maize plants as potential biological control agents. Biodiversitas, 20(5), 1435–1441. https://doi.org/10.13057/biodiv/d200536
Nicolopoulou-Stamati, P., Maipas, S., Kotampasi, C., Stamatis, P., & Hens, L. 2016. Chemical Pesticides and Human Health: The Urgent Need for a New Concept in Agriculture. Frontiers in Public Health, 4(July), 1–8. https://doi.org/10.3389/fpubh.2016.00148
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Praja, R. N., & Yudhana, A. 2018. Isolasi Dan Identifikasi Aspergillus Spp pada Paru-Paru Ayam Kampung Yang Dijual di Pasar Banyuwangi. Jurnal Medik Veteriner, 1(1), 6. https://doi.org/10.20473/jmv.vol1.iss1.2017.6-11
Qian, K., Wei, X. Q., Zeng, X. P., Liu, T., & Gao, X. W. 2010. Stage-dependent tolerance of the German cockroach, Blattella germanica for dichlorvos and propoxur. Journal of Insect Science, 10(194), 1–10. https://doi.org/10.1673/031.010.20101
Ratnaseelan, A. M., Tsilioni, I., & Theoharides, T. C. 2018. Effects of Mycotoxins on Neuropsychiatric Symptoms and Immune Processes. Clinical Therapeutics, 40(6), 903–917. https://doi.org/10.1016/j.clinthera.2018.05.004
Robles-acosta, Indira, N., Julio, C., Reyna, I., Landeros-Flores, Jerónimo, Vanoye-Eligio, & Venancio. 2019. Entomopathogenic Fungi as Biological Control Agents of Phyllocoptruta oleivora ( Prostigmata?: Eriophyidae ) under Greenhouse Conditions Entomopathogenic fungi as biological control agents of Phyllocoptruta oleivora ( Prostigmata?: Eriophyidae ) under gre. Florida Entomologist, 102(2), 303–308.
Sanchez, C. J., Chiu, C. W., Zhou, Y., González, J. M., Vinson, S. B., & Liang, H. 2015. Locomotion control of hybrid cockroach robots. Journal of the Royal Society Interface, 12(105). https://doi.org/10.1098/rsif.2014.1363
Schiavone, M., Vax, A., Formosa, C., Martin-Yken, H., Dague, E., & François, J. M. 2014. A combined chemical and enzymatic method to determine quantitatively the polysaccharide components in the cell wall of yeasts. FEMS Yeast Research, 14(6), 933–947. https://doi.org/10.1111/1567-1364.12182
Schuster, E., Dunn-Coleman, N., Frisvad, J., & Van Dijck, P. 2002. On the safety of Aspergillus niger - A review. Applied Microbiology and Biotechnology, 59(4–5), 426–435. https://doi.org/10.1007/s00253-002-1032-6
Septiana, N., Rosa, E., & Ekowati, C. N. 2019. Efektivitas Jamur Entomopatogen sebagai Bioinsektisida Lalat Rumah (Musca domestica). Biosfer: Jurnal Tadris Biologi, 10(1), 87–94.
Soesanto, L., Rahmaddila, A., Hartono, R., Mugiastuti, E., & Widarta, H. 2020. Seed-borne pathogenic fungi on some soybean varieties. 21(9), 4010–4015. https://doi.org/10.13057/biodiv/d210911
Supiyanto, Rosa, E., Irawan, B., & Nukmal, N. 2019. Isolasi dan Uji Patogenitas Isolat Fungi Entomopatogen Terhadap Stadium Dewasa Nyamuk A e des aegypti. 11(1), 33–41. https://doi.org/10.31957/jbp.832
Suryadi, Y., Priyatno, T. P., Samudra, I. M., Susilowati, D. N., Lawati, N., & Kustaman, E. 2016. Pemurnian Parsial dan Karakterisasi Kitinase Asal Jamur Entomopatogen Beauveria bassiana Isolat BB200109. Jurnal AgroBiogen, 9(2), 77. https://doi.org/10.21082/jbio.v9n2.2013.p77-84
Tuininga, A. R., Miller, J. L., Morath, S. U., Daniels, T. J., Falco, R. C., Marchese, M., Sahabi, S., Rosa, D., & III, K. C. S. 2009. Isolation of Entomopathogenic Fungi From Soils and Ixodes scapularis (Acari: Ixodidae) Ticks: Prevalence and Methods. J Med Entomol, 46(3), 557–565. https://doi.org/10.1161/CIRCULATIONAHA.110.956839
Utami, R. S., & Ambarwati, R. 2014. Eksplorasi dan Karakterisasi Cendawan Entomopatogen Beauveria bassiana dari Kabupaten Malang dan Magetan Exploration and Characterization of Entomopathogenic Fungi Beauveria bassiana from Malang and Magetan Regency. Lentera Bio, 3(1), 59–66. http://ejournal.unesa.ac.id/index.php/lenterabio
Veliz, E. A., Martínez-Hidalgo, P., & M. Hirsch, A. 2017. Chitinase-producing bacteria and their role in biocontrol. AIMS Microbiology, 3(3), 689–705. https://doi.org/10.3934/microbiol.2017.3.689
Visagie, C. M., Houbraken, J., Frisvad, J. C., Hong, S. B., Klaassen, C. H. W., Perrone, G., Seifert, K. A., Varga, J., Yaguchi, T., & Samson, R. A. 2014. Identification and nomenclature of the genus Penicillium. Studies in Mycology, 78(1), 343–371. https://doi.org/10.1016/j.simyco.2014.09.001
Yu, J.-H. 2010. Regulation of Development in Aspergillus nidulans and Aspergillus fumigatus . Mycobiology, 38(4), 229. https://doi.org/10.4489/myco.2010.38.4.229
Yunizar, N. 2018. Patogenitas Isolat Jamur Entomopatogenik Metarhizium anisopliae terhadap Lalat Rumah Musca domestica L . ( Diptera?: Muscidae ). Protobiont, 7, 77–82.
Yusof, A. M. 2018. Identification of cockroaches as mechanical vector for parasitic infections and infestations in Kkuantan, Malaysia. Journal of Entomology, 15(3), 143–148. https://doi.org/10.3923/je.2018.143.148
Zahraei-Ramazani, A. R., Saghafipour, A., & Vatandoost, H. 2018. Control of American Cockroach (Periplaneta americana) in municipal sewage disposal system, Central Iran. Journal of Arthropod-Borne Diseases, 12(2), 172–179. https://doi.org/10.18502/jad.v12i2.43
Zain, M. E. 2011. Impact of mycotoxins on humans and animals. Journal of Saudi Chemical Society, 15(2), 129–144. https://doi.org/10.1016/j.jscs.2010.06.006
Atiokeng Tatang, R. J., Tsila, H. G., & Wabo Poné, J. 2017. Medically Important Parasites Carried by Cockroaches in Melong Subdivision, Littoral, Cameroon. Journal of Parasitology Research, 2017. https://doi.org/10.1155/2017/7967325
Barnet, H. L., & Hunter, B. 1998. Ilustrated Genera of Imperfect Fungi (4th ed.). Macmillian Publishing Company.
Berini, F., Katz, C., Gruzdev, N., Casartelli, M., Tettamanti, G., & Marinelli, F. 2018. Microbial and viral chitinases: Attractive biopesticides for integrated pest management. Biotechnology Advances, 36(3), 818–838. https://doi.org/10.1016/j.biotechadv.2018.01.002
Brzezinska, M. S., Jankiewicz, U., Burkowska, A., & Walczak, M. 2014. Chitinolytic microorganisms and their possible application in environmental protection. Current Microbiology, 68(1), 71–81. https://doi.org/10.1007/s00284-013-0440-4
Dhawan, M., & Joshi, N. 2017. Enzymatic comparison and mortality of Beauveria bassiana against cabbage caterpillar Pieris brassicae LINN. Brazilian Journal of Microbiology, 48(3), 522–529. https://doi.org/10.1016/j.bjm.2016.08.004
Gutierrez, A. C., Go??biowski, M., Pennisi, M., Peterson, G., García, J. J., Manfrino, R. G., & López Lastra, C. C. 2015. Cuticle Fatty Acid Composition and Differential Susceptibility of Three Species of Cockroaches to the Entomopathogenic Fungi Metarhizium anisopliae (Ascomycota, Hypocreales). Journal of Economic Entomology, 108(2), 752–760. https://doi.org/10.1093/jee/tou096
Jain, A., Jain, R., & Jain, S. 2020. Isolation of Coprophilous Fungi (Moist Chamber Method). In: Basic Techniques in Biochemistry, Microbiology and Molecular Biology. Springer Protocols Handbooks. https://doi.org/10.1007/978-1-4939-9861-6_32
Lechuga, E. G. O., Zapata, I. Q., & Niño, K. A. 2016. Detection of extracellular enzymatic activity in microorganisms isolated from waste vegetable oil contaminated soil using plate methodologies. African Journal of Biotechnology, 15(11), 408–416. https://doi.org/10.5897/ajb2015.14991
Litwin, A., Nowak, M., & Ró?alska, S. 2020. Entomopathogenic fungi: unconventional applications. Reviews in Environmental Science and Biotechnology, 19(1), 23–42. https://doi.org/10.1007/s11157-020-09525-1
Lopes, R. B., Martins, I., Souza, D. A., & Faria, M. 2013. Influence of some parameters on the germination assessment of mycopesticides. In Journal of Invertebrate Pathology (Vol. 112, Issue 3). https://doi.org/10.1016/j.jip.2012.12.010
Mantzoukas, S., & Eliopoulos, P. A. 2020. Endophytic entomopathogenic fungi: A valuable biological control tool against plant pests. Applied Sciences (Switzerland), 10(1). https://doi.org/10.3390/app10010360
Martindah, E., & Bahri, S. 2016. Kontaminasi Mikotoksin pada Rantai Makanan. Wartazoa, 26(3), 115–124. http://linkinghub.elsevier.com/retrieve/pii/S2211601X15001431
Moges, F., Eshetie, S., Endris, M., Huruy, K., Muluye, D., Feleke, T., Silassie, F. G., Ayalew, G., & Nagappan, R. 2016. Cockroaches as a Source of High Bacterial Pathogens with Multidrug Resistant Strains in Gondar Town, Ethiopia. BioMed Research International, 2016. https://doi.org/10.1155/2016/2825056
Mongeau, J. M., Demir, A., Dallmann, C. J., Jayaram, K., Cowan, N. J., & Full, R. J. 2014. Mechanical processing via passive dynamic properties of the cockroach antenna can facilitate control during rapid running. Journal of Experimental Biology, 217(18), 3333–3345. https://doi.org/10.1242/jeb.101501
Nelly, N., Syahrawati, M., Hamid, H., Habazar, T., & Gusnia, D. N. 2019. Diversity and characterization of entomopathogenic fungi from rhizosphere of maize plants as potential biological control agents. Biodiversitas, 20(5), 1435–1441. https://doi.org/10.13057/biodiv/d200536
Nicolopoulou-Stamati, P., Maipas, S., Kotampasi, C., Stamatis, P., & Hens, L. 2016. Chemical Pesticides and Human Health: The Urgent Need for a New Concept in Agriculture. Frontiers in Public Health, 4(July), 1–8. https://doi.org/10.3389/fpubh.2016.00148
Perinotto, W. M. S., Golo, P. S., Coutinho, C. J. B., Sá, F. A., Santi, L., Beys, W. O., Junges, A., Vainstein, M. H., Schrank, A., Salles, C. M. C., & Bittencourt, V. R. E. P. 2014. Veterinary Parasitology Enzymatic activities and effects of mycovirus infection on the virulence of Metarhizium anisopliae in Rhipicephalus microplus. Veterinary Parasitology, 203(1–2), 189–196. https://doi.org/10.1016/j.vetpar.2014.02.011
Praja, R. N., & Yudhana, A. 2018. Isolasi Dan Identifikasi Aspergillus Spp pada Paru-Paru Ayam Kampung Yang Dijual di Pasar Banyuwangi. Jurnal Medik Veteriner, 1(1), 6. https://doi.org/10.20473/jmv.vol1.iss1.2017.6-11
Qian, K., Wei, X. Q., Zeng, X. P., Liu, T., & Gao, X. W. 2010. Stage-dependent tolerance of the German cockroach, Blattella germanica for dichlorvos and propoxur. Journal of Insect Science, 10(194), 1–10. https://doi.org/10.1673/031.010.20101
Ratnaseelan, A. M., Tsilioni, I., & Theoharides, T. C. 2018. Effects of Mycotoxins on Neuropsychiatric Symptoms and Immune Processes. Clinical Therapeutics, 40(6), 903–917. https://doi.org/10.1016/j.clinthera.2018.05.004
Robles-acosta, Indira, N., Julio, C., Reyna, I., Landeros-Flores, Jerónimo, Vanoye-Eligio, & Venancio. 2019. Entomopathogenic Fungi as Biological Control Agents of Phyllocoptruta oleivora ( Prostigmata?: Eriophyidae ) under Greenhouse Conditions Entomopathogenic fungi as biological control agents of Phyllocoptruta oleivora ( Prostigmata?: Eriophyidae ) under gre. Florida Entomologist, 102(2), 303–308.
Sanchez, C. J., Chiu, C. W., Zhou, Y., González, J. M., Vinson, S. B., & Liang, H. 2015. Locomotion control of hybrid cockroach robots. Journal of the Royal Society Interface, 12(105). https://doi.org/10.1098/rsif.2014.1363
Schiavone, M., Vax, A., Formosa, C., Martin-Yken, H., Dague, E., & François, J. M. 2014. A combined chemical and enzymatic method to determine quantitatively the polysaccharide components in the cell wall of yeasts. FEMS Yeast Research, 14(6), 933–947. https://doi.org/10.1111/1567-1364.12182
Schuster, E., Dunn-Coleman, N., Frisvad, J., & Van Dijck, P. 2002. On the safety of Aspergillus niger - A review. Applied Microbiology and Biotechnology, 59(4–5), 426–435. https://doi.org/10.1007/s00253-002-1032-6
Septiana, N., Rosa, E., & Ekowati, C. N. 2019. Efektivitas Jamur Entomopatogen sebagai Bioinsektisida Lalat Rumah (Musca domestica). Biosfer: Jurnal Tadris Biologi, 10(1), 87–94.
Soesanto, L., Rahmaddila, A., Hartono, R., Mugiastuti, E., & Widarta, H. 2020. Seed-borne pathogenic fungi on some soybean varieties. 21(9), 4010–4015. https://doi.org/10.13057/biodiv/d210911
Supiyanto, Rosa, E., Irawan, B., & Nukmal, N. 2019. Isolasi dan Uji Patogenitas Isolat Fungi Entomopatogen Terhadap Stadium Dewasa Nyamuk A e des aegypti. 11(1), 33–41. https://doi.org/10.31957/jbp.832
Suryadi, Y., Priyatno, T. P., Samudra, I. M., Susilowati, D. N., Lawati, N., & Kustaman, E. 2016. Pemurnian Parsial dan Karakterisasi Kitinase Asal Jamur Entomopatogen Beauveria bassiana Isolat BB200109. Jurnal AgroBiogen, 9(2), 77. https://doi.org/10.21082/jbio.v9n2.2013.p77-84
Tuininga, A. R., Miller, J. L., Morath, S. U., Daniels, T. J., Falco, R. C., Marchese, M., Sahabi, S., Rosa, D., & III, K. C. S. 2009. Isolation of Entomopathogenic Fungi From Soils and Ixodes scapularis (Acari: Ixodidae) Ticks: Prevalence and Methods. J Med Entomol, 46(3), 557–565. https://doi.org/10.1161/CIRCULATIONAHA.110.956839
Utami, R. S., & Ambarwati, R. 2014. Eksplorasi dan Karakterisasi Cendawan Entomopatogen Beauveria bassiana dari Kabupaten Malang dan Magetan Exploration and Characterization of Entomopathogenic Fungi Beauveria bassiana from Malang and Magetan Regency. Lentera Bio, 3(1), 59–66. http://ejournal.unesa.ac.id/index.php/lenterabio
Veliz, E. A., Martínez-Hidalgo, P., & M. Hirsch, A. 2017. Chitinase-producing bacteria and their role in biocontrol. AIMS Microbiology, 3(3), 689–705. https://doi.org/10.3934/microbiol.2017.3.689
Visagie, C. M., Houbraken, J., Frisvad, J. C., Hong, S. B., Klaassen, C. H. W., Perrone, G., Seifert, K. A., Varga, J., Yaguchi, T., & Samson, R. A. 2014. Identification and nomenclature of the genus Penicillium. Studies in Mycology, 78(1), 343–371. https://doi.org/10.1016/j.simyco.2014.09.001
Yu, J.-H. 2010. Regulation of Development in Aspergillus nidulans and Aspergillus fumigatus . Mycobiology, 38(4), 229. https://doi.org/10.4489/myco.2010.38.4.229
Yunizar, N. 2018. Patogenitas Isolat Jamur Entomopatogenik Metarhizium anisopliae terhadap Lalat Rumah Musca domestica L . ( Diptera?: Muscidae ). Protobiont, 7, 77–82.
Yusof, A. M. 2018. Identification of cockroaches as mechanical vector for parasitic infections and infestations in Kkuantan, Malaysia. Journal of Entomology, 15(3), 143–148. https://doi.org/10.3923/je.2018.143.148
Zahraei-Ramazani, A. R., Saghafipour, A., & Vatandoost, H. 2018. Control of American Cockroach (Periplaneta americana) in municipal sewage disposal system, Central Iran. Journal of Arthropod-Borne Diseases, 12(2), 172–179. https://doi.org/10.18502/jad.v12i2.43
Zain, M. E. 2011. Impact of mycotoxins on humans and animals. Journal of Saudi Chemical Society, 15(2), 129–144. https://doi.org/10.1016/j.jscs.2010.06.006
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