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Toxicity of Some Entomopathogenic Fungi Combined with Boric Acid Againts Adults of American Cockroach Periplaneta americana (L.) (Blattodea: Blattidae)

Year 2023, Volume: 26 Issue: 4, 795 - 805, 31.08.2023

İbrahim Ersin Bozdoğan , Hasan Tunaz

https://doi.org/10.18016/ksutarimdoga.vi.1221835

Abstract

In this study, the pathogenicity of some entomopathogenic fungi on American cockroach Periplaneta americana (L.) adults and the effect of the most effective fungus isolate combined with boric acid on the virulence of the fungus were investigated in laboratory conditions. According to the results obtained from the experiments, the most effective isolate was found as Beauveria bassiana 5-4 and when it was used on insects, it caused 0%, 66.6% and 93.3% mortality at the dose of 0.1×109 conidia cm-2 at 72, 96 and 120 hours, respectively. This fungus also caused 0%, 20% and 20% mortality, respectively, at dose of 0.05×109 conidia cm-2 in the same time period. When boric acid was used on insects, it caused 6.6%, 40% and 66.6% mortality at dose of 1 mg cm-2 at 72, 96 and 120 hours, respectively. When 0.1×109 conidia cm-2 dose of B. bassiana 5-4 was used together with 1 mg cm-2 dose of boric acid, 33.3%, 60% and 93.3% mortality occurred at 72, 96 and 120 hours, respectively. When 0.05×109 conidia cm-2 dose of B. bassiana 5-4 was used together with 1 mg cm-2 dose of boric acid, 33.3%, 60% and 86.6% mortality occurred at 72, 96 and 120 hours, respectively. The results showed that the combined use of boric acid and B. bassiana 5-4 increased the virulence of the fungus at short exposure times (72 and 96 hours), but did not significantly affect the virulence of the fungus at long exposure times (120 hours and above).

Keywords

Periplaneta americana Beauveria bassiana Boric acid Entomopathogen fungus Biological control

Thanks

This work is part of the first author's master's thesis. Thanks to Prof. Dr. Mehmet Kubilay ER and Dr. Cebrail BARIŞ for providing entomopathogenic fungal cultures.

References

  • Artyukhina, I. N. & Evokimov, M. P. (1973). Duration of persistence in and excretion of Shigella flexeri and Shigella sonnei by Blattella germanica (L.) in individual dosed feedings (in Russian). Medical Parazitol Parazit Bol. 42(5), 602–606.
  • Ash, N. & Greenberg, B. (1980). Vector potential of the German cockroach (Dictyoptera: Blattellidae) in dissemination of Salmonella interitidis serotype typhimurium. Journal of Medical Entomology. 17(5), 417–423.
  • Barış, C. & Er, M. K. (2021). Examining Some Cereals for Mass Production of Beauveria bassiana (Balsamo) Vuillemin Conidia by Solid State Fermentation. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi. 24(6), 1263-1270.
  • Baumholtz, M. A., Parish, L. C., Witkowski, J. A. & Nutting, W. B. (1997). The medical importance of cockroaches. International Journal of Dermatology. 36(2), 90–96.
  • Burgess, N. R., McDermott, S. M. & Whiting, J. (1973a). Aerobic bacteria occurring in the hindgut of the cockroach Blatta orientalis. Journal of Hygiene. 71(1), 1–7.
  • Burgess, N. R., McDermott, S. M. & Whiting, J. (1973b). Laboratory transmission of Enterobacteriaceae by the oriental cockroach, Blatta orientalis. Journal of Hygiene. 71(1), 9–14.
  • Burgess, N. R., Chetwyn, K. N., Nunn, C J. & Shuttleworth, A. E. (1974). Some preliminary work on cockroach-infested sewers in Landon. Transactions of the Royal Society of Tropical Medicine and Hygiene. 68(1), 16. Cochran D. G. (1995). Toxic effects of boric acid on the German cockroach. Experientia. 51(6), 561–563.
  • Burgess, N. R., Chetwyn, K. N., Nunn, C J. & Shuttleworth, A. E. (1974). Some preliminary work on cockroach-infested sewers in Landon. Transactions of the Royal Society of Tropical Medicine and Hygiene. 68(1), 16. Cochran D. G. (1995). Toxic effects of boric acid on the German cockroach. Experientia. 51(6), 561–563.
  • Cochran, D. G., & World Health Organization. (‎1999)‎. Communicable Diseases Prevention and Control Dept. WHO Pesticide Evaluation Scheme. Cockroaches: their biology, distribution and control by Donald G. Cochran. World Health Organization.
  • Cochran, D. G., & World Health Organization. (‎1999)‎. Communicable Diseases Prevention and Control Dept. WHO Pesticide Evaluation Scheme. Cockroaches: their biology, distribution and control by Donald G. Cochran. World Health Organization.
  • Cornwell, P. B. & Mendes, M. F. (1981). Disease organisms carried by oriental cockroaches, Blatta orientalis, in relation to acceptable standards of hygiene. lnternatational Pest Control. 23(3), 72-74.
  • Cox, C. (2004). Boric acid and borates. Journal of Pesticide Reform. 24(2), 10–15.
  • Dayer M. S., Karvandian K. (2016). Toxicity of Metarhizium anisopliae (Deuteromycota: Hyphomycetes) and boric acid against nosocomial cockroaches, Blattella germanica. Arthropods. 5(3), 114–124. Ebeling, W. (1995). Understanding and Controlling the German Cockroach. Inorganic insecticides and dusts. pp. 193–230.
  • Dayer M. S., Karvandian K. (2016). Toxicity of Metarhizium anisopliae (Deuteromycota: Hyphomycetes) and boric acid against nosocomial cockroaches, Blattella germanica. Arthropods. 5(3), 114–124. Ebeling, W. (1995). Understanding and Controlling the German Cockroach. Inorganic insecticides and dusts. pp. 193–230.
  • 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.
  • Er, M. K., Işıkber, A. A., & Tunaz, H. (2016). Effect of short time exposure of Rhyzopertha dominica adults to Beauveria bassiana conidia mixed in wheat grains. Presented at the 7th International Scientific Agriculture Symposium (Agrosym 2016) .
  • Fotedar, R., Shiniwas, U. & Verma, A. (1991). Cockroaches, Blattella germanica, as carriers of microorganisms of medical importance in hospitals. Epidemiology & lnfection. 107(1), 181-188.
  • Goettel, M. S., Lacey L. A. (1995). Current developments in microbial control of insect pests and prospects for the early 21st century. Entomophaga. 40(1), 3-27.
  • Gore, J. C., & Schal C., (2004). Laboratory evaluation of boric acid-sugar solutions as baits for management of German cockroach infestations. Journal of Economic Entomology. 97(2), 581–587.
  • Gwokyalya, R., & Altuntaş, H. (2019). Boric acid-induced immunotoxicity and genotoxicity in model insect Galleria mellonella L. (Lepidoptera: Pyralidae). Archives of insect biochemistry and physiology. 101(4), e21588.
  • Hernández-Ramírez, G., Sánchez-arroyo, H., Alatorre-Rosas, R., Robinson, W. H., & Bajomi, D. (2008). Patogenicity of Metarhizium anisopliae and Beauveria bassiana to the American cockroach (Dictyoptera: Blattidae). Proceedings of the Sixth International Conference on Urban Pests (Robinson WH, Bajomi D, eds). 143-144, OOK-Press, Kft, Hungary.
  • Hubner-Campos R.F., Leles R.N., Rodrigues J., Luz C. (2013). Efficacy of entomopathogenic hypocrealean fungi against Periplaneta americana. Parasitology International. 62(6), 517–521.
  • Khachatourians, G. G. (1998). Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria. Canadian Medical Association Journal. 159(9) 1129-1136.
  • Klowden, M. J. & Greenburg, B. (1976). Salmonella in the American cockroach: evaluation of vector potential through dosed feeding experiments. Journal of Hygiene. 77(1), 105-111.
  • Mantzoukas S., Eliopoulos P. A. 2020. Endophytic entomopathogenic fungi: A valuable biological control tool against plant pests. Applied Sciences (Switzerland). 10(1), 360. Minitab 17 Statistical Software, 2010, State College, PA: Minitab, Inc. (www.minitab.com).
  • Mantzoukas S., Eliopoulos P. A. 2020. Endophytic entomopathogenic fungi: A valuable biological control tool against plant pests. Applied Sciences (Switzerland). 10(1), 360. Minitab 17 Statistical Software, 2010, State College, PA: Minitab, Inc. (www.minitab.com).
  • Moore, R. C., Lalicker, C. G. & Fischer, A. C. (1952). lnvertebrate Fossils. McGraw-Hill, N. Y. p. 571.
  • Mullins, D. E. & Cochran, D. G. (1973). Tryptophan metabolite excretion by the American cockroach. Comparative Biochemistry & Physiology. 44(2), 549-555.
  • Murray, F. J. (1998). A comparative review of the pharmacokinetics of boric acid in rodents and humans. Biological Trace Element Research. 66(1-3), 331–341.
  • 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 Public Health. 4, 148.
  • Nirmala R., Ramanujan B., Rabindra R. J., & Rao N. S. (2005). Growth parameters of some isolates of entomofungal pathogens and production of dust-free conidia on rice medium. Journal of Biological Control. 19(2), 121-128.
  • Roth, L. M. & Willis, E. R. (1957a). The medical and veterinary importance of cockroaches. Smithsonian Miscellaneous Collections. 134(10), 1-147.
  • Roth, L. M. & Willis, E .. R. (1960). The biotoc association of cockroaches. Smithsonian Miscellaneous Collections. 141(1), 1-470.
  • Toledo-Hernández R. A., Toledo J., Valle-Mora J., Holguín-Meléndez F., Liedo P., Huerta-Palacios G. (2019). Pathogenicity and Virulence of Purpureocillium lilacinum (Hypocreales: Ophiocordycipitaceae) on Mexican Fruit Fly Adults. Florida Entomologist. 102(2), 309-314.
  • Ulewicz. K. & Zawistowski, S. (1973). Experimental studies on the epidemiological importance of the cockroach Blattella germanica (L.) in streptococcal infections on ships. Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. Erste Abteilung Originale. Reihe A: Medizinische Mikrobiologie und Parasitologie. 223(1), 77-82.
  • Yang, R., Zhang, M., Schal, C., Jiang, M., Cai, T., & Zhang, F. (2021). Boric acid enhances Metarhizium anisopliae virulence in Blattella germanica (L.) by disrupting the gut and altering its microbial community. Biological Control. 152, 104430.
  • 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.
  • Zurek, L., Watson, D.W., & Schal, C. (2002). Synergism between Metarhizium anisopliae (Deuteromycota: Hyphomycetes) and Boric Acid against the German Cockroach (Dictyoptera: Blattellidae). Biological Control. 23(4), 296-302.
  • Zurek L., Gore J.C., Stringham S.M., Watson D.W., Aldvogelm G.W., & Schal C. (2003). Boric acid dust as a component of an integrated cockroach management program in confined swine production. Journal of Economic Entomology. 96(4), 1362-1366.

Bazı Entomopatojen Fungusların Borik Asitle Birlikte Kullanımının Amerikan Hamamböceği Periplaneta americana (L.) (Blattodea: Blattidae) Erginlerine Karşı Toksisitesi

Year 2023, Volume: 26 Issue: 4, 795 - 805, 31.08.2023

İbrahim Ersin Bozdoğan , Hasan Tunaz

https://doi.org/10.18016/ksutarimdoga.vi.1221835

Abstract

Bu çalışmada, laboratuvar koşullarında bazı entomopatojen fungusların Amerikan hamamböceği Periplaneta americana (L.) erginlerine patojenitesi ve en etkili fungus izolatının borik asit ile birlikte kullanımının fungusun virülensliği üzerindeki etkisi araştırılmıştır. Testlerden elde edilen sonuçlara göre en etkili izolat Beauveria bassiana 5-4 olmuştur ve böcekler üzerinde tek başına kullanıldığında 72, 96 ve 120 saatlerde 0.1×109 konidi cm-2 dozunda sırasıyla %0, %66.6 ve %93.3 ölüm meydana getirmiştir. Bu fungus aynı zaman aralığında 0.05×109 konidi cm-2 dozunda sırasıyla %0, %20 ve %20 ölüm meydana getirmiştir. Borik asit böcekler üzerinde tek başına kullanıldığında 72, 96 ve 120 saatlerde 1 mg cm-2 dozunda sırasıyla %6.6, %40 ve %66.6 ölüm meydana getirmiştir. B. bassiana 5-4’ün 0.1×109 konidi cm-2 dozu borik asidin 1 mg cm-2 dozu ile birlikte kullanıldığında 72, 96 ve 120 saatlerde sırasıyla %33.3, %60 ve %93.3 ölüm meydana getirmiştir. B. bassiana 5-4’ün 0.05×109 konidi cm-2 dozu borik asidin 1 mg cm-2 dozu ile birlikte kullanıldığında sırasıyla 72, 96 ve 120 saatlerde %33.3, %60 ve %86.6 ölüm meydana getirmiştir. İstatistiksel analizler borik asit ve B. bassiana 5-4’ün kombine kullanımının kısa maruz kalma sürelerinde (72 ve 96 saat) fungusun virülanslığını artırdığını ancak uzun maruz kalma sürelerinde (120 saat ve üzeri) fungusun virülanslığına önemli bir etki etmediğini göstermiştir.

Keywords

Periplaneta americana Beauveria bassiana Borik asit Entomopatojen fungus Biyolojik kontrol

References

  • Artyukhina, I. N. & Evokimov, M. P. (1973). Duration of persistence in and excretion of Shigella flexeri and Shigella sonnei by Blattella germanica (L.) in individual dosed feedings (in Russian). Medical Parazitol Parazit Bol. 42(5), 602–606.
  • Ash, N. & Greenberg, B. (1980). Vector potential of the German cockroach (Dictyoptera: Blattellidae) in dissemination of Salmonella interitidis serotype typhimurium. Journal of Medical Entomology. 17(5), 417–423.
  • Barış, C. & Er, M. K. (2021). Examining Some Cereals for Mass Production of Beauveria bassiana (Balsamo) Vuillemin Conidia by Solid State Fermentation. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi. 24(6), 1263-1270.
  • Baumholtz, M. A., Parish, L. C., Witkowski, J. A. & Nutting, W. B. (1997). The medical importance of cockroaches. International Journal of Dermatology. 36(2), 90–96.
  • Burgess, N. R., McDermott, S. M. & Whiting, J. (1973a). Aerobic bacteria occurring in the hindgut of the cockroach Blatta orientalis. Journal of Hygiene. 71(1), 1–7.
  • Burgess, N. R., McDermott, S. M. & Whiting, J. (1973b). Laboratory transmission of Enterobacteriaceae by the oriental cockroach, Blatta orientalis. Journal of Hygiene. 71(1), 9–14.
  • Burgess, N. R., Chetwyn, K. N., Nunn, C J. & Shuttleworth, A. E. (1974). Some preliminary work on cockroach-infested sewers in Landon. Transactions of the Royal Society of Tropical Medicine and Hygiene. 68(1), 16. Cochran D. G. (1995). Toxic effects of boric acid on the German cockroach. Experientia. 51(6), 561–563.
  • Burgess, N. R., Chetwyn, K. N., Nunn, C J. & Shuttleworth, A. E. (1974). Some preliminary work on cockroach-infested sewers in Landon. Transactions of the Royal Society of Tropical Medicine and Hygiene. 68(1), 16. Cochran D. G. (1995). Toxic effects of boric acid on the German cockroach. Experientia. 51(6), 561–563.
  • Cochran, D. G., & World Health Organization. (‎1999)‎. Communicable Diseases Prevention and Control Dept. WHO Pesticide Evaluation Scheme. Cockroaches: their biology, distribution and control by Donald G. Cochran. World Health Organization.
  • Cochran, D. G., & World Health Organization. (‎1999)‎. Communicable Diseases Prevention and Control Dept. WHO Pesticide Evaluation Scheme. Cockroaches: their biology, distribution and control by Donald G. Cochran. World Health Organization.
  • Cornwell, P. B. & Mendes, M. F. (1981). Disease organisms carried by oriental cockroaches, Blatta orientalis, in relation to acceptable standards of hygiene. lnternatational Pest Control. 23(3), 72-74.
  • Cox, C. (2004). Boric acid and borates. Journal of Pesticide Reform. 24(2), 10–15.
  • Dayer M. S., Karvandian K. (2016). Toxicity of Metarhizium anisopliae (Deuteromycota: Hyphomycetes) and boric acid against nosocomial cockroaches, Blattella germanica. Arthropods. 5(3), 114–124. Ebeling, W. (1995). Understanding and Controlling the German Cockroach. Inorganic insecticides and dusts. pp. 193–230.
  • Dayer M. S., Karvandian K. (2016). Toxicity of Metarhizium anisopliae (Deuteromycota: Hyphomycetes) and boric acid against nosocomial cockroaches, Blattella germanica. Arthropods. 5(3), 114–124. Ebeling, W. (1995). Understanding and Controlling the German Cockroach. Inorganic insecticides and dusts. pp. 193–230.
  • 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.
  • Er, M. K., Işıkber, A. A., & Tunaz, H. (2016). Effect of short time exposure of Rhyzopertha dominica adults to Beauveria bassiana conidia mixed in wheat grains. Presented at the 7th International Scientific Agriculture Symposium (Agrosym 2016) .
  • Fotedar, R., Shiniwas, U. & Verma, A. (1991). Cockroaches, Blattella germanica, as carriers of microorganisms of medical importance in hospitals. Epidemiology & lnfection. 107(1), 181-188.
  • Goettel, M. S., Lacey L. A. (1995). Current developments in microbial control of insect pests and prospects for the early 21st century. Entomophaga. 40(1), 3-27.
  • Gore, J. C., & Schal C., (2004). Laboratory evaluation of boric acid-sugar solutions as baits for management of German cockroach infestations. Journal of Economic Entomology. 97(2), 581–587.
  • Gwokyalya, R., & Altuntaş, H. (2019). Boric acid-induced immunotoxicity and genotoxicity in model insect Galleria mellonella L. (Lepidoptera: Pyralidae). Archives of insect biochemistry and physiology. 101(4), e21588.
  • Hernández-Ramírez, G., Sánchez-arroyo, H., Alatorre-Rosas, R., Robinson, W. H., & Bajomi, D. (2008). Patogenicity of Metarhizium anisopliae and Beauveria bassiana to the American cockroach (Dictyoptera: Blattidae). Proceedings of the Sixth International Conference on Urban Pests (Robinson WH, Bajomi D, eds). 143-144, OOK-Press, Kft, Hungary.
  • Hubner-Campos R.F., Leles R.N., Rodrigues J., Luz C. (2013). Efficacy of entomopathogenic hypocrealean fungi against Periplaneta americana. Parasitology International. 62(6), 517–521.
  • Khachatourians, G. G. (1998). Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria. Canadian Medical Association Journal. 159(9) 1129-1136.
  • Klowden, M. J. & Greenburg, B. (1976). Salmonella in the American cockroach: evaluation of vector potential through dosed feeding experiments. Journal of Hygiene. 77(1), 105-111.
  • Mantzoukas S., Eliopoulos P. A. 2020. Endophytic entomopathogenic fungi: A valuable biological control tool against plant pests. Applied Sciences (Switzerland). 10(1), 360. Minitab 17 Statistical Software, 2010, State College, PA: Minitab, Inc. (www.minitab.com).
  • Mantzoukas S., Eliopoulos P. A. 2020. Endophytic entomopathogenic fungi: A valuable biological control tool against plant pests. Applied Sciences (Switzerland). 10(1), 360. Minitab 17 Statistical Software, 2010, State College, PA: Minitab, Inc. (www.minitab.com).
  • Moore, R. C., Lalicker, C. G. & Fischer, A. C. (1952). lnvertebrate Fossils. McGraw-Hill, N. Y. p. 571.
  • Mullins, D. E. & Cochran, D. G. (1973). Tryptophan metabolite excretion by the American cockroach. Comparative Biochemistry & Physiology. 44(2), 549-555.
  • Murray, F. J. (1998). A comparative review of the pharmacokinetics of boric acid in rodents and humans. Biological Trace Element Research. 66(1-3), 331–341.
  • 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 Public Health. 4, 148.
  • Nirmala R., Ramanujan B., Rabindra R. J., & Rao N. S. (2005). Growth parameters of some isolates of entomofungal pathogens and production of dust-free conidia on rice medium. Journal of Biological Control. 19(2), 121-128.
  • Roth, L. M. & Willis, E. R. (1957a). The medical and veterinary importance of cockroaches. Smithsonian Miscellaneous Collections. 134(10), 1-147.
  • Roth, L. M. & Willis, E .. R. (1960). The biotoc association of cockroaches. Smithsonian Miscellaneous Collections. 141(1), 1-470.
  • Toledo-Hernández R. A., Toledo J., Valle-Mora J., Holguín-Meléndez F., Liedo P., Huerta-Palacios G. (2019). Pathogenicity and Virulence of Purpureocillium lilacinum (Hypocreales: Ophiocordycipitaceae) on Mexican Fruit Fly Adults. Florida Entomologist. 102(2), 309-314.
  • Ulewicz. K. & Zawistowski, S. (1973). Experimental studies on the epidemiological importance of the cockroach Blattella germanica (L.) in streptococcal infections on ships. Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. Erste Abteilung Originale. Reihe A: Medizinische Mikrobiologie und Parasitologie. 223(1), 77-82.
  • Yang, R., Zhang, M., Schal, C., Jiang, M., Cai, T., & Zhang, F. (2021). Boric acid enhances Metarhizium anisopliae virulence in Blattella germanica (L.) by disrupting the gut and altering its microbial community. Biological Control. 152, 104430.
  • 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.
  • Zurek, L., Watson, D.W., & Schal, C. (2002). Synergism between Metarhizium anisopliae (Deuteromycota: Hyphomycetes) and Boric Acid against the German Cockroach (Dictyoptera: Blattellidae). Biological Control. 23(4), 296-302.
  • Zurek L., Gore J.C., Stringham S.M., Watson D.W., Aldvogelm G.W., & Schal C. (2003). Boric acid dust as a component of an integrated cockroach management program in confined swine production. Journal of Economic Entomology. 96(4), 1362-1366.
There are 39 citations in total.

Details

Primary Language English
Subjects Agricultural, Veterinary and Food Sciences
Journal Section RESEARCH ARTICLE
Authors

İbrahim Ersin Bozdoğan 0000-0002-9841-9744

Hasan Tunaz 0000-0003-4942-6056

Early Pub Date May 15, 2023
Publication Date August 31, 2023
Submission Date December 20, 2022
Acceptance Date February 2, 2023
Published in Issue Year 2023Volume: 26 Issue: 4

Cite

APA Bozdoğan, İ. E., & Tunaz, H. (2023). Toxicity of Some Entomopathogenic Fungi Combined with Boric Acid Againts Adults of American Cockroach Periplaneta americana (L.) (Blattodea: Blattidae). Kahramanmaraş Sütçü İmam Üniversitesi Tarım Ve Doğa Dergisi, 26(4), 795-805. https://doi.org/10.18016/ksutarimdoga.vi.1221835
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