Efficacy of Native Beauveria bassiana and B. pseudobassiana Isolates Against Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae)
Yıl 2022,
Cilt: 5 Sayı: 3, 227 - 233, 01.07.2022
İsmail Oğuz Özdemir
,
Elif Yıldırım
,
Mansur Uluca
,
Celal Tuncer
Öz
Invasive brown marmorated stinkbug (BMSB), [Halyomorpha halys (Hemiptera: Pentatomidae)] are caused significant yield and quality losses in hazelnut orchards. This study evaluated the efficacy of 7 native Beauveria bassiana and B. pseudobassiana isolates against BMSB adults at 1×108 conidia mL-1 concentration under laboratory conditions. The LT50 and LT90 values for all isolates used in the study ranged between 5.37-7.74 and 9.85-18.35 days, respectively. Moreover, the mortality rates caused by all isolates were between 72 and 96%. The lowest LT50 value (5.37 days) was recorded for TR-SM-11, whereas the lowest LT90 (9.85 days) value was noted for TR-D-1 isolate. Similarly, the LT90 and LT50 values were 10.82 and 7.74 days for TR-SM-11 and TR-D-1, respectively. The LT90 and LT50 values for TR-SK-1 isolate were 6.16 and 10.25 days, respectively. These isolates (TR-D-1, TR-SK-1, TR-SM-11) caused the highest mortality rates (96, 96 and 92%, respectively) at the end of the 11th day. TR-SM-11, TR-D-1 and TR-SK-1 isolates of B. bassiana seemed to be one of the most promising and potential biological control agents against BMSB. However, further studies are needed to evaluate the efficacy of these isolates against BMSB under field conditions.
Teşekkür
We thank M.S. Ercan Altanlar, M.S. Mehmet Yıldırım and M.S. Mertcan Cengiz for their support in some parts of the study.
Kaynakça
- Abbott WS. 1925. A method of computing the effectiveness of an insecticide. J Econ Entomol, 18: 265-267.
- Ak K, Uluca M, Aydin Ö, Gokturk T. 2019. Important invasive species and its pest status in Turkey: Halyomorpha halys (Stål) (Heteroptera: Pentatomidae). J Plant Dis Prot, 126(5): 401-408.
- Anonymous 2018. State-by-state. Stop Halyomorpha halys: management of brown marmorated stink bug in US specialty crops. URL: https://www.stopbmsb.org/where-is-bmsb/state-by-state/ (access date: March 11, 2022).
- Bariselli M, Bugiani R, Maistrello L. 2016. Distribution and damage caused by Halyomorpha halys in Italy. EPPO Bull, 46: 332-334.
- Bugti AG, Bin W, Ahmed Memo S, Khaliq G, Abuzar Jaf M. 2020. Entomopathogenic fungi: Factors involved in successful microbial control of insect pests. J Entomol, 17: 74-83.
- Burjanadze M, Kharabadze N, Сhkhidze N. 2020. Testing local isolates of entomopathogenic microorganisms against Brown Marmorated Stink Bug Halyomorpha halys in Georgia. In: Phytosanitary Technologies in Ensuring Independence and Competitiveness of the Agricultural Sector of Russia, September 9-11, 2020, St. Petersburg, Russia, pp: 6.
- Butt T, Coates C, Dubovskiy I, Ratcliffe N. 2016. Entomopathogenic fungi: new insights into host–pathogen interactions. Adv Genet, 94: 307-364.
- Erper I, Saruhan I, Akca I, Aksoy H, Tuncer C. 2016. Evaluation of some entomopathogenic fungi for controlling the Green Shield Bug, Palomena prasina L. (Heteroptera: Pentatomidae). Egypt J Biol Pest Co, 26: 573.
- Gouli V, Gouli S, Skinner M, Hamilton G, Kim JS, Parker BL. 2012. Virulence of select entomopathogenic fungi to the brown marmorated stink bug, Halyomorpha halys (Stål)(Heteroptera: Pentatomidae). Pest Manag Sci 68: 155-157.
- Haye T, Abdallah S, Gariepy T, Wyniger PS. 2014. Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci, 87: 407-418.
- Hoebeke ER, Carter ME. 2003. Halyomorpha halys (Stål)(Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc, 105: 225-237.
- Karun N, Sridhar K. 2013. Incidence of Entomophagous Medicinal Fungus, Ophiocordyceps nutans on Stink Bug, Halyomorpha halys (Stål) in the Western Ghats of India. Biol Control, 27: 139-143.
- Kistner JK. 2017. Climate change impacts on the potential distribution and abundance of the brown marmorated stink bug (Hemiptera: Pentatomidae) with special reference to North America and Europe. Environ Entomol, 46: 1212-1224.
- Kocacevik S, Sevim A, Eroğlu M, Demirbağ Z, Demir I. 2016. Virulence and horizontal transmission of Beauveria pseudobassiana SA Rehner & Humber in Ips sexdentatus and Ipstypographus (Coleoptera: Curculionidae). Turk J Agric Forest, 40(2): 241–248.
- Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively GP, Hooks CRR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka Loehr C, Myers E, Inkley D, Hoelmer KA, Lee D, Wright SE. 2012. Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag, 23: 218-226.
- Lopes RB, Laumann RA, Blassioli-Moraes MC, Borges M, Faria M. 2015. The fungistatic and fungicidal effects of volatiles from metathoracic glands of soybean-attacking stink bugs (Heteroptera: Pentatomidae) on the entomopathogen Beauveria bassiana. J Invertebr Pathol, 132: 77-85.
- Moraglio ST, Tortorici F, Pansa MG, Castelli G, Pontini M, Scovero S, Visentin S, Tavella L. 2019. A 3-year survey on parasitism of Halyomorpha halys by egg parasitoids in northern Italy. J Pest Sci, 93: 183-194.
- Nielsen AL, Hamilton GC. 2009. Life History of the Invasive Species Halyomorpha halys (Hemiptera: Pentatomidae) in Northeastern United States. J Econ Entomol, 102(4): 608-616.
- Ozdemir IO, Tuncer C, Ozer G. 2021. Molecular characterisation and efficacy of entomopathogenic fungi against the Green shield bug Palomena prasina (L.) (Hemiptera: Pentatomidae) under laboratory conditions. Biocontrol Sci Techn, 31(12), 1298-1313.
- Ozdemir IO, Tuncer C. 2021. A new invasive polyphagous pest in Turkey, brown marmorated stink bug [Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae)]: identification, similar species and current status. BSJ Eng Sci, 4(2): 58-67.
- Parker BL, Skinner M, Gouli S, Gouli V, Kim JS. 2015. Virulence of BotaniGard® to second instar brown marmorated stink bug, Halyomorpha halys (Stål)(Heteroptera: Pentatomidae). Insects, 6: 319-324.
- Patel DT, Fuxa JR, Stout MJ. 2006. Evaluation of B. bassiana for control of Oebalus pugnax (Hemiptera: Pentatomidae) in rice. J Entomol Sci, 41: 126-146.
- Peverieri GS, Talamas E, Bon MC, Marianelli L, Bernardinelli I, Malossini G, Benvenuto L, Roversi PF, Hoelmer K. 2018. Two asian egg parasitoids of Halyomorpha halys (Stål)(Hemiptera, Pentatomidae) emerge in northern italy: Trissolcus mitsukurii (Ashmead) and Trissolcus japonicus (Ashmead)(Hymenoptera, Scelionidae). J Hymenopt Res, 67: 37.
- Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T. 2014. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integrated Pest Manag, 5(3): A1–A13.
- Robertson JL, Russell RM, Preisler HK, Savin N. 2017. Bioassays with arthropods. CRC Press, New York, US, pp: 212.
- Sevim A, Demir I, Höfte M, Humber RA, Demirbag Z. 2010. Isolation and characterization of entomopathogenic fungi from hazelnut-growing region of Turkey. Biocontrol, 55: 279-297.
- Sosa-Gómez DR, Moscardi F. 1998. Laboratory and field studies on the infection of Stink Bugs, Nezara viridula, Piezodorus guildinii, and Euschistus heros (Hemiptera: Pentatomidae) with Metarhizium anisopliae and B. bassiana in Brazil. J Invertebr Pathol, 71: 115-120.
- Stahl J, Tortorici F, Pontini M, Bon MC, Hoelmer K, Marazzi C, Tavella L, Haye T. 2019. First discovery of adventive populations of Trissolcus japonicus in Europe. J Pest Sci, 92: 371-379.
- Talamas EJ, Herlihy MV, Dieckhoff C, Hoelmer KA, Buffington M, Bon MC, Weber DC. 2015. Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America. J Hymenopt Res, 43: 119.
- Tozlu E, Saruhan I, Tozlu G, Dadaşoğlu F, Tekiner N. 2019. Potentials of some entomopathogens against the brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae). Egypt J Biol Pest Cont, 29(1): 1-8.
- Tuncer C, Kushiyev R, Erper I, Ozdemir IO, Saruhan I. 2019. Efficacy of native isolates of Metarhizium anisopliae and B. bassiana against the invasive ambrosia beetle, Xylosandrus germanus Blandford (Coleoptera: Curculionidae: Scolytinae). Egypt J Biol Pest Cont, 29(1): 28.
- Yang Z-Q, Yao Y-X, Qiu L-F, Li Z-X. 2009. A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology. Ann Entomol Soc Am, 102: 39-47.
- Zhu G, Bu W, Gao Y, Liu G 2012. Potential Geographic Distribution of Brown Marmorated Stink Bug Invasion (Halyomorpha halys). PloS One, 7(2): e31246.
Yıl 2022,
Cilt: 5 Sayı: 3, 227 - 233, 01.07.2022
İsmail Oğuz Özdemir
,
Elif Yıldırım
,
Mansur Uluca
,
Celal Tuncer
Kaynakça
- Abbott WS. 1925. A method of computing the effectiveness of an insecticide. J Econ Entomol, 18: 265-267.
- Ak K, Uluca M, Aydin Ö, Gokturk T. 2019. Important invasive species and its pest status in Turkey: Halyomorpha halys (Stål) (Heteroptera: Pentatomidae). J Plant Dis Prot, 126(5): 401-408.
- Anonymous 2018. State-by-state. Stop Halyomorpha halys: management of brown marmorated stink bug in US specialty crops. URL: https://www.stopbmsb.org/where-is-bmsb/state-by-state/ (access date: March 11, 2022).
- Bariselli M, Bugiani R, Maistrello L. 2016. Distribution and damage caused by Halyomorpha halys in Italy. EPPO Bull, 46: 332-334.
- Bugti AG, Bin W, Ahmed Memo S, Khaliq G, Abuzar Jaf M. 2020. Entomopathogenic fungi: Factors involved in successful microbial control of insect pests. J Entomol, 17: 74-83.
- Burjanadze M, Kharabadze N, Сhkhidze N. 2020. Testing local isolates of entomopathogenic microorganisms against Brown Marmorated Stink Bug Halyomorpha halys in Georgia. In: Phytosanitary Technologies in Ensuring Independence and Competitiveness of the Agricultural Sector of Russia, September 9-11, 2020, St. Petersburg, Russia, pp: 6.
- Butt T, Coates C, Dubovskiy I, Ratcliffe N. 2016. Entomopathogenic fungi: new insights into host–pathogen interactions. Adv Genet, 94: 307-364.
- Erper I, Saruhan I, Akca I, Aksoy H, Tuncer C. 2016. Evaluation of some entomopathogenic fungi for controlling the Green Shield Bug, Palomena prasina L. (Heteroptera: Pentatomidae). Egypt J Biol Pest Co, 26: 573.
- Gouli V, Gouli S, Skinner M, Hamilton G, Kim JS, Parker BL. 2012. Virulence of select entomopathogenic fungi to the brown marmorated stink bug, Halyomorpha halys (Stål)(Heteroptera: Pentatomidae). Pest Manag Sci 68: 155-157.
- Haye T, Abdallah S, Gariepy T, Wyniger PS. 2014. Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci, 87: 407-418.
- Hoebeke ER, Carter ME. 2003. Halyomorpha halys (Stål)(Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc, 105: 225-237.
- Karun N, Sridhar K. 2013. Incidence of Entomophagous Medicinal Fungus, Ophiocordyceps nutans on Stink Bug, Halyomorpha halys (Stål) in the Western Ghats of India. Biol Control, 27: 139-143.
- Kistner JK. 2017. Climate change impacts on the potential distribution and abundance of the brown marmorated stink bug (Hemiptera: Pentatomidae) with special reference to North America and Europe. Environ Entomol, 46: 1212-1224.
- Kocacevik S, Sevim A, Eroğlu M, Demirbağ Z, Demir I. 2016. Virulence and horizontal transmission of Beauveria pseudobassiana SA Rehner & Humber in Ips sexdentatus and Ipstypographus (Coleoptera: Curculionidae). Turk J Agric Forest, 40(2): 241–248.
- Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively GP, Hooks CRR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka Loehr C, Myers E, Inkley D, Hoelmer KA, Lee D, Wright SE. 2012. Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag, 23: 218-226.
- Lopes RB, Laumann RA, Blassioli-Moraes MC, Borges M, Faria M. 2015. The fungistatic and fungicidal effects of volatiles from metathoracic glands of soybean-attacking stink bugs (Heteroptera: Pentatomidae) on the entomopathogen Beauveria bassiana. J Invertebr Pathol, 132: 77-85.
- Moraglio ST, Tortorici F, Pansa MG, Castelli G, Pontini M, Scovero S, Visentin S, Tavella L. 2019. A 3-year survey on parasitism of Halyomorpha halys by egg parasitoids in northern Italy. J Pest Sci, 93: 183-194.
- Nielsen AL, Hamilton GC. 2009. Life History of the Invasive Species Halyomorpha halys (Hemiptera: Pentatomidae) in Northeastern United States. J Econ Entomol, 102(4): 608-616.
- Ozdemir IO, Tuncer C, Ozer G. 2021. Molecular characterisation and efficacy of entomopathogenic fungi against the Green shield bug Palomena prasina (L.) (Hemiptera: Pentatomidae) under laboratory conditions. Biocontrol Sci Techn, 31(12), 1298-1313.
- Ozdemir IO, Tuncer C. 2021. A new invasive polyphagous pest in Turkey, brown marmorated stink bug [Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae)]: identification, similar species and current status. BSJ Eng Sci, 4(2): 58-67.
- Parker BL, Skinner M, Gouli S, Gouli V, Kim JS. 2015. Virulence of BotaniGard® to second instar brown marmorated stink bug, Halyomorpha halys (Stål)(Heteroptera: Pentatomidae). Insects, 6: 319-324.
- Patel DT, Fuxa JR, Stout MJ. 2006. Evaluation of B. bassiana for control of Oebalus pugnax (Hemiptera: Pentatomidae) in rice. J Entomol Sci, 41: 126-146.
- Peverieri GS, Talamas E, Bon MC, Marianelli L, Bernardinelli I, Malossini G, Benvenuto L, Roversi PF, Hoelmer K. 2018. Two asian egg parasitoids of Halyomorpha halys (Stål)(Hemiptera, Pentatomidae) emerge in northern italy: Trissolcus mitsukurii (Ashmead) and Trissolcus japonicus (Ashmead)(Hymenoptera, Scelionidae). J Hymenopt Res, 67: 37.
- Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T. 2014. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integrated Pest Manag, 5(3): A1–A13.
- Robertson JL, Russell RM, Preisler HK, Savin N. 2017. Bioassays with arthropods. CRC Press, New York, US, pp: 212.
- Sevim A, Demir I, Höfte M, Humber RA, Demirbag Z. 2010. Isolation and characterization of entomopathogenic fungi from hazelnut-growing region of Turkey. Biocontrol, 55: 279-297.
- Sosa-Gómez DR, Moscardi F. 1998. Laboratory and field studies on the infection of Stink Bugs, Nezara viridula, Piezodorus guildinii, and Euschistus heros (Hemiptera: Pentatomidae) with Metarhizium anisopliae and B. bassiana in Brazil. J Invertebr Pathol, 71: 115-120.
- Stahl J, Tortorici F, Pontini M, Bon MC, Hoelmer K, Marazzi C, Tavella L, Haye T. 2019. First discovery of adventive populations of Trissolcus japonicus in Europe. J Pest Sci, 92: 371-379.
- Talamas EJ, Herlihy MV, Dieckhoff C, Hoelmer KA, Buffington M, Bon MC, Weber DC. 2015. Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America. J Hymenopt Res, 43: 119.
- Tozlu E, Saruhan I, Tozlu G, Dadaşoğlu F, Tekiner N. 2019. Potentials of some entomopathogens against the brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae). Egypt J Biol Pest Cont, 29(1): 1-8.
- Tuncer C, Kushiyev R, Erper I, Ozdemir IO, Saruhan I. 2019. Efficacy of native isolates of Metarhizium anisopliae and B. bassiana against the invasive ambrosia beetle, Xylosandrus germanus Blandford (Coleoptera: Curculionidae: Scolytinae). Egypt J Biol Pest Cont, 29(1): 28.
- Yang Z-Q, Yao Y-X, Qiu L-F, Li Z-X. 2009. A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology. Ann Entomol Soc Am, 102: 39-47.
- Zhu G, Bu W, Gao Y, Liu G 2012. Potential Geographic Distribution of Brown Marmorated Stink Bug Invasion (Halyomorpha halys). PloS One, 7(2): e31246.