Türkiye’de istilacı kahverengi kokarcanın [Halyomorpha Halys Stal (Hemiptera: Pentatomidae)] yerli yumurta parazitoiti Telenomus Turesis (Walker)’in ilk kaydı

Year 2023, Volume: 38 Issue: 2, 373 - 384, 04.07.2023

İsmail Oğuz Özdemir

https://doi.org/10.7161/omuanajas.1284171

Cited By: 1

Abstract

Halyomorpha halys (Hemiptera: Pentatomidae) Doğu Asya (Çin, Japonya, Kore ve Tayvan) kökenli bir türdür ve doğal yaşam alanlarında önemli bir polifag zararlı olup, yayılış gösterdiği alanları kısa zaman içerisinde yüksek bir popülasyon meydana getirerek istila etmekte ve tarımsal üretim için önemli bir tehdit oluşturmaktadır. Türkiye’de özellikle Karadeniz sahil şeridi boyunca yayılış gösterdiği alanlar içerisinde başta fındık olmak üzere pek çok üründe önemli kalite ve verim kaybına sebep olabilir. Bu çalışma, Sakarya’da farklı habitatlarda H. halys'in yerli yumurta parazitoitlerini ve bu türlerin etkinliklerini belirlemeyi amaçlamaktadır. Bu amaçla, arazi şartlarında elde edilen bir günlük yaştaki 20 yumurta paketi (600 yumurta) 9 farklı lokasyonda farklı bitkilere asılmış ve 4 gün sonra toplanarak laboratuvara getirilmiştir. Toplanan yumurtaların genel parazitlenme oranı %7,5 olmasına rağmen, bu yumurtalardan başarılı bir şekilde yalnızca üç parazitoit çıkışı meydana gelmiştir. Morfolojik olarak teşhisleri yapılan bu parazitoitler, sitokrom c oksidaz alt birim I genine (CO1) dayalı moleküler teşhis ile doğrulanarak, Telenomus turesis (Walker) olduğu belirlenmiştir. Halyomorpha halys’in yerli yumurta parazitoit türü, bu çalışma ile Türkiye’de ilk kez rapor edilmektedir. Bu kapsamda istilacı türün ülkemizde yayılış gösterdiği alanlarda doğal düşman faunasının araştırılması, mücadele için önemli aşamalardan birisi olup daha fazla araştırmaya ihtiyaç duyulmaktadır. Ek olarak, uzun vadeli sürdürülebilir yaklaşım olan klasik biyolojik mücadele kapsamında, ithalatı gerçekleştirilen Trissolcus japonicus (Ashmead)’un hızlı ve kontrollü bir şekilde kitlesel üretimine geçilmesi ve salımı yüksek derece önem arz etmektedir.

Keywords

Türkiye, İstilacı tür, Pis kokulu böcek, Biyolojik mücadele, Doğal düşman

Supporting Institution

-

Project Number

-

Thanks

Parazitoitlerin morfolojik teşhisinin yapılması hususunda destek veren Dr. Francesco Tortorici’ye ve çalışmanın bazı kısımlarında yardım eden Arş. Gör. Furkan Doğan’a teşekkür ederim.

First record of Telenomus turesis (Walker), native egg parasitoid of invasive brown marmorated stink bug [Halyomorpha halys stal (Hemiptera: Pentatomidae)] in Turkey

Abstract

Halyomorpha halys (Hemiptera: Pentatomidae) is a native insect to East Asia (China, Japan, Korea, and Taiwan), and the insect, which is an important polyphagous pest in its natural habitat, invades areas where it poses a significant threat to crop production, establishing a large population in a short period. It may significantly decrease the yield and quality on many products, as well as hazelnuts, especially in areas where it spreads along Turkey's Black Sea coastline. The purpose of this research is to determine the native egg parasitoids of H. halys and their effectiveness in various habitats in Sakarya. For this reason, 20 egg masses (600 eggs) of H. halys at < 24 h-old obtained under field conditions were exposed to field condition on different plants in 9 different locations, and these were carried to the laboratory, collecting 4 days after field exposure. Despite the fact that the overall parasitism rate of the collected eggs was 7.5%, only three parasitoids emerged successfully from these eggs. These parasitoids were identified morphologically as Telenomus turesis (Walker), which was confirmed by molecular identification using the cytochrome c oxidase subunit I gene (CO1). With this study, the native egg parasitoid species was reported for the first time in Turkey. One of the critical stages of the management is the investigation of natural enemy fauna in areas in which invasive species have spread in Turkey, and additional studies are needed. Furthermore, quick and controlled mass production and release of imported Trissolcus japonicus (Ashmead) is critical within the framework of classical biological control, which is a long-term sustainable method.

Keywords

Turkey, Invasive species, Stink bug, Biological control, Natural enemy

Project Number

-

References

• Abram, P.K., Gariepy, T.D., Boivin, G., Brodeur, J., 2014. An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biological Invasions, 16, 1387–1395.
• Abram, P.K., Brodeur, J., Burte, V. Boivin, G., 2016. Parasitoid-induced host egg abortion: an underappreciated component of biological control services provided by egg parasitoids. Biological Control, 98, 52–60.
• Abram, P.K., Brodeur, J., Urbaneja, A., Tena, A., 2019. Nonreproductive effects of insect parasitoids on their hosts. Annual Review of Entomology, 64, 259–276.
• Adachi, I., Uchino, K., Mochizuki, F., 2007. Development of a pyramidal trap for monitoring fruit-piercing stink bugs baited with Plautia crossota stali (Hemiptera: Pentatomidae) aggregation pheromone. Applied entomology and Zoology, 42(3), 425-431.
• Ak, K., Uluca, M., Tuncer, C., 2023. Distribution and population density of Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) in Black Sea Region of Türkiye. Turkish Journal of Zoology, 47(2), 120-129.
• Ak, K., Uluca, M., Aydın, O., Göktürk, T., 2019. Important invasive species and its pest status in Turkey: Halyomorpha halys (Stål)(Heteroptera: Pentatomidae). Journal of Plant Diseases and Protection, 126(5), 401-408.
• Altanlar, E., Kılıc, M., Altas, K., Talamas, E., Tuncer, C., 2023. First Record of Native Egg Parasitoid, Anastatus bifasciatus, on Halyomorpha halys (Stål, 1855)(Hemiptera: Pentatomidae) Eggs in Türkiye. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 26(3), 545-551.
• Anonymous, 2018. State-by-state. Stop Halyomorpha halys: management of brown marmorated stink bug in US specialty crops. https://www.stopbmsb.org/whereis-bmsb/stateby-state/ (Erişim Tarihi: 18 Nisan 2019)
• Bariselli, M., Bugiani, R., Maistrello, L., 2016. Distribution and damage caused by Halyomorpha halys in Italy. Eppo Bulletin, 46(2), 332-334.
• Bout, A., Tortorici, F., Hamidi, R., Warot, S., Tavella, L., Thomas, M., 2021. First detection of the adventive egg parasitoid of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) in France. Insects. 12, 761.
• Çerci, B., Koçak, O., 2017. Further contribution to the Heteroptera (Hemiptera) fauna of Turkey with a new synonymy. Acta Biologica Turcica, 30(4), 121-127.
• Gariepy, T.D., Haye, T., Zhang, J., 2014. A molecular diagnostic tool for the preliminary assessment of host-parasitoid associations in biological control programmes for a new invasive pest. Molecular Ecology 23, 3912–3924.
• Gariepy, T.D., Bruin, A., Konopka, J., Scott-Dupree, C., Fraser, H., 2019. A modified DNA barcode approach to define trophic interactions between native and exotic pentatomids and their parasitoids. Molecular Ecology 28, 456–470.
• Güncan, A., Gümüş, E., 2019. Brown marmorated stink bug, Halyomorpha halys (Stål, 1855)(Hemiptera: Heteroptera, Pentatomidae), a new and important pest in Turkey. Entomological News, 128(2), 204-210.
• Haye, T., Abdallah, S., Gariepy, T., Wyniger, D., 2014. Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. Journal of Pest Science, 87(3), 407-418.
• Haye, T., Gariepy, T., Hoelmer, K., Rossi, J. P., Streito, J. C., Tassus, X., Desneux, N., 2015. Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. Journal of Pest Science, 88(4), 665-673.
• Herlihy, M.V., Talamas, E.J., Weber, D.C., 2016. Attack and success of native and exotic parasitoids on eggs of Halyomorpha halys in three Maryland habitats. PLoS ONE, 11:e0150275.
• Hoebeke, E. R., Carter, M. E., 2003. Halyomorpha halys (Stǻl) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proceedings of the Entomological Society of Washington, 105 (1), 225-237.
• Inkley, D. B., 2012. Characteristics of home invasion by the brown marmorated stink bug (Hemiptera: Pentatomidae). Journal of Entomological Science, 47(2), 125-130.
• Jones, A.L., Jennings, D.E., Hooks, C.R.R., Shrewsbury, P.M., 2014. Sentinel eggs underestimate rates of parasitism of the exotic brown marmorated stink bug, Halyomorpha halys. Biological Control, 78, 61–66.
• Kaser, J.M., Nielsen, A.L., Abram, P.K., 2018. Biological control effects of non-reproductive host mortality caused by insect parasitoids. Ecological Applications 28, 1081–1092.
• Konopka, J.K., Gariepy, T.D., Haye, T., Zhang, J., Rubin, B.D., McNeil, J.N., 2019. Exploitation of pentatomids by native egg parasitoids in the native and introduced ranges of Halyomorpha halys: a molecular approach using sentinel egg masses. Journal of Pest Science 98, 609–619.
• Kuhar, T.H., Kamminga, K.L., 2017. Review of the chemical control research on Halyomorpha halys in the USA, Journal of pest science, 90, 1021–1031.
• Leskey, T. C., Hamilton, G. C., Nielsen, A. L., Polk, D. F., Rodriguez-Saona, C., Bergh, J. C., …Wright, S. E., 2012a. Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks on Pest Management, 23(5), 218-226.
• Leskey, T. C., Lee, D. H., Short, B. D., Wright, S. E., 2012b. Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. Journal of Economic Entomology, 105(5), 1726-1735.
• Lee, D.H., Short, B.D., Joseph, S.V., Bergh, J.C., Leskey, T.C., 2013. Review of the biology; ecology; and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China; Japan; and the Republic of Korea. Environmental Entomology, 42, 627–641.
• Leskey, T. C., Nielsen, A. L., 2018. Impact of the invasive brown marmorated stink bug in North America and Europe: history, biology, ecology, and management. Annual Review of Entomology, 63, 599-618.
• Moraglio, S. T., Tortorici, F., Pansa, M. G., Castelli, G., Pontini, M., Scovero, S., …Tavella, L., 2020. A 3-year survey on parasitism of Halyomorpha halys by egg parasitoids in northern Italy. Journal of Pest Science, 93, 183-194.
• Moraglio, S. T., Tortorici, F., Giromini, D., Pansa, M. G., Visentin, S., Tavella, L., 2021. Field collection of egg parasitoids of Pentatomidae and Scutelleridae in Northwest Italy and their efficacy in parasitizing Halyomorpha halys under laboratory conditions. Entomologia Experimentalis et Applicata, 169(1), 52-63.
• Morrison III, W. R., Blaauw, B. R., Nielsen, A. L., Talamas, E., Leskey, T. C., 2018. Predation and parasitism by native and exotic natural enemies of Halyomorpha halys (Stål)(Hemiptera: Pentatomidae) eggs augmented with semiochemicals and differing host stimuli. Biological Control, 121, 140-150.
• Nielsen, A. L., Hamilton, G. C., 2009. Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in northeastern United States. Annals of the Entomological Society of America, 102(4), 608-616.
• Ogburn, E.C., Bessin, R., Dieckhoff, C., Dobson, R., Grieshop, M., Hoelmer, K.A., Mathews, C., Moore, J., Nielsen, A.L., Poley, K., et al., 2016. Natural enemy impact on eggs of the invasive brown marmorated stink bug; Halyomorpha halys (Stål) (Hemiptera: Pentatomidae); in organic agroecosystems: A regional assessment. Biological Control, 101, 39–51.
• Ozdemir, I. O., Tuncer, C., Tortorici, F., Ozer, G., 2022. Egg parasitoids of green shield bug, Palomena prasina L.(Hemiptera: Pentatomidae) in hazelnut orchards of Turkey. Biocontrol Science and Technology, 33(1), 65-75.
• Qiu, L.-F., 2010. Natural enemy species of Halyomorpha halys and control effects of the parasitoids species in Beijing. Northern Hortic, 9, 181–183.
• Rice, K. B., Bergh, C. J., Bergmann, E. J., Biddinger, D. J., Dieckhoff, C., Dively, G., ... Tooker, J. F., 2014. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). Journal of Integrated Pest Management, 5(3), A1-A13.
• Roversi, P.F., Maltese, M., Simoni, S., Cascone, P., Binazzi, F., Strangi, A., Sabbatini Perevieri, G., Guerrieri, E., 2016. Graphosoma lineatum (Hemiptera: Pentatomidae): A suitable host for mass rearing Ooencyrtus telenomicida (Hymenoptera: Encyrtidae). International Journal of Pest Management, 64, 294–302.
• Sabbatini Peverieri, G., Talamas, E.J., Bon, M.-C. Marianelli, L., Bernardinelli, I., Malossini, G., Benvenuto, L., Roversi, P.F., 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). Journal of Hymenopteran Research, 67, 37–53.
• Sabbatini-Peverieri G., Dieckhoff C., Giovannini L., Marianelli L., Roversi P.F., Hoelmer K., 2020. Rearing Trissolcus japonicus and Trissolcus mitsukurii for biological control of Halyomorpha halys. Insects. 11,787.
• Şener, A., Uçkan, F., Koçak, E., & Soydabaş, H.K., 2018. Egg parasitoids of Sunn Pest and their effectiveness in Kocaeli province. Kocaeli Univeristesi Fen Bilimleri Dergisi, 1(1), 8–12.
• Stahl, J., Tortorici, F., Pontini, M., Bon, M. C., Hoelmer, K., Marazzi, C., ... Haye, T., 2019. First discovery of adventive populations of Trissolcus japonicus in Europe. Journal of Pest Science, 92, 371-379.
• Talamas, E.J., Herlihy, M.V., Dieckhoff, C., Hoelmer, K.A., Buffington, M., Bon, M.-C., Weber, D.C., 2015. Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America. Journal of Hymenopteran Research, 43, 119–128.
• Talamas, E.J., Bon, M.C., Hoelmer, K.A., Buffington, M.L., 2019. Molecular phylogeny of Trissolcus wasps (Hymenoptera, Scelionidae) associated with Halyomorpha halys (Hemiptera, Pentatomidae). Journal of Hymenoptera Research, 73, 201.
• Weber, D.C., Leskey, T.C., Walsh, G.C., Khrimian, A., 2014. Synergy of aggregation pheromone with methyl (E, E, Z) -2, 4, 6-decatrienoate in attraction of Halyomorpha halys (Hemiptera: Pentatomidae). Journal of Economic Entomology, 107, 1061–1068.
• Weber, D. C., Morrison, W. R., Khrimian, A., Rice, K. B., Leskey, T. C., Rodriguez-Saona, C., Blaauw, B. R., 2017. Chemical ecology of Halyomorpha halys: discoveries and applications. Journal of Pest Science, 90(4), 989-1008.
• 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. Annals of the Entomological Society of America, 102, 39–47.
• Zapponi, L., Tortorici, F., Anfora, G., Bardella, S., Bariselli, M., Benvenuto, L., ... Sabbatini-Peverieri, G., 2021. Assessing the distribution of exotic egg parasitoids of Halyomorpha halys in Europe with a large-scale monitoring program. Insects, 12(4), 316.
• Zhang, J., Zhang, F., Gariepy, T., Mason, P., Gillespie, D., Talamas, E., Haye, T., 2017. Seasonal parasitism and host specificity of Trissolcus japonicus in northern China. Journal of Pest Science 90, 1127–1141.