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Surveys for Halyomorpha halys (Stål)(Hemiptera: Pentatomidae) and its biocontrol potential by parasitic wasps in the Republic of Georgia (Sakartvelo)

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Abstract

During field surveys in Georgia, in the 2019 and 2020 growing seasons, we investigated hazelnut orchards in four regions of Georgia: Achara, Guria, Samegrelo and Kakheti for Brown Marmorated Stink Bug (BMSB) – Halyomorpha halys (Stål)(Hemiptera: Pentatomidae). Additionally, we conducted surveys in apple and peach orchards in the Kartli and Kakheti regions to find out if there was damage caused by pentatomids and search for BMSB. Fruit damage was investigated and causes of damages were classified. Monitoring of the pest was carried out by plant beating and visual observation of trees. The BMSB was found in all visited orchards in western Georgia, while it was not detected in eastern Georgian orchards. Parasitoids were collected with sweeping nets and by rearing them from field-collected egg masses. Five species of Trissolcus Ashmead (Hymenoptera: Scelionidae), which are known parasitoids of Pentatomidae, were identified. Four of these are documented for the first time from Georgia, and two are new records for the Caucasus region.

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References

  • Bosco, L., Moraglio, S., & Tavella, L. (2018). Halyomorpha halys, a serious threat for hazelnut in newly invaded areas. Journal of Pest Science, 113, 661–670.

    Article  Google Scholar 

  • Claerebout, S., Haye, T., Ólafsson, E., Pannier, E., & Bultot, J. (2018). Première occurrence de Halyomorpha halys (Stål, 1855) (Hemiptera: Heteroptera: Pentatomidae) pour la Belgique et actualisation de sa distribution en Europe. Bullin De La Societe Royale Belge D’entomologie, 154, 205–227.

    Google Scholar 

  • Erper, I., Saruhan, I., Akca, H., Aksoy, M., & Tuncer, C. (2016). Evaluation of Some Entomopathogenic Fungi for Controlling the Green Shield bug, Palomena prasina L. (Heteroptera: Pentatomidae). Egyptian Journal of Biological Pest Control, 26, 573–578.

    Google Scholar 

  • Faundez, E., & Rider, D. (2017). The brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) in Chile. Arquivos Entomoloxicos, 17, 305–307.

    Google Scholar 

  • Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

    PubMed  CAS  Google Scholar 

  • Ganjisaffar, F., Talamas, E. J., & Bon, M. C. (2020). Perring TM First report and integrated analysis of two native Trissolcus species utilizing Bagrada hilaris eggs in California. Journal of Hymenoptera Research, 80, 49–70.

    Article  Google Scholar 

  • Gapon, D. (2019). First Records of the Brown Marmorated Stink Bug Halyomorpha halys (Stål, 1855) (Heteroptera, Pentatomidae) in Russia, Abkhazia, and Georgia. Entomological Review, 96, 1086–1088.

    Article  Google Scholar 

  • Hamilton, G. C. (2009). Brown marmorated stink bug. American. Entomologist, 55, 19–20.

    Article  Google Scholar 

  • Haye, T., Fischer, S., Zhang, J., & Gariepy, T. (2015). Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe? Journal of Pest Science, 88, 693–705.

    Article  Google Scholar 

  • Haye, T., Moraglio, S., Stahl, J., Visentin, S., Gregorio, T., & Tavella, L. (2019). Fundamental host range of Trissolcus japonicus in Europe. Journal of Pest Science, 93, 171–182.

    Article  Google Scholar 

  • Hedstrom, C., Shearer, P., Miller, J., & Walton, V. (2014). The Effects of Kernel Feeding by Halyomorpha halys (Hemiptera: Pentatomidae) on Commercial Hazelnuts. Journal of Economical Entomoltomology, 107, 1858–1865.

    Article  CAS  Google Scholar 

  • Japoshvili, G. (2000). Checklist of encyrtids (Hymenoptera: Chalcidoidea, Encyrtidae) in Georgia. Procedings of the Institute of Zoology, Georgian Academy of Science, 20, 162–173.

    Google Scholar 

  • Japoshvili, G., & Noyes, J. S. (2005). Checklist and new data on Encyrtidae (Hymenoptera: Chalcidoidea) of the Transcaucasus and Turkey. Zoosystematica Rossica, 14, 135–145.

    Article  Google Scholar 

  • Khan, F. R., & Alhewairini, S. S. (2019). Effects of insecticides on natural population of hymenopterous parasitoids in Alfalfa (Medicago sativa L.) agro-ecosystem. Pakistan Journal of Agricultural Sciences, 56, 1087–1093.

    Google Scholar 

  • Kereselidze, M., Aleksidze, G., & Haye, T. (2018). First record native parasitoid attacking Halyomorpha halys (Heteroptera: Pentatomidae) in Georgia. Bulletin. Georgian Academy of Agricultural Science, 39, 127–129.

    Google Scholar 

  • Konopka, J. K., Haye, T., Gariepy, T., Mason, P., Gillespie, D., & McNeil, J. N. (2016). An exotic parasitoid provides an invasional lifeline for native parasitoids. Ecology and Evolution, 7, 277–284.

    Article  Google Scholar 

  • Lagerstedt, H. B. (1977). The occurrence of blanks in the Þlbert Corylus Avellana L. and possible causes. Economic Botany, 31, 153–159.

    Article  Google Scholar 

  • Leskey, T., & Nielsen, A. (2018). Impact of the Invasive Brown Marmorated Stink Bug in North America and Europe: History, Biology, Ecology, and Management. Annual Revew of Entomology, 63, 599–618.

    Article  CAS  Google Scholar 

  • Leskey, T., Lee, D. H., Short, B., & Wright, S. (2012). Impact of Insecticides on the Invasive Halyomorpha halys (Hemiptera: Pentatomidae): Analysis of Insecticide Lethality. Journal of Economic Entomology, 105, 1726–1735.

    Article  CAS  Google Scholar 

  • Medal, J., Smith, T., Fox, A., Cruz, A. S., Poplin, A., & Hodges, A. (2012). Rearing the Brown Marmorated Stink Bug Halyomorpha halys (Heteroptera: Pentatomidae). Florida Entomologist, 95, 800–802.

    Article  Google Scholar 

  • Moraglio, S., Ingegno, B., & Tavella, L. (2014). Studies on Semiochemicals Produced by Gonocerus acuteangulatus for Their Use as Control Methods in Hazelnut Orchards. Proc. VIIIth International Congress on Hazelnut Eds.: P. Grau Beretta and M. Ellena. Acta Horticulture, 1052, ISHS, 281–288.

  • Murvanidze, M., Krawczyk, G., Inasaridze, N., Dekanoidze, L., Samsonadze, N., Macharashvili, M., Khutsishvili, S., & Shengelaia, S. (2018). Preliminary data on the biology of brown marmorated stink bug Halyomorpha halys (Hemiptera, Pentatomidae) in Georgia. Turkish Journal of Zoology, 42, 617–624.

    Article  Google Scholar 

  • Noyes, J. (2019). Universal Chalcidoidea Database. Available from http://www.nhm.ac.uk/chalcidoids. Accessed 12 Aug 2020

  • Rice, K. B., Bergh, C. J., Bergmann, E. J., Biddinger, D. J., Dieckhoff, C., Dively, G., Fraser, H., Gariepy, T., Hamilton, G., Haye, T., Herbert, A., Hoelmer, K., Hooks, C. R., Jones, A., Krawczyk, G., Kuhar, T., Martinson, H., Mitchell, W., Nielsen, A. L., … Tooker, J. F. (2014). Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). Journal of Integrated Pest Management, 5, 1–13.

    Article  Google Scholar 

  • Rider, D. (2015). Pentatomoidea Home page. https://www.ndsu.edu/faculty/rider/Pentatomoidea/index.htm. Accessed 15 Sept 2020

  • Roversi P. F., Binazzi F., Marianelli L., Costi E., Maistrello L. & Sabbatini Peverieri G. (2016). Searching for native egg-parasitoidsof the invasive alien species Halyomorpha halys Stal (Heteroptera, Pentatomidae) in Southern Europe. REDIA, 63–70.

  • Sabbatini Peverieri, G., Mitroiu, M.-D., Bon, M.-C., Balusu, R., Benvenuto, L., Bernardinelli, I., Fadamiro, H., Falagiarda, M., Fusu, L., Grove, E., Haye, T., Hoelmer, K., Lemke, E., Malossini, G., Marianelli, L., Moore, M. R., Pozzebon, A., Roversi, P.-F., Scaccini, D., … Talamas, E. J. (2018). Surveys of stink bug egg parasitism in Asia, Europe and North America, morphological taxonomy, and molecular analysis reveal the Holarctic distribution of Acroclisoides sinicus (Huang & Liao) (Hymenoptera, Pteromalidae). Journal of Hymenoptera Ressearch, 74, 123–151. https://doi.org/10.3897/jhr.74.46701

    Article  Google Scholar 

  • Santacruz, E., Venette, R., Dieckhoff, C., Hoelmer, K., & Koch, R. (2017). Cold tolerance of Trissolcus japonicus and T. cultratus, potential biological control agents of Halyomorpha halys, the brown marmorated stink bug. Biological Control, 107, 11–20.

    Article  Google Scholar 

  • Saruhan, I., & Tuncer, C. (2010). Research on damage rate and type of green shieldbug (Palomena prasina L. Heteroptera: Pentatomidae) on hazelnut. Anadolu Journal of Agricultural Science, 25, 75–83

  • Talamas, E., Buffington, M. & Hoelmer, K. (2017). Revision of Palearctic Trissolcus Ashmead (Hymenoptera: Scelionidae). In: Talamas, E.J.; Buffington, M.L. (Eds) Advances in the Systematics of Platygastroidea. Journal of Hymenoptera Research, 56, 3–185.

  • Tavella, L., Arzone, A., Sargiotto, C., & Sonnati, C. (1997). Coreidae and Pentatomidae harmful to hazelnuts in northern Italy (Rhynchota Heteroptera). Acta Horticulture, 445, 530–509.

    Google Scholar 

  • Tavella, L., Sonnati, C., & Arzone, A. (2001a). Sampling of Coreidae and Pentatomidae (Heteroptera) in hazelnut orchards of Piemonte, north-western Italy. Ricerca, 3, 55–59.

    Google Scholar 

  • Tavella, L., Arzone, A., Miaja, M., & Sonnati, C. (2001b). Influence of bug (Heteroptera, Coreidae and Pentatomidae) feeding activity on hazelnut in northwestern Italy. . Proc. V Int Congress on Hazelnut, Acta HortIculture, 556, 461–467.

    Google Scholar 

  • Tortorici, F., Talamas, E.J., Moraglio, S.T., Pansa, M.G., Asadi-Farfar, M., Tavella, L. & Caleca, V. (2019). A morphological, biological and molecular approach reveals four cryptic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), egg parasitoids of Pentatomidae (Hemiptera). In: Talamas, E. (Ed) Advances in the Systematics of Platygastroidea II. Journal of Hymenoptera Research, 73, 153–200.

  • Trjapitzin, V. A. (1968). survey of the encyrtid fauna (Hym. Encyrtidae) of the Caucasus. Trudy Vsesoyuznogo Entomologicheskogo Obshchestvo, 52, 43–125.

    Google Scholar 

  • Tuncer, C., Saruhan, I., & Akça, I. (2005). The Insect Pest Problem Affecting Hazelnut Kernel Quality in Turkey . Proc. VI Int Congress on Hazelnut, Acta Horticulture, 686, 367–376.

    Google Scholar 

  • Tuncer, C., Saruhan, I., & Akca, I. (2014). Seasonal Occurrence and Species Composition of True Bugs in Hazelnut Orchards . Proc. VIII Int Congress on Hazelnut, Acta Horticulture, 1052, 263–268.

    Google Scholar 

  • Wermelinger, B., Wyniger, D., & Forster, B. (2008). First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitteilungen Der Schweizerischen Entomologischen Gesellschaft, 81, 1–8.

    Google Scholar 

  • Zaitseva, I. (1997). Synopsis on the fauna of heteropterans of Georgia. Georgian Academy of Science, 1, 52.

    Google Scholar 

  • Zaitseva, I. (1998). Synopsis on the fauna of heteropterans of Georgia. Georgian Academy of Science, 2, 76.

    Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0031246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

The authors thank Jon Bremer, Matthew Moore, Cheryl Roberts and Lynn Combee for generating sequence data and uploading it to Genbank. Elijah Talamas was supported by the Florida Department of Agriculture and Consumer Services, Division of Plant Industry. Authors are grateful to Shota Rustaveli National Science Foundation and National Food Agency for financial support to conduct this study within project Ref. #NFA-SRNSF-18-121.

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Authors and Affiliations

  1. Institute of Entomology, Agricultural University of Georgia, 0159, Tbilisi, Georgia

    G. Japoshvili, T. Arabuli, M. Salakaia, Z. Tskaruashvili & G. Kirkitadze

  2. Institute of Zoology, Ilia State University, Tbilisi, Georgia

    T. Arabuli

  3. Florida Department of Agriculture and Consumer Services, Division of Plant Industry, Florida State Collection of Arthropods, Gainesville, FL, USA

    E. Talamas

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  1. G. Japoshvili
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Japoshvili, G., Arabuli, T., Salakaia, M. et al. Surveys for Halyomorpha halys (Stål)(Hemiptera: Pentatomidae) and its biocontrol potential by parasitic wasps in the Republic of Georgia (Sakartvelo). Phytoparasitica 50, 127–137 (2022). https://doi.org/10.1007/s12600-021-00949-1

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