New records of the parasitoids of Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) in newly invaded areas in Turkey: molecular identification

Yıl 2020, , 71 - 79, 01.03.2020

Gülay Kaçar

https://doi.org/10.16970/entoted.607415

Cited By: 6

Öz

Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) is an invasive pest species of various fruit crops in the USA and Europe. Although D. suzukii has been recently reported in strawberry in Erzurum and other newly invaded areas in Turkey (e.g., Ankara, Bolu, Çanakkale and Düzce), there is only limited information on its indigenous parasitoids. In this study, four hymenopteran parasitoids, the larval parasitoids of Leptopilina boulardi (Barbotin, Carton & Kelner-Pillault, 1979), Leptopilina heterotoma (Thomson, 1862) (Figitidae) and the pupal parasitoids of Pachycrepoideus vindemmiae (Rondani, 1875) (Pteromalidae) and Trichopria drosophilae (Perkins, 1910) (Diapriidae), were collected from frugivorous drosophilid species. Leptopilina boulardi and T. drosophilae were found for the first time in Turkey. Leptopilina heterotoma and P. vindemmiae were the most common parasitoid species, reared from field-collected fruit samples in this study. The laboratory assays revealed that both pupal parasitoids developed from D. suzukii pupae, but the association of L. heterotoma and L. boulardi with D. suzukii is yet to be confirmed. The PCR amplification of the cytochrome c oxidase subunit I loci of mtDNA of the representative four parasitoid samples produced different lengths of DNA fragments, ranging from 633 bp to 658 bp. BLASTn queries based on the COI of the parasitoid samples showed that the sequences were 99-100% identical to those of the corresponding species in the GenBank database.

Anahtar Kelimeler

Molecular diagnostic, new parasitoids, spotted wing drosophila, Turkey

Teşekkür

The author thanks to Assoc. Prof. Göksel Özer (Bolu Abant Izzet Baysal University, Agriculture and Science Faculty, Bolu, Turkey) for cooperation with the molecular identification.

Türkiye’de yeni istila edilen alanlarda Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae)’nin yeni parazitoit kayıtları: moleküler tanımlamaları

Öz

Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae), Avrupa ve Amerika’da çeşitli meyvelerde zarara neden olan istilacı bir türdür. Drosophila suzukii, son zamanlarda Türkiye’de Erzurum’da çilekte rapor edilmesine ve o zamandan beri yeni alanları (Ankara, Bolu, Çanakkale ve Düzce vs.) istila etmesine rağmen, onun yerli parazitoitleri çok az bilinmektedir. Bu çalışmada, dört hymenopter parazitoit, larval parazitoitler Leptopilina boulardi (Barbotin, Carton & Kelner-Pillault, 1979), Leptopilina heterotoma (Thomson, 1862) (Figitidae) ve pupal parazitoitler Pachycrepoideus vindemmiae (Rondani, 1875) (Pteromalidae) ve Trichopria drosophilae (Perkins, 1910) (Diapriidae) türleri, meyvelerde bulunan drosophilid türlerinden elde edilmiştir. Leptopilina boulardi ve T. drosophilae türlerinin Türkiye’de ilk defa varlığı belirlenmiştir. Leptopilina heterotoma ve P. vindemmiae, toplanan örneklerden en fazla bulunan türler olmuştur. Laboratuvar denemeleri iki pupa parazitoitinin D. suzukii pupalarından geliştiğini belirlenmesine rağmen, L. heterotoma ve L. boulardi’nin D. suzukii’den geliştiklerini hala doğrulanamamıştır.  Dört parazitoit türü temsil eden örneklerin mitokondrial DNA’sının cytochrome c oxidase subunit I lokusunun PCR ile çoğaltılması sonucu 633 bp ile 658 bp arasında DNA segmentlerini ürettiği belirlenmiştir. Bu ürünlerin BLASTn analizi sonucu GenBank’daki referans bireylerin sekanslarıyla %99-100 benzerliğe sahip olduğu tespit edilmiştir.

Anahtar Kelimeler

Moleküler tanımlama, yeni parazitoitler, noktalı kanatlı drosophila, Türkiye

Kaynakça

• Allemand, R., C. Lemaître, F. Frey, M. Boulétreau, F. Vavre, G. Nordlander, J. van Alphen & Y. Carton, 2002. Phylogeny of six African Leptopilina species (Hymenoptera: Cynipoidea, Figitidae), parasitoids of Drosophila, with description of three new species. Annales de la Société Entomologique de France, 38: 319-332.
• Berry, J. A., 2012. Pest Risk Assessment: Drosophila suzukii: spotted wing drosophila (Diptera: Drosophilidae) on fresh fruit from the USA. Ministry for Primary Industries. MPI Technical Paper No: 2012/05, New Zealand Government, Ministry for Primary Industries. (Web page: www.mpi.govt.nz/documentvault/2897) (Date accessed: August 2019).
• Bolda, M., R. E. Goodhue & F. G. Zalom, 2010. Spotted wing drosophila: potential economic impact of a newly established pest. Giannini Foundation of Agricultural Economics, University of California Agricultural and Resource Economics, 13: 5-8.
• Boucek, Z. & J. Y. Rasplus, 1991. Illustrated Key to West-Palearctic Genera of Pteromalidae (Hymenoptera: Chalcidoidea). INRA, Paris, 140 pp.
• Carton, Y., M. Boule´treau, J. J. M. Van Alphen & J. C. van Lenteren, 1986. “The Drosophila Parasitic Wasps, 347-394”. In: The Genetics and Biology of Drosophila (Eds. M. Ashburner, H. L. Carson & J. N. Thompson) Volume 3e. Academic Press, New York, USA, 430 pp.
• Chabert, S., R. Allemand, M. Poyet, P. Eslin & P. Gibert, 2012. Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biological Control, 63: 40-47.
• Daane, K. M., X. G. Wang, A. Biondi, B. Miller, J. C. Miller, H. Riedl, P. W. Shaerer, E. Guerrieri, M. Giorgini, M. Buffıngton, K. van Achterberg, Y. Song, T. Kang, H. YI, C. Jung, D. W. Lee, B. Chung, K. A. Hoelmer & V. M. Walton, 2016. First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. Journal of Pest Science, 89: 823-835.
• Dalton, D. T., V. M. Walton, P. W. Shearer, D. B. Walsh, J. Caprile & R. Isaacs, 2011. Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific Northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Management Science, 67: 1368-1374.
• Depra, M., J. L. Poppe, H. J. Schmits, C. Toni & V. L. S. Valente, 2014. The first records of the Drosophila suzukii invasive pest in the South American continent. Journal of Pest Sciences, 87: 379-383.
• Efil, L., 2018. Çanakkale İli çilek alanlarında yeni bir zararlı Drosophila suzukii (Matsumura) (Diptera: Drosophilidae)’nin yayılış alanları ve bulaşıklılığı. Türk Tarım ve Doğa Bilimleri Dergisi, 5 (3): 280-284.
• Emiljanowicz, L. M., G. D. Ryan, A. Langille & J. Newman, 2014. Development, reproductive output and population growth of the fruit fly pest Drosophila suzukii (Diptera: Drosophilidae) on artificial diet. Journal of Economic Entomology, 107 (4): 1392-1398.
• EPPO, 2002. Drosophila suzukii (DROSSU). (Web page: https://gd.eppo.int/taxon/DROSSU) (Date accessed: August 2019).
• Farrokhzadeh, H., G. Moravvej, M. M. Awal & J. Karımı, 2014. Molecular and morphological identification of hymenoptran parasitoids from the pomegranate aphid, Aphis punicae in RazavinKhorasan province, Iran. Turkish Journal of Entomology, 38 (3): 291-306.
• Fleury, F., N. Ris, R. Allemand, P. Fouillet, Y. Carton & M. Boule´treau, 2004. Ecological and genetic interactions in Drosophila-parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in southeastern France. Genetica, 120 (1-3):181-194.
• Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5): 294-299.
• Fre´zal, L. & R. Leblois, 2008. Four years of DNA barcoding: current advances and prospects. Infection, Genetics and Evolution, 8: 727-736. Gabarra, R., J. Riudavets, G. A. Rodriguez, J. Pujade-Villar & J. Arno, 2015. Prospects for the biological control of Drosophila suzukii. Biocontrol, 60: 331-339.
• Giorgini, M., X. G. Wang, Y. Wang, F.-S. Chen, E. Hougardy, E., H.-M.·Zhang, Z.-Q. Chen, H.-Y. Chen, C.-X. Liu, P. Cascone, G. Formisano, G. A. Carvalho, A. Biondi, M. Buffington, K. M. Daane, K. A. Hoelmer & E. Guerrieri, 2019. Exploration for native parasitoids of Drosophila suzukii in China reveals a diversity of parasitoid species and narrow host range of the dominant parasitoid. Journal of Pest Science, 92: 509-522.
• Girod, G., O. Lierhmann, T. Urvois, T. C. J. Turlings, M. Kenis & T. Haye, 2018a. Host specifcity of Asian parasitoids for potential classical biological control of Drosophila suzukii. Journal of Pest Science, 91: 1241-1250.
• Girod, P., N. Borowiec, M. Buffington, G. Chen, Y. Fang, M. T. Kimura, F. J. Peris-Felipo, N. Ris, H. Wu, C. Xiao, J. Zhang, A. Aebi, T. Haye & M. Kenis, 2018b. The parasitoid complex of D. suzukii and other fruit feeding Drosophila species in Asia. Scientific Reports, 8: 11839.
• Girod, P., L. Rossignaud, T. Haye, T. C. J. Turlings & M. Kenis, 2018c. Development of Asian parasitoids in larvae of Drosophila suzukii feeding on blueberry and artificial diet. Journal of Applied Entomology, 142: 483-494.
• Hanson, P. E. & I. D. Gauld, 1995. The Hymenoptera of Costa Rica. Oxford University Press, Oxford, UK, 893 pp.
• Harvey, J. A. M. Fei, M. Lammers, M. Kos, F. Zhu, R. Heinen, E. H. Poelman & R. Gols, 2016. Development of a solitary koinobiont hyperparasitoid in different instars of its primary and secondary hosts. Journal of Insect Physiology, 90: 36-42.
• Hauser, M., 2011. A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Management Science, 67: 1352-1357.
• Hertlein, M. B., 1986. Seasonal development of Leptopilina boulardi (Hymenoptera: Eucoilidae) and its hosts Drosophila melanogaster and D. simulans in California. Environmental Entomology, 15: 859-866.
• Kaçar, G. & A. S. Koca, 2017. “First recording of spotted wing drosophila in Bolu and Düzce of Turkey and moleculer identification, 66”. II. International Iğdır Symposium (9-11 October 2017, Iğdır, Turkey), 488 pp.
• Kaçar, G., X. G. Wang, A. Biondi & K. M. Daane, 2017. Linear functional response by two pupal Drosophila parasitoids foraging within single or multiple patch environments. PLoS One, 12 (8): e0183525.
• Kanzawa, T., 1939. Studies on Drosophila suzukii Mats. Yamanashi Prefecture Agricultural Experimental Station, Kofu, Japan, 49 pp. (Web page: www.cabdirect.org/cabdirect/abstract/19410501073) (Date accessed: August 2019).
• Kasap, İ. & E. Özdamar, 2019. Population development of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in vineyards of Çanakkale Province. Turkish Journal of Entomology, 43 (1): 57-62.
• Kimura, M. T. & B. Novkovic, 2015. Local adaptation and ecological fitting in host use of the Drosophila parasitoid Leptopilina japonica. Ecological Research, 30: 499-505.
• Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7): 1870-1874.
• Lee, J. C., D. J. Bruck, H. Curry, D. Edwards, D. R. Haviland, R. A. van Steenwyk & B. M. Yorgey, 2011. The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii. Pest Management Science, 67: 1358-1367.
• Legner, E. E., I. Moore & G. S. Olton, 1976. Tabular keys & biological notes to common parasitoids of synanthropic Diptera breeding in accumulated animal wastes. Entomological News, 87 (5/6): 113-144.
• Linares, M. C., N. I. Soto-Caldero, D. Lees & N. M. Anthony, 2009. High mitochondrial diversity in geographically widespread butterflies of Madagascar: a test of the DNA barcoding approach. Molecular Phylogenetics and Evolution, 50: 485-495.
• Markow, T. & P. O'Grady, 2006. Drosophila. A Guide to Species Identification and Use. Elsevier Inc., USA, 272 pp.
• Mazzetto, F., E. Marchetti, N. Amiresmaeili, D. Sacco, S. Francati, C. Jucker, M. L. Dindo, D. Lupi & L. Tavella, 2016. Drosophila parasitoids in northern Italy and their potential to attack the exotic pest Drosophila suzukii. Journal of Pest Science, 89: 837-850.
• Milek, T. M., G. Seljak, M. Simala & M. Bjelis, 2011. First record of Drosophila suzukii (Matsumara, 1931) (Diptera: Drosophilidae) in Croatia. (Prvi nalaz Drosophila suzukii (Matsumara, 1931) (Diptera: Drosophilidae) u Hrvatskoj). Glasilo Biljne Zastite, 11 (5): 377-382.
• Mitsui, H., K. van Achterberg, G. Nordlander & M. T. Kimura, 2007. Geographical distributions and host associations of larval parasitoids of frugivorous Drosophilidae in Japan. Journal of Natural History, 41: 1731-1738.
• Novkovic, B., H. Mitsui, A. Suwito & M. T. Kimura, 2011. Taxonomy and phylogeny of Leptopilina species (Hymenoptera: Cynipoidea: Figitidae) attacking frugivorous drosophilid flies in Japan, with description of three new species. Entomological Science, 14: 333-346.
• Ögür, E., L. Ünlü & F. Canbulat, 2018. New record for spotted wing drosophila, Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) in Karaman, Central Anatolia. Agriculture & Forestry, 64 (1): 189-197.
• Önder, S., U. Ufuk, R. Orhan, G. Tozlu & B. Aslantaş, 2016. “Anadolu’da yeni bir meyve zararlısı olan Drosophila suzukii’nin kolanizasyon senaryosu, 36”. 23. Ulusal Biyoloji Kongresi (5-9 Eylül 2016, Gaziantep, Türkiye), 472 pp.
• Orhan, A., R. Aslantaş, B. S. Önder & G. Tozlu, 2016. First record of the invasive vinegar fly Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) from eastern Turkey. Turkish Journal of Zoology, 40: 290-293.
• Poyet, M., S. Havard, G. Prévost, O. Chabrerie, G. Doury, P. Gibert & P. Eslin, 2013. Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load. Hysiological Entomology, 38: 45-53.
• Rossi Stacconi, M. V., M. Buffington, K. M. Daane, D. T. Dalton, A. Grassia, G. Kaçar, B. Miller, J. C. Miller, N. Baserf, C. Loriatti, V. M. Waltond, N. G. Wimand, X. Wang & G. Anfora, 2015. Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biological Control, 84: 28-35.
• Rossi Stacconi, M. V., A. Grassi, D. T. Dalton, B. Miller, M. Ouantar, A. Loni, C. Ioriatti, V. M. Walton & G. Anfora, 2013. First field records of Pachycrepoideus vindemiae as a parasitoid of Drosophila suzukii in European and Oregon Small fruit production areas. Entomologia, 1: e3.
• Rossi Stacconi, M. V., A. Panel, N. Baser, C. Ioriatti, T. Pantezzi & G. Anfora, 2017. Comparative life history traits of indigenous Italian parasitoids of Drosophila suzukii and their effectiveness at different temperatures. Biological Control, 112: 20-27.
• Rossi Stacconi, M. V., N. Amiresmaeili, A. Biondi, C. Carli, S. Caruso, M. L. Dindo, S. Francati, A. Gottardello, Grassi, A. Lupi, D. Marchetti, E. Mazzetto, F. Mori, N. Pantezzi, T. Tavella, L. Garzia, G. T. Tonina, L. Vaccari, G. Anfora & C. Ioriatti, 2018. Host location and dispersal ability of the cosmopolitan parasitoid Trichopria drosophilae released to control the invasive spotted wing drosophila. Biological Control, 117: 188-196.
• Sasaki, M. & R. Sato, 1995. Bionomics of the cherry drosophila, Drosophila suzukii Matsumura (Diptera: Drosophilidae) in Fukushima Prefecture (Japan). Annual Report of the Society of Plant Protection of North Japan, 46: 164-172.
• Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10: 512-526.
• Thompson, J. D., D. G. Higgins & T. J. Gibson, 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22: 4673-4680.
• Tomanovic, Z., N. G. Kavallieratos & P. Starý, 2003. Aphidius Nees aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) in Serbia and Montenegro: tritrophic associations and key. Acta Entomologica Serbica, 8: 15-39.
• Tozlu, G., R. Aslantaş, B. Ş. Önder & A. Orhan, 2016. “Türkiye için önemli bir meyve zararlısı: istilacı tür Drosophila suzukii, 260”. Uluslararası Türkiye VI. Bitki Koruma Kongresi (5-8 Eylül 2016, Konya, Türkiye), 938 pp.
• Van Noort, S., M. L. Buffington & M. Forshage, 2015. Afrotropical Cynipoidea (Hymenoptera). ZooKeys, 493: 1-176.
• Walsh, D. B., M. P. Bolda, R. E. Goodhue, A. J. Dreeves, J. C. Lee, D. J. Bruck, V. M. Walton, S. D. O’Neal & F. G. Zalom, 2011. Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management, 1: 1-7.
• Wang, X. G., G. Kaçar, A. Biondi & K. M. Daane, 2016. Life-history and host preference of Trichopria drosophilae. Biological Control, 61: 387-397.
• Wang, X. G. & R. H. Messing, 2004. The ectoparasitic pupal parasitoid, Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae), attacks other primary fruit by parasitoids: host expansion and potential non-target risk. Biological Control, 31 (2): 227-236.
• Westphal, V., S. O. Rizzoli, M. A. Lauterbach, D. Kamin, R. Jahn & S. W. Hell, 2008. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science, 320: 246-249.
• Withers, P. & R. Allemand, 2012. The drosophilids of Rhône-Alpes (SE France) (Diptera, Drosophilidae). Bulletin de la Société Entomologique de France, 117 (4): 473-482.