Feza CAN CENGIZ, Kamuran KAYA, Başak ULAŞLI, Jérôme MORINIÈRE

First record of the egg parasitoids of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) in Turkey using DNA barcoding

Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) is an invasive insect species attacking maize (Zea mays L.) and other cereal crops causing important yield losses. The occurrence of this insect in Turkey was first reported in maize growing areas of some provinces in the East Mediterranean region of Turkey in 2014. Chemical or other pest control methods do not always provide acceptable control of this pest, so biological control is considered an important alternative. However, for a successful biological control, the first step is to reliably identify the natural enemies of a target pest, which is difficult to achieve using methods based on morphology. Recent developments in molecular techniques allow more reliable identification of insect species and their parasitoids. Therefore, the aim of this study was to identify the egg parasitoids of C. partellus by molecular methods. Parasitized eggs were collected from maize fields in Hatay province, Turkey, from September to October 2014 and in September 2015. Eggs were maintained in the laboratory and emerging adult parasitoids were subjected to molecular analysis. Using DNA barcoding, two native natural enemies, Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae) and Telenomus busseolae (Gahan) (Hymenoptera: Platygastridae) were identified as egg parasitoids of C. partellus for the first time in Turkey.

Keywords:

Trichogramma brassicae, Telenomus busseolae, COI, spotted stem borer,

PDF

___

Aeschlimann, J. P., 1990. Simultaneous occurrence of thelytoky and bisexuality in hymenopteran species, and its implications for the biological control of pests. Entomophaga 35: 3–5.
Alexandri, M. P. & J. A. Tsitsipis, 1990. Influence of the egg parasitoid Platytelenomus busseolae (Hym.; Scelionidae) on the population of Sesamia nonagrioides (Lep.; Noctuidae) in Central Greece. Entomophaga, 35: 16-25.
Avcı, M., 2003. Parasitism of egg-batches of the cedar processionary moth, Traumatocampa ispartaensis in Turkey. Phytoparasitica 31 (2): 1-6.
Bayram, A. & A. Tonğa, 2015. First report of Chilo partellus in Turkey, a new invasive maize pest for Europe. Journal of Applied Entomology, 140 (3): 236-240.
Bonhof, M. J., 2000. The Impact of Predators on Maize Stem Borers in Coastal Kenya . Wageningen University, PhD thesis, The Netherlands,181 pp.
Borror, D. J., D. M. De Long & C. A. Triplehorn, 1981. An Introduction to the Study of Insects. Saunders College Publishing, 827 pp.
Bournier, J. P., 1982. “Behaviour of various strains of Trichogramma towards eggs of Heliothis armigera Hbn (Lep. Noctuidae) and Chilo partellus Swinhoe (Lep. Pyralidae), 85-96” .Les trichogrammes. Ier Symposium International (10-15 November 1986, Guangzhou-Chine).
Chang, S. C, N. T. Hu, C. Y. Hsin & C. N. Sun, 2001. Characterization of differences between two Trichogramma wasps by molecular markers. Biological Control 21 (1): 75–78.
Divya, K., K. N. Marulasiddesha, K. Krupanidhi & M. Sankar, 2009. Population dynamics of spotted stem borer, Chilo partellus (Swinhoe) and its interaction with natural enemies is sorghum. Indian Journal of Science and Technology, 3 (1): 70-74.
Edgar, R. C., 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5): 1792-1797.
FAO-STAT, 2014. Food and Agriculture Organization of the United States Statistics, (Web page: http://faostat.fao.org), (Date accessed: January 2016).
Farid, A., M. I. N. Khan, A. Khan, S. U. K. Khattak & A. Sattar, 2007. Studies on maize stem borer, Chilo partellus in Peshawar Valley. Pakistan Journal of Zoology, 39 (2): 127-131.
Grabenweger, G., P. Kehrli, I. Zweimüller, S. Augustin, N. Avtzis, S. Bacher, J. Freise, S. Girardoz, S. Guichard, W. Heitland, C. Lethmayer, M. Stolz, R. Tomov, L. Volter & M. Kenis, 2010. Temporal and spatial variations in the parasitoid complex of the horse chestnut leafminer during its invasion of Europe. Biological Invasions, 12: 2797–2813.
Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. Deward, 2003. Biological identifications through DNA barcodes. Proceedings Royal Society London Biological Sciences, 270:313–321.
Hoy, M.A., A. Jeyaprakash, R. Morakote, P. K. C. Lo & R. Nguyen, 2000. Genomic analyses of two populations of Ageniaspis citricola (Hymenoptera: Encyrtidae) suggest that a cryptic species may exist. Biological Control 17: 1–10.
Jalali, S. K. & S. P. Singh, 2006. Biological control of Chilo partellus using egg parasitoid Trichogramma chilonis and Bacillus thuringiensis. Indian Journal of Agricultural Research 40 (3): 184-189.
Kfir, R., 1990. Parasites of the spotted stalk borer, Chilo partellus (Lep: Pyralidae) in South Africa. Entomophaga 35 (3): 403-410.
Khan, Z. R., P. Chiliswa, K. Ampong-Nyarko, L. E. Smart, A. Polaszek, J. Wandera & M. A. Mulaa, 1997. Utilisation of wild gramineous plants for the management of cereal stemborers in Africa. International Journal of Tropical Insect Science, 17 (1): 143–150.
Kornoşor, S., E. Sertkaya & A. Özpınar, 1994. “Distribution of the egg parasitoid Platytelenomus busseolae (Gahan) (Hym., Scelionidae) and its effect on the population of Sesamia nonagrioides Lef. (Lep., Noctuidae) in the Mediterranean Region of Turkey, 193-200”. 4th. International Symposium on Trichogramma and Other Egg Parasites (4-7 October, Cairo, Egypt).
Kumar, H. & J. A. Mihm, 1995. Antibiosis and tolerance to fall armyworm, Spodoptera frugiperda (J. E. Smith), southwestern corn borer, Diatraea grandiosella Dyar and sugarcane borer, Diatraea saccharalis Fabricius in selected maize hybrids and varieties. Maydica. 40: 245-251.
Kumar, H., 2002. Resistance in maize to larger grain borer, Prosphanus truncates (Horn) (Coleoptera: Bostrichidae). Journal of Stored Products Research, 38: 267-280.
Landry, B. S., L. Dextraze & G. Boivin, 1993. Random amplified polymorphic DNA markers for DNA fingerprinting and genetic variability assessment of minute parasitic wasp species (Hymenoptera: Mymaridae and Trichogrammatidae) used in biological control programs of phytophagous insects. Genome, 36 (3): 580–587.
LaSalle, J. & I. D. Gauld, 1991. Parasitic Hymenoptera and the biodiversity crisis. Redia, 74 (3): 315–334.
Leray, M., J. Y. Yang., C. P. Meyer, S. C. Mills, N. Agudelo, V. Ranwez, J. T. Boehm & R. J. Machida, 2013. A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Frontiers in Zoology, 10: 34.
Li, S. Y., D. E. Henderson & J. H. Meyer, 1994. Selection of suitable Trichogramma species for potential control of the blackheaded fire worm infesting cranberries. Biocontrol, 4 (3): 244-248.
Masner, L. & N. F. Johnson, 1979. A new species of Telenomus (Hymenoptera: Scelionidae) an egg parasite of the Ambush bug, Phymata sp. (Heteroptera: Phymatidae). Canadian Entomologist 111 (10): 1115-1119.
Midega, C. A. O., C. K. P. O. Ogol & W. A. Overholt, 2004. Effect of agroecosystem diversity on natural enemies of maize stemborers in coastal Kenya. International Journal of Tropical Insect Science, 4 (4): 280-286.
Nasir, M. F., G. Hagedorn, C. Büttner, C. Reichmuth & M. Schöller, 2013. Molecular identification of Trichogramma species from Pakistan, using ITS-2 region of rDNA. BioControl 58 (4): 483-491.
Neupane, F. P., H. C. Coppel & R. K. Chapman, 1985. Bionomics of the maize borer, Chilo partellus (Swinhoe), in Nepal. International Journal of Tropical Insect Science. 6 (4): 547-553.
Pinto, J. D., R. K. Velten, G. R. Platner & E. R. Oatman, 1989. Phenotypic plasticity and characters in Trichogramma. Annals of the Entomological Society America, 85: 413–422.
Pinto, J. D. & R. Stouthamer, 1994. “Systematics of the Trichogrammatidae with Emphasis on Trichogramma.1-36”. In: Biological Control with Egg Parasitoids (Eds: E. Wajnberg & S. A. Hassan). CAB international, 266 pp.
Pomari- Fernandes, A., A. F. Bueno, A. P. Queiroz & S. A. De Bortoli, 2015. Biological parameters and parasitism capacity of Telenomus remus Nixon (Hymenoptera: Platygastridae) reared on natural and factitious hosts for successive generations. African Journal of Agricultural Research, 10 (33): 3225-3233.
Poorjavad, N., S. H. Goldansaz, T. Machtelinckx, L. Tirry, R. Stouthamer & T. van Leeuwen, 2012. Iranian Trichogramma: ITS2 DNA characterization and natural Wolbachia infection. BioControl, 57 (3): 361-374.
Ratnasingham, S. & P. D. Hebert, 2007. BOLD: The Barcode of Life Data System (http://www. barcodinglife.org). Molecular Ecology Notes, 7 (3), 355-364.
Rebe, M., J. Van Den Berg & M. A. McGeoch, 2004. Colonization of cultivated and indigenous graminaceous host plants by Busseola fusca (Fuller) (Lepidoptera: Noctuidae) and Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) under field conditions. African Entomolology, 12 (2): 187-199.
Rwomushana, I., S. Kyamanywa, A. J. Ngi-Song & C. O. Omwega, 2005. Incidence of larval and pupal parasitoids of Lepidoptera in Uganda with special reference to new associations. International Journal of Tropical Insect Science, 25 (4): 274-280.
Sertkaya, E., V. Akmeşe & E. Atay, 2014. Türkiye’de mısırda yeni bir zararlı, Chilo partellus (Swinhoe) (Lepidoptera: Crambidae). Türkiye Entomoloji Bülteni, 4 (3): 197-200.
Seshu Reddy, K. V., 1988. Assessment of on-farm yield losses in sorghum due to insect pests. International Journal of Tropical Insect Science, 9: 679-685.
Sétamou, M. & F. Schulthess, 1995. The influence of egg parasitoids belonging to Telenomus busseolae (Hym. Scelionidae) species complex on Sesamia calamistis (Lepidoptera: Noctuidae) population in maize fields in Southern Benin. Biocontrol Science and Technology 5: 69–81.
Smith, S. M. & M. Hubbes, 1986. Strains of the egg parasitoid Trichogramma minutum Riley. Journal of Applied Entomology, 101 (1‐5) : 223-239.
Somchoudhury, A. K. & N. Dutt, 1988. Influence of hosts and host ages on the bionomics of Trichogramma perkinsi Girault and Trichogramma australicum Girault. Indian Journal of Entomology, 50 (3): 374-379.
Sorokina, A. P., 1993. Keys to the Species of Genus Trichogramma Westw. (Hymenoptera: Trichogrammatidae) of the World Fauna. Kolos Publishing House, Moscow, 77 pp.
Sümer, F., A. S. Tunçbilek, S. Öztemiz, B. Pintureau, P. Rugman-Jones & R. Stouthamer, 2009. A molecular key to the common species of Trichogramma of the Mediterranean region. BioControl, 54: 617-624.
Tagne, A., T. P. Feujio & C. Sonna, 2008. “Essential oil and plant extracts as potential substitutes to synthetic fungicides in the control of fungi” ENDURE International Conference, Diversifying crop protection (12-15 October 2008, La Grande-Motte-France), 42. Oral presentation.
Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30 (12): 2725–2729.
TÜİK, 2014. Türkiye İstatistik Kurumu. (Web page: http://www.tuik.gov.tr/PreTablo.do?alt_id=1001), (Date accessed: January 2016).
Valentini, A., F. Pompanon & P. Taberlet, 2009. Barcoding for ecologist. Trends in Ecology and Evolution, 24: 110–117.
Van den Berg, J., A. F. Nur & A. Polaszek, 1998. “Cultural Control, 333–347” In: Cereal Stem Borers in Africa: Economic Importance, Taxonomy, Natural Enemies and Control (Ed. A. Polaszek). International Institute of Entomology. CAB International, 592 pp.
Van den Berg, J., 2009. “Can Vetiver grass be used to manage insect pests on crops, 254-264”. Third International Conference on Vetiver (6-9 October 2003, Guangzhou- China), China Agriculture Press, 572 pp.
Wakeil-El, N., N. Gaafar, A. Sallam & C. Volkmar, 2013. Side effects of insecticides on natural enemies and possibility of their integration in plant protection strategies. Insecticides-development of safer and more effective tecnologies-Chapter 1-January 2013. 56 pp.
Yuliarti, N., P. Hidayat & D. Buchori, 2002. Molecular identification of egg parasitoid, Telenomus spp. (Hym.: Scelionidae) from several locations in Java using RAPD-PCR. Biotropia 19: 57-64.