Occurrence and Distribution of Entomopathogenic Nematodes (Steinernematidae and Heterorhabditidae) in Ordu Province, Turkey

Year 2014, Volume: 1 Issue: 4, 469 - 480, 05.11.2014

Ömer Ertürk , Fikret Ustaoğlu Faruk Akyazı

Abstract

During 2009-2010, a survey was conducted to investigate the presence of entomopathogenic nematodes (EPNs) and to characterize the species in Ordu province, Turkey. In total, 156 soil samples were collected randomly from different cultivated and non-cultivated areas. Soil samples were tested for the presence of Steinernematid and Heterorhabditid nematodes by baiting with Galleria mellonella larvae. From the total of 156 soil samples, 8 (5.1%) samples tested were found positive for the presence of EPNs, containing the genera Steinernema and Heterorhabditis. Morphological characterization and sequence analysis of the ITS regions of ribosomal DNA allowed the identification of EPN isolates. Four Steinernema spp. were recovered including S. feltiae, S. carpocapsae, S. kraussei and one new undescribed species. Among the Steinernematids, S. feltiae was found the most common species. Heterorhabditis bacteriophora was the only Heterorhabditid recovered during this survey. H. bacteriophora was only found in a corn field while Steinernema species were present in hazelnut orchard, forest, potato field, rangeland and wheat field.

Keywords

-

Ordu ilinde Entomopatojenik Nematodlar (Steinernematidae and Heterorhabditidae)’ın Varlığı ve Dağılımları

Abstract

Ordu ilinde entomopatojenik nematodların (EPNs) varlığını ve bulunan türlerin özelliklerini ortaya çıkarmak için 2009-2010 yıllarında bir sürvey yapılmıştır. Farklı ürünlerin yetiştirildiği alanlardan ve kültür yapılmayan alanlardan rastgele toplam 156 toprak örneği toplanmıştır. Toprak örneklerindeki Steinernematid ve Heterorhabditid nematodların varlığı Galleria mellonella larvalarının kullanıldığı tuzak böcek yöntemi ile tespit edilmiştir. Toplam incelenen 156 örnekten 8 (%5.1) tanesi Steinernema ve Heterorhabditis cinslerine ait entomopatojen nematodlar yönünden pozitif olarak bulunmuştur. EPN izolatlarının teşhisi morfolojik karekterler ve ribozomal DNA’nın ITS bölgesinin sekans analizi yapılarak sağlanmıştır. Steinernema feltiae, Steinernema carpocapsae, Steinernema kraussei ve bir tane teşhis edilemeyen 4 tür bulunmuştur. Steinernematid nematodlar arasında en yaygın tür Steinernema feltiae bulunmuştur. Yapılan surveyde Heterorhabditid tür olarak sadece Heterorhabditis bacteriophora tespit edilmiştir. Steinernema türleri fındık bahçelerinde, ormanlarda, patates alanlarında, meralarda ve buğday alanlarında bulunabilirken Heterorhabditis bacteriophora yalnızca mısır yetiştirilen alanlarda bulunmuştur.

Keywords

Heterorhabditis bacteriophora, ITS, Steinernema feltiae, Steinernema carpocapsae, Steinernema kraussei

References

• Akhurst R.J. and Bedding, R.A., 1986. Natural occurrence of insect pathogenic nematodes (Steinernematidae and Heterorhabditidae) in soil in Australia. Journal of the Australian Entomological Society 25: 241-244.
• Ansari, M.A., Evans, M. and Butt, T.M., 2009. Identification of pathogenic strains of entomopathogenic nematodes and fungi for wireworm control. Crop Protection28: 269-22. Aydin, M.S., 2007. Entomopatojen nematodların (Steinernematidae ve Heterorhabditidae) Aydın ili ve çevresindeki topraklarda tür çesitliliği ve dağılımlarının belirlenmesi, Yüksek Lisans Tezi. Adnan Menderes Üniversitesi Fen Bilimleri Enstitüsü, Aydın, 55 s.
• Bedding, R.A. and Akhurst, R.J., 1975. A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica 21: 109-110. Campbell, J.F., Orza, G., Yoder, F., Lewis, E. and Gaugler, R., 1998. Spatial and temporal distribution of endemic and released entomopathogenic nematode populations in turf grass. Entomologia Experimentalis et Applicata 86:1-11.
• Ehlers, R.U., Deseo, K.V., Stackebrandt, E., 1991. Identification of Steinernema spp. (Nematoda) and theirsymbiotic bacteria Xenorhabdus spp. from Italian and German soils. Nematologica 37: 360-364.
• Erbaş, Z.,Gökçe, C., Hazır, S., Demirbağ, Z. And Demir, İ., 2014. Isolation and identification of entomopathogenic nematodes (Nematoda: Rhabditida) from the Eastern Black Sea region and their biocontrol potential against Melolontha melolontha (Coleoptera: Scarabaeidae) larvae. Turkish Journal of Agriculture and Forestry 38: 187-197.
• Garcia Del Pino F. And Palomo, A., 1996. Natural occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Spanish soils. Journal of Invertebrate Pathology 68:84–90. Gaugler, R., 2007. Entomopathogenic Nematology. CABI Publishing. pp. 388.Wallingford, UK Georgis, R., Koppenhofer, A.M., Lacey, L.A., Belair, G., Duncan, L.W., Grewal, P.S., Samish, M., Tan, L., Torr, P. and Van Tol, R.W.H.M., 2006. Successes and failures in the use of parasitic nematodes for pest control. Biological Control 38: 103-123. Glazer, I., Liran, N., Poinar, G.O. and Smits, P.H., 1993. Identification and biological activity of newly isolated heterorhabditid populations from Israel. Fun. Appl. Nematol. 16: 467-472. Gokce, C., Yilmaz, H., Erbas, Z., Demirbag, Z. and Demir, I., 2013. First Record of Steinernema kraussei (Rhabditida: Steinernematidae) from Turkey and Its Virulence against Agrotis segetum (Lepidoptera: Noctuidae). Journal of Nematology 45: 253–259. Gökçe, C., Yilmaz, H., Demir, I. and Demirbağ, Z., 2010. A survey study on entomopathogenic nematodes in East Black Sea Region of Turkey, 43th Annual Meeting of the Society for Invertebrate Pathology, Karadeniz Technical University, 11-15 July 2010, Trabzon, p. 60 Griffin, C.T., Finnegan, M.M., Downes, M.J., 1994. Environmental tolerances and the dispersal of Heterorhabditis survival and infectivity of Europen Heterorhabditis following prolonged immersion in seawater. Fundamental Applied Nematology, 17, 415-421. Grewal, P.S., Ehlers, R.U. and Shapiro-Ilan D.I. (Eds) 2005. Nematodes as biocontrol agents. CAB International, New York. Güneş, C., 2008. Marmara Bölgesi’ndeki Entomopatojen Nematod Faunasının Belirlenmesi. Yüksek lisans Tezi, Onsekiz Mart Üniversitesi Fen Bilimleri Enstitüsü, Çanakkale, 95 s Hara, A.H., Gaugler, R., Kaya, H.K. and Lebeck, L.M., 1991. Natural populations of entomopathogenic Nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) from Hawaiian Islands. Environmental Entomology 20: 211-216. Haukeland, S., 1993. Entomopathogenic nematodes found in Norway. Norwegian Journal of Agricultural Sciences 7: 17-27. Hazir, S., Stock, S.P. and Keskin, N., 2003a. A new entomopathogenic nematode, Steinernema anatoliense n. sp. (Rhabditida: Steinernematidae), from Turkey. Systematic Parasitology 55: 211-220. Hazir, S., Keskin, N., Stock, P.S., Kaya, H.K. and Özcan, S., 2003b. Diversity and distribution of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Turkey. Biodiversity and Conservation 12: 375-386. Hominick, W.M. and Briscoe, B.R., 1990. Occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in British soil. Parasitology 100: 295-302. Hominick, W.M., 2002. Biogeography. Pp. 115-143. In: Entomopathogenic Nematology (R.GauglerEd.). CABI Publishing, Wallingford, UK.
• Hominick, W.M.,Reid, A.P. and Briscoe, B.R., 1995. Prevalence and habitat specificity of steinernematid and heterorhabditid nematodes isolated during soil surveys of the UK and The Netherlands. Journal of Helminthology 69: 27–32. Hominick, W.M., Reid, A.P., Boham, A.P., Briscoe, B.R., 1996. Entomopathogenic nematodes: Biodiversity, geographical distribution and the convention on biological diversity. Biocontrol Science and Technology. 6:317–331.
• Hominick, W.M., Briscoe, B.R., Del-Pino, F.G., Heng, J., Hunt, D.J., Kozodoy, E., Mracek, Z., Nguyen, K.B., Reid, A.P., Spiridonov, S., Stock, P., Sturhan, D., Waturu, C. andYoshida, M., 1997. Biosystematics of entomopathogenic nematodes: current status, protocols and definitions. Journal of Helminthology 71: 271-298.
• Joyce, S.A., Reid, A., Driver, F. and Curran, J., 1994. Application of polymerase chain reaction (PCR) methods to identification of entomopathogenic nematodes. In: Biotechnology: Genetics of entomopathogenic nematode bacteria complexes.(A.M., Burnell, R.U. Ehlers,and J.P. Masson (Eds.).pp. 178-187. DG XII, Europen Commission, Luxembourg. Kaya, H.K., 1990. Soil ecology. In: Entomopathogenic nematodes in biological control. (R., Gaugler, H.K. Kaya, Eds.).pp. 93–115. CRC Press, Boca Raton.
• Kaya, H.K. and Stock, S.P., 1997. Techniques in insect nematology. In: Manual of techniques in insect pathology (Lacey, L.A. Ed.). pp. 281-324. Academic Press, London Kepenekçi, I., Babaroğlu, N.E., Öztürk, G. and Halici, S., 1999. A new entomopathogenic nematode; Heterorhabditis bacteriophora Poinar, 1976: (Rhabditida: Heterorhabditidae) for Turkey. Turkish Journal of Entomology 9: 587-596. Kepenekçi, I., Susurluk, I.A., 2000. A new entomopathogenic nematode species for Turkey; Heterorhabditis marelatus Luiand Berry, 1996 (Rhabditida: Heterorhabditidae). Journal of Agricultural Sciences 6: 59-64. Kepenekçi, I., 2002. Entomopathogenic nematodes (Rhabditida) in the Mediterranean region of Turkey. Nematologia Mediterranea 30: 13-15. Kepenekçi, I. and Susurluk, I.A., 2003. Three entomopathogenic nematodes (Rhabditida) from Turkey. Pakistan Journal of Nematology 21:19-23. Lacey, L.A., Arthurs, S.P., Unruh, T.R., Headrick, H. and Fritts, R.Jr., 2006. Entomopathogenic nematodes for control of codling moth (Lepidoptera: Tortricidae) in apple and pear orchards: effect of nematode species and seasonal temperatures, adjuvant, application equipment and post-application irrigation. Biological Control 37:214–223.
• Mracek, Z. and Webster, J.M., 1993. Survey of Heterorhabditidae and Steinernematidae (Rhabditida, Nematoda) in Western Canada. Journal of Nematology 25: 710-717.
• Mracek, Z., 1977. Steinernema kraussei, a parasite of the body cavity of the sawfly, Cephaleia abietis, in Czechoslovakia. Journal of Invertebrate Pathology 30:87-94.
• Mracek, Z., 1994. Steinernema kraussei (Steiner, 1923) (Nematoda: Rhabditida: Steinernematidae): Redescription of its topotype from West phalia. Folia Parasitologica 41: 59–64. Mracek, Z., Becvar, S., Kindlmann, P. and Jersakova, J., 2005. Habitat preference for entomopathogenic nematodes, their insect hosts and new faunistic records for the Czech Republic. Biological Control 34:27–37. Mracek, Z. and Webster, J.M., 1993. Survey of Heterorhabditidae and Steinernematidae (Rhabditida: Nematoda) in western Canada. Journal of Nematology 25:710-717.
• Nguyen, K.B. and Smart, Jr. G.C., 1995. Morphometrics of infective juveniles of Steinernema spp. and Heterorhabditis bacteriophora (Nemata: Rhabditida). Journal of Nematology 27: 206-212. Özer, N., Keskin, N., Kirbaş, Z., 1995. Occurrence of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) in Turkey. Nematologica 41: 639-640.
• Peters, A., 1996. The natural host range of Steinernema and Heterorhabditis spp. and their impact on insect populations. Biocontrol Scienceand Technology 6: 389-402. Poinar, G.O. Jr., 1979. Nematodes for biological control of insects. pp. 277, CRS Press. Florida. Shapiro-Ilan, D.I., Han, R. and Qiu, X., 2014. Production of entomopathogenic nematodes. In: Mass production of beneficial organisms Invertebrates and entomopathogens (J.Morales-Ramos, G. Rojas, and D.I. Shapiro-Ilan, Eds).pp. 321-356. Academic Press. San Diego, CA.
• Spiridonov, S.E.,Reid, A.P., Podrucka, K., Subbotin, S.A. and Moens, M., 2004. Phylogenetic relationships within the genus Steinernema (Nematoda: Rhabditida) as inferred from analyses of sequences of the ITS1-5.8S-ITS2 region of rDNA and morphological features. Nematology 6: 547-566.
• Spiridonov, S.E. and Moens, M., 1999. Two previously unreported species of steinernematids from woodlands in Belgium. Russian Journal of Nematology7:39-42. Stock, S.P., Pryor, B.M. and Kaya, H.K., 1999. Distribution of entomopathogenic nematodes (Steinernematidae, Heterorhabditidae) in natural habitats in California. Biodiversity and Conservation 8:339-345. Stock, S.P., Mracek, Z. and Webster, J.M., 2000. Morphological variation between allotropic populations of Steinernema kraussei (Steiner, 1923) (Rhabditida: Steinernematidae). Nematology2:143-152. Sturhan, D. and Liskova, M., 1999. Occurrence and distribution of entomopathogenic nematodes in the Slovak Republic. Nematology 1:273-277. Susurluk, A., Dix, I., Stackebrandt, E., Strauch, O., Wyss, U. and Ehlers, R.U., 2001. Identification and ecological characterization of three entomopathogenic nematode-bacterium complexes from Turkey. Nematology 3: 833-841. Susurluk, A., Hollmer, S., Mehta, U.K., Han, R., Tarasco, E., Triggiani, O., Peters, A. and Ehlers, R.U., 2003.Molecular identification of entomopathogenic nematodes from Turkey, India, China, Italy, Norway, Albania and Germany by PCR-RFLP. In: 9th European Meeting of the IOBC/WPRS Working Group, Schloss Salzau, Germany. Steiner, G., 1923. Aplectana kraussei n. sp., eine in der Blattwespe Lyda sp. Parasitierende Nematoden Form, nebst Bemerkungenüber das Seitenorgan der parasitischen Nematoden. Zentralblatt fur Bakteriologie Parasitenkunde Infektionskranheiten und Hygiene Abteilung 59: 14–18. Steiner, W.A., 1996. Distribution of entomophilic nematodes in the Swiss Alps. Revue Suisse de Zoologie 103: 439-452. Ünlü, I.O., Ehlers, R.U. and Susurluk, A., 2007. Additional data and first record of entomopathogenic nematode Steinernema weiseri from Turkey. Nematology 9: 739-741. Yilmaz, H., Waeyenberge, L., Demir, I., Demirbag, Z., Moens, M., 2008. Distribution of entomopathogenic nematodes from the Eastern Black Sea region of Turkey. Book of Abstracts of 60th International Symposium on Crop Protection, May 20, Gent, Belgium. pp 199.
• Yılmaz, H., Waeyenberge, L., Demir, I., Moens, M., and Demirbag, Z., 2009. A new entomopathogenic nematode species for Turkey, Heterorhabditis megidis Poinar, Jackson and Klein 1987 (Rhabditida: Heterorhabditidae). Turkish Journal of Agriculture and Forestry 33: 385-391.
• Yoshida, M., 2003. Intraspecific variation in RFLP patterns and morphological studies on Steinernema feltiae and S. kraussei (Rhabditida:Steinernematidae) from Hokkaido, Japan. Nematology 5: 735-746. Vanninen, I., Husberg, G.B. and Hokkanen, H.M.T., 1989. Occurrence of entomopathogenic fungi and nematodes in cultivated soils in Finland. Acta Entomologica Fennica 53: 65-71. Wright, P.J., 1992. Cool temperature reproduction of Steinernematid and Heterorhabditid. Journal of Invertebrate Pathology 60:148-15.