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http://dx.doi.org/10.5656/KSAE.2008.47.4.435

Efficacy of an Integrated Biological Control of an Egg Parasitoid, Trichogramma evanescens Westwood, and Microbial Insecticide Against the Oriental Tobacco Budworm, Helicoverpa assulta (Guenée) Infesting Hot Pepper  

Kim, Geun-Seob (Department of Bioresource Sciences, Andong National University)
Heo, Hye-Jung (Department of Bioresource Sciences, Andong National University)
Park, Jung-A (Department of Bioresource Sciences, Andong National University)
Yu, Yong-Suk (Agricultural Environment Research Center, NABIS Co., Ltd.)
Hahm, Eun-Hye (Agricultural Environment Research Center, NABIS Co., Ltd.)
Kang, Sung-Young (Agricultural Environment Research Center, NABIS Co., Ltd.)
Kwon, Ki-Myeon (Agricultural Environment Research Center, NABIS Co., Ltd.)
Lee, Keon-Hyung (Agricultural Environment Research Center, NABIS Co., Ltd.)
Kim, Yong-Gyun (Department of Bioresource Sciences, Andong National University)
Publication Information
Korean journal of applied entomology / v.47, no.4, 2008 , pp. 435-445 More about this Journal
Abstract
Due to internal feeding behavior, the oriental tobacco budworm, Helicoverpa assulta ($Guen\acute{e}e$), infesting hot pepper has been regarded to be effectively controlled by targeting egg and neonate larval stages just before entering the fruits. This study aimed to develop an efficient biological control method focusing on these susceptible stages of H. assulta. An egg parasitoid wasp, Trichogramma evanescens Westwood, was confirmed to parasitize the eggs of H. assulta. A mixture of Gram-positive soil bacterium, Bacillus thuringiensis subsp. kurstaki, and Gram-negative entomopathogenic bacterium, Xenorhabdus nematophila ANU101, could effectively kill neonate larvae of H. assulta. A sex pheromone trap monitored the occurrence of field H. assulta adults. The microbial insecticide mixture was proved to give no detrimental effects on immature development and adult survival of the wasp by both feeding and contact toxicity tests. A combined treatment of egg parasitoid and microbial pesticide was applied to hot pepper fields infested by H. assulta. The mixture treatment of both biological control agents significantly decreased the fruit damage, which was comparable to the chemical insecticide treatment, though either single biological control agent did not show any significant control efficacy. This study also provides morphological and genetic characters of T. evanescens.
Keywords
Trichogramma evanescens; Bacillus thuringiensis; Xenorhabdus nematophila; Helicoverpa assulta; Integrated biological control;
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1 Büyükgüzel, E., H. Tunaz, D. Stanley and K. Büyükgüzel. 2007. Eicosanoids mediate Galleria mellonella cellular immune response to viral infection. J. Insect Physiol 53: 99-105   DOI   ScienceOn
2 Doutt, R.L. 1964. Biological characteristics of entomophagous adults. pp. 145-167. In Biological control of insect pests and weeds. eds. by P. Debach. Reinhold, New York
3 Le Ralec, A. and E. Wajnberg. 1990. Sensory receptors of the ovipositor of Trichogramma maidis [Hym.: Trichogrammatidae]. Entomophaga 35: 293-299   DOI
4 Lord, J.C., S. Anderson and D.W. Stanley. 2002. Eicosanoids mediate Manduca sexta cellular response to the fungal pathogen Beauveria bassiana: a role for lipoxygenase pathway. Arch. Insect Biochem. Physiol. 51: 46-54   DOI   ScienceOn
5 McIver, S.B. 1975. Structure of cuticular mechanoreceptors of arthropods. Annu. Rev. Entomol. 20: 381-397   DOI   ScienceOn
6 Nalini, M., Y. Lee and Y. Kim. 2007. Pyriproxyfen inhibits hemocytic phagocytosis of the beet armyworm. Spodoptera exigua. Kor. J. Pesti. Sci. 11: 164-170   과학기술학회마을
7 Park, Y. and Y. Kim. 2000. Eicosanoids rescue Spodoptera exigua infected with Xenorhabdus nematophila, the symbiotic bacteria to the entomopathogenic nematode Steinernema carpocapsae. J. Insect Physiol. 46: 1469-1476   DOI   ScienceOn
8 Park, Y. and Y. Kim. 2003. Xenorhabdus nematophilus inhibits p-bromophenacyl bromide (BPB)-sensitive PLA2 of Spodoptera exigua. Arch. Insect Biochem. Physiol. 54: 134-142
9 SAS Institute. 1989. SAS/STAT User's Guide, Release 6.03. Ed. Cary, N.C
10 Shrestha, S. and Y. Kim. 2007a. An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits hemocyte phagocytosis of Spodoptera exigua by inhibiting phospholipase $A_2$. J. Invertebr. Pathol. 96: 64-70   DOI   ScienceOn
11 Shrestha, S. and Y. Kim. 2008. Eicosanoids mediate prophenoloxidase release from oenocytoids in the beet armyworm Spodoptera exigua. Insect Biochem. Mol. Biol. 38: 99-112   DOI   ScienceOn
12 Smith, E.L. 1970. Evolutionary morphology of the external insect genitalia. 2. Hymenoptera. Ann. Entomol. Soc. Am. 63: 1-27   DOI
13 Smith, S.M. 1996. Biological control with Trichogramma: advances, successes, and potential of their use. Annu. Rev. Entomol. 41: 375-406   DOI   ScienceOn
14 Dennis, E.A. 1997. The growing phospholipase A2 superfamily of signal transduction enzymes. Trends. Biochem. Sci. 22: 1-2   DOI   ScienceOn
15 Strand, M.R. and L.L. Pech. 1995. Immunological basis for compatibility in parasitoid host relationships. Annu. Rev. Entomol. 40: 31-56   DOI   ScienceOn
16 ffrench-Constant, R.H., N. Waterfield and P. Daborn. 2005. Insecticidal toxins from Photorhabdus and Xenorhabdus, pp. 239- 253. In Comprehensive molecular insect science, eds. by L.I. Gilbert, I. Kostas and S.S. Gill. Elsevier, New York
17 Tanaka, H., J. Ishibashi, K. Fujita, Y. Nakajima, A. Sagisaka, K. Tomimoto, N. Suzuki, M. Yoshiyama, Y. Kaneko, T. Iwasaki, T. Sunagawa, K. Yamaji, A. Asaoka, K. Mita and M. Yamakawa. 2008. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem. Mol. Biol. (In press)
18 Akhurst, R.J. 1980. Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J. Gen. Microbiol. 121: 303-309
19 Ishidora, N., F. Bin and S.B. Vinson. 1996. Morphology of antennal gustatory sensilla and glands in some parasitoid Hymenoptera with hypothesis on their role in sex and host recognition. J. Hym. Res. 5: 200-239
20 Shrestha, S. and Y. Kim. 2007b. Factors affecting the activation of hemolymph prophenoloxidase of Spodoptera exigua (Lepidoptera: Noctuidae). J. Asia-Pac. Entomol. 10: 131-135   과학기술학회마을   DOI
21 Gahan, L.J., F. Gould and D.G. Heckel. 2001. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293: 857-860   DOI   ScienceOn
22 Nandihalli, B.S. 1994. Ecology of an egg parasitoid, Trichogramma chilonis Ishii, and a larval parasitoid, Campoletis chlorideae Uchida, of the Oriental tobacco budworm, Helicoverpa assulta (Guenée). PhD thesis. pp. 106. Seoul National University, Seoul, Korea
23 Amornsak, W., B. Cribb and G. Gordh. 1998. External morphology of antennal sensilla of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae). Int. J. Insect Morph. Embryol. 27: 67-82   DOI   ScienceOn
24 Jung, J.K., J.H. Park, D.J. Im and T.M. Han. 2005. Parasitism of Trichogramma evanescens and T. ostriniae (Hymenoptera: Trichogrammatidae) to eggs of the asian corn borer, Ostrinia furacalis (Lepidoptera: Pyralidae). Kor. J. Appl. Entomol. 44: 43-50   과학기술학회마을
25 Jung, S. and Y. Kim. 2006. Synergistic effect of Xenorhabdus nematophila K1 and Bacillus thuringiensis subsp. aizawai against Spodoptera exigua (Lepidoptera: Noctuidae). Biol. Control 39: 201-209   DOI   ScienceOn
26 Ohta, I., K. Miura and M. Kobayashi. 1994. Effect of the scalehair of the common cutworm egg mass on the oviposition behavior of Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae). Appl. Entomol. Zool. 29: 608-609   DOI
27 Dennis, E.A. 1994. Diversity of group types, regulation, and function of phospholipase A2. J. Biol. Chem. 269: 13057-13060
28 Dunphy, G.B. and J.M. Webster. 1991. Antihemocytic surface components of Xenorhabdus nematophilus var. dutki and their modification by serum of nonimmune larvae of Galleria mellonella. J. Invertebr. Pathol. 58: 40-51   DOI
29 Li, L.Y. 1994. Worlwide use of Trichogramma for biological control on different crops: a survey, pp. 37-53. In Biological control with egg parasitoids, eds. by E. Wajnberg and S.A. Hassan. CAB international, Wallingford, PA
30 Voegelé, J., J. Cals-Usciati, J.P. Pihan and J. Daumal. 1975. Structure de l'antenne des Trichogrammes. Entomophaga 20: 161-169   DOI
31 Stanley, D. 2000. Eicosanoids in invertebrate signal transduction systems. Priceton University Press, New Jersey
32 Park, Y. and Y. Kim. 2007. An entomopathogenic bacterium, Xenorhabdus nematophila, induces insect immunosuppression by inhibiting phospholipase $A_2$. J. Basic Life Res. Sci. 7: 31-37
33 Schmidt, J.M. 1994. Host recognition and acceptance by Trichogramma, pp. 165-200. In Biological control with egg parasitoids, eds. by E. Wajnberg and S.A. Hassan. CAB International, Wallingford, PA
34 Van Rie, J., S. Jansens, H. Hofte, D. Degheele and H. Van Mellaert. 1989. Specificity of Bacillus thuringiensis-endotoxins. Importance of specific receptors on the brush border membrane of the midgut of target insects. Eur. J. Biochem. 186: 239-247   DOI   ScienceOn
35 Flanders, S.E. 1930. Mass production of egg parasites of the genus Trichogramma. Hilgardia 4: 145-167
36 Kim, Y., D. Ji, S. Cho and Y. Park. 2005. Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase $A_2$ to induce host immunodepression. J. Invertebr. Pathol. 89: 258-264   DOI   ScienceOn
37 Kwon, B. and Y. Kim (2008) Benzylideneacetone, an immunosuppressant, enhances virulence of Bacillus thuringiensis against beet armyworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 101: 36-41   DOI
38 Barlin, M.R. and S.B. Vinson. 1981. Multiporous plate sensilla in antennae of the Chalcidoidea (Hymenoptera) Int. J. Insect Morph. Embryol. 10: 29-42   DOI
39 Qin, J.D. and Z.X. Wu. 1988. Studies on cultivation of Trichogramma in vitro: ovipositional behaviour and larval nutritional requirements of T. dendrolimi. Coll INRA 43: 379-387
40 Rajendram, G.F. 1978. Oviposition behavior of Trichogramma californicum on artificial substrates. Ann. Entomol. Soc. Am. 71: 92-94   DOI
41 Forst, S., B. Dowds, N. Boemare and E. Stackebrandt. 1997. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 51: 47-72   DOI   ScienceOn
42 Garcia, E.S., E.M.M. Machado and P. Azambuja. 2004. Effects of eicosanoid biosynthesis inhibitors on the prophenoloxidaseactivating system and microaggregation reactions in the hemolymph of Rhodnius prolixus infected with Trypanosoma rangeli. J. Insect Physiol. 50: 157-165   DOI   ScienceOn
43 Olson, D.M. and D.A. Andow. 1993. Antennal sensilla of female Trichogramma nubilale (Ertle and Davis) Hymenoptera: Trichogrammatidae) and comparisons with other parasitic Hymenoptera. Int. J. Insect Morph. Embryol. 22: 507-520   DOI
44 Schmidt, J.M. and J.J.B. Smith. 1985. Host volume and measurement by the parasitoid wasp Trichogramma minutum: the roles of curvature and surface area. Entomol. Exp. Appl. 39: 213-221   DOI   ScienceOn
45 Cônsoli, F.L., E.W. Kitajima and J.R.P. Parra. 1999. Sensilla on the antenna and ovipositor of the parasitic wasps Trichogramma galloiz Zucchi and T. pretiosum Piley (Hym., Trichogrammatidae). Microsc. Res. Tech. 45: 313-324   DOI   ScienceOn
46 Gillespie, J.P., M.R. Kanost and T. Trenczek. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42: 611-643   DOI   ScienceOn
47 Hoffmann, C., H. Vanderbruggen, H. Hofte, J. Van Rie, S. Jansens and H. Van Mellaert. 1988. Specificity of Bacillus thuringiensisendotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midgets. Proc. Natl. Acad. Sci. USA 85: 7844-7848
48 Bae, S. and Y. Kim. 2003. Lysozyme of the beet armyworm, Spodoptera exigua: activity induction and cDNA structure. Comp. Biochem. Physiol. 135B: 511-519
49 Boo, K.S. and J.P. Yang. 2000. Kairomones used by Trichogramma chilonis to find Helicoverpa assulta eggs. J. Chem. Ecol. 26: 359-374   DOI   ScienceOn
50 Nettles, W.C. Jr., R.K. Morrison, Z.N. Xie, D. Ball, C.A. Shenkir and S.B. Vinson. 1983. Effect of cations, anions and salt concentrations on oviposition by Trichogramma pretiosum in wax eggs. Entomol. Exp. Appl. 33: 283-289   DOI   ScienceOn
51 Pinto, J.D. and R. Stouthamer. 1994. Systematics of the Trichogrammatidae with emphasis on Trichogramma. pp. 1-36. In Biological control with egg parasitoids, eds. by E. Wajnberg and S. A. Hassan. CAB International, Wallingford, PA. USA
52 Boo, K.S. and J.P. Yang. 1998. Olfactory response of Trichogramma chilonis to Capsicum annum. J. Asia-Pac. Entomol. 1: 123-129   DOI
53 Pinto, J.D. 1997. Taxonomia de Trichogrammatidae (Hymenoptera) com énfase nos géneros que parasitam Lepidoptera, pp. 13-39. In Trichogramma e o controle biológico aplicado, eds. by J.R.P. Parra and R.A. Zucchi. FEALQ, Piracicaba
54 Kwon, S. and Y. Kim (2007) Immunosuppressive action of pyriproxyfen, a juvenile hormone analog, enhances pathogenicity of Bacillus thuringiensis subsp. kurstaki against diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Biol. Control 42: 72-76   DOI   ScienceOn
55 Abdel-latief, M. and M. Hilker. 2008. Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. Insect Biochem. Mol. Biol. 38: 136-145   DOI   ScienceOn
56 Hassan, S.A. 1994. Strategies to select Trichogramma species for use in biological control. pp. 55-71. In Biological control with egg parasitoids, eds. by E. Wajnberg and S.A. Hassan. 286 pp. CAB International, Wallingford, PA
57 Gill, M. and D. Ellar. 2002. Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac1. Insect Mol. Biol. 11: 619-625   DOI   ScienceOn
58 Ji, D. and Y. Kim. 2004. An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits the expression of an antibacterial peptide, cecropin, of the beet armyworm, Spodoptera exigua. J. Insect Physiol. 50: 489-496   DOI   ScienceOn
59 Rajagopal, R., S. Sivakumar, N. Agrawal, P. Malhotra and R.K. Bhatnagar. 2002. Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA established its role as Bacillus thuringiensis toxin receptor. J. Biol. Chem. 277: 46849- 46851   DOI   ScienceOn
60 Vinson, S.B. 1994. Physiological interactions between egg parasitoids and their hosts. pp. 201-217. In Biological control with egg parasitoids, eds. by E. Wajnberg and S.A. Hassan. CAB International, Wallingford, PA
61 Dunphy, G.B. and J.M. Webster. 1984. Interaction of Xenorhabdus nematophilus subsp. nematophilus with the haemolymph of Galleria mellonella. J. Insect Physiol. 30: 883-889   DOI   ScienceOn
62 Kaya, H.K. and R. Gaugler. 1993. Entomopathogenic nematodes. Annu. Rev. Entomol. 38: 181-206   DOI   ScienceOn
63 Stanley, D. 2006. Prostaglandins and other eicosanoids in insects: biological significance. Annu. Rev. Entomol. 51: 25-44   DOI   ScienceOn
64 Gorman, M.J., P. Kankanala and M.J. Kanost. 2004. Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Mol. Biol. 13: 19-24   DOI   ScienceOn
65 Boemare, N. 2002. Biology, taxonomy and systematics of Photorhabdus and Xenorhabdus, pp. 35-56. In Entomopathogenic nematology, eds. by R. Gaugler. CABI Publishing, New York
66 Klomp, H. and B.J. Teerink. 1962. Host selection and number of eggs per oviposition in the egg parasite Trichogramma embryophagum Htg. Nature 195: 1020-1021   DOI
67 Salt, G. 1935. Experimental studies in insect parasitism. III. Host selection. Proc. R. Entomol. Soc. Lond. 117: 413-435
68 Schmidt, J.M. and J.J.B. Smith. 1987. Measurement of host curvature by the parasitoid wasp Trichogramma minutum, and its effect on host examination and progeny allocation. J. Exp. Biol. 129: 151-164
69 Clark, K.D., Y. Kim and M.R. Strand. 2005. Plasmatocyte sensitivity to plasmatocyte spreading peptide (PSP) fluctuates with the larval molting cycle. J. Insect Physiol. 51: 587-596   DOI   ScienceOn