Korean journal of applied entomology (한국응용곤충학회지)

Korean Society of Applied Entomology (한국응용곤충학회)
권호 표지
DOI QR코드

DOI QR Code

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

고추를 가해하는 담배나방[Helicoverpa assulta (Guenée)]의 효과적 방제를 위한 쌀좀알벌(Trichogramma evanescens Westwood)과 미생물제제의 종합생물방제 효과

  • 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)
  • 김근섭 (안동대학교 생명자원과학과) ;
  • 허혜정 (안동대학교 생명자원과학과) ;
  • 박정아 (안동대학교 생명자원과학과) ;
  • 유용석 ((주) 나비스 중앙연구소) ;
  • 함은혜 ((주) 나비스 중앙연구소) ;
  • 강성영 ((주) 나비스 중앙연구소) ;
  • 권기면 ((주) 나비스 중앙연구소) ;
  • 이건형 ((주) 나비스 중앙연구소) ;
  • 김용균 (안동대학교 생명자원과학과)
  • Published : 2008.12.30
Download PDF
⟨ Previous Next ⟩

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.

고추를 가해하는 담배나방(Helicoverpa assulta ($Guen\acute{e}e$))의 최적 방제 적기는 과실 내부로 침투하기 이전 시기인 알과 어린 유충으로 인식되고 있다. 본 연구는 담배나방의 이러한 감수성 발육시기를 대상으로 하는 효과적 생물적 방제 기술을 개발하는 데 목표를 두었다. 쌀좀알벌(Trichogramma evanescens Westwood)은 알기생봉으로 담배나방 알도 기생시키는 것이 본 연구를 통해 관찰되었다. 그람양성균인 토양 곤충병원세균(Bacillus thuringiensis subsp. kurstaki)과 그람음성균인 곤충병원세균(Xenorhabdus nematophila ANU101)은 어린 담배나방 유충을 대상으로 상호 협력적 병원력을 발휘하였다. 고추 포장의 담배나방 성충 발생은 페로몬트랩을 통해 모니터링하였다. 혼합 미생물제제는 접촉과 섭식 독성 분석 모두에서 쌀좀알벌의 유충 발육과 성충 생존에 영향을 주지 않는 것으로 판명되었다. 담배나방 성충 발생이 성페로몬 트랩으로 확인된 시기에 고추포장에 쌀좀알벌과 미생물제제의 혼합 처리가 실시되었다. 혼합 생물방제 처리는 화학농약과 비슷한 수준으로 과실의 피해를 현저히 감소시킨 반면, 단독 생물방제 처리는 효과가 현저히 낮았다. 아울러 본 연구는 쌀좀알벌의 형태적 및 유전적 특징을 분석했다.

Keywords

References

  1. 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 https://doi.org/10.1016/j.ibmb.2007.10.001
  2. 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
  3. 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 https://doi.org/10.1016/S0020-7322(98)00003-8
  4. Bae, S. and Y. Kim. 2003. Lysozyme of the beet armyworm, Spodoptera exigua: activity induction and cDNA structure. Comp. Biochem. Physiol. 135B: 511-519
  5. 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 https://doi.org/10.1016/0020-7322(81)90011-8
  6. 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
  7. Boo, K.S. and J.P. Yang. 1998. Olfactory response of Trichogramma chilonis to Capsicum annum. J. Asia-Pac. Entomol. 1: 123-129 https://doi.org/10.1016/S1226-8615(08)60014-X
  8. Boo, K.S. and J.P. Yang. 2000. Kairomones used by Trichogramma chilonis to find Helicoverpa assulta eggs. J. Chem. Ecol. 26: 359-374 https://doi.org/10.1023/A:1005453220792
  9. 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 https://doi.org/10.1016/j.jinsphys.2006.10.012
  10. 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 https://doi.org/10.1016/j.jinsphys.2005.03.002
  11. 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 https://doi.org/10.1002/(SICI)1097-0029(19990515/01)45:4/5<313::AID-JEMT15>3.0.CO;2-4
  12. Dennis, E.A. 1994. Diversity of group types, regulation, and function of phospholipase A2. J. Biol. Chem. 269: 13057-13060
  13. Dennis, E.A. 1997. The growing phospholipase A2 superfamily of signal transduction enzymes. Trends. Biochem. Sci. 22: 1-2 https://doi.org/10.1016/S0968-0004(96)20031-3
  14. 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
  15. 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 https://doi.org/10.1016/0022-1910(84)90063-5
  16. 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 https://doi.org/10.1016/0022-2011(91)90160-R
  17. 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
  18. Flanders, S.E. 1930. Mass production of egg parasites of the genus Trichogramma. Hilgardia 4: 145-167
  19. Forst, S., B. Dowds, N. Boemare and E. Stackebrandt. 1997. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 51: 47-72 https://doi.org/10.1146/annurev.micro.51.1.47
  20. 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 https://doi.org/10.1126/science.1060949
  21. 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 https://doi.org/10.1016/j.jinsphys.2003.11.002
  22. 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 https://doi.org/10.1046/j.1365-2583.2002.00373.x
  23. Gillespie, J.P., M.R. Kanost and T. Trenczek. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42: 611-643 https://doi.org/10.1146/annurev.ento.42.1.611
  24. 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 https://doi.org/10.1111/j.1365-2583.2004.00454.x
  25. 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
  26. 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
  27. 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
  28. 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 https://doi.org/10.1016/j.jinsphys.2004.03.005
  29. 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
  30. 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 https://doi.org/10.1016/j.biocontrol.2006.07.002
  31. Kaya, H.K. and R. Gaugler. 1993. Entomopathogenic nematodes. Annu. Rev. Entomol. 38: 181-206 https://doi.org/10.1146/annurev.en.38.010193.001145
  32. 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 https://doi.org/10.1016/j.jip.2005.05.001
  33. 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 https://doi.org/10.1038/1951020a0
  34. 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 https://doi.org/10.1016/j.biocontrol.2007.03.006
  35. 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 https://doi.org/10.1603/0022-0493(2008)101[36:BAIEVO]2.0.CO;2
  36. Le Ralec, A. and E. Wajnberg. 1990. Sensory receptors of the ovipositor of Trichogramma maidis [Hym.: Trichogrammatidae]. Entomophaga 35: 293-299 https://doi.org/10.1007/BF02374805
  37. 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
  38. 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 https://doi.org/10.1002/arch.10049
  39. McIver, S.B. 1975. Structure of cuticular mechanoreceptors of arthropods. Annu. Rev. Entomol. 20: 381-397 https://doi.org/10.1146/annurev.en.20.010175.002121
  40. 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
  41. 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
  42. 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 https://doi.org/10.1111/j.1570-7458.1983.tb03270.x
  43. 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 https://doi.org/10.1303/aez.29.608
  44. 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 https://doi.org/10.1016/0020-7322(93)90037-2
  45. 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 https://doi.org/10.1016/S0022-1910(00)00071-8
  46. 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
  47. 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
  48. 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
  49. 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
  50. 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
  51. 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 https://doi.org/10.1074/jbc.C200523200
  52. Rajendram, G.F. 1978. Oviposition behavior of Trichogramma californicum on artificial substrates. Ann. Entomol. Soc. Am. 71: 92-94 https://doi.org/10.1093/aesa/71.1.92
  53. SAS Institute. 1989. SAS/STAT User's Guide, Release 6.03. Ed. Cary, N.C
  54. Salt, G. 1935. Experimental studies in insect parasitism. III. Host selection. Proc. R. Entomol. Soc. Lond. 117: 413-435
  55. 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
  56. 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 https://doi.org/10.1111/j.1570-7458.1985.tb00462.x
  57. 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
  58. 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 https://doi.org/10.1016/j.jip.2007.02.009
  59. 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 https://doi.org/10.1016/S1226-8615(08)60343-X
  60. 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 https://doi.org/10.1016/j.ibmb.2007.09.013
  61. Smith, E.L. 1970. Evolutionary morphology of the external insect genitalia. 2. Hymenoptera. Ann. Entomol. Soc. Am. 63: 1-27 https://doi.org/10.1093/aesa/63.1.1
  62. Smith, S.M. 1996. Biological control with Trichogramma: advances, successes, and potential of their use. Annu. Rev. Entomol. 41: 375-406 https://doi.org/10.1146/annurev.en.41.010196.002111
  63. Stanley, D. 2000. Eicosanoids in invertebrate signal transduction systems. Priceton University Press, New Jersey
  64. Stanley, D. 2006. Prostaglandins and other eicosanoids in insects: biological significance. Annu. Rev. Entomol. 51: 25-44 https://doi.org/10.1146/annurev.ento.51.110104.151021
  65. Strand, M.R. and L.L. Pech. 1995. Immunological basis for compatibility in parasitoid host relationships. Annu. Rev. Entomol. 40: 31-56 https://doi.org/10.1146/annurev.en.40.010195.000335
  66. 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)
  67. 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 https://doi.org/10.1111/j.1432-1033.1989.tb15201.x
  68. 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
  69. Voegelé, J., J. Cals-Usciati, J.P. Pihan and J. Daumal. 1975. Structure de l'antenne des Trichogrammes. Entomophaga 20: 161-169 https://doi.org/10.1007/BF02371656

Cited by

  1. Developmental Performance and Parasitism of Trichogramma chilonis Ishii on Eggs of the Oriental Tobacco Budworm, Helicoverpa assulta(Guenee), and the American Bollworm, Helicoverpa armigera (Hubner) Depending on Previous Hosts vol.49, pp.4, 2010, https://doi.org/10.5656/KSAE.2010.49.4.393