Korean Journal of Environmental Biology (환경생물)

Korean Society of Environmental Biology (한국환경생물학회)
권호 표지
DOI QR코드

DOI QR Code

First report of Telenomus remus Nixon(Scelionidae), an egg parasitoid of Spodoptera frugiperda(J.E. Smith)(Noctuidae) in Korea and its biological characteristics

한국에서 열대거세미나방 알기생벌 Telenomus remus Nixon (가칭: 밤나방검정알벌)[검정알벌과]의 첫 보고 및 생물적 특성 연구

  • Jum Rae Cho (Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Bo Yoon Seo (Crop Foundation Division, National Institute of Crop Science, Rural Development Administration) ;
  • June Yeol Choi (Crop Foundation Division, National Institute of Crop Science, Rural Development Administration) ;
  • Gwan Seok Lee (Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Meeja Seo (Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Jeong Hwan Kim (Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration)
  • 조점래 (농촌진흥청 국립농업과학원 작물보호과) ;
  • 서보윤 (농촌진흥청 국립식량과학원 작물기초기반과) ;
  • 최준열 (농촌진흥청 국립식량과학원 작물기초기반과) ;
  • 이관석 (농촌진흥청 국립농업과학원 작물보호과) ;
  • 서미자 (농촌진흥청 국립농업과학원 작물보호과) ;
  • 김정환 (농촌진흥청 국립농업과학원 작물보호과)
  • Received : 2022.05.11
  • Accepted : 2022.06.17
  • Published : 2022.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

In this study, Telenomus remus Nixon (Hymenoptera: Scelionidae) was first reported as a natural enemy of the fall armyworm Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) egg collected from corn fields in Korea, and its biological characteristics was studied. Based on morphological and molecular analysis, the parasitoid emerged from S. frugiperda eggs was identified as T. remus. We found that T. remus can attack the eggs of S. frugiperda, Spodoptera litra and Spodoptera exigua under a laboratory condition. The longevity of T. remus female adult was longer than that of male adult. The egg-to-adult period of T. remus was not affected by the host age and sex. T. remus female adult laid at least 1-3 eggs a day to a maximum of 37 or more eggs, and the most oviposited on the 3rd to 4th day after emergence. The host preference for oviposition of T. remus adult was high in the order of S. litura>S. exigua>S. frugiperda. T. remus preferred to parasitize 1- and 2-day-old host egg rather than 3-day-old host egg. When compared to the sex ratio of T. remus progeny, the rate of female progeny was higher at the initiation time of oviposition, while the proportion of male progeny increased significantly with female adult age, especially after 8-day-old adult. This information may be useful for improving T. remus mass rearing system and developing a biological control program to control S. frugiperda.

본 연구에서는 국내 옥수수 포장에서 채집한 열대거세미나방 알덩어리로부터 우화한 알기생벌을 형태 및 분자동정하여 검정알벌과(Scelionidae)의 Telenomus remus Nixon (1937) [(가칭)밤나방검정알벌]로 최초로 확인되었다. T. remus 성충의 수명 및 발육기간(알-성충까지)은 기주 종류 및 성별에 따른 차이가 없었다. T. remus 암컷 성충은 우화 후 바로 산란하고, 하루에 1~3개에서부터 최고 37개까지 산란하였으며, 우화 후 1~2일째 가장 많이 산란하였다. 총 산란수는 기주로 열대거세미나방 알을 사용하였을 경우 평균 118.4 (7.0~352.0)개, 담배거세미나방의 알에서는 평균 164.9 (5.0~372.0)개로 담배거세미나방 알을 사용하였을 때 산란수가 많았으나, 유의미한 차이는 없었다. T. remus의 산란 기주 선호도는 담배거세미나방>파밤나방>열대거세미나방 순으로 높았다. 기주 알의 나이에 따라 T. remus의 선호도가 달랐는데, 1~2일 된 알을 선호하였다. T. remus 자손의 암수 비율은 기주와 상관없이 암컷의 비율이 수컷보다 높았으며, 산란 초기에는 암컷 산자의 비율이 높다가 나이가 들수록 수컷 산자의 비율이 현저하게 높았다. 교미하지 않은 T. remus 암컷이 산란하여 부화한 경우, 100% 수컷 성충으로 arrhenotoky type의 단위생식을 보여주었으며, 교미하여 산란한 경우, 암수의 비율은 8.0 : 2.0로 암컷의 비율이 높았다. T. remus는 중복기생자(gregarious egg parasitoid)가 아닌 단독기생자(solitary egg parasitoid)로 판단된다. 본 연구에서 보고한 T. remus의 생물적 특성에 관한 연구 결과는 실험실 조건에서 대량생산을 위한 정보로 활용하거나 생물적방제 프로그램을 개발할 때 활용될 수 있을 것이다.

Keywords

Acknowledgement

본 연구는 농촌진흥청 국제농업기술협력사업(과제번호:PJ0164962022)예산 지원으로 수행하였습니다.

References

  1. Bartlett BR and JC Ball. 1964. The developmental biologies of two encyrtid parasites of Coccus hesperidum and their intrinsic competition. Ann. Entomol. Soc. Am. 57:496-503. https://doi.org/10.1093/aesa/57.4.496
  2. Bartlett BR and RA Medved. 1966. The biology and effectiveness of Diversinervus elegans (Encyrtidae: Hymenoptera), an impor-ted parasite of lecaniine scale insects in California. Ann. Entomol. Soc. Am. 59:974-976. https://doi.org/10.1093/aesa/59.5.974
  3. Borges M, MLM Costa, ER Sujii, M Cavalcanti, GF Redigolo, TS Resck and EF Vilela. 1999. Semiochemical and physical stimuli involved in host recognition by Telenomus podisi (Hymenoptera: Scelionidae) toward Euchistus heros (Heteroptera: Pentatomidae). Physiol. Entomol. 24:227-233. https://doi.org/10.1046/j.1365-3032.1999.00136.x
  4. Bueno RCOF, TR Carneiro, AF Bueno, D Pratissoli, OA Fernandes and SS Vieira. 2010. Parasitism capacity of Telenomus remus Nixon (Hymenoptera: Scelionidae) on Spodoptera frugiperda (Smith)(Lepidoptera: Noctuidae) eggs. Braz. Arch. Biol. Techn. 53:133-139. https://doi.org/10.1590/S1516-89132010000100017
  5. Bueno RCOF, JRP Parra, AF Bueno and ML Haddad. 2009. Desempenho de Tricogramatideos como potenciais agentes de controle de Pseudoplusia includens Walker (Lepidoptera: Noctuidae). Neotrop. Entomol. 38:389-394. https://doi.org/10.1590/S1519-566X2009000300015
  6. Casmuz A, ML Juarez, MG Socias, MG Murua, S Prieto and S Medina. 2010. Revision de los hospederos del gusano cogollero del maiz, Spodoptera frugiperda (Lepidoptera: Noctuidae). J. Ar. Entomol. Soc. 69:209-231.
  7. Cave RD. 2000. Biology, ecology and use in pest management of Telenomus remus. Biocontrol News Inf. 21:21N-26N.
  8. Choi JY. 1999. Taxonomic study on the family Scelionidae in Korea (Hymenoptera: Platygastroidea). Ph.D. dissertation, Seoul National University. Seoul.
  9. Chou LY. 1987. Note on Telenomus remus(Hymenoptera: Scelionidae). Bull. Soc. Entomol. Nat. Chung-Hsing Univ. 20:15-20.
  10. Consoli FL, EW Kitajima and JRP Parra. 1999. Ultrastructure of the natural and factitious host eggs of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera, Trichogrammatidae). Int'l. J. Insect Morphol. Embryol. 28:211-229. https://doi.org/10.1016/S0020-7322(99)00026-4
  11. Dorn S and NE Beckage. 2007. Superparasitism in gregarious hymenopteran parasitoids: ecological, behavioural and physiological perspectives. Physiol. Entomol. 32:199-211. https://doi.org/10.1111/j.1365-3032.2007.00576.x
  12. Folmer O, M Black, W Hoeh, R Lutz and R Vrijenhoek. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3:294-299.
  13. Goergen G, PL Kumar, SB Sankung, A Togola and M Tamo. 2016. First report of outbreaks of the fall armyworm Spodoptera frugiperda (JE Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. PLoS One 11:e0165632.
  14. Goulart MMP, AF Bueno, RCOF Bueno and AF Diniz. 2011. Host preference of the egg parasitoids Telenomus remus and Trichogramma pretiosum in laboratory. Rev. Brasil. Entomol. 55:129-133. https://doi.org/10.1590/S0085-56262011000100021
  15. Grbic M, PJ Ode and MR Strand. 1992. Sibling rivalry and brood sex ratios in polyembryonic wasps. Nature 360:254.
  16. Hendery S.2020. New study reveals natural enemies of fall armyworm in both Asia and Africa. Entomol. Today. Entomol. Soc. Am. Retrieved 23 July 2020.
  17. Hilker M and T Meiners. 2002. Chemoecology of Insect Eggs and Egg Deposition. Blackwell. Berlin. p. 390.
  18. Houseweart MW, DT Jennings, C Welty and SG Southard. 1983. Progeny production by Trichogramma minutum (Hymenoptera: Trichogrammatidae) utilizing eggs for Choristoneura fumiferana (Lepidoptera: Tortricidae) and Sitotroga cerealella (Lepidoptera: Gelechiidae). Can. Entomol. 115:1245-1252. https://doi.org/10.4039/Ent1151245-10
  19. Johnson SJ. 1987. Migration and the life history strategy of the fall armyworm, Spodoptera frugiperda in the Western Hemisphere. Insect Sci. Appl. 8:543-549.
  20. Kenis M, H du Plessis, J van den Berg, MN Ba, G Goergen, KE Kwadjo, I Baoua, T Tefera, A Buddie, G Cafa, L Offord, I Rwomushana and A Polaszek. 2019. Telenomus remus, a candidate parasitoid for the biological control of Spodoptera frugiperda in Africa, is already present on the continent. Insects 10:92.
  21. Koffi D, R Kyerematen, VY Eziah, K Agboka, M Adom, G Georgen and R Meagher. 2020. Natural enemies of the fall armyworm, Spodoptera frugiperda (J.E. Smith)(Lepidoptera: Noctuidae) in Ghana. Fla. Entomol. 103:85-90. https://doi.org/10.1653/024.103.0414
  22. Kumar S, G Stecher and K Tamura. 2015. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33:1870-1874. https://doi.org/10.1093/molbev/msw054
  23. Lee GS, BY Seo, J Lee, H Kim, JH Song and W Lee. 2020. First report of the fall armyworm, Spodoptera frugiperda (Smith, 1797) (Lepidoptera, Noctuidae), a new migratory pest in Korea. Korean J. Appl. Entomol. 59:73-78.
  24. Li XJ, MF Wu, J Ma, BY Gao, QL Wu, AD Chen, J Liu, YY Jiang, BP Zhai, R Early, JW Chapman and G Hu. 2019. Prediction of migratory routes of the invasive fall armyworm in eastern China using a trajectory analytical approach. Pest Manag. Sci. 76:454-463.
  25. Li XF, ZK Li, JC Zhu, BY Zheng, P Tang and XX Chen. 2021. The mitochondrial genome of Telenomus remus (Hymenoptera: Platygastridae), Mitochondrial DNA Part B-Resour. 6:844-845. https://doi.org/10.1080/23802359.2021.1884028
  26. Liao YL, B Yang, MF Xu, W Lin, DS Wang, KW Chen and HY Chen. 2019. First report of Telenomus remus parasitizing Spodoptera frugiperda and its natural parasitism in south China. J. Hymenoptera Res. 73:95-102. https://doi.org/10.3897/jhr.73.39136
  27. Mayhew PJ and JM van Alphen. 1999. Gregarious development in alysiine parasitoids evolved through a reduction in larval aggression. Anim. Behav. 58:131-141. https://doi.org/10.1006/anbe.1999.1106
  28. Mitchell ER, JN McNeil, JK Westbrook, JF Silvain, B Lalanne-Cassou, RB Chalfant, SD Pair, VH Waddill, A Sotomayor-Rios and FI Proshold. 1991. Seasonal periodicity of fall armyworm,(Lepidoptera: Noctuidae) in the Caribbean Basin and northward to Canada. J. Entomol. Sci. 26:39-50.
  29. Morales J, JS Gallardo, C Vasquez and Y Rios. 2000. Patron de emergencia, longevidad, parasitismo y proporcion sexual de Telenomus remus (Hymenoptera: Scelionidae) con relacion al cogollero del maiz. Bioagro. 12:47-54.
  30. Nagoshi RN, G Goergen, KA Tounou, K Agboka, D Koffi and RL Meagh. 2018. Analysis of strain distribution, migratory potential, and invasion history of fall armyworm populations in northern Sub-Saharan Africa. Sci. Rep. 8:3710.
  31. Naranjo-Guevara N, LAOD Santos, NCCP Barbosa, AC Morales Correa e Castro and OA Fernandes. 2020. Long-term mass rearing impacts performance of the egg parasitoid Telenomus remus (Hymenoptera: Platygastridae). J. Entomol. Sci. 55:69-86.
  32. Nixon GEJ. 1937. Some Asiatic Telenominae (Hym., Proctotrupoidea). Ann. Mag. Natural History. 20:444-475. https://doi.org/10.1080/00222933708655367
  33. Penaflor MFGV, MMM Sarmento, CSB Silva, AG Werneburg and JMS Bento. 2012. Effect of host egg age on preference, development and arrestment of Telenomus remus (Hymenoptera: Scelionide). Eur. J. Entomol. 109:15-20. https://doi.org/10.14411/eje.2012.003
  34. Pexton JJ and PJ Mayhew. 2002. Siblicide and life-history evolution in parasitoids. Behav. Ecol. 13:690-695. https://doi.org/10.1093/beheco/13.5.690
  35. Pyke GH, HR Pulliam and EI Charnov. 1977. Optimal foraging: a selective review of theory and tests. Q. Rev. Biol. 52:137-154. https://doi.org/10.1086/409852
  36. Schwartz A and D Gerling. 1974. Adult biology of Telenomus remus (Hymenoptera: Scelionidae) under laboratory conditions. Entomophaga 19:482-492.
  37. Schmidt JM and JJB Smith. 1985. Host volume 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
  38. Seo BY, CG Park, YH Koh, JK Jung, J Cho and C Kang. 2017. ITS2 DNA Sequence analysis for eight species of delphacid planthoppers and a loop-mediated isothermal amplification method for the brown planthopper-specific detection. Korean J. Appl. Entomol. 56:377-385.
  39. Sparks AN. 1979. A review of the biology of the fall armyworm. Fla. Entomol. 62:82-86. https://doi.org/10.2307/3494083
  40. Strand MR and SB Vinson. 1983. Analysis of an egg recognition kairomone of Telenomus heliothidis (Hymenoptera: Scelionidae). Isolation and host function. J. Chem. Ecol. 9:423-432. https://doi.org/10.1007/BF00988459
  41. Tang YL, KW Chen and ZF Xu. 2010. Study on ontogenesis of Telenomus remus Nixon (Hymenoptera: Scelionidae). J. Changjiang Vege. 18:1-3.
  42. Vinson SB. 1976. Host selection by insect parasitoids. Ann. Rev. Entomol. 21:109-134. https://doi.org/10.1146/annurev.en.21.010176.000545
  43. Vinson SB. 1984. Parasitoid-host relationships. pp. 205-233. In: Chemical Ecology of Insects (Bell WJ and Carde RT eds.). Chapman and Hall, London.
  44. Vinson SB, F Bin and LEM Vet. 1998. Critical issues in host selection by insect parasitoids. Biol. Control 11:77-78. https://doi.org/10.1006/bcon.1997.0600
  45. Wengrat APGS, A Coelho Jr and JRP Parra. 2021. Integrative taxonomy and phylogeography of Telenomus remus (Scelionidae), with the first record of natural parasitism of Spodoptera spp. in Brazil. Sci. Rep. 11:14110.
  46. Westbrook JK, RN Nagoshi, RL Meagher, SJ Fleischer and S Jairam. 2016. Modeling seasonal migration of fall armyworm moths. Int. J. Biometeorol. 60:255-267. https://doi.org/10.1007/s00484-015-1022-x
  47. White TJ, T Bruns, S Lee and J Taylor. 1990. Amplification and direct sequencing of fungal ribosomal genes for phylogenetics. pp. 315-322. In: PCR Protocols: a Guide to Methods and Applications (Innis MA, DH Gelfand, JJ Sninsky and TJ White, eds.). Academic Press, Inc., New York.