Hostname: page-component-848d4c4894-2xdlg Total loading time: 0 Render date: 2024-06-19T18:30:28.408Z Has data issue: false hasContentIssue false

Number of attacks by Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) affects the successful parasitism of Ostrinia furnacalis (Lepidoptera: Crambidae) eggs

Published online by Cambridge University Press:  11 April 2017

J. Huang
Affiliation:
Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
H.-Q. Hua
Affiliation:
Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
L.-Y. Wang
Affiliation:
Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
F. Zhang
Affiliation:
Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
Y.-X Li*
Affiliation:
Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
*
*Author for correspondence Fax/Phone: 862584395868 E-mail: yxli@njau.edu.cn

Abstract

In laboratories, the parasitism rate of Ostrinia furnacalis (Güenée) (Lepidoptera: Crambidae) eggs by Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) is low; however, efforts to control O. furnacalis with T. dendrolimi in the field have been successful. In this study, the effects of the number of attacks by T. dendrolimi against O. furnacalis eggs and diet of O. furnacalis larva on wasp development were investigated. The results indicated that more attacks increased significantly not only the successful parasitism rate of O. furnacalis eggs by T. dendrolimi, but also the percentage of host eggs that failed to develop into either O. furnacalis larvae or T. dendrolimi. Both the size and female proportion of T. dendrolimi offspring decreased as the number of attacks increased. The number of T. dendrolimi eggs laid in per host egg increased significantly as the ratio of wasps to host eggs increased from 1:5 to 3:5. Host diet also significantly affected the developmental time of immaturity and the emergence rate of adults of T. dendrolimi. These results illustrate how inundative releases of T. dendrolimi can successfully control O. furnacalis despite the fact that pest parasitism by the subsequent wasp generation decreases sharply in the field. The suitability of O. furnacalis eggs to T. dendrolimi and the superparasitism effects on offspring of T. dendrolimi are discussed.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-latief, M. & Hilker, M. (2008) Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. Insect Biochemistry and Molecular Biology 38, 136145.10.1016/j.ibmb.2007.10.001Google Scholar
Abram, P.K., Brodeur, J., Burte, V. & Boivin, G. (2016) Parasitoid-induced host egg abortion: an underappreciated component of biological control services provided by egg parasitoids. Biological Control 98, 5260.10.1016/j.biocontrol.2016.04.002Google Scholar
Babendreier, D., Rostas, M., Hofte, M.C.J., Kuske, S. & Bigler, F. (2003) Effects of mass releases of Trichogramma brassicae on predatory insects in maize. Entomologia Experimentalis et Applicata 108, 115124.10.1046/j.1570-7458.2003.00075.xGoogle Scholar
Bai, W., Sun, Z.X., Zheng, J.M., Hou, Z.Y., Liu, Y., Feng, L.S. & Yang, N. (2014) Effect of different planting patterns on maize growth and yield in western Liaoning province. Acta Agronomica Sinica 40, 181189.10.3724/SP.J.1006.2014.00181Google Scholar
Barrett, M. & Schmidt, J.M. (1991) A comparison between the amino acid composition of an egg parasitoid wasp and some of its hosts. Entomologia Experimentalis et Applicata 59, 2941.10.1111/j.1570-7458.1991.tb01483.xGoogle Scholar
Boivin, G. & Martel, V. (2012) Size-induced reproductive constraints in an egg parasitoid. Journal of Insect Physiology 58, 16941700.10.1016/j.jinsphys.2012.10.014Google Scholar
Chen, T.H., Li, M., Wang, J.H., Zhang, F. & Li, Y.X. (2013) Vulnerability window for laying male eggs and superparasitism in producing female offspring of Encarsia sophia on Bemisia tabaci B biotype. BioControl 58, 2736.Google Scholar
Corrigan, J.E., Laing, J.E. & Zubricky, J.S. (1995) Effects of parasitoid to host ratio and time of day of parasitism on development and emergence of Trichogramma minutum (Hymenoptera: Trichogrammatidae). Annals of the Entomological Society of America 88, 773780.10.1093/aesa/88.6.773Google Scholar
Dasilva, C.S.B., Morelli, R. & Parra, J.R.P. (2016) Effects of self-superparasitism and temperature on biological traits of two neotropical Trichogramma (Hymenoptera: Trichogrammatidae) species. Journal of Economic Entomology 109, 15551563.10.1093/jee/tow126Google Scholar
Dias, N.D.S., Parra, J.R.P. & Cônsoli, F.L. (2010) Egg laying and development of Neotropical Trichogrammatid species in artificial eggs. Entomologia Experimentalis et Applicata 137, 126131.10.1111/j.1570-7458.2010.01045.xGoogle Scholar
Doutt, R.L. (1959) The biology of parasitic hymenoptera. Annual Review of Entomology 4, 161182.10.1146/annurev.en.04.010159.001113Google Scholar
Durocher-Granger, L., Martel, V. & Boivin, G. (2011) Gamete number and size correlate with adult size in the egg parasitoid Trichogramma euproctidis. Entomologia Experimentalis et Applicata 140, 262268.Google Scholar
Feng, J.G. (1996) The effect and influence factors on the use of Trichogramma dendrolimi to control Ostrinia furnacalis. Entomological Journal of East China 5, 4550.Google Scholar
Feng, G., Li, Y.Y., Jing, X.Q., Wang, L. & Huang, C.L. (2011) Effects on agronomic characteristics and yield of maize planting density. Journal of Maize Sciences 19, 109111.Google Scholar
Godin, C. & Boivin, G. (2000) Effects of host age on parasitism and progeny allocation in Trichogrammatidae. Entomologia Experimentalis et Applicata 97, 149160.Google Scholar
Grenier, S., Grille, G., Basso, C. & Pintureau, B. (2001) Effects of the host species and the number of parasitoids per host on the size of some Trichogramma species (Hymenoptera: Trichogrammatidae). Biocontrol Science and Technology 11, 2126.10.1080/09583150020029709Google Scholar
Gu, C.Y., Liang, Y.C. & Zhang, G.Z. (1989) The damage of corn borer to maize yield in Heilongjiang province. Acta Phytophylacica Sinica 16, 265268.Google Scholar
Hamilton, W.D. (1967) Extraordinary sex ratio. Science 156, 477488.Google Scholar
Honěk, A. (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66, 483492.Google Scholar
Huang, J., Zhang, B., Zhang, F. & Li, Y.X. (2015) Effect of rearing host on the size and egg load of three Trichogramma species (Hymenoptera: Trichogrammatidae). Acta Entomologica Sinica 58, 10981107.Google Scholar
Jarjees, E.A. & Merritt, D.J. (2004) The effect of parasitization by Trichogramma australicum on Helicoverpa armigera host eggs and embryos. Journal of Invertebrate Pathology 85, 18.10.1016/j.jip.2003.12.001Google Scholar
Klomp, H. & Teerink, B.J. (1962) Host selection and number of eggs per oviposition in the egg parasite Trichogramma embryophagum Htg. Nature 195, 10201021.10.1038/1951020a0Google Scholar
Klomp, H. & Teerink, B.J. (1978) The elimination of supernumerary larvae of the gregarious egg-parasitoid, Trichogramma embryophagum (Hym.: Trichogrammatidae) in eggs of the host Ephestia kuehniella (Lep.: Pyralidae). Entomophaga 23, 153159.10.1007/BF02371721Google Scholar
Li, Y., Dai, H., Jiang, J., Fu, W. & Sun, Z. (2002) Comparison study of suitability of Ostrinia furnacalis eggs for three Trichogramma species. Journal of Nanjing Agricultural University 25, 3538.Google Scholar
Li, Y.X., Dai, H.G. & Fu, W.J. (2008) Suitability of Corcyra cephalonica to three Trichogramma species and change of the content of free amino acids in its eggs parasitized. Acta Entomologica Sinica 51, 628634.Google Scholar
Liu, S.S. & He, J.H. (1991) Observing ovipositional behaviour of Trichogramma dendrolimi Matsumura. pp. 7376 in Wajnberg, E. & Vinson, S.B. (Eds) Trichogramma and Other Egg Parasitoids, Colloques De L INRA. Volume 56. San Antonio, TX, Third International Symposium on Trichogramma and Other Egg Parasitoids, May 23–27, 1990.Google Scholar
Liu, S.S., Zhang, G.M. & Zhang, F. (1998) Factors influencing parasitism of Trichogramma dendrolimi on eggs of the Asian corn borer, Ostrinia furnacalis. BioControl 43, 273287.10.1023/A:1009984125066Google Scholar
Martel, V. & Boivin, G. (2004) Impact of competition on sex allocation by Trichogramma. Entomologia Experimentalis et Applicata 111, 2935.10.1111/j.0013-8703.2004.00146.xGoogle Scholar
Miura, K., Matsuda, S. & Kobayashi, M. (1994) Discrimination between parasitized and unparasitized hosts in an egg parasitoid, Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae). Applied Entomology and Zoology 29, 317322.Google Scholar
Narendran, T.C. (1985) An analysis of the superparasitic behavior and host discrimination of chalcid wasps (Hymenoptera: Chalcidoidea). Proceeding of Indian Academic Science (Anim Sci) 94, 325331.Google Scholar
Nathan, S.S., Kalaivani, K., Mankin, R.W. & Murugan, K. (2006) Effects of millet, wheat, rice, and sorghum diets on development of Corcyra cephalonica (Stainton) (Lepidoptera: Galleriidae) and its suitability as a host for Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae). Environmental Entomology 35, 784788.10.1603/0046-225X-35.3.784Google Scholar
Nettles, W.C., Morrison, R.K., Xie, Z.N., Ball, D., Shenkir, C.A. & Vinson, S.B. (1983) Effect of cations, anions and salt concentrations on oviposition by Trichogramma pretiosum Riley in wax eggs. Entomologia Experimentalis et Applicata 33, 283289.10.1111/j.1570-7458.1983.tb03270.xGoogle Scholar
Pavlík, J. (1993) Variability in the host acceptance of European corn borer, Ostrinia nubilalis Hbn. (Lep., Pyralidae) in strains of the egg parasitoid Trichogramma spp. (Hym., Trichogrammatidae). Journal of Applied Entomology 115, 7784.10.1111/j.1439-0418.1993.tb00366.xGoogle Scholar
Pizzol, J., Desneux, N., Wajnberg, E. & Thiéry, D. (2012) Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. Journal of Pest Science 85, 489496.Google Scholar
Ruberson, J.R. & Kring, T.J. (1993) Parasitism of developing eggs by Trichogramma pretiosum (Hymenoptera: Trichogrammatidae): host age preference and suitability. Biological Control 3, 3946.10.1006/bcon.1993.1007Google Scholar
Salt, G. (1938) Experimental studies in insect parasitism. VI. host suitability. Bulletin of Entomological Research 29, 223246.Google Scholar
Shen, X.C., Wang, K.Z. & Meng, G. (1986) Field experiment of inoculative releases of Trichogramma spp. in the early season in Henan province. Chinese Journal of Biological Control 2, 152154.Google Scholar
Song, S.J., Bourchier, R.S. & Smith, S.M. (1997) Effect of host diet on acceptance of eastern spruce budworm eggs by Trichogramma minutum. Entomologia Experimentalis et Applicata 84, 4147.Google Scholar
Suzuki, Y., Tsuji, H. & Sasakawa, M. (1984) Sex allocation and effects of superparasitism on secondary sex ratios in the gregarious parasitoid, Trichogramma chilonis (Hymenoptera: Trichogrammatidae). Animal Behaviour 32, 478484.Google Scholar
Takada, Y., Kawamura, S. & Tanaka, T. (2000) Biological characteristics: growth and development of the egg parasitoid Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) on the cabbage armyworm Mamestra brassicae (Lepidoptera: Noctuidae). Applied Entomology and Zoology 35, 369379.Google Scholar
Trauer-Kizilelma, U. & Hilker, M. (2015) Impact of transgenerational immune priming on the defence of insect eggs against parasitism. Developmental and Comparative Immunology 51, 126133.Google Scholar
van Alphen, J.J.M. & Visser, M.E. (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology 35, 5979.Google Scholar
van Dijken, M.J. & Waage, J.K. (1987) Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomologia Experimentalis et Applicata 43, 183192.Google Scholar
van Lenteren, J.C. & Bakker, K. (1975) Discrimination between parasitised and unparasitised hosts in the parasitic wasp Pseudeucoila bochei: a matter of learning. Nature 254, 417419.Google Scholar
Vinson, S.B. (1976) Host selection by insect parasitoids. Annual Review of Entomology 21, 109133.Google Scholar
Vinson, S.B. & Iwantsch, G.F. (1980) Host suitability for insect parasitoids. Annual Review of Entomology 25, 397419.Google Scholar
Waage, J.K. & Ming, N.S. (1984) The reproductive strategy of a parasitic wasp. I. Optimal progeny and sex allocation in Trichogramma evanescens. Journal of Animal Ecology 53, 401416.Google Scholar
Wang, Z.Y. & Zhou, D.R. (1998) Comparison the virulence of the Asian corn borer larvae reared for different generations on a semi-artificial diet to a susceptible corn hybrid. Plant Protection 24, 35.Google Scholar
Wang, Z., Lu, X., He, K. & Zhou, D. (2000) Review of history, present situation and prospect of the Asian maize borer research in China. Journal of Shenyang Agricultural University 31, 402412.Google Scholar
Wang, Z.Y., He, K.L., Zhang, F., Lu, X. & Babendreier, D. (2014) Mass rearing and release of Trichogramma for biological control of insect pests of corn in China. Biological Control 68, 136144.Google Scholar
Wang, D., Lu, L., He, Y., Shi, Q., Tu, C. & Gu, J. (2016) Mate choice and host discrimination behaviour of the parasitoid Trichogramma chilonis. Bulletin of Entomological Research 106, 530537.Google Scholar
Zhang, Z.L., Huang, R.S., Zhu, Y., Wang, S.Q., Kang, Z.J., Pan, Y.C., Yin, Y.H., Zhang, W.S., Yun, X.Q. & Sun, A.H. (1979) Primary study on controlling Ostrinia furnacalis by using Trichogramma ostriniae. Chinese Bulletin of Entomology 16, 207210.Google Scholar
Zhang, J., Wang, J.L., Cong, B. & Yang, C.C. (1990) A faunal study of Trichogramma (Hym.: Trichogrammatidae) species on Ostrinia furnacalis (Lep.: Pyralidae) in China. Chinese Journal of Biological Control 6, 4953.Google Scholar
Zhang, Y.F., Song, Q.T., Zhang, F. & Li, Y.X. (2010) Comparison of superparasitism and suitability to superparasitism between Trichogramma ostriniae and T. dendrolimi. Chinese Journal of Biological Control 26, 377384.Google Scholar
Zhou, D.R., Wang, Y.Y., Liu, B.L. & Ju, Z.L. (1980) Studies on the mass rearing of corn borer I. Development of a satisfactory artificial diet for larval growth. Acta Phytophylacica Sinica 7, 113122.Google Scholar
Zhou, S.X., Lu, X., Wang, Z.Y., Li, L.J., Zhang, G.H. & Ding, Y. (2014) Study on the corn yield loss damaged by the second generation of Asian corn borer, Ostrinia furnacalis (Güenée). Chinese Journal of Applied Entomology 51, 676679.Google Scholar
Zhu, P., Zhang, Y.F., Song, Q.T., Zhang, F. & Li, Y.X. (2014) The suitability of Ostrinia furnacalis (Lepidoptera: Crambidae) eggs for Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) can be changed by T. ostriniae. Applied Entomology and Zoology 49, 265272.Google Scholar