Skip to main content
SpringerLink
Log in

Factitious host species impact on the outcome of multiparasitism between egg parasitoids

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Trichogramma parasitoids are biological control agents of a large number of lepidopterous pests. Mass production of these Trichogramma parasitoids is carried out on different factitious host eggs where the cost for mass rearing is high and the production efficiency is low. Therefore, efficient means and techniques for mass production of these parasitoids are needed. Host eggs of Chinese oak silkworm, Antheraea pernyi, not only proved effective for the mass production of a single Trichogramma species but also showed great potential for simultaneously producing two different Trichogramma species through multiparasitism. Here, we evaluated the outcomes of multiparasitism between Trichogramma chilonis and T. leucaniae reared on the eggs of two factitious hosts, Antheraea pernyi and Corcyra cephalonica. Our study indicated that parental wasps of both Trichogramma species reared on A. pernyi performed outstandingly in all aspects of multiparasitism on A. pernyi eggs. In contrast, significantly low parasitism rates for parental wasps reared on C. cephalonica and subsequently low emergence rates for their offspring were recorded for multiparasitism on A. pernyi eggs. Parental wasps reared on different host eggs significantly affected the emerged offspring numbers for both Trichogramma species per A. pernyi egg. Significantly high numbers of offspring for specific species of Trichogramma emerged per A. pernyi egg when the parental wasps of that species were reared on A. pernyi eggs compared to the other species reared on C. cephalonica eggs. The present study concluded that rearing host species had a great impact on the performance of parental wasps in the multiparasitism of Trichogramma parasitoids on A. pernyi eggs and clearly confirmed that T. chilonis and T. leucaniae parasitoids can be massively produced on A. pernyi eggs through multiparasitism. Our results provide useful information about rearing hosts, which could provide two different Trichogramma species in the field at a time for the suppression of pest populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Andrade GS, Pratissoli D, Dalvi LP, Desneux N, Gogcalves HJ (2011) Performance of four Trichogramma species (Hymenoptera: Trichogrammatidae) as biocontrol agents of Heliothis virescens (Lepidoptera: Noctuidae) under various temperature regimes. J Pest Sci 84:313–320

    Article  Google Scholar 

  • Bergeijk KE, Bigler F, Kaashoek NK, Pak GA (1989) Changes in host acceptance and host suitability as an effect of rearing Trichogramma maidis on a factitious host. Entomol Exp Appl 52:229–238

    Article  Google Scholar 

  • Chailleux A, Desneux N, Seguret J, Maignet P, Khanh HDT, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE 7:e48068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013a) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest, Tuta absoluta. J Pest Sci 86:533–541

    Article  Google Scholar 

  • Chailleux A, Biondi A, Han P, Tabone E, Desneux N (2013b) Suitability of the pest-plant system Tuta absoluta (Lepidoptera: Gelechiidae)–tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control. J Econ Entomol 106:2310–2321

    Article  PubMed  Google Scholar 

  • Corrigan JE, Laing JE (1994) Effects of the rearing host species and the host species attacked on performance by Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae). Environ Entomol 3:755–760

    Article  Google Scholar 

  • Cusumano A, Peri E, Vinson SB, Colazza S (2012) Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids. Biocontrol 57:719–734

    Article  Google Scholar 

  • Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE (2009a) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160:387–398

    Article  PubMed  Google Scholar 

  • Desneux N, Starỳ P, Delebecque CJ, Gariepy TD, Barta RJ, Hoelmer KA, Heimpel GE (2009b) Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxyx koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae). Ann Entomol Soc Am 102:925–936

    Article  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narvaez-Vasquez CA, Gonzalez-Carbrera J, Catalan Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbanrja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, history of invasion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Blahnik R, Delebecque CJ, Heimpel GE (2012) Host phylogeny and host specialization in parasitoids. Ecol Lett 15:453–460

    Article  PubMed  Google Scholar 

  • Du WM, Xu J, Hou YY, Lin Y, Zang LS, Yang X, Zhang JJ, Ruan CC, Desneux N (2017) Trichogramma parasitoids can distinguish between fertilized and unfertilized host eggs. J Pest Sci 91:771–780

    Article  Google Scholar 

  • El-Arnaouty A, Pizzol J, Galal HH, Kortam MN, Afifi AI, Beyssat V, Desneux N, Biondi A, Heikal IH (2014) Assessment of the efficacy of two Trichogramma species in controlling Tuta absoluta in North African tomato greenhouses. African Entomology 22:801–809

    Article  Google Scholar 

  • Greenberg SM, Donald AN, Zhixin W (1998) Influence of rearing host on adult size and ovipositional behavior of mass produced female Trichogramma minutum Riley and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Biol Control 11:43–48

    Article  Google Scholar 

  • Hassan SA, Liscsinszky H, Zhang G (2004) The oak-silkworm egg Antheraea pernyi (Lepidoptera: Anthelidae) as a mass rearing host for parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae). Biocontrol Sci Technol 14:269–279

    Article  Google Scholar 

  • Huang SS, Zang LS, Ruan CC (2013) Parasitization ecology, mass production, and application of Trichogramma. Science Press, Beijing, pp 116–140

    Google Scholar 

  • Huang J, Hua HQ, Zhang F, Li YX (2017) Suitability assessment of three Trichogramma species in the control of Mythimna separate (Lepidoptera: Noctuidae). J Appl Entomol 142:131–140

    Article  CAS  Google Scholar 

  • Institute SAS (2010) SAS/STAT v.9.1. SAS Institute, Cary, NC

    Google Scholar 

  • Li TH, Tian CY, Zang LS, Hou YY, Ruan CC, Yang XB, Lucie M, Desneux N (2018) Multiparasitism with Trichogramma dendrolimi on egg of Chinese oak silkworm, Antheraea pernyi, enhances emergence of Trichogramma ostriniae. J Pest Sci https://doi.org/10.1007/s10340-018-1018-5

  • Liu SS, Zhang GM, Zhang F (1998) Factors influencing parasitism of Trichogramma dendrolimi on eggs of the Asian corn borer, Ostrinia furnacalis. Biocontrol 43:273–287

    Article  Google Scholar 

  • Liu ZC, Liu JF, Zhang F, Li DS, Feng XX (2000) Production and field application techniques of Trichogramma. Golden Shield Press, Beijing

    Google Scholar 

  • Liu PC, Wang JJ, Zhao B, Men J, Wei JR (2017) Influence of natal host and oviposition experience on sex allocation in a solitary egg parasitoid, Anastatus disparis (Hymenoptera, Eupelmidae). J Hymenopt Res 58:29–40

    Article  Google Scholar 

  • Monticelli LS, Nguyen LTH, Amiens-Desneux E, Luo C, Desneux N (2019) The preference-performance relationship as a means of classifying parasitoids according to their specialization degree. Accepted pending revisions. Evolutionary Ecology. Accepted

  • Moser SE, Alleyne M, Wiedenmann RN, Hanks LM (2008) Influence of oviposition experience on multiparasitism by Pimpla disparis Vierick and Itoplectis conquisitor Say (Hymenoptera: Ichneumonidae). Environ Entomol 37:1307–1312

    Article  PubMed  Google Scholar 

  • Pinto JD (1992) Novel taxa of Trichogramma from the new world tropics and Australia (Hymenoptera: Trichogrammatidae). J N Y Entomol Soc 100:621–633

    Google Scholar 

  • Pizzol J, Pintureau B, Khoualdia O, Desneux N (2010) Temperature-dependent differences in biological traits between two strains of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). J Pest Sci 83:447–452

    Article  Google 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. J Pest Sci 85:489–496

    Article  Google Scholar 

  • Price PW (1972) Parasitoids utilizing the same host: adaptive nature of difference in size and form. Ecology 53:190–195

    Article  Google Scholar 

  • Schmidt JM (1994) Host recognition and acceptance by Trichogramma. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp 165–200

    Google Scholar 

  • Shi ZH, Liu SS (2003) Interspecific interactions between Cotesia plutellae and Oomyzus sokolowskii, two major parasitoids of diamondback moth, Plutella xylostella. Chin J Appl Ecol 14:949–954

    Google Scholar 

  • Smith SM (1996) Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol 41:375–406

    Article  CAS  PubMed  Google Scholar 

  • Song LW, Wen XY, Zang LS, Ruan CC, Shi SS, Shao XW, Zhang F (2015) Parasitism and suitability of different egg ages of the Leguminivora glycinivorella (Lepidoptera: Tortricidae) for three indigenous Trichogramma species. J Econ Entomol 108:933–939

    Article  CAS  PubMed  Google Scholar 

  • Stouthamer R, Hu J, van Kan FJPM, Platner GR, Pinto JD (1999) The utility of internally transcribed spacer 2 DNA sequences of the nuclear ribosomal gene for distinguishing sibling species of Trichogramma. Biocontrol 43:421–440

    Article  Google Scholar 

  • Tabone T, Bardon C, Desneux N, Wajnberg E (2010) Comparative assessment of parasitism of different Trichogramma spp. on Plutella xylostella L. on greenhouse cauliflower. J Pest Sci 83:251–256

    Article  Google Scholar 

  • Velzen EV, Vila SP, Etienne RS (2016) The role of within-host competition for coexistence in multiparasitoid-host systems. Am Nat 87:48–59

    Article  Google Scholar 

  • Wan FH, Ye ZC, Guo JY, Xie M (2000) Advances and prospects of biological control in China. Entomol Knowl 37:65–74

    Google Scholar 

  • Wang CL, Zhang J, Huo ST (1998) Study, reproduction and utilization of Trichogramma. In: Bao JZ, Gu DX (eds) Biological control in China. Shanxi Science and Technology Press, Taiyuan, pp 67–123

    Google Scholar 

  • Wang ZY, He KL, Yan S (2005) Large-scale augmentative biological control of Asian corn borer using Trichogramma in China: a success story. In: Conference paper: second international symposium on biological control of arthropods, Davos, Switzerland, pp 487–494

  • Wang JJ, Wei JR, Wang YZ, Zhang YC (2012) Relationship between temperature and development of Ooencyrtus kuvanae (Hymenoptera: Encyrtidae), the egg parasitoid of Lymantria dispar (Lepidoptera: Lymantriidae), with an evaluation of its offspring quality reared from eggs of the substitute host Antheraea pernyi (Lepidoptera: Saturniidae). Acta Entomol Sinica 55:570–574

    Google Scholar 

  • Wang JJ, Liu XB, Zhang YA, Wen C, Wei JR (2013) The reproductive capability of Ooencyrtus kuvanae reared on eggs of the factitious host Antheraea pernyi. J Appl Entomol 138:267–272

    Article  Google Scholar 

  • Wang ZY, He KL, Zhang F, Lu X, Babendreier D (2014) Mass rearing and release of Trichogramma for biological control of insect pests of corn in China. Biol Control 68:136–144

    Article  Google Scholar 

  • Yuan XH, Song LW, Zhang JJ, Zang LS, Zhu L, Ruan CC, Sun GZ (2012) Performance of four Chines Trichogramma species as biocontrol agents of the rice striped stem borer, Chilo suppressalis, under various temperature and humidity regimes. J Pest Sci 85:497–504

    Article  Google Scholar 

  • Zang LS (2015) Mass production of Trichogramma dendrolimi using eggs of Antheraea pernyi, and field application in the suppression of Ostrinia furnacalis in Jilin Province, China. IOBC Newsl 98:9

    Google Scholar 

  • Zhang JJ, Zhang X, Zang LS, Du WM, Hou YY, Ruan CC, Desneux N (2018) Advantages of diapause in Trichogramma dendrolimi mass production via eggs of the Chinese silkworm, Antheraea pernyi. Pest Manag Sci 74:959–965

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was funded by the National Natural Science Foundation of China (31572058) and the National Key R&D Program of China (2017YFD0201000).

Author information

Authors and Affiliations

  1. Jilin Engineering Research Center of Resource Insects Industrialization, Institute of Biological Control, Jilin Agricultural University, Changchun, China

    Asim Iqbal, Yong-Ming Chen, Yang-Yang Hou & Lian-Sheng Zang

  2. USDA-ARS Sino-American Biological Control Laboratory/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China

    Lisheng Zhang

  3. INRA (French National Institute for Agricultural Research), CNRS UMR 1355-7254, Institute Sophia Agrobiotech, Université Côte D’Azur, 06903, Sophia-Antipolis, France

    Nicolas Desneux

Authors
  1. Asim Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yong-Ming Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang-Yang Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lisheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicolas Desneux
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lian-Sheng Zang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lian-Sheng Zang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Communicated by M. Traugott.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iqbal, A., Chen, YM., Hou, YY. et al. Factitious host species impact on the outcome of multiparasitism between egg parasitoids. J Pest Sci 92, 1261–1269 (2019). https://doi.org/10.1007/s10340-019-01122-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-019-01122-8

Keywords

Search

Navigation