Skip to main content
SpringerLink
Log in

Trichogramma parasitoids can distinguish between fertilized and unfertilized host eggs

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

Abstract

Host quality varies with size, age, and species, and influences the parasitism preference of parasitoids and the fitness of their offspring. However, it is still unclear whether parasitoids have the ability to recognize fertilized and unfertilized host eggs. We studied the performance of three Trichogramma species, T. japonicum, T. chilonis, and T. leucaniae, on both fertilized and unfertilized eggs of their host Corcyra cephalonica at different host ages. In no-choice tests, three Trichogramma species parasitized significantly more fertilized than unfertilized eggs when host age was 0 days old. In choice tests, all parasitoids parasitized significantly more fertilized than unfertilized eggs at all host ages. Furthermore, the frequency of fertilized eggs visited by Trichogramma parasitoids were significantly higher than those of unfertilized eggs. The number of unfertilized eggs visited by parasitoids without ovipositing was approximately 3.7 times greater than those of fertilized eggs. In addition, all Trichogramma parasitoids developed significantly faster on fertilized than unfertilized eggs at all host ages. In summary, we find that Trichogramma were able to recognize fertilized and unfertilized host eggs in parasitism, which is conducive to biological control programs, since unfertilized eggs enlarge the host reservoir for parasitoid augmentation.

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
Fig. 2

Similar content being viewed by others

References

  • Alfaro C, Navarro-Llopis V, Primo J (2009) Optimization of pheromone dispenser density for managing the rice striped stem borer, Chilo suppressalis (Walker), by mating disruption. Crop Prot 28:567–572

    Article  CAS  Google Scholar 

  • Beevers M, Joe Lewis W, Gross JRHR, Nordlund DA (1981) Kairomones and their use for management of entomophagous of host-finding behavior of Trichogramma pretiosum Riley with a kairomone extracted from Heliothis zea (Boddie) moth scales. J Chem Ecol 7:635–648

    Article  CAS  PubMed  Google Scholar 

  • Bjorksten TA, Hoffmann AA (1998) Plant cues influence searching behaviour and parasitism in the egg parasitoid Trichogramma nr. brassicae. Ecol Entomol 23:355–362

    Article  Google Scholar 

  • Botto E, Glaz P (2010) Potential for controlling codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) in Argentina using the sterile insect technique and egg parasitoids. J Appl Entomol 134:251–260

    Article  Google Scholar 

  • Brodeur J, Boivin G (2004) Functional ecology of immature parasitoids. Annu Rev Entomol 49:27–49

    Article  CAS  PubMed  Google Scholar 

  • Cagnotti CL, Hernandez CM, Andormo AV, Viscarret M, Riquelme M, Botto EN, Lopez SN (2016) Acceptability and suitability of Tuta absoluta eggs from irradiated parents to parasitism by Trichogramma nerudai and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Agric For Entomol 18:198–205

    Article  Google Scholar 

  • Carpenter JE, Bloem S, Hofmeyr HJ (2004) Acceptability and suitability of eggs of false codling moth (Lepidoptera: Tortricidae) from irradiated parents to parasitism by Trichogrammatoidea cryptophlebiae (Hymenoptera: Trichogrammatidae). Biol Control 30:351–359

    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 

  • Cho WL, Tsao SM, Hays AR, Walter R, Chen JS, Snigirevskaya ES, Raikhel AS (1999) Mosquito cathepsin B-like protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. J Biol Chem 274:13311–13321

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Ramirez-Romero R (2009) Plant characteristics mediated by growing conditions can impact parasitoid’s ability to attack host aphids in winter canola. J Pest Sci 82:335–342

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

    Article  Google Scholar 

  • Fagotto F (1990) Yolk degradation in thick eggs: I. Occurrence of a Cathepsin L-like acid proteinase in yolk spheres. Arch Insect Biochem Physiol 14:217–235

    Article  CAS  PubMed  Google Scholar 

  • Fatouros NE, Huigens ME, van Loon JJA, Dicke M, Hilker M (2005) Chemical communication: butterfly anti-anphrodisiac lures parasitic wasps. Nature 433:704

    Article  CAS  PubMed  Google Scholar 

  • Fialho E, Silveira AB, Masuda H, Silva-Neto MAC (2002) Oocyte fertilization triggers acid phosphatase activity during Rhodnius prolixus embryogenesis. Insect Biochem Mol Biol 32:871–880

    Article  CAS  PubMed  Google Scholar 

  • Godfray HCJ (1994) Behavioral and evolutionary ecology. In: Krebs JR, Clutton-Brock T (eds) Parasitoids. Princeton University Press, Princeton

    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 Sci Technol 11:21–26

    Article  Google Scholar 

  • Häckermann J, Rott AS, Dorn S (2007) How two different host species influence the performance of a gregarious parasitoid: host size is not equal to host quality. J Anim Ecol 76:376–383

    Article  PubMed  Google Scholar 

  • Hintz JL, Andow DA (1990) Host age and host selection by Trichogramma nubilale. Entomophaga 35:141–150

    Article  Google Scholar 

  • Juliano SA (1982) Influence of host age on host acceptability and suitability for a species of Trichogrammatidae attacking aquatic Diptera. Can Entomol 114:713–720

    Article  Google Scholar 

  • Kazmer DJ, Luck RF (1995) Field-tests of the size-fitness hypothesis in the egg parasitoid Trichogramma pretiosum. Ecology 76:412–425

    Article  Google Scholar 

  • Klomp H, Teerink BJ (1962) Host selection and number of eggs per oviposition in the egg-parasite Trichogramma embryophagum Htg. Nature 4845:1020–1021

    Article  Google Scholar 

  • Krugner R (2014) Suitability of non-fertilized eggs of Homalodisca vitripennis for the egg parasitoid Gonatocerus morrilli. Biocontrol 59:167–174

    Article  Google Scholar 

  • Kumar Jalali SK, Venkatasan T, Stouthamer R, Niranjana P, Lalitha Y (2009) Internal transcribed spacer-2 restriction fragment length polymorphism (ITS-2-RFLP) tool to differentiate some exotic and indigenous trichogrammatid egg parasitoids in India. Biol Control 49:207–213

    Article  Google Scholar 

  • Laing J (1937) Host-finding by insect parasites I observations on the finding of hosts by Alysia manducator, Mormoniella vitripennis and Trichogramma evanescents. J Anim Ecol 6:298–317

    Article  Google Scholar 

  • Legault S, Hébert C, Berthiaume R, Brodeur J (2013) Effects of seasonal variation in host quality and availability on parasitism by the egg parasitoid Telenomus coloradensis. Entomol Exp Appl 148:142–151

    Article  Google Scholar 

  • Li LY (1994) Worldwide use of Trichogramma for biological control on different crops: a survey. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp 37–51

    Google Scholar 

  • Liu X, McCarron RC, Nordin JH (1996) A cysteine protease that process insect vitellin. Purification and partial characterization of the enzyme and the proenzyme. J Biol Chem 271:33344–33351

    Article  CAS  PubMed  Google Scholar 

  • Manoukis NC, Geib SM, Vargas RI (2014) Effect of host Bactrocera dorsalis sex on yield and quality of the parasitoid Fopius arisanus. Biocontrol 59:395–402

    Article  Google Scholar 

  • Mills NJ, Kuhlmann U (2004) Oviposition behavior of Trichogramma platneri Nagarkatti and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) in patches of single and clustered host eggs. Biol Control 30:42–51

    Article  Google Scholar 

  • Milonas PG (2005) Influence of initial egg density and host size on the development of the gregarious parasitoid Bracon hebetor on three different host species. Biocontrol 50:415–428

    Article  Google Scholar 

  • Nisani Z, Honda JY (2010) Does the polyphagous egg parasitoid Trichogramma platneri Nagarkatti (Hymenoptera: Trichogrammatidae) display behavioral plasticity when parasitizing different hosts? J Insect Behav 23:81–89

    Article  Google Scholar 

  • Noldus LPJJ, Potting RPJ, Barendregt HE (1991a) Moth sex-pheromone adsorption to leaf surface-bridge in time for chemical spies. Physiol Entomol 16:329–344

    Article  Google Scholar 

  • Noldus LPJJ, Van Lenteren JC, Lewis WJ (1991b) How Trichogramma parasitoids use moth sex pheromones as kairomones: orientation behaviour in a wind tunnel. Physiol Entomol 16:313–327

    Article  Google Scholar 

  • Pak GA (1986) Behavioural variations among strains of Trichogramma spp.: a review of the literature on host-age selection. J Appl Entomol 101:55–64

    Article  Google Scholar 

  • Pak GA, Oatman ER (1982) Biology of Trichogramma brevicapillum. Entomol Exp Appl 32:61–67

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

    Google Scholar 

  • Pizzol J, Desneux N, Wajnberg E, Denis 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 

  • Pompanon F, Michel Boulétreau M (1997) Effect of diapause and developmental host species on the circadian locomotor activity rhythm of Trichogramma brassicae females. Entomol Exp Appl 82:231–234

    Article  Google Scholar 

  • Renou M, Nagnan P, Berthier A, Durier C (1992) Identification of compounds from the eggs of Ostrinia nubilalis and Mamestra brassicae having kairomone activity on Trichogramma brassicae. Entomol Exp Appl 63:291–303

    Article  CAS  Google Scholar 

  • Reznik SY, Umarova TY (1990) The influence of host’s age on the selectivity of parasitism and fecundity of Trichogramma. Entomophaga 35:31–37

    Article  Google Scholar 

  • Ruan YM, Luan JB, Zang LS, Liu SS (2007) Observing and recording copulation events of whiteflies on plants using a video camera. Entomol Exp Appl 124:229–233

    Article  Google Scholar 

  • Saour G (2004) Parasitization of potato tuber moth eggs (Lep., Gelechiidae) from irradiated adults by Trichogramma (Hym., Trichogrammatidae) and control of moth population with combined releases of sterile insect and egg parasitoid. J Appl Entomol 128:681–686

    Article  Google Scholar 

  • Smith SM (1996) Biological control with Trichogramma: advances, success, 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  PubMed  Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172

    Article  Google Scholar 

  • Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and their impact on pest management. J Chem Ecol 36:80–100

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Yang X, Lin Y, Zang LS, Tian CY, Ruan CC (2016) Effect of fertilized, unfertilized, and UV-irradiated hosts on parasitism and suitability for Trichogramma parasitoids. Entomol Exp Appl 161:50–56

    Article  CAS  Google Scholar 

  • Yuan XH, Song LW, Zhang JJ, Zang LS, Zhu L, Ruan CC, Sun GZ (2012) Performance of four Chinese 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 

  • Zhang JJ, Du WM, Ruan CC, Zang LS, Sun GZ (2012) Effect of different artificial diets on growth, development and fecundity of Corcyra cephalonice. J Jilin Agric Univ 34:603–606

    Google Scholar 

  • Zhang JJ, Ren BZ, Yuan XH, Zang LS, Ruan CC, Sun GZ, Shao XW (2014) Effects of host-egg ages on host selection and suitability of four Chinese Trichogramma species, egg parasitoids of the rice striped stem borer, Chilo suppressalis. Biocontrol 59:159–166

    Article  CAS  Google Scholar 

  • Zhang JJ, Ruan CC, Zang LS, Shao XW, Shi SS (2015) Technological improvements for mass production of Trichogramma and current status of their applications for biological control on agricultural pests in China. Chin J Biol Control 31:638–646

    Google Scholar 

Download references

Acknowledgements

We thank Prof. Shoushan Huang for the Trichogramma species identification. This research was funded by the National Key R&D Program of China (SQ2017ZY060059), and the National Natural Science Foundation of China (31572058). The granting agencies had no role in study design, data collection and analysis, decision to publish, or manuscript preparation.

Author information

Authors and Affiliations

  1. Engineering Research Center of Biological Control, Institute of Biological Control, Jilin Agricultural University, Changchun, 130118, China

    Wen-Mei Du, Jing Xu, Yang-Yang Hou, Ying Lin, Lian-Sheng Zang, Jun-Jie Zhang & Chang-Chun Ruan

  2. University of California Davis, Salinas, CA, 93905, USA

    Xiangbing Yang

  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. Wen-Mei Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jing Xu
    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. Ying Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lian-Sheng Zang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiangbing Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jun-Jie Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chang-Chun Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nicolas Desneux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lian-Sheng Zang or Xiangbing Yang.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Communicated by M. Traugott.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Du, WM., Xu, J., Hou, YY. et al. Trichogramma parasitoids can distinguish between fertilized and unfertilized host eggs. J Pest Sci 91, 771–780 (2018). https://doi.org/10.1007/s10340-017-0919-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-017-0919-z

Keywords

Search

Navigation