Skip to main content
SpringerLink
Log in

Effects of insecticides on sex pheromone communication and mating behavior in Trichogramma chilonis

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

Abstract

Trichogramma chilonis Ishii is an important natural enemy of several lepidopterous pests on crops. The effects of two common insecticides on sex pheromone communication and mating behavior in T. chilonis were evaluated in the laboratory. When only males were exposed to insecticide, beta-cypermethrin LC20 exposure induced significant decrease in sex pheromone perception by males and significant increase in males’ courtship and copulation frequency; beta-cypermethrin LC1 exposure caused significant decrease in males’ courtship and copulation frequency. Males exposed to spinosad LC20 exhibited significantly slower initiated courtship and significantly shorter total copulation duration, and the males exposed to spinosad LC1 exhibited significantly increased sex pheromone perception, compared with control. When both males and females were exposed to insecticide, significantly more courtship and copulation were conducted by treated pairs that survived insecticide (beta-cypermethrin or spinosad) LC20 than control pairs. Our study suggests that even the LC1 and LC20 of tested insecticides could affect the sex pheromone communication and mating behavior in T. chilonis.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abbes K, Biondi A, Kurtulus A, Ricupero M, Russo A, Siscaro G, Chermiti B, Zappalà L (2015) Combined non-target effects of insecticide and high temperature on the parasitoid Bracon nigricans. PLoS ONE 10:e0138411

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderbrant O, Hansson BS, Hallberg E, Geri C, Varama M, Hedenström E, Högberg HE, Fägerhag J, Edlund H, Wassgren AB, Bergström G, Löfqvist J (1995) Electrophysiological and morphological characteristics of pheromone receptors in male pine sawflies, Diprion pini (Hymenoptera: Diprionidae), and behavioural response to some compounds. J Insect Physiol 41:395–401

    Article  CAS  Google Scholar 

  • Andrade GS, Pratissoli D, Dalvi LP, Desneux N, dos Santos Junior HJG (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 

  • Ballal CR, Srinivasan R, Jalali SK (2009) Evaluation of an endosulfan tolerant strain of Trichogramma chilonis on cotton. BioControl 54:723–732

    Article  CAS  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012a) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalà L, Desneux N (2012b) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8:e76548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biondi A, Campolo O, Desneux N, Siscaro G, Palmeri V, Zappalà L (2015) Life stage-dependent susceptibility of Aphytis melinus DeBach (Hymenoptera: Aphelinidae) to two pesticides commonly used in citrus orchards. Chemosphere 128:142–147

    Article  CAS  PubMed  Google Scholar 

  • Bourdais D, Vernon P, Krespi L, van Baaren J (2012) Behavioural consequences of cold exposure on males and females of Aphidius rhopalosiphi De Stephani Perez (Hymenoptera: Braconidae). BioControl 57:349–360

    Article  Google Scholar 

  • Brown RA (1989) Pesticides and non-target terrestrial invertebrates: an industrial approach. In: Jepson PC (ed) Pesticides and non-target invertebrates. Intercept Ltd, Wimborne, pp 19–42

    Google Scholar 

  • Chailleux A, Desneux N, Seguret J, Do Thi Khanh H, Maignet P, 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, Biondi A, Han P, Tabone E, Desneux N (2013) 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 

  • Chang SC, Hu NT, Hsin CY, Sun CN (2001) Characterization of differences between two Trichogramma wasps by molecular markers. Biol Control 21:75–78

    Article  CAS  Google Scholar 

  • Delpuech JM, Froment B, Fouillet P, Pompanon F, Janillon S, Bouletreau M (1998a) Inhibition of sex pheromone communications of Trichogramma brassicae (Hymenoptera) by the insecticide chlorpyrifos. Environ Toxicol Chem 17:1107–1113

    Article  CAS  Google Scholar 

  • Delpuech JM, Gareau E, Terrier O, Fouillet P (1998b) Sublethal effects of the insecticide chlorpyrifos on the sex pheromonal communication of Trichogramma brassicae. Chemosphere 36:1775–1785

    Article  CAS  Google Scholar 

  • Delpuech JM, Legallet B, Terrier O, Fouillet P (1999) Modifications of the sex pheromonal communication of Trichogramma brassicae by a sublethal dose of deltamethrin. Chemosphere 38:729–739

    Article  CAS  PubMed  Google Scholar 

  • Delpuech JM, Legallet B, Fouillet P (2001) Partial compensation of the sublethal effect of deltamethrin on the sex pheromonal communication of Trichogramma brassicae. Chemosphere 42:985–991

    Article  CAS  PubMed  Google Scholar 

  • Delpuech JM, Dupont C, Allemand R (2012) Effects of deltamethrin on the specific discrimination of sex pheromones in two sympatric Trichogramma species. Ecotox Environ Safe 84:32–38

    Article  CAS  Google Scholar 

  • Desneux N, Pham-Delègue MH, Kaiser L (2004) Effects of sub-lethal and lethal doses of lambda-cyhalothrin on oviposition experience and host-searching behaviour of a parasitic wasp, Aphidius ervi. Pest Manag Sci 60:381–389

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Fauvergue X, Dechaume-Moncharmont FX, Kerhoas L, Ballanger Y, Kaiser L (2005) Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J Econ Entomol 98:9–17

    Article  PubMed  Google Scholar 

  • Desneux N, Denoyelle R, Kaiser L (2006a) A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere 65:1697–1706

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Ramirez-Romero R, Kaiser L (2006b) Multistep bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment. Environ Toxicol Chem 25:2675–2682

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  PubMed  Google Scholar 

  • Doyon J, Boivin G (2006) Impact of the timing of male emergence on mating capacity of males in Trichogramma evanescens Westwood. BioControl 51:703–713

    Article  Google Scholar 

  • Dupont C, Allemand R, Delpuech JM (2010) Induction by chlorpyrifos, of the confusion of males in discriminating female sexual pheromones used for mate finding by two sympatric Trichogramma species (Hymenoptera: Trichogrammatidae). Environ Entomol 39:535–544

    Article  CAS  PubMed  Google Scholar 

  • Fan XJ, Li Y, Li Y, Li LS, Zhang CF (2010) Research progress of insect sex pheromone. J Anhui Agric Sci 38:4636–4638

    CAS  Google Scholar 

  • Finney DJ (1971) Probit analysis. Cambridge University, Cambridge

    Google Scholar 

  • Gu D, Wright DJ, Waage JK (1995) Effects of sublethal doses of insecticides on the mating behaviour of male parasitoid, Diadegma eucerophaga. J South China Agric Univ 16:55–59

    Google Scholar 

  • Gu XZ, Zhang GY, Chen L, Dai RL, Yu YC (2008) Persistence and dissipation of synthetic pyrethroid pesticides in red soils from the Yangtze River Delta area. Environ Geochem Health 30:67–77

    Article  CAS  PubMed  Google Scholar 

  • Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62

    Article  CAS  PubMed  Google Scholar 

  • Hansson BS (1995) Olfaction in lepidoptera. Experientia 51:1003–1027

    Article  CAS  Google Scholar 

  • Hansson BS, Almaas TJ, Anton S (1995) Chemical communication in heliothine moths V. Antennal lobe projection patterns of pheromone-detecting olfactory receptor neurons in the male Heliothis virescens (Lepidoptera: noctuidae). J Comp Physiol A 177:535–543

    Article  CAS  Google Scholar 

  • Hardy ICW (1994) Sex ratio and mating structure in the parasitoid Hymenoptera. Oikos 69:3–20

    Article  Google Scholar 

  • He Y, Pang X (2000) Species and parasitism of Trichogramma on the diamond back moth, Plutella xylostella in Shenzhen, China. Nat Enemies Insects 22:1–5

    CAS  Google Scholar 

  • He Y, Lü L, Pang X (2001) Selection of effective species of Trichogramma egg parasitoids of diamondback moth: I. Laboratory evaluation on the parasitizating capacity of several Trichogramma and Trichogrammatoidea species. Chin J Biol Control 17:6–9

    Google Scholar 

  • He Y, Chen K, Pang X (2002) Egg parasitoids of Plutella xylostella (L.) in South China. In: Kirk AA, Bordat D (eds) Improving biocontrol of Plutella xylostella: proceedings of the international symposium. CIRAD, Montpellier, pp 267–273

  • Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53:209–230

    Article  CAS  PubMed  Google Scholar 

  • Huang KC, Zeng XN, Li ZY (2010) Insecticides-induced hormesis on insects. Asian J Ecotoxicol 5:26–31

    Google Scholar 

  • Hussain D, Ali H, Qasim M, Khan J (2015) Insecticidal susceptibility and effectiveness of Trichogramma chilonis as parasitoids of tomato fruit borer, Helicoverpa armigera. Pak J Zool 47:1427–1432

    CAS  Google Scholar 

  • Jacob S, Boivin G (2004) Insemination potential of male Trichogramma evanescens. Entomol Exp Appl 113:181–186

    Article  Google Scholar 

  • Jin T, Zeng L, Lin Y, Lu Y, Liang G (2011) Insecticide resistance of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in mainland China. Pest Manag Sci 67:370–376

    Article  CAS  PubMed  Google Scholar 

  • Jin T, Lin YY, Jin QA, Wen HB, Peng ZQ (2015) Population susceptibility to insecticides and the development of resistance in Bactrocera cucurbitae (Diptera: Tephritidae). J Econ Entomol 109:837–846

    Article  Google Scholar 

  • King BH, Saporito KB, Ellison JH, Bratzke RM (2005) Unattractiveness of mated females to males in the parasitoid wasp Spalangia endius. Behav Ecol Sociobiol 57:350–356

    Article  Google Scholar 

  • Ko K, Liu YD, Hou ML, Babendreier D, Zhang F, Song K (2015) Toxicity of insecticides targeting rice planthoppers to adult and immature stages of Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Econ Entomol 108:69–76

    Article  PubMed  Google Scholar 

  • Liang P, Tian YA, Biondi A, Desneux N, Gao XW (2012) Short-term and transgenerational effects of the neonicotinoid nitenpyram on susceptibility to insecticides in two whitefly species. Ecotoxicology 21:1889–1898

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365

    Article  CAS  PubMed  Google Scholar 

  • Lund HO (1938) Studies on longevity and productivity in Trichogramma evanescens. J Agric Res 56:421–439

    Google Scholar 

  • Martel V, Doyon J, Boivin G (2010) Partial local mate competition in the wasp Trichogramma euproctidis: the role of emergence sex ratio on female mating behaviour. Ecol Entomol 35:698–703

    Article  Google Scholar 

  • McClure M, Whistlecraft J, McNeil JN (2007) Courtship behavior in relation to the female sex pheromone in the parasitoid, Aphidius ervi (Hymenoptera: Braconidae). J Chem Ecol 33:1946–1959

    Article  CAS  PubMed  Google Scholar 

  • Michalko R, Košulič O (2015) Temperature-dependent effect of two neurotoxic insecticides on predatory potential of Philodromus spiders. J Pest Sci 89:517–527

    Article  Google Scholar 

  • Monti L, Lalanne-Cassou B, Lucas P, Malosse C, Silvain JF (1995) Differences in sex pheromone communication systems of closely related species: Spodoptera latifascia (Walker) and S. descoinsi Lalanne-Cassou and Silvain (Lepidoptera: Noctuidae). J Chem Ecol 21:641–660

    Article  CAS  PubMed  Google Scholar 

  • Pasquet A, Tupinier N, Mazzia C, Capowiez Y (2016) Exposure to spinosad affects orb-web spider (Agalenatea redii) survival, web construction and prey capture under laboratory conditions. J Pest Sci 89:507–515

    Article  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 

  • Pompanon F, Fouillet P, Boulétreau M (1995) Emergence rhythms and protandry in relation to daily patterns of locomotor activity in Trichogramma species. Evol Ecol 9:467–477

    Article  Google Scholar 

  • Prasifka JR, Lopez MD, Hellmich RL, Prasifka PL (2008) Effects of insecticide exposure on movement and population size estimates of predatory ground beetles (Coleoptera: Carabidae). Pest Manag Sci 64:30–36

    Article  CAS  PubMed  Google Scholar 

  • Preetha G, Stanley J, Suresh S, Kuttalam S, Samiyappan R (2009) Toxicity of selected insecticides to Trichogramma chilonis: assessing their safety in the rice ecosystem. Phytoparasitica 37:209–215

    Article  CAS  Google Scholar 

  • Sántis EL, Hernández LA, Martínez AM, Campos J, Figueroa JI, Lobit P, Chavarrieta JM, Viñuela E, Smagghe G, Pineda S (2012) Long-term foliar persistence and efficacy of spinosad against beet armyworm under greenhouse conditions. Pest Manag Sci 68:914–921

    Article  PubMed  Google Scholar 

  • Shan C, Ma S, Wang M, Gao G (2012) Evaluation of insecticides against the western flower thrips, Frankliniella occidentals (Thysanoptera: Thripidae), in the laboratory. Fla Entomol 95:454–460

    Article  CAS  Google Scholar 

  • Sharma A, Srivastava A, Ram B, Srivastava PC (2007) Dissipation behaviour of spinosad insecticide in soil, cabbage and cauliflower under subtropical conditions. Pest Manag Sci 63:1141–1145

    Article  CAS  PubMed  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 

  • Sparks TC, Crouse GD, Durst G (2001) Natural products as insecticides: the biology, biochemistry and quantitative structure-activity relationships of spinosyns and spinosoids. Pest Manag Sci 57:896–905

    Article  CAS  PubMed  Google Scholar 

  • Tabarean IV, Narahashi T (2001) Kinetics of modulation of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels by tetramethrin and deltamethrin. J Pharmacol Exp Ther 299:988–997

    CAS  PubMed  Google Scholar 

  • Tabone E, Bardon C, Desneux N, Wajnberg E (2010) Parasitism of different Trichogramma species and strains on Plutella xylostella L. on greenhouse cauliflower. J Pest Sci 83:251–256

    Article  Google Scholar 

  • Wang DS, Pan F, He YR, Guo XL, Chen Q (2011) Sublethal effects of eleven insecticides of different categories on reproduction of Trichogrammatoidea bactrae Nagaraja (Hymenoptera: Trichogrammatidae). Acta Entomol Sin 54:56–63

    Google Scholar 

  • Wang DS, He YR, Guo XL, Luo YL (2012) Acute toxicities and sublethal effects of some conventional insecticides on Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Econ Entomol 105:1157–1163

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wu C, Cang T, Yang L, Yu W, Zhao X, Wang Q, Cai L (2014) Toxicity risk of insecticides to the insect egg parasitoid Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). Pest Manag Sci 70:398–404

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Lü L, He Y, Shi Q, Tu C, Gu J (2016a) Mate choice and host discrimination behavior of the parasitoid Trichogramma chilonis. Bull Entomol Res 106:530–537

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Lü L, He Y, Shi Q, Wang G (2016b) Effects of insecticides on oviposition and host discrimination behavior in Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Econ Entomol 109:2380–2387

    Article  PubMed  Google Scholar 

  • Wang D, Lü L, He Y (2017) Effects of two conventional insecticides on male-specific sex pheromone discrimination and mate choice in Trichogramma chilonis (Hymenoptera: Trichogrammatidae). Environ Entomol. doi:10.1093/ee/nvw172

    Google Scholar 

  • Williams T, Valle J, Vinuela E (2003) Is the naturally derived insecticide Spinosad (R) compatible with insect natural enemies? Biocontrol Sci Technol 13:459–475

    Article  Google Scholar 

  • Xia Y, Lu Y, Shen J, Gao X, Qiu H, Li J (2014) Resistance monitoring for eight insecticides in Plutella xylostella in central China. Crop Prot 63:131–137

    Article  CAS  Google Scholar 

  • Xiao D, Zhao J, Guo X, Chen H, Qu M, Zhai W, Desneux N, Biondi A, Zhang F, Wang S (2016) Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata. Ecotoxicology 25:1782–1793

    Article  CAS  PubMed  Google Scholar 

  • Zheng X, Ren X, Su J (2011) Insecticide susceptibility of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) in China. J Econ Entomol 104:653–658

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by National Basic Research Program of China (973 project, 2013CB127604), Special Fund for Agro-scientific Research in the Public Interest of China (No. 201103021) and State Scholarship Fund of China.

Author information

Authors and Affiliations

  1. Key Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Agriculture, South China Agricultural University, Guangzhou, 510642, Guangdong Province, China

    Desen Wang & Yurong He

  2. Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, Guangdong Province, China

    Lihua Lü

Authors
  1. Desen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lihua Lü
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yurong He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yurong He.

Additional information

Communicated by N. Desneux.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (MP4 12254 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, D., Lü, L. & He, Y. Effects of insecticides on sex pheromone communication and mating behavior in Trichogramma chilonis . J Pest Sci 91, 65–78 (2018). https://doi.org/10.1007/s10340-017-0864-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-017-0864-x

Keywords

Search

Navigation