Skip to main content
Log in

A push–pull strategy to control aphids combines intercropping with semiochemical releases

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

A Correction to this article was published on 20 October 2017

This article has been updated

Abstract

Even if insect pest populations can be reduced by increasing plant diversity through intercropping, natural enemies are not always favored in such systems. Alternatively, semiochemical substances have been tested to enhance biological control, with inconsistent results. Combining both strategies can be an interesting way to maximize pest control. In this work, a 2-year setup involving wheat–pea strip intercropping combined with the release of E-β-farnesene (EBF) or methyl salicylate (MeSA) was tested as a push–pull strategy to simultaneously repel aphids and attract beneficials. Two types of slow-release formulation (i.e., oil and alginate beads) containing EBF or MeSA were deployed with the intercropping. The abundance of aphids was significantly decreased, while hoverfly larvae and mummified aphids increased on both pea plants and wheat tillers by the release of oil-formulated EBF and MeSA. The proportion parasitism of the aphid-parasitism rate [mummies/(aphids + mummies)] was also increased by treating both crops in both years. Releasing EBF through oil rather than alginate beads proved significantly better for attracting natural enemies and reducing aphids. Aphids were negatively correlated with the density of hoverflies (both adults and larvae) and numbers of mummies. All these results showed that combining intercropping with the release of EBF or MeSA formulated in oil can significantly reduce aphid density and attract their natural enemies. Therefore, the combination of both strategies could help farmers reduce the use of insecticides.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Change history

  • 20 October 2017

    The author name was published wrongly in the original publication of the article. The correct author name is “Qingxuan Xu”. The author apologized for this error.

References

  • Alhmedi A, Haubruge E, Bodson B et al (2007) Aphidophagous guilds on nettle (Urtica dioica) strips close to fields of green pea, rape and wheat. Insect Sci 14:419–424

    Article  Google Scholar 

  • Alhmedi A, Haubruge E, Francis F (2009) Effect of stinging nettle habitats on aphidophagous predators and parasitoids in wheat and green pea fields with special attention to the invader Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Entomol Sci 12:349–358

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B et al (2014) Lme4: Linear mixed-effects models using Eigen and S4. R package version

  • Beale MH, Birkett MA, Bruce TJA et al (2006) Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc Natl Acad Sci USA 103:10509–10513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bedoussac L, Justes E (2010) The efficiency of a durum wheat-winter pea intercrop to improve yield and wheat grain protein concentration depends on N availability during early growth. Plant Soil 330:19–35

    Article  CAS  Google Scholar 

  • Bedoussac L, Journet EP, Hauggaard-Nielsen H et al (2015) Ecological principles underlying the increase of productivity achieved by cereal-grain legume intercrops in organic farming. A review. Agron Sustain Dev 35:911–935

    Article  Google Scholar 

  • Blackman R, Eastop V (2008) Aphids on the world’s herbaceous plants and shrubs, vol 2 Set. Wiley, Hoboken

    Google Scholar 

  • Boo KS, Chung IB, Han KS et al (1998) Response of the lacewing Chrysopa cognata to pheromones of its aphid prey. J Chem Ecol 24:631–643

    Article  CAS  Google Scholar 

  • Brewer MJ, Goodell PB (2012) Approaches and incentives to implement integrated pest management that addresses regional and environmental issues. Annu Rev Entomol 57:41–59

    Article  CAS  PubMed  Google Scholar 

  • Cui LL, Francis F, Heuskin S et al (2012) The functional significance of E-β-Farnesene: does it influence the populations of aphid natural enemies in the fields? Biol Control 60:108–112

    Article  CAS  Google Scholar 

  • Daems F, Béra F, Lorge S et al (2016) Impact of climatic factors on the release of E-β-caryophyllene from alginate beads. Biotechnol Agron Soc Env 20:130–142

    Google Scholar 

  • Dahlin I, Vucetic A, Ninkovic V (2015) Changed host plant volatile emissions induced by chemical interaction between unattacked plants reduce aphid plant acceptance with intermorph variation. J Pest Sci 88:249–257

    Article  Google Scholar 

  • Du Y, Poppy GM, Powell W et al (1998) Identification of senmiochemical released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355–1368

    Article  CAS  Google Scholar 

  • Foster SP, Denholm I, Thompson R et al (2005) Reduced response of insecticide-resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade-off. Bull Entomol Res 95:37–46

    Article  CAS  PubMed  Google Scholar 

  • Francis F, Lognay G, Haubruge E (2004) Olfactory responses to aphid and host plant volatile releases: (E)-β-farnesene an effective kairomone for the predator Adalia bipunctata. J Chem Ecol 30:741–755

    Article  CAS  PubMed  Google Scholar 

  • Francis F, Martini T, Lognay G, Haubruge E (2005) Role of (E)-β-farnesene in systematic aphid prey location by Episyrphus balteatus larvae (Diptera: Syrphidae). Eur J Entomol 102:431–436

    Article  CAS  Google Scholar 

  • Glinwood RT, Pettersson J (2000) Change in response of Rhopalosiphum padi spring migrants to the repellent winter host component methyl salicylate. Entomol Exp Appl 94:325–330

    Article  CAS  Google Scholar 

  • Gonzales WL, Fuentes-Contreras E, Niemeyer HM (1999) Semiochemicals associated to spacing behaviour of the bird cherry-oat aphid Rhopalosiphum padi L. (Hem., Aphididae) do not affect the olfactometric behaviour of the cereal aphid parasitoid Aphidius rhopalosiphi De Stephani-Pérez (Hym., Braconidae). J Appl Ent 123:413–415

    Article  CAS  Google Scholar 

  • Gordon GUS, Wratten SD, Jonsson M et al (2013) “Attract and reward”: combining a herbivore-induced plant volatile with floral resource supplementation–Multi-trophic level effects. Biol Control 64:106–115

    Article  Google Scholar 

  • Hassanali A, Herren H, Khan ZR et al (2008) Integrated pest management: the push-pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philos Trans R Soc Lond B 363:611–621

    Article  Google Scholar 

  • Hatano E, Kunert G, Weisser WW (2010) Aphid wing induction and ecological costs of alarm pheromone emission under field conditions. PLoS ONE 5:e11188

    Article  PubMed  PubMed Central  Google Scholar 

  • Hatt S, Lopes T, Boeraeve F et al (2017) Pest regulation and support of natural enemies in agriculture: experimental evidence of within field wildflower strips. Ecol Eng 98:240–245

    Article  Google Scholar 

  • Hauggaard-Nielsen H, Jørnsgaard B, Kinane J et al (2008) Grain legume-cereal intercropping: the practical application of diversity, competition and facilitation in arable and organic cropping systems. Renew Agric Food Syst 23:3–12

    Article  Google Scholar 

  • Heuskin S, Lorge S, Lognay G et al (2012a) A semiochemical slow-release formulation in a biological control approach to attract hoverflies. J Environ Ecol 3:72–85

    Google Scholar 

  • Heuskin S, Lorge S, Godin B et al (2012b) Optimisation of a semiochemical slow-release alginate formulation attractive towards Aphidius ervi Haliday parasitoids. Pest Manag Sci 68:127–136

    Article  CAS  PubMed  Google Scholar 

  • Hokkanen H (2015) Integrated pest management at the crossroads: science, politics, or business (as usual)? Arthropod Plant Interact 9:543–545

    Article  Google Scholar 

  • James DG (2003a) Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing Chrysopa nigricornis. J Chem Ecol 29:1601–1609

    Article  CAS  PubMed  Google Scholar 

  • James DG (2003b) Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ Entomol 32:977–982

    Article  CAS  Google Scholar 

  • James DG (2006) Methyl salicylate is a field attractant for the goldeneyed lacewing, Chrysopa oculata. Biocontrol Sci Technol 16:107–110

    Article  Google Scholar 

  • Knops J, Tilman D, Naeem S et al (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol Lett 2:285–293

    Article  Google Scholar 

  • Kunert G, Otto S, Rose USR et al (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids Grit Kunert. Ecol Lett 8:596–603

    Article  Google Scholar 

  • Lenteren JC, Woets J (1988) Biological and integrated pest control in greenhouse. Annu Rev Entomol 33:239–269

    Article  Google Scholar 

  • Leroy PD, Schillings T, Farmakidis J et al (2012) Testing semiochemicals from aphid, plant and conspecific: attraction of Harmonia axyridis. Insect Sci 19:372–382

    Article  CAS  Google Scholar 

  • Letourneau D, Armbrecht I, Rivera B et al (2011) Does plant diversity benefit agroecosystems? Ecol Appl 21:9–21

    Article  PubMed  Google Scholar 

  • Lithourgidis A, Dordas C, Damalas C et al (2011) Annual intercrops: an alternative pathway for sustainable agriculture. Aust J Crop Sci 5:396–410

    Google Scholar 

  • Lopes L, Bodson B, Francis F (2015) Associations of wheat with pea can reduce aphid infestations. Neotrop Entomol 44:286–293

    Article  CAS  PubMed  Google Scholar 

  • Lopes T, Hatt S, Xu Q et al (2016) Wheat (Triticum aestivum L.)-based intercropping systems for biological pest control: a review. Pest Manag Sci 72:2193–2202

    Article  CAS  PubMed  Google Scholar 

  • Malakar J, Nayak AK, Pal D et al (2013) Potato starch-blended alginate beads for prolonged release of tolbutamide: development by statistical optimization and in vitro characterization. Asian J Pharm 7:43–51

    Article  Google Scholar 

  • Malézieux E, Crozat Y, Dupraz C et al (2009) Mixing plant species in cropping systems: Concepts, tools and models: a review. Springer, Dordrecht

    Book  Google Scholar 

  • Mallinger RE, Hogg DB, Gratton C (2011) Methyl salicylate attracts natural enemies and reduces populations of soybean aphids (Hemiptera: Aphididae) in soybean agroecosystems. J Econ Entomol 104:115–124

    Article  PubMed  Google Scholar 

  • Martini X, Pelz-Stelinski K, Stelinski L (2014) Plantpathogen-induced volatiles attract parasitoids to increase parasitism of an insectvector. Ecol Evol 2:1–8

    Google Scholar 

  • Mensah R, Moore C, Watts N et al (2014) Discovery and development of a new semiochemical biopesticide for cotton pest management: assessment of extract effects on the cotton pest Helicoverpa spp. Entomol Exp Appl 152:1–15

    Article  Google Scholar 

  • Ndzana RA, Magro A, Bedoussac L et al (2014) Is there an associational resistance of winter pea-durum wheat intercrops towards Acyrthosiphon pisum Harris? J Appl Entomol 138:577–585

    Article  Google Scholar 

  • Ninkovic V, Ahmed E, Glinwood R et al (2003) Effects of two types of semiochemical on population development of the bird cherry oat aphid Rhopalosiphum padi in a barley crop. Agric For Entomol 5:27–34

    Article  Google Scholar 

  • Poggio SL (2005) Structure of weed communities occurring in monoculture and intercropping of field pea and barley. Agric Ecosyst Environ 109:48–58

    Article  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. Vienna

  • Rodríguez LC, Niemeyer HM (2005) Integrated pest management, semiochemicals and microbial pest-controlagents in Latin American agriculture. Crop Prot 24:615–623

    Article  Google Scholar 

  • Rodriguez-Saona C, Kaplan I, Braasch J et al (2011) Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biol Control 59:294–303

    Article  CAS  Google Scholar 

  • Root R (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica Oleracea). Ecol Monogr 43:95–120

    Article  Google Scholar 

  • Roy HE, Brown PMJ, Comont RF (2013) Ladybirds, naturalists’handbook 10. Pelagic, Exeter

    Google Scholar 

  • San Martin G (2004) Clé de détermination des Chrysopidae de Belgique. Jeunes & Nature, Wavre

  • Sarles L, Verhaeghe A, Francis F et al (2015) Semiochemicals of Rhagoletis fruit flies: potential for integrated pest management. Crop Prot 78:114–118

    Article  CAS  Google Scholar 

  • Seidenglanz M, Hunady I, Poslusna J et al (2011) Influence of intercropping with spring Cereals on the occurrence of pea aphids (Acyrthosiphon pisum Harris, 1776) and their natural enemies in field pea (Pisum sativum L.). Plant Prot Sci 47:25–36

    Google Scholar 

  • Taylor L (1981) Aphid forecasting and pathogens & a handbook for aphid identification. Rothamsted Experimental Station, Harpenden

    Google Scholar 

  • Thieme T, Dixon AFG (2015) Is the response of aphids to alarm pheromone stable? J Appl Entomol 139:741–746

    Article  CAS  Google Scholar 

  • Veen VM (2010) Hoverflies of northwest Europe: identification keys to the syrphidae (Hardback). KNNV, Utrecht

    Google Scholar 

  • Verheggen FJ, Fagel Q, Heuskin S et al (2007) Electrophysiological and behavioral responses of the multicolored Asian ladybeetle, Harmonia axyridis Pallas, to sesquiterpene semiochemicals. J Chem Ecol 33:2148–2155

    Article  CAS  PubMed  Google Scholar 

  • Verheggen FJ, Mescher MC, Haubruge E et al (2008a) Emission of alarm pheromone in aphids: a non-contagious phenomenon. J Chem Ecol 34:1146–1148

    Article  CAS  PubMed  Google Scholar 

  • Verheggen FJ, Arnaud L, Bartram S et al (2008b) Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly. J Chem Ecol 34:301–307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang G, Cui LL, Dong J et al (2011) Combining intercropping with semiochemical releases: optimization of alternative control of Sitobion avenae in wheat crops in China. Entomol Exp Appl 140:189–195

    Article  Google Scholar 

  • Yosha I, Shani A, Magdassi S (2008) Slow release of pheromones to the atmosphere from gelatin-alginate beads. J Agric Food Chem 56:8045–8049

    Article  CAS  PubMed  Google Scholar 

  • Zappalà L, Biondi A, Alma A (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and middle east, and their potential use in pest control strategies. J Pest Sci 86:635–647

    Article  Google Scholar 

  • Zhou H, Chen J, Cheng DF et al (2009) Effects of wheat–pea intercropping on the population dynamics of Sitobion avenae (Homoptera: Aphididae) and its main natural enemies. Acta Entomol Sin 52:775–782

    Google Scholar 

  • Zhou H, Chen L, Liu Y et al (2016) Use of slow-release plant infochemicals to control aphids: a first investigation in a Belgian wheat field. Sci Rep 6:1–8

    Article  Google Scholar 

  • Zhu J, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator. J Chem Ecol 31:1733–1745

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the technical support provided by the Experimental Farm of Gembloux Agro-Bio Tech (University of Liège) for the installation and management of experimental fields, and Sidonie Artru for providing the data about the weather conditions. The research was funded by the CARE Agriculture Is Life (University of Liège). Qinxuan Xu was supported by National Key R & D Plan in China (2016YFD0300701), Cooperation Project between Belgium and China from MOST (2014DF32270), Séverin Hatt by CARE Agriculture Is Life (University of Liège), and Thomas Lopes by a PhD scholarship from FRIA (Fonds pour la Recherche en Industrie et Agronomie).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Julian Chen or Frédéric Francis.

Additional information

Communicated by I. Hiltpold.

A correction to this article is available online at https://doi.org/10.1007/s10340-017-0922-4.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Q., Hatt, S., Lopes, T. et al. A push–pull strategy to control aphids combines intercropping with semiochemical releases. J Pest Sci 91, 93–103 (2018). https://doi.org/10.1007/s10340-017-0888-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-017-0888-2

Keywords

Navigation