, Volume 61, Issue 5, pp 485–496 | Cite as

Field evaluation of synthetic aphid sex pheromone in enhancing suppression of aphid abundance by their natural enemies

  • Yoshitaka NakashimaEmail author
  • Takashi Y. Ida
  • Wilf Powell
  • John A. Pickett
  • Michael A. Birkett
  • Hisatomo Taki
  • Junji Takabayashi


The effects of lures containing aphid sex pheromone components (4aS,7S,7aR)-nepetalactone and (1R,4aS,7S,7aR)-nepetalactol on abundance of pea aphid, Acyrthosiphon pisum Harris, aphid parasitoids, predators and hyperparasitoids in alfalfa fields were investigated over three years. Although aphid abundance was variable among years, pheromone lure treatment significantly decreased aphid abundance. Among natural enemies of the aphids, only parasitism by the aphid parasitoids Aphidius ervi Haliday and Praon barbatum Mackauer was affected by pheromone lure treatment, with parasitism rates being significantly increased. In contrast, no pheromone lure effects on abundance were detected for predacious species and hyperparasitoids. These results indicate that slow-release formulations of synthetic aphid sex pheromone can attract primary aphid parasitoids and enhance their ability to suppress aphid abundance in the field, and that negative effects on biological control by hyperparasitoids and intraguild predation are not promoted by pheromone lure treatment.


Aphid parasitoid Host location Parasitism Biological control Intraguild predation Hyperparasitism 



We would like to thank the laboratory students of Obihiro University of Agriculture and Veterinary Medicine for field survey assistance. We have also appreciated the support from the staff at the University farm. This study was partially founded by Grants-in-Aid for Regional R&D Proposal-Based Program from Northern Advancement Center for Science & Technology of Hokkaido, Japan. Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom.


  1. Birkett MA, Pickett JA (2003) Aphid sex pheromones: from discovery to commercial production. Phytochemistry 62:651–656CrossRefPubMedGoogle Scholar
  2. Brodeur J, Rosenheim JA (2000) Intraguild interactions in aphid parasitoids. Entomol Exp Appl 97:93–108CrossRefGoogle Scholar
  3. Buitenhuis R, Vet LEM, Boivin G, Brodeur J (2005) Foraging behaviour at the fourth trophic level: a comparative study of host location in aphid hyperparasitoids. Entomol Exp Appl 114:107–117CrossRefGoogle Scholar
  4. Cuperus GW, Radcliffe EB, Barnes DK, Marten GC (1982) Economic injury levels and economic thresholds for pea aphid, Acyrthosiphon pisum (Harris), on alfalfa. Crop Prot 1:453–463CrossRefGoogle Scholar
  5. Dawson GW, Griffiths DC, Merritt LA, Mudd A, Pickett JA, Wadhams LJ, Woodcock CM (1990) Aphid semiochemicals: a review, and recent advances on the sex pheromone. J Chem Ecol 16:3019–3030CrossRefPubMedGoogle Scholar
  6. Dean GJ, Jones MG, Powell W (1981) The relative abundance of the hymenopterous parasites attacking Metopolophium dirhodum (Walker) and Macrosiphum avenae (F.) (Hemiptera: Aphididae). Bull Entomol Res 71:307–315CrossRefGoogle Scholar
  7. Ekbom B (1994) Arthropod predators of the pea aphid, Acyrthosiphon pisum Harris. (Hom., Aphidae) in peas (Pisum sativum L.), clover (Trifolium pratense L.) and alfalfa (Medicago sativa L.). J Appl Entomol 117:469–476CrossRefGoogle Scholar
  8. Fernandez-Grandon GM, Woodcock CM, Poppy GM (2013) Do asexual morphs of the peach-potato aphid, Myzus persicae, utilise the aphid sex pheromone? Behavioural and electrophysiological responses of M. persicae virginoparae to (4aS,7S,7aR)-nepetalactone and its effect on aphid performance. Bull Entomol Res 103:466–472CrossRefPubMedGoogle Scholar
  9. Fitzmaurice GM, Laird NM, Ware JH (2004) Applied longitudinal analysis. Wiley-Interscience, HobokenGoogle Scholar
  10. Glinwood RT, Powell W, Tripathi CPM (1998) Increased prasitization of aphids on trap plants alongside vials releasing synthetic aphid sex pheromone and effective range of the pheromone. Biocontrol Sci Technol 8:607–614CrossRefGoogle Scholar
  11. Glinwood RT, Du YJ, Powell W (1999a) Responses to aphid sex pheromones by the pea aphid parasitoids Aphidius ervi and Aphidius eadyi. Entomol Exp Appl 92:227–232CrossRefGoogle Scholar
  12. Glinwood RT, Du YJ, Smiley DWM, Powell W (1999b) Comparative responses of parasitoids to synthetic and plant-extracted nepetalactone component of aphid sex pheromones. J Chem Ecol 25:1481–1488CrossRefGoogle Scholar
  13. Graves S (2003) The role of component ratio integrity in host plant selection: a chemical and biological approach. PhD Thesis, University College, London, UKGoogle Scholar
  14. Hardie J, Nottingham SF, Powell W, Wadhams LJ (1991) Synthetic aphid sex pheromone lures female parasitoids. Entomol Exp Appl 61:97–99CrossRefGoogle Scholar
  15. Hardie J, Hick AJ, Höller C, Mann J, Merritt L, Nottingham SF, Powell W, Wadhams LJ, Witthinrich J, Wright AF (1994) The responses of Praon spp. parasitoids to aphid sex-pheromone components in the field. Entomol Exp Appl 71:95–99CrossRefGoogle Scholar
  16. Hoelmer KA, Osborne LS, Yokomi RK (1994) Interactions of the whitefly predator Delphastus pusillus (Coleoptera: Coccinellidae) and parasitized sweet potato whitefly (Homoptera: Aleyrodidae). Environ Entomol 23:136–139CrossRefGoogle Scholar
  17. Hooper AM, Donato B, Woodcock CM, Park JH, Paul RL, Boo KS, Hardie J, Pickett JA (2002) Characterization of (1R,4S,4aR,7S,7aR)-dihydronepetalactol as a semiochemical for lacewings, including Chrysopa spp. and Peyerimhoffina gracilis. J Chem Ecol 28:849–864CrossRefPubMedGoogle Scholar
  18. Horn DJ (1989) Secondary parasitism and population dynamics of aphid parasitoids (Hymenoptera: Aphidiidae). J Kans Entomol Soc 62:203–210Google Scholar
  19. James D, Grasswitz TR (2005) Synthetic herbivore-induced plant volatiles increase field capture of parasitic wasps. BioControl 50:871–880CrossRefGoogle Scholar
  20. Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997CrossRefPubMedGoogle Scholar
  21. Koczor S, Szentkiralyi F, Birkett MA, Pickett JA, Voigt E, Toth M (2010) Attraction of Chrysoperla carnea complex and Chrysopa spp. lacewings (Neuroptera: Chrysopidae) to aphid sex pheromone components and a synthetic blend of floral compounds in Hungary. Pest Manag Sci 66:1374–1379CrossRefPubMedGoogle Scholar
  22. Lewis WJ, Martin WR (1990) Semiochemicals for use with parasitoids: status and future. J Chem Ecol 16:3067–3089CrossRefPubMedGoogle Scholar
  23. Lewis WJ, Jones RL, Sparks AN (1972) A host-seeking stimulant for the egg parasite Trichogramma evanescens: its source and a demonstration of its laboratory and field activity. Ann Entomol Soc Am 65:1087–1089CrossRefGoogle Scholar
  24. Mallinger RE, Hogg DB, Gratton C (2013) Methyl salicylate attracts natural enemies and reduces populations of soybean aphids (Hemiptera: Aphididae) in soybean agroecosystems. J Econ Entomol 104:115–124CrossRefGoogle Scholar
  25. McEwen PK, Jervis MA, Kidd NAC (1994) Use of a sprayed l-tryptophan solution to concentrate numbers of the green lacewing Chrysoperla carnea in olive tree canopy. Entomol Exp Appl 70:97–99CrossRefGoogle Scholar
  26. Milliken GA, Johnson DH (1984) Analysis of messy data, vol 1. van Nostrand Reinhold, New YorkGoogle Scholar
  27. Mizutani N, Wada T, Higuchi H, Ono M, Leal WS (1997) A component of a synthetic aggregation pheromone of Riptortus clavatus (Thuberg) (Heteroptera: Alydidae), that attracts an egg parasitoid, Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae). Appl Entomol Zool 32:504–507Google Scholar
  28. Nakashima Y, Akashi M (2005) Temporal and within-plant distribution of the parasitoid and predator complexes associated with Acyrthosiphon pisum and A. kondoi (Homoptera: Aphididae) on alfalfa in Japan. Appl Entomol Zool 40:137–144CrossRefGoogle Scholar
  29. Pickett JA, Allemann R, Birkett MA (2013) The semiochemistry of aphids. Nat Product Rep 30:1277–1283CrossRefGoogle Scholar
  30. Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE, Jongema Y, van Loon JJA, Vet LEM, Harvey JA, Dicke M (2012) Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biol 10:1–13CrossRefGoogle Scholar
  31. Polgár LA, Hardie J (2000) Diapause induction in aphid parasitoids. Entomol Exp Appl 97:21–27CrossRefGoogle Scholar
  32. Powell W (1986) Enhancing parasitoid activity in crops. In: Waage J, Greathead D (eds), Insect Parasitoids. 13th Symposium of the Royal Entomological Society of London, Academic, London, UK, 18–19 Sept pp 319–340Google Scholar
  33. Powell W, Pickett JA (2003) Manipulation of parasitoids for aphid pest management: progress and prospects. Pest Manag Sci 59:149–155CrossRefPubMedGoogle Scholar
  34. Powell W, Hardie J, Hick AJ, Höller C, Mann J, Merritt L, Nottingham SF, Wadhams LJ, Witthinrich J, Wright AF (1993) Responses of the parasitoid Praon volucre (Hymenoptera: Braconidae) to aphid sex pheromone lures in cereal fields in autumn: implications for parasitoid manipulation. Europ J Entomol 90:435–438Google Scholar
  35. Rosenheim JA (1998) Higher-order predators and regulation of insect herbivore populations. Ann Rev Entomol 43:421–447CrossRefGoogle Scholar
  36. SAS Institute (2013) SAS OnlineDoc 9.3. SAS Institute Inc, CaryGoogle Scholar
  37. Senoo N, Ochiai Y, Nakashima Y (2002) Seasonal abundance of primary parasitoids and hyperparasitoids associated with Acyrthosiphon pisum (Harris) and Acyrthosiphon kondoi Shinji (Homoptera: Aphididae) on Alfalfa. Jpn J Appl Entomol Zool 46:96–98CrossRefGoogle Scholar
  38. Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI, Orre-Gordon GUS (2011) Attract and reward: combining chemical ecology and habitat manipulation to enhance biological control in field crops. J Appl Ecol 48:580–890CrossRefGoogle Scholar
  39. Stroup WW (2013) Generalized linear mixed models: modern concepts, methods and applications. CRC Press, Boca RatonGoogle Scholar
  40. Sullivan DJ (1988) Hyperparasites. In: Minks AK, Harrewijn P (eds) World crop pests, 2B. Aphids, their natural enemies and control. Elsevier, Amsterdam, pp 189–204Google Scholar
  41. Sullivan DJ, van den Bosch R (1971) Field ecology of the primary parasites and hyperparasites of the potato aphid, Macrosiphum euphobiae, in the East San Francisco Bay area. Ann Entomol Soc Am 64:389–394CrossRefGoogle Scholar
  42. Sullivan DJ, Völkl W (1999) Hyperparasitism: mutitrophic ecology and behaviour. Annu Rev Entomol 44:291–315CrossRefPubMedGoogle Scholar
  43. Takada H (1968) Aphidiidae of Japan (Hymenoptera). Insecta Matsumurana 30:67–124Google Scholar
  44. Uefune M, Choh Y, Abe J, Shiojiri K, Sano K, Takabayashi J (2012) Application of synthetic herbivore-induced plant volatiles causes increased parasitism of herbivores in the field. J Appl Entomol 136:561–567CrossRefGoogle Scholar
  45. Vickerman GP, Wratten SD (1979) The biology and pest status of cereal aphids (Hemiptera: Aphididae) in Europe: a review. Bull Entomol Res 69:1–32CrossRefGoogle Scholar
  46. Wells ML, McPherson RM, Ruberson JR (2001) Predation of parasitized and unparasitized cotton aphids (Homoptera: Aphididae) by larvae of two coccinellids. J Entomol Sci 36:93–96Google Scholar
  47. Wheeler AG (1977) Studies on the arthropod fauna of alfalfa. VII. Predaceous insects. Can Entomol 109:423–427CrossRefGoogle Scholar
  48. Wheeler AG, Hayes JT, Stephens JL (1968) Insect predators of mummified pea aphids. Can Entomol 100:221–222CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2016

Authors and Affiliations

  • Yoshitaka Nakashima
    • 1
    Email author
  • Takashi Y. Ida
    • 1
  • Wilf Powell
    • 2
  • John A. Pickett
    • 2
  • Michael A. Birkett
    • 2
  • Hisatomo Taki
    • 3
  • Junji Takabayashi
    • 1
  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan
  2. 2.Rothamsted ResearchHarpendenUK
  3. 3.Department of Forest EntomologyForestry and Forest Products Research InstituteTsukubaJapan

Personalised recommendations