Journal of Chemical Ecology

, Volume 42, Issue 4, pp 305–313 | Cite as

Influence of Two Acyclic Homoterpenes (Tetranorterpenes) on the Foraging Behavior of Anthonomus grandis Boh

  • D. M. Magalhães
  • M. Borges
  • R. A. Laumann
  • C. M. Woodcock
  • J. A. Pickett
  • M. A. Birkett
  • Maria Carolina Blassioli-Moraes


Previous studies have shown that the boll weevil, Anthonomus grandis, is attracted to constitutive and conspecific herbivore-induced cotton volatiles, preferring the blend emitted by cotton at the reproductive over the vegetative stage. Moreover, this preference was paralleled by the release of the acyclic homoterpenes (tetranorterpenes) (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT) in Delta Opal cotton being higher at the vegetative than at the reproductive stage. Here, we evaluated whether this difference in release of acyclic homoterpenes also occurred in other cotton varieties, and if boll weevils could recognize these compounds as indicators of a specific cotton phenological stage. Results showed that cotton genotypes CNPA TB-90, BRS-293 and Delta Opal all produced higher levels of DMNT and TMTT at the vegetative stage than at the reproductive stage and that these homoterpenes allowed for principal component analysis separation of volatiles produced by the two phenological stages. Electroantennograms confirmed boll weevil antennal responses to DMNT and TMTT. Behavioral assays, using Y-tube olfactometers, showed that adding synthetic homoterpenes to reproductive cotton volatiles (mimicking cotton at the vegetative stage in terms of homoterpene levels) resulted in reduced attraction to boll weevils compared to that to unmodified reproductive cotton. Weevils showed no preference when given a choice between plants at the vegetative stage and the vegetative stage-mimicked plant. Altogether, the results show that DMNT and TMTT are used by boll weevils to distinguish between cotton phenological stages.


Cotton Homoterpenes Host plant Phenological stages Plant volatiles Ontogenetic Coleoptera Curculionidae 



We thank Hélio Moreira dos Santos for helping with laboratory rearing of weevils and Dr. Fabio Aquino de Albuquerque for providing cotton seeds. We also thank the Post-Graduate Zoology Program of the University of Brasília (UnB) for use of their facility. This work received financial support from the Coordination of Superior Level Staff Improving’s (CAPES) through a grant to DMM (no. 99999.014964/2013-09), National Counsel of Technological and Scientific Development (CNPq), Federal District Research Foundation (FAP-DF) and the Brazilian Corporation of Agricultural Research (EMBRAPA). Rothamsted Research received grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom.


  1. Addesso KM, Mcauslane HJ, Alborn HT (2011) Attraction of pepper weevil to volatiles from damaged pepper plants. Entomol Exp Appl 138:1–11CrossRefGoogle Scholar
  2. Arimura GI, Ozawa R, Shimoda T, Nishioka R, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defense genes in lima bean leaves. Nature 406:512–515CrossRefPubMedGoogle Scholar
  3. Barton KE, Hanely ME (2013) Seedling-herbivore interactions: insights into plant defence and regeneration patterns. Ann Bot 112:643–650CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bichão H, Borg-Karlson AK, Araújo J, Mustaparta H (2005) Five types of olfactory receptor neurons in the strawberry blossom weevil Anthonomus rubi: selective responses to inducible host-plant volatiles. Chem Senses 30:153–170CrossRefPubMedGoogle Scholar
  5. Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects – Finding the right mix. Phytochemistry 72:1605–1611CrossRefPubMedGoogle Scholar
  6. De Boer JG, Posthumus MA, Dicke M (2004) Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J Chem Ecol 30:2215–2230CrossRefPubMedGoogle Scholar
  7. Diezel C, Allmann S, Baldwin I (2011) Mechanisms of optimal defense patterns in Nicotiana attenuate: flowering attenuates herbivory-elicited ethylene and jasmonate signalling. J Integr Plant Biol 53:971–983CrossRefPubMedGoogle Scholar
  8. Hare J (2010) Ontogeny and season constrain the production of herbivore-inducible plant volatiles in the field. J Chem Ecol 36:1–12CrossRefGoogle Scholar
  9. Hegde M, Oliveira JN, Costa JG, Bleicher E, Santana AEG, Bruce TJA, Caulfield J, Dewhirst SY, Woodcock CM, Pickett JA, Birkett MA (2011) Identification of semiochemicals released by cotton, Gossypium hirsutum, upon infestation by the cotton aphid, Aphis gossypii. J Chem Ecol 37:741–750CrossRefPubMedGoogle Scholar
  10. Hoballah ME, Kollner TG, Degenhrdt J, Turlings CJ (2004) Costs of induced volatile production in maize. Oikos 105:168–180CrossRefGoogle Scholar
  11. Kalinová B, Stransky K, Harmatha J, Ctvrtecka R, Zd’arek J (2000) Can chemical cues from blossom buds influence cultivar preference in the apple blossom weevil (Anthonomus pomorum)? Entomol Exp Appl 95:47–52CrossRefGoogle Scholar
  12. Kaur H, Heinzel N, Schottner M, Baldwin IT, Gális I (2010) R2R3-NaMYB8 Regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol 152:1731–1747CrossRefPubMedPubMedCentralGoogle Scholar
  13. Khan ZR, Ampong-Nyarko K, Chiliswa P, Hassanali A, Kimani S, Lwande W, Overholt WA, Pickett JA, Smart LE, Woodcock CM (1997) Intercropping increases parasitism of pests. Nature 388:632–632CrossRefGoogle Scholar
  14. Leopold EJ (1990) Selective hydroboration of a 1,3,7-triene homogeraniol. Org Synth 64:164–171Google Scholar
  15. Lucero M, Estell R, Tellez M, Fredrickson E (2009) A retention index calculator simplifies identification of plant volatile organic compounds. Phytochem Anal 20:378–384CrossRefPubMedGoogle Scholar
  16. Magalhães DM, Borges M, Laumann RA, Sujii ER, Mayor P, Caulfield JC, Midega CA, Khan ZR, Pickett JA, Birkett MA, Blassioli-Moraes MC (2012) Semiochemicals from herbivory induced cotton plants enhance the foraging behaviour of the cotton boll weevil, Anthonomus grandis. J Chem Ecol 38:1528–1538CrossRefPubMedGoogle Scholar
  17. NIST (2008) Software NIST/EPA/NIH Mass Spectral Library 2008Google Scholar
  18. Oliveira CM, Auad AM, Mendes SM, Frizzas MR (2014) Crop losses and economic impact of insect pests on Brazilian agriculture. Crop Prot 56:50–54CrossRefGoogle Scholar
  19. Oluwafemi S, Bruce TJA, Pickett JA, Ton J, Birkett MA (2011) Behavioral Responses of leafhopper, Cicadulina storeyi China, a major vector of maize streak virus, to volatile cues from intact and leafhopper-damaged maize. J Chem Ecol 37:40–48CrossRefPubMedGoogle Scholar
  20. Optiz S, Kunert G, Gersehenzon J (2008) Increased terpenoid accumulation in cotton (Gossypium hirsutum) foliage is a general wound response. J Chem Ecol 34:508–522CrossRefGoogle Scholar
  21. Ribeiro PA, Sujii ER, Diniz IR, Medeiros MA, Salgado-Labouriau ML, Branco MC, Pires CSS, Fontes EMG (2010) Alternative food sources and overwintering feeding behaviour of the boll weevil, Anthonomus grandis Boehman (Coleoptera: Curculionidae), under the tropical conditions of Central Brazil. Neotropical Entomol 39:28–34CrossRefGoogle Scholar
  22. Rodriguez-Saona C, Crafts-Brandner SJ, Cañas LA (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29:2539–2550CrossRefPubMedGoogle Scholar
  23. Röse URS, Tumlinson JH (2004) Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds. Planta 218:824–832CrossRefPubMedGoogle Scholar
  24. Röse URS, Manukian A, Heath RR, Tumlinson JH (1996) Volatile semiochemicals released from undamaged cotton leaves. Plant Physiol 111:487–495PubMedPubMedCentralGoogle Scholar
  25. Rummel DR, Curry GL (1986) Dinâmica populacional e níveis de dano econômico. In: Barbosa S, Lukefarh MJ, Sobrinho RB (eds) O bicudo do algodoeiro, Vol 4. Departamento de Difusao Tecnologica de Documentos, Embrapa, pp 201–220Google Scholar
  26. Sappington TW, Spurgeon DW (2000) Preferred technique for adult sex determination of the boll weevil (Coleoptera: Curculionidae). Ann Entomol Soc Am 93:610–615CrossRefGoogle Scholar
  27. Schmidt FGV, Monnerat RG, Borges M, Carvalho R (2001) Metodologia de criação de insetos para avaliação de agentes entomopatogênicos. Circular Técnica N-11, Embrapa, Brasília, pp 20Google Scholar
  28. Schwarz J, Gries R, Hillier K, Vickers N, Gries G (2009) Phenology of semiochemical-mediated host foraging by the western boxelder bug, Boisea rubrolineata, an aposematic seed predator. J Chem Ecol 35:58–70CrossRefPubMedGoogle Scholar
  29. Sun XL, Wang GC, Gao Y, Chen ZM (2012) Screening and field evaluation of synthetic volatile blends attractive to adults of the tea weevil, Myllocerinus aurolineatus. Chemoecology 22:229–237CrossRefGoogle Scholar
  30. Tamiru A, Bruce TJA, Woodcock CM, Caulfield JC, Midega CAO, Ogol CKPO, Mayon P, Birkett MA, Pickett JA, Khan ZR (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol Lett 14:1075–1083CrossRefPubMedGoogle Scholar
  31. Tasin M, Betta E, Carlin S, Gasperi F, Mattivi F, Pertot I (2011) Volatiles that encode host-plant quality in grapevine moth. Phytochemistry 72:1999–2005CrossRefPubMedGoogle Scholar
  32. Tholl D, Sohrabi R, Huh JH, Lee S (2011) The biochemistry of homoterpenes – common constituents of floral and herbivore-induced plant volatiles. Phytochemistry 72:1635–1646CrossRefPubMedGoogle Scholar
  33. van Tol RW, Bruck DJ, Griepink FC, de Kogel WJ (2012) Field attraction of the vine weevil Otiorhynchus sulcatu to kairomones. J Econ Entomol 105:169–75CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • D. M. Magalhães
    • 1
    • 2
  • M. Borges
    • 1
  • R. A. Laumann
    • 1
  • C. M. Woodcock
    • 3
  • J. A. Pickett
    • 3
  • M. A. Birkett
    • 3
  • Maria Carolina Blassioli-Moraes
    • 1
  1. 1.Laboratório de Semioquímicos, Embrapa Recursos Genéticos e BiotecnologiaBrasíliaBrazil
  2. 2.Departamento de Zoologia, Instituto de Ciências BiológicasUniversidade de BrasíliaBrasíliaBrazil
  3. 3.Biological Chemistry and Crop Protection Department, Rothamsted ResearchHarpendenUK

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