Do Helicoverpa armigera Moths Signal Their Fecundity by Emission of an Antagonist?

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Female Helicoverpa armigera emit a pheromone, comprised of a 98:2 ratio of (Z)-11-hexadecenal to (Z)-9-hexadecenal, to attract males. It has been proposed that “immature” female H. armigera modulate attraction of males by emitting an antagonist, (Z)-11-hexadecenol, along with pheromone during the first two nights of calling. However, it is unclear why females would call and simultaneously release pheromone and an antagonist. We conducted observations of female calling during the first five nights after adult emergence to determine periodicity. We also measured the relative abundance of (Z)-11-hexadecenol to the major component, (Z)-11-hexadecenal, on the surface of the gland of calling females and compared it to the ratio of these two compounds inside the gland over the first three nights after adult emergence to determine how much antagonist may be released. We found that young females (< 1-d-old) are unlikely to call and, based on the relative proportion of (Z)-11-hexadecenol on the gland surface, even if they did call would be unlikely to release sufficient (Z)-11-hexadecenol to diminish male attraction.

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  1. Cardé RT, Haynes KF (2004) Structure of the pheromone communication channel in moths. In: Cardé RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, New York, pp 283–332

  2. Cardé RT, Roelofs WL, Doane CC (1973) Natural inhibitor of the gypsy moth sex attractant. Nature 241:474–475.

  3. Chang H, Liu Y, Ai D, Jiang X, Dong S, Wang G (2017) A pheromone antagonist regulates optimal mating time in the moth Helicoverpa armigera. Curr Biol 27:1–6.

  4. Coffelt JA, Sower LL, Vick KW (1978) Quantitative analysis of identified compounds in pheromone gland rinses of Plodia interpunctella and Ephestia cautella at different times of day. Environ Entomol 7:502–505.

  5. Cusson M, McNeil JN (1989) Involvement of juvenile hormone in the regulation of pheromone release activities in a moth. Science 243:210–212.

  6. Czepak C, Albernaz KC, Vivan LM, Guimarães HO, Carvalhais T (2013) First reported occurrence of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Brazil. Pesqui Agropecu Trop 43:110–113.

  7. Foster SP, Anderson KG (2018) Differential pheromone sampling of the gland of female Heliothis virescens moths reveals glandular differences in composition and quantity. J Chem Ecol 44:452–462.

  8. Foster SP, Anderson KG (2019) Production and distribution of aldehyde and alcohol sex pheromone components in the pheromone gland of females of the moth Chloridea virescens. J Chem Ecol 45:9–17.

  9. Foster SP, Anderson KG, Casas J (2018) The dynamics of pheromone gland synthesis and release: a paradigm shift for understanding sex pheromone quantity in female moths. J Chem Ecol 44:525–533.

  10. Gago R, Allison JD, McElfresh JS, Haynes KF, McKenney J, Guerrero A, Millar JG (2013) A tetraene aldehyde as the major sex pheromone component of the promethea moth (Callosamia promethea (Drury)). J Chem Ecol 39:1263–1272.

  11. Groot AT, Schöfl G, Inglis O, Donnerhacke S, Classen A, Schmalz A, Santangelo RG, Emerson J, Gould F, Schal C, Heckel DG (2014) Within-population variability in a moth sex pheromone blend: genetic basis and behavioural consequences. Proc R Soc B 281:20133054.

  12. Groot AT, Nojima S, Heath JJ, Ammagarahalli B, van Wijk M, Claβen A, Santagelo RG, Lopez J, Schal C (2018) Alcohol contributes to attraction of Heliothis (= Chloridea) virescens males to females. J Chem Ecol 44:621–630.

  13. Hillier NK, Baker TC (2016) Pheromones of Heliothine Moths. In: Allison JD, Cardé RT (eds) Pheromone communication in moths: evolution, behavior, and application. University of California Press, Oakland, pp 301–333

  14. Kehat M, Dunkelblum E (1990) Behavioral responses of male Heliothis armigera (Lepidoptera: Noctuidae) moths in a flight tunnel to combinations of components identified from female sex pheromone glands. J Insect Behav 3:75–83.

  15. Kehat M, Gothilf S, Dunkelblum E, Greenberg S (1980) Field evaluation of female sex pheromone components of the cotton bollworm, Heliothis armigera. Entomol Exp Appl 27:188–193.

  16. Kou R, Chow YS (1987) Calling behavior of the cotton bollworm, Heliothis armigera (Lepidoptera: Noctuidae). Ann Entomol Soc Am 80:490–493.

  17. López C, Ardanuy A, Eizaguirre M, Albajes R (2011) Pheromone antagonism in lepidopteran maize pests. IOBC/wprs Bulletin 72:105–111

  18. Millar JG, McElfresh JS, Romero C, Vila M, Marí-Mena N, Lopez-Vaamonde C (2010) Identification of the sex pheromone of a protected species, the Spanish moon moth Graellsia isabellae. J Chem Ecol 36:923–932.

  19. Ming QL, Yan YH, Wang CZ (2007) Mechanisms of premating isolation between Helicoverpa armigera (Hübner) and Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae). J Insect Physiol 53:170–178.

  20. Nesbitt BF, Beevor PS, Hall DR, Lester R (1979) Female sex pheromone of the cotton bollworm, Heliothis armigera. J Insect Physiol 25:535–541.

  21. Nojima S, Classen A, Groot AT, Schal C (2018) Qualitative and quantitative analysis of chemicals emitted from the pheromone gland of individual Heliothis subflexa females. PLOS ONE:1–13.

  22. Pope MM, Gaston LK, Baker TC (1982) Composition, quantification, and periodicity of sex pheromone gland volatiles from individual Heliothis virescens females. J Chem Ecol 8:1043–1055.

  23. Pope MM, Gaston LK, Baker TC (1984) Composition, quantification, and periodicity of sex pheromone volatiles from individual Heliothis zea females. J Insect Physiol 30:943–945.

  24. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  25. Raina AK, Klun JA (1984) Brain factor control of sex pheromone production in the female corn earworm moth. Science 225:531–533.

  26. Raina AK, Klun JA, Stadelbacher EA (1986) Diel periodicity and effect of age and mating on female sex pheromone titer in Heliothis zea (Lepidoptera: Noctuidae). Ann Entomol Soc Am 79:128–131.

  27. Raina AK, Jaffe H, Kempe TG, Keim P, Blacher RW, Fales HM, Riley CT, Klun JA, Ridgway RL, Hayes DK (1989) Identification of a neuropeptide hormone that regulates sex pheromone production in female moths. Science 244:796–798.

  28. Riley JR, Armes NJ, Reynolds DR, Smith AD (1992) Nocturnal observations on the emergence and flight behavior of Helicoverpa armigera (Lepidoptera: Noctuidae) in the post-rainy season in Central India. Bull Entomol Res 82:243–256.

  29. Roelofs W L and Cardé RT (1977) Responses of Lepidoptera to synthetic sex pheromone chemicals and their analogues Annu Rev Entomol 22:377–405.

  30. Rothschild GHL, Nesbitt BF, Beevor PS, Cork A, Hall DR, Vickers RA (1982) Studies of the female sex pheromone of the native budworm, Heliothis punctigera. Entomol Exp Appl 31:395–401.

  31. Sower LL, Gaston LK, Shorey HH (1971) Sex pheromones of noctuid moths. XXVI. Female release rate, male response threshold, and communication distance for Trichoplusia ni. Ann Entomol Soc Am 64:448–456.

  32. Swier SR, Rings RW, Musick GJ (1977) Age-related behavior of the black cutworm, Agrotis ipsilon. Ann Entomol Soc Am 70:919–924.

  33. Teal PEA, Tumlinson JH (1986) Terminal steps in pheromone biosynthesis by Heliothis virescens and H. zea. J Chem Ecol 12:353–366.

  34. Teal PEA, Tumlinson JH (1991) Sex pheromone production in moths: endogenous regulation of initiation and inhibition. In: Hedin PA (ed) Naturally occurring pest bioregulators. American Chemical Society, Washington, DC, pp 66–77

  35. Teal PEA, Tumlinson JH, McLaughlin JR, Heath R (1984) (Z)-11-Hexadecen-1-ol: A behavioral modifying chemical present in the pheromone gland of female Heliothis zea (Lepidoptera: Noctuidae). Can Entomol 116:777–779.

  36. Umbers KDL, Symonds MRE, Kokko H (2015) The mothematics of female pheromone signaling: strategies for aging virgins. Am Nat 185:417–432.

  37. Vickers NJ (2017) Animal communication: when I’m calling you, will you answer too? Curr Biol 27:R713–R715

  38. Weatherston J, Maclean W (1974) The occurrence of (E)-11-tetradecen-1-ol, a known sex attractant inhibitor, in the abdominal tips of virgin female eastern spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). Can Entomol 106:281–284.

  39. Wu KM, Guo YY (2005) The evolution of cotton pest management practices in China. Annu Rev Entomol 50:31–52.

  40. Xu M, Guo H, Hou C, Wu H, Huang LQ, Wang CZ (2016) Olfactory perception and behavioral effects of sex pheromone gland components in Helicoverpa armigera and Helicoverpa assulta. Sci Rep 6:22998–22914.

  41. Zhang JP, Salcedo C, Fang YL, Zhang RJ, Zhang ZN (2012) An overlooked component: (Z)-9-tetradecenal as a sex pheromone in Helicoverpa armigera. J Insect Physiol 58:1209–1216.

  42. Zhao XC, Yan YH, Wang CZ (2006) Behavioral and electrophysiological responses of Helicoverpa assulta, H. armigera (Lepidoptera: Noctuidae), their F1 hybrids and backcross progenies to sex pheromone component blends. J Comp Physiol A 192:1037–1047.

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This work was funded in part by United States Department of Agriculture-Animal and Plant Health Inspection Service grants (to RTC). We are grateful to Dr. Allard Cossé of APHIS for facilitating funding, Prof. Myron Zalucki of the University of Queensland for providing H. armigera eggs, Lucio Rodriguez for assisting in wind-tunnel assays, and Dr. Emerson Lacey for his assistance in maintaining our colony and conducting observations of calling moths. Prof. Stephen Foster of North Dakota State University provided very useful comments on our study.

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Correspondence to Gabriel P. Hughes.

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Hughes, G.P., Cardé, R.T. Do Helicoverpa armigera Moths Signal Their Fecundity by Emission of an Antagonist?. J Chem Ecol 46, 21–29 (2020).

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  • Pheromone
  • Antagonist
  • Calling behavior
  • SPME
  • Pheromone gland extract