Skip to main content
Log in

Chemical Identification, Emission Pattern and Function of Male-Specific Pheromones Released by a Rarely Swarming Locust, Schistocerca americana

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Pheromones serve key functions in the biology of swarming locusts. However, research has focused largely on the mass-swarming desert locust, Schistocerca gregaria. We extended these investigations to the pheromonal profile of the rarely swarming American bird grasshopper, S. americana (Drury). The headspace of mature gregarious S. americana males contained three characteristic electroantennogram-active components: (Z)-3-nonen-1-ol, (Z)-2-octen-1-ol, and nonanal. These substances were accompanied by aromatics such as phenol that are also released by females and immatures. Male-specific pheromone components were released independently from epidermal gland cells, with the highest emission rate being for (Z)-3-nonen-1-ol from the abdomen and legs. The emission of the major compound, (Z)-3-nonen-1-ol, is stress-sensitive, and coincides with sexual maturity and crowding. The emission pattern strongly supports a role of (Z)-3-nonen-1-ol in the reproductive biology of S. americana. The pheromone is involved in courtship-inhibition and is used as mate assessment pheromone in cryptic female choice. In double mating experiments, females choose sperm of males with high (Z)-3-nonen-1-ol emission. Furthermore the pheromone accelerated maturation of immature adults and supports synchronization of sexual development.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Amerasinghe, F. P. 1978. Pheromonal effects on sexual maturation, yellowing, and the vibration reaction in immature male desert locusts (Schistocerca gregaria). J. Insect Physiol. 24:309–314.

    Article  Google Scholar 

  • Assad, Y. O. H., Hassanali, A., Torto, B., Mahamat, H., Bashir, N. H. H., and El Bashir, S. 1997. Effects of fifth-instar volatiles on sexual maturation of adult desert locust Schistocerca gregaria. J. Chem. Ecol. 23:1373–1388.

    Article  CAS  Google Scholar 

  • Boeve, J. L., Gfeller, H., Schlunegger, U. P., and Francke, W. 1997. The secretion of the ventral glands in Hoplocampa sawfly larvae. Biochem. Syst. Ecol. 25:195–201.

    Article  CAS  Google Scholar 

  • Boorman, E. and Parker, G. A. 1976. Sperm (ejaculate) competition in Drosophila melanogaster, and the reproductive value of females to males in relation to female age and mating status. Ecol. Entomol. 1:145–155.

    Article  Google Scholar 

  • Byers, J. A. 1991. Pheromones and chemical ecology of locusts. Biol. Rev. 66:347–378.

    Article  Google Scholar 

  • Cook, P. A., Harvey, I. F., and Parker, G. A. 1997. Predicting variation in sperm precedence. Phil. Trans. R. Soc. Lond. B. 352:771–780.

    Article  Google Scholar 

  • Davenport, A. P. and Evans, P. D. 1984. Stress-induced changes in the octopamine levels of insect haemolymph. Insect Biochem. 14:135–143.

    Article  CAS  Google Scholar 

  • DeGroot, P. and Poland, T. M. 2003. Attraction of Hylastes opacus (Coleoptera: Scolytidae) to nonanal. Can. Entomol. 135:309–311.

    Article  Google Scholar 

  • Dickens, J. C. 2006. Plant volatiles moderate response to aggregation pheromone in Colorado potato beetle. J. Appl. Entomol. 130:26–31.

    Article  Google Scholar 

  • Dillon, R. and Charnley, K. 2002. Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res. Microbiol. 153:503–509.

    Article  PubMed  CAS  Google Scholar 

  • Dirsh, V. M. 1974. Genus Schistocerca (Acridomorpha, Insecta). W. Junk, The Hague.

    Google Scholar 

  • Eberhard, W. G. 1996. Female control: Sexual selection by cryptic female choice. Princeton University Press, Princeton.

    Google Scholar 

  • Farine, J. P., Everaerts, C., LeQuere, J. L., Semon, E., Henry, R., and Brossut, R. 1997. The defensive secretion of Eurycotis floridana (Dictyoptera, Blattidae, Polyzosteriinae): Chemical identification and evidence of an alarm function. Insect Biochem. Molec. Biol. 27:577–586.

    Article  CAS  Google Scholar 

  • Farine, J. P., Semon, E., Everaerts, C., Abed, D., Grandcolas, P., and Brossut, R. 2002. Defensive secretion of Therea petiveriana: chemical identification and evidence of an alarm function. J. Chem. Ecol. 28:1629–1640.

    Article  PubMed  CAS  Google Scholar 

  • Fedina, T. J. and Lewis, S. M. 2008. An integrative view of sexual selection in Tribolium flour beetles. Biol. Rev. 83:151–171.

    Article  PubMed  Google Scholar 

  • Ferenz, H. J. 1990. Locust pheromones - basic and applied aspects. Bol. San. Veg. Plagas (Fuera de serie). 20:29–37.

    Google Scholar 

  • Ferenz, H. J. and Seidelmann, K. 2003. Pheromones in relation to aggregation and reproduction in desert locusts. Physiol. Entomol. 28:11–18.

    Article  CAS  Google Scholar 

  • Fuzeau-Braesch, S., Genin, E., Jullien, R., Knowles, E., and Papin, C. 1988. Composition and role of volatile substances in atmosphere surrounding two gregarious locusts, Locusta migratoria and Schistocerca gregaria. J. Chem. Ecol. 14:1023–1033.

    Article  CAS  Google Scholar 

  • Griffiths, J. T. and Thompson, W. L. 1952. Grasshoppers in citrus groves. Univ. Fla. Agric. Exp. Station Bull. 496:1–26.

    Google Scholar 

  • Grunshaw, J. P., Guermouche, H., Guermouche, S., Jago, N. D., Jullien, R., Knowles, E., and Perez, F. 1990. Chemical taxonomic studies of cuticular hydrocarbones in locusts of the Schistocerca americana complex (Acrididae: Cyrtacanthacridinae): chemical relationships between new world and old world species. J. Chem. Ecol. 16:2835–2858.

    Article  CAS  Google Scholar 

  • Harvey, A. W. 1979. Hybridization studies in the Schistocerca-Americana Complex. I. Specific status of the Central American locust. Biol. J. Linn. Soc. 12:349–355.

    Article  Google Scholar 

  • Harvey, A. W. 1982. Hybridization studies in the Schistocerca-Americana Complex. II. The Peruvian Locust. Biol. J. Linn. Soc. 17:217–223.

    Article  Google Scholar 

  • Hassanali, A., Njagi, P. G. N., and Bashir, M. O. 2005. Chemical ecology of locusts and related acridids. Annul. Rev. Entomol. 50:223–245.

    Article  CAS  Google Scholar 

  • Hawkes, F., Rzepka, J., and Gontrand, G. 1987. The scent glands of the male South American locust Schistocerca cancellata, an electron microscope study. Tissue Cell. 19:687–703.

    Article  PubMed  CAS  Google Scholar 

  • Jago, N. D., Antoniou, A., and Scott, P. 1979. Laboratory evidence showing the separate species status of Schistocerca gregaria, americana and cancellata (Acrididae, Crytacanthacridinae). Syst. Entomol. 4:133–142.

    Article  Google Scholar 

  • Johansson, B. G. and Jones, T. M. 2007. The role of chemical communication in mate choice. Biol. Rev. 82:265–289.

    Article  PubMed  Google Scholar 

  • Jones, T. M. and Hamilton, J. G. C. 1998. A role for pheromones in mate choice in a lekking sandfly. An. Behav. 56:891–898.

    Article  Google Scholar 

  • Kosal, E. F. and Niedzlek-Feaver, M. 1997. Female preferences for large, heavy mates in Schistocerca americana (Orthoptera: Acrididae). J. Insect Behav. 10:711–725.

    Article  Google Scholar 

  • Kosal, E. F. and Niedzlek-Feaver, M. 2007. Parental Size Influence on Offspring Phenotype in Schistocerca americana (Orthoptera: Acrididae). J. Orthoptera Res. 16:51–55.

    Article  Google Scholar 

  • Kroiss, J., Schmitt, T., Schreier, P., Strohm, E., and Herzner, G. 2006. A selfish function of a “social”gland? A postpharyngeal gland function as a sex pheromone reservoir in males of the solitary wasp Philanthus triangulum. J. Chem. Ecol. 32:2763–2776.

    Article  PubMed  CAS  Google Scholar 

  • Kubo, A., Lunde, C. S., and Kubo, I. 1995. Antimicrobial activity of the olive oil flavour compounds. J. Agric. Food Chem. 43:1629–1633.

    Article  CAS  Google Scholar 

  • Kuitert, L. C. and Connin, R. V. 1952. Biology of the American grasshopper in the south eastern United States. Fla. Entomol. 35:22–33.

    Article  Google Scholar 

  • Lewis, S. M. and Austad, S. N. 1994. Sexual selection in flour beetles - the relationship between sperm precedence and male olfactory attractiveness. Behav. Ecol. 5:219–224.

    Article  Google Scholar 

  • Loher, W. 1961. The chemical acceleration of the maturation process and its hormonal control in the male of the desert locust. Proc. R. Soc. Lond. B. 153:380–397.

    Article  Google Scholar 

  • Loher, W. 1990. Pheromones and phase transformation in locusts, pp. 337–355, in R. F. Chapman and A. Joern (eds.), Biology of grasshoppers. Wiley, New York.

    Google Scholar 

  • Lovejoy, N. R., Mullen, S. P., Sword, G. A., Chapman, R. F., and Harrison, R. G. 2006. Ancient trans-Atlantic flight explains locust biography: molecular phylogenetics of Schistocerca. Proc. R. Soc. Lond. B. 273:767–774.

    Article  CAS  Google Scholar 

  • Mahamat, H., Hassanali, A., Odongo, H., Torto, B., and El-Bashir, S. 1993. Studies on the maturation-accelerating pheromone of the desert locust Schistocerca gregaria (Orthoptera: Acrididae). Chemoecology 4:159–164.

    Article  CAS  Google Scholar 

  • Mahamat, H., Hassanali, A., and Odongo, H. 2000. The role of different components of the pheromone emission of mature males of the desert locust, Schistocerca gregaria (Forskål) (Orthoptera: Acrididae) in accelerating maturation of immature adults. Insect Sci. Appl. 20:1–5.

    CAS  Google Scholar 

  • Brunnemann, U. 1996. Identifizierung und Synthese von Heuschreckenpheromonen. PhD dissertation. University of Hamburg.

  • Squitier, J. M. and Capinera, J. L. 1996. American grasshopper, Schistocerca americana (Drury) (Insecta: Orthoptera: Acrididae). Institute of Food and Agricultural Sciences, University of Florida.

  • Nemoto, T., Kuwahara, Y., and Suzuki, T. 1990. Isolation and identification of male sex pheromone present in the wing gland of Achroia innotata obscurevittella Ragonot (Lepidoptera: Pyralidae). Appl. Ent. Zool. 25:261–264.

    CAS  Google Scholar 

  • Norris, M. J. 1954. Sexual maturation in the desert locust (Schistocerca gregaria Forskål) with special reference to the effects of grouping. Anti-Locust Bull. 18:1–44.

    Google Scholar 

  • Parker, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45:525–567.

    Article  Google Scholar 

  • Perić-Mataruga, V., Nenadović, V., and Ivanović, J. 2006. Neurohormones in insect stress: a review. Arch. Biol. Sci. 58:1–12.

    Article  Google Scholar 

  • Pierce, A. M., Pierce, H. D., Oehlschlager, A. C., and Borden, J. H. 1991. 1-octen-3-ol, attractive semiochemical for foreign grain beetle, Ahasverus advena (Waltl) (Coleoptera: Cucujidae). J. Chem. Ecol. 17:567–580.

    Article  CAS  Google Scholar 

  • Pureswaran, D. S., Gries, R., Borden, J. H., and Pierce Jr., H. D. 2000. Dynamics of pheromone production and communication in the mountain pine beetle, Dendroctonus ponderosae Hopkins, and the pine engraver, Ips pini (Say) (Coleoptera: Scolytidae). Chemoecology 10:153–168.

    Article  CAS  Google Scholar 

  • Raina, A. K. 1993. Neuroendocrine control of sex pheromone biosynthesis in Lepidoptera. Annu. Rev. Entomol. 38:329–349.

    Article  PubMed  CAS  Google Scholar 

  • Robacker, D. C. and Hart, W. G. 1985. (Z)-3-nonenol, (Z, Z)-3,6-nonadienol and (S, S)-(-)-epianastrephin: male produced pheromones of the Mexican fruit fly. Entomol. Exp. Appl. 39:103–108.

    Article  CAS  Google Scholar 

  • Rocca, J. R., Nation, J. L., Strekowski, L., and Battiste, M. A. 1992. Comparison of volatiles emitted by male Caribbean and Mexican fruit flies. J. Chem. Ecol. 18(2):223–244.

    Article  CAS  Google Scholar 

  • Schmidt, G. H. and Albütz, R. 2002. Sexual maturation and yellow coloration of adult males in the gregarious desert locust, Schistocerca gregaria, in relation to volatiles emitted (Caelifera: Acrididae). Entomol. Gener. 26:121–141.

    Google Scholar 

  • Schwab, W. and Schreier, P. 2002. Enzymic formation of flavour volatiles from lipids, pp. 293–318, in T. M. Kuo and H. W. Gardner (eds.), Lipid biotechnology. Marcel Dekker, New York.

    Google Scholar 

  • Seidelmann, K. 2006. The courtship-inhibiting pheromone is ignored by female-deprived gregarious desert locust males. Biol. Lett. 2:525–527.

    Article  PubMed  Google Scholar 

  • Seidelmann, K. and Warnstorff, K. 2001. Ein kombiniertes Y-T-Olfaktometer für Biotests mit großen Insekten. Mitt. Dtsch. Ges. Allg. Angew. Ent. 13:403–408.

    Google Scholar 

  • Seidelmann, K., Luber, K., and Ferenz, H. J. 2000. Analysis of release and role of benzyl cyanide in male desert locusts, Schistocerca gregaria. J. Chem. Ecol. 26:1897–1910.

    Article  CAS  Google Scholar 

  • Seidelmann, K., Weinert, H., and Ferenz, H. J. 2003. Wings and legs are production sites for the desert locust courtship-inhibiting pheromone, phenylacetonitrile. J. Insect Physiol. 49:1125–1133.

    Article  PubMed  CAS  Google Scholar 

  • Seidelmann, K., Warnstorff, K., and Ferenz, H. J. 2005. Phenylacetonitrile is a male specific repellent in gregarious desert locusts, Schistocerca gregaria. Chemoecology 15:37–43.

    Article  CAS  Google Scholar 

  • Siljander, E., Gries, R., Khaskin, G., and Gries, G. 2008. Identification of the airborne aggregation pheromone of the common bed bug, Cimex lectularius. J. Chem. Ecol. 34:708–718.

    Article  PubMed  CAS  Google Scholar 

  • Song, H. 2004. On the origin of the desert locust Schistocerca gregaria (Forskål) (Orthoptera: Acrididae: Cyrtacanthacridinae). Proc. R. Soc. Lond. B. 271:1641–1648.

    Article  Google Scholar 

  • Song, H. 2005. Phylogentic perspectives on the evolution of locust phase polyphenism. J. Orthoptera Res. 14:235–245.

    Article  Google Scholar 

  • Song, H. and Wenzel, J. W. 2007. Phylogeny of bird-grasshopper subfamily Cyrtacanthacridinae (Orthoptera: Acrididae) and the evolution of locust phase polyphenism. Cladistics 23:1–28.

    Article  Google Scholar 

  • Staples, J. K., Krall, B. S., Bartelt, R. J., and Whitman, D. W. 2002. Chemical defense in the plant bug Lopidea robiniae (Uhler). J. Chem. Ecol. 28:601–615.

    Article  PubMed  CAS  Google Scholar 

  • Sword, G. A. 2003. To be or not to be a locust? A comparative analysis of behavioural phase change in nymphs of Schistocerca americana and Schistocerca gregaria. J. Insect Physiol. 49:709–717.

    Article  PubMed  CAS  Google Scholar 

  • Symonds, M. R. E. and Elgar, M. A. 2008. The evolution of pheromone diversity. Trends Ecol. Evol. 23:220–228.

    Article  PubMed  Google Scholar 

  • Torto, B., Obeng-Ofori, D., Njagi, P. G. N., Hassnali, A., and Amiani, H. 1994. Aggregation pheromone system of adult gregarious desert locust Schistocerca gregaria (Forskål). J. Chem. Ecol. 20:1749–1762.

    Article  CAS  Google Scholar 

  • Torto, B., Njagi, P. G. N., Hassanali, A., and Amiani, H. 1996. Aggregation pheromone system of nymphal gregarious desert locust, Schistocerca gregaria (Forskål). J. Chem. Ecol. 22:2273–2281.

    Article  CAS  Google Scholar 

  • Türker, L., Togan, I., Ergezen, S., and Özer, M. 1993. Novel attractants of Galleria mellonella L (Lepidoptera Pyralidae Galleriinae). Apidologie 24:425–430.

    Article  Google Scholar 

  • Uvarov, B. 1977. Grasshoppers and locusts: a handbook of general acridology II. Centre for Overseas Pest Research. United Kingdom, Cambridge.

    Google Scholar 

  • Wood, W. F. and Weldon, P. J. 2002. The scent of the reticulated giraffe (Giraffa camelopardalis reticulate). Biochem. Syst. Ecol. 30:913–917.

    Article  CAS  Google Scholar 

  • Zhang, A., Robbins, P. S., Averill, A. L., Weber, D. C., Linn Jr., C. E., Roelofs, W. L., and Villani, M. G. 2003. Identification of the female-produced sex pheromone of the scarab beetle, Hoplia equina. J. Chem. Ecol. 29:1635–1642.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Q. H., Chauhan, K. R., Erbe, E. F., Vellore, A. R., and Aldrich, J. R. 2004. Semiochemistry of the goldeneyed lacewing Chrysopa oculata: attraction of males to a male-produced pheromone. J. Chem. Ecol. 30:1849–1870.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to R. Csuk (Dep. Org. Chem., Univ. Halle) for the synthesis of (E)-3-nonen-1-ol and (Z)-2-octen-1-ol as basis for the identification of stereoisomers. The sterioisomeric analysis was kindly executed by P. Lindemann (Dep. Pharmac. Biotech., Univ. Halle). R. Gerlach (Dep. Radiation Therapy, Univ. Halle) provided technical support for the sterilization of locusts. We thank S. Hertel for technical assistance and maintenance of the locust culture. Financial support from Max Planck Gesellschaft is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christiane Stahr.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

Accurate mass spectra of compounds 1-3 measured on Masspec GC-MS instrument; Peak 1 NIST database hit (Purity/Mixture) 961/963 for 2-octen-1-ol, peak 2 hit 983/983 for nonanal and the major peak 3 hit 989/989 for 3-nonen-1-ol (PDF 16 kb)

Fig. S1

Adducts of acetylation and following DMDS derivatisation of (Z)-3-nonen-1-ol (a) and (Z)-2-octen-1-ol (b) (PDF 24 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stahr, C., Svatoš, A. & Seidelmann, K. Chemical Identification, Emission Pattern and Function of Male-Specific Pheromones Released by a Rarely Swarming Locust, Schistocerca americana . J Chem Ecol 39, 15–27 (2013). https://doi.org/10.1007/s10886-012-0233-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0233-4

Keywords

Navigation