Journal of Chemical Ecology

, Volume 35, Issue 1, pp 8–19 | Cite as

Response of the Egg Parasitoids Trissolcus basalis and Telenomus podisi to Compounds from Defensive Secretions of Stink Bugs

  • Raúl A. Laumann
  • Michely F. S. Aquino
  • Maria C. B. Moraes
  • Martín Pareja
  • Miguel Borges


We tested the hypotheses that host-searching behavior of the egg parasitoids Telenomus podisi and Trissolcus basalis may be differentially influenced by the different blends of volatiles released from the metathoracic glands of adult stink bug host species. We further studied whether such a differential response is due to different individual components of these glands and whether these responses reflect host preferences. Y-tube olfactometer bioassays were carried out with crude extracts of metathoracic glands of five different host species of neotropical stink bugs. Additionally, we tested the parasitoids’ responses to synthetic standards of individual compounds identified in these stink bug glands. Results showed that females of T. basalis and T. podisi responded differentially to crude gland extracts of the different species of host stink bugs and to the compounds tested. The parasitoid T. basalis showed a positive taxic behavior to Nezara viridula methathoracxic gland extracts of a host species preferred in the field, i.e., N. viridula. Furthermore, T. basalis responded positively to 4-oxo-(E)-2-hexenal and (E)-2-decenal, two components of N. viridula glandular secretion. Higher residence time, reduced linear velocity, and higher tortuosity in the arm of the olfactometer supplied with 4-oxo-(E)-2-hexenal showed that this compound modifies the kinetics of some traits of T. basalis walking pattern and suggests that it might stimulate the searching behavior of this parasitoid. The parasitoid T. podisi was attracted to crude gland extracts of the preferred host (Euschistus heros) and also to 4-oxo-(E)-2-hexenal. Additionally, this parasitoid responded positively to (E)-2-hexenal and to the hydrocarbon tridecane, both of which are defensive compounds released from the metathoracic glands by several stink bugs. The results indicate some degree of specialization in the response of two generalist parasitoid species toward defensive secretions of stink bugs.


Defensive compounds Host searching Host–parasitoid interactions Kairomones Host preference Hymenoptera Sceolionidae Hemiptera Pentatomidae 



We thank H. Santos and D. Tiburcio, for helping with field collection and laboratory rearing of the insects used. We are grateful to Monika Hilker for assistance with editorial corrections and suggestions that helped us improve the work, and to two anonymous reviewers for comments on the first version of this work. This work received financial support from the Brazilian Council for Scientific and Technological Development (CNPq), Distrito Federal Research Foundation (FAPDF), Catholic University (scientific initiation studentship to MFSA), and EMBRAPA.


  1. Aldrich, J. R. 1985. Pheromone of a true bug (Hemiptera: Heteroptera): attractant for the predator, Podisus maculiventris and kairomonal effects, pp. 95–119, in T.E. Acree, and M.D. Soderlund (eds.). Semiochemistry: Flavors and Pheromones. Proceedings of the Amercian Chemical Society Symposium, Washington, D.C., August 1983. W. de Gruyter, New York.Google Scholar
  2. Aldrich, J. R. 1995. Chemical communication in the true bugs and parasitoid exploitation, pp. 318–363, in R.T. Cardé, and W.J. Bell (eds.). Chemical Ecology of Insects II Chapman and Hall, New York.Google Scholar
  3. Arakaki, N., Wakamura, S., and Yasuda, T. 1996. Phoretic egg parasitoid, Telenomus euproctidis (Hymenoptera: Scelionidae), uses sex pheromone of tussock moth Euproctis taiwana (Lepidoptera: Lymantriidae) as a kairomone. J. Chem. Ecol. 22:1079–1085.CrossRefGoogle Scholar
  4. Arakaki, N., Wakamura, S., Yasuda, T., and Yamagishi, K. 1997. Two regional strains of phoretic egg parasitoid, Telenomus euproctidis (Hymenoptera: Scelionidae), that use different sex pheromones of two allopatric tussock moth species as kairomones. J. Chem. Ecol. 23:153–161.CrossRefGoogle Scholar
  5. Arias-Penna, T. M. 2002. Lista de los géneros y especies de la superfamília Platygastroidea (Hymenoptera) de la Región Neotropical. Biota Colombiana 3:215–233.Google Scholar
  6. Austin, A. D., Johnson, N. F., and Dowton, M. 2005. Systematic, evolution and biology of scelionid and platygastrid wasps. Annu. Rev. Entomol. 50:553–582.PubMedCrossRefGoogle Scholar
  7. Bin, F., Vinson, S. B., Starnd, M. R., Colazza, S., and Jones, W. A. Jr. 1993. Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula. Physiol. Entomol. 18:7–15.CrossRefGoogle Scholar
  8. Borges, M., and Aldrich, J. R. 1992. Instar-specific defensive secretions of stink bugs (Heteroptera: Pentatomidae). Experientia 48:893–896.CrossRefGoogle Scholar
  9. Borges, M., and Aldrich, J. R. 1994. Estudos de semioquímicos para o manejo de Telenominae, insetos benéficos. Ann. Soc. Entomol. Brasil 23:575–577.Google Scholar
  10. Borges, M., Medeiros, M. A., Mori, K., Zarbin, P. H. G., and Ferreira, J. T. B. 1998. Field responses of stink bugs to the natural and synthetic pheromone of the Neotropical Brown Stink Bug, Euschistus heros (Heteroptera: Pentatomidae). Physiol. Entomol. 23:202–207.CrossRefGoogle Scholar
  11. Borges, M., Costa, M. L. M., Sujii, E. R., Cavalcanti, M., Das, G., Redígolo, G. F., Resck, I. S., and Vilela, E. F. 1999. Semiochemical and physical stimuli involved in host recognition by Telenomus podisi (Hymenoptera: Scelionidae) toward Euschistus heros (Heteroptera: Pentatomidae). Physiol. Entomol. 24:227–233.CrossRefGoogle Scholar
  12. Borges, M., Colazza, S., Ramirez-Lucas, P., Chauhan, K. R., Moraes, M. C. B., and Aldrich, J. R. 2003. Kairomonal effect of walking traces from Euschistus heros (Heteroptera: Pentatomidae) on two strains of Telenomus podisi (Hymenoptera: Scelionidae). Physiol. Entomol. 28:349–355.CrossRefGoogle Scholar
  13. Borges, M., Millar, J. G., Laumann, R. A., and Moraes, M. C. B. 2007. A male produced sex pheromone from the neotropical redbanded stink bug Piezodorus guildinii (F.) (Heteroptera: Pentatomidae). J. Chem. Ecol. 33:1235–1248.PubMedCrossRefGoogle Scholar
  14. Bruni, R., SantÁna, J., Aldrich, J. R., and Bin, F. 2000. Influence of host pheromone on egg parasitism by scelionid wasps: comparison of phoretic and nonphoretic parasitoids. J. Ins. Behav. 13:165–173.CrossRefGoogle Scholar
  15. Colazza, S., Rosi, M. C., and Clemente, A. 1997. Response of egg parasitoid Telenomus busseolae to sex pheromone of Sesamia nonagroides. J. Chem. Ecol. 23:1437–1444.CrossRefGoogle Scholar
  16. Colazza, S., Salerno, G., and Wajnberg, E. 1999. Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol. Control 16:310–317.CrossRefGoogle Scholar
  17. Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E., and Bin, F. 2004. Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J. Exp. Biol. 207:47–53.PubMedCrossRefGoogle Scholar
  18. Conti, E., Salerno, G., Bin, F., Williams, H. J., and Vinson, S. B. 2003. Chemical cues from Murgantva histrionica eliciting host location and recognition in the egg parasitoid Trissolcus brochymenae. J. Chem Ecol. 29:115–130.PubMedCrossRefGoogle Scholar
  19. Conti, E., Salerno, G., Bin, F., and Vinson, S. B. 2004. The role of host semiochemicals in parasitoid specificity: a case study with Trissolcus brochymenae and Trissolcus simoni on pentatomid bugs. Biol. Control 29:435–444.CrossRefGoogle Scholar
  20. Corrêa-Ferreira, B. S., and Moscardi, F. 1995. Seasonal occurrence and host spectrum of egg parasitoids associated with soybean stink bugs. Biol. Control 5:196–202.CrossRefGoogle Scholar
  21. Fatouros, N. E., Dicke, M., Mumm, R., Meiners, T., and Hilker, M. 2008. Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19:677–689. doi: 10.1093/beheco/arn011.CrossRefGoogle Scholar
  22. Hatanaka, A. 1993. The biogeneration of green odour by green leaves. Phytochemistry 34:1201–1218.CrossRefGoogle Scholar
  23. Howard, J. H., and Wiemer, D. F. 1983. The defensive secretion of Edessa rufomarginata. Naturwissenschaften 70:202–203.CrossRefGoogle Scholar
  24. Kivan, M., and Kilic, N. 2002. Host preference: parasitism, emergence and development of Trissolcus semistriatus (Hym., Scelionidae) in various host eggs. J. Appl. Entomol. 126:395–399.CrossRefGoogle Scholar
  25. Kivan, M., and Kilic, N. 2004. Parasitism and development of Trissolcus simoni in eggs of different host species. Phytoparasitica 32:57–60.CrossRefGoogle Scholar
  26. Laumann, R. A., Moraes, M. C. B., Cokl, A., and Borges, M. 2007. Eavesdropping on the sexual vibratory communication of stink bugs (Hemiptera: Pentatomidae) by the egg parasitoid Telenomus podisi. Anim. Behav. 73:637–649.CrossRefGoogle Scholar
  27. Laumann, R. A., Moraes, M. C. B., Pareja, M., Alarcão, G. C., Botelho, A. C., Maia, A. N. H., Leonardecz, Neto, E., and Borges, M. 2008. Comparative biology and functional response of Trissolcus spp. (Hymenoptera: Scelionidae) and implications for stink-bugs (Hemiptera: Pentatomidae) biological control. Biol. Control 44:32–41.CrossRefGoogle Scholar
  28. Lewis, W. J., and Martin, W. R. 2000. Semiochemicals for use with parasitoids: status and future. J. Chem. Ecol. 16:306–309.Google Scholar
  29. Masner, L. 1993. Superfamily Platygastroidea, pp. 558–565, in H. Goulet, and J.T. Huber (eds.). Hymenoptera of the World: An identification guide to familiesAgriculture Canada, Ottawa.Google Scholar
  30. Mattiaci, L., Vinson, S. B., Williams, H. J., Aldrich, J. R., and Bin, F. 1993. A long range attractant kairomone for egg parasitoid Trissolcus basalis, isolated from defensive secretion of its host, Nezara viridula. J. Chem. Ecol. 19:1167–1181.CrossRefGoogle Scholar
  31. Medeiros, M. A., Schmidt, F. V. G., Loiácono, M. S., Carvalho, V., and Borges, M. 1997. Parasitismo e predação em ovos de Euschistus heros (Fab.) (Heteroptera: Pentatomidae) no Distrito Federal, Brasil. An. Soc. Entomol. Brasil 26:397–401.Google Scholar
  32. Medeiros, M. A., Loiácono, M. S., Borges, M., and Schmidt, F. V. G. 1998. Incidência natural de parasitóides em ovos de percevejos (Hemíptera; Pentatomidae) encontrados na soja no distrito Federal. Pesq. Agropec. Bras. 33:1431–1435.Google Scholar
  33. Meiners, T., Westerhaus, C., and Hilker, M. 2000. Specificity of chemical cues used by a specialist egg parasitoid during host location. Entomol. Exp. Appl. 95:151–159.CrossRefGoogle Scholar
  34. Moraes, M. C. B., Laumann, R. A., Sujii, E. R., Pires, C., and Borges, M. 2005a. Induced volatiles in soybean and pigeon pea plants artificially infested with the neotropical stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi. Entomol. Exp. Appl. 115:227–237.CrossRefGoogle Scholar
  35. Moraes, M. C. B., Millar, J. G., Laumann, R. A., Sujii, E. R., Pires, C. S. S., and Borges, M. 2005b. Sex attractant pheromone from the neotropical red-shouldered stink bug, Thyanta perditor (F.). J. Chem. Ecol. 31:1415–1427.PubMedCrossRefGoogle Scholar
  36. Moraes, M. C. B., Pareja, M. F., Laumann, R. A., Hoffmann-Campo, C. B., and Borges, M. 2008. Response of the parasitoid Telenomus podisi to induced volatiles from soybean damaged by stink bug herbivory and oviposition. J. Plant Int. 3:1742–1756.Google Scholar
  37. Nordlund, D. A., Lewis, W. J., and Gueldner, R. C. 1983. Kairomones and their use for management of entomophagous insects: XIV. Response of Telenomus remus to abdominal tips of Spodoptera frugiperda, (Z)-9-tetradecene-1-ol acetate and (Z)-9-dodecene-1-ol acetate. J. Chem. Ecol. 9:695–701.CrossRefGoogle Scholar
  38. Orr, D. B. 1988. Scelionid wasps as biological control agents: a review. Fla. Entomol. 71:506–528.CrossRefGoogle Scholar
  39. Pacheco, D. J. P., and Corrêa-Ferreira, B. S. 2000. Parasitismo de Telenomus podisi Ashmead (Hymenoptera: Scelionidae) em populações de percevejos pragas da soja. Ann. Soc. Entomol. Brasil 29:295–302.Google Scholar
  40. Pareja, M., Borges, M., Laumann, R. A., and Moraes, M. C. B. 2007. Inter- and intraspecific variation in defensive compounds produced by five neotropical stink bug species (Hemiptera: Pentatomidae). J. Insect. Physiol. 53:639–648.PubMedCrossRefGoogle Scholar
  41. Pires, C. S. S., Sujii, E. R., Borges, M., Schmidt, F., Zarbin, P. H. G., Azevedo, V. C. R., Lacerda, A. L., and Pantaleão, D. 2001. Ação cairomonal de componentes do feromônio de alarme do percevejo verde pequeno da soja, Piezodorus guildinii, sobre o parasitóide de ovos Telenomus podisi. Embrapa, Boletim de Pesquisa e Desenvolvimento no. 129.Google Scholar
  42. Powell, W. A., and Pickett, J. A. 2003. Manipulation of parasitoids for aphid pest management: progress and prospects. Pest. Manag. Sci. 59:149–155.PubMedCrossRefGoogle Scholar
  43. Salerno, G., Conti, E., Peri, E., Colazza, S., and Bin, F. 2006. Kairomone involvement in host specificity of the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Eur. J. Entomol. 103:311–318.Google Scholar
  44. Silva, C. C., Moraes, M. C. B., Laumann, R. A., and Borges, M. 2006. Sensory response of the egg parasitoid, Telenomus podisi to stimuli from the bug, Euschistus heros. Pesq. Agropec. Bras. 41:1093–1098.Google Scholar
  45. Steidle, J. L. M., and Van, Loon, J. J. A. 2002. Chemoecology of parasitoid and predator oviposition behaviour, pp. 291–317, in M. Hilker, and T. Meiners (eds.). Chemoecology of Insect Eggs and Egg DepositionBlackwell Publishing, Oxford and Berlin.Google Scholar
  46. Steidle, J. L. M., and Van, Loon, J. J. A. 2003. Dietary specialization and infochemical use in carnivorous arthropods: testing a concept. Entomol. Exp. Appl. 108:133–148.CrossRefGoogle Scholar
  47. Sujii, E. R., Costa, M. L. M., Pires, C. S., Colazza, S., and Borges, M. 2002. Inter and intra-guild interactions in egg parasitoid species of the soybean stink bug complex. Pesq. Agropec. Bras. 37:1541–1549.Google Scholar
  48. Vet, L. E. M., and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tri-trophic context. Annu. Rev. Entomol. 47:141–172.CrossRefGoogle Scholar
  49. Vet, L. E. M., Wackers, F. L., and Dicke, M. 1991. How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids. Neth. J. Zool. 41:202–213.CrossRefGoogle Scholar
  50. Vet, L. E. M., Lewis, W. J., and Cardé, R. T. 1995. Parasitoid foraging and learning, pp. 65–101, in R.T. Cardé, and W. J. Bell (eds.). Chemical Ecology of Insects IIChapman and Hall, New York.Google Scholar
  51. Vinson, S. B. 1985. The behaviour of parasitoids, pp. 417–469, in G.A. Kerkut, and L.I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and PharmacologyPergamon Press, New York.Google Scholar
  52. Vinson, S. B. 1998. The general host selection behaviour of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol. Control 11:79–96.CrossRefGoogle Scholar
  53. Zarbin, P. H. G., Borges, M., dos, Santos, A. A., de, Oliveira, A. R. M., Simonelli, F., and Marques, F. D. A. 2000. Alarm pheromone system of stink bug Piezodorus guildinii (Heteroptera: Pentatomidae). J. Braz. Chem. Soc. 11:424–428.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Raúl A. Laumann
    • 1
  • Michely F. S. Aquino
    • 1
    • 2
  • Maria C. B. Moraes
    • 1
  • Martín Pareja
    • 1
    • 3
  • Miguel Borges
    • 1
  1. 1.Embrapa Recursos Genéticos e BiotecnologiaBrasíliaBrazil
  2. 2.Department of BiologyCatholic University of BrasíliaBrasíliaBrazil
  3. 3.Department of EcologySwedish University of Agricultural Sciences—SLUUppsalaSweden

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