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

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Abstract

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.

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References

  • 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 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Borges, M., and Aldrich, J. R. 1992. Instar-specific defensive secretions of stink bugs (Heteroptera: Pentatomidae). Experientia 48:893–896.

    Article  CAS  Google Scholar 

  • Borges, M., and Aldrich, J. R. 1994. Estudos de semioquímicos para o manejo de Telenominae, insetos benéficos. Ann. Soc. Entomol. Brasil 23:575–577.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hatanaka, A. 1993. The biogeneration of green odour by green leaves. Phytochemistry 34:1201–1218.

    Article  CAS  Google Scholar 

  • Howard, J. H., and Wiemer, D. F. 1983. The defensive secretion of Edessa rufomarginata. Naturwissenschaften 70:202–203.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kivan, M., and Kilic, N. 2004. Parasitism and development of Trissolcus simoni in eggs of different host species. Phytoparasitica 32:57–60.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lewis, W. J., and Martin, W. R. 2000. Semiochemicals for use with parasitoids: status and future. J. Chem. Ecol. 16:306–309.

    Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • Orr, D. B. 1988. Scelionid wasps as biological control agents: a review. Fla. Entomol. 71:506–528.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • Powell, W. A., and Pickett, J. A. 2003. Manipulation of parasitoids for aphid pest management: progress and prospects. Pest. Manag. Sci. 59:149–155.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

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Acknowledgment

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.

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Laumann, R.A., Aquino, M.F.S., Moraes, M.C.B. et al. Response of the Egg Parasitoids Trissolcus basalis and Telenomus podisi to Compounds from Defensive Secretions of Stink Bugs. J Chem Ecol 35, 8–19 (2009). https://doi.org/10.1007/s10886-008-9578-0

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