Skip to main content
Log in

Attraction of Telenomus podisi to volatiles induced by Euschistus heros in three different plant species

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Specialized natural enemies that forage for polyphagous hosts need to locate hosts on different plants. Telenomus podisi (Hymenoptera: Platygastridae) is a stink bug egg parasitoid with a preference for Euschistus heros (Hemiptera, Pentatomidae), a polyphagous species. The aim of this study was to evaluate the induction of defences in three E. heros host plants: maize (Zea mays), sunflower (Helianthus annuus) and pigeon pea (Cajanus cajan). We hypothesized that E. heros damage to these three plants enhances the attraction of the parasitoid T. podisi as has been observed in other systems. Using Y-tube olfactometer bioassays, we tested parasitoid responses to combinations of the following odour sources: clean air, undamaged plants and plants damaged by stink bug feeding. Volatiles were collected by means of dynamic headspace collection and analysed by gas chromatography coupled to mass spectrometry. T. podisi did not distinguish odours from undamaged plants against air for any of the three plant species. For maize, the parasitoid preferred the odour from herbivore-damaged plants over both clean air and undamaged plants. For sunflower, the parasitoid only preferred the odour of herbivore-damaged plants over the odour of undamaged plants. For pigeon pea, no preferences were observed. Quantitative differences in the volatile profile of damaged and undamaged plants were observed in each plant species. We conclude that sunflower and maize plants, when damaged by E. heros, release volatiles that attract the parasitoid T. podisi; the parasitoid appears to use a different blend composition to distinguish herbivore-damaged plants of each species.

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

Similar content being viewed by others

References

  • Borges M, Costa MLM, Sujii ER, Cavalcanti MG, Redígolo GF, Resck IS, Vilela EF (1999) Semiochemical and physical stimuli involved in host recognition by Telenomus podisi (Hymenoptera: Scelionidae) toward Euschistus heros (Heteroptera: Pentatomidae). Physiological Entomology 24:227–233

    Article  Google Scholar 

  • Borges M, Laumann RA, Silva CC, Moraes MCB, Santo SHM, Ribeiro DT (2006) Metodologias de criação e manejo de colônias de percevejos da soja (Hemiptera: Pentatomidae) para estudos de comportamento e ecologia química. Brasília: Embrapa – Cenargen. 18p. Documentos, n. 182

  • Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects—finding the right mix. Phytochemistry 72:1605–1611. doi:10.1016/j.phytochem.2011.04.011

    Article  CAS  PubMed  Google Scholar 

  • Colazza S, Fucarino A, Peri E, Salerno G, Conti E, Bin F (2004a) Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J Exp Biol 207:47–53

    Article  PubMed  Google Scholar 

  • Colazza S, McElfresh JS, Millar JG (2004b) Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J Chem Ecol 30:945–964

    Article  CAS  PubMed  Google Scholar 

  • Copatti JF, Oliveira NC (2011) Danos iniciais causados pelos percevejos Dichelops melacanthus e Euschistus heros (Hemiptera: Pentatomidae) em plantas de milho. Campo Digit Campo Mourão 6:1–8

    Google Scholar 

  • D’Alessandro M, Brunner V, Gv Mérey, Turlings TCJ (2009) Strong attraction of the parasitoid Cotesia marginiventris towards minor volatile compounds of maize. J Chem Ecol 35:999–1008. doi:10.1007/s10886-009-9692-7

    Article  PubMed  Google Scholar 

  • de Boer JG, Hordijk CA, Posthumus MA, Dicke M (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J Chem Ecol 34:281–290

    Article  PubMed  PubMed Central  Google Scholar 

  • De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • Development Core Team R (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175. doi:10.1016/j.tplants.2009.12.002

    Article  CAS  PubMed  Google Scholar 

  • Du Y-J, Poppy GM, Powell W (1996) Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi. J Chem Ecol 22:1591–1605

    Article  CAS  PubMed  Google Scholar 

  • Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689. doi:10.1093/beheco/arn011

    Article  Google Scholar 

  • Fritzsche Hoballah ME, Tamò C, Turlings TCJ (2002) Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid Cotesia marginiventris: is quality or quantity important? J Chem Ecol 28:951–968

    Article  Google Scholar 

  • Gouinguené S, Degen T, Turlings TCJ (2001) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors. Chemoecology 11:9–16

    Article  Google Scholar 

  • Higuchi H (1992) Population prevalence of occurrence and spatial distribution pattern of Piezodorus hybneri adults (Heteroptera: Pentatomidae) on soybeans. Appl Entomol Zool 27:363–369

    Google Scholar 

  • Hilker M, McNeil JN (2008) Chemical and behavioral ecology in insect parasitoids: how to behave optimally in a complex odorous environment. In: Wajnberg E, Bernstein C, Van Alphen JJM (eds) Behavioral ecology of insect parasitoids: from theoretical approaches to field applications. Blackwell, Malden, pp 97–100

    Google Scholar 

  • Hilker M, Meiners T (2010) How do plants ‘‘notice’’ attack by herbivorous arthropods? Biol Rev 85:267–280. doi:10.1111/j.1469-185X.2009.00100.x

    Article  PubMed  Google Scholar 

  • Hilker M, Kobs C, Varama M, Schrank K (2002) Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. J Exp Biol 205:455–461

    PubMed  Google Scholar 

  • Karban R, Myers JH (1989) Induced plant-responses to herbivory. Annu Rev Ecol Syst 20:331–348

    Article  Google Scholar 

  • Kariyat RR, Mauck KE, De Moraes CM, Stephenson AG, Mescher MC (2012) Inbreeding alters volatile signalling phenotypes and influences tri-trophic interactions in horsenettle (Solanum carolinense L.). Ecol Lett 15:301–309. doi:10.1111/j.1461-0248.2011.01738.x

    Article  PubMed  Google Scholar 

  • Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844. doi:10.1104/pp.107.112029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laumann RA, Aquino MFS, Moraes MCB, Pareja M, Borges M (2009) Response of the egg parasitoids trissolcus basalis and Telenomus podisi to compounds from defensive secretions of stink bugs. J Chem Ecol 35:8–19. doi:10.1007/s10886-008-9578-0

    Article  CAS  PubMed  Google Scholar 

  • Laumann RA, Cokl A, Lopes APS, Fereira JBC, Moraes MCB, Borges M (2011) Silent singers are not safe: selective response of a parasitoid to substrate-borne vibratory signals of stink bugs. Anim Behav 82:1175–1183. doi:10.1016/j.anbehav.2011.08.017

    Article  Google Scholar 

  • Lopes APS, Diniz IR, Moraes MCB, Borges M, Laumann RA (2012) Defesas induzidas por herbivoria e interações específicas no sistema tritrófico soja percevejos parasitoides de ovos. Pesquisa Agropecuária Brasileira 47:875–878

    Article  Google Scholar 

  • Malaguido AB, Panizzi AR (1998) Damage of Euschistus heros (F.) (Hemiptera: Pentatomidae) to sunflower seeds. Anais da Sociedade Entomológica do Brasil 27:535–541

    Article  Google Scholar 

  • McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310. doi:10.1016/j.tplants.2012.03.012

    Article  Google Scholar 

  • Melo Machado RC, Sant’Ana J, Blassioli-Moraes MC, Laumann RA, Borges M (2014) Herbivory-induced plant volatiles from Oryza sativa and their influence on chemotaxis behaviour of Tibraca limbativentris Stal. (Hemiptera: Pentatomidae) and egg parasitoids. Bull Entomol Res 104:347–356. doi:10.1017/S0007485314000133

    Article  CAS  PubMed  Google Scholar 

  • Michereff MFF, Laumann RA, Borges M, Michereff-Filho M, Diniz IR, Neto ALF, Moraes MCB (2011) Volatiles mediating a plant-herbivore-natural enemy interaction in resistant and susceptible soybean cultivars. J Chem Ecol 37:273–285. doi:10.1007/s10886-011-9917-4

    Article  CAS  PubMed  Google Scholar 

  • Michereff MFF, Borges M, Laumann RA, Diniz IR, Neto ALF, Moraes MCB (2013) Influence of volatile compounds from herbivore-damaged soybean plants on searching behavior of the egg parasitoid Telenomus podisi. Entomol Exp Appl 147:9–17

    Article  CAS  Google Scholar 

  • Moraes MCB, Laumann R, Sujii ER, Pires C, Borges M (2005) Induced volatiles in soybean and pigeon pea plants artificially infested with the neotropical brown stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi. Entomol Exp Appl 115:227–237

    Article  CAS  Google Scholar 

  • Moraes MCB, Pareja M, Laumann RA, Hoffmann-Campo CB, Borges M (2008) Response of the parasitoid Telenomus podisi to induced volatiles from soybean damaged by stink bug herbivory and oviposition. J Plant Interact 3:111–118

    Article  CAS  Google Scholar 

  • Moraes MCB et al (2009) Attraction of the stink bug egg parasitoid Telenomus podisi to defence signals from soybean activated by treatment with cis-jasmone. Entomol Exp Appl 131:178–188. doi:10.1111/j.1570-7458.2009.00836.x

    Article  CAS  Google Scholar 

  • Mumm R, Hilker M (2005) The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem Senses 30:337–343. doi:10.1093/chemse/bji028

    Article  CAS  PubMed  Google Scholar 

  • Mumm R, Schrank K, Wegener R, Schulz S, Hilker M (2003) Chemical analysis of volatiles emitted by Pinus sylvestris after induction by insect oviposition. J Chem Ecol 29:1235–1252

    Article  CAS  PubMed  Google Scholar 

  • NIST (2008) NIST/EPA/NIH Mass Spectral Library 2008

  • Ode PJ (2013) Plant defences and parasitoid chemical ecology. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley, Oxford, pp 11–36

    Google Scholar 

  • Panizzi AR (1997) Wild hosts of pentatomids: ecological significance and role in their pest status on crops. Annu Rev Entomol 42:99–122

    Article  CAS  PubMed  Google Scholar 

  • Panizzi AR, Vivan LM (1997) Seasonal abundance of the neotropical brown stink bug, Euschistus heros, in overwintering sites, and the breaking of dormancy. Entomol Exp Appl 82:213–217

    Article  Google Scholar 

  • Pareja M, Mohib A, Birkett MA, Dufour S, Glinwood RT (2009) Multivariate statistics coupled to generalized linear models reveal complex use of chemical cues by a parasitoid. Anim Behav 77:901–909. doi:10.1016/j.anbehav.2008.12.016

    Article  Google Scholar 

  • Pashalidou FG, Huigens ME, Dicke M, Fatouros NE (2010) The use of oviposition-induced plant cues by Trichogramma egg parasitoids. Ecol Entomol 35:748–753. doi:10.1111/j.1365-2311.2010.01235.x

    Article  Google Scholar 

  • Piñero JC, Dorn S (2007) Synergism between aromatic compounds and green leaf volatiles derived from the host plant underlies female attraction in the oriental fruit moth. Entomol Exp Appl 125:185–194

    Article  Google Scholar 

  • Rodriguez-Saona C, Kaplan I, Braasch J, Chinnasamy D, Williams L (2011) Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biol Control 59:294–303. doi:10.1016/j.biocontrol.2011.06.017

    Article  CAS  Google Scholar 

  • Rodríguez-Saona C, Chalmers JA, Raj S, Thaler JS (2005) Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid. Oecologia 143:566–577

    Article  PubMed  Google Scholar 

  • Silva CC, Laumann RA, Blassioli MC, Pareja M, Borges M (2008) Euschistus heros mass rearing technique for the multiplication of Telenomus poldisi. Pesquisa Agropecuária Brasileira 43:575–580

    Google Scholar 

  • Storeck A, Poppy GM, van Emden HF, Powell W (2000) The role of plant chemical cues in determining host preference in the generalist aphid Aphidius colemani. Entomol Exp Appl 97:41–46

    Article  CAS  Google Scholar 

  • Sujii ER, Costa MLM, Pires CSS, Colazza S, Borges M (2002) Inter and intra-guild interactions in egg parasitoid species of the soybean stink bug complex. Pesquisa Agropecuária Brasileira 37:1541–1549

    Article  Google Scholar 

  • Tillman PG, Northfield TD, Mizell RF, Riddle TC (2009) Spatiotemporal patterns and dispersal of stink bugs (Heteroptera: Pentatomidae) in peanut-cotton farmscapes. Environ Entomol 38:1038–1052

    Article  CAS  PubMed  Google Scholar 

  • van Poecke RMP, Dicke M (2004) Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant. Plant Biol 6:387–401

    Article  PubMed  Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritophic context. Annu Rev Entomol 37:141–172

    Article  Google Scholar 

  • Wäschke N, Meiners T, Rostás M (2013) Foraging strategies of parasitoids in complex chemical environments. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley, Chichester, pp 37–63

    Chapter  Google Scholar 

Download references

Acknowledgments

This work received financial support from the Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq, through a studentship to AMD, as well as grants from Embrapa, CNPq and FAP-DF. MP was supported by a FAEPEX-PAPDIC grant from UNICAMP.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martín Pareja.

Additional information

Handling Editor: Jarmo Holopainen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dias, A.M., Pareja, M., Laia, M. et al. Attraction of Telenomus podisi to volatiles induced by Euschistus heros in three different plant species. Arthropod-Plant Interactions 10, 419–428 (2016). https://doi.org/10.1007/s11829-016-9453-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-016-9453-9

Keywords

Navigation