Journal of Chemical Ecology

, Volume 42, Issue 10, pp 1016–1027 | Cite as

Volatiles Mediating Parasitism of Euschistus conspersus and Halyomorpha halys Eggs by Telenomus podisi and Trissolcus erugatus

  • Roberta Tognon
  • Josué Sant’Ana
  • Qing-He Zhang
  • Jocelyn G. Millar
  • Jeffrey R. Aldrich
  • Frank G. Zalom


This study identified chemicals found on the eggs of two stink bug species, one native to western North America, Euschistus conspersus, and an invasive species from Asia, Halyomorpha halys. The responses of two scelionid egg parasitoids, Trissolcus erugatus and Telenomus podisi, toward natural stink bug egg volatiles, and synthetic reconstructions of egg volatiles, were tested in bioassays. A compound, methyl (2E,4Z)-2,4-decadienoate, previously identified as the major component of the male-produced aggregation pheromone of E. conspersus, was the major volatile identified from extracts of E. conspersus eggs. In contrast, for H. halys, the sesquiterpenoids that compose the male-produced aggregation pheromone of this species were not detected on eggs, whereas the presence of hexadecanal, octadecanal, and eicosanal was detected. In laboratory olfactometer tests, both Tr. erugatus and Te. podisi females were attracted to extracts of E. conspersus eggs, and to synthetic methyl (2E,4Z)-2,4-decadienoate. However, female Tr. erugatus and Te. podisi wasps were repelled, both by extracts of H. halys eggs and by a blend of the aldehydes identified from H. halys eggs. A follow-up field study, using hexane-washed and intact E. conspersus as sentinel eggs, showed that the parasitoids Trissolcus erugatus and Gryon obesum emerged from these eggs. Sentinel hexane-washed eggs treated with 3 ng of methyl (2E,4Z)-2,4-decadienoate were parasitized more by these two species than were hexane-washed or unwashed eggs, whereas hexane-washed eggs treated with a comparable dose of the C16,18,20 aldehyde mixture were avoided by these parasitoids. In a further field experiment, Trissolcus basalis was the primary parasitoid found in sticky traps baited with methyl (2E,4Z)-2,4-decadienoate, indicating that this species was attracted to, but either did not oviposit or develop in the E. conspersus sentinel eggs in the previous experiment.


Egg parasitoids Kairomones Biological control Octadecanal Methyl (2E,4Z)-2,4-decadienoate Hopkins’ host-selection principle Heteroptera Pentatomidae Scelionidae 



We thank Matthew Buffington, Elijah Talamas, and Michael Gates, USDA-ARS Systematic Entomology Laboratory, Washington, D.C., USA, for identifying the parasitoids. We also are grateful to Dr. Jocelia Grazia, Universidade Federal do Rio Grande do Sul, Brazil, for discussions on phylogenetics of the Pentatomidae. RT thanks the Coordination for the Improvement of Higher Education Personnel (CAPES) from Brazil for financial support, and JGM acknowledges support from Hatch Act project CA-R*-ENT-5181-H.


  1. Aldrich JR (1988) Chemical ecology of the Heteroptera. Annu Rev Entomol 33:211–238CrossRefGoogle Scholar
  2. Aldrich JR, Kochansky JP, Abrams CB (1984) Attractant for a beneficial insect and its parasitoids: pheromone of the predatory spined soldier bug, Podisus maculiventris (Hemiptera: Pentatomidae. Environ Entomol 13:1031–1036CrossRefGoogle Scholar
  3. Aldrich JR, Hoffmann MP, Kochansky JP, Lusby WR, Eger JE, Payne JA (1991) Identification and attractiveness of a major pheromone component for Nearctic Euschistus spp. stink bugs (Heteroptera: Pentatomidae. Environ Entomol 20:477–483CrossRefGoogle Scholar
  4. Aldrich JR, Oliver JE, Lusby WR, Kochansky JP, Borges M (1994) Identification of male-specific volatiles from Nearctic and Neotropical stink bugs (Heteroptera: Pentatomidae. J Chem Ecol 20:1103–1111CrossRefPubMedGoogle Scholar
  5. Ayres M, Ayres M Jr, Ayres D, Santos A (2007) BioEstat 5.0 Aplicações Estatísticas nas Áreas da Ciências Bio-médicas. Belém, Sociedade Civil Mamirauá. 339 pGoogle Scholar
  6. Barron AB (2001) The life and death of Hopkins’ host-selection principle. J Insect Behav 14:725–737CrossRefGoogle Scholar
  7. Bin F, Vinson SB, Strand MR, Colazza S, Jones WA (1993) Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula. Physiol Entomol 18:7–15CrossRefGoogle Scholar
  8. Blum MS (1974) Deciphering the communicative Rosetta stone. Bull Entomol Soc Amer 20:30–35CrossRefGoogle Scholar
  9. Borges M, Aldrich JR (1994) Attractant pheromone for Nearctic stink bug, Euschistus obscurus (Heteroptera: Pentatomidae): insight into a Neotropical relative. J Chem Ecol 20:1095–1102CrossRefPubMedGoogle Scholar
  10. Borges M, Costa MLM, Sujii E, Cavalcanti MDG, Redigolo G, Resck I, Vilela E (1999) Semiochemical and physical stimuli involved in host recognition by Telenomus podisi (hymenoptera: Scelionidae) toward Euschistus heros (Heteroptera: Pentatomidae. Physiol Entomol 24:227–233CrossRefGoogle Scholar
  11. Bruni R, Sant’Ana J, Aldrich JR, Bin F (2000) Influence of host pheromone on egg parasitism by scelionid wasps: Comparison of phoretic and non-phoretic parasitoids. J Insect Behavior 13:165–172CrossRefGoogle Scholar
  12. Cira TM, Venette RC, Aigner J, Kuhar T, Mullins DE, Gabbert SE, Hutchison W (2016) Cold tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) across geographic and temporal scales. Environ Entomol 45:484–491CrossRefPubMedGoogle Scholar
  13. Colazza S, McElfresh JS, Millar JG (2004) Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J Chem Ecol 30:945–964CrossRefPubMedGoogle Scholar
  14. Colazza S, Aquila G, De Pasquale C, Peri E, Millar JG (2007) The egg parasitoid Trissolcus basalis uses n-nonadecane, a cuticular hydrocarbon from its stink bug host Nezara viridula, to discriminate between female and male hosts. J Chem Ecol 33:1405–1420CrossRefPubMedGoogle Scholar
  15. Conti E, Colazza S (2012) Chemical Ecology of egg parasitoids associated with true bugs. Psyche 2012:11. doi: 10.1155/2012/651015 Google Scholar
  16. Corbet SA (1985) Insect chemosensory responses: a chemical legacy hypothesis. Ecol Entomol 10:143–153CrossRefGoogle Scholar
  17. Cribb BW, Siriwardana KN, Walter GH (2006) Unicellular pheromone glands of the pentatomid bug Nezara viridula (Heteroptera: Insecta): ultrastructure, classification, and proposed function. J Morphol 267:831–840CrossRefPubMedGoogle Scholar
  18. Cullen EM, Zalom FG (2005) Relationship between Euschistus conspersus (hem., Pentatomidae) pheromone trap catch and canopy samples in processing tomatoes. J Appl Entomol 129:505–514CrossRefGoogle Scholar
  19. Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689CrossRefGoogle Scholar
  20. Fogain R, Graff S (2011) First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Ontario and Quebec. J Entomol Soc Ontario 142:45–48Google Scholar
  21. Gariepy T, Bruin A, Haye T, Milonas P, Vétek G (2015) Occurrence and genetic diversity of new populations of Halyomorpha halys in Europe. J Pest Sci 88:451–460CrossRefGoogle Scholar
  22. Haye T, Fischer S, Zhang J, Gariepy T (2015) Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe? J Pest Sci 88:693–705CrossRefGoogle Scholar
  23. Herlihy MV, Talamas EJ, Weber DC (2016) Attack and success of native and exotic parasitoids on eggs of Halyomorpha halys in three Maryland habitats. PLoS One 11:e0150275CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stal) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237Google Scholar
  25. Hoffmann M, Davidson N, Wilson L, Ehler L, Jones W, Zalom F (1991) Imported wasp helps control southern green stink bug. Calif Agric 45:20–22Google Scholar
  26. Hopkins AD (1917) A discussion of C. G. Hewitt’s paper on “insect behaviour”. J Econ Entomol 10:92–93Google Scholar
  27. Inkley DB (2012) Characteristics of home invasion by the brown marmorated stink bug (Hemiptera: Pentatomidae. J Entomol Sci 47:125–130CrossRefGoogle Scholar
  28. Jeffries M, Lawton J (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286CrossRefGoogle Scholar
  29. Johnson NF (1984) Systematics of nearctic Telenomus: classification and revisions of the podisi and phymatae species groups (Hymenoptera: Scelionidae). Bull Ohio Biol Survey 6:1–113Google Scholar
  30. Joseph SV, Nita M, Leskey TC, Bergh JC (2015) Temporal effects on the incidence and severity of brown marmorated stink bug (Hemiptera: Pentatomidae) feeding injury to peaches and apples during the fruiting period in Virginia. J Econ Entomol 108:592–599CrossRefPubMedGoogle Scholar
  31. Khrimian A, Zhang A, Weber DC, Ho H-Y, Aldrich JR, Vermillion KE, Siegler MA, Shirali S, Guzman F, Leskey TC (2014) Discovery of the aggregation pheromone of the brown marmorated stink bug (Halyomorpha halys) through the creation of stereoisomeric libraries of 1-bisabolen-3-ols. J Nat Prod 77:1708–1717CrossRefPubMedGoogle Scholar
  32. Krupke CH, Brunner JF (2003) Parasitoids of the consperse stink bug (Hemiptera: Pentatomidae) in north Central Washington and attractiveness of a host-produced pheromone component. J Entomol Sci 38:84–92Google Scholar
  33. Lara J, Pickett C, Ingels C, Haviland D, Grafton-Cardwell E, Doll D, Bethke J, Faber B, Dara S, Hoddle M (2016) Biological control program is being developed for brown marmorated stink bug. Calif Agric 70:15–23CrossRefGoogle Scholar
  34. Laumann RA, Aquino MF, Moraes MC, Mn P, Borges M (2009) Response of the egg parasitoids Trissolcus basalis and Telenomus podisi to compounds from defensive secretions of stink bugs. J Chem Ecol 35:8–19CrossRefPubMedGoogle Scholar
  35. Lee D-H, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641CrossRefPubMedGoogle Scholar
  36. Mattiacci L, Vinson SB, Williams HJ, Aldrich JR, 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 19:1167–1181CrossRefPubMedGoogle Scholar
  37. McBrien HL, Millar JG, Rice RE, McElfresh JS, Cullen E, Zalom FG (2002) Sex attractant pheromone of the red-shouldered stink bug Thyanta pallidovirens: a pheromone blend with multiple redundant components. J Chem Ecol 28:1797–1818CrossRefPubMedGoogle Scholar
  38. Michereff M, Borges M, Aquino M, Laumann R, Mendes GA, Blassioli-Moraes M (2016) The influence of volatile semiochemicals from stink bug eggs and oviposition-damaged plants on the foraging behaviour of the egg parasitoid Telenomus podisi. Bull Entomol Res. doi: 10.1017/S0007485316000419 PubMedGoogle Scholar
  39. Millar JG (2005) Pheromones of true bugs. Topics Current Chem 240:37–84Google Scholar
  40. Palumbo JC, Perring TM, Millar JG, Reed DA (2016) Biology, ecology, and management of an invasive stink bug, Bagrada hilaris, in North America. Annu Rev Entomol 61:453–473CrossRefPubMedGoogle Scholar
  41. Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks CR, Jones A, Krawczyk G, Kuhar T, Martinson H, Mitchell W, Nielsen AL, Pfeiffer DG, Raupp MJ, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman NG, Leskey TC, Tooker JF (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manage 5:A1–A13. doi: 10.1603/IPM14002 CrossRefGoogle Scholar
  42. Rider D (2016) Pentatomoidea Home Page
  43. Salerno G, Frati F, Conti E, De Pasquale C, Peri E, Colazza S (2009) A finely tuned strategy adopted by an egg parasitoid to exploit chemical traces from host adults. J Exp Biol 212:1825–1831CrossRefPubMedGoogle Scholar
  44. Silva CC, Moraes MCB, Laumann RA, Borges M (2006) Sensory response of the egg parasitoid Telenomus podisi to stimuli from the bug Euschistus heros. Pesq Agropec Bras 41:1093–1098CrossRefGoogle Scholar
  45. Sithanantham S, Ballal CR, Jalali S, Bakthavatsalam N (2013) Biological control of insect pests using egg parasitoids. Springer, New DelhiCrossRefGoogle Scholar
  46. (2015) Where is BMSB?
  47. Taekul C, Valerio AA, Austin AD, Klompen H, Johnson NF (2014) Molecular phylogeny of telenomine egg parasitoids (Hymenoptera: Platygastridae s.l.: Telenominae): evolution of host shifts and implications for classification. Syst Entomol 39:24–35CrossRefGoogle Scholar
  48. Talamas E, Buffington M (2015) Fossil Platygastroidea in the National Museum of Natural History, Smithsonian Institution. J Hymenop Res 47:1–52CrossRefGoogle Scholar
  49. Talamas EJ, Herlihy MV, Dieckhoff C, Hoelmer KA, Buffington M, Bon M-C, Weber DC (2015a) Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America. J Hymenop Res 43:119–128CrossRefGoogle Scholar
  50. Talamas EJ, Johnson NF, Buffington M (2015b) Key to Nearctic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), natural enemies of native and invasive stink bugs (Hemiptera, Pentatomidae). J Hymenop Res 43:45–110CrossRefGoogle Scholar
  51. Tillman P (2010) Parasitism and predation of stink bug (Heteroptera: Pentatomidae) eggs in Georgia corn fields. Environ Entomol 39:1184–1194CrossRefPubMedGoogle Scholar
  52. Tillman PG (2011) Natural biological control of stink bug (Heteroptera: Pentatomidae) eggs in corn, peanut, and cotton farmscapes in Georgia. Environ Entomol 40:303–314CrossRefGoogle Scholar
  53. Tillman PG, Aldrich JR, Khrimian A, Cottrell TE (2010) Pheromone attraction and cross-attraction of Nezara, Acrosternum, and Euschistus spp. stink bugs (Heteroptera: Pentatomidae) in the field. Environ Entomol 39:610–617CrossRefPubMedGoogle Scholar
  54. Tillman PG, Greenstone MH, JS H (2015) Predation of stink bugs (Hemiptera: Pentatomidae) by a complex of predators in cotton and adjoining soybean habitats in Georgia, USA. Fla Entomol 98:1114–1126CrossRefGoogle Scholar
  55. Tognon R, Sant’Ana J, Jahnke SM (2013) Aprendizagem e memória de Telenomus podisi (Hymenoptera, Platygastridae). Iheringia, Série Zoologia, Porto Alegre 103:266–271CrossRefGoogle Scholar
  56. Tognon R, Sant’Ana J, Jahnke S (2014) Influence of original host on chemotaxic behaviour and parasitism in Telenomus podisi Ashmead (hymenoptera: Platygastridae. Bull Entomol Res 104:781–787CrossRefPubMedGoogle Scholar
  57. Vet LE, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172CrossRefGoogle Scholar
  58. Weber CA, Smilanick JM, Ehler LE, Zalom FG (1996) Ovipositional behavior and host discrimination in three scelionid egg parasitoids of stink bugs. Biol Control 6:245–252CrossRefGoogle Scholar
  59. Weber DC, Walsh GC, DiMeglio AS, Athanas MM, Leskey TC, Khrimian A (2014) Attractiveness of harlequin bug, Murgantia histrionica, aggregation pheromone: field response to isomers, ratios, and dose. J Chem Ecol 40:1251–1259CrossRefPubMedGoogle Scholar
  60. Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitteliungen der Schweizerischen Entomologischen Gesellschaft 81:1–8Google Scholar
  61. Zalom FG, Smilanick JM, Ehler L (1997) Fruit damage by stink bugs (Hemiptera: Pentatomidae) in bush-type tomatoes. J Econ Entomol 90:1300–1306CrossRefGoogle Scholar
  62. Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS One 7:31246CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Roberta Tognon
    • 1
  • Josué Sant’Ana
    • 1
  • Qing-He Zhang
    • 2
  • Jocelyn G. Millar
    • 3
  • Jeffrey R. Aldrich
    • 4
    • 5
  • Frank G. Zalom
    • 5
  1. 1.PPG-Fitotecnia, Faculdade de AgronomiaUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Sterling International, Inc.SpokaneUSA
  3. 3.Department of EntomologyUniversity of CaliforniaRiversideUSA
  4. 4.Jeffrey R. Aldrich Consulting LLCSanta CruzUSA
  5. 5.Department of Entomology and NematologyUniversity of CaliforniaDavisUSA

Personalised recommendations