Journal of Insect Behavior

, Volume 29, Issue 6, pp 643–665 | Cite as

Vibratory Communication and its Relevance to Reproductive Isolation in two Sympatric Stink Bug Species (Hemiptera: Pentatomidae: Pentatominae)

  • Raul A. Laumann
  • Andrej Čokl
  • Maria Carolina Blassioli-Moraes
  • Miguel Borges


Communication is in phytophagous stink bugs of the subfamily Pentatominae related to mating behavior that among others includes location and recognition of the partner during calling and courting. Differences in temporal and frequency parameters of vibratory signals contributes to species reproductive isolation. Chinavia impicticornis and C. ubica are two green Neotropical stink bugs that live and mate on the same host plants. We tested the hypothesis that differences in temporal and spectral characteristics of both species vibratory signals enable their recognition to that extent that it interrupts further interspecific communication and copulation. To confirm or reject this hypothesis we monitored both species mating behaviour and recorded their vibratory songs on the non-resonant loudspeaker membranes and on the plant. The level of interspecific vibratory communication was tested also by playback experiments. Reproductive behavior and vibratory communication show similar patterns in both Chinavia species. Differences observed in temporal and spectral characteristics of female and male signals enable species discrimination by PCA analyses. Insects that respond to heterospecific vibratory signals do not step forward to behaviors leading to copulation. Results suggest that species isolation takes place in both investigated Chinavia species at an early stage of mating behavior reducing reproductive interference and the probability of heterospecific mating.


Chinavia mate system multimodal communication reproductive interference pheromone vibratory signals 



The authors are grateful to Samantha da Silveira for technical support with insect rearing and playback experiments and colleague from The National Institute of Biology in Ljubljana and from the Semiochemical Laboratory, EMBRAPA Genetic Resources and Biotechnology in Brasilia for fruitful discussion with comments on the manuscript. We also thank two anonymous reviewers for their useful comments that help to improve first version of the manuscript. This work received financial support from Slovenian Research Agency, program number: P1-0255, project number: BI-BR/12-12/002 and CNPq-MHNEST 40245/2011-0. FAP-DF project 193.000.023-2012 and Embrapa.

Supplementary material

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  1. Aldrich JR (1988) Chemical ecology of the Heteroptera. Annu Rev Entomol 33:211–238CrossRefGoogle Scholar
  2. Aldrich JR, Oliver JE, Lusby WR, Kochhar TS, Lockwood JA (1987) Pheromone strains of the cosmopolitan pest, Nezara viridula (Heteroptera: Pentatomidae). J Exp Zool 244:171–175CrossRefGoogle Scholar
  3. Baker R, Borges M, Cooke NG, Herbert RH (1987) Identification and synthesis of (Z)-(1'S,3'R,4'S)(−)-2-(3',4'-epoxy-4'-methylcyclohexyl)-6-methylhepta-2,5-diene, the sex pheromone of the southern green stink bug, Nezara viridula (L.). J Chem Soc Chem Commun 6:414–416CrossRefGoogle Scholar
  4. Blassioli-Moraes MCB, Laumann RA, Čokl A, Borges M (2005) Vibratory signals of four Neotropical stink bug species. Physiol Entomol 30:175–188CrossRefGoogle Scholar
  5. Blassioli-Moraes MCB, Pareja M, Laumann RA, Borges, M (2008) The chemical volatiles (Semiochemicals) produced by neotropical stink bugs (Hemiptera: Pentatomidae) Neotrop Entomol 37:489–505Google Scholar
  6. Blassioli-Moraes MC, Laumann RA, Oliveira MWM, Woodcock CM, Mayon P, Hooper A, Pickett JA, Birkett MA, Borges M (2012) Sex pheromone communication in two sympatric Neotropical stink bug species Chinavia ubica and Chinavia impicticornis. J Chem Ecol 38:836–845CrossRefPubMedGoogle Scholar
  7. Blassioli-Moraes MC, Magalhães DM, Čokl A, Laumann RA, Silva JP, Cleonor Silva CCA, Borges M (2014) Vibrational communication and mating behavior of Dichelops melacanthus (Hemiptera: Pentatomidae) recorded from loudspeaker membranes and plants. Physiol Entomol 39:1–11CrossRefGoogle Scholar
  8. Borges M, Jepson P, Howse P (1987) Long-range mate location and close-range courtship behaviour of the green stink bug, Nezara viridula and its mediation by sex pheromones. Entomol Exp Appl 44:205–212CrossRefGoogle Scholar
  9. Broughton WB (1963) Methods in bio-acoustic terminology. In: Busnel RG (ed) Acoustic Behaviour of Animals.: Elsevier Publishing Company, Amsterdam-London-New York, pp 3–24Google Scholar
  10. Claridge MF, Morgan JC (1993) Geographical variation in acoustic signals of the planthopper, Nilaparvata bakeri (Muir), in Asia: species recognition and sexual selection. Biol J Linn Soc 48:267–281CrossRefGoogle Scholar
  11. Claridge MF, Den Hollander J, Morgan JC (1985) The status of weed-associated populations of the brown planthopper, Nilaparuata lugens (Stål)-host race or biological species? Zool J Linnean Soc 84:77–90CrossRefGoogle Scholar
  12. Claridge MF, Den Hollander J, Morgan JC (1988) Variation in host plant relations and courtship signals of weed-associated populations of the brown planthopper, Nilaparuata lugens (Stål), from Australia and Asia: a test of the recognition species concept. Biol J Linn Soc 35:79–93CrossRefGoogle Scholar
  13. Cocroft RB, Rodrígues RL (2005) The behavioural ecology of insect vibrational communication. Biosci 55:323–334CrossRefGoogle Scholar
  14. Cocroft RB, Rodríguez RL, Hunt RE (2010) Host shifts and signal divergence: mating signals covary with host use in a complex of specialized plant-feeding insects. Biol J Linn Soc 99:60–72CrossRefGoogle Scholar
  15. Čokl A (2008) Stink bug interaction with host plants during communication. J Insect Physiol 54:1113–1124CrossRefPubMedGoogle Scholar
  16. Čokl A, Virant-Doberlet M (2003) Communication with substrate-borne signals in small plant-dwelling insects. Annu Rev Entomol 48:29–50CrossRefPubMedGoogle Scholar
  17. Čokl A, Virant Doberlet M, Stritih N (2000) The structure and function of songs emitted by southern green stink bugs from Brazil, Florida, Italy and Slovenia. Physiol Entomol 25:1–10CrossRefGoogle Scholar
  18. Čokl A, McBrien H, Millar JG (2001) Comparison of substrate-borne vibrational signals of two stink bugs species, Acrosternum hilare and Nezara viridula (Heteroptera: Pentatomidae). Ann Entomol Soc Am 94:71–479CrossRefGoogle Scholar
  19. Čokl A, Zorović M, Žunič Kosi A, Stritih N, Virant-Doberlet M (2014) Communication through plants in a narrow frequency window. In: Cocroft RB, Gogala M, hill PSM, Wessel a, (eds)studying vibrational communication. Springer, Heidelberg, New York, Dordercht, London, pp. 171–189Google Scholar
  20. Čokl A, Laumann RA, Žunič Kosi A, Blassioli-Moraes MC, Virant-Doberlet M, Borges M (2015) Interference of overlapping insect vibratory communication signals: an Eushistus heros model. PLoS One 10(6):e0130775. doi: 10.1371/journal.pone.0130775 CrossRefPubMedPubMedCentralGoogle Scholar
  21. de Groot M, Čokl A, Virant-Doberlet M (2010) Effects of heterospecific and conspecific vibrational signal overlap and signal-to-noise ratio on male responsiveness in Nezara viridula (L.). J Exp Biol 213:3213–3222CrossRefPubMedGoogle Scholar
  22. Den Bieman CFM (1986) Acoustic differentiation and variation in planthoppers of the genus Ribautodelphax (Homoptera, Delphacidae). Neth J Zool 36:461–480CrossRefGoogle Scholar
  23. Dobler S, Stumpner A, Heller KG (1994) Sex-specific spectral tuning for the partner’s song in the duetting bush-cricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Com Physiol A 175:303–310Google Scholar
  24. Endler JA (1993) Some general comments on the evolution and design of animal communication systems. Philos Trans R Soc Lond Ser B Biol Sci 340:215–225CrossRefGoogle Scholar
  25. Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931CrossRefGoogle Scholar
  26. Forrest TG, Lajoie DR, Cusick D (2006) Calling songs, duets, and auditory tuning in two cryptic katydids (Tettigoniidae: Phaneropterinae: Amblycorypha). Ann Entomol Soc Am 99:978–987CrossRefGoogle Scholar
  27. Greenfield MD (2002) Signals and receivers. Mechanism and evolution of arthropod communication. Oxford University Press, New YorkGoogle Scholar
  28. Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282CrossRefPubMedGoogle Scholar
  29. Haccou P, Meelis E (1992) Statistical analysis of behavioural data: an approach based on time-structured models. Oxford University Press, OxfordGoogle Scholar
  30. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Pal Elect 4:1–9 Available at Google Scholar
  31. Harris VE, Todd JW (1980) Temporal and numerical patterns of reproductive behavior in the southern green stink bug, Nezara viridula (Hemiptera: Pentatomidae). Entomol Exp Appl 27:105–116CrossRefGoogle Scholar
  32. Higuchi H (1992) Population prevalence of occurrence and spatial distribution pattern of Piezodorus hybneri adults (Heteroptera: Pentatomidae) on soybeans. Appl Entomol Zool 27:363–369Google Scholar
  33. Kirkpatrick M, Ravigne V (2002) Speciation by natural and sexual selection: models and experiments. Am Nat 159:S22–S35CrossRefPubMedGoogle Scholar
  34. Kon M, Oe A, Numata H, Hidaka T (1988) Comparison of the mating behaviour between two sympatric species, Nezara viridula and N. antennata (Heteroptera: Pentatomidae), with special reference to sound emission. J Ethol 6:91–98CrossRefGoogle Scholar
  35. Kon M, Oe A, Numata H (1993) Intra- and interspecific copulations in the two congeneric green stink bugs, Nezara antennata and N. viridula (Heteroptera, Pentatomidae), with reference to postcopulatory changes in the spermatheca. J Ethol 11:83–89CrossRefGoogle Scholar
  36. Kon M, Oe A, Numata H (1994) Ethological isolation between two congeneric green stink bugs, Nezara antennata and N. viridula (Heteroptera, Pentatomidae). J Ethol 12:67–71CrossRefGoogle Scholar
  37. Laumann RA, Kavčič A, Moraes MCB, Borges M, Čokl A (2013) Reproductive behaviour and vibratory communication of the neotropical predatory stink bug Podisus nigrispinus. Physiol Entomol 38:71–80CrossRefGoogle Scholar
  38. McBrien HL, Millar JG (2003) Substrate-borne vibrational signalling in the consperse stink bug, Euschistus conspersus. Can Entomol 135:555–567CrossRefGoogle Scholar
  39. McBrien HL, Millar JG, Gottlieb L, Chen X, Rice RE (2001) Male-produced sex attractant pheromone of the green stink bug, Acrosternum hilare (say). J Chem Ecol 27:1821–1839CrossRefPubMedGoogle Scholar
  40. Mendelson TC, Shaw KL (2002) Genetic and behavioural components of the cryptic species boundary between Laupala cerasina and L. kohalensis (Orthoptera: Gryllidae). Genet 116:301–310CrossRefGoogle Scholar
  41. Mendelson TC, Shaw KL (2012) The (mis) conception of species recognition. Trends Ecol Evol 27:421–427CrossRefPubMedGoogle Scholar
  42. Miklas N, Čokl A, Renou M, Virant-Doberlet M (2003) Variability of vibratory signals and mate choice selectivity in the southern green stink bug. Behav Process 61:131–142CrossRefGoogle Scholar
  43. Panizzi AR, McPherson JE, James DG, Javahery M, McPherson RM (2000) Economic importance of stink bugs (Pentatomidae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, Florida, pp. 421–474Google Scholar
  44. Polajnar J, Čokl A (2008) The effect of vibratory disturbance on sexual behaviour of the southern green stink bug Nezara viridula (Heteroptera, Pentatomidae). Cen Eur J Biol 3:189–197Google Scholar
  45. Ritchie MG (1996) The shape of female mating preferences. Proc Natl Acad Sci U S A 93:14628–14631CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102CrossRefGoogle Scholar
  47. Ritchie MG, Halsey EJ, Gleason JM (1999) Drosophila Song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster Song. Anim Behav 58:649–657CrossRefPubMedGoogle Scholar
  48. Rodríguez RL, Cocroft RB (2006) Divergence in female duetting signals in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Ethol 112:1231–1238CrossRefGoogle Scholar
  49. Rodríguez RL, Sullivan LE, Cocroft RB (2004) Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Evol 58:571–578CrossRefGoogle Scholar
  50. Rodriguez RL, Ramaswamy K, Cocroft RB (2006) Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects. Proc R Soc B Biol Sci 273:2585–2593CrossRefGoogle Scholar
  51. Roggia RCRK (2009) Spatial and temporal distribution of soybean stink bug and behaviour of Piezodorus guildinii (Westwood, 1837) (Hemiptera: Pentatomidae) on soybean (Glycine max (L.) on day time. Doctoral Thesis, Universidade Federal de Santa MariaGoogle Scholar
  52. Ryan RJ, Rand AS (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evol 47:647–657CrossRefGoogle Scholar
  53. Schwertner CF, Grazia JO (2007) O gênero Chinavia Orian (Hemiptera, Pentatomidae, Pentatominae) no Brasil, com chave pictórica para os adultos. Rev Bras Entomol 51:416–435CrossRefGoogle Scholar
  54. Scott-Philips TC (2008) Defining biological communication. J Evol Biol 21:387–395CrossRefGoogle Scholar
  55. Seyfarth RM, Cheney DL, Bergman T, Fischer J, Zuberbühler K, Hammerschmidt K (2010) The central importance of information in studies of animal communication. Anim Behav 80:3–8CrossRefGoogle Scholar
  56. Shestakov LS (2015) A comparative analysis of vibrational signals in 16 sympatric species (Pentatomidae, Heteroptera). Entomol Rev 95:310–325CrossRefGoogle Scholar
  57. Silva CCA, Laumann RA, Ferreira JBC, Blassioli-Moraes MC, Borges M, Čokl A (2012) Reproductive Biology, mating Behavior, and Vibratory Communication of the Brown-winged Stink Bug, Edessa meditabunda (Fabr.) (Heteroptera: Pentatomidae). Psyche 2012: 1–9. doi:nnn10.1155/2012/598086Google Scholar
  58. Silva CC, Laumann RA, Blassioli-Moraes MC, Aquino MFS, Borges M (2015) Comparative biology of two congeneric stinkbugs, Chinavia impicticornis and C. ubica (Hemiptera: Pentatomidae) Pesq Agropec Bras 50:355–362Google Scholar
  59. Tillman PG, Northfield TD, Mizell RF, Riddle TC (2009) Spatiotemporal patterns and dispersal of stink bugs (Heteroptera: Pentatomidae) in peanut-cotton farmscapes. Environ Entomol 38:1038–1052CrossRefPubMedGoogle Scholar
  60. Vignal C, Kelley D (2007) Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis. Proc R Soc B Biol Sci 274:479–488CrossRefGoogle Scholar
  61. Wang Q, Millar JG (1997) Reproductive behavior of Thyanta pallidovirens (Heteroptera: Pentatomidae). Ann Entomol Soc Am 90:380–388CrossRefGoogle Scholar
  62. West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183CrossRefGoogle Scholar
  63. Zahn DK, Girling RD, McElfresh JS, Cardé RT, Millar JG (2008) Biology and reproductive behavior of Murgantia histrionica (Heteroptera: Pentatomidae). Ann Entomol Soc Am 101:215–228CrossRefGoogle Scholar
  64. Žunič A, Čokl A, Virant-Doberlet M, Millar J (2008) Communication with signals produced by abdominal vibration, tremulation and percussion in Podisus maculiventris (Heteroptera: Pentatomidae). Ann Entomol Soc Am 101:1169–1178CrossRefGoogle Scholar
  65. Žunič A, Virant-Doberlet M, Čokl A (2011) Species recognition during substrate-borne communication in Nezara viridula (L.) (Pentatomidae: Heteroptera). J Insect Behav 24:468–487CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Raul A. Laumann
    • 1
  • Andrej Čokl
    • 2
  • Maria Carolina Blassioli-Moraes
    • 1
  • Miguel Borges
    • 1
  1. 1.Semiochemicals LaboratoryEmbrapa Genetic Resources and BiotechnologyBrasíliaBrazil
  2. 2.Department of Organisms and EcosystemsNational Institute of BiologyLjubljanaSlovenia

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