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

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Abstract

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.

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References

  • Aldrich JR (1988) Chemical ecology of the Heteroptera. Annu Rev Entomol 33:211–238

    Article  Google Scholar 

  • Aldrich JR, Oliver JE, Lusby WR, Kochhar TS, Lockwood JA (1987) Pheromone strains of the cosmopolitan pest, Nezara viridula (Heteroptera: Pentatomidae). J Exp Zool 244:171–175

    Article  CAS  Google Scholar 

  • 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 6:414–416

    Article  Google Scholar 

  • Blassioli-Moraes MCB, Laumann RA, Čokl A, Borges M (2005) Vibratory signals of four Neotropical stink bug species. Physiol Entomol 30:175–188

    Article  Google Scholar 

  • Blassioli-Moraes MCB, Pareja M, Laumann RA, Borges, M (2008) The chemical volatiles (Semiochemicals) produced by neotropical stink bugs (Hemiptera: Pentatomidae) Neotrop Entomol 37:489–505

  • 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 38:836–845

    Article  CAS  PubMed  Google Scholar 

  • 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 39:1–11

    Article  Google Scholar 

  • 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 44:205–212

    Article  CAS  Google Scholar 

  • Broughton WB (1963) Methods in bio-acoustic terminology. In: Busnel RG (ed) Acoustic Behaviour of Animals.: Elsevier Publishing Company, Amsterdam-London-New York, pp 3–24

  • 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 48:267–281

    Article  Google Scholar 

  • 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 84:77–90

    Article  Google Scholar 

  • 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 35:79–93

    Article  Google Scholar 

  • Cocroft RB, Rodrígues RL (2005) The behavioural ecology of insect vibrational communication. Biosci 55:323–334

    Article  Google Scholar 

  • 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 99:60–72

    Article  Google Scholar 

  • Čokl A (2008) Stink bug interaction with host plants during communication. J Insect Physiol 54:1113–1124

    Article  PubMed  Google Scholar 

  • Čokl A, Virant-Doberlet M (2003) Communication with substrate-borne signals in small plant-dwelling insects. Annu Rev Entomol 48:29–50

    Article  PubMed  Google Scholar 

  • 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 25:1–10

    Article  Google Scholar 

  • 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 94:71–479

    Article  Google Scholar 

  • 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. 171–189

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 213:3213–3222

    Article  PubMed  Google Scholar 

  • Den Bieman CFM (1986) Acoustic differentiation and variation in planthoppers of the genus Ribautodelphax (Homoptera, Delphacidae). Neth J Zool 36:461–480

    Article  Google Scholar 

  • 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 175:303–310

    Google Scholar 

  • Endler JA (1993) Some general comments on the evolution and design of animal communication systems. Philos Trans R Soc Lond Ser B Biol Sci 340:215–225

    Article  CAS  Google Scholar 

  • Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931

    Article  Google Scholar 

  • Forrest TG, Lajoie DR, Cusick D (2006) Calling songs, duets, and auditory tuning in two cryptic katydids (Tettigoniidae: Phaneropterinae: Amblycorypha). Ann Entomol Soc Am 99:978–987

    Article  Google Scholar 

  • Greenfield MD (2002) Signals and receivers. Mechanism and evolution of arthropod communication. Oxford University Press, New York

    Google Scholar 

  • Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282

    Article  PubMed  Google Scholar 

  • Haccou P, Meelis E (1992) Statistical analysis of behavioural data: an approach based on time-structured models. Oxford University Press, Oxford

    Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Pal Elect 4:1–9 Available at http://palaeo-electronica.org/2001_1/past/issue1_01.htm

    Google Scholar 

  • 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 27:105–116

    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 

  • Kirkpatrick M, Ravigne V (2002) Speciation by natural and sexual selection: models and experiments. Am Nat 159:S22–S35

    Article  PubMed  Google Scholar 

  • 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 6:91–98

    Article  Google Scholar 

  • 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 11:83–89

    Article  Google Scholar 

  • Kon M, Oe A, Numata H (1994) Ethological isolation between two congeneric green stink bugs, Nezara antennata and N. viridula (Heteroptera, Pentatomidae). J Ethol 12:67–71

    Article  Google Scholar 

  • 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 38:71–80

    Article  Google Scholar 

  • McBrien HL, Millar JG (2003) Substrate-borne vibrational signalling in the consperse stink bug, Euschistus conspersus. Can Entomol 135:555–567

    Article  Google Scholar 

  • 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 27:1821–1839

    Article  CAS  PubMed  Google Scholar 

  • Mendelson TC, Shaw KL (2002) Genetic and behavioural components of the cryptic species boundary between Laupala cerasina and L. kohalensis (Orthoptera: Gryllidae). Genet 116:301–310

    Article  CAS  Google Scholar 

  • Mendelson TC, Shaw KL (2012) The (mis) conception of species recognition. Trends Ecol Evol 27:421–427

    Article  PubMed  Google Scholar 

  • 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 61:131–142

    Article  Google Scholar 

  • 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. 421–474

    Google Scholar 

  • 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 3:189–197

    Google Scholar 

  • Ritchie MG (1996) The shape of female mating preferences. Proc Natl Acad Sci U S A 93:14628–14631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102

    Article  Google Scholar 

  • 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 58:649–657

    Article  PubMed  Google Scholar 

  • Rodríguez RL, Cocroft RB (2006) Divergence in female duetting signals in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Ethol 112:1231–1238

    Article  Google Scholar 

  • Rodríguez RL, Sullivan LE, Cocroft RB (2004) Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Evol 58:571–578

    Article  Google Scholar 

  • 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 273:2585–2593

    Article  Google Scholar 

  • 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 Maria

  • Ryan RJ, Rand AS (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evol 47:647–657

    Article  Google Scholar 

  • Schwertner CF, Grazia JO (2007) O gênero Chinavia Orian (Hemiptera, Pentatomidae, Pentatominae) no Brasil, com chave pictórica para os adultos. Rev Bras Entomol 51:416–435

    Article  Google Scholar 

  • Scott-Philips TC (2008) Defining biological communication. J Evol Biol 21:387–395

    Article  Google Scholar 

  • 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 80:3–8

    Article  Google Scholar 

  • Shestakov LS (2015) A comparative analysis of vibrational signals in 16 sympatric species (Pentatomidae, Heteroptera). Entomol Rev 95:310–325

    Article  Google Scholar 

  • 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:nnn10.1155/2012/598086

  • 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 50:355–362

  • 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 

  • Vignal C, Kelley D (2007) Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis. Proc R Soc B Biol Sci 274:479–488

    Article  Google Scholar 

  • Wang Q, Millar JG (1997) Reproductive behavior of Thyanta pallidovirens (Heteroptera: Pentatomidae). Ann Entomol Soc Am 90:380–388

    Article  Google Scholar 

  • West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183

    Article  Google Scholar 

  • Zahn DK, Girling RD, McElfresh JS, Cardé RT, Millar JG (2008) Biology and reproductive behavior of Murgantia histrionica (Heteroptera: Pentatomidae). Ann Entomol Soc Am 101:215–228

    Article  Google Scholar 

  • 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 101:1169–1178

    Article  Google Scholar 

  • Žunič A, Virant-Doberlet M, Čokl A (2011) Species recognition during substrate-borne communication in Nezara viridula (L.) (Pentatomidae: Heteroptera). J Insect Behav 24:468–487

    Article  Google Scholar 

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Acknowledgments

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.

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Correspondence to Raul A. Laumann.

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Laumann, R.A., Čokl, A., Blassioli-Moraes, M.C. et al. Vibratory Communication and its Relevance to Reproductive Isolation in two Sympatric Stink Bug Species (Hemiptera: Pentatomidae: Pentatominae). J Insect Behav 29, 643–665 (2016). https://doi.org/10.1007/s10905-016-9585-x

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