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Stink Bug Inter-Plant Communication with Signals Produced by Vibration of Lifted Wings

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Abstract

Stink bugs communicate while mating on a plant by means of the substrate-borne component of the species and sex-specific calling, courtship and rival signals, produced by vibration of the abdomen. Courtship conducted over a close visual distance, chemical contact and mechanical exchange of information terminates in copulation. Here we describe characteristics, differences between species, transmission properties and the behavioral context of the stink bugs Chinavia impicticornis, C. ubica and Euschistus heros in relation to their buzzing signals, produced by vibration of lifted wings. Comparison between species reveals their species’ non-specific temporal parameters, characterized by irregular repetition rate and highly variable duration. Frequency spectral bands extend to several kHz above approximately 100 Hz, which is the fundamental frequency and significantly higher in E. heros compared with both Chinavia species. Buzzing signals, recorded predominantly in the very early phase of mating behavior, precede emission of signals produced by abdomen vibration. Males and females emit signals spontaneously when alone on a plant or together with conspecific or alien species mates. Transmission of wing-produced signals along the plant shows characteristics similar to those produced by abdomen vibration. We suggest that amplitudes, measured on distant plants in direct contact or through soil and roots, together with the high sensitivity of relevant vibrational receptors, enable stink bugs to communicate between plants, using substrate-borne vibratory signals outside the limits of the single plant.

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References

  • Aldrich JR, Oliver JE, Lusby WR, Kochansky JP, 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 D 6:414–416

    Google Scholar 

  • Barth FG (2002) A spider world: senses and behavior. Springer, Berlin

    Book  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 

  • Borges M, Jepson PC, Howse PE (1987) Long-range mate location and close range courtship behavior of the green stink bug, Nezara viridula and its mediation by sex pheromones. Entomol Exp Appl 44:205–212

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Borges M, Aldrich JR (1994) Attractant pheromone for Nearctic stink bug, Euschistus obscurus (Heteroptera: Pentatomidae): insight into a Neotropical relative. J Chem Ecol 20:1095–1102

    Article  CAS  PubMed  Google Scholar 

  • Borges M, Blassioli-Moraes MC (2017) The semiochemistry of Pentatomidae in stinkbugs. In: Čokl A, Borges M (eds) Biorational control based on communication processes, 1st edn. CRC Press Taylor & Francis Group, Boca Raton London New York, pp 95–124

    Chapter  Google Scholar 

  • Broughton WB (1963) Methods in bioacoustic terminology. In: Busnel R-G (ed) Acoustic behaviour of animals, 1st edn. Elsevier Publishing Company, Amsterdam London New York, pp 3–24

    Google Scholar 

  • Claridge M (2006) Insect sounds and communication—an introduction. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behavior, ecology and evolution, 1st edn. CRC Press Taylor & Francis Group, Boca Raton, pp 3–10

    Google Scholar 

  • Cocroft RB, Rodriguez RL (2005) The behavioral ecology of insect vibrational communication. Bioscience 55:323–334

    Article  Google Scholar 

  • Conchou L, Lucas P, Meslin C, Proffit M, Staudt M, Renou M (2019) Insect odorscapes: from plant volatiles to natural olfactory scenes. Front Physiol 10:972

    Article  PubMed  PubMed Central  Google Scholar 

  • Costa MLM, Borges M, Vilela EF (1998) Biologia reprodutiva de Euschistus heros (F.) (Heteroptera: Pentatomidae). An Soc Ent Bras 27:559–568

    Article  Google Scholar 

  • Crossley SA (1986) Courtship sounds and behavior of the four species of the Drosophila bipunctata complex. Anim Behav 34:1146–1159

    Article  Google Scholar 

  • Čokl A (1983) Functional properties of vibroreceptors in the legs of Nezara viridula (L.) (Heteroptera, Pentatomidae). J Comp Physiol 150:261–269

    Article  Google Scholar 

  • Čokl A, Zorović M, Žunič A, Virant-Doberlet M (2005) Tuning of host plants with vibratory songs of Nezara viridula (Heteroptera: Pentatomidae). J Exp Biol 208:1481–1488

    Article  PubMed  Google Scholar 

  • Čokl A, Nardi C, Bento JMS, Hirose E, Panizzi AR (2006) Transmission of stridulatory signals of the burrower bugs, Scaptocoris castanea and Scaptocoris carvalhoi (Heteroptera: Cydnidae) through the soil and soybean. Physiol Entomol 31:371–438

    Article  Google Scholar 

  • Čokl A, Zorović M, Millar JG (2007) Vibrational communication along plants by the stink bugs Nezara viridula and Murgantia histrionica. Behav Process 75:40–54

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Čokl A, Zorović M, Žunič A, Stritih N, Virant-Doberlet M (2014) Communication through plants in a narrow frequency window. In: Cocroft RG, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational behavior, 1st edn. Springer, Berlin, pp 1712–2195

    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 Euschistus heros model. PLoS ONE 10:1–16

    Article  CAS  Google Scholar 

  • Čokl A, Laumann RA, Stritih N (2017) Substrate-borne vibratory communication. In: Čokl A, Borges M (eds) Biorational control based on communication processes, 1st edn. CRC Press Taylor and Francis Group, Boca Raton London New York, pp 125–164

    Chapter  Google Scholar 

  • Čokl A, Moreira Dias A, Blassioli-Moraes MC, Borges M, Laumann RA (2017) Rivalry between stink bug females in a vibrational communication network. J Insect Behav 30:741–758

    Article  Google Scholar 

  • Čokl A, Blassioli-Moraes MC, Laumann RA, Žunič A, Borges M (2019) Stinkbugs—multisensory communication with chemical and vibratory signals transmitted through different media. In: Hill PSM, Lakes-Harlan R, Mazzoni V, Narins PM, Virant-Doberlet M, Wessel A (eds) Biotremology—studying vibrational behavior, 1st edn. Springer, New York, pp 91–122

    Chapter  Google Scholar 

  • Čokl A, Žunič A, Laumann RA, Virant-Doberlet M (2020) Female competition for availability for males in insects: the Nezara viridula (Linnaeus, 1758) model. Insect Sci 27:804–814

    Article  Google Scholar 

  • Duelli P, Johnson JB (1982) Behavioral organ of tremulation and possible stridulation, in green lacewings (Neuroptera: Chrysopidae). Psyche 88:375–381

    Article  Google Scholar 

  • Eben A, Mühlethaler R, Gross J, Hoch H (2015) First evidence of acoustic communication in the pear psyllid Cacopsylla pyri L. (Hemiptera: Psyllidae). J Pest Sci 88:87–95

    Article  Google Scholar 

  • Eriksson A, Anfora G, Lucchi A, Virant-Doberlet M, Mazzoni V (2011) Inter-plant vibrational communication in a leafhopper insect. PLoS ONE 6:1–6

    Article  Google Scholar 

  • Esch H, Wilson D (1967) The sounds produced by flies and bees. Z Vergl Physiol 54:256–267

    Article  Google Scholar 

  • Ewing AW (1989) Mechanisms of sound production. In: Ewing AW (ed) Arthropod bioacoustics, 1st edn. Edinburg University Press, Edinburg, pp 17–57

    Google Scholar 

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

    Article  Google Scholar 

  • Gnazy W, Hausslein R (1986) Digger wasp against crickets I Receptors involved in the antipredator strategies of the prey. Naturwissenschaften 73:212–215

    Article  Google Scholar 

  • Gogala M (2006) Vibratory signals produced by Heteroptera. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology and evolution, 1st edn. CRC Press Taylor & Francis Group, Boca Raton London New York, pp 275–296

    Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Hoikkala A (2006) Inheritance of male sound characteristics in Drosophila species. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology and evolution, 1st edn. CRC Press Taylor & Francis Group, Boca Raton London New York, pp 167–177

    Google Scholar 

  • Hrncir M, Gravel AI, Schorkopf DLP, Schmidt VM, Zucchi R, Barth FG (2008) Thoracic vibrations in stingless bees (Melipona seminigra): resonances of the thorax influence vibrations associated with flight but not those associated with sound production. J Exp Biol 211:678–685

    Article  PubMed  Google Scholar 

  • Hrncir M, Schorkopf DLP, Schmidt VM, Zucchi R, Barth FG (2008) The sound field generated by tethered stingless bees (Melipona scutellaris): inferences on its potential as a recruitment mechanism inside the hive. J Exp Biol 211:686–698

    Article  PubMed  Google Scholar 

  • Hrncir M (2009) Mobilizing the foraging force—mechanical signals in stingless bee recruitment. In: Jarau S, Hrncir M (eds) Food exploitation by social insects- ecological, behavioral, and theoretical approaches, 1st edn. CRC Press Taylor & Francis Group, Boca Raton, pp 199–221

    Chapter  Google Scholar 

  • Hrncir M, Barth FG (2014) Vibratory communication in stingless bees (Meliponini): the challenge of interpreting the signals. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication, 1st edn. Springer, Heidelberg New York Dordrecht London, pp 349–374

    Chapter  Google Scholar 

  • Kavčič A, Čokl A, Laumann RA, Moraes MCB, Borges M (2013) Tremulatory and abdomen vibration signals enable communication through air in the stink bug Eushistus heros. PLoS ONE 8:1–10

    Article  CAS  Google Scholar 

  • Kon M, Oe A, Numata H, Hidaka T (1988) Comparison of the mating behaviour between the sympatric species Nezara antennata and N. viridula (Heteroptera: Pentatomidae) with special reference to sound emission. J Ethol 6:91–98

    Article  Google Scholar 

  • Kuštor V (1989) Activity of muscles of the vibration producing organ of the bug Nezara viridula. MSc Thesis, University of Ljubljana Slovenia

  • Larsen O, Gleffe G, Tengö J (1986) Vibration and sound communication in solitary bees and wasps. Physiol Entomol 11:287–296

    Article  Google Scholar 

  • Laumann RA, Kavčič A, Blassioli Moraes MC, 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 

  • Laumann RA, Čokl A, Blassioli-Moraes MC, Borges M (2016) Vibratory communication and its relevance to reproductive isolation in two sympatric stink bug species (Hemiptera: Pentatomidae: Pentatominae). J Insect Behav 29:643–665

    Article  Google Scholar 

  • Liao Y-C, Yang M-M (2015) Acoustic communication of three closely related psyllid species: a case study in clarifying allied species using substrate-borne signals (Hemiptera: Psyllidae: Cacopsylla). Ann Entomol Soc Am 108:902–911

    Article  Google Scholar 

  • Markl H (1983) Vibrational communication. In: Huber F, Markl H (eds) Neuroethology and behavioural physiology, 1st edn. Springer, Berlin Heidelberg New York, pp 332–353

    Chapter  Google Scholar 

  • Michelsen A (2014) Physical aspects of vibrational communication. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication, 1st edn. Springer, Heidelberg New York Dordrecht London, pp 199–213

    Chapter  Google Scholar 

  • Nunes-Silva P (2011) Capacidade vibratória e polinização por vibração nas abelhas do gênero Melipona (Apidae, Meliponini) e Bombus (Apidae, Bombini). PhD thesis, University of São Paulo-Ribeirão Preto, Brazil

  • Oppedisano T, Polajnar J, Kostanjšek R, De Cristofaro A, Ioriatti C, Virant-Doberlet M, Mazzoni V (2020) Substrate-borne vibrational communication in the vector of apple proliferation disease Cacopsylla picta (Hemiptera: Psyllidae). J Econom Entomol 113:596–603

    Article  CAS  Google Scholar 

  • Panizzi AR, McPherson JE, James DG, Javahery M, McPherson RM (2000) Stink bugs (Pentatomidae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance, 1st edn. CRC Press, Boca Raton, pp 421–474

    Google Scholar 

  • Pavlovčič P, Čokl A (2001) Songs of Holcostethus strictus (Fabricius): a different repertoire among land bugs. Behav Proc 53:65–73

    Article  Google Scholar 

  • Polajnar J, Svenšek D, Čokl A (2012) Resonance in herbaceous plant stems as a factor in vibrational communication of pentatomide bugs (Heteroptera: Pentatomidae). J R Soc Interfaces 9:1898–1907

    Article  Google Scholar 

  • Schwertner CF, Grazia J (2007) O genero Chinavia Orian (Hemiptera, Pentatomidae, Pentatominae) no Brazil, com chave pictorica para os adultos. Rev Bras Entomol Soc 51:416–435

    Article  Google Scholar 

  • Schneider P (1975) Versuche zur Erzeugung des Verteidigungstones bei Hummeln. Zool Jahrb Allg Zool 79:111–127

    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 CC, Laumann RA, Blassioli-Moraes MC, Aquino MFS, Borges M (2015) Comparative biology of two congener stinkbugs, Chinavia impicticornis and C. ubica (Hemiptera: Pentatomidae). Pesq Agropec Bras 50:355–362

    Article  Google Scholar 

  • da Silveira S, Dias AM, Gomes Lagoa AC, Blassioli-Moraes MC, Borges M, Čokl A, Laumann RA (2019) Specificity of male responses to female vibratory signals in two Chinavia species (Hemiptera: Pentatomidae) is based on signal structure and narrow temporal parameters. Anim Behav Cogn 6:1–12

    Article  Google Scholar 

  • Strauss J, Stritih-Peljhan N, Lakes-Harlan R (2017) Determining vibroreceptor sensitivity in insects: influence of experimental parameters and recording techniques. In: Hill PSM, Lakes-Harlan R, Mazzoni V, Narins PM, Virant-Doberlet M, Wessel A (eds) Biotremology: studying vibrational behavior, 1st edn. Springer Nature, Switzerland, pp 209–233

    Google Scholar 

  • Šolinc G (2017) Influence of temporal and spatial properties of airflow on the response of filiform sensilla of the bug Pyrrhocoris apterus. MSc Thesis, University of Ljubljana, Slovenia

  • Tautz J, Markl H (1978) Caterpillars detect flying wasps by hairs sensitive to medium vibration. Behav Ecol Sociobiol 4:101–110

    Article  Google Scholar 

  • Žunič A, Čokl A, Virant-Doberlet M, Millar JG (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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Acknowledgements

The authors thank for the financial support to the Research Support Foundation of the Federal District (FAP-DF, Project 193.000.978/2015), the Brazilian Agricultural Research Corporation (EMBRAPA), the National Council for Scientific and Technological Development (CNPq) and to the Slovenian Research Agency (research core funding No. P1-0255 B, Project J1-8142). The authors are grateful to Mrs. Susan Casement for improving the language of the text.

Funding

The research was supported by the Research Support Foundation of the Federal District (FAP-DF, Project 193.000.978/2015), the Brazilian Agricultural Research Corporation (EMBRAPA), the National Council for Scientific and Technological Development (CNPq) and the Slovenian Research Agency (research core funding No. P1-0255 B), project J1-8142).

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Authors and Affiliations

  1. Department of Organisms and Ecosystems Research, National Institute of Biology, Večna pot 111, 1000, Ljubljana, Slovenia

    Andrej Čokl

  2. Parque Estacao Biologica, EMBRAPA Genetic Resources and Biotechnology, W5 Norte (Final), Brasília, 7077-917, Brazil

    Alenka Žunič Kosi, Maria Carolina Blassioli Moraes, Miguel Borges & Raul Alberto Laumann

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  1. Andrej Čokl
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  2. Alenka Žunič Kosi
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  3. Maria Carolina Blassioli Moraes
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  4. Miguel Borges
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  5. Raul Alberto Laumann
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All authors contributed to the study conception and design. AČ and RAL conceived, designed, performed the experiments and analyzed data. AČ and RAL wrote the first draft of the manuscript and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Andrej Čokl.

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Čokl, A., Kosi, A.Ž., Moraes, M.C.B. et al. Stink Bug Inter-Plant Communication with Signals Produced by Vibration of Lifted Wings. J Insect Behav 34, 194–210 (2021). https://doi.org/10.1007/s10905-021-09780-2

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