Advertisement

Journal of Insect Behavior

, Volume 25, Issue 5, pp 419–440 | Cite as

Duetting Behaviour in the Leafhopper Aphrodes makarovi (Hemiptera: Cicadellidae)

  • Maarten de Groot
  • Maja Derlink
  • Petra Pavlovčič
  • Janez Prešern
  • Andrej Čokl
  • Meta Virant-Doberlet
Article

Abstract

Mate recognition and location in Cicadellidae is mediated exclusively via substrate-borne vibrational signals. In the present study we investigated vibrational signals and mate searching behaviour of the leafhopper Aphrodes makarovi. We studied mating behaviour and exchange of vibrational signals between live insects and in playback experiments. Males emitted long and complex calling signals composed of several sections. Female reply was long and always overlapped the end of the male call. The exchange of male and female vibrational signals was a complex and dynamic interaction during which both partners modified their signals according to partner’s reply. The duration of female reply was influenced by the duration of the male call to which she was responding, while the duration of male call was influenced by the duration of the previous female reply. Such relationship suggests the role of sexual selection in the evolution of male vibrational signals.

Keywords

Vibrational communication mate recognition searching behavior leafhopper duet sexual selection 

Notes

Acknowledgements

The work was supported by funding from the Slovenian National Research Agency (PhD fellowships 1000-07-310030 and 1000-09-310031 to MdG and MD, respectively and research project J1-2181). We wish to thank Dr Alenka Žunič and Jernej Polajnar for technical help and Dr Andrej Blejec for interesting discussions about statistics.

References

  1. Bailey WJ (2003) Insect duets: underlying mechanisms and their evolution. Physiol Entomol 28:157–174CrossRefGoogle Scholar
  2. Bailey WJ, Field G (2000) Acoustic satellite behaviour in the Australian bushcricket Elephantodeta nobilis (Phaneropterinae, Tettigoniidae, Orthoptera). Anim Behav 59:361–369PubMedCrossRefGoogle Scholar
  3. Bailey WJ, Hammond TJ (2003) Duetting in insects—does call length influence reply latency. J Zool Lond 260:267–274CrossRefGoogle Scholar
  4. Bailey WJ, Hammond TJ (2004) Female reply strategies in a duetting Australian bushcricket Caedicia sp. (Phaneropterinae: Tettigoniidae: Orthoptera). J Exp Biol 207:803–811PubMedCrossRefGoogle Scholar
  5. Barth FG (1998) The vibrational sense of spiders. In: Hoy RR, Popper A, Fay R (eds) Comparative hearing: insects, Vol. 10. Springer, New York, pp 228–278CrossRefGoogle Scholar
  6. Bateson M, Healy SD (2005) Comparative evaluation and its implication for mate choice. Trends Ecol Evol 20:659–664PubMedCrossRefGoogle Scholar
  7. Booij CJH (1982) Biosystematics of the Muellerianella complex (Homoptera: Delphacidae), interspecific and geographic variation in acoustic behaviour. Z Tierpsychol 58:31–52CrossRefGoogle Scholar
  8. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, SunderlandGoogle Scholar
  9. Broughton WB (1963) Method in bioacoustic terminology. In: Busnel RG (ed) Acoustic behaviour of animals. Amsterdam London New York, pp 3–24Google Scholar
  10. Charif RA, Waack AM, Strickman LM (2008) Raven Pro 1.3 user’s manual. Cornell Lab of Ornithology, IthacaGoogle Scholar
  11. Claridge MF (1985a) Acoustic signals in the Homoptera; behavior, taxonomy and evolution. Annu Rev Entomol 30:297–317CrossRefGoogle Scholar
  12. Claridge MF (1985b) Acoustic behavior of leafhoppers and planthoppers: species problems and speciation. In: Nault LR, Rodriguez JG (eds) The leafhoppers and planthoppers. Wiley, New York, pp 103–125Google Scholar
  13. Claridge MF, Nixon GA (1986) Oncopsis flavicollis (L.) associated with tree birches (Betula): a complex of biological species or a host plant utilization polymorphism. Biol J Linn Soc 27:381–397CrossRefGoogle Scholar
  14. Cocroft RB (2003) The social environment of an aggregating, ant-attended treehopper (Hemiptera: Membracidae: Vanduzea arquata). J Insect Behav 16:79–95CrossRefGoogle Scholar
  15. Cocroft RB, McNett GD (2006) Vibratory communication in treehoppers (Hemiptera: Membracidae). In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication. Physiology, behaviour, ecology and evolution. Taylor and Francis, Boca Raton, pp 305–317Google Scholar
  16. Cocroft RB, Rodríguez RL (2005) The behavioural ecology of insect vibrational communication. BioScience 55:323–334CrossRefGoogle Scholar
  17. Čokl A, Virant-Doberlet M (2003) Communication with substrate-borne signals in small plant-dwelling insects. Annu Rev Entomol 48:29–50PubMedCrossRefGoogle Scholar
  18. 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 213:3213–3222PubMedCrossRefGoogle Scholar
  19. De Groot M, Čokl A, Virant-Doberlet M (2011) Search behaviour of two hemipteran species using vibrational communication. Cent Eur J Biol 6:756–769CrossRefGoogle Scholar
  20. De Luca PA, Cocroft RB (2009) Age-related changes in an insect mating signal have no effect on female choice. Behav Ecol Sociobiol 63:1787–1798CrossRefGoogle Scholar
  21. den Bieman CFM (1986) Acoustic differentiation and variation in planthoppers of the genus Ribautodelphax (Homoptera, Delphacidae). Neth J Zool 36:461–480Google Scholar
  22. de Vrijer PWF (1984) Variability in calling signals of the planthopper Javesella pellucida (F.) (Homoptera: Delphacidae) in relation to temperature and consequences for species recognition during distant communication. Neth J Zool 34:388–406CrossRefGoogle Scholar
  23. de Vrijer PWF (1986) Species distinctiveness and variability of acoustic signals in the planthopper genus Javesella (Homoptera: Delphacidae). Neth J Zool 36:162–175Google Scholar
  24. Dietrich CH (2004) Phylogeny of the leafhopper subfamily Evacanthinae with a review of Neotropical species and notes on related groups (Hemiptera: Membracoidea: Cicadellidae). Syst Entomol 29:455–487CrossRefGoogle Scholar
  25. Dobler S, Stumpner A, Heller K-G (1994) Sex-specific tuning for the partner’s song in the duetting bushcricket Ancistrura nigrovitatta (Orthoptera: Paneropteridae). J Comp Physiol A 175:303–310Google Scholar
  26. Eyre MD (2005) Habitat diversity in the conservation of the grassland Auchenorrhyncha (Homoptera: Cercopidae, Cicadellidae, Cixidae, Delphacidae) of northern Britain. J Insect Conserv 9:309–317CrossRefGoogle Scholar
  27. Gerhardt HC (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42:615–635CrossRefGoogle Scholar
  28. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, ChicagoGoogle Scholar
  29. Gillham MC (1992) Variation in acoustic signals within and among leafhopper species of the genus Alebra (Homoptera, Cicadellidae). Biol J Linn Soc 45:1–15CrossRefGoogle Scholar
  30. Gogala M (2006) Vibratory signals produced by Heteroptera—Pentatomorpha and Cimicomorpha. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication. Physiology, behaviour, ecology and evolution. Taylor and Francis, Boca Raton, pp 275–295Google Scholar
  31. Greenfield MD (2002) Signallers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, New YorkGoogle Scholar
  32. Hamilton KGA (1983) Introduced and native leafhoppers common to the old and new worlds (Rhynchota: Homoptera: Cicadellidae). Can Entomol 115:473–511CrossRefGoogle Scholar
  33. Heady SE, Nault LR (1991) Acoustic signals of Graminella nigrifrons (Homoptera: Cicadellidae). Great Lakes Entomol 24:9–16Google Scholar
  34. Heady SE, Nault LR, Shambaugh GF, Fairchild L (1986) Acoustic and mating behaviour Dalbulus leafhoppers (Homoptera: Cicadellidae). Ann Entomol Soc Am 79:727–736Google Scholar
  35. Heller K-G (1990) Evolution of song pattern in east Mediterranean Phaneropterinae: constrains by the communication system. In: Bailey WJ, Rentz DCF (eds) The Tettigoniidae: biology, systematics and evolution. Crawford House, Bathurst, pp 130–151Google Scholar
  36. Heller K-G, von Helversen D (1986) Acoustic communication in phaneropterid bushcrickets: species-specific delay of female stridulatory response and matching male sensory time window. Behav Ecol Sociobiol 18:189–198CrossRefGoogle Scholar
  37. Henry CS, Wells MLM (2006) Testing the ability of males and females to respond to altered songs in the duetting green lacewing Chrysoperla plorabunda (Neuroptera: Chrysopidae). Behav Ecol Sociobiol 61:39–51CrossRefGoogle Scholar
  38. Hunt RE, Morton TL (2001) Regulation of chorusing in the vibrational communication system of the leafhopper Graminella nigrifrons. Amer Zool 41:1222–1228CrossRefGoogle Scholar
  39. Hunt RE, Nault LR (1991) Roles of interplant movement, acoustic communication and phototaxis in mate-location behavior of the leafhopper Graminella nigrifrons. Behav Ecol Sociobiol 28:315–320CrossRefGoogle Scholar
  40. Hunt RE, Fox JP, Haynes KF (1992) Behavioral response of Graminella nigrifrons (Homoptera: Cicadellidae) to experimentally manipulated vibrational signals. J Insect Behav 5:1–13CrossRefGoogle Scholar
  41. Inoue H (1982) Species-specific calling sounds as a reproductive isolating mechanism in Nephotettix spp. (Hemiptera: Cicadellidae). Appl Entomol Zool 17:253–262Google Scholar
  42. Jennions MD, Petrie M (1997) Variations in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327PubMedCrossRefGoogle Scholar
  43. Kanmiya K (2006) Mating behaviour and vibratory signals of whiteflies (Hemiptera: Aleyrodidae). In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication. Physiology, behaviour, ecology and evolution. Taylor and Francis, Boca Raton, pp 365–376Google Scholar
  44. Maczey N, Masters GJ, Hollier JA, Mortimer SR, Brown VK (2005) Community associations of chalk grassland leafhoppers (Hemiptera: Auchenorrhycha): conclusions for habitat conservation. J Insect Conserv 9:281–297CrossRefGoogle Scholar
  45. Mazzoni V, Lucchi A, Čokl A, Prešern J, Virant-Doberlet M (2009a) Disruption of the reproductive behaviour of Scaphoideus titanus by playback of vibrational signals. Entomol Exp Appl 133:174–185CrossRefGoogle Scholar
  46. Mazzoni V, Prešern J, Lucchi A, Virant-Doberlet M (2009b) Reproductive strategy of the Nearctic leafhopper Scaphoideus titanus Ball (Hemiptera: Cicadellidae). Bull Entomol Res 99:401–413PubMedCrossRefGoogle Scholar
  47. McCullagh P, Nelder JA (1989) Generalized linear models. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  48. McNett GD, Luan LH, Cocroft RB (2010) Wind induced noise alters signaler and receiver behavior in vibrational communication. Behav Ecol Sociobiol 64:2043–2051CrossRefGoogle Scholar
  49. Michelsen A, Fink F, Gogala M, Traue D (1982) Plants as transmission channels for insect vibrational songs. Behav Ecol Sociobiol 11:269–281CrossRefGoogle Scholar
  50. Nickel H, Remane R (2002) Check list of the planthoppers and leafhoppers of Germany with notes on food plants, diet width, life cycles, geographic range and conservation status (Hemiptera, Fulgomorpha and Cicadomorpha). Beiträge zur Zikadenkunde 5:27–67Google Scholar
  51. Nuhardiyati M, Bailey W (2005) Calling and duetting behavior in the leafhopper Balclutha incisa (Hemiptera: Cicadellidae): opportunity for female choice? J Insect Behav 18:259–280CrossRefGoogle Scholar
  52. Percy DM, Day MF (2005) Observations of unusual acoustic behaviour in two Australian leafhoppers (Hemiptera; Cicadellidae). J Nat Hist 39:3407–3417CrossRefGoogle Scholar
  53. Percy DM, Taylor GS, Kennedy M (2006) Psyllid communication: acoustic diversity, mate recognition and phylogenetic signal. Invertebr Syst 20:431–445CrossRefGoogle Scholar
  54. Percy DM, Ea B, Hoddle MS (2008) Observations of acoustic signaling in three sharpshooters: Homalodisca vitripennis, Homalodisca liturata and Graphocephala atropunctata (Hemiptera: Cicadellidae). Ann Entomol Soc Am 101:253–259CrossRefGoogle Scholar
  55. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  56. Rodríguez RL, Cocroft RB (2006) Divergence in female duetting signals in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Ethology 112:1231–1238CrossRefGoogle Scholar
  57. Rupprecht R (1975) Die Kommunikation von Sialis (Megaloptera) durch Vibrationssignale. J Insect Physiol 21:305–320CrossRefGoogle Scholar
  58. Saxena KN, Kumar H (1984) Acoustic communication in the sexual behaviour of the leafhopper Amrasca devastans. Physiol Entomol 9:77–86CrossRefGoogle Scholar
  59. Seljak G (2004) Contribution to the knowledge of planthoppers and leafhoppers of Slovenia (Hemiptera: Auchenorrhyncha). Acta Entomol Slov 12:189–216Google Scholar
  60. Steel RDG (1959) A multiple comparison rank test: treatments versus control. Biometrics 15:560–572CrossRefGoogle Scholar
  61. Steel RDG (1960) A rank test for comparing all pairs of treatments. Technometrics 2:197–207Google Scholar
  62. Stewart KW, Sandberg JB (2006) Vibratory communication and mate searching behaviour in stoneflies. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication. Physiology, behaviour, ecology and evolution. Taylor and Francis, Boca Raton, pp 179–186Google Scholar
  63. Stewart KW, Abbott JC, Bottorff RL (1995) The drumming signals of two stonefly species Cosumnoperla bypocrena (Perlodidae) and Paraperla wilsoni (Chloroperlidae); a newly discovered duet pattern in Plecoptera. Entomol News 106:13–18Google Scholar
  64. Strübing H, Hasse A (1975) Ein Beitrag zur Neuen Systematik – demonstriert am Beispiel zweier Javesella-Arten (Homoptera-Cicadina: Delphacidae). Zool Beitr 21:517–543Google Scholar
  65. Stumpner A, Meyer S (2001) Songs and the function of song elements in four duetting bushcricket species (Ensifera, Phaneropteridae, Barbitistes). J Insect Behav 14:511–534CrossRefGoogle Scholar
  66. Sullivan-Beckers L, Cocroft RB (2010) The importance of female choice, male–male competition and signal transmission as causes of selection on male mating signals. Evolution 64:3158–3171PubMedCrossRefGoogle Scholar
  67. Tauber E, Pener MP (2000) Song recognition in female bushcrickets Phaneroptera nana. J Exp Biol 203:597–603PubMedGoogle Scholar
  68. Tishechkin DYu (1998) Acoustic signals and morphological characters of leafhoppers belonging to Aphrodes bicinctus group (Homoptera, Cicadellidae) from European Russia. Entomol Rev 78:370–377Google Scholar
  69. Tishechkin DYu (2000) Vibrational communication in Aphrodinae leafhoppers (Deltocephalinae auct., Homoptera: Cicadellidae) and related groups with notes on classification of higher taxa. Russian Entomol J 9:1–66Google Scholar
  70. Tishechkin DYu (2006) Acoustic characters in the classification of higher taxa of Auchenorrhyncha (Hemiptera). In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication. Physiology, behaviour, ecology and evolution. Taylor and Francis, Boca Raton, pp 319–329Google Scholar
  71. Virant-Doberlet M, Čokl A (2004) Vibrational communication in insects. Neotrop Entomol 33:121–134CrossRefGoogle Scholar
  72. Virant-Doberlet M, Žežlina I (2007) Vibrational communication of Metcalfa pruinosa (Hemiptera: Fulgoroidea: Flatidae). Ann Entomol Soc Am 100:73–82CrossRefGoogle Scholar
  73. Virant-Doberlet M, King RA, Polajnar R, Symondson WOC (2011) Molecular diagnostics reveal spiders that exploit vibrational signals used in sexual communication. Mol Ecol 20:2204–2216PubMedCrossRefGoogle Scholar
  74. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer Verlag, HeidelbergCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Maarten de Groot
    • 1
  • Maja Derlink
    • 1
  • Petra Pavlovčič
    • 1
  • Janez Prešern
    • 1
  • Andrej Čokl
    • 1
  • Meta Virant-Doberlet
    • 1
  1. 1.Department of EntomologyNational Institute of BiologyLjubljanaSlovenia

Personalised recommendations