Skip to main content

Mating behavior and vibrational mimicry in the glassy-winged sharpshooter, Homalodisca vitripennis

Abstract

The glassy-winged sharpshooter (GWSS), Homalodisca vitripennis, is an important vector of Xylella fastidiosa, the causal agent of Pierce’s disease of grapevine. GWSS control relies mainly on insecticides; therefore, an alternative method, such as vibrational mating disruption, is required. However, knowledge of GWSS intraspecific communication is necessary to evaluate applicability of such methods. Mating behavior and associated vibrational signals were described in different social contexts: individuals, pairs, and one female with two competing males. Behavioral analysis showed that GWSS mating communication involved the emission of three male and two female signals, with specific roles in two distinct phases of mating behavior, identification and courtship. Mating success depended on vibrational duets between genders, which were temporarily interrupted in the presence of male rivalry. Male rivalry behavior involved the emission of three distinct rivalry signals. Two rivalry signals resemble female signals and were associated with replacement of the female in the duet by the rival male. The third rivalry signal was emitted by competing males. Data suggested that rival males used mimicry and hostile signals to interrupt the ongoing duet and gain access to a female. In the future, knowledge acquired from this study will be essential to develop a mechanical mating disruption method for GWSS control.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Alexander RD (1967) Acoustical communication in arthropods. Annu Rev Entomol 12:495–526

    Article  Google Scholar 

  2. Alexander RD, Marshall DC, Cooley JR (1997) Evolutionary perspectives on insect mating. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 4–31

    Chapter  Google Scholar 

  3. Bailey WJ (2003) Insect duets: underlying mechanisms and their evolution. Physiol Entomol 28:157–174

    Article  Google Scholar 

  4. Bailey W, Macleay C, Gordon T (2006) Acoustic mimicry and disruptive alternative calling tactics in an Australian bushcricket (Caedicia; Phaneropterinae; Tettigoniidae; Orthoptera): does mating influence male calling tactic? Physiol Entomol 31:201–210

    Article  Google Scholar 

  5. Blua AMJ, Redak RA, Morgan DJW, Costa HS (2001) Seasonal flight activity of two Homalodisca species (Homoptera: Cicadellidae) that spread Xylella fastidiosa in Southern California. J Econ Entomol 94:1506–1510

    CAS  Article  PubMed  Google Scholar 

  6. Booij CJH (1982) Biosystematics of the Muellerianella complex (Homoptera, Delphacidae), interspecific and geographic variation in acoustic behaviour. Z Tierpsychol 58:31–52

    Article  Google Scholar 

  7. Boumans L, Johnsen A (2015) Stonefly duets: vibrational sexual mimicry can explain complex patterns. J Ethol 33:87–107

    Article  Google Scholar 

  8. Charif RA, Waack AM, Strickman LM (2010) Raven Pro 1.4 user’s manual. Cornell Laboratory of Ornithology, Ithaca

    Google Scholar 

  9. Chen W, Leopold RA, Boetel MA (2010) Host plant effects on development and reproduction of the glassy-winged sharpshooter, Homalodisca vitripennis (Homoptera: Cicadellidae). Environ Entomol 39:1545–1553

    Article  PubMed  Google Scholar 

  10. Claridge M (1985) Acoustic signals in the Homoptera: behavior, taxonomy, and evolution. Annu Rev Entomol 30:297–317

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. 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 

  13. Dalziell AH, Welbergen JA, Igic B, Magrath RD (2015) Avian vocal mimicry: a unified conceptual framework. Biol Rev 90:643–668

    Article  PubMed  Google Scholar 

  14. Davis MJ, Purcell AH, Thomson SV (1978) Pierce’s disease of grapevines: isolation of the causal bacterium. Science 199:75–77

    CAS  Article  PubMed  Google Scholar 

  15. de Groot M, Derlink M, Pavlovčič P, Prešern J, Čokl A, Virant-Doberlet M (2012) Duetting behaviour in the leafhopper Aphrodes makarovi (Hemiptera: Cicadellidae). J Insect Behav 25:419–440

    Article  Google Scholar 

  16. Eriksson A, Anfora G, Lucchi A, Lanzo F, Virant-Doberlet M, Mazzoni V (2012) Exploitation of insect vibrational signals reveals a new method of pest management. PLoS ONE 7:e32954

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Fabre CCG, Hedwig B, Conduit G, Lawrence PA, Goodwin SF, Casal J (2012) Substrate-borne vibratory communication during courtship in Drosophila melanogaster. Curr Biol 22:2180–2185

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Field SA, Keller MA (1993) Alternative mating tactics and female mimicry as post-copulatory mate-guarding behaviour in the parasitic wasp Cotesia rubecula. Anim Behav 46:1183–1189

    Article  Google Scholar 

  19. Forsyth A, Alcock J (1990) Female mimicry and resource defense polygyny by males of a tropical rove beetle, Leistotrophus versicolor (Coleoptera: Staphylinidae). Behav Ecol Sociobiol 26:325–330

    Article  Google Scholar 

  20. Goodman LA (1968) The analysis of cross-classified data: independence, quasi-independence, and interactions in contingency tables with or without missing entries. J Am Stat Assoc 63:1091–1131

    Google Scholar 

  21. Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, New York

    Google Scholar 

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

    Google Scholar 

  23. Heady SE, Nault LR, Shambaugh GF, Fairchild L (1986) Acoustic and mating behavior of Dalbulus leaf hoppers (Homoptera: Cicadellidae). Ann Entomol Soc Am 79:727–736

    Article  Google Scholar 

  24. Hummel NA, Zalom FG, Toscano NC, Burman P, Peng CYS (2006) Seasonal patterns of female Homalodisca coagulata (say) (Hemiptera: Cicadellidae) reproductive physiology in Riverside, California. Environ Entomol 35:901–906

    Article  Google Scholar 

  25. 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 28:315–320

    Article  Google Scholar 

  26. Hunt RE, Fox JP, Haynes KF (1992) Behavioral response of Graminella nigrifrons (Homoptera: Cicadellidae) to experimentally manipulated vibrational signals. J Insect Behav 5:1–13

    Article  Google Scholar 

  27. Ichikawa T, Ishii S (1974) Mating signal of the brown planthopper, Nilaparvata lugens Stal (Homoptera: Delphacidae): vibration of the substrate. Appl Entomol Zool 9:196–198

    Google Scholar 

  28. Krugner R (2010) Differential reproductive maturity between geographically separated populations of Homalodisca vitripennis (Germar) in California. Crop Prot 29:1521–1528

    Article  Google Scholar 

  29. Krugner R, Groves RL, Johnson MW, Flores AP, Hagler JR, Morse JG (2009) Seasonal population dynamics of Homalodisca vitripennis (Hemiptera: Cicadellidae) in sweet orange trees maintained under continuous deficit irrigation. J Econ Entomol 102:960–973

    Article  PubMed  Google Scholar 

  30. Kuhelj A, de Groot M, Pajk F, Simčič T, Virant-Doberlet M (2015) Energetic cost of vibrational signalling in a leafhopper. Behav Ecol Sociobiol 69:815–828

    Article  Google Scholar 

  31. Luo C, Wei C (2015) Intraspecific sexual mimicry for finding females in a cicada: males produce “female sounds” to gain reproductive benefit. Anim Behav 102:69–76

    Article  Google Scholar 

  32. Mazzoni V, Lucchi A, Čokl A, Prešsern J, Virant-Doberlet M (2009a) Disruption of the reproductive behaviour of Scaphoideus titanus by playback of vibrational signals. Entomol Exp Appl 133:174–185

    Article  Google Scholar 

  33. Mazzoni V, Prešern J, Lucchi A, Virant-Doberlet M (2009b) Reproductive strategy of the Nearctic leafhopper Scaphoideus titanus Ball (Hemiptera: Cicadellidae). Bull Entomol Res 99:401–413

    Article  PubMed  Google Scholar 

  34. Mazzoni V, Lucchi A, Ioriatti C, Virant-Doberlet M, Anfora A (2010) Mating behavior of Hyalesthes obsoletus (Hemiptera: Cixiidae). Ann Entomol Soc Am 103:813–822

    Article  Google Scholar 

  35. Mazzoni V, Eriksson A, Anfora G, Lucchi A, Virant-Doberlet M (2014) Active space and the role of amplitude in plant–borne vibrational communication. In: Cocroft RB, Gogala M, Hill P, Wessel A (eds) Studying vibrational communication. Springer, Heidelberg, pp 125–145

  36. Miranda X (2006) Substrate-borne signal repertoire and courtship jamming by adults of Ennya chrysura (Hemiptera: Membracidae). Ann Entomol Soc Am 99:374–386

    Article  Google Scholar 

  37. New M (1994) Statistics for the behavioural sciences. Behav Res Ther 32:591

    Article  Google Scholar 

  38. Nuhardiyati M, Bailey W (2005) Calling and duetting behavior in the leafhopper Balclutha incisa (Hemiptera: Cicadellidae: Deltocephalinae): opportunity for female choice? J Insect Behav 18:259–280

    Article  Google Scholar 

  39. Percy DM, Boyd EA, Hoddle MS (2008) Observations of acoustic signaling in three sharpshooters: Homalodisca vitripennis, Homalodisca liturata, and Graphocephala atropunctata (Hemiptera: Cicadellidae). Ann Entomol Soc Am 101:253–259

    Article  Google Scholar 

  40. Polajnar J, Eriksson A, Rossi Stacconi MV, Lucchi A, Anfora G, Virant-Doberlet M, Mazzoni V (2014) The process of pair formation mediated by substrate-borne vibrations in a small insect. Behav Process 107:68–78

    Article  Google Scholar 

  41. Polajnar J, Eriksson A, Virant-Doberlet M, Mazzoni V (2016) Mating disruption of a grapevine pest using mechanical vibrations: from laboratory to the field. J Pest Sci 89(4):909–921

    Article  Google Scholar 

  42. Ryan TH (1960) Significance tests for multiple comparison of proportions, variances, and other statistics. Psychol Bull 57:318–328

    CAS  Article  PubMed  Google Scholar 

  43. Saxena KN, Kumar H (1984) Acoustic communication in the sexual behaviour of the leafhopper, Amrasca devastans. Physiol Entomol 9:77–86

    Article  Google Scholar 

  44. Sisterson MS (2008) Effects of insect-vector preference for healthy or infected plants on pathogen spread: insights from a model. J Econ Entomol 101:1–8

    Article  PubMed  Google Scholar 

  45. Sisterson MS (2012) Host selection by Homalodisca vitripennis: the interplay between feeding, egg maturation, egg load, and oviposition. Arthropod Plant Interact 6:351–360

    Article  Google Scholar 

  46. Sisterson MS (2014) Evaluation of a method to quantify glassy-winged sharpshooter (Hemiptera: Cicadellidae) egg maturation during a feeding assay. J Econ Entomol 107:206–214

    Article  PubMed  Google Scholar 

  47. Sisterson MS, Stenger DC (2016) Disentangling effects of vector birth rate, mortality rate, and abundance on spread of plant pathogens. J Econ Entomol 109:487–501

    Article  PubMed  Google Scholar 

  48. Sorensen JT, Gill RJ (1996) A range extension of Homalodisca coagulata (Say) (Hemiptera: Clypeorrhyncha: Cicadellidae) to southern California. Pan Pac Entomol 72:160–161

    Google Scholar 

  49. Stenger DC, Sisterson MS, French R (2010) Population genetics of Homalodisca vitripennis reovirus validates timing and limited introduction to California of its invasive insect host, the glassy-winged sharpshooter. Virology 407:53–59

    CAS  Article  PubMed  Google Scholar 

  50. Triapitsyn SV, Phillips PA (2000) First record of Gonatocerus triguttatus (Hymenoptera: Mymaridae) from eggs of Homalodisca coagulata (Homoptera: Cicadellidae) with notes on the distribution of the host. Fla Entomol 83:200–203

    Article  Google Scholar 

  51. Virant-doberlet M, Žežlina I (2007) Vibrational communication of Metcalfa pruinosa (Hemiptera: Fulgoroidea: Flatidae). Ann Entomol Soc Am 100:73–82

    Article  Google Scholar 

  52. Zar JH (1999) Biostatistical analysis. Pearson Education India. New Delhi, India

Download references

Acknowledgements

We thank Theresa de la Torre, Matthew Escoto, and Melissa Fujioka for providing technical assistance.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Rachele Nieri.

Ethics declarations

Funding

This study was funded by United States Department of Agriculture-Agricultural Research Service (Project # 2034-22000-010-00D), Fondazione Edmund Mach, and a California Department of Food and Agriculture/Pierce’s Disease Board grant awarded to RK and VM.

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.

Communicated by A.R. Horowitz.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 39 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nieri, R., Mazzoni, V., Gordon, S.D. et al. Mating behavior and vibrational mimicry in the glassy-winged sharpshooter, Homalodisca vitripennis . J Pest Sci 90, 887–899 (2017). https://doi.org/10.1007/s10340-017-0840-5

Download citation

Keywords

  • Vibrational communication
  • Mating disruption
  • Rivalry
  • Leafhopper
  • Xylella fastidiosa