Intrasexual Vibrational Behavior of Philaenus spumarius in Semi-Field Conditions
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Insect Collection and Rearing
2.2. Signal Recording
2.3. Analyzed Parameters
2.4. Statistical Analyses
2.4.1. Vibrational Signaling throughout the Season and during the Day
2.4.2. Types of Signals throughout the Season
2.4.3. Signaling According to the Number of Individuals and Type of Signals
2.4.4. Types of Interactions
3. Results
3.1. Vibrational Signaling throughout the Season and during the Day
3.2. Types of Signals in “Early” and “Late” Season
3.3. Signaling According to the Number of Individuals and Type of Signals
3.4. Type of Interactions
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Hill, P.S. Vibrational Communication in Animals; Harvard University Press: London, UK, 2008. [Google Scholar]
- Čokl, A.; Virant-Doberlet, M. Communication with substrate-borne signals in small plant-dwelling insects. Annu. Rev. Entomol. 2003, 48, 29–50. [Google Scholar] [CrossRef] [PubMed]
- Virant-Doberlet, M.; Mazzoni, V.; De Groot, M.; Polajnar, J.; Lucchi, A.; Symondson, W.O.; Čokl, A. Vibrational communication networks: Eavesdropping and biotic noise. In Studying Vibrational Communication; Cocroft, R.B., Gogala, M., Hill, P.S.M., Wessel, A., Eds.; Springer: Berlin/Heidelberg, Germany, 2014; pp. 93–123. [Google Scholar]
- Castellanos, I.; Barbosa, P. Evaluation of predation risk by a caterpillar using substrate-borne vibrations. Anim. Behav. 2006, 72, 461–469. [Google Scholar] [CrossRef]
- Evans, T.A.; Inta, R.; Lai, J.C.; Prueger, S.; Foo, N.W.; Fu, E.W.e.; Lenz, M. Termites eavesdrop to avoid competitors. Proc. R. Soc. B Biol. Sci. 2009, 276, 4035–4041. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mazzoni, V.; Lucchi, A.; Ioriatti, C.; Virant-Doberlet, M.; Anfora, G. Mating behavior of Hyalesthes obsoletus (Hemiptera: Cixiidae). Ann. Entomol. Soc. Am. 2010, 103, 813–822. [Google Scholar] [CrossRef] [Green Version]
- Mazzoni, V.; Presern, J.; Lucchi, A.; Virant-Doberlet, M. Reproductive strategy of the nearctic leafhopper Scaphoideus titanus Ball (Hemiptera: Cicadellidae). Bull. Entomol. Res. 2009, 99, 401. [Google Scholar] [CrossRef]
- Cocroft, R.B. Vibrational communication facilitates cooperative foraging in a phloem-feeding insect. Proc. R. Soc. B Biol. Sci. 2005, 272, 1023–1029. [Google Scholar] [CrossRef]
- Virant-Doberlet, M.; Kuhelj, A.; Polajnar, J.; Šturm, R. Predator-prey interactions and eavesdropping in vibrational communication networks. Front. Ecol. Evol. 2019, 7, 203. [Google Scholar] [CrossRef] [Green Version]
- Bedoya, C.L.; Brockerhoff, E.G.; Hayes, M.; Leskey, T.C.; Morrison, W.R., III; Rice, K.B.; Nelson, X.J. Brown marmorated stink bug overwintering aggregations are not regulated through vibrational signals during autumn dispersal. R. Soc. Open Sci. 2020, 7, 201371. [Google Scholar] [CrossRef]
- Hill, P.S.M.; Mazzoni, V.; Narins, P.; Virant-Doberlet, M.; Wessel, A. Quo Vadis, Biotremology? In Biotremology: Studying Vibrational Behavior; Hill, P.S.M., Lakes-Harlan, R., Mazzoni, V., Narins, P.M., Virant-Doberlet, M., Wessel, A., Eds.; Springer International Publishing: Cham, Switzerlands, 2019; pp. 3–14. [Google Scholar]
- Virant-Doberlet, M.; Cokl, A. Vibrational communication in insects. Neotrop. Entomol. 2004, 33, 121–134. [Google Scholar] [CrossRef]
- Mazzoni, V.; Lucchi, A.; Čokl, A.; Prešern, J.; Virant-Doberlet, M. Disruption of the reproductive behaviour of Scaphoideus titanus by playback of vibrational signals. Entomol. Exp. Appl. 2009, 133, 174–185. [Google Scholar] [CrossRef]
- Kuhelj, A.; Virant-Doberlet, M. Male–male interactions and male mating success in the leafhopper Aphrodes makarovi. Ethology 2017, 123, 425–433. [Google Scholar] [CrossRef]
- Addesso, K.M.; McAuslane, H.J.; Cherry, R. Aggregation behavior of the southern chinch bug (Hemiptera: Blissidae). Environ. Entomol. 2012, 41, 887–895. [Google Scholar] [CrossRef] [Green Version]
- Biedermann, R. Aggregation and survival of Neophilaenus albipennis (Hemiptera: Cercopidae) spittlebug nymphs. Eur. J. Entomol. 2003, 100, 493–500. [Google Scholar] [CrossRef] [Green Version]
- Kusmayadi, A.; Kuno, E.; Sawada, H. The spatial distribution pattern of the brown planthopper Nilaparvata lugens Stål (Homoptera: Delphacidae) in west Java, Indonesia. Popul. Ecol. 1990, 32, 67–83. [Google Scholar] [CrossRef]
- Park, Y.-L.; Perring, T.M.; Farrar, C.A.; Gispert, C. Spatial and temporal distributions of two sympatric Homalodisca spp.(Hemiptera: Cicadellidae): Implications for areawide pest management. Agric. Ecosyst. Environ. 2006, 113, 168–174. [Google Scholar] [CrossRef]
- Pérez-Rodríguez, J.; Martínez-Blay, V.; Soto, A.; Selfa, J.; Monzó, C.; Urbaneja, A.; Tena, A. Aggregation patterns, sampling plan, and economic injury levels for the new citrus pest Delottococcus aberiae (Hemiptera: Pseudococcidae). J. Econ. Entomol. 2017, 110, 2699–2706. [Google Scholar] [CrossRef]
- Cornara, D.; Bosco, D.; Fereres, A. Philaenus spumarius: When an old acquaintance becomes a new threat to European agriculture. J. Pest Sci. 2018, 91, 957–972. [Google Scholar] [CrossRef]
- Saponari, M.; Loconsole, G.; Cornara, D.; Yokomi, R.K.; De Stradis, A.; Boscia, D.; Bosco, D.; Martelli, G.P.; Krugner, R.; Porcelli, F. Infectivity and transmission of Xylella fastidiosa by Philaenus spumarius (Hemiptera: Aphrophoridae) in Apulia, Italy. J. Econ. Entomol. 2014, 107, 1316–1319. [Google Scholar] [CrossRef] [Green Version]
- Schneider, K.; Van der Werf, W.; Cendoya, M.; Mourits, M.; Navas-Cortés, J.A.; Vicent, A.; Oude Lansink, A. Impact of Xylella fastidiosa subspecies pauca in European olives. Proc. Natl. Acad. Sci. USA 2020, 117, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Avosani, S.; Daher, E.; Franceschi, P.; Ciolli, M.; Verrastro, V.; Mazzoni, V. Vibrational communication and mating behavior of the meadow spittlebug Philaenus spumarius. Entomol. Gen. 2020, 307–321. [Google Scholar] [CrossRef]
- Avosani, S.; Franceschi, P.; Ciolli, M.; Verrastro, V.; Mazzoni, V. Vibrational playbacks and microscopy to study the signalling behaviour and female physiology of Philaenus spumarius. J. Appl. Entomol. 2021, 145, 518–529. [Google Scholar] [CrossRef]
- Bodino, N.; Cavalieri, V.; Dongiovanni, C.; Plazio, E.; Saladini, M.A.; Volani, S.; Simonetto, A.; Fumarola, G.; Di Carolo, M.; Porcelli, F. Phenology, seasonal abundance and stage-structure of spittlebug (Hemiptera: Aphrophoridae) populations in olive groves in Italy. Sci. Rep. 2019, 9, 17725. [Google Scholar] [CrossRef] [PubMed]
- Bodino, N.; Cavalieri, V.; Dongiovanni, C.; Saladini, M.A.; Simonetto, A.; Volani, S.; Plazio, E.; Altamura, G.; Tauro, D.; Gilioli, G. Spittlebugs of Mediterranean olive groves: Host-plant exploitation throughout the year. Insects 2020, 11, 130. [Google Scholar] [CrossRef] [Green Version]
- Mangan, R.; Wutz, A. Aggregation patterns of meadow spittlebugs, Philaenus spumarius L. (Homoptera: Cercopidae), on old-field alfalfa plants. Environ. Entomol. 1983, 12, 151–157. [Google Scholar] [CrossRef]
- Weaver, C.R.; King, D. Meadow spittlebug, Philaenus leucophthalmus (L.). Ohio Agric. Exp. Stn. Res. Bull. 1954, 741, 1–99. [Google Scholar]
- Broughton, W. Method in bio-acoustic terminology. Acoust. Behav. Anim. 1963, 3–24. [Google Scholar]
- Team, R.C. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2020. [Google Scholar]
- Wickham, H. ggplot2. Wiley Interdisciplinary Reviews. Comput. Stat. 2011, 3, 180–185. [Google Scholar] [CrossRef]
- Pinheiro, J.; Bates, D.; DebRoy, S.; Sarkar, D.; Team, R.C. Linear and nonlinear mixed effects models. R Package Version 2007, 3, 1–89. [Google Scholar]
- Lenth, R.; Lenth, M.R. Package ‘lsmeans’. Am. Stat. 2018, 34, 216–221. [Google Scholar]
- Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’hara, R.; Simpson, G.L.; Solymos, P.; Stevens, M.H.H.; Wagner, H. Package ‘vegan’. Community Ecol. Package Version 2013, 2, 1–295. [Google Scholar]
- Legendre, F.; Marting, P.R.; Cocroft, R.B. Competitive masking of vibrational signals during mate searching in a treehopper. Anim. Behav. 2012, 83, 361–368. [Google Scholar] [CrossRef]
- Nieri, R.; Mazzoni, V.; Gordon, S.D.; Krugner, R. Mating behavior and vibrational mimicry in the glassy-winged sharpshooter, Homalodisca vitripennis. J. Pest Sci. 2017, 90, 887–899. [Google Scholar] [CrossRef]
- Kuhelj, A.; De Groot, M.; Pajk, F.; Simčič, T.; Virant-Doberlet, M. Energetic cost of vibrational signalling in a leafhopper. Behav. Ecol. Sociobiol. 2015, 69, 815–828. [Google Scholar] [CrossRef]
- Greenfield, M.D. Cooperation and conflict in the evolution of signal interactions. Annu. Rev. Ecol. Syst. 1994, 25, 97–126. [Google Scholar] [CrossRef]
- West-Eberhard, M.J. Sexual selection, competitive communication and species specific signals in insects. In Insect Communication, Proceedings of the 12th Symposium of the Royal Entomological Society of London, London, UK, 7–9 September 1984; Acedemic Press: London, UK, 1984. [Google Scholar]
- Greenfield, M.D. Signalers and Receivers: Mechanisms and Evolution of Arthropod Communication; Oxford University Press: New York, NY, USA, 2002. [Google Scholar]
- Wynne-Edwards, V.C. Animal Dispersion: In Relation to Social Behaviour; Hafner Publishing Company: Edinburgh, UK, 1962. [Google Scholar]
- Greenfield, M.D. Synchronous and alternating choruses in insects and anurans: Common mechanisms and diverse functions. Am. Zool. 1994, 34, 605–615. [Google Scholar] [CrossRef] [Green Version]
- Mazzoni, V.; Eriksson, A.; Anfora, G.; Lucchi, A.; Virant-Doberlet, M. Active space and the role of amplitude in plant-borne vibrational communication. In Studying Vibrational Communication; Springer: Berlin/Heidelberg, Germany, 2014; pp. 125–145. [Google Scholar]
- Hunt, R.E.; Morton, T.L. Regulation of chorusing in the vibrational communication system of the leafhopper Graminella nigrifrons. Am. Zool. 2001, 41, 1222–1228. [Google Scholar]
- Malone, M.; Watson, R.; Pritchard, J. The spittlebug Philaenus spumarius feeds from mature xylem at the full hydraulic tension of the transpiration stream. New Phytol. 1999, 143, 261–271. [Google Scholar] [CrossRef]
- Wise, M.J.; Kieffer, D.L.; Abrahamson, W.G. Costs and benefits of gregarious feeding in the meadow spittlebug, Philaenus spumarius. Ecol. Entomol. 2006, 31, 548–555. [Google Scholar] [CrossRef]
- McEvoy, P.B. Niche partitioning in spittlebugs (Homoptera: Cercopidae) sharing shelters on host plants. Ecology 1986, 67, 465–478. [Google Scholar] [CrossRef]
- Nieri, R.; Anfora, G.; Mazzoni, V.; Rossi Stacconi, M.V. Semiochemicals, semiophysicals and their integration for the development of innovative multi-modal systems for pest monitoring and control. Entomol. Gen. 2021, 12, 287. [Google Scholar]
Sex | Parameter | Estimate | Std. Error | T-Value | p-Value |
---|---|---|---|---|---|
Males | Intercept | 1.087 | 3.174 | 0.342 | 0.734 |
Date | 0.174 | 0.052 | 3.368 | 0.001 | |
Period Evening | 24.967 | 8.656 | 2.884 | 0.007 | |
Period Morning | 7.078 | 5.626 | 1.258 | 0.217 | |
Females | Intercept | −1.271 | 1.099 | −1.157 | 0.256 |
Date | 1.041 | 0.191 | 5.427 | <0.001 | |
Period Evening | −2.010 | 6.349 | −0.316 | 0.753 | |
Period Morning | −1.522 | 2.305 | −0.660 | 0.514 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Akassou, I.; Avosani, S.; Caorsi, V.; Verrastro, V.; Ciolli, M.; Mazzoni, V. Intrasexual Vibrational Behavior of Philaenus spumarius in Semi-Field Conditions. Insects 2021, 12, 584. https://doi.org/10.3390/insects12070584
Akassou I, Avosani S, Caorsi V, Verrastro V, Ciolli M, Mazzoni V. Intrasexual Vibrational Behavior of Philaenus spumarius in Semi-Field Conditions. Insects. 2021; 12(7):584. https://doi.org/10.3390/insects12070584
Chicago/Turabian StyleAkassou, Imane, Sabina Avosani, Valentina Caorsi, Vincenzo Verrastro, Marco Ciolli, and Valerio Mazzoni. 2021. "Intrasexual Vibrational Behavior of Philaenus spumarius in Semi-Field Conditions" Insects 12, no. 7: 584. https://doi.org/10.3390/insects12070584
APA StyleAkassou, I., Avosani, S., Caorsi, V., Verrastro, V., Ciolli, M., & Mazzoni, V. (2021). Intrasexual Vibrational Behavior of Philaenus spumarius in Semi-Field Conditions. Insects, 12(7), 584. https://doi.org/10.3390/insects12070584