Abstract
Substrate-borne signals are widely used in Hemiptera and are known to be utilized in mate searching and recognition. Within this Order, the superfamily Psylloidea is a diverse taxon which uses this type of signal modality during mating behavior between the two sexes. This study describes and compares the previously unreported vibrational communication of two closely related species of Macrohomotoma (Homotomidae). Both genders of these two species, Macrohomotoma gladiata Kuwayama 1908 and Macrohomotoma robusta Yang 1984, emit vibrational signals and establish duets during mating. The structure of male calling consists of two chirps while the female response is a single chirp. Males may sometimes follow the female response by emitting a single chirp that sounds similar to the female response with respect to the chirp duration and dominant frequency. This behavior is novel among Psylloidea and its potential function is discussed. Specific comparison of signal characteristics has revealed that the two species of Macrohomotoma are clearly distinguishable from each other which opens the possibility of acoustic signals being used for species delineation.
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References
Bella S, Rapisarda C (2014) New findings in Italy of the recently introduced alien psyllid Macrohomotoma gladiata and additional distributional records of Acizzia jamatonica and Cacopsylla fulguralis (Hemiptera Psylloidea). REDIA 97:151–155
Boumans L, Johnsen A (2015) Stonefly duets: vibrational sexual mimicry can explain complex patterns. J Ethol 33:87–107. https://doi.org/10.1098/rspb.2004.3041
Brown RL, Landolt PJ, Horton DR, Zack RS (2009) Attraction of Cacopsylla pyricola (Hemiptera: Psyllidae) to female psylla in pear orchards. Environ Entomol 38:815–822. https://doi.org/10.1603/022.038.0335
Burckhardt D, Ouvrard D (2012) A revised classification of the jumping plant-lice (Hemiptera: Psylloidea). Zootaxa 3509:1–34. 10.11646/zootaxa.3509.1.1
Claridge M (1985) Acoustic behavior of leafhoppers and planthoppers: species problems and speciation. In: Nault LR, Rodriguez JG, DeLong DM (eds) The leafhoppers and planthoppers. Wiley, New York, pp 103–125
Cocroft RB (2005) Vibrational communication facilitates cooperative foraging in a phloem-feeding insect. Proc R Soc B 272:1023–1029. https://doi.org/10.1098/rspb.2004.3041
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. https://doi.org/10.1016/j.beproc.2007.01.003
David JAO, Zefa E, Fontanetti CS (2003) Cryptic species of Gryllus in the light of bioacoustic (Orthoptera: Gryllidae). Neotrop Entomol 32:75–80. https://doi.org/10.1590/S1519-566X2003000100010
Donelson NC, van Staaden MJ (2005) Alternate tactics in male bladder grasshoppers (Orthoptera: Pneumoridae). Behaviour 142:761–778. https://doi.org/10.1163/1568539054729088
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. https://doi.org/10.1007/s10340-014-0588-0
Eberhard MJ, Eberhard SH (2013) Evolution and diversity of vibrational signals in Mantophasmatodea (Insecta). J Insect Behav 26:352–370. https://doi.org/10.1007/s10905-012-9352-6
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. https://doi.org/10.1371/journal.pone.0032954
Hammer Ø, Harper D, Ryan P (2001) PAST: paleontological statistics software package for education and data analysis. http://palaeo-electronica.org/2001_1/past/issue1_01htm. Accessed 30 Jan 2015
Henry CS, Wells MM (2010) Acoustic niche partitioning in two cryptic sibling species of Chrysoperla green lacewings that must duet before mating. Anim Behav 80:991–1003. https://doi.org/10.1016/j.anbehav.2010.08.021
Henry CS, Brooks SJ, Duelli P, Johnson JB (2002) Discovering the true Chrysoperla carnea (Insecta: Neuroptera: Chrysopidae) using song analysis, morphology, and ecology. Ann Entomol Soc Am 95:172–191. https://doi.org/10.1603/0013-8746(2002)095[0172:DTTCCI]2.0.CO;2
Hill PS (2012) Do insect drummers actually drum? Studying vibrational communication across taxa. Mitt Dtsch Ges Allg Angew Ent 18:603–611
Hoch H, Deckert J, Wessel A (2006) Vibrational signalling in a Gondwanan relict insect (Hemiptera: Coleorrhyncha: Peloridiidae). Biol Lett 2:222–224. https://doi.org/10.1098/rsbl.2006.0451
Horton DR, Landolt PJ (2007) Attraction of male pear psylla, Cacopsylla pyricola, to female-infested pear shoots. Entomol Exp Appl 123:177–183. https://doi.org/10.1111/j.1570-7458.2007.00537.x
Hunt RE (1994) Vibrational signals associated with mating behavior in the treehopper, Enchenopa binotata say (Hemiptera: Homoptera: Membracidae). J N Y Entomol Soc 102:266–270
Kanmiya K (2005) Mating behaviour and vibratory signals in whiteflies (Hemiptera: Aleyrodidae). In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology, and evolution. CRC Press, Boca Raton, pp 365–379
Kon M, Oe A, Numata H, Hidaka T (1988) Comparison of the mating behaviour between two sympatric species, Nezara Antennata and N. Viridula (Heteroptera: Pentatomidae), with special reference to sound emission. J Ethol 6:91–98. https://doi.org/10.1007/BF02350873
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. https://doi.org/10.1007/s00265-015-1898-9
Kuwayama S (1908) Die Psylliden Japans I. Trans Sapporo Nat Hist Soc 2:149–189
Laborda R, Galán-Blesa J, Sánchez-Domingo A et al (2015) Preliminary study on the biology, natural enemies and chemical control of the invasive Macrohomotoma gladiata (Kuwayama) on urban Ficus microcarpa L. trees in Valencia (SE Spain). Urban For Urban Green 14:123–128. https://doi.org/10.1016/j.ufug.2014.12.007
Laumann RA, Moraes MCB, Čokl A, Borges M (2007) Eavesdropping on sexual vibratory signals of stink bugs (Hemiptera: Pentatomidae) by the egg parastitoids Telenomus podisi. Anim Behav 73:637–649. https://doi.org/10.1016/j.anbehav.2006.09.011
Laumann RA, Kavčič A, 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. https://doi.org/10.1111/phen.12005
Li F (2011) Psyllidomorpha of China (Insecta: Hemiptera). Science Press, Beijing
Liao YC, Yang MM (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. https://doi.org/10.1093/aesa/sav071
Liao YC, Huang SS, Yang MM (2016) Substrate-borne signals, specific recognition, and plant effects on the acoustics of two allied species of Trioza, with the description of a new species (Psylloidea: Triozidae). Ann Entomol Soc Am 6:906–917. https://doi.org/10.1093/aesa/saw060
Lubanga UK, Guédot C, Percy DM, Steinbauer MJ (2014) Semiochemical and vibrational cues and signals mediating mate finding and courtship in Psylloidea (Hemiptera): a synthesis. Insects 5:577–595. https://doi.org/10.3390/insects5030577
Lubanga UK, Peters RA, Steinbauer MJ (2016) Substrate-borne vibrations of male psyllids vary with body size and age but females are indifferent. Anim Behav 120:173–182. https://doi.org/10.1016/j.anbehav.2016.07.033
Mankin RW, Rohde BB, McNeill SA, Paris TM, Zagvazdina NI, Greenfeder S (2013) Diaphorina citri (Hemiptera: Liviidae) responses to microcontroller-buzzer communication signals of potential use in vibration traps. Fla Entomol 96:1546–1555. https://doi.org/10.1653/024.096.0437
Mankin RW, Rohde B, Mcneill S (2016) Vibrational duetting mimics to trap and disrupt mating of the devastating Asian citrus psyllid insect pest. Proc Mtgs Acoust 25:1–9. https://doi.org/10.1121/2.0000185
Mazzoni V, Lucchi A, Čokl A, Prešern J, Virant-Doberlet M (2009) Disruption of the reproductive behaviour of Scaphoideus titanus by playback of vibrational signals. Entomol Exp Appl 133:174–185. https://doi.org/10.1111/j.1570-7458.2009.00911.x
Meyhöfer R, Casas J (1999) Vibratory stimuli in host location by parasitic wasps. J Insect Physiol 45:967–971. https://doi.org/10.1016/S0022-1910(99)00060-8
Mifsud D, Porcelli F (2012) The psyllid Macrohomotoma gladiata Kuwayama, 1908 (Hemiptera: Psylloidea: Homotomidae): a Ficus pest recently introduced in the EPPO region. EPPO Bull 42:161–164. https://doi.org/10.1111/j.1365-2338.2012.02544.x
Otte D (1992) Evolution of cricket songs. J Orthop Res 1:25–49
Ouvrard D (2016) Psyl'list-the world psylloidea database. http://www.hemiptera-databases.org/psyllist/. Accessed 30 July 2016
Ouvrard D, Burckhardt D (2008) Molecular phylogeny of psyllids: implications for the classification. Bull Insectol 61:117
Pedata PA, Burckhardt D, Mancini D (2012) Severe infestations of the jumping plant-louse Macrohomotoma gladiata, a new species for Italy in urban Ficus plantations. Bull Insectol 65:95–98
Percy DM, Taylor GS, Kennedy M (2006) Psyllid communication: acoustic diversity, mate recognition and phylogenetic signal. Invertebr Syst 20:431–445. https://doi.org/10.1071/IS05057
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. https://doi.org/10.1603/0013-8746(2008)101[253:OOASIT]2.0.CO;2
Pfannenstiel R, Hunt R, Yeargan K (1995) Orientation of a hemipteran predator to vibrations produced by feeding caterpillars. J Insect Behav 8:1–9. https://doi.org/10.1007/BF01990965
Polajnar J, Eriksson A, Lucchi A, Anfora G, Virant-Doberlet M, Mazzoni V (2014) Manipulating behaviour with substrate-borne vibrations–potential for insect pest control. Pest Manag Sci 71:15–23. https://doi.org/10.1002/ps.3848
Prestwich KN (1994) The energetics of acoustic signaling in anurans and insects. Am Zool 34:625–643. https://doi.org/10.1093/icb/34.6.625
Rung A (2016) A new pest of ficus in California: Macrohomotoma gladiata Kuwayama, 1908 (Hemiptera: Psylloidea: Homotomidae), new to North America. Check List 12:1882. 10.15560/12.3.1882
Soroker V, Talebaev S, Harari AR, Wesley SD (2004) The role of chemical cues in host and mate location in the pear psylla Cacopsylla bidens (Homoptera: Psyllidae). J Insect Behav 17:613–626. https://doi.org/10.1023/B:JOIR.0000042544.35561.1c
Sueur J, Aubin T (2002) Acoustic communication in the Palaearctic red cicada, Tibicina haematodes: chorus organisation, calling-song structure, and signal recognition. Can J Zool 80:126–136. https://doi.org/10.1139/z01-212
Sueur J, Aubin T (2003) Specificity of cicada calling songs in the genus Tibicina (Hemiptera: Cicadidae). Syst Entomol 28:481–492. https://doi.org/10.1046/j.1365-3113.2003.00222.x
Tauber E, Cohen D, Greenfield MD, Pener MP (2001) Duet singing and female choice in the Bushcricket Phaneroptera nana. Behaviour 138:411–430. https://doi.org/10.2307/4535831
Taylor KL (1962) The Australian genera Cardiaspina Crawford and Hyalinaspis Taylor, (Homoptera: Psyllidae). Aust J Zool 10:307. https://doi.org/10.1071/ZO9620307#sthash.46czXXSW.dpuf
Taylor KL (1985) A possible stridulatory organ in some Psylloidea (Homoptera). Aust J Entomol 24:77–80. https://doi.org/10.1111/j.1440-6055.1985.tb00190.x
Tishechkin DY (2005) Vibratory communication in Psylloidea (Hemiptera). In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology, and evolution. CRC Press, Boca Raton, pp 357–363
Tishechkin DY (2006) On the structure of stridulatory organs in jumping plant lice (Homoptera: Psyllinea). Russ Entomol J 15:335–340
Tishechkin DY (2007) New data on vibratory communication in jumping plant lice of the families Aphalaridae and Triozidae (Homoptera, Psyllinea). Entomol Rev 87:394–400. https://doi.org/10.1134/S0013873807040021
Villarreal SM, Gilbert C (2014) Male Scudderia pistillata katydids defend their acoustic duet against eavesdroppers. Behav Ecol Sociobiol 68:1669–1675. https://doi.org/10.1007/s00265-014-1775-y
Virant-Doberlet M, King RA, Polajnar J, Symondson WO (2011) Molecular diagnostics reveal spiders that exploit prey vibrational signals used in sexual communication. Mol Ecol 20:2204–2216. https://doi.org/10.1111/j.1365-294X.2011.05038.x
Wenninger EJ, Hall DG (2007) Daily timing of mating and age at reproductive maturity in Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 90:715–722. https://doi.org/10.1653/0015-4040(2007)90[715:DTOMAA]2.0.CO;2
Wenninger EJ, Stelinski LL, Hall DG (2008) Behavioral evidence for a female-produced sex attractant in Diaphorina citri. Entomol Exp Appl 128:450–459. https://doi.org/10.1111/j.1570-7458.2008.00738.x
Wenninger EJ, Hall DG, Mankin RW (2009) Vibrational communication between the sexes in Diaphorina citri (Hemiptera: Psyllidae). Ann Entomol Soc Am 102:547–555. https://doi.org/10.1603/008.102.0327
Wood RM, Peters RA, Taylor GS, Steinbauer MJ (2015) Characteristics of the signals of male Anoeconeossa bundoorensis Taylor and Burckhardt (Hemiptera: Aphalaridae) associated with female responsiveness. J Insect Behav 29:1–14. https://doi.org/10.1007/s10905-015-9539-8
Yang CT (1984) Psyllidae of Taiwan. Taiwan Mus Spec Publ Ser 3:1–305
Yang MM, Yang CT, Chao JT (1986) Reproductive isolation and taxonomy of two Taiwanese Paurocephala species (Homoptera: Psylloidea). Taiwan Mus Spec Publ 6:176–203
Žunič A, Cokl A, Doberlet MV, 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. https://doi.org/10.1603/0013-8746-101.6.1169
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. https://doi.org/10.1007/s10905-011-9272-x
Acknowledgements
We are grateful to the following persons: Ching-Yi Chien, Shen-Feng Lin, and Zong-Zhe Wu for their help during field collection, Wesley Hunting for his kind help in English editing, and Lan-Yu Liu for giving comments on the initial draft.
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Liao, YC., Yang, MM. First Evidence of Vibrational Communication in Homotomidae (Psylloidea) and Comparison of Substrate-Borne Signals of Two Allied Species of the Genus Macrohomotoma Kuwayama. J Insect Behav 30, 567–581 (2017). https://doi.org/10.1007/s10905-017-9640-2
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DOI: https://doi.org/10.1007/s10905-017-9640-2