Please use this identifier to cite or link to this item:
標題: Sound producing behavior of psyllids (Hemiptera: Psylloidea): functional morphology and mechanisms
作者: 吳宗澤
Zong-Ze Wu
關鍵字: Psyllids;Sound producing mechanism;Axillary sclerite;Anal area of forewing;Axillary cord;木蝨;發聲機制;翅鍵骨;前翅臀區;翅基索
引用: Alexander RD. 1957. Sound production and associated behavior in insects. Ohio Journal of Science, 57: 101-103. Bell PD. 1980. Multimodal communication by the black-horned tree cricket, Oecanthus nigricornis (Walker) (Orthoptera: Gryllidae). Canadian Journal of Zoology, 58: 1861-1868. Bennet-Clark H. 1997. Tymbal mechanics and the control of song frequency in the cicada Cyclochila australasiae. Journal of Experimental Biology, 200: 1681-1694. Bennet-Clark H. 1999. Resonators in insect sound production: how insects produce loud pure-tone songs. Journal of Experimental Biology, 202: 3347-3357. Birch M, Keenlyside J. 1991. Tapping behavior is a rhythmic communication in the death-watch beetle, Xestobium rufovillosum (Coleoptera: Anobiidae). Journal of Insect Behavior, 4: 257-263. Buckley TR, Cordeiro M, Marshall DC, Simon C. 2006. Differentiating between hypotheses of lineage sorting and introgression in New Zealand alpine cicadas (Maoricicada Dugdale). Systematic Biology, 55: 411-425. Campbell K. 1964. Sound production by Psyllidae (Hemiptera). Journal of the Entomological Society of Australia, 1: 3-4. Claridge M. 1985. Acoustic behavior of leafhoppers and planthoppers: species problems and speciation. pp. 103-125. In: Nault LR, Rodriguez JG, DeLong DM (Eds.), The Leafhoppers and Planthoppers. John Wiley & Sons Inc., New York. Cocroft RB. 2005. Vibrational communication facilitates cooperative foraging in a phloem-feeding insect. Proceedings of the Royal Society B-Biological Sciences, 272: 1023-1029. Cocroft RB, Rodriguez RL, Hunt RE. 2008. Host shifts, the evolution of communication, and speciation in the Enchenopa binotata species complex of treehoppers. pp. 88-100. In: Tilmon KJ (Ed.), Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. University of California Press, California. Cocroft RB, RodrIGuez RL. 2005. The behavioral ecology of insect vibrational communication. BioScience, 55: 323-334. Cocroft RB, RodrIGuez RL, Hunt RE. 2010. Host shifts and signal divergence: mating signals covary with host use in a complex of specialized plant-feeding insects. Biological Journal of the Linnean Society, 99: 60-72. Čokl A, Virant-Doberlet M. 2009. Chapter 262 - Vibrational communication. 1034-1038. In: Vincent HR, Ring TC (Eds.), Encyclopedia of Insects (Second Edition). Academic Press, San Diego. Conner WE. 1999. 'Un chant d''appel amoureux': acoustic communication in moths. Journal of Experimental Biology, 202: 1711-1723. Cui Y, Xie Q, Hua J, Dang KAI, Zhou J, Liu X, Wang G, Yu XIN, Bu W. 2013. Phylogenomics of Hemiptera (Insecta: Paraneoptera) based on mitochondrial genomes. Systematic Entomology, 38: 233-245. Duffels JP. 1993. The systematic position of Moana expansa (Homoptera: Cicadidae), with reference to sound organs and the higher classification of the superfamily Cicadoidea. Journal of Natural History, 27: 1223-1237. Eben A, Muhlethaler R, Gross J, Hoch H. 2014. First evidence of acoustic communication in the pear psyllid Cacopsylla pyri L. (Hemiptera: Psyllidae). Journal of Pest Science, online: 1-9. Ellis D. 2007. mp3read and mp3write. Retrieved: 2014. Evans TA, Lai JCS, Toledano E, McDowall L, Rakotonarivo S, Lenz M. 2005. Termites assess wood size by using vibration signals. Proceedings of the National Academy of Sciences of the United States of America, 102: 3732-3737. Field LH, Bailey WJ. 1997. Sound production in primitive Orthoptera from Western Australia: sounds used in defence and social communication in Ametrus sp. and Hadrogryllacris sp. (Gryllacrididae: Orthoptera). Journal of Natural History, 31: 1127-1141. Fonseca PJ, SerrAO EA, Pina-Martins F, Silva P, Mira S, Quartau JA, Paulo OS, Cancela L. 2008. The evolution of cicada songs contrasted with the relationships inferred from mitochondrial DNA (Insecta, Hemiptera). Bioacoustics, 18: 17-34. Gillham MC. 1992. Variation in acoustic signals within and among leafhopper species of the genus Alebra (Homoptera, Cicadellidae). Biological Journal of the Linnean Society, 45: 1-15. Grasso DA, Mori A, Le Mou F, Giovannotti M, Fanfani A. 1998. The stridulatory organ of four Messor ant species (Hymenoptera, Formicidae). Italian Journal of Zoology, 65: 167-174. Henry CS, Brooks SJ, Duelli P, Johnson JB, Wells MM, Mochizuki A. 2013. Obligatory duetting behaviour in the Chrysoperla carnea-group of cryptic species (Neuroptera: Chrysopidae): its role in shaping evolutionary history. Biological Reviews, 88: 787-808. Henry CS, Wells MLM, Simon CM. 1999. Convergent evolution of courtship songs among cryptic species of the carnea group of green lacewings (Neuroptera: Chrysopidae: Chrysoperla). Evolution, 53: 1165-1179. Henry CS, Wells MM, Pupedis RJ. 1993. Hidden taxonomic diversity within Chrysoperla plorabunda (Neuroptera: Chrysopidae): Two new species based on courtship songs. Annals of the Entomological Society of America, 86: 1-13. Heslop-Harrison G. 1952. XXVII.—The number and distribution of the spiracles of the adult psyllid. Annals & Magazine of Natural History, 5: 248-260. Heslop-Harrison G. 1960. Sound production in the Homoptera with special reference to sound producing mechanisms in the Psyllidae. Journal of Natural History Series 13, 3: 633-640. Holman J. 1994. Possible sound producing structures present in some Macrosiphini (Homoptera: Aphididae). European Journal of Entomology, 91: 97-97. Hoy RR, Hoikkala A, Kaneshiro K. 1988. Hawaiian courtship songs: evolutionary innovation in communication signals of Drosophila. Science, 240: 217-219. Hrncir M, Barth FG, Tautz J. 2005. Vibratory and airborne-sound signals in bee communication (Hymenoptera). pp. 421-436 In: Drosopoulos S, Claridge MF (Eds.), Insect Sounds and Communication: Physiology, Behaviour, Ecology, and Evolution. CRC Press, Boca Raton, FL. Hunt RE. 1994. Vibrational signals associated with mating behavior in the treehopper, Enchenopa binotata Say (Hemiptera: Homoptera: Membracidae). Journal of the New York Entomological Society, 102: 266-270. Kanmiya K. 1996. Discovery of male acoustic signals in the greenhouse whitefly, Trialeurodes vaporariorum (Westwood)(Homoptera: Aleyrodidae). Applied Entomology and Zoology, 31: 255-262. Kanmiya K. 2005. Mating behaviour and vibratory signals in whiteflies (Hemiptera: Aleyrodidae). pp. 365-379. In: Drosopoulos S, Claridge MF (Eds.), Insect Sounds and Communication: Physiology, Behaviour, Ecology, and Evolution. CRC Press, Boca Raton, FL. Kubota S. 1985. Rubbing behaviours in some aphids. Japanese Journal of Entomology, 53: 595-603. Luca PAD, Morris GK. 1998. Courtship communication in meadow katydids: female preference for large male vibrations. Behaviour, 135: 777-794. Mankin R, Anderson J, Mizrach A, Epsky N, Shuman D, Heath R, Mazor M, Hetzroni A, Grinshpun J, Taylor P. 2004. Broadcasts of wing-fanning vibrations recorded from calling male Ceratitis capitata (Diptera: Tephritidae) increase captures of females in traps. Journal of Economic Entomology, 97: 1299-1309. Ossiannilsson F. 1950. Sound production in psyllids (Hem. Hom.). Opuscula Entomologica, 15: 202. Ouvrard D, Burckhardt D, Soulier-Perkins A, Bourgoin T. 2008. Comparative morphological assessment and phylogenetic significance of the wing base articulation in Psylloidea (Insecta, Hemiptera, Sternorrhyncha). Zoomorphology, 127: 37-47. Paterson HE. 1980. A comment on 'mate recognition systems'. Evolution, 34: 330-331. Percy DM. 2005. Other psyllid songs. Retrieved: 2014. Percy DM, Taylor GS, Kennedy M. 2006. Psyllid communication: acoustic diversity, mate recognition and phylogenetic signal. Invertebrate Systematics, 20: 431-445. Pratt G, Wood TK. 1992. A phylogenetic analysis of the Enchenopa binotata species complex (Homoptera: Membracidae) using nymphal characters. Systematic Entomology, 17: 351-357. Rodriguez RL, Ramaswamy K, Cocroft RB. 2006. Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects. Proceedings of the Royal Society B-Biological Sciences, 273: 2585-2593. Roth LM, Hartman HB. 1967. Sound production and its evolutionary significance in the Blattaria. Annals of the Entomological Society of America, 60: 740-752. Simmons P, Young D. 1978. The tymbal mechanism and song patterns of the bladder cicada, Cystosoma saundersii. Journal of Experimental Biology, 76: 27-45. Taylor KL. 1985. A possible stridulatory organ in some Psylloidea (Homoptera). Australian Journal of Entomology, 24: 77-80. Tishechkin DY. 2005. Vibratory communication in Psylloidea (Hemiptera). pp. 357-363. In: Drosopoulos S, Claridge MF (Eds.), Insect Sounds and Communication: Physiology, Behaviour, Ecology, and Evolution. CRC Press, Boca Raton, FL. Tishechkin DY. 2006. On the structure of stridulatory organs in jumping plant lice (Homoptera: Psyllinea). Russian Entomological Journal, 15: 335-340. Tuthill LD. 1952. On the Psyllidae of New Zealand (Homoptera). Pacific Science, 6: 83-125. Ulyshen MD, Mankin RW, Chen Y, Duan JJ, Poland TM, Bauer LS. 2011. Role of emerald ash borer (Coleoptera: Buprestidae) larval vibrations in host-quality assessment by Tetrastichus planipennisi (Hymenoptera: Eulophidae). Journal of Economic Entomology, 104: 81-86. Villet MH. 1997. The cicada genus Stagira Stal 1861 (Homoptera Tibicinidae): systematic revision. Tropical Zoology, 10: 347-392. Vincent C. 2010. Vuvuzela sound denoising algorithm. Retrieved: 2014. Virant-Doberlet M, Cokl A. 2004. Vibrational communication in insects. Neotropical Entomology, 33: 121-134. Wenninger EJ, Hall DG. 2007. Daily timing of mating and age at reproductive maturity in Diaphorina citri (Hemiptera: Psyllidae). Florida Entomologist, 90: 715-722. Wenninger EJ, Hall DG, Mankin RW. 2009. Vibrational communication between the sexes in Diaphorina citri (Hemiptera: Psyllidae). Annals of the Entomological Society of America, 102: 547-555. Wenninger EJ, Stelinski LL, Hall DG. 2008. Behavioral evidence for a female-produced sex attractant in Diaphorina citri. Entomologia Experimentalis et Applicata, 128: 450-459. Williams CM, Galambos R. 1950. Oscilloscopic and stroboscopic analysis of the flight sounds of Drosophila. Biological Bulletin, 99: 300-307. Yack JE, Smith ML, Weatherhead PJ. 2001. Caterpillar talk: Acoustically mediated territoriality in larval Lepidoptera. Proceedings of the National Academy of Sciences, 98: 11371-11375. Yang MM, Burckhardt D, Fang SJ. 2009. Psylloidea of Taiwan volume Ⅰ: Families Calophyidae, Carsidaridae, Homotomidae and Phacopteronidae, with overview and keys to families and genera of Taiwanese Psylloidea (Insecta: Hemiptera). Taichung, Taiwan: National Chung Hsing University. p 13-14. Yang MM, Yang CT, Chao JT. 1986. Reproductive isolation and taxonomy of two taiwanese Paurocephala species (Homoptera: Psylloidea). Monograph of Taiwan Museum, 6: 176-203. Zhivomirov H. 2012. Sound analysis with Matlab implementation. Retrieved: 2014.
Sound production in psyllids has been described but to date, the exact mechanism has remained unclear. Several sound production mechanisms in psyllids have been proposed, with most suggesting stridulation between the anal area of forewing and axillary cord as the mode of action. The aim of this study is to determine the specific sound producing structures and mechanisms of the psyllids. Extensive tests were implemented on the species Macrohomotama gladiata Kuwayama belonging to Homotomidae. Through cutting off possible sound producing organs and observing wing-beat frequency with a high-speed camera, acoustic signals were recorded to examine six possible hypotheses. These hypotheses include wing-beating, wing-wing rubbing, wing-thorax rubbing, wing-leg rubbing, leg-abdomen rubbing, and axillary sclerite rubbing. In order to confirm whether a particular mechanism is common in psyllids, other species belonging to different families were also examined, including Trioza sozanica (Boselli) (Triozidae), Mesohomotama camphorae Kuwayama (Carsidaridae), Psylla oluanpiensis Yang and Psylla tobirae Miyatake (Psyllidae). Scanning electron microscopy (SEM) was used to observe the existence of special features that might serve as sound producing structures. Results indicate that psyllids were not able to make any signal after the entire forewing was removed, leading to a rejection of the wing-leg rubbing hypothesis. The wing-beating frequency did not match the dominant frequency of sound, resulting in the rejection of wing-beating hypothesis. Psyllids are still able to produce signals following the removal of the anal area of the forewing so the wing-thorax rubbing hypothesis is also rejected. Psyllids with the forewing membrane area removed can also still make signals, so the hypotheses of wing-wing rubbing and wing-leg rubbing are rejected. Therefore, the axillary sclerite-rubbing hypothesis is accepted due to the fact that the remaining axillary sclerites can not rub each other or rub legs. However, removal of the anal and membrane area of forewing produces sound with weaker amplitude and the modification is more obvious in the former than in the latter. Because to keep anal area of forewing without axillary sclerite is impossible, the hypothesis of wing-thorax rubbing was rejected due to the ablility of sound production with the axillary sclerite present. Our work suggests that psyllids likely make sound by rubbing axillary cord and anal area of forewing. We also further inspected the surface of the axillary sclerite because of the known rough surface on the axillary cord of psyllids. SEM photographs show that the secondary axillary sclerite is stronger than other axillary sclerites and also bears many protuberances that would be suitable for stridulation. In conclusion, the sound producing mechanism of psyllids involves two groups of morphological structures. The first group of stridulation structures is the anal area of forewing and the axillary cord, and the second one is the axillary sclerite of forewing and the mesothorax.

木蝨發聲行為已在許多文獻中記載,但對於發聲機制仍停留於推測階段。多數文獻推測木蝨是藉由前翅翅臀區 (anal area of forewing) 摩擦翅基索 (axillary cord) 而產生聲音。本研究以榕木蝨科的高背木蝨 (Macrohomotama gladiata Kuwayama) 為主要材料,透過切除可能發聲位置與利用高速攝影機觀察翅震動頻率,配合錄音與觀察實驗,以瞭解木蝨發聲結構與機制,並驗證「翅震發聲假說」、「翅翅摩擦發聲假說」、「翅胸摩擦假說」、「足腹摩擦假說」、「翅足摩擦假說」以及「翅鍵骨 (axillary sclerite) 發聲假說」之可能性。同時檢視不同科的物種以確定發聲機制的普遍性,包括三叉木蝨科的虎皮楠木蝨 (Trioza sozanica (Boselli))、錦葵木蝨科的黃槿木蝨 (Mesohomotama camphorae Kuwayama)、與木蝨科的台灣桐木蝨 (Psylla oluanpiensis Yang) 及海桐木蝨 (Psylla tobirae Miyatake)。進一步透過掃描式電子顯微鏡 (SEM) 之檢視,瞭解其發聲結構是否具有特殊構造用於發聲。結果顯示,切除完整前翅的組別之木蝨無法產生聲音訊號,因此排除足腹摩擦假說與後翅涉及發聲的可能性;翅震頻率與聲音主頻率不一致,排除翅震發聲假說;移除前翅臀區的木蝨依然可以發出聲音訊號,排除翅胸摩擦假說;在切除前翅膜質區的組別中,所有的木蝨皆可產生聲音訊號,由於僅剩的左右兩側之翅鍵骨無法相互摩擦,亦無法進行翅足摩擦,因此拒絕翅翅摩擦與翅足摩擦假說並接受翅鍵骨假說。切除翅臀區與切除翅膜質區後,2組實驗皆可錄得聲音訊號但明顯為弱,且發現翅臀區切除後聲音訊號的改變量大於移除翅鍵骨後聲音訊號的改變量。由於實驗無法移除翅鍵骨而保留翅臀區,在翅鍵骨存在可發聲的情況下造成翅胸摩擦假說被拒絕。以上實驗支持木蝨可能藉由翅基索與前翅翅臀區摩擦發聲。目前已知木蝨翅基索具有粗糙的表面結構,本研究進一步檢視翅鍵骨之表面結構。SEM結果顯示,木蝨之第二翅鍵骨較其他翅鍵骨發達,且表面具有凸起結構適合用於摩擦發聲。本研究認為木蝨發聲涉及2組形態構造,第一組為翅臀區摩擦翅基索,第二組為翅鍵骨摩擦中胸。
其他識別: U0005-1107201410344400
Rights: 同意授權瀏覽/列印電子全文服務,2017-07-15起公開。
Appears in Collections:昆蟲學系

Files in This Item:
File SizeFormat Existing users please Login
nchu-103-7101036005-1.pdf3.32 MBAdobe PDFThis file is only available in the university internal network    Request a copy
Show full item record

Google ScholarTM


Items in DSpace are protected by copyright, with all rights reserved, unless otherwise indicated.