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Comparative morphology of ovipositor in cicadas (Hemiptera: Cicadidae), with considerations on their taxonomic significance

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Abstract

Although previous studies have documented the morphology of ovipositor in Cicadidae, little is known about the morphology and ultrastructure of their gonapophyses, which may be closely related to the divergence of related groups and the host plant selection in oviposition. The morphology and ultrastructure of gonapophyses of 13 representative cicadas, belonging to the three subfamilies of Cicadidae, is investigated using scanning electron microscopy. The results show that the morphology of gonapophyses can be adopted in cicada taxonomy at both higher and species levels, and some characters may be promising for phylogenetic analysis of Cicadidae. With regard to the genus Karenia, whose systematic status remains controversial, it resembles members of Cicadinae more than those of Cicadettinae (=Tibicininae auct.) in morphology of gonapophyses. This indicates that it is more reasonable to place this genus into Cicadinae instead of Cicadettinae. The various types of sensilla on the gonapophyses and their distribution are described in detail, and their functions were discussed. Our results supply information not only for future study of taxonomy and phylogeny of the Cicadoidea, but also for researches of oviposition behavior and oviposition-site selection of cicadas.

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References

  • Altner H, Routil C, Loftus R (1981) The structure of bimodal chemo-, thermo-, and hygroreceptive sensilla on the antenna of Locusta migratoria. Cell Tissue Res 215:289–308

    CAS  PubMed  Google Scholar 

  • Banga N, Albert PJ, Kapoor NN, Mcneil JN (2003) Structure, distribution, and innervation of sensilla on the ovipositor of the spruce budworm, Choristoneura fumiferana, and evidence of a gustatory function for type II sensilla. Can J Zool 81:2032–2037

    Article  Google Scholar 

  • Boulard M (1965) L’appareil génital ectodermique des Cigales femelles. Ann Soc Entomol Fr 1:797–812

    Google Scholar 

  • Boulard M (1973) Les Ydiellinae: sous-famille nouvelle de cigales Platypediidae: Clé des familles et sous-familles des Homoptères Cicadoidea. Ann Soc Entomol Fr 9:841–852

    Google Scholar 

  • Boulard M (1976a) Un type nouveau d’appareil stridulant accessoire pour les Cicadoidea. Révision de la classification superieure de la supérfamille (Hom.). J Nat Hist 10:399–407

    Article  Google Scholar 

  • Boulard M (1976b) Sur une deuxième cigale africaine dépourvue d’appareil sonore (Homoptera). Bulletin l’Institut Fondamental d’Afrique Noire Série A 37:629–636

    Google Scholar 

  • Boulard M (1996) Les cigales de la France méditerranéene (généralités et particularités). In: Boulard M, Mondon B (eds) Vies & Mémoires de Cigales Provence Languedoc Méditerranée, pp 5–72

  • Bowen MF (1995) Sensilla basiconica (grooved pegs) on the antennae of female mosquitoes: electrophysiology and morphology. Entomol Exp Appl 77:233–238

    Article  Google Scholar 

  • Chadha GK, Roome RE (1980) Oviposition behaviour and the sensilla of the ovipositor of Chilo partellus and Spodoptera littoralis (Lepidoptera: Noctuidae). J Zool 192:169–178

    Article  Google Scholar 

  • Chou I, Lei Z, Li L, Lu X, Yao W (1997) The Cicadidae of China (Homoptera: Cicadoidea). Tianze Eldoneio, Hong Kong

    Google Scholar 

  • Davis EE, Sokolove PG (1975) Temperature responses of antennal receptors of the mosquito, Aedes aegypti. J Comp Physiol 96:223–236

    Article  Google Scholar 

  • Di Giulio A, Maurizi E, Stacconi MV, Romani R (2012) Functional structure of antennal sensilla in the myrmecophilous beetle Paussus favieri (Coleoptera, Carabidae, Paussini). Micron 43:705–719

    Article  PubMed  Google Scholar 

  • Dietrich CH (1989) Surface sculpturing of the abdominal integument of Membracidae and other Auchenorrhyncha (Homoptera). P Entomol Soc Wash 91:143–152

    Google Scholar 

  • Dweck HK, Gadallah NS, Darwish E (2008) Structure and sensory equipment of the ovipositor of Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Micron 39:1255–1261

    Article  PubMed  Google Scholar 

  • Emeljanov AF (2014) The evolutionary role and fate of the primary ovipositor in insects. Entomol Rev 94:367–396

    Article  Google Scholar 

  • Faucheux MJ (1991) Morphology and distribution of sensilia on the cephalic appendages, tarsi and ovipositor of the European sunflower moth, Homoeosoma nebulella Den. & Schiff. (Lepidoptera: Pyralidae). Int J Insect Morphol Embryol 20:291–307

    Article  Google Scholar 

  • Gillott C (2005) Entomology, 3rd edn. Springer, Netherlands

    Google Scholar 

  • Gracco M, Catalá S (2000) Inter-specific and developmental differences on the array of antennal chemoreceptors in four species of Triatominae (Hemiptera: Reduviidae). Mem I Oswaldo Cruz 95:67–74

    Article  CAS  Google Scholar 

  • Hallberg E, Ahman I (1987) Sensillar types of the ovipositor of Dasineura brassicae: structure and relation to oviposition behaviour. Physiol Entomol 12:51–58

    Article  Google Scholar 

  • Hawke SD, Farley RD, Greany PD (1973) The fine structure of sense organs in the ovipositor of the parasitic wasp, Orgilus lepidus Muesebeck. Tissue Cell 5:171–184

    Article  CAS  PubMed  Google Scholar 

  • Hilsman I (1921) The ovipositor of the cicada. Dissertation. University of Kansas, Lawrence

  • Hummel NA, Zalom FG, Peng CYS (2006) Structure of female genitalia of glassy-winged sharpshooter, Homalodisca coagulata (Say) (Hemiptera: Cicadellidae). Arthropod Struct Dev 35:111–125

    Article  PubMed  Google Scholar 

  • King PE, Fordy MR (1970) The external morphology of the ‘pore’ structures on the tip of the ovipositor in Hymenoptera. Entomol Mon Mag 106:64–66

    Google Scholar 

  • Kramer S (1950) The morphology and phylogeny of Auchenorrhynchous Homortera (Insecta). Ill Biol Monogr 20:i–vii, 1–111

  • Kudryasheva IV (1979) Larvae of song cicadas (Homoptera, Cicadidae) of the USSR fauna. Nauka, Moscow, p 159

    Google Scholar 

  • Li Q, Zhong H, Zhang Y, Wei C (2015) Comparative morphology of the distal segments of Malpighian tubules in cicadas and spittlebugs, with reference to their functions and evolutionary indications to Cicadomorpha (Hemiptera: Auchenorrhyncha). Zool Anz 258:54–68

    Article  Google Scholar 

  • Liang AP, Fletcher JM (2002) Morphology of the antennal sensilla in four Australian spittlebug species (Hemiptera: Cercopidae) with implications for phylogeny. Aust J Entomol 41:39–44

    Article  Google Scholar 

  • Lloyd M, White JA (1987) Xylem feeding by periodical cicada nymphs on pine and grass roots, with novel suggestions for pest control in conifer plantations and orchards. The Ohio J Sci 87:50–54

    Google Scholar 

  • Maier CT (1980) A mole’s-eye view of seventeen-year periodical cicada nymphs, Magicicada septendecim (Hemiptera: Homoptera: Cicadidae). Ann Entomol Soc Am 73:147–152

    Article  Google Scholar 

  • Mciver SB (1985) Mechanoreception. In: Kerkut GA, Gilbert LI (eds) Comparative insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 71–132

    Google Scholar 

  • Mejdalani G (1998) Morfologia externa dos Cicadellinae (Homoptera, Cicadellidae): comparação entre Versigonalia ruficauda (Walker) (Cicadellini) e Tretogonia cribrata Melichar (Proconiini), com notas sobre outras espécies e análise da terminologia. Rev Bras Zool 15:451–544

    Article  Google Scholar 

  • Mejdalani G, Silva RS (2010) Notes on Neotropical Proconiini (Hemiptera: Cicadellidae: Cicadellinae). VII: first detailed description of the female genitalia of a Diestostemma species. Zoologia 27:813–819

    Article  Google Scholar 

  • Meng Z, Yang M (2012) Female genitalia of Seasogonia Young from China, with a new synonym and a new record (Hemiptera, Cicadellidae, Cicadellini). Zookeys 164:24–40

    Article  Google Scholar 

  • Merivee E, Ploomi A, Rahi M, Bresciani J, Ravn HP, Luik A, Sammelselg V (2002) Antennal sensilla of the ground beetle Bembidion properans Steph. (Coleoptera, Carabidae). Micron 33:429–440

    Article  PubMed  Google Scholar 

  • Miller F, Crowley W (1998) Effects of periodical cicada ovipositional injury on woody plants. J Arboric 24:248–253

    Google Scholar 

  • Moulds MS (2005) An appraisal of the higher classification of cicadas (Hemiptera: Cicadoidea) with special reference to the Australian fauna. Rec Aust Mus 57:375–446

    Article  Google Scholar 

  • Müller HJ (1942) Über bau und funktion des legeapparates der zikaden (Homoptera Cicadina). Zoomorphology 38:534–629

    Article  Google Scholar 

  • Myers JG (1928) The morphology of the Cicadidae (Homoptera). Proc Zool Soc Lond 2:365–472

    Google Scholar 

  • Nielson MW (1965) A revision of the genus Cuerna (Homoptera, Cicadellidae). Technical bulletin of the United States Department of Agriculture 1318:1–48

  • Oberdorster U, Grant PR (2006) Predicting emergence, chorusing, and oviposition of periodical cicadas. Ecology 87:409–418

    Article  PubMed  Google Scholar 

  • Ostry ME, Anderson NA (1983) Infection of trembling aspen by Hypoxylon mammatum through cicada oviposition wounds. Phytopathology 73:1092–1096

    Article  Google Scholar 

  • Peregrine DJ (1972) Fine structure of sensilla basiconica on the labium of the cotton stainer, Dysdercus fasciatus (Signoret) (Heteroptera: Pyrrhocoridae). Int J Insect Morphol Embryol 1:241–251

    Article  Google Scholar 

  • Readio PA (1922) Ovipositors of the Cicadellidae (Homoptera). University of Kansas, Lawrence

    Google Scholar 

  • Rebora M, Piersanti S, Dell’otto A, Gaino E (2013) The gustatory sensilla on the endophytic ovipositor of Odonata. Arthropod Struct Dev 42:127–134

    Article  PubMed  Google Scholar 

  • Rodrigues LGN, Mejdalani G (2009) Description of the Aguatala compsa Young (Hemiptera: Cicadellidae: Cicadellinae) female. Neotrop Entomol 38:508–511

    Article  PubMed  Google Scholar 

  • Sanborn AF (2013) Catalogue of the Cicadoidea (Hemiptera: Auchenorrhyncha). Academic Press, London

    Google Scholar 

  • Saxena RC, Barrion AA, Soriano MV (1985) Comparative morphometrics of male and female genitalia and abdominal characters in Nephotettix virescens (Distant) populations from Bangladesh and the Philippines. Int Rice Res Newsl 10:27–28

    Google Scholar 

  • Schneider D (1964) Insect antennae. Annu Rev Entomol 9:103–122

    Article  Google Scholar 

  • Scudder GGE (1957) Reinterpretation of some basal structures in the insect ovipositor. Nature 180:340–341

    Article  Google Scholar 

  • Scudder GGE (1961a) The comparative morphology of the insect ovipositor. Ecol Entomol 113:25–40

    Google Scholar 

  • Scudder GGE (1961b) The functional morphology and interpretation of the insect ovipositor. Can Entomol 93:267–272

    Article  Google Scholar 

  • Scudder GGE (1964) Further problems in the interpretation and homology of the insect ovipositor. Can Entomol 96:405–417

    Article  Google Scholar 

  • Shields VDC, Hildebrand JG (1999) Fine structure of antennal sensilla of the female sphinx moth, Manduca sexta (Lepidoptera: Sphingidae). II. Auriculate, coeloconic, and styliform complex sensilla. Can J Zool 77:302–313

    Article  Google Scholar 

  • Shields VDC, Hildebrand JG (2001) Recent advances in insect olfaction, specifically regarding the morphology and sensory physiology of antennal sensilla of the female sphinx moth Manduca sexta. Microsc Res Tech 55:307–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith FF, Linderman RG (1974) Damage to ornamental trees and shrubs resulting from oviposition by periodical cicada. Environ Entomol 3:725–732

    Article  Google Scholar 

  • Snodgrass RE (1926) Morphology of the insect abdomen. Smithsonian Institution City of Washington, Washington, DC

    Google Scholar 

  • Spänhoff B, Alecke C, Kaschek N, Lange J, Meyer EI (2003) Morphological characteristics of sensilla on the female ovipositor of Lype phaeopa (Psychomyiidae; Trichoptera). J Insect Sci 3:1–7

    Article  Google Scholar 

  • Weber H (1930) Biologie der Hemipteren. Julius Springer, Berlin

    Book  Google Scholar 

  • Williams KS, Simon C (1995) The ecology, behavior, and evolution of periodical cicadas. Ann Rev Entomol 40:269–295

    Article  CAS  Google Scholar 

  • Yokohari F, Tominaga Y, Tateda H (1982) Antennal hygroreceptors of the honey bee, Apis mellifera L. Cell Tissue Res 226:63–73

    Article  CAS  PubMed  Google Scholar 

  • Zacharuk RY (1985) Antennae and sensilla. In: Kerkut GA, Gilbert LI (eds) Comparative insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 1–69

    Google Scholar 

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Acknowledgements

We are sincerely grateful to Prof. John Richard Schrock (Emporia State University, USA) and anonymous referees for their critical review of this manuscript. This research is supported by the National Natural Science Foundation of China (Grant Nos. 31170360, 31572302, 31493021).

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Correspondence to Cong Wei.

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Zhong, H., Zhang, Y. & Wei, C. Comparative morphology of ovipositor in cicadas (Hemiptera: Cicadidae), with considerations on their taxonomic significance. Zoomorphology 136, 461–481 (2017). https://doi.org/10.1007/s00435-017-0363-x

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