, Volume 136, Issue 4, pp 461–481 | Cite as

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

  • Haiying Zhong
  • Yalin Zhang
  • Cong Wei
Original paper


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.


Cicadomorpha Female Genitalia Ultrastructure Sensilla Taxonomy 



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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. 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 215:289–308PubMedGoogle Scholar
  2. 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 81:2032–2037CrossRefGoogle Scholar
  3. Boulard M (1965) L’appareil génital ectodermique des Cigales femelles. Ann Soc Entomol Fr 1:797–812Google Scholar
  4. Boulard M (1973) Les Ydiellinae: sous-famille nouvelle de cigales Platypediidae: Clé des familles et sous-familles des Homoptères Cicadoidea. Ann Soc Entomol Fr 9:841–852Google Scholar
  5. 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 10:399–407CrossRefGoogle Scholar
  6. Boulard M (1976b) Sur une deuxième cigale africaine dépourvue d’appareil sonore (Homoptera). Bulletin l’Institut Fondamental d’Afrique Noire Série A 37:629–636Google Scholar
  7. 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 5–72Google Scholar
  8. Bowen MF (1995) Sensilla basiconica (grooved pegs) on the antennae of female mosquitoes: electrophysiology and morphology. Entomol Exp Appl 77:233–238CrossRefGoogle Scholar
  9. Chadha GK, Roome RE (1980) Oviposition behaviour and the sensilla of the ovipositor of Chilo partellus and Spodoptera littoralis (Lepidoptera: Noctuidae). J Zool 192:169–178CrossRefGoogle Scholar
  10. Chou I, Lei Z, Li L, Lu X, Yao W (1997) The Cicadidae of China (Homoptera: Cicadoidea). Tianze Eldoneio, Hong KongGoogle Scholar
  11. Davis EE, Sokolove PG (1975) Temperature responses of antennal receptors of the mosquito, Aedes aegypti. J Comp Physiol 96:223–236CrossRefGoogle Scholar
  12. 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 43:705–719CrossRefPubMedGoogle Scholar
  13. Dietrich CH (1989) Surface sculpturing of the abdominal integument of Membracidae and other Auchenorrhyncha (Homoptera). P Entomol Soc Wash 91:143–152Google Scholar
  14. Dweck HK, Gadallah NS, Darwish E (2008) Structure and sensory equipment of the ovipositor of Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Micron 39:1255–1261CrossRefPubMedGoogle Scholar
  15. Emeljanov AF (2014) The evolutionary role and fate of the primary ovipositor in insects. Entomol Rev 94:367–396CrossRefGoogle Scholar
  16. 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 20:291–307CrossRefGoogle Scholar
  17. Gillott C (2005) Entomology, 3rd edn. Springer, NetherlandsGoogle Scholar
  18. 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 95:67–74CrossRefGoogle Scholar
  19. Hallberg E, Ahman I (1987) Sensillar types of the ovipositor of Dasineura brassicae: structure and relation to oviposition behaviour. Physiol Entomol 12:51–58CrossRefGoogle Scholar
  20. 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 5:171–184CrossRefPubMedGoogle Scholar
  21. Hilsman I (1921) The ovipositor of the cicada. Dissertation. University of Kansas, LawrenceGoogle Scholar
  22. Hummel NA, Zalom FG, Peng CYS (2006) Structure of female genitalia of glassy-winged sharpshooter, Homalodisca coagulata (Say) (Hemiptera: Cicadellidae). Arthropod Struct Dev 35:111–125CrossRefPubMedGoogle Scholar
  23. King PE, Fordy MR (1970) The external morphology of the ‘pore’ structures on the tip of the ovipositor in Hymenoptera. Entomol Mon Mag 106:64–66Google Scholar
  24. Kramer S (1950) The morphology and phylogeny of Auchenorrhynchous Homortera (Insecta). Ill Biol Monogr 20:i–vii, 1–111Google Scholar
  25. Kudryasheva IV (1979) Larvae of song cicadas (Homoptera, Cicadidae) of the USSR fauna. Nauka, Moscow, p 159Google Scholar
  26. 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 258:54–68CrossRefGoogle Scholar
  27. Liang AP, Fletcher JM (2002) Morphology of the antennal sensilla in four Australian spittlebug species (Hemiptera: Cercopidae) with implications for phylogeny. Aust J Entomol 41:39–44CrossRefGoogle Scholar
  28. 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 87:50–54Google Scholar
  29. Maier CT (1980) A mole’s-eye view of seventeen-year periodical cicada nymphs, Magicicada septendecim (Hemiptera: Homoptera: Cicadidae). Ann Entomol Soc Am 73:147–152CrossRefGoogle Scholar
  30. Mciver SB (1985) Mechanoreception. In: Kerkut GA, Gilbert LI (eds) Comparative insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 71–132Google Scholar
  31. 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 15:451–544CrossRefGoogle Scholar
  32. 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 27:813–819CrossRefGoogle Scholar
  33. Meng Z, Yang M (2012) Female genitalia of Seasogonia Young from China, with a new synonym and a new record (Hemiptera, Cicadellidae, Cicadellini). Zookeys 164:24–40CrossRefGoogle Scholar
  34. 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 33:429–440CrossRefPubMedGoogle Scholar
  35. Miller F, Crowley W (1998) Effects of periodical cicada ovipositional injury on woody plants. J Arboric 24:248–253Google Scholar
  36. Moulds MS (2005) An appraisal of the higher classification of cicadas (Hemiptera: Cicadoidea) with special reference to the Australian fauna. Rec Aust Mus 57:375–446CrossRefGoogle Scholar
  37. Müller HJ (1942) Über bau und funktion des legeapparates der zikaden (Homoptera Cicadina). Zoomorphology 38:534–629CrossRefGoogle Scholar
  38. Myers JG (1928) The morphology of the Cicadidae (Homoptera). Proc Zool Soc Lond 2:365–472Google Scholar
  39. Nielson MW (1965) A revision of the genus Cuerna (Homoptera, Cicadellidae). Technical bulletin of the United States Department of Agriculture 1318:1–48Google Scholar
  40. Oberdorster U, Grant PR (2006) Predicting emergence, chorusing, and oviposition of periodical cicadas. Ecology 87:409–418CrossRefPubMedGoogle Scholar
  41. Ostry ME, Anderson NA (1983) Infection of trembling aspen by Hypoxylon mammatum through cicada oviposition wounds. Phytopathology 73:1092–1096CrossRefGoogle Scholar
  42. 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 1:241–251CrossRefGoogle Scholar
  43. Readio PA (1922) Ovipositors of the Cicadellidae (Homoptera). University of Kansas, LawrenceGoogle Scholar
  44. Rebora M, Piersanti S, Dell’otto A, Gaino E (2013) The gustatory sensilla on the endophytic ovipositor of Odonata. Arthropod Struct Dev 42:127–134CrossRefPubMedGoogle Scholar
  45. Rodrigues LGN, Mejdalani G (2009) Description of the Aguatala compsa Young (Hemiptera: Cicadellidae: Cicadellinae) female. Neotrop Entomol 38:508–511CrossRefPubMedGoogle Scholar
  46. Sanborn AF (2013) Catalogue of the Cicadoidea (Hemiptera: Auchenorrhyncha). Academic Press, LondonGoogle Scholar
  47. 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 10:27–28Google Scholar
  48. Schneider D (1964) Insect antennae. Annu Rev Entomol 9:103–122CrossRefGoogle Scholar
  49. Scudder GGE (1957) Reinterpretation of some basal structures in the insect ovipositor. Nature 180:340–341CrossRefGoogle Scholar
  50. Scudder GGE (1961a) The comparative morphology of the insect ovipositor. Ecol Entomol 113:25–40Google Scholar
  51. Scudder GGE (1961b) The functional morphology and interpretation of the insect ovipositor. Can Entomol 93:267–272CrossRefGoogle Scholar
  52. Scudder GGE (1964) Further problems in the interpretation and homology of the insect ovipositor. Can Entomol 96:405–417CrossRefGoogle Scholar
  53. 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 77:302–313CrossRefGoogle Scholar
  54. 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 55:307–329CrossRefPubMedPubMedCentralGoogle Scholar
  55. Smith FF, Linderman RG (1974) Damage to ornamental trees and shrubs resulting from oviposition by periodical cicada. Environ Entomol 3:725–732CrossRefGoogle Scholar
  56. Snodgrass RE (1926) Morphology of the insect abdomen. Smithsonian Institution City of Washington, Washington, DCGoogle Scholar
  57. 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 3:1–7CrossRefGoogle Scholar
  58. Weber H (1930) Biologie der Hemipteren. Julius Springer, BerlinCrossRefGoogle Scholar
  59. Williams KS, Simon C (1995) The ecology, behavior, and evolution of periodical cicadas. Ann Rev Entomol 40:269–295CrossRefGoogle Scholar
  60. Yokohari F, Tominaga Y, Tateda H (1982) Antennal hygroreceptors of the honey bee, Apis mellifera L. Cell Tissue Res 226:63–73CrossRefPubMedGoogle Scholar
  61. Zacharuk RY (1985) Antennae and sensilla. In: Kerkut GA, Gilbert LI (eds) Comparative insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 1–69Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, Entomological MuseumNorthwest A&F UniversityYanglingChina
  2. 2.State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and MicrobiologyZhejiang Academy of Agricultural SciencesHangzhouChina

Personalised recommendations