Skip to main content
Log in

Ultrastructure of antennal sensory organs of horse nasal-myiasis fly, Rhinoestrus purpureus (Diptera: Oestridae)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Rhinoestrus purpureus (Brauer, 1858) (Diptera: Oestridae) is an economically important parasite that can cause severe nasal myiasis in equids or even attacking humans. The antennae of R. purpureus were examined using stereoscopic microscopy and scanning electron microscopy. The general morphology was provided detailedly, together with distribution, type, size, and ultrastructure of antennal sensilla. All the three antennal segments, antennal scape, pedicel, and funiculus, are interspersed by microtrichiae. Only mechanoreceptors are detected on antennal scape and pedicel. On antennal funiculus, three types of sensilla were observed, including basiconic sensilla, coeloconic sensilla and clavate sensilla. Two features are characterized of this host-specific bot fly: (1) numerous sensory pits with branched basiconic sensilla on antennal funiculus and (2) the absence of trichoid sensilla. The function of these distinctive traits are discussed in association with the life history. We suggest that more sensory pits with branched sensilla could increase the sensitivity of olfactory system for host orientation, while the capability of pheromone identification might be reduced due to the absence of trichoid sensilla. Besides, we support both thermo- and chemo-functions of coeloconic sensilla.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altner H, Schalle L, Stetter H, Wohlrab I (1983) Poreless sensilla with inflexible sockets: a comparative study of a fundamental type of insect sensilla probably comprising thermo- and hygroreceptors. Cell Tissue Res 234:279–307

    Article  CAS  PubMed  Google Scholar 

  • Amer A, Mehlhorn H (2006) The sensilla of Aedes and Anopheles mosquitoes and their importance in repellency. Parasitol Res 99:491–499

    Article  PubMed  Google Scholar 

  • Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552

    Article  PubMed  Google Scholar 

  • Catts EP, Garcia R (1963) Drinking by adult Cephenemyia (Diptera: Oestridae). Ann Entomol Soc Am 56:660–663

    Article  Google Scholar 

  • Catts EP (1964) Field behavior of adult Cephenemyia (Diptera: Oestridae). Can Entomol 96:579–585

    Article  Google Scholar 

  • Colwell DD, Hall MJR, Scholl PJ (2006) The Oestrid flies: biology, host-parasite relationships, impact and management. CABI Publishing, Cambridge

    Book  Google Scholar 

  • Colwell DD, Otranto D, Horak IG (2007) Comparative scanning electron microscopy of Gasterophilus third instars. Med Vet Entomol 21:255–264

    Article  CAS  PubMed  Google Scholar 

  • Clyne PJ, Certel SJ, de Bruyne M, Zaslavsky L, Johnson WA, Carlson JR (1999) The odor specificities of a subset of olfactory receptor neurons are governed by Acj6, a POU-domain transcription factor. Neuron 22:339–347

    Article  CAS  PubMed  Google Scholar 

  • Deconinck P, Pangui LJ, Githego A, Dorchies P (1996) Prévalence de Rhinoestrus usbekistanicus (Gan 1947) chezl’âne (Equus asinus) au Sénégal. Rev Elev Med Vet Pays Trop 49:38–40

    CAS  PubMed  Google Scholar 

  • Fernandes FF, Freitas EPS, Linardi PM, Pimenta PFP (2005) Ultrastructure of contact-chemoreceptor sensilla found among the genae of female Gasterophilus nasalis. J Parasitol 91:1218–1220

    Article  Google Scholar 

  • Green P, Hartenstein V (1997) Structure and spatial pattern of the sensilla of the body segments of insect larvae. Microsc Res Tech 39:470–478

    Article  CAS  PubMed  Google Scholar 

  • Grunin KYA (1959) Aggregation of bot fly males on the highest points in the locality and its cause. Zool Zhurn 38:1683–1688

    Google Scholar 

  • Guha L, Seenivasagan T, Bandyopadhyay P, Thanvir IS, Sathe M, Sharma P, Parashar BD, Kaushik MP (2012) Oviposition and flightorientation response of Aedes aegypti to certain aromatic aryl hydrazono esters. Parasitol Res 111:975–982

    Article  PubMed  Google Scholar 

  • Hall MJ (1995) Trapping the flies that cause myiasis: their responses to host-stimuli. Ann Trop Med Parasit 89:333–357

    CAS  PubMed  Google Scholar 

  • Hunter FF, Adserballe CF (1996) Cuticular structures on the antennae of Hypoderma bovis De Geer (Diptera: Oestridae) females. Int J Insect Morphol Embryol 25:173–181

    Article  Google Scholar 

  • Kaboret Y, Deconinck P, Pangui J, Akakpo J, Dorchies P (1997) Lésion de larhinoestrose spontanéeà Rhinoestrus usbekistanicus (Gan 1947) chezlesâne (Equus asinus) au Sénégal. Rev Med Vet 148:123–126

    Google Scholar 

  • Liu XH, Zhang M, Shi JN, Li K, Zhang D (2013) Ultrastructure of antennal sensilla of a parasitoid fly, Pales pavida Meigen (Diptera: Tachinidae). Micron 2013:36–42

    Article  Google Scholar 

  • McIver SB (1969) Antennal sense organs of female Culex tarsalis (Diptera: Culicidae). Ann Entomol Soc Am 62:1455–1461

    Article  CAS  PubMed  Google Scholar 

  • McIver S, Beech M (1986) Prey finding behavior and mechanosensilla of larval Toxorhynchites brevipalpis Theobald (Diptera: Culicidae). Int J Insect Morphol Embryol 15:213–225

    Article  Google Scholar 

  • Ochieng SA, Park KC, Zhu JW, Baker TC (2000) Functional morphology of antennal chemoreceptors of the parasitoid Microplitis croceipes (Hymenoptera: Braconidae). Arthropod Struct Dev 29:231–240

    Article  CAS  PubMed  Google Scholar 

  • Olson DM, Andow DA (1993) Antennal sensilla of female Trichogramma nubilale (Ertle and Davis) (Hymenoptera: Trichogrammatidae) and comparisons with other parasitic Hymenoptera. Int J Insect Morphol Embryol 22:507–520

    Article  Google Scholar 

  • Otranto D, Colwell DD, Milillo P, Marco VD, Paradies P, Napoli C, Giannetto S (2004) Report in Europe of nasal myiasis by rhinoestrus spp. in horses and donkeys: seasonal patterns and taxonomical considerations. Vet Parasitol 122:79–88

    Article  PubMed  Google Scholar 

  • Otranto D, Milillo P, Traversa D, Colwell DD (2005) Morphological variability and genetic identity in Rhinoestrus spp. causing horse nasal myiasis. Med Vet Entomol 19:96–100

    Article  CAS  PubMed  Google Scholar 

  • Papavero N (1977) The world Oestridae (Diptera) mammals and continental drift. Springer, Hague

    Book  Google Scholar 

  • Peyresblanques J (1964) Myases oculares. Annuales d’Oculistic 197:271–295

    CAS  Google Scholar 

  • Poddighe S, Dekker T, Scala A, Angioy AM (2010) Olfaction in the female sheep botfly. Naturwissenschaften 97:827–835

    Article  CAS  PubMed  Google Scholar 

  • Renthal R, Velasquez D, Olmos D, Hampton J, Wergin WP (2003) Structure and distribution of antennal sensilla of the red imported fire ant. Micron 34:405–413

    Article  PubMed  Google Scholar 

  • Ross KTA, Anderson M (1987) Morphology of the antennal sensilla of the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae). Int J Insect Morphol Embryol 16:331–342

    Article  Google Scholar 

  • Ross KTA (1992) Comparative study of the antennal sensilla of five species of root maggots: Delia radicum L., D. floralis F., D. antique Mg., D. platura Mg. (Diptera: Antomyiidae), and Psila rosae F. (Diptera: Psilidae). Int J Insect Morphol Embryol 21:175–197

    Article  Google Scholar 

  • Shanbhag SR, Singh K, Singh RN (1995) Fine structure and primary sensory projections of sensilla located in the sacculus of the antenna of Drosophila melanogaster. Cell Tissue Res 282:237–249

    Article  CAS  PubMed  Google Scholar 

  • Shanbhag SR, Muller B, Steinbrecht RA (2000) Atlas of olfactory organs of Drosophila melanogaster. 2. Internal organization and cellular architecture of olfactory sensilla. Arthropod Struct Dev 29:211–229

    Article  CAS  PubMed  Google Scholar 

  • Smallegange RC, Kelling RJ, Den Otter CJ (2008) Types and numbers of sensilla on antennae and maxillary palps of small and large houseflies, Musca domestica (Diptera, Muscidae). Microsc Res Tech 71:880–886

    Article  PubMed  Google Scholar 

  • Sukontason K, Sukontason KL, Piangjai S, Boonchu N, Chaiwong T, Ngern-klun R, Sripakdee D, Vogtsberger RC, Olson JK (2004) Antennal sensilla of some forensically important flies in families Calliphoridae, Sarcophagidae and Muscidae. Micron 35:671–679

    Article  PubMed  Google Scholar 

  • Sukontason K, Sukontason KL, Vogtsberger RC, Boonchu N, Chaiwong T, Piangjai S, Disney H (2005) Ultrastructure of Coeloconic Sensilla on Postpedicel and Maxillary Palp of Megaselia scalaris (Diptera: Phoridae). Ann Entomol Soc Am 98:113–118

    Article  Google Scholar 

  • Sukontason K, Methanitikorn R, Chaiwong T, Kurahashi H, Vogtsberger RC, Sukontason KL (2007) Sensilla of the antenna and palp of Hydrotaea chalcogaster (Diptera: Muscidae). Micron 38:218–223

    Article  PubMed  Google Scholar 

  • Tibayrenc R, Garba D, Dorchies P (1999) Prévalence de Rhinoestrus usbekistanicus (Gan 1947) chezl’âne (Equus asinus) dans larégion de Niamey, Niger. Rev Elev Med Vet Pays Trop 52:113–115

    Google Scholar 

  • Ullrich H (1939) Zur Biologie der Rachenbremsen unseres einheimischen Wildes, Genus Cephenomyia Latreille und Genus Pharyngomyia Schiner. Verh VII int Kongr Ent 3:2149–2171

    Google Scholar 

  • Wang X, Zhong M, Wen J, Cai J, Jiang H, Li Y, Al SM, Xiong F (2012) Molecular characterization and expression pattern of an odorant receptor from the myiasis-causing blowfly, Lucilia sericata (Diptera: Calliphoridae). Parasitol Res 110:843–851

    Article  PubMed  Google Scholar 

  • Wang QK, Yang YZ, Liu MQ, Zhang D (2014) Fine structure of Delia platura (Meigen) (Diptera: Anthomyiidae) revealed by scanning electron microscopy. Microsc Res Tech 77:619–630

    Article  PubMed  Google Scholar 

  • Zacharuk RY (1985) Antennal sensilla. In: Kerkut GA, Gilbert LI (eds) Comparative insect physiology, biochemistry and pharmacology, vol 6. Pergamon, Oxford, pp 1–69

    Google Scholar 

  • Zayed AA (1992) Studies on Rhinoestrus purpureus (Diptera: Oestridae) larvae infesting donkeys (Equus asinus) in Egypt. III. Pupal duration under controlled conditions. Vet Parasitol 44:285–290

    Article  CAS  PubMed  Google Scholar 

  • Zayed AA, Hilali ME, Metenawy TM (1993) Studies on Rhinoestrus purpureus (Diptera: Oestridae) larvae infesting donkeys (Equus asinus) in Egypt. J Equine Vet Sci 13:46–49

    Article  Google Scholar 

  • Zhang D, Wang QK, Hu DF, Li K (2012a) Sensilla on the antennal funiculus of the stomach bot fly, Gasterophilus nigricornis (Diptera: Oestridae). Med Vet Entomol 26:314–322

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Wang QK, Hu DF, Li K (2012b) Cuticular structures on antennae of the bot fly, Portschinskia magnifica (Diptera: Oestridae). Parasitol Res 111:1651–1659

    Article  PubMed  Google Scholar 

  • Zhang D, Wang QK, Yang YZ, Chen YO, Li K (2013a) Sensory organs of the antenna of two medically and hygienically important Fannia species (Diptera: Fanniidae). Parasitol Res 112:2177–2185

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Liu XH, Li XY, Zhang M, Li K (2013b) Antennal sensilla of the green bottle fly, Lucilia sericata (Meigen) (Diptera: Calliphoridae). Parasitol Res 112:3843–3850

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Wang QK, Liu XH, Li K (2013c) Sensilla on antenna and maxillary palp of predaceous fly, Lispe neimongola Tian et Ma (Diptera: Muscidae). Micron 49:33–39

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Liu XH, Li XY, Cao J, Chu HJ, Li K (2015) Ultrastructural investigation of antennae in three cutaneous myiasis flies: Melophagus ovinus, Hippobosca equina, and Hippobosca longipennis (Diptera: Hippoboscidae). Parasitol Res doi:10.1007/s00436-015-4376-4

  • Zumpt F (1965) Myiasis in man and animals in the Old World. Butterworths, London

    Google Scholar 

Download references

Acknowledgments

This study was supported by the Beijing Higher Education Young Elite Teacher Project (no. YETP0771), Program for New Century Excellent Talents in University (no. NCET-12-0783).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Zhang.

Additional information

X. H. Liu and X. Y. Li contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X.H., Li, X.Y., Li, K. et al. Ultrastructure of antennal sensory organs of horse nasal-myiasis fly, Rhinoestrus purpureus (Diptera: Oestridae). Parasitol Res 114, 2527–2533 (2015). https://doi.org/10.1007/s00436-015-4453-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4453-8

Keywords

Navigation