Abstract
Hypoderma lineatum (Villers, 1789) (Diptera: Oestridae) is a hypodermosis fly that has resulted in great economic losses worldwide. The antennae of cattle grub males and females were examined through stereoscopic microscopy and scanning electron microscopy to reveal the general morphology, combined with distribution, type, size, and ultrastructure of the antennal sensilla. All of the three antennal segments (antennal scape, pedicel, and funiculus) possess microtrichiae on their surface. Mechanoreceptors only exist on the antennal scape and pedicel. The antennal funiculus presents four types of antennal sensilla: trichoid, basiconic, coeloconic, and clavate sensilla. Three distinctive characters of H. lineatum are obvious: (1) the relatively slender, flexible, and equal-height mechanoreceptors; (2) the enlarged antennal pedicel, and numerous antennal sensory pits and pit sensilla on the antennal funiculus; and (3) all types of antennal sensilla clustered in sensory pits, respectively. Additionally, the enlarged antennal pedicel and abundant sensory pits and pit sensilla might facilitate odor detection, enhance olfactory sensitivity and accuracy, and also protect the fragile antennal sensilla from mechanical irritation or damage.
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References
Amer A, Mehlhorn H (2006) The sensilla of Aedes and Anopheles mosquitoes and their importance in repellency. Parasitol Res 99:491–499
Ayaz MM (1998) Prevalence and treatment of goat warbles in Fort Munro and Rakni, Pakistan. Pak Vet J 18:162–164
Baker JR (1967) A review of the role played by the Hippoboscidae (Diptera) as vectors of endoparasites. J Parasitol 1967:412–418
Bromely AK, Dunn JA, Anderson M (1980) Ultrastructure of the antennal sensilla of aphids. II. Trichoid, chordotonal and campaniform sensilla. Cell Tissue Res 205:493–551
Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552
Carriço C, Mendonça PM, Cortinhas LB, Santos-Mallet JR, Carvalho-Queiroz MM (2015) Ultrastructural studies of some character of Diptera (Muscidae) of forensically importance. Acta Trop 142:96–102
Colwell DD (1989) Scanning electron microscopy of the posterior spiracles of cattle grubs Hypoderma bovis and Hypoderma lineatum. Med Vet Entomol 3:391–398
Colwell DD, Baron RW (1990) Early detection of cattle grub (Hypoderma lineatum and H. bovis) (Diptera, Oestridae) using ELISA. Med Vet Entomol 4:35–42
Colwell DD, Hall MJR, Scholl PJ (2006) The oestrid flies: biology, host-parasite relationships, impact and management. CABI Publishing, Cambridge
Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547
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
Guha L, Seenivasagan T, Bandyopadhyay P, Thanvir IS, Sathe M, Sharma P, Parashar BD, Kaushik MP (2012) Oviposition and flight orientation response of Aedes aegypti to certain aromatic aryl hydrazono esters. Parasitol Res 111:975–982
Hal H, Wall R (1995) Myiasis of humans and domestic animals. Adv Parasitol 35:257–334
Hall MJ (1995) Trapping the flies that cause myiasis: their responses to host-stimuli. Ann Trop Med Parasitol 89:333–357
Hassan M, Khan MN, Musthaq M, Iqbal Z, Farooq AA, Sajid MS, Waheed HM (2007) Prevalence of warble fly infestation in buffalo in Chakwal, Punjab. Ital J Anim Sci 6:942–944
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
Ismail IA (1964) Comparative study of sense organs in the antennae of culicine and anopheline female mosquitoes. Acta Trop 21:155
Jobling B (1928) The structure of the head and mouth-parts in the Nycteribiidae (Diptera: Pupipara). Parasitology 20:254–272
Khan MN, Sajid MS, Iqbal Z, Anwar M (2007) Emergence season of Hypoderma lineatum warbles in southern Punjab, Pakistan. Anim Sci J 78:206–210
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 54:36–42
Liu XH, Li XY, Li K, Zhang D (2015) Ultrastructure of antennal sensory organs of horse nasal-myiasis fly, Rhinoestrus purpureus (Diptera: Oestridae). Parasitol Res 114:2527–2533
McIver SB (1975) Structure of cuticular mechanoreceptors of arthropods. Annu Rev Entomol 20:381–397
Otranto D, Traversa D, Tarsitano E, Stevens J (2003) Molecular differentiation of Hypoderma bovis and Hypoderma lineatum (Diptera, Oestridae) by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP). Vet Parasitol 112:197–201
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
Panadero R, Fernández M, Vázquez L, López C, Dacal V, Cienfuegos S, Díaz P, Morrondo P, Díez-Baños P (2007) Occurrence and larval growth of Hypoderma lineatum in the oesophagi of cattle from northwest Spain: influence of geographical and climatic conditions. Med Vet Entomol 21:225–230
Panadero R, Martínez-Carrasco C, León-Vizcaíno L, López C, Díez-Baños P, Morrondo MP, Alonso F (2010) Use of a crude extract or purified antigen from first-instar cattle grubs, Hypoderma lineatum, for the detection of anti-Hypoderma antibodies in free-ranging cervids from southern Spain. Med Vet Entomol 24:418–424
Papavero N (1977) The world Oestridae (Diptera) mammals and continental drift. Springer, Hague
Poddighe S, Dekker T, Scala A, Angioy AM (2010) Olfaction in the female sheep botfly. Naturwissenschaften 97:827–835
Ross KTA (1992) Comparative stud of the antennal sensilla of five species of root maggots: Delia radicum L., D. floralis F., D. antique Mg., D. platura Mg. (Diptera: Antomyidae), and Psila rosae F. (Diptera: Psilidae). Int J Insect Morphol Embryol 21:175–197
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
Seenivasagan T, Sharma KR, Prakash S (2012) Electroantennogram, flight orientation and oviposition responses of Anopheles stephensi and Aedes aegypti to a fatty acid ester-propyl octadecanoate. Acta Trop 124:54–61
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
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
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
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
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
Webster KA, Tarry DW (1997) Warble fly in Britain—an update. In: Guthrie A, Brein D (eds) Improvements of control methods for warble fly in cattle and goats. COST, Brussels, pp 122–125
Weigl SG, Testini A, Parisi F, Dantas-Torres D, Traversa Colwell DD, Otranto D (2010) The mitochondrial genome of the common cattle grub, Hypoderma lineatum. Med Vet Entomol 24:329–335
Yadav A, Katoch R, Khajuria JK, Godara R, Agrawal R (2013) Prevalence of Hypoderma lineatum in cattle of Jammu region. J Parasit Dis 37:196–198
Zhang F, Zhang ZN (2000) Comparative study on the antennal sensilla of various forms of Myzus persicae. Acta Entomol Sin 143:131–136
Zhang D, Wang QK, Hu DF, Li K (2012a) Cuticular structures on antennae of the bot fly, Portschinskia magnifica (Diptera: Oestridae). Parasitol Res 111:1651–1659
Zhang D, Wang QK, Hu DF, Li K (2012b) Sensilla on the antennal funiculus of the stomach bot fly, Gasterophilus nigricornis (Diptera: Oestridae). Med Vet Entomol 26:314–322
Zhang D, Wang QK, Liu XH, Li K (2013a) Sensilla on antenna and maxillary palp of predaceous fly, Lispe neimongola Tian et Ma (Diptera: Muscidae). Micron 49:33–39
Zhang D, Wang QK, Yang YZ, Chen YO, Li K (2013b) Sensory organ of the antenna of two Fannia species (Diptera: Fanniidae). Parasitol Res 112:2177–2185
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 114:1887–1896
Zumpt F (1965) Myiasis in man and animals in the Old World. Butterworths, London
Acknowledgments
This study was supported by the Fundamental Research Funds for the Central Universities (No. JC2015-04), Program for New Century Excellent Talents in University (No. NCET-12-0783), Beijing Higher Education Young Elite Teacher Project (No. YETP0771), National Science Foundation of China (No. 31201741), and the State Scholarship Fund of China Scholarship Council (No. 201306515009).
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X. Y. Li, X. H. Liu, and Y. Q. Ge contributed equally to this work.
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Li, X.Y., Liu, X.H., Ge, Y.Q. et al. Scanning electron microscopy of antennal sensory organs of the cattle grub, Hypoderma lineatum (Diptera: Oestridae). Parasitol Res 114, 3865–3871 (2015). https://doi.org/10.1007/s00436-015-4617-6
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DOI: https://doi.org/10.1007/s00436-015-4617-6