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Sensilla of haematophagous insects sensitive to vertebrate host-associated stimuli

Published online by Cambridge University Press:  19 September 2011

Susan B. McIver
Affiliation:
Department of Environmental Biology, University of Guelph, Guelph, Ontario, Canada N1G 2W1
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Abstract

The morphology of the sensilla sensitive to vertebrate host-associated stimuli is diverse reflecting the numerous independent origins of haematophagy within the insects. Using electron microscopic techniques, the sensilla of mosquitoes and blackflies have been the most thoroughly studied, although numerous works have been conducted on other blood-feeders. Notably lacking are fine structure studies on blood-feeding maggots and ectoparasitic, adult Muscomorpha.

In comparing blood-feeders with other insects it becomes apparent that: (1) carbon dioxide plays a significantly greater role in location of food by haematophagous insects than by phytophagous and saprophagous species; (2) only in blood-feeders do the adenosine phosphate nucleotides, a single group of compounds, appear to be the phagostimulants for almost all species; and (3) feeding deterrents are unknown in haematophagous insects.

When the sensory complements of the various groups of blood-feeders are compared, three points emerge. First, reduction in numbers of olfactory chemosensilla that mediate odour cues used in long-distance, host-orientation occurs in male nematocerans and in females of completely autogenous species of mosquitoes and black flies. Second, there is a striking correlation between the number of labial chemo- and mechanosensilla and the feeding behaviour of the insect. Third, there is a possible positive correlation between the number of chemosensitive antennal neurones and the distance travelled by the insect to the host.

Résumé

La morphologie des sensilles associés à la recherche d'hôtes vertébrés est variée, ce qui reflète les diverses origines de l'hématophagie chez les insectes. Utilisant la microscopie électronique, les sensilles des moustiques et mouches noires ont été étudiés en détail, en parallèle, de nombreux autres travaux ont porté sur d'autres espèces hématophages. La description de l'ultrastructure des sensilles d'asticots hématophages et ectoparasites a jusqu'à présent été négligée.

En comparant les insectes hématophages avec les autres insectes non hématophages il devient apparent que; (1) le dioxide de carbone joue un rôle beaucoup plus important chez les hématophages que chez les phytophages et les détritivores, (2) les nucleotides adénosine phosphates agissent en tant que phagostimulants seulement chez les hématophages, ce chez presque toutes les espèces et (3) il n'y a aucun agent phago répresseur identifié a ce jour chez les hématophages.

Trois phénomènes émergent lorsqu'on compare les processus sensitifs de divers groupes d'insectes hématophages. Preièrement, la réduction du nombre des chemosensilles olfactifs qui captent les stimuli olfactifs sur de longues distances, l'orientation vers l'hôte se produit aussi bien chez les mâles et femelles d'espèces autogènes de mostiques et de mouches noires. Deuxièmement, il y a une corrélation évidente entre le nombre de chemo- et mécano-sensilles labiaux et le comportement alimentaire des insectes. Troisièmement, il y a la possibilité d'une corrélation positive entre le nombre de neuronnes chemosensitifs des antennes et la distance parcourue par l'insecte pour atteindre l'hôte.

Type
Symposium V: Host-seeking Mechanisms of Arthropods of Medical and Veterinary Importance
Copyright
Copyright © ICIPE 1987

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References

REFERENCES

Adams, J. R., Holbert, P. E. and Forgash, A. J. (1965) Electron microscopy of the contact chemoreceptors of the stable fly, Stomoxys calcitrans (Diptera: Muscidae). Ann. Ent. Soc. Am. 58, 909917.CrossRefGoogle ScholarPubMed
Amrine, J. W. and Jerabek, M. A. (1983) Possible ultrasonic receptors on fleas. Ann. Ent. Soc. Am. 76, 395399.CrossRefGoogle Scholar
Amrine, J. W. and Lewis, R. E. (1978) The topography of the exoskeleton of Cediopsylla simplex (Baker 1895) (Siphonaptera: Pulicidae). 1. The head and its appendages. J. Parasitol. 64, 343358.CrossRefGoogle Scholar
Amrine, J. W. and Lewis, R. E. (1986) The topography of the exoskeleton of Cediopsylla simples (Baker, 1895) (Siphonaptera: Pulicidae): The thorax, abdomen, and associated appendages. J. Parasitol. 72, 7177.CrossRefGoogle Scholar
Baldwin, W. F., Knight, A. G. and Lynn, K. R. (1971) A sex pheromone in the insect Rhodnius prolixus (Hemiptera: Reduviidae). Can. Ent. 103, 1822.CrossRefGoogle Scholar
Bernard, J. (1974) Étudé électrophysiologie de récepteurs impliqués dans l'orientation vers l'hôte et dans l'acte hémaphage chez un Hémiptère: Triatoma infestons. Thèse, Université de Rennes.Google Scholar
Burgess, L. and Rempel, J. G. (1964) The stomodaeal nervous system, neuro-secretion, and related endocrine and nervous structures In Aedes aegypti (L.) (Diptera: Culicidae). Can. Ent. 96, 105106.CrossRefGoogle Scholar
Burgess, L. and Rempel, J. G. (1966) The stomodaeal nervous system, the neuro-secretory system, and the gland complex in Aedes aegypti (L.) (Diptera: Culicidae). Can. J. Zool. 44, 731765.CrossRefGoogle Scholar
Carr, W. S., Gleeson, R. A., Ache, B. W. and Milstead, M. L. (1986) Olfactory receptors of the spiny lobster: ATP-sensitive cells with similarities to P2-type purinoceptors of vertebrates. J. Comp. Physiol. A158, 331338.CrossRefGoogle Scholar
Chaika, S. Yu (1980a) Chemoreceptor organs of antennae and maxillary palps of fleas (Siphonaptera). Parazitologiya 14, 319325 [In Russian].Google Scholar
Chaika, S. Yu (1980b) Ultrastructure of the antennal sensilla of the bug Rhodnius prolixus. Parazitologiya 14, 486492. (In Russian).Google ScholarPubMed
Chapman, R. F. (1982) Chemoreception: The significance of receptor numbers., Adv. Insect. Physiol. 16, 247356.CrossRefGoogle Scholar
Childress, S. A. and Mclver, S. B. (1984) Morphology of the deutocerebrum of female Aedes aegypti (Diptera: Culicidae). Can. J. Zool. 62, 13201328.CrossRefGoogle Scholar
Chu-Wang, I.-W., Axtell, R. C. and Kline, D. L. (1975) Antennal and palpal sensilla of the sandfly Culicoides furens (Poey) (Diptera: Ceratopogonidae). Int. J. Insect Morphol. Embryol. 4, 131149.CrossRefGoogle Scholar
Christophers, S. R. (1960) Aedes aegypti (L.) The Yellow Fever Mosquito. Its Life History, Bionomics and Structure. Cambridge University Press.Google Scholar
Clements, A. N. (1963) The Physiology of Mosquitoes. Pergamon Press, London.Google Scholar
Davis, E. E. and Sokolove, P. G. (1975) Temperature responses of the Antennal receptors of the mosquito, Aedes aegypti. J. Comp. Physiol. 96, 223233.CrossRefGoogle Scholar
Dethier, V. G. (1976) The Hungry Fly. Cambridge, Mass., Harvard University Press.Google Scholar
Doane, J. E. and Klingler, J. (1978) Location of CO2-receptive sensilla on larvae of the wireworms Agriotes lineatus-obscurus and Limonius californicus. Ann. Ent. Soc. Am. 71, 357363.CrossRefGoogle Scholar
Downes, J. A. (1971) The ecology of blood-sucking Diptera: An evolutionary perspective. In Ecology and Physiology of Parasites. (Edited by Fallis, A. M.) pp. 232258. Univ. Toronto Press.CrossRefGoogle Scholar
Elizarov Yu, A. and Chaika, S. Yu (1977) Ultrastructure of olfactory sensillae of the blood-sucking horse-flies (Diptera, Tabanidae). Ent. Obozr. 56, 283291.Google Scholar
Flanagan, T. (1984) Wholemount histofluorescence of catecholamine-containing neurones in a hemipteran brain. J. Insect Physiol. 30, 697704.CrossRefGoogle Scholar
Friend, W. G. and Smith, J. J. B. (1977) Factors affecting feeding by blood-sucking insects. A. Rev. Ent. 22, 309331.CrossRefGoogle Scholar
Galun, R. (1975) The role of host blood in the feeding behavior of ectoparasites. In Sensory Physiology and Behavior, (Edited by Galun, R., Human, P., Parnas, I. and Werman, R.), pp. 211221. New York, Plenum.CrossRefGoogle Scholar
Galun, R., Koontz, L. C. and Gwadz, R. W. (1985) Engorgement response of anopheline mosquitoes to blood fraction and artificial solutions. Physiol. Ent. 10, 145149.CrossRefGoogle Scholar
Greenwood, M. T. and Holdich, D. M. (1979) A structural study of the sensillum of two species of bird flea, Ceratophyllus (Insecta: Siphonaptera). J. Zool., Lond. 187, 2138.CrossRefGoogle Scholar
Harwood, R. F. and James, M. T. (1979) Entomology in Human and Animal Health. 7th ed. Macmillan. Toronto.Google Scholar
Hennig, W. (1969) Die Strammesgeschichte der Insekten. Frankfurt am Main, waldemar Kramer.Google Scholar
Hinke, W. (1961) Das relative postembryonale Wachstum der hirnteile von Culex pipiens, Drosophila melanogaster und Drosophila -mutanten. Z. Morphol. Oekol. Tiere 50, 81118.CrossRefGoogle Scholar
Hodgson, E. S. (1968) Taste receptors in arthropods. Symp. Zool. Soc. London 23, 269277.Google Scholar
Kellogg, F. E. (1970) Water vapor and carbon dioxide receptors In Aedes aegypti (L.). J. Insect. Physiol. 16, 99108.CrossRefGoogle Scholar
Lacher, V. (1964) Elektrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, Kohlendioxyd, Luftfeuchtigkeit und Temperatur auf den Antennen Arbeitsbiene und der Drohne (Apis mellifica L.) Z. Vgl. Physiol. 48, 274278.CrossRefGoogle Scholar
Lall, S. B. (1970) Loci, structure and function of contact chemical sensilla in haematophagous tabanids (Diptera). J. Med. Ent. 7, 205222.CrossRefGoogle ScholarPubMed
Lee, R. M. K. W. and Craig, D. A. (1983a) Cibarial sensilla and armature in mosquito adults (Diptera: Culicidae). Can. J. Zool. 61, 633646.CrossRefGoogle Scholar
Lee, R. M. K. L. and Craig, D. A. (1983b) The labrum and labral sensilla of mosquitoes (Diptera: Culicidae): a scanning electron microscope study. Can. J. Zool. 61, 15681579.CrossRefGoogle Scholar
Lent, H. and Wygodzinsky, P. (1979) Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas' disease. Bull. Am. Museum Nat. Hist. 163, 123520.Google Scholar
Levinson, H. Z. and Bar Ilan, A. R. (1971) Assembling and altering scents produced by the bedbug Cimex lectularius L. Experientia 27, 102103.CrossRefGoogle Scholar
Levinson, H. Z., Levinson, A. R., Müller, B. and Steinbrecht, R. A. (1974) Structure of sensilla, olfactory perception, and behaviour of the bed bug, Cimex lectularius, in response to its alarm pheromone. J. Insect Physiol. 20, 12311248.CrossRefGoogle ScholarPubMed
Lewis, C. T. (1970) Structure and function in some external receptors. Symp. Roy. Ent. Soc. London 5, 5976.Google Scholar
Lewis, C. T. (1971) Superficial sense organs of the antennae of the fly, Stomoxys calcitrans. J. Insect Physiol. 17, 449461.CrossRefGoogle Scholar
Lyal, C. H. C. (1985) Phylogeny and classification of the Psocodea with particular reference to the lice (Psocodea: Phthiraptera). Syst. Ent. 10, 145164.CrossRefGoogle Scholar
Mclver, S. B. (1972) Fine structure of pegs on the palps of female culicine mosquitoes. Can. J. Zool. 50, 571576.CrossRefGoogle Scholar
Mclver, S. (1978) Structure of sensilla trichodea of female Aedes aegypti with comments on innervation of antennal sensilla. J. Insect Physiol. 24, 383390.CrossRefGoogle Scholar
Mclver, S. B. (1980) Sensory aspects of mate-finding behavior in male mosquitoes (Diptera: Culicidae). J. Med. Ent. 17, 5457.CrossRefGoogle Scholar
Mclver, S. B. (1982) Sensilla of mosquitoes (Diptera: Culicidae). J. Med. Ent. 19, 489535.CrossRefGoogle Scholar
Mclver, S. B. and Hudson, A. (1972) Sensilla on the antennae and palps of selected Wyeomyia mosquitoes. J. Med. Ent. 9, 337345.CrossRefGoogle Scholar
Mclver, S. and Siemicki, R. (1975) Palpal sensilla of selected anopheline mosquitoes. J. Parasitol. 61, 535538.CrossRefGoogle Scholar
Mclver, S. and Siemicki, R. (1984a) Fine structure of pegs on the maxillary palps of adult Toxorhynchites brevipalpis Theobald (Diptera: Culicidae). Int. J. Insect Morphol. Embryol. 13, 1120.CrossRefGoogle Scholar
Mclver, S. and Siemicki, R. (1984b) Fine structure of antennal mechanosensilla of adult Rhodnius prolixus St 1 (Hemiptera: Reduviidae). J. Morphol. 180, 1928.CrossRefGoogle Scholar
Mclver, S. and Siemicki, R. (1985) Fine structure of antennal putative thermo-/hygrosensilla of adult Rhodnius prolixus St 1 (Hemiptera: Reduviidae). J. Morphol. 183, 1523.CrossRefGoogle Scholar
Mclver, S., Siemicki, R. and Sutcliffe, J. (1980) Bifurcate sensilla on the tarsi of female blackflies, Simulium venustum (Diptera: Simuliidae): Contact chemosensilla adapted for olfaction? J. Morphol. 165, 111.CrossRefGoogle Scholar
Mclver, S. B. and Sutcliffe, J. R. (1986) Sensory basis of behavior and structural adaptations for feeding in blackflies (Diptera: Simuliidae). In Black Flies: Ecology, Population Management, and Annotated World List (Edited by Kim, K. C. and Merrit, ). Penn. State Univ. Press. (in Press).Google Scholar
McKeever, S. and Pound, J. M. (1979) The mouthparts of female Corethrella brakeleyi and C. wirthi (Diptera: Chaoboridae). J. Morphol. 161, 157168.CrossRefGoogle Scholar
Medvedev, S. G. (1982) Peculiarities of the structure of antennae in fleas (Siphonaptera) and their use in systematics. I. Ent. Obozr. 61, 418427. (see Ent. Rev. 61, 170–184).Google Scholar
Mercer, K. L. and Mclver, S. B. (1973a) Studies on the antennal sensilla of selected blackflies (Diptera: Simuliidae). Can. J. Zool. 51, 729734.CrossRefGoogle ScholarPubMed
Mercer, K. L. and Mclver, S. B. (1973b) Sensilla on the palps of selected blackflies (Diptera: Simuliidae). J. Med. Ent. 10, 236239.CrossRefGoogle ScholarPubMed
Miller, F. H. Jr (1969) Antennal tuft organs of Pediculus humanus Linn, and Phthirus pubis (Linn.) (Anoplura: Pediculidae). J.N.Y. Ent. Soc. 77, 8589.Google Scholar
Miller, F. H. Jr (1970a) Scanning electron microscopy of antennal structures of Polyplax serrata (Burmeister) (Anoplura: Hoplopleuridae). J.N. Y. Ent. Soc. 78, 3337.Google Scholar
Miller, F. H. Jr (1970b) Scanning electron microscopy of Solenopotes capillatus Enderlein (Anoplura: Linognathidae). J.N.Y. Ent. Soc. 78, 139145.Google Scholar
Miller, F. H. Jr (1971a) Scanning electron microscopy of antennal structures of five Haematopinus (Anoplura: Haematopinidae). J.N.Y. Ent. Soc. 79, 1926.Google Scholar
Miller, F. H. Jr (1971b) Scanning electron microscopy of Echnophthirus horridus (von Olfers), Antarctophthirus callorhini (Osborn), and Proechinophthirus fluctus (Ferris) with emphasis on the antennal structures (Anoplura: Echinophthiriidae). J. Parasitol. 57, 668674.CrossRefGoogle Scholar
Mitchell, B. K. (1976) ATP reception by the tsetse fly, Glossina morsitans West. Experientia 32, 192193.CrossRefGoogle ScholarPubMed
Molyneux, D. H. (1980) Host-trypanosome interactions in Glossina. Insect Sci. Applic. 1, 3946.Google Scholar
Molyneux, D. H. and Jenni, L. (1981) Mechanoreceptors, feeding behaviour and trypanosome transmission in Glossina. Trans. Roy. Soc. Trop. Med. Hyg. 75, 160162.CrossRefGoogle ScholarPubMed
Molyneux, D. H., Lavin, D. R. and Elce, B. (1979) A possible relationship between Salivarian trypanosomes and Glossina labrum mechano-receptors. Ann. Trop. Med. Parasitol. 73, 287290.CrossRefGoogle ScholarPubMed
Muhammed, S., Butler, J. F. and Carlson, D. A. (1975) Stablefly sex attractant and mating pheromone found in female body hydrocarbons. J. Chem. Ecol. 1, 387398.CrossRefGoogle Scholar
O'Grady, G. E. and Mclver, S. B. (1987) Fine structure of the compound eye of the blackfly, Simulium vittatum (Diptera: Simuliidae)., Can. J. Zool. (in press).CrossRefGoogle Scholar
Paysinger, J. T., Noblet, R., Adkins, T. R. Jr and Vaughn, E. A. (1978) Scanning electron microscopy of the adult mouthparts of the hornfly and the facefly. J. Georgia Ent. Soc. 13, 2839.Google Scholar
Peterson, B. V. (1959) Notes on the biology of some species of Utah blackflies (Diptera: Simuliidae). Mosq. News 19, 8690.Google Scholar
Popham, E. J. and Abdillahi, M. (1979) Labellar microstructure in tsetse flies (Glossinidae). Syst. Ent. 4, 6570.CrossRefGoogle Scholar
Puchkova, L. V. and Smolina, N. A. (1979) Deutocerebrum of bloodsucking mosquitoes (Culicidae) and its neuronal connections. Dokl. Akad. Nauk. Ukr. USSR No. 10, pp. 863865.Google Scholar
Reinouts van Haga, H. A. and Mitchell, B. K. (1975) Temperature receptors on tarsi of the tsetse fly Glossina morsitans West. Nature 255, 225226.CrossRefGoogle ScholarPubMed
Rice, M. J., Galun, R. and Margalit, J. (1973a) Mouthpart sensilla of the tsetse fly and their function II: Labial sensilla. Ann. Trop. Med. Parasitol. 67, 101107.CrossRefGoogle ScholarPubMed
Rice, M. J., Galun, R. and Margalit, J. (1973b) Mouthpart sensilla of the tsetse fly and their function III: Labrocibarial sensilla. Ann. Trop. Med. Parasitol. 67, 109116.CrossRefGoogle Scholar
Rowley, W. A. and Cornford, M. (1972) Scanning electron microscopy of the pit of the maxillary palp of selected species of Culicoides. Can. J. Zool. 50, 12071210.CrossRefGoogle Scholar
Schofield, C. J. and Patterson, J. W. (1977) Assembly pheromone of Triatoma infestans and Rhodnius prolixus nymphs (Hemiptera: Reduviidae). J. Med. Ent. 13, 727734.CrossRefGoogle ScholarPubMed
Schuh, R. T. (1986) The influence of cladistics on heteropteran classification. A. Rev. Ent. 31, 6793.CrossRefGoogle Scholar
Seifert, P., Wunderer, H. and Smola, U. (1985) Regional differences in a nematoceran retina (Insecta, Diptera). Zoomorphology 105, 99107.CrossRefGoogle Scholar
Settembrini, B. P. (1984) The compound eyes of Triatoma infestans and Rhodnius prolixus (Hemiptera: Redviidae). J. Med. Ent. 21, 477479.CrossRefGoogle Scholar
Shevchenko, A. K. and Djafarov, SH. M. (1968) Sensillae on the antennae of blood-sucking biting midges (Diptera, Ceratopogonidae). Zool. Zhurn. 47, 145148. [In Russian, English summary].Google Scholar
Slifer, E. H. (1962) Sensory hairs with permeable tips on the tarsi of the yellow-fever mosquito, Aedes aegypti. Ann. Ent. Soc. Am. 55, 531535.Google Scholar
Slifer, E. (1980) Chemoreceptors and other sense organs on the antennal flagellum of the flea, Ctenocephalides canis (Siphonaptera: Pulicidae). Ann Ent. Soc. Am. 73, 418419.CrossRefGoogle Scholar
Slifer, E. H. and Sekhon, S. S. (1980) Sense organs on the antennal flagellum of the human louse, Pediculus humanus (Anoplura). J. Morphol. 164, 161166.CrossRefGoogle ScholarPubMed
Smith, S. A. and Clay, M. E. (1985) Morphology of the antennae of the bat flea Myodopsylla insignis (Siphonaptera: Ischnopsyllidae). J. Med. Ent. 22, 6471.CrossRefGoogle Scholar
Steinbrecht, R. A. and Müller, B. (1976) Fine structure of the antennal receptors of the bed bug, Cimex lectularius L. Tissue Cell 8, 615636.CrossRefGoogle ScholarPubMed
Stoffolano, J. G. Jr and Yin, L. R. S. (1983) Comparative study of the mouthparts and associated sensilla of adult male and female Tabanus nigrovittatus (Diptera: Tabanidae). J. Med. Ent. 20, 1132.CrossRefGoogle Scholar
Sutcliffe, J. F. (1985) Anatomy of membranous mouthpart cuticles and their roles in feeding in blackflies (Diptera: Simuliidae). J. Morphol. 186, 5368.CrossRefGoogle Scholar
Sutcliffe, J. F. and Mclver, S. B. (1976) External morphology of sensilla on the legs of selected blackfly species (Diptera: Simuliidae). Can. J. Zool. 54, 17791787.CrossRefGoogle ScholarPubMed
Sutcliffe, J. F. and Mclver, S. B. (1982) Innervation and structure of mouthpart sensilla in females of the blackfly Simulium venustum (Diptera: Simuliidae). J. Morphol. 171, 245258.CrossRefGoogle ScholarPubMed
Sutcliffe, J. F. and Mclver, S. B. (1984) Mechanics of blood-feeding in blackflies (Diptera, Simuliidae). J. Morphol. 180, 125144.CrossRefGoogle ScholarPubMed
Sutcliffe, J. F. and Mclver, S. B. (1987) Fine structure of tarsal sensilla of male and female Simulium vittatum (Diptera: Simuliidae). J. Morphol. 192, 1326.CrossRefGoogle ScholarPubMed
Ubelaker, J. E., Payne, E., Allison, V. F. and Moore, D. V. (1973) Scanning electron microscopy of the human pubic louse, Pthirus pubis (Linnaeus, 1758). J. Parasitol. 59, 913919.CrossRefGoogle ScholarPubMed
Wachmann, E. (1972) Das Auge des Hühnerflohs Ceratophyllus gallinae (Schrank) (Insecta, Siphonaptera). Z. Morphol. Tiere 73, 315324.CrossRefGoogle Scholar
Waladde, S. M., Kokwaro, E. D., Galun, R. and Chimtawi, M. (1984) Tibial campaniform sensilla of Glossina morsitans. J. Insect Physiol. 30, 751755.CrossRefGoogle Scholar
Wenk, P. (1981) Bionomics of adult blackflies. In Blackflies. The Future for Biological Methods in Integrated Control. (Edited by Laird, M.), pp. 259279. Academic Press, Toronto.Google Scholar
White, R. A., Paim, U. and Seabrook, W. D. (1974) Maxillary and labial sites of carbon dioxide-sensitive receptors of larval Orthosoma brunneum (Forster) (Coleoptera, Cerambycidae). J. Comp. Physiol. 88, 235246.CrossRefGoogle Scholar
White, S. L. and Bay, D. E. (1980) Antennal olfactory sensilla of the hornfly, Haematobia irritons irritions (L.) (Diptera: Muscidae). J. Kansas Ent. Soc. 53, 641652.Google Scholar
Wigglesworth, V. B. and Gillet, J. D. (1934) The function of the antennae in Rhodnius prolixus (Hemiptera) and the mechanism of orientation to the host, and confirmatory experiments. J. Exp. Biol. 11, 120139.CrossRefGoogle Scholar
Wirth, W. W. and Navai, S. (1978) Terminology of some antennal sensory organs of Culicoides biting midges (Diptera: Ceratopogonidae). J. Med. Ent. 15, 4349.CrossRefGoogle Scholar
Wunderer, H. and Smola, U. (1987) Functional morphology of the retina of Chrysops caecutiens L. and Haematopota pluvialis L. (Diptera: Tabanidae): Region around eye equator. Int. J. Insect Morphol. Embryol. 15, 311319CrossRefGoogle Scholar