Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-22T15:25:48.286Z Has data issue: false hasContentIssue false

FEEDING AND MATING IN THE INSECTIVOROUS CERATOPOGONINAE (DIPTERA)

Published online by Cambridge University Press:  31 May 2012

Get access

Abstract

The subfamily Ceratopogoninae (sensu Wirth, 1965a) is probably a natural (monophyletic) group but includes both blood sucking forms (Culicoidini) and predators on small insects. The insectivorous forms consist of a diversified array of six tribes and many genera represented in moist habitats throughout the world and especially abundant at lake margins.Many predator/prey observations are recorded. The prey consists almost exclusively of the males of other Nematocera or the smaller Ephemeroptera, which the female captures in flight by entering the male (mating) swarms of these insects and hovering until in a position to strike. The initial response is to the swarm-determining landmark, and the female hovers there whether or not potential prey is in flight; groups of hovering females can be induced artificially by suitable markers. These midges themselves form male swarms which the female enters for mating, and the unique method of hunting thus follows a pattern of behaviour already established in relation to another function. The insectivorous tribes have probably been derived from the more plesiomorphic Culicoidini, but the stages in the development of their radically different manner of hunting are not clear.The characteristic form of the mouthparts in the insectivorous genera is described and figured. The prey, after capture in flight, is usually held by the raptorial legs and quickly perforated by the mandibles. A proteolytic saliva is injected and the cellular tissue, except in the longer appendages, is liquefied and sucked out. In most species a single prey individual is not sufficient for one ovarian cycle, and the midge feeds several times. There is some degree of prey specificity, based at least in part on specific responses to the swarm-marker. In several genera there are long tubular "glands" in the abdomen, often everted in flight, whose function is not clearly established. Mobbing of the predator by the intended prey (mosquitoes) is described.The distinctive feature of mating is that the female, in addition to her other prey, often eats the male during mating. Nearly all the records come from the three tribes Heteromyiini, Sphaeromiini, and Palpomyiini. In these tribes (which probably form a relatively apomorphic monophyletic group) the male is usually a dwarf, and the plumose (auditory) antenna is more or less strongly reduced. It is suggested that the female remains in hunting phase when entering her conspecific swarm and captures the male as prey, and that the typical auditory recognition of female by male has become reduced or vestigial. In the more plesiomorphic tribes Ceratopogonini and Stilobezziini the male is normal in size and the antennal plume is fully developed, as in Culicoides, and there are only two records, at most, of the male being eaten during mating.The males eaten during mating are pierced through the head and reduced to an empty cuticle by the action of the lytic saliva. The terminalia however retain their hold, perhaps because of the early destruction of the suboesophageal ganglion, and the dry male cuticle often breaks away leaving the terminalia still attached. The structure of the terminalia and the mating position is described and discussed. Insemination is by spermatophore, which if the male is eaten never leaves the male duct. The terminalia of the male are inverted during mating and in some genera become so permanently early in adult life.An attempt is made throughout to view the phenomena in a phylogenetic context.Numerous illustrations are provided.

Type
Research Article
Copyright
Copyright © Entomological Society of Canada 1978

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Areán, V.M. and Fox, I.. 1955. Dermal alterations in severe reaction to the bite of the sandfly, Culicoides furens. Am. J. clin. Path. 25: 13591366.Google Scholar
Atchley, W.R. 1969. Description of the male, pupa, and larval habitat of Nilobezzia brevicornis (Diptera: Ceratopogonidae). J. Kans. ent. Soc. 42: 5657.Google Scholar
Atchley, W.R. 1970. A biosystematic study of the subgenus Selfia of Culicoides (Diptera: Ceratopogonidae). Kans. Univ. Sci. Bull. 49: pp. 181336.Google Scholar
Brower, L.P., Brower, J. van Z., and Westcott, P.W.. 1960. Experimental studies of mimicry. 5. The reactions of toads (Bufo terrestris) to bumblebees (Bombus americanorum) and their robberfly mimics (Mallophora bomboides), with a discussion of aggressive mimicry. Am. Nat. 94: 343355.Google Scholar
Clements, A.N. 1963. The physiology of mosquitoes. Pergamon Press, Oxford.Google Scholar
Davis, N.T. 1967. Leishmaniasis in the Sudan Republic. 28. Anatomical studies on Phlebotomus orientalis Parrot and P. papatasi Scopoli. J. med. Ent. 4: 5065.Google Scholar
Debenham, M.L. 1970. Australasian Ceratopogonidae. (Diptera, Nematocera). Part XIII: Australian and New Guinea species of Echinohelea Macfie. Proc. Linn. Soc. N.S.W. 94: 145159.Google Scholar
Debenham, M.L. 1974. A revision of the Australian and New Guinea predatory Ceratopogonidae (Diptera: Nematocera) of the tribes Heteromyiini and Sphaeromiini. Aust. J. Zool. Suppl. Ser. 28. 92 pp.Google Scholar
DeMeillon, B. 1939. A new subgenus of Ceratopogon. Pp. 103107in Macfie, J.W.S., Ceratopogonidae; Ruwenzori Expedition 1: 81107. British Museum (Nat. Hist.), London.Google Scholar
DeMeillon, B. and Hardy, F.. 1954. New records and species of biting insects from the Ethiopian Region. V. J. ent. Soc. Sth. Afr. 17: 6285.Google Scholar
Downes, J.A. 1950. Habits and life-cycle of Culicoides nubeculosus(Mg.). Nature, Lond. 166: 510511.Google Scholar
Downes, J.A. 1955 a. Observations on the swarming flight and matinlof Culicoides (Diptera: Ceratopogonidae). Trans. R. ent. Soc. Lond. 106: 213236.Google Scholar
Downes, J.A. 1955 b. The food habits and description of Atrichopogon pollinivorus sp.n. (Diptera: Ceratopogonidae). Trans. R. ent. Soc. Lond. 106: 439453.Google Scholar
Downes, J.A. 1958 a. The feeding habits of biting flies and their significance in classification. A. Rev. Ent. 3: 249266.Google Scholar
Downes, J.A. 1958 b. Assembly and mating in the biting Nematocera. Proc. Tenth int. Congr. Ent. (Montreal) 1956. Vol. 2, pp. 425434.Google Scholar
Downes, J.A. 1962 a. What is an arctic insect? Can. Ent. 94: 143162.Google Scholar
Downes, J.A. 1962 b. Feeding and mating, and their interrelationship in the insectivorous Ceratopogoninae (Abstract). Verh. XI int. Kongr. Ent., Wien (1960) 1: 618.Google Scholar
Downes, J.A. 1969. The swarming and mating flight of Diptera. A. Rev. Ent. 14: 271298.Google Scholar
Downes, J.A. 1970. The feeding and mating behaviour of the specialized Empidinae (Diptera); observations on four species of Rhamphomyia in the high arctic and a general discussion. Can. Ent. 102: 769791.Google Scholar
Downes, J.A. 1971. The ecology of blood-sucking Diptera; an evolutionary perspective. Pp. 232258 in Fallis, A.M. (Ed.), Ecology and physiology of parasites. Univ. of Toronto Press.Google Scholar
Downes, J.A. 1974. The feeding habits of adult Chironomidae. Ent. Tidskr. 95, Suppl.: 8490.Google Scholar
Edwards, F.W. 1920 a. Some records of predaceous Ceratopogoninae (Diptera). Entomologist's mon. Mag. 56: 203205.Google Scholar
Downes, J.A. 1920 b. Scent-organs (?) in female midges of the Palpomyia group. Ann. Mag. nat. Hist. (9) 6: 365368.Google Scholar
Downes, J.A. 1923. New and old observations on ceratopogonine midges attacking other insects. Ann. trop. Med. Parasit. 17: 1929.Google Scholar
Downes, J.A. 1926. On the British biting midges (Diptera, Ceratopogonidae). Trans. ent. Soc. Lond. 1926: 389426.Google Scholar
Edwards, J.S. 1961. The action and composition of the saliva of an assassin bug Platymeris rhadamanthus Gaerst. (Hemiptera: Reduviidae). J. exp. Biol. 38: 6177.Google Scholar
Gad, A.M. 1951. The head-capsule and mouthparts in the Ceratopogonidae. Bull. Soc. Fouad I Ent. 35: 1775.Google Scholar
Goetghebuer, M. 1914. Note à propos l'accouplement de Johannseniella Will.(Ceratolophus Mg.) nitida Macq. Annls Soc. ent. Belg. 58: 202204.Google Scholar
Goetghebuer, M. 1921. Chironomides de Belgique. Mém. Mus. r. Hist. nat. Belg. 8(4): 1208.Google Scholar
Goetghebuer, M. 1949. Biologie des Ceratopogonides (Diptères Némocères). Biol. Jaarb. 16: 113117.Google Scholar
Jobling, B. 1928. The structure ol the head and mouthparts tn Culicoides pulicaris L. (Diptera Nematocera). Bull. ent. Res. 18: 211236.Google Scholar
Jones, J.C. 1968. The sexual life of a mosquito. Scient. Am. 218: 108116.Google Scholar
Kettle, D.S. and Lawson, J.W.H.. 1952. The early stages of British biting midges Culicoides Latreille (Diptera, Ceratopogonidae) and allied genera. Bull. ent. Res. 43: 421467.Google Scholar
Kieffer, J.J. 1925. Diptères: Chironomidae Ceratopogoninae. Faune Fr. 11. 139 pp.Google Scholar
Lane, J. 1944. As espécies neotrópicas do gênero Clinohelea Kieffer, 1917 (Diptera, Ceratopogonidae). Revta Ent., Rio de J. 15: 249261.Google Scholar
Lane, J. 1948 (1947). Novos Ceratopogonideos do Brasil (Diptera, Ceratopogonidae). Archos Fac. Hig. Saúde públ. Univ. S. Paulo 1: 225239.Google Scholar
Lindroth, C.H. 1931. Die Insektenfauna Islands und ihre Probleme. Almqvist and Wiksells, Uppsala.Google Scholar
Linley, J.R. and Adams, G.M.. 1972. A study of the mating behaviour of Culicoides melleus Coquillett) (Diptera: Ceratopogonidae). Trans. R. ent. Soc. Lond. 124: 81121.Google Scholar
Lloyd, J.E. 1965. Aggressive mimicry in Photuris: firefly femmes fatales. Science, N.Y. 149: 653654.Google Scholar
Lloyd, J.E. 1975. Aggressive mimicry in Photuris fireflies: signal repetoires by femmes fatales. Science, N.Y. 187: 452453.Google Scholar
Malloch, J. 1914. Notes on North American Diptera, with descriptions of new species from the collection of Illinois State Laboratory of Natural History. Bull. Ill. St. Lab. nat. Hist. 10: 213243.Google Scholar
Mayer, K. 1933. Zur Imaginalbiologie der Ceratopogoniden (Dipt.). Dt. ent. Z. 1933, pp. 5663.Google Scholar
McDaniel, I.N. and Horsfall, W.R.. 1957. Induced copulation of mosquitoes. Science, N.Y. 125: 745.Google Scholar
Melin, D. 1923. Contributions to the knowledge of the biology, metamorphosis and distribution of the Swedish asilids. Almqvist and Wiksells, Uppsala.Google Scholar
Oliver, D.R. 1968. Adaptations of arctic Chironomidae. Ann. Zool. Fenn. 5: 111118.Google Scholar
Pickford, G.E. and Dorris, F.. 1934. Micro methods for the detection of proteases and amylases. Science, N.Y. 80: 317319.Google Scholar
Pomerantzev, B.I. 1932. Beitrage zur Morphologie und Anatomie der Genitalien von Culicoides [in Russian, German summary]. Mag. Parasit., Leningrad 3: 183214.Google Scholar
Richards, O.W. 1927. Sexual selection and allied problems in the insects. Biol. Rev. Cambridge phil. Soc. 2: 298360.Google Scholar
Roeder, K.D. (Ed.). 1953. Insect physiology. Wiley, New York.Google Scholar
Shorey, H.H. 1973. Behavioral responses to insect pheromones. A. Rev. Ent. 18: 349380.Google Scholar
Staeger, C. 1839. Systematisk fortegnelse over de i Danmark hidtilfundne Diptera. Naturh. Tidskrift 2: 549600.Google Scholar
Thienemann, A. 1954. Chironomus. Nagele, Stuttgart.Google Scholar
Thomsen, L.C. 1937. Aquatic Diptera 5. Ceratopogonidae. Cornell Univ. agric. Exp. Stn Mem. 210.Google Scholar
Tonnoir, A.L. 1933. Descriptions of remarkable Indian Psychodidae and their early stages. Rec. Ind. Mus. 35: 5375.Google Scholar
Varley, G.C. 1948. A ceratopogonid fly, Palpomyia semifumosa Goet., feeding on mayflies. Enlomologist's mon. Mag. 84: 3638.Google Scholar
Weerekoon, A.C.J. 1953. On the behaviour of certain Ceratopogonidae (Diptera). Proc. R. ent. Soc. Lond. (A) 28: 8592.Google Scholar
Weerekoon, A.C.J. 1956. Studies on the biology of Loch Lomond. I. Ceylon J. Sci. (C) 7 (I N.S.): 194.Google Scholar
Wenk, P. 1962. Anatomie des Kopfes von Wilhelmia equina L. ♀ (Simuliidae syn. Melusinidae, Diptera). Zool. Jb. Anat. Bd. 80: 81134.Google Scholar
Wirth, W.W. 1951. New species and records of Virginia Heleidae (Diptera). Proc. ent. Soc. Wash. 53: 313326.Google Scholar
Wirth, W.W. 1952. The Heleidae of California. Univ. Calif. Publs Ent. 9: 92266.Google Scholar
Wirth, W.W. 1962. A reclassification of the Palpomyia — Bezzia — Macropeza groups, and a revision of the North American Sphaeromiini (Diptera, Ceratopogonidae). Ann. ent. Soc. Am. 55: 272287.Google Scholar
Wirth, W.W. 1965 a. Family Ceratopogonidae (Heleidae). Pp. 121142in A catalog of the Diptera of America north of Mexico. Agric. Handb. 276. Gov't. Printing Office, Washington, D.C.Google Scholar
Wirth, W.W. 1965 b. A revision of the genus Parabezzia Malloch. Proc. ent. Soc. Wash. 67: 215230.Google Scholar
Wirth, W.W. 1971. Six new North American species of Probezzia (Diptera: Ceratopogonidae), with biological notes and a key to species. Ann. ent. Soc. Am. 64: 729739.Google Scholar
Wirth, W.W. and Blanton, F.S.. 1970 a. New genera of neotropical Ceratopogonidae. Fla ent. 53: 714.Google Scholar
Wirth, W.W. 1970 b. Notes on Brachypogon Kieffer (Diptera, Ceratopogonidae), a new species, and two new neotropical genera of the tribe Ceratopogonini. Fla Ent. 53: 93104.Google Scholar
Wirth, W.W. and Hubert, A.A.. 1959. Trithecoides, a new subgenus of Culicoides (Diptera, Ceratopogonidae). Pacif. Insects 1: 138.Google Scholar
Wirth, W.W. and Ratanaworabhan, N.C.. 1971. Ceratoculicoides, a new genus related to Ceratopogon Meigen (Diptera: Ceratopogonidae). Proc. ent. Soc. Wash. 73: 170177.Google Scholar
Wirth, W.W. and Ratanaworabhan, N.C.. 1972. A revision of the tribe Stenoxenini (Diptera: Ceratopogonidae). Ann. ent. Soc. Am. 65: 13681388.Google Scholar
Wirth, W.W. and Williams, R.W.. 1964. New species and records of North American Monohelea (Diptera: Ceratopogonidae). Ann. ent. Soc. Am. 57: 302310.Google Scholar