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The behavioural ecology of host selection in Anopheles implexus (Theobald) (Diptera, Culicidae)

Published online by Cambridge University Press:  10 July 2009

A. W. R. McCrae
Affiliation:
East African Virus Research Institute, Entebbe, Uganda
P. F. L. Boreham
Affiliation:
Department of Zoology and Applied Entomology, Imperial College of Science and Technology, Prince Consort Road, London SW7 2AZ, U.K..
Y. Ssenkubuge
Affiliation:
East African Virus Research Institute, Entebbe, Uganda

Abstract

Anopheles implexus (Theo.) was studied at the Zika Forest near Entebbe, Uganda, from 1966 to 1971, with central reference to biting activities and host selection. Seasonal fluctuations of populations appeared to be correlated with lake levels, not with local rainfall. Results of biting, resting and nectar-feeding catches at various points across the forest floor indicated that diel activity patterns of man-biting were related primarily to the proximity of resting female A. implexus and only secondarily to the influence of environmental variables. Latent effects of moon phase on day-time man-biting activity patterns support this view. Blood-meal identifications showed that the great majority of blood-fed females resting in forest had fed on cattle, indicating that they left the forest at night. This was confirmed by direct catching from cattle outside forest, while the virtual absence of A. implexus resting near these bait animals, together with the fact that man is very seldom attacked away from forest, indicated that different kinds of host selection strategy were involved. The diel activity pattern of biting on cattle taken into forest was then found to be very different from that on man. Age-grading studies helped to substantiate these differences. Hourly sampling of A. implexus arriving at representative resting sites in forest indicated an exodus of most of the adult mosquito population from forest at dusk and a return shortly after sunrise. The two basic host selection strategies evidently involved (a) active or (in effect) ‘hunting’ flight, mainly outside forest with a tendency to restrict choice to most strongly attractive hosts, and (b) passive or opportunistic attack from rest, in which some of the unfed females sheltering may be activated by the proximity of a host which need not be strongly attractive. The latter situation was investigated further through analysis of short-term day-time patterns of attack on man in forest which are postulated to be a function of mosquito response delay (involving both resident and incoming elements of the sheltering population), which in turn determines depletion rates (involving only the resident element available at the time of the host's arrival). In A. implexus the response delay appears to vary according to time of day. Anomalous results are finally re-considered and it is concluded that the different patterns of active and passive host selection could arise from a single circadian rhythm of responsiveness, with flight characteristics and day-time inhibition modulating responses to specific and non-specific host stimuli in different ways.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 1976

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References

Antonipulle, P., David, H. V. & Karunaratne, M. D. R. (1958). Biology and control of Taeniorhynchus (Mansonioides) uniformis Theobald, the chief vector of rural filariasis in Ceylon.—Bull. Wld Hlth Org. 19, 285295.Google ScholarPubMed
Benoit, P. L. G. (1964). Mission de zoologie medicale au Maniema (Congo, Leopoldville). Diptera-Culicidae.—Annls Mus. r. Afr. cent. Sér. 8vo. no. 132, 297320.Google Scholar
Berge, T. O. (Ed.) (1975). International catalogue of arboviruses including certain other viruses of vertebrates.—2nd edn, 789 pp. U.S. Dept. of Hlth, Edn & Welfare publ. no. (CDC) 75-8301. Washington, D.C., U.S. Govt Printing Office.Google Scholar
Bidlingmayer, W. L. (1964). The effect of moonlight on the flight activity of mosquitoes.—Ecology 45, 8794.CrossRefGoogle Scholar
Bidlingmayer, W. L. (1967). A comparison of trapping methods for adult mosquitoes: species response and environmental influence.—J. med. Ent. 4, 200220.CrossRefGoogle Scholar
Bidlingmayer, W. L. (1971). Mosquito flight paths in relation to the environment. I.—Illumination levels, orientation, and resting areas.—Ann. ent. Soc. Amer. 64, 11211131.CrossRefGoogle Scholar
Bidlingmayer, W. L., Franklin, B. P., Jennings, A. M. & Cody, E. F. (1974). Mosquito flight paths in relation to the environment. Influence of blood meals, ovarian stage and parity.—Ann. ent. Soc. Amer. 67, 919927.CrossRefGoogle Scholar
Boreham, P. F. L. (1972). Serological identification of arthropod bloodmeals and its application.—PANS 18, 205209.Google Scholar
Bowden, J. (1973). The influence of moonlight on catches of insects in light-traps in Africa. Part I.—The moon and moonlight.—Bull. ent. Res. 63, 113128.CrossRefGoogle Scholar
Brady, J. (1975). Circadian changes in central excitability—the origin of behavioural rhythms in tsetse flies and other animals?J. Ent. (A) 50, 7995.Google Scholar
Bursell, E. (1961). The behaviour of tsetse flies (Glossina swynnertoni Austen) in relation to problems of sampling.—Proc. R. ent. Soc. Lond. (A) 36, 920.Google Scholar
Buxton, A. P. (1952). Observations on the diurnal behaviour of the redtail monkey (Cercopithecus ascanius schmidti Matschie) in a small forest in Uganda.—J. Anim. Ecol. 21, 2558.CrossRefGoogle Scholar
Colless, D. H. (1956). The Anopheles leucosphyrus group.—Trans. R. ent. Soc. Lond. 108, 37116.CrossRefGoogle Scholar
Corbet, P. S. (1963). Seasonal patterns of age-composition of sylvan mosquito populations in Uganda (Diptera, Culicidae).—Bull. ent. Res. 54, 213227.CrossRefGoogle Scholar
Corbet, P. S. (1964). Observations on mosquitoes ovipositing in small containers in Zika Forest, Uganda.—J. Anim. Ecol. 33, 141164.CrossRefGoogle Scholar
Corbet, P. S. & Ssenkubuge, Y. (1962). Mosquitoes attracted to various baits in forest.—Rept. E. Afr. Virus Res. Inst. 1961–62, no. 12, 49–56.Google Scholar
Davies, J. B. (1975). Moonlight and the biting activity of Culex (Melanoconion) portesi Senevet & Abonnenc and C. (M.) taeniopus D. & K. (Diptera, Culicidae) in Trinidad forests.—Bull. ent. Res. 65, 8196.CrossRefGoogle Scholar
Davies, J. B., Corbet, P. S., Gillies, M. T. & McCrae, A. W. R. (1971). Parous rates in some Amazonian mosquitoes collected by three different methods.—Bull. ent. Res. 61, 125132.CrossRefGoogle Scholar
De Meillon, B. (1947). The Anophelini of the Ethiopian geographical region.—Publ. S. Afr. Inst. med. Res. no. 49, 272 pp.Google Scholar
Detinova, T. S. (1962). Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria.—Monograph Ser. W.H.O. no. 47, 216 pp.Google ScholarPubMed
Disney, R. H. L. (1972). Observations on chicken-biting blackflies in Cameroon with a discussion of parous rates of Simulium damnosum.—Ann. trop. Med. Parasit. 66, 149158.CrossRefGoogle ScholarPubMed
Division of Malaria Eradication, W.H.O. & Lister Institute (1960). A study of the blood-feeding patterns of Anopheles mosquitos through precipitin tests.—Bull. Wld Hlth Org. 22, 685-720.Google Scholar
Evans, A. M. (1938). Mosquitoes of the Ethiopian region. II.—Anophelini adults and early stages.—404 pp. London, Brit. Mus. (Nat. Hist.).Google Scholar
Garnham, P. C. C. (1966). Malaria parasites and other Haemosporidia.1114 pp. Oxford, Blackwell Scientific Publications.Google Scholar
Garrett-Jones, C. (1950). A dispersion of mosquitoes by wind.—Nature, Lond. 165, 285.CrossRefGoogle ScholarPubMed
Garrett-Jones, C. (1957). Migratory flight in anopheline mosquitoes in the Middle East.—Bull, endem. Dis. 2, 7987.Google Scholar
Garrett-Jones, C. (1962). The possibility of active long-distance migrations by Anopheles pharoensis Theobald.—Bull. Wld Hlth Org. 27, 299302.Google ScholarPubMed
Germain, M., Eouzan, J. P., Ferrara, L. & Button, J. P. (1973). Données complémentaires sur le comportement et l'écologie d' Aedes africanus (Theobald) dans le nord du Cameroun occidental.—Cah. ORSTOM, Sér. Ent. méd. et Parasitol. 11, 127146.Google Scholar
Gillett, J. D. (1971). Mosquitoes.274 pp. London, Weidenfeld & Nicolson.Google Scholar
Gillett, J. D., Haddow., A. J. & Corbet, P. S. (1962). The sugar-feeding-cycle in a cage-population of mosquitoes.—Ent. exp. appl. 5, 223232.CrossRefGoogle Scholar
Gillies, M. T. (1954 a). Studies of house leaving and outside resting of Anopheles gambiae Giles and Anopheles funestus Giles in East Africa. I.—The outside resting population. —Bull. ent. Res. 45, 361373.CrossRefGoogle Scholar
Gillies, M. T. (1954 a). II.—The exodus from houses and the house resting population.—Bull. ent. Res., 375387.CrossRefGoogle Scholar
Gillies, M. T. (1954 b). The recognition of age-groups within populations of Anopheles gambiae by the pre-gravid rate and the sporozoite rate.—Ann. trop. Med. Parasit. 48, 5874.CrossRefGoogle ScholarPubMed
Gillies, M. T. (1955). The pre-gravid phase of ovarian development in Anopheles funestus.—Ann. trop. Med. Parasit. 49, 320325.CrossRefGoogle ScholarPubMed
Gillies, M. T. (1957). Age-groups in the biting cycle in Anopheles gambiae. A preliminary investigation.—Bull. ent. Res. 48, 553559.CrossRefGoogle Scholar
Gillies, M. T. (1970). Assessment of control. Some problems in the measurement of anopheline populations.—Misc. Publ. ent. Soc. Amer. 7, 156167.Google Scholar
Gillies, M. T. (1972). Some aspects of mosquito behaviour in relation to the transmission of parasites, pp. 69-81 in Canning, E. U. & Wright, C. A. (Eds.). Behavioural aspects of parasite transmission.219 pp. London, Linnean Society, Academic Press.Google Scholar
Gillies, M. T. & De Meillon, B. (1968). The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical Region).—Publ. S. Afr. Inst. med. Res. no. 54, 343 pp.Google Scholar
Gillies, M. T. & Wilkes, T. J. (1969). A comparison of the range of attraction of animal baits and of carbon dioxide for some West African mosquitoes.—Bull. ent. Res. 59, 441456.CrossRefGoogle ScholarPubMed
Gillies, M. T. & Wilkes, T. J. (1970). The range of attraction of single baits for some West African mosquitoes.—Bull. ent. Res. 60, 225235.CrossRefGoogle ScholarPubMed
Gillies, M. T. & Wilkes, T. J. (1972). The range of attraction of animal baits and carbon dioxide for mosquitoes. Studies in a freshwater area of West Africa.—Bull. ent. Res. 61, 389404.CrossRefGoogle Scholar
Goma, L. K. H. (1965). The flight activity of some East African mosquitos (Diptera, Culicidae). I.—Studies on a high steel tower in Zika Forest, Uganda.—Bull. ent. Res. 56, 1735.CrossRefGoogle ScholarPubMed
Haddow, A. J. (1942). The mosquito fauna and climate of native huts at Kisumu, Kenya.—Bull. ent. Res. 33, 91142.CrossRefGoogle Scholar
Haddow, A. J. (1945). The mosquitoes of Bwamba County, Uganda. II.—Biting activity with special reference to the influence of the microclimate.—Bull. ent. Res. 36, 3373.CrossRefGoogle Scholar
Haddow, A. J. (1954). Studies of the biting-habits of African mosquitos. An appraisal of methods employed, with special reference to the twenty-four-hour catch.—Bull. ent. Res. 24, 199242.CrossRefGoogle Scholar
Haddow, A. J. (1961). Studies on the biting habits and medical importance of East African mosquitos in the genus Aedes. II.—Subgenera Mucidus, Diceromyia, Finlaya and Stegomyia.—Bull. ent. Res. 52, 317351.CrossRefGoogle Scholar
Haddow, A. J. (1964). Observations on the biting habits of mosquitoes in the forest canopy at Zika, Uganda with special reference to the crepuscular periods.—Bull. ent. Res. 55, 589608.CrossRefGoogle Scholar
Haddow, A. J. & Corbet, P. S. (1961). Entomological studies from a high tower in Mpanga Forest, Uganda. V.—Swarming activity above the forest.—Trans. R. ent. Soc. Lond. 113, 284300.CrossRefGoogle Scholar
Haddow, A. J., Gillett, J. D. & Highton, R. B. (1947). The mosquitoes of Bwamba County, Uganda. V.—The vertical distribution and biting-cycle of mosquitoes in rain-forest, with further observations on microclimate.—Bull. ent. Res. 37, 301330.CrossRefGoogle Scholar
Haddow, A. J. & Ssenkubuge, Y. (1965). Entomological studies from a high steel tower in Zika Forest, Uganda. Part I.—The biting activity of mosquitoes and Tabanids as shown by twenty-four-hour catches.—Trans. R. ent. Soc. Lond. 117, 215243.CrossRefGoogle Scholar
Haddow, A. J. & Ssenkubuge, Y. (1974). The mosquitoes of Bwamba County, Uganda. X.—Observations on the biting behaviour of Anopheles spp. other than A. gambiae Giles, with notes on the behaviour of these species in the Entebbe area.—Bull. ent. Res. 64, 4551.CrossRefGoogle Scholar
Haddow, A. J., van Someren, E. C. C, Lumsden, W. H. R., Harper, J. O. & Gillett, J. D. (1951). The mosquitoes of Bwamba County, Uganda. VIII.—Records of occurrence, behaviour and habitat.—Bull. ent. Res. 42, 207238.CrossRefGoogle Scholar
Haddow, A. J., Williams, M. C, Woodall, J. P., Simpson, D. I. H. & Goma, L. K. H. (1964). Twelve isolations of Zika virus from Aedes (Stegomyia) africanus (Theobald) taken in and above a Uganda forest.—Bull. Wld Hlth Org. 31, 5769.Google ScholarPubMed
Hamon, J. (1963). Les moustiques anthropophiles de la region de Bobo-Dioulasso (République de Haute-Volta). Cycles d'aggressivite et variations saisonnieres.—Ann. Soc. ent. France 132, 85144.Google Scholar
Hanney, P. W. (1960). The mosquitos of Zaria Province, Northern Nigeria.—Bull. ent. Res. 51, 145171.CrossRefGoogle Scholar
Harley, J. M. B. (1967). The influence of sampling method on the trypanosome infection rates of catches of Glossina pallidipes and G. fuscipes.—Ent. exp. appl. 10, 240252.CrossRefGoogle Scholar
Hocking, B. (1971). Blood-sucking behaviour of terrestrial arthropods.—Ann. Rev. Ent. 16, 126.CrossRefGoogle ScholarPubMed
Holstein, M. (1952). Biologie d'Anopheles gambiae.—Monograph Ser. W.H.O. no. 9, 176 pp.Google Scholar
Johnson, C. G. (1969). Migration and dispersal of insects by flight.763 pp. London, Methuen.Google Scholar
Kennedy, J. S. (1961). A turning point in the study of insect migration.—Nature, Lond. 189, 785791.CrossRefGoogle Scholar
Lewis, T. & Taylor, L. R. (1965). Diurnal periodicity of flight by insects.—Trans. R. ent. Soc. Lond. 116, 393469.CrossRefGoogle Scholar
Lips, M. (1960). Anopheles du Congo Beige. 2. Quelques especes des galeries forestieres.—Riv. Parassit. 21, 3964.Google Scholar
McClelland, G. A. H. & Weitz, B. (1963). Serological identification of the natural hosts of Aedes aegypti (L.) and some other mosquitoes (Diptera, Culicidae) caught resting in vegetation in Kenya and Uganda.—Ann. trop. Med. Parasit. 57, 214224.CrossRefGoogle ScholarPubMed
McCrae, A. W. R. (1972). Age-composition of man-biting Aedes (Stegomyia) simpsoni (Theobald) (Diptera: Culicidae) in Bwamba County, Uganda.—J. med. Ent. 9, 545550.CrossRefGoogle ScholarPubMed
McCrae, A. W. R. (1976). The association between larval parasitic water mites (Hydracarina) and Anopheles implexus (Theobald) (Diptera, Culicidae).—Bull. ent. Res. 66CrossRefGoogle Scholar
McCrae, A. W. R., Henderson, B. E., Kirya, B. G. & Sempala, S. D. K. (1971). Chikungunya virus in the Entebbe area of Uganda: isolations and epidemiology.—Trans. R. Soc. trop. Med. Hyg. 65, 152168.CrossRefGoogle ScholarPubMed
McCrae, A. W. R., Manuma, P., Ssenkubuge, Y., Kitama, A. & Mawejje, C. (1969 a). Natural biting rates of mosquitoes related to the initial appearance of human hosts.—Rep. E. Afr. Virus Res. Inst.1968, no. 18, 9597.Google Scholar
McCrae, A. W. R., Ssenkubuge, Y., Manuma, P., Mawejje, C. & Kitama, A. (1969 b). Mosquito and tabanid activity at plant sugar sources.—Rep. E. Afr. Virus Res. Inst. 1968, no. 18, 96102.Google Scholar
Mattingly, P. F. (1965). Intercurrent resting, a neglected aspect of mosquito behaviour.—Cah. ORSTOM Ser. Ent. med. no. 3/4, 187.Google Scholar
Mattingly, P. F. (1966). Intercurrent resting, a neglected aspect of mosquito behaviour.—Proc. 1st int. Congr. Parasit., Roma 2, 910911.Google Scholar
Minnaert, M. (1954). The nature of light and colour.—362 pp. New York, Dover Publications.Google Scholar
Moorhouse, D. E. & Wharton, R. H. (1965). Studies on Malayan vectors of malaria; methods of trapping, and observations on biting cycles.—J. med. Ent. 1, 359370.CrossRefGoogle Scholar
Muirhead-Thomson, R. C. (1940). Studies on the behaviour of Anopheles minimus. Part I.—The selection of the breeding place and the influence of light and shade.—J. Malar. Inst. India 3, 265294.Google Scholar
Pajot, F.-X., Le Pont, F. & Molez, J.-F. (1975). Donnees sur l'alimentation non sanguine chez Anopheles (Nyssorhynchus) darlingi Root, 1926 (Diptera, Culicidae) en Guyane francaise.—Cah. ORSTOM Ser. Ent. med. et Parasitol. 13, 131134.Google Scholar
Rees, D. M. (1945). Notes on mosquito migration in Salt Lake City in 1945.—Mosq. News 5, 134.Google Scholar
Rennison, B. D. & Smith, I. M. (1961). Studies on the sampling of Glossina pallidipes Aust. IV.—Some aspects of the use of Morris traps.—Bull. ent. Res. 52, 609619.CrossRefGoogle Scholar
Ribbands, C. R. (1946). Moonlight and house-haunting habits of female Anophelines in West Africa.—Bull. ent. Res. 36, 395417.CrossRefGoogle ScholarPubMed
Scanlon, J. E. & Sandihand, U. (1965). The distribution and biology of Anopheles balabacensis in Thailand (Diptera: Culicidae).—J. med. Ent. 2, 6169.CrossRefGoogle Scholar
Senior-White, R. A. (1952). Studies on the bionomics of Anopheles aquasalis Curry. Part III. —Indian J. Malar. 6, 2972.Google ScholarPubMed
Service, M. W. (1969). Observations on the ecology of some British mosquitoes.—Bull. ent. Res. 59, 161194.CrossRefGoogle Scholar
Service, M. W. (1971). The daytime distribution of mosquitoes resting in vegetation.—J. med. Ent. 8, 271278.CrossRefGoogle Scholar
Service, M. W. (1976). Mosquito ecology.583 pp. London, Applied Science Publishers.Google Scholar
Smith, A. (1958). Outdoor cattle feeding and resting of A. gambiae Giles and A. pharoensis Theo. in the Pare-Taveta area of East Africa.—E. Afr. med. J. 35, 559567.Google Scholar
Smith, I. M. & Rennison, B. D. (1961). Studies on the sampling of Glossina pallidipes Aust. I.—The numbers caught daily on cattle, in Morris traps and on a fly-round.—Bull. ent. Res. 52, 165182.CrossRefGoogle Scholar
Smith, I. M. & Rennison, B. D. (1961). II—The daily pattern of flies caught on cattle.—Bull. ent. Res., 183189.CrossRefGoogle Scholar
Smith, I. M. & Rennison, B. D. (1961). III.—The hunger states of the male flies caught on cattle and in a Morris trap.—Bull. ent. Res., 601607.CrossRefGoogle Scholar
Van Someren, E.C. C. & Furlong, M. (1964). The biting habits of Aedes (Skusea) pembaensis Theo. and some other mosquitos of Faza, Pate Island, East Africa.—Bull. ent. Res. 55, 97124.CrossRefGoogle Scholar
Van Someren, G. R. C. (1976). A further note on swarming of male mosquitoes and other Nematocera in Kenya.—Entomologist's mon. Mag. 111, 147160.Google Scholar
Symes, C. B. (1932). Notes on the infectivity, food and breeding waters of anophelines in Kenya.—Rec. med. Res. Lab. Nairobi no. 4, 28 pp.Google Scholar
Teesdale, C. (1955). Studies on the bionomics of Aedes aegypti (L.) in its natural habitats in a coastal region of Kenya.—Bull. ent. Res. 46, 711742.CrossRefGoogle Scholar
Vincke, I. H. (1946). Note sur la biologie des Anopheles d'Elisabethville et environs.—Annls. Soc. beige Med. trop. 26, 385481.Google Scholar
Vincke, I. H. & Leleup, N. (1949). Notes biologiques et éthologiques sur les Anophèles dendrophiles du Katanga.—Revue Zool. Bot. afr. 42, 250258.Google Scholar
Weitz, B. (1956). Identification of blood meals of blood-sucking arthropods.—Bull. Wld Hlth Org. 15, 473490.Google ScholarPubMed
Weitz, B. (1963). The feeding habits of Glossina.—Bull. Wld Hlth Org. 28, 711729.Google ScholarPubMed
Williams, M. C. (1963). Studies on mosquitos (Diptera, Culicidae) biting birds, using twenty-four-hour catches, in the Entebbe area, Uganda.—Bull. ent. Res. 54, 407424.CrossRefGoogle Scholar