Hostname: page-component-848d4c4894-nmvwc Total loading time: 0 Render date: 2024-06-25T09:50:48.317Z Has data issue: false hasContentIssue false

Comparative studies on sibling species of the Anopheles gambiae Giles complex (Dipt., Culicidae). III. The distribution, ecology, behaviour and vectorial importance of species D in Bwamba County, Uganda, with an analysis of biological, ecological, morphological and cytogenetical relationships of Ugandan species D*

Published online by Cambridge University Press:  10 July 2009

G. B. White
Affiliation:
Wellcome Parasitology Unit No. 2, Haile Sellassie I University, Addis Ababa, Ethiopia

Abstract

Studies on mosquitoes of the Anopheles gambiae Giles complex at Bwamba, Uganda, showed that the newly recognized sibling species D may be restricted to breeding areas where waters contain unusual solutes, the effluent from hot springs at Buranga being particularly favourable. Two other members of the complex, species A and B, were also detected in the neighbourhood apparently breeding only in more normal situations. Species D specimens were usually identified cytotaxonomically, from the presence of XR potytene chromosomes of the type also occurring in species C and A. melas (Theo.) (neither of which is known from the area). Most species D females have distinctively pale palps, a valuable although limited distinguishing feature. Features of setation on larvae and pupae were discerned which might serve usefully as meristic chaetotaxonomic factors, at least locally, if tested further. Although it is unquestionable that a large proportion of species D females forage in the Semliki forest, feeding on primates, bovids, suids or unsuspected hosts, it was demonstrated that many species D females are markedly anthropophilic and display strong endophilic and endophagic tendencies, to the extent that they may be primary vectors of human malaria and filariasis over a limited range. Species D males were rare indoors and remained mainly within the forest, where great numbers rest low on vegetation in company with unfed females, near to breeding areas of brackish marsh. Two polymorphic chromosomal inversions in species D apparently embody the genetical causes of its differentiation. Cytogenetical evidence indicates that species D is phylogenetically nearly intermediate between A. melas and species C of the A. gambiae complex.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 1973

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

Arad, A. & Morton, W.H. (1969). Mineral springs and saline lakes of the Western Rift Valley, Uganda. – Geochim. cosmochim. Acta 33, 11691181.CrossRefGoogle Scholar
Bates, M. (1939). The use of salt solutions for the demonstration of physiological differences between the larvae of certain European Anopheline mosquitoes. – Am. J. trop. Med. 19, 357384.CrossRefGoogle Scholar
Bates, M. (1949). The natural history of mosquitoes. – 379 pp. New York, Macmillan.Google Scholar
Cahen, L. & Snelling, N.J. (1966). The geochronology of equatorial Africa. – 195 pp. Amsterdam, North-Holland.Google Scholar
Chapin, J.P. (1923). Ecological aspects of bird distribution in tropical Africa. – Am. Nat. 57, 106125.Google Scholar
Clarke, J.L. (1971). Potential use of the spermatheca in the separation of species A and B females of the Anophelas gambiae complex in northern Nigeria. – Bull Wld Hlth Org. 45, 260263.Google Scholar
Coluzzi, M. (1964). Morphological divergences in the Anophelas gambiae complex. – Riv. Malar. 43, 197232.Google ScholarPubMed
Coluzzi, M. (1968). Cromosomi politenici delle cellule nutrici ovariche nel complesso gambiae del genere Anopheles. – Parassitologia 10, 179183.Google Scholar
Coluzzi, M. (1970). Sibling species in Anopheles and their importance in malariology. – Misc. Publs ent. Soc. Am. 7, 6372.Google Scholar
Coluzzi, M. & Sabatini, A. (1967). Cytogenetic observations on species A and B of the Anopheles gambiae complex. – Parassitologia 9, 7388.Google Scholar
Coluzzi, M. & Sabatini, A. (1968). Cytogenetic observations on species C of the Anopheles gambiae complex. – Parassitologia 10, 155165.Google Scholar
Coluzzi, M. & Sabatini, A. (1969). Cytogenetic observations on the saltwater species, Anopheles merus and Anopheles melas, of the gambiae complex. – Parassitologia 11, 177187.Google Scholar
Davidson, G. (1964). Anopheles gambiae, a complex of species. – Bull. Wld Hlth Org. 31, 625634.Google ScholarPubMed
Davidson, G. (1966). Distribution records of member species of the Anopheles gambiae complex (identifications up to May, 1966). – WHO/Mal/66.570, 16 pp.Google Scholar
Davidson, G. & Hunt, R.H. (in press). The crossing and chromosome characteristics of a new, sixth, species in the Anopheles gambiae complex. – Parassitologia.Google Scholar
Davidson, G., Paterson, H.E., Coluzzi, M., Mason, G.F. & Micks, D.W. (1967). The Anopheles gambiae complex. In Wright, J. W. & Pal, R. (Ed.) Genetics of insect vectors of disease. – 211250. Amsterdam,.Elsevier.Google Scholar
Davidson, G. & White, G.B. (1972). The crossing characteristics of a new, sixth species in the Anopheles gambiae complex. – Trans. R. Soc. trop. Med. Hyg. 66, 531532.Google Scholar
DeMeillon, B. (1947). The Anophelini of the Ethiopean geographical region. – Publs S. Afr. Inst. med. Res. no. 49, 272 pp.Google Scholar
Dutton, J.E. & Todd, J.L. (1906). Rapport sur l' expédition au Congo (1903–1905). – Mem. L'pool Sch. trop. Med. no. 20, 172.Google Scholar
Edwards, F.W. (1923). Oligocene mosquitoes in the British Museum; with a summary of our present knowledge concerning fossil Culicidae. – Q. Jl Geol. Soc. Lond. 79, 139154.Google Scholar
Evans, A.M. (1938). Mosquitoes of the Ethiopean Region. II. – Anophelini, adults and early stages. – 404 pp. London, British Museum (Natural History).Google Scholar
French, W.L., Baker, R.H & Kitzmiller, J.B. (1962). Preparation of mosquito chromosomes. – Mosquito News 22, 377383.Google Scholar
Gibbins, E. G. (1932). Natural malaria infection of house-frequenting Anopheles mosquitoes in Uganda. – Ann. trop. Med. Parasit. 26, 239266.CrossRefGoogle Scholar
Gibbins, E.G. (1936). On a melanic inland race of Anopheles costalis Giles (gambiae) in Uganda. – Ann, trop. Med. Parasit. 30, 275282.Google Scholar
Gillies, M.T. & DeMeillon, B. (1968). The Anophelinae of Africa south of the Sahara (Ethiopean zoogeographical region. – Publs S. Afr. Inst. med. Res. no. 54, 343 pp.Google Scholar
Goma, L.K.H. (1960). The swamp-breeding mosquitoes of Uganda: records of larvae and their habitats. – Bull. ent. Res. 51, 7794.CrossRefGoogle Scholar
Green, C.A. (1971). The practical problem of identifying members of the Anopheles gambiae complex in autecological studies. – Parassitologia 13, 421427.Google Scholar
Green, C.A. (1972). Cytological maps for the practical identification of females of three freshwater species of the Anopheles gambiae complex. – Ann. trop. Med. Parasit. 66, 143147.CrossRefGoogle ScholarPubMed
Haddow, A.J. (1942). The mosquito fauna and climate of native huts at Kisumu, Kenya. – Bull. ent. Res. 33, 91142.Google Scholar
Haddow, A.J. (1945a). On the mosquitoes of Bwamba County, Uganda. I. – Description of Bwamba with special reference to mosquito ecology. – Proc. zool. Soc. Lond. 115, 113.CrossRefGoogle Scholar
Haddow, A.J. (1945b). The mosquitoes of Bwamba County, Uganda. II. Biting activity with special reference to the influence of microclimate. – Bull. ent. Res. 36, 3373.Google Scholar
Haddow, A.J. (1945c). The mosquitoes of Bwamba County, Uganda. III. – The vertical distribution of mosquitoes in a banana plantation and the biting cycle of Aëdes (Stegomyia) simpsoni Theo. – Bull. ent. Res. 36, 297304.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. 45, 199242.Google Scholar
Haddow, A.J.Dick, G.W.A. (1948). Catches of biting Diptera in Uganda, with anaesthetized monkeys as bait. – Ann. trop. Med. Parasit. 42, 271277.CrossRefGoogle ScholarPubMed
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.Google Scholar
Haddow, A.J. & Mahaffy, A.F. (1949). The mosquitoes of Bwamba County, Uganda. VII. – Intensive catching on tree-platforms with further observations on Aëdes (Stegomyia) africanus Theobald. – Bull. ent. Res. 40 169178.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
Holstein, M. (1954). Biology of Anopheles gambiae. Research in French West Africa. – Monogr. Ser. Wld Hlth Org. no. 9, 172 pp.Google Scholar
Hunt, R.H. (1972). Cytological studies on a new member of the Anopheles gambiae complex. – Trans. R. Soc. trop. Med. Hyg. 66, 532.Google ScholarPubMed
Hunt, R.H. & Krafsur, E.S. (1972). Cytological demonstration of some heterozygous reciprocal translocations in Anopheles gambiae species A. – Trans. R. Soc. trop. Med. Hyg. 66, 23.Google Scholar
Ismail, I.A.H. & Hammoud, E.I. (1968). The use of coeloconic sensillae on the female antenna in differentiating the members of the Anopheles gambiae Giles complex. – Bull. Wld Hlth Org. 38, 814821.Google ScholarPubMed
James, T.C. (1967). Thermal springs in Tanzania. – Trans. Instn. Min. Metall. 76, 1B–18B.Google Scholar
Kingdon, J. (1971). East African mammals. An atlas of evolution in Africa. Vol. I. – 446 pp. London, Academic Press.Google Scholar
Lumsden, W.H.R. (1951). Probable insect vectors of yellow fever virus, from monkey to man, in Bwamba County, Uganda. – Bull. ent. Res. 42, 317330.Google Scholar
Lumsden, W.H.R. (1952). The crepuscular biting activity of insects in the forest canopy in Bwamba, Uganda. A study in relation to the sylvan epidemiology of yellow fever. – Bull. ent. Res. 42, 721760.CrossRefGoogle Scholar
Lumsden, W.H.R. (1955). Entomological studies, relating to yellow fever epidemiology, at Gede and Taveta, Kenya. – Bull. ent. Res. 46, 149183.Google Scholar
Mattingly, P.F. (1949). Studies on West African forest mosquitoes. – Part I. The seasonal distribution, biting cycle and vertical distribution of four of the principal species. – Bull. ent. Res. 40, 149168.Google Scholar
Mayr, E. (Ed.) (1957). The species problem. A symposium presented at the Atlanta meeting of the American Association for the Advancement of Science, December 28–29,1955. – Publs Am. Ass. Advmt Sci. no. 50, 395pp.Google Scholar
Mayr, E. (1966). Animal species and evolution.797pp. Harvard, University Press.Google Scholar
Mayr, E., Linsley, E.G. & Usinger, R.L. (1953). Methods and principles of systematic zoology.328pp. New York, McGraw-Hill.Google Scholar
McConnell, R.B. & Brown, J.M. (1954). Drilling for geothermal power at Buranga Hot Springs, Toro. Unpublished progress report (JMB 17/RBM 16) of the Geographical Survey and Mines Department, Uganda.Google Scholar
McCrae, A.W.R., Ssenkubuge, Y., Kitama, A. & Ssaku, C. (1970). Studies on the Anopheles gambiae species complex. – Rep. E. Afr. Virus Res. Inst. 1969, 6163.Google Scholar
Muirhead-Thomson, R.C. (1951). Mosquito behaviour in relation to malaria transmission and control in the tropics. – 219pp. London, Edward Arnold.Google Scholar
Neri, P. (1965). Revue taxonomique, aspect écologique et biologique des Diptères (Culicidae) présents dans la forêt de Manéra (Province du Kafa) Ethiopia. – Cah. ORSTOM – Ent. med. 3, 4756.Google Scholar
Neri, P., Sérié, C., Andral, L. & Poirier, A. (1968). Etude sur la fièvre jaune en Ethiopie. 4. Recherches entomologiques à la station de Manéra. – Bull. Wld Hlth Org. 38, 863872.Google Scholar
Njogu, A.R. & Kinoti, G.K. (1971). Observations on the breeding sites of mosquitoes in Lake Manyara, a saline lake in the East African Rift Valley. – Bull. ent. Res. 60, 473479.Google Scholar
Ovazza, M., Hamon, J. & Neri, P. (1956). Contribution à l'étude des diptéres vulnérants de l'empire d'Ethiopie. I. Culicidae. – Bull. Soc. Path. exot. 49, 151182.Google ScholarPubMed
Paterson, H.E., Paterson, J.S. & Van Eeden, G.J. (1963). A new member of the Anopheles gambiae complex. A preliminary report. – Med. Proc. 9, 414417.Google Scholar
Reid, J.A. (1968). Anopheline mosquitoes of Malaya and Borneo. – Stud. Inst. Med. Res., Malaysia, no. 31, 520pp.Google Scholar
Reid, J.A. (1970). Anopheline systematics and malaria control with special reference to Southeast Asia. – Misc. Publs ent. Soc. Am. 7, 5662.Google Scholar
Ribbands, C.R. (1944a). Differences between Anopheles melas (A. gambiae var. melas) and Anopheles gambiae. I. The larval pecten. – Ann. trop. Med. Parasit. 38, 8586.CrossRefGoogle Scholar
Ribbands, C.R. (1944b). Differences between Anopheles melas and Anopheles gambiae. II. Salinity relations of larvae and maxillary palp banding of adult females. –Ann. trop. Med. Parasit. 38, 8799.Google Scholar
Smith, A. & Vail, J.W. (1959). Relationship between salinity and breeding of Anopheles gambiae in north-eastern Tanganyika. – Nature, Lond. 183, 12031204.CrossRefGoogle ScholarPubMed
Turner, R.L. (1972). Malaria epidemiological observations from unsprayed study districts in Ethiopia. – Mosquito News 32, 608613.Google Scholar
White, G.B. (1970). Chromosomal evidence for natural interspecific hybridization by mosquitoes of the Anopheles gambiae complex. – Nature, Lond. 231, 184185.Google Scholar
White, G.B. (1972). The Anopheles gambiae complex and malaria transmission around Kisumu, Kenya. – Trans. R. Soc. trop. Med. Hyg. 66, 572581.CrossRefGoogle ScholarPubMed
White, G.B. & Davidson, G. (1972). Melanic variants of Anopheles larvae. – Trans. R. Soc. trop. Med. Hyg. 66, 532533.Google Scholar
White, G.B., Magayuka, S.A & Boreham, P.F.L. (1972). Comparative studies on sibling species of the Anopheles gambiae Giles complex (Dipt., Culicidae): bionomics and vectorial activity of species A and species B at Segera, Tanzania. – Bull. ent. Res. 62, 295317.Google Scholar
White, G.B. & Muniss, J.N. (1970). General surveys in East Africa of sibling species belonging to the Anopheles gambiae complex. – Rep. E. Afr. Inst. Malar. 1970.Google Scholar
White, G.B. & Muniss, J.N. (1971). Further surveys in East Africa of sibling species belonging to the Anopheles gambiae complex. 1971. – Rep. E. Afr. Inst. Malar. 1971.Google Scholar
White, G.B. & Muniss, J.N. (1972). Taxonomic value of spermatheca size for distinguishing between four members of the Anopheles gambiae complex of mosquitoes in East Africa. – Bull. Wld Hlth Org. 46, 793799.Google ScholarPubMed
White, G.B. & Rosen, P. (1973). Comparative studies on sibling species of the Anopheles gambiae Giles complex (Diptera : Culicidae). II. Ecology of species A and species B in savanna around Kaduna, Nigeria, during transition from wet to dry season. – Bull. ent. Res. 62, 613625.Google Scholar
Wigglesworth, V.B. (1965). The principles of insect physiology.6th edn, 741pp. London, Methuen.Google Scholar
Zahar, A.R., Hills, M. & Davidson, G. (1970). An attempt to group freshwater species of the Anopheles gambiae complex by some morphological larval and adult characters. – Parassitologia 12, 3146.Google Scholar