Density-dependent processes in the transmission of human onchocerciasis: Relationship between microfilarial intake and mortality of the simuliid vector

Parasitology

Volumn 113, Issue 4, 1996, Pages 331-355

  Basanez M G ^a,c   Townson, H ^b   Williams, J R ^c   Frontado, H ^d   Villamizar, N J ^d   Anderson, R M ^c  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d CAICET   (Venezuela)

Author keywords

age dependent fly survival; cibarial armature; Onchocerca volvulus; parasite induced vector mortality; Simulium

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HOST PARASITE INTERACTION; MODEL; MORTALITY; NONHUMAN; ONCHOCERCA VOLVULUS; ONCHOCERCIASIS; PARASITE TRANSMISSION; PRIORITY JOURNAL; SIMULIUM; SURVIVAL; VECTOR CONTROL;

ANIMALIA; ONCHOCERCA VOLVULUS; SIMULIIDAE; SIMULIUM DAMNOSUM; SIMULIUM GUIANENSE; SIMULIUM OCHRACEUM;

EID: 0029743454     PISSN: 00311820     EISSN: None     Source Type: Journal    
DOI: 10.1017/s003118200006649x     Document Type: Article

References (119)

1. ANDERSON, R. M. & MAY, R. M. (1979). Prevalence of schistosome infections within molluscan populations: observed patterns and theoretical predictions. Parasitology 79, 63-94.
2. ANDERSON, R. M. & WHITFIELD, P. J. (1975). Survival characteristics of the free-living cercarial population of the ectoparasitic digenean Transversotrema patialensis (Soparker, 1924). Parasitology 70, 295-310.
3. ANDERSON, R. M., WHITFIELD, P. J. & MILLS, C. A. (1977). An experimental study of the population dynamics of an ectoparasitic digenean Transversotrema patialense: the cercarial and adult stages. Journal of Animal Ecology 46, 555-580.
4. ANDERSON, R. M., MERCER, J. G., WILSON, R. A. & CARTER, N. P. (1982). Transmission of Schistosoma mansoni from man to snail: experimental studies of miracidial survival and infectivity in relation to larval age, water temperature, host size and host age. Parasitology 85, 339-360.
5. ARMITAGE, P. & BERRY, G. (1987). Statistical Methods in Medical Research. 2nd Edn. Blackwell Scientific Publications, Oxford.
6. BAIN, O. (1971). Transmission des filarioses. Limitation des passages des microfilaires ingérées vers l'hémocèle du vecteur; interprétation. Annales de Parasitologie 46, 613-631.
7. BAIN, O. (1976). Traversée de la paroi stomacale du vecteur par les microfilaires: Techniques d'étude utilisées, importance épidémiologique. Bulletin of the World Health Organisation 54, 397-401
8. BAIN, O., DURETTE-DESSET, M. C. & DE LEÓN, R. (1974). Onchocercose au Guatemala: L'ingestion des microfilaires par Simulium ochraceum et leur passage dans l'hémocèle de ce vecteur. Annales de Parasitologie 49, 467-487.
9. BASAÑEZ, M. G., YARZABAL, L., TAKAOKA, H., SUZUKI, H., NODA, S. & TADA, I. (1988). The vectorial role of several blackfly species (Diptera: Simuliidae) in relation to human onchocerciasis in the Sierra Parima and Upper Orinoco regions of Venezuela. Annals of Tropical Medicine and Parasitology 82, 597-611.
10. BASAÑEZ, M. G., BOUSSINESQ, M., PROD'HON, J., FRONTADO, H., VILLAMIZAR, N. J., MEDLEY, G. F. & ANDERSON, R. M. (1994). Density-dependent processes in the transmission of human onchocerciasis: intensity of microfilariae in the skin and their uptake by the simuliid host. Parasitology 108, 115-127.
11. BASAÑEZ, M. G., REMME, J. H. F., ALLEY, E. S., BAIN, O., SHELLEY, A. J., MEDLEY, G. F. & ANDERSON, R. M. (1995). Density-dependent processes in the transmission of human onchocerciasis: relationship between the numbers of microfilariae ingested and successful larval development in the simuliid vector. Parasitology 110, 409-427.
12. BECKETT, E. B. (1971). Histological changes in mosquito flight muscle fibres associated with parasitization by filarial larvae. Parasitology 63, 365-372.
13. BERRY, W. J., ROWLEY, W. A. & CHRISTENSEN, B. M. (1986). Influence of developing Brugia pahangi on spontaneous flight activity of Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 23, 441-445.
14. BEYER, W. H. (1991). CRC Standard Mathematical Tables and Formulae, 29th Edn. Boca Raton, CRC Press, Florida.
15. BILLINGSLEY, P. F., MEDLEY, G. F., CHARLWOOD, J. D. & SINDEN, R. E. (1994). Relationship between prevalence and intensity of Plasmodium falciparum infection in natural populations of Anopheles mosquitoes. American Journal of Tropical Medicine and Hygiene 51, 260-270.
16. BIRLEY, M. H., WALSH, J. F. & DAVIES, J. B. (1983). Development of a model for Simulium damnosum s.l. recolonization dynamics at a breeding site in the Onchocerciasis Control Programme area when control is interrupted. Journal of Applied Ecology 20, 507-519.
17. BROADBENT, S. (1958). Simple mortality rates. Applied Statistics 7, 86-95.
18. CHEKE, R. A., GARMS, R. & KERNER, M. (1982). The fecundity of Simulium damnosum s.l. in northern Togo and infections with Onchocerca spp. Annals of Tropical Medicine and Parasitology 76, 561-568.
19. CHRISTENSEN, B. M. (1978). Dirofilaria immitis: effect on the longevity of Aedes trivittatus. Experimental Parasitology 44, 116-123.
20. CLEMENTS, A. N. & PATERSON, G. D. (1981). The analysis of mortality and survival rates in wild populations of mosquitoes. Journal of Applied Ecology 18, 373-399.
21. COLLINS, R. C., CAMPBELL, C. C., WILTON, D. P. & NEWTON, L. (1977). Quantitative aspects of the infection of Simulium ochraceum by Onchocerca volvulus. Tropenmedizin und Parasitologie 28, 235-243.
22. COLLINS, R. C., LEHMANN, T., VIEIRA, G. J. C. & GUDERIAN, R. H. (1992a). Onchocerciasis transmission in Ecuador: vector capacity of Simulium exiguum. American Journal of Tropical Medicine and Hygiene (Suppl.) 47, 151-152.
23. COLLINS, R. C., LEHMANN, T., VIEIRA, G. J. C. & GUDERIAN, R. H. (1995). Vector competence of Simulium exiguum for Onchocerca volvulus: implications for the epidemiology of onchocerciasis. American Journal of Tropical Medicine and Hygiene 52, 213-218.
24. COLLINS, R. C., OCHOA, J. O., CUPP, E. W., GONZALEZ-PERALTA, C. & PORTER, C. H. (1992b). Microepidemiology of onchocerciasis in Guatemala: dispersal and survival of Simulium ochraceum. American Journal of Tropical Medicine and Hygiene 47, 147-155.
25. COX, D. R. & OAKES, D. (1984). Analysis of Survival Data. Chapman and Hall, London.
26. CUPP, E. W. & COLLINS, R. C. (1979). The gonotrophic cycle in Simulium ochraceum. American Journal of Tropical Medicine and Hygiene 28, 422-426.
27. DALMAT, H. T. & GIBSON, C. L. (1952). A study of flight ranges and longevity of blackflies (Diptera: Simuliidae) infected with Onchocerca volvulus. Annals of the Entomological Society of America 45, 605-612.
28. DE LEÓN, J. & DUKE, B. O. L. (1966). Experimental studies on the transmission of Guatemalan and West African strains of Onchocerca volvulus by Simulium ochraceum, S. metallicum and S. callidum. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 735-752.
29. DIETZ, K. (1982). The population dynamics of onchocerciasis. In Population Dynamics of Infectious Diseases (ed. Anderson, R. M.), pp. 209-241. London: Chapman and Hall.
30. DUKE, B. O. L. (1962a). Studies on factors influencing the transmission of onchocerciasis. I. The survival rate of Simulium damnosum under laboratory conditions and the effect upon it of Onchocerca volvulus. Annals of Tropical Medicine and Parasitology 56, 130-135.
31. DUKE, B. O. L. (1962b). Studies on factors influencing the transmission of onchocerciasis. II. The intake of Onchocerca volvulus microfilariae by Simulium damnosum and the survival of the parasites in the fly under laboratory conditions. Annals of Tropical Medicine and Parasitology 56, 255-263.
32. DUKE, B. O. L. (1966). Onchocerca Simulium complexes. III. The survival of Simulium damnosum after high intakes of microfilariae of incompatible strains of Onchocerca volvulus and the survival of the parasite in the fly. Annals of Tropical Medicine and Parasitology 60, 495-500.
33. DUKE, B. O. L. (1968a). Studies on factors influencing the transmission of onchocerciasis. IV. The biting-cycles, infective biting density and transmission potential of 'forest' Simulium damnosum. Annals of Tropical Medicine and Parasitology 62, 95-106.
34. DUKE, B. O. L. (1968b). Studies on factors influencing the transmission of onchocerciasis. V. The stages of Onchocerca volvulus in wild 'forest' Simulium damnosum, the fate of the parasites in the fly, and the age-distribution of the biting population. Annals of Tropical Medicine and Parasitology 62, 107-116.
35. DUKE, B. O. L. (1970). Onchocerca Simulium complexes. VI. Experimental studies on the transmission of Venezuelan and West African strains of Onchocerca volvulus by Simulium metallicum and S. exiguum in Venezuela. Annals of Tropical Medicine and Parasitology 64, 421-431.
36. DUKE, B. O. L. (1973). Studies on factors influencing the transmission of onchocerciasis. VIII. The escape of infective Onchocerca volvulus larvae from feeding 'forest' Simulium damnosum. Annals of Tropical Medicine and Parasitology 67, 95-99.
37. DUKE, B. O. L. & MOORE, P. J. (1968). The contribution of different age groups to the transmission of onchocerciasis in a Cameroon forest village. Transactions of the Royal Society of Tropical Medicine and Hygiene 62, 22-28.
38. DYE, C. (1990). Epidemiological significance of vector-parasite interactions. Parasitology 101, 409-415.
39. DYE, C. (1992). The analysis of parasite transmission by bloodsucking insects. Annual Review of Entomology 37, 1-19.
40. DYE, C. (1994). The epidemiological context of vector control. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 147-149.
41. DYE, C. & BAKER, R. H. A. (1986). Measuring the capacity of blackflies as vectors of onchocerciasis: Simulium damnosum s.l. in southwest Sudan. Journal of Applied Ecology 23, 883-893.
42. DYE, C., GUY, M. W., ELKINS, D. B., WILKES, T. J. & KILLICK-KENDRICK, R. (1987). The life expectancy of phlebotomine sandflies: first field estimates from southern France. Medical and Veterinary Entomology 1, 417-425
43. DYE, C. & WILLIAMS, B. G. (1995). Non-linearities in the dynamics of indirectly-transmitted infections (or, does having a vector make a difference?). In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. & Dobson, A. P.), pp. 260-279. Cambridge University Press, Publications of the Newton Institute, Cambridge: Cambridge University Press.
44. EICHNER, M., RENZ, A., WAHL, G. & ENYONG, P. (1991). Development of Onchocerca volvulus microfilariae injected into Simulium species from Cameroon. Medical and Veterinary Entomology 5, 293-297.
45. ELLROTT, D. (1987). The effect of different microfilarial densities of Brugia malayi in Mastomys natalensis on the mortality of the vector Aedes aegypti. Tropical Medicine and Parasitology 38, 344.
46. FINDLAY, W. & WATT, D. A. (1985). Pascal. An Introduction to Methodical Programming, 3rd. Edn. Pitman, London.
47. GAD, A. M., MAIER, W. A. & PIEKARSKI, G. (1979). Pathology of Anopheles stephensi after infection with Plasmodium berghei berghei. I. Mortality rate. Zeitschrift für Parasitenkunde 60, 249-261.
48. GALLIARD, P. H. (1957). Mortalité chez les culicidés infestés par Dirofilaria immitis et Wuchereria bancrofti. Zeitschrift für Tropenmedizin und Parasitologie 8, 476-485.
49. GARMS, R. (1975). Observations on filarial infections and parous rates of anthropophilic blackflies in Guatemala, with reference to the transmission of Onchocerca volvulus. Tropenmedizin und Parasitologie 26, 169-182.
50. GARRETT-JONES, C. (1964). Prognosis for the interruption of malaria transmission through assessment of the mosquito's vectorial capacity. Nature 204, 1173-1175.
51. GILLIES, M. T. (1961). Studies on the dispersion and survival of Anopheles gambiae Giles in East Africa by means of marking and release experiments. Bulletin of Entomological Research 52, 99-127.
52. GILLIES, M. T. & WILKES, T. J. (1965). A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bulletin of Entomological Research 56, 237-262.
53. GOMPERTZ, B. (1825). On the nature of the function expressive of the law of human mortality, and on a new mode of determining the value of life contingencies. Philosophical Transactions of the Royal Society 115, 513-585.
54. HACKER, C. S. (1971). The differential effect of Plasmodium gallinaceum on the fecundity of several strains of Aedes aegypti. Journal of Invertebrate Pathology 18, 373-377.
55. HAM, P. J. & BANYA, A. J. (1984). The effect of experimental Onchocerca infections on the fecundity and oviposition of laboratory reared Simulium sp (Diptera, Simuliidae). Tropenmedizin und Parasitologie 35, 61-66.
56. HAM, P. J. & GALE, C. L. (1984). Blood meal enhanced Onchocerca development and its correlation with fecundity in laboratory reared blackflies (Diptera, Simuliidae). Tropenmedizin und Parasitologie 35, 212-216.
57. HASHIGUCHI, Y., KAWABATA, M., ITO, S. & RECINOS, M. M. (1981). Limited fly load and development of Onchocerca volvulus microfilariae in Guatemalan Simulium ochraceum. Journal of Helminthology 55, 189-196.
58. HASTINGS, N. A. J. & PEACOCK, J. B. (1974). Statistical Distributions. Butterworths, London.
59. HUSAIN, A. & KERSHAW, W. E. (1971). The effect of filariasis on the ability of a vector mosquito to fly and feed and to transmit the infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 617-619.
60. JORDAN, P. & GOATLY, K. D. (1962). Bancroftian filariasis in Tanganyika: A quantitative study of the uptake, fate and development of microfilariae of Wuchereria bancrofti in Culex fatigans. Annals of Tropical Medicine and Parasitology 56, 173-187.
61. KAHN, H. A. & SEMPOS, C. T. (1989). Statistical Methods in Epidemiology. Oxford University Press, Oxford.
62. KERSHAW, W. E., CHALMERS, T. A. & DUKE, B. O. L. (1954). Studies on the intake of microfilariae by their insect vectors, their survival, and their effect on the survival of their vectors. IV. The survival rate of Chrysops under laboratory conditions, and the effect upon it of Loa loa. Annals of Tropical Medicine and Parasitology 48, 329-339.
63. KERSHAW, W. E., CHALMERS, T. A. & LAVOIPIERRE, M. M. J. (1954). Studies on arthropod survival. I. The pattern of mosquito survival in laboratory conditions. Annals of Tropical Medicine and Parasitology 48, 442-450.
64. KERSHAW, W. E., LAVOIPIERRE, M. M. J. & CHALMERS, T. A. (1953). Studies on the intake of microfilariae by their insect vectors, their survival, and their effect on the survival of their vectors. I. Dirofilaria immitis and Aèdes aegypti. Annals of Tropical Medicine and Parasitology 47, 207-224.
65. KIRKWOOD, B. R. (1988). Essentials of Medical Statistics. Oxford Scientific Publications, Oxford.
66. KLEIN, T. A., HARRISON, B. A., ANDRÉ, R. G., WHITMIRE, R. E. & INLAO, I. (1982). Detrimental effects of Plasmodium cynomolgy infections on the longevity of Anopheles dims. Mosquito News 42, 265-271.
67. KLEIN, T. A., HARRISON, B. A., GROVE, J. S., DIXON, S. V. & ANDRÉ, R. G. (1986). Correlation of survival rates of Anopheles dirus A (Diptera: Culicidae) with different infection densities of Plasmodium cynomolgy. Bulletin of the World Health Organization 64, 901-907.
68. KRAFSUR, E. S. & GARRETT-JONES, C. (1977). The survival in nature of Wuchereria-infected Anopheles funestus Giles in North-eastern Tanzania. Transacions of the Royal Society of Tropical Medicine and Hygiene 71, 155-160.
69. LAURENCE, B. R. (1963). Natural mortality in two filarial vectors. Bulletin of the World Health Organization 28, 229-234.
70. LAVOIPIERRE, M. M. J. (1958). Studies on the host-parasite relationships of filarial nematodes and their arthropod hosts. II. The arthropod as a host to the nematode: a brief appraisal of our present knowledge, based on a study of the more important literature from 1878 to 1957. Annals of Tropical Medicine and Parasitology 52, 326-345.
71. LAVOIPIERRE, M. M. J. (1961). Blood-feeding, fecundity and ageing in Aedes aegypti var. queenslandensis. Nature 191, 575-576.
72. LE BERRE, R. (1966). Contribution a l'étude biologique et écologique de Simulium damnosum Theobald, 1903 (Diptera Simuliidae). Mémoires de l'Office de la Recherche Scientifique et Technique Outre-Mer 17, 204.
73. LE BERRE, R., BALAY, G., BRENGUES, J. & COZ, J. (1964). Biologie et écologie de la femelle de Simulium damnosum Theobald, 1903, en fonction des zones bioclimatiques d'Afrique occidentale. Influence sur l'epidemiologie de l'onchocercose. Bulletin of the World Health Organization 31, 843-855.
74. LEWIS, D. J. (1953). Simulium damnosum and its relation to onchocerciasis in the Anglo-Egyptian Sudan. Bulletin of Entomological Research 43, 597-644.
75. LINDSAY, S. W. & DENHAM, D. A. (1986). The ability of Aedes aegypti mosquitoes to survive and transmit infective larvae of Brugia pahangi over successive blood meals. Journal of Helminthology 60, 159-168.
76. LINES, J. D., WILKES, T. J. & LYIMO, E. O. (1991). Human malaria infectiousness measured by age-specific sporozoite rates in Anopheles gambiae in Tanzania. Parasitology 102, 167-177.
77. LYIMO, E. O. & KOELLA, J. C. (1992). Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology 104, 233-237.
78. MACDONALD, G. (1952a). The analysis of the sporozoite rate. Tropical Diseases Bulletin 49, 569-586.
79. MACDONALD, G. (1952b). The analysis of equilibrium in malaria. Tropical Diseases Bulletin 49, 813-829.
80. MACDONALD, G. (1957). The Epidemiology and Control of Malaria. Appendix I. Mathematical Statement. Oxford University Press, London.
81. MAIER, W. A., BECKER-FELDMAN, H. & SEITZ, H. M. (1987). Pathology of malaria-infected mosquitoes. Parasitology Today 3, 216-218.
82. MEDLEY, G. F., SINDEN, R. E., FLECK, S., BILLINGSLEY, P. F., TIRAWANCHAI, N. & RODRIGUEZ, M. H. (1993). Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 106, 441-449.
83. MILLEST, A. L., CHEKE, R. A., HOWE, M. A., LEHANE, M. J. & GARMS, R. (1992). Determining the ages of adult females of different members of the Simulium damnosum complex (Diptera: Simuliidae) by the pteridine accumulation method. Bulletin of Entomological Research 82, 219-226.
84. OMAR, M. S. & GARMS, R. (1975). The fate and migration of microfilariae of a Guatemalan strain of Onchocerca volvulus in Simulium ochraceum and S. metallicum, and the role of the buccopharyngeal armature in the destruction of microfilariae. Tropenmedizin und Parasitologie 26, 183-190.
85. OMAR, M. S. & GARMS, R. (1977). Lethal damage to Simulium metallicum following high intakes of Onchocerca volvulus microfilariae in Guatemala. Tropenmedizin und Parasitologie 28, 109-119.
86. PHILIPPON, B. (1977). Étude de la transmission d'Onchocerca volvulus (Leuckart, 1893) (Nematoda, Onchocercidae) par Simulium damnosum Theobald, 1903 (Diptera, Simuliidae) en Afrique tropicale. Travaux et Documents de l'Office de la Recherche Scientifique et Technique Outre-Mer 63, 308.
87. PHILIPPON, B. & BAIN, O. (1972). Transmission de l'onchocercose humaine en zone de savane d'Afrique occidentale, passage des microfilaires d'Onchocerca volvulus Leuck. dans l'hémocèle de la femelle de Simulium damnosum Th. Cahiers O.R.S.T.O.M., série Entomologie médicale et Partisitologie 10, 251-261.
88. PICHON, G. (1974). Relations mathematiques entre le nombre des microfilaires ingérées et le nombre des parasites chez différents vecteurs natureles ou expérimentaux de filarioses. Cahiers O.R.S.T.O.M., série Entomologie médicale et Parasitologie 12, 199-216.
89. PICHON, G., PERRAULT, G. & LAIGRET, J. (1974). Rendement parasitaire chez les vecteurs de filarioses. Bulletin of the World Health Organization 51, 517-524.
90. PLAISIER, A. P., VAN OORTMARSSEN, G. J., REMME, J. & HABBEMA, J. D. F. (1991). The reproductive lifespan of Onchocerca volvulus in West African savanna. Acta Tropica 48, 271-284.
91. PORTER, C. H. & COLLINS, R. C. (1985). The gonotrophic cycle of wild Simulium ochraceum and the associated development of Onchocerca volvulus. American Journal of Tropical Medicine and Hygiene 34, 302-309.
92. PORTER, C. H. & COLLINS, R. C. (1988a). Biting activity of blackflies in Guatemala: parity rates and differences between localities and habitats. American Journal of Tropical Medicine and Hygiene 38, 142-152.
93. PORTER, C. H. & COLLINS, R. C. (1988b). Seasonality of adult blackflies and Onchocerca volvulus transmission in Guatemala. American Journal of Tropical Medicine and Hygiene 38, 153-167.
94. RENSHAW, M. & HURD, H. (1994a). The effects of Onchocerca lienalis infection on vitellogenesis in the British blackfly Simulium ornatum. Parasitology 109, 337-343.
95. RENSHAW, M. & HURD, H. (1994b). Vitellogenin sequestration by Simulium oocytes: the effect of Onchocerca infection. Physiological Entomology 19, 70-74.
96. RENZ, A., BARTHELMESS, C. & EISENBEISS, W. (1987). Vectorial capacity of Simulium damnosum s.l. populations in Cameroon. Tropical Medicine and Parasitology 38, 344-345.
97. ROWLAND, M. & BOERSMA, E. (1988). Changes in the spontaneous flight activity of the mosquito Anopheles stephensi by parasitization with the rodent malaria Plasmodiiim yoelii. Parasitology 97, 221-227.
98. ROWLAND, M. W. & LINDSAY, S. W. (1986). The circadian flight activity of Aedes aegypti parasitized with the filarial nematode Brugia pahangi. Physiological Entomology 11, 325-334.
99. RUSSELL, P. F. & RAO, T. R. (1942). Observations on longevity of Anopheles culicifacies imagines. American Journal of Tropical Medicine 22, 517-533.
100. SACHER, G. A. (1956). On the statistical nature of mortality with special reference to chronic radiation mortality. Radiology 67, 250-258.
101. SACHER, G. A. & TRUCCO, E. (1962). The stochastic theory of mortality. Annals of the New York Academy of Sciences 96, 985-1007.
102. SAMARAWICKREMA, W. A. (1967). A study of the age-composition of natural populations of Culex pipiens fatigans Wiedemann in relation to the transmission of filariasis due to Wuchereria bancrofti (Cobbold) in Ceylon. Bulletin of the World Health Organization 37, 117-137.
103. SAMARAWICKREMA, W. A. & LAURENCE, B. R. (1978). Loss of filarial larvae in a natural mosquito population. Annals of Tropical Medicine and Parasitology 72, 561-565.
104. SCHIEFER, B. A., WARD, R. A. & ELDRIDGE, B. K. (1977). Plasmodium cynomolgy: effects of malaria infection on laboratory flight performance of Anopheles stephensi mosquitoes. Experimental Parasitology 41, 397-404.
105. SHELLEY, A. J. (1988). Vector aspects of the epidemiology of onchocerciasis in Latin America. Annual Review of Entomology 30, 337-366.
106. SHELLEY, A. J. (1991). Simuliidae and the transmission and control of human onchocerciasis in Latin America. Cadernos de Saúde Pública, RJ 7, 310-327.
107. SHELLEY, A. J. (1994). Factors affecting filarial transmission by simuliids. In Advances in Disease Vector Research (ed. Harris, K. F.), Vol. 10, pp. 183-214. Springer-Verlag, New York.
108. SHELLEY, A. J., LUNA-DIAS, A. P. A., MORAES, M. A. P. & PROCUNIER, W. S. (1987). The status of Simulium oyapockense and S. limbatum as vectors of human onchocerciasis in Brazilian Amazonia. Medical and Veterinary Entomology 1, 219-234.
109. SINTON, J. A. SHUTE, P. G. (1938). A report on the longevity of mosquitoes in relation to the transmission of malaria in nature. Reports of Public Health and Medical Subjects, Ministry of Health, London 85, 1-45.
110. SOUTHWOOD, T. R. E. (1978). Ecological Methods With Particular Reference to the Study of Insect Populations 2nd Edn. Chapman and Hall, London.
111. TAKAOKA, H., OCHOA, J. O., JUAREZ, E. L. & HANSEN, K. M. (1982). Effects of temperature on development of Onchocerca volvulus in Simulium ochraceum, and longevity of the simuliid vector. Journal of Parasitology 68, 478-483.
112. TAKAOKA, H., SUZUKI, H., NODA, S., OCHOA, J. O. & TADA, I. (1984a). The intake, migration and development of Onchocerca volvulus microfilariae in Simulium haematopotum in Guatemala. Japanese Journal of Sanitary Zoology 35, 121-127.
113. TAKAOKA, H., SUZUKI, H., NODA, S., TADA, I., BASAÑEZ, M. G. & YARZABAL, L. (1984b). Development of Onchocerca volvulus larvae in Simulium pintoi in the Amazonas region of Venezuela. American Journal of Tropical Medicine and Hygiene 33, 414-419.
114. TOWNSON, H. (1970). The effect of infection with Brugia pahangi on the flight of Aedes aegypti. Annals of Tropical Medicine and Parasitology 64, 411-420.
115. TOWNSON, H. (1971). The mortality of various genotypes of the mosquito Aedes aegypti following the uptake of microfilariae of Brugia pahangi. Annals of Tropical Medicine and Parasitology 65, 93-106.
116. WHARTON, R. H. (1957). Studies on filariasis in Malaya: The efficiency of Mansonia longipalpis as an experimental vector of Wuchereria malayi. Annals of Tropical Medicine and Parasitology 51, 422-439.
117. WILLIAMS, P. & KERSHAW, W. K. (1961). Studies on the intake of microfilariae by their insect vectors, their survival, and their effect on the survival of their vectors. X. The survival of the tropical rat mite, the vector of filariasis in the cotton rat. Annals of Tropical Medicine and Parasitology 55, 217-230.
118. WORLD HEALTH ORGANIZATION (1987). WHO Expert Committee on Onchocerciasis. WHO Technical Report Series No. 752. Geneva.
119. ZAHEDI, M. & WHITE, G. B. (1994). Filaria vector competence of some Anopheles species. Tropical Medicine and Parasitology 45, 27-32.