Authors:
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-
1
Hacker CS, 1971. The differential effect of Plasmodium gallinaceum on the fecundity of several strains of Aedes aegypti.J Invert Pathol 18 :373–377.
-
2
Hacker CS, Kilama WL, 1974. The relationship between Plasmodium gallinaceum density and the fecundity of Aedes aegypti.J Invert Pathol 23 :101–105.
-
3
Freier JE, Friedman S, 1976. Effect of host infection with Plasmodium gallinaceum on the reproductive capacity of Aedes aegypti.J Invert Pathol 28 :161–166.
-
4
Hogg JC, Hurd H, 1995. Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Med Vet Ent 9 :176–180.
-
5
Hogg JC, Hurd H, 1995. Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology 111 :555–562.
-
6
Hogg JC, Hurd H, 1997. The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae s.l. in north east Tanzania. Parasitology 114 :325–331.
-
7
Anderson RA, Knols BG, Koella JC, 2000. Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. Parasitology 129 :329–333.
-
8
Ferguson HM, Read AF, 2002. Why is the effect of malaria parasites on mosquito survival still unresolved? Trends Parasitol 18 :256–261.
-
9
Ferguson HM, Read AF, 2002. Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proc R Soc Lond B Biol Sci 269 :1217–1224.
-
10
Carwardine SL, Hurd H, 1997. Effects of Plasmodium yoelii nigeriensis infection on Anopheles stephensi egg development and resorption. Med Vet Ent 11 :265–269.
-
11
Hopwood J, Ahmed A, Polwart A, Williams G, Hurd H, 2001. Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. J Exp Biol 204 :2773–2780.
-
12
Ahmed AM, Maingon RD, Taylor PJ, Hurd H, 1999. The effects of infection with Plasmodium yoelii nigeriensis on the reproductive fitness of the mosquito Anopheles gambiae.Invert Reprod Dev 36 :217–222.
-
13
Ferguson H, Rivero A, Read A, 2003. The influence of malaria parasite genetic diversity and anaemia on mosquito feeding and fecundity. Parasitology 127 :9–19.
-
14
Beier JC, 1998. Malaria parasite development in mosquitoes. Ann Rev Ent 43 :519–543.
-
15
Shililu JI, Maier WA, Seitz HM, Orago AS, 1998. Seasonal density, sporozoite rates and entomological inoculation rates of Anopheles gambiae and Anopheles funestus in a high-altitude sugarcane growing zone in Western Kenya. Trop Med Intl Health 3 :706–710.
-
16
Molineux L, Gramiccia G, 1980. The Garki Project: Research on the Epidemiology and Control of Malaria in the Sudan Savanna of West Africa. Geneva: World Health Organization.
-
17
Smith T, Charlwood J, Kihonda J, Mwankusye S, Billingsley P, Meuwissen J, Lyimo E, Takken W, Teuscher T, Tanner M, 1993. Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Tropica 54 :55–72.
-
18
Gouagna L, Ferguson HM, Okech BA, Killeen GF, Kabiru EW, Beier JC, Githure JI, Yan G, 2004. Plasmodium falciparum malaria disease manifestations in humans and transmission to Anopheles gambiae: a field study in Western Kenya. Parasitology 128 :235–243.
-
19
Minakawa N, Githure JI, Beier JC, Yan G, 2001. Anopheline mosquito survival strategies during the dry period in western Kenya. J Med Ent 38 :388–392.
-
20
Minakawa N, Mutero CM, Githure JI, Beier JC, Yan G, 1999. Spatial distribution and habitat characterization of anopheline mosquito larvae in western Kenya. Am J Trop Med Hyg 61 :1010–1016.
-
21
Briegel H, 1980. Determination of uric acid and hematin in a single sample of excreta from blood-fed insects. Experientia 36 :1428.
-
22
Snow R, Craig M, Deichmann U, Marsh K, 1999. Estimating mortality, morbidity and disability due to malaria among Africa’s non-pregnant populations. Bull WHO 77 :624–640.
-
23
Almeida AP, Billingsley PF, 1999. Induced immunity against the mosquito Anopheles stephensi: reactivity characteristics of immune sera. Med Vet Ent 13 :53–64.
-
24
Zacharski LR, Ornstein DL, Woloshin S, Schwartz LM, 2000. Association of age, sex, and race with body iron stores in adults: analysis of NHANES III data. Am Heart J 140 :98–104.
-
25
Langman LJ, Cole DE, 1999. Homocysteine. Crit Rev Clin Lab Sci 36 :365–406.
-
26
Proenza A, Crespi C, Roca P, Palou A, 2001. Gender related differences in the effect of aging on blood amino acid compartmentation. J Nutrl Biol 12 :431–440.
-
27
Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE, 1995. Pyrimethamine and proguanil resistance conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg 52 :565–568.
-
28
Abdel-Wahab A, Abdel-Muhsin A, Ali E, Suleiman S, Ahmed A, Walliker D, Babiker HA, 2002. Dynamics of gametocytes among Plasmodium falciparum clones in natural infections in an area of highly seasonal transmission. J Infect Dis 185 :1838–1842.
-
29
SAS II, 1997. SAS/STAT Software: Changes and Enhancements Through Release 6.12. Cary, NC: SAS Institute Inc.
-
30
Takken W, Klowden MJ, Chambers GM, 1998. Effect of body size on host seeking and blood meal utilization in Anopheles gambiae sensu stricto (Diptera: Culicidae): the disadvantage of being small. J Med Ent 35 :639–645.
-
32
Bonnet S, Gouagna L, Paul R, Safeukui I, Meunier J, Boudin C, 2003. Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans R Soc Trop Med Hyg 97 :53–59.
-
33
Muirhead-Thomson R, 1954. Factors determining the true reservoir of infection of Plasmodium falciparum and Wucheria bancrofti in a West African village. Trans R Soc Trop Med Hyg 48 :208–225.
-
34
Muirhead-Thomson R, 1957. The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae): random xenodiagnostic survey. Am J Trop Med Hyg 6 :971–979.
-
35
Mulder B, Tchuinkam T, Dechering K, Verhave J, Carnevale P, Meuwissen J, Robert V, 1994. Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg 88 :121–125.
-
36
Enwonwu C, Afolabi B, Salako L, Idigbe E, Bashirelani N, 2000. Increased plasma levels of histidine and hisamine in falciparum malaria: relevance to severity of infection. J Neur Trans 107 :1273–1287.
-
37
Dimond JB, Lea AO, Hahnert WF, DeLong DM, 1956. The amino acids required for egg production in Aedes aegypti.Can Ent 88 :57–62.
-
38
Uchida K, Moribayashi A, Matsuoka H, Oda T, 2003. Effects of mating on oogenesis induced by amino acid infusion, amino acid feeding, or blood feeding in the mosquito Anopheles stephensi (Diptera: Culicidae). J M Ent 40 :441–446.
-
39
Uchida K, 1993. Balanced amino acid composition essential for infusion-induced egg development in the mosquito (Culex pipiens pallens). J Insect Physiol 39 :615–621.
-
40
Uchida K, Oda T, Matsuoka H, Moribayashi A, Ohmori D, Eshita Y, Fukunaga A, 2001. Induction of Oogenesis in mosquitoes (Diptera: Culicidae) by infusion of the hemocoe with amino acids. J Med Ent 38 :572–575.
-
41
Hurd H, Hogg JC, Renshaw M, 1995. Interactions between bloodfeeding, fecundity and infection in mosquitoes. Parasitol Today 11 :411–416.
-
42
Ferguson H, Mackinnon M, Chan B, Read A, 2003. Mosquito mortality and the evolution of malaria virulence. Evolution 57 :2792–2804.
-
43
Agnew P, Koella J, Michalakis Y, 2000. Host life history responses to parasitism. Microbes Infect 2 :891–896.
-
44
Stearns SC, 1992. The Evolution of Life Histories. Oxford: Oxford University Press.
-
45
Hurd H, 2003. Manipulation of medically important insect vectors by their parasites. Ann Rev Ent 48 :141–161.
-
46
Charlwood JD, Vij R, Billingsley PF, 2000. Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of east Africa. Am J Trop Med Hyg 62 :726–732.
-
47
Charlwood JD, Pinto J, Sousa CA, Ferreira C, Gil V, Do Rosario VE, 2003. Mating does not affect the biting behaviour of Anopheles gambiae from the islands of Sao Tome and Principe, West Africa. Annals Trop Med Parasitol 97 :751–756.
-
48
Gillies M, 1955. The recognition of age-groups within populations of Anopheles gambiae by the pre-gravid rate and the sporozoite rate. Ann Trop Med Parasitol 48 :58–74.
-
49
Briegel H, Horler E, 1993. Multiple blood meals as a reproductive strategy in Anopheles (Diptera: Culicidae). J Med Ent 30 :975–985.
-
50
Hocking KS, MacInnes DG, 1948. Notes on the bionomics of Anopheles gambiae and A. funestus in East Africa. Bull Entomol Res 39 :453–465.
-
51
Lyimo EO, Takken W, 1993. Effects of adult body size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania. Med Vet Ent 7 :328–332.
THE PRESENCE OF PLASMODIUM FALCIPARUM GAMETOCYTES IN HUMAN BLOOD INCREASES THE GRAVIDITY OF ANOPHELES GAMBIAE MOSQUITOES
HEATHER M. FERGUSON
HEATHER M. FERGUSON
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK; Mbita Point Research & Training Centre, International Centre for Insect Physiology and Ecology, Mbita, Kenya; Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida
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LOUIS C. GOUAGNA
LOUIS C. GOUAGNA
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK; Mbita Point Research & Training Centre, International Centre for Insect Physiology and Ecology, Mbita, Kenya; Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida
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PETER OBARE
PETER OBARE
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK; Mbita Point Research & Training Centre, International Centre for Insect Physiology and Ecology, Mbita, Kenya; Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida
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ANDREW F. READ
ANDREW F. READ
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK; Mbita Point Research & Training Centre, International Centre for Insect Physiology and Ecology, Mbita, Kenya; Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida
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HAMZA BABIKER
HAMZA BABIKER
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK; Mbita Point Research & Training Centre, International Centre for Insect Physiology and Ecology, Mbita, Kenya; Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida
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JOHN GITHURE
JOHN GITHURE
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK; Mbita Point Research & Training Centre, International Centre for Insect Physiology and Ecology, Mbita, Kenya; Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida
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JOHN C. BEIER
JOHN C. BEIER
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK; Mbita Point Research & Training Centre, International Centre for Insect Physiology and Ecology, Mbita, Kenya; Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida
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We conducted a field study in an area of endemic malaria transmission in western Kenya to determine whether mosquitoes that feed on gametocyte-infected blood but do not become infected have reduced or enhanced fecundity in comparison to mosquitoes fed on uninfected blood. Fifteen paired membrane-feeding experiments were conducted in which two strains of Anopheles gambiae mosquitoes were simultaneously fed on either Plasmodium falciparum–infected blood from children or uninfected control blood from adults. The presence of noninfecting gametocytes in blood increased the probability that An. gambiae would produce eggs after one blood meal by sixfold (odds ratio for control relative to infected blood group 0.16; 95% CI 0.10–0.23). This result could not be explained by variation in blood meal size or hemoglobin content between hosts. When children cleared their infections, the difference in gravidity between mosquitoes fed on their blood and uninfected adults disappeared, suggesting this phenomenon is due to the presence of Plasmodium gametocytes in blood and not to host-specific factors such as age. This result was observed in two mosquito strains that differ in their innate fecundity, suggesting it may apply generally. To our knowledge, this is the first time that Plasmodium has been implicated as enhancing vector gravidity.
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RefWorks
Reference Manager
BibTeX
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-
1
Hacker CS, 1971. The differential effect of Plasmodium gallinaceum on the fecundity of several strains of Aedes aegypti.J Invert Pathol 18 :373–377.
-
2
Hacker CS, Kilama WL, 1974. The relationship between Plasmodium gallinaceum density and the fecundity of Aedes aegypti.J Invert Pathol 23 :101–105.
-
3
Freier JE, Friedman S, 1976. Effect of host infection with Plasmodium gallinaceum on the reproductive capacity of Aedes aegypti.J Invert Pathol 28 :161–166.
-
4
Hogg JC, Hurd H, 1995. Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Med Vet Ent 9 :176–180.
-
5
Hogg JC, Hurd H, 1995. Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology 111 :555–562.
-
6
Hogg JC, Hurd H, 1997. The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae s.l. in north east Tanzania. Parasitology 114 :325–331.
-
7
Anderson RA, Knols BG, Koella JC, 2000. Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. Parasitology 129 :329–333.
-
8
Ferguson HM, Read AF, 2002. Why is the effect of malaria parasites on mosquito survival still unresolved? Trends Parasitol 18 :256–261.
-
9
Ferguson HM, Read AF, 2002. Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proc R Soc Lond B Biol Sci 269 :1217–1224.
-
10
Carwardine SL, Hurd H, 1997. Effects of Plasmodium yoelii nigeriensis infection on Anopheles stephensi egg development and resorption. Med Vet Ent 11 :265–269.
-
11
Hopwood J, Ahmed A, Polwart A, Williams G, Hurd H, 2001. Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. J Exp Biol 204 :2773–2780.
-
12
Ahmed AM, Maingon RD, Taylor PJ, Hurd H, 1999. The effects of infection with Plasmodium yoelii nigeriensis on the reproductive fitness of the mosquito Anopheles gambiae.Invert Reprod Dev 36 :217–222.
-
13
Ferguson H, Rivero A, Read A, 2003. The influence of malaria parasite genetic diversity and anaemia on mosquito feeding and fecundity. Parasitology 127 :9–19.
-
14
Beier JC, 1998. Malaria parasite development in mosquitoes. Ann Rev Ent 43 :519–543.
-
15
Shililu JI, Maier WA, Seitz HM, Orago AS, 1998. Seasonal density, sporozoite rates and entomological inoculation rates of Anopheles gambiae and Anopheles funestus in a high-altitude sugarcane growing zone in Western Kenya. Trop Med Intl Health 3 :706–710.
-
16
Molineux L, Gramiccia G, 1980. The Garki Project: Research on the Epidemiology and Control of Malaria in the Sudan Savanna of West Africa. Geneva: World Health Organization.
-
17
Smith T, Charlwood J, Kihonda J, Mwankusye S, Billingsley P, Meuwissen J, Lyimo E, Takken W, Teuscher T, Tanner M, 1993. Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Tropica 54 :55–72.
-
18
Gouagna L, Ferguson HM, Okech BA, Killeen GF, Kabiru EW, Beier JC, Githure JI, Yan G, 2004. Plasmodium falciparum malaria disease manifestations in humans and transmission to Anopheles gambiae: a field study in Western Kenya. Parasitology 128 :235–243.
-
19
Minakawa N, Githure JI, Beier JC, Yan G, 2001. Anopheline mosquito survival strategies during the dry period in western Kenya. J Med Ent 38 :388–392.
-
20
Minakawa N, Mutero CM, Githure JI, Beier JC, Yan G, 1999. Spatial distribution and habitat characterization of anopheline mosquito larvae in western Kenya. Am J Trop Med Hyg 61 :1010–1016.
-
21
Briegel H, 1980. Determination of uric acid and hematin in a single sample of excreta from blood-fed insects. Experientia 36 :1428.
-
22
Snow R, Craig M, Deichmann U, Marsh K, 1999. Estimating mortality, morbidity and disability due to malaria among Africa’s non-pregnant populations. Bull WHO 77 :624–640.
-
23
Almeida AP, Billingsley PF, 1999. Induced immunity against the mosquito Anopheles stephensi: reactivity characteristics of immune sera. Med Vet Ent 13 :53–64.
-
24
Zacharski LR, Ornstein DL, Woloshin S, Schwartz LM, 2000. Association of age, sex, and race with body iron stores in adults: analysis of NHANES III data. Am Heart J 140 :98–104.
-
25
Langman LJ, Cole DE, 1999. Homocysteine. Crit Rev Clin Lab Sci 36 :365–406.
-
26
Proenza A, Crespi C, Roca P, Palou A, 2001. Gender related differences in the effect of aging on blood amino acid compartmentation. J Nutrl Biol 12 :431–440.
-
27
Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE, 1995. Pyrimethamine and proguanil resistance conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg 52 :565–568.
-
28
Abdel-Wahab A, Abdel-Muhsin A, Ali E, Suleiman S, Ahmed A, Walliker D, Babiker HA, 2002. Dynamics of gametocytes among Plasmodium falciparum clones in natural infections in an area of highly seasonal transmission. J Infect Dis 185 :1838–1842.
-
29
SAS II, 1997. SAS/STAT Software: Changes and Enhancements Through Release 6.12. Cary, NC: SAS Institute Inc.
-
30
Takken W, Klowden MJ, Chambers GM, 1998. Effect of body size on host seeking and blood meal utilization in Anopheles gambiae sensu stricto (Diptera: Culicidae): the disadvantage of being small. J Med Ent 35 :639–645.
-
32
Bonnet S, Gouagna L, Paul R, Safeukui I, Meunier J, Boudin C, 2003. Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans R Soc Trop Med Hyg 97 :53–59.
-
33
Muirhead-Thomson R, 1954. Factors determining the true reservoir of infection of Plasmodium falciparum and Wucheria bancrofti in a West African village. Trans R Soc Trop Med Hyg 48 :208–225.
-
34
Muirhead-Thomson R, 1957. The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae): random xenodiagnostic survey. Am J Trop Med Hyg 6 :971–979.
-
35
Mulder B, Tchuinkam T, Dechering K, Verhave J, Carnevale P, Meuwissen J, Robert V, 1994. Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg 88 :121–125.
-
36
Enwonwu C, Afolabi B, Salako L, Idigbe E, Bashirelani N, 2000. Increased plasma levels of histidine and hisamine in falciparum malaria: relevance to severity of infection. J Neur Trans 107 :1273–1287.
-
37
Dimond JB, Lea AO, Hahnert WF, DeLong DM, 1956. The amino acids required for egg production in Aedes aegypti.Can Ent 88 :57–62.
-
38
Uchida K, Moribayashi A, Matsuoka H, Oda T, 2003. Effects of mating on oogenesis induced by amino acid infusion, amino acid feeding, or blood feeding in the mosquito Anopheles stephensi (Diptera: Culicidae). J M Ent 40 :441–446.
-
39
Uchida K, 1993. Balanced amino acid composition essential for infusion-induced egg development in the mosquito (Culex pipiens pallens). J Insect Physiol 39 :615–621.
-
40
Uchida K, Oda T, Matsuoka H, Moribayashi A, Ohmori D, Eshita Y, Fukunaga A, 2001. Induction of Oogenesis in mosquitoes (Diptera: Culicidae) by infusion of the hemocoe with amino acids. J Med Ent 38 :572–575.
-
41
Hurd H, Hogg JC, Renshaw M, 1995. Interactions between bloodfeeding, fecundity and infection in mosquitoes. Parasitol Today 11 :411–416.
-
42
Ferguson H, Mackinnon M, Chan B, Read A, 2003. Mosquito mortality and the evolution of malaria virulence. Evolution 57 :2792–2804.
-
43
Agnew P, Koella J, Michalakis Y, 2000. Host life history responses to parasitism. Microbes Infect 2 :891–896.
-
44
Stearns SC, 1992. The Evolution of Life Histories. Oxford: Oxford University Press.
-
45
Hurd H, 2003. Manipulation of medically important insect vectors by their parasites. Ann Rev Ent 48 :141–161.
-
46
Charlwood JD, Vij R, Billingsley PF, 2000. Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of east Africa. Am J Trop Med Hyg 62 :726–732.
-
47
Charlwood JD, Pinto J, Sousa CA, Ferreira C, Gil V, Do Rosario VE, 2003. Mating does not affect the biting behaviour of Anopheles gambiae from the islands of Sao Tome and Principe, West Africa. Annals Trop Med Parasitol 97 :751–756.
-
48
Gillies M, 1955. The recognition of age-groups within populations of Anopheles gambiae by the pre-gravid rate and the sporozoite rate. Ann Trop Med Parasitol 48 :58–74.
-
49
Briegel H, Horler E, 1993. Multiple blood meals as a reproductive strategy in Anopheles (Diptera: Culicidae). J Med Ent 30 :975–985.
-
50
Hocking KS, MacInnes DG, 1948. Notes on the bionomics of Anopheles gambiae and A. funestus in East Africa. Bull Entomol Res 39 :453–465.
-
51
Lyimo EO, Takken W, 1993. Effects of adult body size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania. Med Vet Ent 7 :328–332.