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Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Research

The impact of low erythrocyte density in human blood on the fitness and energetic reserves of the African malaria vector Anopheles gambiae

Authors: S Noushin Emami, Lisa C Ranford-Cartwright, Heather M Ferguson

Published in: Malaria Journal | Issue 1/2013

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Abstract

Background

Anaemia is a common health problem in the developing world. This condition is characterized by a reduction in erythrocyte density, primarily from malnutrition and/or infectious diseases such as malaria. As red blood cells are the primary source of protein for haematophagous mosquitoes, any reduction could impede the ability of mosquito vectors to transmit malaria by influencing their fitness or that of the parasites they transmit. The aim of this study was to determine the impact of differences in the density of red blood cells in human blood on malaria vector (Anopheles gambiae sensu stricto) fitness. The hypotheses tested are that mosquito vector energetic reserves and fitness are negatively influenced by reductions in the red cell density of host human blood meals commensurate with those expected from severe anaemia.

Methods

Mosquitoes (An. gambiae s.s.) were offered blood meals of different packed cell volume (PCV) of human blood consistent with those arising from severe anaemia (15%) and normal PCV (50%). Associations between mosquito energetic reserves (lipid, glucose and glycogen) and fitness measures (reproduction and survival) and blood meal PCV were investigated.

Results

The amount of protein that malaria vectors acquired from blood feeding (indexed by haematin excretion) was significantly reduced at low blood PCV. However, mosquitoes feeding on blood of low PCV had the same oviposition rates as those feeding on blood of normal PCV, and showed an increase in egg production of around 15%. The long-term survival of An. gambiae s.s was reduced after feeding on low PCV blood, but PCV had no significant impact on the proportion of mosquitoes surviving through the minimal period required to develop and transmit malaria parasites (estimated as 14 days post-blood feeding). The impact of blood PCV on the energetic reserves of mosquitoes was relatively minor.

Conclusions

These results suggest that feeding on human hosts whose PCV has been depleted due to severe anaemia does not significantly reduce the fitness or transmission potential of malaria vectors, and indicates that mosquitoes may be able exploit resources for reproduction more efficiently from blood of low rather than normal PCV.
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Literature
1.
go back to reference Bukar M, Audu BM, Yahaya UR, Melah GS: Anaemia in pregnancy at booking in Gombe, North-eastern Nigeria. J Obstet Gynaecol. 2008, 28: 775-778. 10.1080/01443610802463835.CrossRefPubMed Bukar M, Audu BM, Yahaya UR, Melah GS: Anaemia in pregnancy at booking in Gombe, North-eastern Nigeria. J Obstet Gynaecol. 2008, 28: 775-778. 10.1080/01443610802463835.CrossRefPubMed
2.
go back to reference Taylor PJ, Hurd H: The influence of host haematocrit on the blood feeding success of Anopheles stephensi: implications for enhanced malaria transmission. Parasitology. 2001, 122: 491-496.CrossRefPubMed Taylor PJ, Hurd H: The influence of host haematocrit on the blood feeding success of Anopheles stephensi: implications for enhanced malaria transmission. Parasitology. 2001, 122: 491-496.CrossRefPubMed
3.
go back to reference Nkuo-Akenji TK, Chi PC, Cho JF, Ndamukong KKJ, Sumbele I: Malaria and helminth co-infection in children living in a malaria endemic setting of Mount Cameroon and predictors of anemia. J Parasitol. 2006, 92: 1191-1195. 10.1645/GE-895R.1.CrossRefPubMed Nkuo-Akenji TK, Chi PC, Cho JF, Ndamukong KKJ, Sumbele I: Malaria and helminth co-infection in children living in a malaria endemic setting of Mount Cameroon and predictors of anemia. J Parasitol. 2006, 92: 1191-1195. 10.1645/GE-895R.1.CrossRefPubMed
4.
go back to reference Van den Broek NR, Letsky EA, White SA, Shenkin A: Iron status in pregnant women: which measurements are valid?. Br J Haematol. 1998, 103: 817-824. 10.1046/j.1365-2141.1998.01035.x.CrossRefPubMed Van den Broek NR, Letsky EA, White SA, Shenkin A: Iron status in pregnant women: which measurements are valid?. Br J Haematol. 1998, 103: 817-824. 10.1046/j.1365-2141.1998.01035.x.CrossRefPubMed
5.
go back to reference Abdelrahim II, Adam GK, Mohmmed AA, Salih MM, Ali NI, Elbashier MI, Adam I: Anaemia, folate and vitamin B-12 deficiency among pregnant women in an area of unstable malaria transmission in eastern Sudan. Trans R Soc Trop Med Hyg. 2009, 103: 493-496. 10.1016/j.trstmh.2008.10.007.CrossRefPubMed Abdelrahim II, Adam GK, Mohmmed AA, Salih MM, Ali NI, Elbashier MI, Adam I: Anaemia, folate and vitamin B-12 deficiency among pregnant women in an area of unstable malaria transmission in eastern Sudan. Trans R Soc Trop Med Hyg. 2009, 103: 493-496. 10.1016/j.trstmh.2008.10.007.CrossRefPubMed
6.
go back to reference Fairbanks VF, Tefferi A: Normal ranges for packed cell volume and hemoglobin concentration in adults: relevance to ‘apparent polycythemia’. Eur Journal Haematol. 2000, 65: 285-296. 10.1034/j.1600-0609.2000.065005285.x.CrossRef Fairbanks VF, Tefferi A: Normal ranges for packed cell volume and hemoglobin concentration in adults: relevance to ‘apparent polycythemia’. Eur Journal Haematol. 2000, 65: 285-296. 10.1034/j.1600-0609.2000.065005285.x.CrossRef
7.
go back to reference Mukiibi JM, Mtimavalye LAR, Broadhead R, Mzula E, Dzinyemba WE, Merrick R, Khoromana CO, Chingani GW: Some hematological parameters in Malawian neonates. East Afr Med J. 1995, 72: 10-14.PubMed Mukiibi JM, Mtimavalye LAR, Broadhead R, Mzula E, Dzinyemba WE, Merrick R, Khoromana CO, Chingani GW: Some hematological parameters in Malawian neonates. East Afr Med J. 1995, 72: 10-14.PubMed
8.
go back to reference Hurd H, Hogg JC, Renshaw M: Interactions between blood feeding, fecundity and infection in mosquitoes. Parasitol Today. 1995, 11: 411-416. 10.1016/0169-4758(95)80021-2.CrossRef Hurd H, Hogg JC, Renshaw M: Interactions between blood feeding, fecundity and infection in mosquitoes. Parasitol Today. 1995, 11: 411-416. 10.1016/0169-4758(95)80021-2.CrossRef
9.
go back to reference Hurd H: Host fecundity reduction: a strategy for damage limitation?. Trends Parasitol. 2001, 17: 363-368. 10.1016/S1471-4922(01)01927-4.CrossRefPubMed Hurd H: Host fecundity reduction: a strategy for damage limitation?. Trends Parasitol. 2001, 17: 363-368. 10.1016/S1471-4922(01)01927-4.CrossRefPubMed
10.
go back to reference Maier WA, Beckerfeldman H, Seitz HM: Pathology of malaria-infected mosquitoes. Parasitol Today. 1987, 3: 216-218. 10.1016/0169-4758(87)90063-9.CrossRefPubMed Maier WA, Beckerfeldman H, Seitz HM: Pathology of malaria-infected mosquitoes. Parasitol Today. 1987, 3: 216-218. 10.1016/0169-4758(87)90063-9.CrossRefPubMed
11.
go back to reference Clements AN: The biology of mosquitoes. 2000, Cambridge: CABI Clements AN: The biology of mosquitoes. 2000, Cambridge: CABI
12.
go back to reference Aboagye-Antwi F, Guindo A, Traore AS, Hurd H, Coulibaly M, Traore S, Tripet F: Hydric stress-dependent effects of Plasmodium falciparum infection on the survival of wild-caught Anopheles gambiae female mosquitoes. Malar J. 2010, 9: 243-10.1186/1475-2875-9-243.PubMedCentralCrossRefPubMed Aboagye-Antwi F, Guindo A, Traore AS, Hurd H, Coulibaly M, Traore S, Tripet F: Hydric stress-dependent effects of Plasmodium falciparum infection on the survival of wild-caught Anopheles gambiae female mosquitoes. Malar J. 2010, 9: 243-10.1186/1475-2875-9-243.PubMedCentralCrossRefPubMed
13.
go back to reference Baton LA, Ranford-Cartwright LC: Spreading the seeds of million-murdering death: metamorphoses of malaria in the mosquito. Trends Parasitol. 2005, 21: 573-580. 10.1016/j.pt.2005.09.012.CrossRefPubMed Baton LA, Ranford-Cartwright LC: Spreading the seeds of million-murdering death: metamorphoses of malaria in the mosquito. Trends Parasitol. 2005, 21: 573-580. 10.1016/j.pt.2005.09.012.CrossRefPubMed
14.
go back to reference Beier JC: Malaria parasite development in mosquitoes. Annu Rev Entomol. 1998, 43: 519-543. 10.1146/annurev.ento.43.1.519.CrossRefPubMed Beier JC: Malaria parasite development in mosquitoes. Annu Rev Entomol. 1998, 43: 519-543. 10.1146/annurev.ento.43.1.519.CrossRefPubMed
15.
go back to reference Daniel TL, Kingsolver JG: Feeding strategy and the mechanics of blood sucking in insects. J Theor Biol. 1983, 105: 661-677. 10.1016/0022-5193(83)90226-6.CrossRefPubMed Daniel TL, Kingsolver JG: Feeding strategy and the mechanics of blood sucking in insects. J Theor Biol. 1983, 105: 661-677. 10.1016/0022-5193(83)90226-6.CrossRefPubMed
16.
go back to reference Shieh JN, Rossignol PA: Opposite influences of host anemia on blood feeding rate and fecundity of mosquitoes. Parasitology. 1992, 105: 159-163. 10.1017/S0031182000074060.CrossRefPubMed Shieh JN, Rossignol PA: Opposite influences of host anemia on blood feeding rate and fecundity of mosquitoes. Parasitology. 1992, 105: 159-163. 10.1017/S0031182000074060.CrossRefPubMed
17.
go back to reference Ferguson HM, Rivero A, Read AF: The influence of malaria parasite genetic diversity and anaemia on mosquito feeding and fecundity. Parasitology. 2003, 127: 9-19. 10.1017/S0031182003003287.CrossRefPubMed Ferguson HM, Rivero A, Read AF: The influence of malaria parasite genetic diversity and anaemia on mosquito feeding and fecundity. Parasitology. 2003, 127: 9-19. 10.1017/S0031182003003287.CrossRefPubMed
18.
go back to reference Rivero A, Ferguson HM: The energetic budget of Anopheles stephensi infected with Plasmodium chabaudi: is energy depletion a mechanism for virulence?. Proc R Soc Lond B Biol Sci. 2003, 270: 1365-1371. 10.1098/rspb.2003.2389.CrossRef Rivero A, Ferguson HM: The energetic budget of Anopheles stephensi infected with Plasmodium chabaudi: is energy depletion a mechanism for virulence?. Proc R Soc Lond B Biol Sci. 2003, 270: 1365-1371. 10.1098/rspb.2003.2389.CrossRef
19.
go back to reference Foster WA: Mosquito sugar feeding and reproductive energetics. Annu Rev Entomol. 1995, 40: 443-474. 10.1146/annurev.en.40.010195.002303.CrossRefPubMed Foster WA: Mosquito sugar feeding and reproductive energetics. Annu Rev Entomol. 1995, 40: 443-474. 10.1146/annurev.en.40.010195.002303.CrossRefPubMed
20.
go back to reference Schiefer B, Ward R, Eldridge B: Plasmodium cynomolgi: effects of malaria infection on laboratory flight performance of Anopheles stephensi mosquitoes. Exp Parasitol. 1977, 41: 397-10.1016/0014-4894(77)90111-4.CrossRefPubMed Schiefer B, Ward R, Eldridge B: Plasmodium cynomolgi: effects of malaria infection on laboratory flight performance of Anopheles stephensi mosquitoes. Exp Parasitol. 1977, 41: 397-10.1016/0014-4894(77)90111-4.CrossRefPubMed
21.
go back to reference Oliveira JH, Goncalves RL, Oliveira GA, Oliveira PL, Oliveira MF, Barillas-Mury C: Energy metabolism affects susceptibility of Anopheles gambiae mosquitoes to Plasmodium infection. Insect Biochem Molec Biol. 2011, 41: 349-355. 10.1016/j.ibmb.2011.02.001.CrossRef Oliveira JH, Goncalves RL, Oliveira GA, Oliveira PL, Oliveira MF, Barillas-Mury C: Energy metabolism affects susceptibility of Anopheles gambiae mosquitoes to Plasmodium infection. Insect Biochem Molec Biol. 2011, 41: 349-355. 10.1016/j.ibmb.2011.02.001.CrossRef
22.
go back to reference Proven D, Singer CRJ, Baglin T, Dokal I: Oxford handbook of clinical haematology. 2009, Oxford: Oxford University PressCrossRef Proven D, Singer CRJ, Baglin T, Dokal I: Oxford handbook of clinical haematology. 2009, Oxford: Oxford University PressCrossRef
23.
go back to reference Carter R, Ranford-Cartwright L, Alano P: The culture and preparation of gametocytes of Plasmodium falciparum for immunochemical, molecular, and mosquito infectivity studies. Methods Mol Biol. 1993, 21: 67-88.PubMed Carter R, Ranford-Cartwright L, Alano P: The culture and preparation of gametocytes of Plasmodium falciparum for immunochemical, molecular, and mosquito infectivity studies. Methods Mol Biol. 1993, 21: 67-88.PubMed
24.
go back to reference Briegel H: Determination of uric-acid and hematin in a single sample of excreta from blood-fed insects. Experientia. 1980, 36: 1428-10.1007/BF01960142.CrossRef Briegel H: Determination of uric-acid and hematin in a single sample of excreta from blood-fed insects. Experientia. 1980, 36: 1428-10.1007/BF01960142.CrossRef
25.
go back to reference Briegel H: Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J Insect Physiol. 1990, 36: 165-172. 10.1016/0022-1910(90)90118-Y.CrossRef Briegel H: Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J Insect Physiol. 1990, 36: 165-172. 10.1016/0022-1910(90)90118-Y.CrossRef
26.
go back to reference Nasci RS: The size of emerging and host-seeking Aedes aegypti and the relation of size to blood-feeding success in the field. J Am Mosq Control Assoc. 1986, 2: 61-62.PubMed Nasci RS: The size of emerging and host-seeking Aedes aegypti and the relation of size to blood-feeding success in the field. J Am Mosq Control Assoc. 1986, 2: 61-62.PubMed
27.
go back to reference Van Handel E, Day JF: Assay of lipids glycogen and sugars in individual mosquitoes correlations with wing length in field-collected Aedes vexans. J Am Mosq Control Assoc. 1988, 4: 549-550.PubMed Van Handel E, Day JF: Assay of lipids glycogen and sugars in individual mosquitoes correlations with wing length in field-collected Aedes vexans. J Am Mosq Control Assoc. 1988, 4: 549-550.PubMed
28.
go back to reference Van Handel E: Rapid determination of total lipids in mosquitoes. J Am Mosq Control Assoc. 1985, 1: 302-304.PubMed Van Handel E: Rapid determination of total lipids in mosquitoes. J Am Mosq Control Assoc. 1985, 1: 302-304.PubMed
29.
go back to reference Van Handel E: Rapid determination of glycogen and sugars in mosquitoes. J Am Mosq Control Assoc. 1985, 1: 299-301.PubMed Van Handel E: Rapid determination of glycogen and sugars in mosquitoes. J Am Mosq Control Assoc. 1985, 1: 299-301.PubMed
30.
go back to reference Aboagye-Antwi F, Tripet F: Effects of larval growth condition and water availability on desiccation resistance and its physiological basis in adult Anopheles gambiae sensu stricto. Malar J. 2010, 9: 225-10.1186/1475-2875-9-225.PubMedCentralCrossRefPubMed Aboagye-Antwi F, Tripet F: Effects of larval growth condition and water availability on desiccation resistance and its physiological basis in adult Anopheles gambiae sensu stricto. Malar J. 2010, 9: 225-10.1186/1475-2875-9-225.PubMedCentralCrossRefPubMed
31.
32.
go back to reference Hougaard P: Frailty models for survival data. Lifetime Data Analysis. 1995, 1: 255-273. 10.1007/BF00985760.CrossRefPubMed Hougaard P: Frailty models for survival data. Lifetime Data Analysis. 1995, 1: 255-273. 10.1007/BF00985760.CrossRefPubMed
33.
go back to reference Anderson RA, Roitberg BD: Modelling trade-offs between mortality and fitness associated with persistent blood feeding by mosquitoes. Ecol Lett. 1999, 2: 98-105. 10.1046/j.1461-0248.1999.22055.x.CrossRef Anderson RA, Roitberg BD: Modelling trade-offs between mortality and fitness associated with persistent blood feeding by mosquitoes. Ecol Lett. 1999, 2: 98-105. 10.1046/j.1461-0248.1999.22055.x.CrossRef
34.
go back to reference Carey JR, Harshman LG, Liedo P, Muller HG, Wang JL, Zhang Z: Longevity-fertility trade-offs in the tephritid fruit fly, Anastrepha ludens, across dietary-restriction gradients. Aging Cell. 2008, 7: 470-477. 10.1111/j.1474-9726.2008.00389.x.PubMedCentralCrossRefPubMed Carey JR, Harshman LG, Liedo P, Muller HG, Wang JL, Zhang Z: Longevity-fertility trade-offs in the tephritid fruit fly, Anastrepha ludens, across dietary-restriction gradients. Aging Cell. 2008, 7: 470-477. 10.1111/j.1474-9726.2008.00389.x.PubMedCentralCrossRefPubMed
35.
go back to reference Dao A, Kassogue Y, Adamou A, Diallo M, Yaro AS, Traore SF: Reproduction-longevity trade-off in Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 2010, 47: 769-777. 10.1603/ME10052.PubMedCentralCrossRefPubMed Dao A, Kassogue Y, Adamou A, Diallo M, Yaro AS, Traore SF: Reproduction-longevity trade-off in Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 2010, 47: 769-777. 10.1603/ME10052.PubMedCentralCrossRefPubMed
36.
go back to reference Stone C, Hamilton I, Foster W: A survival and reproduction trade-off is resolved in accordance with resource availability by virgin female mosquitoes. Anim Behav. 2011, 81: 765-774. 10.1016/j.anbehav.2011.01.008.PubMedCentralCrossRefPubMed Stone C, Hamilton I, Foster W: A survival and reproduction trade-off is resolved in accordance with resource availability by virgin female mosquitoes. Anim Behav. 2011, 81: 765-774. 10.1016/j.anbehav.2011.01.008.PubMedCentralCrossRefPubMed
37.
go back to reference Flatt T: Survival costs of reproduction in Drosophila. Exp Gerontol. 2011, 46: 369-375. 10.1016/j.exger.2010.10.008.CrossRefPubMed Flatt T: Survival costs of reproduction in Drosophila. Exp Gerontol. 2011, 46: 369-375. 10.1016/j.exger.2010.10.008.CrossRefPubMed
38.
go back to reference De Loof A: Longevity and aging in insects: Is reproduction costly; cheap; beneficial or irrelevant? A critical evaluation of the “trade-off” concept. J Insect Physiol. 2011, 57: 1-11. 10.1016/j.jinsphys.2010.08.018.CrossRefPubMed De Loof A: Longevity and aging in insects: Is reproduction costly; cheap; beneficial or irrelevant? A critical evaluation of the “trade-off” concept. J Insect Physiol. 2011, 57: 1-11. 10.1016/j.jinsphys.2010.08.018.CrossRefPubMed
40.
go back to reference Lyimo EO, Takken W: Effects of adult body-size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania. Med Vet Entomol. 1993, 7: 328-332. 10.1111/j.1365-2915.1993.tb00700.x.CrossRefPubMed Lyimo EO, Takken W: Effects of adult body-size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania. Med Vet Entomol. 1993, 7: 328-332. 10.1111/j.1365-2915.1993.tb00700.x.CrossRefPubMed
41.
go back to reference Briegel H: Fecundity, metabolism, and body size in Anopheles (Diptera, Culicidae), vectors of malaria. J Med Entomol. 1990, 27: 839-850.CrossRefPubMed Briegel H: Fecundity, metabolism, and body size in Anopheles (Diptera, Culicidae), vectors of malaria. J Med Entomol. 1990, 27: 839-850.CrossRefPubMed
42.
go back to reference Hogg JC, Hurd H: Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Med Vet Entomol. 1995, 9: 176-180. 10.1111/j.1365-2915.1995.tb00175.x.CrossRefPubMed Hogg JC, Hurd H: Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Med Vet Entomol. 1995, 9: 176-180. 10.1111/j.1365-2915.1995.tb00175.x.CrossRefPubMed
43.
go back to reference Briegel H, Rezzonico L: Blood meal concentration and fecundity in the malaria mosquito Anopheles. Experientia. 1985, 41: 1224- Briegel H, Rezzonico L: Blood meal concentration and fecundity in the malaria mosquito Anopheles. Experientia. 1985, 41: 1224-
44.
go back to reference Stearns SC: The evolution of life histories. 1992, Oxford: Oxford University Press Stearns SC: The evolution of life histories. 1992, Oxford: Oxford University Press
45.
go back to reference Carlson KA, Harshman LG: Extended longevity lines of Drosophila melanogaster: Abundance of yolk protein gene mRNA in fat body and ovary. Exp Gerontol. 1999, 34: 173-184. 10.1016/S0531-5565(98)00071-0.CrossRefPubMed Carlson KA, Harshman LG: Extended longevity lines of Drosophila melanogaster: Abundance of yolk protein gene mRNA in fat body and ovary. Exp Gerontol. 1999, 34: 173-184. 10.1016/S0531-5565(98)00071-0.CrossRefPubMed
46.
go back to reference Price PW: Insect Ecology. 1984, New York: Wiley Price PW: Insect Ecology. 1984, New York: Wiley
47.
go back to reference Nayar JK, Sauerman DM: Effects of nutrition on survival and fecundity in Florida mosquitoes. 3. Utilization of blood and sugar for fecundity. J Med Entomol. 1975, 12: 220-225.CrossRefPubMed Nayar JK, Sauerman DM: Effects of nutrition on survival and fecundity in Florida mosquitoes. 3. Utilization of blood and sugar for fecundity. J Med Entomol. 1975, 12: 220-225.CrossRefPubMed
48.
go back to reference Okech BA, Gouagna LC, Killeen GF, Knols BGJ, Kabiru EW, Beier JC, Yan G, Githure JI: Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in western Kenya. J Med Entomol. 2003, 40: 657-663. 10.1603/0022-2585-40.5.657.CrossRefPubMed Okech BA, Gouagna LC, Killeen GF, Knols BGJ, Kabiru EW, Beier JC, Yan G, Githure JI: Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in western Kenya. J Med Entomol. 2003, 40: 657-663. 10.1603/0022-2585-40.5.657.CrossRefPubMed
49.
go back to reference Impoinvil DE, Kongere JO, Foster WA, Njiru BN, Killeen GF, Githure JI, Beier JC, Hassanali A, Knols BGJ: Feeding and survival of the malaria vector Anopheles gambiae on plants growing in Kenya. Med Vet Entomol. 2004, 18: 108-115. 10.1111/j.0269-283X.2004.00484.x.CrossRefPubMed Impoinvil DE, Kongere JO, Foster WA, Njiru BN, Killeen GF, Githure JI, Beier JC, Hassanali A, Knols BGJ: Feeding and survival of the malaria vector Anopheles gambiae on plants growing in Kenya. Med Vet Entomol. 2004, 18: 108-115. 10.1111/j.0269-283X.2004.00484.x.CrossRefPubMed
50.
go back to reference Manda H, Gouagna LC, Foster WA, Jackson RR, Beier JC, Githure JI, Hassanali A: Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malar J. 2007, 6: 113-10.1186/1475-2875-6-113.PubMedCentralCrossRefPubMed Manda H, Gouagna LC, Foster WA, Jackson RR, Beier JC, Githure JI, Hassanali A: Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malar J. 2007, 6: 113-10.1186/1475-2875-6-113.PubMedCentralCrossRefPubMed
51.
go back to reference Boreham PFL, Lenahan JK, Boulzaguet R, Storey J, Ashkar TS, Nambiar R, Matsushima T: Studies on multiple feeding by Anopheles gambiae s.l. in a Sudan savanna area of North Nigeria. Trans R Soc Trop Med Hyg. 1979, 73: 418-423. 10.1016/0035-9203(79)90167-6.CrossRefPubMed Boreham PFL, Lenahan JK, Boulzaguet R, Storey J, Ashkar TS, Nambiar R, Matsushima T: Studies on multiple feeding by Anopheles gambiae s.l. in a Sudan savanna area of North Nigeria. Trans R Soc Trop Med Hyg. 1979, 73: 418-423. 10.1016/0035-9203(79)90167-6.CrossRefPubMed
52.
go back to reference Garrett-Jones C: Prognosis for interruption of malaria transmission through assessment of mosquito’s vectorial capacity. Nature. 1964, 204: 1173-1175. 10.1038/2041173a0.CrossRefPubMed Garrett-Jones C: Prognosis for interruption of malaria transmission through assessment of mosquito’s vectorial capacity. Nature. 1964, 204: 1173-1175. 10.1038/2041173a0.CrossRefPubMed
Metadata
Title
The impact of low erythrocyte density in human blood on the fitness and energetic reserves of the African malaria vector Anopheles gambiae
Authors
S Noushin Emami
Lisa C Ranford-Cartwright
Heather M Ferguson
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-45

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