Skip to main content
Top
Published in: Malaria Journal 1/2012

Open Access 01-12-2012 | Research

Modeling the role of environmental variables on the population dynamics of the malaria vector Anopheles gambiae sensu stricto

Authors: Paul E Parham, Diane Pople, Céline Christiansen-Jucht, Steve Lindsay, Wes Hinsley, Edwin Michael

Published in: Malaria Journal | Issue 1/2012

Login to get access

Abstract

Background

The impact of weather and climate on malaria transmission has attracted considerable attention in recent years, yet uncertainties around future disease trends under climate change remain. Mathematical models provide powerful tools for addressing such questions and understanding the implications for interventions and eradication strategies, but these require realistic modeling of the vector population dynamics and its response to environmental variables.

Methods

Published and unpublished field and experimental data are used to develop new formulations for modeling the relationships between key aspects of vector ecology and environmental variables. These relationships are integrated within a validated deterministic model of Anopheles gambiae s.s. population dynamics to provide a valuable tool for understanding vector response to biotic and abiotic variables.

Results

A novel, parsimonious framework for assessing the effects of rainfall, cloudiness, wind speed, desiccation, temperature, relative humidity and density-dependence on vector abundance is developed, allowing ease of construction, analysis, and integration into malaria transmission models. Model validation shows good agreement with longitudinal vector abundance data from Tanzania, suggesting that recent malaria reductions in certain areas of Africa could be due to changing environmental conditions affecting vector populations.

Conclusions

Mathematical models provide a powerful, explanatory means of understanding the role of environmental variables on mosquito populations and hence for predicting future malaria transmission under global change. The framework developed provides a valuable advance in this respect, but also highlights key research gaps that need to be resolved if we are to better understand future malaria risk in vulnerable communities.
Appendix
Available only for authorised users
Literature
1.
go back to reference McMichael A, Woodruff R, Hales S: Climate change and human health: present and future risks. Lancet. 2006, 367: 859-10.1016/S0140-6736(06)68079-3.CrossRefPubMed McMichael A, Woodruff R, Hales S: Climate change and human health: present and future risks. Lancet. 2006, 367: 859-10.1016/S0140-6736(06)68079-3.CrossRefPubMed
2.
go back to reference WHO: The global burden of disease: 2004 update. 2008, World Health Organization, Geneva WHO: The global burden of disease: 2004 update. 2008, World Health Organization, Geneva
3.
go back to reference Hay SI, Cox J, Rogers DJ, Randolph SE, Stern DI, Shanks GD, Myers MF, Snow RW: Climate change and the resurgence of malaria in the East African highlands. Nature. 2002, 415: 905-909. 10.1038/415905a.PubMedCentralCrossRefPubMed Hay SI, Cox J, Rogers DJ, Randolph SE, Stern DI, Shanks GD, Myers MF, Snow RW: Climate change and the resurgence of malaria in the East African highlands. Nature. 2002, 415: 905-909. 10.1038/415905a.PubMedCentralCrossRefPubMed
4.
go back to reference Pascual M, Ahumada JA, Chaves LF, Rodo X, Bouma M: Malaria resurgence in the East African highlands: temperature trends revisited. Proc Natl Acad Sci USA. 2006, 103: 5829-5834. 10.1073/pnas.0508929103.PubMedCentralCrossRefPubMed Pascual M, Ahumada JA, Chaves LF, Rodo X, Bouma M: Malaria resurgence in the East African highlands: temperature trends revisited. Proc Natl Acad Sci USA. 2006, 103: 5829-5834. 10.1073/pnas.0508929103.PubMedCentralCrossRefPubMed
5.
go back to reference Craig MH, Snow RW, le Sueur D: A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol Today. 1999, 15: 105-111. 10.1016/S0169-4758(99)01396-4.CrossRefPubMed Craig MH, Snow RW, le Sueur D: A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol Today. 1999, 15: 105-111. 10.1016/S0169-4758(99)01396-4.CrossRefPubMed
6.
go back to reference Rogers DJ, Randolph SE: The global spread of malaria in a future, warmer world. Science. 2000, 289: 1763-1766.CrossRefPubMed Rogers DJ, Randolph SE: The global spread of malaria in a future, warmer world. Science. 2000, 289: 1763-1766.CrossRefPubMed
7.
go back to reference Ermert V, Fink A, Jones A, Morse A: Development of a new version of the Liverpool Malaria Model. II. Calibration and validation for West Africa. Malar J. 2011, 10: 62-10.1186/1475-2875-10-62.PubMedCentralCrossRefPubMed Ermert V, Fink A, Jones A, Morse A: Development of a new version of the Liverpool Malaria Model. II. Calibration and validation for West Africa. Malar J. 2011, 10: 62-10.1186/1475-2875-10-62.PubMedCentralCrossRefPubMed
9.
go back to reference Martens P: Health and climate change: modeling the impacts of global warming and ozone depletion. 1998, Earthscan, Oxford, UK, 176- Martens P: Health and climate change: modeling the impacts of global warming and ozone depletion. 1998, Earthscan, Oxford, UK, 176-
10.
go back to reference Depinay J-M, Mbogo C, Killeen G, Knols B, Beier J, Carlson J, Dushoff J, Billingsley P, Mwambi H, Githure J, Toure A, McKenzie F: A simulation model of African Anopheles ecology and population dynamics for the analysis of malaria transmission. Malar J. 2004, 3: 29-10.1186/1475-2875-3-29.PubMedCentralCrossRefPubMed Depinay J-M, Mbogo C, Killeen G, Knols B, Beier J, Carlson J, Dushoff J, Billingsley P, Mwambi H, Githure J, Toure A, McKenzie F: A simulation model of African Anopheles ecology and population dynamics for the analysis of malaria transmission. Malar J. 2004, 3: 29-10.1186/1475-2875-3-29.PubMedCentralCrossRefPubMed
11.
go back to reference Ermert V, Fink A, Jones A, Morse A: Development of a new version of the Liverpool Malaria Model. I. Refining the parameter settings and mathematical formulation of basic processes based on a literature review. Malar J. 2011, 10: 35-10.1186/1475-2875-10-35.PubMedCentralCrossRefPubMed Ermert V, Fink A, Jones A, Morse A: Development of a new version of the Liverpool Malaria Model. I. Refining the parameter settings and mathematical formulation of basic processes based on a literature review. Malar J. 2011, 10: 35-10.1186/1475-2875-10-35.PubMedCentralCrossRefPubMed
12.
go back to reference White MT, Griffin JT, Churcher TS, Ferguson NM, Basanez MG, Ghani AC: Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit Vectors. 2011, 4: 153-10.1186/1756-3305-4-153.PubMedCentralCrossRefPubMed White MT, Griffin JT, Churcher TS, Ferguson NM, Basanez MG, Ghani AC: Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit Vectors. 2011, 4: 153-10.1186/1756-3305-4-153.PubMedCentralCrossRefPubMed
13.
go back to reference Meyrowitsch DW, Pedersen EM, Alifrangis M, Scheike TH, Malecela MN, Magesa SM, Derua YA, Rwegoshora RT, Michael E, Simonsen PE: Is the current decline in malaria burden in sub-Saharan Africa due to a decrease in vector population?. Malar J. 2011, 10: 188-10.1186/1475-2875-10-188.PubMedCentralCrossRefPubMed Meyrowitsch DW, Pedersen EM, Alifrangis M, Scheike TH, Malecela MN, Magesa SM, Derua YA, Rwegoshora RT, Michael E, Simonsen PE: Is the current decline in malaria burden in sub-Saharan Africa due to a decrease in vector population?. Malar J. 2011, 10: 188-10.1186/1475-2875-10-188.PubMedCentralCrossRefPubMed
14.
go back to reference Crouse DT, Crowder LB, Caswell H: A stage-based population model for loggerhead sea turtles and implications for conservation. Ecology. 1987, 68: 1412-1423. 10.2307/1939225.CrossRef Crouse DT, Crowder LB, Caswell H: A stage-based population model for loggerhead sea turtles and implications for conservation. Ecology. 1987, 68: 1412-1423. 10.2307/1939225.CrossRef
15.
go back to reference Diuk-Wasser MA, Toure MB, Dolo G, Bagayoko M, Sogoba N, Traore SF, Manoukis N, Taylor CE: Vector abundance and malaria transmission in rice-growing villages in Mali. Am J Trop Med Hyg. 2005, 72: 725-731.PubMedCentralPubMed Diuk-Wasser MA, Toure MB, Dolo G, Bagayoko M, Sogoba N, Traore SF, Manoukis N, Taylor CE: Vector abundance and malaria transmission in rice-growing villages in Mali. Am J Trop Med Hyg. 2005, 72: 725-731.PubMedCentralPubMed
16.
go back to reference Koenraadt CJM, Githeko AK, Takken W: The effects of rainfall and evapotranspiration on the temporal dynamics of Anopheles gambiae s.s. and Anopheles arabiensis in a Kenyan village. Acta Trop. 2004, 90: 141-153. 10.1016/j.actatropica.2003.11.007.CrossRefPubMed Koenraadt CJM, Githeko AK, Takken W: The effects of rainfall and evapotranspiration on the temporal dynamics of Anopheles gambiae s.s. and Anopheles arabiensis in a Kenyan village. Acta Trop. 2004, 90: 141-153. 10.1016/j.actatropica.2003.11.007.CrossRefPubMed
17.
go back to reference Allen RG, Pereira LS, Raes D, Smith M: Crop evapotranspiration – Guidelines for computing crop water requirements. FAO Irrigation and drainage paper 56. Rome. 1998, FAO – Food and Agriculture Organization of the United Nations,   Allen RG, Pereira LS, Raes D, Smith M: Crop evapotranspiration – Guidelines for computing crop water requirements. FAO Irrigation and drainage paper 56. Rome. 1998, FAO – Food and Agriculture Organization of the United Nations,  
19.
go back to reference Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH, Gething PW, Kabaria CW, Okara RM, Van Boeckel T, Godfray HC, Harbach RE, Hay SI: The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2010, 3: 117-10.1186/1756-3305-3-117.PubMedCentralCrossRefPubMed Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH, Gething PW, Kabaria CW, Okara RM, Van Boeckel T, Godfray HC, Harbach RE, Hay SI: The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2010, 3: 117-10.1186/1756-3305-3-117.PubMedCentralCrossRefPubMed
20.
go back to reference Bi P, Tong S, Donald K, Parton K, Ni J: Climatic variables and transmission of malaria: a 12-year data analysis in Shuchen County. China. Public Health Reports. 2003, 118: 65-10.1016/S0033-3549(04)50218-2.CrossRefPubMed Bi P, Tong S, Donald K, Parton K, Ni J: Climatic variables and transmission of malaria: a 12-year data analysis in Shuchen County. China. Public Health Reports. 2003, 118: 65-10.1016/S0033-3549(04)50218-2.CrossRefPubMed
21.
go back to reference Gimnig JE, Ombok M, Kamau L, Hawley WA: Characteristics of larval anopheline (Diptera: Culicidae) habitats in Western Kenya. J Med Entomol. 2001, 38: 282-288. 10.1603/0022-2585-38.2.282.CrossRefPubMed Gimnig JE, Ombok M, Kamau L, Hawley WA: Characteristics of larval anopheline (Diptera: Culicidae) habitats in Western Kenya. J Med Entomol. 2001, 38: 282-288. 10.1603/0022-2585-38.2.282.CrossRefPubMed
22.
go back to reference McCrae AW: Oviposition by African malaria vector mosquitoes. II. Effects of site tone, water type and conspecific immatures on target selection by freshwater Anopheles gambiae Giles, sensu lato. Ann Trop Med Parasitol. 1984, 78: 307-318.PubMed McCrae AW: Oviposition by African malaria vector mosquitoes. II. Effects of site tone, water type and conspecific immatures on target selection by freshwater Anopheles gambiae Giles, sensu lato. Ann Trop Med Parasitol. 1984, 78: 307-318.PubMed
23.
go back to reference Munga S, Minakawa N, Zhou G, Barrack OO, Githeko AK, Yan G: Effects of larval competitors and predators on oviposition site selection of Anopheles gambiae sensu stricto. J Med Entomol. 2006, 43: 221-224. 10.1603/0022-2585(2006)043[0221:EOLCAP]2.0.CO;2.CrossRefPubMed Munga S, Minakawa N, Zhou G, Barrack OO, Githeko AK, Yan G: Effects of larval competitors and predators on oviposition site selection of Anopheles gambiae sensu stricto. J Med Entomol. 2006, 43: 221-224. 10.1603/0022-2585(2006)043[0221:EOLCAP]2.0.CO;2.CrossRefPubMed
24.
go back to reference Sumba LA, Ogbunugafor CB, Deng AL, Hassanali A: Regulation of oviposition in Anopheles gambiae s.s.: role of inter- and intra-specific signals. J Chem Ecol. 2008, 34: 1430-1436. 10.1007/s10886-008-9549-5.CrossRefPubMed Sumba LA, Ogbunugafor CB, Deng AL, Hassanali A: Regulation of oviposition in Anopheles gambiae s.s.: role of inter- and intra-specific signals. J Chem Ecol. 2008, 34: 1430-1436. 10.1007/s10886-008-9549-5.CrossRefPubMed
25.
go back to reference Sumba LA, Okoth K, Deng AL, Githure J, Knols BG, Beier JC, Hassanali A: Daily oviposition patterns of the African malaria mosquito Anopheles gambiae Giles (Diptera: Culicidae) on different types of aqueous substrates. J Circadian Rhythms. 2004, 2: 6-10.1186/1740-3391-2-6.PubMedCentralCrossRefPubMed Sumba LA, Okoth K, Deng AL, Githure J, Knols BG, Beier JC, Hassanali A: Daily oviposition patterns of the African malaria mosquito Anopheles gambiae Giles (Diptera: Culicidae) on different types of aqueous substrates. J Circadian Rhythms. 2004, 2: 6-10.1186/1740-3391-2-6.PubMedCentralCrossRefPubMed
26.
go back to reference Kramer WL, Mulla MS: Oviposition attractants and repellents of mosquitoes: oviposition responses of Culex mosquitoes to organic infusions. Environ Entomol. 1979, 8: 1111-1117.CrossRef Kramer WL, Mulla MS: Oviposition attractants and repellents of mosquitoes: oviposition responses of Culex mosquitoes to organic infusions. Environ Entomol. 1979, 8: 1111-1117.CrossRef
27.
go back to reference Paaijmans KP, Wandago MO, Githeko AK, Takken W: Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS One. 2007, 2: e1146-10.1371/journal.pone.0001146.PubMedCentralCrossRefPubMed Paaijmans KP, Wandago MO, Githeko AK, Takken W: Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS One. 2007, 2: e1146-10.1371/journal.pone.0001146.PubMedCentralCrossRefPubMed
28.
go back to reference Romoser W, Lerdthusnee K, Berry R, Kittayapong P: Effect of mechanical shock on hydrostatic balance and survival of mosquito pupae. J Am Mosq Control Assoc. 1994, 10: 10-PubMed Romoser W, Lerdthusnee K, Berry R, Kittayapong P: Effect of mechanical shock on hydrostatic balance and survival of mosquito pupae. J Am Mosq Control Assoc. 1994, 10: 10-PubMed
29.
go back to reference Koenraadt CJ, Paaijmans KP, Githeko AK, Knols BG, Takken W: Egg hatching, larval movement and larval survival of the malaria vector Anopheles gambiae in desiccating habitats. Malar J. 2003, 2: 20-10.1186/1475-2875-2-20.PubMedCentralCrossRefPubMed Koenraadt CJ, Paaijmans KP, Githeko AK, Knols BG, Takken W: Egg hatching, larval movement and larval survival of the malaria vector Anopheles gambiae in desiccating habitats. Malar J. 2003, 2: 20-10.1186/1475-2875-2-20.PubMedCentralCrossRefPubMed
30.
go back to reference Beier JC, Copeland R, Oyaro C, Masinya A, Odago WO, Oduor S, Koech DK, Roberts CR: Anopheles gambiae complex egg-stage survival in dry soil from larval development sites in western Kenya. J Am Mosq Control Assoc. 1990, 6: 105-109.PubMed Beier JC, Copeland R, Oyaro C, Masinya A, Odago WO, Oduor S, Koech DK, Roberts CR: Anopheles gambiae complex egg-stage survival in dry soil from larval development sites in western Kenya. J Am Mosq Control Assoc. 1990, 6: 105-109.PubMed
31.
go back to reference Shililu JI, Grueber WB, Mbogo CM, Githure JI, Riddiford LM, Beier JC: Development and survival of Anopheles gambiae eggs in drying soil: influence of the rate of drying, egg age, and soil type. J Am Mosq Control Assoc. 2004, 20: 243-247.PubMed Shililu JI, Grueber WB, Mbogo CM, Githure JI, Riddiford LM, Beier JC: Development and survival of Anopheles gambiae eggs in drying soil: influence of the rate of drying, egg age, and soil type. J Am Mosq Control Assoc. 2004, 20: 243-247.PubMed
32.
go back to reference Huang J, Walker ED, Vulule J, Miller JR: Daily temperature profiles in and around Western Kenyan larval habitats of Anopheles gambiae as related to egg mortality. Malar J. 2006, 5: 87-10.1186/1475-2875-5-87.PubMedCentralCrossRefPubMed Huang J, Walker ED, Vulule J, Miller JR: Daily temperature profiles in and around Western Kenyan larval habitats of Anopheles gambiae as related to egg mortality. Malar J. 2006, 5: 87-10.1186/1475-2875-5-87.PubMedCentralCrossRefPubMed
33.
go back to reference Bayoh MN, Lindsay SW: Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae). Bull Entomol Res. 2003, 93: 375-381.PubMed Bayoh MN, Lindsay SW: Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae). Bull Entomol Res. 2003, 93: 375-381.PubMed
34.
go back to reference Kirby MJ, Lindsay SW: Effect of temperature and inter-specific competition on the development and survival of Anopheles gambiae sensu stricto and An. arabiensis larvae. Acta Trop. 2009, 109: 118-123. 10.1016/j.actatropica.2008.09.025.CrossRefPubMed Kirby MJ, Lindsay SW: Effect of temperature and inter-specific competition on the development and survival of Anopheles gambiae sensu stricto and An. arabiensis larvae. Acta Trop. 2009, 109: 118-123. 10.1016/j.actatropica.2008.09.025.CrossRefPubMed
35.
go back to reference Bayoh MN, Lindsay SW: Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory. Med Vet Entomol. 2004, 18: 174-179. 10.1111/j.0269-283X.2004.00495.x.CrossRefPubMed Bayoh MN, Lindsay SW: Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory. Med Vet Entomol. 2004, 18: 174-179. 10.1111/j.0269-283X.2004.00495.x.CrossRefPubMed
36.
go back to reference Armstrong JA, Bransby-Williams WR: The maintenance of a colony of Anopheles gambiae, with observations on the effects of changes in temperature. Bull World Health Organ. 1961, 24: 427-435.PubMedCentralPubMed Armstrong JA, Bransby-Williams WR: The maintenance of a colony of Anopheles gambiae, with observations on the effects of changes in temperature. Bull World Health Organ. 1961, 24: 427-435.PubMedCentralPubMed
37.
go back to reference Paaijmans K, Jacobs A, Takken W, Heusinkveld B, Githeko A, Dicke M, Holtslag A: Observations and model estimates of diurnal water temperature dynamics in mosquito breeding sites in western Kenya. Hydrological Processes. 2008, 22: 4789-4801. 10.1002/hyp.7099.CrossRef Paaijmans K, Jacobs A, Takken W, Heusinkveld B, Githeko A, Dicke M, Holtslag A: Observations and model estimates of diurnal water temperature dynamics in mosquito breeding sites in western Kenya. Hydrological Processes. 2008, 22: 4789-4801. 10.1002/hyp.7099.CrossRef
38.
go back to reference Tsila HaM J, Foko Dadji GA: Adaptative responses of Anopheles gambiae in crowding larvae conditions in laboratory. Asian J Biol Sci. 2011, 4: 259-265.CrossRef Tsila HaM J, Foko Dadji GA: Adaptative responses of Anopheles gambiae in crowding larvae conditions in laboratory. Asian J Biol Sci. 2011, 4: 259-265.CrossRef
39.
go back to reference Service MW: Mortalities of the immature stages of species B of the Anopheles gambiae complex in Kenya: comparison between rice fields and temporary pools, identification of predators, and effects of insecticidal spraying. J Med Entomol. 1977, 13: 535-545.CrossRefPubMed Service MW: Mortalities of the immature stages of species B of the Anopheles gambiae complex in Kenya: comparison between rice fields and temporary pools, identification of predators, and effects of insecticidal spraying. J Med Entomol. 1977, 13: 535-545.CrossRefPubMed
40.
go back to reference Gimnig JE, Ombok M, Otieno S, Kaufman MG, Vulule JM, Walker ED: Density-dependent development of Anopheles gambiae (Diptera: Culicidae) larvae in artificial habitats. J Med Entomol. 2002, 39: 162-172. 10.1603/0022-2585-39.1.162.CrossRefPubMed Gimnig JE, Ombok M, Otieno S, Kaufman MG, Vulule JM, Walker ED: Density-dependent development of Anopheles gambiae (Diptera: Culicidae) larvae in artificial habitats. J Med Entomol. 2002, 39: 162-172. 10.1603/0022-2585-39.1.162.CrossRefPubMed
41.
go back to reference Mogi M, Miyagi I, Cabrera BD: Development and survival of immature mosquitoes (Diptera: Culicidae) in Philippine rice fields. J Med Entomol. 1984, 21: 283-291.CrossRefPubMed Mogi M, Miyagi I, Cabrera BD: Development and survival of immature mosquitoes (Diptera: Culicidae) in Philippine rice fields. J Med Entomol. 1984, 21: 283-291.CrossRefPubMed
42.
go back to reference Koenraadt CJ, Takken W: Cannibalism and predation among larvae of the Anopheles gambiae complex. Med Vet Entomol. 2003, 17: 61-66. 10.1046/j.1365-2915.2003.00409.x.CrossRefPubMed Koenraadt CJ, Takken W: Cannibalism and predation among larvae of the Anopheles gambiae complex. Med Vet Entomol. 2003, 17: 61-66. 10.1046/j.1365-2915.2003.00409.x.CrossRefPubMed
43.
go back to reference Service MW: Studies on sampling larval populations of the Anopheles gambiae complex. Bull World Health Organ. 1971, 45: 169-180.PubMedCentralPubMed Service MW: Studies on sampling larval populations of the Anopheles gambiae complex. Bull World Health Organ. 1971, 45: 169-180.PubMedCentralPubMed
44.
45.
go back to reference Mogi M, Okazawa T, Miyagi I, Sucharit S, Tumrasvin W, Deesin T, Khamboonruang C: Development and survival of anopheline immatures (Diptera: Culicidae) in rice fields in northern Thailand. J Med Entomol. 1986, 23: 244-250.CrossRefPubMed Mogi M, Okazawa T, Miyagi I, Sucharit S, Tumrasvin W, Deesin T, Khamboonruang C: Development and survival of anopheline immatures (Diptera: Culicidae) in rice fields in northern Thailand. J Med Entomol. 1986, 23: 244-250.CrossRefPubMed
47.
go back to reference Lindsay SW, Birley MH: Climate change and malaria transmission. Ann Trop Med Parasitol. 1996, 90: 573-588.PubMed Lindsay SW, Birley MH: Climate change and malaria transmission. Ann Trop Med Parasitol. 1996, 90: 573-588.PubMed
48.
go back to reference Kirby MJ, Lindsay SW: Responses of adult mosquitoes of two sibling species, Anopheles arabiensis and A-gambiae s.s. (Diptera : Culicidae), to high temperatures. Bull Entomol Res. 2004, 94: 441-448.PubMed Kirby MJ, Lindsay SW: Responses of adult mosquitoes of two sibling species, Anopheles arabiensis and A-gambiae s.s. (Diptera : Culicidae), to high temperatures. Bull Entomol Res. 2004, 94: 441-448.PubMed
49.
50.
go back to reference Essential malariology. Edited by: Warrell DA, Gilles HM. 2002, xii + 348-4 Essential malariology. Edited by: Warrell DA, Gilles HM. 2002, xii + 348-4
51.
go back to reference Gillies MT, Wilkes TJ: A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bull Entomol Res. 1965, 56: 237-262. 10.1017/S0007485300056339.CrossRefPubMed Gillies MT, Wilkes TJ: A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bull Entomol Res. 1965, 56: 237-262. 10.1017/S0007485300056339.CrossRefPubMed
52.
go back to reference Clements A, Paterson G: The analysis of mortality and survival rates in wild populations of mosquitoes. J Appl Ecology. 1981, 18: 373-399. 10.2307/2402401.CrossRef Clements A, Paterson G: The analysis of mortality and survival rates in wild populations of mosquitoes. J Appl Ecology. 1981, 18: 373-399. 10.2307/2402401.CrossRef
53.
go back to reference Charlwood J, Smith T, Kihonda J, Heiz B, Billingsley P, Takken W: Density independent feeding success of malaria vectors (Diptera: Culicidae) in Tanzania. Bull Entomol Res. 1995, 85: 29-35. 10.1017/S0007485300051981.CrossRef Charlwood J, Smith T, Kihonda J, Heiz B, Billingsley P, Takken W: Density independent feeding success of malaria vectors (Diptera: Culicidae) in Tanzania. Bull Entomol Res. 1995, 85: 29-35. 10.1017/S0007485300051981.CrossRef
54.
go back to reference Caswell H: Matrix population models: Construction, analysis, and interpretation. 2001, Sinauer Associates, Inc, Sunderland, 2 Caswell H: Matrix population models: Construction, analysis, and interpretation. 2001, Sinauer Associates, Inc, Sunderland, 2
55.
go back to reference Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D, Killeen GF: Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010, 7: e1000303-10.1371/journal.pmed.1000303.PubMedCentralCrossRefPubMed Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D, Killeen GF: Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010, 7: e1000303-10.1371/journal.pmed.1000303.PubMedCentralCrossRefPubMed
Metadata
Title
Modeling the role of environmental variables on the population dynamics of the malaria vector Anopheles gambiae sensu stricto
Authors
Paul E Parham
Diane Pople
Céline Christiansen-Jucht
Steve Lindsay
Wes Hinsley
Edwin Michael
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2012
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-11-271

Other articles of this Issue 1/2012

Malaria Journal 1/2012 Go to the issue