ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Toure YT, Petrarca V, Traore SF, Coulibaly A, Maiga HM, Sankare O, Sow M, Di Deco MA, Coluzzi M, 1998. The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. Parassitologia 40: 477–511.
-
2.
Toure YT, Petrarca V, Traore SF, Coulibaly A, Maiga HM, Sankare O, Sow M, Di Deco MA, Coluzzi M, 1994. Ecological genetic studies in the chromosomal form Mopti of Anopheles gambiae s.str. in Mali, West Africa. Genetica 94: 213–223.
-
3.
Fontenille D, Lochouarn L, Diagne N, Sokhna C, Lemasson JJ, Diatta M, Konate L, Faye F, Rogier C, Trape JF, 1997. High annual and seasonal variations in malaria transmission by anophelines and vector species composition in Dielmo, a holoendemic area in Senegal. Am J Trop Med Hyg 56: 247–253.
-
4.
Beier JC, Copeland RS, Oyaro C, Masinya A, Odago WO, Odour S, Koech DK, Roberts CR, 1990. Anopheles gambiae complex egg stage survival in dry soil from larval development sites in western Kenya. J Am Mosq Control Assoc 6: 105–109.
-
5.
Minakawa N, Githure JI, Beier JC, Yan G, 2001. Anopheline mosquito survival strategies during the dry period in western Kenya. J Med Entomol 38: 388–392.
-
6.
Koenraadt CJ, Paaijmans KP, Githeko AK, Knols BG, Takken W, 2003. Egg hatching, larval movement and larval survival of the malaria vector Anopheles gambiae in desiccating habitats. Malar J 2: 20.
-
7.
Yaro AS, Dao A, Adamou A, Crawford JE, Ribeiro JM, Gwadz R, Traore SF, Lehmann T, 2006. The distribution of hatching time in Anopheles gambiae. Malar J 5: 19.
-
8.
Gillies MT, De Meillon B, 1968. The Anophelinae of Africa South of the Sahara, 2nd ed. Johannesburg: South African Institute for Medical Research.
-
9.
Lehmann T, Diabate A, 2008. The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect Genet Evol 8: 737–746.
-
10.
Holstein MH, 1954. Biology of Anopheles gambiae. Research in French West Africa. Geneva: World Health Organization.
-
11.
Omer SM, Cloudsley-Thomson JL, 1968. Dry season biology of Anopheles gambiae Giles in the Sudan. Nature 217: 879–880.
-
12.
Benoit JB, Denlinger DL, 2007. Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens. J Exp Biol 210: 217–226.
-
13.
Robich RM, Denlinger DL, 2005. Diapause in the mosquito Culex pipiens evokes a metabolic switch from blood feeding to sugar gluttony. Proc Natl Acad Sci USA 102: 15912–15917.
-
14.
Bradshaw WE, Holzapfel CM, 1977. Interaction between photoperiod, temperature, and chilling in dormant larvae of the tree-hole mosquito, Toxorhynchites rutilus Coq. Biol Bull 152: 147–158.
-
15.
Bradshaw WE, Zani PA, Holzapfel CM, 2004. Adaptation to temperate climates. Evolution 58: 1748–1762.
-
16.
Reisen WK, Baker RH, Sakai RK, Aziz-Javed A, Aslam Y, Siddiqui TF, 1977. Observations on mating behavior and survivorship of Culex tritaeniorhynchus Giles (Diptera: Culicidae) during late autumn. Southeast Asian J Trop Med Public Health 8: 537–545.
-
17.
Denlinger DL, 1986. Dormancy in tropical insects. Annu Rev Entomol 31: 239–264.
-
18.
Tauber MJ, Tauber CA, Masaki S, 1986. Seasonal Adaptations of Insects. New York: Oxford University Press.
-
19.
Ramsdale CD, Fontaine RE, 1970. Ecological Investigations On Anopheles gambiae and Anopheles funestus I. Dry Season Studies in Villages near Kaduna Nigeria. Geneva: World Health Organization.
-
20.
Warburg A, Toure YT, 2002. Aestivation of Anopheles gambiae: Potential Habitats and Physiology. US Agency for International Development (USAID).
-
21.
Simard F, Lehmann T, Lemasson JJ, Diatta M, Fontenille D, 2000. Persistence of Anopheles arabiensis during the severe dry season conditions in Senegal: an indirect approach using microsatellite loci. Insect Mol Biol 9: 467–479.
-
22.
Omer SM, Cloudsley-Thompson JL, 1970. Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull World Health Organ 42: 319–330.
-
23.
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.
-
24.
Jawara M, Pinder M, Drakeley CJ, Nwakanma DC, Jallow E, Bogh C, Lindsay SW, Conway DJ, 2008. Dry season ecology of Anopheles gambiae complex mosquitoes in The Gambia. Malar J 7: 156.
-
25.
Ramsdale CD, Fontaine RE, 1970. Ecological Investigations of Anopheles gambiae and Anopheles funestus II. Dry Season Studies with Colony-Reared A. gambiae Species B, Kaduna Nigeria. Geneva: World Health Organization.
-
26.
Taylor CE, Toure YT, Coluzzi M, Petrarca V, 1993. Effective population size and persistence of Anopheles arabiensis during the dry season in West Africa. Med Vet Entomol 7: 351–357.
-
27.
Lehmann T, Hawley WA, Grebert H, Collins FH, 1998. The effective population size of Anopheles gambiae in Kenya: implications for population structure. Mol Biol Evol 15: 264–276.
-
28.
Donnelly MJ, Simard F, Lehmann T, 2002. Evolutionary studies of malaria vectors. Trends Parasitol 18: 75–80.
-
29.
Service MW, 1993. Mosquito Ecology Field Sampling Methods. Essex: Elsevier Applied Science.
-
30.
Lemasson JJ, Fontenille D, Lochouarn L, Dia I, Simard F, Ba K, Diop A, Diatta M, Molez JF, 1997. Comparison of behavior and vector efficiency of Anopheles gambiae and An. arabiensis (Diptera:Culicidae) in Barkedji, a Sahelian area of Senegal. J Med Entomol 34: 396–403.
-
31.
Sogoba N, Doumbia S, Vounatsou P, Baber I, Keita M, Maiga M, Traore SF, Toure A, Dolo G, Smith T, Ribeiro JM, 2007. Monitoring of larval habitats and mosquito densities in the Sudan savanna of Mali: implications for malaria vector control. Am J Trop Med Hyg 77: 82–88.
-
32.
Coluzzi M, 1984. Heterogeneities of the malaria vectorial system in tropical Africa and their significance in malaria epidemiology and control. Bull World Health Organ 62 (Suppl): 107–113.
-
33.
Fontenille D, Lochouarn L, Diatta M, Sokhna C, Dia I, Diagne N, Lemasson JJ, Ba K, Tall A, Rogier C, Trape JF, 1997. Four years entomological study of the transmission of seasonal malaria in Senegal and the bionomics of Anopheles gambiae and An. arabiensis. Trans R Soc Trop Med Hyg 91: 647–652.
-
34.
Toure YT, Dolo G, Petrarca V, Traore SF, Bouare M, Dao A, Carnahan J, Taylor CE, 1998. Mark-release-recapture experiments with Anopheles gambiae s.l. in Banambani Village, Mali, to determine population size and structure. Med Vet Entomol 12: 74–83.
-
35.
Toure YT, Traore SF, Sankare O, Sow MY, Coulibaly A, Esposito F, Petrarca V, 1996. Perennial transmission of malaria by the Anopheles gambiae complex in a north Sudan Savanna area of Mali. Med Vet Entomol 10: 197–199.
-
36.
Costantini C, Li SG, della Torre A, Sagnon N, Coluzzi M, Taylor CE, 1996. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a West African Sudan savanna village. Med Vet Entomol 10: 203–219.
-
37.
Gillies MT, 1961. Studies on the dispersion and survival of Anopheles gambiae in East Africa, by means of marking and release experiments. Bull Entomol Res 52: 99–127.
-
38.
Benoit JB, Lopez-Martinez G, Phillips ZP, Patrick KR, Denlinger DL, 2010. Heat shock proteins contribute to mosquito dehydration tolerance. J Insect Physiol 56: 151–156.
-
39.
Sim C, Denlinger DL, 2008. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc Natl Acad Sci USA 105: 6777–6781.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2675 | 2446 | 34 |
| Full Text Views | 629 | 35 | 0 |
| PDF Downloads | 257 | 39 | 0 |
Aestivation of the African Malaria Mosquito, Anopheles gambiae in the Sahel
Tovi Lehmann
Tovi Lehmann
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali
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Adama Dao
Adama Dao
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali
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Alpha Seydou Yaro
Alpha Seydou Yaro
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali
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Abdoulaye Adamou
Abdoulaye Adamou
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali
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Yaya Kassogue
Yaya Kassogue
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali
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Moussa Diallo
Moussa Diallo
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali
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Traoré Sékou
Traoré Sékou
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali
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Cecilia Coscaron-Arias
Cecilia Coscaron-Arias
Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali
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The African malaria mosquito, Anopheles gambiae, inhabits diverse environments including dry savannas, where surface waters required for larval development are absent for 4–8 months per year. Under such conditions, An. gambiae virtually disappears. Whether populations survive the long dry season by aestivation (a dormant state promoting extended longevity during the summer) or are reestablished by migrants from distant locations where larval sites persist has remained an enigma for over 60 years. Resolving this question is important, because fragile dry season populations may be more susceptible to control. Here, we show unequivocally that An. gambiae aestivates based on a demographic study and a mark release–recapture experiment spanning the period from the end of one wet season to the beginning of the next. During the dry season, An. gambiae was barely detectable in Sahelian villages of Mali. Five days after the first rain, before a new generation of adults could be produced, mosquito abundance surged 10-fold, implying that most mosquitoes were concealed locally until the rain. Four days after the first rain, a marked female An. gambiae s.s. was recaptured. Initially captured, marked, and released at the end of the previous wet season, she has survived the 7-month-long dry season. These results provide evidence that An. gambiae persists throughout the dry season by aestivation and open new questions for mosquito and parasite research. Improved malaria control by targeting aestivating mosquitoes using existing or novel strategies may be possible.
Author Notes
Financial support: This study was supported by the Intramural Research Program in National Institutes of Health, National Institute of Allergy and Infectious Diseases.
Authors' addresses: Tovi Lehmann and Cecilia Coscaron-Arias, Laboratory of Malaria and Vector Research, National Institutes of Health, National Institute of Allergy and Infectious Diseases, Rockville, MD, E-mails: tlehmann@niaid.nih.gov, and coscaron@verizon.net. Adama Dao, Alpha Seydou Yaro, Abdoulaye Adamou, Yaya Kassogue, Moussa Diallo, and Traoré Sékou, Malaria Research and Training Center, University of Bamako, Bamako, Mali, E-mails: adama@MRTCBKO.org, yaro@icermali.org, Adamou@MRTCBKO.org, ykassogue@MRTCBKO.org, moussad@icermali.org, and cheick@mrtcbko.org.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Toure YT, Petrarca V, Traore SF, Coulibaly A, Maiga HM, Sankare O, Sow M, Di Deco MA, Coluzzi M, 1998. The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. Parassitologia 40: 477–511.
-
2.
Toure YT, Petrarca V, Traore SF, Coulibaly A, Maiga HM, Sankare O, Sow M, Di Deco MA, Coluzzi M, 1994. Ecological genetic studies in the chromosomal form Mopti of Anopheles gambiae s.str. in Mali, West Africa. Genetica 94: 213–223.
-
3.
Fontenille D, Lochouarn L, Diagne N, Sokhna C, Lemasson JJ, Diatta M, Konate L, Faye F, Rogier C, Trape JF, 1997. High annual and seasonal variations in malaria transmission by anophelines and vector species composition in Dielmo, a holoendemic area in Senegal. Am J Trop Med Hyg 56: 247–253.
-
4.
Beier JC, Copeland RS, Oyaro C, Masinya A, Odago WO, Odour S, Koech DK, Roberts CR, 1990. Anopheles gambiae complex egg stage survival in dry soil from larval development sites in western Kenya. J Am Mosq Control Assoc 6: 105–109.
-
5.
Minakawa N, Githure JI, Beier JC, Yan G, 2001. Anopheline mosquito survival strategies during the dry period in western Kenya. J Med Entomol 38: 388–392.
-
6.
Koenraadt CJ, Paaijmans KP, Githeko AK, Knols BG, Takken W, 2003. Egg hatching, larval movement and larval survival of the malaria vector Anopheles gambiae in desiccating habitats. Malar J 2: 20.
-
7.
Yaro AS, Dao A, Adamou A, Crawford JE, Ribeiro JM, Gwadz R, Traore SF, Lehmann T, 2006. The distribution of hatching time in Anopheles gambiae. Malar J 5: 19.
-
8.
Gillies MT, De Meillon B, 1968. The Anophelinae of Africa South of the Sahara, 2nd ed. Johannesburg: South African Institute for Medical Research.
-
9.
Lehmann T, Diabate A, 2008. The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect Genet Evol 8: 737–746.
-
10.
Holstein MH, 1954. Biology of Anopheles gambiae. Research in French West Africa. Geneva: World Health Organization.
-
11.
Omer SM, Cloudsley-Thomson JL, 1968. Dry season biology of Anopheles gambiae Giles in the Sudan. Nature 217: 879–880.
-
12.
Benoit JB, Denlinger DL, 2007. Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens. J Exp Biol 210: 217–226.
-
13.
Robich RM, Denlinger DL, 2005. Diapause in the mosquito Culex pipiens evokes a metabolic switch from blood feeding to sugar gluttony. Proc Natl Acad Sci USA 102: 15912–15917.
-
14.
Bradshaw WE, Holzapfel CM, 1977. Interaction between photoperiod, temperature, and chilling in dormant larvae of the tree-hole mosquito, Toxorhynchites rutilus Coq. Biol Bull 152: 147–158.
-
15.
Bradshaw WE, Zani PA, Holzapfel CM, 2004. Adaptation to temperate climates. Evolution 58: 1748–1762.
-
16.
Reisen WK, Baker RH, Sakai RK, Aziz-Javed A, Aslam Y, Siddiqui TF, 1977. Observations on mating behavior and survivorship of Culex tritaeniorhynchus Giles (Diptera: Culicidae) during late autumn. Southeast Asian J Trop Med Public Health 8: 537–545.
-
17.
Denlinger DL, 1986. Dormancy in tropical insects. Annu Rev Entomol 31: 239–264.
-
18.
Tauber MJ, Tauber CA, Masaki S, 1986. Seasonal Adaptations of Insects. New York: Oxford University Press.
-
19.
Ramsdale CD, Fontaine RE, 1970. Ecological Investigations On Anopheles gambiae and Anopheles funestus I. Dry Season Studies in Villages near Kaduna Nigeria. Geneva: World Health Organization.
-
20.
Warburg A, Toure YT, 2002. Aestivation of Anopheles gambiae: Potential Habitats and Physiology. US Agency for International Development (USAID).
-
21.
Simard F, Lehmann T, Lemasson JJ, Diatta M, Fontenille D, 2000. Persistence of Anopheles arabiensis during the severe dry season conditions in Senegal: an indirect approach using microsatellite loci. Insect Mol Biol 9: 467–479.
-
22.
Omer SM, Cloudsley-Thompson JL, 1970. Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull World Health Organ 42: 319–330.
-
23.
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.
-
24.
Jawara M, Pinder M, Drakeley CJ, Nwakanma DC, Jallow E, Bogh C, Lindsay SW, Conway DJ, 2008. Dry season ecology of Anopheles gambiae complex mosquitoes in The Gambia. Malar J 7: 156.
-
25.
Ramsdale CD, Fontaine RE, 1970. Ecological Investigations of Anopheles gambiae and Anopheles funestus II. Dry Season Studies with Colony-Reared A. gambiae Species B, Kaduna Nigeria. Geneva: World Health Organization.
-
26.
Taylor CE, Toure YT, Coluzzi M, Petrarca V, 1993. Effective population size and persistence of Anopheles arabiensis during the dry season in West Africa. Med Vet Entomol 7: 351–357.
-
27.
Lehmann T, Hawley WA, Grebert H, Collins FH, 1998. The effective population size of Anopheles gambiae in Kenya: implications for population structure. Mol Biol Evol 15: 264–276.
-
28.
Donnelly MJ, Simard F, Lehmann T, 2002. Evolutionary studies of malaria vectors. Trends Parasitol 18: 75–80.
-
29.
Service MW, 1993. Mosquito Ecology Field Sampling Methods. Essex: Elsevier Applied Science.
-
30.
Lemasson JJ, Fontenille D, Lochouarn L, Dia I, Simard F, Ba K, Diop A, Diatta M, Molez JF, 1997. Comparison of behavior and vector efficiency of Anopheles gambiae and An. arabiensis (Diptera:Culicidae) in Barkedji, a Sahelian area of Senegal. J Med Entomol 34: 396–403.
-
31.
Sogoba N, Doumbia S, Vounatsou P, Baber I, Keita M, Maiga M, Traore SF, Toure A, Dolo G, Smith T, Ribeiro JM, 2007. Monitoring of larval habitats and mosquito densities in the Sudan savanna of Mali: implications for malaria vector control. Am J Trop Med Hyg 77: 82–88.
-
32.
Coluzzi M, 1984. Heterogeneities of the malaria vectorial system in tropical Africa and their significance in malaria epidemiology and control. Bull World Health Organ 62 (Suppl): 107–113.
-
33.
Fontenille D, Lochouarn L, Diatta M, Sokhna C, Dia I, Diagne N, Lemasson JJ, Ba K, Tall A, Rogier C, Trape JF, 1997. Four years entomological study of the transmission of seasonal malaria in Senegal and the bionomics of Anopheles gambiae and An. arabiensis. Trans R Soc Trop Med Hyg 91: 647–652.
-
34.
Toure YT, Dolo G, Petrarca V, Traore SF, Bouare M, Dao A, Carnahan J, Taylor CE, 1998. Mark-release-recapture experiments with Anopheles gambiae s.l. in Banambani Village, Mali, to determine population size and structure. Med Vet Entomol 12: 74–83.
-
35.
Toure YT, Traore SF, Sankare O, Sow MY, Coulibaly A, Esposito F, Petrarca V, 1996. Perennial transmission of malaria by the Anopheles gambiae complex in a north Sudan Savanna area of Mali. Med Vet Entomol 10: 197–199.
-
36.
Costantini C, Li SG, della Torre A, Sagnon N, Coluzzi M, Taylor CE, 1996. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a West African Sudan savanna village. Med Vet Entomol 10: 203–219.
-
37.
Gillies MT, 1961. Studies on the dispersion and survival of Anopheles gambiae in East Africa, by means of marking and release experiments. Bull Entomol Res 52: 99–127.
-
38.
Benoit JB, Lopez-Martinez G, Phillips ZP, Patrick KR, Denlinger DL, 2010. Heat shock proteins contribute to mosquito dehydration tolerance. J Insect Physiol 56: 151–156.
-
39.
Sim C, Denlinger DL, 2008. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc Natl Acad Sci USA 105: 6777–6781.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2675 | 2446 | 34 |
| Full Text Views | 629 | 35 | 0 |
| PDF Downloads | 257 | 39 | 0 |