ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1
Dye C, 1992. The analysis of parasite transmission by bloodsucking insects. Annu Rev Entomol 37 :1–19.
-
2
Clements AN, Paterson GD, 1981. The analysis of mortality and survival rates in wild populations of mosquitoes. J Appl Ecol 18 :373–399.
-
3
MacDonald G, 1952. The analysis of the sporozoite rate. Trop Dis Bull 49 :569–586.
-
4
Russel PF, Rao TR, 1942. Observations on longevity of Anopheles culicifacies imagines. Am J Trop Med 22 :517–533.
-
5
Keener GG Jr, 1945. Detailed observations on the life history of Anopheles quadrimaculatus. J Natl Malaria Soc 4 :263–270.
-
6
Kershaw WE, Chalmers TA, Lavoipierre MMJ, 1954. Studies on arthropod survival. I.—The pattern of mosquito survival in laboratory conditions. Ann Trop Med Parasitiol 48 :442–450.
-
7
Gillies MT, Wilkes TJ, 1965. A study of the age-compositions of populations of Anopheles gambiae Giles and A. funestus Giles in north-eastern Tanzania. Bull Entomol Res 56 :237–262.
-
8
Briegel H, Kaiser C, 1973. Life-span of mosquitoes (Culicidae, Diptera) under laboratory conditions. Gerontologia 19 :240–249.
-
9
Harrington LC, Buonaccorsi JP, Edman JD, Costero A, Kittayapong P, Clark GG, Scott TW, 2001. Analysis of survival of young and old Aedes aegypti (Diptera: Culicidae) from Puerto Rico and Thailand. J Med Entomol 38 :537–547.
-
10
Okech BA, Gouagna LC, Killeen GF, Knols BG, Kabiru EW, Beier JC, Yan G, Githure JI, 2003. Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in Western Kenya. J Med Entomol 40 :657–663.
-
11
Nayar JK, Sauerman DM Jr, 1973. A comparative study of flight performance and fuel utilization as a function of age in females of Florida mosquitoes. J Insect Physiol 19 :1977–1988.
-
12
Christensen BM, LaFond MM, Christensen LA, 1986. Defense reactions of mosquitoes to filarial worms: Effect of host age on the immune response to Dirofilaria immitis microfilariae. J Parasitol 72 :212–215.
-
13
Beckett EB, 1990. Development and aging of the salivary glands of adult female Aedes aegypti (L.) and Aedes togoi (Theobald) mosquitoes (Diptera: Culicidae). Int J Insect Morphol Embryol 19 :277–290.
-
14
Hazelton GA, Lang CA, 1984. Glutathione levels during the mosquito life span with emphasis on senescence. Proc Soc Exp Biol Med 176 :249–256.
-
15
Lines JD, Nassor NS, 1991. DDT resistance in Anopheles gambiae declines with mosquito age. Med Vet Entomol 5 :261–265.
-
16
Gillies MT, 1988. Anopheles mosquitoes: Vector behavior and bionomics. In: Wernsdorfer WH, McGregor IA, eds. Malaria: Principles and Practice of Malariology. New York: Churchill Livingstone, 453–485.
-
17
Ishikawa H, Ishii A, Nagai N, Ohmae H, Harada M, Suguri S, Leafasia J, 2003. A mathematical model for the transmission of Plasmodium vivax malaria. Parasitol Int 52 :81–93.
-
18
Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF, Beier JC, 2000. A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. Am J Trop Med Hyg 62 :535–544.
-
19
Smith DL, Dushoff J, McKenzie FE, 2004. The risk of a mosquito-borne infection in a heterogeneous environment. PLoS Biol 2 :e368.
-
20
Focks DA, Daniels E, Haile DG, Keesling JE, 1995. A simulation model of the epidemiology of urban dengue fever: literature analysis, model development, preliminary validation, and samples of simulation results. Am J Trop Med Hyg 53 :489–506.
-
21
Promislow DEL, Tatar M, Pletcher S, Carey JR, 1999. Below-threshold mortality: implications for studies in evolution, ecology and demography. J Evol Biol 12 :314–328.
-
22
Dye C, 1990. Epidemiological significance of vector-parasite interactions. Parasitiology 101 :409–415.
-
23
Alto BW, Lounibos LP, Juliano SA, 2003. Age-dependent blood-feeding of Aedes aegypti and Aedes albopictus on artificial and living hosts. J Am Mosq Control Assoc 19 :347–352.
-
24
Chun J, Riehle M, Paskewitz SM, 1995. Effect of mosquito age and reproductive status on melanization of Sephadex beads in Plasmodium-refractory and -susceptible strains of Anopheles gambiae. J Invertebr Pathol 66 :11–17.
-
25
Mourya DT, Hemingway J, Leake CJ, 1993. Changes in enzyme titres with age in four geographical strains of Aedes aegypti and their association with insecticide resistance. Med Vet Entomol 7 :11–16.
-
26
Soliman B, Ghalia AA, Shoukry A, Merdan A, 1993. Mosquito age as a factor influencing the transmission of Wuchereria bancrofti. Journal of the Eqyptian Society of Parasitology 23 :717– 721.
-
27
Hillyer JF, Schmidt SL, Fuchs JF, Boyle JP, Christensen BM, 2005. Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cell Microbiol 7 :39–51.
-
28
Garrett-Jones C, 1964. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ 30 :241–261.
-
29
Christophers SSR, 1960. Aedes aegypti (L.)—The Yellow Fever Mosquito. London: Cambridge University Press.
-
30
Nasci R, 1986. 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 2 :61–62.
-
31
Scott TW, Morrison AC, Lorenz LH, Clark GG, Strickman D, Kittayapong P, Zhou H, Edman JD, 2000. Longitudinal Studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puer-to Rico: Population dynamics. J Med Entomol 37 :77–88.
-
32
Carey JR, 1993. Applied Biodemography for Biologists with Special Emphasis on Insects. New York: Oxford University Press.
-
33
Pletcher S, 1999. WinModest 1.0. Demographic Analysis Tool [computer program]. Rostock, Germany: Max Planck Institute for Demographic Research.
-
34
SAS Institute, 1999. SAS System for Windows [computer program]. Version 8. Cary, NC: SAS Institute.
-
35
Styer L, Minnick S, Sun A, Scott TW, 2007. Mortality and reproductive dynamics of Aedes aegypti (Diptera:Culicidae) fed human blood. Vector Borne Zoonotic Dis.: in press.
-
36
Saul AJ, Graves PM, Kay BH, 1990. A cyclical feeding model for pathogen transmission and its application to determine vectorial capacity from vector infection rates. J Appl Ecol 27 :123–133.
-
37
Gubler D, 1997. Dengue and dengue hemorrhagic fever: its history and resurgence as a global public health problem. In: Gubler D, Kuno G, eds. Dengue and Dengue Hemorrhagic Fever. Oxford, UK, CAB International, 1–22.
-
38
Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Strickman D, Kittayapong P, Edman JD, 2000. Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: Blood feeding frequency. J Med Entomol 37 :89–101.
-
39
Harrington LC, Vermeylen F, Jones JJ, Kitthawee S, Sithiprasasna R, Edman JD, Scott TW, 2007. Age-dependent survival of the dengue vector, Aedes aegypti, demonstrated by simultaneous release-recapture of different age cohorts. Am J Trop Med Hyg.: in press.
-
40
Vaupel JW, Carey JR, Christensen K, Johnson TE, Yashin AI, Holm NV, Iachine IA, Kannisto V, Khazaeli AA, Liedo P, Longo VD, Zeng Y, Manton KG, Curtsinger JW, 1998. Bio-demographic trajectories of longevity. Science 280 :855–860.
-
41
Rosenberg R, Andre RG, Somchit L, 1990. Highly efficient dry season transmission of malaria in Thailand. Trans R Soc Trop Med Hyg 84 :22–28.
-
42
Gadawski RM, Smith SM, 1992. Nectar sources and age structure in a population of Aedes provocans (Diptera: Culicidae). J Med Entomol 29 :879–886.
-
43
Sheppard PM, Macdonald WW, Tonn RJ, Grab B, 1969. The dynamics of an adult population of Aedes aegypti in relation to dengue haemorrhagic fever in Bangkok. J Anim Ecol 38 :661–702.
-
44
Hay SI, Myers MF, Burke DS, Vaughn DW, Endy T, Ananda N, Shanks GD, Snow RW, Rogers DJ, 2000. Etiology of interepidemic periods of mosquito-borne disease. Proc Natl Acad Sci USA 97 :9335–9339.
-
45
Hayes EJ, Wall R, 1999. Age-grading adult insects: a review of techniques. Physiol Entomol 24 :1–10.
-
46
Desena ML, Clark JM, Edman JD, Symington SB, Scott TW, Clark GG, Peters TM, 1999. Potential for aging female Aedes aegypti (Diptera: Culicidae) by gas chromatographic analysis of cuticular hydrocarbons, including a field evaluation. J Med Entomol 36 :811–823.
-
47
Hugo LE, Kay BH, Eaglesham GK, Holling N, Ryan PA, 2006. Investigation of cuticular hydrocarbons for determining the age and survivorship of Australasian mosquitoes. Am J Trop Med Hyg 74 :462–474.
-
48
Carey JR, 2001. Insect biodemography. Annu Rev Entomol 46 :79–110.
-
49
Wang J-L, Muller H-G, Capra WB, 1998. Analysis of oldest-old mortality: Lifetables revisited. Ann Statist 26 :126–163.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 326 | 240 | 5 |
| Full Text Views | 410 | 5 | 0 |
| PDF Downloads | 108 | 5 | 0 |
MOSQUITOES DO SENESCE: DEPARTURE FROM THE PARADIGM OF CONSTANT MORTALITY
LINDA M. STYER
LINDA M. STYER
Department of Entomology, University of California, Davis, California; Department of Statistics, University of California, Davis, California
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JAMES R. CAREY
JAMES R. CAREY
Department of Entomology, University of California, Davis, California; Department of Statistics, University of California, Davis, California
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JANE-LING WANG
JANE-LING WANG
Department of Entomology, University of California, Davis, California; Department of Statistics, University of California, Davis, California
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THOMAS W. SCOTT
THOMAS W. SCOTT
Department of Entomology, University of California, Davis, California; Department of Statistics, University of California, Davis, California
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Although variation in mortality is considered by virtually all vector-borne disease specialists to be one of the most important determinants of an arthropod’s capacity to transmit pathogens, the operational assumption often is that insect vector mortality is independent of age. Acceptance of the non-senescence assumption leads to the erroneous conclusion that mosquito age is unimportant, results in misleading predictions regarding disease reductions after vector control, and represses study of other aspects of mosquito biology that change with age. We brought large-scale laboratory life table techniques (N > 100,000) to bear on the question of age-dependent mortality in the mosquito vector of dengue virus, Aedes aegypti. Mortality was highly age dependent in both sexes. Mortality was low at young ages (< 10 days old), steadily increased at middle ages, and decelerated at older ages. A newly derived age-dependent model of pathogen transmission shows the importance of young mosquitoes and population age structure to transmission dynamics. Departure from the age-independent mortality paradigm encourages research on overlooked complexities in mosquito biology, the need for innovative methods to study mosquito population dynamics, and the need to study age-dependent changes for an accurate understanding of mosquito biology and pathogen transmission.
Author Notes
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1
Dye C, 1992. The analysis of parasite transmission by bloodsucking insects. Annu Rev Entomol 37 :1–19.
-
2
Clements AN, Paterson GD, 1981. The analysis of mortality and survival rates in wild populations of mosquitoes. J Appl Ecol 18 :373–399.
-
3
MacDonald G, 1952. The analysis of the sporozoite rate. Trop Dis Bull 49 :569–586.
-
4
Russel PF, Rao TR, 1942. Observations on longevity of Anopheles culicifacies imagines. Am J Trop Med 22 :517–533.
-
5
Keener GG Jr, 1945. Detailed observations on the life history of Anopheles quadrimaculatus. J Natl Malaria Soc 4 :263–270.
-
6
Kershaw WE, Chalmers TA, Lavoipierre MMJ, 1954. Studies on arthropod survival. I.—The pattern of mosquito survival in laboratory conditions. Ann Trop Med Parasitiol 48 :442–450.
-
7
Gillies MT, Wilkes TJ, 1965. A study of the age-compositions of populations of Anopheles gambiae Giles and A. funestus Giles in north-eastern Tanzania. Bull Entomol Res 56 :237–262.
-
8
Briegel H, Kaiser C, 1973. Life-span of mosquitoes (Culicidae, Diptera) under laboratory conditions. Gerontologia 19 :240–249.
-
9
Harrington LC, Buonaccorsi JP, Edman JD, Costero A, Kittayapong P, Clark GG, Scott TW, 2001. Analysis of survival of young and old Aedes aegypti (Diptera: Culicidae) from Puerto Rico and Thailand. J Med Entomol 38 :537–547.
-
10
Okech BA, Gouagna LC, Killeen GF, Knols BG, Kabiru EW, Beier JC, Yan G, Githure JI, 2003. Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in Western Kenya. J Med Entomol 40 :657–663.
-
11
Nayar JK, Sauerman DM Jr, 1973. A comparative study of flight performance and fuel utilization as a function of age in females of Florida mosquitoes. J Insect Physiol 19 :1977–1988.
-
12
Christensen BM, LaFond MM, Christensen LA, 1986. Defense reactions of mosquitoes to filarial worms: Effect of host age on the immune response to Dirofilaria immitis microfilariae. J Parasitol 72 :212–215.
-
13
Beckett EB, 1990. Development and aging of the salivary glands of adult female Aedes aegypti (L.) and Aedes togoi (Theobald) mosquitoes (Diptera: Culicidae). Int J Insect Morphol Embryol 19 :277–290.
-
14
Hazelton GA, Lang CA, 1984. Glutathione levels during the mosquito life span with emphasis on senescence. Proc Soc Exp Biol Med 176 :249–256.
-
15
Lines JD, Nassor NS, 1991. DDT resistance in Anopheles gambiae declines with mosquito age. Med Vet Entomol 5 :261–265.
-
16
Gillies MT, 1988. Anopheles mosquitoes: Vector behavior and bionomics. In: Wernsdorfer WH, McGregor IA, eds. Malaria: Principles and Practice of Malariology. New York: Churchill Livingstone, 453–485.
-
17
Ishikawa H, Ishii A, Nagai N, Ohmae H, Harada M, Suguri S, Leafasia J, 2003. A mathematical model for the transmission of Plasmodium vivax malaria. Parasitol Int 52 :81–93.
-
18
Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF, Beier JC, 2000. A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. Am J Trop Med Hyg 62 :535–544.
-
19
Smith DL, Dushoff J, McKenzie FE, 2004. The risk of a mosquito-borne infection in a heterogeneous environment. PLoS Biol 2 :e368.
-
20
Focks DA, Daniels E, Haile DG, Keesling JE, 1995. A simulation model of the epidemiology of urban dengue fever: literature analysis, model development, preliminary validation, and samples of simulation results. Am J Trop Med Hyg 53 :489–506.
-
21
Promislow DEL, Tatar M, Pletcher S, Carey JR, 1999. Below-threshold mortality: implications for studies in evolution, ecology and demography. J Evol Biol 12 :314–328.
-
22
Dye C, 1990. Epidemiological significance of vector-parasite interactions. Parasitiology 101 :409–415.
-
23
Alto BW, Lounibos LP, Juliano SA, 2003. Age-dependent blood-feeding of Aedes aegypti and Aedes albopictus on artificial and living hosts. J Am Mosq Control Assoc 19 :347–352.
-
24
Chun J, Riehle M, Paskewitz SM, 1995. Effect of mosquito age and reproductive status on melanization of Sephadex beads in Plasmodium-refractory and -susceptible strains of Anopheles gambiae. J Invertebr Pathol 66 :11–17.
-
25
Mourya DT, Hemingway J, Leake CJ, 1993. Changes in enzyme titres with age in four geographical strains of Aedes aegypti and their association with insecticide resistance. Med Vet Entomol 7 :11–16.
-
26
Soliman B, Ghalia AA, Shoukry A, Merdan A, 1993. Mosquito age as a factor influencing the transmission of Wuchereria bancrofti. Journal of the Eqyptian Society of Parasitology 23 :717– 721.
-
27
Hillyer JF, Schmidt SL, Fuchs JF, Boyle JP, Christensen BM, 2005. Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cell Microbiol 7 :39–51.
-
28
Garrett-Jones C, 1964. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ 30 :241–261.
-
29
Christophers SSR, 1960. Aedes aegypti (L.)—The Yellow Fever Mosquito. London: Cambridge University Press.
-
30
Nasci R, 1986. 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 2 :61–62.
-
31
Scott TW, Morrison AC, Lorenz LH, Clark GG, Strickman D, Kittayapong P, Zhou H, Edman JD, 2000. Longitudinal Studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puer-to Rico: Population dynamics. J Med Entomol 37 :77–88.
-
32
Carey JR, 1993. Applied Biodemography for Biologists with Special Emphasis on Insects. New York: Oxford University Press.
-
33
Pletcher S, 1999. WinModest 1.0. Demographic Analysis Tool [computer program]. Rostock, Germany: Max Planck Institute for Demographic Research.
-
34
SAS Institute, 1999. SAS System for Windows [computer program]. Version 8. Cary, NC: SAS Institute.
-
35
Styer L, Minnick S, Sun A, Scott TW, 2007. Mortality and reproductive dynamics of Aedes aegypti (Diptera:Culicidae) fed human blood. Vector Borne Zoonotic Dis.: in press.
-
36
Saul AJ, Graves PM, Kay BH, 1990. A cyclical feeding model for pathogen transmission and its application to determine vectorial capacity from vector infection rates. J Appl Ecol 27 :123–133.
-
37
Gubler D, 1997. Dengue and dengue hemorrhagic fever: its history and resurgence as a global public health problem. In: Gubler D, Kuno G, eds. Dengue and Dengue Hemorrhagic Fever. Oxford, UK, CAB International, 1–22.
-
38
Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Strickman D, Kittayapong P, Edman JD, 2000. Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: Blood feeding frequency. J Med Entomol 37 :89–101.
-
39
Harrington LC, Vermeylen F, Jones JJ, Kitthawee S, Sithiprasasna R, Edman JD, Scott TW, 2007. Age-dependent survival of the dengue vector, Aedes aegypti, demonstrated by simultaneous release-recapture of different age cohorts. Am J Trop Med Hyg.: in press.
-
40
Vaupel JW, Carey JR, Christensen K, Johnson TE, Yashin AI, Holm NV, Iachine IA, Kannisto V, Khazaeli AA, Liedo P, Longo VD, Zeng Y, Manton KG, Curtsinger JW, 1998. Bio-demographic trajectories of longevity. Science 280 :855–860.
-
41
Rosenberg R, Andre RG, Somchit L, 1990. Highly efficient dry season transmission of malaria in Thailand. Trans R Soc Trop Med Hyg 84 :22–28.
-
42
Gadawski RM, Smith SM, 1992. Nectar sources and age structure in a population of Aedes provocans (Diptera: Culicidae). J Med Entomol 29 :879–886.
-
43
Sheppard PM, Macdonald WW, Tonn RJ, Grab B, 1969. The dynamics of an adult population of Aedes aegypti in relation to dengue haemorrhagic fever in Bangkok. J Anim Ecol 38 :661–702.
-
44
Hay SI, Myers MF, Burke DS, Vaughn DW, Endy T, Ananda N, Shanks GD, Snow RW, Rogers DJ, 2000. Etiology of interepidemic periods of mosquito-borne disease. Proc Natl Acad Sci USA 97 :9335–9339.
-
45
Hayes EJ, Wall R, 1999. Age-grading adult insects: a review of techniques. Physiol Entomol 24 :1–10.
-
46
Desena ML, Clark JM, Edman JD, Symington SB, Scott TW, Clark GG, Peters TM, 1999. Potential for aging female Aedes aegypti (Diptera: Culicidae) by gas chromatographic analysis of cuticular hydrocarbons, including a field evaluation. J Med Entomol 36 :811–823.
-
47
Hugo LE, Kay BH, Eaglesham GK, Holling N, Ryan PA, 2006. Investigation of cuticular hydrocarbons for determining the age and survivorship of Australasian mosquitoes. Am J Trop Med Hyg 74 :462–474.
-
48
Carey JR, 2001. Insect biodemography. Annu Rev Entomol 46 :79–110.
-
49
Wang J-L, Muller H-G, Capra WB, 1998. Analysis of oldest-old mortality: Lifetables revisited. Ann Statist 26 :126–163.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 326 | 240 | 5 |
| Full Text Views | 410 | 5 | 0 |
| PDF Downloads | 108 | 5 | 0 |