Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi

Parasites and Vectors

Volumn 6, Issue 1, 2013, Pages

  Takken, Willem ^a   Smallegange, Renate C ^a,b   Vigneau, Antoine J ^c,d   Johnston, Valerie ^c   Brown, Margaret ^c,e   Mordue Luntz, A Jenny ^c   Billingsley, Peter F ^c,f  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b Current Address: Wageningen Academic Publishers   (Netherlands)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d Robert Gordon University ^*  (United Kingdom)

^e ROBERT GORDON UNIVERSITY   (United Kingdom)

^f SANARIA INC   (United States)

Author keywords

Anopheles gambiae sensu stricto; Anopheles stephensi; Blood feeding; Body size; Fitness; Mosquito; Plasmodium yoelii nigeriensis

Indexed keywords

GLYCOGEN; LIPID; PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANOPHELES GAMBIAE; ANOPHELES STEPHENSI; ARTICLE; BODY SIZE; CONTROLLED STUDY; DIET; DISSECTION; DRY WEIGHT; FEMALE; FORELIMB; GLYCOGEN ANALYSIS; GONAD DEVELOPMENT; LARVA; MIDGUT; MOUSE; NONHUMAN; NUTRITIONAL STATUS; OOCYST; OOCYTE MATURATION; OVARY DEVELOPMENT; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PARASITE TRANSMISSION; PLASMODIUM YOELII; PLASMODIUM YOELII INFECTION; PLASMODIUM YOELII NIGERIENSIS; PROTEIN ANALYSIS; PROTEIN CONTENT; REPRODUCTIVE SUCCESS; TEST MEAL;

ANOPHELES (GENUS); ANOPHELES GAMBIAE; ANOPHELES STEPHENSI; PLASMODIUM YOELII NIGERIENSIS;

ANIMAL FEED; ANIMALS; ANOPHELES; BIOMETRY; FEEDING BEHAVIOR; FEMALE; INSECT VECTORS; LARVA; MICE; PLASMODIUM YOELII;

EID: 84889837697     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-6-345     Document Type: Article

References (54)

1. Fecundity, metabolism, and body size in Anopheles (Diptera: Culicidae), Vectors of Malaria. Briegel H, J Med Entomol 1990 27 839 850 2231621
2. Effect of body size on host seeking and blood meal utilization in Anopheles gambiae sensu stricto (Diptera: Culicidae): the disadvantage of being small. Takken W, Klowden MJ, Chambers GM, J Med Entomol 1998 35 639 645 9775585 (Pubitemid 128463422)
3. Sexual selection in mosquito swarms: may the best man lose? Ng'habi KR, Huho BJ, Nkwengulila G, Killeen GF, Knols BGJ, Ferguson HM, Anim Behav 2008 76 105 112 10.1016/j.anbehav.2008.01.014
4. Interactions between parasites and insects vectors. Hurd H, Mem Inst Oswaldo Cruz 1994 89 Suppl 2 27 30 7565125
5. The recognition of age-groups within populations of Anopheles gambiae by the pre-gravid rate and the sporozoite rate. Gillies MT, Ann Trop Med Parasitol 1954 48 58 74 13149120
6. The pre-gravid phase of ovarian development in Anopheles funestus. Gillies MT, Ann Trop Med Parasit 1955 49 320 325 13259446
7. Manipulation of medically important insect vectors by their parasites. Hurd H, Annu Rev Entomol 2003 48 141 161 10.1146/annurev.ento.48.091801.112722 12414739 (Pubitemid 37365389)
8. The energetic budget of Anopheles stephensi infected with Plasmodium chabaudi: is energy depletion a mechanism for virulence? Rivero A, Ferguson HM, Proc R Soc Lond Ser B-Biol Sci 2003 270 1365 1371 10.1098/rspb.2003.2389 (Pubitemid 36831297)
9. Anopheles mortality is both age- and Plasmodium-density dependent: implications for malaria transmission. Dawes EJ, Churcher TS, Zhuang S, Sinden RE, Basáñez MF, Malar J 2009 8 228 10.1186/1475-2875-8-228 19822012
10. Interactions between bloodfeeding, fecundity and infection in mosquitoes. Hurd H, Hogg JC, Renshaw M, Parasitol Today 1995 11 411 416 10.1016/0169-4758(95)80021-2
11. The effect of Plasmodium yoelii nigeriensis infection on ovarian protein accumulation by Anopheles stephensi. Hogg JC, Carwardine S, Hurd H, Parasitol Res 1997 83 374 379 9134561 (Pubitemid 27198471)
12. Effects of adult body size on fecundity and the pregravid rate of Anopheles gambiae females in Tanzania. Lyimo EO, Takken W, Med Vet Entomol 1993 7 328 332 10.1111/j.1365-2915.1993.tb00700.x 8268486 (Pubitemid 24417692)
13. Larval habitats of Anopheles gambiae s.s. (Diptera: Culicidae) influences vector competence to Plasmodium falciparum parasites. Okech BA, Gouagna LC, Yan G, Githure JI, Beier JC, Malar J 2007 6 50 10.1186/1475-2875-6-50 17470293 (Pubitemid 46761810)
14. Rapid determination of glycogen and sugars in mosquitoes. Van Händel E, J Am Mosq Control Assoc 1985 1 299 301 2906671
15. Rapid determination of total lipids in mosquitoes. Van Händel E, J Am Mosq Control Assoc 1985 1 302 304 2906672
16. Blood digestion in the mosquito, Anopheles stephensi Liston (Diptera: Culicidae): activity and distribution of trypsin, aminopeptidase, and alpha-glucosidase in the midgut. Billingsley PF, Hecker H, J Med Entomol 1991 28 865 871 1770523
17. Detection of mature malaria infections in live mosquitoes. Billingsley PF, Hodivala KJ, Winger LA, Sinden RE, Trans R Soc Trop Med Hyg 1991 85 450 453 10.1016/0035-9203(91)90215-K 1755048
18. Sokal RR, Rohlf FJ, Biometry: the Principles and the Practice of Statistics in Biological Research New York: WH Freeman and Company 3 1998
19. Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Hogg JC, Hurd H, Med Vet Entomol 1995 9 176 180 10.1111/j.1365-2915.1995.tb00175.x 7787226
20. Relationship between prevalence and intensity of Plasmodium falciparum infection in natural populations of Anopheles mosquitos. Billingsley PF, Medley GF, Charlwood D, Sinden RE, Am J Trop Med Hyg 1994 51 260 270 7943543 (Pubitemid 24300816)
21. The development of the egg follicle in anophelines. Christophers SR, Paludism 1911 2 73 78
22. Oude Voshaar JH, Statistiek voor Onderzoekers. Met voorbeelden uit de Landbouw en Milieuwetenschappen The Netherlands: Wageningen Pers, Wageningen 1994
23. Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Medley GF, Sinden RE, Fleck S, Billingsley PF, Tirawanchai N, Rodriguez MH, Parasitology 1993 106 441 449 10.1017/S0031182000076721 8341579 (Pubitemid 23169804)
24. Nectar-related vs. human-related volatiles: behavioural response and choice by female and male Anopheles gambiae (Diptera: Culicidae) between emergence and first feeding. Foster WA, Takken W, Bull Entomol Res 2004 94 145 157 10.1079/BER2003288 15153297 (Pubitemid 38583780)
25. Cannibalism and predation among larvae of the Anopheles gambiae complex. Koenraadt CJM, Takken W, Med Vet Entomol 2003 17 61 66 10.1046/j.1365-2915.2003. 00409.x 12680927 (Pubitemid 36409130)
26. Effect of rearing temperature and larval density on larval survival, age at pupation and adult size of Anopheles gambiae. Lyimo EO, Takken W, Koella JC, Entomol Exp Appl 1992 63 265 271 10.1111/j.1570-7458.1992.tb01583.x
27. Relationship between pupal mass and adult survivorship and fecundity for Aedes aegypti. Steinwascher K, Environ Entomol 1982 11 150 153
28. Size variation and reproductive success of female Aedes punctor (Diptera: Culicidae). Packer MJ, Corbet P, Ecol Entomol 1989 14 297 309 10.1111/j.1365-2311.1989.tb00960.x (Pubitemid 20423268)
29. Survival and infection probabilities of anthropophagie anophelines from an area of high prevalence of Plasmodium falciparum in humans. Charlwood JD, Smith T, Billingsley FF, Takken W, Lyimo EOK, Meuwissen JHET, Bull Entomol Res 1997 87 445 453 10.1017/S0007485300041304 (Pubitemid 128724090)
30. Physiological bases of mosquito ecology. Briegel H, J Vector Ecol 2003 28 1 11 12831123 (Pubitemid 38994564)
31. Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? Harrington LC, Edman JD, Scott TW, J Med Entomol 2001 38 411 422 10.1603/0022-2585-38.3.411 11372967 (Pubitemid 33614607)
32. Behavioural determinants of gene flow in malaria vector populations: Anopheles gambiae males select large females as mates. Okanda FM, Dao A, Njiru BN, Arija J, Akelo HA, Toure Y, Odulaja A, Beier JC, Githure JI, Yan G, et al. Malar J 2002 1 10 10.1186/1475-2875-1-10 12296972
33. Factors associated with male mating success of the dengue vector mosquito, Aedes aegypti. Ponlawat A, Harrington LC, Am J Trop Med Hyg 2009 80 395 400 19270288
34. High heterogeneity in the number of Plasmodium falciparum gametocytes in the bloodmeal of mosquitoes fed on the same host. Pichon G, Awono-Ambene HP, Robert V, Parasitology 2000 121 115 120 10.1017/S0031182099006277 11085230
35. Relationship between body size of adult Anopheles gambiae s.l. and infection with malaria parasite Plasmodium falciparum. Lyimo EO, Koella JC, Parasitology 1992 104 233 237 10.1017/S0031182000061667 1594289 (Pubitemid 23400900)
36. Plasmodium-mosquito interactions: a tale of dangerous liaisons. Barillas Mury C, Kumar S, Cell Microbiol 2005 7 1539 1545 10.1111/j.1462-5822.2005.00615. x 16207241 (Pubitemid 41511911)
37. The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, Fowler K, Billker O, Franke-Fayard B, Janse CJ, Waters A, et al. Int J Parasit 2003 33 933 943 10.1016/S0020-7519(03)00112-7 (Pubitemid 37297460)
38. Corrigendum to: the dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti (vol 33, pg 933, 2003). Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, Fowler K, Billker O, Franke-Fayard B, Janse CJ, Waters A, et al. Int J Parasit 2004 34 245 247 10.1016/j.ijpara.2003.05.001 (Pubitemid 38229828)
39. Mosquito immune defenses against Plasmodium infection. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G, Dev Comp Immunol 2010 34 387 395 10.1016/j.dci.2009.12.005 20026176
40. Innate immune defense against malaria infection in the mosquito. Dimopoulos G, Muller HM, Levashina EA, Kafatos FC, Curr Opin Immunol 2001 13 79 88 10.1016/S0952-7915(00)00186-2 11154922 (Pubitemid 32096965)
41. Conserved mosquito/parasite interactions affect development of Plasmodium falciparum in Africa. Mendes AM, Schlegelmilch T, Cohuet A, Awono-Ambene P, De Iorio M, Fontenille D, Morlais I, Christophides GK, Kafatos FC, Vlachou D, PLoS Path 2008 4 1000069 10.1371/journal.ppat.1000069 (Pubitemid 351811529)
42. Immunity-related genes and gene families in Anopheles gambiae. Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, et al. Science 2002 298 159 165 10.1126/science.1077136 12364793
43. Plasmodium development in the mosquito: biology bottlenecks and opportunities for mathematical modeling. Drexler AL, Vodovotz Y, Luckhart S, Trends Parasitol 2008 24 333 336 10.1016/j.pt.2008.05.005 18603475
44. Environmental influence on the genetic basis of mosquito resistance to malaria parasites. Lambrechts L, Chavatte JM, Snounou G, Koella JC, P Roy Soc B-Biol Sci 2006 273 1501 1506 10.1098/rspb.2006.3483 (Pubitemid 47308738)
45. Reproductive success in Anopheles arabiensis and the M and S molecular forms of Anopheles gambiae: do natural sporozoite infection and body size matter? Yaro AS, Toure AM, Guindo A, Coulibaly MB, Dao A, Diallo M, Traore SF, Acta Trop 2012 122 87 93 10.1016/j.actatropica.2011.12.005 22198241
46. The effects of infection with Plasmodium yoelii nigeriensis on the reproductive fitness of the mosquito Anopheles gambiae. Ahmed AM, Maingon RD, Taylor PJ, Hurd H, Invertebr Reprod Dev 1999 36 217 222 10.1080/07924259.1999. 9652703 (Pubitemid 29407590)
47. Infection rates in, and the number of Plasmodium falciparum genotypes carried by Anopheles mosquitoes in Tanzania. Taylor LH, Ann Trop Med Parasitol 1999 93 659 662 10.1080/00034989958168 10707111 (Pubitemid 29438136)
48. A quantitative study of naturally-acquired malaria infections in Anopheles gambiae and Anopheles funestus in a highly malarious area of East Africa. Pringle G, Trans R Soc Trop Med Hyg 1966 60 626 632 10.1016/0035- 9203(66)90009-5 6006329
49. Absence of relationships between selected human factors and natural infectivity of Plasmodium falciparum to mosquitoes in an area of high transmission. Haji H, Smith T, Charlwood JD, Meuwissen JH, Parasitology 1996 113 425 431 10.1017/S0031182000081488 8893528 (Pubitemid 26354536)
50. Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. Hopwood JA, Ahmed AM, Polwart A, Williams GT, Hurd H, J Exp Biol 2001 204 2773 2780 11683433 (Pubitemid 34861387)
51. Why is the effect of malaria parasites on mosquito survival still unresolved? Ferguson HM, Read AF, Trends Parasitol 2002 18 256 260 10.1016/S1471-4922(02)02281-X 12036738 (Pubitemid 34569235)
52. Effects of sugar availability on the blood-feeding behavior of Anopheles gambiae (Diptera: Culicidae). Straif SC, Beier JC, J Med Entomol 1996 33 608 612 8699455 (Pubitemid 126429423)
53. Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in western Kenya. Okech BA, Gouagna LC, Killeen GF, Knols BG, Kabiru EW, Beier JC, Yan G, Githure JI, J Med Entomol 2003 40 657 663 10.1603/0022-2585-40.5.657 14596279 (Pubitemid 37399538)
54. Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. Anderson RA, Knols BG, Koella JC, Parasitology 2000 120 329 333 10.1017/S0031182099005570 10811273 (Pubitemid 30204302)