Anopheline Larval Habitats Seasonality and Species Distribution: A Prerequisite for Effective Targeted Larval Habitats Control Programmes

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Kweka, Eliningaya J ^a,b,d   Zhou, Guofa ^c   Munga, Stephen ^a   Lee, Ming Chieh ^c   Atieli, Harrysone E ^a   Nyindo, Mramba ^b   Githeko, Andrew K ^a   Yan, Guiyun ^c  

^a KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^b KILIMANJARO CHRISTIAN MEDICAL UNIVERSITY COLLEGE   (Tanzania)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TROPICAL PESTICIDES RESEARCH INSTITUTE   (Tanzania)

Author keywords

[No Author keywords available]

Indexed keywords

FERTILIZER; GOLD;

AGRICULTURAL LAND; ANOPHELES; ANOPHELES ARABIENSIS; ANOPHELES GAMBIAE; ARTHROPOD LARVA; ARTICLE; BIODIVERSITY; DISEASE CARRIER; GEOGRAPHIC DISTRIBUTION; GRASS; HABITAT; INSECT CONTROL; KENYA; LAND USE; MINING; NONHUMAN; PASTURELAND; PHYSICAL PARAMETERS; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; PREDATOR; SEASONAL VARIATION; SPECIES DISTRIBUTION; SWAMP;

ANIMALS; ANOPHELES; ECOSYSTEM; ENVIRONMENT; HUMANS; KENYA; LARVA; MALARIA; MOSQUITO CONTROL; PLANTS; POPULATION DYNAMICS; SEASONS;

EID: 84871288440     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052084     Document Type: Article

References (74)

1. Afrane YA, Lawson BW, Githeko AK, Yan G, (2005) Effects of microclimatic changes caused by land use and land cover on duration of gonotrophic cycles of Anopheles gambiae (Diptera: Culicidae) in western Kenya highlands. J Med Entomol 42: 974-980.
2. Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G, (2006) Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in western Kenya highlands. Am J Trop Med Hyg 74: 772-778.
3. Balls MJ, Bodker R, Thomas CJ, Kisinza W, Msangeni HA, et al. (2004) Effect of topography on the risk of malaria infection in the Usambara Mountains, Tanzania. Trans R Soc Trop Med Hyg 98: 400-408.
4. Bodker R, Akida J, Shayo D, Kisinza W, Msangeni HA, et al. (2003) Relationship between altitude and intensity of malaria transmission in the Usambara Mountains, Tanzania. J Med Entomol 40: 706-717.
5. Bodker R, Msangeni HA, Kisinza W, Lindsay SW, (2006) Relationship between the intensity of exposure to malaria parasites and infection in the Usambara Mountains, Tanzania. Am J Trop Med Hyg 74: 716-723.
6. Githeko AK, Ndegwa W (2001) Predicting malaria epidemics in the Kenyan highlands using climate data: a tool for decision makers. Global Change & Human Health 2 54-63.
7. Kweka EJ, Zhou G, Lee MC, Gilbreath TM, 3rd, Mosha F, et al (2011) Evaluation of two methods of estimating larval habitat productivity in western Kenya highlands. Parasit Vectors 4: 110.
8. Lindsay SW, Bødker R, Malima R, Msangeni HA, Kisinza W, (2000) Effect of 1997?98 EI Niño on highland malaria in Tanzania. The Lancet 355: 989-990.
9. Githeko AK, Ayisi JM, Odada PK, Atieli FK, Ndenga BA, et al. (2006) Topography and malaria transmission heterogeneity in western Kenya highlands: prospects for focal vector control. Malar J 5: 107.
10. Minakawa N, Omukunda E, Zhou G, Githeko A, Yan G, (2006) Malaria vector productivity in relation to the highland environment in Kenya. Am J Trop Med Hyg 75: 448-453.
11. Minakawa N, Sonye G, Mogi M, Githeko A, Yan G, (2002) The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. J Med Entomol 39: 833-841.
12. Munga S, Minakawa N, Zhou G, Githeko AK, Yan G, (2007) Survivorship of immature stages of Anopheles gambiae s.l. (Diptera: Culicidae) in natural habitats in western Kenya highlands. J Med Entomol 44: 758-764.
13. Munga S, Minakawa N, Zhou G, Mushinzimana E, Barrack OO, et al. (2006) Association between land cover and habitat productivity of malaria vectors in western Kenyan highlands. Am J Trop Med Hyg 74: 69-75.
14. Munga S, Yakob L, Mushinzimana E, Zhou G, Ouna T, et al. (2009) Land use and land cover changes and spatiotemporal dynamics of anopheline larval habitats during a four-year period in a highland community of Africa. Am J Trop Med Hyg 81: 1079-1084.
15. Mutuku FM, Bayoh MN, Gimnig JE, Vulule JM, Kamau L, et al. (2006) Pupal habitat productivity of Anopheles gambiae complex mosquitoes in a rural village in western Kenya. Am J Trop Med Hyg 74: 54-61.
16. Yasuoka J, Levins R, (2007) Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Am J Trop Med Hyg 76: 450-460.
17. Khaemba BM, Mutani A, Bett MK, (1994) Studies of anopheline mosquitoes transmitting malaria in a newly developed highland urban area: a case study of Moi University and its environs. East Afr Med J 71: 159-164.
18. Ndenga B, Githeko A, Omukunda E, Munyekenye G, Atieli H, et al. (2006) Population dynamics of malaria vectors in western Kenya highlands. J Med Entomol 43: 200-206.
19. Ndenga BA, Simbauni JA, Mbugi JP, Githeko AK, Fillinger U, (2011) Productivity of malaria vectors from different habitat types in the western Kenya highlands. PLoS One 6: e19473.
20. Shililu JI, Maier WA, Seitz HM, Orago AS, (1998) Seasonal density, sporozoite rates and entomological inoculation rates of Anopheles gambiae and Anopheles funestus in a high-altitude sugarcane growing zone in Western Kenya. Trop Med Int Health 3: 706-710.
21. Chuma J, Okungu V, Molyneux C, (2010) Barriers to prompt and effective malaria treatment among the poorest population in Kenya. Malar J 9: 144.
22. Greenwood B, Mutabingwa T, (2002) Malaria in 2002. Nature 415: 670-672.
23. Yakob L, Yan G, (2009) Modeling the effects of integrating larval habitat source reduction and insecticide treated nets for malaria control. PLoS One 4: e6921.
24. Zhou G, Githeko AK, Minakawa N, Yan G, (2010) Community-wide benefits of targeted indoor residual spray for malaria control in the western Kenya highland. Malar J 9: 67.
25. Wanjala CL, Waitumbi J, Zhou G, Githeko AK, (2011) Identification of malaria transmission and epidemic hotspots in the western Kenya highlands: its application to malaria epidemic prediction. Parasit Vectors 4: 81.
26. Kebede A, McCann JC, Kiszewski AE, Ye-Ebiyo Y, (2005) New evidence of the effects of agro-ecologic change on malaria transmission. Am J Trop Med Hyg 73: 676-680.
27. Ye-Ebiyo Y, Pollack RJ, Kiszewski A, Spielman A, (2003) A component of maize pollen that stimulates larval mosquitoes (Diptera: Culicidae) to feed and increases toxicity of microbial larvicides. J Med Entomol 40: 860-864.
28. Ye-Ebiyo Y, Pollack RJ, Kiszewski A, Spielman A, (2003) Enhancement of development of larval Anopheles arabiensis by proximity to flowering maize (Zea mays) in turbid water and when crowded. Am J Trop Med Hyg 68: 748-752.
29. Ye-Ebiyo Y, Pollack RJ, Spielman A, (2000) Enhanced development in nature of larval Anopheles arabiensis mosquitoes feeding on maize pollen. Am J Trop Med Hyg 63: 90-93.
30. Fillinger U, Sonye G, Killeen GF, Knols BG, Becker N, (2004) The practical importance of permanent and semipermanent habitats for controlling aquatic stages of Anopheles gambiae sensu lato mosquitoes: operational observations from a rural town in western Kenya. Trop Med Int Health 9: 1274-1289.
31. Fillinger U, Ndenga B, Githeko A, Lindsay SW, (2009) Integrated malaria vector control with microbial larvicides and insecticide-treated nets in western Kenya: a controlled trial. Bull World Health Organ 87: 655-665.
32. Fillinger U, Lindsay SW, (2006) Suppression of exposure to malaria vectors by an order of magnitude using microbial larvicides in rural Kenya. Trop Med Int Health 11: 1629-1642.
33. Shililu J, Mbogo C, Ghebremeskel T, Githure J, Novak R, (2007) Mosquito larval habitats in a semiarid ecosystem in Eritrea: impact of larval habitat management on Anopheles arabiensis population. Am J Trop Med Hyg 76: 103-110.
34. Mutuku FM, Bayoh MN, Hightower AW, Vulule JM, Gimnig JE, et al. (2009) A supervised land cover classification of a western Kenya lowland endemic for human malaria: associations of land cover with larval Anopheles habitats. Int J Health Geogr 8: 19.
35. Himeidan YE, Zhou G, Yakob L, Afrane Y, Munga S, et al. (2009) Habitat stability and occurrences of malaria vector larvae in western Kenya highlands. Malar J 8: 234.
36. Gillies TM, Coetzee M (1987) Supplement of the Anopheles of Africa South of Sahara (Afrotropical Region). Johannesburg, Republic of South Africa Publication of The S. Afr. Insti. Med Research.
37. Scott JA, Brogdon WG, Collins FH, (1993) Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49: 520-529.
38. Alatalo R, Alatalo R, (1977) Components of Diversity: Multivariate Analysis with Interaction. Ecology 58: 900-906.
39. Norris JL, Pollock KH, (1998) Non-parametric MLE for Poisson species abundance models allowing for heterogeneity between species. Environmental and Ecological Statistics 5: 391-402.
40. Chaki PP, Govella NJ, Shoo B, Hemed A, Tanner M, et al. (2009) Achieving high coverage of larval-stage mosquito surveillance: challenges for a community-based mosquito control programme in urban Dar es Salaam, Tanzania. Malar J 8: 311.
41. Geissbuhler Y, Kannady K, Chaki PP, Emidi B, Govella NJ, et al. (2009) Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in urban Dar es Salaam, Tanzania. PLoS One 4: e5107.
42. Mwangangi JM, Shililu J, Muturi EJ, Muriu S, Jacob B, et al. (2010) Anopheles larval abundance and diversity in three rice agro-village complexes Mwea irrigation scheme, central Kenya. Malar J 9: 228.
43. Minakawa N, Sonye G, Mogi M, Yan G, (2004) Habitat characteristics of Anopheles gambiae s.s. larvae in a Kenyan highland. Med Vet Entomol 18: 301-305.
44. Minakawa N, Sonye G, Yan G, (2005) Relationships between occurrence of Anopheles gambiae s.l. (Diptera: Culicidae) and size and stability of larval habitats. J Med Entomol 42: 295-300.
45. Munga S, Minakawa N, Zhou G, Barrack OO, Githeko AK, et al. (2005) Oviposition site preference and egg hatchability of Anopheles gambiae: effects of land cover types. J Med Entomol 42: 993-997.
46. Tuno N, Okeka W, Minakawa N, Takagi M, Yan G, (2005) Survivorship of Anopheles gambiae sensu stricto (Diptera: Culicidae) larvae in western Kenya highland forest. J Med Entomol 42: 270-277.
47. Palmquist KR, Jepson PC, Jenkins JJ, (2008) Impact of aquatic insect life stage and emergence strategy on sensitivity to esfenvalerate exposure. Environmental Toxicology and Chemistry 27: 1728-1734.
48. Gimnig JE, Ombok M, Kamau L, Hawley WA, (2001) Characteristics of larval anopheline (Diptera: Culicidae) habitats in Western Kenya. J Med Entomol 38: 282-288.
49. Mutero CM, Ng'ang'a PN, Wekoyela P, Githure J, Konradsen F, (2004) Ammonium sulphate fertiliser increases larval populations of Anopheles arabiensis and culicine mosquitoes in rice fields. Acta Trop 89: 187-192.
50. Victor TJ, Reuben R, (2000) Effects of organic and inorganic fertilisers on mosquito populations in rice fields of southern India. Med Vet Entomol 14: 361-368.
51. Muturi EJ, Mwangangi J, Shililu J, Muriu S, Jacob B, et al. (2007) Mosquito species succession and physico-chemical factors affecting their abundance in rice fields in Mwea, Kenya. J Med Entomol 44: 336-344.
52. Mwangangi J, Shililu J, Muturi E, Gu W, Mbogo C, et al. (2006) Dynamics of immature stages of Anopheles arabiensis and other mosquito species (Diptera: Culicidae) in relation to rice cropping in a rice agro-ecosystem in Kenya. J Vector Ecol 31: 245-251.
53. Mwangangi JM, Muturi EJ, Shililu J, Muriu SM, Jacob B, et al. (2006) Survival of immature Anopheles arabiensis (Diptera: Culicidae) in aquatic habitats in Mwea rice irrigation scheme, central Kenya. Malar J 5: 114.
54. Blaustein L, Chase JM, (2007) Interactions between mosquito larvae and species that share the same trophic level. Annu Rev Entomol 52: 489-507.
55. McCrae AW, (1984) 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 78: 307-318.
56. Minakawa N, Mutero CM, Githure JI, Beier JC, Yan G, (1999) Spatial distribution and habitat characterization of anopheline mosquito larvae in Western Kenya. Am J Trop Med Hyg 61: 1010-1016.
57. Paaijmans KP, Takken W, Githeko AK, Jacobs AF, (2008) The effect of water turbidity on the near-surface water temperature of larval habitats of the malaria mosquito Anopheles gambiae. Int J Biometeorol 52: 747-753.
58. Shililu J, Ghebremeskel T, Seulu F, Mengistu S, Fekadu H, et al. (2003) Larval habitat diversity and ecology of anopheline larvae in Eritrea. J Med Entomol 40: 921-929.
59. Gimnig JE, Ombok M, Otieno S, Kaufman MG, Vulule JM, et al. (2002) Density-dependent development of Anopheles gambiae (Diptera: Culicidae) larvae in artificial habitats. J Med Entomol 39: 162-172.
60. 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.
61. Mala AO, Irungu LW, Shililu JI, Muturi EJ, Mbogo CC, et al. (2011) Dry season ecology of Anopheles gambiae complex mosquitoes at larval habitats in two traditionally semi-arid villages in Baringo, Kenya. Parasit Vectors 4: 25.
62. Paaijmans KP, Wandago MO, Githeko AK, Takken W, (2007) Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS One 2: e1146.
63. Wellborn G, Skelly D, Werner E, (1996) Mechanisms creating community structure across a freshwater habitat gradient. Ann rev ecology and systematics 27: 337-363.
64. Coetzee M, Craig M, le Sueur D, (2000) Distribution of African malaria mosquitoes belonging to the Anopheles gambiae complex. Parasitol Today 16: 74-77.
65. Minakawa N, Seda P, Yan G, (2002) Influence of host and larval habitat distribution on the abundance of African malaria vectors in western Kenya. Am J Trop Med Hyg 67: 32-38.
66. Mutero CM, Blank H, Konradsen F, van der Hoek W, (2000) Water management for controlling the breeding of Anopheles mosquitoes in rice irrigation schemes in Kenya. Acta Trop 76: 253-263.
67. Kweka EJ, Zhou G, Gilbreath TM 3rd, Afrane Y, Nyindo M, et al (2011) Predation efficiency of Anopheles gambiae larvae by aquatic predators in western Kenya highlands. Parasit Vectors 4: 128.
68. Munga S, Minakawa N, Zhou G, Barrack OO, Githeko AK, et al. (2006) Effects of larval competitors and predators on oviposition site selection of Anopheles gambiae sensu stricto. J Med Entomol 43: 221-224.
69. Service MW (1977) 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 13: 535-545.
70. Silberbush A, Markman S, Lewinsohn E, Bar E, Cohen JE, et al. (2010) Predator-released hydrocarbons repel oviposition by a mosquito. Ecol Lett 13: 1129-1138.
71. Mwingira VS, Mayala BK, Senkoro KP, Rumisha SF, Shayo EH, et al. (2009) Mosquito larval productivity in rice-fields infested with Azolla in Mvomero District, Tanzania. Tanzan J Health Res 11: 17-22.
72. Rajendran R, Reuben R, (1991) Evaluation of the water fern Azolla microphylla for mosquito population management in the rice-land agro-ecosystem of south India. Med Vet Entomol 5: 299-310.
73. Baolin L, (1998) The effect of Azolla on mosquito breeding. Parsitol Today 4: 328-329.
74. Mogi M, Okazawa T, Miyagi I, Sucharit S, Tumrasvin W, et al. (1986) Development and survival of anopheline immatures (Diptera: Culicidae) in rice fields in northern Thailand. J Med Entomol 23: 244-250.