Unexpected High Losses of Anopheles gambiae Larvae Due to Rainfall

Background Immature stages of the malaria mosquito Anopheles gambiae experience high mortality, but its cause is poorly understood. Here we study the impact of rainfall, one of the abiotic factors to which the immatures are frequently exposed, on their mortality. Methodology/Principal Findings We show that rainfall significantly affected larval mosquitoes by flushing them out of their aquatic habitat and killing them. Outdoor experiments under natural conditions in Kenya revealed that the additional nightly loss of larvae caused by rainfall was on average 17.5% for the youngest (L1) larvae and 4.8% for the oldest (L4) larvae; an additional 10.5% (increase from 0.9 to 11.4%) of the L1 larvae and 3.3% (from 0.1 to 3.4%) of the L4 larvae were flushed away and larval mortality increased by 6.9% (from 4.6 to 11.5%) and 1.5% (from 4.1 to 5.6%) for L1 and L4 larvae, respectively, compared to nights without rain. On rainy nights, 1.3% and 0.7% of L1 and L4 larvae, respectively, were lost due to ejection from the breeding site. Conclusions/Significance This study demonstrates that immature populations of malaria mosquitoes suffer high losses during rainfall events. As these populations are likely to experience several rain showers during their lifespan, rainfall will have a profound effect on the productivity of mosquito breeding sites and, as a result, on the transmission of malaria. These findings are discussed in the light of malaria risk and changing rainfall patterns in response to climate change.

[1]  John B. Silver,et al.  Mosquito Ecology: Field Sampling Methods , 2008 .

[2]  C. Dye,et al.  World Malaria Report, 2008. , 2008 .

[3]  A. Githeko,et al.  Interspecific variation in diving activity among Anopheles gambiae Giles, An. arabiensis Patton, and An. funestus Giles (Diptera: Culicidae) larvae , 2007, Journal of vector ecology : journal of the Society for Vector Ecology.

[4]  Jeffrey A. Shaman,et al.  Reproductive Phase Locking of Mosquito Populations in Response to Rainfall Frequency , 2007, PloS one.

[5]  H. L. Miller,et al.  Climate Change 2007: The Physical Science Basis , 2007 .

[6]  E. Walker,et al.  Life on the edge: African malaria mosquito (Anopheles gambiae s. l.) larvae are amphibious , 2007, Naturwissenschaften.

[7]  E. Walker,et al.  Pupal habitat productivity of Anopheles gambiae complex mosquitoes in a rural village in western Kenya. , 2006, The American journal of tropical medicine and hygiene.

[8]  G. R. Okogun Life-table analysis of Anopheles malaria vectors: generational mortality as tool in mosquito vector abundance and control studies. , 2005, Journal of vector borne diseases.

[9]  M. Takagi,et al.  Survivorship of Anopheles gambiae sensu stricto (Diptera: Culicidae) Larvae in Western Kenya Highland Forest , 2005, Journal of medical entomology.

[10]  Weltgesundheitsorganisation World malaria report , 2005 .

[11]  G. Killeen,et al.  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 , 2004, Tropical medicine & international health : TM & IH.

[12]  A. Githeko,et al.  Diving Ability of Anopheles gambiae (Diptera: Culicidae) Larvae , 2004, Journal of medical entomology.

[13]  S W Lindsay,et al.  Temperature‐related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory , 2004, Medical and veterinary entomology.

[14]  G. Dolo,et al.  Survivorship and Distribution of Immature Anopheles gambiae s.l. (Diptera: Culicidae) in Banambani Village, Mali , 2004, Journal of medical entomology.

[15]  W. Takken,et al.  The effects of rainfall and evapotranspiration on the temporal dynamics of Anopheles gambiae s.s. and Anopheles arabiensis in a Kenyan village. , 2004, Acta tropica.

[16]  S W Lindsay,et al.  Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae) , 2003, Bulletin of Entomological Research.

[17]  W. Takken,et al.  Egg hatching, larval movement and larval survival of the malaria vector Anopheles gambiae in desiccating habitats , 2003, Malaria Journal.

[18]  W. Takken,et al.  Cannibalism and predation among larvae of the Anopheles gambiae complex , 2003, Medical and veterinary entomology.

[19]  John E. Gimnig,et al.  Density-Dependent Development of Anopheles gambiae (Diptera: Culicidae) Larvae in Artificial Habitats , 2002, Journal of medical entomology.

[20]  Ruth M. Doherty,et al.  African climate change: 1900-2100 , 2001 .

[21]  W. Hawley,et al.  Characteristics of Larval Anopheline (Diptera: Culicidae) Habitats in Western Kenya , 2001, Journal of medical entomology.

[22]  J. Breman,et al.  The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. , 2001, The American journal of tropical medicine and hygiene.

[23]  M. Bayoh,et al.  Studies on the development and survival of Anopheles gambiae sensu stricto at various temperatures and relative humidities , 2001 .

[24]  W. Takken,et al.  Interspecific competition between sibling species larvae of Anopheles arabiensis and An. gambiae , 2000, Medical and veterinary entomology.

[25]  O. Planchon,et al.  Rainfall is not a direct mortality factor for anopheline larvae. , 1999, Parasite.

[26]  W. S. Romoser,et al.  Buoyancy and diving behavior in mosquito pupae. , 1999, Journal of the American Mosquito Control Association.

[27]  A. Haines,et al.  Climate change and human health. An assessment by a Task Group on behalf of the World Health Organization the World Meteorological Organization and the United Nations Environment Programme. , 1996 .

[28]  J. Charlwood,et al.  Polymerase chain reaction used to describe larval habitat use by Anopheles gambiae complex (Diptera: Culicidae) in the environs of Ifakara, Tanzania. , 1996, Journal of medical entomology.

[29]  Nigel E. Stork,et al.  Insects in a changing environment , 1995 .

[30]  Jan Rotmans,et al.  Climate change and vector-borne diseases. A global modelling perspective. , 1995 .

[31]  K. Lerdthusnee,et al.  Effect of mechanical shock on hydrostatic balance and survival of mosquito pupae. , 1994, Journal of the American Mosquito Control Association.

[32]  H. Briegel,et al.  Water depth and larval density affect development and accumulation of reserves in laboratory populations of mosquitoes , 1993 .

[33]  C. Mutero,et al.  Vertical Estimates of Survivorship of Larvae and Pupae of Anopheles Gambiae Giles Complex in Baringo District, Kenya , 1993 .

[34]  W. Takken,et al.  Effect of rearing temperature and larval density on larval survival, age at pupation and adult size of Anopheles gambiae , 1992 .

[35]  M. Gillies.,et al.  A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region). , 1987 .

[36]  M. Service 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. , 1977, Journal of medical entomology.

[37]  M. Service Studies on sampling larval populations of the Anopheles gambiae complex. , 1971, Bulletin of the World Health Organization.

[38]  M. Gillies.,et al.  The Anophelinae of Africa South of the Sahara , 1968 .

[39]  Practical Malariology , 1964 .

[40]  W. F. Jepson,et al.  The malaria problem in Mauritius; the bionomics of Mauritian anophelines. , 1947, Bulletin of entomological research.