Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Anopheles farauti is a homogeneous population that blood feeds early and outdoors in the Solomon Islands

Authors: Tanya L. Russell, Nigel W. Beebe, Hugo Bugoro, Allan Apairamo, Frank H. Collins, Robert D. Cooper, Neil F. Lobo, Thomas R. Burkot

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

In the 1970s, Anopheles farauti in the Solomon Island responded to indoor residual spraying with DDT by increasingly feeding more outdoors and earlier in the evening. Although long-lasting insecticidal nets (LLINs) are now the primary malaria vector control intervention in the Solomon Islands, only a small proportion of An. farauti still seek blood meals indoors and late at night where they are vulnerable to being killed by contract with the insecticides in LLINs. The effectiveness of LLINs and indoor residual spraying (IRS) in controlling malaria transmission where the vectors are exophagic and early biting will depend on whether the predominant outdoor or early biting phenotypes are associated with a subpopulation of the vectors present.

Methods

Mark-release-recapture experiments were conducted in the Solomon Islands to determine if individual An. farauti repeat the same behaviours over successive feeding cycles. The two behavioural phenotypes examined were those on which the WHO recommended malaria vector control strategies, LLINs and IRS, depend: indoor and late night biting.

Results

Evidence was found for An. farauti being a single population regarding time (early evening or late night) and location (indoor or outdoor) of blood feeding. Individual An. farauti did not consistently repeat behavioural phenotypes expressed for blood feeding (e.g., while most mosquitoes that fed early and outdoors, and would repeat those behaviours, some fed late at night or indoors in the next feeding cycle).

Conclusions

The finding that An. farauti is a homogeneous population is significant, because during the multiple feeding cycles required to complete the extrinsic incubation period, many individual female anophelines will enter houses late at night and be exposed to the insecticides used in LLINs or IRS. This explains, in part, the control that LLINs and IRS have exerted against a predominantly outdoor feeding vector, such as An. farauti. These findings may be relevant to many of the outdoor feeding vectors that dominate transmission in much of the malaria endemic world and justifies continued use of LLINs. However, the population-level tendency of mosquitoes to feed outdoors and early in the evening does require complementary interventions to accelerate malaria control towards elimination.
Literature
2.
go back to reference Hoffman AA, Hercus MJ. Environmental stress as an evolutionary force. Bioscience. 2000;50:217–26.CrossRef Hoffman AA, Hercus MJ. Environmental stress as an evolutionary force. Bioscience. 2000;50:217–26.CrossRef
3.
go back to reference Candolin U, Wong BB. Behavioural responses to a changing world: mechanisms and consequences. Oxford: Oxford University Press; 2012.CrossRef Candolin U, Wong BB. Behavioural responses to a changing world: mechanisms and consequences. Oxford: Oxford University Press; 2012.CrossRef
5.
go back to reference Elliott R. The influence of vector behaviour on malaria transmission. Am J Trop Med Hyg. 1972;21:755–63.PubMed Elliott R. The influence of vector behaviour on malaria transmission. Am J Trop Med Hyg. 1972;21:755–63.PubMed
6.
go back to reference Hamon J, Mouchet J, Brengues J, Chauvet G. Problems facing Anopheline vector control. Vector ecology and behaviour before, during, and after application of control measures. Misc Publ Entomol Soc Am. 1970;7:28–44. Hamon J, Mouchet J, Brengues J, Chauvet G. Problems facing Anopheline vector control. Vector ecology and behaviour before, during, and after application of control measures. Misc Publ Entomol Soc Am. 1970;7:28–44.
7.
go back to reference Mattingly PF. Mosquito behaviour in relation to disease eradication programmes. Annu Rev Entomol. 1962;7:419–36.CrossRefPubMed Mattingly PF. Mosquito behaviour in relation to disease eradication programmes. Annu Rev Entomol. 1962;7:419–36.CrossRefPubMed
8.
go back to reference Slooff R. Observations on the effect of residual DDT house spraying on behaviour and mortality in species of the Anopheles punctulatus group. Final report on a research project in West New Guinea [PhD Thesis]. Leyden: University of Leyden; 1964. Slooff R. Observations on the effect of residual DDT house spraying on behaviour and mortality in species of the Anopheles punctulatus group. Final report on a research project in West New Guinea [PhD Thesis]. Leyden: University of Leyden; 1964.
9.
go back to reference Thevasagayam ES. Malaria control strategies in the Southwest Pacific countries-reappraisal. Kuala Lumpur: World Health Organization; 1983. Thevasagayam ES. Malaria control strategies in the Southwest Pacific countries-reappraisal. Kuala Lumpur: World Health Organization; 1983.
10.
go back to reference Sundararaman S. The behaviour of A. sundaicus Rodenwaldt in relation to the application of residual insecticides in Tjilatjap, Indonesia. Indian J Malariol. 1958;12:129–56.PubMed Sundararaman S. The behaviour of A. sundaicus Rodenwaldt in relation to the application of residual insecticides in Tjilatjap, Indonesia. Indian J Malariol. 1958;12:129–56.PubMed
11.
go back to reference de Zulueta J, Garrett-Jones C. An investigation of the persistence of malaria transmission in Mexico. Geneva: World Health Organization; 1963. de Zulueta J, Garrett-Jones C. An investigation of the persistence of malaria transmission in Mexico. Geneva: World Health Organization; 1963.
12.
go back to reference Martinez-Palomo A, de Zulueta J. Ethological changes in Anopheles pseudopunctipennis in Mexico after prolonged use of DDT. Geneva: World Health Organization; 1964. Martinez-Palomo A, de Zulueta J. Ethological changes in Anopheles pseudopunctipennis in Mexico after prolonged use of DDT. Geneva: World Health Organization; 1964.
13.
go back to reference Trapido H. Modified response of Anopheles albimanus to DDT residual house spraying in Panama. Am J Trop Med Hyg. 1952;1:853–61.PubMed Trapido H. Modified response of Anopheles albimanus to DDT residual house spraying in Panama. Am J Trop Med Hyg. 1952;1:853–61.PubMed
16.
go back to reference Gimonneau G, Bouyer J, Morand S, Besansky NJ, Diabate A, Simard F. A behavioral mechanism underlying ecological divergence in the malaria mosquito Anopheles gambiae. Behavioral Ecol. 2010;21:1087–92. doi:10.1093/beheco/arq114.CrossRef Gimonneau G, Bouyer J, Morand S, Besansky NJ, Diabate A, Simard F. A behavioral mechanism underlying ecological divergence in the malaria mosquito Anopheles gambiae. Behavioral Ecol. 2010;21:1087–92. doi:10.​1093/​beheco/​arq114.CrossRef
17.
go back to reference Coluzzi M, Sabatini A, Petrarca V, Di Deco MA. Behavioural divergences between mosquitoes with different inversion karyotypes in polymorphic populations of the Anopheles gambiae complex. Nature. 1977;266:832–3. doi:10.1038/266832a0.CrossRefPubMed Coluzzi M, Sabatini A, Petrarca V, Di Deco MA. Behavioural divergences between mosquitoes with different inversion karyotypes in polymorphic populations of the Anopheles gambiae complex. Nature. 1977;266:832–3. doi:10.​1038/​266832a0.CrossRefPubMed
19.
go back to reference Bugoro H, Iro’ofa C, Mackenzie D, Apairamo A, Hevalao W, Corcoran S, et al. Changes in vector species composition and current vector biology and behaviour will favour malaria elimination in Santa Isabel Province, Solomon Islands. Malar J. 2011;10:287. doi:10.1186/1475-2875-10-287.CrossRefPubMedPubMedCentral Bugoro H, Iro’ofa C, Mackenzie D, Apairamo A, Hevalao W, Corcoran S, et al. Changes in vector species composition and current vector biology and behaviour will favour malaria elimination in Santa Isabel Province, Solomon Islands. Malar J. 2011;10:287. doi:10.​1186/​1475-2875-10-287.CrossRefPubMedPubMedCentral
23.
go back to reference Russell TL, Beebe NW, Bugoro H, Apairamo A, Chow W, Cooper RD et al. Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors. Malar J. 2016. doi:10.1186/s12936-016-1195-8. Russell TL, Beebe NW, Bugoro H, Apairamo A, Chow W, Cooper RD et al. Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors. Malar J. 2016. doi:10.​1186/​s12936-016-1195-8.
24.
go back to reference Brookfield HC, Hart D. Rainfall in the tropical southwest Pacific. Canberra: Department of Geography, Publ G/3, The Australian National University; 1966. Brookfield HC, Hart D. Rainfall in the tropical southwest Pacific. Canberra: Department of Geography, Publ G/3, The Australian National University; 1966.
26.
go back to reference Belkin JN. The mosquitoes of the South Pacific (Diptera, Culicidae). Berkeley and Los Angeles: University of California Press; 1962. Belkin JN. The mosquitoes of the South Pacific (Diptera, Culicidae). Berkeley and Los Angeles: University of California Press; 1962.
27.
go back to reference Beebe NW, Saul A. Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction—restriction fragment length polymorphism analysis. Am J Trop Med Hyg. 1995;53:478–81.PubMed Beebe NW, Saul A. Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction—restriction fragment length polymorphism analysis. Am J Trop Med Hyg. 1995;53:478–81.PubMed
28.
go back to reference Russell TL, Beebe NW, Bugoro H, Apairamo A, Cooper RD, Lobo NF et al. Dataset for mark-release-recapture experiments detailing the place and time of feeding by Anopheles farauti in Haleta village, Solomon Islands. James Cook University Tropical Data Hub; 2016. doi:10.4225/28/56BD124CC9260. Russell TL, Beebe NW, Bugoro H, Apairamo A, Cooper RD, Lobo NF et al. Dataset for mark-release-recapture experiments detailing the place and time of feeding by Anopheles farauti in Haleta village, Solomon Islands. James Cook University Tropical Data Hub; 2016. doi:10.​4225/​28/​56BD124CC9260.
29.
go back to reference R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2013. R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2013.
30.
go back to reference Taylor B. Changes in the feeding behaviour of a malaria vector, Anopheles farauti Lav., following the use of DDT as a residual spray in houses in the British Solomon Islands Protectorate. Trans R Entomol Soc London. 1975;127:227–92. Taylor B. Changes in the feeding behaviour of a malaria vector, Anopheles farauti Lav., following the use of DDT as a residual spray in houses in the British Solomon Islands Protectorate. Trans R Entomol Soc London. 1975;127:227–92.
31.
go back to reference Paik Y-H, Avery JG. Problem areas in the malaria eradication programme in the British Solomon Islands. P N G Med J. 1973;17:61–7. Paik Y-H, Avery JG. Problem areas in the malaria eradication programme in the British Solomon Islands. P N G Med J. 1973;17:61–7.
32.
go back to reference Charlwood JD, Graves PM, Birley MH. Capture-recapture studies with mosquitos of the group of Anopheles punctulatus Dönitz (Diptera, Culicidae) from Papua New Guinea. Bull Entomol Res. 1986;76:211–27. doi:10.1017/S000748530001470X.CrossRef Charlwood JD, Graves PM, Birley MH. Capture-recapture studies with mosquitos of the group of Anopheles punctulatus Dönitz (Diptera, Culicidae) from Papua New Guinea. Bull Entomol Res. 1986;76:211–27. doi:10.​1017/​S000748530001470​X.CrossRef
33.
go back to reference Hii JLK. Antimalaria program. WHO assignment report. (WP)MAL/SOL/MAL/001-E. Honiara: WHO Regional Office for the Western Pacific; 1988. Hii JLK. Antimalaria program. WHO assignment report. (WP)MAL/SOL/MAL/001-E. Honiara: WHO Regional Office for the Western Pacific; 1988.
34.
go back to reference Charlwood JD, Graves PM. The effect of permethrin-impregnated bednets on a population of Anopheles farauti in coastal Papua New Guinea. Med Vet Entomol. 1987;1:319–27.CrossRefPubMed Charlwood JD, Graves PM. The effect of permethrin-impregnated bednets on a population of Anopheles farauti in coastal Papua New Guinea. Med Vet Entomol. 1987;1:319–27.CrossRefPubMed
36.
go back to reference Chiang GL, Loong KP, Chan ST, Eng KL, Yap HH. Capture-recapture studies with Anopheles maculatus Theobald (Diptera: Culicidae) the vector of malaria in peninsular Malaysia. Southeast Asian J Trop Med Public Health. 1991;22:643–7.PubMed Chiang GL, Loong KP, Chan ST, Eng KL, Yap HH. Capture-recapture studies with Anopheles maculatus Theobald (Diptera: Culicidae) the vector of malaria in peninsular Malaysia. Southeast Asian J Trop Med Public Health. 1991;22:643–7.PubMed
37.
go back to reference Hii JL. Evidence for the existence of genetic variability in the tendency of Anopheles balabacensis to rest in houses and to bite man. Southeast Asian J Trop Med Public Health. 1985;16:173–82.PubMed Hii JL. Evidence for the existence of genetic variability in the tendency of Anopheles balabacensis to rest in houses and to bite man. Southeast Asian J Trop Med Public Health. 1985;16:173–82.PubMed
38.
go back to reference Hii JL, Chew M, Sang VY, Munstermann LE, Tan SG, Panyim S, et al. Population genetic analysis of host seeking and resting behaviors in the malaria vector, Anopheles balabacensis (Diptera: Culicidae). J Med Entomol. 1991;28:675–84.CrossRefPubMed Hii JL, Chew M, Sang VY, Munstermann LE, Tan SG, Panyim S, et al. Population genetic analysis of host seeking and resting behaviors in the malaria vector, Anopheles balabacensis (Diptera: Culicidae). J Med Entomol. 1991;28:675–84.CrossRefPubMed
39.
40.
go back to reference Moiroux N, Gomez MB, Pennetier C, Elanga E, Djènontin A, Chandre F, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206:1622–9. doi:10.1093/infdis/jis565.CrossRefPubMed Moiroux N, Gomez MB, Pennetier C, Elanga E, Djènontin A, Chandre F, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206:1622–9. doi:10.​1093/​infdis/​jis565.CrossRefPubMed
Metadata
Title
Anopheles farauti is a homogeneous population that blood feeds early and outdoors in the Solomon Islands
Authors
Tanya L. Russell
Nigel W. Beebe
Hugo Bugoro
Allan Apairamo
Frank H. Collins
Robert D. Cooper
Neil F. Lobo
Thomas R. Burkot
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1194-9

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue