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Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Shady business: understanding the spatial ecology of exophilic Anopheles mosquitoes

Authors: Yared Debebe, Sharon R. Hill, Habte Tekie, Rickard Ignell, Richard J. Hopkins

Published in: Malaria Journal | Issue 1/2018

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Abstract

Background

Understanding the ecology of exophilic anophelines is a key step toward developing outdoor control strategies to complement existing indoor control tools against malaria vectors. This study was conducted to assess the movement pattern of exophilic Anopheles mosquitoes between blood meal sources and resting habitats, and the landscape factors dictating their resting habitat choice.

Results

Resting clay pots were placed at 5 m, 25 m, 50 m, 75 m and 100 m away from isolated focal houses, radiating from them in four directions. The locations of the clay pots represent heterogeneous land cover types at a relatively fine spatial scale in the landscape. The effect of the landscape characters on the number of both female and male anophelines caught was modelled using zero-inflated negative binomial regression with a log link function. A total of 420 Anopheles mosquitoes (353 females and 67 males) belonging to three species; Anopheles arabiensis, Anopheles pharoensis, and Anopheles tenebrosus were caught in the resting clay pots, with An. arabiensis being the dominant species. Canopy cover, distance from the house, and land cover type were the significant landscape characters influencing the aggregation of resting mosquitoes. Both the count and binary models showed that canopy cover was the strongest predictor variable on the counts and the presence of Anopheles mosquitoes in the clay pots. Female Anopheles were most frequently found resting in the pots placed in banana plantations, and at sampling points that were at the greater distances (75 m and 100 m) from the focal house.

Conclusions

This study showed that exophilic Anopheles mosquitoes tend to rest in shaded areas some distance away from human habitation. These findings are important when targeting mosquitoes outdoors, complementing the existing effort being made to control malaria vectors indoors.
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Literature
1.
go back to reference Cibulskis RE, Alonso P, Aponte J, Aregawi M, Barrette A, Bergeron L, et al. Malaria. Global progress 2000–2015 and future challenges. Infect Dis Poverty. 2016;5:61.CrossRef Cibulskis RE, Alonso P, Aponte J, Aregawi M, Barrette A, Bergeron L, et al. Malaria. Global progress 2000–2015 and future challenges. Infect Dis Poverty. 2016;5:61.CrossRef
2.
go back to reference WHO. World malaria report 2015. Geneva: World Health Organization; 2015. WHO. World malaria report 2015. Geneva: World Health Organization; 2015.
3.
go back to reference Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2010;30:1–8. Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2010;30:1–8.
4.
go back to reference WHO. Global plan for insecticide resistance management in malaria vectors. Geneva: World Health Organization; 2014. WHO. Global plan for insecticide resistance management in malaria vectors. Geneva: World Health Organization; 2014.
5.
go back to reference Sougoufara S, Doucouré S, Sembène PM, Harry M, Sokhna C. Challenges for malaria vector control in sub-Saharan Africa: resistance and behavioral adaptations in Anopheles populations. J Vector Borne Dis. 2017;54:4–15.PubMed Sougoufara S, Doucouré S, Sembène PM, Harry M, Sokhna C. Challenges for malaria vector control in sub-Saharan Africa: resistance and behavioral adaptations in Anopheles populations. J Vector Borne Dis. 2017;54:4–15.PubMed
6.
go back to reference Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011;10:184.CrossRef Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011;10:184.CrossRef
7.
go back to reference Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.CrossRef Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.CrossRef
8.
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.CrossRef 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.CrossRef
9.
go back to reference Yohannes M, Boelee E. Early biting rhythm in the Afro-tropical vector of malaria, Anopheles arabiensis, and challenges for its control in Ethiopia. Med Vet Entomol. 2011;26:103–5.CrossRef Yohannes M, Boelee E. Early biting rhythm in the Afro-tropical vector of malaria, Anopheles arabiensis, and challenges for its control in Ethiopia. Med Vet Entomol. 2011;26:103–5.CrossRef
10.
go back to reference Sougoufara S, Diédhiou SM, Doucouré S, Diagne N, Sembène PM, Harry M, et al. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J. 2014;13:125.CrossRef Sougoufara S, Diédhiou SM, Doucouré S, Diagne N, Sembène PM, Harry M, et al. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J. 2014;13:125.CrossRef
12.
go back to reference WHO. World malaria report 2017. Geneva: World Health Organization; 2017. WHO. World malaria report 2017. Geneva: World Health Organization; 2017.
13.
go back to reference Govella NJ, Ferguson H. Why use of interventions targeting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Front Physiol. 2012;3:199.CrossRef Govella NJ, Ferguson H. Why use of interventions targeting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Front Physiol. 2012;3:199.CrossRef
14.
go back to reference Killeen GF, Marshall JM, Kiware SS, South AB, Tusting LS, Chaki PP, et al. Measuring, manipulating and exploiting behaviours of adult mosquitoes to optimize malaria vector control impact. BMJ Global Health. 2017;2:e000212.CrossRef Killeen GF, Marshall JM, Kiware SS, South AB, Tusting LS, Chaki PP, et al. Measuring, manipulating and exploiting behaviours of adult mosquitoes to optimize malaria vector control impact. BMJ Global Health. 2017;2:e000212.CrossRef
15.
go back to reference Zhu L, Muller GC, Marshall JM, Arheart K, Qualls WA, et al. Is outdoor vector control needed for malaria elimination? An individual based modeling study. Malar J. 2017;16:266.CrossRef Zhu L, Muller GC, Marshall JM, Arheart K, Qualls WA, et al. Is outdoor vector control needed for malaria elimination? An individual based modeling study. Malar J. 2017;16:266.CrossRef
16.
go back to reference Gillies MT. Studies of house leaving and outside resting of Anopheles gambiae Giles and Anopheles funestus Giles in east Africa. I. The outside resting population. Bull Ent Res. 1954;45:361–74.CrossRef Gillies MT. Studies of house leaving and outside resting of Anopheles gambiae Giles and Anopheles funestus Giles in east Africa. I. The outside resting population. Bull Ent Res. 1954;45:361–74.CrossRef
17.
go back to reference Gillies MT. Studies of house leaving and outside resting of Anopheles gambiae Giles and Anopheles funestus Giles in east Africa. II. The exodus from houses and the house resting population. Bull Ent Res. 1954;45:375–87.CrossRef Gillies MT. Studies of house leaving and outside resting of Anopheles gambiae Giles and Anopheles funestus Giles in east Africa. II. The exodus from houses and the house resting population. Bull Ent Res. 1954;45:375–87.CrossRef
18.
go back to reference Güneralp B, Lwasa S, Masundire H, Parnell S, Seto KC. Urbanization in Africa: challenges and opportunities for conservation. Environ Res Lett. 2017;13:015002.CrossRef Güneralp B, Lwasa S, Masundire H, Parnell S, Seto KC. Urbanization in Africa: challenges and opportunities for conservation. Environ Res Lett. 2017;13:015002.CrossRef
19.
go back to reference Burkett-Cadena ND, Eubanks MD, Unnasch TR. Preference of female mosquitoes for natural and artificial resting sites. J Am Mosq Control Assoc. 2008;24:228–35.CrossRef Burkett-Cadena ND, Eubanks MD, Unnasch TR. Preference of female mosquitoes for natural and artificial resting sites. J Am Mosq Control Assoc. 2008;24:228–35.CrossRef
20.
go back to reference Service MW. Mosquito ecology: field sampling methods. 2nd ed. London: Elsevier Applied Science; 1993. Service MW. Mosquito ecology: field sampling methods. 2nd ed. London: Elsevier Applied Science; 1993.
21.
go back to reference Paaijmans KP, Thomas MB. The influence of mosquito resting behaviour and associated microclimate for malaria risk. Malar J. 2011;10:183.CrossRef Paaijmans KP, Thomas MB. The influence of mosquito resting behaviour and associated microclimate for malaria risk. Malar J. 2011;10:183.CrossRef
22.
go back to reference Burkett-Cadena ND, McClure CJW, Estep LK, Eubanks MD. Host or habitats: what drives the spatial distribution of mosquitoes? Ecosphere. 2013;4:30.CrossRef Burkett-Cadena ND, McClure CJW, Estep LK, Eubanks MD. Host or habitats: what drives the spatial distribution of mosquitoes? Ecosphere. 2013;4:30.CrossRef
23.
go back to reference Overgaard HJ, Ekbom B, Suwonkerd W, Takagi M. Effect of landscape structure on anopheline mosquito density and diversity in northern Thailand: implications for malaria transmission and control. Landscape Ecol. 2003;18:605–19.CrossRef Overgaard HJ, Ekbom B, Suwonkerd W, Takagi M. Effect of landscape structure on anopheline mosquito density and diversity in northern Thailand: implications for malaria transmission and control. Landscape Ecol. 2003;18:605–19.CrossRef
24.
go back to reference Forattini OP, Kakitani I, Massad E, Marucci D. Studies on mosquitoes (Diptera: Culicidae) and anthropic environment. A—survey of resting adults and synanthropic behaviour in South-Eastern Brazil. Rev Saude Publica. 1993;27:398–411.CrossRef Forattini OP, Kakitani I, Massad E, Marucci D. Studies on mosquitoes (Diptera: Culicidae) and anthropic environment. A—survey of resting adults and synanthropic behaviour in South-Eastern Brazil. Rev Saude Publica. 1993;27:398–411.CrossRef
25.
go back to reference Verrone GA. Outline for the determination of malarial mosquitoes in Ethiopia. Mosq News. 1962;22:37–49. Verrone GA. Outline for the determination of malarial mosquitoes in Ethiopia. Mosq News. 1962;22:37–49.
26.
go back to reference Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara. Johannesburg: South African Institute of Medical Research; 1987. Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara. Johannesburg: South African Institute of Medical Research; 1987.
27.
go back to reference World Health Organization. Manual on practical entomology in malaria. Part 2: methods and techniques. Geneva: World Health Organization; 1975. World Health Organization. Manual on practical entomology in malaria. Part 2: methods and techniques. Geneva: World Health Organization; 1975.
28.
go back to reference Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.CrossRef Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.CrossRef
29.
30.
go back to reference Ibry WS, Apperson CS. Spatial and temporal distribution of resting mosquitoes (Diptera: Culicidae) in the coastal plain of North Carolina. J Med Entomol. 1992;29:150–9.CrossRef Ibry WS, Apperson CS. Spatial and temporal distribution of resting mosquitoes (Diptera: Culicidae) in the coastal plain of North Carolina. J Med Entomol. 1992;29:150–9.CrossRef
31.
go back to reference Githeko AK, Service MW, Mbogo CM, Atieli FK. Resting behaviour, ecology and genetics of malaria vectors in large scale agricultural areas of western Kenya. Parasitologia. 1996;38:481–9. Githeko AK, Service MW, Mbogo CM, Atieli FK. Resting behaviour, ecology and genetics of malaria vectors in large scale agricultural areas of western Kenya. Parasitologia. 1996;38:481–9.
32.
go back to reference Gillies MT. Anopheline mosquitoes: vector behaviour and bionomics. In: Wernsdorfer WH, McGregor I, editors. Malaria: Principles and practice of malariology. Edinburgh: Churchill Livingstone; 1991. p. 453–86. Gillies MT. Anopheline mosquitoes: vector behaviour and bionomics. In: Wernsdorfer WH, McGregor I, editors. Malaria: Principles and practice of malariology. Edinburgh: Churchill Livingstone; 1991. p. 453–86.
33.
go back to reference Benoit JB, Patrick KR, Desai K, Hardesty JJ, Krause TB, Denlinger DL. Repeated bouts of dehydration deplete nutrient reserves and reduce egg production in the mosquito Culex pipiens. J Exp Biol. 2010;213:2763–9.CrossRef Benoit JB, Patrick KR, Desai K, Hardesty JJ, Krause TB, Denlinger DL. Repeated bouts of dehydration deplete nutrient reserves and reduce egg production in the mosquito Culex pipiens. J Exp Biol. 2010;213:2763–9.CrossRef
34.
go back to reference Chown SL, Sørensen JG, Terblanche JS. Water loss in insects: an environmental change perspective. J Insect Physiol. 2011;57:1070–84.CrossRef Chown SL, Sørensen JG, Terblanche JS. Water loss in insects: an environmental change perspective. J Insect Physiol. 2011;57:1070–84.CrossRef
35.
go back to reference Ye-Ebiyo Y, Pollack RJ, Spielman A. Enhanced development in nature of larval Anopheles arabiensis mosquitoes feeding on maize pollen. Am J Trop Med Hyg. 2000;63:9093.CrossRef Ye-Ebiyo Y, Pollack RJ, Spielman A. Enhanced development in nature of larval Anopheles arabiensis mosquitoes feeding on maize pollen. Am J Trop Med Hyg. 2000;63:9093.CrossRef
36.
go back to reference Ye-Ebiyo Y, Pollack RJ, Kiszewski A, Spielman A. 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. 2003;68:748–52.CrossRef Ye-Ebiyo Y, Pollack RJ, Kiszewski A, Spielman A. 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. 2003;68:748–52.CrossRef
37.
go back to reference Kebede A, McCann JC, Kiszewski AE, Ye-Ebiyo Y. New evidence of the effects of agro-ecologic change on malaria transmission. Am J Trop Med Hyg. 2005;73:676–80.CrossRef Kebede A, McCann JC, Kiszewski AE, Ye-Ebiyo Y. New evidence of the effects of agro-ecologic change on malaria transmission. Am J Trop Med Hyg. 2005;73:676–80.CrossRef
38.
go back to reference Wondwosen B, Hill SR, Birgersson G, Seyoum E, Tekie H, Ignell R. A(maize)ing attraction: gravid Anopheles arabiensis are attracted and oviposit in response to maize pollen odours. Malar J. 2017;16:39.CrossRef Wondwosen B, Hill SR, Birgersson G, Seyoum E, Tekie H, Ignell R. A(maize)ing attraction: gravid Anopheles arabiensis are attracted and oviposit in response to maize pollen odours. Malar J. 2017;16:39.CrossRef
39.
go back to reference Kivuyo HS, Mbazi PH, Kisika DS, Munga S, Rumisha SF, Urasa FM, et al. Performance of five food regimes on Anopheles gambiae senso stricto larval rearing to adult emergence in insectary. PLoS ONE. 2014;9:e110671.CrossRef Kivuyo HS, Mbazi PH, Kisika DS, Munga S, Rumisha SF, Urasa FM, et al. Performance of five food regimes on Anopheles gambiae senso stricto larval rearing to adult emergence in insectary. PLoS ONE. 2014;9:e110671.CrossRef
40.
go back to reference Araujo M, Gil LH, De-Almeida e-Silva A. Larval food quantity affects development time, survival and adult biological traits that influence the vectorial capacity of Anopheles darling under laboratory conditions. Malar J. 2012;11:261.CrossRef Araujo M, Gil LH, De-Almeida e-Silva A. Larval food quantity affects development time, survival and adult biological traits that influence the vectorial capacity of Anopheles darling under laboratory conditions. Malar J. 2012;11:261.CrossRef
41.
go back to reference Oliver SV, Brooke BD. The effect of larval nutritional deprivation on the life history and DDT resistance in laboratory strains of the malaria vector Anopheles arabiensis. Malar J. 2013;12:44.CrossRef Oliver SV, Brooke BD. The effect of larval nutritional deprivation on the life history and DDT resistance in laboratory strains of the malaria vector Anopheles arabiensis. Malar J. 2013;12:44.CrossRef
42.
go back to reference Mendez W, Liria J, Navarro J, García CZ, Freier JE, Salas R, et al. Spatial dispersion of adult mosquitoes (Diptera: Culicidae) in a sylvatic focus of Venezuelan equine encephalitis virus. J Med Entomol. 2001;38:813–21.CrossRef Mendez W, Liria J, Navarro J, García CZ, Freier JE, Salas R, et al. Spatial dispersion of adult mosquitoes (Diptera: Culicidae) in a sylvatic focus of Venezuelan equine encephalitis virus. J Med Entomol. 2001;38:813–21.CrossRef
43.
go back to reference Moncayo AC, Edman JD, Finn JT. Application of geographic information technology in determining risk of eastern equine encephalomyelitis virus transmission. J Am Mosq Control Assoc. 2000;16:28–35.PubMed Moncayo AC, Edman JD, Finn JT. Application of geographic information technology in determining risk of eastern equine encephalomyelitis virus transmission. J Am Mosq Control Assoc. 2000;16:28–35.PubMed
44.
go back to reference Diuk-Wasser MA, Brown HE, Andreadis TG, Fish D. Modeling the spatial distribution of mosquito vectors for West Nile virus in Connecticut. USA. Vector Borne Zoonotic Dis. 2006;6:283–95.CrossRef Diuk-Wasser MA, Brown HE, Andreadis TG, Fish D. Modeling the spatial distribution of mosquito vectors for West Nile virus in Connecticut. USA. Vector Borne Zoonotic Dis. 2006;6:283–95.CrossRef
45.
go back to reference Trawinski PR, Mackay DS. Identification of environmental covariates of West Nile virus vector mosquito population abundance. Vector Borne Zoonotic Dis. 2010;10:515–26.CrossRef Trawinski PR, Mackay DS. Identification of environmental covariates of West Nile virus vector mosquito population abundance. Vector Borne Zoonotic Dis. 2010;10:515–26.CrossRef
Metadata
Title
Shady business: understanding the spatial ecology of exophilic Anopheles mosquitoes
Authors
Yared Debebe
Sharon R. Hill
Habte Tekie
Rickard Ignell
Richard J. Hopkins
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2499-7

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