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Open Access 01-12-2016 | Research

Determinants of host feeding success by Anopheles farauti

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

Published in: Malaria Journal | Issue 1/2016

Abstract

Background

The proportion of blood meals that mosquitoes take from a host species is a function of the interplay of extrinsic (abundance and location of potential hosts) and intrinsic (innate preference) factors. A mark-release-recapture experiment addressed whether host preference in a population of Anopheles farauti was uniform or if there were anthropophilic and zoophilic subpopulations. The corresponding fitness associated with selecting different hosts for blood meals was compared by measuring fecundity.

Methods

The attractiveness of humans for blood meals by An. farauti in the Solomon Islands was compared to pigs using tent traps. Host fidelity was assessed by mark-release-recapture experiments in which different colour dusts were linked to the host to which the mosquito was first attracted. Outdoor resting An. farauti were captured on barrier screens and the human blood index (HBI) as well as the feeding index were calculated. The fecundity of individual An. farauti after feeding on either humans or pigs was assessed from blood-fed mosquitoes held in individual oviposition chambers.

Results

Anopheles farauti were more attracted to humans than pigs at a ratio of 1.31:1.00. The mark-release-recapture experiment found evidence for An. farauti being a single population regarding host preference. The HBI of outdoor resting An. farauti was 0.93 and the feeding index was 1.29. Anopheles farauti that fed on a human host laid more eggs but had a longer oviposition time compared to An. farauti that had blood fed on a pig.

Conclusions

One of the strongest drivers for host species preference was the relative abundance of the different host species. Here, An. farauti have a slight preference for humans over pigs as blood meal sources. However, the limited availability of alternative hosts relative to humans in the Solomon Islands ensures a very high proportion of blood meals are obtained from humans, and thus, the transmission potential of malaria by An. farauti is high.

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MacDonald G. The epidemiology and control of malaria. London: Oxford University Press; 1957.

Bruce-Chwatt LJ, Garrett-Jones C, Weitz B. Ten years’ study (1955-64) of host selection by anopheline mosquitos. Bull World Health Organ. 1966;35:405–39.PubMedPubMedCentral

Garrett-Jones C, Boreham PFL, Pant CP. Feeding habits of anophelines (Diptera: Culicidae) in 1971–78, with reference to the human blood index: a review. Bull Entomol Res. 1980;70:165–85. doi:10.1017/S0007485300007422.CrossRef

Takken W, Verhulst NO. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol. 2013;58:433–53. doi:10.1146/annurev-ento-120811-153618.CrossRefPubMed

Burkot TR, Graves PM, Paru R, Lagog M. Mixed blood feeding by the malaria vectors in the Anopheles punctulatus complex (Diptera: Culicidae). J Med Entomol. 1988;25:213–65.CrossRef

Lyimo IN, Ferguson HM. Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol. 2009;25:189–96. doi:10.1016/j.pt.2009.01.005.CrossRefPubMed

Lyimo IN, Haydon DT, Russell TL, Mbina KF, Daraja AA, Mbehela EM, et al. The impact of host species and vector control measures on the fitness of African malaria vectors. Proc R Soc Lond B. 2013;280:20122823. doi:10.1098/rspb.2012.2823.CrossRef

Takken W, Stuke K, Klowden MJ. Biological differences in reproductive strategy between the mosquito sibling species Anopheles gambiae sensu stricto and An. quadriannulatus. Entomol Exp Appl. 2002;103:83–9. doi:10.1046/j.1570-7458.2002.00957.x.CrossRef

Mayagaya V, Nkwengulila G, Lyimo I, Kihonda J, Mtambala H, Ngonyani H, et al. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar J. 2015;14:17. doi:10.1186/s12936-014-0536-8.CrossRefPubMedPubMedCentral

10.

Iwashita H, Dida G, Sonye G, Sunahara T, Futami K, Njenga S, et al. Push by a net, pull by a cow: can zooprophylaxis enhance the impact of insecticide treated bed nets on malaria control? Parasit Vectors. 2014;7:52. doi:10.1186/1756-3305-7-52.CrossRefPubMedPubMedCentral

11.

Burkot TR, Dye C, Graves PM. An analysis of some factors determining the sporozoite rates, human blood indicies, and biting rates of members of the Anopheles punctulatus complex in Papua New Guinea. Am J Trop Med Hyg. 1989;40:229–34.PubMed

12.

Githeko AK, Service MW, Mbogo CM, Atieli FK, Juma FO. Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya. Acta Trop. 1994;58:307–16.CrossRefPubMed

13.

Garrett-Jones C. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ. 1964;30:241–61.PubMedPubMedCentral

14.

Burkot TR, Russell TL, Reimer LJ, Bugoro H, Beebe NW, Cooper RD, et al. Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes. Malar J. 2013;12:49. doi:10.1186/1475-2875-12-49.CrossRefPubMedPubMedCentral

15.

Silver JB. Mosquito ecology: field sampling methods. 3rd ed. New York: Springer; 2008.CrossRef

16.

Kay BH, Boreham PFL, Edman JD. Application of the feeding index concept to studies of mosquito host-feeding patterns. Mosq News. 1979;39:68–72.

17.

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

18.

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

19.

Hii J, Vun Y. The influence of a heterogeneous environment on host feeding behaviour of Anopheles balabacensis (Diptera: Culicidae). Trop Biomed. 1987;4:67–70.

20.

Nutsathapana S, Sawasdiwongphorn P, Chitprarop U, Cullen JR, Gass RF, Green CA. A mark-release-recapture demonstration of host-preference heterogeneity in Anopheles minimus Theobald (Diptera: Culicidae) in a Thai village. Bull Entomol Res. 1986;76:313–20. doi:10.1017/S0007485300014784.CrossRef

21.

Ulloa A, Arredondo-Jiménez JI, Rodriguez MH, Fernández-Salas I. Mark-recapture studies of host selection by Anopheles (Anopheles) vestitipennis. J Am Mosq Control Assoc. 2002;18:32–5.PubMed

22.

Gillies MT. Selection for host preference in Anopheles gambiae. Nature. 1964;203:852–4.CrossRefPubMed

23.

McCall PJ, Kelly DW. Learning and memory in disease vectors. Trends Parasitol. 2002;18:429–33. doi:10.1016/S1471-4922(02)02370-X.CrossRefPubMed

24.

Alonso WJ, Schuck-Paim C. The ‘ghosts’ that pester studies on learning in mosquitoes: guidelines to chase them off. Med Vet Entomol. 2006;20:157–65. doi:10.1111/j.1365-2915.2006.00623.x.CrossRefPubMed

25.

Mukwaya LG. Genetic control of feeding preferences in the mosquitoes Aedes (Stegomyia) simpsoni and aegypti. Physiol Entomol. 1977;2:133–45. doi:10.1111/j.1365-3032.1977.tb00091.x.CrossRef

26.

Lulu M, Hadis M, Makonnen Y, Asfaw T. Chromosomal inversion polymorphisms of Anopheles arabiensis from some localities in Ethiopia in relation to host feeding choice. Ethiop J Health Dev. 1998;12:23–8.

27.

Mnzava AE, Mutinga MJ, Staak C. Host blood meals and chromosomal inversion polymorphism in Anopheles arabiensis in the Baringo District of Kenya. J Am Mosq Control Assoc. 1994;10:507–10.PubMed

28.

Russell TL, Beebe NW, Bugoro H, Apairamo A, Chow WK, 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.PubMedPubMedCentral

29.

Brookfield HC, Hart D. Rainfall in the tropical southwest Pacific, Department of Geography, Publ G/3. Canberra: The Australian National University; 1966.

30.

Belkin JN. The mosquitoes of the South Pacific (Diptera, Culicidae). Berkeley and Los Angeles: University of California Press; 1962.

31.

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

32.

Kent RJ, Norris DE. Identification of mammalian blood meals in mosquitoes by a multiplexed Polymerase Chain Reaction targeting Cytochrome B. Am J Trop Med Hyg. 2005;73:336–42.PubMedPubMedCentral

33.

Das S, Henning T, Simubali L, Hamapumbu H, Nzira L, Mamini E, et al. Underestimation of foraging behaviour by standard field methods in malaria vector mosquitoes in southern Africa. Malar J. 2015;14:12. doi:10.1186/s12936-014-0527-9.CrossRefPubMedPubMedCentral

34.

Russell TL, Beebe NW, Bugoro H, Apairamo A, Cooper RD, Lobo NF et al. Dataset examining host feeding parameters of Anopheles farauti in Haleta village, Solomon Islands. James Cook University Tropical Research Hub. 2016. doi:10.4225/28/56BD6DF7C9CB8.

35.

R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2013.

36.

Ferguson HM, Rivero A, Read AF. The influence of malaria parasite genetic diversity and anaemia on mosquito feeding and fecundity. Parasitol. 2003;127:9–19. doi:10.1017/S0031182003003287.CrossRef

37.

Roitberg BD, Gordon I. Does the Anopheles blood meal-fecundity curve, curve? J Vector Ecol. 2005;30:83.PubMed

38.

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

39.

Graves PM, Burkot TR, Saul A, Hayes RJ, Carter R. Estimation of Anopheline survival rate, vectoral capacity and mosquito infection probability from malaria vector infection rates in villages near Madang, Papua New Guinea. J Appl Ecol. 1990;27:124–47.CrossRef

40.

Spencer M. Blood preferences of Anopheles farauti. P N G Med J. 1964;7:19.

41.

Black RH. Observations on the behavior of Anopheles farauti laveran, an important malaria vector in the territory of Papua New Guinea. Med J Aust. 1955;42:949–55.PubMed

42.

Afifi SE, Spencer M, Hudson PB, Tavil NW. Biting prevalence and malaria transmission patterns in the Anopheles punctulatus complex (Diptera: Culicidae) in Papua New Guinea. Aust J Exp Biol Med. 1980;58:1–17.CrossRef

43.

Hii JLK, Mai A, Mellor S, Lewis D, Alexander N, Alpers M. Spatial and temporal variation in abundance of Anopheles (Diptera: Culicidae) in a malaria endemic area in Papua New Guinea. J Med Entomol. 1997;34:193–205.CrossRefPubMed

44.

Charlwood JD, Dagoro H, Paru R. Blood-feeding and resting behaviour in the Anopheles punctulatus Dönitz complex (Diptera: Culicidae) from coastal Papua New Guinea. Bull Entomol Res. 1985;75:463–76.CrossRef

45.

Chow CY. Ecology of malaria vectors in the Pacific. Cah ORSTOM ser Ent med et Parasitol. 1969;7:93–7.

46.

Ambrose L, Cooper RD, Russell TL, Burkot TR, Lobo NF, Collins FH, et al. Microsatellite and mitochondrial markers reveal strong gene flow barriers for Anopheles farauti in the Solomon Archipelago: implications for malaria vector control. Int J Parasitol. 2014;44:225–33. doi:10.1016/j.ijpara.2013.12.001.CrossRefPubMedPubMedCentral

47.

Loong K, Chiang G, Eng K, Chan S, Yap H. Survival and feeding behaviour of Malaysian strain of Anopheles maculatus Theobald (Diptera: Culicidae) and their role in malaria transmission. Trop Biomed. 1990;7:71–6.

48.

Rawlings P, Curtis CF. Tests for the existence of genetic variability in the tendency of Anopheles culicifacies species B to rest in houses and to bite man. Bull World Health Organ. 1982;60:427–32.PubMedPubMedCentral

Title: Determinants of host feeding success by Anopheles farauti
Authors: Tanya L. Russell
Nigel W. Beebe
Hugo Bugoro
Allan Apairamo
Robert D. Cooper
Frank H. Collins
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/s12936-016-1168-y

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