The online version of this article (doi:10.1186/1475-2875-11-425) contains supplementary material, which is available to authorized users.
The authors declare that they have no competing interests.
INL and HMF designed the research. INL, AAD, KFM and EMM performed the research. INL and HMF analyzed and interpreted the data. DTH and RR assisted with analysis. INL drafted the manuscript. DTH, RR and HMF commented on the manuscript. All authors read and approved the final manuscript.
Host responses are important sources of selection upon the host species range of ectoparasites and phytophagous insects. However little is known about the role of host responses in defining the host species range of malaria vectors. This study aimed to estimate the relative importance of host behaviour to the feeding success and fitness of African malaria vectors, and assess its ability to predict their known host species preferences in nature.
Paired evaluations of the feeding success and fitness of African vectors Anopheles arabiensis and Anopheles gambiae sensu stricto in the presence and limitation of host behaviour were conducted in a semi-field system (SFS) at Ifakara Health Institute, Tanzania. In one set of trials, mosquitoes were released within the SFS and allowed to forage overnight on a host that was free to exhibit a natural behaviour in response to insect biting. In the other, mosquitoes were allowed to feed directly on from the skin surface of immobile hosts. The feeding success and subsequent fitness of vectors under these conditions were investigated on six host types (humans, calves, chickens, cows, dogs and goats) to assess whether physical movements of preferred host species (cattle for An. arabiensis, humans for An. gambiae s. s.) were less effective at preventing mosquito bites than those of common alternatives.
Anopheles arabiensis generally had greater feeding success when applied directly to host skin than when foraging on unrestricted hosts (in five of six host species). However, An. gambiae s.s. obtained blood meals from free and restrained hosts with similar success from most host types (four out of six). Overall, the blood meal size, oviposition rate, fecundity and post-feeding survival of mosquito vectors were significantly higher after feeding on hosts free to exhibit behaviour, than those who were immobilized during feeding trials.
Allowing hosts to move freely during exposure to mosquitoes was associated with moderate reductions in mosquito feeding success, but no detrimental impact to the subsequent fitness of mosquitoes that were able to feed upon them. This suggests that physical defensive behaviours exhibited by common host species including humans do not impose substantial fitness costs on African malaria vectors.
Jaenike J: Host specialization in phytophagous insects. Annu Rev Ecol Syst. 1990, 21: 243-273. 10.1146/annurev.es.21.110190.001331. CrossRef
Bryant JP, Provenza FD, Pastor J, Reichardt PB, Clausen TP, du Toit JT: Interactions between woody plants and browsing mammals mediated by secondary metabolites. Annu Rev Ecol Syst. 1991, 22: 431-446. 10.1146/annurev.es.22.110191.002243. CrossRef
Edman JD, Scott TW: Host defensive behaviour and the feeding success of mosquitoes. Insect Sci Appl. 1987, 8: 617-622.
Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE, Sachs J: A global index representing the stability of malaria transmission. Am J Trop Med Hyg. 2004, 70: 486-498. PubMed
Edman JD, Kale HW: Host behaviour: its influence on the feeding success of mosquitoes. Ann Entomol Soc Am. 1971, 64: 513-516. CrossRef
Anderson RA, Roitberg BD: Modelling trade-offs between mortality and fitness associated with persistent blood feeding by mosquitoes. Ecol Lett. 1999, 2: 98-105. 10.1046/j.1461-0248.1999.22055.x. CrossRef
Darbro JM, Harrington LC: Avian defensive behavior and blood-feeding success of the West Nile vector mosquito, Culex pipiens. Behav Ecol. 2007, 18: 750-10.1093/beheco/arm043. CrossRef
Clarke JL, Rowley WA, Asman M: The effect of colonization on the laboratory flight ability of Culex tarsalis (Diptera: Culicidae). J Florida Anti-mosquito Assoc. 1983, 54: 23-26.
Khokhlova IS, Ghazaryan L, Krasnov BR, Degen AA: Effects of parasite specificity and previous infestation of hosts on the feeding and reproductive success of rodent-infesting fleas. Funct Ecol. 2008, 22: 530-536. 10.1111/j.1365-2435.2008.01393.x. CrossRef
Bize P, Jeanneret C, Klopfenstein A, Roulin A: What makes a host profitable? Parasites balance host nutritive resources against immunity. Amer Nat. 2008, 171: 107-118. 10.1086/523943. CrossRef
Lefevre T, Gouagna LC, Dabire KR, Elguero E, Fontenille D, Renaud F, Costantini C, Thomas F: Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am J Trop Med Hyg. 2009, 81: 1023-1029. 10.4269/ajtmh.2009.09-0124. CrossRefPubMed
Ferguson H, Ng'habi K, Walder T, Kadungula D, Moore S, Lyimo I, Russell T, Urassa H, Mshinda H, Killeen G, Knols B: Establishment of a large semi-field system for experimental study of African malaria vector ecology and control in Tanzania. Malar J. 2008, 7: 158-10.1186/1475-2875-7-158. PubMedCentralCrossRefPubMed
Lyimo IN, Haydon DT, Russell TL, Mbina KF, Daraja AA, Mbehela EM, Reeve R, Heather MF: The impact of host species and vector control measures on the fitness of African malaria vectors. Proc R Soc B. In press
Lyimo I: Ecological and evolutionary determinants of Anopheline host species choice and its implications for malaria transmission. 2010, Glasgow: University of Glasgow, College of Medical, Veterinary and Life Sciences
Killeen GF, Kihonda J, Lyimo E, Oketch FR, Kotas ME, Mathenge E, Schellenberg JA, Lengeler C, Smith TA, Drakeley CJ: Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006, 6: 161-10.1186/1471-2334-6-161. PubMedCentralCrossRefPubMed
Briegel H: Determination of uric acid and haematin in a single sample of excreta from blood-fed insects. Cell Mol Life Sci. 1980, 36: 1428-1428. 10.1007/BF01960142. CrossRef
Crawley MJ: The R book. 2007, Chichester, UK: John Wiley & Sons Ltd CrossRef
Holm S: A simple sequentially rejective multiple test procedure. Scand J Stat. 1979, 6: 65-70.
Muriu SM, Muturi EJ, Shililu JI, Mbogo CM, Mwangangi JM, Jacob BG, Irungu LW, Mukabana RW, Githure JI, Novak RJ: Host choice and multiple blood feeding behaviour of malaria vectors and other anophelines in Mwea rice scheme, Kenya. Malar J. 2008, 7: 1-20. 10.1186/1475-2875-7-1. CrossRef
Dekker T, Takken W, Knols BGJ, Bouman E, Laak S, Bever A, Huisman PWT: Selection of biting sites on a human host by Anopheles gambiae s.s., An. arabiensis and An. quadriannulatus. Entomol Exp Appl. 1998, 87: 295-300. 10.1046/j.1570-7458.1998.00334.x. CrossRef
Hurd H, Hogg J, Renshaw M: Interaction between bloodfeeding, fecundity, and infection in mosquitoes. Parasitol Today. 1995, 11: 411-416. 10.1016/0169-4758(95)80021-2. CrossRef
Wintrobe MM: Variations in the size and hemoglobin content of erythrocytes in the blood of various vertebrates. Folia Haematol. 1933, 51: 32-49.
Lyimo IN, Keegan SP, Ranford-Cartwright LC, Ferguson HM: The impact of uniform and mixed species blood meals on the fitness of the mosquito vector Anopheles gambiae s.s: does a specialist pay for diversifying its host species diet?. J Evol Biol. 2012, 25: 452-460. 10.1111/j.1420-9101.2011.02442.x. CrossRefPubMed
Edman JD, Lynn HC: Relationship between blood meal volume and ovarian development in Culex nigripalpus (Diptera: Culicidae). Entomol Exp Appl. 1975, 18: 492-496. 10.1111/j.1570-7458.1975.tb00427.x. CrossRef
Briegel H: Protein catabolism and nitrogen partitioning during oögenesis in the mosquito Aedes aegypti. J Insect Physiol. 1986, 32: 455-462. 10.1016/0022-1910(86)90006-5. CrossRef
Roitberg BD, Gordon I: Does the Anopheles blood meal - fecundity curve, curve?. J Vector Ecol. 2005, 30: 83-86. PubMed
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: 83-89. 10.1046/j.1570-7458.2002.00957.x. CrossRef
Briegel H: Mosquito reproduction: Incomplete utilization of the blood meal protein for oogenesis. J Insect Physiol. 1985, 31: 15-21. 10.1016/0022-1910(85)90036-8. CrossRef
WHO: World malaria report. 2011, Geneva, Switzerland: World Health Organization, 27-34.
Pluess B, Tanser F, Lengeler C, Sharp B: Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010, 2: 1-46.
Kirby MJ, Ameh D, Bottomley C, Green C, Jawara M, Milligan PJ, Snell PC, Conway DJ, Lindsay SW: Effect of two different house screening interventions on exposure to malaria vectors and on anaemia in children in The Gambia: a randomised controlled trial. Lancet. 2009, 374: 998-1009. 10.1016/S0140-6736(09)60871-0. PubMedCentralCrossRefPubMed
Lengeler C: Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev. 2004, 2: CD000363- PubMed
- The fitness of African malaria vectors in the presence and limitation of host behaviour
Issa N Lyimo
Daniel T Haydon
Kasian F Mbina
Ally A Daraja
Edgar M Mbehela
Heather M Ferguson
- BioMed Central
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