The fitness of African malaria vectors in the presence and limitation of host behaviour

Issa N Lyimo,Kasian F Mbina,Heather M Ferguson,Daniel T Haydon,Richard Reeve,Edgar M Mbehela,Ally A Daraja

doi:10.1186/1475-2875-11-425

Issa N Lyimo, Kasian F Mbina + Show 5 more

Open Access

https://doi.org/10.1186/1475-2875-11-425

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Abstract

BackgroundHost 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.MethodsPaired 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.ResultsAnopheles 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.ConclusionsAllowing 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.

Highlights

Host responses are important sources of selection upon the host species range of ectoparasites and phytophagous insects
Overall, the recapture rates of mosquitoes exposed to hosts under semi-field system (SFS) conditions were higher for An. gambiae s.s than An. arabiensis, but did not vary between host species for either mosquito species (An. arabiensis: χ2 5 = 10.00, P = 0.07, and An. gambiae s.s: χ2 5 = 7.87, P = 0.16, Table 1)
Mosquito feeding success The feeding success of An. arabiensis was related to host species in semi-field experiments with free moving hosts (χ2 5 = 43.27, P < 0.001, Figure 1a), and in conditions where hosts were immobilized during mosquito

Summary

Introduction

Host responses are important sources of selection upon the host species range of ectoparasites and phytophagous insects. Relatively little is known about the importance of physical behaviours mounted by vertebrate hosts in generating selection for host specificity in insect disease vectors [6]. The frequency with which mosquito vectors feed on humans, and adult mosquito survival, are key determinants of malaria transmission intensity [7,9] Both of these phenomena may be influenced by host physical movements. Hosts that are free to exhibit behavioural responses can prevent mosquitoes from biting [10,11], and/or interrupt their blood feeding [12] These host responses could limit parasite transmission by reducing host – vector contact rates and increasing the risk of mortality in host-seeking mosquitoes [13]. Host behavioural responses could have substantial impacts on the fitness of both malaria parasites and their vectors, and correspondingly generate selection for specificity on poorly defensive host types

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