The impact of low erythrocyte density in human blood on the fitness and energetic reserves of the African malaria vector Anopheles gambiae

S Noushin Emami,Heather M Ferguson,Lisa C Ranford-Cartwright

doi:10.1186/1475-2875-12-45

Abstract

BackgroundAnaemia is a common health problem in the developing world. This condition is characterized by a reduction in erythrocyte density, primarily from malnutrition and/or infectious diseases such as malaria. As red blood cells are the primary source of protein for haematophagous mosquitoes, any reduction could impede the ability of mosquito vectors to transmit malaria by influencing their fitness or that of the parasites they transmit. The aim of this study was to determine the impact of differences in the density of red blood cells in human blood on malaria vector (Anopheles gambiae sensu stricto) fitness. The hypotheses tested are that mosquito vector energetic reserves and fitness are negatively influenced by reductions in the red cell density of host human blood meals commensurate with those expected from severe anaemia.MethodsMosquitoes (An. gambiae s.s.) were offered blood meals of different packed cell volume (PCV) of human blood consistent with those arising from severe anaemia (15%) and normal PCV (50%). Associations between mosquito energetic reserves (lipid, glucose and glycogen) and fitness measures (reproduction and survival) and blood meal PCV were investigated.ResultsThe amount of protein that malaria vectors acquired from blood feeding (indexed by haematin excretion) was significantly reduced at low blood PCV. However, mosquitoes feeding on blood of low PCV had the same oviposition rates as those feeding on blood of normal PCV, and showed an increase in egg production of around 15%. The long-term survival of An. gambiae s.s was reduced after feeding on low PCV blood, but PCV had no significant impact on the proportion of mosquitoes surviving through the minimal period required to develop and transmit malaria parasites (estimated as 14 days post-blood feeding). The impact of blood PCV on the energetic reserves of mosquitoes was relatively minor.ConclusionsThese results suggest that feeding on human hosts whose PCV has been depleted due to severe anaemia does not significantly reduce the fitness or transmission potential of malaria vectors, and indicates that mosquitoes may be able exploit resources for reproduction more efficiently from blood of low rather than normal PCV.

Highlights

Anaemia is a common health problem in the developing world
These results suggest that contact with human hosts whose packed cell volume (PCV) has been depleted due to severe anaemia may not significantly reduce the fitness or transmission potential of malaria vectors
As reductions in blood PCV had few detrimental impacts on the mosquito fitness traits measured it may be unlikely to have large impacts on mosquito energetic reserves. These results illustrate how variation in the PCV of human blood meals influences the fitness of An. gambiae s.s

Summary

Introduction

Anaemia is a common health problem in the developing world This condition is characterized by a reduction in erythrocyte density, primarily from malnutrition and/or infectious diseases such as malaria. As red blood cells are the primary source of protein for haematophagous mosquitoes, any reduction could impede the ability of mosquito vectors to transmit malaria by influencing their fitness or that of the parasites they transmit. The hypotheses tested are that mosquito vector energetic reserves and fitness are negatively influenced by reductions in the red cell density of host human blood meals commensurate with those expected from severe anaemia. Anaemia is characterized by a change in the biochemical composition of several haematological factors [5], with the most notable being a marked reduction in the density of red blood cells (erythrocytes). As PCV is a measure of the number of erythrocytes per unit volume of blood, and haemoglobin the amount of protein (in erythrocytes) per unit volume of blood, PCV and Hb levels are generally highly correlated [6]

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