Avian malaria on Madagascar: bird hosts and putative vector mosquitoes of different Plasmodium lineages

Sandrine Schmid,Fano José Randrianambinintsoa,Ute Mackenstedt,Friederike Woog,Sébastien Boyer,Anke Dinkel,Michaël Luciano Tantely

doi:10.1186/s13071-016-1939-x

Abstract

BackgroundAvian malaria occurs almost worldwide and is caused by Haemosporida parasites (Plasmodium, Haemoproteus and Leucocytozoon). Vectors such as mosquitoes, hippoboscid flies or biting midges are required for the transmission of these parasites. There are few studies about avian malaria parasites on Madagascar but none about suitable vectors.MethodsTo identify vectors of avian Plasmodium parasites on Madagascar, we examined head, thorax and abdomen of 418 mosquitoes from at least 18 species using a nested PCR method to amplify a 524 bp fragment of the haemosporidian mitochondrial cytochrome b gene. Sequences obtained were then compared with a large dataset of haemosporidian sequences detected in 45 different bird species (n = 686) from the same area in the Maromizaha rainforest.ResultsTwenty-one mosquitoes tested positive for avian malaria parasites. Haemoproteus DNA was found in nine mosquitoes (2.15%) while Plasmodium DNA was found in 12 mosquitoes (2.87%). Seven distinct lineages were identified among the Plasmodium DNA samples. Some lineages were also found in the examined bird samples: Plasmodium sp. WA46 (EU810628.1) in the Madagascar bulbul, Plasmodium sp. mosquito 132 (AB308050.1) in 15 bird species belonging to eight families, Plasmodium sp. PV12 (GQ150194.1) in eleven bird species belonging to eight families and Plasmodium sp. P31 (DQ839060.1) was found in three weaver bird species.ConclusionThis study provides the first insight into avian malaria transmission in the Maromizaha rainforest in eastern Madagascar. Five Haemoproteus lineages and seven Plasmodium lineages were detected in the examined mosquitoes. Complete life-cycles for the specialist lineages WA46 and P31 and for the generalist lineages mosquito132 and PV12 of Plasmodium are proposed. In addition, we have identified for the first time Anopheles mascarensis and Uranotaenia spp. as vectors for avian malaria and offer the first description of vector mosquitoes for avian malaria in Madagascar.

Highlights

Avian malaria occurs almost worldwide and is caused by Haemosporida parasites (Plasmodium, Haemoproteus and Leucocytozoon)
These positive samples were of the mosquito species Anopheles mascarensis, Culex annulioris, C. pipiens, Uranotaenia alboabdominalis, Uranotaenia neireti, Uranotaenia n. sp
WA46 is transmitted from mosquitoes of the genus Uranotaenia to birds belonging to the family Pycnonotidae

Summary

Introduction

Avian malaria occurs almost worldwide and is caused by Haemosporida parasites (Plasmodium, Haemoproteus and Leucocytozoon). Vectors such as mosquitoes, hippoboscid flies or biting midges are required for the transmission of these parasites. For natural transmission of Plasmodium to the vertebrate host, the parasite undergoes a series of obligatory developmental, propagative and migrational processes inside a mosquito vector. These include zygote formation and ookinete development in the midgut lumen, oocyst formation and sporogony on the basal side of the midgut, sporozoite migration through the haemocoel, and invasion of the salivary glands [5]. Most studies use molecular methods to identify vector feeding preferences [9] and sporogonic stages of the parasites in salivary glands to identify potential vectors [10]

Objectives

Methods

Results

Discussion

Conclusion