Abstract
BackgroundHaemoproteus parasites are widespread, and some species cause disease in wild and domestic birds. However, the insect vectors remain unknown for the majority of species and genetic lineages of avian Haemoproteus. This information is crucial for better understanding the biology of haemoproteids, the epidemiology of haemoproteosis, and the development of morphological characters of sporogonic stages in wildlife haemosporidian parasites. It remains unclear whether the specificity of Haemoproteus parasites for vectors is broad or the transmission of a given parasite can be restricted to a single or few species of vectors. The aim of this study was to examine the sporogonic development of four species of common European avian haemoproteids in the common biting midge Culicoides impunctatus.MethodsWild-caught females of C. impunctatus were infected experimentally by allowing them to take blood meals on naturally infected Muscicapa striata, Cyanistes caeruleus, Ficedula hypoleuca and Motacilla flava harbouring mature gametocytes of Haemoproteus balmorali (genetic lineage hSFC9), H. majoris (hPARUS1), H. motacillae (hYWT1) and H. pallidus (hPFC1), respectively. Infected insects were collected, maintained under laboratory conditions and dissected daily in order to detect the development of ookinetes, oocysts and sporozoites. Microscopic examination and polymerase chain reaction based methods were used to detect the parasites. Bayesian analysis was applied to identify phylogenetic relationships among Haemoproteus lineages.ResultsAll investigated parasites completed sporogony in C. impunctatus, indicating broad susceptibility of this biting midge for numerous Haemoproteus parasites. Ookinetes, oocysts and sporozoites were reported, described and compared morphologically. The investigated parasite species can be distinguished at the sporogony stage, particularly with regards to the morphology and rate of development of mature ookinetes. Analysis of data from the literature, and this study, shows that 12 genetically distantly related Haemoproteus parasites complete sporogony in C. impunctatus.ConclusionsSusceptibility of C. impunctatus is broad for Haemoproteus parasites, indicating that this biting midge is an important natural vector of numerous species of avian haemoproteids in Europe. Some Haemoproteus species can be readily distinguished using morphological characters of ookinetes and sporozoites, as well as the rate of ookinete development. These characters can be used for the identification of Haemoproteus species during sporogony in vectors, and are worth more attention in these parasite taxonomy studies at the species levels.
Highlights
Haemoproteus parasites are widespread, and some species cause disease in wild and domestic birds
Microscopic examination and PCR-based testing of wild-caught insects and birds All biting midges used in experiment belonged to C. impunctatus
Experimental birds were naturally infected with single Haemoproteus infections: M. striata was parasitized by H. balmorali (Fig. 1c-g), C. caeruleus by H. majoris (Fig. 1b-f), M. flava by H. motacillae (Fig. 1d-h) and F. hypoleuca by H. pallidus (Fig. 1a-e)
Summary
Haemoproteus parasites are widespread, and some species cause disease in wild and domestic birds. The insect vectors remain unknown for the majority of species and genetic lineages of avian Haemoproteus This information is crucial for better understanding the biology of haemoproteids, the epidemiology of haemoproteosis, and the development of morphological characters of sporogonic stages in wildlife haemosporidian parasites. The detection of infective sporozoites is required to prove that a given insect species can act as a vector This is a sensitive issue, due to the possibility of long-lasting abortive sporogonic development of Haemoproteus parasites in resistant insects. Recent experimental studies show that PCR-based diagnostics should be used carefully in vector studies because they can detect DNA of parasites in insects for several weeks after the initial infection They do not identify abortive sporogonic development and cannot prove if the insects are competent vectors of the parasites [11]
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