Unravelling the patterns of exo-erythrocytic development of Haemoproteus parasites (Haemoproteidae, Haemosporida), with a case of abortive tissue stages in a naturally infected bird.

Haemoproteus species (Haemosporida, Haemoproteidae) are cosmopolitan blood parasites that affect bird fitness and health. Recent discoveries based on the application of molecular markers showed that exo-erythrocytic or tissue stages of haemoproteids damage various internal organs including the brain. However, the patterns of exo-erythrocytic development remain unclear for most of the described species. This study aimed to understand the exo-erythrocytic development of Haemoproteus parasitesin naturally infected Thrush nightingales Luscinia luscinia (Muscicapidae). Infections were confirmed in eight bird individuals by microscopic examination and PCR-based methods. Organs were examined using histology and in situ hybridization, which applied genus-specific and lineage-specific oligonucleotideprobes targeting the 18S rRNA of the parasites. Exo-erythrocytic meronts of Haemoproteus attenuatus (lineage hROBIN1) were found and described for the first known time in this avian host. Most meronts were seen in the lungs, with a few also present in the liver, heart, and pectoral muscle. The available data suggest that this parasite produces only meronts, and not megalomeronts. However, numerous megalomeronts at different stages of development were observed in the gizzard and the heart of one individual. Based on the morphology, location in organs, and diagnostics using the lineage-specific probes, the megalomeronts were attributed to Haemoproteu smajoris (lineage hWW2). Two cases of empty capsular-like walls of megalomeronts were seen in the gizzard, indicating that the megalomeronts had already ruptured and degenerated. The extensive microscopic examination did not reveal gametocytes of H. majoris, obviously indicating an abortive development. Abortive haemosporidian infections were often speculated to occur in wildlife but have not been documented in naturally infected birds. This study recognised patterns in the exo-erythrocytic development of H. attenuatus, and is to our knowledge the first documentation of abortive Haemoproteus infection in a naturally infected bird during exo-erythrocytic development.

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Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.