Natural Vector of Avian Haemoproteus asymmetricus Parasite and Factors Altering the Spread of Infection.

Simple Summary: Avian haemoproteids are prevalent parasites known to induce pathology or mortality in birds. Culicoides biting midges act as vectors for these parasites. Despite the annual arrival of various haemoproteids to Europe with migrant birds, not all these parasites undergo local transmission. The factors constraining the local spread of these pathogens remain incompletely understood. Our study investigates if the ecological isolation of birds from vectors, either temporally or spatially during the breeding period when transmission occurs, could lead to the cessation of transmission. Biting midges were systematically collected from two distinct habitats between May and September. A total of 1135 parous Culicoides females were identified and examined for the presence of Haemoproteus parasites using both microscopy and molecular tools. Notably, we report the first detection of Haemoproteus asymmetricus sporozoites in the salivary glands of Culicoides festivipennis females. The sporozoites of four Haemoproteus genetic lineages were also identified in Culicoides segnis, C. festivipennis, and C. kibunensis, further validating their status as potential Haemoproteus vectors. While the highest abundance of collected Culicoides females occurred in June, the peak prevalence of Haemoproteus parasites in biting midges was observed in July. Interestingly, the abundance of Culicoides was significantly greater in woodlands compared to reeds throughout the season. Avian haemosporidians (Apicomplexa, Haemosporida) are widespread blood protists, often causing severe haemosporidiosis, pathology, or even mortality in their hosts. Migrant birds regularly bring various haemosporidian parasites from wintering grounds to European breeding areas. Some haemosporidian parasites are prevalent in breeding sites and complete their life cycles in temperate climate zones and can be transmitted, but others do not. The factors altering the spread of these haemosporidians are not fully understood. Culicoides biting midges (Diptera: Ceratopogonidae) play an important role in the transmission of worldwide distributed avian haemosporidian parasites belonging to the genus Haemoproteus, but this information is particularly scarce and insufficient. The key factors limiting the spread of these pathogens in temperate climate zones, which we suspect and aim to study, are the absence of susceptible vectors and the ecological isolation of birds from vectors during the breeding period when transmission occurs. The primary objective of this study was to evaluate how the habitats of biting midges and bird breeding sites influence parasite transmission while also seeking to expand our understanding of the natural vectors for these parasites. Biting midges were collected using UV traps on the Curonian Spit, Lithuania, in different habitats, such as woodland and reeds, from May to September. Parous Culicoides females were identified, dissected, and investigated for the presence of Haemoproteus parasites using both microscopy and PCR-based tools. Among the dissected 1135 parous Culicoides females, the sporozoites of Haemoproteus asymmetricus (genetic lineage hTUPHI01) have been detected for the first time in the salivary glands of Culicoides festivipennis. The sporozoites of four Haemoproteus lineages were detected in Culicoides segnis, C. festivipennis, and Culicoides kibunensis biting midges. PCR-based screening showed that the females of seven Culicoides species were naturally infected with Haemoproteus parasites. The DNA of the parasite of owls, Haemoproteus syrnii (hSTAL2), was detected for the first time in Culicoides punctatus. The highest abundance of collected Culicoides females was in June, but the highest prevalence of Haemoproteus parasites in biting midges was in July. The abundance of Culicoides was higher in the woodland compared with reeds during the season. The acquired findings indicate the varied abundance and diversity of biting midges throughout the season and across distinct habitats. This variability could potentially impact the transmission of Haemoproteus parasites among birds with diverse breeding site ecologies. These outcomes hold the potential to enhance our understanding of the epizootiology of Haemoproteus infections within temperate climatic zones. [ABSTRACT FROM AUTHOR]