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

Abstract

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.

Raising the bar: genus-specific nested PCR improves detection and lineage identification of avian haemosporidian parasites

“…The standard nested PCR method remains the method of choice in the most recent studies conducted (e.g. Žiegytė et al., 2023 ; González-Olvera et al., 2023 ; Han et al., 2023 ). It was only complemented by the utilization of multiplex PCRs ( Pacheco et al., 2018b ; Ciloglu et al., 2019 ) in some studies (e.g.…”

High Abundance of Haemoproteus Parasites in Culicoides (Diptera, Ceratopogonidae), with a Confirmation of Culicoides reconditus as a New Vector of These Avian Blood Parasites

“…Some Culicoides species can be considered as rare in Lithuania, such as C. fagineus , C. albicans , C. fascipennis , C. newsteadi , C. chiopterus , and C. deltus [ 10 , 12 , 13 , 14 ]. None of these species were collected in the present study.…”

“…The main reason being the necessity to use an integrative approach, which consists of a combination of classical parasitology (with insect dissection and microscopic examination to confirm the presence of sporozoites) with molecular methods (to obtain the parasite DNA and confirm its species and lineage) [ 9 ]. Until now, such an approach was only used by a few research groups in the haemosporidian field, mainly in Europe [ 8 , 10 , 11 , 12 , 13 , 14 ].…”

“…Currently, only nine Haemoproteus species (5.1% of the described ones) and 11 lineages (0.5% of the described ones) have had their natural vectors identified [ 10 , 11 , 12 , 13 , 14 ]. This represents a small proportion of the existing parasite species and lineages and shows the huge gap that needs to be filled in the Haemoproteus–Culicoides system.…”

“…In wild-caught and naturally infected Culicoides , from the 1347 described existing species [ 15 ], only five were confirmed to support the sporogonic development of Haemoproteus , all of them in Europe, namely C. pictipennis , C. festivipennis , C. segnis , C. kibunensis , and C. punctatus [ 10 , 11 , 12 , 13 , 14 ]. Previous studies have experimentally addressed this issue and showed that 11 other Culicoides species can support the sporogonic development of Haemoproteus [ 16 ].…”