Dataset Information

Blood parasites in Passeriformes in central Germany: prevalence and lineage diversity of Haemosporida (Haemoproteus, Plasmodium and Leucocytozoon) in six common songbirds.

ABSTRACT: Background:Avian Haemosporida are vector-borne parasites that commonly infect Passeriformes. Molecular analyses revealed a high number of different lineages and lineage specific traits like prevalence and host-specificity, but knowledge of parasite prevalence and lineage diversity in wild birds in Central Germany is still lacking. Results:Blood samples from a total of 238 adult and 122 nestling songbirds belonging to six species were investigated for infections with avian haemosporidian genera and lineages (Haemoproteus spp., Plasmodium spp., Leucocytozoon spp.) and Trypanosoma avium using PCR, targeting the parasite mitochondrial cytochrome b gene and 18S ribosomal RNA. In total, the prevalence in adult birds was 31.3% infected with Haemoproteus, 12.5% with Plasmodium and 71.0% with Leucocytozoon (nestlings excluded). None of the tested birds was infected with Trypanosoma avium. Only in two nestling birds, aged 12-17 days, a Leucocytozoon spp. infection was proven. Among 225 successfully sequenced samples, we found four Haemoproteus, three Plasmodium and 19 Leucocytozoon lineages, including two new Leucocytozoon lineages. Furthermore, we report two new host-lineage associations. Conclusions:As first study investigating avian haemosporidian parasites in Central Germany, we provide new information on genetic diversity of Haemosporida infecting Passeriformes. We show that even with a small sample size new lineages as well as previously unknown linkages between certain lineages and host species can be detected. This may help to elucidate the diversity of lineages as well as lineage-host-connections of avian Haemosporida.

SUBMITTER: Schumm YR

PROVIDER: S-EPMC6360073 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Blood parasites in Passeriformes in central Germany: prevalence and lineage diversity of Haemosporida (<i>Haemoproteus</i>, <i>Plasmodium</i> and <i>Leucocytozoon</i>) in six common songbirds.

Schumm Yvonne R YR Wecker Christine C Marek Carina C Wassmuth Mareike M Bentele Anna A Willems Hermann H Reiner Gerald G Quillfeldt Petra P

PeerJ 20190131

<h4>Background</h4>Avian Haemosporida are vector-borne parasites that commonly infect Passeriformes. Molecular analyses revealed a high number of different lineages and lineage specific traits like prevalence and host-specificity, but knowledge of parasite prevalence and lineage diversity in wild birds in Central Germany is still lacking.<h4>Results</h4>Blood samples from a total of 238 adult and 122 nestling songbirds belonging to six species were investigated for infections with avian haemospo ...[more]

PMID: 30723612

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Project description:BackgroundHaemoproteus is a sister genus to malaria parasites (Plasmodium), which both belong to the order Haemosporida (Apicomplexa). Parasites of both genera are flourishing in birds, however, Haemoproteus species are noticeably less investigated. This is unfortunate because knowledge about close relatives of malaria pathogens is important for better understanding the evolutionary origin and basic biological features of the entire group of haemosporidian infections. Moreover, recent findings show that Haemoproteus species can cause severe damage of various bird organs due to megalomeronts and other exo-erythrocytic stages. These haemosporidians are remarkably diverse, but remain neglected partly due to difficulties in species identification. Hundreds of Haemoproteus genetic lineages have been reported in birds, and numerous new lineages are found each year, but most remain unidentified to the species level. Numerous new Haemoproteus pathogens were described during the past 20 years. However, keys for their identification are absent. Identification of Haemoproteus species remains a difficult task and is an obstacle for better understanding of the distribution and epidemiology of these parasites. This study aimed to develop comprehensive keys for the identification of described avian Haemoproteus species using morphological features of their blood stages (gametocytes).MethodsType and voucher preparations of avian Haemoproteus species were accessed in museums in Europe, Australia and the USA. Gametocytes of most described species were examined, and these data formed a background for this study. The data also were considered from published articles containing parasite species descriptions. The method of dichotomous keys was applied. The most difficult steps in the keys were accompanied with references to the corresponding parasite pictures.ResultsIn all, 201 published articles were included in this review. Morphological diagnostic features of gametocytes of all described Haemoproteus species were analysed and compared. Illustrated keys for identification of these parasite species were developed. Available information about the molecular characterization of Haemoproteus parasites was provided.ConclusionThis review shows that 177 described species of avian Haemoproteus can be distinguished and identified in blood films using morphological characters of their gametocytes and host cells. These species were incorporated in the keys. Information about possible morphologically cryptic parasites was provided. Molecular markers are available for only 42% of the described Haemoproteus parasites, calling for researchers to fill this gap.

Project description:Leucocytozoon parasites (Haemosporida, Leucocytozoidae) are haemosporidians whose diversity, exo-erythrocytic development and potential vectors are the least studied. The knowledge about their exo-erythrocytic development and pathogenicity is fragmentary, resulting in an incomplete comprehension of the impact of these parasites on avian hosts. For a long time, Leucocytozoon infections were considered benign to wild birds, even though they were virulent in poultry and responsible for some wild bird population declines. This study aimed to investigate the presence of Leucocytozoon species exo-erythrocytic stages in song thrushes Turdus philomelos using conventional histological techniques (sections stained by H&E) and chromogenic in situ hybridization (CISH). Tissues from ten birds (seven naturally infected and three opportunistic samplings) were examined using both methods. Parasite lineages were identified from blood samples using PCR-based techniques. Leucocytozoon species meronts were found in five individuals (in four birds using H&E staining protocol, and in three in CISH-treated histological sections). Meronts were found mainly in the kidneys, but some meronts were also present in the lungs. It was possible to observe different maturation stages of meronts in the same bird individual, indicating an asynchronous development. Cytomeres were readily visible in developing meronts. One megalomeront-like structure was present close to a blood vessel in the heart. It was covered with a prominent capsular-like wall. No inflammatory reaction or necrosis was seen in the tissues surrounding the meronts or the megalomeront-like structure. We could confirm the transmission of three Leucocytozoon lineages (lTUPHI14, lSTUR1 and lTUPHI13) in Europe, and add evidence of the transmission of two Plasmodium lineages, including Plasmodium circumflexum (pTURDUS1), and Haemoproteus asymmetricus (hTUPHI01). We call for further research to better understand Leucocytozoon parasite exo-erythrocytic development.

Project description:BackgroundAvian haemosporidian parasites can cause severe disease in their hosts due to excessive exo-erythrocytic merogony and anaemia caused by blood stages. Notably, the development of megalomeronts by species of Haemoproteus and Leucocytozoon has been associated with mortalities in birds. Diagnosis of lethal infections is currently accomplished by the detection of parasites' tissue stages in histological sections combined with PCR and sequencing. However, sequences frequently are not reliably obtained and the generic discrimination of exo-erythrocytic tissue stages based on morphological characters is challenging. Therefore, the present study aimed at developing specific molecular probes for the identification of Haemoproteus spp. and Leucocytozoon spp. in histological sections using chromogenic in situ hybridization.MethodsParasite subgenus-specific oligonucleotide probes were designed to target the 18S ribosomal RNA of Haemoproteus species (subgenus Parahaemoproteus) and Leucocytozoon spp. (subgenus Leucocytozoon) and were in situ hybridized to sections from formalin-fixed, paraffin-embedded tissue samples determined positive for these parasites by PCR and histopathology. To confirm the presence of parasites at sites of probe hybridization, consecutive sections were stained with haematoxylin-eosin and examined.ResultsParahaemoproteus- and Leucocytozoon-specific probes labelled erythrocytic and exo-erythrocytic stages of Haemoproteus spp. and Leucocytozoon spp., respectively. Binding of probes to parasites was consistent with detection of the same exo-erythrocytic meronts in consecutive haematoxylin-eosin-stained sections. Cross-reactivity of the probes was ruled out by negative chromogenic in situ hybridization when applied to samples positive for a parasite of a genus different from the probes' target.ConclusionsChromogenic in situ hybridization using 18S ribosomal RNA-specific oligonucleotide probes reliably identifies and discriminates Haemoproteus and Leucocytozoon parasites in tissue sections and enables unequivocal diagnosis of haemosporidioses.

Project description:BackgroundA high prevalence of parasites may result from life-long persistence of infection or from high reinfection rates. We have studied blood parasites in a breeding population of the accipitrid raptor, Eurasian sparrowhawk (Accipiter nisus), to determine parasite diversity and turnover.MethodsDuring this 7-year study, 210 adult Eurasian sparrowhawks breeding in the city of Prague were checked for parasites using several diagnostic methods.ResultsIn both female and male raptors, parasites of the genus Leucocytozoon were the most prevalent (92% and 85%, respectively) followed in decreasing order of prevalence by those of genus Trypanosoma (74% and 68%, respectively) and genus Haemoproteus (46% and 16%, respectively). The prevalence of all parasites increased with age in both sexes, with the females at each respective age having the higher prevalence. There was a positive association between Haemoproteus and Leucocytozoon infections. Persistence at the individual level was higher than incidence for Trypanosoma and Haemoproteus. In the case of Leucocytozoon and Trypanosoma, most individuals probably become infected in their first year of life or even before dispersal from the nest. The detected parasites belonged to Trypanosoma avium sensu stricto, Leucocytozoon sp. (haplotypes ACNI1 and ACNI3) and Leucocytozoon mathisi (haplotype ACNI4) and two new lineages of the Haemoproteus elani complex (ACCNIS6 and ACCNIS7). Detailed analysis of parasite lineages in individuals that were repeatedly sampled revealed lineage turnover that would otherwise remain hidden. Phylogenetic analysis revealed that the detected Haemoproteus belongs to a phylogenetically distant group whose taxonomic position requires further analysis.ConclusionsAll three genera of blood parasites persist in infected individuals, thus enabling sustainability of vector transmission cycles. Prevalence increases with age; however, there is a high turnover of Leucocytozoon lineages. No clear evidence of parasite-induced mortality was found, and most of the individuals were infected early in life, particularly in the case of Leucocytozoon.

Project description:BackgroundHaemoproteus (Parahaemoproteus) species (Haemoproteidae) are widespread blood parasites that can cause disease in birds, but information about their vector species, sporogonic development and transmission remain fragmentary. This study aimed to investigate the complete sporogonic development of four Haemoproteus species in Culicoides nubeculosus and to test if phylogenies based on the cytochrome b gene (cytb) reflect patterns of ookinete development in haemosporidian parasites. Additionally, one cytb lineage of Haemoproteus was identified to the species level and the in vitro gametogenesis and ookinete development of Haemoproteus hirundinis was characterised.MethodsLaboratory-reared C. nubeculosus were exposed by allowing them to take blood meals on naturally infected birds harbouring single infections of Haemoproteus belopolskyi (cytb lineage hHIICT1), Haemoproteus hirundinis (hDELURB2), Haemoproteus nucleocondensus (hGRW01) and Haemoproteus lanii (hRB1). Infected insects were dissected at intervals in order to detect sporogonic stages. In vitro exflagellation, gametogenesis and ookinete development of H. hirundinis were also investigated. Microscopic examination and PCR-based methods were used to confirm species identity. Bayesian phylogenetic inference was applied to study the relationships among Haemoproteus lineages.ResultsAll studied parasites completed sporogony in C. nubeculosus. Ookinetes and sporozoites were found and described. Development of H. hirundinis ookinetes was similar both in vivo and in vitro. Developing ookinetes of this parasite possess long outgrowths, which extend longitudinally and produce the apical end of the ookinetes. A large group of closely related Haemoproteus species with a similar mode of ookinete development was determined. Bayesian analysis indicates that this character has phylogenetic value. The species identity of cytb lineage hDELURB2 was determined: it belongs to H. hirundinis.ConclusionsCulicoides nubeculosus is susceptible to and is a likely natural vector of numerous species of Haemoproteus parasites, thus worth attention in haemoproteosis epidemiology research. Data about in vitro development of haemoproteids provide valuable information about the rate of ookinete maturation and are recommended to use as helpful step during vector studies of haemosporidian parasites, particularly because they guide proper dissection interval of infected insects for ookinete detection during in vivo experiments. Additionally, in vitro studies readily identified patterns of morphological ookinete transformations, the characters of which are of phylogenetic value in haemosporidian parasites.

Dataset Information

Blood parasites in Passeriformes in central Germany: prevalence and lineage diversity of Haemosporida (Haemoproteus, Plasmodium and Leucocytozoon) in six common songbirds.

Publications

Blood parasites in Passeriformes in central Germany: prevalence and lineage diversity of Haemosporida (<i>Haemoproteus</i>, <i>Plasmodium</i> and <i>Leucocytozoon</i>) in six common songbirds.

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