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Background: The globally transmitted avian malaria parasite Plasmodium relictum (lineage SGS1) has been found to infect hundreds of different bird species with differences in infection outcomes ranging from more or less latent to potentially mortal. However, to date basic knowledge about the links between genetic differentiation and variation in infection outcome within this single malaria parasite species is lacking. Methods: In this study, two different isolates of SGS1, obtained in the wild from two different host species, were used to investigate differences in their development in the blood and virulence in the experimentally infected canaries. Simultaneously, 258 kb of the parasite genome was screened for genetic differences using parasite mRNA and compared between experimental groups. Results: The two isolates showed differences in development and caused mortality as well as effects on the blood parameters of their hosts. Although previous studies using single genes have shown very limited within lineage genetic diversity in the European population of SGS1, 226 SNPs were found across 322 genes, which separated the two experimental groups with a total of 23 SNPs that were fixed in either of the experimental groups. Moreover, genetic variation was found within each experimental group, hinting that each avian malaria infection harbours standing genetic variation that might be selected during each individual infection episode. Conclusion: These results highlight extensive genetic variation within the SGS1 population that is transferred into individual infections, thus adding to the complexity of the infection dynamics seen in these host–parasite interactions. Simultaneously, the results open up the possibility of understanding how genetic variation within the parasite populations is linked to the commonly observed differences in infection outcomes, both in experimental settings and in the wild. Graphical : (Figure presented.).

Avian malaria parasites (Haemosporida, Plasmodium) are of cosmopolitan distribution, and they have a significant impact on vertebrate host fitness. Experimental studies show that high parasitemia often develops during primary malaria infections. However, field studies only occasionally reveal high parasitemia in free-living birds sampled using the traditional methods of mist-netting or trapping, and light chronic infections predominate. The reason for this discrepancy between field observation and experimental data remains insufficiently understood. Since mist-netting is a passive capture method, two main parameters determine its success in sampling infected birds in wildlife, i. e. the presence of parasitized birds at a study site and their mobility. In other words, the trapping probability depends on the survival rate of birds and their locomotor activity during infection. Here we test (1) the mortality rate of wild birds infected with Plasmodium relictum (the lineage pSGS1), (2) the changes in their behaviour during presence of an aerial predator, and (3) the changes in their locomotor activity at the stage of high primary parasitemia.We show that some behavioural features which might affect a bird's survival during a predator attack (time of reaction, speed of flush flight and take off angle) did not change significantly during primary infection. However, the locomotor activity of infected birds was almost halved compared to control (non-infected) birds during the peak of parasitemia. We report (1) the markedly reduced mobility and (2) the 20% mortality rate caused by P. relictum and conclude that these factors are responsible for the underrepresentation of birds in mist nets and traps during the stage of high primary parasitemia in wildlife. This study indicates that the widespread parasite, P. relictum (pSGS1) influences the behaviour of birds during primary parasitemia. Experimental studies combined with field observations are needed to better understand the mechanisms of pathogenicity of avian malaria parasites and their influence on bird populations.

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.

Several studies have shown associations between shorter telomere length in blood and weakened immune function, susceptibility to infections, and increased risk of morbidity and mortality. Recently, we have shown that malaria accelerates telomere attrition in blood cells and shortens lifespan in birds. However, the impact of infections on telomere attrition in different body tissues within an individual is unknown. Here, we tested whether malarial infection leads to parallel telomere shortening in blood and tissue samples from different organs. We experimentally infected siskins (Spinus spinus) with the avian malaria parasite Plasmodium ashfordi, and used realtime quantitative polymerase chain reaction (PCR) to measure telomere length in control and experimentally infected siskins. We found that experimentally infected birds showed faster telomere attrition in blood over the course of infection compared with control individuals (repeatedly measured over 105 days post-infection (DPI)). Shorter telomeres were also found in the tissue of all six major organs investigated (liver, lungs, spleen, heart, kidney, and brain) in infected birds compared with controls at 105 DPI. To the best of our knowledge, this is the first study showing that an infectious disease results in synchronous telomere shortening in the blood and tissue cells of internal organs within individuals, implying that the infection induces systemic stress. Our results have far-reaching implications for understanding how the short-term effects of an infection can translate into long-term costs, such as organ dysfunction, degenerative diseases, and ageing.

As bloodsuckers of birds, Culicoides biting midges (Diptera, Ceratopogonidae) play an important role in the transmission of avian haemosporidian (Haemoproteus) parasites, which are prevalent in many bird populations and cause disease, pathology, or even mortality in their hosts. Information about the role of the various Culicoides species in the transmission of Haemoproteus parasites remains insufficient. This presents an obstacle for the better understanding of the epizootiology of haemoproteosis. The aim of this study was to determine new Culicoides species involved in the transmission of Haemoproteus parasites in the wild. Biting midges were collected using UV traps on the Curonian Spit, Lithuania. Only parous Culicoides females were investigated: they were identified and were diagnosed for the presence of Haemoproteus parasites using both microscopy and PCR-based methods. We collected and dissected 420 parous Culicoides females. PCR-based screening showed that 28 parous Culicoides biting midges were infected with avian Haemoproteus parasites. Haemoproteid DNA was detected in Culicoides kibunensis, Culicoides pictipennis, Culicoides festivipennis, Culicoides segnis, Culicoides pallidicornis, and Culicoides obsoletus biting midges. The DNA of Haemoproteus palloris, genetic lineage hWW1, was found for the first time in C. pallidicornis. Haemoproteus sporozoites were detected in the salivary glands of two Culicoides segnis biting midges. According to the PCR results, one female contained Haemoproteus tartakovskyi (genetic lineage hHAWF1) DNA and another Haemoproteus majoris (genetic lineage hCCF5) DNA. The sporozoites of Haemoproteus parasites were also detected in the salivary glands of four C. pictipennis biting midges using microscopy, and this finding was confirmed by PCR as Haemoproteus parabelopolskyi DNA (genetic lineage hSYAT02) was detected in three out of the four biting midges. The obtained results supplement existing information about Culicoides biting midges as natural vectors of Haemoproteus spp. and add two new Culicoides species to the vector list, showing the low specificity of these parasites for the invertebrate hosts.

Background: Culicoides biting midges (Diptera, Ceratopogonidae) are known vectors of avian Haemoproteus parasites. These parasites cause diseases, pathology and even mortality in birds. The diversity of biting midges in Europe is great, but only four Culicoides species are known to be vectors of avian Haemoproteus parasites. In general, our knowledge about the role of the particular Culicoides species in the transmission of Haemoproteus parasites remains insufficient. Information gaps hinder a better understanding of parasite biology and the epizootiology of parasite-caused diseases. The aim of this study was to determine new Culicoides species involved in the transmission of Haemoproteus parasites. Methods: Biting midges were collected using a UV trap as well as sticky traps installed in bird nest boxes. Individual parous females were diagnosed for the presence of haemoproteids using both PCR-based and microscopic methods. Results: We collected and dissected 232 parous Culicoides females from 9 species using a UV trap and 293 females from 11 species from bird nest boxes. Culicoides obsoletus was the dominant species collected using a UV trap, and Culicoides kibunensis dominated among midges collected in nest boxes. PCR-based screening showed that 5.2% of parous biting midges collected using a UV trap and 4.4% of midges collected from nest boxes were infected with avian haemosporidian parasites. Haemoproteid DNA was detected in C. kibunensis, Culicoides pictipennis, Culicoides punctatus, Culicoides segnis and Culicoides impunctatus females. The sporozoites of Haemoproteus minutus (genetic lineages hTURDUS2 and hTUPHI01) were detected in the salivary glands of two C. kibunensis females using microscopy, and this finding was confirmed by PCR. Conclusions: Culicoides kibunensis was detected as a new natural vector of Haemoproteus minutus (hTURDUS2 and hTUPHI01). Haemoproteid DNA was detected in females from five Culicoides species. This study contributes to the epizootiology of avian Haemoproteus infections by specifying Culicoides species as vectors and species that are likely to be responsible for the transmission of haemoproteids in Europe.[Figure not available: see fulltext.].

The avian malaria parasite Plasmodium relictum (genetic lineage pGRW4) is known to cause severe pathology in nonadapted vertebrate hosts. This parasite is prevalent in some bird species in Northern Europe, however the records obtained are only from adult long-distance migrant birds after their return from the wintering grounds. A recent experimental study showed that this parasite completes sporogonic development in the local European vector Culex pipiens at a controlled mean temperature of 19 °C. Thereby, temperature limits for the transmission of this parasite in Northern Europe remain unknown. In this study, we took a step further and tested the impact of different temperature conditions, including some extreme fluctuations between 23 °C down to 7 °C, on the sporogonic development of P. relictum (pGRW4) in the vector Culex pipiens form molestus. Mosquitoes were exposed to infection and kept under different air-temperature conditions: (i) constant warm temperature, (ii) natural outdoor temperatures and (iii) temporary exposure to low temperatures. Plasmodium relictum (pGRW4) completed sporogony in mosquitoes of all experimental groups, however different patterns of the sporogonic development depending on temperature conditions were observed. Based on these results, we conclude that the cool air temperature of Northern Europe in summer is not a limiting factor in successful development of the parasite. However, delayed sporogony caused by low summer temperatures may have a detrimental impact on the active transmission of this parasite in Northern Europe.

Eurasian griffon vultures (Gyps fulvus) are endangered scavenger birds. Haemosporidian parasites infect the blood cells and organs of many avian species globally, using blood-sucking insect vectors, and they negatively affect health of birds and subsequently wildlife biodiversity. Fifty-nine vultures were admitted to the Greek wildlife rehabilitation center “ANIMA” and included in this study. Blood samples were collected, and the microscopy of stained blood smears was performed. Moreover, DNA was extracted, samples were screened for Leucocytozoon, Haemoproteus, and Plasmodium spp. following nested PCR protocols, and positive samples were sequenced. The detected haemosporidians are reported for the first time in Eurasian griffon vultures globally. The overall prevalence was 11.9% (Leucocytozoon spp. 5.1%, Haemoproteus spp. 5.1%, Plasmodium spp. 3.4%); this further corroborates the statement that the vultures’ immunity protects them from blood parasites. Notably, new genetic lineages of Leucocytozoon (GYPFUL02), Haemoproteus (GYPFUL01), and Plasmodium (GYPFUL03) species were recorded for the first time. Furthermore, it was the first molecular isolation of Haemoproteus in Old World vultures and Haemoproteus brachiatus was isolated for the first time from a vulture species. Moreover, this demonstrates the first record of Parahaemoproteus genetic lineages in vultures. Results highlight the genetic diversity of haemosporidians in griffon vultures and the need for additional studies.

Background Avian malaria parasites (genus Plasmodium ) are cosmopolitan and some species cause severe pathologies or even mortality in birds, yet their virulence remains fragmentally investigated. Understanding mechanisms and patterns of virulence during avian Plasmodium infections is crucial as these pathogens can severely affect bird populations in the wild and cause mortality in captive individuals. The goal of this study was to investigate the pathologies caused by the recently discovered malaria parasite Plasmodium homocircumflexum (lineage pCOLL4) in four species of European passeriform birds. Methods One cryopreserved P. homocircumflexum strain was multiplied and used for experimental infections. House sparrows ( Passer domesticus ), common chaffinches ( Fringilla coelebs ), common crossbills ( Loxia curvirostra ) and common starlings ( Sturnus vulgaris ) were exposed by subinoculation of infected blood. Experimental and control groups (8 individuals in each) were observed for over 1 month. Parasitaemia, haematocrit value and body mass were monitored. At the end of the experiment, samples of internal organs were collected and examined using histological and chromogenic in situ hybridization methods. Results All exposed birds were susceptible, with similar average prepatent period and maximum parasitaemia, yet virulence was different in different bird species. Mortality due to malaria was reported in chaffinches, house sparrows and crossbills (7, 5 and 3 individuals died respectively), but not in starlings. Exoerythrocytic meronts (phanerozoites) were observed in the brain of all dead experimental birds. Blockage of blood vessels in the brain led to cerebral ischaemia, invariably causing brain damage, which is likely the main reason of mortality. Phanerozoites were observed in parenchymal organs, heart and muscles of all infected individuals, except starlings. Conclusion This study shows that P. homocircumflexum is generalist and the same lineage caused similar parasitaemia-related pathologies in different host species. Additionally, the mode of exo-erythrocytic development is different in different birds, resulting in different mortality rates. This should be taken into consideration in studies addressing pathology during avian malaria infections.

BackgroundPlasmodium elongatum (cytochrome b lineage pGRW6) is a widespread avian malaria parasite, often causing severe disease in non-adapted hosts. This parasite lineage is of global distribution however, its virulence remains insufficiently understood, particularly in wild birds. Surprisingly, this infection has never been reported in Common starlings Sturnus vulgaris and Common crossbills Loxia curvirostra, common European songbirds which were extensively sampled across Europe. A hypothesis was proposed that these birds might be resistant to the pGRW6 infection. The aim of this study was to test this hypothesis.MethodsLineage pGRW6 was isolated from a naturally infected Eurasian reed warbler, multiplied in vivo and inoculated in Common starlings and Common crossbills. Experimental and control groups (8 birds in each) were maintained in controlled conditions and examined microscopically every 4days. Haematocrit value and body mass were monitored in parallel. At the end of the experiment (44days post exposure), samples of internal organs were collected and examined using histological methods for possible presence of phanerozoites.ResultsAll control birds remained uninfected. Experimental starlings were resistant. All exposed crossbills were susceptible and survived until the end of this study. Prepatent period was 12-16days post exposure. Light parasitaemia (<0.7%) developed in all birds, and only few phanerozoites were seen in bone marrow cells of 5 of 8 experimentally infected crossbills. Significant changes were reported only in haematocrit value but not body mass in the exposed crossbills compared to controls.ConclusionPlasmodium elongatum (pGRW6) is of low virulence in Common crossbills and is unable to develop in Common starlings, indicating innate resistance of the later bird species. Low virulence in Common crossbills is likely due to the inability or low ability of this parasite lineage to develop phanerozoites resulting in light (if at all) damage of stem bone marrow cells. This study suggests that susceptibility of different bird species to the lineage pGRW6 is markedly variable. The global distribution of this parasite might be due to low virulence in wild adapted avian hosts, which survive this infection and serve as reservoirs host for non-adapted birds in whom this infection is often lethal.