Parasite Prevalence Corresponds to Host Life History in a Diverse Assemblage of Afrotropical Birds and Haemosporidian Parasites

Avian host life history traits have been hypothesized to predict rates of infection by haemosporidian parasites. Using molecular techniques, we tested this hypothesis for parasites from three haemosporidian genera (Plasmodium, Haemoproteus, and Leucocytozoon) collected from a diverse sampling of birds in northern Malawi. We found that host life history traits were significantly associated with parasitism rates by all three parasite genera. Nest type and nest location predicted infection probability for all three parasite genera, whereas flocking behavior is an important predictor of Plasmodium and Haemoproteus infection and habitat is an important predictor of Leucocytozoon infection. Parasite prevalence was 79.1% across all individuals sampled, higher than that reported for comparable studies from any other region of the world. Parasite diversity was also exceptionally high, with 248 parasite cytochrome b lineages identified from 152 host species. A large proportion of Plasmodium, Haemoproteus, and Leucocytozoon parasite DNA sequences identified in this study represent new, previously undocumented lineages (n = 201; 81% of total identified) based on BLAST queries against the avian malaria database, MalAvi.     

The occurrence of haemosporidian parasites in the Fennoscandian bluethroat ( Luscinia svecica) population

A total of 86 adult bluethroats (Luscinia svecica) from nine different localities, covering the full length of the Fennoscandian mountain range, were screened for blood parasites of the three genera Haemoproteus, Plasmodium and Leucocytozoon using a recently developed polymerase chain reaction method. The overall occurrence of infection was 59.3%. Prevalence of Leucocytozoon spp. (47.7%), Plasmodium spp. (23.3%) and Haemoproteus spp. (1.2%) was detected. Of the infected birds, 15.1% carried mixed infections. Five different mitochondrial DNA-lineages of Leucocytozoon spp., eight lineages of Plasmodium spp. and one lineage of Haemoproteus spp. were found. Due to large sequence divergence these corresponded to at least five different species, but with the possibility of all 14 being independent evolutionary units with the potential of evolving different effects on the host. Of the lineages of Leucocytozoon spp., the most common was found throughout the range. The occurrence of the second most common lineage of Leucocytozoon spp. showed significant variation in prevalence between sites. The data also showed molecular evidence of one lineage of Leucocytozoon sp. existing in more than one species of avian host, thus challenging the use of host taxon as a taxonomic character when distinguishing between different species leucocytozoids.Communicated by F. Bairlein     

Haemosporidian prevalence,parasitaemia and aggregation in relation to avian assemblage life history traits at different elevations

The transmission of vector-borne protozoa such as parasites of the Order Haemosporida is dependent on both biotic and abiotic factors such as host life history traits and environmental conditions. This study aimed to identify the variables that determine haemosporidian prevalence, parasitaemia and aggregation within the context of elevation and avian life history traits in Central Veracruz, Mexico. We sampled 607 birds from 88 species; we used microscopy and the mtDNA cytochrome b gene to detect parasites. We found an overall prevalence of 32.3%. Haemosporidian prevalence was 21.6% in tropical sub-deciduous forest (at sea level), 38% in tropical deciduous forest (265 m above sea level (asl)), 19.4% in montane cloud forest (1630 m asl), and 51.7% in pine-oak forest (2790 m asl). The prevalence of each parasite genus was strongly influenced by elevation (a proxy of habitat type). Plasmodium showed the highest prevalence at low elevation. Haemoproteus increased in prevalence with elevation. Leucocytozoon displayed the highest prevalence at the highest elevation (pine-oak forest). Haemoproteus spp. and Leucocytozoon spp. prevalences were higher in open cup than in closed nests. Haemoproteus prevalence and haemosporidian parasitaemia were lower in solitary birds than birds with pairing and gregarious behavior. Haemosporidian aggregation decreased with elevation, yielding the significantly lowest values at the pine-oak forest. Elevation distribution patterns of prevalence for each genus were similar to those previously reported in other geographical areas (e.g., South America, Europe).     

Robust geographical determinants of infection prevalence and a contrasting latitudinal diversity gradient for haemosporidian parasites in Western Palearctic birds

Identifying robust environmental predictors of infection probability is central to forecasting and mitigating the ongoing impacts of climate change on vector‐borne disease threats. We applied phylogenetic hierarchical models to a data set of 2,171 Western Palearctic individual birds from 47 species to determine how climate and landscape variation influence infection probability for three genera of haemosporidian blood parasites (Haemoproteus, Leucocytozoon, and Plasmodium). Our comparative models found compelling evidence that birds in areas with higher vegetation density (captured by the normalized difference vegetation index [NDVI]) had higher likelihoods of carrying parasite infection. Magnitudes of this relationship were remarkably similar across parasite genera considering that these parasites use different arthropod vectors and are widely presumed to be epidemiologically distinct. However, we also uncovered key differences among genera that highlighted complexities in their climate responses. In particular, prevalences of Haemoproteus and Plasmodium showed strong but contrasting relationships with winter temperatures, supporting mounting evidence that winter warming is a key environmental filter impacting the dynamics of host‐parasite interactions. Parasite phylogenetic community diversities demonstrated a clear but contrasting latitudinal gradient, with Haemoproteus diversity increasing towards the equator and Leucocytozoon diversity increasing towards the poles. Haemoproteus diversity also increased in regions with higher vegetation density, supporting our evidence that summer vegetation density is important for structuring the distributions of these parasites. Ongoing variation in winter temperatures and vegetation characteristics will probably have far‐reaching consequences for the transmission and spread of vector‐borne diseases.     

Migratory birds have higher prevalence and richness of avian haemosporidian parasites than residents

Individuals of migratory species may be more likely to become infected by parasites because they cross different regions along their route, thereby being exposed to a wider range of parasites during their annual cycle. Conversely, migration may have a protective effect since migratory behaviour allows hosts to escape environments presenting a high risk of infection. Haemosporidians are one of the best studied, most prevalent and diverse groups of avian parasites, however the impact of avian host migration on infection by these parasites remains controversial. We tested whether migratory behaviour influenced the prevalence and richness of avian haemosporidian parasites among South American birds. We used a dataset comprising ~ 11,000 bird blood samples representing 260 bird species from 63 localities and Bayesian multi-level models to test the impact of migratory behaviour on prevalence and lineage richness of two avian haemosporidian genera (Plasmodium and Haemoproteus). We found that fully migratory species present higher parasite prevalence and higher richness of haemosporidian lineages. However, we found no difference between migratory and non-migratory species when evaluating prevalence separately for Plasmodium and Haemoproteus, or for the richness of Plasmodium lineages. Nevertheless, our results indicate that migratory behaviour is associated with an infection cost, namely a higher prevalence and greater variety of haemosporidian parasites.     

Impacts of selective logging on haemosporidian infection and physiological correlates in tropical birds

Tropical forest degradation affects host-parasite interactions, determining the probability of animals acquiring an infection. The activation of an immune response to fight off infections requires energy and other resources such as antioxidants which may be redirected from growth and reproduction. A key question is how selective logging—the most common form of tropical forest degradation—impacts the prevalence of avian haemosporidian infection and its correlated physiological responses (nutritional and oxidative status markers). We investigated the prevalence of Plasmodium, Haemoproteus, and Leucocytozoon parasites in 14 understorey bird species in lowland, logged and unlogged, old-growth forests of Borneo. Prevalences of infections were similar between selectively logged and unlogged forests. To explore nutritional and oxidative status effects of haemosporidian infections, we examined associations between infections and plasma proteins, plasma triglycerides, and multiple blood-based markers of oxidative status, testing for an impact of selective logging on those markers. Birds infected with Plasmodium showed higher levels of plasma proteins and non-enzymatic antioxidant capacity, and lower levels of plasma triglycerides and glutathione, compared with haemosporidian-free individuals. Conversely, birds infected with Haemoproteus showed no changes in nutritional or physiological markers compared with uninfected individuals. These results indicate higher metabolic and physiological costs of controlling Plasmodium infection, compared with Haemoproteus, possibly due to higher pathogenicity of Plasmodium. Selectively logged forests had no effect on the responses of birds to infection, suggesting that the environmental conditions of degraded forests do not appear to induce any appreciable physiological demands in parasitised birds.     

Seasonal dynamics in mosquito abundance and temperature do not influence avian malaria prevalence in the Himalayan foothills

We examined seasonal prevalence in avian haemosporidians (Plasmodium and Haemoproteus) in migrant and resident birds in western Himalaya, India. We investigated how infection with haemosporidians in avian hosts is associated with temporal changes in temperature and mosquito abundance along with host abundance and life‐history traits (body mass). Using molecular methods for parasite detection and sequencing partial cytochrome b gene, 12 Plasmodium and 27 Haemoproteus lineages were isolated. Our 1‐year study from December 2008 to December 2009 in tropical Himalayan foothills revealed a lack of seasonal variation in Plasmodium spp. prevalence in birds despite a strong correlation between mosquito abundance and temperature. The probability of infection with Plasmodium decreased with increase in temperature. Total parasite prevalence and specifically Plasmodium prevalence showed an increase with average avian body mass. In addition, total prevalence exhibited a U‐shaped relationship with avian host abundance. There was no difference in prevalence of Plasmodium spp. or Haemoproteus spp. across altitudes; parasite prevalence in high‐altitude locations was mainly driven by the seasonal migrants. One Haemoproteus lineage showed cross‐species infections between migrant and resident birds. This is the first molecular study in the tropical Himalayan bird community that emphasizes the importance of studying seasonal variation in parasite prevalence. Our study provides a basis for further evolutionary study on the epidemiology of avian malaria and spread of disease across Himalayan bird communities, which may not have been exposed to vectors and parasites throughout the year, with consequential implications to the risk of infection to naïve resident birds in high altitude.     

Insights on the taxonomy of Haemoproteus parasites infecting cracid birds

The Haemosporida order is a well-supported clade of heteroxenous parasites transmitted by dipteran insects and frequently found parasitizing wild birds. These parasites have already been reported in all zoogeographic regions of the world, except for Antarctica. One of the potential hosts of haemosporidians is the Cracidae family, which includes approximately 50 species, 22 of which are present in Brazil, classified within nine genera. Data on haemosporidian infecting individuals of the Cracidae family is scarce, with only three Haemoproteus species being recorded in this group of birds. We found Haemoproteus spp. infection in all Penelope obscura bronzina analyzed. Among the parasites found, we observed two lineages of Haemoproteus (PENOBS02 and PENOBS03), which were characterized by morphological, molecular and phylogenetic approaches. The morphological data on cracid haemosporidian parasites, together with our phylogenetic results, allows discussions on the taxonomy of the Haemoproteus parasites that infect birds of the Cracidae family.     

Complex interactions between bacteria and haemosporidia in coinfected hosts: An experiment

1. Hosts are typically coinfected by multiple parasite species whose interactions might be synergetic or antagonistic, producing unpredictable physiological and pathological impacts on the host. This study shows the interaction between Plasmodium spp. and Leucocytozoon spp. in birds experimentally infected or not infected with Mycoplasma gallisepticum.
2. In 1994, the bacterium Mycoplasma gallisepticum jumped from poultry to wild birds in which it caused a major epidemic in North America. Birds infected with M. gallisepticum show conjunctivitis as well as increased levels of corticosterone.
3. Malaria and other haemosporidia are widespread in birds, and chronic infections become apparent with the detectable presence of the parasite in peripheral blood in response to elevated levels of natural or experimental corticosterone levels.
4. Knowing the immunosuppressive effect of corticosterone on the avian immune system, we tested the hypothesis that chronic infections of Plasmodium spp. and Leucocytozoon spp. in house finches would respond to experimental inoculation with M. gallisepticum as corticosterone levels are known to increase following inoculation.
5. Plasmodium spp. infection intensity increased within days of M. gallisepticum inoculation as shown both by the appearance of infected erythrocytes and by the increase in the number and the intensity of positive PCR tests.
6. Leucocytozoon spp. infection intensity increased when Plasmodium spp. infection intensity increased, but not in response to M. gallisepticum inoculation. Leucocytozoon spp. and Plasmodium spp. seemed to compete in the host as shown by a negative correlation between the changes in their PCR score when both pathogens were present in the same individual.
7. Host responses to coinfection with multiple pathogens measured by the hematocrit and white blood cell count depended on the haemosporidian community composition. Host investment in the leukocyte response was higher in the single‐haemosporidia‐infected groups when birds were infected with M. gallisepticum.
8. A trade‐off was observed between the immune control of the chronic infection (Plasmodium spp./Leucocytozoon spp.) and the immune response to the novel bacterial infection (M. gallisepticum).

     

Distribution,diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations

Avian species are commonly infected by multiple parasites, however few studies have investigated the environmental determinants of the prevalence of co-infection over a large scale. Here we believe that we report the first, detailed ecological study of the prevalence, diversity and co-infections of four avian blood-borne parasite genera: Plasmodium spp., Haemoproteus spp., Leucocytozoon spp. and Trypanosoma spp. We collected blood samples from 47 resident and migratory bird species across a latitudinal gradient in Alaska. From the patterns observed at collection sites, random forest models were used to provide evidence of associations between bioclimatic conditions and the prevalence of parasite co-infection distribution. Molecular screening revealed a higher prevalence of haematozoa (53%) in Alaska than previously reported. Leucocytozoons had the highest diversity, prevalence and prevalence of co-infection. Leucocytozoon prevalence (35%) positively correlated with Trypanosoma prevalence (11%), negatively correlated with Haemoproteus prevalence (14%) and had no correlation with Plasmodium prevalence (7%). We found temperature, precipitation and tree cover to be the primary environmental drivers that show a relationship with the prevalence of co-infection. The results provide insight into the impacts of bioclimatic drivers on parasite ecology and intra-host interactions, and have implications for the study of infectious diseases in rapidly changing environments.     

A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data

Biogeographic patterns of parasite diversity are useful for determining how host–parasite interactions can influence speciation. However, variation in methodologies and sampling effort can skew diversity estimates. Avian haemosporidians are vector-transmitted blood parasites represented by over 1300 unique genetic lineages spread across over 40 countries. We used a global database of lineage distributions for two avian haemosporidian genera, Plasmodium and Haemoproteus, to test for congruence of diversity among haemosporidians and their avian hosts across 13 geographic regions. We demonstrated that avian haemosporidians exhibit similar diversity patterns to their avian hosts; however, specific patterns differ between genera. Haemoproteus spp. diversity estimates were significantly higher than those of Plasmodium spp. in all areas where the genera co-occurred, apart from the Plasmodium spp.-rich region of South America. The geographic distributions of parasite genera also differed, with Haemoproteus spp. absent from the majority of oceanic regions while Plasmodium spp. were cosmopolitan. These findings suggest fundamental differences in the way avian haemosporidians diverge and colonise new communities. Nevertheless, a review of the literature suggests that accurate estimates of avian haemosporidian diversity patterns are limited by (i) a concentration of sampling towards passerines from Europe and North America, (ii) a frequent failure to include microscopic techniques together with molecular screening and (iii) a paucity of studies investigating distributions across vector hosts.     

High prevalence of haemosporidians in Reed Warbler Acrocephalus scirpaceus and Sedge Warbler Acrocephalus schoenobaenus in Spain

Apicomplexan blood parasites (genera Haemoproteus, Plasmodium and Leucocytozoon) prevalence in two related species (Reed Warbler Acrocephalus scirpaceus and Sedge Warbler A. schoenobaenus) was studied in 2006 at the Natural Reserve of Castronu?o-Vega del Duero, Western Spain, a stopover area during the autumn migration. A fragment of the mitochondrial cytochrome b gene of the parasites was amplified, using a nested PCR assay, from avian blood samples. High prevalence of malaria parasites was found in both species, 84.6% in Reed Warbler and 71.8% in Sedge Warbler, and the degree of infection reach 100% of the population that breed at the Reserve, suggesting good conditions for the development of dipteran vectors in this area. By sequencing 464 nucleotides of the obtained fragments, we found four different mitochondrial haplotypes of Haemoproteus or Plasmodium in the two species analysed. Leucocytozoon infection was not detected, in contrast to the high prevalence of this parasite in other avian species in Spain, probably because the water course studied is not an adequate habitat for its vectors.     

Host specificity of avian haemosporidian parasites is unrelated among sister lineages but shows phylogenetic signal across larger clades

Parasites can vary in the number of host species they infect, a trait known as “host specificity”. Here we quantify phylogenetic signal—the tendency for closely related species to resemble each other more than distantly related species—in host specificity of avian haemosporidian parasites (genera Plasmodium, Haemoproteus and Leucocytozoon) using data from MalAvi, the global avian haemosporidian database. We used the genetic data (479 base pairs of cytochrome b) that define parasite lineages to produce genus level phylogenies. Combining host specificity data with those phylogenies revealed significant levels of phylogenetic signal while controlling for sampling effects; phylogenetic signal was higher when the phylogenetic diversity of hosts was taken into account. We then tested for correlations in the host specificity of pairs of sister lineages. Correlations were generally close to zero for all three parasite genera. These results suggest that while the host specificity of parasite sister lineages differ, larger clades may be relatively specialised or generalised.     

The first report of nine species of haemosporidian parasites (Haemosporida: <Emphasis Type="Italic">Haemoproteus,Plasmodium</Emphasis> and <Emphasis Type="Italic">Leucocytozoon</Emphasis>) in wild birds from Slovakia

During 2009 and 2010 samples from 251 wild birds (37 species) from nine sites of Slovakia were collected. Blood samples were tested for Plasmodium, Haemoproteus, and Leucocytozoon spp. parasites using both PCR-based and microscopy techniques. The overall prevalence of infection was 56.6%, while prevalence of Haemoproteus a Plasmodium spp. (were evaluated separately from Leucocytozoon) was 46.6% and the prevalence of Leucocytozoon spp. was 33.9%. After microscopic examination of stained blood smears the identification of haemoproteids was performed. There were 14 species of three genera identified, i.e., Haemoproteus parabelopolskyi, H. belopolskyi, H. magnus, H. fallisi, H. fringillae, H. balmorali, H. dolniki, H. tartakovskyi, H. lanii, Leucocytozoon majoris, L. dubreuili, Plasmodium vaughani, P. relictum, P. circumflexum. Except for H. fringillae, H. balmorali, H. belopolskyi, L. majoris and L. dubreuili, the mentioned species of parasites were recorded for the first time in Slovakia.     

Avian malaria on Madagascar: prevalence,biodiversity and specialization of haemosporidian parasites

Previous studies about geographic patterns of species diversity of avian malaria parasites and others in the Order Haemosporida did not include the avian biodiversity hotspot Madagascar. Since there are few data available on avian malaria parasites on Madagascar, we conducted the first known large-scale molecular-based study to investigate their biodiversity. Samples (1067) from 55 bird species were examined by a PCR method amplifying nearly the whole haemosporidian cytochrome b gene (1063?bp). The parasite lineages found were further characterized phylogenetically and the degree of specialization was determined with a newly introduced host diversity index (Hd). Our results demonstrate that Madagascar indeed represents a biodiversity hotspot for avian malaria parasites as we detected 71 genetically distinct parasite lineages of the genera Plasmodium and Haemoproteus. Furthermore, by using a phylogenetic approach and including the sequence divergence we suspect that the detected haemosporidian lineages represent at least 29 groups i.e. proposed species. The here presented Hd values for each parasite regarding host species, genus and family strongly support previous works demonstrating the elastic host ranges of some avian parsites of the Order Haemosporida. Representatives of the avian parasite genera Plasmodium and Leucocytozoon tend to more often be generalists than those of the genus Haemoproteus. However, as demonstrated in various examples, there is a large overlap and single parasite lineages frequently deviate from this rule.     

Haematozoa in forest birds from southern Chile: Latitudinal gradients in prevalence and parasite lineage richness

Abstract The existence of latitudinal gradients in species richness and their abundance is known for many free living organisms but few cases have been reported for parasitic diseases. In addition, asymmetries between the Northern and Southern Hemispheres in several characteristics may affect the distribution and diversity of species at all ecological levels. In this respect, we study the distribution of several genera of blood parasites infecting birds along a latitudinal gradient that includes the world's southernmost forests ecosystems. Birds were mist‐netted and sampled for blood in localities across Chile ranging from 33°S to 55°S during the years 2003–06. Overall, 26 bird species were sampled and 27 parasite lineages were identified. The latter belonged to three genera: Plasmodium (8), Haemoproteus (8) and Leucocytozoon (11). We found a positive significant relationship between prevalence and latitude for Leucocytozoon lineages and a negative relationship for Haemoproteus, Plasmodium and mixed infections. However, we did not find a significant relationship between parasite diversity and latitude. We found 18 lineages infecting only one species of host, and 19 lineages appear in only one of the localities of sampling. This pattern implies that some parasite lineages may evolve in isolation in some species/localities. In addition, specificity at the host‐family level was only found for Haemoproteus lineages infecting birds in the family Emberizidae. Individuals of the long distance migrant bird white‐crested elaenia (Elaenia albiceps), were found infected by the same parasite lineages in localities separated by 20° of latitude. Infections by these lineages were detected in other sedentary birds including juveniles and nestlings of different bird species. Therefore, long distance migrants are able to distort the presence of latitudinal gradients of diseases due to the potential role of migrants in spreading infections. Geographical gradients in prevalence of avian haematozoa differ between parasite genera and hemispheres, probably in relation to the existence of appropriate vector–parasite–host interactions.     

Genetic Diversity and Host Specificity Varies across Three Genera of Blood Parasites in Ducks of the Pacific Americas Flyway

Birds of the order Anseriformes, commonly referred to as waterfowl, are frequently infected by Haemosporidia of the genera Haemoproteus, Plasmodium, and Leucocytozoon via dipteran vectors. We analyzed nucleotide sequences of the Cytochrome b (Cytb) gene from parasites of these genera detected in six species of ducks from Alaska and California, USA to characterize the genetic diversity of Haemosporidia infecting waterfowl at two ends of the Pacific Americas Flyway. In addition, parasite Cytb sequences were compared to those available on a public database to investigate specificity of genetic lineages to hosts of the order Anseriformes. Haplotype and nucleotide diversity of Haemoproteus Cytb sequences was lower than was detected for Plasmodium and Leucocytozoon parasites. Although waterfowl are presumed to be infected by only a single species of Leucocytozoon, L. simondi, diversity indices were highest for haplotypes from this genus and sequences formed five distinct clades separated by genetic distances of 4.9%–7.6%, suggesting potential cryptic speciation. All Haemoproteus and Leucocytozoon haplotypes derived from waterfowl samples formed monophyletic clades in phylogenetic analyses and were unique to the order Anseriformes with few exceptions. In contrast, waterfowl-origin Plasmodium haplotypes were identical or closely related to lineages found in other avian orders. Our results suggest a more generalist strategy for Plasmodium parasites infecting North American waterfowl as compared to those of the genera Haemoproteus and Leucocytozoon.