Blood parasites of Nearctic-Neotropical migrant passerine birds during spring trans-Gulf migration: impact on host body condition

To test the hypothesis that migrants infected with blood parasites arrive on the northern coast of the Gulf of Mexico in poorer condition than uninfected birds, we examined 1705 migrant passerine birds representing 54 species of 11 families from 2 Gulf Coast sites for blood parasites. Three hundred and sixty (21.1%) were infected with 1 or more species of 4 genera of blood parasites. The prevalence of parasites was as follows: Haemoproteus spp. (11.7%), Plasmodium spp. (6.7%), Leucocytozoon spp. (1.3%), and Trypanosoma spp. (1.2%). Both prevalence and density of Haemoproteus spp. infection varied among species. We found no relationship of gender or age with the prevalence of Haemoproteus spp. infection or Plasmodium spp. infection, with the exception of the orchard oriole (Icterus spurius) for which older birds were more likely to be infected with Haemoproteus spp. than younger birds. We also found that scarlet tanagers and summer tanagers infected with species of Haemoproteus have lower fat scores than uninfected individuals and that rose-breasted grosbeaks and Baltimore orioles infected with Haemoproteus spp. have a smaller mean body mass than uninfected individuals. Blood parasites do seem to pose a physiological cost for Neotropical migrant passerines and may be important components of the ecology of these species.     

Paucity of hematozoa in Colombian birds

Sixty-four birds of 43 species were caught at six localities in Colombia during the dry season in March 1998 and investigated for hematozoa by microscopic examination of stained blood films. Haemoproteus coatneyi, Plasmodium vaughani, Leucocytozoon sp., and microfilariae were identified. The overall prevalence of infection was 8%. Prevalences of infection for Haemoproteus spp., Plasmodium spp., Leucocytozoon spp., and microfilariae were 3%, 2%, 2%, and 3%, respectively. All hemosporidian infections encountered were of low intensity (< 1% of infected erythrocytes). The low prevalences and intensities of hemosporidian parasites in this study are in accord with other records from the Neotropics.     

A comparison of the blood parasites in three subspecies of the yellow wagtail Motacilla flava

One-hundred and eighty yellow wagtails Motacilla flava belonging to 3 subspecies (Motacilla flava feldegg, Motacilla flava flava, Motacilla flava thunbergi) were caught during the spring migration in south Kazakhstan and investigated by microscopic examination of stained blood smears. Haemoproteus anthi, Haemoproteus motacillae, Leucocytozoon fringillinarum, Leucocytozoon majoris, Plasmodium relictum, Plasmodium polare, Atoxoplasma sp., Trypanosoma sp., and microfilariae were identified. The overall prevalence of infection was 47.8%. Prevalences of Haemoproteus spp. (27.2%), Plasmodium spp. (25.0%), Leucocytozoon spp. (8.9%), Atoxoplasma spp. (4.4%), Trypanosoma spp. (1.1%), and microfilariae (0.6%) were recorded. No differences were discernible in parasite fauna or intensities of infection between males and females or between different subspecies. However, prevalence of infection of Haemoproteus, Leucocytozoon, and Plasmodium spp. was different in different host subspecies. These differences can be explained by differences in geographical location of breeding areas of these birds.     

Avian hemosporidian parasites from northern California oak woodland and chaparral habitats

During spring-summer 2003-2004, the avian community was surveyed for hemosporidian parasites in an oak (Quercus spp.) and madrone (Arbutus spp.) woodland bordering grassland and chaparral habitats at a site in northern California, a geographic location and in habitat types not previously sampled for these parasites. Of 324 birds from 46 species (21 families) sampled (including four species not previously examined for hemosporidians), 126 (39%) were infected with parasites identified as species of one or more of the genera Plasmodium (3% of birds sampled), Haemoproteus (30%), and Leucocytozoon (11%). Species of parasite were identified by morphology in stained blood smears and were consistent with one species of Plasmodium, 11 species of Haemoproteus, and four species of Leucocytozoon. We document the presence of one of the parasite genera in seven new host species and discovered 12 new parasite species-host species associations. Hatching-year birds were found infected with parasites of all three genera. Prevalence of parasites for each genus differed significantly for the entire sample, and prevalence of parasites for the most common genus, Haemoproteus, differed significantly among bird families. Among families with substantial sample sizes, the Vireonidae (63%) and Emberizidae (70%) were most often infected with Haemoproteus spp. No evidence for parasite between-genus interaction, either positive or negative, was found. Overall prevalence of hemosporidians at the northern California sites and predominance of Haemoproteus spp. was similar to that reported in most other surveys for the USA, Canada, and the Caribbean islands.     

Prevalence of avian haemosporidian parasites and their host fidelity in the central Philippine islands

We examined the prevalence and host fidelity of avian haemosporidian parasites belonging to the genera Haemoproteus, Leucocytozoon and Plasmodium in the central Philippine islands by sampling 23 bird families (42 species). Using species-specific PCR assays of the mitochondrial cytochrome b gene (471base pairs, bp), we detected infections in 91 of the 215 screened individuals (42%). We also discriminated between single and multiple infections. Thirty-one infected individuals harbored a single Haemoproteus lineage (14%), 18 a single Leucocytozoon lineage (8%) and 12 a single Plasmodium lineage (6%). Of the 215 screened birds, 30 (14%) presented different types of multiple infections. Intrageneric mixed infections were generally more common (18 Haemoproteus/Haemoproteus, 3 Leucocytozoon/Leucocytozoon, and 1 Plasmodium/Plasmodium) than intergeneric mixed infections (7 Haemoproteus/Leucocytozoon and 1 Haemoproteus/Leucocytozoon/Plasmodium). We recovered 81 unique haemosporidian mitochondrial haplotypes. These clustered in three strongly supported monophyletic clades that correspond to the three haemosporidian genera. Related lineages of Haemoproteus and Leucocytozoon were more likely to derive from the same host family than predicted by chance; however, this was not the case for Plasmodium. These results indicate that switches between host families are more likely to occur in Plasmodium. We conclude that Haemoproteus has undergone a recent diversification across well-supported host-family specific clades, while Leucocytozoon shows a longer association with its host(s). This study supports previous evidence of a higher prevalence and stronger host-family specificity of Haemoproteus and Leucocytozoon compared to Plasmodium.     

Incidence and Seasonal Variations in Blood and Tissue Parasites of Yellow-Billed Magpies

SYNOPSIS. Blood and tissue smears from 156 yellow-billed magpies showed infection with hematozoa in 154 (99%). Leucocytozoon berestneffi was found in 149 (96%), Haemoproteus picae in 40 (26%), Plasmodium relictum , in 32 (21%), Trypanosoma sp. in 3 (2%), and microfilariae in 42 (27%). Fifty-two birds were infected with two genera of parasites, 27 with 3, and 4 with 4. Leucocytozoon, Plasmodium and microfilariae showed a higher incidence in tissue than in blood smears.     

No evidence for avian malaria infection during the nestling phase in a passerine bird

One of many uncertainties concerning the epidemiology of avian malaria in wild bird populations is the age at first infection. While nestlings, being naked and presumably immunologically na?ve would seem a likely stage of first infection, most age-stratified prevalence studies have not examined the nestling cohort, whereas those that have use relatively insensitive blood smear examination to diagnose infection. In the study presented here, we used sensitive nested polymerase chain reaction methods to screen blood samples from 195, 14-day-old blue tit (Cyanistes caeruleus) nestlings for avian malaria parasites (species of Plasmodium and Haemoproteus). Adults in this population are commonly infected with Plasmodium spp. (prevalence c. 30%). No avian malaria infections were found in nestlings, but a single positive identification of the related hematozoan parasite, Leucocytozoon sp., was made. Our results suggest either that the nestlings were infected but the disease had not yet reached patency, or that young birds in the nest are not bitten by the insect vectors of the disease.     

Prevalence of blood parasites in European passeriform birds

Variation in the prevalence of blood parasites among species of birds has been used to test hypotheses about the effects of sexual selection and parental investment on disease resistance, and how vector abundance influences infection. However, the factors causing this variation are still poorly understood. We assessed the statistical effects of biogeographic, plumage-related and life-history traits on the prevalence of the blood parasites Plasmodium, Haemoproteus, Leucocytozoon and Trypanosoma in European passerine birds. Most of the variation in parasite prevalence occurred at low taxonomic levels. Brighter male plumage and greater host body mass were associated with higher prevalence, explaining 32% of the total variation. Male plumage brightness remained a significant factor when we controlled for phylogenetic effects. These relationships were driven primarily by simuliid-transmitted parasites (Leucocytozoon, Trypanosoma), which were more frequent in species with northern distributions. Host species with greater maximum longevity and shorter nestling periods had higher prevalences of Plasmodium; however, the effect was not stable after controlling for phylogeny using pairwise contrasts. Coevolution between hosts and parasites appears to create temporal and spatial variation that disconnects haematozoan prevalence from evolutionarily conservative life-history traits while creating some positive associations with traits that are phylogenetically labile. Clearly, ecologists should be cautious in relating patterns of variation in haematozoan prevalence to particular host traits.     

Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats

Land use changes including deforestation, road construction and agricultural encroachments have been linked to the increased prevalence of several infectious diseases. In order to better understand how deforestation affects the prevalence of vector-borne infectious diseases in wildlife, nine paired sites were sampled (disturbed vs. undisturbed habitats) in Southern Cameroon. We studied the diversity, prevalence and distribution of avian malaria parasites ( Plasmodium spp.) and other related haemosporidians (species of Haemoproteus and Leucocytozoon ) from these sites in two widespread species of African rainforest birds, the yellow-whiskered greenbul ( Andropadus latirostris , Pycnonotidae) and the olive sunbird ( Cyanomitra olivacea , Nectariniidae). Twenty-six mitochondrial cytochrome b lineages were identified: 20 Plasmodium lineages and 6 Haemoproteus lineages. These lineages showed no geographic specificity, nor significant differences in lineage diversity between habitat types. However, we found that the prevalence of Leucocytozoon and Haemoproteus infections were significantly higher in undisturbed than in deforested habitats ( Leucocytozoon spp. 50.3% vs. 35.8%, Haemoproteus spp. 16.3% vs. 10.8%). We also found higher prevalence for all haemosporidian parasites in C. olivacea than in A. latirostris species (70.2% vs. 58.2%). Interestingly, we found one morphospecies of Plasmodium in C. olivacea , as represented by a clade of related lineages, showed increased prevalence at disturbed sites, while another showed a decrease, testifying to different patterns of transmission, even among closely related lineages of avian malaria, in relation to deforestation. Our work demonstrates that anthropogenic habitat change can affect host–parasite systems and result in opposing trends in prevalence of haemosporidian parasites in wild bird populations.     

Blood parasites in owls with conservation implications for the Spotted Owl (Strix occidentalis)

The three subspecies of Spotted Owl (Northern, Strix occidentalis caurina; California, S. o. occidentalis; and Mexican, S. o. lucida) are all threatened by habitat loss and range expansion of the Barred Owl (S. varia). An unaddressed threat is whether Barred Owls could be a source of novel strains of disease such as avian malaria (Plasmodium spp.) or other blood parasites potentially harmful for Spotted Owls. Although Barred Owls commonly harbor Plasmodium infections, these parasites have not been documented in the Spotted Owl. We screened 111 Spotted Owls, 44 Barred Owls, and 387 owls of nine other species for haemosporidian parasites (Leucocytozoon, Plasmodium, and Haemoproteus spp.). California Spotted Owls had the greatest number of simultaneous multi-species infections (44%). Additionally, sequencing results revealed that the Northern and California Spotted Owl subspecies together had the highest number of Leucocytozoon parasite lineages (n = 17) and unique lineages (n = 12). This high level of sequence diversity is significant because only one Leucocytozoon species (L. danilewskyi) has been accepted as valid among all owls, suggesting that L. danilewskyi is a cryptic species. Furthermore, a Plasmodium parasite was documented in a Northern Spotted Owl for the first time. West Coast Barred Owls had a lower prevalence of infection (15%) when compared to sympatric Spotted Owls (S. o. caurina 52%, S. o. occidentalis 79%) and Barred Owls from the historic range (61%). Consequently, Barred Owls on the West Coast may have a competitive advantage over the potentially immune compromised Spotted Owls.     

A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood

Many bird species host several lineages of apicomplexan blood parasites (Protista spp., Haemosporida spp.), some of which are shared across different host species. To understand such complex systems, it is essential to consider the fact that different lineages, species, and families of parasites can occur in the same population, as well as in the same individual bird, and that these parasites may compete or interact with each other. In this study, we present a new polymerase chain reaction (PCR) protocol that, for the first time, enables simultaneous typing of species from the 3 most common avian blood parasite genera (Haemoproteus, Plasmodium, and Leucocytozoon). By combining the high detection rate of a nested PCR with another PCR step to separate species of Plasmodium and Haemoproteus from Leucocytozoon, this procedure provides an easy, rapid, and accurate method to separate and investigate these parasites within a blood sample. We have applied this method to bird species with known infections of Leucocytozoon spp., Plasmodium spp., and Haemoproteus spp. To obtain a higher number of parasite lineages and to test the repeatability of the method, we also applied it to blood samples from bluethroats (Luscinia svecica), for which we had no prior knowledge regarding the blood parasite infections. Although only a small number of different bird species were investigated (6 passerine species), we found 22 different parasite species lineages (4 Haemoproteus, 8 Plasmodium, and 10 Leucocytozoon).     

Incidence of malaria in a wintering population of canvasbacks (Aythya valisineria) on Chesapeake Bay

Canvasback ducks wintering on Chesapeake Bay had a 6% incidence of Leucocytozoon simondi and 2% incidence of Haemoproteus. Subinoculation of whole blood into Pekin ducklings produced a Plasmodium infection rate of 31%. Females were more frequently infected (12/22) than males (15/68). The parasite was identified as P. circumflexum.     

Hematozoa in endemic subspecies of common kestrel in the Cape Verde Islands

We examined 130 Common Kestrel (Falco tinnunculus) representing two endemic subspecies and nine resident island populations on the Cape Verde archipelago between 1996 and 1999 to study diversity, prevalence, and intensity of hematozoa. Hematozoan diversity was very low; we detected only Plasmodium fallax, a species that is rarely found in Falconoformes, and, possibly, Haemoproteus brachiatus. Moreover, prevalence of Plasmodium fallax was low (1.5%) with a mean intensity of infection of 0.05 protozoa/10(-3) erythrocytes. Only one bird (0.8%) was infected with a gametocyte that was most likely Haemoproteus brachiatus; the intensity in this infected bird was 1.5 protozoa/10(-3) erythrocytes. A single parasite or two parasites were observed in blood smears in four additional birds, but identification to genus was not possible. This is the first record of blood parasites in birds on the Cape Verde Archipelago. The low prevalence of these parasites might be because of arid and less-favorable conditions for the pathogen's vectors. The sedentary nature and high level of isolation of the island kestrel populations are also factors that could decrease the probability of infection.     

Blood parasites in wood storks (Mycteria americana) from the southeastern United States

Wood storks (Mycteria americana) are endangered throughout their breeding range in the United States. Because of this, researchers have had little opportunity to thoroughly examine the continental wood stork population for endoparasites. The blood protozoan Haemoproteus crumenium has been identified from several populations of wood storks in North America. However, there have been no reports of wood storks being infected with species of Plasmodium or Leucocytozoon. During 2003, 42 nestling wood storks were captured at sites in Georgia and 27 free-ranging wood storks were captured at postbreeding dispersal sites in Mississippi and Louisiana. Two thin blood smears were made from each bird, and they were examined for parasites. Haemoproteus crumenium was found in 5 wood storks (7.2%), whereas Leucocytozoon sp., Plasmodium sp., and microfilariae were not observed. Mean intensity of H. crumenium was 4.4 +/- 0.7 (SE) per 2,000 erythrocytes counted. All infected wood storks were subadult or adult and were from postbreeding dispersal sites in Mississippi.     

Hematological responses to hematozoa in North American and neotropical songbirds

Hematocrit (Hct), hemoglobin concentration, RBC count, and blood parasite loads (Plasmodium, Leucocytozoon, Haemoproteus, Trypanosoma, microfilariae) were measured in 688 passerine birds captured at four sites in the US and Belize, C.A., to assess physiological consequences of parasitemia. Parasite loads were low overall: 80% of birds had <5 parasites/10000 RBCs; median infection intensity was 1 per 10000 RBCs. Infection prevalence and intensity were higher in Belize than in the US. Analyses across and within taxa revealed no significant linear correlations between hematology values and parasite load, though infected birds were more likely to be anemic. Neotropical migrants reaching the southern US had lower parasite loads than migrants wintering in Belize. Mean Hct was significantly elevated among infected migrants (but not uninfected migrants) reaching the US relative to migrants in Belize. Long-distance migration thus appears to act as a filter for heavily parasitized and anemic birds. Geographic and seasonal variations in hematology indices were similar within and between taxa, suggesting that community-wide factors, rather than phylogenetic attributes or species-specific pathogens, account for the majority of hematological variation. The low parasite loads and weak correlation between parasite load and hematology indices have implications for attempts to test the version of the 'good genes' hypothesis.     

Haemosporidian blood parasites in European birds of prey and owls

Avian blood parasites have been intensively studied using morphological methods with limited information on their host specificity and species taxonomic status. Now the analysis of gene sequences, especially the mitochondrial cytochrome b gene of the avian haemosporidian species of Haemoproteus, Plasmodium, and Leucocytozoon, offers a new tool to review the parasite specificity and status. By comparing morphological and genetic techniques, we observed nearly the same overall prevalence of haemosporidian parasites by microscopy (19.8%) and polymerase chain reaction (PCR) (21.8%) analyses. However, in contrast to the single valid Leucocytozoon species (L. toddi) in the Falconiformes we detected 4 clearly distinctive strains by PCR screening. In the Strigiformes, where the only valid Leucocytozoon species is L. danilewskyi, we detected 3 genetically different strains of Leucocytozoon spp. Two strains of Haemoproteus spp. were detected in the birds of prey and owls examined, whereas the strain found in the tawny owl belonged to the morphospecies Haemoproteus noctuae. Three Plasmodium spp. strains that had already been found in Passeriformes were also detected in the birds of prey and owls examined here, supporting previous findings indicating a broad and nonspecific host spectrum bridging different bird orders.     

Low haemosporidian diversity and one key-host species in a bird malaria community on a mid-Atlantic island (São Miguel, Azores)

When host species colonize new areas, the parasite assemblage infecting the hosts might change, with some parasite species being lost and others newly acquired. These changes would likely lead to novel selective forces on both host and its parasites. We investigated the avian blood parasites in the passerine bird community on the mid-Atlantic island of S?o Miguel, Azores, a bird community originating from continental Europe. The presence of haemosporidian blood parasites belonging to the genera Haemoproteus, Plasmodium, and Leucocytozoon was assessed using polymerase chain reaction. We found two Plasmodium lineages and two Leucocytozoon lineages in 11 bird species (84% of all breeding passerine species) on the island. These lineages were unevenly distributed across bird species. The Eurasian Blackbird (Turdus merula) was the key-host species (total parasite prevalence of 57%), harboring the main proportion of parasite infections. Except for Eurasian Blackbirds, all bird species had significantly lower prevalence and parasite diversity compared to their continental populations. We propose that in evolutionary novel bird communities, single species may act as key hosts by harboring the main part of the parasite fauna from which parasites "leak" into the other species. This would create very different host-parasite associations in areas recently colonized by hosts as compared to in their source populations.     

The sensitivity of microscopy and PCR-based detection methods affecting estimates of prevalence of blood parasites in birds

Inferences about the evolution of host-parasitic relationships are often made based on the prevalence of avian malaria, which is usually estimated in a large sample of birds using either microscopic or molecular screening of blood samples. However, different techniques often have variable accuracy; thus, screening methodology can raise issues about statistical bias if method sensitivity varies systematically across parasites or hosts. To examine this possibility, published information was collected on the prevalence of species in 4 genera of avian blood parasites ( Plasmodium, Haemoproteus, Leucocytozoon, and Trypanosoma) from various sources that used different tools. The data were tested to determine if the application of different methods provided different estimates for the same hosts. In these comparisons between the main methodologies, the PCR-based molecular methods were generally found to provide higher estimates for Plasmodium spp. prevalence than microscopic tools, while there was no significant tendency for such a trend in species of Haemoproteus and Leucocytozoon. When analyzing intraspecific variance of prevalence within molecular studies, some studies provided consistently higher estimates for Haemoproteus spp. prevalence than others, indicating that differences between studies can affect detected estimates. Within microscopic studies, surveys that examined more microscopic fields were more likely to report higher prevalence for Plasmodium spp. than those relying on fewer microscopic fields. Consequently, studies making comparisons across parasite genera and/or host species from different sources need to consider several types of bias originating from variation in method sensitivity.     

A SURVEY OF BLOOD PARASITES OF BIRDS IN THE MASCARENE ISLANDS, INDIAN OCEAN: WITH DESCRIPTIONS OF TWO NEW SPECIES AND TAXONOMIC DISCUSSION

A survey was carried out on the prevalence of blood parasites in birds in the Mascarene Islands. Smears from 357 birds of 25 species in 12 families were examined, of which 150 (42%) were found to harbour blood parasites. The most common parasites were Leucocytozoon ; a new species, L. zosteropis , is described from the Grey White-eye Zosterops borbonica mauritiana. This parasite was observed in smears from 68 birds of three species: Z. borbonica, Z. chloronothos and Z. olivacea. Other species of Leucocytozoon identified were L. fringillinarum from fodies, sparrows and a bulbul and L. marchouxi from two doves.
Haemoproteus was found only in domestic pigeons Columba livia and identified as H. columbae. Plasmodium relictum, P. vaughani and an unidentified species with elongate gametocytes were found in Zosterops , and Plasmodium sp. of low infection observed in other hosts. Trypanosoma mayae is redescribed from the House Sparrow Passer domesticus and the Mauritius Fody Foudia rubra , and considered to be a valid species. A new species of trypanosome, Trypanosoma phedinae , is described from the Malagasy Swallow Phedina b. borbonica. Other birds were found to harbour low infections of unidentified species of trypanosomes. A small number of birds were infected with Atoxoplasma , haemogregarines and Rickettsia-like organisms. An unidentified organism with a predilection for eosinophils was observed in several Mascarene Swiftlets Collocalia francica.
The results are discussed in relation to the possible effects of the parasites on the birds of the Mascarene Islands and comparisons made with the results of similar surveys on other Indian Ocean Islands.     

Hematozoa from the spotted owl

One hundred five spotted owls (Strix occidentalis) from seven populations and three subspecies were examined for hematozoa. Haemoproteus noctuae, H. syrnii, Leucocytozoon ziemanni, Trypanosoma avium, Atoxoplasma sp. and unidentified microfilariae were recorded. All northern (S. occidentalis caurina), California (S. occidentalis occidentalis) and Mexican (S. occidentalis lucida) spotted owls were infected with at least one hematozoan; 79% had multiple infections. Twenty-two percent of the owls were infected with as many as four species of parasites. There were significant differences in the prevalence of these species of parasites occurring among the five populations of northern and California spotted owls sampled in California. Haemoproteus noctuae, H. syrnii and Atoxoplasma sp. represented new host records for this host species.