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.     

Further observations on the blood parasites of birds in Uganda

Birds from three National Parks (Bwindi Impenetrable, Kibale, and Queen Elizabeth) in western Uganda were surveyed during the dry season in July 2003 and investigated for hematozoa by microscopic examination of stained blood films. Of 307 birds examined, representing 68 species of 15 families and four orders, 61.9% were found to be infected with blood parasites. Species of Haemoproteus (15.3% prevalence), Plasmodium (20.5%), Leucocytozoon (40.1%), Trypanosoma (11.4%), Hepatozoon (2.6%), Atoxoplasma (0.3%), and microfilariae (3.9%) were recorded. Except for Haemoproteus spp. infections, the overall prevalence of hematozoa belonging to all genera was significantly higher in this study than was previously reported in Uganda. Thirty-six species of birds were examined for blood parasites for the first time and 112 new host-parasite associations were identified. Eighty-one were at the generic and 31 at the specific level of the hematozoa. Hepatozoon and Atoxoplasma spp. were detected for the first time in Uganda.     

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.     

Survey of blood parasites in two forest owls, Northern Saw-whet Owls and Flammulated Owls, of western North America

Except for a few studies in the eastern United States, little has been published on hemoparasites in owls. We surveyed the blood parasites of 108 Northern Saw-whet Owls (Aegolius acadicus) and 24 Flammulated Owls (Otus flammeolus) in Idaho during autumn migration in 1999 and 2000. We also surveyed 15 Flammulated Owls (FLOW) during breeding season in Utah from 2000. Leucocytozoon ziemanni, Haemoproteus syrnii, Haemoproteus noctuae, and Trypanosoma avium were identified. The overall prevalence of infection was 53% (78/147) and for the combined species, prevalences of Haemoproteus, Leucocytozoon, and Trypanosoma species were 20%, 39%, and 4%, respectively. Northern Saw-whet Owls (NSWO) had an overall prevalence of 51% (55/108), with prevalences of 6%, 47%, and 4% by hemoparasite genus, respectively. Flammulated Owls had an overall prevalence of 59% (23/39), with prevalences of 56%, 18%, and 5% by genus, respectively. This study provides baseline hematozoa information for two boreal owl species.     

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.     

Blood parasites of birds in Cameroon

Birds from south-central Cameroon, western Africa, were surveyed for blood parasites from August to October 1986. Of 331 birds examined, representing 65 species of 15 families and 6 orders (mostly passerines), 55 (17%) were found to be infected with 1 or more genera of hemotropic parasites. These included: Haemoproteus spp. (11% prevalence), Leucocytozoon spp. (3%), Plasmodium spp. (2%), Trypanosoma spp. (1%), and microfilariae of filariid nematodes (1%). Several new host-parasite associations were identified.     

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.     

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.     

Seasonal and age-related changes in blood parasite prevalence in Dark-eyed Juncos (Junco hyemalis, Aves, Passeriformes)

We determined seasonal changes in blood parasite infections in a free-living population of Dark-eyed Juncos (Junco hyemalis) breeding in interior Alaska (65 degrees N; 148 degrees W). The common parasites found in blood smears were Leucocytozoon fringillinarum (56%), Trypanosoma avium (33%), and Haemoproteus fringillae (9%). In males, parasite prevalences were relatively high at arrival on breeding grounds and increased during the breeding season. Intensity of infection with Leucocytozoon also increased between spring and summer, and then decreased at the time of migration (September). This decrease did not occur in adult females. Elevated prevalences during the breeding season probably reflected the addition of new cases via vector activity to positive status resulting from spring relapse. We observed neither an association between parasite species nor a consistent relationship between parasite intensity and body condition. To further study relationships between reproductive system activity and parasite infections, we compared prevalences in adult males that were undergoing their first cycle of gonadal development and regression (males in their second calendar year, or SY) with those of older males (males in their third or more calendar year, i.e., after-second-year males or ASY). Circulating testosterone concentrations declined in both groups between arrival on breeding grounds (end of April-early May) and the end of the reproductive period (July), and they were higher in May in ASY than in SY males. At the peak of the breeding season (June), ASY males also had a higher parasite prevalence than SY males. This difference may have resulted from immunosuppressive effects of gonadal hormones and/or from behavioral differences between SY and ASY males such that older males were exposed to more insect vectors than younger males. .     

Blood parasites in birds from Burkina Faso

This study aims at evaluating the prevalence and density of haemoparasites in a native population of immature and adult male and female birds of Burkina Faso. Protists from the orders Eucoccidiorida, Kinetoplastida, as well as microfilaria were found. During the period from the 27th to the 29th of November 2003, we trapped 110 birds: on 101 sampled birds, 47 harboured blood parasites, with an overall prevalence of infection of 46.5%; 15 birds (14.8%) harboured mixed infections. Haemoproteus (prevalence of infection 30.7%), Plasmodium (13.9%), Trypanosoma (10.9%), microfilaria (8.9%) and Leucocytozoon (5.9%) were most frequently recorded. Occurrence of blood parasites was very high in comparison to that seen in birds from other areas of Africa.     

Prevalence of avian hematozoa in central Vermont

Peripheral blood smears from 1,547 birds, of 50 species, from 15 families trapped in Northfield, Vermont were examined for hematozoa. Numerous new host-parasite relationships were identified. The prevalence of all species of parasites over the 3 yr of the study was 42.5%. Prevalence of the genera of parasites were: Leucocytozoon--36.5%; Trypanosoma--7.3%; Haemoproteus--6.3%; microfilariae--1.0%; Plasmodium--1.0%. Peak prevalence (78.9%) occurred in the first half of July. Peak intensity was seen in the last half of June. Evidence from immature birds suggested that active transmission of all genera of hematozoans took place in the study area. Leucocytozoon gametocytes, unlike Haemoproteus gametocytes, were detected in smears from birds during all seasons of the year, and showed no period of complete remission. Trypanosoma and microfilariae also were seen throughout the year.     

Additional observations on blood parasites of birds in Costa Rica

Birds from the Area de Conservacion Guanacaste in northwestern Costa Rica were surveyed for blood parasites in June 2001 and December 2001-January 2002. Of 354 birds examined, representing 141 species of 35 families and 15 orders, 44 (12.4%) were infected with blood parasites. Species of Haemoproteus (4.8% prevalence), Plasmodium (0.6%), Leucocytozoon (0.3%), Trypanosoma (2.0%), and microfilariae (7.6%) were recorded. Twelve species of birds in this survey were examined for blood parasites for the first time. Several new host-parasite associations were identified.     

Blood parasites in sage-grouse from Nevada and Oregon

Peripheral blood smears from 196 adult and yearling female greater sage-grouse (Centrocercus urophasianus) were examined for blood parasites (167 from the breeding and 29 from the brood-rearing season) to determine prevalence of blood parasites, to attempt to correlate infection with chick survival, and to establish base-line values of prevalence in sage-grouse from Nevada and Oregon (USA). Birds were captured and released on two study areas during 1999-2001; Sheldon National Wildlife Refuge (SNWR) in northwestern Nevada, and Hart Mountain National Antelope Refuge (HMNAR) in southeastern Oregon. Birds from a third study area, Beaty's Butte grazing allotment (BB) in southeastern Oregon, were sampled in 2000 and 2001. Overall, 19 birds (10%) were positive for Leucocytozoon lovati (= L. bonasae), 1 (0.5%) for Plasmodium pedioecetii, and 2 (1%) for microfilariae. Although prevalence of L. lovati on HMNAR was 39% during the breeding season in 1999 and 100% during the brood-rearing season in 2000, statistically, prevalence of L. lovati among study areas and years was not different. However, there were statistical differences between capture periods. Overall, 31% of the hens were positive for L. lovati during the brood-rearing season compared to 6% during the breeding season. There was no difference in packed cell volume between infected and non-infected birds and no difference between age-classes. However, mean sage-grouse productivity on HMNAR was higher (1.6 chicks/hen) for non-infected (n = 10) compared to infected hens (0.7 chicks/hen; n = 7), during 1999. Based on these limited observations on HMNAR in 1999, the possible effects that L. lovati may have on young sage-grouse could be detrimental to sage-grouse populations in Nevada and Oregon.     

Presence of Plasmodium and Haemoproteus in breeding prothonotary warblers (Protonotaria citrea: Parulidae): temporal and spatial trends in infection prevalence

Prothonotary warbler (Protonotaria citrea) has shown a long-term decline in abundance in the United States. As a long-range migrant, these warblers are exposed to parasites in both tropical and temperate regions. The focus of this study was to use molecular techniques to examine the temporal prevalence patterns of heamosopridian parasites Plasmodium and Haemoproteus in breeding prothonotary warblers. The prevalence (presence or absence) of Plasmodium and Haemoproteus species was assayed using primer sets for the cytochrome b gene of the mitochondrial DNA. Blood samples were obtained from 187 adult prothonotary warblers collected at 3 central Virginia, U.S.A., breeding sites. The relationship between haemosporidian parasite infections and reproductive success also was examined. We found that 71% of captured prothonotary warblers were infected with haemosporidian parasites, specifically, with 36% prevalence for Haemoproteus spp. and 44% prevalence for Plasmodium spp., during the 2008 breeding season; for both parasites, prevalence increased throughout the season. We found significant variation in haemosporidian parasite prevalence across the breeding season that was strongly site specific. Conversely, we found no significant effects of haemosporidian parasite infections on the reproductive success of prothonotary warblers. This is in sharp contrast to recent reports suggesting considerable effects of these parasites on the reproductive success of wild birds.     

Prevalence of hematozoa in overwintering American redstarts (Setophaga ruticilla): no evidence for local transmission

We examined American redstarts (Setophaga ruticilla) for protozoan blood parasites on their wintering grounds to determine whether transmission of these parasites occurs prior to spring migration. A total of 73 blood smears from 37 birds were examined for presence and intensity of infection. Thirty-six birds were sampled in the fall, soon after arriving from northern breeding grounds, and the spring prior to departure. Two (5%) of the samples collected in the fall were positive for Haemoproteus fringillae and one (3%) had detectable infections of Trypanosoma avium. Individuals infected with H. fringillae were hatching year redstarts sampled in September and October. Intensity of infection was 78 and < 1 infected erythrocytes per 10,000 erythrocytes, respectively. None of the birds had detectable infections when resampled prior to spring migration the following March.     

Hematozoa of raptors from southern New Jersey and adjacent areas

Blood smears from 259 birds of 12 species, representing four families of raptors, from New Jersey, Pennsylvania, Delaware, and Virginia were examined for blood parasites. Infected birds constituted 59.1% of the total. Birds were infected with one or more of the following genera of protozoa: Leucocytozoon (43.2%); Haemoproteus (21.6%); Plasmodium (1.2%); and Trypanosoma (1.2%). Blood culture of 142 raptors of 11 species for Trypanosoma revealed a prevalence of 41.5%. Plasmodium circumflexum is reported for the first time in Accipiter striatus, and Trypanosoma sp. in Buteo jamaicensis.     

Hematozoa from montane forest birds in Papua New Guinea

Blood smears were examined from 141 montane forest birds of 45 species in southeastern Papua New Guinea. Haemoproteus spp. occurred in 46 (32.6%), Leucocytozoon fringillinarum Woodcock, 1910 in five, Trypanosoma sp. in one and Haemogregarina sp. in one. Intensity of infection by Haemoproteus was highest in those avian species and families with the highest prevalence; increasing altitude had no demonstrable effect on the prevalence of Haemoproteus spp.     

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.     

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.     

Interspecific differences in hematozoan infection in Sonoran desert Aimophila sparrows

Numerous studies have identified factors that control avian hematozoan infections, but the mechanisms that account for host differences in parasitemia remain largely speculative. To address this issue, we compared the prevalence of these parasites in stained blood smears from four conspecific Sonoran desert Aimophila sparrow species sampled during their breeding season: rufous-winged (Aimophila carpalis; RWSP), rufous-crowned (Aimophila ruficeps; RCSP), Cassin's (Aimophila cassinii, CASP), and Botteri's (Aimophila botterii; BOSP) sparrows. Blood smears contained Haemoproteus fringillae (RWSP), Trypanosoma everetti (RWSP, RCSP, BOSP), Trypanosoma avium (CASP), and microfilariae (all species). Most (92.5%) RWSP (n=40) were infected with Haemoproteus, but this parasite was not detected in RCSP (n=20) or BOSP (n=20) and was found only in one (2.5%) CASP (n=40). Trypanosoma spp. and microfilariae were detected in all species, but prevalence differed between these four sparrow species. Species differences in parasite prevalence were not due to difference in sex, age, adult body mass, incubation period, breeding habitat, or plumage colorfulness. However, differences in Haemoproteus sp. prevalence correlated with preferred nesting height, as RWSP generally nest above ground, whereas the other species nest on or close to the ground. Elevated H. fringillae prevalence in breeding-condition RWSP presumably does not result from a seasonal relapse associated with breeding or require new infection because 1) this prevalence did not differ in males sampled during and outside (n=21) the breeding season, and 2) all male RWSP (n=25) that we held in captivity and shielded from new infections and influence of natural photoperiod for 1 yr had viable blood H. fringillae gametocytes. H. fringillae prevalence in fall-sampled hatch-year male RWSP (n=11) was 63.6%, demonstrating that this parasite can be transmitted on the breeding grounds and during the first months of life. T. everetti prevalence in RWSP was lower in winter than in summer and also in long-term captive than in free-ranging adults. Presence of this parasite in the blood of breeding males may depend on recrudescence of existing infections or new infections.