Blood parasites of some waterfowl from Victoria, Australia.

A total of 316 anatids (5 species) from Serendip Wildlife Research Station, Lara, Victoria, were examined for blood parasites. Twenty-two of the ducks (all five species) harbored Haemoproteus nettionis and one also harbored Plasmodium relictum. None of 12 dusky moorhens (Gallinula tenebrosa) were infected. There was no significant difference in the prevalence of H. nettionis between species or age groups of ducks. No evidence of infection with Leucocytozoon, Trypanosoma or microfilaria was obtained.     

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.     

Blood parasites of mallard and pintail ducks from central Alberta and the Mackenzie Delta, Northwest Territories.

Blood films from 60 mallard (Anas platyrhynchos) and 67 pintail (A. acuta) ducks, collected in Alberta and the Mackenzie Delta, Northwest Territories, during 1973 and 1974, were examined for blood parasites. Twenty-two (37%) of the mallards and fourteen (21%) of the pintails were infected with one or more species of hematozoa. Infections of Leucocytozon simondi occurred more frequently (86%) than Haemoproteus nettionis (22%) in the infected birds. Trypanosoma avium occurred in one individual of each species of duck; one pintail harbored an unidentified microfilaria. Differences of prevalence between species are predicted on the basis of host attractancy to vectors and/or host habitat selection, and are discussed.     

Hematozoa of hatch-year common mergansers from Michigan

Fifty-five hatch-year common mergansers (Mergus merganser) were sampled for hematozoa from Douglas Lake (Michigan, USA) on 17 July 1995. Forty-one (75%) were infected with hematozoa. Haemoproteus greineri and Leucocytozoon simondi were common, infecting 28 (51%) and 26 (47%) common mergansers, respectively. Plasmodium circumflexum infected two (4%) birds. The common merganser is a new host record for H. greineri and P. circumflexum. Intensity data indicate possible negative interspecific interaction between H. greineri and L. simondi.     

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.     

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.     

Patterns of Haemoproteus beckeri parasitism in the gray catbird (Dumatella carolinensis) during the breeding season

We determined the prevalence and intensity of blood parasites in breeding gray catbirds (Dumatella carolinensis) at Killbuck Wildlife Area in Wayne and Holmes Counties, Ohio (USA) from June through August 2000. Of 98 catbirds sampled, 40 (40.8%) had detectable infections of Haemoproteus beckeri. Overall prevalence of H. beckeri in this population is high relative to that reported in earlier blood parasite surveys of both breeding and migrant catbirds. Mean intensity of H. beckeri infection did not vary significantly between young and old birds or among sampling periods. We found no effect of age on prevalence or intensity of H. beckeri infection. Older birds were not more likely to be infected than younger birds, despite longer exposure to arthropod vectors. Prevalence varied significantly with season and was highest in June and lowest in August. This pattern also was observed in older birds sampled repeatedly. This seasonal variation may reflect both newly acquired infections and chronic infections relapsing in response to hormonal changes associated with breeding. Evidence of transmission was observed in the single hatching year bird that lacked detectable infection in early summer, but demonstrated a very high intensity infection in late summer. These observations provide supportive evidence that hematozoa infections are acquired on the breeding grounds during the first year of life and relapse during the breeding season in subsequent years.     

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.     

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.     

Haemoproteus balearicae and other blood parasites of free-ranging Florida sandhill crane chicks

We obtained blood smears from 114 Florida sandhill crane (Grus canadensis pratensis) chicks in Osceola and Lake Counties, Florida, USA, during 1998-2000. Leucocytozoon grusi was observed in 11 (10%) chicks; Haemoproteus antigonis was observed in eight (7%) chicks; and three (3%) chicks were infected with Haemoproteus balearicae. One chick infected with H. balearicae suffered from severe anemia (packed cell volume = 13%) and was later found moribund. At necropsy this bird also had severe anemia and damage to the heart possibly due to hypoxia. This is the first report of H. balearicae in free-ranging North American cranes.     

Demographic and Spatiotemporal Patterns of Avian Influenza Infection at the Continental Scale,and in Relation to Annual Life Cycle of a Migratory Host

Since the spread of highly pathogenic avian influenza (HPAI) H5N1 in the eastern hemisphere, numerous surveillance programs and studies have been undertaken to detect the occurrence, distribution, or spread of avian influenza viruses (AIV) in wild bird populations worldwide. To identify demographic determinants and spatiotemporal patterns of AIV infection in long distance migratory waterfowl in North America, we fitted generalized linear models with binominal distribution to analyze results from 13,574 blue-winged teal (Anas discors, BWTE) sampled in 2007 to 2010 year round during AIV surveillance programs in Canada and the United States. Our analyses revealed that during late summer staging (July-August) and fall migration (September-October), hatch year (HY) birds were more likely to be infected than after hatch year (AHY) birds, however there was no difference between age categories for the remainder of the year (winter, spring migration, and breeding period), likely due to maturing immune systems and newly acquired immunity of HY birds. Probability of infection increased non-linearly with latitude, and was highest in late summer prior to fall migration when densities of birds and the proportion of susceptible HY birds in the population are highest. Birds in the Central and Mississippi flyways were more likely to be infected compared to those in the Atlantic flyway. Seasonal cycles and spatial variation of AIV infection were largely driven by the dynamics of AIV infection in HY birds, which had more prominent cycles and spatial variation in infection compared to AHY birds. Our results demonstrate demographic as well as seasonal, latitudinal and flyway trends across Canada and the US, while illustrating the importance of migratory host life cycle and age in driving cyclical patterns of prevalence.     

Characteristics of the haemoproteid community in an expanding white-winged dove population

The haemoproteid community of 171 eastern white-winged doves (Zenaida asiatica asiatica) from the expanding Texas population was examined using thin blood smears. During summer 1997, heart blood was taken from doves within their historical breeding range (Lower Rio Grande Valley of Texas), an intermediate region (San Antonio and surrounding area), and the new breeding periphery (north central to southeast Texas). Two species were found: Haemoproteus columbae and Haemoproteus sacharovi. Infracommunities rarely occurred in heart blood, as only 20 of 132 infected doves demonstrated gametocytes of both species. Overall prevalence of H. columbae and H. sacharovi was 77 and 15%, respectively. Prevalence of H. columbae was higher in the Lower Rio Grande Valley (LRGV) and intermediate regions than at the periphery, higher in adults than juveniles, and similar between males and females. Prevalence of H. sacharovi was lower in the LRGV than intermediate and peripheral regions, similar between juveniles and adults, and higher in females than males. Mean density of H. columbae and H. sacharovi was 15.9 +/- 2.7 and 0.3 +/- 0.1 (mean +/- SE per 3,000 erythrocytes), respectively. Overall mean abundance of H. columbae and H. sacharovi was 12.2 +/- 2.2 and 0.04 +/- 0.02, respectively. Mean abundance of H. columbae was higher in the LRGV and intermediate regions than at the periphery and was similar between host age and between host sex; H. sacharovi was similar among regions, host age, and host sex. This study emphasizes the importance of using prevalence, density, and abundance data to assess haemoproteid community structure and pattern.     

Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the swallow-tailed gull (Lariidae), with remarks on the host range of hippoboscid-transmitted avian hemoproteids

Haemoproteus (Haemoproteus) jenniae n. sp. (Haemosporida: Haemoproteidae) is described from a Galapagos bird, the swallow-tailed gull Creagrus furcatus (Charadriiformes, Laridae), based on the morphology of its blood stages and segments of the mitochondrial cytochrome b (cyt b) gene. The most distinctive features of H. jenniae development are the circumnuclear gametocytes occupying all cytoplasmic space in infected erythrocytes and the presence of advanced, growing gametocytes in which the pellicle is closely appressed to the erythrocyte envelope but does not extend to the erythrocyte nucleus. This parasite is distinguishable from Haemoproteus larae, which produces similar gametocytes and parasitizes closely related species of Laridae. Haemoproteus jenniae can be distinguished from H. larae primarily due to (1) the predominantly amoeboid outline of young gametocytes, (2) diffuse macrogametocyte nuclei which do not possess distinguishable nucleoli, (3) the consistent size and shape of pigment granules, and (4) the absence of rod-like pigment granules from gametocytes. Additionally, fully-grown gametocytes of H. jenniae cause both the marked hypertrophy of infected erythrocytes in width and the rounding up of the host cells, which is not the case in H. larae. Phylogenetic analyses identified the DNA lineages that are associated with H. jenniae and showed that this parasite is more closely related to the hippoboscid-transmitted (Hippoboscidae) species than to the Culicoides spp.-transmitted (Ceratopogonidae) species of avian hemoproteids. Genetic divergence between morphologically well-differentiated H. jenniae and the hippoboscid-transmitted Haemoproteus iwa, the closely related parasite of frigatebirds (Fregatidae, Pelecaniformes), is only 0.6%; cyt b sequences of these parasites differ only by 1 base pair. This is the first example of such a small genetic difference in the cyt b gene between species of the subgenus Haemoproteus. In a segment of caseinolytic protease C gene (ClpC), genetic divergence is 4% between H. jenniae and H. iwa. This study corroborates the conclusion that hippoboscid-transmitted Haemoproteus parasites infect not only Columbiformes birds but also infect marine birds belonging to Pelecaniformes and Charadriiformes. We conclude that the vertebrate host range should be used cautiously in identification of subgenera of avian Haemoproteus species and that the phylogenies based on the cyt b gene provide evidence for determining the subgeneric position of avian hemoproteids.     

High prevalence and diversity of blood parasites of passerine birds in Southern Turkmenistan

Thirty nine specimens of passerine birds belonging to 19 species and eight families were investigated by blood smear technique in four localities of Southern Turkmenistan in 3-18 August 1991. The overall prevalence of infection was 59%. Protists from the orders Haemosporida (genera Haemoproteus, Plasmodium, Leucocytozoon), Kinetoplastida (Trypanosoma), and Adeleida (Hepatozoon), as well as Microfilaria were found. Haemoproteids (the prevalence of infection is 44%), leucocytozoids (23%), malarial parasites (13%) and trypanosomes (13%) were most frequently recorded. Only low chronic infections (< 1% of infected cells for the great majority of intracellular parasites, and a few trypanosomes and Microfilaria in each blood smear) were seen. Haemoproteus belopolskyi, H. balmorali, H. dolniki, H. magnus, H. minutus, H. fringillae, H. majoris, Leucocytozoon dubreuili, and Trypanosoma avium were recorded for the first time in Turkmenistan. The former five above-mentioned species of haemoproteids are new records for the fauna of Middle Asia. Gametocytes of leucocytozoids in fusiform host cells were found for the first time in passerine birds in the Holarctic. The host is Parus bokharensis. Due to the wide distribution and the opportunity to collect a large parasitological material using harmless for hosts methods, bird haemosporidian parasites can be used as convenient models for ecological and evolutionary biology studies in South Turkmenistan. The heavily infected Orphean Warbler Sylvia hortensis is an especially convenient host for such purposes.     

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.     

Haemoproteus spp. and Leukocytozoon spp. in a captive raptor population

Raptors are commonly infected with two blood parasites of the family Haemoproteidae, Haemoproteus spp. and Leukocytozoon spp. To determine if age or length of time in captivity influence prevalence of Haemoproteus spp. and Leukocytozoon spp. infection in captive raptors, blood samples were collected from 55 birds from April 1999 to May 2000. Blood smears were examined for parasitemia and influence of age and length of time in captivity at the time of sample collection were compared. We found juvenile and adult birds were more likely to be infected with Leukocytozoon spp. than were nestlings (P = 0.006) and birds present for > 365 days were more likely to be infected with Haemoproteus spp. and/or Leukocytozoon spp. than were birds captive for < 365 days.     

Occurrence and seasonal transmission of hematozoa in wild turkeys

The occurrence and seasonal patterns of transmission of the blood protozoa of wild turkeys (Meleagris gallopavo silvestris) were studied at Tallahala Wildlife Management Area (TWMA) (Jasper County, Mississippi, USA). Blood smears obtained from wild turkeys in winter, spring and summer, and from sentinel domestic turkeys throughout the year were examined for Haemoproteus meleagridis and Leucocytozoon smithi. Whole blood from wild turkeys captured in summer was subinoculated into malaria-free domestic turkey poults and recipient birds were examined for Plasmodium spp. The prevalence of H. meleagridis and L. smithi were not different (P greater than 0.05) between adults and juveniles or between male and female turkeys in any season. Leucocytozoon smithi was not detected in poults in summer or in juveniles examined in winter. Sentinel studies and information from wild birds revealed that transmission of H. meleagridis and L. smithi did not overlap. Haemoproteus meleagridis was transmitted from May through November, while L. smithi was transmitted only from January through April. The onset of transmission of H. meleagridis coincided with peak hatching (mid-May) and brood-rearing (May-November) of turkey poults. Plasmodium spp. were not found in turkeys from TWMA (n = 27) nor in birds from three widely separated counties (n = 28) in Mississippi.     

Molecular phylogenetic analysis of circumnuclear hemoproteids (Haemosporida: Haemoproteidae) of sylviid birds, with a description of Haemoproteus parabelopolskyi sp. nov

Haemoproteus spp., with circumnuclear gametocytes and tentatively belonging to Haemoproteus belopolskyi, are widespread and prevalent in warblers belonging to the Sylviidae, with numerous mitochondrial cytochrome b (cyt b) lineages detected among them.We sampled the hemoproteids from 6 species of warblers adjacent to the Baltic Sea. Parasites were identified to species based on morphology of their gametocytes, and a segment of the parasite's cyt b gene was sequenced. Sixteen mitochondrial cyt b lineages of hemoproteids with circumnuclear gametocytes were recorded. Two clades of lineages (clade A in species of Acrocephalus and Hippolais and clade B in species of Sylvia) with sequence divergence between their lineages >5% are distinguished in the phylogenetic tree. Within the clades A and B, the genetic distance between the lineages is < or = 3.9 and < and = 2.8%, respectively. We compared the morphology of gametocytes of 3 lineages (hHIICT1, hMW1, and hSYAT2) in detail. The lineages hHIICTI and hMW1 (clade A) belong to the morphospecies H. belopolskyi. Parasites of the lineage hSYAT2 (clade B) are described as a new species Haemoproteus parabelopolskyi, which can be readily distinguished from H. belopolskyi by the significantly smaller nuclei of its macrogametocytes. Lineages closely related to H. belopolskyi and H. parabelopolskyi are identified. The sequence divergence between lineages of these 2 morphospecies ranges between 5.3 and 8.1%. It seems probable that avian Haemoproteus spp. with a genetic differentiation of > or =5% in mitochondrial cyt b gene might be morphologically differentiated at the stage of gametocytes. This study establishes the value of both PCR and morphology in identification of avian hemoproteids.