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.     

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.     

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.     

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.     

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.     

Hematozoa from Southern African vultures, with a description of Haemoproteus janovyi sp. n.

This study represents the first major survey of avian hematozoa from southern Africa and the only one dealing with blood parasites of vultures. Blood smears from 506 Rhodesian, Botswanan and South African vultures (Hooded, White-headed, Lappetfaced, Cape Griffon and Whitebacked Vultures) were examined for hematozoa. Haemoproteus janovyi sp. n. was observed in 35.2% of the vultures, Leucocytozoon toddi in 0.8%, Plasmodium fallax in 0.6%, Atoxoplasma sp. in 1.4% and microfilariae in 0.2%. Hematozoan prevalence increased with age of the vultures. Only 2 of 133 nestlings sampled during the dry season had patent parasitemias (L. toddi). Haemoproteid prevalence in immature vultures was depressed during the dry season, whereas it was stable throughout the year in adults. The only species which nests on cliffs (the Cape Griffon Vulture) did not harbor hematozoa whereas the other species which nest and roost in trees were infected with at least one hematozoan species.     

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.     

A survey of infectious diseases in wild turkeys (Meleagridis gallopavo silvestris) from Arkansas

Wild turkeys (Meleagridis gallopavo silvestris) trapped as part of a relocation program by the Arkansas Game and Fish Commission were tested for selected infectious diseases and parasites. The 45 birds were trapped at four locations in Pope, Scott, and Montgomery counties (Arkansas, USA). Forty-four blood samples for serology, 27 blood smears and 12 fecal samples were collected. Of the serum samples tested, 20 of 44 (45%) were positive for Pasteurella multocida by enzyme-linked immunosorbent assay (ELISA), 42 of 44 (95%) were positive for Bordetella avium by ELISA, and 15 of 44 (34%) were positive for Newcastle disease virus antibody by the hemagglutination inhibition test. All serum samples were negative for Mycoplasma gallisepticum, Mycoplasma synoviae, avian paramyxovirus 3, avian influenza, hemorrhagic enteritis, Marek's disease, avian encephalomyelitis, laryngotracheitis, Salmonella pullorum and Salmonella gallinarum. Haemoproteus meleagridis was found in eight of 27 (30%) and Leucocytozoon smithi in nine of 27 (33%) blood smears; all smears were negative for Plasmodium hermani. Enteric parasites included Ascaridia dissimilis, Heterakis gallinarum, Eimeria dispersa and Raillietina spp. This study was an attempt to document the health status and disease exposure of wild turkeys in Arkansas to aid in managing and preventing the spread of disease agents to wild turkeys and other species of birds.     

Blood parasites of some columbiform and passeriform birds from Chile.

Ninety-one birds of 23 species from Chile were examined for haematozoa; 13 birds of seven species harbored species of Haemoproteus, Leucocytozoon, Plasmodium, Trypanosoma and microfilariae. Haemoproteids (representing four species) were the most common parasites and occurred in 10 of the 13 infected birds.     

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.     

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.     

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.     

Standard sampling techniques underestimate prevalence of avian hematozoa in willow ptarmigan (Lagopus lagopus)

A total of 68 willow ptarmigan (Lagopus lagopus L.) was collected during September 1995 from two localities in Troms County, northern Norway. Thin blood smears were prepared and examined for blood parasites. Of the 68 willow ptarmigan examined, 94% harbored one or more species of hematozoa. There were four (6%), 44 (65%), 16 (24%), and four (6%) birds infected by zero, one, two, and three species of parasites, respectively. Prevalences at the coastal locality, Kattfjord (n = 43), were Leucocytozoon lovati 86%, Trypanosoma avium (26%), and microfilariae (30%). At the inland locality, Iselvdalen (n = 25), prevalences were L. lovati 96%, T. avium 12%, and microfilariae 0%. We also searched connective tissues for the filaroid nematode Splendidofilaria papillocerca; in Kattfjord this parasite only occurred in adult hosts where prevalence was 94%, but the parasite was not found in Iselvdalen. To estimate the efficiency of parasite detection by standard blood sampling techniques, we sampled peripheral blood from the brachial wing vein and blood from the pulmonary system from willow ptarmigan. Sampling peripheral blood from the brachial vein led to underestimates of the prevalence of microfilariae. There was no significant difference between L. lovati and T. avium prevalence in blood collected from the brachial vein or deep circulation. Age of host had a strong impact on prevalence, especially for S. papillocerca and microfilariae.     

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.     

Blood Parasitism in Cliff Swallows from the Sacramento Valley

SYNOPSIS. Hematozoa were found in 89 (30.6%) of 291 cliff swallows ( Petrochelidon pyrrhonota ), captured for banding purposes. Hepatozoon was found in 73 (25%), Trypanosoma in 13 (4.5%), microfilariae in 9 (3%), and Haemoproteus and Leucocytozoon in 1 bird each. Multiple infections were found in only 7 of the swallows.     

Interspecific variability of prevalence in blood parasites of adult passerine birds during the breeding season in Alaska

Blood parasite prevalence based on microscopic examination of stained blood smears was determined in adults of 11 passerine bird species sampled during their breeding season (May and June 1997-98) in interior Alaska (USA). These species included primarily Nearctic migratory species such as the dark-eyed junco (Junco hyemalis) and neotropical migratory species such as the blackpoll warbler (Dendroica striata), alder flycatcher (Empidonax alnorum), Swainson's thrush (Catharus ustulatus), northern waterthrush (Seiurus noveboracensis), and bank swallow (Riparia riparia) as well as one long-distance palearctic migrant, the arctic warbler (Phylloscopus borealis). The more prevalent parasites were Leucocytozoon dubreuili (73% of the sampled turdinids), L. fringillinarum (42% of the sampled fringillids and parulids), and Trypanosoma avium (39% of the sampled hosts). Other parasites (H. fallisi: 18% of the sampled turdinids; Haemoproteus paruli: 14% of the sampled parulids; H. fringillae: 5% of the sampled fringillids; microfilariae: 4% of the sampled hosts) were observed less frequently. Plasmodium vaughani was found only in two yellow warblers (Dendroica petechia). Overall parasite prevalence varied between 0% in the alder flycatcher to >80% in Swainson's thrush, arctic warbler, and Townsend's warbler (Dendroica townsendi). Prevalence of various hematozoa also was bird species-dependent. No relationship was observed between prevalence and either foraging (aerial versus trees/shrubs) or nesting habits (ground versus arboreal) or general location of the wintering area of the different species examined. Prevalence also was unrelated to average dates of arrival on breeding grounds and, therefore, to potential duration of exposure to local insect vectors before capture. Differences in blood parasite prevalence among species breeding in a same region and in the same type of habitat may result from differences in host specificity such as immunological resistance to infection or blood meal preference by potential vectors and/or in behavioral adjustments/physiological traits that alter exposure to vectors.     

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).     

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.     

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.     

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.