The Blood Protozoa of Seventeen Species of Sparrows and Other Fringillidae

SUMMARY. A total of 1037 birds, belonging to 17 species of Fringillidae (order Passeres) and nearly all collected in or near Syracuse, N. Y., were examined for blood parasites. Of the species of avian malaria, Plasmodium cathemerium occurred most frequently, followed by P. hexamerium, P. relictum, P. elongatum , and P. circumflexum. Other species were not seen, although some (e.g. P. nucleophilum, P. polare, P. vaughani ) are known to occur in Central New York.
A number of song, chipping, and field sparrows were given experimental inoculations of Plasmodium vaughani -infected blood and liberated. A few were recaught at varying intervals, but none were infected, suggesting that these species are insusceptible to this type of avian malaria.
Malaria in song sparrows, which were caught in large numbers, is common and probably endemic, not varying greatly in frequency from year to year. But the incidence shows a sharp peak in the spring, most cases apparently being low-grade relapses, which probably serve to reestablish the infection in the new crop of mosquitoes. There are indications that Haemoproteus and Leucocytozoon behave similarly.
Infection with these last two parasites occurred in most of the species examined, but the incidence varied greatly, being especially high in white-throated and white-crowned sparrows. Reproductive stages of Haemoproteus were observed in the lungs of song and chipping sparrows.     

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.     

Blood Protozoa of Imported Birds

SYNOPSIS. Large numbers of birds, until recently, were brought into the United States each year. Countries of origin were varied, and included those of Australasia, Africa, South America, and the Caribbean Islands, as well as other places. With them of course come their parasites, some of which may be potential pathogens to domestic avifauna. In part for this reason, a survey was undertaken of blood parasites of birds from pet shops and importers. So far a total of 1234 birds belonging to 186 species has been examined. Several new species and subspecies of avian Plasmodium have been found in the course of this study, including P. octamerium Manwell, 1968 in a Pintail Whydah, Vidua macoura , from Africa; P. paranucleophilum Manwell & Sessler, 1971 in a South American tanager, Tachyphonus sp.; and P. nucleophilum toucani Manwell & Sessler 1971 in a Swainson's Toucan, Ramphastos s. swainsonii. Plasmodium huffi Muniz, Soares & Battista is undoubtedly a synonym pro parte for the last. Plasmodium tenue Laveran & Marullaz, long thought to be a synonym of Plasmodium vaughani Novy & MacNeal, was rediscovered and found to be a valid species. Plasmodium nucleophilum , infrequently seen in the New World, occurred in many Asian and African birds, and especially in starlings. Infections with other species of Plasmodium were common. Haemoproteus was the commonest blood parasite; Leucocytozoon was very rare as was Atoxoplasma (Lankesterella). The 2 families of birds best represented were the Fringillidae and the Psittacidae, but no blood parasites were seen in the latter. It is clear that imported birds are often infected with blood protozoa, some of which are unknown from native birds.     

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.     

Haematozoa of East African birds: III. Three years' observations on the blood parasites of birds from Ngulia

A survey of blood parasites of birds from Ngulia in Kenya was carried out during the period November-December for the years 1973–1975. A total of 468 birds was examined of which 179 (38.2%) were infected with one or more parasites. Together with a re-examination of material from previous surveys for taxonomic purposes, the following species were identified; Haemoproteus anthi, H. centropi, H. columbae, H. coraciae, H. fallisi, H. fringillae, H. lanii, H. morneti, H. orizivorae, H. sanguinis, H. tendeiroi, H. zosteropsi, Leucocytozoon brimonti, L. coccyzus, L. dinizi, L. dub-reuili, L. eurystomi, L. fringillinarum, L. marchouxi, Plasmodium relictum, P. rouxi, P. vaughani, Trypanosoma everetti, T. mayae, T. pycnonoti and Babesiu rustica. Unidentified species of haemogregarines, Aegyptianella, Rickettsia and microfilaria were also observed. The significance of migrant birds as reservoirs of infection, together with the probable seasonality of patent infections in the resident population is discussed.     

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.     

Blood parasites of some birds from Ghana

A total of 135 birds of 26 species in 13 families was examined for blood parasites; 43 birds (31.9%) of 13 species were infected; species of the Ploceidae were the most heavily infected. Species of Haemoproteus occurred most commonly 29 birds) while Leucocytozoon and Plasmodium species were virtually absent. There was no significant difference in the prevalence of hematozoa in birds from the mature rainforest and those in a savannah-urban setting.     

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.     

Blood parasites of some birds from Senegal

A total of 809 birds from Senegal, including 43 species and 21 families, were examined for hematozoans; 93 birds (11.5%) harbored blood parasites, with only 7 (7.5%) harboring mixed infections. Species of Haemoproteus occurred in 81.7% of the infected birds while species of Plasmodium. Trypanosoma, microfilaria and Leucocytozoon were encountered less frequently. The majority of the sample was composed of species of ploceids and estrildidis and blood parasites were most prevalent in the colonial-nesting ploceids. Prevalence of blood parasites in Senegal was low in comparison to that seen in birds from other parts of Africa.     

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.     

Bird hosts, blood parasites and their vectors--associations uncovered by molecular analyses of blackfly blood meals

The level of host specificity of blood-sucking invertebrates may have both ecological and evolutionary implications for the parasites they are transmitting. We used blood meals from wild-caught blackflies for molecular identification of parasites and hosts to examine patterns of host specificity and how these may affect the transmission of avian blood parasites of the genus Leucocytozoon . We found that five different species of ornithophilic blackflies preferred different species of birds when taking their blood meals. Of the blackflies that contained avian blood meals, 62% were infected with Leucocytozoon parasites, consisting of 15 different parasite lineages. For the blackfly species, there was a significant association between the host width (measured as the genetic differentiation between the used hosts) and the genetic similarity of the parasites in their blood meals. The absence of similar parasite in blood meals from blackflies with different host preferences is interpreted as a result of the vector–host associations. The observed associations between blackfly species and host species are therefore likely to hinder parasites to be transmitted between different host-groups, resulting in ecologically driven associations between certain parasite lineages and hosts species.     

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.     

Vertebrate host specificity of two avian malaria parasites of the subgenus Novyella: Plasmodium nucleophilum and Plasmodium vaughani

The susceptibility of wild-caught European passeriform birds to naturally isolated malaria parasites, Plasmodium (Novyella) nucleophilum and Plasmodium (Novyella) vaughani, was studied by means of intramuscular subinoculation of infected citrated blood. Plasmodium nucleophilum of the great tit, Parus major, was transmitted to 3 great tits, but 3 blackcaps (Sylvia atricapilla) were not susceptible. Plasmodium vaughani of the robin, Erithacus rubecula, was transmitted to 1 robin and 1 blackcap, but 1 dunnock, Prunella modularis, was not susceptible. The prepatent period was between 8 and 10 days in all experimental infections. Maximum experimental parasitemia (3.4% of red cells) was detected in great tits infected with P. nucleophilum 23 days postexposure. A light (<0.01%) transient parasitemia of P. vaughani developed in the robin and blackcap. This study is in accord with former experimental observations on host specificity of P. nucleophilum and P. vaughani, which are characterized by a wide, but selective, range of avian hosts. Two new host-parasite associations were recorded.     

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.     

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.     

Haemoproteus and Leucocytozoon infections in birds of the Oklahoma City Zoo

A total of 222 birds, captive or free-flying in the Oklahoma City Zoo, were examined for blood parasites; 31 (14%) harbored Haemoproteus and/or Leucocytozoon. While 21% of the indigenous avifauna were infected, only 8% of the exotic bird species harbored haemoproteids and these parasites were also exotic to North America. There was no evidence to indicate that exotic infections were transmitted to native birds or vice versa.     

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.     

Evidence for cryptic speciation of Leucocytozoon spp. (Haemosporida, Leucocytozoidae) in diurnal raptors

Species of Leucocytozoon (Haemosporida, Leucocytozoidae) traditionally have been described based on morphological characters of their blood stages and host cells, with limited information on their avian host specificity. Based on the current taxonomy, Leucocytozoon toddi is the sole valid species of leucocytozoids parasitizing falconiform birds. Using a nested polymerase chain reaction protocol, we determined the prevalence of Leucocytozoon infection in 5 species of diurnal raptors from California. Of 591 birds tested, 177 (29.9%) were infected with Leucocytozoon toddi. Subsequent phylogenetic analysis of the cytochrome b gene revealed that distinct haplotypes are present in hawks of these genera. Haplotypes present in Buteo spp. are not found in Accipiter spp., and there is a 10.9% sequence divergence between the 2 lineage clades. In addition, Leucocytozoon sp. from Accipiter spp. from Europe group more closely with parasites found in Accipiter spp. from California than the same California Accipiter species do with their sympatric Buteo spp. Similarly, a Leucocytozoon haplotype from a Common Buzzard (Buteo buteo) from Kazakhstan forms a monophyletic lineage with a parasite from B. jamaicensis from California. These results suggest that Leucocytozoon toddi is most likely a group of cryptic species, with 1 species infecting Buteo spp. and 1 or more species, or subspecies, infecting Accipiter 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.