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.     

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.     

Haematozoa of East African birds: II. Redescription of Haemoproteus centropi, a parasite of the Cuculidae

The avian haemoproteid, Haemoproteus centropi de Mello, a blood parasite found in members of the family Cuculidae, is redescribed from Clamator jacobinus Boddaert from Ngulia in Kenya. Haemoproteus froilanoi Tendeiro is considered to be a synonym of H. centropi. The reasons for this are discussed.     

The Host-Restriction of Haemoproteus sp. indet. of the Wood-Pigeon Columba p. palumbus

SYNOPSIS. Earlier experiments suggested that the species of Haemoproteus which infects English wood-pigeons ( Columba p. palumbus ) and is transmitted by the hippoboscid dipteran fly Ornithomya avicularia , was unable to infect Columba livia domestica , a host of H. columbae . This has now been confirmed by the injection of sporozoites into two pairs of pigeons, one of each species; in both experiments the C. palubus developed parasitemia while the C. livia did not. It has also been shown that this species of Haemoproteus can complete sporogony in a small proportion (2/73) of Pseudolynchla canariensis , the vector of H. columbae .     

The haemoproteids (Apicomplexa: Haemoproteidae) of the flowerpeckers of the avian family Dicaeidae (Passeriformes)

The haemoproteids of the flowerpecker family Dicaeidae are reviewed. Two new species, Haemoproteus dicaeus and H. nucleophilus, are described. Haemoproteus nucleophilus appears to be endemic in the dicaeids endemic to the New Guinea archipelago.     

Revision of the Thelastomatoidea,Oxyurida of invertebrate hosts I. Thelastomatidae

Haemoproteus psittaci n. sp., a microsomal halteridial haemoproteid, is described from the African grey parrot Psittacus erithacus. This species differs from Haemoproteus handai, the only other haemoproteid described from the Psittaciformes, in that it is halteridial, not circumnuclear, is much smaller in all dimensions and has only 10–12 pigment granules compared to 20–24 noted in the latter species.     

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.     

Haemoproteids of the avian family Dicruridae (the drongos)

Dicrurids are a widespread avian family in Africa and Asia. Earlier surveys of this family in these areas have reported the presence of hematozoa and 1 species of Haemoproteus, i.e., Haemoproteus dicruri (De Mello, 1935). One species of drongo occurs in Madagascar and has not been examined previously. Blood smears collected from wild-caught crested drongos, Dicrurus forficatus, in Madagascar were examined using a compound microscope for the presence of hematozoa. A new species, Haemoproteus khani, is described in this study. This new species has circumnuclear gametocytes, in contrast to the halteridial H. dicruri. In addition, H. dicruri is reported for the first time from the crested drongo and is redescribed. This is the first report of hematozoa in drongos of Madagascar.     

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.     

Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region

The degree to which widespread avian blood parasites in the genera Plasmodium and Haemoproteus pose a threat to novel hosts depends in part on the degree to which they are constrained to a particular host or host family. We examined the host distribution and host-specificity of these parasites in birds from two relatively understudied and isolated locations: Australia and Papua New Guinea. Using polymerase chain reaction (PCR), we detected infection in 69 of 105 species, representing 44% of individuals surveyed (n = 428). Across host families, prevalence of Haemoproteus ranged from 13% (Acanthizidae) to 56% (Petroicidae) while prevalence of Plasmodium ranged from 3% (Petroicidae) to 47% (Ptilonorhynchidae). We recovered 78 unique mitochondrial lineages from 155 sequences. Related lineages of Haemoproteus were more likely to derive from the same host family than predicted by chance at shallow (average LogDet genetic distance = 0, n = 12, P = 0.001) and greater depths (average distance = 0.014, n = 11, P < 0.001) within the parasite phylogeny. Within two major Haemoproteus subclades identified in a maximum likelihood phylogeny, host-specificity was evident up to parasite genetic distances of 0.029 and 0.007 based on logistic regression. We found no significant host relationship among lineages of Plasmodium by any method of analysis. These results support previous evidence of strong host-family specificity in Haemoproteus and suggest that lineages of Plasmodium are more likely to form evolutionarily-stable associations with novel hosts.     

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.     

Hematozoa of the avian family Brachypteraciidae (the ground-rollers)

The Brachypteraciidae is an avian family endemic to Madagascar. Members of this family were mist-netted in Madagascar, and blood smears were made to screen for the presence of hematozoa. Smears were stained with Giemsa and examined at x100, x160, and x1000 for hematozoa. Three new species of avian hematozoa from wild-caught ground-rollers in Madagascar are described. Haemoproteus goodmani n. sp. is found in the pitta-like ground-roller (Atelornis pittoides), whereas Haemoproteus forresteri n. sp. and Leucocytozoon frascai n. sp. are from the rufous-headed ground-roller (Atelornis crossleyi). These represent the first hematozoa described from this family.     

Widespread and structured distributions of blood parasite haplotypes across a migratory divide of the Swainson's thrush (Catharus ustulatus)

We examined the phylogenetic distribution of cytochrome b haplotypes of the avian blood parasite genera Haemoproteus and Plasmodium across the migratory divide of the Swainson's thrush (Catharus ustulatus) in British Columbia, Canada. From 87 host individuals, we identified 8 parasite haplotypes; 4 of Plasmodium and 4 of Haemoproteus. Six haplotypes were novel; 1 Haemoproteus haplotype was identical to H. majoris found in the blue tit (Parus caeruleus) in Sweden, and another halotype was identical to a Plasmodium haplotype found in the white-crowned sparrow (Zonotrichia leucophrys) in Oregon. The 2 most abundant parasite haplotypes were widely distributed across the contact zone, whereas 2 other parasite haplotypes seem to have structured distributions. Compared with 74 Plasmodium and Haemoproteus haplotypes published in GenBank, haplotypes recovered from Swainson's thrushes do not form monophyletic groups, and they are closely related to haplotypes from a variety of other hosts and localities. In addition, we recovered 2 Swainson's thrush Plasmodium haplotypes from the nonmigratory orange-billed nightingale thrush (Catharus aurantiirostris) in Costa Rica. This study is the first to elucidate avian blood parasite transmission, distribution, and phylogenetic relationships in an avian contact zone in North America.     

New avian Haemoproteus species (Haemosporida: Haemoproteidae) from African birds, with a critique of the use of host taxonomic information in hemoproteid classification

Haemoproteus (Parahaemoproteus) micronuclearis n. sp., Haemoproteus (Parahaemoproteus) nucleofascialis n. sp., Haemoproteus (Parahaemoproteus) paranucleophilus n. sp., and Haemoproteus (Parahaemoproteus) homobelopolskyi n. sp. (Haemosporida, Haemoproteidae) are described from African passeriform birds based on the morphology of their blood stages and segments of the mitochondrial cytochrome b gene. Red-billed quelea (Quelea quelea), red-headed malimbe (Malimbus rubricollis), and black-headed weaver (Ploceus melanocephalus) are the type vertebrate hosts of new hemoproteids. It is probable that new species have wide distribution in weavers in sub-Saharan Africa. Both H. micronuclearis and H. nucleofascialis can be readily distinguished from other avian hemoproteids by tiny, compact microgametocyte nuclei that are significantly smaller than macrogametocyte nuclei and are a rare character of hemosporidian parasites. Gametocytes of H. paranucleophilus are closely appressed to the erythrocyte nuclei and do not touch the erythrocyte envelope along their entire margin at all stages of their development, including fully grown gametocytes. A particularly distinctive feature of H. homobelopolskyi development is the presence of circumnuclear dumbbell-shaped macrogametocytes. Illustrations of blood stages of the new species are given, and morphological and phylogenetic analyses identify the DNA lineages that are associated with these parasites. Numerous recent studies show that some lineages of hemoproteids are often present in birds belonging to different families. As a result, the use of the host family as a taxonomic character should be questioned and preferably discouraged in hemoproteid taxonomy, particularly with regard to the parasites of passerine birds. Microscopic identification of avian hemoproteids requires comparison of Haemoproteus species described from birds of different families, as is an established practice with avian Plasmodium spp. Development of bar-coding techniques remains essential in taxonomic and field studies of hemosporidian parasites.     

Avian haematozoa: some taxonomic and nomenclatural problems arising from the Russian literature.

It is evident from a survey of the Russian literature that many species of avian haematozoa recorded do not meet the basic criteria required by the International Code of Zoological Nomenclature. Thus 28 species of Haemoproteus and 4 species of Leucocytozoon are considered to be nomina nuda, while 1 species, Leucocytozoon turtur orientalis is a synonym of L. marchouxi.     

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.     

A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences

A phylogeny of haemosporidian parasites (phylum Apicomplexa, family Plasmodiidae) was recovered using mitochondrial cytochrome b gene sequences from 52 species in 4 genera (Plasmodium, Hepatocystis, Haemoproteus, and Leucocytozoon), including parasite species infecting mammals, birds, and reptiles from over a wide geographic range. Leucocytozoon species emerged as an appropriate out-group for the other malarial parasites. Both parsimony and maximum-likelihood analyses produced similar phylogenetic trees. Life-history traits and parasite morphology, traditionally used as taxonomic characters, are largely phylogenetically uninformative. The Plasmodium and Hepatocystis species of mammalian hosts form 1 well-supported clade, and the Plasmodium and Haemoproteus species of birds and lizards form a second. Within this second clade, the relationships between taxa are more complex. Although jackknife support is weak, the Plasmodium of birds may form 1 clade and the Haemoproteus of birds another clade, but the parasites of lizards fall into several clusters, suggesting a more ancient and complex evolutionary history. The parasites currently placed within the genus Haemoproteus may not be monophyletic. Plasmodium falciparum of humans was not derived from an avian malarial ancestor and, except for its close sister species, P. reichenowi, is only distantly related to haemospordian parasites of all other mammals. Plasmodium is paraphyletic with respect to 2 other genera of malarial parasites, Haemoproteus and Hepatocystis. Explicit hypothesis testing supported these conclusions.     

Detrimental effects of Haemoproteus infections on the survival of biting midge Culicoides impunctatus (Diptera: Ceratopogonidae)

The effects of Haemoproteus belopolskyi, Haemoproteus fringillae, and Haemoproteus lanii on the survival of their vector the biting midge Culicoides impunctatus were examined. Wild-caught females were infected experimentally by allowing them to feed on naturally infected birds. A group of flies, which fed on an uninfected bird, was used as a control. There was a highly significant difference in the survival rate between the noninfected group and all groups of infected flies for postfeeding (PF) periods 1-2, 3-4, 5-6, and 7-8 days. For days 7-8, the percentage of noninfected surviving flies was 4.4 times higher than the percentage of infected surviving flies, testifying to the detrimental effects of avian Haemoproteus infections on the longevity of C. impunctatus. The mortality rates of the infected flies were highest for days 1-2 and 3-4 PF, indicating possible negative effects of ookinetes and early oocysts on the vector.