''Haemoproteus'' is a

genus Genus ( plural genera ) is a taxonomic rank used in the biological classification of living and fossil organisms as well as viruses. In the hierarchy of biological classification, genus comes above species and below family. In binomial nom ...

of alveolates that are parasitic in

bird Birds are a group of warm-blooded vertebrates constituting the class Aves (), characterised by feathers, toothless beaked jaws, the laying of hard-shelled eggs, a high metabolic rate, a four-chambered heart, and a strong yet lightweig ...

s, reptiles and amphibians. Its name is derived from

Greek Greek may refer to: Greece Anything of, from, or related to Greece, a country in Southern Europe: *Greeks, an ethnic group. *Greek language, a branch of the Indo-European language family. **Proto-Greek language, the assumed last common ancestor ...

: ''Haima'', "blood", and ''Proteus'', a sea god who had the power of assuming different shapes. The name ''Haemoproteus'' was first used in the description of '' H. columbae'' in the blood of the pigeon ''

Columba livia The rock dove, rock pigeon, or common pigeon ( also ; ''Columba livia'') is a member of the bird family Columbidae (doves and pigeons). In common usage, it is often simply referred to as the "pigeon". The domestic pigeon (''Columba livia domes ...

'' by Kruse in 1890. This was also the first description of this genus. Two other genera — '' Halteridium'' and '' Simondia'' — are now considered to be synonyms of ''Haemoproteus''. The protozoa are intracellular parasites that infect the

erythrocytes Red blood cells (RBCs), also referred to as red cells, red blood corpuscles (in humans or other animals not having nucleus in red blood cells), haematids, erythroid cells or erythrocytes (from Greek ''erythros'' for "red" and ''kytos'' for "holl ...

. They are transmitted by blood sucking insects including

mosquito Mosquitoes (or mosquitos) are members of a group of almost 3,600 species of small flies within the family Culicidae (from the Latin ''culex'' meaning " gnat"). The word "mosquito" (formed by ''mosca'' and diminutive ''-ito'') is Spanish for "li ...

es, biting midges (''

Culicoides ''Culicoides'' is a genus of biting midges in the family Ceratopogonidae. There are over 1000 species in the genus,Connelly, C. RBiting midges: ''Culicoides'' spp.Featured Creatures, Entomology and Nematology Department, University of Florida IF ...

''), louse flies (''

Hippoboscidae __NOTOC__ Hippoboscidae, the louse flies or keds, are obligate parasites of mammals and birds. In this family, the winged species can fly at least reasonably well, though others with vestigial or no wings are flightless and highly apomorphic. As ...

'') and horse-flies (" tabanids", "tabanid flies"). Infection with this genus is sometimes known as pseudomalaria because of the parasites' similarities with ''

Plasmodium ''Plasmodium'' is a genus of unicellular eukaryotes that are obligate parasites of vertebrates and insects. The life cycles of ''Plasmodium'' species involve development in a blood-feeding insect host which then injects parasites into a ver ...

'' species. Within the genus there are at least 173

species In biology, a species is the basic unit of classification and a taxonomic rank of an organism, as well as a unit of biodiversity. A species is often defined as the largest group of organisms in which any two individuals of the appropriate s ...

, 5

varieties Variety may refer to: Arts and entertainment Entertainment formats * Variety (radio) * Variety show, in theater and television Films * ''Variety'' (1925 film), a German silent film directed by Ewald Andre Dupont * ''Variety'' (1935 film), ...

and 1 subspecies. Of these over 140 occur in birds, 16 in reptiles and 3 in amphibia: 14 orders and 50

families Family (from la, familia) is a group of people related either by consanguinity (by recognized birth) or affinity (by marriage or other relationship). The purpose of the family is to maintain the well-being of its members and of society. Ideal ...

of birds are represented. These include gamebirds (''

Galliformes Galliformes is an order of heavy-bodied ground-feeding birds that includes turkeys, chickens, quail, and other landfowl. Gallinaceous birds, as they are called, are important in their ecosystems as seed dispersers and predators, and are ofte ...

''), waterfowl ('' Anseriformes''), raptors (''

Accipitriformes The Accipitriformes (; from Latin ''accipiter''/''accipitri-'' "hawk", and New Latin ''-formes'' "having the form of") are an order of birds that includes most of the diurnal birds of prey, including hawks, eagles, vultures, and kites, but not f ...

'', ''

Falconiformes The order Falconiformes () is represented by the extant family Falconidae (falcons and caracaras) and a handful of enigmatic Paleogene species. Traditionally, the other bird of prey families Cathartidae (New World vultures and condors), Sagitt ...

'', '' Strigiformes''), pigeons and doves (''

Columbiformes Columbidae () is a bird family consisting of doves and pigeons. It is the only family in the order Columbiformes. These are stout-bodied birds with short necks and short slender bills that in some species feature fleshy ceres. They primarily ...

''), and perching birds or songbirds (''

Passeriformes A passerine () is any bird of the order Passeriformes (; from Latin 'sparrow' and '-shaped'), which includes more than half of all bird species. Sometimes known as perching birds, passerines are distinguished from other orders of birds by th ...

'').

Taxonomy and systematics

Evolution

The earliest known fossil is of a ''Haemoproteus''-like organism ('' Paleohaemoproteus burmacis'') was found in the abdominal cavity of a female

biting midge Ceratopogonidae is a family of flies commonly known as no-see-ums, or biting midges, generally in length. The family includes more than 5,000 species, distributed worldwide, apart from the Antarctic and the Arctic. Ceratopogonidae are holomet ...

trapped 100 million years ago in

amber Amber is fossilized tree resin that has been appreciated for its color and natural beauty since Neolithic times. Much valued from antiquity to the present as a gemstone, amber is made into a variety of decorative objects."Amber" (2004). In ...

found in

Myanmar Myanmar, ; UK pronunciations: US pronunciations incl. . Note: Wikipedia's IPA conventions require indicating /r/ even in British English although only some British English speakers pronounce r at the end of syllables. As John Wells explai ...

Taxonomic history

The first description of this genus was in 1890 by Kruse who described '' H. columbae'' in the blood of the pigeon ''

''. McCallum in 1897 showed that the process of exflagellation was part of

sexual reproduction Sexual reproduction is a type of reproduction that involves a complex life cycle in which a gamete ( haploid reproductive cells, such as a sperm or egg cell) with a single set of chromosomes combines with another gamete to produce a zygote th ...

in these parasites and thought it probable that the same process occurred in ''

''. The first record of a haemoproteid parasite in a reptile was by Simond in 1901 who gave it the name '' H. metchnikovi''. The Sergent brothers in 1906 showed that the ectoparasitic fly ''

Pseudolynchia canariensis ''Pseudolynchia canariensis'', the pigeon louse fly or pigeon fly, is a species of biting fly in the family of louse flies, Hippoboscidae. Distribution ''Pseudolynchia canariensis'' are species-specific (Columbidae) obligate ectoparasites potent ...

'' was the

vector Vector most often refers to: *Euclidean vector, a quantity with a magnitude and a direction *Vector (epidemiology), an agent that carries and transmits an infectious pathogen into another living organism Vector may also refer to: Mathematic ...

of ''H. columbae''. Aragao in 1908 demonstrated the schizogonic stages of ''H. columbae'' in the endothelial cells of the lungs of

nestling Birds are a group of warm-blooded vertebrates constituting the class Aves (), characterised by feathers, toothless beaked jaws, the laying of hard-shelled eggs, a high metabolic rate, a four-chambered heart, and a strong yet lightweight s ...

pigeons infected by the bite of infected ''Pseudolynchia''. It was generally believed that transmission of the parasites was by regurgitation during a blood meal until Adie showed that the parasites develop in the

salivary gland The salivary glands in mammals are exocrine glands that produce saliva through a system of ducts. Humans have three paired major salivary glands ( parotid, submandibular, and sublingual), as well as hundreds of minor salivary glands. Salivary ...

s in a fashion analogous to that of ''Plasmodium'' in

es. The genus '' Halterium'' was created by the French parasitologist Alphonse Labbe for a species he observed with

gametocyte A gametocyte is a eukaryotic germ cell that divides by mitosis into other gametocytes or by meiosis into gametids during gametogenesis. Male gametocytes are called ''spermatocytes'', and female gametocytes are called ''oocytes''. Development ...

s in

erythrocyte Red blood cells (RBCs), also referred to as red cells, red blood corpuscles (in humans or other animals not having nucleus in red blood cells), haematids, erythroid cells or erythrocytes (from Greek ''erythros'' for "red" and ''kytos'' for "holl ...

s, with pigment granules, and halter-shaped when fully formed. This genus was soon subsumed into the genus ''Haemoproteus''. The genus '' Haemocystidium'' was created to give a name to the haemoproteid of a gecko belonging to the genus ''

Hemidactylus __NOTOC__ ''Hemidactylus'' is a genus of the common gecko family, Gekkonidae. It has 189 described species, newfound ones being described every few years. These geckos are found in all the tropical regions of the world, extending into the subtrop ...

'' in Sri Lanka by Castellani and Willey in 1904. A second species in this genus was described in 1909 by Johnston and Cleland who found pigmented gametocytes in the blood of the Australian tortoise ''

Chelodina longicollis The eastern long-necked turtle (''Chelodina longicollis'')Kennett, R., Roe, J., Hodges, K., and Georges, A. 2009. ''Chelodina longicollis'' (Shaw 1784) – eastern long-necked turtle, common long-necked turtle, common snake-necked turtle. ''In'': ...

''. These species were transferred to ''Haemoproteus'' in 1926 by Wenyon. The genus was resurrected by Garnham in 1966 when he created a new generic name — '' Simondia'' — for the haemoproteids of

chelonia The green sea turtle (''Chelonia mydas''), also known as the green turtle, black (sea) turtle or Pacific green turtle, is a species of large sea turtle of the family Cheloniidae. It is the only species in the genus ''Chelonia''. Its range exten ...

ns. He followed the opinions of Wenyon, Hewitt and DeGiusti and suggested that all these parasites belonged to the one species — '' Simondia metchnikovi''. He retained the name ''Haemocystidium'' for the haemoproteids of lizards. A different genus of vectors was identified in 1957 by Fallis and Wood when they identified '' H. nettionis'' in '' Culicoides downesi'' Wirth and Hubert in

Ontario Ontario ( ; ) is one of the thirteen provinces and territories of Canada.Ontario is located in the geographic eastern half of Canada, but it has historically and politically been considered to be part of Central Canada. Located in Central C ...

, Canada. Levine and Campbell in 1971 moved all the species in ''Simondia'' and ''Haemocystidium'' into ''Haemoproteus'', an opinion that was followed by subsequent authors. The genus ''Haemocystidium'' was resurrected again by Telford in 1996 when he described three new species of protozoa in geckos from

Pakistan Pakistan ( ur, ), officially the Islamic Republic of Pakistan ( ur, , label=none), is a country in South Asia. It is the world's fifth-most populous country, with a population of almost 243 million people, and has the world's second-lar ...

. This genus like those of many protozoa may be further modified once additional DNA sequences are available. For instance, many DNA sequences have been identified for ''Haemoproteus'' in birds around the world in recent years, leading to new knowledge about the previously unknown diversity of this parasite in different regions.

Subgenera

The species infecting avian hosts have been divided into two subgenera — ''Haemoproteus'' and ''Parahaemoproteus'' — a division proposed in 1965 by Bennett ''et al''. These may be distinguished as follows: ': Vectors are hippoboscid flies (''

''). Exflagellation does not occur below 20 degrees Celsius. Mature oocysts have diameters greater than 20 micrometres. The average length of the

sporozoite Apicomplexans, a group of intracellular parasites, have life cycle stages that allow them to survive the wide variety of environments they are exposed to during their complex life cycle. Each stage in the life cycle of an apicomplexan organism is ...

s is less than 10 micrometres. One end of the sporozoite is more pointed than the other. Although the majority are parasites of the

, some species from this subgenus have also been reported in the

Charadriiformes Charadriiformes (, from ''Charadrius'', the type genus of family Charadriidae) is a diverse order of small to medium-large birds. It includes about 390 species and has members in all parts of the world. Most charadriiform birds live near water an ...

Pelecaniformes The Pelecaniformes are an order of medium-sized and large waterbirds found worldwide. As traditionally—but erroneously—defined, they encompass all birds that have feet with all four toes webbed. Hence, they were formerly also known by such n ...

and

Suliformes The order Suliformes (, dubbed "Phalacrocoraciformes" by ''Christidis & Boles 2008'') is an order recognised by the International Ornithologist's Union. In regard to the recent evidence that the traditional Pelecaniformes is polyphyletic, it has ...

. ': Parasites of birds other than the

. Vectors are biting midges (''

Ceratopogonidae Ceratopogonidae is a family of flies commonly known as no-see-ums, or biting midges, generally in length. The family includes more than 5,000 species, distributed worldwide, apart from the Antarctic and the Arctic. Ceratopogonidae are holomet ...

''). Exflagellation occurs below . Mature oocysts have diameters less than 20 micrometres. The average length of the sporozoites is greater than 10 micrometres. Both ends of the sporozoite are equally pointed. While it was previously thought that ''Haemoproteus'' was limited to doves and related species, species in this genus have been isolated from

frigatebird Frigatebirds are a family of seabirds called Fregatidae which are found across all tropical and subtropical oceans. The five extant species are classified in a single genus, ''Fregata''. All have predominantly black plumage, long, deeply forked ...

Species list

Haemoproteus columbae ''Haemoproteus columbae'' is a species of blood parasite related to ''Plasmodium'' and other malaria parasites. Phylogenetic relationships among the Haemosporidia ''Haemoproteus columbae'' is a true member of the genus ''Haemoproteus'', basal t ...

Haemoproteus parabelopolskyi ''Haemoproteus parabelopolskyi '' is a species of parasitic alveolates that infects birds. Seventeen strains of ''H. parabelopolskyi'' are found only in the blackcap, and form a monophyletic group; three further members of that group are found ...

'' *''Haemoproteus paramultipigmentatus'' *''Haemoproteus paranucleophilus'' *''Haemoproteus paruli'' *''Haemoproteus passeris'' *''Haemoproteus payevskyi'' *''Haemoproteus peltocephali'' *''Haemoproteus peircei'' *''Haemoproteus pelouri'' *''Haemoproteus phyllodactyli'' *''Haemoproteus piresi'' *''Haemoproteus plataleae'' *''Haemoproteus pratosi'' *''Haemoproteus prognei'' *''Haemoproteus psittaci'' *''Haemoproteus pteroclis'' *''Haemoproteus ptyodactyli'' *''Haemoproteus quelea'' *''Haemoproteus raymundi'' *''Haemoproteus rileyi'' *''Haemoproteus rupicola'' *''Haemoproteus sacharovi'' *''Haemoproteus sanguinus'' *''Haemoproteus sanîosdiasï'' *''Haemoproteus sauianae'' *''Haemoproteus sequeirae'' *''Haemoproteus serini'' *''Haemoproteus silvaï'' *''Haemoproteus sturni'' *''Haemoproteus sylvae'' *''Haemoproteus syrnii'' *''Haemoproteus tarentolae'' *''Haemoproteus tartakovskyi'' *''Haemoproteus telfordi'' *''Haemoproteus tendeiroi'' *''Haemoproteus tinnunculi'' *''Haemoproteus thraupi'' *''Haemoproteus trionyxi'' *''Haemoproteus turtur'' *''Haemoproteus uraeginthus'' *''Haemoproteus vacuolatus'' *''Haemoproteus valkiūnasi'' *''Haemoproteus vangii'' *''Haemoproteus velans'' *''Haemoproteus vireonis'' *''Haemoproteus wenyoni'' *''Haemoproteus witti'' *''Haemoproteus xantholemae'' *''Haemoproteus zosteropsis''

Life cycle

Haemoproteus ilanpapernai parasite130095-fig1

The infective stage is the

which is present in the

s of the vector. Once the vector bites a new host, the sporozoites enter the blood stream and invade endothelial cells of blood vessels within various tissues including those of the lung, liver and spleen. Within the endothelial cells, the sporozoites undergo asexual reproduction becoming schizonts. These in turn produce numerous merozoites which penetrate the

s and mature into either female gametocytes (macrogametocytes) or male gametocytes (microgametocytes). Gametocytes can then be ingested by another blood-sucking insect where they undergo

in the midgut of the insect to produce oocysts. The oocysts rupture and release numerous sporozoites that invade the salivary gland and serve as a focus of subsequent infection for another host once the insect takes its next blood meal.

Description

Only gametocytes are found in the blood. Asexual reproduction occurs in body organs, especially the liver. The organisms occupy the majority of the cytoplasm, leaving the light magenta, finely granular, pink Cell nucleus, nucleus centrally located. Taxonomy of this genus is difficult as there are few distinct morphological differences between the recognised species. Many of them were described under the 'one species-one host' hypothesis which is now thought to be potentially misleading. The morphological features most commonly used to describe a species include the number of pigment granules, the degree of encirclement of the host nucleus, the size of the parasite, the degree of host nucleus displacement and the degree of host cell enlargement. DNA studies should help to clarify this area but to date have rarely been undertaken. The gametocytes have five basic forms: *thin gametocytes with incomplete margins (''Haemoproteus balearicae, H. balearicae'', ''Haemoproteus pelouri, H. pelouri'') *halterial gametocytes (''Haemoproteus maccullumi, H. maccullumi'') *thick sausage shaped gametocytes that fill most of the host cell and displace the host nucleus laterally (''Haemoproteus halyconis, H. halyconis'', ''Haemoproteus plataleae, H. plataleae'') *gametocytes that encircle the host nucleus and fill the host cell (''Haemoproteus telfordi, H. telfordi'') *straight gametocytes that normally occur in anucleate cells and are almost as long as the host cell (''Haemoproteus enucleator, H. enucleator'')

Diagnostic criteria

*Gametocytes are only present within

s * Gametocytes have a "halter-shaped" appearance with little displacement of the host nucleus (cell), nucleus * Schizonts are not seen on peripheral blood smears * Multiple pigment granules (hemozoin) are present within the erythrocytes Pigment granules are refractile and yellow to brown in colour.

Pathology

Infections with most ''Haemoproteus'' species appear to produce subclinical infections. Post-mortem findings include enlargement of the spleen, liver and kidneys. These organs may appear chocolate-brown due to hemozoin deposition. Cytologic imprints may reveal schizont-laden endothelial cells. Some species of ''Haemoproteus'' will also form large, cyst-like bodies within the skeletal muscles that resembling those seen with ''Sarcocystis'' species infections. Pigeons infected with '' H. columbae'' may develop enlarged gizzards; and anemia has been recorded. Flocks of bobwhite quail (''Colinus virginianus'') may become infected with ''Haemoproteus lophortyx, H. lophortyx''. Infected birds may suffer from reluctance to move, ruffled appearance, prostration and death. Other findings include parasitemia and anemia. Large megaloschizonts may be present in skeletal muscles, particularly those of the thighs and back. The average cumulative mortality for flocks experiencing outbreaks may be over 20%. Experimental infection of turkeys with ''Haemoproteus meleagridis, H. meleagridis'' resulted in lameness, diarrhea, depression, emaciation, anorexia and occasionally anemia. Muscovey ducks infected with '' H. nettionis'' suffered lameness, dyspnea and sudden death. In other avian species, anemia and anorexia have been reported occasionally. Importantly, new records of ''Haemoproteus'' are discovered constantly and should still be monitored for effects on host condition.

Effect on vectors

''H. columbae'' infects rock pigeons (''

'') and is

ed by a hippoboscid fly (''

''). Both sexes of vector can transmit the parasite. Species of the ''Hippoboscoidea'' the superfamily to which ''Ps. canariensis'' belongs do not lay Egg (biology), eggs. Instead the larvae hatch ''in utero'', are fed internally by 'milk glands' and pass through three morphological stages before being deposited to pupate. The survival of female flies is significantly reduced when they were infected with the parasite. In contrast no effect is seen on male fly survival. Additionally the females produce fewer offspring when infected but the quality of the offspring does not seem to be affected.

Host records

Avian hosts

*''H. anthi'' — yellow wagtails (''Motacilla flava'') *''H. antigonis'' — Florida sandhill crane (''Grus canadensis pratensis'') *''H. balearicae'' — black crowned crane (''Balearica pavonina gibbericeps'', ''Balearica pavonina pavonina, B. p. pavonina''), Florida sandhill crane (''Grus canadensis pratensis'') *''H. bambusicolae'' — bamboo partridge (''Bambusicola thoracica sonorivox'') *''H. beckeri'' — gray catbird (''Dumetella carolinensis'') *''H. (Parahaemoproteus) belopolskyi'' — blackcaps (''Sylvia atricapilla'') *''H. bennetti'' — greater yellownape (''Picus flavinucha'') *''H. borgesi'' — red cockaded woodpecker (''Picoides borealis'') *''H. brachiatus'' — saker falcon (''Falco cherrug'') *''H. bucerotis'' — red billed hornbill (''Tockus erythrorhynchus'') *''H. (Parahaemoproteus) canachites'' — grouse *''H. (Parahaemoproteus) catharti'' — turkey vulture (''Cathartes aura'') *''H. (Parahaemoproteus) coatneyi'' — bananaquit (''Coereba flaveola''), white-crowned sparrows (''Zonotrichia leucophrys'') *''H. (Haemoproteus) columbae'' — Japanese black wood pigeons (''Columba janthina''), pigeon (''

''), doves (''Columbina talpacoti'', ''Scardafella squammata'', ''Zenaida auriculata''), laughing dove (''Stigmatopelia senegalensis''), eastern white-winged doves (''Zenaida asiatica asiatica, Z. asiatica asiatica''), mourning doves (''Zenaida macroura, Z. macroura'') *''H. (Parahaemoproteus) concavocentralis'' — hawfinch (''Coccothraustes coccothraustes'') *''H. cornuata'' — coppersmith barbet (''Megalaima haemacephala'') *''H. crumenium'' — wood stork (''Mycteria americana'') *''H. (Parahaemoproteus) cyanomitrae'' — olive sunbird (''Nectarinia olivacea'', ''Cyanomitra olivacea'') *''H. (Parahaemoproteus) danilewskyi'' — blue jays (''Cyanocitta cristata'') *''H. (Parahaemoproteus) desseri'' — blossom headed parakeet (''Psittacula roseata'') *''H. dicruri'' — fork tailed drongo (''Dicrurus adsimilis''), crested drongos (''Dicrurus forficatus, D. forficatus'') *''H. elani'' — Cooper's hawk (''Accipiter cooperii''), sharp shinned hawk (''Accipiter striatus, A. striatus'') *''H. enucleator'' — kingfisher (''Ispidina picta'') *''H. (Parahaemoproteus) fringillae'' — rufous-winged (''Aimophila carpalis''), house finch (''Carpodacus mexicanus''), hawfinch (''Coccothraustes coccothraustes''), oriental magpie robin (''Copsychus saularis''), dark-eyed juncos (''Junco hyemalis''), American redstarts (''Setophaga ruticilla'') *''H. forresteri'' — rufous-headed ground-roller (''Atelornis crossleyi'') *''H. gabaldoni'' — Muscovy duck (''Cairina moschata'') *''H. (Parahaemoproteus) garnhami'' — sparrows *''H. goodmani'' — pitta-like ground-roller (''Atelornis pittoides'') *''H. greineri'' — wood ducks (''Aix sponsa''), common mergansers (''Mergus merganser''), common pochard (''Aythya ferina'') *''H. handai'' — lesser sulphur-crested cockatoo (''Cacatua sulphurea''), plum-headed parakeet (''Psittacula cyanocephala''), ring necked parakeet (''Psittacula krameri manillensis'') *''H. himalayanus'' — rufous sibia (''Heterophasia capistrata'') *''H. (Parahaemoproteus) homobelopolskyi'' — red headed malimbe (''Malimbus rubricollis''), black headed weaver (''Ploceus melanocephalus''), red billed quelea (''Quelea quelea'') *''H. (Parahaemoproteus) homopalloris'' - wood warblers (''Phylloscopus sibilatrix'') *''H. (Parahaemoproteus) homovelans'' — grey-faced woodpecker (''Picus canus'') *''H. (Parahaemoproteus) hudaidensis'' — blue checked bee-eater (''Merops superciliosus persicus'' Pallas) *''H. ilanpapernai'' — spotted wood owl (''Strix seloputo''), Brown Hawk-Owl (''Ninox scutulata'') *''H. iwa'' — great frigatebirds (''Fregata minor''), magnificent frigatebirds (''Fregata magnificens, F. magnificens'') *''H. janovyi'' — whitebacked vulture (''Gyps africanus''), hooded vulture (''Necrosyrtes monachus''), white-headed vulture (''Trigonoceps occipitalis'') lappet faced vulture (''Torgos tracheliotus'') *''H. (Haemoproteus) jenniae'' — swallow tailed gull (''Creagrus furcatus'') *''H. khani'' — crested drongos (''Dicrurus forficatus'') *''H. (Parahaemoproteus) lanii'' — red backed shrike (''Lanius collurio''), woodchat shrike (''Lanius senator, L. senator'') *''H. lari'' — Caspian gulls (''Larus cachinnans'') *''H. (Parahaemoproteus) lophortyx'' — California quail (''Callipepla californica''), scaled quail (''Callipepla squamata''), bobwhite quail (''Colinus virginianus'') *''H. maccallumi'' — mourning doves (''Zenaida macroura'') *''H. macrovacuolatus'' — black-bellied whistling duck (''Dendrocygna autumnalis'') *''H. madagascariensis'' — hook billed vanga (''Vanga curvirostris'') *''H. majoris'' — Swainson's thrush (''Catharus ustulatus''), blue tit (''Cyanistes caeruleus''), collared flycatcher (''Ficedula albicollis''), pied flycatcher (''Ficedula hypoleuca, F. hypoleuca'') *''H. mansoni'' — blue grouse (''Dendragapus obscurus''), ptarmigan (''Lagopus lagopus'') *''H. meleagridis'' — turkey (''Meleagris gallopavo'') *''H. (Parahaemoproteus) micronuclearis'' — red headed malimbe (''Malimbus rubricollis''), black headed weaver (''Ploceus melanocephalus''), red billed quelea (''Quelea quelea'') *''H. (Haemoproteus) multipigmentatus'' — Galapagos dove (''Zenaida galapagoensis'') *''H. motacillae'' — yellow wagtails (''Motacilla flava'') *''H. (Haemoproteus) multivolutinus'' — tambourine dove (''Tambourine dove, Turtur timpanistria'') *''H. (Parahaemoproteus) nettionis'' — wood ducks (''Aix sponsa''), blue-winged teals (''Anas discors''), Pekin duck (''Anas platyrhynchos''), lesser scaups (''Aythya affinis''), common pochard (''Aythya ferina''), ring-necked ducks (''Aythya collaris''), Muscovey duck (''Cairina moschata''), trumpeter swans (''Cygnus buccinator'') *''H. nisi'' — Cooper's hawk (''Accipiter cooperii''), sharp shinned hawk (''Accipiter striatus, A. striatus'') *''H. (Parahaemoproteus) nucleofascialis'' — red headed malimbe (''Malimbus rubricollis''), black headed weaver (''Ploceus melanocephalus''), red billed quelea (''Quelea quelea'') *''H. noctuae'' — snowy owls (''Nyctea scandiaca''), spotted owl (''Strix occidentalis'') *''H. orioli'' — golden oriole (''Oriolus oriolus'') *''H. oryzivorae'' — oriental magpie robin (''Copsychus saularis''), Indian silverbill (''Lonchura malabarica''), tricoloured munia (''Lonchura malacca ruboniger, L. malacca ruboniger''), scaly-breasted munia (''Lonchura punctulata, L. punctulata''), baya weaver (''Ploceus philippinus''), jungle babbler (''Turdoides striata'') *''H. palumbus'' — pigeon (''Columba palumbus palumbus'') *''H. pallidus'' — pied flycatcher (''Ficedula hypoleuca''), collared flycatcher (''Ficedula albicollis, F. albicollis'') *''H. pallidulus'' — blackcap (''Sylvia atricapilla'') *''H. parabelopolskyi'' — blackcap (''Sylvia atricapilla'') *''H. (Haemoproteus) paramultipigmentatus'' — Socorro common ground dove (''Columbina passerina socorroensis'') *''H. passeris'' — Israeli house sparrow (''Passer domesticus biblicus'') *''H. pasteris'' — pied myna (''Sturnus contra''), grey headed myna (''Sturnus malabaricus, S. malabaricus'') *''H. pastoris'' — greater blue eared glossy starling (''Lamprotornis chalybaeus''), pied myna (''Sturnus contra'') *''H. payevskyi'' — great reed warbler (''Acrocephalus arundinaceus''), marsh warbler (''Acrocephalus palustris, A. palustris'') *''H. (Haemoproteus) piresi'' — pigeon (''

'') *''H. plataleae'' — glossy ibis (''Plegadis falcinellus'') *''H. pratosi'' — Ahanta francolin (''Francolinus ahantensis'') *''H. pratasi'' — helmeted guineafowl (''Numida meleagris'') *''H. prognei'' — purple martin (''Progne subis'') *''H. psittaci'' — African grey parrot (''Psittacus erithacus'') *''H. raymundi'' — eastern olive sunbird (''Nectarinia olivacea'') *''H. (Haemoproteus) sacharovi'' — eastern white-winged doves (''Zenaida asiatica asiatica''), mourning doves (''Zenaida macroura, Z. macroura'') *''H. sangunis'' — red whiskered bulbul (''Pycnonotus jocosus emeria'') *''H. (Parahaemoproteus) sanîosdiasï'' — chicken (''Gallus gallus'') *''H. silvaï'' — guinea fowl (''Numida meleagris mitrata'') *''H. sylvae'' — great reed warbler (''Acrocephalus arundinaceus'') *''H. syrnii'' — tawny owl (''Strix aluco''), spotted owl (''Strix occidentalis, S. occidentalis''), European scops owl (''Otus scops'') *''H. telfordi'' — MacQueen's bustards (''Chlamydotis macqueenii''), rufous-crested bustards (''Eupodotis ruficrista''), great bustard (''Otis tarda'') *''H. tendeiroi'' — MacQueen's bustards (''Chlamydotis macqueenii''), rufous-crested bustards (''Eupodotis ruficrista''), great bustard (''Otis tarda'') *''H. tinnunculi'' — American kestrel (''Falco sparverius''), Chimango caracara (''Milvago chimango'') *''H. (Haemoproteus) turtur'' — turtle dove (''Streptopelia turtur'') *''H. (Parahaemoproteus) vacuolatus'' — yellow whiskered greenbul (''Andropadus latirostris'') *''H. (Parahaemoproteus) valkiūnasi'' — great frigatebirds (''Fregata minor''), lesser frigatebirds (''Fregata ariel, F. ariel''), Ascension frigatebirds (''Fregata aquila, F. aquila'') *''H. vangii'' — hook billed vanga (''Vanga curvirostris'') *''H. (Parahaemoproteus) velans'' — red-bellied woodpecker (''Melanerpes carolinus''), red-cockaded woodpecker (''Picoides borealis'') *''H. zosteropsis'' — oriental white eye (''Zosterops palpebrosa palpebrosa'')

Reptile hosts

*''H. anatolicum'' — tortoise (''Testudo graeca'') *''H. balli'' — Egyptian cobra (''Naja haje, Naja haje haje'') *''H. chelodina'' — saw-shelled tortoise (''Elseya latisternum'') *''H. edomensis'' — lizard (''Agama stellio'') *''H. geochelonis'' — tortoise (''Geochelone denticulata'') *''H. kopki'' — spotted Indian house gecko (''Hemidactylus brookei''), giant frog eye gecko (''Teratoscincus scincus'') *''H. mackerrasi'' — Binoe's prickly gecko (''Heteronotia binoei'') *''H. mesnili'' — spitting cobra (''Naja nigricollis, Naja nigricollis nigricolli'') *''H. metchnikovi'' — turtle (''Chrysemys picta''), yellow bellied terrapin (''Tramchemys (pseudemys) scripta scripta, Tramchemys scripta'') *''H. oedurae'' — Australian northern velvet gecko (''Oedura castelnaui'') *''H. peltocephali'' — river turtle (''Peltocephalus dumerilianus'') *''H. phyllodactyli'' — gekkonid (''Ptyodactylus elisa'') *''H. ptyodactyli'' — Kramer's yellow fan-fingered gecko (''Ptyodactylus hasselquistii'') *''H. tarentolae'' — Moorish gecko (''Tarentola mauritanica'') *''H. trionyxi'' — Ganges softshell turtle (''Trionyx gangeticus'')

Amphibian hosts

*''H. ovalis'' — cricket frog (''Rana limnocharis'')

Hosts known to be infected but ''Haemoproteus'' species not identified

*common myna (''Acridotheres tristis'') *Blyth's reed warbler (''Acrocephalus dumetorum'') *sedge warblers (''Acrocephalus schoenobaenus'') *reed warbler (''Acrocephalus scirpaceus'') *clamorous reed warbler (''Acrocephalus stentoreus'') *black throated sunbird (''Aethopyga saturata'') *Spanish red-legged partridge (''Alectoris rufa'') *imperial eagles (''Aquila heliaca'') *canvasbacks (''Aythya valisineria'') *white cockatoo (''Cacatua alba'') *sulphur-crested cockatoo (''Cacatua galerita'') *speckled pigeon (''Columba guinea'') *white-rumped shama (''Copsychus malabaricus'') *green jays (''Cyanocorax yncas, Cyanocorax yncas glaucescens'') *European bee-eaters (''Merops apiaster'') *mute swan (''Cygnus olor'') *magnificent bird of paradise (''Diphyllodes magnificus, Diphyllodes magnificus hunsteini'') *red munia (''Estrilda amandava'') *lesser kestrel (''Falco naumanni'') *common kestrel (''Falco tinnunculus'') *Swainson's francolin (''Francolinus swainsonii'') *magnificent frigatebirds (''Fregata magnificens'') *chaffinch (''Fringilla coelebs'') *hill mynah (''Gracula religiosa, Gracula religiosa intermedia'') *long tailed shrike (''Lanius schach'') *superb bird of paradise (''Lophorina superba'') *Egyptian kites (''Milvus migrans, Milvus migrans aegypticus'') *Guianan red-capped cardinal (''Paroaria gularis, Paroaria gularis gularis'') *lesser flamingos (''Phoeniconaias minor'') *New Holland honeyeaters (''Phylidonyris novaehollandiae'') *streaked weaver (''Ploceus manyar'') *Surinam crested oropendola (''Psarocolius decumanus, Psarocolius decumanus decumanus'') *Montezuma oropendolas (''Psarocolius montezuma'') *Guianan turquoise tanager (''Tangara mexicana, Tangara mexicana mexicana'') *blue-necked tanager (''Tangara cyanicollis, Tangara cyanicollis caeruleocephala'') *sacred ibis (''Threskiornis aethiopicus'') *white-crowned sparrows (''Zonotrichia leucophrys, Zonotrichia leucophrys oriantha'')

Vectors

*''H. balmorali'' — ''Culicoides impunctatus'' *''H. belopolskyi'' — ''Culicoides impunctatus'' *''H. columbae'' — ''Ornithomyia avicularia'', ''

'' *''H. danilewskyi'' — ''Culicoides arboricola'', ''Culicoides edeni'', ''Culicoides knowltoni'' *''H. dolniki'' — ''Culicoides impunctatus'' *''H. fringillae'' — ''Culicoides impunctatus'' *''H. lanii'' — ''Culicoides impunctatus'' *''H. lophortyx'' — ''Culicoides bottimeri'', ''Lynchia hirsuta'', ''Stilbometopa impressa'' *''H. metchinikovi'' — ''Chrysops callidus'' *''H. nettionis'' — '' Culicoides downesi'' *''H. sacharovi'' — ''Peseudolynchia maura'' *''H. syrnii'' — ''Ornithomyia avicularia'' *''H. tartakovskyi'' — ''Culicoides impunctatus'' *''H. turtur'' — ''

Avian families affected

The concept of a "one host-one species" was originally used in the taxonomy of this genus as it appears that the parasites are at least moderately host specific. After this rule was found to be incorrect, it was suggested that the avian parasite species were limited to single avian families. From an inspection of the host records above it is clear that this is not the case. The avian species known to be infected are listed below: Order

Family Accipitridae *Cooper's hawk (''Accipiter cooperii'') *Sharp shinned hawk (''Accipiter striatus'') *Eastern imperial eagle (''Aquila heliaca'') *White-backed vulture (''Gyps africanus'') *Black kite (''Milvus migrans'') *Hooded vulture (''Necrosyrtes monachus'') *White-headed vulture (''Trigonoceps occipitalis'') *Lappet faced vulture (''Torgos tracheliotos'') Family Cathartidae *Turkey vulture (''Cathartes aura'') Order Anseriformes Family Anatidae *Wood duck (''Aix sponsa'') *Blue winged teal (''Anas discors'') *Mallard duck (''Anas platyrhynchos'') *Lesser scaup (''Aythya affinis'') *Ring necked duck (''Aythya collaris'') *Canvasback (''Aythya valisineria'') *Muscovy duck (''Cairina moschata'') *Trumpeter swan (''Cygnus buccinator'') *Mute swan (''Cygnus olor'') *Black-bellied whistling duck (''Dendrocygna autumnalis'') *Common merganser (''Mergus merganser'') Order

Family Laridae *Swallow tailed gull (''Creagrus furcatus'') *Caspian gull (''Larus cachinnans'') Order Ciconiiformes Family Ciconiidae *Wood stork (''Mycteria americana'') Order

Family Columbidae *Speckled pigeon (''Columba guinea'') *Japanese wood pigeon (''Columba janthina'') *Rock pigeon (''

'') *Common wood pigeon (''Columba palumbus'') *Socorro common ground dove (''Columbina passerina, Columbina passerina socorroensis'') *Ruddy ground dove (''Columbina talpacoti'') *Tambourine dove (''Tambourine dove, Turtur timpanistria'') *Scaled dove (''Scardafella squammata'') *European turtle dove (''Streptopelia turtur'') *Laughing dove (''Stigmatopelia senegalensis'') *White-winged dove (''Zenaida asiatica'') *Eared dove (''Zenaida auriculata'') *Galápagos Dove (''Zenaida galapagoensis'') *Mourning dove (''Zenaida macroura'') Order Coraciiformes Family Alcedinidae *African pygmy kingfisher (''Ispidina picta'') Family Brachypteraciidae *Rufous headed ground roller (''Atelornis crossleyi'') *Pitta like ground roller (''Atelornis pittoides'') Family Bucerotidae *Red-billed hornbill (''Tockus erythrorhynchus'') Family Meropidae *Blue checked bee-eater (''Merops superciliosus'') Order

Family Falconidae *Saker falcon (''Falco cherrug'') *Lesser kestrel (''Falco naumanni'') *American kestrel (''Falco sparverius'') *Common kestrel (''Falco tinnunculus'') *Chimango caracara (''Milvago chimango'') Order

Family Numididae *Helmeted guineafowl (''Numida meleagris'') Family Odontophoridae *California quail (''Callipepla californica'') *Scaled quail (''Callipepla squamata'') *Bobwhite quail (''Colinus virginianus'') Family Phasianidae *Red legged partridge (''Alectoris rufa'') *Chinese bamboo partridge (''Bambusicola thoracicus'') *Ahanta francolin (''Francolinus ahantensis'') *Swainson's francolin (''Francolinus swainsonii'') *Chicken (''Gallus gallus'') *Willow grouse (''Lagopus lagopus'') *Wild turkey (''Meleagris gallopavo'') Family Tetraonidae *Dusky grouse (''Dendragapus obscurus'' Order Gruiformes Family Gruidae *Black crowned crane (''Balearica pavonina'') *Sandhill crane (''Grus canadensis'') Family Otidae *MacQueen's bustard (''Chlamydotis macqueenii'') *Red crested bustard (''Eupodotis ruficrista'') *Great bustard (''Otis tarda'') Order

Family Acrocephalidae *Great reed warbler (''Acrocephalus arundinaceus'') *Blyth's reed warbler (''Acrocephalus dumetorum'') *Marsh warbler (''Acrocephalus palustris'') *Sedge warbler (''Acrocephalus schoenobaenus'') *Reed warbler (''Acrocephalus scirpaceus'') *Clamorous reed warbler (''Acrocephalus stentoreus'') Family Corvidae *Blue jay (''Cyanocitta cristata'') *Green jay (''Cyanocorax yncas'') Family Dicruridae *Fork-tailed drongo (''Dicrurus adsimilis'') *Crested drongo (''Dicrurus forficatus'') Family Emberizidae *Dark eyed junco (''Junco hyemalis'') *Rufous winged sparrow (''Aimophila carpalis, Peucaea carpalis'') *White crowned sparrow (''Zonotrichia leucophrys'') Family Estrildidae *Red munia (''Amandava amandava'') *Indian silverbill (''Euodice malabarica'') *Tricoloured munia (''Lonchura malacca'') *Scaly breasted munia (''Lonchura punctulata'') Family Fringillidae *House finch (''Carpodacus mexicanus'') *Hawfinch (''Coccothraustes coccothraustes'') *Chaffinch (''Fringilla coelebs'') Family Hirundinidae *Purple martin (''Progne subis'') Family Icteridae *Crested oropendola (''Psarocolius decumanus'') *Montezuma oropendola (''Psarocolius montezuma'') Family Laniidae *Red backed shrike (''Lanius collurio'') *Long tailed shrike (''Lanius schach'') *Woodchat shrike (''Lanius senator'') Family Meliphagidae *New Holland honeyeaters (''Phylidonyris novaehollandiae'') Family Mimidae *Gray catbird (''Dumetella carolinensis'') Family Motacillidae *Yellow wagtail (''Motacilla flava'') Family Muscicapidae *White rumped shama (''Copsychus malabaricus'') *Oriental magpie robin (''Copsychus saularis'') Family Nectariniidae *Black throated sunbird (''Aethopyga saturata'') *Olive sunbird (Nectarinia olivacea, Cyanomitra olivacea'') Family Oriolidae *Golden oriole (''Oriolus oriolus'') Family Paridae *Blue tit (''Cyanistes caeruleus'') Family Paradisaeidae *Magnificent bird of paradise (''Cicinnurus magnificus'') *Superb bird of paradise (''Lophorina superba'') Family Parulidae *American redstart (''Setophaga ruticilla'') Family Passeridae *House sparrow (''Passer domesticus'') Family Ploceidae *Red headed malimbe (''red-headed malimbe, Malimbus rubricollis'') *Streaked weaver (''Ploceus manyar'') *Black-headed weaver (''Ploceus melanocephalus'') *Baya weaver (''Ploceus philippinus'') *Red billed quelea (''Quelea quelea'') Family Pycnonotidae *Yellow whiskered bulbul (''Andropadus latirostris'') *Red whiskered bulbul (''Pycnonotus jocosus'') Family Sturnidae *Common myna (''Acridotheres tristis'') *Common hill myna (''Gracula religiosa'') *Chestnut tailed starling (''Sturnia malabarica'') *Asian pied starling (''Sturnus contra'') *Greater blue eared glossy starling (''Lamprotornis chalybaeus'') Family Sylviidae *Blackcap (''Sylvia atricapilla'') Family Thraupidae *Bananaquit (''Coereba flaveola'') *Red capped cardinal (''Paroaria gularis'') *Blue necked tanager (''Tangara cyanicollis'') *Turquoise tanager (''Tangara mexicana'') Family Timaliidae *Rufous sibia (''Heterophasia capistrata'') *Jungle babbler (''Turdoides striata'') Family Turdidae *Swainson's thrush (''Catharus ustulatus'') Family Vangidae *Hook billed vanga (''Vanga curvirostris'') Family Zosteropidae *Oriental white eye (''Zosterops palpebrosus'') Order

Family Fregatidae *Magnificent frigatebird (''Fregata magnificens'') *Great frigatebird (''Fregata minor'') Family Threskiornithidae *African sacred ibis (''Threskiornis aethiopicus'') *Glossy ibis (''Plegadis falcinellus'') Order Piciformes Family Megalaimidae *Coppersmith barbet (''Megalaima haemacephala'') Family Picidae *Red bellied woodpecker (''Melanerpes carolinus'') *Red cockaded woodpecker (''Picoides borealis'') *Grey faced woodpecker (''Picus canus'') *Greater yellownape (''Picus flavinucha'') Order Phoenicopteriformes Family Phoenicopteridae *Lesser flamingo (''Phoenicopterus minor'') Order Psittaciformes Family Cacatuidae *White cockatoo (''Cacatua alba'') *Sulphur crested cockatoo (''Cacatua galerita'') *Yellow crested cockatoo (''Cacatua sulphurea'') Family Psittacidae *Plum headed parakeet (''Psittacula cyanocephala'') *Rose ringed parakeet (''Psittacula krameri'') *Blossom headed parakeet (''Psittacula roseata'') *African grey parrot (''Psittacus erithacus'') Order Strigiformes Family Strigidae *Snowy owl (''Bubo scandiacus'') *Brown Hawk-Owl (''Ninox scutulata'') *European scops owl (''Otus scops'') *Brown owl (''Strix aluco'') *Spotted owl (''Strix occidentalis'') *Spotted wood owl (''Strix seloputo'')

Notes

''Haemoproteus balazuci'' Dias 1953 is a junior synonym of ''Haemoproteus testudinalis, H. testudinalis'' ''Haemoproteus gymnorhidis'' de Mello 1936, ''Haemoproteus granulosum'' Rey Vila 1945, ''Haemoproteus danilewskyi var. urbanensis'' Sachs 1953 and ''Haemoproteus zasukhini'' Burtikashvili 1973 are considered to be synonyms of ''Haemoproteus passeris, H. passeris'' Kruse 1890. ''Haemoproteus rouxi'' Novy and MacNeal 1904 is a ''nomen nudum''.

References

{{Taxonbar, from=Q5638270 Haemosporida Apicomplexa genera Poultry diseases Veterinary protozoology Parasites of reptiles Parasites of amphibians