Haemoproteus

While it was previously thought that Haemoproteus was limited to doves and related species, species in this genus have been isolated from frigatebirds.^[4]

Species list

Life cycle

The infective stage is the

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 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 (H. balearicae, H. pelouri)
• halterial gametocytes (H. maccullumi)
• thick sausage shaped gametocytes that fill most of the host cell and displace the host nucleus laterally (H. halyconis, H. plataleae)
• gametocytes that encircle the host nucleus and fill the host cell (H. telfordi)
• straight gametocytes that normally occur in anucleate cells and are almost as long as the host cell (H. enucleator)

Diagnostic criteria

• erythrocytes
• Gametocytes have a "halter-shaped" appearance with little displacement of the host
  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.^[5]

Flocks of bobwhite quail (

Experimental infection of turkeys with 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.^[6]

Effect on vectors

H. columbae infects rock pigeons (

• H. anatolicum — tortoise (
  Testudo graeca
  )
• H. balli — Egyptian cobra (
  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 nigricolli
  )
• H. metchnikovi — turtle (
  Chrysemys picta), yellow bellied terrapin (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 —
  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)^[15]
• sulphur-crested cockatoo (
  Cacatua galerita)^[15]
• speckled pigeon (
  Columba guinea
  )
• white-rumped shama (
  Copsychus malabaricus
  )
• green jays (
  Cyanocorax yncas glaucescens
  )
• European bee-eaters (
  Merops apiaster
  )
• mute swan (
  Cygnus olor
  )
• magnificent bird of paradise (
  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 intermedia
  )
• long tailed shrike (
  Lanius schach
  )
• superb bird of paradise (
  Lophorina superba
  )
• Egyptian kites (
  Milvus migrans aegypticus
  )
• Guianan red-capped cardinal (
  Paroaria gularis gularis
  )
• lesser flamingos (
  Phoeniconaias minor
  )
• New Holland honeyeaters (
  Phylidonyris novaehollandiae
  )
• streaked weaver (
  Ploceus manyar
  )
• Surinam crested oropendola (
  Psarocolius decumanus decumanus
  )
• Montezuma oropendolas (
  Psarocolius montezuma
  )
• Guianan turquoise tanager (
  Tangara mexicana mexicana
  )
• blue-necked tanager (
  Tangara cyanicollis caeruleocephala
  )
• sacred ibis (
  Threskiornis aethiopicus
  )
• white-crowned sparrows (
  Zonotrichia leucophrys oriantha
  )

• H. balmorali —
  Culicoides impunctatus
• H. belopolskyi —
  Culicoides impunctatus
• H. columbae — Ornithomyia avicularia, Pseudolynchia canariensis
• 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 — Pseudolynchia canariensis

Avian families affected

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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 Accipitriformes

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
  )

A 2024 study found that the Haemoproteus species from accipitrid birds formed a distinct clade, found in these birds only and which might be classified into a separate subgenus or even genus.^[16]

Family

• 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 Charadriiformes

Family Laridae

• Swallow tailed gull (
  Creagrus furcatus
  )
• Caspian gull (
  Larus cachinnans
  )

Order

Family

• Wood stork (
  Mycteria americana
  )

Order

Family Columbidae

• Speckled pigeon (
  Columba guinea
  )
• Japanese wood pigeon (
  Columba janthina
  )
• Rock pigeon (
  Columba livia
  )
• Common wood pigeon (
  Columba palumbus
  )
• Socorro common ground dove (
  Columbina passerina socorroensis
  )
• Ruddy ground dove (
  Columbina talpacoti
  )
• 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

• African pygmy kingfisher (
  Ispidina picta
  )

Family

• Rufous headed ground roller (
  Atelornis crossleyi
  )
• Pitta like ground roller (
  Atelornis pittoides
  )

Family

• Red-billed hornbill (
  Tockus erythrorhynchus
  )

Family

• Blue checked bee-eater (
  Merops superciliosus
  )

Order Falconiformes

Family Falconidae

• Saker falcon (
  Falco cherrug
  )
• Lesser kestrel (
  Falco naumanni
  )
• American kestrel (
  Falco sparverius
  )
• Common kestrel (
  Falco tinnunculus
  )
• Chimango caracara (
  Milvago chimango
  )

Order Galliformes

Family

• Helmeted guineafowl (
  Numida meleagris
  )

Family

• 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

• Dusky grouse (
  Dendragapus obscurus

Order Gruiformes

Family

• 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

• Fork-tailed drongo (
  Dicrurus adsimilis
  )
• Crested drongo (
  Dicrurus forficatus
  )

Family

• Dark eyed junco (
  Junco hyemalis
  )
• Rufous winged sparrow (
  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

• House finch (
  Carpodacus mexicanus
  )
• Hawfinch (
  Coccothraustes coccothraustes
  )
• Chaffinch (
  Fringilla coelebs
  )

Family

• Purple martin (
  Progne subis
  )

Family

• Crested oropendola (
  Psarocolius decumanus
  )
• Montezuma oropendola (
  Psarocolius montezuma
  )

Family

• Red backed shrike (
  Lanius collurio
  )
• Long tailed shrike (
  Lanius schach
  )
• Woodchat shrike (
  Lanius senator
  )

Family

• New Holland honeyeaters (
  Phylidonyris novaehollandiae
  )

Family

• Gray catbird (
  Dumetella carolinensis
  )

Family Motacillidae

• Yellow wagtail (
  Motacilla flava
  )

Family

• White rumped shama (
  Copsychus malabaricus
  )
• Oriental magpie robin (
  Copsychus saularis
  )

Family

• Black throated sunbird (
  Aethopyga saturata
  )
• Olive sunbird (
  Cyanomitra olivacea
  )

Family

• Golden oriole (
  Oriolus oriolus
  )

Family

• Blue tit (
  Cyanistes caeruleus
  )

Family

• Magnificent bird of paradise (
  Cicinnurus magnificus
  )
• Superb bird of paradise (
  Lophorina superba
  )

Family

• American redstart (
  Setophaga ruticilla
  )

Family

• House sparrow (
  Passer domesticus
  )

Family Ploceidae

• Red headed malimbe (Malimbus rubricollis)
• Streaked weaver (
  Ploceus manyar
  )
• Black-headed weaver (
  Ploceus melanocephalus
  )
• Baya weaver (
  Ploceus philippinus
  )
• Red billed quelea (
  Quelea quelea
  )

Family

• Yellow whiskered bulbul (
  Andropadus latirostris
  )
• Red whiskered bulbul (
  Pycnonotus jocosus
  )

Family

• 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

• Bananaquit (
  Coereba flaveola
  )
• Red capped cardinal (
  Paroaria gularis
  )
• Blue necked tanager (
  Tangara cyanicollis
  )
• Turquoise tanager (
  Tangara mexicana
  )

Family

• Rufous sibia (
  Heterophasia capistrata
  )
• Jungle babbler (
  Turdoides striata
  )

Family

• Swainson's thrush (
  Catharus ustulatus
  )

Family

• Hook billed vanga (
  Vanga curvirostris
  )

Family

• Oriental white eye (
  Zosterops palpebrosus
  )

Order Pelecaniformes

Family

• 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

• Red bellied woodpecker (
  Melanerpes carolinus
  )
• Red cockaded woodpecker (
  Picoides borealis
  )
• Grey faced woodpecker (
  Picus canus
  )
• Greater yellownape (
  Picus flavinucha
  )

Order Phoenicopteriformes

Family

• Lesser flamingo (
  Phoenicopterus minor
  )

Order

Family

• 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

Family

• 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 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 H. passeris Kruse 1890.

Haemoproteus rouxi Novy and MacNeal 1904 is a nomen nudum.

References