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Haemoproteus aegnithidaede |
Haemoproteus is a genus of protozoa that are parasitic in birds, reptiles and amphibians. The genus created was by Kruse in 1890. Its name is derived from Greek: Haima - blood and Proteus - a sea god who had the power of assuming different shapes. Three other genera - Halteridium, Haemocystidium and Simondia - are now considered to be synonyms of Haemoproteus.
The protozoa are intracellular parasites that infect the erythrocytes. They are transmitted by blood sucking insects including mosquitoes, louse flies (Hippoboscidae) and biting midges (Culicoides). Infection with this genus is sometimes know as pseudomalaria because of the parasites' similarities with Plasmodium species.
Within the genus there are 134 species, 5 varieties and 1 subspecies. Of these 114 occur in birds, 16 in reptiles and 3 in amphibia: 14 orders and 47 families of birds are represented. These include gamebirds (Galliformes), waterfowl (Anseriformes), raptors (Accipitriformes, Falconiformes, Strigiformes), pigeons and doves (Columbiformes), and perching birds or songbirds (Passeriformes).
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Life cycle
The infective stage is the sporozoite which is present in the salivary glands 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 erythrocytes and mature into either female gametocytes (macrogametocytes) or male gametocytes (microgametocytes). Gametocytes can then be ingested by another blood-sucking insect where they undergo sexual reproduction 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.
Evolution
The earliest known fossil is of a Haemoproteus like organism was found in the abdominal cavity of a female biting midge trapped 100 million years ago in amber and found in Myanmar.[1]
Diagnostic criteria
- Gametocytes are only present within 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 Haemoproteus columbae may develop enlarged gizzards.
Flocks of bobwhite quail (Colinus virginianus) may become infected with Haemoproteus lophortyx. Infected birds may suffer from reluctance to move, ruffled appearance, prostration and death. Other fidings 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 resulted in lameness, diarrhea, depression, emaciation, anorexia and occasionally anemia.
Muscovey ducks infected with Haemoproteus nettionis suffered lameness, dyspnea and sudden death.
In other avian species, anemia, anorexia and depression have been reported occasionally.
Host records
- 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), Florida sandhill crane (Grus canadensis pratensis)
- H. bambusicolae - bamboo partridge (Bambusicola thoracica sonorivox)
- H. balli - Egyptian cobra (Naja haje haje)
- H. beckeri - gray catbird (Dumatella carolinensis)
- H. belopolskyi - blackcaps (Sylvia atricapilla)
- H. borgesi - red-cockaded woodpecker (Picoides borealis)
- H. brachiatus - saker falcon (Falco cherrug)
- H. bucerotis - red-billed hornbill (Tockus erythrorhynchus)
- H. chelodina - saw-shelled tortoise (Elseya latisternum)
- H. coatneyi - white-crowned sparrows (Zonotrichia leucophrys)
- H. columbae - Japanese black wood pigeons (Columba janthina), pigeon (Columba livia), doves (Columbina talpacoti, Scardafella squammata, Zenaida auriculata), laughing dove (Streptopelia senegallus), eastern white-winged doves (Zenaida asiatica asiatica), mourning doves (Zenaida macroura)
- H. crumenium - wood stork (Mycteria americana)
- H. danilewskyi - blue jays (Cyanocitta cristata)
- H. dicruri - crested drongos (Dicrurus forficatus)
- H. edomensis - lizard (Agama stellio)
- H. elani - Cooper's hawk (Accipiter cooperii), sharp shinned hawk (Accipiter striatus)
- H. enucleator - kingfisher (Ispidina picta)
- H. fringillae - rufous-winged (Aimophila carpalis), house finch (Carpodacus mexicanus), hawfinch (Coccothraustes coccothraustes), dark-eyed juncos (Junco hyemalis), American redstarts (Setophaga ruticilla)
- H. forresteri - rufous-headed ground-roller (Atelornis crossleyi)
- H. geochelonis - tortoise (Geochelone denticulata)
- H. goodmani - pitta-like ground-roller (Atelornis pittoides)
- H. greineri - wood ducks (Aix sponsa), common mergansers (Mergus merganser)
- H. handai - lesser sulphur-crested cockatoo (Cacatua sulphurea)
- H. iwa - great frigatebirds (Fregata minor)
- H. janovyi - whitebacked vulture (Gyps africanus), hooded vulture (Necrosyrtes monachus), white-headed vulture (Trigonoceps occipitalis) lappet faced vulture (Torgos tracheliotus)
- H. khani - crested drongos (Dicrurus forficatus)
- H. kopki - spotted Indian house gecko (Hemidactylus brookei), giant frog eye gecko (Teratoscincus scincus)
- H. lanii - red backed shrike (Lanius collurio), woodchat shrike (Lanius senator)
- H. lari - Caspian gulls (Lams cachinnans)
- H. lophortyx - California quail (Callipepla californica), scaled quail (Callipepla squamata), bobwhite quail (Colinus virginianus)
- H. maccallumi - mourning doves (Zenaida macroura)
- H. mackerrasi - Binoe's prickly gecko (Heteronotia binoei)
- H. madagascariensis - hook-billed vanga (Vanga curvirostris)
- H. majoris - Swainson's thrush (Catharus ustulatus), blue tits (Cyanistes caeruleus, Parus caeruleus)
- H. mansoni - blue grouse (
Dendragapus obscurus ), ptarmigan (Lagopus lagopus)
- H. meleagridis - turkey (Meleagris gallopavo)
- H. mesnili - spitting cobra (Naja nigricollis nigricolli)
- H. metchnikovi - turtle (Chrysemys picta), yellow bellied terrapin (Tramchemys scripta)
- H. motacillae - yellow wagtails (Motacilla flava)
- H. nettionis - wood ducks (Aix sponsa), blue-winged teals (Anas discors), Pekin duck (Anas platyrhynchos), lesser scaups (Aythya affinis), ring-necked ducks (Aythya collaris), Muscovey duck (Cairina moschata), trumpeter swans (Olor buccinator)
- H. nisi - Cooper's hawk (Accipiter cooperii), sharp shinned hawk (Accipiter striatus)
- H. noctuae - snowy owls (Nyctea scandiaca), spotted owl (Strix occidentaiis)
- H. oedurae - Australian northern velvet gecko (Oedura castelnaui)
- H. orioli - golden oriole (Oriolus oriolus)
- H. palumbis - pigeon (Columba palumbis)
- H. pallidulus - blackcap (Sylvia atricapilla)[2]
- H. parabelopolskyi - blackcap (Sylvia atricapilla)
- H. passeris - Israeli house sparrow (Passer domesticus biblicus)
- H. pastoris - greater blue-eared glossy starling (Lamprotornis chalybaeus)
- H. peltocephali - river turtle (Peltocephalus dumerilianus)
- H. phyllodactyli - gekkonid (Ptyodactylus elisa)
- H. plataleae - glossy ibis (Plegadis falcinellus
- H. pratosi - Ahanta francolin (Francolinus ahantensis)
- H. pratasi - helmeted guineafowls (Numida meleagris)
- H. prognei - purple martin (Progne subis)
- H. psittaci - African grey parrot (Psittacus erithacus)
- H. ptyodactyli - Kramer's yellow fan-fingered gecko (Ptyodactylus hasselquistii)
- H. raymundi - eastern olive-sunbird (Cyanomitra olivacea)
- H. sacharovi - eastern white-winged doves (Zenaida asiatica asiatica), mourning doves (Zenaida macroura)
- H. sylvae - great reed warbler (Acrocephalus arundinaceus)
- H. syrnii - tawny owl (Strix aluco), spotted owl (Strix occidentaiis)
- H. tarentolae - Moorish gecko (Tarentola mauritanica)
- H. telfordi - houbara bustards (Chlamydotis undulata macqueenit), rufous-crested bustards (Eupodotis ruficrista), great bustard (Otis tarda)
- H. tendeiroi - houbara bustards (Chlamydotis undulata macqueenit), rufous-crested bustards (Eupodotis ruficrista), great bustard (Otis tarda)
- H. tinnunculi - American kestrels (Falco sparverius), Chimango caracara (Milvago chimango)
- H. vacuolatus - yellow-whiskered greenbul (Andropadus latirostris)
- H. vangii - hook-billed vanga (Vanga curvirostris)
- H. velans - red-bellied woodpecker (Melanerpes carolinus), red-cockaded woodpecker (Picoides borealis)
Hosts known to be infected but Haemoproteus species not identified
- common myna (Actidothetes tristis)
- great reed warbler (Acrocephalus arundinaceus)
- sedge warblers (Acrocephalus schoenobaenus
- reed warbler (Acrocephalus scirpaceus)
- Spanish red-legged partridge (Alectoris rufa)
- imperial eagles (Aquila heliaca)
- canvasbacks (Aythya valisineria)
- speckled pigeon (Columba guinea)
- Michigan blue jays (Cyanocitta cristata)
- green jays (Cyanocoraxyncas glaucescens)
- mute swan (Cygnus olor)
- magnificent bird of paradise (Diphyllodes magnificus hunsteini)
- hill mynahs (Gracula religiosa intermedia)
- lesser kestrels (Falco naumanni)
- common kestrel (Falco tinnunculus)
- Swainson's francolin (Francolinus swainsonii)
- magnificent frigatebirds (Fregata magnificens)
- chaffinch (Fringilla coelebs)
- superb bird of paradise (Lophorina superba)
- Egyptian kites (Milvus migrans aegypticus)
- Guianan red-capped cardinal (Paroaria gularis gularis)
- English sparrow (Passer domesticus)
- lesser flamingos (Phoeniconaias minor)
- New Holland honeyeaters (Phylidonyris novaehollandiae)
- 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)
- Galapagos doves (Zenaida galapagoensis)
- white-crowned sparrows (Zonotrichia leucophrys oriantha)
Vectors
- H. balmorali - Culicoides impunctatus
- H. belopolskyi - Culicoides impunctatus
- H. columbae - 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. sacharovi - Peseudolinchia maura
- H. tartakovskyi - Culicoides impunctatus
- H. turtur - Pseudolynchia canariensis
References
- ^ G. Poinar Jr., S.R. Telford Jr. (2005) Paleohaemoproteus burmacis gen. n., sp. n. (Haemospororida: Plasmodiidae) from an Early Cretaceous biting midge (Diptera: Ceratopogonidae) Parasitology 131(1)79-84
- ^ Križanauskienė A, Pérez-Tris J, Palinauskas V, Hellgren O, Bensch S, Valkiūnas G. (2009) Molecular phylogenetic and morphological analysis of haemosporidian parasites (Haemosporida) in a naturally infected European songbird, the blackcap Sylvia atricapilla, with description of Haemoproteus pallidulus sp. nov. Parasitology
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