Haemoproteus is a genus of protozoa that are parasitic in bird

Bird

Birds are feathered, winged, bipedal, endothermic , egg-laying, vertebrate animals. Around 10,000 living species and 188 families makes them the most speciose class of tetrapod vertebrates. They inhabit ecosystems across the globe, from the Arctic to the Antarctic. Extant birds range in size from...

s, reptile

Reptile

Reptiles are members of a class of air-breathing, ectothermic vertebrates which are characterized by laying shelled eggs , and having skin covered in scales and/or scutes. They are tetrapods, either having four limbs or being descended from four-limbed ancestors...

s and amphibian

Amphibian

Amphibians , are a class of vertebrate animals including animals such as toads, frogs, caecilians, and salamanders. They are characterized as non-amniote ectothermic tetrapods...

s. Its name is derived from Greek

Greek language

Greek is an independent branch of the Indo-European family of languages. Native to the southern Balkans, it has the longest documented history of any Indo-European language, spanning 34 centuries of written records. Its writing system has been the Greek alphabet for the majority of its history;...

: 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 Haemoproteus columbae in the blood of the pigeon Columba livia 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. They are transmitted by blood sucking insects including mosquito

Mosquito

Mosquitoes are members of a family of nematocerid flies: the Culicidae . The word Mosquito is from the Spanish and Portuguese for little fly...

es, biting midges (Culicoides

Culicoides

Culicoides is a genus of biting midges in the subfamily Ceratopogonidae. Around 500 species of Ceratopogonidae are at present placed in the genus and this is split into many subgenera. Several species are known to be vectors of various diseases and parasites which can affect animals.-Notable...

), louse flies (Hippoboscidae

Hippoboscidae

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

) and tabanid flies (Tabanidae). Infection with this genus is sometimes known as pseudomalaria because of the parasites' similarities with Plasmodium

Plasmodium

Plasmodium is a genus of parasitic protists. Infection by these organisms is known as malaria. The genus Plasmodium was described in 1885 by Ettore Marchiafava and Angelo Celli. Currently over 200 species of this genus are recognized and new species continue to be described.Of the over 200 known...

 species.

Within the genus there are at least 173 species, 5 varieties and 1 subspecies. Of these over 140 occur in birds, 16 in reptiles and 3 in amphibia: 14 orders and 50 families of birds are represented. These include gamebirds (Galliformes

Galliformes

Galliformes are an order of heavy-bodied ground-feeding domestic or game bird, containing turkey, grouse, chicken, New and Old World Quail, ptarmigan, partridge, pheasant, and the Cracidae. Common names are gamefowl or gamebirds, landfowl, gallinaceous birds or galliforms...

), waterfowl (Anseriformes

Anseriformes

The order Anseriformes contains about 150 living species of birds in three extant families: the Anhimidae , Anseranatidae , and the Anatidae, which includes over 140 species of waterfowl, among them the ducks, geese, and swans.All species in the order are highly adapted for an aquatic existence at...

), raptors (Accipitriformes

Accipitriformes

The Accipitriformes is an order that has been proposed to include most of the diurnal birds of prey: hawks, eagles, vultures, and many others, about 225 species in all. For a long time, the majority view has been to include them with the falcons in the Falconiformes, but some authorities have...

, Falconiformes

Falconiformes

The order Falconiformes is a group of about 290 species of birds that comprises the diurnal birds of prey. Raptor classification is difficult and the order is treated in several ways.- Classification problems :...

, Strigiformes), pigeons and doves (Columbiformes

Columbiformes

Columbiformes are an avian order that includes the very widespread and successful doves and pigeons, classified in the family Columbidae, and the extinct Dodo and the Rodrigues Solitaire, long classified as a second family Raphidae. 313 species, found worldwide, comprise the Columbiformes order....

), and perching birds or songbirds (Passeriformes).

History

The first description of this genus was in 1890 by Kruse who described Haemoproteus columbae in the blood of the pigeon
Columba livia. McCallum in 1897 showed that the process of exflagellation was part of sexual reproduction in these parasites and thought it probable that the same process occurred in Plasmodium

Plasmodium

Plasmodium is a genus of parasitic protists. Infection by these organisms is known as malaria. The genus Plasmodium was described in 1885 by Ettore Marchiafava and Angelo Celli. Currently over 200 species of this genus are recognized and new species continue to be described.Of the over 200 known...

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

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:They are found in most parts of the tropical world where domestic pigeons are kept...

 was the vector of Haemoproteus columbae. Aragao in 1908 demonstrated the schizogonic stages of Haemoproteus columbae in the endothelial cells of the lung

Lung

The lung is the essential respiration organ in many air-breathing animals, including most tetrapods, a few fish and a few snails. In mammals and the more complex life forms, the two lungs are located near the backbone on either side of the heart...

s of nestling 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 glands in a fashion analogous to that of Plasmodium in mosquito

Mosquito

Mosquitoes are members of a family of nematocerid flies: the Culicidae . The word Mosquito is from the Spanish and Portuguese for little fly...

es.

The genus Halterium was created by the French parasitologist Alphonse Labbe for a species he observed with gametocytes in erythrocytes, with pigment granules, and halter-shaped when fully formed. This genus was soon subsumed into the genus Haemoproteus.

The genus Haemocystidium

Haemocystidium

Haemocystidium is a genus of parasitic protozoa belonging to the phylum Apicomplexia.-History:The genus Haemocystidium was created to give a name to the haemoproteid of a gecko belonging to the genus Hemidactylus in Sri Lanka by Castellani and Willey in 1904...

 was created to give a name to the haemoproteid of a gecko belonging to the genus Hemidactylus

Hemidactylus

Hemidactylus is a genus of the family of typical geckos, Gekkonidae. It is the second-most speciose genus in the family, with about 90 described species, newfound ones being described every few years. These geckos are found in all the tropical regions of the world, extending into the subtropical...

 in Sri Lanka

Sri Lanka

Sri Lanka, officially the Democratic Socialist Republic of Sri Lanka is a country off the southern coast of the Indian subcontinent. Known until 1972 as Ceylon , Sri Lanka is an island surrounded by the Indian Ocean, the Gulf of Mannar and the Palk Strait, and lies in the vicinity of India and the...

 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 Australia

Australia

Australia , officially the Commonwealth of Australia, is a country in the Southern Hemisphere comprising the mainland of the Australian continent, the island of Tasmania, and numerous smaller islands in the Indian and Pacific Oceans. It is the world's sixth-largest country by total area...

n tortoise

Tortoise

Tortoises are a family of land-dwelling reptiles of the order of turtles . Like their marine cousins, the sea turtles, tortoises are shielded from predators by a shell. The top part of the shell is the carapace, the underside is the plastron, and the two are connected by the bridge. The tortoise...

 Chelodina longicollis. 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
chelonian

Chelonian

Chelonian has multiple, interrelated meanings:*Green turtle*Chelonia, the superorder uniting turtles, tortoises and terrapins with the "proto-turtle" Australochelys*Chelonians, monsters from Doctor Who...

s. 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 lizard

Lizard

Lizards are a widespread group of squamate reptiles, with nearly 3800 species, ranging across all continents except Antarctica as well as most oceanic island chains...

s.

A different genus of vectors was identified in 1957 by Fallis and Wood when they identified Haemoproreus nettionis in Culicoides downesi Wirth and Hubert in Ontario

Ontario

Ontario is a province of Canada, located in east-central Canada. It is Canada's most populous province and second largest in total area. It is home to the nation's most populous city, Toronto, and the nation's capital, Ottawa....

, Canada

Canada

Canada is a North American country consisting of ten provinces and three territories. Located in the northern part of the continent, it extends from the Atlantic Ocean in the east to the Pacific Ocean in the west, and northward into the Arctic Ocean...

.

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

Pakistan , officially the Islamic Republic of Pakistan is a sovereign state in South Asia. It has a coastline along the Arabian Sea and the Gulf of Oman in the south and is bordered by Afghanistan and Iran in the west, India in the east and China in the far northeast. In the north, Tajikistan...

.

This genus like those of many protozoa may be further modified once additional DNA sequences are available.

Life cycle

The infective stage is the sporozoite which is present in the salivary gland

Salivary gland

The salivary glands in mammals are exocrine glands, glands with ducts, that produce saliva. They also secrete amylase, an enzyme that breaks down starch into maltose...

s of the vector. Once the vector bites a new host, the sporozoites enter the blood stream and invade endothelial cells of blood vessel

Blood vessel

The blood vessels are the part of the circulatory system that transports blood throughout the body. There are three major types of blood vessels: the arteries, which carry the blood away from the heart; the capillaries, which enable the actual exchange of water and chemicals between the blood and...

s within various tissues including those of the lung

Lung

The lung is the essential respiration organ in many air-breathing animals, including most tetrapods, a few fish and a few snails. In mammals and the more complex life forms, the two lungs are located near the backbone on either side of the heart...

, liver

Liver

The liver is a vital organ present in vertebrates and some other animals. It has a wide range of functions, including detoxification, protein synthesis, and production of biochemicals necessary for digestion...

 and spleen

Spleen

The spleen is an organ found in virtually all vertebrate animals with important roles in regard to red blood cells and the immune system. In humans, it is located in the left upper quadrant of the abdomen. It removes old red blood cells and holds a reserve of blood in case of hemorrhagic shock...

. Within the endothelial cells, the sporozoites undergo asexual reproduction

Asexual reproduction

Asexual reproduction is a mode of reproduction by which offspring arise from a single parent, and inherit the genes of that parent only, it is reproduction which does not involve meiosis, ploidy reduction, or fertilization. A more stringent definition is agamogenesis which is reproduction without...

 becoming schizonts. These in turn produce numerous merozoites which penetrate the erythrocytes and mature into either female gametocytes (macrogametocytes) or male gametocytes (microgametocytes). Gametocyte

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....

s can then be ingested by another blood-sucking insect where they undergo sexual reproduction

Sexual reproduction

Sexual reproduction is the creation of a new organism by combining the genetic material of two organisms. There are two main processes during sexual reproduction; they are: meiosis, involving the halving of the number of chromosomes; and fertilization, involving the fusion of two gametes and the...

 in the midgut

Midgut

The midgut is the portion of the embryo from which most of the intestines develop. After it bends around the superior mesenteric artery, it is called the "midgut loop"...

 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 (Paleohaemoproteus burmacis) was found in the abdominal cavity of a female biting midge trapped 100 million years ago in amber

Amber

Amber is fossilized tree resin , which has been appreciated for its color and natural beauty since Neolithic times. Amber is used as an ingredient in perfumes, as a healing agent in folk medicine, and as jewelry. There are five classes of amber, defined on the basis of their chemical constituents...

 found in Myanmar

Myanmar

Burma , officially the Republic of the Union of Myanmar , is a country in Southeast Asia. Burma is bordered by China on the northeast, Laos on the east, Thailand on the southeast, Bangladesh on the west, India on the northwest, the Bay of Bengal to the southwest, and the Andaman Sea on the south....

.

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.

General description

Only gametocytes are found in the blood

Blood

Blood is a specialized bodily fluid in animals that delivers necessary substances such as nutrients and oxygen to the cells and transports metabolic waste products away from those same cells....

.

Asexual reproduction occurs in body organs especially the liver

Liver

The liver is a vital organ present in vertebrates and some other animals. It has a wide range of functions, including detoxification, protein synthesis, and production of biochemicals necessary for digestion...

.

The organisms occupy the majority of the cytoplasm

Cytoplasm

The cytoplasm is a small gel-like substance residing between the cell membrane holding all the cell's internal sub-structures , except for the nucleus. All the contents of the cells of prokaryote organisms are contained within the cytoplasm...

, leaving the a light magenta, finely granular, pink nucleus

Cell nucleus

In cell biology, the nucleus is a membrane-enclosed organelle found in eukaryotic cells. It contains most of the cell's genetic material, organized as multiple long linear DNA molecules in complex with a large variety of proteins, such as histones, to form chromosomes. The genes within these...

 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 hos't 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)

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:

Haemoproteus: Parasites of the Columbiformes

Columbiformes

Columbiformes are an avian order that includes the very widespread and successful doves and pigeons, classified in the family Columbidae, and the extinct Dodo and the Rodrigues Solitaire, long classified as a second family Raphidae. 313 species, found worldwide, comprise the Columbiformes order....

. Vectors are hippoboscid flies (Hippoboscidae

Hippoboscidae

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

). Exflagellation does not occur below 20 degrees Celsius. Mature oocysts have diameters greater than 20 micrometres. The average length of the sporozoites is less than 10 micrometres. One end of the sporozoite is more pointed than the other.

Parahaemoproteus: Parasites of birds other than the Columbiformes. Vectors are biting midges (Ceratopogonidae

Ceratopogonidae

Ceratopogonidae, or biting midges , are a family of small flies in the order Diptera...

). Exflagellation occurs below 20 degrees Celsius. 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.

Pathology

Infections with most Haemoproteus species appear to produce subclinical infections.

Post-mortem findings include enlargement of the spleen

Spleen

The spleen is an organ found in virtually all vertebrate animals with important roles in regard to red blood cells and the immune system. In humans, it is located in the left upper quadrant of the abdomen. It removes old red blood cells and holds a reserve of blood in case of hemorrhagic shock...

, liver

Liver

The liver is a vital organ present in vertebrates and some other animals. It has a wide range of functions, including detoxification, protein synthesis, and production of biochemicals necessary for digestion...

 and kidney

Kidney

The kidneys, organs with several functions, serve essential regulatory roles in most animals, including vertebrates and some invertebrates. They are essential in the urinary system and also serve homeostatic functions such as the regulation of electrolytes, maintenance of acid–base balance, and...

s. 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

Sarcocystis

Sarcocystis is a genus of protozoa. Species in this genus infect reptiles, birds and mammals. The name is dervived from Greek: sarx = flesh and kystis = bladder.There are about 130 recognised species in this genus...

 species infections.

Pigeons infected with Haemoproteus columbae

Haemoproteus columbae

Haemoproteus columbae is a species of parasitic protozoa that infects pidgeons. It is slated for genome sequencing....

 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.

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), 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 (Columba livia), doves (Columbina talpacoti, Scardafella squammata, Zenaida auriculata), laughing dove (Stigmatopelia senegalensis), eastern white-winged doves (Zenaida asiatica asiatica), mourning doves (Zenaida macroura)
• H. cornuata - coppersmith barbet (Megalaima haemacephala)
• H. crumenium - wood stork (Mycteria americana)
• H. (Parahaemoproteus) cyanomitrae - olive sunbird (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)
• H. elani - Cooper's hawk (Accipiter cooperii), sharp shinned hawk (Accipiter 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)
• 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. 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. (Parahaemoproteus) lanii - red backed shrike (Lanius collurio), woodchat shrike (Lanius 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. 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
  Dendragapus obscurus
  The Dusky Grouse is a species of forest-dwelling grouse native to the Rocky Mountains in North America. It is closely related to the Sooty Grouse , and the two were previously considered a single species, the Blue Grouse.-Description:Adults have a long square tail, gray at the end...
  
  ), ptarmigan (Lagopus lagopus)
• H. meleagridis - turkey (Meleagris gallopavo)
• H. (Haemoproteus) multipigmentatus - Galapagos dove (Zenaida galapagoensis)
• H. motacillae - yellow wagtails (Motacilla flava)
• H. (Parahaemoproteus) 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 (Cygnus buccinator)
• H. nisi - Cooper's hawk (Accipiter cooperii), sharp shinned hawk (Accipiter striatus)
• 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), scaly-breasted munia (Lonchura punctulata), baya weaver (Ploceus philippinus), jungle babbler (Turdoides striata)
• H. palumbus - pigeon (Columba palumbus palumbus)
• H. pallidulus - blackcap (Sylvia atricapilla)
• H. parabelopolskyi - blackcap (Sylvia atricapilla)
• H. passeris - Israeli house sparrow (Passer domesticus biblicus)
• H. pasteris - pied myna (Sturnus contra), grey headed myna (Sturnus 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)
• H. (Haemoproteus) piresi - pigeon (Columba livia)
• 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. raymundi - eastern olive-sunbird (Nectarinia olivacea)
• H. (Haemoproteus) sacharovi - eastern white-winged doves (Zenaida asiatica asiatica), mourning doves (Zenaida 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), 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 kestrels (Falco sparverius), Chimango caracara (Milvago chimango)
• H. (Haemoproteus) turtur - turtle dove (Streptopelia turtur)
• H. (Parahaemoproteus) vacuolatus - yellow-whiskered greenbul (Andropadus latirostris)
• 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. 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
  Heteronotia binoei
  Heteronotia binoei, commonly known as Binoe's prickly gecko, is a species of lizard endemic to Australia. One of Australia's least habitat-specific geckos, it occurs naturally across much of the country, and has also established in areas where it does not occur naturally, such as urban Perth,...
  
  )
• H. mesnili - spitting cobra (Naja nigricollis nigricolli
  Naja nigricollis
  Naja nigricollis is a species of spitting cobra found in Sub Saharan Africa. It is feared throughout its range and has the capability of spraying venom at attackers as a defensive mechanism...
  
  )
• 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 - Ganges softshell turtle (Trionyx gangeticus)

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 glaucescens)
• 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)

Vectors

• H. balmorali - Culicoides impunctatus
• H. belopolskyi - Culicoides impunctatus
• H. columbae - Ornithomyia avicularia, Pseudolynchia canariensis
  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:They are found in most parts of the tropical world where domestic pigeons are kept...
  
  
• 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. tartakovskyi - Culicoides impunctatus
• H. turtur - Pseudolynchia canariensis
  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:They are found in most parts of the tropical world where domestic pigeons are kept...
  
  

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 Accipitriformes

Accipitriformes

The Accipitriformes is an order that has been proposed to include most of the diurnal birds of prey: hawks, eagles, vultures, and many others, about 225 species in all. For a long time, the majority view has been to include them with the falcons in the Falconiformes, but some authorities have...

Family Accipitridae

Accipitridae

The Accipitridae, one of the two major families within the order Accipitriformes , are a family of small to large birds with strongly hooked bills and variable morphology based on diet. They feed on a range of prey items from insects to medium-sized mammals, with a number feeding on carrion and a...

• 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

Anseriformes

The order Anseriformes contains about 150 living species of birds in three extant families: the Anhimidae , Anseranatidae , and the Anatidae, which includes over 140 species of waterfowl, among them the ducks, geese, and swans.All species in the order are highly adapted for an aquatic existence at...

Family Anatidae

Anatidae

Anatidae is the biological family of birds that includes ducks, geese and swans. The family has a cosmopolitan distribution, occurring on all the world's continents except Antarctica and on most of the world's islands and island groups...

• 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)
• common merganser (Mergus merganser)

Order Charadriiformes

Charadriiformes

Charadriiformes is a diverse order of small to medium-large birds. It includes about 350 species and has members in all parts of the world. Most Charadriiformes live near water and eat invertebrates or other small animals; however, some are pelagic , some occupy deserts and a few are found in thick...

Family Laridae

• Caspian gull (Larus cachinnans)

Order Ciconiiformes

Ciconiiformes

Traditionally, the order Ciconiiformes has included a variety of large, long-legged wading birds with large bills: storks, herons, egrets, ibises, spoonbills, and several others. Ciconiiformes are known from the Late Eocene...

Family Ciconiidae

• wood stork (Mycteria americana)

Order Columbiformes

Columbiformes

Columbiformes are an avian order that includes the very widespread and successful doves and pigeons, classified in the family Columbidae, and the extinct Dodo and the Rodrigues Solitaire, long classified as a second family Raphidae. 313 species, found worldwide, comprise the Columbiformes order....

Family Columbidae

• speckled pigeon (Columba guinea)
• Japanese wood pigeon (Columba janthina)
• rock pigeon (Columba livia)
• common wood pigeon (Columba palumbus)
• ruddy ground dove (Columbina talpacoti)
• 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

Coraciiformes

The Coraciiformes are a group of usually colorful near passerine birds including the kingfishers, the Hoopoe, the bee-eaters, the rollers, and the hornbills...

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)

Order Falconiformes

Falconiformes

The order Falconiformes is a group of about 290 species of birds that comprises the diurnal birds of prey. Raptor classification is difficult and the order is treated in several ways.- Classification problems :...

Family Falconidae

Falconidae

The falcons and caracaras are around 60 species of diurnal birds of prey that make up the family Falconidae. The family is divided into two subfamiles, Polyborinae, which includes the caracaras and forest falcons, and Falconinae, the falcons, kestrels and falconets.-Description:Falcons and...

• saker falcon (Falco cherrug)
• lesser kestrel (Falco naumanni)
• American kestrel (Falco sparverius)
• common kestrel (Falco tinnunculus)
• chimango caracara (Milvago chimango)

Order Galliformes

Galliformes

Galliformes are an order of heavy-bodied ground-feeding domestic or game bird, containing turkey, grouse, chicken, New and Old World Quail, ptarmigan, partridge, pheasant, and the Cracidae. Common names are gamefowl or gamebirds, landfowl, gallinaceous birds or galliforms...

Family Numididae

• helmeted guineafowl (Numida meleagris)

Family Odontophoridae

• California quail (Callipepla californica)
• scaled quail (Callipepla squamata)
• bobwhite quail (Colinus virginianus)

Family Phasianidae

Phasianidae

The Phasianidae is a family of birds which consists of the pheasants and partridges, including the junglefowl , Old World Quail, francolins, monals and peafowl. The family is a large one, and is occasionally broken up into two subfamilies, the Phasianinae, and the Perdicinae...

• 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
  Dendragapus obscurus
  The Dusky Grouse is a species of forest-dwelling grouse native to the Rocky Mountains in North America. It is closely related to the Sooty Grouse , and the two were previously considered a single species, the Blue Grouse.-Description:Adults have a long square tail, gray at the end...
  
  

Order Gruiformes

Gruiformes

The Gruiformes are an order containing a considerable number of living and extinct bird families, with a widespread geographical diversity. Gruiform means "crane-like"....

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 Passeriformes

Family Acrocephalidae

Acrocephalidae

Acrocephalidae is a family of oscine passerine birds, in the superfamily Sylvioidea....

• 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

Corvidae

Corvidae is a cosmopolitan family of oscine passerine birds that contains the crows, ravens, rooks, jackdaws, jays, magpies, treepies, choughs and nutcrackers. The common English names used are corvids or the crow family , and there are over 120 species...

• blue jay (Cyanocitta cristata)
• green jay (Cyanocorax yncas)

Family Dicruridae

• fork-tailed drongo (Dicrurus adsimilis)
• crested drongo (Dicrurus forficatus)

Family Emberizidae

Emberizidae

The Emberizidae are a large family of passerine birds. They are seed-eating birds with a distinctively shaped bill.In Europe, most species are called buntings. In North America, most of the species in this family are known as sparrows, but these birds are not closely related to the sparrows, the...

• 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 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

Motacillidae

The Motacillidae are a family of small passerine birds with medium to long tails. There are around 65 species in 6 genera and they include the wagtails, longclaws and pipits. The longclaws are entirely restricted to the Afrotropics, and the wagtails are predominately found in Europe, Africa and...

• 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 (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

• streaked weaver (Ploceus manyar)
• baya weaver (Ploceus philippinus)

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

Sylviidae

Sylviidae is a family of passerine birds that was part of an assemblage known as the Old World warblers. The family was formerly a wastebin taxon with over 400 species of bird in over 70 genera. The family was poorly defined with many characteristics shared with other families...

• 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 Pelecaniformes

Pelecaniformes

The Pelecaniformes is a 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 names as totipalmates or steganopodes...

Family Fregatidae

• magnificent frigatebird (Fregata magnificens)
• great frigatebird (Fregata minor)

Family Threskiornithidae

Threskiornithidae

The family Threskiornithidae includes 34 species of large terrestrial and wading birds, falling into two subfamilies, the ibises and the spoonbills. It was formerly known as Plataleidae. The spoonbills and ibises were once thought to be related to other groups of long-legged wading birds in the...

• African sacred ibis (Threskiornis aethiopicus)
• glossy ibis (Plegadis falcinellus)

Order Piciformes

Piciformes

Nine families of largely arboreal birds make up the order Piciformes, the best-known of them being the Picidae, which includes the woodpeckers and close relatives...

Family Megalaimidae

Megalaimidae

A family of birds comprising the Asian barbets, the Megalaimidae were once united with all other barbets in the Capitonidae but they have turned out to be distinct...

• coppersmith barbet (Megalaima haemacephala)

Family Picidae

Picidae

The woodpeckers, piculets and wrynecks are a family, Picidae, of near-passerine birds. Members of this family are found worldwide, except for Australia and New Zealand, Madagascar, and the extreme polar regions...

• red bellied woodpecker (Melanerpes carolinus)
• red cockaded woodpecker (Picoides borealis)
• 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)
• European scops owl (Otus scops)
• brown owl (Strix aluco)
• spotted owl (Strix occidentalis)