Haemoproteus is a genus of alveolates that are parasitic in birds, reptiles, and amphibians. Its name is derived from Greek: haima 'blood' and Proteus, a sea god that had the power to assume various shapes. The name Haemoproteus was first used in the description of H. columbae in the blood of the pigeon Columba livia by Walther 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 mosquitoes, biting midges (Culicoides), louse flies (Hippoboscidae) and horse-flies ("tabanids", "tabanid flies"). Infection with this genus is sometimes known as pseudomalaria because of the parasites' similarities with Plasmodium 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), waterfowl (Anseriformes), raptors (Accipitriformes, Falconiformes, Strigiformes), pigeons and doves (Columbiformes), and perching birds or songbirds (Passeriformes).
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 trapped 100 million years ago in amber found in Myanmar.
Taxonomic history The first description of this genus was in 1890 by Kruse, who described H. 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. 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 was the vector of H. columbae. Aragao in 1908 demonstrated the schizogonic stages of H. columbae in the endothelial cells of the lungs 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 mosquitoes.
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 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. 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. 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 chelonians. 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, 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.
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 (Hippoboscidae). 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. Although the majority are parasites of the Columbiformes, some species from this subgenus have also been reported in the Charadriiformes, Pelecaniformes and Suliformes.
: Parasites of birds other than the Columbiformes. Vectors are biting midges (Ceratopogonidae). 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 frigatebirds.
Species list
Haemoproteus aegnithidae Haemoproteus aegyptius Haemoproteus africanus Haemoproteus alaudae Haemoproteus anatolicum Haemoproteus anthi Haemoproteus antigonis Haemoproteus asturisdussumieri Haemoproteus attenatus Haemoproteus balearicae Haemoproteus balli Haemoproteus balmorali Haemoproteus bambusicolae Haemoproteus bennetti Haemoproteus brachiatus Haemoproteus beckeri Haemoproteus belopolskyi Haemoproteus bennetti Haemoproteus borgesi Haemoproteus brodkorbi Haemoproteus bubalornis Haemoproteus bucerotis Haemoproteus canachites Haemoproteus caprimulgi Haemoproteus catharti Haemoproteus catenatus Haemoproteus cellii Haemoproteus centropi Haemoproteus chelodina Haemoproteus coatneyi Haemoproteus columbae Haemoproteus concavocentralis Haemoproteus cornuata Haemoproteus crumenius Haemoproteus cyanomitrae Haemoproteus danilewskyi Haemoproteus desseri Haemoproteus dicaeus Haemoproteus dicruri Haemoproteus dolniki Haemoproteus edomensis Haemoproteus elani Haemoproteus enucleator Haemoproteus forresteri Haemoproteus fringillae Haemoproteus fusca Haemoproteus gabaldoni Haemoproteus garnhami Haemoproteus geochelonis Haemoproteus greineri
Haemoproteus goodmani Haemoproteus halcyonis Haemoproteus handai Haemoproteus hirundinis Haemoproteus himalayanus Haemoproteus homobelopolskyi Haemoproteus homopalloris Haemoproteus homovelans Haemoproteus hudaidensis Haemoproteus iwa Haemoproteus janovyi Haemoproteus jenniae Haemoproteus khani Haemoproteus kopki Haemoproteus krylovi Haemoproteus lanii Haemoproteus lari Haemoproteus lophortyx Haemoproteus kopki Haemoproteus maccallumi Haemoproteus mackerrasi Haemoproteus macrovacuolatus Haemoproteus madagascariensis Haemoproteus majoris Haemoproteus mansoni Haemoproteus mathislegeri Haemoproteus melopeliae Haemoproteus meleagridis Haemoproteus meropis Haemoproteus mesnili Haemoproteus metchnikovi Haemoproteus micronuclearis Haemoproteus minutus Haemoproteus motacillae Haemoproteus multipigmentatus Haemoproteus multivolutinus Haemoproteus nebraskensis Haemoproteus nettionis Haemoproteus nisi Haemoproteus noctuae Haemoproteus nucleofascialis Haemoproteus nucleophilus Haemoproteus oedurae Haemoproteus orioli Haemoproteus oryzivora Haemoproteus ovalis Haemoproteus pallidus Haemoproteus pallidulus Haemoproteus palumbis Haemoproteus pasteris
Haemoproteus pastoris Haemoproteus parabelopolskyi 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
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.
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
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 H. columbae may develop enlarged gizzards; and anemia has been recorded.