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Haemoproteus

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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.

Haemoproteus
H. syrnii
Scientific classification Edit this classification
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Alveolata
Phylum: Apicomplexa
Class: Aconoidasida
Order: Chromatorida
Family: Haemoproteidae
Genus: Haemoproteus
Kruse, 1890
Species

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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

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Evolution

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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.[1]

Taxonomic history

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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.[2]

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.[3]

Subgenera

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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: 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.

Parahaemoproteus: Parasites of birds other than the Columbiformes. Vectors are biting midges (Ceratopogonidae). Exflagellation occurs below 20 °C (68 °F). 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.[4]

Species list

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Select 'show' (at right) to expand list

Life cycle

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ilanpapernai

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

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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

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Pigment granules are refractile and yellow to brown in colour.

Pathology

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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 (Colinus virginianus) may become infected with 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 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

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H. columbae infects rock pigeons (Columba livia) and is vectored by a hippoboscid fly (Pseudolynchia canariensis).[7] Both sexes of the vector can transmit the parasite. Species of the Hippoboscoidea, the superfamily to which Ps. canariensis, belongs do not lay 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 are infected with the parasite. In contrast, no effect is seen on male fly survival. In addition, the females produce fewer offspring when infected but the quality of the offspring does not seem to be affected.

Host records

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Avian hosts

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Reptile hosts

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Amphibian hosts

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Hosts known to be infected but Haemoproteus species not identified

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Vectors

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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

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 Cathartidae

Order Anseriformes

Family Anatidae

Order Charadriiformes

Family Laridae

Order Ciconiiformes

Family Ciconiidae

Order Columbiformes

Family Columbidae

Order Coraciiformes

Family Alcedinidae

Family Brachypteraciidae

Family Bucerotidae

Family Meropidae

Order Falconiformes

Family Falconidae

Order Galliformes

Family Numididae

Family Odontophoridae

Family Phasianidae

Family Tetraonidae

Order Gruiformes

Family Gruidae

Family Otidae

Order Passeriformes

Family Acrocephalidae

Family Corvidae

Family Dicruridae

Family Emberizidae

Family Estrildidae

Family Fringillidae

Family Hirundinidae

Family Icteridae

Family Laniidae

Family Meliphagidae

Family Mimidae

Family Motacillidae

Family Muscicapidae

Family Nectariniidae

Family Oriolidae

Family Paridae

Family Paradisaeidae

Family Parulidae

Family Passeridae

Family Ploceidae

Family Pycnonotidae

Family Sturnidae

Family Sylviidae

Family Thraupidae

Family Timaliidae

Family Turdidae

Family Vangidae

Family Zosteropidae

Order Pelecaniformes

Family Fregatidae

Family Threskiornithidae

Order Piciformes

Family Megalaimidae

Family Picidae

Order Phoenicopteriformes

Family Phoenicopteridae

Order Psittaciformes

Family Cacatuidae

Family Psittacidae

Order Strigiformes

Family Strigidae

Notes

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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

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  1. ^ Poinar G, Telford SR (2005). "Paleohaemoproteus burmacis gen. n., sp. n. (Haemospororida: Plasmodiidae) from an Early Cretaceous biting midge (Diptera: Ceratopogonidae)". Parasitology. 131 (1). Cambridge University Press (CUP): 79–84. doi:10.1017/S0031182005007298. PMID 16038399. S2CID 23877176.
  2. ^ Telford, SR (1996). "Two new species of Haemocystidium Castellani & Willey (Apicomplexa: Plasmodiidae) from Pakistani lizards, and the support their meronts provide for the validity of the genus". Systematic Parasitology. 34 (3): 197–214. doi:10.1007/bf00009387. S2CID 2801447.
  3. ^ Clark, Nicholas; Clegg, Sonya; Lima, Marcos (2014). "A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data". International Journal for Parasitology. 44 (5): 329–338. doi:10.1016/j.ijpara.2014.01.004. hdl:10072/61114. PMID 24556563.
  4. ^ Levin, II; Valkiūnas, G; Santiago-Alarcon, D; Cruz, LL; Iezhova, TA; O'Brien, SL; Hailer, F; Dearborn, D; Schreiber, EA; Fleischer, RC; Ricklefs, RE; Parker, PG (2015). "Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa". International Journal for Parasitology. 41 (10): 1019–27. doi:10.1016/j.ijpara.2011.03.014. PMID 21683082.
  5. ^ Markus, MB; Oosthuizen, JH (1972). "Pathogenicity of Haemoproteus columbae". Transactions of the Royal Society of Tropical Medicine and Hygiene. 66 (1): 186–187. doi:10.1016/0035-9203(72)90072-7. PMID 4625895.
  6. ^ Clark, Nicholas; Adlard, Robert; Clegg, Sonya (2014). "First evidence of avian malaria in Capricorn Silvereyes (Zosterops lateralis chlorocephalus) on Heron Island". The Sunbird. 44: 1–11.
  7. ^ Waite, JL; Henry, AR; Adler, FR; Clayton, DH (2012). "Sex-specific effects of an avian malaria parasite on an insect vector: support for the resource limitation hypothesis". Ecology. 93 (11): 2448–55. Bibcode:2012Ecol...93.2448W. doi:10.1890/11-2229.1. PMID 23236915.
  8. ^ Iezhova TA, Valkiūnas G, Loiseau C, Smith TB, Sehgal RN (2010). "Haemoproteus cyanomitrae sp. nov. (Haemosporida: Haemoproteidae) from a widespread African songbird, the olive sunbird, Cyanomitra olivacea". Journal of Parasitology. 96 (1): 137–143. doi:10.1645/GE-2198.1. PMID 19691417. S2CID 3183752.
  9. ^ a b Elahi, Rubayet; Islam, Ausraful; Hossain, Mohammad Sharif; Mohiuddin, Khaja; Mikolon, Andrea; Paul, Suman Kumer; Hosseini, Parviez Rana; Daszak, Peter & Alam, Mohammad Shafiul (2014). "Prevalence and Diversity of Avian Haematozoan Parasites in Wetlands of Bangladesh". Journal of Parasitology Research. 2014: 1–12. doi:10.1155/2014/493754. PMC 3918735. PMID 24587896.
  10. ^ Karadjian, G.; Martinsen, E.; Duval, L.; Chavatte, J.-M.; Landau, I. (2014). "Haemoproteus ilanpapernai n. sp. (Apicomplexa, Haemoproteidae) in Strix seloputo from Singapore: morphological description and reassignment of molecular data". Parasite. 21: 17. doi:10.1051/parasite/2014018. PMC 3996868. PMID 24759652.
  11. ^ a b Valkiūnas, Gediminas (2005). Avian Malaria Parasites and Other Haemosporidia (English ed.). Boca Raton, Fla, US: CRC Press. pp. x+932+III Plates. doi:10.1201/9780203643792. ISBN 978-0-415-30097-1. LCCN 2004050268. OCLC 55066316. S2CID 83186449. ISBN 978-0-203-64379-2. OCLC 70294116.
  12. ^ Križanauskiene A, Pérez-Tris J, Palinauskas V, Hellgren O, Bensch S, Valkiūnas G (2010). "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. 137 (2): 217–27. doi:10.1017/S0031182009991235. PMID 19765350. S2CID 34115999.
  13. ^ Karadjian, G.; Puech, M.-P.; Duval, L.; Chavatte, J.-M.; Snounou, G.; Landau, I. (2013). "Haemoproteus syrnii in Strix aluco from France: morphology, stages of sporogony in a hippoboscid fly, molecular characterization and discussion on the identification of Haemoproteus species". Parasite. 20: 32. doi:10.1051/parasite/2013031. PMC 3771403. PMID 24029169.
  14. ^ Merino, Santiago; Hennicke, Janos; Martínez, Javier; Ludynia, Katrin; Torres, Roxana; Work, Thierry M.; Stroud, Stedson; Masello, Juan F.; Quillfeldt, Petra (2012). "Infection by Haemoproteus parasites in four species of frigatebirds and the description of a new species of Haemoproteus (Haemosporida: Haemoproteidae)" (PDF). Journal of Parasitology. 98 (2): 388–97. doi:10.1645/GE-2415.1. PMID 21992108. S2CID 3846342. Archived from the original (PDF) on 2016-12-10. Retrieved 2015-05-14.
  15. ^ a b Cordon, G.; Hitos Prados, A.; Romero, D.; Sánchez Moreno, M.; Pontes, A.; Osuna, A.; Rosales, M.J.; et al. (2009). "Intestinal and haematic parasitism in the birds of the Almunecar (Granada, Spain) ornithological garden". Veterinary Parasitology. 165 (3–4): 361–6. doi:10.1016/j.vetpar.2009.07.027. PMID 19682800.
  16. ^ Harl, Josef; Fauchois, Anaïs; Puech, Marie-Pierre; Gey, Delphine; Ariey, Frédéric; Izac, Brigitte; Weissenböck, Herbert; Chakarov, Nayden; Iezhova, Tatjana; Valkiūnas, Gediminas; Duval, Linda (2024). "Novel phylogenetic clade of avian Haemoproteus parasites (Haemosporida, Haemoproteidae) from Accipitridae raptors, with description of a new Haemoproteus species". Parasite. 31: 5. doi:10.1051/parasite/2023066. ISSN 1776-1042. PMC 10854483. PMID 38334685.  
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