Leucocytozoon (or Leukocytozoon) is a genus of parasitic alveolates belonging to the phylum Apicomplexa (which also includes the malaria parasites).
The species of this genus use either blackflies (Simulium species) or a biting midge as their definitive host and birds as their intermediate host.[1] There are over 100 species in this genus. Over 100 species of birds have been recorded as hosts to these parasites.
Life cycle
Blood from a chicken infected with a male gametocyte (left) and a female gametocyte (right).
Parasites in the genus Leucocytozoon have a life cycle that involves both a bird host, and a black fly (with the exception of Leucocytozoon caulleryi which cycles between a bird host and a biting midge).[1] Parasites enter the bird host in a form called a sporozoite through the bite of the blood-sucking black fly.[1] The sporozoites invade host cells in the liver where they undergo asexual replication, forming numerous daughter cells called merozoites within 4–5 days.[1] The duration of this stage depends in part upon the species. In some species this stage may occur in the endothelial cells instead of the liver.
The newly released merozoites infect either erythrocytes, leukocytes, macrophages or endothelial cells. Those infecting the macrophages or endothelial cells develop into megaloschizonts. The megaloschizonts divide into primary cytomeres, which in turn multiply into smaller cytomeres, which mature into schizonts, which in turn divide into merozoites. In erythrocytes or leukocytes, merozoites develop into gametocytes.
The gametocytes are taken up by a blood-sucking fly as it bites the bird host. Gametocytes then mature in the insect midgut into macrogametocytes (female) with red-staining nuclei and microgametocytes (male) with pale-staining diffuse nuclei: these fuse to form an ookinete. The male gametocytes normally give rise to eight microgametes. The ookinete penetrates an intestinal cell of the fly and matures into an oocyst. After several days the oocyst produces ~100 sporozoites that leave and migrate to the salivary glands of the fly.
Description
The nuclei of the schizonts is enclosed in a trilaminar membrane with peripherally arranged chromatin. The schizonts also contain numerous cytomers also with trilaminar membranes and containing multiple ribosomes. Repeated invagination of the cytomeres gives rise to the merozoites which also have a trilaminar membrane.
The merozoites have rhoptries, micronemes and three apical rings. The mitochondrion contains vesicular cristae. There may be one or two paranuclear bodies in some species. Their function is unknown.
Two gametocyte forms are recognised: an elongated (sail-like) form and a compact spherical form. These are usually 12–14 micrometres long. The large gametocytes tend to grossly distort the infected cells and make cell identification difficult. A pseudopigment known as volutin may be present.
Evolution
It has been suggested that this genus arose after the two others genera Plasmodium and Haemoproteus, the latter originating from the late Oligocene or early Eocene at about the same time as Piciformes and Coraciiformes.[2]
Taxonomy
The genus is divided into two subgenera—Akiba and Leucocytozoon—based on the vector species.
The only known member of the subgenus Akiba is Leucocytozoon (Akiba) caulleryi which uses members of the genus Culicoides as its vectors.
The remaining species in the genus use members of the genus Simulium as their vectors.
In 1977, Greiner and Kocan in an extensive examination of species in the order Falconiformes declared that the only valid species infecting this order was L. toddi.[3]
L. dubreuili is considered to be restricted to the family Turdidae; L. fringillinarum is considered to be restricted to several passiform families; and L. majoris is considered restricted to the family Paridae.[citation needed]
Form gamonts in white blood cells and/or erythrocytes. Gametocytes cause marked enlargement and distortion of the infected cell producing a football-like appearance.
No merogony occurs in either leucocytes or erythrocytes.
Merogony occurs in the parenchyma of liver, heart, kidney, or other organs. Meronts may form large bodies divided into cytomeres.
Hemozoin deposits (pigment) are not formed—a useful distinguishing feature for Leucocytozoon from Haemoproteus and Plasmodium.
Oocysts develop rapidly in 3–5 days. The oocysts are small and nonexpanding, reaching 13 micrometres in diameter and typically have less than 100 short, thick sporozoites.
The typical pathology of infection with these parasites includes anaemia and enlargement of the liver and spleen. Gross lesions also include pulmonary congestion and pericardial effusion.
Megaloschizonts appear as grey-white nodules found in the heart, liver, lung or spleen. Microscopically there is ischemic necrosis and associated inflammation in the heart, brain, spleen and liver due to occlusion of blood vessels by megaloschizonts in endothelial cells. Ruptured schizonts may induce granulomatous reactions in the surrounding tissues.
Clinically the majority of birds affected with leucocytozoonosis exhibit no signs. Among those that do the signs include mild to severe signs of anorexia, ataxia, weakness, anemia, emaciation and difficulty breathing.
The excess mortality due to Leucocytozoon in adult birds seems to occur as a result of debilitation and increased susceptibility to secondary infection.
Epidemiology
L. simondi is suspected to be a major parasite of Canada geese in some areas, including the upper Midwestern United States and Canada. L. smithi affects turkey farms in the southeastern United States.
Like many protist species and genera this genus is subject to ongoing revision especially in the light of DNA based taxonomy. Described species may be subject to revision.
L. anatis and L. anseris are considered to be synonyms of L. simondi.
L. andrewsi and L. schoutedeni are considered to be synonyms.
L. bonasae, L. jakamowi and L. mansoni are considered to be synonyms of L. lovati.
L. brimonti is considered to be a synonym of L. fringillinarum.
L. costai and L. numidae are considered to be synonyms of L. neavei.
L. francolini, L. kerandeli, L. martini, L. mesnili, L. sabrazesi and L. schuffneri are considered to be synonyms of L. macleani.
The species L. galli is open to some doubt.
L. molpastis is considered to be a synonym of L. brimonti
L. monardi is considered to be a synonym of L. gentili
L. toddi seems likely to be a cryptic species complex.
L. turtur and its subspecies L. turtur orientalis are considered a synonym of L. marchouxi
History
Drawing of owl blood cells parasitized by Leukocytozoen danilewskyi by Hans Ziemann in 1898
The first described observation of a Leucocytozoon parasite may have been by Vasily Danilewsky, who described certain parasites he observed in the blood of birds as "Leucocytozaire" in 1888 (as they appeared to infect leukocytes).[20] A more detailed description of parasites resembling Leucocytozoon was published in 1894 by N. Sakharoff from the blood of birds near Tbilisi.[21] Soon thereafter in 1898, Hans Ziemann described a Leucocytozoon parasite from the blood of the owl Athene noctua, naming it Leukocytozoen danilewskyi in honor of Danilewsky.[21] N. M. Berestneff was the first to use the current genus name Leucocytozoon while describing parasites he called Leucocytozoon danilewskyi from several common birds.[21] The genus was subsequently formally defined in 1908 by Louis Sambon, and has remained largely unchanged since.[21] In 1930 and 1931, Earl O'Roke and Louis V. Skidmore independently discovered black flies to be the vector of Leucocytozoon species.[21]
References
^ abcdValkiunas G (2004). "Life Cycle and Morphology of Leucocytozoidae Species". Avian Malaria Parasites and Other Haemosporidia (1 ed.). CRC Press. pp. 36–45. doi:10.1201/9780203643792. ISBN978-0-415-30097-1.
^Bennett, GF (1993). "Phylogenetic distribution and possible evolution of the avian species of the Haemoproteidae". Syst. Parasitol. 26 (1): 39–44. doi:10.1007/bf00009646. S2CID35811974.
^Greiner EC, Kocan AA (1977). "Leucocytozoon (Haemosporida; Leucocytozoidae) of the falconiformes". Can. J. Zool. 55 (5): 761–70. doi:10.1139/z77-099. PMID406030.
^Evans, M; Otter, A (18 July 1998). "Fatal combined infection with Haemoproteus noctuae and Leucocytozoon ziemanni in juvenile snowy owls (Nyctea scandiaca)". The Veterinary Record. 143 (3): 72–6. doi:10.1136/vr.143.3.72. PMID9717222. S2CID23546240.
^Atchley, F.O. (1951). "Leucocytozoon andrewsi n. sp., from chickens observed in a survey of blood parasites in domestic animals in South Carolina". J. Parasitol. 37 (5): 483–8. doi:10.2307/3273257. JSTOR3273257.
^Peirce, M.A.; Adlard, R.D.; Lederer, R. (2005). "A new species of Leucocytozoon Berestneff, 1904 (Apicomplexa: Leucocytozoidae) from the avian family Artamidae". Syst. Parasitol. 60 (2): 151–4. doi:10.1007/s11230-004-1387-4. PMID15841351. S2CID1135988.
^Savage, A.F.; Ariey, F.; Greiner, E.C. (2006). "Leucocytozoon atkinsoni n. sp. (Apicomplexa: Leucocytozoidae) from the avian family Timaliidae". Syst. Parasitol. 64 (2): 105–9. doi:10.1007/s11230-005-9023-5. PMID16612655. S2CID11870669.
^Savage, A.F.; Greiner, E.C. (2004). "Hematozoa of the avian family Brachypteraciidae (the ground-rollers)". J. Parasitol. 90 (6): 1468–72. doi:10.1645/ge-227r. PMID15715245. S2CID3260365.
^ abSavage, A.F. (2004). "Hematozoa of the avian family Philepittidae (the asities and sunbird asities)". J. Parasitol. 90 (6): 1473–4. doi:10.1645/ge-228r. PMID15715246. S2CID24081599.
^Bennett, G.F.; Khan, R.A.; Campbell, A.G. (1974). "Leucocytozoon grusi sp. n. (Sporozoa: Leucocytozoidae) from a sandhill crane, Grus canadensis (L.)". J. Parasitol. 60 (2): 359–363. doi:10.2307/3278486. JSTOR3278486. PMID4206882.
^Valkiünas, G.; Iezhova, T.A.; Mironov, S.V. (2002). "Leucocytozoon hamiltoni n. sp. (Haemosporida, Leucocytozoidae) from the Bukharan great tit Parus bokharensis". J. Parasitol. 88 (3): 577–581. doi:10.2307/3285453. JSTOR3285453. PMID12099430.
^Greiner, E.C. (1976). "Leucocytozoon maccluri sp. n. (Haemosphorida: Leucocytozoidae) from a Thailand thrush, Zoothera marginata Blyth". J. Parasitol. 62 (4): 545–7. doi:10.2307/3279409. JSTOR3279409. PMID822146.
^Bunbury, N.; Barton, E.; Jones, C.G.; Greenwood, A.G.; Tyler, K.M.; Bell, D.J. (2007). "Avian blood parasites in an endangered columbid: Leucocytozoon marchouxi in the Mauritian Pink Pigeon Columba mayeri". Parasitology. 134 (6): 797–804. CiteSeerX10.1.1.391.9645. doi:10.1017/s0031182006002149. PMID17201998. S2CID8703315.
^ abJones, H.I.; Sehgal, R.N.; Smith, T.B. (2005). "Leucocytozoon (Apicomplexa: Leucocytozoidae) from West African birds, with descriptions of two species". J. Parasitol. 91 (2): 397–401. doi:10.1645/ge-3409. PMID15986615. S2CID7661872.
^Sato Y, Tamada A, Mochizuki Y, Nakamura S, Okano E, Yoshida C, Ejiri H, Omori S, Yukawa M, Murata K (2009). "Molecular detection of Leucocytozoon lovati from probable vectors, black flies (Simuliudae) collected in the alpine regions of Japan". Parasitol. Res. 104 (2): 251–5. doi:10.1007/s00436-008-1183-1. PMID18791737. S2CID10885934.
