Leucocytozoon (orLeukocytozoon) is agenus of parasiticalveolates belonging to the phylumApicomplexa (which also includes the malaria parasites).
The species of this genus use either blackflies (Simulium species) or abiting midge as their definitive host andbirds 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.
Blood from a chicken infected with a male gametocyte (left) and a female gametocyte (right).
Parasites in the genusLeucocytozoon have a life cycle that involves both a bird host, and ablack fly (with the exception ofLeucocytozoon caulleryi which cycles between a bird host and abiting midge).[1] Parasites enter the bird host in a form called asporozoite 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 calledmerozoites 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 eithererythrocytes,leukocytes,macrophages orendothelial cells. Those infecting the macrophages or endothelial cells develop intomegaloschizonts. The megaloschizonts divide into primarycytomeres, which in turn multiply into smaller cytomeres, which mature into schizonts, which in turn divide into merozoites. In erythrocytes or leukocytes, merozoites develop intogametocytes.
The gametocytes are taken up by a blood-sucking fly as it bites the bird host. Gametocytes then mature in the insectmidgut intomacrogametocytes (female) with red-staining nuclei andmicrogametocytes (male) with pale-staining diffuse nuclei: these fuse to form anookinete. The male gametocytes normally give rise to eightmicrogametes. The ookinete penetrates an intestinal cell of the fly and matures into anoocyst. After several days the oocyst produces ~100 sporozoites that leave and migrate to the salivary glands of the fly.
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 haverhoptries,micronemes and three apical rings. Themitochondrion 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.
It has been suggested that this genus arose after the two others generaPlasmodium andHaemoproteus, the latter originating from the lateOligocene or earlyEocene at about the same time asPiciformes andCoraciiformes.[2]
The genus is divided into two subgenera—Akiba andLeucocytozoon—based on the vector species.
The only known member of the subgenusAkiba isLeucocytozoon (Akiba) caulleryi which uses members of the genusCulicoides as its vectors.
The remaining species in the genus use members of the genusSimulium as their vectors.
In 1977, Greiner and Kocan in an extensive examination of species in the orderFalconiformes declared that the only valid species infecting this order wasL. toddi.[3]
L. dubreuili is considered to be restricted to the familyTurdidae;L. fringillinarum is considered to be restricted to several passiform families; andL. majoris is considered restricted to the familyParidae.[4]
Form gamonts in white blood cells and/or erythrocytes.Gametocytes cause marked enlargement and distortion of the infected cell producing a football-like appearance.
Nomerogony occurs in either leucocytes or erythrocytes.
Merogony occurs in the parenchyma of liver, heart, kidney, or other organs.Meronts may form large bodies divided intocytomeres.
Hemozoin deposits (pigment) are not formed—a useful distinguishing feature forLeucocytozoon fromHaemoproteus andPlasmodium.
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 includesanaemia and enlargement of theliver andspleen. Gross lesions also include pulmonary congestion and pericardial effusion.
Megaloschizonts appear as grey-white nodules found in theheart, 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 ofanorexia,ataxia, weakness, anemia,emaciation and difficulty breathing.
The excess mortality due toLeucocytozoon in adult birds seems to occur as a result of debilitation and increased susceptibility to secondary infection.
L. simondi is suspected to be a major parasite ofCanada geese in some areas, including the upper MidwesternUnited States andCanada.L. smithi affectsturkey 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 andL. anseris are considered to be synonyms ofL. simondi.
L. andrewsi andL. schoutedeni are considered to be synonyms.
L. bonasae,L. jakamowi andL. mansoni are considered to be synonyms ofL. lovati.
L. brimonti is considered to be a synonym ofL. fringillinarum.
L. costai andL. numidae are considered to be synonyms ofL. neavei.
L. francolini,L. kerandeli,L. martini,L. mesnili,L. sabrazesi andL. schuffneri are considered to be synonyms ofL. macleani.
The speciesL. galli is open to some doubt.
L. molpastis is considered to be a synonym ofL. brimonti
L. monardi is considered to be a synonym ofL. gentili
L. toddi seems likely to be a cryptic species complex.
L. turtur and its subspeciesL. turtur orientalis are considered a synonym ofL. marchouxi
Drawing of owl blood cells parasitized byLeukocytozoen danilewskyi by Hans Ziemann in 1898
The first described observation of aLeucocytozoon parasite may have been byVasily Danilewsky, who described certain parasites he observed in the blood of birds as "Leucocytozaire" in 1888 (as they appeared to infectleukocytes).[21] A more detailed description of parasites resemblingLeucocytozoon was published in 1894 by N. Sakharoff from the blood of birds nearTbilisi.[22] Soon thereafter in 1898, Hans Ziemann described aLeucocytozoon parasite from the blood of the owlAthene noctua, naming itLeukocytozoen danilewskyi in honor of Danilewsky.[22] N. M. Berestneff was the first to use the current genus nameLeucocytozoon while describing parasites he calledLeucocytozoon danilewskyi from several common birds.[22] The genus was subsequently formally defined in 1908 byLouis Sambon, and has remained largely unchanged since.[22] In 1930 and 1931,Earl O'Roke andLouis V. Skidmore independently discovered black flies to be the vector ofLeucocytozoon species.[22]
^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 theHaemoproteidae".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 ofLeucocytozoon 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 familyTimaliidae".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 familyBrachypteraciidae (the ground-rollers)".J. Parasitol.90 (6):1468–72.doi:10.1645/ge-227r.PMID15715245.S2CID3260365.
^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 PigeonColumba 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 ofLeucocytozoon 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.
