Plate 14 a-e (p. 73) and Fig. 2 (p. 90)
Species affected
In various freshwater and marine fish; in Africa: in Cichlidae, Clarias spp., Bagrus spp.,
Synodontidae, Mormyridae, Mugilidae and Protopterus aethiopicus.
Geographic range
Trypanosomes have been reported in all major water systems of Africa (Wenyon, 1908;
Hoare, 1932; Dias, 1952; Baker, 1960, 1961), with some species apparently distributed
as widely as their hosts (cf. Clarias gariepinus). Trypanosomes occur in C. lazera, in the
Near East, but not in cichlids or cyprinids. Trypanosomes have also been reported from
introduced Oreochromis mossambicus in India (Mandal, 1977). Trypanosomes (T. cf.
mugicola Becker & Overstreet, 1979) are widespread in grey mullet (Mugilidae) of the
lagoons and rivers of southern Africa. There are no reports of vascular Cryptobia from
Africa.
Description, taxonomy and diagnosis
Piscine haemoflagellates swim freely in the blood. Members of the genus Trypanosoma
are spindle shaped, 25–95 μm long, a single flagellum originating from a usually apical
kinetoplast is connected longitudinally to the trypanosome body by an undulating
membrane. The nucleus is usually single, except in the course of division and centrally
positioned.
Cryptobia, also previously called Trypanoplasma, are reminiscent of trypanosomes in shape, but have two flagellae connected to a single kinetoplast, one free and one tied longitudinally by an undulating membrane. Although the two are seemingly related in morphology and in means of transmission via leeches, there are sufficient biological differences to separate the two. Cryptobia, unlike trypanosomes, are not exclusively vascular parasites and (even sometimes the same species) also occur as ectoparasites on the fish body surface and in the digestive tract. Transmission may also be direct or by predation (Woo, 1987).
Infections in the blood are readily detected either by direct microscopic observation of fresh blood or more easily from plasma from the surface of the packed erythrocyte layer of blood, centrifuged in a heparinized haematocrit capillary. Smears prepared from whole blood or centrifuged material, after being air dried and immersed in absolute methanol, are stained in diluted Giemsa (1/10 in pH 7.0–7.4 phosphate buffer).
Morphology and morphometrics are considered insufficient for specific determination of trypanosomes, and comparison of the isoenzymes of in-vitro cultured isolates is currently the established taxonomic methodology. This methodology is already applied to differentiate amphibian trypanosomes but thus far not to those of fish species.
Life history and biology
Trypanosome binary division is rarely observed in the blood. At the present state of
knowledge it will be difficult to establish if pleomorphism, e.g. small and large forms
reported in non-African species (Khan, 1976) occurs in infections of African fish. It was
not evident in grey mullet infections.
In the leech, ingested trypanosomes in the crop undergo several successive divisions, yielding morphologically diverse generations; amastigotes, sphaeromastigotes, and epimastigotes, which migrate to the proboscis and transform into metatrypanosomes - the infective stage, which will enter fish blood during feeding (Khan, 1976).
Sphaeromastigotes and epimastigotes were revealed attached to the crop epithelial lining of an estuarine piscicolid leech (a new, yet to be described species, by Oosthuizen, J.H., University of Pretoria, R.S.A) removed from the mouth of a trypanosome-infected grey mullet (Mugil cephalus; see also Chapter 17.), from Swartkop estuary, Cape region, South Africa.
Epimastigotes (Critidia) were also found in Batrachobdelloides tricarinata, removed from Protopterus aethiopicus and Barbus altianalis from Lake Victoria, where trypanosomes (T. mukasai) are common. Cichlids and Bagrus bayad are additional hosts. (Baker, 1960, 1961). This leech, as well as trypanosomes, frequently infect Clarias gariepinus in Israel.
The development of Cryptobia in the leech does not resemble the sequential development of trypanosomes. Cryptobia ingested with blood becomes rounded and following binary fission apparently yields infective forms which migrate (within 72 hours, compared with weeks in trypanosomes) to the proboscis. Reciprocal transformation of vascular stages into ectoparasitic forms also allows direct transmission between fish hosts (Woo, 1987).
Pathology and epizootiology
Natural infection with trypanosomes may be very common, particularly where the leech
vector is also common (see Chapter 17.). In Lake Victoria, 54% of Oreochromis variabilis
and 50% of O. esculenta were infected, and 20% of Oreochromis niloticus in Lake
George (Baker, 1960, 1961). Infection in catfish (Clarias gariepinus and Bagrus spp.)
also seems to be very high (in all four Bagrus docmac examined in L. Victoria) but
quantitative data are lacking. Prevalence of infection, in Cape riverine and estuarine
mullets, is about 50%, but heavy infections are rarer (about 15%). In none of the
instances of natural infection was there any evidence of adverse effects on the host.
Decrease in haematocrit and haemoglobin levels and evidence of accelerated
haemopoiesis have been reported in some infections (by T. murmanensis, Khan, 1977).
In experimental infections of carp fingerlings with T. danilewskyi, where levels of
parasitaemia reached 105 per mm3, some fish develop ascites, others become
oedematous; infiltrative and proliferative changes occur in the renal tissue, the pancreas
and in various connective tissues (Lom, Dykova & Machackova, 1986). Anaemia and
anorexia were reported in goldfish with high levels of parasitaemia, with the same
trypanosome (Nazrul Islam & Woo, 1991, 1991a). The vector leech of T. danilewskyi
(Piscicola geometra) is a cold water species (Lom, 1979), unlikely to be introduced into
warm water carp rearing systems.
Infections with vascular Cryptobia are far more pathogenic, causing anaemia, splenomegalia, exophthalmia and ascites; anorexia has also been reported. Juvenile fish, salmonids and carp, are particularly susceptible, but all cases are in coldwater culture systems (Lom et al., 1986; Woo, 1987).
Control
At present the only practical means which may be recommended is environmental
control by elimination of leeches (see Chapter 17.).
Species affected
Freshwater and marine fish. In Africa, Dactylosoma has been found in cichlids (species
of Oreochromis, Astatorheochromis and Haplochromis) and grey mullets (Mugilidae -Mugil cephalus,
Liza dummerelli and L. richardsoni). The latter two species of grey
mullets are thus far the only known African hosts for Hemogregarina.
Geographic range
Data on piscine hemogregarines and dactylosomes in Africa are scanty. Dactylosomes
in cichlids (D. mariae - Hoare, 1930; Baker, 1960) were thus far only found in Lakes
Victoria and George, with a single record from O. mossambicus in Transvaal, South
Africa, while Dactylosoma hannesi and hemogregarines were only found in grey mullets
from Southern Cape rivers (South Africa).
Description, taxonomy
Parasites of the circulating erythrocytes -- Dactylosoma [syn.: Babesiosoma,
Haemohormidium] or of both circulating erythrocytes and of the reticulo-endothelial
tissues - Haemogregarina [and Cyrilia in South America]. Only asexually dividing and
resting stages (merogony stages and gametocytes) occur in the piscine host, while the
gamogonous process takes place in the invertebrate (vector) host, which is a leech.
Infected cells are detected from blood smears and tissue imprints (touch preparations),
air dried, absolute methanol fixed and Giemsa stained (same as for Haemoflagellates).
Waiting comma-shaped gametocystes of Dactylosoma are readily confused with young
stages of hemogregarines. Fully grown hemogregarine meronts and gametocytes
occupy the entire long axis of the erythrocyte, and division is longitudinal. Piscine
dactylosomes divide either into 4, in cross-like, or into 8 in octagonal, formation.
Dactylosomes are related to hemogregarines, and both show affinities with mammalian piroplasms (Bartha & Desser, 1989). Dactylosomids with only quadruple division were regarded as a separate genus Babesiosoma (Jakowska & Nigrelli, 1956) while those dividing to 8 were named Haemohormidium (Khan, 1980), but it appears that the same species had alternating generations forming 4 and 8 progeny (Paperna, 1981).
Life history and biology
The definitive host and vector of both dactylosomes and hemogregarines are leeches
(Lainson, 1984; Bartha & Desser, 1989; Siddal & Desser, 1992). Infection is transmitted
to and from the leech during blood sucking. Ingested macrogametocytes, while
becoming associated with a microgametocyte (syzygy process), penetrate the surface
of the gut epithelial cell. Development of piscine dactylosomes in the leech is unknown.
In the frog species, Dactylosoma stadleri, gametocytes are isogamous and only one
microgamete is formed. The zygote penetrates the epithelial cell where it divides into 8
sporozoites. Sporozoites migrate into the salivary cells, where following a division into
four (a merogony), infective stages are formed (Bartha & Desser, 1989). In piscine
hemogregarines (H. myxocephali and Cyrilia gomesi) four a-flagellate microgametes are
formed of which one fertilises the macrogametocyte. In piscine hemogregarines, the
zygote undergoes multiple divisions producing 16–32 sporozoites (Lainson, 1984; Siddal
& Desser, 1992). Released sporozoites reinfect the epithelial cells to undergo a
subsequent division (merogony). Offspring of this division migrate into the salivary cells
connected to the proboscis (Siddal & Desser, 1993).
In the fish host, merogonous division of dactylosomes occurs only in erythrocytes. Piscine hemogregarines divide in the erythrocytes, while some (such as H. simondi in Solea solea, Kirmse, 1979) will also have a pre-erythrocytic merogony in circulating and tissue leucocytes (macrophages). Furthermore, large cyst-like bodies, containing numerous hemogregarine merozoites, were reported in the visceral organs and muscles of several, thus far only marine, fish (Furguson & Roberts, 1975; Paperna, 1979; Paperna & Sabnai, 1982). It is not known if these resting stages are transmissible through predation.
Pathology and epizootiology
The only pathologically significant infections are the leucocytic hemogregarines which
induce proliferative lesions, thus far reported only from cultured marine fish. Lesions may
be comprised either entirely of encapsulated aggregates of merozoites (Paperna, 1979)
or of infected macrophages embedded in granulomatous tissue (Furguson and Roberts,
1975).
Incidence of infection by D. mariae in L. Victoria, in O. esculenta is 46% and in O. variabilis 70%. D. hannesi infection in grey mullets of the Cape coastal rivers is sporadic, only occurring in one fish species (M. cephalus) where the level of parasitaemia reached 3.2% and revealed dividing stages. In the remaining fish, parasitaemia was below 0.06%, and infection was comprised predominantly of non-dividing stages. Infection by hemogregarines in the same fish was rare.
Control
Not studied.
REFERENCES
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Baker, J. R., 1961. Trypanosomes of African freshwater fish: an addendum. Parasitol., 51: 263.
Bartha, J.R. & Desser, S.S., 1989. Development of Babesiosoma stableri (Dactylosomatidae; Adeleida; Apicomplexa) in its leech vector (Batrachobdella picta) and the relationship of the dactylosomatids to the piroplasms of higher vertebrates. J. Protozool., 36: 241–253.
Becker, C.D. & Overstreet, R.M., 1979. Hematozoa of marine fishes from the northern Gulf of Mexico. J. Fish. Dis., 2: 469–479.
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Furguson, H.W. & Roberts, R.J., 1975. Myeloid leucosis associated with sporozoan infection in cultured turbot (Scophthalmus maximus L.). J. Comp. Path., 85: 317–236.
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Khan, R. A., 1977. Blood changes in Atlantic Cod (Gadus morhua) infected with Trypanosoma murmanensis. J. Fish. Res. Board Canada, 34: 2193–2196.
Khan, R.A., 1980. The leech as a vector of a fish piroplasm. Can. J. Zool., 58: 1631–1637.
Kirmse, P., 1979. Redescription of the life cycle of Haemogregarina simondi (Laveran and Mesnil, 1901) in its vertebrate host the marine fish Solea solea (Linnaeus). Z. Parasitenk., 59: 141–150.
Lainson, R., 1984. On Cirilia gomesi (Neiva & Pinto, 1926) gen. nov. (Haemogregarinidae) and Trypanosoma bourouli Neiva & Pinto, in the fish Synbranchus marmoratus: simultaneous transmission by the leech Haementeria lutzi. In: Canning, E.U. (ed.) Parasitological Topics, Special Publication No. 1. Society of Protozoologists pp. 150–158.
Lom, J., 1979. Biology of fish trypanosomes and trypanoplasms. In: Biology of Kinetoplastida Vol. II, Lumsden, W.H.R. & Evans, D.A. (ed.) Academic Press, New York pp. 269–377.
Lom, J., Dykova, I. & Machackova, B., 1986. Experimental evidence of pathogenicity of Trypanoplasma boreli and Trypanosoma danilewskyi for carp fingerlings. Bull. Eur. Ass. Fish Pathol., 6: 87–88.
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ILLUSTRATIONS
Fig. 2. Haemosporida, Myxosporea and Microsporea: A. Dactylosoma hannesi from Mugil cephalus, Kowie lagoon southeastern Cape, South Africa. B. Myxobolus sp. from gills and dermal cysts in cichlids of Lake Victoria. C. Myxobolus from viscera of cichlids in Southern Africa, and the East African lakes. D. Myxobolus from gills of Labeo spp. from Ruaha river, Tanzania. E. Myxobolus sp. from gills of Labeo senegalensis, Volta lake. F. Myxobolus equatorialis Landsberg, 1985, from tilapia hybrids, Israel. G. Myxobolus amieti, Fomena et al., 1984/1985, from Ctenopoma nanum, Cameroon. H. Henneguya from gills of Lates albertianus, L. Albert (x). I. Henneguya from gills of Citharinus citharus, Volta lake, Ghana. Continued overleaf.
Fig. 2 legend continued from previous page J. Henneguya laterocapsulata Landsberg, 1986, from skin of Clarias lazera, Israel. K. Myxidium heterofilamentatus, Landsberg, 1986, gall bladder of Clarias lazera Israel. Sphaerospora inequalis Landsberg, 1986, kidneys of Clarias lazera, Israel. M. Microspora xenoma in muscles. N. Ultrastructural image of a Microspora spore (After Nosematoides tilapiae, Sakiti & Bouix, 1987; size: 3 × 2 μm). en, endospore; ex, exospore; f, filament; n, nucleus; p, polar cap; pb, polaroblast; s, sporoplasm; v, posterior vacuole.
