© 2000, Annual Reports of the Zoological Institute RAS.


Specificity of coccidia of fishes (Sporozoa, Coccidiida)

Larissa M. Belova, Mstislav V. Krylov

Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, St. Petersburg, 199034, Russia

For the first time coccidia in fishes were found and described 110 years ago (Thelohan, 1890). During that period a number of reviews on regional and world fauna of coccidia of fishes were published (Labbe, 1896; Stankovitch, 1921). The largest reports on world fauna of coccidia were published by Pellerdy (1974) and Dykova and Lom (1983). Pellerdy (1974) in the monograph "Coccidia and Coccidiosis" gives the names of 66 species of coccidia in infected fishes. Dykova and Lom (1983) de-scribed as many as 127 species of coccidia in fishes.

Within the last 10-15 years the study of fauna of coccidia of fishes was carried out rather intensively and by the end of the twentieth century the number of coccidia species found in fishes approached 250. Vast data on systematics of coccidia parasitizing fishes (Lom & Dykova, 1992; Ellis et al., 1998) and fish fauna have been accumulated (Eschmeyer, 1990). Therefore, an analysis of the modern data is of certain practical and theoretical interest.

Distribution of families and genera of Coccidia by class of fishes

The first that arrests attention in the distribution of families and gen-era of coccidia in the higher taxa of fishes is that coccidia have not been described in representatives of the class Holocephali, and class Sarcop-terygii, and that the fauna of coccidia in fishes of the class Elasmobranchii is much poorer, than in representatives of the class Actinopterygii.

Coccidia belonging to only one family Eimeriidae and two genera Eimeria and Goussia were found in Elasmobranchii, whereas coccidia of three families (Calyptosporidae, Cryptosporidiidae, Eimeriidae) and eight genera (Calyptospora, Cryptosporidium, Crystallospora, Eimeria, Epieimeria, Goussia, Isospora, Octosporella) were found in Actinopterygii. How can we explain this situation? It is obvious, that now it is not possible to answer a number of questions. However if we assume, that the study of fauna of coccidia of different groups of fishes proceeded with more or less similar intensity, it appears that the available material illustrates the law, well known in parasitology: parasitic organisms thrive when their hosts thrive. That is why in Actinopterygii, one of the most highly organized groups of fishes rich in species and forms, the richest parasitic fauna belonging to coccidia was found. It is obvious that the fauna of coccidia investigated in groups of fishes has been better un-derstood in fishes of commercial importance.

At present it is difficult to judge of the reasons of the absence of in-formation about finds of coccidia in Holocephali: either coccidia do not parasitize them, or fishes that belonging to this class have been insufficiently studied because of the features of their mode of life, relatively small number and narrow distribution. It is probable that the latter circumstance provides a more plausible explanation of the existing situation, and coccidia of this class of fishes will be described in the future. 

Distribution of coccidia by order of fishes

Fishes are considered to include 56 orders. Of these class Sarcopterygii includes 3 orders, the class Elasmobranchii includes 12 orders, the class Holocephali includes 1 order and the class Actinopterygii includes 40 orders (Eschmeyer, 1990). Coccidia are found in representatives of only 25 orders (Table 1).

Coccidia have been described in fishes belonging to 6 orders of the class Elasmobranchii, i.e. in one half of the known groups. In the orders Lamniformes, Torpediniformes, Rajiformes and Myliobatiformes coccidia belonging only to the genus Eimeria have been found; and in fishes of the order Squaliformes coccidia of the genus Goussia only have been described. In the representatives of the order Carchariniformes coccidia belonging two genera Eimeria and Goussia were found. In other six orders of the class Elasmobranchii (Hexanchiformes, Heterodontiformes, Orectolobiformes, Pristiophoriformes, Squatiniformes, Pristiformes) coccidia have not been described. Representatives of these orders are characterized by low abundance and a small number of species. In our point of view it is this circumstance that explains their absence in the description of coccidia.

A very similar situation is observed in orders of the class Actinopterygii. Coccidia are found only in 19 of 42 orders, which are included in this class of fishes. As in the class Elasmobranchii, coccidia parasitizing fishes of the class Actinopterygii were not found in orders, which are characterized by low abundance and a small number of species.

The richest fauna of coccidia was found in fishes of the largest orders. Thus, coccidia belonging to 5 genera (Calyptospora, Eimeria, Goussia, Isospora, Octosporella) were found in fishes of the order Cypriniformes. The same number of genera of coccidia (Calyptospora, Cryptosporidium, Eimeria, Epieimeria, Goussia) were described in fishes of the order Perciformes.

Coccidia belonging to three genera were described in representatives of four orders Anguilliformes, Gadiformes, Cyprinodontiformes and Scorpaeniformes (Table 1). Coccidia belonging to one or two genera were found in 13 more orders of fishes. Such distribution of systematic groups of coccidia by order of fishes is apparently defined by two major factors: quantitative and qualitative structure of orders of fishes and the intensity of survey.

Table 1. Distribution of genera of coccidia by order of fishes

 

Genera of coccidia

Orders of fishes

Ca

Cry

Crys

E

Ep

G

I

O

Elasmobranchii

 

 

 

 

 

 

 

 

 Lamniformes

 

 

 

 

 

 

 

 Carchariniformes 

 

 

 

 

 

 

 Squaliformes 

 

 

 

 

 

 

 

 Torpediniformes 

 

 

 

 

 

 

 

 Rajiformes

 

 

 

+

 

 

 

 

 Myliobatiformes

 

 

 

+

 

 

 

 

Actinopterygii

 

 

 

 

 

 

 

 

 Acipenseriformes

 

 

 

+

 

+

 

 

 Osteoglossiformes

 

 

 

+

 

 

 

 

 Anguilliformes

 

 

 

+

+

+

 

 

 Clupeiformes

 

 

 

+

 

+

 

 

 Cypriniformes

+

 

 

+

 

+

+

+

 Siluriformes

 

 

 

+

 

 

 

 

 Salmoniformes

 

 

 

+

 

+

 

 

 Myctophiformes

 

 

 

+

 

 

 

 

 Gadiformes

 

 

+

+

 

+

 

 

 Batrachoidiformes

 

 

 

+

 

 

 

 

 Gobiesociformes

 

 

 

 

 

+

 

 

 Atheriniformes

+

 

 

+

 

 

 

 

 Cyprinodontiformes

+

 

 

+

 

+

 

 

 Beloniformes

 

 

 

 

 

+

 

 

 Beryciformes

 

 

 

+

 

  

 

 

 Gasterosteiformes

 

 

 

+

 

+

 

 

 Scorpaeniformes

 

 

 

+

+

+

 

 

 Perciformes

+

+

 

+

+

+

 

 

 Pleuronectiformes

 

 

 

+

 

 

 

 

 

Note:

Ca - Calyptospora; Cry - Cryptosporidium; Crys - Crystallospora; E - Eimeria; Ep - Epieimeria; G - Goussia; I - Isospora; O - Octosporella. '+' - coccidia found, identified to a genus.

 

The results of the analysis of occurrence of various taxonomic groups of coccidia in fishes have appeared rather interesting. Coccidia of the genera Eimeria and Goussia were found in fishes most frequently (Table 1). Coccidia of the genus Cryptosporidium have been found only in fishes of the order Perciformes. Coccidia of the genera Isospora and Octosporella occurred only in Cypriniformes. Coccidia belonging to the genera Cryptosporidium, Isospora and Octosporella are easily diagnosed, therefore the subjective factor in the identification is minimal in this case. Obviously the observed situation reflects objectively the existing law: the genera Cryptosporidium, Isospora and Octosporella have rather limited distribution in fishes. The only find of coccidia of the genus Crystallospora in fishes for 110 years shows a very narrow distribution of coccidia of this genus (Daoudi, 1987). To judge of the real distribution of coccidia belonging to the genus Epieimeria in fishes is difficult because of the objective difficulties in the identification of endogeneous development stages.

Distribution of species of coccidia among different taxa of fishes

The specificity of coccidia in various groups of animals was studied with different intensity. The vast experimental material on this problem has been accumulated on coccidia (fam. Eimeriidae) of birds and mammals (Pellerdy, 1974). The numerous experiments on infection of hosts by heterogeneous coccidia have shown, that coccidia have typically narrow specificity in most cases. As a rule, it is not possible to infect hosts belonging to different families and even different genera of one family with a heterogeneous coccidia (Krylov, 1961; Pellerdy, 1965; Noton & Peirce, 1971; Shah & Johnson, 1971).

The analysis of occurrence of the species of coccidia in various taxonomic groups of fishes basically confirms the data on narrow specificity of coccidia that were obtained on coccidia of birds and mammals. The greatest number of species of coccidia (184) was revealed only in one genus of fishes. A considerably smaller number species of coccidia (17) were described in various species of fishes of one genus, and also in fishes belonging to different genera of one family (27) and in fishes, belonging to different families of one order (6).

Special attention should be paid to the finds of the same species of coccidia in fishes of two, three and even four different orders. What does this mean? Is this a really wide host specificity of coccidia in fishes or is this the result of erroneous species identification in coccidia? The latter assumption is highly probable, but the final resolution of this problem is possible only by means of experiment.

Conclusions

Pisces is the richest group of vertebrates in respect of number and systematics. According to the different researchers it numbers from 20000 up to 25000 species. Only about 250 species of coccidia were described for this large number of fish species. It can be assumed, that the fauna of coccidia of fishes is more rich, because, as a rule, coccidia have narrow specificity and we can suggest, that each species of the host or close species of hosts are parasitized by specific species of coccidia. If we assume, that one species of fishes may be parasitized not by one but more species of coccidia (Table 2), the supposed number of existing, but not yet described species of the parasites will increase considerably. The curve of an increase in the number of de-scribed species of coccidia at various periods of time does not flatten out, which also suggests a large number of species of coccidia existing in fishes, but yet unknown to science.

Table 2. The maximal number of species of coccidia, described in one of fish species

Host

Number of the speciesof coccidia

Alburnus alburnus

5

Hypophthalmichthys molitrix

5

Notropis cornutus

6

Rutilus rutilus

8

Scardinius erythrophthalmus

8

Carassius auratus

10

 

In the systematic respect coccidia of fishes have been studied much better. Eight genera of coccidia have been found in fishes. Four genera of coccidia were described from fishes and were found only in fishes (Calyptospora - 5 species, Crystallospora - 1 species, Epieimeria - 5 species, Goussia - 69 species). Representatives of other four genera of coccidia parasitize not only in fishes, but also in other groups of vertebrates. Thus, coccidia of the genus Cryptosporidium have been found in birds and mammals. Of about 10 total species of cryptosporidia only one species C. nasoris (Hoover et al., 1981) was described. Coccidia of the genus Isospora parasitize in amphibians, reptiles, birds and mammals. Of approximately 360 species known, only one nominal species I. sinensis (Chen, 1984) was described in fishes and three other species were identified to a genus (Davronov, 1987). As we can see, the genus Isospora is represented very poorly in fishes, in comparison with other groups of vertebrates. Six species of the genus Octosporella were described, three of these were found in fishes (O. opeongoensis, O. sasajewunensis, O. notropis) (Li & Desser, 1985).

Representatives of the genus Eimeria are widely spread among vertebrates and now number more that 1700 species. The same pattern is observed in fishes. 157 species of coccidia belonging to the genus Eimeria were found.

Thus, the qualitative analysis of fauna of coccidia in fishes shows that they are represented by a large number of taxa. However expected number of species and systematic diversity of coccidia of fishes may considerably surpass the known number. Researchers look forward to new interesting discoveries.

Acknowledgements

The studies were carried out with financial support Russian Foundation for Basic Research (grant 99-04-49579) and Biodiversity Grant. The authors are grateful to Dr. O.N. Pugachev for the help in the collection of the information on the fauna of coccidia, and also to Dr. A.V. Balushkin and to Dr. N. G. Bogutskaya for advice on systematics of fishes.

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