Bull. Eur. Ass. Pathol., 30(1) 2010, 8 A comparative study on the parasite fauna of wels catfish glanis (L.) from a heated- water-channel fish farm and a natural water body

E. Sobecka*, J. Wierzbicka and M. Hałupka

Division of Fish Diseases, West Pomeranian University of Technology, ul. Kazimierza Królewicza 4, 71- 550 Szczecin,

Abstract Parasitological studies have been carried out on wels catfish from a heated-water-channel fish farm near the power plant and the natural water body. The cultured and free living wels catfish contained 9 and 18 parasite species, respectively. The species richness and diversity of parasites are much higher for the free living fish and the abundance of parasites in this group of fish was many times higher than that in the group of cultured fish. Faunistic similarity of both parasite communities was low. The dominant group of parasites in cultured fish was digeneans, while in free living fish it was monogeneans. Two species were only found on cultured fish, while three species were only associated with free living wels catfish.

Eight new records have been reported in Poland for the following genus and species: 1 myxozoan parasites (Myxobolus sp.), 4 species of ciliates (Ichthyophthyrius multifiliis (Fouquet, 1876), Chilodonella piscicola (Zacharias, 1894), Trichodina siluri (Lom, 1970), Capriniana piscium (Bütschli, 1889) Jankowski, 1973, 1 digenean (Orientocreadium siluri (Bychowski and Dubinina, 1954), 1 ( (Linnaeus, 1758) and 1 bivalve larvae (Unio sp.).

Introduction Lake Dąbie is one of the largest lakes in Poland. a common freshwater fish in Poland, but in It receives a large inflow of fresh water supplied heated water they were cultured for over a primarily by the Odra River. The discharge decade. The main aim of this work was to channel of the cooling water from the Dolna study the parasite community of a population Odra power station lies in the lower course of of catfish and to compare the parasite fauna of the Odra River below the water course joining free living and cultured catfish from the above the Odra River with Lake Dąbie. Because of described different type of environments. high temperatures of the channel water (the annual mean is + 12.9ºC) it is the habitat of Material and methods many species of cultured and free living fish Free living catfish from Lake Dąbie were (Zmysłowska et al., 2000). Wels catfish are caught during industrial catchment and

* Corresponding author’s e-mail: [email protected] Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 9 farmed catfish were collected from Dolna Odra was comprised of 2425 individuals (18 power station at Nowe Czarnowo. All organs species) in free living S. glanis and 131 of the fish body were studied except for the individuals (9 species) in cultured fishes . The quantitative descriptors of parasite (Table 1). The parasites of catfish from Lake populations such as prevalence (P %), mean Dąbie belonged to Myxosporea, Ciliophora, infection intensity (Mi), relative density (Rd), Monogenea, Digenea, Cestoda, Nematoda, frequency and dominance (D) were determined Acanthocephala, Mollusca, Copepoda, and (Bush et al., 1997; Czachorowski, 2006). The . Myxobolus sp., Eustrongylides dominance values allowed classification of mergorum larva, Argulus foliaceus and Unio the species as eudominant (> 10%), dominant sp., which were found in catfish make the new (5.1–10%), subdominant (2.1–5.0%), recedent host records in Poland. The cultured catfish (1.1–2%) and subrecedent (< 1.0% of given parasites belonged to Ciliophora, Monogenea, species) (Niedbała & Kasprzak, 1993). It is the Digenea, Nematoda and Mollusca. On the ratio of the number of individuals in the given of three fishes, Capriniana piscium were species to the total number of individuals in found for first time in Poland. all species. Among the parasites of both fish groups, The characterisation of the parasite community digeneans occurred at the highest frequency. structure was done using the total number The species diversity index of the parasites of parasite species (species richness S), the was higher for free living . The Shannon-Weaver species diversity index (H’), dominance index was higher in cultured fish the Berger-Parker species dominance index (D) (Table 2), which was accompanied by lower and the Jaccard faunistic similarity coefficient species diversity of the cultured fish parasite (Wxy) (Trojan, 1992; Kennedy & Pojmańska, community. 1996). The above parameters and classification were applied mostly to countable parasites. The eudominant parasite of free living catfish Parasite communities of wels catfish from two was Silurodiscoides vistulensis, the dominant sites were characterised and classified (Price, were Orientocreadium pseudobagri and Unio sp., 1980; Esch et al., 1988). while, Proteocephalus osculatus and Ergasilus sieboldi were the recedent parasites. The other Results parasites were subrecedents (Table 1). Free living catfish from Lake Dąbie (35 specimens) had a mean total length of 36.0±59.1 The eudominant parasite of cultured catfish cm and mean weight of 620.0±771.2 g. The was Diplostomum spp. larvae and unidentified mean total length of catfish (36 specimens) Nematoda larvae. The recedent parasites from the cage farm was 35.6±5.1 cm and the were Gyrodactylus sp. and S. vistulensis. No mean body weight was 339.4±115.5 g. All parasites found belonged to the dominant, fish studied from Lake Dąbie and 97.2% fish subdominant and subrecedent species groups. from the fish farm were infected by at least The dominance describes the share of the one parasite species. The parasite community given species in an assemblage of parasites. Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 10

Table 1. Infection parameters of the species parasitizing cultured and free living Silurus glanis.

Prevalence Mean Relative Dominance Species [%] intensity density [%] Parasites cultured S. glanis Chilodonella piscicola (Zacharias, 1894) 50 Ichthyophthyrius multifiliis 69.44 (Fouquet, 1876) Trichodina siluri (Lom, 1970) 75 Gyrodactylus sp 5.56 1 0.06 1.53 Diplostomum spp. 86.11 3.52 3.03 83.21 Capriniana piscium 5.56 (Bütschli, 1889) Jankowski, 1973 Silurodiscoides vistulensis (Siwak, 1932) 2.8 2 0.06 1.53 Unio sp. (larvae) 8.33 Nematoda (larvae) 5.56 9 0.50 13.74 Parasites free living S. glanis Myxobolus sp. 2.86 Chilodonella piscicola (Zacharias, 1894) 2.86 Trichodina siluri (Lom, 1970) 45.71 Silurodiscoides vistulensis (Siwak, 1932) 94.29 57.52 54.23 78.27 Unio sp. (larvae) 34.29 13.33 4.57 6.60 Diplostomum spp. (larvae) 22.86 2.63 0.60 0.87 Azygia lucii (Müller, 1776) 8.57 9.67 0.83 1.20 Bucephalus polymorphus (Baer, 1827) 5.71 3.50 0.20 0.29 Orientocreadium pseudobagri 31.43 15.64 4.91 7.09 (Yamaguti, 1954) Orientocreadium siluri 5.71 1.5 0.09 0.12 (Bychowski and Dubinina, 1954) Proteocephalus osculatus (Goeze, 1782) 22.86 5.38 1.23 1.77 Raphidascaris acus (Bloch, 1799) (larvae) 2.86 2 0.06 0.08 Eustrongylides mergorum 2.86 1 0.03 0.04 (Rudolphi, 1809) (larvae) Rhabdochona denudata (Dujardin, 1845) 8.57 3 0.26 0.37 Acanthocephalus lucii (Müller, 1776) 2.86 8 0.23 0.33 Neoechinorhynchus rutili (Müller, 1780) 8.57 2.67 0.23 0.33 Argulus foliaceus (Linnaeus, 1758) 31.43 2.18 0.69 0.99 Ergasilus sieboldi (Nordmann, 1832) 20.00 5.71 1.14 1.65 Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 11

Table 2. The indices of species richness, dominance and diversity of cultured and free living catfish parasites.

Species Berger-Parker Shannon- Number of Fish richness dominance index Weaver`s index specimens (S) (D) (H’) Cultured catfish 131 9 83.21 0.48 Free living catfish 2425 18 77.50 0.81

The faunistic similarity of both parasite Argulus foliaceus was found on the skin and component communities was low (22%). fins of free living catfish from Lake Dąbie. The Chilodonella piscicola, Trichodina siluri, skin and fins of cultured fishes were free of Diplostomum spp., S. vistulensis and Unio sp. any Argulus sp. were the taxa found for the fish from both groups. The majority of catfish parasites were autogenic species. Allogenic parasites were The communities of parasites were metacercariae of Diplostomum spp. (fish from taxonomically similar. In free living catfish both groups) and E. mergorum larvae (fish from the spores in the cysts of Myxobolus sp., 2 Lake Dąbie). The most frequent autogenic Ciliophora species (C. piscicola, T. siluri), parasites were the monogeneans S. vistulensis monogeneans S. vistulensis, copepods Ergasilus in free living fish, while the highest prevalence sieboldi and larvae of Unio sp. were found. In from among the allogenic parasites was noted cultured fish also Ichthiophthirius multifiliis and for Diplostomum spp. larvae, occurring in Capriniana piscium (Ciliophora), monogeneans cultured fish. Gyrodactylus sp. and Unio sp. were identified, but no presence of Myxobolus sp. and E. sieboldi The parasites of catfish were mostly were detected. generalists. The specialists comprised only of T. siluri and S. vistulensis in the free living and The community of intestinal parasites cultured fish. of free living catfish was composed of 4 digeneans species (Azygia lucii, Bucephalus The most numerous group in free living polymorphus, Orientocreadium pseudobagri, catfish was monogeneans which hosted 1898 O. siluri), 1 tapeworm (P. osculatus), 3 specimens (S. vistulensis). Cultured fishes were (Raphidascaris acus, Rhabdochona infected only by 4 specimens of Monogenea, denudata, Eustrongylides mergorum) and 2 the most numerous parasites were Diplostomum acanthocephalans (Acanthocephalus lucii, spp. larvae (109 specimens). Neoechinorhynchus rutili). Only the larvae of one unidentified species were Discussion detected in digestive tract of cultured S. The list of catfish parasites found in Poland glanis. comprises 27 species (Grabda, 1971; Pojmańska Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 12

& Cielecka, 2001); in the rest of it is own and other fish species. Grownup fish almost twice as long (Byhovsky, 1962; Dezfuli, extend their diet and feed mainly on fish, 1992; Molnar, 1993; Euzet & Pariselle, 1996; bivalves, snails, , crayfish, water Banuš et al., 1997; Lim et al., 2001; Galli et and leeches (Brylińska, 2000). The very wide al., 2003). A total of 22 parasite species were diet spectrum facilitates the transmission of recovered from the fish necropsed during the parasites of complex life cycle. For the the current study. According to Kennedy and majority of intestinal parasites, free living Guegan (1994), the structure of a parasite catfish are the final hosts (all digeneans and community depends on local conditions and acanthocephalans, the tapeworm). From the number of species in certain ecosystems among the nematodes found only E. mergorum is always lower than the number of species ends its life cycle in water birds and its described for the host’s entire range of presence in catfish was probably accidental. distribution. Free living fish examined during The other two species (R. acus, R. denudata) the current study hosted more than double were found in catfish in the larval stage (from the number of parasites (H´=0.81) and over 18 freshly eaten fish that are intermediate hosts times greater number of parasite specimens of nematodes and belong to catfish diet) and compared with farmed fish. The majority of the in adult stage (Pojmańska, et al., 2007). parasite species (77.8%–7 species) of cultured catfish were ectoparasites, and three of them The intestinal fauna of catfish cultured in cages (C. piscicola, I. multifiliis, T. siluri) occurred in cooling water pond was poor. In this type of with high prevalence. This unexpectedly rich culture the fish are fed mainly on granulated ectoparasite fauna of cultured fish are probably fodder of properly adjusted composition related to the environmental conditions (Zmysłowska et al., 2000). The natural food favouring its development (Niewiadomska, they intake is accidental, depends on the 1977) and perhaps low effectiveness of the availability and makes a small contribution preventive treatments. Free living catfish in the diet. The presence of nematode larvae hosted 7 species of ectoparasites (38.9%), of and digeneans Diplostomum spp. indicate high which the prevalence of S. vistulensis was availability of snails from the genus Radix and the highest. The presence of was free living plankton crustaceans that enriched noted only in this group of fish studied. the diet of cultured catfish.

Our studies have revealed that the parasite A comparison of our results with the earlier fauna of catfish from Lake Dąbie is richer published data on catfish parasitic fauna in than that of cultured fish, in particular that Poland (Grabda, 1971) has shown that the of the community of intestinal parasites. The qualitative structure of parasite communities catfish is predacious and the type of their diet has been enriched by 1 myxozoan parasite depends on the food availability and the age (Myxobolus sp.), 4 species of ciliates (I. multifiliis, of the fish. Fry and young fish feed mostly on C. piscicola T. siluri, C. piscium), 1 digenean (O. fine crustaceans, larvae (Chironomidae, siluri),1 crustacean (A. foliaceus) and 1 bivalve Diptera, Trichoptera) and the hatch of their larvae. European literature on catfish parasites Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 13

of Poland.” Wydawnictwo Naukowe PWN does not mention the presence of C. piscicola Warszawa. ISBN 83 01 131004. and C. piscium. The prevalence of S. vistulensis in free living fish was the highest, which Bush AO, Lafferty KD, Lotz JM and Shostak conflicts with the previous report by Ejsymont AW (1997). Parasitology meets ecology in own terms: Margolis et al. revisited. Journal of (1970) who showed that the prevalence was Parasitology 83, 575–583. lower in free living fish. The prevalence of P. osculatus and O. pseudobagri in this study Byhovsky BE (1962). “Opredelitel reached 22.86% and 31.43% respectively, and presnovodnyh ryb SSSR.” Akademiâ Nauk SSSR. was almost double that reported by Ejsymont (1970). Combes C (1999). “Interactions durables. Ecologie et évolution du parasitisme.” Only four parasites of catfish were classified Masson, Editeur, Paris. ISBN 2-10-005753-7. as specialists (T. siluri and S. vistulensis in Czachorowski S (2006). Descriptive method of cultured fish and S. vistulensis O. siluri, P. biocoenosis – zoocoenology. www.uwm.edu. osculatus in free living fish). According to pl/czachor/publik/pdf-inne/zoocenozy.pdf. Price (1977) the more ancient host species Dezfuli BS (1992). Occurrence of harbour more specific parasites. This should Pomphorhynchus laevis Müller 1776 result from beer adaptation of parasites to (Acanthocephala) in Silurus glanis (L.) from the conditions offered by the host aVer a lapse the river Po. Parassitologia 34, 71–82. of time (Combes, 1999). The results of our Ejsymont L (1970). Parasites of the sheatfish, study suggest a rather short time of parasite Silurus glanis L., from the river Biebrza and adaptation to catfish. its tributaries. Acta Parasitologica Polonica 17, 203–216. Generalists who are most likely to spread and Euzet L and Pariselle A (1996). Le parasitisme colonise many host species in particular in des poissons Siluroidei: un danger pour the natural water bodies (Manter, 1967) were l´? Aquatic Living Resources 9, common parasites of both free living and 145–151. cultures fish. Galli P, Stefani F, Bezoni F, Grosa G and Zullini A (2003). New record of alien monogeneans Acknowledgements from Lepomis gibbosus and Silurus glanis in We would like to thank Agnieszka Oleś for the . Parassitologia 45, 147–149. technical support of the part of this work. Grabda J (1971). “Katalog fauny pasożytniczej Polski (Catalogus Faunae Parasiticae References Poloniae). Pasożyty krągłoustych i ryb Banuš V, Moravec F and Špakulova M (1997). (Parasiti Cyclostomatorum et Piscium).“ The red data list of helminths parasitizing fishes PWN, Warszawa–Wrocław. of the orders Cypriniformes, Siluriformes and Gadiformes in the Czech Republic and Slovak EsN G, Kennedy CR, BusN AO and Aho JM Republic. Helminthologia 34, 35–44. (1988). Paerns in helminths communities in freshwater fish in Great Britain: alternative Brylińska M (2000). “The freshwater fishes strategies for colonisation. Parasitology 96, Bull. Eur. Ass. Fish Pathol., 30(1) 2010, 14

519–532. 0 134 985.

Kennedy R and Guegan JF (1994). Regional Price PW (1977). General concepts on the versus local helminth parasites richness evolutionary biology of parasites. Evolution in British : saturated or 31, 405–420. unsaturated parasite communities? Parasitology 109, 175–185. Price PW (1980). “Evolutionary biology of parasites.” Princeton University Press. Kennedy CR and Pojmańska T (1996). Princeton. ISBN 13 978 0 691 08257 8. Richness and diversity of helminth parasite communities in the common carp and in three Trojan P (1992). Fauna structure analysis. more recently introduced carp species. Journal Memorabilia Zoologica 47, 1–120. of Fish Biology 48, 89–100. Zmysłowska I, Guziur J, Woźniak M Harnisz Lim HS, Timofeeva TA and Gibson DI M and Mientki C (2000). Effect of cage culture (2001). Dactylogyrean monogeneans of the of the sheatfish (Silurus glanis L.) on the Siluriformes of the Old World. Systematic hygienic state of fish and water environment. Parasitology 50, 15–197. Bulletin VURH, Vodnany, 36, 90–98.

Manter H (1967). Some aspects of the geographical distribution of parasites. Journal of Parasitology 53, 1–9.

Molnar K (1993). Sphaerospora siluri n. sp. (Myxosporea: Sphacrosporidae) in the kidney of the sheatfish (Silurus glanis). Acta Veterinaria Hungarica 41, 341–347.

Niedbała W and Kasprzak K. 1993. Biocenotic indexes used in the ordering and analysis of data in quantitative studies. In “Methods in Soil Zoology” (M. Górny and M. Grüm, Eds.), pp. 379–396. Elsevier, Amsterdam, PWN, Warszawa. ISBN 13: 0444988238.

Niewiadomska K (1977). Parasites of some fish species from the Konin region lakes . Roczniki Nauk Rolniczych 97, 45–57.

Pojmańska T and Cielecka D (2001). “Cestodes associated with the aquatic environment.” Polish Society of Hydrobiology: Freshwater fauna in Poland, 32. Wydawnictwo Uniwersytetu Łódzkiego. ISBN 83 7171 525 0.

Pojmańska T, Niewiadomska K and Okulewicz A (2007). “Parasitic helminths in Poland. Species, hosts and a missing piece.” Polish Society of Parasitology, Warszawa. ISBN 839