Occurence of helminths in Chub, Leuciscus cephalus, of the Doganci (Bursa) dam lake, Turkey

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1 Bull. Eur. Ass. Fish Pathol., 21(6) 2001, 246 Occurence of helminths in Chub, Leuciscus cephalus, of the Doganci (Bursa) dam lake, Turkey Ali Aydogdu F. Naci Altunel & Hikmet Sami Yildirimhan Uludag Universty, Science and Art Faculty, Department of Biology, Görükle - Bursa, Turkey Abstract In this study, helminth parasites in chub of Dogancı Dam Lake and seasonal variation of these parasites were investigated monthly from December 1998 to November A total of 5 species of helminth parasites were found on 29 of 77 fish examined. The following parasites were found: Dactylogyrus folkmanovae, D. vistulae, Paradiplozoon megan, in gills of host fish, and Bothriocephalus acheilognathi, Rhabdochona denudata in intestine of host fish. Dactylogyrus folkmanovae was the dominant parasite species found in chub. The infection was the highest in May during the years of the study. The second dominant parasite, D. vistulae was also the highest in May. The third dominant parasite Rhabdochona denudata was highest during June and November. Paradiplozoon megan and Bothriocephalus acheilognathi were present only in very small numbers. Only three Bothriocephalus acheilognathi were found in the intestine. Occurrence and seasonal variation of the parasite species are discussed. Introduction The helminth fauna of fish from Dam Lake habitats have rarely been investigated and consequently little is known about it in comparison with lakes and breeding ponds. On the other hand, the helminth fauna of Turkey freshwater fishes are still little known too and only limited studies have examined parasites of fish in Turkey ( Aydogdu 1996, Aydogdu et. al 1996, 1997, 2000), Altunel (1981, 1982), Cantoray and Özcan ( 1975). One such species is chub (Leuciscus cephalus). As far as we know only Cantoray and Özcan ( 1975) investigated helminth parasites in chub and found Ligula intestinalis from Keban Dam Lake. In comparison with other countries (Czechoslovakia, Norway) the number of the helminth parasites in chub in Turkey is rather poor. As many as 15 species of helminth were recorded in this fish in Czechoslovakia according to Moravec and Scholz (1991) and a total number of 2149 parasites belonging to 38 taxa according to Gelnar et. al (1997) in Czechoslovakia and 8 parasites in Norway according to Sterud and Appleby (1997). In other European countries where chub has been examined, only a small number of parasite species were recorded from them (1 species in England for example, Bates and Kennedy (1990)). The present study aims to increase our knowledge on the occurrence of parasites of L. cephalus in Turkey. Material And Methods All fishes were collected by net from the Dogancı Dam lake, samples being taken at monthly intervals from this locality from December 1998 to November During

2 Bull. Eur. Ass. Fish Pathol., 21(6) 2001, Number of parasites Temperature Dactylogyrus folkmanovae December 98 January 99 February 99 March 99 April 99 May-99 June 99 July 99 August 99 September 99 October 99 November 99 Fig.1. Water temperature of Dogancı Dam Lake and Occurrence of Dactylogyrus spp. in Chub this study, the fish were always transported to the laboratory alive, in aerated cans or polyethylene bags inflated with oxygen. If sampling was performed in summer, the water used for transporting the fish to the laboratory was cooled with ice. Fish transported to our laboratory were placed in flow through type concrete basins and aquaria, and dissected as soon as possible, generally within a few days of catching. During the dissection, all internal organs (liver, kidney, heart, intestine, swimbladder, gallbladder) the gill filaments, the eyes, the fins and the skin were examined. The parasitological findings were based upon the examination of small pieces taken from the individual organs. The examinations included dissection under stereomicroscope and light microscopic examination. Parasites found on gills and in intestine were counted and for later studies some of them were fixed in Bouin s solution. The fixed samples were kept in the lithium carbonate solution until they lost their yellow colour caused by Bouin fixation. Subsequently, samples were passed through a water bath and then stained. The samples were repassed through a water bath then dehydrated stepwise in ethanol (70% for minute, 80% for10 min, 90% for 5 min and 100% for 5 min). The materials were kept in xylol for two minutes and mounted in Canada Balsam. In the staining procedure aceto-carmine and borax carmine were used. The taxonomic classification of the parasites was done according to Bychovskaya - Pavloskaya (1962), Markevic (1951), Moravec (1994) and Yamaguti (1961, 1963). Results We examined 77 specimens of chub from Dogancı Dam Lake. During our study, three

3 Bull. Eur. Ass. Fish Pathol., 21(6) 2001, 248 ectoparasites on the gills and two endoparasites in the intestine of the studied chub were recorded: Dactylogyrus folkmanovae,, Paradiplozoon megan, Bothriocephalus acheilognathi and Rhabdochona denudata. The first three were found on the gills and the other two in the intestine However, one of these parasites, Bothriocephalus acheilognathi, was present only in very small numbers, while the others dominated, especially, Dactylogyrus folkmanovae) Among the parasites, the dominant group was Dactylogyrus spp. It noteworthy that Dactylogyrus folkmanovae was found on Leucıscus cephalus Its typical host. Seasonal variation of this species is seen in Figure I The fish were free of parasites from December 98 to March 99 but a rapid rise in infection occurred in May. The infection was the highest in May and stopped in July and August. A slight increase in numbers was observed in September and October. The second dominant parasite was also recorded in the host fish gills, at high occurrence in spring (May). The third species is Paradiplozoon megan. 16 of 77 fish were infected by Paradiplozoon megan. Six fish containing a total of 16 parasites were found. The infection was recorded in May, June, September. The infection was the highest in September. A single species of Cestoda was found in Leuciscus cephalus. It is Bothriocephalus acheilognathi. This cestode species occurred in the locality rarely in the intestine of chub, the findings were in May and June (a single specimen in June ) two fish containing a total of 3 parasites were found. The fifth species R. denudata was also recorded in the host intestine. 21 of 77 fish were infected by R. denudata. A survey of the chub examined and their infection with R. denudata is given in Table I. Their infection in monthly samples was highest during June and November. 21 fish containing a total of 47 parasites were found. Discussion Three helminth parasites were found in gills of the host fish: D. folkmanovae, D. vistulae, P. megan, two helminth parasites were found in intestine of host fish: 1 Cestoda, 1 Nematoda. Two of five parasites found (Bothriocephalus acheilognathi and P. megan) were rare. Bothriocephalus acheilognathi was determined to be the least prevalent parasite and found only in the intestine. The study results show that in chub the major parasite is D. folkmanovae followed by D. vistulae, R. denudata and P. megan in descending order. Seasonal variation and the infection of these species can be seen in Figure 1. The infection of Dactylogyrus spp. correlates with changes in water temperature. Several studies have been published on the seasonal changes of monogenean infection in fish (Chubb 1977), Shulman 1989). Furthermore temperature is commonly regarded as one of the most important factors determining the occurrence and abundance of monogenean parasites (Scott and Nokes 1984, Hanzelova and Zitnan 1985, Gelnar 1987). The seasonal occurrence of dactylogyrids is sometimes more influenced by other abiotic or biotic factors than by temperature. For example, Dactylogyrus solidus is very sensitive to oxygen depletion. This species occurs on carp only during the cold period when oxygen concentration of the water is high (Bauer 1961). In this study, there is a clear relation with in-

4 Bull. Eur. Ass. Fish Pathol., 21(6) 2001, 249 Parasite species Number of Chub examined Dactylogyrus folkmanovae Paradiplozoon megan Bothriocephalus acheilognathi Rhabdochona denudata Months Number of Chub infected Percent of infected fishes Number infection December January February March April May June July August September October November Total , Dactylogyrus folkmanovae Paradiplozoon megan Bothriocephalus acheilognathi Rhabdochona denudata Dactylogyrus folkmanovae Paradiplozoon megan Bothriocephalus acheilognathi Rhabdochona denudata Table. 1. Survey of Leuciscus cephalus examined from the Dogancı Dam Lake and their infection with helminth parasites. fection level of Dactylogyrus spp. In the present case, it can be concluded that the high dactylogyrid intensities in spring and early summer are apparently influenced by temperature. The melting of ice cover in May and rising temperatures seem to be important factors, but the decrease in intensity in the middle of the summer is probably caused by other factors. For example, the fish may acquire a better immunological response to these parasites when the temperature rises. However, the composition of the helminth fauna is considerably affected by diet of the host. There can be no doubt that the parasite fauna is in relation with the host s diet. Responsible for this relation is the fact that many parasites effect their entry into the host through the alimentary canal by being swallowed with the food. Apart from this relationship, the character of the diet exerts no less important indirect influence on the process of formation of the parasite fauna. It determines the entire physiology of digestion of the host, the chemical processes in the various parts of the alimentary canal, the degree of fragmentation of food with the related hazard which mastication presents to the parasite. The chub fed mainly on larvae of aquatic insects such as mayflies, caddis flies, stone flies, chironomids, but occasionally also on terrestrial insects (Hemiptera, Coleoptera) spiders, snails and plant material (algae, leaves). Larvae of mayflies, the main intermediate hosts of R. denudata nematodes, were part of the chub s diet. In this study, the third dominant parasite R. denudata is a common intestinal parasite of

5 Bull. Eur. Ass. Fish Pathol., 21(6) 2001, 250 many species of cyprinid fishes and is widely distributed over Europe and Palaeartic Asia (Moravec 1975). The life cycle of R. denudata has not hitherto been studied experimentally, however, the findings of naturally infected invertebrates suggest that it is similar to that in other congenerıc species utilising mayflies (Ephemeroptera) and possibly some other aquatic insects as obligate intermediate hosts. The naturally infected intermediate host of R. denudata were recorded by Shtein (1959). In addition cyclopoid copepods are the intermediate hosts B. acheilognathi. The rate of infection in chub is concerned. It is obvious that cestodes and nematodes larvae penetrate actively into the fish, infections by all remaining helminths are acquired by chub pv.os. while swallowing free infective stages of parasite infected benthic or planktonic invertebrates such as oligochaetes, copepods (B.acheilognathi), ostracods, ısopods and aquatic insects (R. denudata). Accordingly, the choice and composıtion of chub s food is very important for the formation of the helminth fauna in this fish, and this is considerably influenced by local ecological conditions. References Altunel, F. N. (1981) Ege kıyılarındaki kefal balıklarının (Mugil cephalus. Liza aurata. L. saliens. L.ramada. Chelon labrosus. Oedalechilus lebeo) plathelminth parazitleri üzerine arastırmalar. TÜBITAK Veterinerlik ve Hayvancılık arastırma grubu Proje Çalısması. No: VHAK 401,Ankara 130 s. Altunel, F. N. (1982) Parasitic infestation of grey mullet (Mugil ssp.)along the Turkish coast of Aegean sea, Pathology in marine aqaculture, Europan aquaculture society, special publication, No:9 Bredene Belgium. Aydogdu, A. (1996) Iznik gölü sazan balıkları (Cyprınus carpio L. ) plathelminth parazitlerinin Tespitine Yönelik Arastırmalar. Master thesis. (unpublished) U. U. Fen. Bil. Enst. Biyoloji Ana bilim Dalı. (in Turkish) (with abstract in English) Aydogdu, A., Yildirimhan, H.S., & Altunel, F. N. (1996) Iznik Gölü Kadife Balıklarının (Tinca tinca L.1758) nın Parazitleri Üzerine Bir Çalısma. T. Parazitoloji Dergisi. 20: (in Turkish) (with abstract in English) Aydogdu, A., Yildirimhan, H.S., & Altunel, F. N. (1997) Iznik Gölünden Yakalanan Akbalık (Rutilus frisii) nın Helminth Faunası üzerine Bir arastırma. IX. Ulusal Su ürünleri Semposyumu: Eylül Isparta. (in Turkish) (with abstract in English ) Aydogdu, A., Yildirmhan, H.S., & Altunel, F. N. (2000) The helminth fauna of Adriatic roach (Rutılus rubilio) in?znik lake. Bull. Eur. Ass. Fish. Pathol. 20 (3).170. Bates, R. M. & C.R. Kennedy, C. R. (1990) Potential interactions between Acanthocephalus aanguilla and Pomphorhynchus laevis in their natural hosts chub, L. cephalus and the European eel A. anguilla. Parasitology 102: Bauer, O. N. (1961) Parasitic diseases of cultured fishes and methods of their prevention and treatment. In: Parasitology of fishes. Pp Oliver & Boyd, Edinburgh, UK. Bychovskya-Pavlovskaya, I.E. (1962) Key to parasites of freshwater fishes of the U.S.S.R., II, Moskova, Leningrad, Trans.Birrow A. and Cale, Z.S. 1964, Israel programme for scientific, translations, Jerusalem, 919 pp. Cantoray, R., & Özcan, A. (1975) Elazıg ve çevresindeki tatlı su balıklarında Ligulose Fırat Univ. Vet. Fak. Derg. 2: (in Turkish) (with abstract in English) Chubb, J. C., (1977) Seasonal occurrence of helminths in freshwater fishes. Part I. Monogenea. Advances in Parasitology 15:

6 Bull. Eur. Ass. Fish Pathol., 21(6) 2001, 251 Gelnar, M., (1987) Experimental verification of the effect of physical condition of Gyrodactylus gobiensis Glaser, 1974 (Monogenea) Folia Parasitologica 34: Gelnar, M., Sebelova, S., Dusek, L., Kaubkova, B., Juradja, B. & Zahradkova, S. (1997) Biodiversity of parasites in freshwater environment in relation to pollution. Parasitologia 39: Hanzelova, V. & Zitnan, R., (1985) Epizootiologic importance of the concurrent monogenean invasions in carp. Helminthologica 22: Markevic, A. P. (1951) Parasitic fauna of freshwater of the fish of the Ukrainian S.S. R.,trans by Rofael, N., Kudus, 157: Moravec, F and Scholz, T. (1991) Occurrence of endohelminths in Chub Leuciscus cephalus, of the Rokytna River, Czechoslovakia. Acta. Soc. Zool. Bohemoslov, 55: Moravec, F. (1975) Reconstruction of the nematode genus of Rhabdochona Railliet, 1916 with a review of the species parasite in fishes of Europe and Asia studic CSAV no: 8 Publ House Academia Prague, pp Scott, M. E. and Nokes, U.S., (1984) Temperature depondent reproduction and survival of Gyrodactylus bullatarudıs (Monogenea) on guppies (Poecilia reticulata) Parasitology 89: Shtein, G. A., (1959) On the questions of the life history and living conditiong of the nematode Rhabdochona denuda. Acad. Sci. 1: 27: (in Russian) Shulman, B.S., (1989) Effect Of Ecological Factors On The Abundance Dynamics Of Gyrodactylus (Monogenea, gyrodactylidae) under polar conditions in Bauer, O. N., ed. Parasites of freshwater fishes of North West Europe. Petrozvodsk, Sterud, E. & Appleby, C. (1997) Parasites of dace (L. leuciscus), ide (L. idus)and chub (L. cephalus), from South-Eastern Norway. Bull.Scand. Parasitol,6(1): Yamaguti, S. (1961) Systema Helminthium Nematodes Vol.III, Inter Science Publishers. New York, London,119 p. Yamaguti, S. (1963) Systema Helminthium Monogenea and Aspidocotylea. Vol.IV, Inter Science Publishers. New York, London, 325 p. Moravec, F. (1994) Parasitic nematodes of freshwater fishes of Europe, Inst. of notes on their distribution. J. Fish Biol., 6,

Helminth parasites (Plathelminthes) of common carp (Cyprinus carpio L.) in Iznik Lake

Bull. Eur. Ass. Fish Pathol., 22(5) 2002, 343 Helminth parasites (Plathelminthes) of common carp (Cyprinus carpio L.) in Iznik Lake Ali Aydogdu* & F. Naci Altunel Uludag University, Science Faculty, Department