Monogenean and cestode parasites of Pseudophoxinus antalyae, Bogutskaya 1992 and Cyprinus carpio, Linnaeus 1758 from Kepez Antalya, Turkey

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1 Bull. Eur. Ass. Fish Pathol., 27(1) 2007, 23 Monogenean and cestode parasites of Pseudophoxinus antalyae, Bogutskaya 1992 and Cyprinus carpio, Linnaeus 1758 from Kepez Antalya, Turkey E. Soylu 1 * and Y. Emre 2 1 Vocational School of Technical Sciences, Fisheries Department, Marmara University, Istanbul 34722, Turkey; 2 Ministry of Agricultural and Rural Affairs, Mediterranean Fisheries Research, Production and Training Institute (MEDFRI), Antalya, Turkey. Abstract In this study, a total of 72 Pseudophoxinus antalyae and 58 Cyprinus carpio have been investigated during February through August In antalyae the prevalence and mean intensity level of Dactylogyrus sphyrna was 2.7% and 1.5±0.5 respectively, D. ergensi was 38.8% and 16.1±1.09 and Paradiplozoon homoion was 73.6% and 8.15±0.47. Two monogeneans were found on the gills of carpio namely D. extensus at a prevalence of 23.6% and a mean intensity of 13.5±2.49 and homoion with a prevalence of 1.3% and mean intensity of 1.0. In the intestine of carpio Caryophllaeus laticeps occurred at a prevalence of 48.2% and mean intensity of 4.03±0.43. Paradiplozoon homoion was the dominant species in antalyae, whilst in carpio the dominant species was laticeps. This report provides the first record of Dactylogyrus ergensi in Turkey. Introduction To date there have been no studies on the parasite fauna of Pseudophoxinus antalyae which is an endemic fish species in Antalya, Turkey. On the other hand, the parasites of carpio in Turkey have been extensively studied (Oguz, 1991; Oguz et al., 1996; Öztürk, 2000; Özer & Erdem, 1998, 1999; Aydogdu et al., 2001a; Aydogdu & Altunel, 2002; Cengizler et al., 2001; Uzunay & Soylu, 2006). The present paper demonstrates the results of the parasitological investigation of antalyae and carpio. Materials and methods The investigation was carried out during February through August 2004 with monthly intervals, at each time period about ten Pseudophoxinus antalyae and eight Cyprinus carpio were caught from Kepez I hydro-electric power plant loading pond (N 36 o 57' 289, E 30 o 37' 624 ). Fish were collected using seine nets and traps. Maximum depth of the pond is about 10 m,water amount changes between 9 and 20 lt/sec in a year. The fish were dissected immediately after sacrifice. Parasites found in the host were removed using a needle. Monogeneans belonging to genus Dactylogyrus were mounted by flattening and were fixed with glycerinammonium picrate. Permanent preparations of monogeneans were also made in lactophenol or glycerin -gelatine. For Paradiplozoon, the haptor of each specimens *Corresponding author s esoylu@marmara.edu.tr

2 Bull. Eur. Ass. Fish Pathol., 27(1) 2007, 24 was excised and fixed in a mixture of glycerin and ammonium-picrate. Measurements were made using a light microscope according to Simkova et al. (2001) and Khotenovsky (1985). Attachment clamp, central hook sickle and egg of the diplozoid species and sclerotised parts of Dactylogyrus specimens, ovarium and head of cestode are shown in figure. Cestode parasites were fixed in Bouin s fluid under coverslip pressure and then cleared in lithium carbonate, stained with aceto-carmine. All slides were studied with Nikon Diapot 300 microscope and photographs were recorded by Sony CCD Iris color-video camera line. Drawings of the specimens were made from computer screen. Measurements are presented in μm unless otherwise indicated. The following references were used for species determination; Bykhovskaya- Pavlovskaya et al. (1962); Gussev (1985); Markevic (1951); Khotenovsky (1985). Preparation of the slides was made according to Bylund et al. (1980) and Fernando et al. (1972). Results A total of 72 Antalyae ( cm total length) and 58 carpio (23-48 cm) were examined. The list of the parasites found in fish that have been examined together with the data concerning their prevalence and intensity of infestation are given in table 1. Data on the morphology of the parasites are given below. Unless otherwise stated, all measurements are in μm. Figure A.. Dactylogyrus ergensi (Molnar,1964). Small worm, total length 475, width 97. Length of anchor 40, base 35, point 8, inner root 9, outer root 5. Size of connecting bar Total length of copulatory organ 33. Length of vaginal tube 45, diameter 1. Figure B. Dactylogyrus sphyrna (Linstow, 1878). Large worm 1500 long and 200 wide. Length of seventh pair of marginal hooks 43, others Total length of anchor 53-70, inner root 47, outer root 13. Size of connecting bar Length of copulative organ 50-62, length of tube 128, diameter of tube 2. Length of vaginal tube 50, diameter 3. Figure Dactylogyrus extensus (Mueller & Van Cleave, 1932). Large worm, total length 1500, width 300.Total length of anchor Inner root 26-33, outer root Size of connecting bar Total length of copulatory organ Figure D. Paradiplozoon homoion (Bychowsky & Nagibina, 1959). Length of body , anterior part of body , posterior part of body Length width of 3rd clamp Length of median plate 102. Length of central hook sickle 22. Figure E. Caryophyllaeus laticeps (Annenkova- Khlopina, 1919). Body unsegmented, sexually mature specimens are about mm long and mm wide. Vitellaria extends between cephalic end and anterior margin of ovary.testes lying in three longitudinal rows. Cirral bursa Seminal receptacle occurs above bridge of ovary. Ovary H shaped, eggs oval Discussion A total of five parasite species were recorded in antalyae and carpio from Kepez I

3 Bull. Eur. Ass. Fish Pathol., 27(1) 2007, 25 Figure 1. Sclerotised parts of haptor and reproductive organs A: Dactylogyrus ergensi; B- D: sphyrna; C- D: extensus; D: Paradiplozoon homoion; E: Caryophyllaeus laticeps a: Median hook; b: dorsal connecting bar; c: ventral connecting bar; d: marginal hook; e: male copulatory organ; f: vaginal armour; g: attachment clamp; h: central hook sickle; i: egg k: ovarium; l: head.

4 Bull. Eur. Ass. Fish Pathol., 27(1) 2007, 26 Host Fishes antalyae antalyae antalyae carpio carpio carpio Parasite species No. of fish infected Prevalence % Intensity range Mean intensity ±SE D. sphyrna ±0. 5 D. ergensi ±1.09 homoion ±0.47 D. extensus ±2.49 homoion laticeps ±0.43 Table 1. Parasites of Pseudophoxinus antalyae (n=72) and Cyprinus carpio (n=58). hydroelectric power plant loading pond. The parasites of Clarias lazera and Carassius carassius have been studied from this pond (Soylu & Emre, 2005). All parasites found in antalyae were monogeneans, two species belonging to Dactylogyrus genus and one species belonging to Diplozoidae family. Most monogeneans typically parasitize gills of fish. When monogeneans occur in small numbers they produce little effect upon the host, when they attain high infection levels, in overcrowded host population like fishponds, they are usually pathogenic (Chapman et al., 2000). In the present study Paradiplozoon homoion was found to be a common parasite of antalyae. Only one specimen of homoion was found on the gills of carpio and should be regarded as an accidental infection. Adult specimen of homoion was found in all months studied from antalyae..paradiplozoon homoion was found in maximum 15 specimens from one individual fish. Parasites into post oncomiracidial stage (diporpa) and juvenile (two diporpa fuse together and form larval stage) were found. Öztürk (2000) recorded homoion on the gills of Rutilus rutilus in Manyas Lake, Aydogdu et al. (2001b) found megan on Leuciscus cephalus as diplozoid in Dogancý dam lake in Bursa. Diplozoids are large bodied monogeneans. Eudiplozoon nipponicum and Diplozoon paradoxum are widely known in parasitology (Matejusova et al., 2002). There are 60 species of diplozoids described to date, of which 15 were recorded in Europe (Khotenovsky, 1985). For species identification of diplozoids five measurements of third pair of clamps and length of central hook sickle are important characters. However, the length of the median plate of the third pair of clamps is more stable for species identification of diplozoids than the length or width of the clamps (Matejusova et al., 2002). Water temperature, host size and geographical origin has been implicated in morphometrical variability of monogenean parasites. In the present study Dactylogyrus sphyrna were found rarely on the gills of 2 of 72 examined antalyae. Dactylogyrus sphyrna were recorded by some investigators in Marmara region including from Rutilus rutilus and Blicca bjoerkna (Soylu, 1991), from B. Bjoerkna (Öztürk, 2000) and from Vimba vimba (Uzunay & Soylu, 2006). Dactylogyrus extensus was found to be the second most common parasite of carpio with 23.6 % prevalence. Oguz et al. (1996),

5 Bull. Eur. Ass. Fish Pathol., 27(1) 2007, 27 Öztürk (2000) and Uzunay & Soylu (2006) recorded D. extensus from carpio in Uluabat, Manyas and Sapanca Lake respectively. Dactylogyrus ergensi is a typical monogenean for Chondrostoma nasus (Gussev, 1985; Simkova et al., 2004). Dactylogyrus ergensi was recorded on the gills of Leuciscus cephalus by Galli et al. (2002). In the present study, small form of D. ergensi was found. Dactylogyrus ergensi is closely related to D. dirigerus, although subtle morphological differences do occur. Dactylogyrus ergensi is the first record of Turkey and antalyae is a new host for this monogenean. Caryophyllaeus laticeps was found in the intestine of carpio with 48.2 % prevalence as dominant parasite. Caryophyllaeus laticeps was recorded in common carp from Dalyan Lagoon, Karacabey by Aydogdu et al. (2001a), from Manyas Lake in V. vimba by Öztürk & Altunel (2001) from Iznik Lake in R. frisii by Aydogdu et al. (1997) from Sapanca Lake in V. vimba. and carpio by Uzunay & Soylu (2006). In conclusion the present study is the first for parasites of antalyae, and the parasities found on antalyae are new records for helminth fauna of Turkey. At the same time, D. ergensi is a new record for Turkey. There was no risk related to epidemic level of values of parasite species except homoion on antalyae. Acknowledgements The authors are grateful to Dr. Iveta Matejusova for confirming the identification of homoion by analysis of the ITS2 rrna sequences. References Aydogdu A, Yildirimhan HS & Altunel FN (1997). An investigation on the helminth fauna of Rutilus frisii caught from Lake Iznik. IX: National Fisheries Symposium, September 17-19, (in Turkish). Aydogdu A, Öztürk MO, Oguz CM, & Altunel NF (2001a). Investigation on metazoon parasites of the common carp (Cyprinus carpio L.1758) in Dalyan Lagoon, Karacabey,Turkey. Acta Veteriharia 51, Aydogdu A, Altunel FN & Yildirimhan HS (2001b). Occurence of helminths in chub, Leuciscus cephalus of the Dogancý Dam Lake (Bursa), Turkey. Bulletin of the European Association of Fish Pathologists 21, Aydogdu A & Altunel FN (2002). Helminths found in some fishes from the Doganci Dam Lake (Bursa). Turkish Journal of Parasitology 26, Bykhovskaya-Pavlovskaya IE, GussevAV, Dubinina MN, Izyumov NA, Simirnova TS, Sokolovskaya IL, Shtein GA, Shulman SS & Epshtein VM (1962). Key to parasites of freshwater fish of the USSR. Izdatelstvi Akademi Nauk SSSR. Moskva Leningrad. (Translated from Russian, Israel Program for Scientific Translation, Jerusalem). Bylund G, Fagerholm HP, Calenius G, Wikgren BJ & Wikstöm M (1980). Parasites of Fish in Finland II. Methods for studying fauna in fish. Acta Academia Aboensis Series B 40, 23 pp. Cengizler I, Aytaç N, Sahan AA, Ozak AA & Genç E (2001). Ecto-Endo Parasite Investigation on Mirror Carp (Cyprinus carpio L.,1758). Captured From the River Seyhan, Turkey. Journal of Fisheries and Aquatic Sciences 18, Chapman LJ, Lanciani CA & Chapman CA(2000). Ecology of a diplozoon parasite on the gills of the African cyprinid Barbus neumayeri. African Journal of Ecology 38,

6 Bull. Eur. Ass. Fish Pathol., 27(1) 2007, 28 Fernando CH, Furdat JI, Gussev AV, Hanek G & Kakonge SA (1972). Methods for the study of fish parasites. University of Waterloo Biology Series pp.76. Galli P, Stefani F, Zaccara S & Crosa G (2002). Occurence of Monogenea in Italian freshwater fish (Po river basin). Parasitologia 44, Gussev AV(1985). Key to the parasites of the freshwater fish fauna of the USSR II, Vol.143 Parasitic Monogeneans (ON Bauer, Ed) Izdat Nauka, Leningrad pp.424,. Khotenovsky IA (1985). The subclass Octomacrinea Khotenovsky. In Key to the parasites of the freshwater fish fauna of the USSR II, Vol.143 Parasitic Monogeneans (O.N. Bauer, Ed.) pp.424, Izdat Nauka, Leningrad. Markevic AP (1951). Parasitic fauna of freshwater fish of the Ukrainian SSR. Oldbourne Press.121, Fleet Street, London, 388 pp. Matejusova I, Koubkova B, Gelnar M & Cunningham CO (2002). Paradiplozoon homoion Bychovsky and Nagibina, 1959 versus gracile Reichenbach-Klike, 1961 (Monogenea): two species or phenotypic plasticity? Systematic Parasitology 53, Oguz MC (1991). An investigation on ectoparasite of carp (Cyprinus carpio,l.) in some freshwater from Bursa region (Kocadere-Ekinli-Uluabat). Acta Parasitologica Turcica 15, (in Turkish). Oguz MC, Öztürk MO, Altunel FN & Ay YD (1996). Parasitological investigation on carp (Cyprinus carpio L.) caught in Lake Uluabat. Turkish Journal of Parasitology 20, Özer A & Erdem O(1998). Ectoparasitic protozoa fauna of the common carp (Cyprinus carpio L.,1758) caught in the Sinop region of Turkey. Journal of Natural History 32, Özer A & Erdem O (1999). The relationship between occurence of ectoparasites, temperature and culture conditions: a comparison of farmed and wild common carp (Cyprinus carpio L.,1758) in the Sinop region of northern Turkey. Journal of Natural History 33, Öztürk MO (2000) Helminth fauna of fishes in Lake Manyas (Kuþ). Uludag University, Institute in Pure and Applied Sciences. PhD. Thesis. 133pp.Bursa. Öztürk MO & Altunel FN (2001). The occurence of cestodes in four species (Blicca bjoerkna, Rutilus rutilus, Scardinius erythrophthalmus, Vimba vimba) of Cyprinidae from Manyas Lake. Ankara University, Journal of Veterinary Faculty 48, Simkova A, Desdevises Y, Gelnar M & Morand S (2001). Morphometric correlates of host specificity in Dactylogyrus species (Monogenea) parasites of European Cyprinid. Fish Parasitology 123, Simkova A, Morand S, Jebet E, Gelnar M & Verneau, O (2004). Molecular phylogeny of Congeneric monogenean parasites (Dactylogyrus): A case of intrahost speciation. Evolution 58, Soylu E (1991). Monogeneans of some fishes from Lake Sapanca.Ýstanbul University, Institute of Marine Sciences and Geography Bulletin 8, Soylu E & Emre Y (2005). Metazoan parasites of Claria lazera Valenciennes, 1840 and Carassius carassius (Linnaeus,1758) from Kepez I Hydro Electric Power Plant Loading Pond Antalya. Turkish Journal of Fisheries and Aquatic Sciences 5, Uzunay E & Soylu E (2006). Metazoan parasites of carp (Cyprinus carpio Linnaeus 1758) and vimba (Vimba vimba Linnaeus,1758) in the Lake Sapanca. Acta Parasitologica Turcica 30,

OCCURRENCE OF DACTYLOGYRUS INFECTION LINKED TO SEASONAL CHANGES AND HOST FISH SIZE ON FOUR CYPRINID FISHES IN LAKE MANYAS, TURKEY

Acta Zoologica Academiae Scientiarum Hungaricae 52 (4), pp. 407 415, 2006 OCCURRENCE OF DACTYLOGYRUS INFECTION LINKED TO SEASONAL CHANGES AND HOST FISH SIZE ON FOUR CYPRINID FISHES IN LAKE MANYAS, TURKEY