Seasonal changes of metazoan parasites in Capoeta tinca and Capoeta capoeta in Almus Dam Lake, Turkey

Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 23 Seasonal changes of metazoan parasites in Capoeta tinca and Capoeta capoeta in Almus Dam Lake, Turkey E. Turgut 1 *, G. Ozgul 1 and E. Buhan 1 1 Department of Aquaculture, Faculty of Agriculture, Gaziosmanpasa University, Tokat, Turkey Abstract A survey was conducted on seasonal changes of metazoan parasites observed in the fish species Capoeta tinca and Capoeta capoeta. Eight species of parasites were identified. Dactylogyrus narzikulovi, Dactylogyrus crucifer, Gyrodactylus varicorhini (Monogenea), Diplostomum sp. (Digenea), and Molnaria intestinalis (Nematoda) were identified from C. tinca while Dactylogyrus pulcher, Dactylogyrus turkestanicus, Gyrodactylus sp. and Diplostomum sp. were identified from C. capoeta. Significant seasonal differences were found in the abundance of parasites species associated with C. tinca. Significantly higher numbers were observed for Dactylogyrus spp. and G. varicorhini in the summer; Diplostomum sp. was most abundant in the autumn; and M. intestinalis was most commonly observed in the spring samples. However, there was no significant seasonal difference in the mean abundance of parasites associated with C. capoeta. To the best of our knowledge, this is the first report of D. narzikulovi, D. crucifer, D. pulcher, D. turkestanicus and G. varicorhini in Turkish freshwater fish. Introduction Capoeta species are widely distributed in Western Asia including Anatolia, Iran, Northern India, Pakistan and Turkmenistan (Geldiay and Balık, 1996). Although these species are widely distributed in this region, there are few studies on their parasitic fauna in the former USSR states (Gussev, 1985), Iran (Coad, 2009) or Turkey (Dorucu et al., 2002; Oktener, 2003; Dorucu and Ispir., 2005; Aksoy et al., 2006). In Turkey, investigations of the parasitic fauna of Capoeta species have mainly been conducted in Capoeta tru a and Capoeta capoeta umbla from the Keban Dam Lake on the Euphrates River in southeastern Turkey (Dorucu et al., 2002; Dorucu and Ispir, 2005; Aksoy et al., 2006). Li le is known about the parasitic fauna in other regions and no work has been done on the seasonal population dynamics of parasites of these species. There are no studies on parasites of Capoeta species in the Yesilırmak River Basin in the Tokat region. Therefore, the objective of the present study is to present the seasonal occurrence of the parasite fauna of C. capoeta (Transcaucasian Barb) and C. tinca (Anatolian khramulya) in the Almus Dam Lake in the Yesilırmak River, Turkey. * Corresponding author s e-mail: emineturgut5@yahoo.com

Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 24 Material and methods The study was conducted in Almus Dam Lake (40 22 348 N - 36 55 789 E), 34 km from the city of Tokat, Turkey. Almus Dam Lake is on the main branch of the Yesilırmak River and an important reservoir in the northern Anatolian region. Sampling was carried out on a three monthly basis from April 2005 to January 2006. Specimens of C. tinca and C. capoeta were collected using a seine net. A total of 67 C. tinca and 19 C. capoeta were studied. During the winter months no fish were sampled due to low water temperature (4.0 ±0.9 C). The number of fish sampled seasonally is shown in Table 1. Seasonal ranges and means for water temperature ( C) and ph levels were recorded using WTW Multi 340I / SET during the study. Fish weighted 105.0± 189.7 gr and measured 20.1± 9.1 cm for C. tinca and weighted 175.6± 96.0 gr and measured 24.7± 6.1 cm for C. capoeta. For parasitological dissection, fish were killed, and a er all necessary data was recorded, (total length and weight) the fish were examined. Routine procedures were used to collect and process parasites. Descriptive morphometric measurements of parasites are taken for identification of parasites and compared with previously published data using the terminology and style of Gussev (1985) and Moravec (1995). The prevalence and mean intensity levels of the parasite species were determined according to Bush et al. (1997). A Kruskal-Wallis analysis of variance was applied to the data to determine significant differences in the mean abundance of the parasite species. All statistical analyses were performed using the statistical program SPSS 15.0. Results A total of 8 parasite species were identified from C. tinca and C. capoeta. These were the monogenean parasites Dactylogyrus narzikulovi, Dactylogyrus crucifer, Gyrodactylus varicorhini; a digenean parasite Diplostomum sp. and the intestinal nematode Molnaria intestinalis in C. tinca and Dactylogyrus pulcher, Dactylogyrus turkestanicus, Gyrodactylus sp. and Diplostomum sp. in C. capoeta (Table 1). Because of mixed infection of D. crucifer and D. narzikulovi on C. tinca and D. pulcher and D. turkestanicus on C. capoeta, it was not possible to separately determine the seasonal variation in prevalence and intensity of these Dactylogyrus species. However, this is the first time D. narzikulovi, D. crucifer, D. pulcher, D. turkestanicus and G. varicorhini have been reported from Turkish freshwater fish. Prevalence levels of G. varicorhini and Dactylogyrus spp. in C. tinca were generally higher in the summer (51.7 % and 82.7 %, respectively) compared to the spring (25.0 %, 50.0 %) and the autumn (16.0 %, 36.0 %). Prevalence level of Diplostomum sp. was higher in the autumn (64.0 %) and decreased in the spring (50.0 %) and the summer (24.1 %) and the prevalence of M. intestinalis was higher in the spring (25.0 %) compared to the summer (6.8 %) but was not found in the autumn (Table 1). Seasonal changes in mean abundance followed in general the seasonal changes in prevalence for the parasite species in C. tinca (Figure 1b and Figure 2b). Significant differences were found between the seasons in mean abundance. The abundance of Dactylogyrus spp. were significantly higher in the summer (53.8 parasites/fish) than during the spring (35.0 parasites/fish) and the autumn (3.4 parasites/fish). G. varicorhini

Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 25 Table 1. Seasonal changes in prevalence and mean abundance of parasites from Capoeta tinca and Capoeta capoeta. Parasite species Spring (n=12) Summer (n=29) Autumn (n=26) Mean abundance Capoeta tinca Prevalence (%) Prevalence (%) (± Sd) Mean abundance (± Sd) Prevalence (%) Mean abundance (± Sd) Dactylogyrus narzikulovi and Dactylogyrus crucifer 50.0 35.0± 11.4 a 82.7 53.8±23.6 b 36.0 3.4±2.9 a Gyrodactylus varicorhini 25.0 3.3±1.5 ab 51.7 9.8±7.7 b 16.0 3.7±0.9 a Diplostomum sp. 50.0 4.8±2.3 a 24.1 2.7±1.2 b 64.0 7.4±8.6 a Molnaria intestinalis 25.0 60.6±31.9 b 6.8 1.5±0.7 ab - - Overall 83.3 23.9±25.4 ab 86.0 29.6±28.8 a 88.0 5.7±6.8 b Capoeta capoeta n=4 n= 6 n=9 Dactylogyrus pulcher and Dactylogyrus turkestanicus 50.0 6.0±1.4 a 50.0 15.0±7 a 55.5 10.2±10.2 a Gyrodactylus sp. 25.0 5.0±0 a 16.7 2.0± a 22.2 2.0±0 a Diplostomum sp. 50.0 3.0±0 a 16.7 2.0± a 66.6 5.5±2.7 a Overall 75.0 4.6±1.7 a b 50.0 9.8±8.6 a 88.0 7.1±7.0 b Water temperature 10.6 C (10.5-10.8) 21.3 C (20.5-22.5) 17.1 C (11.5-22.8) ph 8.6 8.5 8.3 Values with the same superscript le er are not significantly different (P<0.05)

Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 26 a b Figure 1. Seasonal changes in prevalence (a) and abundance (b) of parasite species in the Capoeta tinca in Almus Dam Lake. also showed significantly higher abundance in the summer (9.8 parasites/fish) than in the autumn (3.7 parasites/fish). Diplostomum sp. was significantly higher in the autumn (7.4 parasites/ fish) than in the summer (2.7 parasites/fish). M. intestinalis was significantly higher in the spring (60.6 parasites/fish) than in the summer (1.5 parasites/fish). Seasonal changes in the prevalence of the parasite species in C. capoeta showed different results compared to the parasites in C. tinca

Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 27 a b Figure 2. Seasonal changes in prevalance (a) and abundance (b) of parasite species from Capoeta capoeta in Almus Dam Lake. for Dactylogyrus spp. and Gyrodactylus sp. This might be because the lower number of C. capoeta compared to the number of C. tinca sampled throughout the year. The highest prevalence of Dactylogyrus spp. was seen during the autumn (55.5 %) and lower in the spring and the summer (50.0 %). The prevalence of Gyrodactylus sp. was highest in spring (25%) followed by the autumn (22.2 %) and the summer (16.7 %). Diplostomum sp. showed the highest prevalence in the autumn (66.6 %) and lower in the spring and summer such as in C. tinca (Figure 2a).

Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 28 No significant seasonal differences in the mean abundance of parasites infecting C. capoeta were detected. However, there was higher mean abundance of Dactylogyrus spp. (15 parasites/ fish) in the summer followed by the autumn (10.2 parasites/fish) and the spring (6.0 parasite/ fish). Mean abundance of Gyrodactylus sp. was highest in the spring (5 parasite/fish) and lower in the summer and the autumn (2.0 parasites/ fish). Further, the abundance of Diplostomum sp was highest in the autumn (5.5 parasites/fish) and lower in the spring (3.0 parasites/fish) and the summer (2.0 parasites/fish). Discussion In the present study, parasitic fauna of C. tinca and C. capoeta of freshwater fish from Turkish Almus Dam Lake were investigated. Five monogenean species were found to be new Turkish records. These are D. narzikulovi, D. crucifer and G. varicorhini from C. tinca, and D. pulcher and D. turkestanicus from C. capoeta. Furthermore, M. intestinalis from C. tinca and Gyrodactylus sp. from C. capoeta, and Diplostomum sp. from both fish species were also identified. Adding these records to the existing list, the number of species in the Turkish metazoan parasites of Capoeta species has risen to 25. D. pulcher was previously recorded from C. capoeta, C. tru a and Varicorhinus capoeta gracilis from former USSR and Iranian freshwater (Gussev, 1985; Pazouki et al., 2006). C. tinca seems to be new host record for D. crucifer and G. varicorhini as D. crucifer has been recorded from Cyprinus carpio, Blicca bjoerkna, Rutilis rutilis and Alburnus alburnus and G. varicorhini from Varicorhinus capoeta (Gussev, 1985; Coad, 2009), Seasonal changes in the population size of parasites may be the result of various factors such as water temperature, parasite and host physiology, host hormonal status, host migration and host immunological response (Hanzelova and Zitnan, 1985; Simkova et al., 2005). Seasonality was also observed in the present study. Although, Dactylogyrus spp. and Gyrodactylus sp. from C. tinca showed highest prevalence and abundance during summer. However, there was no significant seasonal difference of Dactylogyrus spp. and Gyrodactylus sp. from C. capoeta which may be due to the inadequate number of fish sampled. It is also reported that fish are more susceptible to parasite infection in periods of reproduction and also higher reproductive investment (Buchmann, 1997; Simkova et al., 2005). Dactylogyrus populations, especially, o en peaked in spring and early summer, at the same time as many of their freshwater fish hosts spawn (Hanzelova and Zitnan, 1985; Buchmann, 1997; Öztürk and Altunel, 2006). This study found that the intensity of Dactylogyrus and Gyrodactylus infections increased in spring when the water temperature began to rise and was highest during summer when the water temperature peaked (22.5 C). This corresponds with the reproduction period for C. capoeta which is from May to August in Turkey (Elp and Karabatak, 2007). Besides the ectoparasitic monogenean species found on C. capoeta and C. tinca, there were also Diplostomum sp. from both fish and M. intestinalis were only identified from C. tinca. Dorucu et al. (2002) reported that the highest infection of Diplostomum sp. from Acanthobrama marmid in Keban Dam Lake occurs during the spring

Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 29 and the autumn while the prevalence and abundance decreased in the summer months. Our results showed similar pa erns. Diplostomum sp. from C. tinca and C. capoeta was highest in the autumn and the spring compared to the summer. Karvonen et al. (2006) also suggested that population dynamics of Diplostomum sp. may also be influenced by the size of the bird population at fish farms. The bird population on Almus Lake is usually highest in spring and late autumn and decreases during summer (personal observations). The seasonal prevalence and abundance of M. intestinalis was highest in the spring and decreased in the summer and there was no infection observed in the autumn. Kılınçaslan (2007) and Dal (2006) reported M. intestinalis from Leuciscus cephalus from Kayseri and from Leuciscus lepidus in Atatürk Dam Lake, Turkey, respectively. Simkova et al. (2005) suggest that B. barbatula is more susceptible to nematode Raphidascaris acus infection during spawning period and also parasite infection may also be affected with change in food composition in different seasons. Knowledge of parasite requirements is important in the development of suitable preventative and control measures, capable of minimizing or eliminating problematic species. Particularly in aquaculture such information may indicate the risks inherent in the introduction and establishment of parasites into new geographical regions and thus provide fishery scientists and legislators with the means to make proper assessments of potential dangers. Acknowledgement This work was supported by Gaziosmanpasa University with a BAP Project no: 2004/12. References Aksoy S, Saglam N and Dorucu M (2006). External parasites of three Cyprinid fish species from lake Hazar in Turkey. Indian Veterinary Journal 83, 100-101. Buchmann K (1997). Population increase of Gyrodactylus derjavini on rainbow trout induced by testosterone treatment of the host. Diseases of Aquatic Organisms 30, 145-150. Bush AO, Lafferty KD, Lotz JM and Shostak AW (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575 583. Coad BW (2009) Freshwater Fishes of Iran. Species Accounts - Cyprinidae Capoeta. URL: http://www.briancoad.com/ species%20accounts/capoeta.htm. Dal A (2006). Parasitological research on rainbow trout (Oncorhynchus mykiss) farming in Atatürk Dam Lake in Adıyaman City. MSc thesis, Çukurova University. Dorucu M and Ispir U (2005). A study on Endoparasites of some fish species caught in Keban Dam Lake. Journal of Science Faculty 17(2), 400-404. Dorucu M, Dilsiz N and Grabbe MJC (2002). Occurrence and effects of Diplostomum sp. infection in eyes of Acanthobrama marmid in Keban Dam Lake, Elazığ, Turkey. Turkish Journal of Veterinary and Animal Sciences 26(2), 239-243. Elp M and Karabatak M (2007). A study on Capoeta capoeta (Guldenstaedt, 1772) population living in Kockopru Dam Lake; Van, Turkey. Journal of Applied and Biological Science 1(2), 57-61. Geldiay R and Balik S (1996). Fresh water fish of Turkey. Ege University Aquaculture Faculty Publication No: 46, Ege University Press,

Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 30 Izmir. Gussev AV (1985). Parasitic metazoans. Class Monogenea. In: Bauer O. N (Ed) Key to the parasites of freshwater fishes of the USSR. Volume 2. Akademiya Nauka SSR, Leningrad, pp. 10-353. Hanzelova V and Zitnan R (1985). Epizootiologic importance of the concurrent monogenean invasion in carp. Helminthologia 22, 277-283. Karvonen A, Savolainen M and Seppala O (2006). Dynamic of Diplostomum spathaceum infection in snail hosts at a fish farm. Parasitology Research 99, 341-345. Kılınçaslan MO (2007). Parasitological research on economic fishes in Yamula Dam Lake. MSc thesis, Çukurova University, Turkey. Moravec F (1995). Parasitic Nematodes of freshwater fishes of Europe. Kluwer academic Publisher. Oktener A (2003). A checklist of metazoan parasites recorded in freshwater fish from Turkey. Zootaxa 394, 1-28. Öztürk MO and Altunel FN (2006). Occurrence of Dactylogyrus infection lined to seasonal changes and host size on four Cyprinid fishes in lake Manyas, Turkey. Acta Zoologica Academia Scientiarium Hungarica 52(4), 407-415. Pazouki J, Ghobadian M and Jalali JB (2006). Monogenean species from freshwater fishes in Zanjan province, Iran. Iranian Journal of fisheries Sciences 6, 103-112. Simkova A, Jarkovsky J, Koubkova B, Barus V and Prokes M (2005). Associations between fish reproductive cycle and the dynamics of metazoan parasite infection. Parasitology Research 95, 65-72.