Bull. Eur. Ass. Fish Pathol., 34(1) 2014, 5

Occurrence of spp. (Diplostomidae) in some fish from Ömerli Dam Lake, İstanbul, Turkey

F. Kırcalar1* and E. Soylu2

1Fisheries Department, Institute for Graduate Studies in Pure and Applied Sciences, Marmara University, Göztepe, TR-34722 Kadıköy, Istanbul, Turkey; 2Fisheries Department, Vocational School of Technical Sciences, Marmara University, Göztepe, TR-34722 Kadıköy, Istanbul, Turkey

Abstract Occurrence and infection dynamics of Diplostomum spp. in the lens of the eyes of bleak Alburnus istanbulensis, Prussian carp Carassius gibelio, chub Squalius cephalus, rudd Scardinius erythrophthal- mus and vimba bream Vimba vimba were studied at monthly intervals. The study was performed between May 2012 and January 2013. In total; 17 A. istanbulensis, 88 C. gibelio, 62 S. cephalus, 19 S. erythrophthalmus and 71 V. vimba specimens were examined. The overall parasite prevalence and mean intensity (MI) respectively for the fish species were;A. istanbulensis, 82.4%, 6.8(MI), C. gibelio 43.2%, 3.4(MI), S. cephalus 62.9%, 6.4(MI), S. erythrophthalmus 15.8%, 1.0(MI) and V. vimba 97.2%, 45.8(MI). The results show that highest prevalence and mean intensity of infection was recorded in V. vimba. Conversely, S. erythrophthalmus has lowest infection rates. Generally, prevalence of the infection was found higher during late summer and early fall.

Introduction Digenean ‘eye fluke’ metacercariae ofDiplostomum above 10oC (Wootten, 1974; Dwyer and Smith, spp. are commonly found in many freshwater 1989). The cercariae penetrate the skin of a fish fish species. The flukes use fish eating birds and migrate to the eye lenses and establish as as definitive hosts, where sexual reproducti- metacercariae (Stables and Chappell, 1986). on takes place (Seppala et al., 2012). Parasite Metacercariae may cause parasitic cataract, eggs are released in water with birds feces, and poor growth, emaciation, cranial deformation develops into free-swimming miracidia. The and mortality both in wild and farmed fish miracidium penetrate a snail and developes (Shariff et al., 1980). The seasonal occurrence into a mother sporocyst, which reproduces of fish trematodes is primarily determined by asexually to produce daughter sporocysts. Each temperature (Chubb, 1979). Diplostomum spp. of these then reproduces asexually to produce metacercariae have been recorded in over 150 several cercariae, which are free-swimming fresh and brackish water fish (Niewiadomska, infective stages released from the snail host 1996). Studies on Diplostomum species in Turkey (Marcogliese et al., 2001). The cercariae emerges are few. Dörücü et al., (2002) studied the oc- from snail into the water only at temperature currence of Diplostomum sp. in

* Corresponding author’s e-mail: [email protected] 6, Bull. Eur. Ass. Fish Pathol., 34(1) 2014 marmid from Keban Dam Lake, and Turgut 62.7 ± 32.8 g (range 23.1-196.3 g) specimens and Özgül (2012) studied seasonal occurrence were collected in the gill nets with 15 mm mesh of Diplostomum sp. in some cyprinid fish from size or by electrofishing. Fish specimens were Almus Dam Lake. The main aim of the present transferred to the laboratory alive in lake water. study was to determine the occurrence and The fish was anaesthetized in MS-222 and the infection dynamics of Diplostomum spp. in the spinal cord was cut. Then the fish was weighed lens of the eyes of bleak Alburnus istanbulensis, to the nearest 0.1 gram and total length was Prussian carp Carassius gibelio, chub Squalius measured to the nearest 0.1 centimeter. The cephalus, rudd Scardinius erythrophthalmus and sex was determined by observing the testes or vimba bream Vimba vimba in the mesothrophic ovaries. Numbers of Diplostomum spp. meta- Ömerli Dam Lake. cercariae were recorded from both eyes of the fish when disected under a stereo-microscope Materials and methods at 10X and 25X magnification.Prevalence and The study was performed between May 2012 mean intensity were calculated according to and January 2013 in Ömerli Dam Lake near Margolis et al. (1982). Istanbul (Latitude 41°02′N, Longitude 29°22′E). In total, 17 A. istanbulensis of mean (± SD) total Results length 19.8 ± 3.2 cm (range 12.8-27.8 cm) and The highest overall prevalence of Diplostomum mean (± SD) weight 90.6 ± 36.2 g (range 38-169.6 spp. was found as 97.2% in V. vimba. The second g), 88 C. gibelio of mean (± SD) total length 17.2 highest value was 82.4% in A. istanbulensis and ± 3.7 cm (range 9.7-28.5 cm) and mean (± SD) the third highest value was 62.9% in S. cephalus. weight 122.9 ± 116.3 g (range 21.7-465.1 g), 62 The lowest prevalences were 43.2% in C. gibelio S. cephalus of mean (± SD) total length 19.5 ± and 15.8% in S. eryththrophthalmus. Mean inten- 2.34 cm (range 15.9-28.9 cm) and mean (± SD) sity of Diplostomum spp. was much higher in weight 100.7 ± 55.9 g (range 46.8-295.7 g), 19 S. V. vimba with 45.8 individual parasite per fish erythrophthalmus of mean (± SD) total length 19 than in the other fish species. In parallel with ± 3.1 cm (range 13.3-24.5 cm) and mean (± SD) lowest prevalence, the lowest mean intensity weight 79.2 ± 27 g (range 36.1-129 g) and 71 V. (1.0) of Diplostomum spp. was found in S. ery- vimba of mean (± SD) total length 17.3 ± 2.3 cm ththrophthalmus . The infection parameters of (range 14.6-28.1 cm) and mean (± SD) weight the fish species are shown in Table 1.

Table 1. Infection parameters of the fish species.

Fish Species Prevalence % Mean Intensity Mean Abundance Alburnus istanbulensis 82.4 6.8 5.6 Carassius gibelio 43.2 3.4 1.5 Squalius cephalus 63 6.4 4 Scardinius eryththrophthalmus 15.8 1 0.2 Vimba vimba 97.2 45.8 44.5 Bull. Eur. Ass. Fish Pathol., 34(1) 2014, 7

Table 2. Seasonal prevalence of Diplostomum spp.

Fish Species Spring Summer Autumn Winter Alburnus istanbulensis 50 100 75 87.5 Carassius gibelio 33.3 39.1 55.6 55.6 Squalius cephalus NF 62.2 75 100 Scardinius eryththrophthalmus 25 0 0 NF Vimba vimba 100 NF 97.3 97 (NF) No fish caught

In general the prevalence of Diplostomum spp. Discussion increased from spring to winter in all fish The highest infection rate of Diplostomum spp. species examined (Table 2). was recorded in V. vimba and lowest rate in S. erythrophthalmus. In the case of the occurrence Infection parameters of Diplostomum spp. in of Diplostomum spp. in the fish species from relation to the size classes (cm) were given for Ömerli Dam Lake, we especially compared the three most caught fish species. Prevalence two fish species with different feeding habits. of Diplostomum spp. in V. vimba were found high in all size classes but mean intensities were V. vimba feeds mostly near the bottom and higher in larger size classes. Prevalence and thus,are in close contact with snails which are mean intensity of Diplostomum spp. according the first intermediate host ofDiplostomum spp. S. to size classes of V. vimba are shown in Figure 1. erythrophthalmus on the other hand, is a pelagic surface feeder that stays more distant from the The prevalence of Diplostomum spp. in C. gibelio snails. According to Campbell (1997) cercariae increased with size classes. The highest mean of Cotylurus flabelliformis can disperse rapidly intensity was found in 12.1-15.0 cm size class as from snails more than 1 m distant. Cercariae of 9.7 individuals. Infection parameters of Diplos- Diplostomum spp. disperse in pelagial zone, and tomum spp. in C. gibelio in relation to size classes consequently decrease their chance to contact are shown in Figure 2. with S. erythrophthalmus. Marcogliese et al. (2001) observed similar results that white sucker The prevalence of Diplostomum spp. in S. cepha- (Catostomus commersoni) is a benthic consumer lus increased with size classes, the highest mean and more heavily infected with Diplostomum intensity was found in 24.1-27.0 cm size class. spp. than the walleye (Stizostedion vitreum), a Infection parameters of Diplostomum spp. in pelagic piscivore, from Lake St. Louis and Lake S. cephalus according to size classes are shown St. Pierre in Quebec, Canada. in Figure 3. 8, Bull. Eur. Ass. Fish Pathol., 34(1) 2014

Figure 1. Prevalence and mean intensity of Diplostomum spp. in different size classes of Vimba vimba.

Figure 2. Prevalence and mean intensity of Diplostomum spp. in different size classes of Carassius gibelio.

Figure 3. Prevalence and mean intensity of Diplostomum spp. in different size classes of Squalius cephalus. Bull. Eur. Ass. Fish Pathol., 34(1) 2014, 9

Marcogliese DJ, Dumont P, Gendron AD., In summary, Diplostomum spp. was found to be Mailhot Y, Bergeron E and McLaughlin prevalent in all fish species examined. The mean JD (2001). Spatial and temporal variation intensity of Diplostomum spp. in V. vimba and S. in abundance of Diplostomum spp. in cephalus were increased with size classes, while walleye (Stizostedion vitreum) and white suckers (Catostomus commersoni) from the St. in C. gibelio there was no differences of mean Lawrence River. Canadian Journal of Zoology intesity with size classes. The dissimilarity in 79, 355–369. the occurrence of Diplostomum spp. in V. vimba Niewiadomska K (1996). The genus Diplostomum and S. erythrophthalmus depends on different – , morphology and biology. Acta ecological characteristics of these fish species. Parasitologica 41, 55-66. Seppala O, Karvonen A and Valtonen ET Acknowledgements (2012). Behavioural mechanisms underlying The authors thank the anonymous reviewer for ‘specific’ host manipulation by a trophically transmitted parasite. Evolutionary Ecology valuable comments on this paper. This article Research 14, 73–81. was extracted from a Master’s thesis conducted Shariff M, Richards RR, and Sommerville C at Marmara University, Institute for Graduate (1980). The histopathology of acute and Studies in Pure and Applied Sciences. chronic infections of rainbow trout Salmo gairdneri Richardson with eye flukes, References Diplostomum spp.. Journal of Fish Diseases Campbell RA (1997). Host-finding behaviour 3, 455–465. of Cotylurus flabelliformís (: Stables JN and Chappell LH (1986). The Strigeidae) cercariae for snail hosts. Folia epidemiology of diplostomiasis in farmed Parasitologica 44, 199-204. rainbow trout from north-east Scotland. Chubb JC (1979). Seasonal occurrence of Parasitology 92, 699-710. helminths in freshwater fishes Part II. Turgut E and Özgül G (2012). Seasonal changes Trematoda. Advances in Parasitology 17, and host size-dependent variation in 141-313. Diplostomum sp. infection of some cyprinid Dörücü M, Dilsiz N and Grabbe MCJ (2002). fish.Pakistan Journal of Zoology 44, 123-128. Occurrence and effects ofDiplostomum sp. Wootten R (1974). Observations on strigeid ınfection in eyes of Acanthobrama marmid in metacercariae in the eyes of fish from Keban Dam Lake, Elazığ, Turkey. Turkish Hanningfield Reservoir, Essex, England. Journal of Veterinary and Sciences 26, Journal of Helminthology 48, 73-83. 239-243. Dwyer WP and Smith CE (1989). Metacercariae of Diplostomum spathaceum in the eyes of fishes from Yellowstone Lake, Wyoming, Journal of Wildlife Disease 25(1), 126-129. Margolis L, Esch GW, Holmes JC, Kuris AM and Schad GA (1982). The use of ecological terms in parasitology (Report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68, 131-133.