Turkish Journal of Zoology Turk J Zool (2013) 37: 441-448 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1205-4

Monogeneans of near Gökçeada,

Ahmet AKMIRZA* Department of Aquaculture, Faculty of Fisheries, İstanbul University, İstanbul, Turkey

Received: 04.05.2012 Accepted: 04.02.2013 Published Online: 24.06.2013 Printed: 24.07.2013

Abstract: In this study, performed in April, July, September, and October 2011 and January 2012 in the northeastern Aegean Sea near Gökçeada in Turkey, 14 of monogenean trematodes (Anthocotyle merlucci, Kuhnia scombri, Mazocraes alosae, Plectanocotyle gurnardi, Choricotyle chrysophrii, trachuri, Amphibdella torpedinis, Bivagina alcedinis, Aspinatrium trachini, Microcotyle erythrini, Atrispinum acarne, Atrispinum salpae, Atrispinum seminalis, and Zeuxapta seriolae) were found in a total of 64 fish samples from 17 fish species (Merluccius merluccius, Trigla lucerna, Lichia amia, Alosa fallax, Trachurus mediterraneus, , Diplodus annularis, Diplodus vulgaris, Pagellus acerna, Pagellus erythrinus, Salpa salpa, Spondyliosoma cantharus, Spicara flexuosa, Sphyraena sphyraena, Trachinus araneus, Scomber japonicus, and Torpedo marmorata) among a total of 721 fish samples from 49 fish species. Amphibdella torpedinis, Bivagina alcedinis, Atrispinum spp., and Zeuxapta seriolae are new records for the study area and Turkey.

Key words: , Trematoda, fish parasites, fish of Gökçeada

1. Introduction 2. Materials and methods Monogenean trematodes belong to one of the most species- The fish samples were caught using various fishing rich classes of fish parasites. They are commonly found on methods such as trawl, gillnet, longline, and vertical fish gills and skin. High abundance of monogeneans may longline near Gökçeada in the northeastern Aegean Sea lead to significant fish mortality as a consequence of tissue in Turkey in April, July, September, and October 2011 damage, respiratory distress, and secondary bacterial and and in January 2012. Fish samples were transported to fungal infections. Many of their biological and ecological the laboratory in aerated tanks and were kept alive until traits (monoxeny, rapid reproduction, hermaphroditism) dissection and parasitological investigation. Fish samples enable them to cause serious damage in both wild species were identified according to Ekingen (2004) and Daniel et and farmed stocks (Dezfuli et al., 2007; Lia et al., 2007; al. (2006). In total, 721 fish specimens were investigated Strona et al., 2010). for monogenean trematodes. Gills were removed and Monogeneans have very high host specificity and, placed in separate petri dishes containing seawater, and hence, host specificity has often been used to estimate they were examined for monogenean parasites under a monogenean species richness as a function of fish stereomicroscope. Monogeneans were removed from the biodiversity. Monogeneans are also very suitable for gills and transferred to petri dishes containing filtered mathematical modeling in ecology (Whittington, 1998). The waters off Gökçeada are characterized by high fish seawater. Live parasites were slightly compressed between species richness. While Ulutürk (1987) reported 144 fish a slide and a cover slip prior to being examined under a species from 60 families near Gökçeada, Keskin and Ünsal light microscope. Microphotographs were taken. Some (1998) detected 76 fish species. Many of these fish species parasites were immediately mounted in glycerin jelly, have commercial value and play an important role in while others were placed in 70% ethanol solution prior Turkish fisheries. Some monogeneans such as Choricotyle to being fixed on slides. Measurements were taken on chrysophrii, , Aspinatrium trachini, fixed specimens using an ocular micrometer or BEL view Microcotyle erythrini, Octosoma scombri, Cyclocotyla camera programs. Identification of the parasites was made bellones, and Gastrocotyle trachuri were found in some according to the works of Dawes (1968), Pugachev et al. parasitic studies performed in this area (Akmırza, 1997, (2010), Chisholm and Whittington (1998), Radujkovic 1998, 2003, 2004). and Euzet (1989), and Yamaguti (1963). * Correspondence: [email protected] 441 AKMIRZA / Turk J Zool

3. Results mm long, 0.8–1.3 mm wide. Haptoral clamps arranged In this study, a total of 721 individual fish were investigated symmetrically in 2 diverging rows of 4 each. Terminal for monogenetic parasites, and 14 species of Monogenea haptoral lappet short, with 2 pairs of anchors. were detected in a total of 64 fish samples from 17 fish long, caeca unbranched, extending into the . Testes species. Abundance, prevalence, and mean intensity of the not numerous, postovarian. Genital pore having genital detected monogenean species on their respective hosts are hooklets in semicircular rows. reported in the Table. Microphotographs representative Mazocraes alosae Herman, 1782 (Figure 3) of the monogenean species found in the area of study are Body tapering to either end, middle region of the body shown in Figures 1–12. flattened, 4–7 mm long, 0.8–1.3 mm wide. Haptor almost Anthocotylidae Price, 1936 triangular, having 4 pairs of clamp-like suckers, 2 pairs Anthocotyle merlucci van Beneden & Hesse, 1863 of anchors on a terminal lappet. Testes numerous, filling (Figure 1) the region between the caeca in the posterior half of the Body symmetrical, tapering anteriorly, with maximum body. Ovary elongate, in front of the testes. Genital pore breadth just in front of the haptor, 4–8 mm long, 0.5–1 mm elongate, with hooklets. wide, haptor with 4 pairs of clamps; the clamps of anterior Plectanocotylidae Monticelli, 1903 pair having a very large dorsal and a ventral valve, small Plectanocotyle gurnardi (van Beneden & Hesse, 1863) clamps are like a short peduncle and a terminal lappet, (Figure 4) bearing 3 pairs of anchors. Testes numerous, confined Body tapering to anterior end, elongate, 1.5–2.5 mm between intestinal caeca in the posterior half of body. long. Haptor symmetrically bearing 3 pairs of clamps on Ovary medium, tubular, located in front of the testes. a short peduncle, terminal lappet with 3 pairs of anchors. Vitellaria extending laterally along the intestine. Ovary lopped, elongated and curved. Testes numerous, Mazocraeidae Price, 1936 postovarian. Kuhnia scombri (Sproston, 1945) (Figure 2) Diclidophoridae Cerfontaine, 1895 Body shape lanceolate, broadest near the midbody, Choricotyle chrysophrii van Beneden & Hesse, 1863 tapering towards the anterior extremity and haptor, 6–9 (Figure 5)

Table. Abundance, prevalence, and mean intensity of the monogeneans found near Gökçeada.

Parasite species Host NEF NIF NP P (%) MI Min–max Merluccius merluccius 9 4 13 44.44 3.25 1–6 Anthocotyle merlucci Sphyraena sphyraena 3 1 2 33.33 2 2 Kuhnia scombri Scomber japonicus 71 11 21 15.49 1.91 1–4 Mazocraes alosae Alosa fallax 6 1 2 16.67 2 2 Plectanocotyle gurnardi Trigla lucerna 7 2 3 28.57 1.5 1–2 Choricotyle chrysophrii Spondyliosoma cantharus 19 1 1 5.26 1 1 Boops boops 49 5 6 10.20 1.2 1–2 Pseudaxine trachuri Trachurus mediterraneus 26 4 8 15.38 2 1–3 Amphibdella torpedinis Torpedo marmorata 7 3 8 42.86 2.67 2–4 Spicara flexuosa 23 5 11 21.74 2.2 1–3 Bivagina alcedinis Spondyliosoma cantharus 19 1 2 5.26 2 2 Aspinatrium trachini Trachinus araneus 9 2 6 22.22 3 2–4 Pagellus erythrinus 12 2 3 16.67 1.5 1–2 Microcotyle erythrini Pagellus acerna 26 2 5 7.69 2.5 2–3 Boops boops 49 1 3 2.04 3 3 Atrispinum acarne Pagellus acerna 26 12 31 46.15 2.58 1–6 Atrispinum salpae Salpa salpa 17 2 7 11.76 3.5 2–5 Diplodus annularis 62 1 2 1.62 2 2 Atrispinum seminalis Diplodus vulgaris 29 3 5 10.34 1.67 1–2 Zeuxapta seriolae Lichia amia 3 1 2 33.33 2 2

NEF: number of examined fish; NIF: number of infested fish; NP: number of parasites; P: prevalence; MI: mean intensity; Min–max: minimum–maximum intensity.

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Figure 1. Anthocotyle merlucci: a) total view; b) anterior part; c) clamps and anchors; d) detail of anchors.

Figure 2. Kuhnia scombri: a) total view; (b) framing of the genital pore; (c) structure of clamp.

Figure 3. Mazocraes alosae: (a) anterior region; b) testes; c) haptor.

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Figure 4. Plectanocotyle gurnardi: a) total view; b) structure of clamp; c) anchor.

Figure 5. Choricotyle chrysophrii: a) total view; b) haptor; c) structure of clamp.

Body fusiform, 4–5 mm long, 1 mm breadth. Haptor Price, 1936 terminal, with 4 pairs of pedunculated clamps. Testes Bivagina alcedinis (Parona & Perugia, 1889) (Figure 8) numerous (~30), postovarian. Ovary folded upon itself. Body lanceolate, 5–6 mm long, 0.9–1.2 mm wide. Price, 1943 Haptor symmetrical with numerous pairs (40–45 pairs) Pseudaxine trachuri Parona & Perugia, 1889 (Figure 6) of similar clamps. Testes not very numerous (8–10 testes), Body 5–6 mm long, 2–2.5 mm wide. Haptor unilateral, postovarian. Vaginal pore double. with a single row of clamps on its oblique lower edge, Aspinatrium trachini Parona & Perugia, 1889 (Figure 9) terminal lappet with one pair of anchors. Cephalic Body 2–5 mm long, 0.6–0.8 mm wide. Haptor region bearing a pair of buccal suckers. Testes numerous, symmetrical with numerous pairs (7–10 pairs) of clamps. postovarian. Ovary U-shaped with unequal arms. Testes numerous (about 20), postovarian. Acanthocotylidae Price, 1936 Microcotyle erythrini van Beneden & Hesse, 1863 Amphibdella torpedinis Chatin, 1874 (Figure 7) (Figure 10) Body elongate and fusiform, 3–5 mm long, 0.6–0.8 mm Body lanceolate, 2–4 mm long, 0.3–0.6 mm wide. wide. Haptor with 2 pairs of large hooks and a single bar. Haptor symmetrical, triangular in profile, with a row of Intestine bifurcate, caeca reaching to the posterior end. numerous small clamps (45–50 clamps on each row). Testes quite elongate longitudinally, postovarian. Ovary About 16–20 testes, postovarian. Ovary looped. Genital elongate and curved. atrium spineless.

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Figure 6. Pseudaxine trachuri: total view and structure of clamp.

Figure 7. Amphibdella torpedinis: a) total view; b) anterior region; c) posterior region.

Atrispinum Maillard & Noisy, 1979 A. salpae Parona & Perugia, 1889 (Figure 11c): 45–50 Body lanceolate. Haptor symmetrical, triangular in pairs of clamps, about 15 testes, genital atrium with 17 profile, with a row of numerous clamps. Testes numerous, peripheral and 5 central spines. A. seminalis Euzet & Maillard, 1973 (Figure 11d): postovarian. Ovary looped. Genital atrium with spines. 60–70 pairs of clamps, about 15 testes, genital atrium with A. acarne Maillard & Noisy, 1979 (Figures 11a and 10–14 peripheral and 10–12 central spines. 11b): 50–55 pairs of clamps, about 15 testes, genital atrium Axinidae Monticelli, 1903 with 15–25 peripheral and 6–7 central spines. Zeuxapta seriolae (Meserve, 1938) (Figure 12)

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Figure 8. Bivagina alcedinis: a) total view; b) anterior region; c) structure of clamp.

Figure 9. Total view of Aspinatrium trachini.

Figure 10. Microcotyle erythrini: a) total view; b) anterior region.

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Figure 11. a) Total view of Atrispinum acarne; b) framing of the genital pore of Atrispinum salpae; c) framing of the genital pore of A. acarne; d) framing of the genital pore of A. seminalis.

Figure 12. Zeuxapta seriolae: a) total view; b) anterior region; c) haptor and testes.

Body elongate, 4–9 mm long, 1.8–2 mm wide. Haptor 4. Discussion asymmetrical, clamps strung in 2 rows unequal in length Monogeneans are viewed as highly host-specific, but similar in structure, 45 clamps on one side, 30 on the but variation in specificity occurs between species of other. Testes numerous, over 100, postovarian. Ovary monogeneans (Strona et al., 2010). For example, some looped. monogeneans such as Microcotyle erythrini show less host specificity, whereas others, like Amphibdella torpedinis,

447 AKMIRZA / Turk J Zool seem to be highly specific. Similar patterns of variability in related to their abundance. For example, Montero et al. host specificity were also observed in this study. (2004) and Lia et al. (2007) observed that a high abundance Monogeneans show variation in geographical of Zeuxapta seriolae led to severe mortality in infected fish distribution. For example, Anthocotyle merlucci, which stocks. The abundance of all monogenean species found we found in European hake, is a widespread parasite of near Gökçeada was very low, suggesting that fish in this hakes (Merluccius spp.) in the Atlantic Ocean Basin, the region are not generally endangered by monogenean southwestern Indian Ocean, and the eastern parasites. Amphibdella torpedinis, Bivagina alcedinis, (Oğuz and Bray, 2008). Kuhnia scombri, which we detected Atrispinum spp., and Zeuxapta seriolae are new records for in Scomber japonicus near Gökçeada, is a parasite of this study area and for Turkey at large. Scomber spp. and has been found in different geographical areas such as the Mediterranean, North America, the Acknowledgments North Sea, Argentina, , , and South Africa This study was supported by the Scientific Research (Rohde and Watson, 1985). Projects Coordination Unit of İstanbul University, Project The damage caused to fish by monogeneans is strongly Number 12105.

References

Akmırza, A. 1997. Kolyoz (Scomber japonicus Houttuyn, 1780) Lia, R.P., Zizzo, N., Tinelli, A., Lionetti, A., Cantacessi, C. and balığının parazit faunasından örnekler. Ege JFAS 14(1–2): Otranto, D. 2007. Mass mortality in wild greater amberjack 173–181 (in Turkish). (Seriola dumerili) infected by Zeuxapta seriolae (Monogenea: Heteraxinidae) in the Ionian Sea. Bull. Eur. Assoc. Fish. P. Akmırza, A. 1998. Kupes (Boops boops Linne, 1758) balığında 27(3): 108–111. rastlanılan parazitik formlar. Ege JFAS 15(3–4): 183–198 (in Turkish). Oğuz, M.C. and Bray, R.A. 2008. Cestoda and Monogenea of some teleost of the Mudanya coast (Sea of Marmara, Turkey). Akmırza, A. 2003. Distribution of parasite fauna of chub Helminthologia 45(4): 192–195. in Aegean and Mediterranean Seas. Turkish J. Marine Sci. 9(3): 187–195. Pugachev, O.N., Gerasev, P.I., Gussev, A.V., Ergens, R. and Khotenowsky, I. 2010. Guide to Monogenoidea of Freshwater Akmırza, A. 2004. Parasite fauna of greater weever (Trachinus draco fish of Palaeartic and Amur Regions. Ledizioni, Milan. Linnaeus, 1758). Acta Adriat. 45(1): 35–41. Radujkovic, B. and Euzet, L. 1989. Parasites des poissons marins du Chisholm, L.A. and Whittington, I.D. 1998. Morphology Monténégro: Monogènes. Acta Adriat. 30(1/2): 51–135. and development of among the Monocotylidae (Monogenea). Hydrobiologica 383: 251–261. Rohde, K and Watson, N. 1985. Morphology, microhabitats and geographical variation of Kuhnia spp. (Monogenea: Daniel, G., Öztürk, B. and Başusta, N. 2006. The fishes of the Eastern Polyophisthocotylea). Int. J. Parasitol. 15(5): 569–586. Mediterranean. Publication No. 24, TÜDAV, İstanbul, Turkey. Strona, G., Stefani, F. and Galli, P. 2010. Monogenoidean parasites Dawes, B. 1968. The Trematoda. Cambridge University Press, of Italian marine fish: an updated checklist. Ital. J. Zool. 77(4): London. 419–437. Dezfuli, B.S., Giari, L., Simoni, E., Menegatti, R., Shinn, A.P. and Ulutürk, T. 1987. Gökçeada çevresinin balık faunası ve çevre fon Manera, M. 2007. Gill histopathology of cultured European radyoaktivitesi. İst. Üniv. Su Ürün. Derg. 1(1): 95–119 (in sea bass, Dicentrarchus labrax (L.), infected with Diplectanum Turkish). aequans (Wagener 1857) Diesing 1958 (Diplectanidae: Monogenea). Parasitol. Res. 100: 707–713. Whittington, I.D. 1998. Diversity “down under”: monogeneans in the Antipodes (Australia) with a prediction of monogenean Ekingen, G. 2004. Türkiye Deniz Balıkları Tanı Anahtarı. Mersin biodiversity worldwide. Int. J. Parasitol. 28: 1481–1493. Üniversitesi Yayınları No: 12, Mersin (in Turkish). Yamaguti, S. 1963. Systema Helminthum Monogenea and Keskin, Ç. and Ünsal, N. 1998. The fish fauna of Gökçeada Island, NE Aspidocotylea. Interscience Publishers, London. Aegean Sea, Turkey. Ital. J. Zool., 65 (Suppl.): 299–302. Montero, F.E., Crespo, S., Padros, F., De la Gandara, F., Garci, A. and Raga, J.A. 2004. Effects of the gill parasiteZeuxapta seriolae (Monogenea: Heteraxinidae) on the amberjack Seriola dumerili Risso (Teleostei: Crangidae). Aquaculture 232(1–4): 153–163.

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