Nematode and Acanthocephalan Parasites of Marine Fish of the Eastern Black Sea Coasts of Turkey
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Turkish Journal of Zoology Turk J Zool (2013) 37: 753-760 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1206-18 Nematode and acanthocephalan parasites of marine fish of the eastern Black Sea coasts of Turkey Yahya TEPE*, Mehmet Cemal OĞUZ Department of Biology, Faculty of Science, Atatürk University, Erzurum, Turkey Received: 13.06.2012 Accepted: 04.07.2013 Published Online: 04.10.2013 Printed: 04.11.2013 Abstract: A total of 625 fish belonging to 25 species were sampled from the coasts of Trabzon, Rize, and Artvin provinces and examined parasitologically. Two acanthocephalan species (Neoechinorhynchus agilis in Liza aurata; Acanthocephaloides irregularis in Scorpaena porcus) and 4 nematode species (Hysterothylacium aduncum in Merlangius merlangus euxinus, Trachurus mediterraneus, Engraulis encrasicholus, Belone belone, Caspialosa sp., Sciaena umbra, Scorpaena porcus, Liza aurata, Spicara smaris, Gobius niger, Sarda sarda, Uranoscopus scaber, and Mullus barbatus; Anisakis pegreffii in Trachurus mediterraneus; Philometra globiceps in Uranoscopus scaber and Trachurus mediterraneus; and Ascarophis sp. in Scorpaena porcus) were found in the intestines of their hosts. The infection rates, hosts, and morphometric measurements of the parasites are listed in this paper. Key words: Turkey, Black Sea, nematode, Acanthocephala, teleost 1. Introduction Bilecenoğlu (2005). The descriptions of the parasites were This is the first paper on the endohelminth fauna of executed using the works of Yamaguti (1963a, 1963b), marine fish from the eastern Black Sea coasts of Turkey. Golvan (1969), Yorke and Maplestone (1962), Gaevskaya The acanthocephalan fauna of Turkey includes 11 species et al. (1975), and Fagerholm (1982). The preparation of the (Öktener, 2005; Keser et al., 2007) and the nematode fauna parasites was carried out according to Kruse and Pritchard includes 16 species (Öktener, 2005). There is currently (1982). no study on acanthocephalans of marine fish from the The parasitological statistics were calculated according Black Sea coasts of the country. In the present study, A. to Bush et al. (1997) and are presented in Table 1. The irregularis, Ascarophis sp., and Philometra globiceps have morphometric values of the parasites are presented in been recorded for the first time from Turkey. The purpose of Tables 2 and 3. this study is to contribute to the fauna of acanthocephalans and nematodes of marine fish from the north of Turkey. 3. Results Acanthocephala 2. Materials and methods Eoacanthocephala The study area is the eastern Black Sea coast of Turkey Neoechinorhynchida (Trabzon: 41°01′N, 39°43′E; Rize: 41°02′N, 40°32′E; and Artvin: 41°25′N 41°23′E) (Figure). Between June Neoechinorhynchidae 2007 and December 2010, 625 fish from 25 species Neoechinorhynchus agilis (Rudolphi, 1819) were collected. The parasites were fixed with 70% ethyl Syn: Echinorhynchus agilis Rudolphi, 1819 alcohol for nematodes and AFA (acetic acid : formalin : Host: Liza aurata alcohol) for acanthocephalans. The samples were brought Infection site: intestine to the Parasitology Research Laboratory of the Biology According to Cleave (1922), Neoechinorhynchus agilis Department of the Faculty of Science of Atatürk University, is restricted to fish of the genus Mugil in the Mediterranean where the materials were deposited in the appropriate Sea. manner. Numerous authors (Keser et al. [2007] in the The identification of the fish was established using the Dardanelles; Merella and Garippa [2001] and Schmidt works of Slastenenko (1955), Geldiay (1969), and Can and and Paperna [1978] in the Mediterranean Sea; Kostylew * Correspondence: [email protected] 753 TEPE and OĞUZ / Turk J Zool BLACK SEA ARTVİN RİZE TRABZON 100 km TURKEY Figure. Sampling area. Table 1. Statistical values of the parasites (L: locality, A: Artvin, R: Rize, T: Trabzon, EFN: examined fish number, IFN: infected fish number, TPN: total parasite number, %: prevalence, MA: mean abundance, MI: mean intensity). PARASITE HOST L EFN IFN TPN % MA MI ACANTHOCEPHALA Neoechinorhynchus agilis Liza aurata A 50 5 23 10 4.6 0.5 Acanthocephaloides irregularis Scorpaena porcus T 115 1 1 1 1.0 0.0 NEMATODA Hysterothylacium aduncum Belone belone A, R, T 36 11 19 31 1.7 0.5 Hysterothylacium aduncum Caspialosa sp. A 13 13 170 100 13.1 13.1 Hysterothylacium aduncum Engraulis encrasicholus A, R, T 71 63 744 89 11.8 10.5 Hysterothylacium aduncum Gaidropsarus mediterranes T 6 2 20 33 10.0 3.3 Hysterothylacium aduncum Gobius niger A, R, T 9 5 27 56 5.4 3.0 Hysterothylacium aduncum Merlangius merlangus euxinus A, R, T 147 138 1384 56 10.0 9.4 Hysterothylacium aduncum Mullus barbatus T 17 16 81 94 5.1 4.8 Hysterothylacium aduncum Neogobius melanostomus A, R, T 11 3 12 27 4.0 1.1 Hysterothylacium aduncum Ophidion rochei T 3 2 17 67 8.5 5.7 Hysterothylacium aduncum Platichthys flesus T 3 1 1 33 1.0 0.3 Hysterothylacium aduncum Sarda sarda T 6 3 45 50 15.0 7.5 Hysterothylacium aduncum Sciaena umbra A 4 1 2 25 2.0 0.5 Hysterothylacium aduncum Scorpaena porcus A, R, T 115 33 89 29 2.7 0.8 Hysterothylacium aduncum Solea vulgaris T 7 2 7 29 3.5 1.0 Hysterothylacium aduncum Spicara smaris A 3 3 85 100 28.3 28.3 Hysterothylacium aduncum Syngnathus acus A 1 1 2 100 2.0 2.0 Hysterothylacium aduncum Trachinus draco R 1 1 32 100 32.0 32.0 Hysterothylacium aduncum Trachurus mediterraneus A, R, T 56 54 510 96 9.4 9.1 Hysterothylacium aduncum Uranoscopus scaber R, T 50 35 276 70 7.9 5.5 Anisakis pegreffii Trachurus mediterraneus T 56 1 11 2 11.0 0.2 Philometra globiceps Trachurus mediterraneus T 56 1 2 2 2.0 0.0 Philometra globiceps Uranoscopus scaber T 50 2 4 4 2.0 0.1 Ascarophis sp. Scorpaena porcus T 115 1 1 1 1.0 0.0 754 TEPE and OĞUZ / Turk J Zool Table 2. Measurements of acanthocephalans (µm) (L: total length; W: width; PL: proboscis length; PW: proboscis width; PSL: proboscis sac length; PSW: proboscis sac width; LL1: lemniscus-1-length; LW1: lemniscus-1-width; LL2: lemniscus-2-length; LW2: lemniscus-2-width; H1: apical hook; H2: median hook; H3: basal hook; ATL: anterior testis length; ATW: anterior testis width; PTL: posterior testis length; PTW: posterior testis width; BL: bursa length; BW: bursa width; EL: egg length; EW: egg width). Values are mean ± SD (min–max). Neoechinorhynchus agilis Acanthocephaloides irregularis General Male Female Female Female Gaevskaya et al., 1975 Present study Present study Amin et al., 2011 Present study 5643 ± 119 12,495 ± 1002 3160 ± 720 L 7000–45,000 7085 (4121–7511) (4852–26,126) (1254–5658) 601 ± 160 711 ± 250 560 ± 170 W 800–1000 954 (426–832) (406–1015) (319–1402) 168 ± 20 183 ± 36 280 ± 40 PL - 234 (137–194) (137–234) (129–371) 127 ± 2 128 ± 29 130 ± 20 PW - 121 (97–170) (97–162) (72–153) 410 ± 130 500 ± 152 452 ± 90 PSL - 610 (178–501) (242–671) (246–615) 152 ± 40 164 ± 37 131 ± 40 PSW - 150 (89–218) (121–202) (73–196) 2195 ± 370 2969 ± 689 560 ± 100 LL1 - 740 (1827–2984) (1989–3451) (369–861) 119 ± 20 132 ± 26 LW1 - - 80 (81–142) (102–162) 1865 ± 370 2390 ± 598 LL2 - - - (1563–2639) (1644–3045) 107 ± 30 117 ± 35 LW2 - - - (81–162) (81–162) 64 ± 20 63 ± 18 36 ± 4 H1 84–140 32 (41–87) (49–87) (26–44) 41 ± 20 41 ± 14 53 ± 6 H2 - 49 (24–61) (26–61) (34–64) 33 ± 10 29 ± 6 19 ± 2 H3 36–60 16 (22–41) (24–37) (13–24) 394 ± 220 ATL 650–1820 - - - (121–670) 296 ± 150 ATW 370–560 - - - (97–467) 449 ± 340 PTL - - - - (145–1076) 297 ± 140 PTW - - - - (129–426) BL - 731 - - - BW - 345 - - 52 ± 12 EL 35–42 - 22 47 (36–76) 12 ± 2 EW 9–12 - 12 14 (8–14) 755 TEPE and OĞUZ / Turk J Zool 756 Table 3. Morphometric measurements of nematodes (µm) (L: length; W: width; A–N: distance of nerve ring to anterior; A–Ex: distance of excretory pore to anterior; EL1: esophagus length; VAL: ventricular appendix length; ICL: intestinal ceca length; VL: ventricles length; TL: tail length; V–A: distance of vulva to anterior; EGGL: egg length; EGGW: egg width; SLL: left spicule length; SRL: right spicule length). Values are mean ± SD (min–max). Hysterothylacium aduncum 3rd stage 4th stage Adult male Adult female Present study Fagerholm, 1982 Present study Fagerholm, 1982 Present study Fagerholm, 1982 Present study Fagerholm, 1982 8326 ± 2055 11,528 ± 4242 25,544 ± 9661 37,770 ± 6771 L 6600–20,600 12,000–31,000 21,900–46,200 26,800–52,000 (4263–14,190) (7613–20,219) (18,879–44,457) (30,958–48,029) 174 ± 41 174 ± 63 344 ± 33 496 ± 138 W 160–330 230–470 300–430 400–790 (73–226) (97–299) (315–406) (348–669) 242 ± 50 304 ± 59 356 ± 23 443 ± 71 A–N 280–450 340–610 480–850 560–840 (162–364) (220–404) (323–372) (356–541) 286 ± 35 335 ± 59 401 ± 17 479 ± 78 A–Ex 310–500 420–640 490–880 620–910 (228–347) (260–444) (388–420) (412–566) 1023 ± 203 1140 ± 306 1983 ± 241 3025 ± 794 EL 1000–2600 1940–3850 2600–4670 3230–6000 (687–1421) (792–1680) (1766–2416) (2314–4283) 350 ± 84 346 ± 147 498 ± 65 684 ± 249 VAL 400–680 610–930 800–1150 1100–1400 (202–480) (192–485) (444–614) (533–1056) 414 ± 84 453 ± 140 569 ± 62 899 ± 257 ICL 330–920 650–1230 690–1180 1040–1550 (240–566) (323–719) (508–687) (649–1299) VL - - - - - - 132 ± 41 181 ± 49 134 ± 40 252 ± 77 TL 120–210 110–290 120–180 310–350 (73–242) (81–244) (81–203) (137–323) 13,515 ± 2338 V–A - - - - - - 10,180–18,350 (11,693–16,849) 43 ± 9 EGGL - - - - - - 63–76 (36–56) 35 ± 6 EGGW - - - - - - 41–57 (32–44) 1119 ± 211 SLL - - 650–2980 (970–1269) SRL 954 890–2180 TEPE and OĞUZ / Turk J Zool Table 3.