FİRST RECORD OF Caligus diaphanus NORDMANN, 1832 FROM TURKİSH MARİNE HABİTATS* Ahmet ÖKTENER 1 ; Ali ALAŞ 2 ; Dilek TÜRKER-ÇAKIR 3

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FİRST RECORD OF Caligus diaphanus NORDMANN, 1832 FROM TURKİSH MARİNE HABİTATS* Ahmet ÖKTENER 1 ; Ali ALAŞ 2 ; Dilek TÜRKER-ÇAKIR 3 Abstract: Caligus diaphanus Nordmann,1832 (Copepoda; Caligidae) was reported for the first time from the gill chambers and inner faces of opercula of Chelidonichthys lucerna (Triglidae) from Aegean Sea Coasts in Turkey. Some morphological characters of this parasitic copepod are given using photograph and drawings. Key words: Chelidonichthys, occurrence, Aegean Sea, Turkey PRİMEİRO REGİSTRO DE Caligus diaphanus NORDMANN, 1832 DA COSTA DA TURQUIA Resumo Caligus diaphanus Nordmann, 1832 (Copepoda; Caligidae) foi relatado pela primeira vez das câmaras branquiais e faces internas dos opérculos de Chelidonichthys lucerna (Triglidae), do Mar Egeu, nas costas da Turquia. Alguns caracteres morfológicos deste copépode parasitário são apresentadas através de fotografia e ilustração. Palavras-chave: Chelidonichthys, Ocorrência, Mar Egeu, Turquia 1 Deparment of Fisheries, Sheep Research Institute, Çanakkele Street 7km., 10200,Bandırma, Balıkesir, Turkey 2Department of Biology, A. K. Education Faculty, Necmettin Erbakan University, B Block, 42090, Meram, Konya, Turkey 3Department of Biology, Science Faculty, Balikesir University, Cagıs Campus, 10300, Balikesir, Turkey *This paper is part of a being prepared PhD thesis. Doi: 10.5007/1678-2305.2016v42n1p203

204 INTRODUCTİON ÖKTENER et al. MATERİAL AND METHODS Sea lice (Caligidae) is the largest group of parasitic copepods of fish, comprising more than 450 species (HO and LIN, 2005). Hitherto, only eleven species of the family Caligidae have been recorded parasitizing fishes in Turkish marine habitats. They are Caligus apodus, Brian (1924), Caligus bonito, Wilson (1905), Caligus brevicaudatus, Scott (1901), Caligus lagocephali, Pillai (1961), Caligus minimus, Otto (1821), Caligus pageti, Russell (1925), Caligus pelamydis, Krøyer (1863), Caligus solea, Demirkale; Özak; Yanar; Boxshall (2014), Caligus temnodontis, Brian (1924), Lepeophtheirus europaensis, Zeddam; Berrebi; Renaud; Raibaut; Gabrion (1988), Caligus ligusticus, Brian (1906) (TAREEN, 1982; OĞUZ and ÖKTENER, 2007; BAKIR et al., 2014; DEMİRKALE et al., 2014; DEMİRKALE et al., 2015). According to BİLECENOĞLU et al., (2014), eight species of searobins are known in the Family Triglidae in Turkey. This study aims to report geographic distribution and first record of the female of Caligus diaphanus with some morphological characters from Turkey. 18 of tub gurnard, Chelidonichthys lucerna (Linnaeus, 1758) (Pisces, Triglidae) were collected by local gears from Edremit Bay (39 33'40.74"N, 26 44'47.55"E, Aegean Sea Coasts of Turkey, Figure 1) in 2014. The parasitic copepods were preserved in 70% ethanol. They were later cleared in 85% lactic acid for 1 to 2 h before dissection. Dissected parts were mounted on slides in glycerin-gelatine mounting medium. Sides of coverslip were coated with colourless nail polish. The drawings of appendages were carried out with the aid of a camera lucida (Olympus U-DA). The photos were taken using a Canon EOS 1100D camera connected to a microscope. Measurements were taken in millimetres (mm), with a micrometrical programme (Pro-way). Scientific names, synonyms of the parasite and the host were checked through WORMS (2015). The identification, scientific names, their synonyms of parasite were checked with BRIAN (1935), KABATA (1979), CRESSEY and CRESSEY (1980), CUBILLA (1985), WORMS (2015). Parasites (MNHN-IU-2013-18733) were deposited in the collections of the Musé um National d Histoire Naturelle (MNHN), Paris, France. Figure 1. Sampling Area

First record of Caligus diaphanus Nordmann, 1832 205 RESULTS Subclass Copepoda Order Siphonostomatoida Family Caligidae Caligus diaphanus Nordmann,1832 (Figure 2) Measurements: Total lenth (including egg sac): 5.079-5.123mm Width: 1.652-1.753mm Egg sac length: 2.253-2.297mm Infestation parameters: All parasites were firmly attached to the gill chambers and inner faces of opercula of host. The prevalence, mean intensity and mean abundance of parasite were 16.6%, 3.33 and 1.8, respectively. Figure 2. Caligus diaphanus Nordmann,1832, female. Description of female. Antennule (Figure 2, Number 3) 2-segmented, with shorter distal segment; proximal segment, with 8 plumose and 3 simple setae on ventral surface; distal segment with 1 subterminal seta on dorsal margin and 10 setae on distal margin. Antenna (Fig. 2, N o 4) 3-segmented; first segment with small, tapering proximal process; second segment nearly

206 ÖKTENER et al. quadrangular; third segment forming long, distally strongly bent curved claw. Maxillule (Fig. 2 N o 5) consisting of papilla bearing 3 unequal setae. Maxilliped (Fig. 2 N o 6) 3-segmented; proximal segment (corpus) largest, unarmed; distal two segments fused to form a claw and carrying a small seta. Maxilla (Fig. 2 N o 7) 2-segmented and brachiform; proximal segment (lacertus) large and unarmed; slender distal segment (brachium) with a small subterminal hyaline membrane on outer edge and 2 unequal elements (calamus and canna) at terminal end. Sternal furca (Fig. 2 N o 8) with nearly parallel tines, tines rounded at tip. Caudal rami (Fig. 2 N 9) with 5 plumose setae. Mandible within mouth tube, tip with 12 teeth. (Fig. 2 N o 10). First leg (Fig. 2 N o 11) basipod with a shorter plumose seta near outer and inner mid-margin; exopod first segment with a short spine on outer distal corner and a row of spinules along inner margin, second segment with 4 outer to terminal spines and 3 inner plumose setae. Second leg (Fig. 2 N o 12) basipod with a short plumose seta on outer distal corner; exopod first and second segments each with a stout spine on outer distal corner and an inner seta, last segment with 3 outer spines and 5 terminal to inner setae; endopod first segment with an inner seta, second segment with a patch of long spinules along outer edge and 2 inner setae, last segment with a patch of long spinules on outer edge and 6 setae. Third leg (Fig. 2 N o 13) exopod first segment with a prominent spine on outer distal corner, second segment with a short spine on outer distal corner and inner seta, last segment with 3 short outer spines and 4 terminal to inner setae; endopod first segment with an inner seta, last segment with 6 terminal setae. Fourth leg (Fig. 2 N o 14) basipod with a small seta on outer distal corner; exopod first segment with a fringed seta on outer distal corner, second segment with fringed seta on outer distal corner, last segment with 3 fringed setae. Fifth leg (Fig. 2 N o 15) represented by 3 short plumose setae.

First record of Caligus diaphanus Nordmann, 1832 207 Figure 2. (N o 3) antennule (scale: 0,8), (N o 4) antenna (scale:0,10), (N o 5) maxillule (scale:0,10), (N o 6) maxilliped, (scale:0,17), (N o 7) maxilla (scale:0,18), (N o 8) sternal furca (scale:0,12), (N o 9) caudal rami (scale:0,13), (N o 10) mandible (scale:0,05), (N o 11) first leg (scale:0,10), (N o 12) second leg (scale: 0,10), (N o 13) third leg (scale: 0,20), (N o 14) fourth leg (scale: 0,20), (N o 15) fifth leg. DİSCUSSİON Caligus diaphanus was widely distributed from British Isles, European, Atlantic, Mediterranean, Adriatic, Indian Ocean. The species is reported parasitizing several fishes including Triglidae (Chelidonichthys cuculus, Chelidonichthys lucerna, Chelidonichthys capensis Eutrigla gurnardus, Trigla lyra, Trigloporus lastoviza, Lepidotrigla cavillone), Sparidae (Pagellus acarne, Pagellus bogaraveo, Pagellus erythrinus, Lithognathus mormyrus, Dentex dentex), Flatfishes (Scophthalmus maximus, Solea solea, Platichthys flesus Lepidorhombus whiffiagonis), Gadoid fishes (Merluccius merluccius, Molva molva, Gadus morhua, Pollachius virens), Carangidae (Caranx hippos, Trachurus trachurus, Trachinotus botla ), Terapontidae (Terapon puta), Belonidae (Belone belone), Scombridae (Scomber scombrus, Scomberomorus tritor), Centropomidae (Lates calcarifer) Lutjanidae (Lutjanus peru) (BRIAN, 1935; KABATA, 1979; CRESSEY and CRESSEY, 1980; CUBILLA, 1985; RADUJKOVIC and RAIBAUT, 1989; RAIBAUT et al., 1998; GONZALEZ et al., 2004; RAMDANE and TRILLES, 2010; WORMS, 2015). Larvae of the copepod Caligus diaphanus infect the gill filaments, but adults prefer the wall of the mouth cavity (ROHDE, 1993). Also, we found adult of Caligus diaphanus on gill chambers and inner faces of opercula of host fish. The general morphology, second antenna, second maxilla, maxilliped, mandible, maxillule of our female specimens and BRIAN (1935); KABATA (1979); CRESSEY and CRESSEY (1980); CUBILLA (1985); RADUJKOVIC and RAIBAUT (1989) drawings are identical. However, some discrepancies are found in the fine details of the structure of the appendages. For instance, we found proximal segment of antennule with 11 setae, distal segment bearing 11 setae while proximal segment with 27 setae, distal segment bearing 14 setae by CRESSEY and CRESSEY (1980); proximal segment with 10 setae, distal segment bearing 8 setae by BRIAN (1935); proximal segment with 24 setae, distal segment bearing 11 setae by CUBILLA (1985). Morphologic features of all dissected parasites permitted identification of this copepod as Caligus diaphanus, Nordmann (1832). This study is so important that it is the first record from Turkey marine habitats according to literature BAKIR et al., (2014). REFERENCES BAKIR A.K.; KATAĞAN, T.; AKER, V.; ÖZCAN, T.; SEZGİN, M.; ATEŞ, A.S.; KOÇAK, C.; KIRKIM, F. 2014 The Marine Arthropods of Turkey. Turkish Journal of Zoology, 38: 765-831. BİLECENOĞLU, M.; KAYA, M.; CİHANGİR, B.; ÇİÇEK, E. 2014 An updated checklist of marine fishes of Turkey. Turkish Journal of Zoology, 38: 901-929. BRIAN, A. 1935 I Caligus parassiti dei pesci del Mediterraneo. (Copepodi). A. Mus. Civ. di St. Di Nat. Di Genova, 57(7): 152-211. CRESSEY, R. and CRESSEY, H.B. 1980 Parasitic copepods of Mackerel- and Tuna-like fishes (Scombridae) of the World. Smith. Contrib. Zool., Washington, 311, 186p. CUBILLA, A.M. 1985 Etudes morphologiques et bioećologiques des Copeṕodes parasites de quelques poissons marins des co tes languedociennes. Universite Aix-Marseille 2, Dissertation: The se 3e cycle: 186p. DEMİRKALE, İ.; ÖZAK, A.A.; YANAR, A.; BOXSHALL, G.A. 2014 Caligus solea n. sp. (Copepoda: Caligidae) parasitic on the common sole Solea solea (Linnaeus) from the north-eastern Mediterranean off the Turkish coast. Systematic Parasitology, 89(1): 23-32. DEMİRKALE, İ.; ÖZAK, A.A.; BOXSHALL, G.A. 2015 The discovery of the male of Caligus ligusticus Brian, 1906 (Copepoda: Caligidae) parasitic on the sand steenbras Lithognathus

208 ÖKTENER et al. mormyrus (L.) in the eastern Mediterranean. Systematic Parasitology, 91(1): 81-90. GONZALAEZ, P.; SANCHEZ, M.I.; CHIRIVELLA, J.; CARBONELL, E.; RIERA, F.; GRAU, A. 2004 A preliminary study on gill metazoan parasites of Dentex dentex (Pisces: Sparidae) from the western Mediterranean Sea (Balearic Islands). J. Appl. Ichthyol., 20: 276-281. HO, J.S. and LIN, C.L. 2005 Sea Lice of Taiwan. The Sueichan Press, Keelung, Taiwan. 388 p. KABATA, Z. 1979 Parasitic Copepoda of British Fishes. Ray Society Publications, The Bristish Museum, London, 152, 468 p. OĞUZ, M.C. and ÖKTENER, A. 2007 Four Parasitic Crustacean Species from marine fishes of Turkey. Türkiye Parazitoloji Dergisi, 31(1): 79-83. RADUJKOVIC, B. and RAIBAUT, A. 1989 Parasites des poissons marins des côtes du Monténégro: Copépodes. Acta adriatica, 28: 237-278. RAIBAUT, A.; COMBES, C.; BENOIT, F. 1998 Analysis of the parasitic copepod species richness among Mediterranean fish. Journal of Marine Systems, 15: 185-206. RAMDANE, Z. and TRILLES, J.P. 2010 New Algerian parasitic copepods. Bulletin of the European Association of Fish Pathologists, 30: 41-47. ROHDE, K. 1993. Ecology of Marine Parasites. 2nd edn. (CAB International: Wallingford, Oxon). TAREEN, I.U. 1982 Parasitic infections of commercially important fish in Turkish water and microhabitat utilization. II. Conferencia Mediterranea de parasitologia (29september- 2 October), Granada (Spain), p175. WORMS 2015 World Register of Marine Species. Available from http://www.marinespecies.org at VLIZ. Accessed 22.07.2015.