New Algerian parasitic copepods

Bull. Eur. Ass. Fish Pathol., 30(2) 2010, 41 New Algerian parasitic copepods Z. Ramdane 1 * and J. Trilles 2 1 Zouhir Ramdane, Université A/Mira Faculté des sciences, Département de biologie TCSN, rue Targa Ouzemour, Béjaïa (6000) Algérie ; 2 Jean-Paul Trilles, UMR 5119 Equipe Adaptation Ecophysiologique et Ontogenèse, Université de Montpellier 2, CC. 092, Place E. Bataillon, 34095 Montpellier Cedex 05, France Abstract Ten copepod species were collected on teleost fishes from the east coast of Algeria. Among them, seven are reported for the first time from Algerian waters: Caligus ligusticus; C. bonito; Pseudocycnus appendiculatus; Neobrachiella triglae; N. bispinosa; N. impudica and Clavella alata. Caligus uranoscopi is new to the east coast of Algeria. New hosts have been identified for Caligus diaphanus and Hatschekia pagellibogneravei. To date 66 species of parasitic copepods are now well known from Algerian coasts. All collected copepods show high degree of specificity for the hosts and the site of a achment. Parasitologic indexes are generally low. Introduction Until now, Algerian ectoparasitic copepods have only been studied by Rose and Vessière (1952), Nunes-Ruivo (1954), Dieuzeide and Roland (1956), Essafi et al. (1983), Ramdane (2003), Hamza et al. (2007) and Ramdane and Trilles (2007). In the present study, ten copepod species are studied: seven are reported for the first time from Algerian waters and one another from the east coast of Algeria; new hosts are identified for two other species. Materials and methods Our study was conducted during the years 2006 and 2007 on the east coast of Algeria (Figure 1). 1166 teleost fish were examined for their ectoparasitic copepods. The collected parasites were preserved in 70% alcohol. The date, locality of sampling, sex and size of the host and the site of the parasite a achment were noted. The parasitologic indexes (Prevalence, P; mean abundance, Am; mean intensity, Im) were calculated according to Margolis et al. (1982) and Bush et al. (1997). For each copepod species, geographic distribution and hosts were specified. Synonyms of the fish names were updated according to Froese and Pauly (2009) and put in brackets. Results Order Siphonostomatoida Burmeister, 1835 Family Caligidae Burmeister, 1835 Genus Caligus Müller, 1785 Caligus ligusticus Brian, 1906 Caligus ligusticus was found on the gills of Lithognathus mormyrus. * Corresponding author s e-mail: zohir22000@yahoo.fr

Bull. Eur. Ass. Fish Pathol., 30(2) 2010, 42 Figure 1. Situation of the Gulf of Béjaïa (East coast of Algeria). In the Mediterranean Sea, this species has been already reported from Lithognathus mormyrus, Diplodus sargus, Pagellus bogaraveo and Sarpa salpa (Raibaut et al., 1998). In Tunisia, it was collected on Lithognathus mormyrus (Benmansour and Ben Hassine 1997). This species seems to infest specifically Sparid fishes. Caligus uranoscopi Vaissière, 1955 This species was collected on the gills of Mullus barbatus barbatus. In the Algerian waters, it has been previously reported by Vaissière (1955) from Trigla lucerna (Chelidonchthys lucerna) and Uranoscopus scaber. M. barbatus barbatus is a new host for C. uranoscopi. This species is maybe uncommon. In the Mediterranean and especially in Tunisia it has not been until now reported (Benmansour and Ben Hassine, 1997; Raibaut et al., 1998). C. uranoscopi is maybe restricted to the Algerian coast. Caligus bonito Wilson, 1905 This species was found on the gills of Euthynnus alle eratus. It has been already reported from the northern and southern Atlantic, the Mediterranean, the Black Sea (Reshetnikova, 1955), in the Pacific and Indian Oceans (Kabata, 1979) and in South Africa (Barnard, 1955a). In the Mediterranean, this species has been reported from Sarda sarda by Raibaut et al. (1998). However the most common hosts of this cosmopolitan parasite are large Scombrid fishes (Kabata, 1979). Family Lernaeopodidae Milne Edwards, 1840 Genus Parabrachiella Wilson 1915 Parabrachiella (=Neobrachiella) triglae (Claus, 1860) This species was collected on the gills of Chelidonichthys lucerna.

Bull. Eur. Ass. Fish Pathol., 30(2) 2010, 43 Table 1. Parasitologic indexes of the collected parasitic copepods. Parasites/Host NEF NIF NP P Am Im Sf Caligidae Burmeister, 1835 Caligus ligusticus Brian, 1909* Lithognathus mormyrus 333 3 3 0.9 0.01 1 Br Caligus uranoscopi Vaissière, 1955* Mullus barbatus barbatus 72 3 3 4.17 0.04 1 Br Caligus bonito Wilson, 1905* Euthynnus alle eratus 18 1 1 5.55 0.05 1 Br Caligus diaphanus Normann, 1832** Eutrigla gurnadus 4 2 2 50 0.5 1 Brc Lernaeopodidae Milne Edwards, 1840 Parabrachiella triglae (Claus, 1860)* Chelidonichthys lucerna 8 2 2 25 0.25 1 Br Parabrachiella bispinosa (Nordmann, 1832)* Chelidonichthys lucerna 8 1 1 12.5 0.12 1 Br Parabrachiella impudica (Von Nordmann, 1832)* Chelidonichthys lucerna 8 2 2 25 0.25 1 Brc Clavella alata Brian, 1906* Phycis phycis 33 6 21 18.18 0.64 3.5 Br Pseudocycnidae Wilson, 1922 Pseudocycnus appendiculatus Heller, 1865* Euthynnus alleteratus 18 1 1 5.55 0.05 1 Br Hatschekiidae Kabata, 1979 Hatschekia pagellibogneravei Hesse, 1879** Boops boops 664 2 4 0.3 0.01 2 Br *: new collected species from Algeria or from the east coast of Algeria; **: new host identified; NEF number of examined fishes; NIF number of infested fishes; NP number of parasite; P prevalence (%); Am Mean Abundance; Im Mean Intensity; Sf site of a achment; Br Branchial arch; Brc Branchial cavity.

Bull. Eur. Ass. Fish Pathol., 30(2) 2010, 44 In the Mediterranean, it was already reported on several Triglidae, from Anchorella triglae by Claus (1860), Kurz (1877) and Richiardi (1880), on Trigla lineata (Trigloporus lastoviza) and Trigla corax (Chelidonichthys lucerna) by Valle (1880), from Aspitrigla obscura (Chelidonichthys obscurus), Trigla lucerna and Trigloporus lastovisa (Raibaut et al., 1998). According to Kabata (1979), this species parasitize exclusively teleost fishes belonging to the family Triglidae. Parabrachiella (=Neobrachiella) impudica (Nordmann, 1832) This species was found on the gills of Chelidonichthys lucerna. It was already collected in several areas (North Sea, Atlantic coast of Europe, British waters, western and eastern parts of the Mediterranean) from different species of Triglidae (Kabata, 1979; Öktener and Trilles, 2004a). Parabrachiella (=Neobrachiella) bispinosa (Nordmann, 1832) Parabrachiella bispinosa was collected from the gills of Chelidonichthys lucerna. It was already reported in several localities almost exclusively on Triglidae: Trigla gurnardus (Eutrigla gurnardus) in Belgium (Beneden, 1871), Scotland and Ireland (Sco, 1913), Trigla spp. in England (Basse -Smith, 1896), Trigla cuculus (Aspitrigla cuculus) in England (Leigh-Sharp, 1928, 1933), Trigla pini (Aspitrigla cuculus) and Acanthias vulgaris (Squalus acanthias) in Scotland, Ireland and Belgium (Oorde-de Lint and Schuurmans Stekhoven, 1936), Trigla lucerna in Mauritania (Brian 1924). In the Mediterranean, this species has been reported from Merluccius merluccius, Trigla lucerna and Trigloporus lastovisa (Raibaut et al. 1998), on Trigla lucerna in Tunisia (Benmansour and Ben Hassine, 1997) and Turkey (Öktener and Trilles, 2004a). Genus Clavella Oken, 1816 Clavella alata Brian, 1906 Clavella alata was collected from the gills of Phycis phycis. In the Mediterranean, this species has been already reported from Phycis mediterranea (Phycis phycis) (Nunes-Ruivo, 1953) and Phycis blennoides (Raibaut et al., 1998). In the Mediterranean Sea, it was collected on Trigla corax in Italy (Richiardi, 1880), Trigla obscura (Chelidonichthys obscurus) and Trigla lucerna in France (Herrera-Cubilla, 1985), Trigla lucerna in Adriatic (Montenegro) (Radujkovic and Raibaut, 1987, 1989). It was recently reported in the Mediterranean on Aspitrigla obscura and Trigla lucerna (Raibaut et al., 1998), on Trigla lucerna in Turkey (Öktener and Trilles, 2004b). There are only two known host fishes for C. alata, both belonging to the gadiform genus Phycis (Kabata, 1979). According to Kabata (1979), this species parasitize specifically P. blennoides, the main host of C. alata. However, as in other Mediterranean localities, Phycis phycis is probably the single host for this species in Algeria.

Bull. Eur. Ass. Fish Pathol., 30(2) 2010, 45 Family Pseudocycnidae Wilson, 1922 Genus Pseudocycnus Heller, 1865 Pseudocycnus appendiculatus Heller, 1865 This species was found on the gills of Euthynnus alleteratus. It was previously reported from Coryphaena hippurus, Katsuwonus pelamis and Thunnus thynnus in the Mediterranean (Raibaut et al., 1998). Kabata (1979) observed that the distribution of this species is as wide as the distribution of its hosts, mainly the big Scombrids. In Algeria, as in other localities, this species parasitize Scombrid fishes. Additional results In Algeria, Ramdane and Trilles (2007) have previously reported Caligus diaphanus Normann, 1832 on Pagellus erythrinus and Hatschekia pagellibogneravei Hesse, 1879 from Pagellus acarne, P. bogaraveo, P. erythrinus and Diplodus vulgaris. In this study, Eutrigla gurnadus and Boops boops are new hosts identified respectively for C. diaphanus and H. pagellibogneravei. Raibaut et al. (1998) also recorded C. diaphanus on E. gurnardus from other Mediterranean areas. Discussion In Algeria, 59 parasitic copepod species have been reported by Ramdane and Trilles (2007). Among them, 19 are new to Algerian waters. Two species of Caligus were previously reported by Ramdane and Trilles (2007): Caligus centrodonti Baird, 1850 and Caligus diaphanus von Nordmann, 1832. In the present study, three other species belonging to the genus Caligus were collected: Caligus ligusticus and C. bonito, new to Algerian waters, and C. uranoscopi, new to the East coast of Algeria. Four species belonging to the family Lerneopodidae were collected: Parabrachiella triglae, Parabrachiella bispinosa, Parabrachiella impudica, Clavella alata. All these species are new for the Algerian waters. The current study therefore increases the total number of parasitic copepod species now reported from Algerian marine fish to 66. Caligus diaphanus and Hatschekia pagellibogneravei were previously reported in Algeria by Ramdane and Trilles (2007). In this study, the new hosts Eutrigla gurnardus and Boops boops are respectively identified for these species. In Algeria, like in the other Mediterranean localities, several Triglidae are parasitized by specific parasitic copepod species (Parabrachiella triglae, P. bispinosa and P. impudica). On Scombrids, C. bonito and P. appendiculatus are reported for the first time from Algerian waters. In Algeria, the general rate of infestation is poor. All collected parasites were a ached on the gills and in the branchial cavities. They show high specificity to their hosts and their site of a achment, geographically respected. These results are similar enough to those obtained by Benmansour and Ben Hassine (1997), Raibaut et al. (1998) and Öktener and Trilles (2004a, b) respectively in Tunisia, Mediterranean Sea and Turkey.

Bull. Eur. Ass. Fish Pathol., 30(2) 2010, 46 Acknowledgements We thank Dr. Jushey Ho (Department of Biological Sciences, California State University, California, USA) for his help in the identification of the species Caligus uranoscopi. Many thanks also to the fishermen of the Béjaïa fishing harbour. We thank the anonymous reviewers for their time in carefully reviewing our manuscript. We believe that their positive comments substantially improved this article. References Barnard KH (1955). South African parasitic Copepoda. Annals of the South African Museum 41, 223-312. Basse -Smith PW (1896). A list the parasitic Copepoda of fish obtained at Plymouth. Journal of the Marine Biological Association of the United Kingdom. 4, 155-163. Benmansour B and Ben Hassine OK (1997). Preliminary analysis of parasitic copepod species richness among coastal fishes of Tunisia. Italian Journal of Zoology 65 Suppl., 341 344. Brian A (1924). Arthropoda (1ère partie) Copepoda. Matériaux pour la faune parasitologique en Mauritanie. Parasitologica Mauritanica. Bulletin du Comité d Études Historiques et Scientifiques de l Afrique Occidentale Française. Juill-Sept, 365-427. 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. Claus C (1860). Zur Morphologie der Copepoden. I. Eine Hemmungsbildung von Cyclops. II. Uber den Bau von Nicothoë. III. Uber die Leibesgliederung und die Mundwerkzeuge der Schmarotzerkrebse. Wûrzburger Naturwissenscha liche Zeitschri 1, 20-36. Dieuzeide R and Roland J, (1956). Observations réalisées sur les sardines. (Sardina pilchardus Walbaum) de la baie de Castiglione parasitées par Peroderma cylindricum Heller. Bulletin Station Agriculture et de Pêche de Castiglione 8, 227 249. Essafi K, Raibaut A and Boudaoud-Krissat K (1983). Colobomatus steenstrupi (Richiardi, 1876) and Colobomatus mulli n. sp. (Copepoda; Phylichthyidae), parasitic on fish of the genus Mullus (Mullidae) in the western mediterranean. Systematic Parasitology 5, 135 142. Froese R and Pauly D (2009). Fishbase: a global information system on fishes. World Wide Web electronic publication. Available from: h p://www.fishbase.org. Hamza F, Boxshall GA and Kechemir-Issad N (2007). New species of Prohatschekia Nunes- Ruivo, 1954 (Copepoda: Hatschekiidae) parasitic on Scorpaena elongata (Cadenat) off Algeria. Systematic Parasitology 67, 119-124. Herrera-Cubilla A (1985). Etudes morphologiques et bio-écologiques des Copépodes parasites de quelques poissons marins des côtes languedociennes. Thèse 3 ème cycle. Université Aix-Marseille II : 187p. Kabata Z (1979). Parasitic Copepoda of British Fishes. Ray Society Publications, The British Museum, London, 152: 468 pp. Kurz W (1877). Studien über die Familie der Lernaepodiden. Zeitschri für Wissenscha liche Zoologie 29, 380 426. Leigh-Sharpe WH (1928). Brachiella obesa, a parasitic copepod of Trigla cuculus with a description of the male. Parasitology 20, 25-31. Leigh-Sharpe WH (1933). A list of British fishes with their characteristic parasitic Copepoda. Parasitology 25, 109-112.

Bull. Eur. Ass. Fish Pathol., 30(2) 2010, 47 Margolis I, Esche W, Holmes JC, Kuris AM and Schad GA (1982). The use ecological terms in parasitology (report of an adhoc commi ee of the American society of parasitologists. Journal of Parasitology 68, 131 133. Nunes-Ruivo L (1953). Copépodes parasites des poissons. Résultats des campagnes du «Pr. Lacaze Duthiers». Vie et Milieu Suppl. 3, 115-138. Nunes-Ruivo L (1954). Copépodes parasites de poissons. Résultats Campagne du Pr Lacaze-Duthiers. I. Algérie 1952. Vie et Milieu Suppl. 3, 115 138. Öktener A and Trilles JP (2004a). Three new parasitic copepod species for the parasites fauna of marine fish of Turkey. Journal of the Black Sea/Mediterranean Environment 10, 71 80. Öktener A and Trilles JP (2004b). Two Lernaepodids and one Pennellid Copepod determined on three marine fishes collected in Turkey. Journal of the Black Sea/Mediterranean Environment 10, 143 152. Oorde-de Lint van GM and Schuurmans Stekhoven JH (1936). Die Tierwelt der Nordund Otsee X.c. Copepoda. X. C2: Copepoda Parasitica, 73-198. Radujkovic B and Raibaut A (1987). Copépodes parasites des poissons des côtes du Monténégro (Adriatique Sud). Première série. Acta Adriatica 28, 121 142. Radujkovic B and Raibaut A (1989). Parasites des poissons marins des côtes du Monténégro: Copépodes. Acta Adriatica 28, 237 278. Raibaut A, Combes C and Benoit F (1998). Analysis of the parasitic copepod species richness among Mediterranean fish. Journal Marine Systems 15, 185 206. de trois poissons Sparidae (Téléostéens) Diplodus cervinus cervinus, Diplodus vulgaris et Lithognathus mormyrus pêchés dans le golfe d Annaba. Mémoire de Magister Université d Annaba: 110pp. Ramdane Z and Trilles JP (2007). Parasitic copepods (Crustacea: Copepoda) from the Algerian marine fauna. Zootaxa 1574, 49-68. Reshetnikova AV (1955). K izucheniyu parasitofauny ryb Chernogo Morya. [Contribution to the study of the parasite fauna of fishes of the Black Sea.] Trudy Karadahs koyi biolohichnoyi stantsiyi 13, 105-121. Richiardi S (1880). Catalogo sistematico dei crostacei che vivono sul corpo degli animali aquatici. Catalogo Sez. Italiana Exposizione Internazionale di Pesca in Berlino, 147 152. Rose M and Vaissiere R (1952). Catalogue préliminaire des Copépodes de l Afrique du Nord («Catalogue préliminaire des Copépodes d Algérie» : Table of contents, p. 226). Bulletin de la Société d Histoire naturelle de l Afrique du Nord 43, 164 176. Sco T and Sco A (1913). The British parasitic Copepoda. Copepoda parasitic on fishes. Ray Society Publications, London, 1, 256 pp; 2: 72 pls. Vaissiere R (1955). Description d un nouveau copépode parasite: Caligus uranoscopi. Bulletin Station Agriculture et de Pêche de Castiglione Nouvelle Série 7, 283-288. Valle A (1880). Crostacei parassiti dei pesci del mare adriatico. Bolle ino della Societ à. adriatica di scienze naturali in Trieste 6, 55 90. Van Beneden PJ (1871). Les poissons des côtes de Belgique, leurs parasites et leurs commensaux. Mémoires de l Académie Royale des Sciences, des Le res et des Beaux-Arts de Belgique 38, i-xx: 1-100. Ramdane Z (2003). Identification et indices parasitaires des Monogènes et des Crustacés