N. Mosbahi 1*, J. C. Dauvin 2, L. Neifar 1

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1 Vie et milieu - Life and environment, 2015, 65 (3): First record of the amphipods Leucothoe incisa (Robertson, 1892) and Lysianassa pilicornis (Heller, 1866) from Tunisian waters (central Mediterranean Sea) N. Mosbahi 1*, J. C. Dauvin 2, L. Neifar 1 1 Laboratoire de Biodiversité et Ecosystèmes Aquatiques, Faculté des Sciences de Sfax, Université de Sfax, BP 1171, 3038, Sfax, Tunisie 2 UNICAEN, CNRS, UMR 6143 M2C, Laboratoire Morphodynamique Continentale et Côtière, 24 rue des Tilleuls, Caen, France Corresponding author: nawfelmosbahi@hotmail.fr AMPHIPODA FIRST RECORD TUNISIA GULF OF GABES ABSTRACT. This study reports for the first time the presence of two amphipod species Leucothoe incisa (Robertson, 1892) and Lysianassa pilicornis (Heller, 1866) in the Gulf of Gabes, southeast Tunisia. Systematic descriptions of both species are presented, as well as a discussion of their ecological and geographical distribution. INTRODUCTION Amphipoda are the most diversified group among the crustaceans. Moreover, amphipods are distributed in all ecosystems worldwide including terrestrial, freshwater and marine aquatic environments. In marine environments, they have been recorded from the intertidal zone to hadal depths (Väinölä et al. 2008, Satheeshkumar 2011). Amphipods play an important role in benthic communities (Sanders 1956, Dauvin 1979, Zakhama-Sraieb 2011), and provide food for aquatic birds and economically important demersal fish as well as mammals (Bell & Harmelin-Vivien 1983, Caine 1989, 1991, Highsmith & Coyle 1992). Moreover, amphipods are used as bioindicators of marine pollution and environmental stress due to their habitat at the sediment-water interface, their relatively long life span and sedentary behaviour (Bellan- Santini 1980, 1981, De-La-Ossa-Carretero et al. 2012). The Mediterranean Sea is one of the most important hotspots of amphipod diversity in the world ocean, with more than 500 species recorded (Ruffo 1998, Väinölä et al. 2008, Coll et al. 2010, Koukouras 2010, Ruffo 2010, Christodoulou et al. 2013, Dauvin et al. 2013). The first marine amphipod inventory for Tunisian waters was given by Chevreux (1911). More recently, Zakhama- Sraieb et al. (2008, 2009) and Zakhama-Sraieb & Charfi- Cheikhrouha (2010) compiled the first complete inventory of benthic marine amphipods on the Tunisian coast, which lists 133 species belonging to 72 genera and 29 families. This inventory shows that the number of Tunisian amphipod taxa remains lower than along the neighboring Algerian coast, where 332 species are recorded (Bakalem & Dauvin 1995, Grimes et al. 2009, Bakalem et al. 2014), as well as along the Italian coast with 365 species (Ruffo 2010), the French Mediterranean coast with 299 species (Dauvin & Bellan-Santini 2002) and the Iberian Mediterranean coast with 152 species (Dela-Ossa-Carretero et al. 2010). However, the number of taxa is higher than that found on the Libyan coast, where 125 species are recorded (Ortiz & Petrescu 2007). In fact, apart from the difference in diversity of marine habitats, the length of the coastline, the decline in diversity from the west basin to the east basin (Tecchio et al. 2011), the main variability in the number of recorded species in different parts of the Mediterranean Sea is linked to the sampling effort. Thus, despite their importance in marine communities, the amphipods of the southern part of the Mediterranean Sea remain relatively poorly studied compared with those in the northern part of the Mediterranean Sea. It is clear that we still have insufficient knowledge of the amphipod fauna along the Tunisian coast. Quantitative surveys carried out between 2013 and 2014 around the Kneiss Islands (Gulf of Gabes) in the framework of the PhD thesis of N. Mosbahi have led to the collection of two amphipod species: Leucothoe incisa (Robertson, 1892) and Lysianassa pilicornis (Heller, 1866), which were recorded for the first time in Tunisian waters. MATERIALS AND METHODS The fauna was sampled with a 0.15 m diameter benthic hand corer at a depth of 30 cm, between 2013 and 2014 in the intertidal zone around the Kneiss Islands (Gulf of Gabes, Tunisia), located at latitudes N and longitudes E (Fig. 1). The collected sediment was sieved through a 1 mm square mesh and preserved in 70 % ethanol. In the laboratory, the fauna was sorted into zoological groups and then identified to species level. The specimens used for the morphological analyses were transferred into glycerin, dissected, mounted on slides, and illustrated using an Olympus BH2 microscope

2 176 N. MOSBAHI, J. C. DAUVIN, L. NEIFAR equipped with a drawing device and DIC optics. Pencil drawings were scanned and digitally inked in Adobe Illustrator using a Wacom Tablet, following the methods of Coleman (2003). RESULTS AND DISCUSSION Order Amphipoda Latreille, 1802 Suborder Senticaudata Lowry and Myers, 2013 Family Leucothoidae Dana, 1852 Genus Leucothoe Leach, 1814 Leucothoe incisa (Robertson, 1892) Description (Fig. 2) Number of specimens recorded: 36 (see Table I). Four specimens (two males and two females) have been sent to the MNHN at Paris, France. Description of males and female specimens examined Fig. 1. Location of the Kneiss Islands (Gulf of Gabes, Tunisia). Maximal length including the telson not exceeding 7 mm, slender body shape, head with a long snout, bent, segments vertically rather short. Light green with red spots on the coxal plates. Intensely red eyes very characteristic. Antennule long, shorter than antenna, with strong peduncle. Peduncle article 3 as long as flagellum articles. Coxae 1-2 short and broad; coxa 4 normally rounded. Gnathopod I with carp hooked to the end, denticulate to the front edge, small dactyl as long as 1/4 to 1/5 of propodus. Male gnathopod II with scalloped carp distal edge, propodus with a small distal tooth. Male gnathopod II longer, propodus > ½ pereon, gnathopod II propodus projecting above dactylus insertion; carpus distally based with U-shaped incision. Female gnathopod II: propodus shorter and broader, carpus less incised. Pereopods 3-7 strong, dactylus shorter than ½ of propodus. Pereopods 5-7 basis large. Uropod III with internal branch longer than the peduncle. Telson twice as long as broad. Fig. 2. Morphology of Leucothoe incisa (Robertson, 1892) (male and female) from the Gulf of Gabes, Tunisia. A, antennule and antenna (male). B, mandibular palp. C, gnathopod I. D, gnathopod II (male). E, gnathopod II (female). F, pereopod VII. G, pereopod IV. H, epimeral plates II, III. I, uropod II. J, uropod III. K, telson.

3 LEUCOTHOE INCISA AND LYSIANASSA PILICORNIS FROM TUNISIA 177 Table I. Coordinates of stations where both amphipod species Lysianassa pilicornis and Leucothoe incisa have been found between 2013 and 2014 in the intertidal zone around the Kneiss Islands (Gabes Gulf, Southern Tunisia). Stations Coordinates Individuals number Longitude Latitude Vegetation Sediment Type (E) (N) Lysianassa pilicornis Leucothoe incisa IK Zostera (Zosterella) noltei Muddy 8 IK Zostera (Zosterella) noltei Muddy 12 6 IK Zostera (Zosterella) noltei Muddy 4 13 IK Zostera (Zosterella) noltei Muddy sand 6 IK Zostera (Zosterella) noltei Muddy sand 13 4 IK Zostera (Zosterella) noltei Muddy sand 6 IK Zostera (Zosterella) noltei Muddy 4 IK Zostera (Zosterella) noltei Muddy 7 Habitat This species has been recorded in the intertidal zone (down to 2 m water depth) in Zostera (Zosterella) noltei Horneman meadows with sediments mainly composed of mud and muddy sand. Leucothoe incisa is found mainly in sand but sometimes in mud in water depths of 8-40 m, and has been recorded at 370 m offshore Corsica (Ruffo 1989). It has been found from the Algerian coast in se veral types of substratum (mud, sandy mud, fine sand and sandy gravel) at water depths of 8 to 63 m (Bakalem & Dauvin 1995). Distribution Leucothoe incisa is a cosmopolitan species, present in the Atlantic and Pacific Oceans (Ruffo 1989, 1998). In the Mediterranean Sea, this species is recorded on the French coast (Marseille, Villefranche-sur- Mer and Corsica), around the Balearic Islands, in the Adriatic Sea, and in Algeria (Annaba and Bou Ismail) (Chevreux 1911, Bakalem & Dauvin 1995). Order Amphipoda Latreille, 1802 Suborder Senticaudata Lowry and Myers, 2013 Family Lysianassidea Dana, 1849 Genus Lysianassa Milne-Edwards, 1830 Lysianassa pilicornis (Heller, 1866) Description (Fig. 3) Number of specimens recorded: 47 (see Table I). Four specimens (two males and two females) have been sent to the MNHN at Paris, France. Fig. 3. Morphology of Lysianassa pilicornis (Heller, 1866) (male and female) from the Gulf of Gabes, Tunisia. A, antennule and antenna (male). B, antennule (female). C, antenna (female). D, maxilliped. E, mandibular palp. F, gnathopod I. G, gnathopod II. H, pereopod IV. I, pereopod VI. J, pereopod VII. K, uropod II. L, uropod III. M, telson.

4 178 N. MOSBAHI, J. C. DAUVIN, L. NEIFAR Description of males and females specimens examined The maximum length including the telson of males is 7 mm (females do not exceed 12 mm). Head with lateral protruding rounded lobes. Males: antennule is shorter than antenna, flagellum with 20 articles. Antenna shorter than body length, flagellum without calceoli, each article with two tufts of long setae. Females: antennular peduncle longer than flagellum, article 1 with two distal teeth, the outer longest, flagellum with articles, accessory flagellum 5-articulated; antenna slender, flagellum longer than peduncle with 14 articles. Maxilliped outer plate strongly dilated, exceeding distal margin of second article. Coxa 4 wide. Posterior margin of epimeral plate 3 truncated. Gnathopod 2 carpus and propodus strong. Pereopod 6 posterior margin of basis distinctly constricted distally, posterodistal lobe truncated; pereopod 7 basis wide, posterior margin straight, posterodistal lobe slightly truncated. Uropod 2-3 strong and fleshy with rami subequal. Telson rounded to the distal edge. Lysianassa pilicornis is characterised by brown eyes, dorsally white with brown spots, laterally orange and scarlet red. Habitat This species has been recorded in the intertidal zone (down to two metre depth) in Zostera (Zosterella) noltei Hornemann meadows with sediments mainly composed of mud and muddy sand. Lysianassa pilicornis has been recorded in a variety of substrates in shallow waters (0-70 m), on Posidonia oceanica (Linnaeus) Delile, 1813 mea dows, photophilous algae, coralline bottoms and coarse sand (Ruffo 1982). Distribution This Atlantic species ranges from Portugal to South Africa and is present in both western and eastern basins of the Mediterranean Sea (Ruffo 1982). It has been reported in Annaba Bay on Posidonia oceanica meadows between 5 and 6 m water depth (Bakalem & Dauvin 1995). Acknowledgements. The authors thank A Chaabane who kindly helped in drawing figures, M Carpenter for the English revision. They thank also anonymous reviewers for their useful suggestions and their constructive comments. REFERENCES Bakalem A, Dauvin JC Inventaire des Crustacés Amphipodes (Gammaridea, Caprellidea, Hyperiidea) des côtes d Algérie : essai de synthèse. Mésogée 54: Bakalem A, Dauvin JC, Grimes S New marine amphipod records on the Algerian coast. J Mar Biol Ass UK 94: Bell JD, Harmelin-Vivien M Fish fauna of French Mediterranean Posidonia oceanica seagrass meadows. II. Feeding habits. Téthys 11: Bellan-Santini D Relationship between populations of amphipods and pollution. Mar Poll Bull 11: Bellan-Santini D Influence des pollutions sur les peuplements d amphipodes dans les biocénoses des algues photophyles. Téthys 10: Caine EA Caprellid amphipod behavior and predatory strikes by fish. J Exp Mar Biol Ecol 126: Caine EA Caprellid amphipods: fast food for the reproductively active. J Exp Mar Biol. Ecol. 148: Chevreux E Campagne de la Melita. Les amphipodes d Algérie et de Tunisie. Mém Soc Zool Fr 23: Christodoulou M, Paraskevopoulou S, Syranidou E, Koukouras A The amphipod (Crustacea: Peracarida) fauna of the Aegean Sea, and comparison with those of the neighbouring seas. J Mar Biol Ass UK 93: Coleman O Digital inking. How to make perfect line drawings on computers. Org Divers Evol Elect Suppl 14: 1-14, senckenberg.de/odes/03-14.htm Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F et al The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5(8): e Dauvin JC Recherches quantitatives sur le peuplement des sables fins de la Pierre Noire, baie de Morlaix, et sur sa perturbation par les hydrocarbures de l Amoco Cadiz. Thèse de Doctorat, Université Pierre et Marie Curie (Paris VI), Paris, France. Dauvin JC, Bellan-Santini D Les Crustacés Amphipodes Gammaridea benthiques des côtes françaises métropolitaines : bilan des connaissances. Crustaceana 75: Dauvin JC, Grimes S, Bakalem A Marine Biodiversity on the Algerian Continental Shelf (Mediterranean Sea). J Nat Hist 47: De-La-Ossa-Carretero JA, Dauvin JC, Del-Pilar-Ruso Y, Gimenez-Casalduero G, Sanchez-Lizaso JL Inventory of benthic amphipods from fine sand community of comunidad Valenciana coast (Spain), Western Mediterranean, with new records. J Mar Biol Ass UK, Mar Biodiv Rec: e119:1-10. De-La-Ossa-Carretero JA, Del-Pilar-Ruso Y, Gimenez-Casalduero F, Sanchez-Lizaso JL, Dauvin JC Sensitivity of amphipods to sewage pollution. Estuar Coast Shelf Sci 96: Grimes S, Dauvin JC, Ruellet T New records of marine amphipod fauna (Crustacea: Peracarida) on the Algerian coast. J Mar Biol Ass UK, Mar Biodiv Rec: e134:1-9. Highsmith RC, Coyle KO Productivity of arctic amphipods relative to gray whale energy requirements. Mar Ecol Prog Ser 83: Koukouras A Check-list of marine species from Greece. Aristotle University of Thessaloniki. Assembled in the framework of the EU FP7 PESI project ( Ortiz M, Petrescu I The marine Amphipoda (Crustacea: Gammaridea) of the Republic of Libya, southeastern Mediterranean. Trav Mus Nat Hist Nat Grigore Antipa 50: Ruffo S ed The Amphipoda of the Mediterranean. Part 1. Gammaridea (Acanthonotozomatidae to Gammaridae). Mém Inst Océano Monaco 13: Ruffo S ed The Amphipoda of the Mediterranean. Part 2. Gammaridea (Haustoriidae to Lysianassidae). Mém Inst Océano Monaco 13:

5 LEUCOTHOE INCISA AND LYSIANASSA PILICORNIS FROM TUNISIA 179 Ruffo S ed The Amphipoda of the Mediterranean. Part 4. Mém Inst Océano Monaco 13: Ruffo S Amphipoda. In Relini G ed. Checklist della Flora e della Fauna dei Mari Italiani (Parte II). Biol Mar Medit 17(Suppl 1): Sanders H The biology of marine bottom communities. Bull Bingham Ocean Coll 15: Satheeshkumar P Intertidal amphipods (Crustacea: Amphipoda) from Pondicherry Mangroves, Southeast Coast of India. J Nat Sci Res 1: Tecchio S, Ramirez-Llodra E, Sardà F, Company B Biodiversity patterns of deep-sea benthic megafauna on western and central Mediterranean basins. Sci Mar 75: Väinölä R, Witt JDS, Grabowski M, Bradbury JH, Jazdzewski K, Sket B Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia 595: Zakhama-Sraieb R, Sghaier YR, Charfi-Cheikhrouha F Les Caprelles (Crustacea: Amphipoda) des côtes tunisiennes. Bull Soc Zool Fr 133: Zakhama-Sraieb R, Charfi-Cheikhrouha F First record of two lessepsian amphipods in Tunisia: Elasmopus pectenicrus and Stenothoe gallenis. J Mar Biol Ass UK 90: Zakhama-Sraieb R, Sghaier YR, Charfi-Cheikhrouha F Amphipod biodiversity of the Tunisian coasts: update and distributional ecology. J Mar Biol Ass UK, Mar Biodiv Rec: e155:1-9. Zakhama-Sraieb R Amphipodes marins de la Tunisie : systématique, diversité et approche écologique. Thèse de Doctorat en Sciences Biologiques. Université de Tunis El Manar, Tunisie. Received on June 23, 2015 Accepted on October 9, 2015 Associate editor: J Orignac

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