Fishes in lagoons and estuaries in the Mediterranean. 3B, Migratory fish 9781786303912, 1786303914

Table of contents :
Content: Foreword viiPreface ixIntroduction xiChapter 1. Mullidae Gunther, 1859 11.1. Mullus Linnaeus, 1758 31.1.1. Mullus barbatus barbatus Linnaeus, 1758 51.1.2. Mullus surmuletus Linnaeus, 1758 231.2. Bibliography 41Chapter 2. Pleuronectidae Norman, 1934 592.1. Platichthys Girard, 1854-1855 [1856] 592.1.1. Platichthys flesus (Linnaeus, 1758) 602.2. Bibliography 70Chapter 3. Soleidae Norman, 1934 753.1. Solea Quensel, 1806 773.1.1. Solea aegyptiaca Chabanaud, 1927 793.1.2. Solea senegalensis Kaup, 1858 853.1.3. Solea solea (Linnaeus, 1758) 913.2. Bibliography 110Chapter 4. Sparidae Jordan and Evermann, 1898 1294.1. Diplodus Rafinesque, 1810 1304.1.1. Diplodus annularis (Linnaeus, 1758) 1354.1.2. Diplodus puntazzo (Cetti, 1777) 1484.1.3. Diplodus sargus sargus (Linnaeus, 1758) 1614.1.4. Diplodus vulgaris (Geoffroy Saint-Hilaire, 1817) 1804.2. Lithognathus Swainson, 1839 1944.2.1. Lithognathus mormyrus (Linnaeus, 1758) 1944.3. Sarpa Bonaparte, 1831 2064.3.1. Sarpa salpa (Linnaeus, 1758) 2064.4. Sparus Linnaeus, 1758 2174.4.1. Sparus aurata Linnaeus, 1758 2184.5. Bibliography 240Glossary 273Index 281

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

Series Editor Françoise Gaill

Fishes in Lagoons and Estuaries in the Mediterranean 3B Migratory Fish

Mohamed Hichem Kara Jean-Pierre Quignard

First published 2019 in Great Britain and the United States by ISTE Ltd and John Wiley & Sons, Inc.

Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the Copyright, Designs and Patents Act 1988, this publication may only be reproduced, stored or transmitted, in any form or by any means, with the prior permission in writing of the publishers, or in the case of reprographic reproduction in accordance with the terms and licenses issued by the CLA. Enquiries concerning reproduction outside these terms should be sent to the publishers at the undermentioned address: ISTE Ltd 27–37 St George’s Road London SW19 4EU UK

John Wiley & Sons, Inc. 111 River Street Hoboken, NJ 07030 USA

www.iste.co.uk

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© ISTE Ltd 2019 The rights of Mohamed Hichem Kara and Jean-Pierre Quignard to be identified as the authors of this work have been asserted by them in accordance with the Copyright, Designs and Patents Act 1988. Library of Congress Control Number: 2019935017 British Library Cataloguing-in-Publication Data A CIP record for this book is available from the British Library ISBN 978-1-78630-391-2

Contents

Foreword . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

vii

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

ix

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

xi

Chapter 1. Mullidae Günther, 1859 . . . . . . . . . . . . . . . . . . . . . . .

1

1.1. Mullus Linnæus, 1758 . . . . . . . . . . . . . . 1.1.1. Mullus barbatus barbatus Linnæus, 1758 1.1.2. Mullus surmuletus Linnæus, 1758 . . . . . 1.2. Bibliography . . . . . . . . . . . . . . . . . . . .

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3 5 23 41

Chapter 2. Pleuronectidae Norman, 1934 . . . . . . . . . . . . . . . . . . .

59

2.1. Platichthys Girard, 1854–1855 [1856] . . . . . . . . . . . . . . . . . . . . 2.1.1. Platichthys flesus (Linnæus, 1758) . . . . . . . . . . . . . . . . . . . 2.2. Bibliography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

59 60 70

Chapter 3. Soleidae Norman, 1934 . . . . . . . . . . . . . . . . . . . . . . .

75

3.1. Solea Quensel, 1806. . . . . . . . . . . . 3.1.1. Solea aegyptiaca Chabanaud, 1927 3.1.2. Solea senegalensis Kaup, 1858 . . . 3.1.3. Solea solea (Linnæus, 1758) . . . . 3.2. Bibliography . . . . . . . . . . . . . . . .

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Chapter 4. Sparidae Jordan and Evermann, 1898 . . . . . . . . . . . . .

129

4.1. Diplodus Rafinesque, 1810 . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.1. Diplodus annularis (Linnæus, 1758) . . . . . . . . . . . . . . . . . .

130 135

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

4.1.2. Diplodus puntazzo (Cetti, 1777) . . . . . . . . . . . 4.1.3. Diplodus sargus sargus (Linnæus, 1758) . . . . . . 4.1.4. Diplodus vulgaris (Geoffroy Saint-Hilaire, 1817) . 4.2. Lithognathus Swainson, 1839 . . . . . . . . . . . . . . . 4.2.1. Lithognathus mormyrus (Linnæus, 1758). . . . . . 4.3. Sarpa Bonaparte, 1831 . . . . . . . . . . . . . . . . . . . 4.3.1. Sarpa salpa (Linnæus, 1758) . . . . . . . . . . . . . 4.4. Sparus Linnæus, 1758 . . . . . . . . . . . . . . . . . . . 4.4.1. Sparus aurata Linnæus, 1758. . . . . . . . . . . . . 4.5. Bibliography . . . . . . . . . . . . . . . . . . . . . . . . .

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148 161 180 194 194 206 206 217 218 240

Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

273

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

281

Foreword

Lagoons, deltas and estuaries are by definition transition zones and represent a distinctive element of the Mediterranean shoreline. In days of old, people used to come here to catch an abundance of fish, and this coastal fishing – practiced behind the shoreline in the channels of the salt marshes and in the estuary mouths – was at that time more highly prized than fishing in the open sea. Nowadays, although lagoon fishing represents only a small fraction of annual fish catches in the Mediterranean, estuarine and lagoon habitats continue to play a major role, be it as nurseries or in supporting an often-intensive mariculture, such as in Egypt, Italy and Greece. This academic publication, patiently compiled by two eminent ichthyologists who are familiar with both shores, covers in three volumes the ichthyofauna of 303 lagoons and estuaries in the Mediterranean region, from the coastline of the Alboran Sea to Anatolia. Volume 1 outlines the vast geographical, geomorphological, hydrological, physicochemical and also historic diversity of Mediterranean lagoons, a diversity that has led to marked differences in the biology, reproduction, genetics, feeding and behavior of lagoon fishes. Furthermore, the reader will find illustrated descriptions of 47 lagoon and estuarine species that have been studied, with a detailed discussion of systematics and of issues relating to biogeography, reproductive and feeding strategies, genetics and biodiversity. Throughout this work, a distinction is drawn between sedentary and migratory species – those that come and go each year between the lagoons where they find refuge, and the sea where they reproduce. However, the dividing line between these two worlds can sometimes be tenuous, and the authors introduce many central issues that remain unresolved, relating to, for instance, the genetic differentiation and adaptation (or preadaptation) between migratory and sedentary stocks, or the respective contributions made to the local fisheries by the lagoon nurseries and the marine shore area. The ichthyofauna of the studied sites is

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remarkably discrete: of the 249 species inventoried in 45 representative estuaries and lagoons, it will be noted that only 15 are found in 50% or more of the studied sites. In the face of increasing anthropic pressures on the Mediterranean coast, already weakened by concrete urban development and its pathogenic wastes, by erosion, climate change, industrial and agricultural discharges into the sea, irresponsible mass tourism and the arrival of invasive Indo-Pacific species, the conservation and sustainable management of these areas and of lagoon fishing take on a certain urgency. The authors consider these topics at some length; their views are invaluable, drawn from their long experience in the field; I hope that many practitioners will find inspiration in them. Because of the variety and expert knowledge of the themes covered, to its extensive bibliography and illustrations, this work is sure to become indispensable to the technicians and managers involved in fisheries and Mediterranean aquaculture. On a wider level, it will interest the many students and researchers working in ichthyology. Frédéric BRIAND Director General CIESM Mediterranean Science Commission

Preface

The conservation of the natural and economic heritage represented by Mediterranean lagoons and estuaries and the associated adjacent areas (wetlands, reed beds, sansouires and salt marshes) calls for an in-depth scientific knowledge of the past and present state and the functioning of these environments, and particularly of their plant and animal components. It is on this basis that appropriate management policies can be formulated. Classed as transition zones between land and sea, these special ecosystems are matters of concern for both scientists and managers. The former group has accumulated significant knowledge of their abiotic characteristics and their functioning. They are now investigating the individuality of the resident populations, their interactions with the adjoining ecosystems and their future in the context of climate change. The latter group is seeking scientific and technical tools that will enable them to use these environments to their full potential, taking into account the increasing anthropic pressures. In this series of books, divided into three stand-alone, complementary volumes, we have brought together scientific knowledge amassed over nearly two centuries on the fishes of the Mediterranean lagoons and estuaries. This summary has been compiled from documents published in local and international reviews and in general or specialized bioecological works on pure and applied ichthyology. We are, however, conscious that an entire fringe of works concerning lagoon and estuarine fishes has been omitted, this being the “gray literature” consisting of expert reports, academic projects and theses, etc. The first volume, entitled Diversity, Bioecology and Exploitation, is a non-exhaustive approach to the characteristics of lagoons and estuaries, from a “geo-geographical”, hydrological and general bioecological viewpoint, and also

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looking at the ecophysiology and behavior of the fishes that live there. The general features of the exploitation and management of fish resources are also considered. The second volume, Sedentary Fish, is devoted to the fishes that are so named because, being very euryvalent, they live out their entire lifecycle inside lagoons and estuaries. These fishes are not all specific to these environments; some have their counterparts in the sea or in fresh water. The third volume, Migratory Fish, is concerned with fishes that, after spending time in lagoons, are obliged to return to their native marine or river environment to complete their lifecycle (genesic migrations), the physicochemical conditions in lagoons and estuaries (temperature, salinity, turbidity, etc.) being incompatible with the water properties required for their reproduction. Strictly hydroclimatic events can also be at the origin of migratory journeys. The data provided in volumes two and three of this series of books are at three taxonomic levels: family, genus and species. Those concerning family and genus are relatively brief and general, while those relating to species are exhaustive and very detailed, for every aspect dealt with: systematics, genetics, phylogenesis, ecology, biology, behavior, etc. This summary has been designed to permit rapid and comprehensive access to the body of scientific knowledge on lagoon and estuarine fishes and their sources. These data are indispensable in order to develop projects of research, infrastructure, management and conservation concerning these environments and their populations. Mohamed Hichem KARA Jean-Pierre QUIGNARD September 2018

Introduction

Unable to carry out their entire lifecycle in lagoons and estuaries, as sedentary species do, so-called “migratory” species make regular movements, at relatively stable dates, which are predictable from one year to the next, between the sea and the lagoon, and vice versa, or between lagoons and freshwater (Hervé and Bruslé, 1979; Lasserre, 1989; Quignard and Zaouali, 1980, 1981; Quignard, 1984, 1994). Egg laying takes place either in the sea or in freshwater, but never in lagoons or estuaries. In this introduction, we will sketch the main lines that characterize the ecology, biology and the exploitation of this guild, before providing a detailed description, species by species. The list of species retained in this context is justified by their frequency in these environments and/or due to their confirmed abundance in the few sites they occupy. It is important to know that many erratic occupants of lagoons and estuaries, still referred to as “casual migrants”, generally make short-lived incursions into these environments. These “episodic visitors” represent about 70% of the species we have mentioned (sedentary, migratory and occasional). Their frequency in the environments studied does not exceed 9% and is generally poorly represented (sometimes only one individual) (see Volume 1). Often, they are carnivorous ichthyophagous, as the Belone belone garfish, the Scombrus mackerel, etc., which chase the schools of small clupeidae Sardina pilchardus, of engraulids Engraulis sp., but also the atherine Atherina hepsetus, the red mullet Mullus sp., etc. In addition to these species, there are some exotic lessepsiens and herculeans whose presence is linked to more or less important geoecological manipulations (modifications of the channels connecting the sea to the lagoons, immersion of artificial reefs, opening of the Suez Canal, etc.) and general hydroclimatic upheaval. From 97 fish censuses carried out in 45 Mediterranean lagoons (see Volume 1), the best-represented families of migrating fish are listed in descending order according

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to their occurrence in the censuses: Anguillidae, Moronidae, Mugilidae, Sparidae, Soleidae: – eight species are present in at least 75% of the environments considered (Anguilla anguilla, Dicentrarchus labrax, Liza aurata, Sparus aurata, Mugil cephalus, Solea solea, Chelon labrosus, Liza ramada); – seven species in at least 50% (Liza saliens, Diplodus annularis, D. sargus, Engraulis encrasicolus, Sarpa salpa, Belone belone, Mullus surmuletus); – eight species in at least 25% (Pomatoschistus minutus, Platichthys flesus, Diplodus vulgaris, Lithognathus mormyrus, Diplodus puntazzo, Mullus barbatus, Boops boops, Scomber scombrus). It is generally accepted that migration from the sea to the lagoon is induced by trophic and “anti-predator” needs, insofar as shallow lagoons are not favorable for the penetration of large predators, and intralagoonal algal and phanerogamic vegetation make “sight hunting” difficult. Lagoon-sea “outmigration” is, in turn, induced by reproductive needs and/or thermal constraints, and probably by other unidentified causes. The specific richness of lagoon-migrating fish varies from one environment to another and depends on: 1) the species richness of the adjacent littoral zone and their morphological and behavioral type; 2) the structure of the channels connecting the lagoon to the sea; 3) the physical, chemical and other characteristics of lagoons; 4) the hydrodynamics of sea–lagoon and lagoon–sea exchanges. Occupation of lagoons and migration phenology In shallow lagoons (approximately 1 m), migrants are generally 0+ young individuals, larvae and juveniles depending on the species, whereas in deep lagoons, individuals of all ages make such displacements, but 0+ are still usually the most abundant age group. Apart from intrinsic lagoon factors, the success of the recruitment of migratory species depends on the success of breeding at sea, hydrographic conditions (survival and dispersal of larvae), the topographic and architectural qualities of the communication channels between the sea and the lagoon and the extent of the volume of water coming out from the lagoons to the sea.

Introduction

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Only a fraction of the marine population migrates to the lagoons (Quignard, 1984; Quignard and Zaouali, 1980, 1981; Lasserre, 1989; Mercier et al., 2012), but we have no estimate of the relative importance of this “migratory phase” in relation to the original marine stock, nor do we have knowledge about the determinism and the “laws” governing fish migrations between sea and lagoons. For example, what is the share that depends on the fish and which part is related to the conditions at sea and/or the lagoon? In other words, within the same species, why do some individuals move, while others remain at their original marine territory? Within a marine or a freshwater population, are there any sedentary or nomadic “genetic lineages” that regularly extend their distribution area to lagoons? Over the past 15 years, genetic, molecular and mineralogical studies (microchemistry of otoliths) have begun to provide interesting information about Mediterranean lagoon-thalassic migrants: the visit of different nurseries by the Gilthead seabream S. aurata (Mercier et al., 2012; Tournois et al., 2013, 2017) and by the eel A. anguilla (Panfili et al., 2012); the return periodicity to the lagoon for the same Gilthead seabream population (Mercier et al., 2012); the independence of lagoon recruitment from nesting sites by the sole S. solea (Morat et al., 2009); differentiation (the existence of exclusive alleles in lagoon migrants) and the genetic adaptation of the Gilthead seabream (Chaoui et al., 2012; Guinand et al., 2016) and the sea bass (Lemaire et al., 2000, 2004–2005; Guinand et al., 2015) to local lagoon conditions; etc. At the genetic level, the question is whether these divergences are premigratory or whether they result from “ongoing” natural selection processes acting on the new recruits that colonize the lagoons, causing an increase in the frequency of the alleles that allows migrants to become adapted to lagoon systems. The return to sea (outmigration) of marine migrants is made against the current during the entry of marine waters by the inlet. These trips are made by fish of all ages having stayed for a few weeks, a few months or a few years (eel) in the lagoons. For each species, they occur in several waves of groups of individuals that are often of the same size and sometimes the same sex, during a fairly constant period, from one year to another. However, we should emphasize that returning to the sea does not always have a “reproductive” purpose, since it involves juveniles that are far from sexual maturity. Perhaps, this could be induced by fall lagoon hydroclimatic conditions being more unfavorable than those at sea (Hotos et al., 2000; Katselis et al., 2007) or by other yet unidentified factors. Lifespan and growth The lifespan and size of migratory species are much higher than those of sedentaries, most of whom are annual or subannual. For example, 12-year-old Gilthead seabreams visit the Mirna estuary in Croatia (Kraljević and Dulčić 1997),

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

11-year-old eels are found in the Commacchio lagoon in Italy (Rossi and Colombo, 1976) and 10-year-old sea basses live on the Tunisian coasts (Bouain, 1977). Migrants with a relatively long lagoon stay in comparison to their lifespan, such as the eel A. anguilla, the common goby P. minutus, two semelparous species, reach their maximum size in lagoons, before moving to lay at sea. As for other migratory species, likely to carry out several relatively short lagoon stays throughout their life, the comparative approach regarding the share of their growth at sea and in the lagoon, for the 0+ and especially for adults, is harder to pin down. Microchemical techniques applied to otoliths could teach us more. The growth performance of migratory species is often judged to be better in lagoons than at sea, an opinion which is not shared by all researchers, some of whom describe these environments as “deadly traps” (Boutière, 1974) and even as “places of death” (Chauvet, 1986). Differences in growth also exist between neighboring lagoons (Bruslé and Cambrony 1992, Cambrony 1983, Quignard et al., 1984; Mosconi and Chauvet, 1990; Isnard, 2015), and even within the same lagoon among different biogeographical sectors (Escalas et al., 2015). Taking into account the “adaptive strategies” deployed by the species occupying lagoon ecosystems (Amanieu and Lasserre, 1982), the chances for better survival and for better growth vary considerably depending on lagoons, intra-lagoonal sites (marine sectors and continental sectors) and on the years (Amanieu, 1973). As a result, no “uniform” scenario can be drawn and the “lagoon advantage” regarding individual growth cannot always be retained. Comparative data between “sea-lagoons”, carried out at the same time (same period, same year), at marine and lagoon sites close to each other, are very little documented or entirely missing. Nevertheless, we can observe that certain lagoons or intralagoonal zones, especially those rich in continental supplies, can help postlarvae and juveniles to have a somatic condition beneficial to their survival and to their subsequent development at sea (Isnard et al., 2015). However, it is still difficult to assess the impact of the benefits gained by these juveniles on the course of their adult lives. However, Lasserre and Labourg (1974) admitted that the sizes reached after a lagoon stay had repercussions on the dynamics of marine “stock”. Shallow lagoons, generally enriched with continental supplies, provide fish larvae and juveniles with better growth conditions than marine lagoons, especially deep ones. These shallow lagoons are often very rich in food and welcome yearly juveniles returning to sea the following year. They, therefore, constitute hot spots of fish larvae and juveniles of very good quality, which will move on and populate the sea, but also the surrounding deep lagoons that also welcome individuals older than 1 year. Shallow lagoons thus contribute to the supply of deep lagoons with good juveniles that, in turn, indirectly provide them with recruitment of new good larvae

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and juveniles born of good male and female spawners which reproduce at sea. The interactive loop, sea–shallow lagoon–deep lagoon–sea, is thus closed. Knowledge of the size and geographical area concerned by this type of interaction is essential for the reasoned management of fishery. Other biological and behavioral traits Migrants are gonochoric, with the exception of Sparidae, and all spawn at sea. Nevertheless, “lagoon egg-laying” has been observed in Gilthead seabream kept in cages in the Messolonghi–Etoliko lagoon (Dimitriou et al., 2007). Unlike sedentary species, their first sexual maturity is usually late (later than 1 year of age). Their eggs are laid in open water; are pelagic, small, very numerous (thousands or even millions) and are not subject to parental care. With the exception of the eel and the P. minutus goby, which only participate in one spawning season in their life (semelparous spawners), all migrants are iteroparous spawners that participate in several spawning seasons during their lifetime. The emission of gametes takes place in large promiscuity, within groups or schools of fish. For the P. minutus, the only migratory nesting species, a female lays successively in the nest of several males (polyandry); thus, there is a formation of ephemeral couples, limited to the duration of the act of laying eggs. While the migratory circuit and spawning sites of eels are becoming better and better known (Amilhat et al., 2016), their spawning behavior still remains mysterious. With the exception of P. minutus, a nesting fish which cares for its eggs, all migrants have a much higher oocyte fecundity than lagoonsedentary species. For example, the absolute fecundity of the flounder is 325,800– 1,450,000 (25–45 cm TL) (Vianet, 1985), whereas it is 50,000–272,000 (36–56 cm TL) for the sea bass (Kara, 1997). For the breeding Gilthead seabream, the relative fecundity is 1,000,000–2,000,000/kg (Zohar et al., 1984). If the lagoon-sedentary species, characterized by their small maximum size, exploit the small planktonic, nectonic and benthic (endogenous and epigeic) preys, the migrants whose individuals have a very wide range of sizes have a dietary behavior which differs largely from one to the other, ranging from micro- to macrophagy of invertebrates and vertebrates. Whether in deep or in laminar lagoons, or in estuaries, they exploit all levels, from the substrate’s bacterial film (some mullets) to mollusks (seabreams), crustaceans, fish (sea bass) and plants for the salema S. salpa, the only lagoon-migratory herbivore. They are also interested in all sizes and all forms of prey (planktonic, endo- and epibenthic, sessile or vagile, nectonic), according to their size and needs. Less subject to predation than sedentary species, they use and export lagoon energetic resources to the sea and to freshwater. The rivalry for the access to prey between individuals in the migratory guild is relatively small, given the relatively high degree of specialization, especially among

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large specimens, be they juveniles or adults. On the other hand, there is significant trophic competition between sedentary and migratory species at the larval, postlarval and juvenile stages (Gisbert et al., 1996; Shaiek et al., 2015). A strong contribution to fishery resources Migratory species represent the main fish richness of lagoons whose production amounts to 156,000 tons/year (Cataudella et al., 2015), that is to say, 17–20% of the total fish caught in the Mediterranean. The yield per hectare is estimated at 118 kg/year (Pérez-Ruzafa and Conceptión, 2012). The main species fished are the eel, the mullet (Liza sp., C. labrosus, M. cephalus), the Gilthead seabream and the sea bass, but in different proportions depending on climatic and geographical zones. In the lagoons of the eastern Mediterranean, the eel production is small and the catches are dominated by various Sparidae, whereas in western lagoons, and especially to the north, these can reach 80% of production. The seasonal rhythmicity of the “coming and going” of migratory fish is used for capturing them at the weirs, using fyke nets, eel baskets and secondarily globes, but it is essentially the individuals leaving the lagoons that are fished, particularly in Italy (De Angelis, 1960; Ravagnan, 1978; Kapesky and Lasserre, 1984), Tunisia (Chauvet, 1984, 1988), Greece (Pearce and Crivelli, 1994; Rosecchi and Charpentier, 1995) and Algeria (Chaoui et al., 2006). For several years, a decrease in lagoon halieutical production has been observed (Skinner and Zalewski 1995; Crespi 2002; Chaoui et al., 2006; Djabou et al., 2012; Zoulias et al., 2014). In the face of this depletion, it has sometimes been sought to strengthen the stock of certain species with fish farming products (the sea bass at Bages-Sigean and at Thau in France, the Gilthead seabream at Bardawil in Egypt). The second attitude that has often been adopted has aimed at conservation, thus prohibiting fishing during a period of the year (North Tunis, Mauguio and other lagoons). With regard to the eel, a plan to ensure that at least 40% of adult individuals leave the lagoons in order to lay their eggs at the Sargasso Sea has been implemented not only to maintain, but to re-establish stocks. We should bear in mind that other fishery products are important resources for fishermen in Mediterranean lagoons. This is the case of the salted and dried eggs obtained from the M. cephalus flathead grey mullet, commonly known as the striped mullet or common mullet. This product sells for around 200 euros/kg regardless of the country (Cataudella et al., 2015). The fishery management of lagoonal ichthyological resources is complicated due to the existence of specific “intra-lagoonal” stocks of sedentary fish (silversides, gobies, blennies, etc.), which are relatively independent from marine stocks, and stocks of migratory species (mullets, Gilthead seabreams, sea basses, etc.) exploited

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in lagoons and at sea (shared fisheries). In the latter case, marine fisheries have an impact, not only on the marine part of the stock, but also on the lagoon part, since the lagoon stock comes from the sea (recruitment from the marine stock). Thus, excessive fishing in the lagoon can only aggravate the situation of an overfished marine stock. It is therefore at interactive fisheries where the mutual impact can be very strong, especially in areas where the lagoon system is highly developed and can, therefore, temporarily accommodate a significant part of the fundamental marine stock of fish of one or more species (recruitment of migrants). Under these conditions, a “concerted” management of the two substocks, marine (fundamental) and lagoonal, is recommended because, until now, the manager has not been able to access reliable information regarding the proportion of migratory individuals in relation to the stock of “sedentary marine” individuals. Nevertheless, using the microchemistry of otoliths, Tournois et al. (2017) have shown that lagoon nurseries contribute more to the local fishery of the Gulf of Lion than the inshore marine area does. In addition, the results of recent works on population genetics tend to show some divergence, from this perspective, between marine and lagoonal stocks of sea bass (Lemaire et al., 2000), Gilthead seabreams (Chaoui et al., 2012), common sole (Murten et al., 2009) and anchovies, among which two species can be recognized (Borsa et al., 2004). Let us observe that the eel, a long-term thalassotoc migrant fish found in lagoons and in freshwater, is a special case. This species is only subject to intralagoonal fishing. Therefore, its management is essentially lagoonal (without forgetting the fresh water) and should seek to ensure the return to sea of a number of spawners compatible with the renewal of the Atlanto-Mediterranean stock. In the world’s lagoons, aquaculture produces about 3.4 million tons (5.7% of global aquaculture production). In the Mediterranean, most of the fish farm production in lagoons is made up of typical migratory lagoonal species (sea bass, Gilthead seabream). In 2008, it reached 66,738 tons for the sea bass and 133,026 tons for the seabream (FAO, 2010). In Egypt, the breeding of mugilids (M. cephalus, L. ramada, L. seheli, L. saliens, L. aurata, Creni mugil sp.) is important, with a production of 986,820 tons (GAFRD, 2012). Most of this activity is based on the fishing of fish fingerlings in lagoons in order to feed livestock farms. However, the impact of this practice on the future of lagoon and marine stocks has not been evaluated yet. As a result, the precautionary principle was adopted by this country as a protective measure prohibiting this practice. Status and threats Finally, among the lagoon-estuarine species, some are threatened, according to the red lists of Mediterranean fish species (Abdul-Malak et al., 2011). The A.

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anguilla is in critical danger of extinction, the P. minitus is vulnerable and the sea bass D. labrax is near threatened. However, these threats concern fewer species than the sedentary guild (of which there are nine in total). Bibliography ABDUL MALAK D., LIVINGSTONE S.R., POLLARD D. et al., “Overview of the Conservation Status of the Marine Fishes of the Mediterranean Sea”, IUCN, Gland, Switzerland and Malaga, Spain, VII: p. 61, 2011. AMANIEU M., “Écologie et exploitation des étangs et lagunes saumâtres du littoral méditerranéen français”, Annales de la Société royale zoologique de Belgique, 103 (1): 79–94, 1973. AMANIEU M., LASSERRE G., “Organisation et évolution des peuples lagunaires”, Oceanology Acta V, suppl. 4: 201–213, 1982. AMILHAT E., AARESTRUP K., FALIEX E., SIMON G., WESTERBERG H., RIGHTON D., “First evidence of European eels exiting the Mediterranean Sea during their spawning migration”, Scientific Reports, 6 (21817), 2016. BORSA P., COLLET A., DURAND J.D., “Nuclear-DNA markers confirm the presence of two anchovy species in the Mediterranean”, Comptes rendus de l’Académie des Sciences (Biologie), 327: 1113–1123, 2004. BOUAIN A., Contribution à l’étude morphologique, anatomique et biologique de Dicentrarchus labrax (Linné, 1758) et Dicentrarchus punctatus (Bloch, 1792) des côtes tunisiennes, Specialized PhD thesis, Faculté des Sciences de Tunis, 1977. BOUTIERE H., “Milieux hyperhalins du complexe lagunaire de Bages-Sigean : l’étang du Doul”, Vie et Milieu, 24 (2): 355–378, 1974. BRUSLE J., CAMBRONY M., “Les lagunes méditerranéennes : des nurseries favorables aux juvéniles de poisons euryhalins et/ou des pièges redoutables pour eux ? Analyse critique de la croissance des populations de muges de plusieurs étangs saumâtres du Languedoc-Roussillon, au cours de leur première année de vie”, Vie et Milieu, 42 (2): 193–205, 1992. CAMBRONY M., Recrutement et biologie des stades juvéniles de mugilidés dans trois milieux lagunaires du Roussillon et du Narbonnais (Sases-Leucate, Lapalme, Bourdigou), Postgraduate thesis, University of Paris IV, 1983. CATAUDELLA S., CROSETTI D., MASSA F. (eds), “Mediterranean coastal lagoons: sustainable management and interactions among aquaculture, capture fisheries and the environment”, Études et Revues de la FAO/CGPM 95, 2015.

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CHAOUI L., KARA M.H., FAURE E., QUIGNARD J.P., “L’ichtyofaune de la lagune du Mellah : diversité, production et analyse des captures commerciales”, Cybium, 30 (2): 123–132, 2006. CHAOUI L., GAGNAIRE P.A., GUIGNAND B., QUIGNARD J.P., KARA H., BONHOMME F., “Microsatellite length variation in candidate genes correlates with habitat in the gilthead sea bream Sparus aurata”, Molecular Ecology, 21: 5497–5511, 2012. CHAUVET C., “La pêcherie du lac de Tunis”, Études et Revues de la FAO/CGPM, 61: 615–694, 1984. CHAUVET C., Exploitation des poissons en milieu lagunaire méditerranéen. Dynamique du peuplement ichtyologique de la lagune de Tunis et des populations exploitées par des bordigues (muges, loups, daurades), PhD thesis, University of Perpignan, 1986. CHAUVET C., “Manuel sur l’aménagement des pêches dans les lagunes côtières : la bordigue méditerranéenne”, Document technique sur les pêches et l’aquaculture de la FAO, 290: 75, 1988. CRESPI V., “Recent evolution of the fishing exploitation in the Thau lagoon, France”, Fisheries Management and Ecology, 9: 19–29, 2002. DE ANGELIS R., “Mediterranean brackish water lagoons and their exploitation”, Études et Revues de la FAO/CGPM, 12: 1–41, 1960. DIMITRIOU E., KATSELIS G., MOUTOPOULOS D.K., AKOVITIOTIS C., KOUTSIKOPOULOS C., “Possible influence of reared gilthead sea bream (Sparus aurata, L.) on wild stock in the area of the Messolonghi lagoon (Ionian Sea, Greece)”, Aquaculture Research, 38: 398–408, 2007. DJABOU H., BRADAI M.N., JARBOUI O., MRABET R., “Quelques considérations sur la diversité ichtyologique et l’exploitation de la lagune d’El Biben”, Ve Rencontres de l’Ichtyologie en France, poster session I-II: 62, Paris, 27-30 March 2012. ESCALAS A., FERRATON F., PAILLON C., VIDY G., CARCAILLET F., SALEN-PICARD C., LE LOC’H F., RICHARD P., DARNAUDE A.M., “Spatial variations in dietary organic matter sources modulate the size and condition of fish juveniles in temperate lagoon nursery sites”, Estuarine, Coastal and Shelf Science, 152: 78– 90, 2015. FAO, Global Number of Fishers, Fishery Statistical Collections, FIGIS Data Collection, FAO Fisheries and Aquaculture Department, Rome, 2010. GAFRD, “General authority for fish resources and development. Statistics of fish production of year 2011”, GAFRD, Ministry of Agriculture and Land Reclamation, Doka, Giza, 2012.

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GISBERT E., CARDONA L., CASTELLO F., “Resource partitioning among planktivorous fish larvae and fry in a Mediterranean Coastal lagoon”, Estuarine, Coastal and Shelf Science, 43: 723–735, 1996. GUINAND B., CHAUVEL C., TOURNOIS J., TSIGENOPOULOS C.S., DARNAUDE A.M., MCKENZIE D.J., GAGNAIRE P.A., “Candidate gene variation in gilthead sea bream reveals complex spatiotemporal selection patterns between marine and lagoon habitats”, Marine Ecology Progress Series, 2016. GUINAND B., QUÉRÉ N., DESMARAIS E., LAGNEL J., TSIGENOPOULOS C.S., BONHOMME F., “From the laboratory to the wild: salinity-based genetic differenciation of the European sea bass (Dicentrarchus labrax) using gene-associated and geneindependent microsatellite”, Marine Biology, 162: 515–538, 2015. HERVE P., BRUSLE J., Les échanges migratoires des poissons entre les étangs littoraux et la mer sur la côte catalane française, Report, Commission internationale pour l’exploration scientifique de la mer Méditerranée (CIESM), 25/26 (10): 31–33, 1979. HOTOS G.N., AVRAMIDOU D., ONDRIAS I., “Reproduction biology of Liza aurata (Risso, 1810), (Pisces Mugilidae) in the lagoon of Klisova (Messolonghi, W. Greece)”, Fisheries Research, 47: 57–67, 2000. ISNARD E., TOURNOIS J., MCKENZIE D.J., FERRATON F., BODIN N., ALIAUME C., DARNAUDE A.M., “Getting a good start in life? A comparative analysis of the quality of lagoons as juvenile habitats for the gilthead seabream Sparus aurata in the Gulf of Lions”, Estuaries and Coasts, 2015. KAPESKY J.M., LASSERRE G., “Aménagement des pêches dans les lagunes côtières”, Études et Revues de la FAO/CGPM, 61 (2): 439–776, 1984. KARA M.H., “Cycle sexuel et fécondité du loup Dicentrarchus labrax (poisson moronidé) du golfe d’Anaba”, Cahiers de Biologie Marine, 38: 161–168, 1997. KATSELIS G., KOUKOU K., DIMITRIOU E., KOUTSIKOPOULOS C., “Short-term seaward fish migration in the Messolonghi-Etoliko lagoons (Western Greek coast) in relation to climatic variables and the lunar cycle”, Estuarine, Coastal and Shelf Science, 73: 571–582, 2007. KRALJEVIĆ M., DULČIĆ J., “Age and growth of gilt-head sea bream (Sparus aurata L.) in the Mirna Estuary, Northern Adriatic”, Fisheries Research, 31: 249–255, 1997. LASSERRE G., “Biologie halieutique des lagunes”, L’Année Biologique, series 4, 28 (3): 161– 186, 1989.

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LASSERRE G., LABOURG P.J., “Étude comparée de la croissance de la daurade Sparus aurata L. des régions d’Arcachon et de Sète”, Vie et Milieu, 24 (1A): 155–170, 1974. LEMAIRE C., ALLEGRUCCI M., NACIRI L., BAHRI-SFAR H., KARA M.H., BONHOMME F., “Do discrepancies between microsatellite and allozyme variation reveal differential selection between sea and lagoon in the sea bass (Dicentarchus labrax)?”, Molecular Ecology, 9: 457–467, 2000. LEMAIRE C., VERSINI J.J., BONHOMME F., “Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers”, Journal of Evolutionary Biology, 18: 70–80, 2004-2005. MERCIER L., MOUILLOT D., BRUGUIER O., VIGLIOLAS L., DARNAUDE A., “Multielement otolith fingerprints unravel sea-lagoon lifetime migrations of gilthead sea bream Sparus aurata”, Marine Ecology Progress Series, 444: 175–194, 2012. MORAT F., BLAMART D., ROBERT M., LECOMTE-FINIGER R., LETOURNEUR Y., “Characterization and discrimination of nurseries for the common sole (Solea solea). The case of four Mediterranean coastal lagoons”, European Conference on Coastal Lagoon Research, Montpellier, 123, 2009. MOSCONI P., CHAUVET C., “Variabilité spatio-temporelle de la croissance des juvéniles de Sparus aurata entre les zones lagunaires et marines du Golfe du Lion”, Vie et Milieu, 40 (4): 305–311, 1990. PANFILI J., DARNAUDE A.M., LIN Y.J., CHEVALLEY M., IIZUKA Y., TZENG W.N., CRIVELLI A.J., “Habitat residence during continental life of the European eel Anguilla anguilla investigated using linear discriminant analysis applied to otolith Sr: Ca ratios”, Aquatic Biology, 15 (2): 175–185, 2012. PEARCE F., CRIVELLI A.J., “Caractéristiques générales des zones humides méditerranéennes”, MedWet Conservation des zones humides méditerranéennes, 1: 90, Tour du Valat, Arles, France, 1994. PÉREZ-RUZAFA A., CONCEPCION M., “Fisheries in coastal lagoons: an assumed but poorly reserached aspect of the ecology and functioning of coastal lagoons”, Estuarine, Coastal and Shelf Science, 110: 15–3, 2012. QUIGNARD J.P., “Poissons des lagunes. Stratégies et tactiques de survie”, Océanorama, 23 : 15–20, 1994. QUIGNARD J.P., MAN-WAI R., VIANET R., “Les poissons de l’étang de Mauguio (Hérault, France) : inventaire, structure du peuplement, croissance et polymorphisme des tailles”, Vie et Milieu, 34 (4) : 173–183, 1984.

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QUIGNARD J.P., ZAOUALI J., “Les lagunes périméditerranéennes. I : les étangs français de Canet à Thau”, Bulletin de l’Office National des Pêches de Tunisie, 4 (2): 41–96, 1980. QUIGNARD J.P., ZAOUALI J., “Les lagunes périméditerranéennes, II : les étangs français d’Ingril à Porto-Vecchio”, Bulletin de l’Office National des Pêches de Tunisie, 5 (1): 41–96, 1981. RAVAGNAN G., Vallicoltura moderna, Edagricole, Bologna, 1978. ROSECCHI E., CHARPENTIER P., “L’Aquaculture en milieux lagunaire et marin côtiers”, MedWet Conservation des zones humides méditerranéennes, Tour du Valat, Arles, France, 3, 1995. ROSSI R., COLOMBO G., “Sex ratio, age and growth of silver eels in two brackish lagoons in the northern Adriatic (Valli di Comacchio and Valle Nuova)”, Archivi di Oceanografla e Limnologia, Venezia, 18: 227–310, 1976. SHAIEK M., ROMDHANE M.S., LE LOCH F., “Study of the ichthyofauna diet in the Ichkeul lake (Tunisia)”, Cybium, 39 (3): 193–210, 2015. SKINNER J., ZALEWSKI S., “Fonctions et valeurs des zones humides méditerranéennes”, MedWet Conservation des zones humides méditerranéennes, Tour du Valat, Arles, France, 2, 1995. TOURNOIS J., DARNAUDE A.M., FERRATON F., ALIAUME C., MERCIER L., MCKENZIE D.J., “Lagoon nurseries make a major contribution to adult populations of a highly prized coastal fish”, Limnology and Oceanography, 2017. TOURNOIS J., FERRATON F., VELEZ L., MCKENZIE D.J., ALIAUME C., MERCIER L., DARNAUDE A., “Temporal stability of otolith elemental fingerprints discriminates among lagoon nursery habitats”, Estuarine, Coastal and Shelf Science, 131: 182–193, 2013. VIANET R., Le flet du Golfe du Lion, Platichthys flesus Linné, 1758. Systématique, écobiologie, pêche, Thesis, USTL Montpellier, 1985. ZOHAR Y., BILLARD R., WEIL C., “La reproduction de la daurade Sparus aurata et du loup Dicentrarchus labrax : connaissance du cycle sexuel et contrôle de la gamétogenèse et de la ponte”, in G. BARNABE, R. BILLARD (eds), L’aquaculture du bar et des Sparidés, pp. 3–24, INRA, Paris, 1984. ZOULIAS T., KAPIRIS K., REIZOPOULOUS., “Ecological indicators based on fisheries landing time-series data: An application to three coastal lagoons in Amvrakikos Gulf (E. Mediterranean, Greece)”, Life and Environment, 64: 9–21, 2014.

1 Mullidae Günther, 1859

Vernacular name: Red mullet. Etymology: It is uncertain, from the Latin mulleus (red-colored like the red shoes of Roman senators) according to Walter and Avenas (2011), or from mullus, meaning soft according to Romero (2002, Fishbase), and also mullus (Latin name of the red surmullet). Brief description: It is characterized by the presence of two mobile barbels (used to detect food). Elongated body containing 23–24 vertebrae. Two widely separated dorsal fins; the first with six to eight spines and the second with one spine and eight to nine soft rays. The anal fin has one or two short spines and five to eight soft rays. The caudal fin is forked. Maximum length 60 cm (Nelson, 2006). They are a characteristic red color only under the effect of excitation or after death. In their environment, the external markings are quite variable, generally greenish-brown on their back, silvery on the underside. They have large deciduous scales and a prominent lateral line. Biogeography: Atlantic, Indian and Pacific Oceans and the Mediterranean Sea. Habitat and bio-ecology: Marine, rarely found in brackish water. Systematics and phylogeny: Based on samples from Greece and Senegal, Mamuris et al. (1999a) showed that genetic distances are smaller between the species Upeneus moluccensis and Pseudupeneus prayensis than between the latter and Mullus barbatus and Mullus surmuletus. Both Mullus species are genetically closer to P. prayensis than U. moluccensis if allozyme markers are taken into account, but the reverse is true if random amplified polymorphic DNA (RAPD) markers and mitochondrial DNA are used. The phylogenetic tree built with neighbor-joining methods and parsimony, using the three markers together, confirms this last result (Figure 1.1).

Fishes in Lagoons and Estuaries in the Mediterranean 3B: Migratory Fish, First Edition. Mohamed Hichem Kara and Jean-Pierre Quignard. © ISTE Ltd 2019. Published by ISTE Ltd and John Wiley & Sons, Inc.

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M. barbatus M. surmuletus U. moluccensis P. prayensis Figure 1.1. Phylogenetic tree based on parsimony analysis using three markers together (allozymes, RAPDs, mitochondrial DNA) (based on Mamuris et al., 1999a)

Turan (2006) compared, using morphology and 12 enzymatic markers, four Mullidae species: Mullus barbatus, M. surmuletus, U. moluccensis, Upeneus pori and a subspecies, M. barbatus ponticus. Significant differences in allelic frequencies were revealed between M. barbatus and M. b. ponticus (P < 0.001). The values of the genetic distances are 0.034 between M. barbatus and M. b. ponticus and 0.341 between M. barbatus and M. surmuletus. The genetic differentiation is relatively high (D = 0.628) between U. moluccensis and U. pori. At the intergeneric level, the greatest genetic distance is between M. surmuletus and U. pori (D = 1.250) and the smallest (D = 1.056) is between M. surmuletus and U. moluccensis. Upeneus pori is remarkably the most genetically distinct species of the genus Mullus (Figure 1.2).

M.surmuletus

U. pori

M. b. ponticus

0.1 100

U. moluccensis

99

M. barbatus

M. surmuletus

Figure 1.2. Neighbor-joining phylogenetic tree based on Nei's genetic distances for allozymes. The lengths of the branches are proportional to the genetic distances between taxa (see scale). The numbers indicate bootstrap values for 1,000 replications (Turan, 2006)

Morphological data, using meristic characters, lead to the same conclusions (Figure 1.3).

Mullidae Günther, 1859

3

U. pori M. b. ponticus

100

98

M. barbatus

U. moluccensis 100.0 M. surmuletus Figure 1.3. Neighbor-joining phylogenetic tree based on Euclidean distances. The scale bar represents the length of the branch. The numbers indicate the bootstrap values (Turan, 2006)

These same taxa were compared by Keskin and Kan (2009) who used mitochondrial markers (cytochrome b, 12S RNA, cytochrome oxidase). The phylogenetic tree, constructed from the results obtained, confirmed the existence of the two genera Mullus and Upeneus, but not that of the subspecies M. barbatus ponticus. Biodiversity: There are six genera Mulloidichthys, Mullus, Parupeneus, Pseudupeneus, Upeneichthys, Upeneus, with approximately 62 species (Nelson, 2006). Three genera exist in the Mediterranean: Mullus, Pseudupeneus (Herculean immigrant), Upeneus (Lessepsian immigrant) (Quignard and Tomasini, 2000). Originality: These fish are characterized by the presence of two barbels that come from the transformation of branchiostegous rays into soft and fleshy appendages, covered with sensory structures (Bougis, 1952a, 1952b; Gosline, 1984; McCormick, 1993; Lombarte and Aguirre, 1995). The ultrastructure of the taste buds of Mediterranean Mullus is described by Lombarte and Aguirre (1997). These taste buds have a pore from which apical endings of different chemoreceptor cells emerge. 1.1. Mullus Linnæus, 1758 Type: Mullus Linnæus, 1758, Syst. Naturae, 10 ed., 1: 299 (species: M. barbatus Linnæus, 1758, by subsequent designation by Bleeker, 1876: 334).

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Etymology: From the Latin mulleus (red) or mullus (name of red surmullet). Brief description: For this, see the “Brief description” section in the box at the beginning of the chapter. A notable characteristic of other genera is the absence of teeth in the upper jaw. Biogeography: Atlantic and Mediterranean Oceans, Black Sea and Sea of Azov. Habitat and bio-ecology: Demersal, marine, 5–500 m deep. Biodiversity: This genus includes four species: Mullus Hubbs and Marini, 1933, Mullus auratus Jordan and Gilbert, 1882, M. surmuletus Linnæus, 1758, M. barbatus. The latter is represented by two subspecies: M. barbatus barbatus Linnæus, 1758 and M. barbatus ponticus Essipov, 1927. Only M. barbatus barbatus and M. surmuletus occur in the Mediterranean. Their distinctive criteria are illustrated in Figure 1.4.

Figure 1.4. First dorsal fin and suborbital scales: (a) Mullus surmuletus; (b) Mullus barbatus (Bauchot and Pras, 1980)

Systematics and phylogeny: See box at the beginning of the chapter, section “Systematics and phylogeny”.

Mullidae Günther, 1859

5

Originality: When threatened, the red mullet makes the first dorsal fin appear bigger, probably to deter any predators; the barbs are then folded into notches under the head. 1.1.1. Mullus barbatus barbatus Linnæus, 1758

1.1.1.1. Nomenclature and systematics Holotype: Mullus barbatus Linnæus, 1758, Syst. Nat., Ed. X: 299 (Habitat in M. Mediterraneo and Oceano septentrionali). Holotype: LS no. 3. Synonyms: Mullus ruber Lacepède, 1801; M. fuscatus Rafinesque, 1810. Vernacular names: Rouget de vase (DZ), salmonete de fango (ES), rougetbarbet de vase (FR), red mullet (GB), koutsomoura (GR), mulit adumma (IS), triglia di fango (IT), trillia bidha, rouget blanc (TN). Etymology: The French name, rouget, is due to its red color, especially as it is seen on the fishmonger’s stall. The scientific name comes from the Latin mulleus (reddish) or mullus (Roman name of this fish) and barbatus (bearded, because of the presence of two barbels). Systematic problems: Two subspecies of red mullet are recognized: Mullus barbatus barbatus Linnæus, 1758 and M. b. ponticus Essipov, 1927. The first has three suborbital scales and its maxilla exceeds the anterior border of the eye in adults. The second usually has four suborbital scales and its maxilla does not reach the anterior edge of the eye. This subspecies is also smaller and more silvery and may live at shallower depths. Its geographical distribution is limited to the Black Sea and the Sea of Azov. Turan (2006) revealed significant differences in allelic frequencies between these two subspecies (P < 0.001), with a genetic distance value of 0.034.

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1.1.1.2. Description Morpho-anatomy: Elongated body with a rather flat ventral profile. The head is short, massive, with a steep profile. The muzzle is short. The chin has a pair of barbs whose length is less than or equal to that of the pectoral fins. These barbs have tactile, olfactory and taste organs, and are able to detect prey in the mud. The operculum is devoid of thorns. The lower jaw has villiform teeth; the upper jaw is edentulous, but teeth are present on the oral vault (vomer bone and palatine plates). Juveniles have teeth on the premaxilla. The cheeks have three large scales; the smallest is colorless. There are two well-separated dorsal fins: the first, colorless, has eight spines, the first of which is very small; the second fin has one spine and eight soft rays. The anal fin has two spines and six to seven soft rays. The scales are large and not very adherent, with 31–35 in the lateral line. They are between 10 and 20 cm in length (8 and 12 cm in the Black Sea), with a maximum of 30 cm. A maximum length of 29.7 cm is reported by Vassilopoulou (1992) in females in Greece. Coloring: The coloring of this species changes according to its environment. On sand, it is beige with a dark horizontal line starting from the eye; on other substrates, it is dark and marbled, especially at the flanks. It is dull and paler at night than by day. With a pink tint, intense colors are more common on fishmonger stalls than in the water; this red hue is enhanced by descaling. The flanks have silvery highlights and the underside is white. The fry are bluish in color. Variations: The morphology of M. barbatus from seven different localities, distributed in the Aegean and Ionian seas, was compared using 15 metric criteria (Mamuris et al., 1998c). The mean value of the features examined differs significantly among the seven populations (analysis of variance, P < 0.05). Principal component analysis showed that the main features responsible for this differentiation are those related to the head and fins, accounting for 58.6% of the variance between seven groups. Sonin et al. (2007) report dwarfism in red mullets in the eastern Mediterranean (Israel: 14.6 cm TL in males, 17.6 cm TL in females, both aged 5 years) compared to those in the western Mediterranean (Strait of Sicily: 19.5 cm TL in males, 21.8 cm in females, aged 5 years). These authors attribute this divergence of sizes to the low productivity of the Levantine basin. In this region, the high temperature would also be responsible for this situation by inducing an intense metabolism that causes premature sexual maturity, itself causing a slowing down of growth. Osteology, otoliths and scales: Contrary to generic descriptions, usually based on adult specimens, Aguirre (1997) indicates that juveniles of M. barbatus have teeth

Mullidae Günther, 1859

7

on the premaxilla. These teeth are no longer visible in specimens larger than 100 mm TL, since they are covered by a labial tissue (Figure 1.5).

Figure 1.5. Ventral view of dissected left premaxilla of M. barbatus: 45 mm (a), 50 mm (b), 60 mm (c), 70 mm (d) and 81 mm (e). The figure shows the alveoli (in black) and the teeth. Bar = 0.1 mm (Aguirre, 1997)

Scott (1906), Sanz Echeverria (1936) and Chaine and Duvergier (1936) provide information on the sagittal otoliths of M. barbatus. More recently, Tuset et al. (2008) gave a detailed description of this otolith in the Mediterranean and north-east Atlantic. From elliptical to oval in shape, its edges are crenellated. The sulcus acusticus is heterosulcoid, ostial and medial. The ostium is funnel shaped. The cauda is tubular, curved, sharply bent from the medial region, ending near the posterior border. The anterior region is pointed. The rostrum and antirostrum are short, broad and pointed. The posterior region is rounded at irregular angles (Figure 1.6).

Figure 1.6. Sagittal otolith of an individual (24.5 cm TL) of M. barbatus from the Western Mediterranean, scale 1 mm (Tuset et al., 2008)

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

This author describes the morphology of sagittal otoliths using the following ratios: otolith length/total length of fish = 1.8–2.2; otolith width/otolith length = 70.3– 80.0; circularity = 16.9–17.3; rectangularity = 0.1–0.2. For north-western Mediterranean samples, Aguirre and Lombarte (1999) give the relationship between the otolith surface area (O) and the total fish length (TL) by the equation O = 0.0097 TL 1.2119 (r2 = 0.9574, n = 72), and indicate that there is no difference between the left and right otolith. Morat et al. (2008) describe the relationship between total fish length (mm) and sagittal otolith length (mm) using the following regression equations for those from the northwestern Mediterranean and the Aegean, respectively: TL = 73.20 Lo – 44.48 (56–235 mm, r = 0.862, P < 0.0001), TL = 74.11 Lo – 45.88 (120–195 mm, r = 0.849, P < 0.0001). The general morphology and ultrastructure of the scales are described by Morales-Nin and Fauquet (1983). These scales are ctenoid. Their anterior field has many circulii 12 µm apart, with denticles. The latter are flattened and 2 µm wide, arranged in groups of two to four units, usually three (60%). The number of radii oscillates between four and eight, usually six (40%). The lateral fields are similar to the anterior field. The posterior field, zone of the visible scales on the body of the fish, is covered by a superficial dermis layer. This region is characterized by the presence of a series of small spines, ctenii, on the edge of the scales. Its entire surface has irregular and short ridges. The lateral line scales have a channel at the central zone whose branches split at the posterior into two branches, which in turn divide further. Karyology: The number of chromosomes in M. barbatus is 2n = 44 (Vitturi et al., 1992; Prazdnikov, 2016). Note the absence of heteromorphic elements (sex chromosomes) in both males and females. Three pairs are metacentric or submetacentric (pair 1–3), eight are subtelocentric (pairs 4–11) and 11 are acrocentric (pairs 12–22) (Vitturi et al., 1992). Protein specificity and genetic diversity: Arias and Morales (1977) compared, by electrophoresis, the soluble proteins in the muscle of M. barbatus and M. surmuletus. Electrophoregrams obtained by different methods show four protein fractions in M. surmuletus and two in M. barbatus. Mammuris et al. (1998a) use 20 enzymatic loci in the search for genetic differences between these two species. Electrophoretic profiles specific to each of them are highlighted in the case of the three systems PGI-2* (phosphoglucose isomerase), PGI-3* and PGM* (phosphoglucomutase). The mean value of Nei’s genetic distance between the two species is 0.329. This distance is 0.068 according to Cammarata et al. (1991) who used seven enzymatic systems. These authors highlight profiles specific to each species in the case of the enzyme SOD and muscle proteins. Basaglia and Callegarini (1988) also find different profiles in the case of lactate dehydrogenase

Mullidae Günther, 1859

9

(LDH) and lens proteins, while malate dehydrogenase (MDH) has the same configuration. Using 20 allozyme markers, Mamuris et al. (1998a) genetically differentiated eight Mediterranean samples from M. barbatus (five from the Aegean Sea: Thermaikos, Allonisos, Kavala, Platania, Kymi; two from the Ionian Sea: Corfu, Amvrakikos; one from the Gulf of Lion) with a significant Fst value (Fst = 0.043; χ2 test, P < 0.05). This differentiation also exists if only the eastern part of the Mediterranean (Fst = 0.041; χ2 test, P < 0.05) is considered. On the other hand, the genetic distance is small, whatever the pair of samples considered (mean D = 0.0039). Mamuris et al. (1998b) analyzed these same samples using 29 RAPDtype molecular markers. Calculated genetic distances are positively correlated with geographic distances (Mantel t-test; r = 0.8531, t = 2.575; P < 0.05). Indeed, the French population of the Gulf of Lion is genetically distinct from the Greek populations and, within Greece, the populations of the Ionian Sea seem to diverge from those of the Aegean Sea. Intraspecific discrepancies are more pronounced with RAPDs than with allozymes. The results obtained on the same samples with restriction fragment length polymorphism (RFLP) markers do not show any significant genetic structuring and are more consistent with the results obtained with allozymes (Mamuris et al., 2001). Arculeo et al. (1999) examined the variability of allozymes in samples from eight Mediterranean localities (Sète, Livorno, Gulf of Castellammare, Gulf of Gela, Strait of Sicily, Venetian Lagoon, Ionian Sea, Aegean Sea). Three of the 25 loci tested were polymorphic (AAT, SDH-2, XDH-2). The observed heterozygosity was 0.043. The Nei index reveals a genetic distance of between 0.000 and 0.002. The Fst values do not show significant differences between the samples analyzed (AAT = 0.009; SDH-2 = 0.015; XDH-2 = 0.003). The average Fst value is 0.009 and the gene flow is estimated at 28 migrants per generation. The first microsatellite markers of M. barbatus were developed and optimized by Garoia et al. (2004). Six microsatellite markers, applied to four red mullet samples from the Adriatic, give evidence that they were heterogeneous, with a low but significant Fst value (0.005, P < 0.01). However, there is no correlation between this genetic differentiation and geographic distance. In a larger geographical study (Gulf of Lion, Tyrrhenian Sea, Strait of Sicily, Ionian Sea, southern and northern Adriatic), using the same microsatellite markers, Maggio et al. (2009) show the spatial heterogeneity of the samples (Fst = 0.003, P < 0.001), with the Adriatic having a certain “singularity”. Ten other microsatellite loci were developed by Galarza et al. (2007). Their application on Mediterranean and Atlantic samples shows that the highly structured genetic distribution of muddy

10

Fishes in Lagoons and Estuaries in the Mediterranean 3B

mullet resembles that of a metapopulation composed of independent subpopulations with autonomous recruitment, despite some connections between them (Galarza et al., 2009). Using the same type of markers, Félix-Hackradt et al. (2013) found complete homogeneity of mullet samples from 13 localities 400 km apart on the Spanish Mediterranean coast. 1.1.1.3. Distribution Its distribution is common in the Mediterranean and the Black Sea, and the British Isles (occasionally in Scandinavia) and Senegal in the East Atlantic. Also present in the Canary Islands and Azores (Figure 1.7).

Figure 1.7. Geographic distribution of Mullus barbatus

1.1.1.4. Ecology Habitat: Demersal and gregarious, adults of this species are found on sandymuddy substrates, usually at depths of between 100 and 300 m, while juveniles are littoral and often live at shallower depths. In the Strait of Sicily, juveniles are recruited very close to the coast (10–30 m) in August–September and are more abundant when the surface water temperature during the early stages of development is higher than the observed average value over a long period of time (Levi et al., 2003). In the Aegean Sea, in the months before spawning, red mullet are more

Mullidae Günther, 1859

11

abundant in the warmer waters to the east and west than in the central region. These regions are shallower (35–60 m deep) and their temperature is 19 °C on the bed, whereas it is below 16 °C elsewhere (Maravelias et al., 2007). In the Heraklion Gulf, fish size increases with depth; the smaller ones prefer shallow and relatively warmer waters (Machias and Labropoulou, 2002). On the western shores of the Mediterranean, Lombarte et al. (2000) find that the bathymetric distribution of this species is limited and does not go beyond 200 m. It is more abundant between 51 and 200 m on mudflats (785 ind·km–2), especially in sites characterized by a large continental shelf (mouth of the Ebro and Segura). This preference is more pronounced among juveniles and coincides with the distribution of their colonization areas defined by García-Rubies and Macpherson (1995). In the Gulf of Lion, this species does not exceed –200 m, but in Corsica it reaches –400 m (Campillo, 1992). In the Ionian Sea, Mytilineou et al. (2005) report red mullet up to 328 m. In the Aegean Sea, it is fished between 0 and 500 m, but is three to five times more abundant in the 0–100 m zone than between 200 and 500 m (Tserpes et al., 1999). However, Planas and Vives (1956) as well as Suau and Vives (1957) observe a higher proportion of red mullets at greater depths. Fiorentino et al. (2008) showed the influence of the 14-year trawling ban on increasing the mean size of mature M. barbatus females as a function of depth in the Gulf of Castellammare. According to García-Rodriguez et al. (2010), the depth itself does not affect the biomass distribution of this species, which seems to be more influenced by salinity, and to a lesser extent by water temperature. Golani (1994) studied the distribution of the two native species, M. barbatus and M. surmuletus, and two Lessepsian colonizers (U. moluccensis and U. pori) along the Mediterranean coasts of Israel. Bathymetry has been shown to be the parameter that most influences the separation of species from their respective feeding habits or spawning seasons. In fact, the colonizers occupy the shallow depths, 20–30 m for U. pori and 40–50 m for U. moluccensis; the native M. barbatus is dominant at depths less than 55 m and M. surmuletus is poorly represented at all depths. Migrations and movement: Suau and Vives (1957) schematized the movements made by a mullet during its life. According to these authors, spawning occurs between May and July in the western Mediterranean and occurs at depths between 80 and 120 m. Eggs and larvae transported by surface currents are brought to the coast. Small red mullet (33.2–44.6 mm on average) are present between late July and early September between two isobaths (60 and 40 m). They follow their progression toward the coast (40–20 m), while acquiring the morphology of an adult. Their color changes from bluish during the pelagic stage to reddish, typical of the species. Fry live in open water and become benthic only above 5 cm in size. They reach the coast in September–October, where they finish this first trip and begin their return to

12

Fishes in Lagoons and Estuaries in the Mediterranean 3B

initial depths, between 80 and 120 m, at a size of 6–7 cm (Larraneta and RodriguezRoda, 1956). Size, lifespan and growth: Depending on the locality, the maximum age of red mullet varies between 3 years (FL = 15.38 cm, TW 57.66 g) in the Bay of Izmir (Kinacigil et al., 2001) and 7 years (around 21 cm) in females in Montenegro (Joksimović et al., 2008) and 7 years in Marseille (Campillo, 1992). Many authors recognize the difficulty of determining the age of M. barbatus from scales and otoliths (Larraneta and Rodriguez-Roda, 1956; Gharbi and Ktari, 1981b) and often use indirect methods of cohort separation (Suau and Vives, 1957; Layachi et al., 2007; Joksimović et al., 2008). Indeed, due to the effect of trawling, caught red mullet are usually free of scales. As for otoliths, they pose the problem of false annual rings that probably correspond to migratory events that characterize the lifecycle of this species, as demonstrated by Larraneta and Rodriguez-Roda (1956). Moreover, Haidar (1970) estimates that the small sizes (about 9 cm at 2 years and 15.5 cm at 4 years) given by Wirszubski (1953) in Israel are the result of a misinterpretation of stunted growth rings (annuli). On Catalan coasts, by the backcalculation of sizes using growth rings on scales from the end of growth, Larraneta and Rodriguez-Roda (1956) indicate that males measure between 11 and 11.5 cm at 1 year and 13.4 cm at 2 years, and females measure between 12–12.5 cm at 1 year and 14.4 cm at 2 years. On Tunisian coasts, the lengths observed, determined by scalimetry, reach 15.42 cm in 4-year-old males (maximum age) and 17.98 cm in 5year-old females (Gharbi and Ktari, 1981b). Growth parameters according to the von Bertalanffy model, obtained in different regions, are presented in Table 1.1. Some equations for length–weight relationship are given in Table 1.2. Bougis (1952a, 1952b) found growth isometry (b = 3.24) in adults in the Gulf of Lion. Haidar (1970) shows that beyond 16 cm, the allometry is greater (b = 3.26). Sites and authors Adriatic Sea (Scaccini, 1947)

Tunisian coasts (Gharbi and Ktari, 1979)

Saranikos Bay, Aegean Sea (Papaconstantinou et al., 1981)

Thermaikos Bay, Aegean Sea (Papaconstantinou et al., 1981)

Sex

L∞ (cm)

K

to

M+F

27.49

0.50

–0.25

*M

18.09

0.49

–0.17

*F

20.46

0.50

–0.04

*M + F

20.25

0.51

–0.01

M

19.23

0.19

–2.81

F

24.00

0.13

–2.94

M

20.91

0.13

–4.25

F

27.54

0.09

–4.30

Mullidae Günther, 1859

13

Catalonia (Sanchez et al., 1983)

M+F

29.70

0.09

–4.42

Gulf of Patraikos (Papaconstantinou et al., 1986)

M+F

23.31

0.04

–

Gulf of Korinthiakos (Papaconstantinou et al., 1986)

M+F

21.49

0.03

–

Ionian Sea (Papaconstantinou et al., 1986)

M+F

22.85

0.04

–

Adriatic Sea (Jukić and Piccinetti, 1988)

M+F

27.00

1.80

–

Saronikos Bay, Aegean Sea (Vrantzas et al., 1992)

M+F

23.50

0.51

–0.86

M

22.5

0.56

–0.24

F

24.5

0.60

–0.20

M

22.71

0.21

–2.13

F

25.49

0.21

–1.85

M+F

19.70

0.36

–1.18

M

22.4

0.28

–1.98

F

24.5

0.27

–1.85

M

22.00

0.74

–

F

29.20

0.68

–

M+F

33.00

0.38

–0.07

M

27.00

0.18

–1.92

Gulf of Lion (Campillo, 1992)

Aegean Sea (Vassilopoulou and Papaconstantinou, 1992) Adriatic Sea (Ungaro et al., 1994) Ionian Sea (Tursi et al., 1994)

Livorno, Ligurian Sea (Voliani et al., 1995) Catalonia (Sanchez et al., 1995)

F

34.50

0.15

–1.53

M+F

31.50

0.18

–1.45

Santo Stefano, Ligurian Sea (Demestre et al., 1997)

M+F

34.50

0.34

–0.14

Adriatic Sea (Ardizzone, 1998)

M+F

27.50

0.50

–

Izmir Bay, Aegean Sea (Kinacigil et al., 2001)

**M + F

19.03

0.43

–0.77

Izmir Bay, Aegean Sea (Özbilgin et al., 2004)

M+F

24.26

0.56

–0.30

Nador Coast, Morocco (Layachi et al., 2007)

M+F

27.00

0.43

–0.09

M

17.81

0.28

–3.01

F

27.47

0.14

–2.68

M+F

30.12

0.11

–3.18

Adriatic Sea (Marano, 1996)

Southern Adriatic (Joksimović et al., 2008)

Table 1.1. Growth parameters of the von Bertalanffy model in Mullus barbatus barbatus in different regions of the Mediterranean: *standard length; **length at the fork

14

Fishes in Lagoons and Estuaries in the Mediterranean 3B

Sites and authors

Sex

a

b

Adriatic Sea (Zupanović, 1963)

M F

0.00655 0.00847

3.17 3.08

Eastern Adriatic (Haidar, 1970)

M + F (small) M + F (large)

0.0088 0.0051

3.05 3.26

Tunisian coasts (Gharbi and Ktari, 1979)

*M *F

– –

3.34 (3.25**) 3.11 (3.04**)

Gulf of Lion, France (Campillo, 1992)

M F

0.0074 0.01

3.14 3.05

Gulf of Korinthiakos, Greece (Papaconstantinou et al., 1986)

M+F

0.000006

3.12

Gulf of Korinthiakos, Greece (Papaconstantinou et al., 1986)

M+F

0.000004

3.16

Ionian Sea (Papaconstantinou et al., 1986)

M+F

0.000012

3.00

Aegean Sea (Vassilopoulou and Papaconstantinou, 1992)

M+F

0.000006

3.17

Adriatic Sea (Ungaro et al., 1994)

M+F

0.008

3.09

Adriatic Sea (Marano, 1996)

M+F

0.0125

2.97

M F

0.000007 –

3.13 3.14

Livorno, Ligurian Sea (Voliani et al., 1998) Izmir Bay, Aegean Sea (Kinacigil et al., 2001)

***M + F

0.0071

3.29

Nador Coast, Morocco (Layachi et al., 2007)

M+F

0.000009

3.03

Gulf of Tunisia (Cherif et al., 2007)

M F M+F

0.0055 (0.0054**) 0.0069 (0.0059**) 0.0072 (0.0066**)

3.21 (3.19**) 3.12 (3.12**) 3.10 (3.09**)

South Adriatic (Joksimović et al., 2008)

M F M+F

0.00773 0.00729 0.00767

3.09 3.11 3.10

Homa Lagoon, Turkey (Acarli et al., 2014)

M+F

0.0060

3.180

Table 1.2. Length–weight relationships (W = aLtb) of M. barbatus barbatus in different localities in the Mediterranean: *standard length; **eviscerated weight; ***length at the fork

Population structure and dynamics: Using data from four consecutive years, analyzed separately, Suau and Vives (1957) always find an overall sex ratio in favor of males in the north-western Mediterranean. Of the 3,966 individuals caught between the Ebro and the south of the Columbretes Islands, 53% were males, 34.2% were females and 12.8% were undetermined (Planas and Vives, 1956). On the coast

Mullidae Günther, 1859

15

of Castellón, males are numerically dominant in small sizes (up to 80% between 8 and 14 cm), females dominate at 16 cm and become exclusive beyond 19 cm (Larraneta and Rodriguez-Roda, 1956). On the other hand, in the Adriatic, females are more numerous (60.85%) (Scaccini, 1947); the same is true in the Gulf of Tunis (68%) where they dominate every month and in all size classes (Chérif et al., 2007) and on the Coast of Morocco, off Nador (Layachi et al., 2007). The difference in sampling depths may explain this discrepancy, since it is proven that males are more numerous in deeper waters. Tserpes et al. (2002) conducted annual trawling surveys covering a large part of the Mediterranean (1,000 sampling points in 15 major regions) from 10 to 800 m annually from 1994 to 2000. They found spatial variations in the abundance of M. barbatus and attribute it to the different modes of exploitation, as well as to the biotic and abiotic conditions of each site. Although the species is under strong fishing pressure, abundance indices do not show a downward trend, suggesting good recruitment. However, the dominance of young fish makes the stock highly vulnerable to fluctuations in recruitment. The size frequency distribution by region is shown in Figure 1.8. In the western Mediterranean, this distribution is generally unimodal and positively asymmetrical, with the exception of the Alboran Sea where three components are identified. In the eastern Mediterranean, this profile is more complex with two modal classes. The first mode corresponds to the juveniles of the year (recruits), the second corresponds to the relatively older individuals. The highest percentage of recruits is recorded in the southern Aegean, followed by the western Ionian and the southern Adriatic Sea. A remarkable profile characterizes the distribution of the northern Adriatic where two modes of the same amplitude are observed at 9 and 12 cm, respectively. Maximum lengths range from 15 (southern Aegean) to 27 cm (Sicily and southern Tyrrhenian Sea) and are generally higher in the western Mediterranean. In most cases, these values range from 20 to 24 and from 18 to 22 cm in the west and east of the Mediterranean, respectively. Predators: Morat (2007) found, in 2006 and 2007, the remains of an individual of M. barbatus in the pellets of the European shag Phalacrocorax aristotelis desmarestii of the Riou archipelago (France), with frequencies of occurrence of 2% and 4%.

16

Fish hes in Lagoons and a Estuaries in n the Mediterran nean 3B

Figure 1.8. 1 Length fre equency distrib bution (TL in cm) c of M. barb batus in differrent areas of the Mediterranean n. Numbers in parenthes ses indicate the average e relative abundan nce over the sampled s perio od, expressed d as number of individualss per km2 (Tserpess et al., 2002)

1.1.1.5. Food and fe eeding behavvior Foodd and feeding behavior: Muullus barbatuss is carnivorouus and feeds m mainly on benthic prey. p Its foodd niche is sepparated from that of the coongenic and ssympatric species M. M surmuletuss. Their prey is i different, bu ut of the samee size, allowinng a good

Mullidae Günther, 1859

17

distribution of available food resources (Labropoulou and Eleftheriou, 1997). These dietary differences are related to morphological differences: for M. barbatus, the length of the digestive tract is greater and the height and width of the head are less than in M. surmuletus (Labropoulou and Eleftheriou, 1997). According to Aguirre and Sánchez (2005), these two species feed from a broad and identical prey spectrum, but the proportions are significantly different depending on the predator ontogeny, and therefore their size. According to their similarity, these are divided into six size groups: 1) the oldest adults of M. surmuletus (21–31 cm TL); 2) newly recruited individuals of both species (6–8 cm TL); 3) the oldest adults of M. barbatus (19–21 cm TL); 4) adults of M. barbatus (12–18 cm TL); 5) juveniles of both species; 6) adults of M. surmuletus (12–20, 22 cm TL). Similar results regarding these interspecific and ontogenetic differences were obtained by Vassilopoulou et al. (2001) and Bautista-Vega et al. (2008). In the western Mediterranean, between the Ebro and to the south of the Columbretes Islands, 2-year-old adults prefer macrourous decapods and their larvae, followed by polychaete annelids, lamellibranch mollusks and isopods (Planas and Vives, 1956). In the Gulf of Tunis, crustaceans are the preferred prey (Fp = 77.02), whereas lamellibranch mollusks (Fp = 31.06), echinoderms (Fp = 17.39) and polychaete annelids (Fp = 15.53) are secondary prey (Gharbi and Ktari, 1979), which is confirmed by Chérif et al. (2011) on the northern coasts of Tunisia. In the south of the Tyrrhenian Sea, crustaceans (including gammarids) also dominate, while mollusks and polychaetes are secondary (Esposito et al., 2014). On the Mediterranean coasts of Morocco, their diet consists mainly of amphipods, annelids and bivalves (Layachi et al., 2007). In the eastern Mediterranean, polychaete annelids dominate. They represent 62.04% of the number and 51.17% of the weight of the prey ingested in Heraklion Bay (Labropoulou and Eleftheriou, 1997) and dominate in the Gulf of Amvrakikos, Greece (Vassilopoulou and Papacanstantinou, 1993), but only in large individuals (TL > 18 cm) (40.2% of weight) in the Gulf of Lion (Bautista-Vega et al., 2008). Caragitsou and Tsimenides (1982) found that in the Aegean Sea, the diet of individuals from 10 to 19 cm is composed mainly of mollusks and crustaceans. In this same region, according to Vassilopoulou et al. (2001), crustaceans, polychaetes and bivalve mollusks are the main categories of prey.

18

Fish hes in Lagoons and a Estuaries in n the Mediterran nean 3B

Feedding habits: Goosline (1984) suggests that the cephalic profile p is an aadaptation of the muscle m involveed in increasinng the strength h of the waterr jet used to aagitate the seabed inn search of prrey. The use of o sounds emiitted by the fiish could alsoo aid their search. A form of coommensalism occurs when n other fish arre attracted bby bottom mud exccavations, takinng advantage of unearthed prey. Dietaary variationss: On the northhwestern shorres of the Mediterranean, S Sabatés et al. (2015) showed thhat during thee oligotrophicc summer season, the verrtical and horizontaal distributionn of M. barbaatus larvae (> >8 mm standarrd length) corrresponds to that of o marine cladocerans, Evaadne and Pen nilia avirostriis. Larger sized larvae mainly consume c naupplii copepods. On the Norrth African cooast, the diet does not vary withh the season, size or sex off the fish (Ghaarbi and Ktarii, 1979; Layacchi et al., 2007). Inn the Gulf of Lion, small crustaceans c aree less frequenntly consumedd by large individuaals in favor of polychaete annelids a and shrimp s (Bautiista-Vega et aal., 2008). Variationns, in terms of both preyy diversity an nd size, is evvident in thee Gulf of Heraklioon (Machias and a Labropoullou, 2002). Sm mall crustaceaans and crabs are more commonn in small inddividuals, whiile the decapo ods Alpheus glaber g and Soolenocera membrannacea dominaate in the largeest individualss. In the south of thee Tyrrhenian Sea, the diet composition varies v with deepth (surf zone, 100, 20, 30 m) in relation to t the availab bility of bentthic prey. Mysids are consumeed mainly in the t surf zone, whereas gam mmarids, decappods and copeepods are the mainn prey in the other depths (E Esposito et al.,, 2014). Feeding rate decreeases during thhe spawning season s (April to July), as iss the case M coasts of Morrocco (Figure 1.9) (Layachii et al., 2007).. on the Mediterranean

Figure 1.9. Monthly variations v in th he stomach va acuity coefficie ent in Mullus b barbatus ast Mediterran nean coast of Morocco (Layyachi et al., 20 007) from the north-ea

Mullidae Günther, 1859

19

Jukic and Zupanovic (1965) note that the amount of food ingested is related to the temperature of the surrounding environment. This value is higher at summer temperatures (18.6–22.8 °C) and lower at winter temperatures (11.9–14.6 °C). Esposito et al. (2014) show that in the surf zone, their diet is composed of mysids and bivalves in summer and of cumaceans, gammarids and polychaetes in winter. At lower depths (10, 20, 30 m), seasonal variations in diet composition reflect fluctuations in gammarid abundance, confirming the opportunistic nature of M. barbatus. At daytime, in Hisarönü Bay (Turkey), the feeding activity of M. barbatus starts at dawn and peaks at noon. From midday until early evening, feeding intensity slows down and then increases slightly at sunset, before stopping almost entirely beyond that (Ünluoglu et al., 2002). However, the relative number of predominantly ingested prey (polychaetes, decapods, bivalves, amphipods) does not show a significant daily variation. 1.1.1.6. Reproduction and reproductive behavior Sexuality: Gonochoric species. First sexual maturity: In general, at first sexual maturity, females are larger in size than males: 13.5 cm versus 11.5 cm (Bougis, 1952a, 1952b) and 13 cm versus 12.5 cm (Campillo, 1992) in the south of France, 10.4 cm versus 9.4 cm in the Aegean Sea (Vassilopoulou and Papaconstantinou, 1992), 12.0 cm versus 10.0 cm in the Gulfs of Saronikos and Thermaikos (Papaconstantinou et al., 1981), 12.2 cm versus 10.1 cm in the Southern Adriatic (Carbonara et al., 2015). On the Tunisian coasts, adult females measure 16.0 cm (2 years) and males 14.0 cm (1 year) (Gharbi and Ktari, 1981a), but in the same zone (Gulf of Tunisia), according to Chérif et al. (2007), females and males reach their first maturity at the same size (13.9 cm). This size is, irrespective of sex, 9.3 cm on the Italian coasts (Voliani et al., 1998), 12.8 in the Gulf of Saroniko, Greece (Vrantzas et al., 1992) and 9 cm in Cyprus (Livadas 1988). In Izmir Bay, 1-year-old red mullet are all adults (Togulga, 1979). On Israel’s Mediterranean coast, Wirszubski (1953) estimated the age of first maturity of females to be 3 years. Spawning site and period: On Israeli coasts, spawning is reported at depths between 10 and 55 m, at temperatures of 16.5–18.5 °C, on muddy and silty sea bed (Wirszubski, 1953). Levi et al. (2003) found a relatively higher abundance of spawners, both at 50 m and over 200 m in two different locations in the Strait of Sicily. In the Gulf of Heraklion, abundance and biomass are relatively high in spring in waters of intermediate depths (71–150 m); this is related to the spawning season when fish travel from the coast to deep offshore waters (Machias and Labropoulou, 2002). In the central-eastern Mediterranean, Carlucci et al. (2009) highlight the presence of M. barbatus nurseries in the southern Adriatic (off the Gargano peninsula and between Molfetta and Monopoli) at a depth of 50 m.

20

Fish hes in Lagoons and a Estuaries in n the Mediterran nean 3B

Spaw wning generallly occurs beetween Aprill and August (Figure 1.110), with significaantly higher goonadosomaticc index (GSI) values in fem males (10% onn average) than in males m (less than 2% on aveerage) (Carbonara et al., 20015). It lasts ffrom 2 to 4 monthss and presentss some regionaal differences (Table 1.3).

Figure 1.10. Box plot of the monthlyy GSI values of o M. barbatuss females and d males in i the low l and high h GSI values and the the soutthern Adriaticc. The bars indicate numberss above indica ate the numbe er of specime ens used in th he analysis (C Carbonara et al., 20 015)

Sites annd authors

J F M A M J

J A S O N D

Gulf of Lion L (Bougis, 19552) Israeli Cooast (Wirszubskii, 1953) Coast of Castellón C (Larraaneta and Rodrigueez-Roda, 1956) Ebro-Collumbretes Islandds (Planas and Vives, V 1956) Gulf of Isskenderun (Akyuuz, 1957) Eastern Adriatic A (Haidar, 1970) Algerian coasts (Lalami, 1971) Egyptian coasts (Hashem m, 1973b) Tunisian coasts (Gharbi et e Ktari, 1981) Gulf of Lion L (Campillo, 1992) 1 Ionian Seea (Tursi et al., 1994) 1 Nador laggoon (Layachi et al., 2007) Gulf of Tunis T (Cherif et al., a 2007) Northwesst Mediterraneann (Ferrer-Maza et e al., 2015) Southern Adriatic (Carboonara et al., 20155) Tab ble 1.3. Spaw wning season of o M. barbatus s barbatus in th he Mediterran nean

Mullidae Günther, 1859

21

Spawning is fractionated as shown by the frequency distribution profile of oocyte diameter given by different authors (Ferrer-Maza et al., 2015; Carbonara et al., 2015). Fecundity: For individuals between 9.4 and 22 cm in size, fished north of the Aegean Sea, Tirasin et al. (2007) give an average absolute fertility of 7,030 (summer 1991) and 7,960 oocytes (spring 1992). To the north-west and north-east of the Levantine Sea, they obtain 11,180 and 13,000 eggs, respectively. In all cases, absolute fecundity is positively correlated with fork length. For all the regions studied, the relative fertility is between 128 and 216 eggs/g per female. Layachi et al. (2007) estimated the average absolute fecundity of red mullet from Nador (Morocco) to be 36,665 ± 19,773 eggs and the relative fecundity to be 513 ± 226 eggs/g per female. On Spanish Mediterranean coasts, Ferrer-Maza et al. (2015) found that fertility by spawning is between 2,408 and 43,736 oocytes (18,163 ± 9,778). It is positively correlated with female size (F = 0.33.TL3.627; r2 = 0.75; n = 89) and their eviscerated mass (F = 272.3. Me – 2554.9; r2 = 0.76; n = 89). Relative fertility by spawning is between 61 and 371 oocytes per gram of eviscerated weight. These authors also show that the most abundant helminth parasites with the highest prevalence (Opecoeloides furcatus and Hysterothylacium spp.) affect the condition of fish and their reproduction during the spawning season. The former causes a decrease in energy reserves, and the latter weakens the quality of eggs laid. There is a positive correlation between total length and fecundity by spawning for the red mullet in the southern Adriatic (F = 0.9993.e0.384. TL, n = 100, r2 = 0.6264), which is higher in May than in June (Carbonara et al., 2015). The diameter of the oocytes and their lipid globule, as well as the amount of plasma vitellogenin, are also positively correlated with female size (Carbonara et al., 2015). Reproductive behavior: Thresher (1984) describes the spawning behavior: males and females swim from the bottom toward the surface where they release their gametes. Spawning is nocturnal. Eggs, larvae and ontogenesis: Raffaele (1888) indicates that there are fewer eggs and fry of M. barbatus than those of M. surmuletus. Montalenti (1937), based on Lo Bianco (1909, pl. II), gives a description and figures of the larvae and fry of M. barbatus measuring 4.5–45 mm; their eggs have a single oil globule. Marinaro (1971) describes eggs as pelagic, spherical, “vesicular” yolk; in the larvae, the oil globule protrudes from the anterior part of the yolk. This author found that on comparing the eggs of the two species, M. b. barbatus and M. surmuletus, in the Bay of Algiers, the eggs of M. b. barbatus are significantly smaller than those of M. surmuletus (Raffaele 1888). In both cases, egg size decreases during the spawning season (Figure 1.11).

22

Fish hes in Lagoons and Estuaries in n the Mediterran nean 3B

Figu ure 1.11. Mea asurements an nd seasonal diistribution of M. M barbatus an nd M. surmulletus eggs in the t Bay of Alg giers (Marinaro o, 1971)

Metrric characterisstics of M. baarbatus barba atus eggs in different d regioons of the Mediterrranean are preesented in Tabble 1.4. Eggg diameter (mm)

Globule diameteer (mm)

Spawningg season

0..68–0.75

0.17–0.21

June––July

Israel (W Wirszubski, 19533)

0.965

0.200–0.233

–

Chioggiaa (Varagnolo, 19964)

0.65

0.20

May––June

0..63–0.80

0.16–0.21

May––July

S Sites and authorss Marseille (Holt, 1899)

Algiers (Marinaro, ( 1971)

Table 1.4. Metric M charactteristics of M. barbatus barb batus eggs in different reg gions of the Mediterranean

1.1.1.7. Economic im mportance Fishiing is semi-iindustrial, arttisanal and recreational. Trawling T is tthe main method used, amongg others, inclluding seine--haul fishing, gillnetting, fyke net fishing, hand h line fishhing and underrwater fishing g. Trammel neets mainly conntribute to catchingg larger indiviiduals, while trawling targ gets smaller individuals i annd newly recruitedd individuals (Martin ( et al., 1999). Red mullet m is reguularly present in Mediterran nean markets and a occasionaally in the Black Sea. S It is solld fresh, chillled, frozen and a salted (F Fischer et all., 1987).

Mullidae Günther, 1859

23

According to FAO data, all its production comes from the Mediterranean, increasing from 3,994 to 15,618 tons between 1985 and 2007. Until 2004, Turkey and Tunisia were the main producers; subsequently, Italy became the largest supplier with around 9,000 tons/year. In 2007, the main producing countries were Italy (9,463 tons), Tunisia (2,807 tons) and Turkey (2,390 tons). These three countries alone account for 93.8% of the Mediterranean produce. Overall, M. barbarus is overfished in the Mediterranean, and in many areas juveniles make up the largest proportion of catches: Gulf of Gabes (Gharbi et al., 2004), Aegean Sea (Vassilopoulou and Papaconstantinou, 1991), Izmir Bay (Özbilgin et al., 2004), Gulf of Saronikos in the Aegean Sea (Napoléon et al., 1991), Ionian Sea (Tursi et al., 1994, 1996) and north-west Mediterranean (Demestre et al., 1997). 1.1.1.8. Protection status, conservation According to the latest report of the European Union, dated December 21, 2006, the capture of any individual under 11 cm is prohibited, regardless of the technique used. – Global IUCN Red List: NE. – Mediterranean IUCN Red List: LC. 1.1.2. Mullus surmuletus Linnæus, 1758

1.1.2.1. Nomenclature and classification Type: Mullus surmuletus Linnæus, 1758, M. Mediterraneo et ad Cornubiam).

Syst.

Synonym: Mullus barbatus surmuletus Day, 1880.

Nat.

Edit.

X: 30

(in

24

Fishes in Lagoons and Estuaries in the Mediterranean 3B

Vernacular names1: Rouget (DZ), salmonete de roca (ES), rouget barbet de roche, surmulet (FR), surmullet (GB), barbouni (GR), mulit happassim (IS), triglia di scoglio (IT), trilja tal-qawwi (MT), trilia hamra, mallou (TN), tekir (TR). Etymology: From the Latin mulleus (reddish, reference to the color of the animal); surmuletus, from sur (superior to) and mullus, muletus (name of the red mullet fish). 1.1.2.2. Description Morpho-anatomy: The surmullet has a fairly compressed body, a convex dorsal head and a slanted snout. Under the chin, there is a pair of barbs that are longer than the pectoral fins. The operculum is spineless. The mouth is small with a maxilla not exceeding the anterior edge of the eye. Small villiform teeth are present on the lower jaw. The upper jaw is edentulous, but teeth are present on the oral vault (vomer bone and palatine plates). The first dorsal fin is colored with contrasting bands, and seven or eight spines, the first of which is very small. The second fin has one spine and seven or eight soft rays; the anal fin has two spines and six or seven soft rays. The caudal fin has no streaks. The scales are large and slightly adherent, 33–37 on the lateral line, two on the suborbital. Maximum length is 40 cm; 25–30 cm is the average size. In the Gulf of Lion, the maximum size is 33 cm, with one exception at 38 cm (Campillo, 1992). Coloring: The coloring is reddish, usually with a dark red longitudinal band from the eye to the caudal fin and three yellowish lines along the flanks. The color varies with age and the surrounding environment, as well as with depth and stress responses. On sandy bottoms, they are paler with a reddish-brown longitudinal line. On rocky surroundings, they are darker in color and often more mottled. The dominant red is reinforced with depth (visible only with a lamp). Tokaҫ et al. (2013) point out abnormal pigmentation in an individual 16.4 cm SL captured in Izmir Bay (Turkey). Variations: Sabatini et al. (2007) studied the spinal morphology of Sardinian surmullets. Although the total number of vertebrae is constant (24), there is a difference in the number of abdominal and intermediate vertebrae with 7 + 3 in 39% and 6 + 4 in 61% in individuals studied, respectively. These differences are not influenced by size or sex, but instead are due to differences in environmental conditions affecting the early stages of ontogenesis.

1 Abbreviations: (DZ) Algeria, (EG) Egypt, (ES) Spain, (FR) France, (GB) Great-Britain, (IS) Israel, (IT) Italy, (MA) Morocco, (MT) Malta, (TN) Tunisia, (TR) Turkey.

Mullidae Günther, 1859

25

Sexual dimorphism: The data provided by Desbrosses (1936) for the North Atlantic may be transposable to individuals in the Mediterranean. This author indicates that at a size greater than 17 cm, the female is distinguished by a more elongated muzzle in relation to the size (TL) and especially to eye diameter, and by the position of its odd fins, which are slightly further back. Males have a short muzzle and relatively bulky eyes, reminiscent of the red mullet. The interorbital space is, on average, less than the eye diameter. Fin rays, scales and vertebrae are similar in both sexes, but the variability is lower in males with less plasticity than females (Desbrosses, 1936). However, in practice, it is only possible to distinguish between sexes during the spawning season, when the female is recognized by her extended abdomen. Osteology, otoliths and scales: Sagittal otolith data are provided by Koken (1884), Sanz Echeverria (1926, 1936) and Chaine (1938). More recently, for WestMediterranean and East-Atlantic otoliths, Tuset et al. (2008) give a very detailed description, including the following characteristics: oval overall shape with crenellated irregular edges (Figure 1.12); otolith length/total length of fish = 1.4–2.0; otolith width/otolith length = 69.5–75.4; circularity = 14.0–19.3; rectangularity = 0.1–0.2.

Figure 1.12. Sagittal otolith of an individual (12.3 cm TL) of M. surmuletus from the Western Mediterranean, scale 1 mm (Tuset et al., 2008)

From north-western Mediterranean samples, Aguirre and Lombarte (1999) expressed the relationship between the otolith surface area (O) and the total fish length

26

Fishes in Lagoons and Estuaries in the Mediterranean 3B

(TL) by the equation O = 0.0159 TL1.1147 (r2 = 0.9750, n = 91). They also give the relationship between the surface of the sulcus acusticus (S) and the total length of the fish by the equation S = 0.0020 TL1.2640 (r2 = 0.9245, n = 82). The S:O ratio changes during development (t = –2.1692, P = 0.0329) increasing with the length of fish. Morat et al. (2008) describe the relationship between the total length (mm) and length of sagittal otoliths (mm) of M. surmuletus using the following regression equations for individuals in the north-western Mediterranean and the Aegean, respectively: TL = 82.33 Lo – 57.87 (79–300 mm, r = 0.870, P < 0.0001), TL = 79.30 Lo – 48.25 (110–205 mm, r = 0.873, P < 0.0001). Mullus surmuletus, like all mullet, has ctenoid scales (Figure 1.13) (Morales-Nin and Fauquet, 1983).

Figure 1.13. Ctenoid scale of M. surmuletus (Morales-Nin and Fauquet, 1983)

The anterior field, deeply embedded in the dermis, has circulii separated by about 11 µm. Under a scanning electron microscope, small protrusions in groups of three to five can be seen on their upper part. Circulii are regularly separated by radii. The number of radii depends on the size and age of the fish. There are between 4

Mullidae Günther, 1859

27

and 6 radii, fewer than in M. barbatus, with 4 being most common. The posterior field is composed of two parts: a large central part known as the lunula and a marginal fringe. The lunula is traversed by thin ridges and is devoid of denticles. The marginal fringe has spines, known as the ctenii. The scales of the lateral line have, in their central zone, a channel that traverses them longitudinally. The inner part has a wide opening. The channel splits in the posterior part of the shell into two which, in turn, divide into secondary channels, which open by four pores. Karyology: The number of chromosomes in M. surmuletus is 2n = 44. They are arranged in 22 pairs. Four pairs are metacentric or submetacentric (1–4), eight are subtelocentric (5–12) and 10 are acrocentric (13–22) (Vitturi et al., 1992). Protein specificity and genetic diversity: The protein specificity of this species is discussed in the equivalent section on M. barbatus barbatus. Using RAPD and allozyme markers, Mamuris et al. (1999b) sought to evaluate genetic polymorphism in M. surmuletus in six Mediterranean locations, five in Greece (three in the Aegean Sea: Trikeri, Kavala, Rhodes; two in the Ionian Sea: Preveza, Corfu) and one in France (Gulf of Lion). Both methods demonstrated a high level of genetic polymorphism, with mean Fst values of 0.053 and 0.035 (P < 0.05) and genetic distances of 0.018 and 0.011, respectively. In both cases, the sample from the Gulf of Lion differs from those of Greece. However, only RAPDs show that there is a correlation between genetic divergences and geographical distances (Mantel t-test, r = 0.72, P < 0.01). On the other hand, greater heterogeneity is found in the Aegean than in the Ionian Sea. Mamuris et al. (2001) used two other types of molecular markers on these same six samples (RFLP and mitochondrial DNA) and came to fairly similar conclusions. They highlight that the species is structured into three distinct clades, reflecting a certain degree of isolation by distance. Two samples from the Aegean Sea (Trikeri and Kavala) form one clade, while the two populations in the Ionian Sea (Preveza and Corfu) and the Gulf of Lion form another clade: the French sample is different to those from the Ionian Sea. The third clade contains only the population from Rhodes (Aegean Sea). Galarza et al. (2009) analyzed the variations in allelic frequencies at 10 microsatellite loci on samples of M. surmuletus from nine Mediterranean sites (Cabo de Gata, Herradura, Majorca, Blanes, Italy, Porticello, Syracuse, Greece and Turkey) and two Atlantic sites (Canary Islands and Conil). There is low heterogeneity in this species in the Mediterranean, as well as a low gene flow between the Mediterranean and the Atlantic. Using 10 microsatellite markers, Félix-Hackradt et al. (2013) found great spatial variability in mullet samples from 13 sites 400 km apart on the Spanish Mediterranean coast. The authors indicate that larval life history traits alone do not explain the dispersal abilities of this species and suggest other mechanisms play an important role, such as small-scale

28

Fishes in Lagoons and Estuaries in the Mediterranean 3B

movements of adults or juveniles, which are not always recognized as promoters of population connectivity. 1.1.2.3. Distribution Common in the Mediterranean and the Black Sea, M. surmuletus is also found in the Red Sea in the Gulf of Eilat (Ben Eliahu and Golani, 1990). It lives in the eastern Atlantic, from Scotland to Senegal and the Canary Islands. Its presence in Norway, Ireland, on the northern coast of England and west of Scotland, is less frequent (Pethon, 1979; Minchin and Molloy, 1980; Davis and Edward, 1988; Gibson and Robb, 1997; Beare et al., 2005) (Figure 1.14).

Figure 1.14. Geographic distribution of M. surmuletus

1.1.2.4. Ecology Habitat: Its habitat is demersal and gregarious, and M. surmuletus is often found on loose substrates: sand, gravel, eelgrass beds or posidonia. However, it may venture close to rocks, seeking food with its two characteristic barbels. In the

Mullidae Günther, 1859

29

north-west Mediterranean (Medes Islands and along the coast between Estartit and Blanes), García-Rubies and MacPherson (1995) found red mullet juveniles (TL > 1.5 cm) mainly at the base of posidonia. Deudero (2002) showed that juveniles of M. surmuletus (2–6 cm) were attracted to light in the epipelagic waters of the continental shelf of Majorca. It should be noted that red mullet sometimes sleep in groups in seagrass beds and have a characteristic marbled hue. On the Cretan coasts (Greece), M. surmuletus is frequently found at depths of –28 and –310 m, at temperatures between 13.6 and 23.8 °C (Machias et al., 1998). From 392 research trawls, conducted between 1994 and 1998 along the Spanish Mediterranean coast between 0 and 400 m, Lombarte et al. (2000) found that this species is more abundant on rough bottoms (gravel, sand) (116.14 ind⋅km–2) than on loose muddy substrates (42.63 ind⋅km–2). Significant differences also exist depending on the depth of the rough substrate, with a maximum abundance near the coast, in shallow waters (146.46 ind⋅km–2). A greater average size is also observed with increasing depth, especially on rough bottoms (10–50 m: 16.47 cm; 200–400 m: 26.25 cm). In addition, sea beds on a narrow continental shelf are more attractive to this species. Levi and Francour (2004) found a lower density of M. surmuletus on substrates colonized by the invasive alga Caulerpa taxifolia, limiting their access to benthic prey. A study conducted in the Gulf of Lion between 1983 and 1992 (Gaertner et al., 1999) shows that the bathymetric distribution of M. surmuletus varies. According to Hureau (1986), its presence is limited to depths less than 100 m, whereas MacPherson and Duarte (1991) find it to be between 12 and 182 m and even –409 m in the Ionian Sea (Mytilineou et al., 2005) and 500–800 m west of Sardinia (Tserpes et al., 2002). Zoubi (1994) rarely found it beyond 200 m in Morocco, with the smallest ones (6–17 cm TL) being more abundant between 0 and 100 m, the others (12–23 cm) beyond 100 m; this increase in size with depth is confirmed by Papaconstantinou et al. (1981). Off Majorca, the highest concentrations are observed between 30 and 70 m (Renones et al., 1995). Machias et al. (1998) studied for three consecutive years and during three seasons (summer, winter and fall), the abundance and the biomass of surmullet at different depths. They found that abundance and biomass are negatively correlated with depth during all seasons. The increase in relative abundance and biomass with depth indicates that fish, generally dominant in shallow waters, increase their presence in intermediate depths (stratum II, 71–150 m) during the spring. The authors suggest seasonal bathymetric movement in relation to recruitment. The relationship between mean total length and depth is significantly positive at all seasons (0.645 ≤ r ≤ 0.833, P = 0.000). Its relationship with temperature is significantly negative in summer (r = –0.670) and winter (r = –0.601), but not in spring (r = –0.215). Size distribution by depth indicates

30

Fishes in Lagoons and Estuaries in the Mediterranean 3B

that individuals larger than 15.5 cm (size at first sexual maturity) are generally found in stratum II during summer and winter. The same is true for individuals over 16.5 cm in the spring. Migrations and movement: One- to 2-month-old surmullets settle on the seabed at the end of June off the Mediterranean French coast (Bougis, 1952a, 1952b). They are 3.5–4 cm in size, but are still very elongated and have a coloring typical in open water: blue-green back and pearly white belly (Louisy, 2005). They reach 6–7 cm in August in Banyuls Bay (Bougis, 1952a, 1952b). In October, individuals approximately 4 months old were fished at depths between 0 and 40 m. In the North Atlantic, the migration of red mullet to greater depths is not directly related to their age, but rather to their size (Desbrosses, 1935a). Due to their faster growth, females are more common than males at greater depths. Ecological valence: Devauchelle (1980, 1983) has experimentally shown that the embryogenesis of red mullet may be affected by changes in environmental factors and degradation of water quality. Significant thermal shock (10–17 °C), short in duration (5–20 min), causes malformations of the spine, resulting in an increase in severity with increasing temperature. Chlorations at 1 ppm for 5–10 min or rapid and fleeting overpressures (2–5 bars) and depressions (0.3 bar) do not modify the eclosion rate. Eggs are more resistant to shock than the larvae. Size, lifespan and growth: In Majorca, M. surmuletus reaches an age of 6 years (females of 31.6 cm TL and males of 23.0 cm TL) (Reñones et al., 1995). According to Quéro and Vayne (1997), the lifespan could be 11 years on the French Atlantic coast. The age of red mullet can be determined on both scales and otoliths. Table 1.5 gives the growth parameters of the von Bertalanffy model and the length–weight relationship, obtained at different Mediterranean sites. Compared to other fish species, M. surmuletus grows relatively slowly. At 3 years old, its average weight is 95 g (19.4 cm) in males and 135 g (21 cm) in females off the Tunisian coast (Gharbi and Ktari, 1981a); along the coasts of Provence in France: 145 g (22.5 cm) and 270 g (27 cm) (Bougis, 1952a, 1952b), where growth is the greatest. Male growth is always lower than that of females (Bougis, 1952a, 1952b; Gharbi and Ktari, 1981a; Renones et al., 1995).

Majorca (Morales-Nin, 1991)

Strait of Sicily (Andaloro and Giarritta, 1985)

Catalonia, Spain (Sánchez et al., 1983)

Tyrrhenian Sea (Andaloro, 1982)

Tunisia (Gharbi and Ktari, 1981)

Sites and authors

23.29 29.76

F+M

34.53

F

M

–

F+M

29.75

F 26.25

32.52

F+M

M

–

–

F

M

–

F+M

30.12

F 25.02

21.51

F+M

M

19.87

21.82

F

M

L∞ (cm)

Sex

0.2376

0.2882

0.1365

–

0.41

0.49

0.1097

–

–

–

0.30

0.24

0.50

0.49

0.51

K (year-1)

–2.64

–3.3250

–3.8210

–

–0.25

–0.31

–3.6478

–

–

–

–2.68

–2.39

–0.116

–0.025

–0.112

t0

2.3231

2.1940

2.2115

–

2.4507

2.6370

2.0632

–

–

–

2.2737

2.3379

2.3643

2.2866

2.3853

Ф

–

–

3.070

–

–

3.10

3.19

2.84

3.2051

–

–

3.283

3.351

b

0.016003 2.91282

–

–

0.0093

–

–

0.0073

0.0069

0.027

0.0067

–

–

0.1443

0.1403

a

9.5–27

9.8-26.7

5–26

4–28

?

Size interval (cm)

Mullidae Günther, 1859 31

F+M

F+M

F+M

Izmir Bay, Turkey (Ilhan et al., 2009)

Edremit Bay, Aegean Sea (Torcu-Koç et al., 2015)

Homa Lagoon, Turkey (Acarli et al., 2014) –

–

27.85

31.74

–

–

0.193

0.47

0.211

0.273

0.205

–

0.53

0.43

–

–

–1.578

–0.3

–2.348

–2.450

–2.605

–

–0.44

–0.60

–

–

2.175

2.67

2.3148

2.2505

2.3192

–

–

–

3.0672

3.1090

3.00

–

–

0.0040

0.0042

0.0083

0.0104

3.372

3.36

3.127

3.0617

0.009101 3.12035

0.01045

0.00950

0.0182

–

–

Table 1.5. Growth parameters of the von Bertalanffy model and size–weight relationship (W = aLb) and growth performance index Ф of Mullus surmuletus in different regions of the Mediterranean

F+M

31.28

F+M

31.90

F 25.54

–

F+M

M

28.5

33.4

M

F

Egypt (Mehanna, 2009)

Majorca (Reñones et al., 1995)

Gulf of Lion, France (Campillo, 1992)

4.7–10.2

7.7–17

6.6–22.6

5–29.1

10–32

–

–

?

32 Fishes in Lagoons and Estuaries in the Mediterranean 3B

Mulllidae Günther, 1859

33

Popuulation structture and dynnamics: In th he Mediterrannean, in Majorca, the majorityy of individualls under 13 cm m are of indeeterminate sexx. Males are ppresent in samples of 11–28 cm m and predom minate between n 14 and 17 cm, while fem males are present between b 12 annd 32 cm and dominate in sizes s larger thaan 19 cm (Figgure 1.15) (Reñonees et al., 1995)).

Figure 1..15. Proportion n of males, fem males and ind dividuals of undetermined d sexes in diffe erent size clas sses of M. surmuletus fished d i Majorca bettween 1990 an in nd 1992 (n = 3541) 3 (Reñones et al., 1995 5)

In thhe Bay of Edrremit in the Aegean A Sea, th he sex ratio iss generally inn favor of males wiith an averagee of 63.46% (T Torcu-Koç et al., 2015). Tserppes et al. (2002) conductted trawl surv veys coveringg a large paart of the Mediterrranean (1,000 sampling poiints in 15 majjor regions) between b 10 annd 800 m annuallyy from 1994 too 2000. Size frrequency distrribution by reggion is shown in Figure 1.16. In the western Meediterranean, this t distributio on is polymoddal. However, although the cohoort of young recruits is cllearly unique in the Ligurrian Sea, norrth of the Tyrrheniian Sea and in Sardinia,, only relativ vely older inndividuals arre found. Similarlyy, in the easttern Mediterraanean, the diistribution is polymodal annd young recruits are a present inn all regions exxcept the nortthern Adriaticc and northernn Aegean. The maxximum averagge length is greater g in the western Medditerranean (222–33 cm) than in the t east (15–228 cm). In thee northwestern n Mediterraneean, M. surmuuletus and M. barbaatus are recruuited mainly in i the fall, wh hich results inn an increasedd number

34

Fish hes in Lagoons and Estuaries in n the Mediterran nean 3B

caught during d this perriod (Lloret annd Lleonart, 2002). 2 It is also between September and Novvember that the t influx of Mullidae is the t greatest inn several Spaanish and Italian poorts (Martin et e al., 1999).

Figure 1.16. 1 Distributiion of length frrequencies (T TL in cm) of M. surmuletus in n different areas off the Mediterrranean. Num mbers in pare entheses indiicate average e relative abundan nce over the period p sample ed, expressed d as number of individualss per km2 (Tserpess et al., 2002)

Mullidae Günther, 1859

35

Predators: The main predators are carnivorous fish: bass, hake, barracudas, conger, monkfish and sharks. 1.1.2.5. Diet and feeding habits Diet: The red mullet is carnivorous (Labropoulou and Eleftheriou, 1997). In the Gulf of Annaba (Algeria), crustaceans (index of relative importance (IRI) = 85.19%) are preferred prey, with annelids in second place (IRI = 11%), followed by mollusks, in particular bivalves, echinoderms, cnidarians, teleosts and plants with IRI values below 2.5% (Derbal et al., 2010). In the Gulf of Tunis, crustaceans are the preferred prey (Cn = 71.86; F = 94.34); lamellibranches (Cn = 9.51; F = 29.63) and echinoderms (Cn = 8.1; F = 23.15) are secondary prey. Polychaete annelids (Cn = 9.72; F = 8.30) and algae (F = 2.78) are accessory prey (Gharbi and Ktari, 1979). Crustaceans, especially the mysids, are particularly common in the diet of mullet on the Tyrrhenian coasts; Nereididae and Owenidae are also quite common (De Pirro et al., 1999) and the species has a trophic overlap with the wrasse Coris julis. On the Cretan coasts, crustaceans (amphipods and decapods) also dominate (Labropoulou et al., 1997), as well as in the Aegean Sea (Vassilopoulou et al., 2001). In the Gulf of Lion, the diet consists mainly of polychaetes and different crustaceans, such as amphipods, shrimps, crabs, cumaceans, krill, mysidae and isopods (Bautista-Vega et al., 2008). In the Stagnone di Marsala lagoon (Sicily), juveniles are strictly benthivorous (Lombarte and Aguirre, 1997). They feed on organisms living in association with Cymodocea nodosa or on the sediment surface where polychaetes and harpacticoid copepods are the preferential prey. Each individual in the population of the Gulf of Annaba ingests an average of eight prey at a total weight of 0.25 g (Derbal et al., 2010). These values are different from those obtained in Crete (N = 6.18; P = 0.43 g) (Lapropoulou et al., 1997). Feeding behavior: Surmullet detects buried prey through their barbels, and then digs the sand with large bites to unearth them. This earth-moving activity often attracts other fish (seabream, wrasse – coris sp. and symphodus sp.), ready to jump on prey that try to escape (Louisy, 2005). The grazing behavior and activity of M. surmuletus are influenced by proportion of vegetation cover at the site. When this coverage (phanerogams and/or macrophyte algae Caulerpaceae) increases, grazing effort and distance traveled in search of prey decreases significantly (Longepierre et al., 2005). Similarly, the survey period increased to ensure the successful location of fish swimming above the sea bed. These changes are related to the development of a dense surface network of rhizomes and stolons and the reduction of space between fronds, which limits access to resources and increases intraspecific trophic competition. From this point of view,

36

Fishes in Lagoons and Estuaries in the Mediterranean 3B

the role of Caulerpa taxifolia does not differ from that of other marine phanerogams, but it induces changes in the structure of Mullidae populations at the local level. Feeding variations and rhythms: In the Stagnone di Marsala lagoon, juveniles feed during the day (Lombarte and Aguirre, 1997). According to Mazzola et al. (1999), the stomach vacuity of juveniles (SL = 48 ± 1.67 mm) varies throughout the day; it is 0% in individuals caught during the day and 100% among those captured at night. The diurnal phase (12–18 h) is characterized by the presence of isopods, ostracods, cumaceans, polychaetes and amphipods in their diet; the nocturnal phase (20–8 h) is characterized by the presence of copepods, mysidae and tanaïdacea. In this same lagoon, 5 cm individuals feed between 8 am and 11 pm, with peaking between 12 pm and 8 pm (La Rosa et al., 1997). At this size, average daily consumption is close to 8% of the body’s dry weight (Mazzola et al., 1999). This diurnal feeding behavior is still found in adults (De Pirro et al., 1999). In the Gulf of Annaba, adults from 12.2 to 28.8 cm TL feed throughout the year, including during the period of gonad maturation (from February to June) and have an average digestive vacuity coefficient of 34.47% (Derbal et al., 2010). This value is between that recorded in Crete (17.26%) (Labropoulou et al., 1997) and that obtained in the Gulf of Tunis (63.8%) (Gharbi and Ktari, 1979). Karachle and Stergiou (2008) recorded a value of 58.2% for individuals with a total length of between 9.1 and 23.1 cm. The predominance of crustaceans, particularly amphipods, was observed regardless of the season and size of the fish in the Gulf of Annaba. However, Spearman’s rank correlation coefficient shows the difference in spring and summer regimes (ρ = 0.75; P = 0.01), on the one hand, and fall and winter (ρ = 0.67; P = 0.01), on the other hand (Derbal et al., 2010). Seasonal variations are also observed in Crete: decapods are more numerous in summer, whereas amphipods dominate in winter and spring (Labropoulou et al., 1997). The composition of the prey ingested also varies according to predator size with the occurrence of cephalopods (majority of the “various” group) exclusively in individuals over 161 mm TL. The average weight of the stomach contents increases significantly in fish larger than 171 mm (TL), whereas the average number of prey does not differ according to size (Labropoulou et al., 1997). In the Gulf of Lion, a change in diet is observed only between average sized individuals (110–180 mm TL) and large individuals (>180 mm TL) (Bautista-Vega et al., 2008), with an increase in the consumption of bivalve mollusks and brittle stars in large individuals. Aguirre and Sanchez (2005) also showed a regime change during the ontogenetic development of fish and a sharing of food resources with the congeneric species M. barbatus in the northwestern Mediterranean; this is also the case in the Aegean Sea (Vassilopoulou et al.,

Mullidae Günther, 1859

37

2001). In addition, the same prey are consumed by males and females in the Gulf of Tunis, but in different amounts (Gharbi and Ktari, 1979). In the Levantine Sea or Lessepsian Sea, M. surmuletus feeds primarily on decapods, particularly the Pasiphaeidae species Leptochela pugnax, native to the Red Sea. This species is also the main prey of the congeneric species M. barbatus and two colonizing species Upeneus asymmetricus and U. moluccensis. The cohabitation, in these conditions of trophic overlap, of native and colonizing species, can be explained by their spatial structuring (Golani and Galil, 1991). 1.1.2.6. Reproduction and reproductive behavior Sexuality: Gonochoric species with lobular testes. Migration of spermatocytes and spermatids takes place centripetally and spermatozoa are collected in the lobule lumen from which they reach the vas deferens (Billard, 1986). First sexual maturity: On Tunisian coasts, the smallest mature female recorded was 13.8 cm TL (10–14 months); the first maturity is at 17 cm, and at 18 cm (end of the second year of life) all individuals are mature. The smallest mature male captured measured 12.6 cm TL (10–14 months). From 14 cm, all males are sexually mature (Gharbi and Ktari, 1981b). In Majorca, sexual maturity is reached at 16.8 and 15 cm in females and males, respectively. They are all immature below 13 cm and 100% mature above 26 cm (Reñones et al., 1995). These values are very similar to those recorded in Provence by Bougis (1952a, 1952b): 16 and 15 cm in females and males, respectively. For the Gulf of Lion, Campillo (1992) indicates a length of 14 cm TL and an age of 2 years. Vassilopoulou and Papaconstantinou (1991) found that the first maturity of males (11.6 cm) and females (13.8 cm) is earlier in Greece. Spawning site and period: The spawning sites of M. surmuletus in the Mediterranean are not documented. In the North Atlantic, mature red mullet are reported by Desbrosses (1935a) beyond a depth of 100 m at temperatures between 9.5 and 11.9 °C and salinities of 35.1–35.6‰. In the Canary Islands, spawning is observed primarily between 19 and 22 °C (Pajuelo et al., 1997). In the Mediterranean, females spawn from spring until early fall (Table 1.6). Sites and authors France, Mediterranean (Bougis, 1952a, 1952b) Algeria (Lalami, 1971)

J

F M A M J

J

A

S O N D

38

Fish hes in Lagoons and Estuaries in n the Mediterran nean 3B

Egypt (Hashem, 1973bb) Tunisia (Gharbi and Ktaari, 1981) Gulf of Lion (Campillo,, 1992) Majorcaa (Renones et al.., 1995) Bay of Edremit, E Aegeaan sea (Torcu--Koç et al., 2015) Table 1.6. Spawning periods of fe emale M. surm muletus s in the Me editerranean in different sites

In Majorca, M the period p of sexuual activity iss shorter in females f than in males (Figure 1.17); it occurrs from March to June with h a maximum m percentage oof mature individuals in April annd May.

Figure e 1.17. Monthlly percentage of mature fem males (1,868) and males (1,,429) in Majorca over o three con nsecutive years rs (Reñones ett al., 1995)

Mulllidae Günther, 1859

39

Figure 1.18.. Monthly varia ations in gonado-somatic index in female (547)) and male (46 69) M. surmule etus in Majorc ca in 1992 (Re eñones et al., 1995)

Althoough mature males m are obsserved through hout the year,, with the excception of Septembber, male sexuaal activity exteends from Deccember to Junee, with a peak in March and Apriil (Figure 1.188) (Reñones ett al., 1995). Gharbi G and Ktaari (1981b) also found a longer sppawning period in males thaan females in Tunisia. T In Majorca, M the maximum m GSI values observ ved are 9% inn females andd 3.5% in males (R Reñones et al., 1995). They are, respectiveely, 5 and 2.7 in Tunisia (G Gharbi and Ktari, 19981b), and aboout 2% in botth sexes in thee Bay of Edreemit in Turkeyy (TorcuKoç et al., 2015). In Provencce (France), Bougis (19552) found m maximum hepatosoomatic index (HSI) values inn May in femaales (3%) andd in July in maales (2%). These vaalues are obseerved at the ennd or after the spawning period, which iis not the case for most fish. The author attribbutes these unu usual kinetics to the dynam mic role of the liverr in red mulleet which transsforms fats an nd does not only o accumulate them, which is the case with other species of fish. Fecundity: In capttivity, a fem male weighing g 400 g is likely to proovide 22 n, with an averrage volume oof 16,200 consecuttive spawning eggs per spaawning season eggs per spawning durring an observaation period of four consecuutive years. In captivity, fecundityy can thus reaach 850,000 eggs e per kilog gram per year (average of 4 years of spawningg by a single female) f (Devauuchelle, 1983)). Egg, larvae and ontogenesis: We W are not awaare of any speecific descriptiion of M. surmulettus eggs in theeir natural enviironment. Thee eggs obtainedd by Raffaele (1888) in an aquarrium have a diiameter of 0.933 mm and a liipid globule off 0.23 mm acccording to Montalleenti (1937); a sketch of the larvae at hatcching and at 6–7 6 days is given. The

40

Fishes in Lagoons and Estuaries in the Mediterranean 3B

larva is characterized by an elongated yolk sac, pointed at the front, and carrying the oil globule anteriorly, which protrudes far beyond the snout. Marinaro (1971) approaches the Mullidae family from this point of view (see M. barbatus barbatus). Table 1.7 provides additional information on the geographical variations on the size of eggs and their lipid globules. Egg diameter (mm)

Globule diameter (mm)

Spawning season

0.93

0.23

May–August

Marseille (Holt, 1899)

0.86–0.87

0.22–0.24

April–May

Marmara (Arim, 1957)

0.82–0.85

0.22–0.23

–

Marseille (Aboussouan, 1964)

0.85–0.89

0.19–0.23

May–July

Algiers (Marinaro, 1971)

0.78–0.93

0.19–0.23

April–June

Sites and authors Naples (Raffaele, 1888)

Table 1.7. Metric characteristics of M. surmuletus eggs in different regions of the Mediterranean

In aquaculture, eggs obtained have only one lipid globule and are small in size. Their average diameter is 0.88 mm with upper and lower values of 0.81– 0.94 mm (Menu and Girin, 1978–1979; Devauchelle, 1983). Egg size is little affected by spawning age (Devauchelle, 1983). 1.1.2.7. Economic importance According to FAO data, M. surmuletus is only captured in the Mediterranean where it is regularly and/or occasionally present on the market. With an irregular progression, its overall production varied from 3,994 to 15,618 tons between 1985 and 2007. Until 2004, Turkey then Tunisia were the main producers with 5,900 tons/year. Since 2005, Italian inputs have increased production to 15,300 tons/year on average by contributing 61.3% to the total production. The fishing of red mullet is semi-industrial and artisanal. Fishing equipment used include beach seines and purse seines, trawls, gillnets, bottom longlines, fyke nets, hand lines and harpoons. Trawl catches dominate, both in number and weight, but vary greatly during the year; the largest quantities are fished in fall (Suquet and Person-Le-Ruyet, 2001). The sizes of the fish caught vary according to the type

Mullidae Günther, 1859

41

of fishing equipment used. According to Martin et al. (1999), in the western Mediterranean, seasonal fishing nets mainly capture adult individuals, while trawling catches newly recruited small individuals. These authors describe the overexploitation of both mullet species (M. surmuletus and M. barbatus) on the coasts of Italy and Spain, particularly the harmful effect of trawls, which catch immature individuals, while traditional methods are more selective and focus mainly on adult individuals. On the Egyptian coast, the exploitation rate E is 0.63 (M = 0.43; F = 0.73) and reflects a state of overexploitation of the stock (Mehanna, 2009). The yield per recruit and the spawning biomass values give an FMSY value of 0.53 and suggest a reduction in F by 27%. This reduction must be accompanied by a 59% increase in the fertile biomass. Surmullets breed in captivity, at least under certain conditions of shelter and feeding. Sequential data sets were obtained between early April and mid-June, corresponding to daylight conditions between 13 and 16 h 30 min and temperatures of 9.5–15 °C (Devauchelle, 1983). Ovules released and fertilized in open water are pelagic. The embryonic and larval development was described in detail by Menu and Girin (1978–1979). The temperature range compatible with embryogenesis covers a relatively wide range, 11–17 °C. Although the number of spawning attempts does not determine larval growth potential or ensure survival, the major difficulty in rearing this species is primarily due to the small size of the larvae at spawning (about 3 mm total length) and its low endogenous reserves, which are resorbed faster the higher the temperature. 1.1.2.8. Protection status, conservation – In the Medes Islands (Catalonia), 44 species were sensitive to fishing bans within a marine reserve, with the exception of surmullet and species from the Serranidae family (García-Rubies and Zabala, 1990). – IUCN Global Red List: NE. – Mediterranean Red List UICN: LC. 1.2. Bibliography ABOUSSOUAN A., “Contribution à l’étude des œufs et larves pélagiques de poissons téléostéens dans le golfe de Marseille”, Recueil des Travaux de la Stations Marine d’Endoume, 32 (48): 87-173, 1964.

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ACARLI D., KARA A., BAYHAN B., “Length-weight relation for 29 fish species from Homa lagoon, Aegean Sea, Turkey”, Acta Ichthyologica et Piscatoria, 44 (3): 249–257, 2014. AGUIRRE H., “Presence of dentition in the premaxilla of juvenile Mullus barbatus and Mullus surmuletus”, Journal of Fish Biology, 51: 1186–1191, 1997. AGUIRRE H., LOMBARTE A., “Ecomorphological comparisons of sagittae in Mullus barbatus and Mullus surmuletus”, Journal of Fish Biology, 55: 105–114, 1999. AGUIRRE H., SANCHEZ P., “Repartición del recurso trófico entre Mullus barbatus y M. surmuletus en el Mar Catalán (Mediterráneo Noroccidental). Feeding resource partitioning between Mullus barbatus and M. surmuletus in the Catalan Sea (Northwestern Mediterranean)”, Ciencias Marinas, 31 (2): 429–439, 2005. AKYUZ E.F., “Observation on the Iskenderum red Mullet (M. barbatus) and its environment”, General Fisheries Commission for the Mediterranean (GFCM) Proceedings and Technical Papers, 4: 93–99, 1957. ANDALORO F., “Résumé des paramètres biologiques sur Mullus surmuletus de la mer Tyrrhénienne méridionale et de la mer Ionienne septentrionale”, FAO Fisheries and Aquaculture Report, 266: 87–88, 1982. ANDALORO F., GIARRITTA S.P., “Contribution to the knowledge of the age and growth of striped mullet, Mullu barbatus (L. 1758) and red mullet, Mullus surmuletus (L. 1758) in the Sicilian Channel”, FAO Fisheries and Aquaculture Report, 336: 89–92, 1985. ARCULEO M., LO BRUTTO S., CAMMARATA M., SCALISI M., PARRINELLO N., “Genetic variability of the Mediterranean Sea Red Mullet, Mullus barbatus (Pisces, Mullidae)”, Russian Journal of Genetics, 35: 292–296, 1999. ARDIZZONE G.D., “Un tentativo di valutazione delle condizioni di Merluccius merluccius e Mullus barbatus nei mari italiani”, Biologia Marina Mediterranea, 5 (2): 151–168, 1998. ARIAS E., MORALES E., “Estudio comparative de los electroforegramas de las proteinas musculares soluble de Mullus surmuletus y Mullus barbatus”, Investigacion Pesquera, 41 (2): 323–330, 1977. ARIM N., “Marmara ve Karadeniz’de Bazı Kemikli Balıkların (Teleost’ların) Yumurta ve Larvalarının Morfolojileri ile Ekolojileri”, Hidrobiyologi mecmuası : İstanbul Üniversitesi Fen Fakültesi Hidrobiologi Araştırma Enstitüsü, Seri A, 4 (1–2): 7– 71, 1957. BASAGLIA F., CALLEGARINI C., “Biochemical characteristics of red mullet of the central Mediterranean”, Comparative Biochemistry and Physiology – Part B: Comparative Biochemistry, 89 (4): 731–736, 1988.

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BAUCHOT M.L., “Mullidae”, in W. FISCHER, M.L. BAUCHOT, M. SCHNEIDER (eds), Fiches FAO d’identification des espèces pour les besoins de la pêche. Méditerranée et mer noire – Zone de pêche 37, vol. 2. Vertébrés, p. 1195–1200, FAO, Rome, 1987. BAUCHOT M.L., PRAS A., Guide des poissons marins d’Europe, Delachaux et Niestlé, Paris, 1980. BAUTISTA-VEGA A.A., LETOURNEUR Y., HARMELIN-VIVIEN M., SALEN-PICARD C., “Difference in diet and size-related trophic level in two sympatric fish species, the red mullets Mullus barbatus and Mullus surmuletus, in the Gulf of Lions (north-west Mediterranean Sea)”, Journal of Fish Biology, 73: 2402–2420, 2008. BEARE D., BURNS B., JONES E., PEACH K., REID D., “Red mullet migration into the northern North Sea during late winter”, Journal of Sea Research, 53: 205–212, 2005. BEN ELIAHU M.N., GOLANI D., “Polycaetes (Annelida) in the gut contents of goatfishes (Mullidae), with new polychaete records for the Mediterranean coast of Israel and the gulf of Eilat (Red Sea)”, Marine Ecology Progress Series, 11: 193–205, 1990. BEN SADOK M., GHARBI H., EZZEDDINE-NAJAI S., “Mortalité par pêche et rendement par recrue du rouget de vase (Mullus barbatus Linnæus, 1758) de Tunisie”, Marine Life, 5(2): 35–46, 1995. BILLARD R., “Spermatogenesis and spermatology of some teleost fish species”, Reproduction, Nutrition, Development, 26: 877–920, 1986. BIZSEL K.C., Seasonal variations in the diet of the red mullets (Mullus barbatus L.) in the northern Sicilian Basin. Msc., Thesis, Institute of Marine Sciences, Middle East Technical University, Ankara, Turkey, 1987. BOUGIS P., “Recherches biométriques sur les rougets (Mullus barbatus L., Mullus surmuletus L.)”, Archives de zoologie expérimentale et générale, 89 (2): 57–174, 1952a. BOUGIS P., Recherches biométriques sur les rougets (Mullus barbatus L. et Mullus surmuletus L.), PhD thesis, University of Paris, 1952b. CAMMARATA M., PARRINELLO N., ARCUELO M., “Biochemical taxonomic differentiation between Mullus barbatus and Mullus surmuletus (pisces, Mullidae)”, Comparative Biochemistry and Physiology – Part B: Comparative Biochemistry, 99 (3): 719–722, 1991. CAMPILLO A., Les pêcheries françaises de Méditerranée : synthèse des connaissances, CEE/ Ifremer, 1992, available at: http://www.archimer/ifremer.fr.

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CARAGITSOU E., TSIMENIDES N., “Seasonal changes and comparative analysis of the food of the red mullet (Mullus barbatus) in the gulfs of Saronikos and Thermaikos”, Thalassographica, 5: 41–61, 1982. CARBONARA P., INTINI S., MODUGNO E., MARADONNA F., SPEDICATO M.T., LEMBO G., ZUPA W., CARNEVALI O., “Reproductive biology characteristics of red mullet (Mullus barbatus L., 1758) in Southern Adriatic Sea and management implications”, Aquatic Living Resources, 28 (1): 21–31, 2015. CARLUCCI R., GIUSEPPE L., PORZIA M., FRANCESCA C., ALESSANDRA M.C., LETIZIA S., TERESA S.M., NICOLA U., ANGELO T., D’ONGHIA G., “Nursery areas of red mullet (Mullus barbatus), hake (Merluccius merluccius) and deep-water rose shrimp (Parapenaeus longirostris) in the Eastern-Central Mediterranean Sea”, Estuarine, Coastal and Shelf Science, 83: 529–538, 2009. CHAINE J., “Recherche sur les otolithes des poissons”, Actes de la Société linnéenne de Bordeaux, 90: 5–258, 1938. CHAINE J., DUVERGIER J., “Recherches sur les otolithes des Poissons”, Actes de la Société linnéenne de Bordeaux, 87: 5–242, 1935 (1936). CHÉRIF M., BEN AMOR M.M., SELMI S., GHARBI H., MISSAOUI H., CAPAPÉ C., “Food and feeding habits of the red mullet, Mullus barbatus (Actinopterygii: Perciformes: Mullidae), off the northern Tunisian coast (Central Mediterranean)”, Acta Ichthyologica et Piscatoria, 41 (2): 109–116, 2011. CHÉRIF M., ZARRAD R., GHARBI H., MISSAOUI H., JARBOUI O., “Some biological parameters of the red mullet, Mullus barbatus L., 1758, from the Gulf of Tunis”, Acta Adriatica, 48 (2): 131–144, 2007. DAVIS P.S., EDWARD A.J., “New records of fishes from the northeast coast of England, with notes on the rediscovery of part of the type collection of marine fishes from the Dove Marine Laboratory, Cullercoats”, Transactions of the Natural History Society of Northumbria, 55: 39–46, 1988. DE PIRRO M., MARCHETTI M., CHELAZZI G., “Foraging interactions among three benthic fish in a Posidonia oceanica reef lagoon along the Tyrrhenian Coast”, Journal of Fish Biology, 54: 1300–1309, 1999. DEMESTRE M., SBRANA M., ALVAREZ F., SÁNCHEZ P., “Analysis of the interaction of fishing gear in Mullus barbatus fisheries of the Western Mediterranean”, Journal of Applied Ichthyology, 13: 49–56, 1997. DENIEL C., Biologie et élevage du rouget barbet Mullus surmuletus en Bretagne, Contract ANVAR-UBO A 8911096 E 00, 1991.

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DERBAL F., SLATNI S., KARA M.H., “Variations saisonnières du régime alimentaire du rouget de roche Mullus surmuletus (Mullidae) des côtes de l’Est de l’Algérie”, Cybium, 34 (4): 373–380, 2010. DESBROSSES P., “Contribution à la connaissance de la biologie du rouget-barbet en Atlantique-nord. Mullus barbatus (rond) surmuletus (fage)”, Revue des travaux de l’Institut des pêches maritimes, 8 (4): 351–376, 1935a. DESBROSSES P., “Contribution à la connaissance de la biologie du rouget barbet en Atlantique nord (II)”, Revue des travaux de l’Institut des pêches maritimes, 8: 255–267, 1935b. DESBROSSES P., “Contribution à la connaissance de la biologie du rouget-barbet en atlantique-nord (IV) – Mullus barbatus (rond) surmuletus (fage)”, Revue des travaux de l’Institut des pêches maritimes, 9 (4): 339–399, 1936. DEUDERO S., “Unexpected large numbers of Mullus surmuletus juveniles in open waters of the Mediterranean sampled with light attraction devices”, Journal of Fish Biology, 61: 1639–1642, 2002. DEVAUCHELLE N., Étude expérimentale sur la reproduction, les œufs et les larves de bar (Dicentrarchus labrax), daurade (Sparus aurata), mullet (Liza ramada), rouget (Mullus surmuletus), sole (Solea solea), turbot (Scophthalmus maximus), PhD thesis, University of Western Britanny, 1980. DEVAUCHELLE N., “Reproduction en captivité du rouget (Mullus surmuletus)”, ICES, F/17, Comité Mariculture, 1983. DUNN M.R., The exploitation of selected non-quota species in the English Channel, PhD thesis, University of Portsmouth, Southsea, United Kingdom, 1999. ESPOSITO V., ANDALORO F., BIANCA D., NATALOTTO A., ROMEO T., SCOTTI G., CASTRIOTA L., “Diet and prey selectivity of the red mullet, Mullus barbatus (Pisces: Mullidae), from the southern Tyrrhenian Sea: the role of the surf zone as a feeding ground”, Marine Biology Research, 10 (2): 167–178, 2014. FÉLIX-HACKRADT F.C., HACKRADT C.W., PÉREZ-RUZAFA A., GARCÍA-CHARTON J.A., “Discordant patterns of genetic connectivity between two sympatric species, Mullus barbatus (Linnæus, 1758) and Mullus surmuletus (Linnæus, 1758) in south-western Mediterranean Sea”, Marine Environmental Research, 92: 23–34, 2013. FERRER-MAZA D., MUNÕZ M., LLORET J., FALIEX E., VILA S., SASAL P., Health and reproduction of red mullet, Mullus barbatus, in the western Mediterranean Sea”, Hydrobiology, 753: 189–204, 2015.

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ÜNLÜOGLU A., CIHANGIR B., KAYA M., BENLI H.A., KATAGAN T., “Variations in the feeding intensity and diet composition of red mullet (Mullus barbatus during 24h period in the summertime in Hisarönü Bay”, Journal of the Marine Biological Association of the United Kingdom, 82 (3): 527–528, 2002. VARAGNOLO S., “Calendario di comparse di uova di Teleostei marini nel plancton di Chioggia”, Archivi di Oceanografia e Limnologia, 13 (2): 249–79, 1964. VASSILOPOULOU V., “Biological aspects of red mullet, Mullus barbatus, off the coasts of central Greece”, Bulletin – Marine Biology Research Center Tajura, 9A, 61–81, 1992. VASSILOPOULOU V., PAPACONSTANTINOU C., “Preliminary biological data of the striped mullet (Mullus surmuletus) in the Aegean Sea”, 4th Session of the Technical Consultation on Stock Assessment in the Eastern Mediterranean, Thessaloniki, Greece, 7–10 October 1991, FAO Fisheries and Aquaculture Report, 477: 85–89, 1991. VASSILOPOULOU V., PAPACONSTANTINOU C., Aspects of the Biology and Dynamics of Red Mullet (Mullus barbatus) in the Aegean Sea, National Center for Marine Research, Athens, 1992. VASSILOPOULOU V., PAPACANSTANTINOU C., “Feeding habits of red mullet (Mullus barbatus) in a gulf in western Greece”, Fisheries Research, 16: 69–83, 1993. VASSILOPOULOU V., PAPACONSTANTINOU C., CHRISTIDES G., “Food segregation of sympatric Mullus barbatus and Mullus surmuletus in the Aegean Sea”, Israel Journal of Zoology, 47 (3): 201–211, 2001. VITTURI R., CATALANO E., BARBIERI R., “Karyological and molecular characterization of Mullus surmuletus and Mullus barbatus (Pisces, Mullidae)”, Cytology, 57: 65–74, 1992. VOLIANI A., ABELLA A., AUTERI R., “Length based methods for determination of growth parameters separately by sex in Mullus barbatus”, Cahiers Options Méditerranéennes, 10: 69–70, 1995. VOLIANI A., ABELLA A., AUTERI R., “Some considerations on the growth performance of Mullus barbatus”, Cahiers Options Méditerranéennes, 35: 98– 106, 1998. VRANTZAS N., KALAGIA M., KARIOU C., “Age, growth and state of stock of red mullet (Mullus barbatus L., 1758) in the Saronikos gulf of Greece”, 4th Session of the Technical Consultation on Stock Assessment in the Eastern Mediterranean – Annex 4, 7–10 October 1991, Thessaloniki, Greece, FAO Fisheries and Aquaculture Report, 477: 51–67, 1992.

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WALTER H., AVENAS P., La fabuleuse histoire du nom des poissons, Robert Laffont, Paris, 2011. WIRSZUBSKI A., “On the biology and biotope of the red mullet M. barbatus L.”, Bulletin Sea Fisheries Research Station, 1–XXXII, 1–20, 1953. ZOUBI A., Biologie, indices d’abondance et distributions de taille des principales ressources démersales en Méditerranée, Rapport de la 7ème consultation technique sur l’évaluation des stocks dans les divisions statistiques Baléares et Golfe du Lion, Commission internationale pour l’exploration scientifique de la mer Méditerranée (CIESM), FAO Fisheries and Aquaculture Report, 537: 121–154, 1994. ZUPANOVIC S., Contribution à la connaissance de la biologie du Mullus baratus (L.) dans l’Adriatique moyen, Report, Commission internationale pour l’exploration scientifique de la mer Méditerranée (CIESM), 17 (2): 346–362, 1963.

2 Pleuronectidae Norman, 1934

Vernacular names: Poissons plats (FR), right-eyed flounders (GB). Etymology: Pleuronectidae, from the Greek pleuro (on the side) and nect (who swims). Brief description: An asymmetrical flatfish with eyes on the right side (rarely on the left side). It has relatively “pointed” snout and single dorsal fin, beginning above or in front of the eyes. Caudal fin is well separated from the dorsal and anal fins. Biogeography: Atlantic Ocean (including Arctic regions), Indian Ocean, Pacific Ocean. Habitat and bioecology: Marine waters, sometimes brackish and rarely freshwater, cold to tropical. Benthic, on soft substrates, up to a depth of 2,000 m. Biodiversity: It includes 40 genera and about 100 species (four subfamilies). Pleuronectinae subfamily with 23 genera and about 60 species according to Nelson (2006). Originality: As with all asymmetrical flatfish, the eggs are pelagic and the planktonic larvae are symmetrical. At a certain stage of development, in Pleuronectidae (with few exceptions), the left eye migrates and joins the one on the right. Other anatomo-morphological changes occur (metamorphosis) and the fish becomes benthic; the blind side then rests on the bottom. The largest flatfish belongs to this family: Hippoglossus hippoglossus, 2.50 m TL, 316 kg, female over 35 years old.

2.1. Platichthys Girard, 1854–1855 [1856] Type: Platichthys rugosus Girard, 1854–1855 [1856] in Proc. Acad. Nat. Sci. Philad., 7: 139. Synonym: Flesus Moreau, 1881, Hist. Nat. Poissons, France, t. 3: 298.

Fishes in Lagoons and Estuaries in the Mediterranean 3B: Migratory Fish, First Edition. Mohamed Hichem Kara and Jean-Pierre Quignard. © ISTE Ltd 2019. Published by ISTE Ltd and John Wiley & Sons, Inc.

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

Etymology: Platichthys, from the Greek platis (flat), ichthys (fish), flesus, perhaps from flounder flet derived from Dutch vlelet (ray and by extension flatfish). Brief description: It has flat, oblong and tall body (maximum height about double the SL). Its scales are small, cycloidal, sometimes modified (tubercles). Eyes are on the right side (dextral), but sometimes on the left side (sinistral). Maximum TL= 91 cm. Biogeography: Atlantic, from the White Sea to Gibraltar. North-western and northeastern coasts of the Mediterranean and Black Sea (one species). North Pacific (one species). Habitat and bio-ecology: Benthic, shallow marine beds (–300 to –400 m maximum) in lagoons, lakes and rivers. Biodiversity: Two species, Platichthys stellatus and Platichthys flesus. 2.1.1. Platichthys flesus (Linnæus, 1758)

2.1.1.1. Nomenclature and systematics Type: Pleuronectes flesus Linnæus, 1758, Syst. Nat., Ed. X: 271 (Habitat in M. Europaeo). Synonyms: Pleuronectes passer Linnæus, 1758, Syst. Nat., Ed. X: 271 (Habitat in Oceano Europaeo); Flesus vulgaris Moreau, 1881, Hist. Nat. Poissons, France, t. 3: 298–299 (Chanel); Pleuronectes italicus Günther, 1862, Cat. Fish Brit. Mus., 4: 452 (Mediterranean); Pleuronectes luscus Pallas, 1811, Zoogr. Rosso-asiatica, 3: 427. Vernacular names: Platija (ES), flet, lou passar, passer (FR), flounder (GB), passara nera (IT).

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Etymology: Flesus, perhaps flounder, derived from the Dutch vlelet (ray and by extension flatfish); from the Latin luscus (one-eyed, because left-hand side is devoid of an eye), italicus (from Italy), passer (sparrow). Systematics problems: According to Norman (1934), the species P. flesus must be divided into three geographical subspecies: P. flesus luscus (Atlantic, north-western Mediterranean), P. flesus italicus (Adriatic) and P. luscus luscus (Black Sea and Sea of Azov). Some authors (Totonese, 1971; Fischer et al., 1987; Nielsen, 1979, 1986) suggest only two subspecies, P. flesus flesus (north European Atlantic, north-west Mediterranean) and P. flesus luscus (North Adriatic and Ionian Sea, Aegean Sea, Black Sea and Sea of Azov), but the majority of the systematicians accept, on morphological and genetic bases, the three “Normanic” subspecies. Borsa et al. (1997) conclude, from a study on enzymatic polymorphism, that “the species P. flesus appears to be paraphyletic and the genetic differentiation between the western Mediterranean and the Atantic P. flesus luscus populations seems to be large enough to recognize them as separate subspecies”. 2.1.1.2. Description Morpho-anatomy: It has oval body. Its maximum height is just over two times its standard length. Its eyes are on the right side of the body, but occasionally on the left. There is presence of a rough postocular crest, ending above the operculum. No thorny fin rays. Pectoral and pelvic fins are present, both well developed on both sides; length of the pectoral fin on the eyed side measuring 1.5 times the length of the head. Height of the caudal peduncle is equal to or less than the distance between the base of the dorsal fin and the beginning of the caudal fin. There is a row with small tubercles at the base of the dorsal and anal fins and some small tubercles at the beginning of the lateral line. There is also an arched lateral line above the chest. A supra-temporal branch is present on the neck. Meristics: D. 52–67 radii, A. 36–46 radii, lateral line: 80 scales, gillrakers (7) 9–13 on the lower branch of the first branchial arch (the subspecies P. luscus luscus has only 7 or 8). Coloring: Brownish and sometimes grayish with some mottling and darker macules. Prominent red-orange spots are present at the time of reproduction. Variations: See systematics problems, subspecies. Sexual dimorphism: No major sexual dimorphism, except during the reproductive period when females have a more prominent abdomen than males. Osteology, otoliths, scales: Sanz Echeverria (1926), Norman (1934), Chaine (1936), Bauzà-Rullàn (1959), Schmidt (1968) and Tuset et al. (2008) give

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

descriptions (drawings, photographs) of sagittal otoliths. According to Tuset et al. (2008), it is oval to oblong, with crenate edges in young individuals (Figure 2.1).

Figure 2.1. Sagittal otolith of an individual (34.6 cm TL) of P. flesus from the north-east Atlantic, scale 1 mm (Tuset et al., 2008)

The otolith length/total length of the fish = 1.9–2.3; the otolith width/otolith length = 50.6–62.5; circularity = 14.5–16.7; rectangularity = 0.2–0.3. Remarkably, according to Vianet et al. (1989), in the flounder of the northern coast of the western Mediterranean, a hyaline ring forms annually in sagittae in summer and an opaque ring in winter. These recruitment seasons are the opposite to what is described in the North Atlantic (Figures 2.2(a) and (b)).

Figure 2.2. Sagittal otolith of Platichthys flesus: (a) in the Atlantic, Bay of Douarnenez (C. Deniel); (b) in the Mediterranean, Thau lagoon (J.P. Quignard)

Karyology: Klinkhardt (1993). Protein specificity and genetic diversity: Galleguillos and Ward (1982), by electrophoresis of enzymes, highlight diagnostic loci to differentiate P. flesus flesus

Pleuronecctidae Norman, 1934

63

(Atlanticc, North Sea), P. P flesus italicuus (Adriatic) and a P. flesus luuscus (Black S Sea). They estimate that the diverrgence occurrred 2 million years y ago. Usiing the same ttechnique for 21 loci, Berrebi et al. (1983, 1985) studieed three Medditerranean poopulations (Mauguiio lagoon, Rhôône river, Poiinte de l’Espig guette in the Gulf G of Lion) and three Atlantic populations (Garonne, ( Arccachon, Loire)) and compareed their resultss to those of Gallegguillos and Ward W (1982). Borsa B et al. (1 1986–1987) taake the same approach and present an enzyymatic analysis of Meditterranean sam mples (Gulf of Lion, G of Therm maikos, Aegeean Sea) and Atlantic (Porttugal). In north-weest Adriatic, Gulf both stuudies, three Mediterraneaan subspeciess (populationns) were saiid to be “perfectlly genetically differentiatedd” (Figure 2.3)).

F Figure 2.3. De endrogram sho owing the thre ee Mediterrane ean subspecie es of floun nder. LON: Lo ondon, PLY: Plymouth-UK, P SWA: S Swanse ea-UK, ADR: A Adriatic, CON: Constantta-Romania-Black Sea, IST T: Istanbul (Berrrebi et al.,198 85)

The phylogenetic p relationships esstablished high hlight two grouups; one madee up of the populatioons from Porttugal, the Arccachon basin, the Garonne, the Loire, the English coasts annd the Gulf of Lion, and the other populatiion from the Adriatic A and thhe Aegean Sea. Theese authors relaate this spatiall structuration to the currentss and the clim matological history (P Pleistocene gllaciation) of thhe Mediterraneean. Borsa et al. (1997) confirm, by enzymatiic electrophoresis, the preesence of thrree subspeciees and show that the divergennce between P. flesus flesus and P. stellatu us is more reccent (2.2 ± 0.5 Ma) than the eventt inducing the isolation of P. P f. italicus/P. f. luscus, 3.5 ± 0.6 million yyears old. Moreoveer, these authorrs indicate thatt Gibraltar is a geographical barrier that haas induced significannt genetic diffferentiation beetween the Atlantic A populaations and thoose of the

64

Fish hes in Lagoons and Estuaries in n the Mediterran nean 3B

western Mediterranean M n, to the extentt that we can distinguish d twoo subspecies. T Tinti et al. (1999) make m a compparative analyssis of the miitochondrial DNA D of threee Adriatic pleuronectiformes. Forr flounder, theey provide in nformation on the phylogennetic links between P. flesus italiicus and P. fleesus flesus an nd confirm thee results obtaiined from previous morphologicaal and molecuular studies. More M locally, Berrebi (19992), using enzymatiic markers, revvealed a certaiin heterogeneitty between laggoons (Ingril, M MauguioOr, Petit Rhône, Francee) and intralagooon interbatch hes, as well as an a intralagunall temporal l inducee a selection pressure p on thee flounder, evolutionn. This author suggests that lagoons a fish thaat does not exhhibit homing behavior b or app pear to have clearly distinct spawning grounds, causing genettic diversificatiion of the popu ulation. More generally, g Vernneau et al. p a conssensual phyloggenetic tree off the pleuronecctiformes, bassed on the (1994) propose electrophhoresis of enzzymes, in which P. flesus from the Meediterranean iss used to representt Pleuronectidaae. 2.1.1.3. Distribution Atlanntic, White Sea S to Gibraaltar, north-weest Mediterraanean, north and east Adriatic,, Ionian Sea, Aegean A Sea, Black B Sea (weest and north--west coasts inn relation to centraal European rivvers) and Sea of Azov (Figure 2.4).

Figure 2.4. 2 Geograph hic distribution of P. flesus (tthe question mark m indicatess the area w where its prese ence has not been b confirme ed)

Pleuronectidae Norman, 1934

65

The area of distribution is almost continuous in the Atlantic, but fragmented in the Mediterranean where it is mainly present in the coolest and least salty zones (influence of the rivers Ebro, Rhône, Po, Neretva, Axios, etc.), which makes flounder look like a glacial relict. Note that P. flesus was accidentally introduced (ballast water) on the coasts of Canada and the United States. 2.1.1.4. Ecology Habitat: Demersal species, living on sandy-muddy to muddy bottoms (sea, estuaries, lagoons and sometimes in freshwater), up to 60 m deep. Platichthys flesus can swim up river, such as the Pô, over a long distance (Alessio and Gandolfi, 1983). In the Venetian lagoon, the 0+ juveniles frequent herbaria and bare muddy surfaces, with the former much more densely populated than the latter (2.6 specimens per purse seine in the herbana compared to 0.15–0.20 in bare muddy surfaces). Sandy bottoms are moderately occupied: 0.30 individuals per purse seine (Franco et al., 2006). Carl et al. (2008) experimentally show that small flounder (24–99 mm TL) prefer bare sandy bottoms occupied by the filamentous algae Enteromorpha sp. They tend to invade sandy and sandy-muddy shallow zones (pollution), usually favorable to the recruitment of these juveniles; this can have negative consequences on the local maintenance of certain populations. Migrations and movements: The flounder is a thalassolagoon, catadromous, lagunotrophic migrant in the juvenile and adult stages, but part of the population do not carry out this migratory cycle. They remain in lagoons or estuaries from a few weeks to a few months. The distances traveled in rivers are greater in the Atlantic than in the Mediterranean, one exception being the Po. In the Gulf of Lion, adults and juveniles migrate from thermally and reproductively from lagoons toward the sea in late fall to early winter (Borsa et al., 1986–1987; Vianet et al., 1989). According to Vianet et al. (1989), after spawning at sea (January–March), metamorphosed juveniles aged about 2 months (about 10 mm TL), 1+ juveniles and adults enter the Mauguio lagoon in April–May and stay there until the end of fall. The 0+ juveniles are then 11–15 cm TL. The proportion of individuals that stay in the lagoons compared to those that remain at sea is unknown. This migratory behavior is found in the Adriatic, in the Po Delta (Gandolfi and Giannini, 1977; Gandolfi et al., 1991; Porcelloti, 2005). Ecological valence: Platichthys flesus is considered to be euryvalent. Gutt (1985) experimentally showed that the growth of 4.2–5.3 mm TL juveniles is optimal for salinities between 5 and 15‰ (18–20°C). The relatively low growth rate at zero salinity could be due to low food intake, and the growth rate recorded at salinities of about 35‰ could be due to poor “conversion” of food consisting of tubifex and mold. However, O’Neill et al. (2011) experimentally showed that (for individuals from the Oranmore

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

River estuary, Ireland) the salinity (0, 10, 20 and 30‰) at a temperature of 11°C has no influence on the condition and growth of postlarvae. The RNA/DNA ratio, which reflects the significance of the physiological “demand” for living in a given environment, has no correlation with the condition, but is significantly higher for a salinity of 30‰ than for 0‰. Size, lifespan and growth: In the Mauguio lagoon and close to the sea (Vianet et al., 1989), the maximum total length is 43 cm TL (a 50 cm specimen) in females and the maximum mass in males is 1,040 g TW (TL max = 35 cm). The maximum age determined by otolithometry (the winter rings coincide with the spawning periods) is 7 years for females and 5 years for males (Table 2.1). TL = L∞ [1 – e-k(t-t0)]

W = aLb

TW = W∞ [1 – e-k(t-t0)]b Validity

n

a

B

R

n

L∞

W∞

L in mm

k

t0

Validity in months

M

897

6.45 × 10–6 3.10

0.99

50–350

345

304.52

315.6

0.99 –0.037

3–60

F

705

4.36 × 10–6 3.19

0.99

50–430

270

386.85

764.5

0.70 –0.015

3–84

JM

535

7.60 × 10–6 3.06

0.97

50–150

684

169.79

50.6

0.18

+1.07

3–12

JF

589

9.37 × 10–6 3.02

0.95

50–150

680

156.67

40.6

0.25

+1.45

3–12

1584 6.32 × 10–6 3.10

0.98

50–430

615

380.76

632.0

0.44

–0.64

3–84

JMF

Table 2.1. Parameters of the von Bertalanffy equations and the mass–length relationship of P. flesus in the Mauguio lagoon and near the sea. F: female, J: individuals less than 1-year old, L: length in mm, n: number, r: correlation coefficient (Vianet et al., 1989)

The linear growth and weight increase in females is greater than that in males; females are significantly larger and heavier than males aged 20–24 months. In the Gulf of Trieste, the maximum age is 5 years (5+), the length is 40 cm TL and the mass TW = 500 g (Gandolfi and Giannini, 1977; Vanzo et al., 1998; Porcelloti, 2005). In la Sacca del Canarin (Po Delta, Italy), 0+ individuals that entered the lagoon in April measured 15–25 mm TL, in June 85 mm TL and in September

Pleuronectidae Norman, 1934

67

100–150 mm TL (approximately 7–8 months) (Gandolfi and Giannini, 1977). In the Gulf of Trieste, growth ceases in December–January. According to Dulčić and Glamuzina (2006), the parameters of the mass (TW g)/size (TL cm) relationship in the Mirna estuary (Croatia) are: a = 0.0070, b = 3.110 (r2 = 0.980, TL = 11.0–43.0 cm, n = 42). In the Homa lagoon in Turkey, a = 0.0070, b = 3.080 (r2 = 0.998, TL = 10.3–15.4, n = 77) (Acarli et al., 2014). Gutt (1985) and O’Neill et al. (2011) give information on growth in relation to salinity and temperature factors (see section 2.1.1.4, “Ecological valence”). Population structure and dynamics: Malavasi et al. (2004) and Franco et al. (2006) indicate the abundance of flounder in the Venetian lagoon according to the seasons and the type of bottom (see habitat). 2.1.1.5. Food and feeding behavior Diet: In the Mauguio Lagoon (France), the diet is mainly based on stray polychaete annelids and small amphipod crustaceans. In winter, mollusks were found in very small quantities (secondary prey) in the stomach contents (Vianet, 1985). In the Gulf of Lion, from December to March, the diet is composed, as in lagoons, of stray polychaete annelids and to lesser extent amphipod crustaceans (Bekhti et al., 1985). In the Gulf of Trieste, crustaceans (amphipods, decapods) account for 70% of ingested food, mollusks 12%, annelids 7%, fish eggs 6%, urochordates 3% and small fish 2% (Gandolfi and Giannini, 1977; Vanzo et al., 1998; Porcelloti, 2005). Variations in diet: In the Po Delta (Italy), young 0+ recruits of about 15–25 mm TL feed on Diptera larvae and then on Polychaete annelids (Nereis sp.). In the fall, larger individuals (100–150 mm TL) consume mainly isopods and amphipods. In the spring, large specimens (1+, 2+, etc.) mainly eat amphipods (Gammarus sp.) and in the fall Crangon crangon shrimp (Gandolfi and Giannini, 1977). 2.1.1.6. Reproduction and reproductive behavior Sexuality: Gonochoric species, iteroparous. The GSI of the females (calculated according to the gross mass pGSI or the eviscerated mass eGSI) is very high (pGSI max. = 41%, eGSI max. ≥ 60%) compared to that of males (Figure 2.5). At the time of spawning, the ovaries are very homogeneous (oocytes all at the same stage of maturity), which would indicate that females release all oocytes within a short period of time.

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

a)

b) Figure 2.5. Monthly variations of RGSe (eviscerated animal weight) between February 1980 and April 1982 in female (a) and male (b) P. flesus in the Gulf of Lion (Vianet, 1985)

Pleuronectidae Norman, 1934

69

First sexual maturity: In the Gulf of Lion, the first sexual maturity, according to the GSI and the macroscopic observation of the gonads, is reached in males at the age of 1 year (1+) and at a size of 160–200 mm TL; females are mature at 2 years (2+) and have a size equal to or greater than 250 mm TL (Vianet, 1985). In the Po Delta (Adriatic), sexual maturity is reached at 2–3 years of age (Gandolfi et al., 1991). Spawning site and period: Spawning occurs at sea, in open water, in coastal sites, under the influence of rivers. It extends from mid-January to early April in the Gulf of Lion and from December to February in the Upper Adriatic. Fecundity: In the Gulf of Lion, the annual absolute fecundity is 100,000 to 2,100,000 oocytes in females of 230–435 TL mm, aged 2–6 years (Vianet, 1985). The relationships between fecundity (F) and size (TL mm) are: F = 7,327.08 TL – 1.65 × 10–6 (r = 0.769) or F = 7.11 × 10–5 TL3.95 (r = 0.814); those between fecundity and gross mass TW (g) are: F = 1,650.84 TW – 135,961 (r = 0.86) or F = 156.43 TW1.34 (r = 0.89). Relationships between absolute age (age-in-years) and fecundity are: F = 68,747. Ag1.726 (r = 0.78) or F = 290,978. Ag – 325,128 (r = 0.76). From these data, it can be estimated that a 6-year-old female can lay about 4,000,000 oocytes during her sexual life (5 years). Relative fecundity (Fr = F/TW = 1,500 ± 440 oocytes, nb = 67) in the Gulf of Lion is not significantly correlated with body mass (Vianet, R.)1. Moreover, there is no difference in fecundity when compared with unit of mass of the left and right ovaries (Vianet, R.)2. In the Adriatic, in the Gulf of Trieste, annual individual fecundity is estimated at between 400,000–2,000,000 oocytes depending on the size of the female (Porcelloti, 2005). Spawning behavior: In the Gulf of Lion, mature flounder gather near the mouth of rivers (the Rhône mainly) where they are caught with trawl nets and gillnets, between the end of December and the end of March–beginning of April, depending on the year (specimens at the prelaying and postlaying stages). In addition, some females present hydrated oocytes at the time of exiting the lagoons, which suggests that egg laying takes place in an area close by. In some areas, including the Baltic, hybrids P. flesus × Pleuronectes platessa were found (Nielsen, 1986). This situation is certainly impossible in the Mediterranean; the presence of P. platessa in this area is questionable (Lleonart and Farrugio, 2012). Egg, larvae and ontogenesis: Ehrenbaum (1905: 161–165), Padoa (1956: 834–838), Varagnolo (1964: 267, pl. VI), Bini (1968, 8: 58), Carausu (1952: 603). In the Gulf of Trieste, pelagic eggs, with no oil globule, measure about 1 mm (Varagnolo, 1964) and incubate for 5–7 days. The hatching larvae are pelagic and 1 Personal communication. 2 Personal communication.

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

measure 2.5–2.6 mm TL. They become benthic after the loss of bilateral symmetry at 2 months of age and at a size of about 10 mm TL (Gandlofi et al., 1991), 12–13 mm TL according to Porcelloti (2005). 2.1.1.7. Pollution Vigano et al. (2001) highlight the sensitivity of P. flesus to the industrial pollutants contained in the sediments of the port of Venice. This sensitivity is expressed by changes in the enzymatic activity of several bioindicators in the liver of these fish (EROD, UDPGT, GST, GR, GPx). The development of Enteromorpha sp. filamentous algae, linked to organic pollution, can have negative consequences on the recruitment of juveniles (Carl et al., 2008) and on the growth of 0+ (Gronkjaer et al., 2007). 2.1.1.8. Economic importance Although fishing at sea, as in lagoons, has been significant over the last century (Specchi et al., 1980), it is now less frequent. 2.1.1.9. Protection status, conservation – Global UICN Red List: LC. – Mediterranean UICN Red List: NT. 2.2. Bibliography ACARLI D., KARA A., BAYHAN B., “Length-weight relation for 29 fish species from Homa lagoon, Aegean Sea, Turkey”, Acta Ichthyologica et Piscatoria, 44 (3): 249–257, 2014. ALESSIO G., GANDOLFI G., “Censimento e distribuzione attuale delle specie ittiche nel bacino del fiume PO”, Quaderni dell’Istituto di Ricerca sulle Acque, 67: VII, 1983. BAUZA RULLAN J., Contribucion al conocimiento de otolitos de peces. Boln. R. Soc. Esp. Hist. Nat. (Biol.), 57: 89–118, 1959. BEKHTI M., VIANET R., BOUIX G., “Glugea stephani (Hagenmüller, 1899) Microsporidie parasite du Flet Platichthys flesus (Linné, 1758) du littoral languedocien. Importance du régime alimentaire de l’hôte dans le cycle du parasite”, Vie Milieu, 35 (2): 107–114, 1985. BERG L.S., “Révision des formes de Pleuronectes flesus”, Notas y resúmenes – Instituto Español de Oceanografía, 58: 1–7, 1932.

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BERREBI P., “Hétérogénité génétique et évolution saisonnière du flet (Platichthys flesus, Osteichtyes, Pleuronectidae) lors de sa phase lagunaire”, Vie et Milieu, 42: 147–156, 1992. BERREBI P., AGNESE J.F., VIANET R., “Structure génétique des Flets (Platichthys flesus, Téléostéens, Pleuronectidae)”, Colloque Bases biologiques de l’aquaculture, (1): 363–372, Ifremer, Montpellier, France, 1983. BERREBI P., LANDAUD P., BORSA P., RENNO J.F., “Esterases of the flounder (Platichthys flesus, Pleuronectidae, Teleostei): development of an identification protocol using starch gel electrophoresis and characterization of loci”, Cellular and Molecular Life Sciences, 46 (8): 863–867, 1990. BERREBI P., VIANET R., AGNESE J.F., QUIGNARD J.P., PASTEUR N., “Variabilité génétique et morphologique de quelques populations de flet Platichys flesus flesus des côtes méditerranéennes et atlantiques françaises”, Biochemical Systematics and Ecology, 13 (1): 55–61, 1985. BERTOLINI F., D’ANCONA U., PADOA MONTALENTI E., RANZI S., SANZO L., SPARTA A., TORTONESE E., VIALLI M., “Uova, larve e stadi giovanili di Teleostei”, Fauna e Flora del Golfo di Napoli, 38: 1–1064, 1956. BORSA P., BERREBI P., BLANQUER A., “Mécanismes de la formation en Méditerranée des sous-espèces du flet Platichthys flesus L. (poisson plat)”, CNRS National, Actes du Collaque, Biologie des populations, Symposium, p. 472–481, Lyon, 4–6 September 1986, 1987. BORSA P., PLANQUER A., BERREBI P., “Genetic structure of the flounders Platichthys flesus and P. stellatus at different geographic scales”, Marine Biology, 129: 233– 246, 1997. CARAUSU S.I., Tratat de Ichtiologie, Editura Academiei Republicii Populare Române, Bucharest, 1952. CARL J.D., SPARREVOHN C.R., NICOLAJSEN H., STØTTRUP J.G., “Substratum selection by juvenile flounder Platichthys flesus (L.): effect of ephemeral filamentous macroalgae”, Journal of Fish Biology, 72: 2570–2578, 2008. CHAINE J., “Recherches sur les otolithes des poissons”, Actes de la Société linnéenne de Bordeaux, 88: 160–214, 1936. COOPER J.A., CHAPLEAU F., “Monophyly and intrarelationships of the family Pleuronectidae (Pleuronectiforms), with a revised classification”, Fishery Bulletin. United States Fish and Wildlife Service, 96 (4): 686–726, 1998. COTTIGLIA M., Pesci lagunari. Guide per il riconoscimento delle specie animali delle acqua lagunari e costiere italiane, C. Sacchi Editore, CNR, Genoa, 1980.

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DARNAUDE A., HARMELIN-VIVIEN M.L., SALEN-PICARD C., “Food partitioning among flatfish (Pisces, Pleuronectiforms) juveniles in a Mediterranean coastal shallow sandy area”, Journal of the Marine Biological Association of the United Kingdom, 81: 119–127, 2001. DULČIĆ J., GLAMUZINA B., “Length–weight relationships for selected fish species from three eartern Adriatic estuarine systems (Croatia)”, Journal of Applied Ichthyology, 22: 254–256, 2006. FISCHER W., SCHNEIDER M., BAUCHOT M.L., Fiches FAO d’identification des espèces pour les besoins de la pêche. Méditerranée et mer noire – Zone de pêche 37, vol. 2. Vertébrés, FAO-CEE, Rome, 1987. FRANCO A., ELLIOTT M., FRANZOI P., TORRICELLI P., “Life strategies of fishes in European estuaries: the functional guild approach”, Marine Ecology Progress Series, 354: 219–228, 2008a. FRANCO A., RICCATO F., MALAVASI S., FRANZOI P., TORRICELLI P., “Food resource utilization by gobies (Pisces, Teleostei) in the shallows of the Venice lagoon”, Biologia Marina Mediterranea, 13 (1): 866–868, 2006. GALLEGUILLOS R.A., WARD R.D., “Genetic and morphological divergence between populations of the flatfish Platichthys flesus (L.) (Pleuronectidae)”, Biological Journal of the Linnean Society, London, 17: 395–408, 1982. GANDOLFI G., GIANNINI M., “L’alimentazione della passera, Platichthys flesus luscus (Pallas), e di altra specie ittiche bentofaghe in un ambiente salmastro del delta del fium Po. Ateneo parmense”, Acta Naturalia, 13: 327–334, 1977. GANDOLFI G., ZERUNIAN S., TORRICELLI P., MARCONATO A., “Plathichthys flesus”, I Pesci delle acqua interne italiane, Istituto Poligrafico e Zecca dello Stato. Libreria dello Stato, Unione Zoologica Italiana, p. 557–561, 1991. GRONKJAER P., CARL J.D., RASMUSSEN T.H. , HANSEN K.W., “Effect of habitat shifts on feeding behavior and growth of 0 year group flounder Platichthys flesus (L.) transferred between macroalgae and bare sand habitats”, Journal of Fish Biology, 70: 1587–1605, 2007. GUTT J., “The growth of juvenile flounders (Plathisthys flesus L.) at salinity of 0, 5, 15 and 35 ‰”, Journal of Applied Ichthyology, 1 (1): 17–26, 1985. KLINKHARDT M., “Zur Zytogenetik von Platichthys flesus und Limanda limanda (Pleuronectidae, Teleostei) und karyoevolution der Pleuronectiformes”, Zeitschrift für Fischkunde, 2: 65–75, 1993. LLEONART J., FARRUGIO H., “Pleuronectes platessa, a ghost fish in the Mediterranean Sea?”, Scientia Marina, 76 (1): 141–147, 2012.

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MALAVASI S., FIORIN R., FRANCO A., FRANZOI P., GRANZOTTO A., RICCATO F., MAINARDI D., “Fish assemblages of Venice lagoon shallow waters: an analysis based on species, families and functional guilds”, Journal of Marine Systems, 51: 19–31, 2004. NELSON J.S., Fishes of the World, John Wiley & Sons, New York, 2006. NIELSEN J.G., “Pleuronectidae” in HUREAU J.C., MONOD T. (eds) Clofnam I. Catalogue des Poissons de l’Atlantique du Nord-Est et de la Méditerranée, Unesco, Paris, p. 623–627, 1973. NIELSEN J.G., “Pleuronectidae” in WHITEHEAD P.J.P., BAUCHOT M.-L., HUREAU J.-C., NIELSEN J., TORTONESE E. (eds), Poissons de l’Atlantique du Nord-Est et de la Méditerranée, Unesco, Paris, 3: 1299–1307, 1986. Norman J.R., “A systematic monograph of the Flatfishes (Heterosomata)”. vol.1, British Museum, London, 459 p, 1934. O’NEILL B., DE RAEDERMAECKER F., MCGRATH D., BROPHY D., “An experimental investigation of salinity effect on growth, development and condition in European flounder (Platichthys flesus L.)”, Journal of Experimental Marine Biology and Ecology, 410: 39–44, 2011. PADOA E., “Heterosomata in Uova, larve e stadi giovanili di Teleostei”, Fauna e Flora del Golfo di Napoli, 38: 834–837, 1956. PORCELLOTTI S., Pesci d’Italia, ittiofauna delle acque dolci, Casa Editrice Plan, Florence, 2005. ROCHARD E., “Le flet, Platichthys flesus (Linné, 1758)”, Les poissons d’eau douce de France, Biotope, Mèze and MNHN, Paris, pp. 508–509, 2001. SANZ ECHEVERRIA J., “Datos sobre elotolito sagitta de los peces de Espana”, Boletín de la Real Sociedad Española de Historia Natural, 26 (1): 145–160, 1926. SCHMIDT W., Vergleichend morphologische studie über die otolithen mariner knochenfischen. Arch. Fish. Wiss., 19(1): 1–96, 1968. SPECCHI M., SCATTARO-MICCOLI G.S., “Osservazioni sulla pesca della passera Platichthys flesus italicus (Günther) (Osteichthyes, Pleuronectiformes) nel Golfo di Trieste”, Quaderni del Laboratorio di Tecnologia della Pesca, 2 (5): 271–284, 1980. SPECCHI M., VALLI G., ZEJN D., “Osservazioni in natura e in laboratorio sulle uova di Platichthys flesus italicus (passera) del Golfo di Trieste”, Quaderni del Laboratorio di Tecnologia della Pesca, 2: 197–205, 1979.

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TINTI F., COLOMBARI A., VALLISNERI M., PICINETTI C., STAGNI A.M., “Comparative analysis of a mitochondrial DNA control region fragment amplified from three Adriatic flatfish species and molecular phylogenesis of Pleuronectiformes”, Marine Biotechnology, 1 (1): 20–24, 1999. TORTONESE E., “I pesci pleuronettiformi delle coste romene del Mar Nero in relazione dalle forme affini viventi nel Mediterraneo”, Annali del Museo civico di storia naturale Giacomo Doria, 7: 322–352, 1971. TUSET V.M., LOMBARTE A., ASSIS C.A., “Otolith Atlas for the Western Mediterranean, north and central eastern Atlantic”, Scientia Marina, 72, S1 (1): 203, 2008. VANZO et al., “Pleuronectids Adriatic flounder Platichthys flesus”, in PORCELLOTI S. (ed.), Pesci d’Italia ittiofauna delle acque dolci, Casa Editrice Plan, Florence, 2005. VARAGNOLO S., “Calendario di comparse di uova pelagiche di Teleostei marini nel plancton di Chioggia”, Archivi di Oceanografia e Limnologia, 13 (2): 249–279, 1964. VEER VAN DER H.W., ZIJLSTRA J.J., “Predation of flatfish larvae by Pleurobrachia pileus in coastal waters”, ICES CM 1982/G: 16, 1982. VERNEAU O., MOREAU C., CATZEFLIS F.M., RENAUD F., “Phylogeny of flatfishes (Pleuronectiformes): comparisons and contradictions of molecular and morphoanatomical data”, Journal of Fish Biology, 45: 685–696, 1994. VIANET R., Le flet du Golfe du Lion, Platichthys flesus Linné 1758. Systématique, écobiologie, pêche, Thesis, Montpellier 2 University (USTL), 1985. VIANET R., QUIGNARD J.P., TOMASINI J.A., “Âge et croissance de quatre poissons Pleuronectiformes (flet, turbot, barbue, sole) du Golfe du Lion”, Cybium, 13 (3): 247–258, 1989. VIGANO L., ARILLO A., FALUGI C., MELODIA F., POLESELLO S., “Biomarkers of exposure and effect in flounder (Platichthys flesus) exposed to sediments of the Adriatic Sea”, Marine Pollution Bulletin, 42 (10): 887–894, 2001.

3 Soleidae Norman, 1934

Vernacular name: Sole. Etymology: Soleidae, from the Latin solea (sandal), in reference to its oval shape and its thin body comparable to the sole of a sandal. Brief description: The body is oval, elongated, very strongly compressed and asymmetric. Both eyes are located on the right side, known as the ocular side, except in a few rare reversed individuals. The upper eye is more advanced than the lower; the snout is rounded into a fleshy lobe; the mouth is small and arched; the teeth are small, velvety, difficult to see, sometimes absent. The preopercule is covered by skin and the entire opercule is covered by scales. The dorsal and anal fins lack spiny rays. The margin front begins at or in front of the anterior edge of the dorsal eye. The caudal fin is either completely separate from the dorsal and anal fins, or joined to them by a thin membrane, or fully fused. The pelvic fins are separated from the anal fin. The lateral line is rectilinear on the middle part of each side; on the head, it manifests as an arcuate line to form the supratemporal line. The body is covered by rough ctenoid scales. The eyed side is brown to dark gray with various patterns: spots, ocelli, dots, bands, mottling; whitish blind side. Biogeography: Often found in tropical and temperate seas, this family is absent from the western Atlantic. In the eastern Atlantic, it is found in southern Iceland (Buglossidium luteum) and in European and African waters from southern Norway to South Africa (Munroe, 2005a). It is found in the Mediterranean and Black Sea (Munroe, 2005a). The species are present in the Indo-Pacific, with maximum diversity in the Indo-Malay Archipelago, north of Australia and in the central Pacific to Hawaii, Easter Island and the Galapagos Archipelago (Munroe, 2005a), where this family is represented only by Herre sole, Aseraggodes herrei (Grove and Lavenberg, 1997). Habitat and bioecology: It is a benthic fish, living in various marine habitats, mainly shallow lagoons and estuaries, on soft bottoms, especially muddy, but rarely rocky. Some species such as Bathysolea profundicola live at depths up to 1,300 m (Quéro et al., 1986). Chapleau and Desoutter (1996) note that Dagetichthys lakdoensis, a freshwater species from Cameroon, can be found up to 1,300 km inland. Other species are found in freshwater in southeastern Asia,

Fishes in Lagoons and Estuaries in the Mediterranean 3B: Migratory Fish, First Edition. Mohamed Hichem Kara and Jean-Pierre Quignard. © ISTE Ltd 2019. Published by ISTE Ltd and John Wiley & Sons, Inc.

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New Guinea, Borneo and northern Australia (for example Brachirus, Achiroides) (Munroe, 2005a). Systematics and phylogeny: Munroe (2005b) summarized the results of morphological studies presenting recently published hypotheses on the interrelationships of flatfish (Figure 3.1). The monophyly and position of certain subgroups within the family Soleidae were established (Desoutter, 1994; Chapleau and Desoutter, 1996; Desoutter-Meninger, 1997) and progress has been made regarding the systematics of these fish (Desoutter, 1987, 1994; Desoutter and Chapleau, 1997). Biodiversity: The family Soleidae includes two subfamilies, the Soleinae and Synapturinae (Chabanaud, 1939). The current classification of the Soleinae subfamily at the genus level is based on morphological characteristics and needs to be revised, since a biochemical genetics study has shown that there are just as many differences between species of the same genus as between species belonging to different genera (Goucha et al., 1987). There are around 22–29 genera and about 89 species of soleids that are currently recognized, accounting for 19.4% of the species diversity of pleuronectiforms (Munroe, 2005b). The evolution curve of the number of valid species as a function of time (Figure 3.2) shows that work must still be done before the number of species in this family can be reliably estimated. Indeed, the status of several genera (such as the genus Pegusa) and species (such as Solea [Pegusa] lascaris, nasuta, impar) and their interrelationships are still poorly understood. In the Mediterranean and the Black Sea, there are 15 or 16 species of Soleidae belonging to seven or nine genera. Among them, there are three Atlantic immigrants: Microchirus hexophthalmus, Solea senegalensis, Synaptura lusitanica (Golani et al., 2002). Originality: As with all asymmetric flatfish, the eggs are pelagic and the planktonic larvae are symmetrical. At a certain stage of development, one of the eyes, the left in the Soleidae (with some exceptions), migrates and joins the eye on the right side. After the acquisition of asymmetry, the fish adopts a benthic life, with the blind side resting on the bottom. The sole Pardachirus marmoratus (Indian Ocean) has, in addition to camouflage, a chemical antipredation system.

Figure 3.1. Diagram interpreting the hypothetical relationships of pleuronectiformes based on recently published morphological data and phylogenetic analyses (Munroe, 2005b)

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Figure 3.2. Cumulative curve of valid Soleidae species described between 1758 and 2000 and recently (2001+) recognized species (Munroe, 2005b)

3.1. Solea Quensel, 1806 Type: Solea vulgaris Quensel, 1806; K. Svensk. Vet. Akad., Nya Handlung, Stockholm, XXVII: 53. Synonyms: Synapturichthys Chabanaud, 1927; Pegusa Günther, 1862 (synonym not always accepted, Vachon et al., 2008). Desoutter-Meniger (1987) considers that both genera are valid. Etymology: Solea, from the Latin solea (sandal), in reference to its oval shape and its thin body, features found on the sole of a sandal. This term is also related to solum (soil). Pegusa is the species name given by Yarrell (1829, Zool. J., vol. IV: 467, pl. 16) to the lemon sole (or the French sole) Solea pegusa. Pegusa comes from “pegouse, pégueux”, an Occitan word meaning sticky. Synapturichthys, from the Greek sùn (with), pteros (wing, fin), ictis (fish), in reference to the dorsal and anal fins of the spotted sole (Klein’s sole), which are joined to the caudal fin by a highly developed membrane. Brief description: Oval body and supratemporal branch of the gently curved lateral line. The dorsal fin starts in front of the eyes. Pectoral fins (with at least 7 rays) are present on both sides. The posterior edge of the pectoral fin (on the occulated side) is rounded. The nostril on the blind side is normal (group Solea) or rosette-shaped and wide (group Pegusa). Biogeography: Species of the genus are found in northern Europe and Iceland, along the eastern Atlantic and in the Indian Ocean to the west-central Pacific.

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Habiitat and bioeccology: Coastaal seabeds (–2 200 m environn), sometimess between rocks. Soome species enter e brackish and even fresshwater lagoonns and estuaries. Biodiiversity: Ninetty-seven speccies have been n described under u this gennus name accordingg to Vachon ett al. (2008), 799 according to Eschmeyer (11998, 2005), buut only 15 if the vaalidity of the genera Soleaa, Pegusa and d Synnapturichhthys is acceppted, nine accordingg to Froese and a Pauly (2015) and eightt according to Vachon et aal. (2008). Accordinng to Vachon et e al. (2008), the t genus Soleea is representeed in the Mediterranean by only three t species: S. S aegyptiaca, S. S senegalensiss and S. solea.

Figure 3.3. Phylogen netic trees of Solea, S Pegusa a and Synaptu urichthys speccies (the wo genera are e not recognizzed by Tinti and Picinetti) ba ased on the co ombined latter tw sequencces of two mito ochondrial DN NA genes). (a)) Maximum pro obability; (b) M Maximum parsimony (Tinti and Picinetti, 2000)

Systeematics and phhylogeny: Soleaa solea (synon nym S. vulgariis) is geneticallly distinct from S. senegalensis s annd S. aegyptiacca (She et al., 1987). Solea aegyptiaca a is ggenetically

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closer to S. senegalensis than S. solea, although morphologically it is very close to being considered a subspecies of the latter (S. vulgaris = S. aegyptiaca) (Chabanaud, 1927). In a study on isozymes (Est-2A and Est-3A), Abd-El-Gawad et al. (1997) discovered a genetic divergence between S. solea and S. aegyptiaca. Cabral et al. (2003) owed the existence of a strong genetic divergence between S. solea and S. senegalensis (work on nine isozyme loci, mean Nei distance = 0.93). Tinti and Picinetti (2000) studied the molecular genetics of the Atlantic-Mediterranean species of the genus Solea by analyzing the sequences of two mitochondrial DNA genes (Figure 3.3). Seven taxa were sampled in the Adriatic, in the gulfs of Taranto and Cadiz. In the genus Solea, four lines have evolved and currently correspond to the species S. solea, S. senegalensis, S. kleini and S. lascaris. The existence of S. aegyptiaca and S. impar is not confirmed by this study and these two species are synonymous with S. solea and S. lascaris, respectively. This taxonomy is consistent with that proposed by BenTuvia (1990) based on the morphology of these species. In addition, the mitochondrial data contradict the relationship recognized between S. kleini and S. lascaris. Tinti and Picinetti (2000) as well as Ben-Tuvia (1990) believe that there is a strong relationship between S. solea and S. senegalensis. Simultaneously, both approaches (molecular and morphological) result in their separation. Borsa and Quignard (2001) show that, both morphologically and genetically, the species S. aegyptiaca and S. solea, as well as the species Solea (Pegusa) impar and S. (Pegusa) lascaris are distinct but related. Originality: See box at the beginning of the chapter, section “Biodiversity”. 3.1.1. Solea aegyptiaca Chabanaud, 1927

3.1.1.1. Nomenclature and systematics Type: Solea vulgaris aegyptiaca Chabanaud, 1927, Bull. Inst. Océanogr. Monaco, 488: 35 (origin not mentioned). Synonym: Solea vulgaris aegyptiaca Chabanaud, 1927.

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Vernacular names: Samak moussa (EG), sole égyptienne (FR), Egyptian sole (GB), mdass, mdès, ndè (TN). Etymology: From the Latin solea (sandal), aegyptiaca (from Egypt). Systematics issues: The status of S. aegyptiaca, Chabanaud, 1927, seems wellestablished at the species level, as well on the basis of morphoanatomical and molecular studies (Quignard et al., 1984, 1986; Goucha et al., 1987; Borsa and Quignard, 2001). Chabanaud considered it to be a subspecies of S. vulgaris = S. solea. However, BenTuvia (1990) and Tinti and Piccinetti (2000), respectively, on morphological and molecular bases believe that the species (subspecies) of Chabanaud should be synonymous to S. solea (Linnæus, 1758). 3.1.1.2. Description Morphoanatomy: It has an oval body. Nostril of the eyed side, bent backwards and does not reach the lower eye. Last ray of the dorsal and anal fins is connected to the caudal fin by a poorly developed membrane. Meristics: D 62-87, A 51-72, P 7-9, Ll 106-150 scales, Vt 39-44. Coloring: It has a brown upper surface with diffuse dark spots. Brown pectoral fin with a large black spot that does not extend to the end of the fin. Variations: There is some geographical heterogeneity with regard to meristic characteristics. Gulf of Lion (Palavasian lagoons): D 70-82, A 56-66, Vt 41-44 (Quignard et al., 1982/1984), North Adriatic (Italy): D 62-73, A 51-59, Vt 39-42 (Pagotto, 1971), Southern Adriatic (Albania): D 76, A 64-65 (Tortonèse, 1946), Egypt: D 69-87, A 53-72, Vt 41-43 (Chabanaud, 1927), Gulf of Gabes: D 6577, A 55-64 (Aldebert and Pichot, 1970); D 68-79, A 53-65, Vt 41-43 (Quignard et al., 1982/1984). Karyology: The chromosomal number is 2n = 42 chromosomes: 8 metacentric, 4 submetacentric and 30 acrocentric (NF = 52). The same organization is found in S. solea and S. senegalensis (Baker 1972; Goucha, 1982). Protein specificity and genetic diversity: Following a genetic (enzymatic systems) and morphometric study, dealing with marine samples (Gulf of Gabes, Tunisia) and lagoon areas (Mauguio, France), Quignard et al. (1982–1984) found that the subspecies S. vulgaris (= solea) aegyptiaca Chabanaud, 1927 and S. vulgaris typica should be considered as separate species: Solea vulgaris Quensel, 1808 = S. solea (Linnæus, 1758) and S. aegyptiaca Chabanaud, 1927. Although sympatric in the Gulf of Lion, these species do not hybridize in this area (Quignard et al., 1982–1984).

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Goucha et al. (1987), based on an electrophoretic study of isoenzymes (24–30 loci) in seven populations of S. senegalensis and S. aegyptiaca, highlight strong polymorphism and great genetic similarity between these two “species”, which are clearly distinguished from six other species of Soleidae including S. vulgaris (= S. solea). These authors suggest that these two soles have a common ancestor and that there is still gene flow between them. Kotulas et al. (1988) confirm the genetic isolation of S. solea and S. aegyptiaca and indicate the presence of S. aegyptiaca × S. senegalensis hybrids in areas where they live in sympatry (introgression). Tinti and Piccinetti (2000), according to a molecular study (16S rDNA and cytochrome b), believe that S. aegyptiaca is not genetically different from S. vulgaris (= S. solea). On the other hand, Borsa and Quignard (2001) confirm, by analyzing nucleotide sequences at the cytochrome b locus, the results obtained by Goucha et al. (1987), without considering genetic exchanges between these two soles (see box at the beginning of the chapter, section “Systematics and phylogeny”). Ouanes et al. (2004) analyzed the genetic structure of Egyptian soles occupying the Bizerte (northern Tunisia) and El Bibane (southern Tunisia) lagoons using isozyme markers. Despite the geographical remoteness of these lagoons, these authors note equivalent intralagunal variability, and a certain heterogeneity between these populations. According to these authors, the genetic structure of samples from the Gulf of Tunis and El Bibane lagoon are similar, but that of individuals from the Bizerte lagoon is clearly distinct. This divergence is related to the genetic exchanges (hybridization) between S. senegalensis and S. aegyptiaca (She et al., 1987). Ouanes et al. (2009 and 2011) have shown that hybridization is common in the Bizerte lagoon where the level of introgression reaches 34.2–36.4% and the hybrids could be fertile (Ouanes et al., 2014). Note that hybridization is, in many cases, considered to be a stimulating factor for “invasive abilities” (Ayres et al., 2009). 3.1.1.3. Distribution An endemic species of the Mediterranean, it is present in the Gulf of Lion (Quignard et al., 1982–1984), the Albanian South Adriatic (Tortonese, 1946) and North Adriatic (Pagotto, 1971), throughout the southeast Mediterranean and Asia Minor (Figure 3.4). It was identified for the first time in Turkey (Levantine Sea) by Bilecenoǧlu et al. (2014). Solea aegyptiaca was one of the few Mediterranean species found in the Suez Canal. It has been reported under the name S. lascaris by Tillier (1902); it is referred to as S. solea by Nordman (1927) and S. solea aegyptiaca by Botros (1971). According to Chabanaud (1930), it crossed the Suez Canal in 1869. It was found, more recently, by She et al. (1987b) alongside S. solea in the Suez Canal, in the Quarun lagoon (salinity = 24–27 g/L) by Ali et al. (2008) and in the Red Sea by Chanet et al. (2012).

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Figure 3.4. Geographical distribution of Solea aegyptiaca

3.1.1.4. Ecology Habitat: Benthic, coastal and lagoon marine environments. This fish lives on sandy-soft to sandy-muddy bottoms (–50 m). Migration and movements: Marine species (spawning at sea) that migrate to lagoons. Ecological valence: Euryhaline species, which, according to its geographical distribution, withstands salinities between 20 and 39‰. Size, lifespan and growth: According to a scalimetric study (Goucha, 1982), S. aegyptiaca from the north coast of Tunisia have a lifespan of about 84–96 months (seven age groups) and a maximum size of 28 cm SL. The parameters of the von Bertalanffy equation are: SL∞ = 30.65 (cm), k = –0.047, t0 = –0.175. For individuals from the same sector, by otolithometry, Chebil-Ajabi and El Abed (2000) give the following values for the von Bertalanffy equation: TL∞ = 43.5 cm, K = 0.072, t0 = –3.81 in males; TL∞ = 47.2 cm, K = 0.076, t0 = –3.56 in females. According to these authors, females grow a little faster than males from the age of 3 years and reach a greater length than that of males by about 1.5 cm (neither ages nor maximum sizes are given). The size–mass relationships for these individuals are: TW = 0.0137 TL2.996 in females, TW = 0.0150 TL2.942 in males (Chebil-Ajabi and El Abed, 2000). In the Nile Delta area (Port Said), the maximum size is 30.8 cm TL (female) (Ahmed et al., 2010). For the same area, the size is 28.9 cm TL (250 g TW) for a maximum age (otolithometry) of 4 years according to

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Mehanna (2007), 3 years according to Ali (1995) (Mehanna, 2007). The size/mass ratio is TW = 0.0086.TL3.0054 (r2 = 0.99; n = 640; 9.5 ≤ TL ≤ 28.9 cm; 8.5 ≤ TW ≤ 250 g). The von Bertalanffy equations are: TL = 30.9 [1 – e–0.53 (t + 0.33)] and TW= 258.48 [1 – e–0.53 (t + 0.33) 3.0054 ] (Mehanna, 2007). In the Egyptian Bardawil lagoon, the oldest individuals are 3 years old and up to 31 cm TL. The von Bertalanffy growth model, determined by the back-calculation of individual age using otolithometry, is written as: TL = 37.52 [1 − e−0.42 (t + 0.4)]. The back-calculated age/length data are: 1 year old, 17.1 cm (43.4 g); 2 years old, 24.1 cm (128.2 g); 3 years old, 28.7 cm (225.3 g). The length–weight relationship is: W = 0.0052.TL3.179 (Gabr, 2015). Population structure and dynamics: Based on sampling in the Port Said (Egypt) region, the M/F sex ratio of the population is balanced (1:1.15). However, females dominate in large size classes and in December (58%) and January (86%), they show a period of high reproductive activity (Ahmed et al., 2010). 3.1.1.5. Food and feeding behavior Cnidarians are preferred prey (frequency: 73%); polychaetes (35%) and mollusks (15%) are secondary prey, while crustaceans are unintentional (Goucha, 1982). 3.1.1.6. Reproduction and reproductive behavior Sexuality: Gonochoric species. The GSI of females (north of Tunisia) peaks in November (Wgonades/EW. 100 = 3.18) and is less than 1 from January to April (Goucha, 1982). According to Chebil-Ajjabi (1998), in the Gulf of Gabes, the maximum GSI is approximately 4.5% for females (November) and about 0.10% for males (October). In the region of Port Said (Egypt), the GSI of females reaches its maximum in January (8.00) and minimum in June (0.64); in males, it is at its maximum in January (0.129) and minimum in August (0.0037) (Ahmed et al., 2010). First sexual maturity: In the Bizerte lagoon (northern Tunisia), the first sexual maturity in females is reached for a few individuals at a length of 19 cm SL, SL50 = 21–23 cm and SL100 = 25 cm (Goucha, 1982). In the region of Port Said (Egypt), the first mature females measure 13.50 cm TL, TL50 = 15 cm and TL100 = 19 cm (Ahmed et al., 2010). Spawning site and period: Spawning at sea, but due to the high percentage of introgression (34.2–36.4%) between S. senegalensis and S. aegyptiaca in the Bizerte lagoon compared to in the sea (Ouanes et al., 2009 and 2011), we can assume that these two soles spawn in this lagoon. The GSI values suggest that, on the northern coast of Tunisia, spawning occurs from October to November, and possibly from September to mid-December (Figure 3.5) (Goucha, 1982); individuals (28 and 12%) were found with “mature” ovaries. In the Gulf of Gabes, the spawning season

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Fish hes in Lagoons and Estuaries in n the Mediterran nean 3B

extends from f Novembber to May (Chhebil-Ajjabi, 1998) and in Port-Saïd P (Egyypt) from (Novembber) Decembeer to March (M May) (Ahmed et al., 2010).

Figure 3.5 5. Monthly varriations in the gonadosomattic index of S aegyptiaca females S. f on the e northern coa ast of Tunisia (Goucha, 198 82)

Fecuundity: In the region of Port-Saïd, th he ovarian fecundity f off females measurinng 13.8–30.5 cm is 9.8998–38.505 maature oocytess (F = 16.911.TL2.265). Relative fecundity is between b 627 and a 1262 oocy ytes/cm TL (A Ahmed et al., 2010). Reprroductive behavior: Solea aegyptiaca and a S. senegaalensis may hybridize (She et al., a 1987; Ouaanes et al., 20009, 2011) and hybrids mayy be fertile (O Ouanes et al., 20144). Egg, larvae and ontogeny: Matuure, hydrated oocytes meassure approxim mately 1.0 mm (Ahmed et al., 20010). mportance 3.1.1.7. Economic im This species is of secondary s ecoonomic interesst, given the loow quantities sampled. Nevertheeless, it couldd potentially be overexploited in the Bardawil lagooon (Gabr, 2015). 3.1.1.8. Protection and a conserva ation status – Gloobal IUCN Reed List: LC. – Meediterranean IU UCN Red Lisst: LC.

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3.1.2. Solea senegalensis Kaup, 1858

3.1.2.1. Nomenclature and systematics Type: Solea senegalensis Kaup, 1858, Arch. Natura., 24 (1): 94 (Senegal). Type MNHN, Paris. Synonym: Solea melanochira Moreau, 1874, Rev. Mag. Zool., (3)2: 115, pl. 15 (Arcachon, France). Type MNHN, Paris. Vernacular names: Sole sénégalaise (DZ), lenguado senegales (ES), sole sénégalaise (FR), Senegal sole (GB), sole sénégalaise, ndès (TN). Etymology: Senegalensis (from Senegal, country of origin of specimen studied by Kaup); melanochira, from the Greek melanos (black) and keir (hand), black hand, referring to its black pectoral fin. 3.1.2.2. Description Morpho-anatomy: Oval body, eyes on the right side, rounded snout, slightly arched mouth, anterior nostril of the eyed surface does not reach the anterior edge of the lower eye. The dorsal fin starts in front of the upper eye. The base of the last ray of the dorsal and anal fins is separated from the start of the caudal fin and is joined to the upper and lower profile of the caudal peduncle by a poorly developed membrane. The scales are ctenoid. Meristics: D: 72–75, A: 61–75, P. dextral: 8–12, P. sinistral: 8–10, Ll.: 120–138 scales, vertebra: 43–46. Coloring: Brownish mottled eyed side; many small blue spots on living individuals. Right pectoral fin with yellowish, grayish, whitish rays connected by a blackish membrane. Caudal fin is a uniform brownish gray. White blind side (left). Osteology, otoliths, scales: Otoliths of S. senegalensis were described by Chaine (1936) and Bauza-Rullàn (1956). Tuset et al. (2008) provide data on otoliths from Mediterranean and Northeast Atlantic specimens, measuring 16.2, 26 and 32.7 cm

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

TL (Figure 3.6). Being round, their contours are sinuous and are characterized by the following ratios: otolith length/total fish length = 1.4–1.6; otolith width/otolith length = 75.6–78.7; circularity = 13.3–14.6; rectangularity = 0.1.

Figure 3.6. Sagittal otolith of an individual (26.0 cm TL) S. senegalensis from the western Mediterranean, scale 1 mm (Tuset et al., 2008)

Karyology: The chromosomal number is 2n = 42 chromosomes: eight metacentric, four submetacentric and 30 acrocentric (NF = 52). The same pattern is found in S. solea and S. aegyptiaca (Baker, 1972; Goucha, 1982). Protein specificity and genetic diversity: Based on an electrophoretic study of isoenzymes (24–30 loci) of seven populations of S. senegalensis and S. aegyptiaca, Goucha et al. (1987) show strong genetic polymorphism and similarity between these two “species” that are significantly different from six other Soleidae species including S. vulgaris (= S. solea). These authors suggest that S. senegalensis and S. aegyptiaca have a common ancestor and that there is still gene flow between them. Ouanes et al. (2004) analyzed the genetic structure of Egyptian sole (S. aegyptiaca) occupying the Bizerte (northern Tunisia) and El Bibane (southern Tunisia) lagoons and the Gulf of Tunis using isoenzymatic markers. According to these authors, the Bizerte sample is distinctly different from the other two. This divergence results from genetic exchanges (hybridization) between S. senegalensis and S. aegyptiaca within this lagoon, which is not the case in the Gulf of Tunis or in El Bibane lagoon. Using enzyme electrophoresis techniques, Kottelat et al. (1988) found that S. solea (S. vulgaris) and S. senegalensis have very clear genetic autonomy in areas where they live in sympatry. On the other hand, in the areas where S. senegalensis and S. aegyptiaca live sympatrically (Gulf of Lion, Gulf of Tunis), they describe a “recent or even current” introgression. Borsa and Quignard (2001) confirmed these results by analyzing nucleotide sequences at the cytochrome b locus, without considering genetic exchanges between these two soles.

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Cabral et al. (2003) confirm that there is a strong divergence between S. senegalensis and S. solea (enzymatic polymorphism, Nei distance = 0.93). The population genetics of this species is summarized by Cerdà et al. (2008). In areas where S. senegalensis and S. aegyptiaca coexist, they can hybridize (She et al. 1987); cases of hybridization are particularly numerous in the Bizerte lagoon where the level of introgression reaches 36.4% (Ouanes et al. 2011). In addition, Ouanes et al. (2014) consider hybrids to be fertile, according to a gonad histological study. Note that hybridization is, in many cases, considered a stimulating factor for “invasive capabilities” (Ayres et al., 2009). 3.1.2.3. Distribution Atlantic: From Senegal to the north of the island of Oléron and on the coasts of Charente-Maritime (France) (Chabanaud, 1927; Lagardère et al., 1979). North and South coasts of the western basin of the Mediterranean: Spain (Borja, 1920), Malaga Spain (Rodriguez and Rodriguez, 1980), Castellon, Spain (Ramos, 1982), Catalonia (Recasens et al., 2001), Gulf of Lion (Quignard et al., 1984), Mauguio lagoon (Quignard and Raibaut, 1993), Bizerte and Ichkeul lagoons, northern Tunisia (Goucha and Ktari, 1981), Algiers (Alili and Marinaro, 1986), Mellah lagoon, Algeria (Chaoui and Kara, 2004) (Figure 3.7).

Figure 3.7. Geographical distribution of S. senegalensis

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

According to a molecular study (Tinti and Piccinetti, 2000), this species is present in the eastern basin of the Mediterranean (Ionian Sea, Gulf of Taranto). 3.1.2.4. Ecology Habitat: Sandy seabeds and lagoons, mostly on sandy-muddy seabeds up to 80 m (100 m) deep. Migration and movements: Marine species, making incursions in the brackish lagoons. Ecological valence: Larvae, after metamorphosis, acclimatize well to very low salinity water (1‰) (Bedoui, 1995). Size, lifespan and growth: In the Ebro Estuary, Garcia-Franquesa et al. (1996) estimate, by otolithometry, the maximum age to be 6 years. According to a scalimetric study, S. senegalensis from the northern coast of Tunisia (Bizerte lagoon) has a lifespan of about 96–108 months (eight age groups) and a maximum size of 33 cm SL (Goucha, 1982). The parameters of the von Bertalanffy equation are: SL∞ = 42.26 (cm), K = 0.053, t0 = – 0.279. In the same area, Chebil-Ajabi and El Abed (2000) obtained the following values for the von Bertalanffy equation using otolithometry: L∞ = 44.1, K = 0.118, t0 = –2.36 in females and L∞ = 42.7, K = 0.108, t0 = –1.94 in males (the valid ages and lengths are not shown). The size–mass relationships are TW = 0.0065.TL3.304, EW = 0.0064.TL3.288 for females and TW = 0.0371.TL2.712, EW = 0.0316 TL2.752 for males. In Algeria, in the Mellah lagoon, the maximum size is TL = 44.6 cm and the mass TW = 438 g (Chaoui and Kara, 2004). 3.1.2.5. Food and feeding habits Diet: Garcia-Franquesa et al. (1996) studied the stomach contents of 376 individuals over four seasons (225 with identifiable content) from the Ebro Estuary (Spain), aged 2–6 years. Crustaceans numerically dominate the food bolus (58.32%), followed by polychaete annelids (35.40%) and mollusks (5.75%). Crustaceans are essentially Tanaidacea, amphipods and decapods (Table 3.1).

Soleidae Norman, 1934

Items Mollusks Philinidae Thyasiridae Mactridae Solenidae Tellinidae Scrobicularidae Donacidae Veneridae Dentaliidae Polychaetes Glyceridae Nereidae Nephtydidae Onuphidae Eunicidae Lumbrineridae Orbinidae Ampharetidae Crustaceans Isopoda Anthuridae Cymothoidae Tanaidacea Apseudidae Amphipoda Leucothoidae Ampeliscidae Decapoda Penseidae Processidae Upogebiidae Paguridae Goneplacidae Other prey Anguillidae Total Mollusks Total Polychaetes Total non-Decapoda Total Decapoda Total other prey Total

N

89

Total number (n = 225) %N %F λ'’

7 1 32 3 2 13 3 2 3

0.61 0.09 2.79 0.26 0.17 1.13 0.26 0.17 0.26

2.67 0.44 4.89 0.89 0.89 3.11 1.33 0.89 1.33

0.21 0.01 1.53 0.17 0.02 0.38 0.18 0.02 1.29

36 1 301 45 7 5 10 1

3.14 0.09 26.24 3.92 0.61 0.44 0.87 0.09

12.00 0.44 53.33 10.22 2.22 1.33 4.00 0.44

4.36 0.02 29.03 2.97 0.19 0.68 1.02 0.02

3 2

0.26 0.17

0.44 0.89

0.23 0.03

174

15.17

38.22

17.10

9 143

0.78 12.47

3.11 20.44

0.21 9.10

2 23 310 2 1

0.17 2.01 27.03 0.17 0.09

0.89 6.67 34.22 0.89 0.44

0.03 1.50 29.42 0.14 0.04

6 66 406 331 338 6 1,147

0.52 5.75 35.40 28.85 29.47 0.52 –

2.67 14.22 64.44 47.56 40.44 2.67 –

0.09 – – – – – –

Table 3.1. Qualitative and quantitative composition of the diet of S. senegalensis in the Ebro estuary (Garcia-Franquesa et al., 1996). N: total number of prey, % N: numerical abundance, % F: frequency of occurrence, λ'’: Simpson’s index

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

In the Bizerte lagoon (north coast of Tunisia), polychaete annelids are the preferred prey of S. senagalensis; fish (gobies) are secondary prey along with crustaceans (crabs, gammaria) and mollusks (Tapes, Pecten, etc.) (Goucha, 1982; Chebil Ajabi and El Abed, 2000). Feeding variations and rhythms: In the Ebro estuary (Spain), Garcia-Franquesa et al. (1996) found differences in diet with sex, age and season, especially in crustaceans. 3.1.2.6. Reproduction and reproductive behavior Sexuality: Gonochoric species. The maximum GSI of females, recorded on the Tunisian coasts, is Wg/EW × 100 = 3.5 (April) (Goucha, 1982). First sexual maturity: In the Bizerte lagoon (north coast of Tunisia), the first sexual maturity is reached by some females at a length of 17 cm SL, 50% at 21–23 cm SL and 100% of individuals for sizes equal to or greater than 23 cm SL (Goucha, 1982). From the 397 individuals collected in the Bizerte region (Bizerte lagoon, oued Tinja), Chebil-Ajabi and El Abed (2000) estimate that the first females to reach first sexual maturity is at 17 cm TL, 50% at 21–23 cm TL and 100% at 23 cm TL. Spawning site and period: Spawning at sea, but due to the high percentage of introgression observed (34.2–36.4%) among S. senegalensis and S. aegyptiaca in the Bizerte lagoon, compared with to that outside of it (Ouanes et al., 2009, 2011), we can assume that they are spawning in this lagoon. On the northern Tunisian coast, Goucha (1982) estimates that S. senegalensis can spawn from April to September (November); the GSI peaks twice, once in April (4.5%) and again in September (2.5%) and presents a very low minimum value in August (0.5%). Nevertheless, during this month, the author found some mature females. These results were confirmed by Chebil-Ajabi and El Abed (2000 for the same region) and, experimentally, by Anguis and Canavata (2004). In fact, specimens living in tanks directly supplied with water from Rio San Pedro (Bay of Cádiz) naturally spawned at temperatures between 13 and 23°C, with maximum emission between 15 and 21°C (Anguis and Canavate, 2004). Under these conditions, spawning was significant between February and May (94.6% of oocytes released), with a secondary release in fall (5.4% of oocytes released). This long spawning period is also confirmed by the presence, over a long period of time, of larvae in the plankton (Cabral et al., 2003). Fecundity: In basins whose water had the same characteristics as those of the lagoon (Rio San Pedro, Bay of Cadiz) from which Senegalese soles originated, they had reproduced “naturally” for 2 years. Their annual fecundity has been estimated at

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1.15 × 106–1.65 × 106 oocytes released per year and per kg of body weight (Anguis and Canavata, 2004). Reproductive behavior: In areas where S. senegalensis and S. aegyptiaca cohabit, hybridization can occur (She et al., 1987). Cases of hybridization are particularly numerous in the Bizerte lagoon (Tunisia). The introgression level is around 36.4% and their hybrids are fertile (Ouanes et al., 2011, 2014). Egg, larvae and ontogenesis: Eggs spawned naturally in seawater (S = 36‰) have a diameter of 0.996–1.025 mm. Incubation lasts 42–48 h at 19°C (Bedoui, 1995). Larvae at eclosion measure approximately 2.4 ± 0.1 mm TL and metamorphosis (eye migration) is reached at a size of 7.3 ± 0.8 mm TL. According to Anguis and Canavate (2004), eggs measure 0.970 ± 0.042 mm. 3.1.2.7. Economic importance Solea senegalensis is a species that has been increasingly sampled over the last decade. Moreover, it is a potentially important species in the field of aquaculture (Imslan et al., 2004; Cerdà et al., 2008), due to its zootechnical mastery of all lifecycle stages (Imsland et al., 2003) and its high market price. However, many problems persist and hinder the consolidation of this species on an industrial scale. One of the main problems is the unpredictability of the reproductive capacity of F1 breeders who fail to reproduce normally (Agulleiro et al., 2006; Howell et al., 2009). The reason behind this dysfunction is unknown, although temperature is suspected to influence it (Agulleiro et al., 2006; Garcia-Lopez et al., 2007). Optimization of production was also not possible because of the great variability in growth rates (Dinis et al., 1999). This may be due to the sex ratio variation among the groups and sexual dimorphism of growth in favor of females. 3.1.2.8. Protection status, conservation – Global Red List IUCN: NE. – Mediterranean Red List IUCN: NE. 3.1.3. Solea solea (Linnæus, 1758)

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

3.1.3.1. Nomenclature and systematics Type: Pleuronectes solea Linnæus, 1758, Syst. Nat., Ed X: 270 (Habitat in M. Europaeo). No specimen type. Synonyms: Pleuronectes solea Linnæus, 1758 Solea vulgaris Quensel, 1806; Solea vulgaris typica Chabanaud, 1927. Vernacular names: Sole (DZ), enguado (ES), sole (FR), common sole, dover sole (GB), sogliola (IT), ingwata tar-ring (MT). Etymology: Solea from the Latin sola (sandal, sole). Systematics problems: Jordan and Goss (1888) consider that Solea vulgaris Quensel 1806 was described by Linnæus (1758) as P. solea. They give a new description and call it S. solea (Linnæus, 1758). 3.1.3.2. Description Morpho-anatomy: The body is oval, elongated, gradually narrowing toward the back. The two eyes are located on the right side, the upper one being separated from the dorsal profile by a length less than its own diameter. The anterior tubular nostril of the ocular side does not exceed the anterior edge of the lower eye. The anterior nostril of the blind side is circled by a small protrusion; the distance separating it from the dorsal profile is between 1.5 and 1.9 times that separating it from the oral commissure. The blind side of the head has many small villi. The snout is rounded. The mouth is small, arched and not terminal. The edge of the preopercule is hidden under the skin. The caudal fin has a rounded edge and is attached to the last ray of the anal and dorsal fins by a well-developed membrane. A summary of studies enabled Shehata (1984) to propose the following meristic formulae: D = 72–97; A = (51) 53–79 (80); P1 = (5) 6–9 (10); P2 = (3/4) 5–9; V1 = (3) 4–6 (7); V2 = (3) 4–5 (6); vertebrae in the Mediterranean = (45) 46–51 (52); vertebrae in the Atlantic = (41–42) – 49–52; laternal line = 113–156 scales. The maximum size in the Atlantic is 70 cm (3 kg) (Wells, 1958) and 49 cm in the Mediterranean (Sartor et al., 2002). Coloring: The color of the zenithal surface varies according to the nature of the environment; it ranges from a very dark brown or a lighter gray-brown (lagoon sole) to light gray (marine sole). They have irregularly arranged marks. Differences in color between individuals are mainly due to mimicry (Shehata, 1984). The pectoral fin on the ocular side is decorated on its distal upper half with a circular black spot, which appears oblong when the fin is not extended. This spot covers four or five

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upper rays. In very young individuals ( 12 cm) (Mariani, 2006). The latter include individuals that rarely leave the lagoon during the cold season. The same structure is found in the Languedoc lagoons (see growth in Mauguio and Prevost) (Man-Wai, 1985). In the central-eastern Adriatic, 82.1% of individuals belong to the two to six-year age groups, with a dominance of five-year-old individuals ranging in size from 11.3 to 17.8 cm (24.8%) (Figure 4.7, Matić-Skoko et al., 2007).

Sparidae Jordan an nd Evermann, 1898

141

Figure 4.6.. Size frequen ncy of D. annularis in the Itallian lagoons Fogliano and d Caprolace (M Mariani, 2006))

Figure 4.7. Age A frequency of males, fem males and und determined sexx of D. annularis in the centrall-eastern Adria o atic (Matić-Sko oko et al., 200 07)

At seea, in the Gulff of Lion, the overall o sex ratiio (mature inddividuals) is F//M = 1.04 and favoors females in large size claasses (Man-W Wai, 1985), theese being the oonly ones present from f 19 to 200 cm TL (onee exception: on ne male measuuring 25.6 cm m TL was capturedd in Thau in May 1983). In thhe Gulf of Gab bes, the sex raatio is generallyy in favor of femalles (57.35%) and increasess as the size increases, i unttil they becom me almost exclusivee from 17 cm m (a single malle of 18.5 cm TL out of 4551) (Bradai, 20000). The dominannce of femaless (1:1.52) in the t Gulf of Gabes G is also confirmed c by Chaouch et al. (20013). In the cenntral eastern Adriatic, A the seex ratio is balaanced (1:1.05) and there was no difference d bettween the average size of males m (13.2 ± 1.74 cm) andd females (12.8 ± 1.94 1 cm) samppled (Matić-Skkoko et al., 200 07).

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Fisshes in Lagoonss and Estuaries in the Mediterra anean 3B

4.1.1.5. Diet and fee eding behaviior Diet:: Diplodus annnularis is om mnivorous. Beiing opportuniistic, it feeds oon varied prey acccording to thee flora and faauna of its biiotope. In thee Adriatic, it feeds on chlorophhytes, decapod crustaceaans, gastrop pod and bivvalve molluusks and spermaphytes, in decrreasing order of preferencee (Matić-Skokko et al., 20044). In the Gulf of Annaba A (Algeeria), macrophhytes, ascidian ns and crustaceans are its dominant prey (Deerbal et al., 20007). On the other o hand, plaants make up only o a small ppart of the stomach contents in annular a giltheead from thee Gulf of Lionn and the Preevost and Mauguioo lagoons (F France), whiich prefer mollusks, m annnelids and decapods (Rosecchhi, 1987). Moollusks (RII = 37.2%) also dominate d in thhe stomach coontents of the Gulff of Gabes (M Mediterraneann-center), folllowed by teleeosts (RII = 29.77%), plants (R RII = 15.96%)) and crustaceaans (14.47%) (Chaouch et al., a 2014). Feedding behaviorr: Diplodus annularis feed ds both durinng the day ((Bell and Harmelinn-Vivien, 19883) and at nighht (Rodriguez--Ruiz et al., 2002). Dietaary variationns and patterrns: The dieet of D. annularis is suubject to ontogeneetic, seasonal and diurnal variations. v Wh hile adults are zoophagous, juveniles tend to consume c plantts in the Adriaatic (Figure 4..8, Matić-Skokko et al., 20044), and to a lesser extent e in the Gulf G of Annabba (Derbal et al., a 2007).

Figu ure 4.8. Variattions in diet acccording to siz ze of D. annula aris in the Adrriatic. Alg: alg lgae, Mag: Ma agnoliophytes, Ant: Anthozo oa, Gas: Gastrropods, Biv: Biivalves, C Crustacea Cru: ans, Bry: Bryo ozoa, Rem: oth her (Matić-Sko oko et al., 200 04)

On thhe other hand,, in the Gulf of o Lion, fry (7– –25 mm) feedd almost excluusively on larvae (aannelids, chirronomids, cruustaceans) an nd some isoppods. Beyond 50 mm, amphipoods and molluusks are the most preferreed prey. Abovve 100 mm, mollusks

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143

(lamellibbranchs, gasteeropods, cephhalopods), ann nelids and deecapods alonee account for 78–881% of ingeested biomasss, but amphipods are stilll the most dominant (Rosecchhi, 1987, Figuure 4.9). In thhe Gulf of Gaabes, the diett is homogeneeous both between juveniles andd adults and beetween males and females (Chaouch ( et aal., 2014).

Figure e 4.9. Ontogen nic variations in i diet of D. an nnularis in the Gulff of Lion (Rose ecchi, 1985)

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

Matić-Skoko et al. (2004) found no significant seasonal difference in the diet of D. annularis in the Adriatic. This difference is great in the Gulf of Lion, both in terms of number and weight (Rosecchi, 1987). In the Gulf of Annaba, Derbal et al. (2007) show the uniqueness of the fall diet, characterized by a predominance of plants. In Cap Palos (southeastern Spain), Rodríguez-Ruiz et al. (2001) show a seasonal diet, consisting of posidonia and algae in summer, algae and hydrozoa in fall and winter, and harpacticoid copepods and gammarid amphipods in spring. Seasonal variation in diet is also evident in the Gulf of Gabes (Chaouch et al., 2014). Rosecchi (1987) highlights feeding differences in the sea and Prevost and Mauguio lagoons (Table 4.3) and finds that these differences lessen when only small size classes are considered. At sea, D. annularis abandons numerous prey (larvae) or colonies (hydra) that it eats in lagoons, in favor of bigger invertebrates such as decapods, annelids and mollusks. There are differences in diet between lagoons themselves, which is the case for populations in the Italian lagoons Fogliano and Caprolace (Mariani et al., 2002). This divergence may reflect differences in available prey and confirm the diet plasticity of these seabream. Prey Preferred prey ≥50% MFI

Secondary prey

Other prey

Lagoons

Sea

22% larvae

24% decapods

20% cnidarians

19% annelids

18% amphipods

12% lamellibranches

12% fish

11% gastropods

10% annelids

10% cnidarians

Others (plants 3%)

Others (plants 0.6%)

Table 4.3. Diet comparison of marine (Gulf of Lion) and lagoon (Prevost and Mauguio) D. annularis (Rosecchi, 1987)

Rodriguez-Ruiz et al. (2002) showed that the stomach contents of D. annularis vary according to whether samples are taken during the day or at night, the size of the individuals and the state of disturbance in the habitat. In trawl beds, young individuals consume planktonic prey (planktonic doliolids and copepods) during the day, while in non-trawled habitats, benthic copepods are dominant. The number of benthic prey increases with fish size, especially for those feeding at night in unsheltered seagrass beds. In addition, Sánchez-Jerez et al. (2002) have shown that

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the installation of artificial reefs on Posidonia oceanica beds causes a change in the relative abundance of different ingested prey, especially in large fish. According to Fabi et al. (2006), these artificial structures provide this species with their main food resources. 4.1.1.6. Reproduction and reproductive behavior Sexuality: Information about the sexuality of D. annularis is still unclear, although, since Syrski (1876), many authors have been interested in this topic. According to Fisher et al. (1987), the sexes are “normally distinct”, but some cases of protandric hermaphroditism have been reported (Salekhova, 1961). Pajuelo et al. (2001) considers D. annularis of the Canary Islands to be a protandric hermaphrodite. Of the 792 individuals examined, 2.8% are intersex. Matić-Skoko et al. (2007) found a single intermediate individual (TL = 12.2 cm, TW = 34.2 g, two years) out of 1,704 fish examined in the Adriatic. The gonads of this specimen presented male tissues and female tissues when viewed under a microscope with a predominance of the former. Bradai (2000) counts 11.83% undifferentiated hermaphrodites and 88.17% gonochoric (839 females and 451 males) out of the 1,463 examined; the number of females increases with size and the males disappear in sizes greater than 19 cm TL. Saied and Kartas (1988) conclude that the hermaphroditism of D. annularis from Kerkennah (Tunisia) is rudimentary, but they did detect some protandric hermaphrodites no larger than 14 cm TL. In the Gulf of Lion, Man-Wai (1985) admits that this species exhibits rudimentary hermaphroditism, with some cases of protandric hermaphroditism, but at least 95% of an individual’s functional sex is determined from the first year of life. The rudimentary hermaphroditism of D. annularis is confirmed by gonad histology, first performed in this species by Alonso-Fernandez et al. (2011). First sexual maturity: In the Gulf of Lion, the first mature female measured 11 cm TL (2 years), TL50 = 13 cm (2 years) TL100 = 15 cm (3 years); the first mature male measured 9.5 cm TL, TL50 = 10 cm (2 years) and TL100 = 13 cm (2 years) (Man-Wai 1985). First sexual maturity is reached at an average total length of about 10.5 cm (1.62 years) in the Gulf of Gabes (Bradai, 2000; Chaouch et al., 2013) and 12.6 cm TL in the Gulf of Annaba (Nouacer and Kara, 2001). On the coasts of Croatia, 50% of males are mature at 9.0 cm TL and 50% of females are mature at 10.0 cm; beyond 13 cm, all individuals are adults (Matić-Skoko et al., 2007). Spawning site and period: Spawning sites are not documented but they are certainly coastal (Rosecchi, 1985). The spawning season is between spring and summer, with slight differences between sites (Table 4.4).

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Sites and authors

J

F M A M

J

J

A S

O N D

Italy (Bini, 1968) Italy (Tortonese, 1975) Northeast Atlantic and Mediterranean (Bauchot and Hureau, 1986) North Adriatic (Bauchot and Hureau, 1986) North Sea (Bauchot and Hureau, 1986) Adriatic (Jardas, 1996) Gulf of Gabès, Tunisia (Bradai, 2000) Izmir Bay, Turkey (Kinacigil and Akyol, 2001) Gulf of Annaba, Algeria (Nouacer and Kara, 2001) East Adriatic (Matić-Skoko et al., 2007) Balearic Islands, Spain (Alonso-Fernandez et al., 2011) Gulf of Gabès, Tunisia (Chaouch et al., 2014) Table 4.4. Reproduction periods of D. annularis in the Mediterranean

In some areas, such as in the central eastern Adriatic, the spawning period is longer, from the end of April to the end of August, with a peak in early to mid-May, as shown by the monthly variations in the gonadosomatic index (GSI) (Figure 4.10) (Matić-Skoko et al., 2007). According to Ayyildiz et al. (2014), D. annularis hatch in the Dardanelles Strait (Aegean Sea) between March and September with a relatively high hatching frequency in June.

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Figure 4.10. Gonadosomatic index (GS SI ± SD) and percentage p of D annularis spawning stages in (a) males and (b)) females of D. A (Matić ć-Skoko et al., 2007) in the central-east Adriatic

Eggss, larvae andd ontogenesis:: Ranzi (1930, 1933), acccording to Loo Bianco (1909), describes d the 10 stages ranging from thee larvae aged a few days (77 mm TL, resorbedd yolk) to the juvenile j stagee (94 mm TL). Metamorphoosis completess at a size of 14 mm m TL. Gray transverse t bannds appear at 19–21 mm TL T and disapppear when their sizee is beyond 94 9 mm; only the black ban nd on the cauudal peduncle remains. Varagnollo (1963) indiccates that eggss have a diametter of 0.75–0.881 mm (mean 0.77 mm) in Chiogggia (Italy) and describees the develo opment of laarvae aged 1–7 days. Divanachh (1985) inddicates that thhe diameter of o eggs obtaiined from aqquaculture studies is between 0.772 and 0.80 mm m (mean = 0.7 759 mm) and that incubatioon time is between 50 and 65 h for f a temperatture of 15–18°°C.

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4.1.1.7. Economic importance Generally, D. annularis is not a fishing target because it is not of great economic interest. The fishing of this species is semi-industrial (Sicily and Adriatic), but most often artisanal. The gear used is typically bottom trawl and pelagic trawl, beach seines, handlines, gillnets, bottom longlines and traps, mainly in lagoons. On the Turkish coasts of the Aegean Sea, the annular gilthead are caught using gillnets of 52–54 mm, and sometimes with other nets. Fishermen use these nets for a period of five months, from April to August, because of the ban on the use of the trawl and purse seines during this period (Özeknci, 2005). On the coasts of Croatia, MatićSkoko et al. (2007) estimate the total mortality coefficient (Z) of D. annularis to be 0.72 (M = 0.39; F = 0.33), which gives a relatively moderate exploitation rate of 0.46. According to FAO statistics, there are no specific data for D. annularis in the Mediterranean. In the Gulf of Lion, sea captures, which amounted to 47 tons in 1977, only totaled 9.5 tons in 1980 and seems to have remained at this level since. Lagoon fisheries only contribute slightly. 4.1.1.8. Protection status and conservation – IUCN Global Red list: NE. – IUCN Mediterranean Red List: LC. 4.1.2. Diplodus puntazzo (Cetti, 1777)

4.1.2.1. Nomenclature and systematics Type: Sparus puntazzo Cetti, 1777; Anfibi e Pesci di Sardegna: 174–175. Holotype MNHN A-8101. Synonyms: Puntazzo puntazzo (Cetti, 1777), Charax puntazzo (Cetti, 1777), Sparus puntazzo Walbaum, 1792.

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Vernacular names: Morua (DZ), morruda (ES), sar à museau pointu (FR), sharpsnout seabream (GB), puntazo (IS), sarago pizzuto (IT), moghza (MT), tchouya (TN), sivriburun karagoz (TR). Etymology: Puntazzo, from the Italian punta (pointed), in reference to its noticeably pointed snout. 4.1.2.2. General description Morpho-anatomy: The body is oval, raised and compressed laterally. The cheeks are scaly, but the preoperculum is bare. The first gill arch has 7–11 lower and 5–7 upper gill rakers. The dorsal fin has 11 spines (the first spine is short) and 12–15 soft rays. The anal fin has three spines and 11–13 soft rays. There are 53–64 scales along the lateral line (excluding the scales of the base of the caudal fin). The lips are thin on a slightly protruded mouth. On each jaw, there are eight incisors inclined forwards and one with two rows of rudimentary molars, regressing in adults. This dentition gives it its pointed snout. The total common length is 30 cm (Bauchot and Hureau, 1990) and reaches 60 cm (Bauchot, 1987). The maximum weight recorded is 1.680 g (IGFA, 2001). Coloring: The most dominant color is silver-gray. There are at least a dozen dark vertical stripes on its back. In older individuals, stripes may be replaced by spots. A dark ring is often present around the caudal peduncle, and is more prominent in juveniles. A dark spot is also visible at the base of the pectoral fins. The caudal fin is forked with black edges. Variations: Morphological differences exist depending on the geographical origin of the individuals. In fish sampled from the Mediterranean (Spain, Italy, Greece) and the Atlantic (Portugal), Palma and Andrade (2002) found significant differences between these four groups, with a clear geographic gradient between the Mediterranean and the Atlantic. By comparing the change in the morphology of D. puntazzo between the larval and juvenile stages (2.6–33 mm TL) via morphogeometry, Kouttouki et al. (2006) identified two inflection points (at 6.2 and 11.4 mm TL), which define three significantly different phases of morphological development. These ontogenetic events are mainly correlated with the development of the fins, the caudal peduncle and the ventral profile of the abdomen. The extent of these changes in shape decreases with body size. Favaloro and Mazzola (2006) examined variations in meristic traits and the incidence of skeletal abnormalities in a wild population of D. puntazzo in southeastern Sicily. The most common skeletal abnormalities were malformations of the pectoral and anal fins and soft rays on the dorsal fin. However,

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there is no correlation between the frequency of these abnormalities and fish size. On the other hand, by examining 60 juveniles and 60 adults from Mediterranean hatcheries, Favaloro and Mazzola (2000) demonstrated that the number of skeletal abnormalities in D. puntazzo decreased with age. In fact, 28 types of abnormalities were recorded in juveniles and 25 in adults. The most significant with respect to the juveniles were: the neural arch (47%), the hemal arc (11th–21st vertebra) (43%), the fusion of the hypural (67%) and the presence of stones in the terminal channel of the urinary tracts (43%). In adults, neural arc defects (43%) and the fusion of hypurals (90%) and epurals (37%) dominate. While abnormalities of the hemal arch decrease with age, the fusion of the hypural and the epurals increases. Few cases of lordosis and mild kyphosis were found in juveniles but had no influence on growth performance and were not life-threatening. Favaloro and Mazzola (2003) found that the number of vertebrae and the number of pectoral fin rays vary significantly between wild and captive populations of D. puntazzo from Sicilian coasts. In addition, the number of skeletal abnormalities is significantly higher in captivity (28) than in nature (14), with a malformation index of 3.6 and 2.5, respectively. Wild fish mainly exhibit an abnormal thorax (58% vs. 2% in captivity), malformations of the hemal arch and/or spine (46% vs. 13% in captivity) and malformations of the pectoral fin rays (deformed, absent, incomplete, multiple) (92% vs. 4% in captivity). In contrast, malformations of the caudal fin (hypural) affect 59% of captive fish and 32% of wild fish; those of the hemal arch and/or the caudal region of the vertebral column are present in 60% in captivity and 1% in nature, whereas those of the neural arc reach 53% vs. 8% in captivity. Similarly, non-severe cases of lordosis and kyphosis are common at 11.13% and 15%, respectively, in captivity, whereas they are absent in nature. Sfakianakis et al. (2005) found that farmed fish have a wider distribution of dorsal fin rays than wild fish. Kouttouki et al. (2006) differentiate wild and reared populations according to the caudal peduncle and the ventral profile of the abdominal region. In aquaculture, Sarà et al. (1999) have shown the influence of rearing conditions (pond monoculture, cage monoculture, pond polyculture) on the morphology of D. puntazzo. After eight months, cage farming has a significant effect on shape variations compared to the other two breeding methods. Fish reared in pools have 37.5–43.7% of forms known as “goitrous” and “flat back”. On the other hand, “belly” forms are more numerous in cages (66.7%). Sexual dimorphism: There is no sexual dimorphism. Osteology, otoliths and scales: Chaine (1937), Sanz Echeverria (1943), Kinacigil et al. (2000) and Tuset et al. (2008) describe the sagittal otoliths of D. puntazzo. This otolith is irregular and oval. The rostrum is salient, the anti-rostrum is flat. The sulcus is very deep. The ostium is hollow in shape. The crests are well defined and

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the tail is deep. The posterior aspect of the tail is curved. The otolith is very convex laterally in its median and concave portion. The sides are lobed and the postrostrum is slightly longer (Figure 4.11).

Figure 4.11. Sagittal otolith from an individual (10.0 cm TL) of the species D. puntazzo from the western Mediterranean, scale 1 mm (Tuset et al., 2008)

According to Tuset et al. (2008), the following ratios are characteristic of this otolith: otolith length/total length of fish = 2.1–5.4; otolith width/otolith length = 56.0– 64.0; circularity = 15.0–16.7; rectangularity = 0.2–0.3. Karyology: 2n = 24, including four pairs of meta/submetacentric chromosomes (pairs 1, 6, 15, 16) and 20 acrocentric pairs (Vitturi et al., 1996). Protein specificity and genetic diversity: Basaglia et al. (1990) compared the expression profiles of three isozymes (lactate dehydrogenase, malate dehydrogenase and glucosephosphate isomerase) of D. puntazzo with those of Sparus aurata and D. sargus. The three protein systems of the three species were different. By analyzing crystalline and muscle proteins in four species of Diplodus (D. annularis, D. sargus, D. vulgaris, D. puntazzo), Basaglia and Marchetti (1990) showed the early divergence of D. puntazzo from the common ancestral lineage. Using the control region of mitochondrial DNA and allozyme markers, Bargelloni et al. (2005) compared samples of D. puntazzo from the Mediterranean (Spain: Alicante, Italy: Otranto, Greece: Heraklion, Messolonghi lagoon) and the Atlantic (Portugal, Strait of Gibraltar). The mitochondrial marker showed a high level of polymorphism, with 111 different haplotypes and a significant genetic difference between the Mediterranean and Atlantic samples (Fst = 0.08; P < 0.0001). In the Mediterranean, the differentiation is significant only when the two most distant sites are compared (Alicante and the Messolonghi lagoon).

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4.1.2.3. Distribution Diplodus puntazzo is found mainly in the Mediterranean and the eastern Atlantic, from the Bay of Biscay (rare) to Sierra Leone, the Canary Islands and Cape Verde. It is also found in South Africa (Figure 4.12).

Figure 4.12. Geographical distribution of D. puntazzo

4.1.2.4. Ecology Habitat: It belongs to nectobenthic species, and is therefore coastal and gregarious. It frequents rocky bottoms up to 60 m, rarely up to 150 m. Adults are rather solitary or live in the company of other Diplodus species (D. sargus or D. vulgaris). Juveniles are also found in lagoons where they enter at the larval stage. A three-year study (May 1993–June 1996) of the colonization by juveniles of 20 stations in five sites in the north-western Mediterranean (Spain: Girona, France: Banyuls and Marseille, Italy: Portofino and Elbe) was carried out on three species of Diplodus: D. puntazzo, D. sargus, D. vulgaris (Vigliola et al., 1998). By combining the results of all three years, combining all sites, only 4% of the colonizers were D. puntazzo whose arrival was recorded around October–November. The intensity of colonization varies both on a large scale (between sites) and on a small scale (between stations of the same site), but does not show interannual variations. On the other hand, in the Kornati archipelago, Croatia, at a given moment, the first colonizers are found in equal

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proportions at all sites considered (Matić-Skoko et al., 2007). In addition, no effect of site protection on habitat intensity was identified (Macpherson et al., 1997). From this three-year study, Macpherson (1998) showed that from the beginning of colonization to recruitment in the adult population, D. puntazzo juveniles undergo ontogenetic changes in their modes of grouping and dispersion and habitat use. The juveniles (1– 1.5 cm), which have remained in the colonization sites for several months, form monospecific groups that never mix with the adults present in the same region. When they reach a size of 5–7 cm, they begin to disperse beyond the nursery area. Due to the low density of conspecific adults, juveniles tend to remain solitary, even if they sometimes join adult schools of D. sargus. At the time of colonization, juveniles of D. puntazzo clearly prefer habitats located on sandy substrates at depths less than 2 m. They share these overlapping habitats with D. sargus, occupying them at different times of the year: D. puntazzo in fall and D. sargus in spring. As the fish grow, their preference for this habitat weakens, in relation to their gregarious behavior. During colonization, juveniles form small monospecific schools and show a clear gregarious distribution. As they grow, these groups gradually fragment, resulting in an increase in numbers, a decrease in their densities and a more widespread distribution. Habitat use and gregarious behavior do not differ during the day and at night and in clear or turbid waters. However, in strong turbulence, the aggregation level of individuals increases, regardless of fish size. Juveniles show great fidelity to the nursery where they live for several months and here is where they show the fastest growth (Matić-Skoko et al., 2007). Dispersion outside this area occurs when individuals reach 4.5–5.5 cm TL. This process occurs simultaneously with the integration of individuals into adult schools of the same species. Dispersal depends on size rather than residence time in the nursery. Diplodus puntazzo remains in the nursery for 7–8 months during the colder months to reach a size (4.5–5.5 cm TL), that allows them to leave this area. Migration and movements: Due to the arrival of larvae during the winter (usually in December), D. puntazzo is rarer than D. sargus, D. cervinus and D. annularis in lagoons that become hostile in winter. It enters the Italian lagoons of Fogliano and Caprolace between January and March (Mariani, 2006). Size, lifespan and growth: The maximum age recorded is 18 years (about 46.7 cm TL) in a female from the eastern Adriatic (Kraljević et al., 2007), whereas it does not exceed six years in the Gulf of Gabes in Tunisia (Bradai, 2000). It is around 10 years in the Atlantic (Domínguez-Seoane et al., 2006). Matić-Skoko et al. (2007) studied the growth of 0+ D. puntazzo juveniles in the Kornati Archipelago in the eastern Adriatic. The first juveniles were caught at the end of November (12.9%). At this time, they measured 1.6–3.1 cm (2.27 ± 0.382 cm) and weighed from 0.06–0.46 g (0.18 ± 0.105 g). They were approximately 2–2.5 months old. Their monthly growth

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during thhe first year of o life is illusstrated in Figu ure 4.13 according to the G Gompertz equationn (Ricker, 19799) (c = 0.038 mm/day; m r2 = 0.832).

Figure 4.13 3. Juvenile gro owth in D. pun ntazzo in the East E Adriatic according to the Gompe ertz equation (Matić-Skoko ( e al., 2007) et

With regard to annuual growth, thhe age of D. pu untazzo is deterrmined by scaalimetry in the easteern Adriatic (K Kraljević et all., 2007) and in i the Gulf off Gabes (Braddai, 2000). Seventeeen age groups (2–18 ( years) were w identified in the first casse and six (1–66 years) in the seconnd. The growthh parameters of o the von Berttalanffy equatiion are: L∞ = 445.28 cm, K = 0.1991/year, t0 = –0.306/year – inn the eastern Adriatic A (Kralljević et al., 22007) and L∞ = 23.19 cm, K = 0.472/year, 0 t0 = –0.248/year in the Gulf off Gabes (Braddai, 2000). No casess of sexual dim morphism of grrowth was high hlighted. Lengtth–weight (totaal weight) relationshhips are given for the Adriattic: P = 0.139 TL3.001 (Kraljeević et al., 20077) and for the Gulf of Gabes in Tuunisia: P = 4.822 × 10–5 TL2.7882 (Bradai, 20000). Popuulation structuure and dynaamics: In thee Italian lagooons of Foglliano and Caprolacce, D. puntazzzo is representted by only on ne cohort (Figgure 4.14) whhose mean total length does not differ betweeen the two sittes (18.8 ± 7//9 cm in Fogliano and 19.7 ± 5..8 cm at Caproolace) and rem mains there for only 7–8 monnths (Mariani, 2006). In the easteern Adriatic, ouut of the 598 individuals i exaamined, Kraljeević et al. (20007) found 41.1% males, m 55.4% females f and 3.5% 3 immaturre. The sex rattio of M:F waas 0.75:1, but varieed with size. Inn the Gulf of Tunis, the sex x ratio also favvors females, eespecially in larger--sized fish (Mouine et al., 20012).

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Figure 4.1 14. Size frequ uency of D. puntazzo in Italia an lagoons (Fogliano and d Caprolace) (Mariani, ( 2006 6)

4.1.2.5. Diet and fee eding behaviior Diet: In the north of the Aegeann Sea (Canakk kale, Turkey), juveniles (133–77 mm mpete with D. vulgaris (Alttin et al., TL) feedd on copepodds and amphippods and com 2015). The T consumpption of copeepods by juveeniles is repoorted by Binni (1968), Tortonesse (1975) and Lasiak (19866). By comparrison, on the coasts c of Soutth Africa, D. puntaazzo larvae feeed on harpactiicoid copepod ds and amphippods. From 2.5 cm TL, they beggin to consumee epiphytes. When W they reaach 13 cm, theey feed on maccrophytes Chaouch, (Cristenssen, 1978). Diplodus D punntazzo is om mnivorous (Jarrdas, 1996; C 2013). Itts diet consists mainly of macrophytes, then sponges and cnidarians (Sala and Balllesteros, 19977). In the cenntral eastern Adriatic, A maccrophytes are the most frequent and abundannt prey, whereeas bivalve mo ollusks are the most consum med prey (Dulčić et al., 2006)). The latter are considereed as the maain prey accoording to Rosecchhi and Nouazee (1987), folllowed by spo onges, polychhaetes and opphiures as secondarry prey. The average numbber and weight of prey peer stomach is 10.6 and 0.35 g, respectively. r I the Gulf off Gabes (Tuniisia), plants reepresent 89.888% of the In total relaative importannce index in the diet of th his species (C Chaouch et al., 2013). Other grroups (teleostss, crustaceanss, annelids) reepresent other prey. In this case, the trophic level is 2.57 ± 0.2. Feedding behaviorr: Sala and Ballesteros B (1997) showedd that there is a clear sharing of food ressources betw ween the threee Diplodus species (D.. sargus, D. vulgaaris, D. punttazzo) in the rocky subtidal zone. Dip iplodus sarguus mainly exploits the agitated surface waters, while D. pun ntazzo and D. vulgaris preffer deeper waters. The habitats of D. puntaazzo and D. vulgaris overrlap, but theyy exploit differentt food resourcees. Mariani (22001) frequenttly found (freqquency of occuurrence = 23.1%) ectoparasite e crrustaceans Calligus sp. (Copeepoda: Caligiddae) in the stoomachs of D. punttazzo juvenilees (30–70 mm m TL) from m the Caproolace lagoon (Central Mediterrranean). This species presents a “clean ner” behavior,, since the paarasite in questionn lives on the bodies b of mulllets and rarely y on seabream m.

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Dietaary variationss and patternns: In the cen ntral eastern Adriatic, thee average monthly coefficient of o stomach vaacuity is 11.4 4%. It varies significantly between seasons (χ2 = 31.3, P < 0.05), with a maximum of o 34% in winnter and a minnimum of 19.2% in summer, but b does not differ betweeen juveniles and adults (χ χ2 = 0.5, P > 0.055). Overall, thee diet does nott vary accordin ng to fish sizee, but the prefeerence for certain prey varies according to seasson (Figure 4.1 15).

Figure e 4.15. Season nal variations in i diet of D. pu untazzo according g to RII of maiin groups of prey p (Dulčić et al., 2006)

These include am mphipods, spoonges, ophiurres and hydrrozoans. A siignificant differencce exists betw ween their dieet in winter an nd their diet in spring andd summer (Dulčić et al., 2006). In the Gulf of o Gabes, the average stom mach vacuity is 56.94% and also varies with thhe seasons, reeaching a max ximum (74.888%) in the sprring and a m (37.38) in the t fall (Chaoouch et al., 20 013). The com mposition of prey also minimum changes with the seasoons. 4.1.2.6. Reproductio on and repro oductive beha avior Sexuaality: This sppecies exhibitss rudimentary y hermaphrodditism (Lissia--Frau and Pala, 19668; Micale et al., 1996; Brradai, 2000; Pajuelo P et al., 2008). The goonads are bisexual at the beginnning of their development. They evolvee toward gonoochorism, called deelayed gonochhorism or ruddimentary herm maphroditism m (Micale et aal., 1996). Nevertheeless, partial protandry is observed in this species in the Canaryy Islands (Pajuelo et al., 2008). Lissia-Frau and a Pala (1968 8) also report that a small pproportion of the poopulation unddergoes sexuaal inversion. Micale M et al. (1996) ( did noot observe

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individuals with sexuual inversion in a three-y year-old captiive populatioon. These ons associatedd with gamettogenesis. authors described thee microscopic transformatio In an ovvary-dominannt ootestis, thhe ovary undeergoes a longg resting periiod, from October to August, during whicch it contain ns oogonia, primary ooccytes and mber and occasionnally vitelline oocytes. Fulll ovary deveelopment occuurs in Septem leads to the formationn of advanced vitellogenic oocytes. o The testicular partt contains only speermatogonia annd appears to regress in 76 6% of the casees examined, w with only a few sppermatogonia isolated withhin a fibrous and well-devveloped strom ma. In the remaininng 24% of cases, the testicular paart, althoughh very small, seems histologiically normal with dense sppermatogonia and with no signs of regreession. In ootestis with testiculaar dominance,, the testis is at rest from November too July. In August, it is maturinng and spawnning takes plaace from September to Occtober by spontaneeous sperm em mission. In fuunctional malees, the ovary contains onlyy oogonia and oocyytes that do not develop beyond the perinuclear p sttage, regardleess of the period off the reproducctive cycle. Firstt sexual matuurity: In the Gulf G of Gabees, the size of o the smallesst mature individual is 16.2 cm m in males annd 17.0 cm in n females (Brradai, 2000). The first m is acqquired at 21.55 ± 0.2 cm TL L (three yearss) in the Gulff of Tunis sexual maturity (Mouinee et al., 2012)). Under expeerimental con nditions, Micaale et al. (19996) found mature inndividuals at two t years old. Spaw wning site andd period: In the t Gulf of Gabes, G the goonad maturatiion phase begins inn August. Thee GSI is maximum in Octo ober and decrreases from O October to Novembber, with spaw wning that lasts a little over a month (Braadai, 2000). It is also in fall that reproduction takes place inn the Gulf of Tunis (Figuree 4.16) (Mouiine et al., 2012).

Figu ure 4.16. Month thly variations in i the gonados somatic index (continuous lin ne) of D. punta azzo and the te emperature (brroken line) in the th Gulf of Tun nis (Mouine et al., 2012)

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Note that in the Atlantic (Canary Islands), breeding occurs in fall and early winter, from September to February (Pajuelo et al., 2008). In captivity, Micale et al. (1996) and Papadaki et al. (2008) recorded spawning between September and December, at a temperature of 18.5–21 °C, and between August and October, respectively. Fecundity: In captivity, the relative fecundity is between 2.4 ± 0.07 and 4.9 ± 0.08 million eggs/kg in females (Papadaki et al., 2008). Reproductive behavior: The long reproductive period highlighted by Pajuelo et al. (2008) indicates serial spawning. In fact, the non-synchronization of the beginning of vitellogenesis in all females and the simultaneous presence of oocytes at all stages of development indicate asynchronous ovarian development. In addition, the copresence of oocytes in the final maturation phase and postovulatory atretic oocytes indicates that D. puntazzo is a multiple spawning fish. Eggs, larvae and ontogenesis: Lo Bianco (1909), Ranzi (1930, 1933), Thomopoulos (1956) and Divanach (1985) provide data on eggs and the larval and postlarval stages. As with other Sparidae, mature ova are transparent spheres with a transparent and colorless yolk, completely filling the sac and containing a single amber-yellow to pink oil globule. The cytoplasm forms a thin cortical layer all around the yolk and is thickened at the animal pole (Divanach, 1985; Kamaci et al., 2005) (Figure 4.17(a)).

Figure 4.17. Diplodus puntazzo: (a) fertilized egg and (b) embryo trying to leave the egg by breaking the chorion with abrupt movements (Kamaci et al., 2005)

The ova have a diameter of 0.76–0.88 mm (average 0.806 mm) and incubation lasts 35–45 h at a temperature of 19–21 °C (Divanach, 1985). Ranzi (1933) describes the development of postlarvae from 1–6.6 cm TL. Kamaci et al. (2005) studied the

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stages of embryonic development of D. puntazzo in captivity. Females lay at 22–24.5°C. The eggs laid are hyponeustonic (81%) and transparent. Their diameter is 801–816 µm (807 ± 08 µm). They contain a single unpigmented oil globule with a diameter of 245 ± 08 µm (Figure 4.17(a)). After 26 h, the egg hatches (Figure 4.17(b)). The mean total length of larvae is 1.90 ± 0.03 mm, with an elliptical yolk sac 0.91 ± 0.08 mm long and 0.51 ± 0.05 mm wide. An oil globule 0.24 ± 0.008 mm in diameter is present in the posterior end of the yolk sac. At this stage, the eyes are not yet pigmented, the fins are absent and the mouth is not yet formed. The heart is visible with rhythmic beats. According to Çoban et al. (2012), at 20 ± 0.5°C, hatching larvae measure 2.91 ± 0.11 mm and reach 3.35 ± 0.13 mm at Day 4 (opening of the mouth). The different stages of larval development are illustrated in Figure 4.18.

Figure 4.18. Ontogenic development of D. puntazzo larvae raised at 20 ± 0.11°C. A: Day 1 post-hatching (2.88 mm Lt), B: Day 4 (3.36 mm), C: Day 10 (5.12 mm), D: Day 15 (5.98 mm), E: Day 24 (7.96 mm), F: Day 30 (11.43 mm), G: Day 37 (13.62 mm), H: Day 42 (16.08 mm) (Çoban et al., 2012). For a color version of this figure, see www.iste.co.uk/kara/fishes3b.zip.

Sfakianakis et al. (2005) studied the development of the spine and fins in D. puntazzo. The onset of spinal ontogeny occurs at a total length of 4.9 mm with

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the formation of the first neuronal process, while the vertebrae form at 5.8 mm and finish developing at 8.1 mm. The pectoral supports (cleithrum, coracoid-scapula, etc.) are the first fin-shaped elements (at 2.9 mm) to develop followed by those of the caudal (4.5 mm), dorsal and anal (6.4 mm) fins and finally the pelvic fin (8.1 mm). The caudal fin is the first to develop rays and reach the final number of lepidotrichia, but the last to complete the formation of all its rays (dermatotrichia, 14.1 mm), followed by the anal (8.5 mm), dorsal (10.1 mm) and finally the pectoral and pelvic fins. 4.1.2.7. Economic importance Diplodus puntazzo is the subject of semi-industrial, artisanal and recreational fishing. The fishing gear used includes trawls, gillnets, bottom longlines and drifters, hand-held lines, beach seines and traps. D. puntazzo is sold as freshly caught in the markets of many Mediterranean countries. FAO statistics do not distinguish D. puntazzo from other Sparidae. However, in the Fogliano and Caprolace lagoons, this species represents 12% and 6%, respectively, of the Sparidae caught in Italian lagoons (Mariani, 2006). In the Mediterranean, D. puntazzo is one of the five species of seabream that is most interesting for aquaculture. The cumulative production of juveniles from 1996 to 2002 reached 34.3 million individuals. Its production peaked at about 10 million fry and 2,500 tons per year in the late 1990s. Later, it dropped to about 5 million fry per 1,200 tons (Suquet et al., 2009), mainly from Italy and Cyprus. The species is well adapted to bream feed and shows growth (280–320 g at 18–24 months; Suquet et al., 2009) and a relatively high feed conversion rate (Favaloro et al., 2002; Hernandez et al., 2003). In addition, the species exhibits net cleaning behavior, which makes it contend with the sea bass in polyculture. However, its production remains low because of problems mainly related to the hatchery (variable survival rate, from 3–40%) and pathologies during growth (Athanassopoulou et al., 1999; Bodington, 2000). Oral parasitic isopods can cause significant mortality during the first year (Suquet et al., 2009). By wet fertilization, Divanach (1985) obtained “D. puntazzo ♀ × D. vulgaris ♂” hybrids. The fish obtained are viable and intermediate between the two species, but closer to D. vulgaris. Dujaković and Glamuzina (1990) crossed “S. aurata ♀ × D. puntazzo ♂”. At 19.5°C, embryogenesis and yolk sac resorption lasted less for time than for S. aurata. At the beginning of exogenous trophic activity, between 6 and 30 days post-hatching, growth and survival did not differ significantly between S. aurata and the hybrids.

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4.1.2.8. Protection status and conservation – IUCN Global Red List: NE. – IUCN Mediterranean Red List: LC. 4.1.3. Diplodus sargus sargus (Linnæus, 1758)

4.1.3.1. Nomenclature and systematics Type: Sparus sargus Linnæus, 1758, Syst. Nat., Ed. X: 278 (Habitat in M. infero). Synonyms: Sargus rondelettii Valenciennes, 1830; Sargus vetula Valenciennes, 1830. Vernacular names: Sargu (AL), ouarka (DZ), sar rayé (FR), shargoush (EG), sargo (ES), sargôs (GR), white seabream, fratar (GB), sargus (IS), sarago, sarago maggiore (IT), sarghoûs (LB), ouarka (MA), sargu (MT), sargun (TN), karagoz (TR). Etymology: From the Greek sargus (name of a fish, Aristotle V, II sargos), perhaps sarx (flesh). Systematics problems: In the species D. sargus, six subspecies can be distinguished, of which only one, D. skotschyi, lives outside the Mediterranean area. Subspecies diversification can be observed morphologically (De la Paz et al., 1973) and molecularly (Summer et al., 2001) and may be due to rapid successive colonization from the eastern Atlantic. This hypothesis is supported by Domingues et al. (2007). Using mitochondrial markers, these authors showed that there is a high genetic homogeneity within D. s. sargus, and that D. sargus lineatus, which originated from the Cape Verde Islands, can be considered as the most ancestral subspecies, suggesting that the other subspecies diversified from this region.

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4.1.3.2. Description Morpho-anatomy: It has an oval compressed body, a slightly protruded mouth and thin lips. Dentition composed of eight incisors on each jaw, rarely 10 in the upper jaw; three or four (rarely five) rows of molars in the upper jaw and two or three (rarely four) rows in the lower jaw (see genus Diplodus). First gill arch with 9– 12 gill rakers on the bottom and six to nine on the top. Dorsal fin with 11 or 12 (rarely 13) spines and 12–15 soft rays; anal fin with three spines and 12–14 soft rays; forked caudal fin. Lateral line with 58–67 scales (excluding scales on the caudal fin). The relationships between total length, fork length and standard lengths are given by Girardin (1978) in the Gulf of Lion: TL = 1.1518. FL – 0.1167 and SL = 0.8865. FL – 0.1325 (9 ≤ TL ≤ 35 cm, 8 ≤ FL ≤ 31 cm) and by Rosecchi (1985) in the Gulf of Lion: TL = 1.2821. SL + 1.091 and FL = 1.1168 SL + 2.7772 (2.7 ≤ TL ≤ 37.5 cm, 2 ≤ SL ≤ 29.8 cm), but this author does not specify the lagoon or marine origin of his samples. Benchalel and Kara (2010) give a complete biometric description of D. s. sargus from the east coast of Algeria. The maximum size in the Mediterranean is 45 cm; sizes between 15 and 30 cm are common (Fisher et al., 1987). The maximum size in the Gulf of Lion is 39 cm TL (Girardin, 1978). Coloring: General coloring is silver-gray, with eight to nine thin transverse stripes, alternate dark and light stripes on two-thirds of the body. These stripes tend to disappear in individuals over 25 cm, and sometimes only five appear in juveniles. There is the presence of interorbital space and a darker muzzle. A large dark saddleshaped spot on the caudal peduncle and another at the upper part of the pectoral axilla. Odd fins are grayish, the dorsal and anal fins are darker on the upper edge and the posterior edge of the caudal fin is black. Variations: Loy et al. (2001) showed changes in the morphology of D. sargus during the early juvenile stages in the Ligurian Sea, during the change in habitat from the shore to deeper waters. These changes are related to their swimming abilities and trophic behavior. Palma and Andrade (2002) found morphological differences between seabream from four countries (Portugal, Spain, Italy, Greece). There is a clear geographic gradient between Atlantic and Mediterranean fish. Via morphogeometry, Kaouèche et al. (2017) separated, on the one hand, white seabream living on both sides of the Sicilian-Tunisian Strait, and, on the other hand, the marine (Bizerte, Mahdia, Gulf of Gabès) and lagoon (Bizerte, Ghar El Melh, El Bibane) samples from the Tunisian coasts. Sexual dimorphism: Benchalel and Kara (2010) showed morphological sexual dimorphism. Predorsal length, pre-anal length, caudal peduncle height and eye diameter have, at equal size, faster growth rates in females.

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Osteology, otoliths and scales: Descriptions, drawings and photographs of sagittal otoliths are given by Koken (1884), Sanz Echeverria (1930), Chaine (1937), Kinacigil et al. (2000) and Tuset et al. (2008). This otolith, elongated and thick, has smooth edges. The posterior dorsal edge is very prominent and the center of the dorsal edge is obtuse, but also salient (Pastor, 2008) (Figure 4.19).

Figure 4.19. Sagittal otolith of an individual (28.0 cm TL) of D. sargus sargus from the western Mediterranean, scale 1 mm (Tuset et al., 2008)

Tuset et al. (2008) characterize the morphology of the sagittal otolith from the western Mediterranean coasts by the following ratios: otolith length/total length of the fish = 2.8–4.2; otolith width/otolith length = 45.5–58.3; circularity = 15.4–17.3; rectangularity = 0.3–0.4. Karyology: The number of chromosomes is 2n = 48. Three pairs are biarmed, one pair is subtelocentric and 20 are acrocentric (Cataudella et al., 1980). Protein specificity and genetic diversity: Basaglia et al. (1990) compared the expression profiles of three isozymes (lactate dehydrogenase, malate dehydrogenase and glucosephosphate isomerase) of D. puntazzo, S. aurata and D. sargus. The three protein systems were clearly different. By analyzing the crystalline and muscle proteins in four species of Diplodus (D. sargus, D. annularis, D. vulgaris, D. puntazzo), Basaglia and Marchetti (1990) showed that D. sargus and D. annularis are closely related and clearly distinct from the other two species. This study using allozyme and molecular markers (mitochondrial DNA control region) does not show any genetic difference between D. sargus from the Mediterranean and Atlantic (Faro, Portugal) (Bargelloni et al., 2005). This is confirmed by Domingues et al. (2007) who discovered genetic isolation with

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increasing distance from the Azores population. These authors believe that this divergence is the consequence of Pleistocene glaciations in the northeast Atlantic. Diplodus sargus would have disappeared at that time from Western Europe and suffered a drastic reduction in its numbers in the Canary Islands and Mauritania, while it flourished in the least-affected regions, such as Madeira, the Azores and the Mediterranean. Indeed, by studying the genetic structure and connectivity between continental and island seabream in the Atlantic and Mediterranean, GonzálezWangüemert et al. (2010, 2011) highlighted the genetic isolation of the population from the Azores archipelago, which is not the case for the Mediterranean islands of Majorca and Castellamare. The influence of the Sicilian-Tunisian Strait on the genetic structuring of D. s. sargus was studied by Kaouèche et al. (2012). Thirteen allozyme markers and a cytochrome b gene fragment are used. The former highlight the differentiation between the north-east (Bizerte and Ghar El Melh lagoons, Mahdia) and the south (Gulf of Gabes, El Bibane lagoon) of Tunisia, whereas the latter indicates genetic homogeneity on both sides of this strait. Using a mitochondrial marker (Cyt b) and nine nuclear markers (microsatellites), GonzálezWangüemert and Perez-Ruzafa (2012) examined the gene flow between seabream from the Mar Menor lagoon (north-eastern Spain) and those of two sites (Banyuls in France and Murcia in Spain). The analysis of molecular variance (AMOVA) between the lagoon and the sea detected population differentiation. The highest genetic diversity was recorded in the lagoon with two specific haplotypes (Cytb-17 and Cytb-18) and the largest number of singletons, some of which with a high number of mutations. These genetic differences between lagoon and marine individuals reveal a high adaptation potential of this species to lagoons and support the existence of genetic selection. Preserving exclusive genotypes in lagoon occupants favors the divergence-with-gene-flow of González-Wangüemert and Perez-Ruzafa (2012). Using eight microsatellite markers, Hernandez-Garcia et al. (2015) suggest the presence of subpopulations or genetic substructures within the population of this same lagoon. This is interpreted as a homogeneous mixture of individuals from three distinct Mediterranean subpopulations leading to the Wahlund effect. This result also indicates that D. sargus adults return to their original spawning grounds, thus maintaining genetic differences among the respective populations over time. At the subspecies level, González-Wangüemert et al. (2006) show that the gene flow between D. s. sargus and D. s. cadenati is weak, imposed by ecological differences on both sides of Gibraltar. However, in a part of the south-western Mediterranean ( 3.92, α = 0.001) (Table 4.14). Function

Gulf of Annaba

Mellah lagoon

tpe (α = 0.001)

tpo (α = 0.001)

FL = f (TL)

FL = 228 TL – 305

FL = 102 TL – 009

875*

–

SL = f (TL)

SL = 107 TL – 026

SL = 102 TL – 017

114

1,871*

Lc = f (TL)

Lc = 228 TL – 363

Lc = 122 TL – 120

668*

–

H = f (TL)

H = 110 TL – 075

Hc = 133 TL – 120

221

3,679*

Hpc = f (TL)

Hpc = 139 TL – 205

Hpc = 114 TL – 144

523*

–

LPd = f (TL)

LPd = 15 TL – 197

LPd = 125 TL – 129

462*

–

LPp = f (TL)

LPp = 131 TL – 134

LPp = 100 TL – 063

878*

–

Lpp = f (TL)

Lpp = 126 TL – 091

Lpp = 117 TL – 074

120

2,717*

LPa = f (TL)

Lpa = 124 TL – 088

Lpa = 117 TL – 072

102

1,874*

Do = f (Lc)

Do = 051 Lc + 027

Do = 087 Lc – 032

461*

–

LPo = f (Lc)

LPo = 073 Lc – 007

LPo = 138 Lc – 125

500*

–

Lpo = f (Lc)

Lpo = 067 Lc – 015

Lpo = 087 Lc – 141

282

1,544*

Lm = f (Lc)

Lm = 082 Lc – 020

Lm = 097 Lc – 037

194

2,343*

TL, total length; FL, length at the caudal fork; SL, standard length; Lc, cephalic length; H, body height; Hpc, height of the caudal peduncle; LPd, predorsal length; LPp, prepectoral length; Lpp, postpectoral length; LPa, preanal length; Do, eye diameter; LPo, preorbital length; Lpo, postorbital length; Lm, upper maxillary length. Table 4.14. Comparison of the slope and the position of the linear regression in S. aurata from the Gulf of Annaba and the Mellah lagoon (*significant difference) (Chaoui et al., 2001)

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

Number of hard rays on dorsal fin

Number of soft rays on dorsal fin

Gulf of Annaba

Mellah lagoon

Gulf of Annaba

Mellah lagoon

Gulf of Annaba

Mellah lagoon

Mean

11

10.90

13.29

12.94

12

11.19

Standard deviation

–

0.38

0.52

0.80

1.22

1.77

Mode

11

11

13

13

11

12

Minimum

11

9

12

8

9

6

Maximum

11

12

14

14

15

14

Characteristics Location

t (α = 0.001)

Number of gill rakers

1.56

3.27

5.05*

–

–

0.26

CD CD, coefficient of difference.

Table 4.15. Comparison of the numeric characteristics found in S. aurata from the Gulf of Annaba and Mellah lagoon (*significant difference) (Chaoui et al., 2001)

Audouin (1962) shows that for Gilthead seabream from the Thau lagoon (from 3 to 62 cm TL), the relative head length and eye diameter decrease with fish size. In contrast, the height and width of the body increase relatively faster than the total length. The predorsal distance shows a negative disharmony with body length up to 31 cm; it presents a weakly positive disharmony when the size increases beyond 31 cm. Also, the preanal distance, compared to the size, shows a negative disharmony up to 22 cm; it shows a positive disharmony between 25 and 31 cm and weakly negative disharmony beyond this. According to the author, the allometries concerning the predorsal and preanal distances are related to the protandric hermaphroditism of this species, since the successive changes observed coincide with the moment of sexual maturity, then with sexual inversion. Chaoui (2007) describes the evolution of the morphology of the Gilthead seabream from the Mellah lagoon during its growth using allometric relations. Osteology, otoliths and scales: Saka et al. (2008) described the development of the cephalic skeleton of S. aurata larvae from 1 day (2.68 ± 0.27 mm TL) to 41 days (10.80 ± 1.24 mm TL) post-hatching. At hatching, larvae are devoid of viscerocranial

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elements. Neurocranial development begins with yolk sac resorption, the formation of trabecular rods and the ethmoid plate at 2.85 mm TL. Jaws begin to develop during the yolk stage. Teeth appear at 7.7 mm TL and the branchial filaments are formed between 8 and 8.9 mm TL. The first ossifications occur at 9.20 mm TL and concern the dentition, jaw and cartilage of Meckel. The osteological development of the caudal fin is described by Koumoundouros et al. (1997) in the larval and juvenile stages. Sparus aurata otolith data are provided by Sanz Echeverria (1926, 1930), Chaine (1937) and more recently by Kinacigil et al. (2000) and Tuset et al. (2008). According to Kinacigil et al. (2000), otoliths are irregularly pentagonal in shape and elongated. The rostrum is wide and elongated. The antirostrum is small and sharply pointed. The sulcus is deep and wide. The cauda is slightly on the ventral side. The dorsal side is wide. The otolith is convex and concave, respectively, on the medial and lateral faces. The sides are set back. In particular, the postrostrum is denticulate like a saw. According to Tuset et al. (2008), otoliths are pentagonal to elliptical, with tooth-like edges (Figure 4.46).

Figure 4.46. Sagittal otolith of an individual (22.5 cm TL) of S. aurata from the western Mediterranean, scale 1 mm (Tuset et al., 2008)

This author indicates the following ratios in Gilthead seabream from the western Mediterranean and north-east Atlantic: otolith length/total length of fish = 2.8–3.1; otolith width/otolith length = 51.2–65.3; circularity = 16.8–18.0; rectangularity = 0.2–0.3. Karyology: The number of chromosomes is 2n = 48. Four pairs are meta or submetacentric, and five pairs are subtelocentric. The other 15 pairs are acrocentric (Cataudella et al., 1980).

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Protein specificity and genetic diversity: Using allozymic markers (21 loci), Ben Slimen et al. (2004) showed the geographical differentiation of Gilthead seabream on both sides of the Siculo-Tunisian Strait, with Fst values between 0.265*** and 0.106*. Note that the Fst value in the western Mediterranean is not significant (Fst = 0.0093). Alarcón et al. (2004) showed a low degree of global differentiation for nine samples analyzed (five Mediterranean: Leros island in the Aegean, Messolonghi lagoon, Trieste, Alicante, Murcia; and four Atlantic: Cadiz, Aveiro, Tavira, Oleron island) using several types of markers (microsatellites: Fst = 0.036, 6 loci, allozymes: Fst = 0.031, 16 loci, mitochondrial DNA control region: no variability). Innocentiis et al. (2004), using four microsatellite loci, studied five samples from the western Mediterranean (Sardinian Sea, Sardinian Channel, Central Tyrrhenian Sea), an Adriatic sample and an Atlantic sample. These authors highlighted a weak but significant overall differentiation (Fst = 0.014***), mainly between the Atlantic, the Adriatic and the western Mediterranean individuals. In the latter, the southernmost sample (southern Sardinia) is distinct from the four others located farther north (Fst = 0.017). Using 10 microsatellite markers, Franchini et al. (2012) found an isolation by the distance of the individuals of the Italian coasts compared to those of the Atlantic, as well as a weak but significant differentiation (Fst = 0.0072) between 12 Italian localities (three in the Adriatic Sea, three in the Tyrrhenian Sea, one in the Ligurian Sea, four on the Sardinian coasts, one in the Sicilian Channel). This weak differentiation between the western Mediterranean and the Siculo-Tunisian and Adriatic straits seems to be confirmed by the analysis of 26 enzymatic loci by Rossi et al. (2006), which gives an Fst of 0.017 between the Adriatic Sea, the Tyrrhenian Sea and the Sardinian Channel. Chaoui et al. (2009) compared four samples of Gilthead seabream from the northern (Thau and Sète-mer) and southern (Annaba Bay and Mellah Lagoon) shores of the western Mediterranean with three microsatellite markers and two RAPD systems. Genetic differentiation observed at microsatellite loci between the two shores was strong and significant at all loci (Fst = 0.069***). The two samples from the Gulf of Lion are not differentiated from one another (Fst = 0.003 ns), while those of the Gulf of Annaba and the Mellah lagoon show variable levels of differentiation according to the marker or the combination of markers used. RAPD data show a similar trend. Rossi et al. (2009) studied temporal variations in the genetic structure of Gilthead seabream, using allozyme and microsatellite markers, in two Italian lagoons of the Tyrrhenian Sea, subject to two different management methods: Sabaudia, naturally populated by larvae and juveniles and sampled three times (2000, 2001, 2002) and Orbetello, reared in a hatchery and sampled five times (2000, 2002, 2003 and twice in 2004). In the first case, all the lagoon samples are homogeneous and do not differ from those of the adjacent shoreline. In the second

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case, differences are highlighted, both temporally (Fst allozymes = 0.0133**, Fst microsatellites = 0.0153**) and between the lagoon and the nearby marine area. In addition, an interlagoon genetic structuration is observed (Fst allozymes = 0.0089**, Fst microsatellites = 0.0058**). Using microsatellite markers, Chaoui et al. (2012) showed that Gilthead seabream caught at sea in the Gulf of Lion belong to the same genetically homogeneous panmictic unit, whereas the individuals from the Or lagoon (or Mauguio lagoon, France) are genetically distinct from the marine individuals. According to these authors, alleles of genetic markers associated with candidate genes, such as prolactin (Pr1, which has a role in osmoregulation) and growth hormone (GH, which plays a role in growth, but which is also involved in osmoregulation), are favored in the lagoon habitat and their length is the underlying cause of this genetic differentiation. Guinand et al. (2016) highlight fewer growth hormone (GH) and prolactin (Prl) gene discrepancies between 0+ specimens entering the Mauguio, Thau and Salses-Leucate lagoons (France) in the spring, and individuals of the same cohort who left in the fall to return to sea, where they were born. Gilthead Seabream juveniles are therefore subject to environmental selection pressures. Differences in genetic polymorphism (seven microsatellite markers) between captive Gilthead seabream and wild Gilthead seabream were found in Greece by Karaiskou et al. (2009). While no significant differences exist between wild populations from the Ionian Sea, Aegean Sea and aquaculture spawners (Fst = 0.009), highly significant Fst values were detected between captive and wild fish (0.009* ≤ Fst ≤ 0.049***). This conclusion confirms the results obtained by Alarcón et al. (2004) and Loukovitis et al. (2012 for other pairs of wild/captive Mediterranean and Atlantic samples. On the other hand, Dogankaya and Bekcan (2012) found no genetic difference (12S rRNA, cytochrome b, cytochrome oxidase II) among or between wild populations of the Turkish coasts and the stocks reared in the region. A weak genetic differentiation (eight microsatellite loci) between wild and captive individuals in the Adriatic was found by Šegvić-Bubić et al. (2011) who suspect genetic pollution by fish escaping from aquaculture farms. 4.4.1.3. Distribution Although common throughout the whole Mediterranean, the Gilthead seabream is less so to the east and south-east (Tortonèse, 1975) and very rare in the Black Sea (Bânârescu, 1964). It is also found in the eastern Atlantic, from the British Isles to the Cape Verde Islands, off the Azores, Madeira and the Canaries. The capture of many juveniles in an estuary in southern Ireland over four months (April–August) suggests the spawning success of this species or at least the success of its establishment in more northerly regions than what was previously thought (Fahy et al., 2005; Craig et al., 2008) (Figure 4.47).

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In addition, Balart et al. (2008) reported for the first time the presence of a S. aurata female (TL = 30 cm, Pt = 356 g) in the Gulf of California.

Figure 4.47. Geographic distribution of S. aurata

4.4.1.4. Ecology Habitat: The Gilthead seabream is a necto-benthic species, often solitary or found in small groups, at shallow depths in the surf zone, as well as in Posidonia meadows, eelgrass beds and sandy and sandy-muddy bottoms. At sea, it is fond of mixed substrates with scattered rocks and small sandy areas, as well as the edges of rocky areas. It is also found in ports and around dykes and in all Mediterranean lagoons. Migrations and movements: Sparus aurata is a euryhaline and eurythermal coastal species. It makes seasonal migrations between the sea and nearby lagoons or estuaries. Following marine spawning events from October to December, juveniles and some adults migrate in early spring to coastal and lagoon waters where they find abundant food resources and favorable temperatures. Very sensitive to the decrease in temperature in late fall, they return to the open sea to reproduce (adults). Young individuals live in shallow water (about 30 m), while adults can go down to –150 m. Note that the migration from lagoon to sea in the fall is not the case for all individuals, since Mercier et al. (2012), based on the microchemical structure (Cr, Mn, Cu, Sr) of otoliths, found that some large Gilthead seabream can spend the winter in lagoons in the Gulf of Lion.

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The migration calendar of Gilthead seabream in French lagoons, and more particularly in the deep Thau lagoon, has been mentioned by many authors2. Hervé (1973) was interested in Gilthead seabream in Salses-Leucate. Audouin (1962) monitored the sea–lagoon–sea migrations of the Thau lagoon Gilthead seabream, identified by markings (Pressadon and Petersen brands). According to this author, fry from the current year, all born at sea, but also juveniles of the previous year (1+) and adults, enter this lagoon from February onwards (individuals 1+, 2+ , 3+, etc. arrive in February and the 0+ end of April). They remain there until October– November. During the last two months, the weather and hydrological conditions, and for adults the need to go to marine nesting sites, forces them to leave the lagoons and enter the sea (note that Mathias and Jalvy (1958) believe that some large individuals exit at the end of August). At sea, these Gilthead seabream first occupy the coastal area, then trawlable sediment between 25 and 50 m. In January, they disappear from the coastal zone and return in February, and then enter the lagoons. Some return to the lagoon in their first year of life, but this is not a general rule and only a very small percentage of individuals over three years old enters the Thau lagoon. Note here 0+ individuals do not return to shallow lagoons, at least those in Languedoc Roussillon (France), after their first winter spent at sea. Amanieu (1973) distinguishes two populations of Gilthead seabream in Sète waters (France): those found in lagoon waters (Thau lagoon) where juveniles and young adults predominate, and those at sea (off Sète) where large adults predominate. Audouin (1962) believes that the migration of Gilthead seabream to lagoons is mainly due to hydroclimatic conditions prevailing in the marine environment that they are occupying at that time. Given the relatively high percentage of recaptures of 1+ individuals in the Thau lagoon (between 2% and 21%), it is likely that most of the bream in this lagoon remain near the ocean mouth of the lagoon, where they went in winter and, for adults, to spawn. Audouin (1962) found that Thau bream showed limited movements at sea in the area between the rivers Aude and Rhône, about 60 and 110 km on both sides of Sète. By tagging (Pressadon brand), Lasserre (1974a, 1974b, 1976) confirms these results. The tagged Gilthead seabream travel from Cap d’Agde (25 km from Thau) and Espiguette (45 km from Thau), with the exception of two individuals that reached Bandol (200 km) in the Var and Barcarès (90 km) in the Aude. This migration evidence and the temporary geotemporal isolation of the lagoon raise questions about possible interlagoon autonomy. Is there a certain trophic homing between individuals that remain in the sea and lagoon-sea migrants? 2 Gourret, 1896a, 1896b; Mathias, 1932, 1954; Mathias and Tcherniakovsky, 1932; Mathias and Jalvy, 1958; Audouin, 1962; Paris and Quignard, 1971; Lasserre, 1972, 1974a, 1974b, 1976; Hervé and Bruslé, 1979.

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According to Audouin (1962), up to four out of five bream (0+ and 1+) tagged in Thau do. The author indicates that, subsequently, there is a mixture of individuals from the initial stock with individuals from other sites, which results in a heterogenization of data in terms of size frequency and fewer good size/age correlations. Lasserre (1976) wrote: “We cannot speak of a Gilthead seabream stock from the Thau lagoon [...] Only a percentage of Gilthead seabream that had entered the previous year will enter the following year; this percentage decreases with age”. Out of 437 juvenile Gilthead seabream (16.4–18.7 cm FL) captured at sea in March in Bages-Sigean and Ayrolle lagoons (Port-la-Nouvelle, France), and released after tagging (dangling-tag) at their place of capture, six were recaptured in sites located northeast toward the Rhône (Gruissan: 6 km, Agde: 45 km, Port Camargue: 133 km and 127 days) (Chauvet et al., 1992). These authors believe that the tagged Gilthead seabream have a gregarious behavior, clearly oriented (not erratic) toward inland waters (see Figure 4.44). Ecological valence: Experiments were conducted by Audouin (1962) on Gilthead seabream from four months to one year old. At a salinity of 37‰, they actively live between 9°C and 33°C. They only survive for a few hours at temperatures below 2.5°C and above 36°C. They can actively live in water with a salinity of between 5 and 44‰. The minimum salinity is 1‰ and the maximum salinity is 54‰ (within temperature limits of 15°C and 25°C). By exposing Gilthead seabream to different salinities (freshwater at 45.1‰, T = 18°C) for 300 days post-hatch, Bodinier et al. (2010) showed that these fish are hyper–hypo–osmotic regulators during all stages of their ontogenetic development. However, their osmoregulatory capacity depends on their age and reaches its maximum level at 96 days post-hatch. It should be noted that Gilthead seabream occupy warm lagoons, such as El Bibane in Tunisia (S‰ = 39–50) and Bardawil in Egypt (S‰ = 39–68), but we have no information concerning its preferential distribution in these lagoons. Madeira et al. (2016) experimentally demonstrated that the biochemical homeostasis of S. aurata larvae may be disturbed in an ecologically realistic thermal range and emphasize the risks of global warming on the evolution of these larvae. Size, lifespan and growth: The extreme ages are recorded at about 8 months (25 cm TL) in laminar lagoons (Mauguio, France), 4 years (30 cm TL) in the Bardawil lagoon in Egypt (Ben-Tuvia, 1979) and in Beymelek, Turkey (35.5 cm TL, 0.92 kg) (Emre et al., 2009), 7 years (61 cm TL, 4 kg) in the Mellah lagoon in Algeria (Chaoui et al., 2006), 10 age groups (69 cm Lt, 5.52 kg) in the Thau lagoon in France (Audouin, 1962) and 12 years (57.5 cm TL) in the estuary of the Mirna River in Croatia (Kraljević and Dulčić, 1997) (Table 4.16). The age is between 2 and 7 years (51.5 cm TL, 2.6 kg) in Güllük Bay, Turkey (Akyol and Gamsiz, 2011) and between 0 and 8 years (35 cm TL) in the Gulf of Gabes, Tunisia (Hadj Taieb et al., 2013a).

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Site and authors Method Age N A B K to L∞ Φ’ Thau, France (Lasserre Scales 1–4 713 0.0226 2.886 62.02 0.221 –0.774 6.745 and Labourg, 1974a, 1974b) Segura, Spain LF 2–6 135 0.0289 2.907 53.00 0.315 – 6.785 (Arnal et al., 1976) Thau, France Scales 1–4 383 0.0121 3.064 57.66 0.272 –0.541 6.807 (Lasserre, 1976) Ebro, Spain 112 × 3.055 62.19 0.171 –0.531 6.494 LF 1–7 611 (Suau and López, 1976) 10–7* Bardawil Lagoon, Egypt 3.73 × 2.810 – 0.26 – – Otoliths 1–4 422 (Ben-Tuvia, 1979) 10–5 Cadiz, Spain 71 × 10– 3.120 84.55 0.130 –1.586 6.834 Scales 1–7 1775 7 * (Arias, 1980) Alexandria, Egypt Scales 1–5 103 – 3.22 62.44 0.234 –0.401 6.816 (Wassef, 1990) Mirna, Croatia Otoliths 1–12 314 0.0112 3.052 59.76 0.153 –1.711 6.303 (Kraljević and Dulčić, 1997) Mellah Lagoon, Algeria Scales 1–7 370 0.0129 3.067 55.33 0.513 –0.282 7.359 (Chaoui et al., 2006) Port Said, Egypt Otoliths 1–4 1714 0.0123 3.0284 37.98 0.500 –0.600 6.581 (Mehanna, 2007) Beymelek Lagoon, Turkey Scales 0–4 1881 0.0174 2.9769 44.60 0.394 –1.331 6.664 (Emre et al., 2009) Güllük Bay, Turkey (Akyol Scales 2–7 332 0.0515 2.737 64.97 0.14 –2.47 6.381 and Gamsiz, 2011) Gulf of Gabès, Turkey Otoliths 0–8 1065 0.0107 3.0797 38.28 0.202 –1.888 5.69 (Hadj-Taieb et al., 2013a) Homa Lagoon, Turkey – Juveniles 105 0.0090 3.150 – – – – (Acarli et al., 2014) *Measurements are in mm and g (for the other authors, the measurements are in cm and in g). The values of Φ’ were calculated for the other authors. LF, length frequency.

Table 4.16. Parameters of absolute (L∞, K, to) and relative (a, b) growth and growth performance indices (Φ’) of S. aurata in different Mediterranean localities (Chaoui et al., 2006)

Audouin (1962) studied lagoon growth (Thau, Palavas, Bages-Sigean lagoons) of the young Gilthead seabream during their first year. At about two months old, they enter the Thau lagoon in late April. At the beginning of May, they measure 4–6 cm (approximately 1.5 g). In July, the smallest individuals measure 7 cm and weigh 4 g; the largest ones measure 12 cm and weigh 22 g (50% measure 9 cm and weigh 8 g). In September, they are between 16 and 21 cm in size. As of October, they begin to regroup and head toward the sea, with 38% of them having a size of 21 cm and a

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Fisshes in Lagoonss and Estuaries in the Mediterra anean 3B

weight of o 120 g. The Gilthead seabbream (0+) thaat spend the fiirst months off their life in the Paalavasian lagooons (Mauguioo, Prévost lago oons, etc.) reaach, at the tim me of their return too sea, a size roughly equaal to that of the t Gilthead seabream in the Thau lagoon: their length is i between 177 and 23 cm m and their weight w betweenn 85 and h of 0+ juveniiles (Figure 4.48) does 155 g. Inn the Bardawil lagoon, the linear growth not diffeer from those from the Palavasian lagoo ons, since theyy measure beetween 16 and 22 cm c in October (Ben-Tuvia, 1979).

Figure 4.48. Growth of 0+ S. aurata in 1972 1 in the Bardawil lagoon. r and the e numbers The verticcal bars repressent the size ranges abovve are the mea asured counts s (Ben-Tuvia, 1979)

How wever, at the same time, the t size of young y Giltheaad seabream from the Bages-Sigean lagoon is between 144 and 19 cm (40% had a modal m length of 16 cm L (19774a, 1974b, 1976) studied the linear groowth and and weigght of 65g). Lasserre weight of 0+ Thau Gilthead seaabream (size frequency polygon, p 19770–1971). Betweenn May and Juuly, the total length increassed from 4.5 cm c (1 g) to 11 cm TL (16.5 g).. Amanieu annd Lasserre (11973) found, in May–June in the Prévost lagoon (Hérault, France), twoo biometrically distinct po opulations of 0+ Gilthead sseabream, isolated by a current forming a hyydrological bo oundary. Withhin each of thhem, they noted veery rapid flucctuations in sttock, average size and biomass. Dimitriiou et al. (2007) showed s that successful s repproduction off captive Giltthead seabreaam in the Messolonghi-Etoliko lagoon (Greecce) and the esscape of manyy larvae and ppostlarvae o wild birds in this enviironment, resulted in a reductiion in the avverage size of followinng a demograpphic overload.

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Several authors haave studied thhe growth of S. aurata in lagoons and estuaries, dividuals captured at theeir “exit” most freequently usinng scalimetryy. From ind (Octoberr) from the Thhau lagoon, Mathias M and Jallvy (1958) and Audouin (19962) give informattion on their linear l growth and weight for fo age groupss 0+ to 7+–10+. Laurent and Lassserre (1974) are particulaarly interested d in 1+–3+ inndividuals. Taable 4.14 summariizes the availaable data andd shows the ex xceptional groowth of this sspecies in the Melllah lagoon (A Algeria), with a growth perfformance indeex Φ’ = ln K + 2 ln L∞ (Munro and Pauly, 19983) of 7.35 (C Chaoui et al., 2006). The paarameters of thhe length– weight reelationship are also given. The geographical comparison of o these data according too Chaoui et aal. (2006) (Figure 4.49) 4 also higghlights the sppecial case of the Mellah Lagoon. Acccording to Chauvet (1981), there is no differencce in zoogeographic growthh with latitude (northern d bettween open, semi-closed s annd closed zones, soouthern zoness), but only differences environm ments, and betw ween lagoons according to their t degree off eutrophicatioon.

Figure 4.49. Comparative C grrowth of S. aurata in differen nt regions in th he M Mediterranean and Atlantic (Chaoui ( et al., 2006). For a color version of w k/kara/fishes3b b.zip thiss figure, see www.iste.co.uk

Laureent and Lasseerre (1974) haave shown diffferences in thhe growth of 1+, 2+ and 3 indivviduals (year 1971–1972) in favor of those caughtt in the Thaau lagoon compareed to those fouund near to seea (Sète). Lassserre and Labbourg (1974a)) indicate that in thhe fall of 1971, for individuuals aged 1–4 4 years, those from the Thaau lagoon are largeer in size andd mass than thhose caught near n to sea, but b this mass does not differ siggnificantly. +

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Fisshes in Lagoonss and Estuaries in the Mediterra anean 3B

Undeer experimentaal conditions, Laiz-Carrión L et e al. (2005) show s a better ggrowth of juvenile Gilthead seabrream acclimatted to a salinitty of 12‰ forr 100 days com mpared to those maaintained at 6‰ ‰ and 38‰. There T are numeerous hypothesses for these ddifferences in growtth (effect of salinity s on dieet, reorganizatiion of metaboolism at the exxpense of growth, stimulation off growth-relateed osmoregulaatory hormonees, genetic facctors), but none havve been veriffied. Papoutsooglou et al. (2 2008) evaluateed the effect of music (Mozart, K525) on capptive fry (1.51 ± 0.01 g) keptt in a closed looop at 80 and 2200 lx and D the firrst 89 days, music m improveed growth subjectedd to 2 and 4 h of music. During comparedd to ambient-ssounding contrrols. Food intak ke increased when w fish were subjected to 4 h off music and 2000 lx. Accordinng to these auth hors, music afffects different aspects of o plasma andd liver fatty accids, brain fish physsiology (digesttive enzymes, composition of neurotrannsmitters). Thhe sensitivity of Gilthead seabream to music is veerified by Papoutsooglou et al. (22015) in juveeniles (11.2 ± 0.02 g), which respond ddifferently accordingg to the appliedd music (Mozaart, Romanza, Bach). Popuulation structuure and dynam mics: In all Mediterranean M lagoons, wheether deep or laminar, there is reccruitment of postlarvae p or juveniles (0+) from the end of winter to the beeginning of sppring. In deep lagoons, thesee 0+ are accom mpanied by m many older individuaals, while these are absent or rare in thee laminar lagooons. Whateveer the age and physsiological stagge, all individuuals will leave the lagoons in the fall to spawn at sea (aduults) or not (juveniles). (j Soome of them m will return to deep lagooons with neonatess (0+); the lattter enter laminnar lagoons alone. a The reccruitment of ppostlarvae + and juveeniles (0 ) takkes place in February–Mar F rch in the Freench lagoons of Thau, Bages annd Palavas (A Audouin, 1962)); it is the sam me in the Italiaan lagoons off Fogliano and Caprrolace (Marianni, 2006) and in the Bardaw wil lagoon, Egyypt (Ben-Tuviia, 1979). The frequency of individuals and a the numb ber of age grooups that makke up the populatioons vary from m one lagoonn to another. For examplee, in the Foglliano and Caprolacce lagoons, onnly one cohoort (0+) with an a age of lesss than eight m months is present (Mariani, ( 20066) (Figure 4.50).

Figure 4.50 0. Size frequen ncy of S. aura ata in the Italia an lagoons of Fogliano and d Caprolace (M Mariani, 2006))

Sparidae Jordan and Evermann, 1898

231

The average size of the individuals prior to their lagoon exit is significantly different between these two environments, with 20.6 ± 0.9 and 19.4 ± 1.3 cm, respectively (P < 0.001). Also, in the Beymelek Lagoon (Turkey), 94% of the Gilthead seabream captured were less than a year old and only 5% are 1 year old (Emre et al., 2009). A similar situation was described in the Cádiz Estuary, whose population is also composed of a single cohort, aged 1 year, with a size between 18.1 and 28 cm, but with a greater number of individuals with sizes 23–26 cm (180– 220 g) (Arias, 1980). On the other hand, in the Thau lagoon (deep lagoon, marinized), 7–10 age groups are present (Mathias and Jalvy, 1958; Audouin, 1962), with a greater representation of 0+, 1+, 2+ (Audouin, 1962), and 1+, 2+, 3+ (Laurent and Lasserre, 1974). In the Bardawil lagoon, four age groups were identified (BenTuvia, 1979). The population of the Mellah Lagoon (Algeria) is composed of seven age cohorts, with a dominance of groups aged 1 (64.8%) and 2 (18.1%) years (Chaoui et al., 2006). The application of a cohort analysis method to the average catches of a pseudo-cohort (1999–2003) gives average annual recruitment, total abundance and total biomass values of 113,617 fry, 1.57 million individuals and 66.7 tons. This method also estimated the year-to-year changes in stock characteristics from 1999 to 2003. Annual recruitment decreases steadily to 43,107 fry in 2003. The total number of fish in the lagoon follows the same trend, with an 81.8% decrease in 2003 compared to 1999 (Chaoui and Kara, 2011). According to Amanieu and Lasserre (1974), in the Thau lagoon (France) the recruitment of 0+ decreases from 1,188,601 on average for the period from May 26 to June 8, 1971 to an average of 178,290 for the period from 8 to 15 June 1971. Beyond this, the catch per unit of fishing effort decreases considerably. In the Prévost lagoon, these authors estimate the summer stock of juveniles to be between 7,000 and 8,000 individuals. Of the 134 ripe Gilthead seabream caught in December in the Bardawil lagoon, Ben-Tuvia (1979) found: 73.9% females, 24.6% males and 1.5% of indeterminate sex. The sex ratio is balanced (F:M = 1:1.11) both in the Beymelek lagoon, Turkey (Emre et al., 2009), and in the Gulf of Gabes (F:M = 1.18:1) (Hadj-Taieb et al., 2013a). 4.4.1.5. Food and feeding behavior Diet: In the Salses-Leucate lagoon, the 0+ food bolus mainly consisted of crustaceans (88%) and then annelids (Hervé, 1978). In the Thau lagoon, the 0+ consumed mainly annelids, crustaceans, some gastropods and lamellibranchs (Mathias and Jalvy, 1958). Large individuals are very malacophagous and devastate mussel and oyster populations. Rosecchi (1987) studied the diet of S. aurata in the Languedoc lagoons of Prévost and Mauguio and at sea. In the lagoons, where

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individuals measured from 25 to 160 mm, amph hipods represeent 54% of thhe prey in fish 25–50 mm in size and 12.5% for those meaasuring 50–1000 mm. Fish sscales are becominng more abunddant in stomacch contents with increasingg fish size and, in many cases, copepods andd sea lice (C Caligidae) aree associated with these. A Annelids, f 75% of prey p biomass in i S. aurata inndividuals lesss than 50 decapods and scales form mm in siize. Larger inddividuals conssumed mostly y fish and varioous crustaceanns, which made upp 90% of the tootal prey masss (Figure 4.51).

Figure e 4.51. Variatiions in numeri rical (N) and grravimetric (P) percentages of prey i S. aurata sttomach conten in nts with increa asing fish size in Prévost an nd Mauguio la agoons (Rose ecchi, 1985)

At seea, where the individuals i exxamined meassured 100–2855 mm in size, mollusks are by faar the most abbundant (N = 55) and heaviiest (67 g) preey. These molllusks are almost exclusively lam mellibranchs. The other o prey aree mainly polycchaete annelid ds (N = 15, P = 15 g) and decapods (N = 12, P = 16 g). Fissh are rare (N = 2, P = 2 g) and plants aree negligible (N N = 1, P < 0.05 g). Overrall, the diets at sea and in lagoons difffer greatly and a Gilthead seabream seem to prefer being at sea since laamellibranchss and decapodds make up 777% of the total MF FI (Table 4.17)).

Sparidae Jordan and Evermann, 1898

Prey

Lagoons

Preferential prey

42% fish

≥ 50% MFI

17% crustaceans

Secondary prey Other prey

233

Sea 59% lamellibranchs

14% scales

18% decapods

9% amphipods

Other

Other

(plants 0.1%)

Table 4.17. Classification of the main prey of S. aurata as a function of % MFI: comparison between sea and lagoon (Rosecchi, 1987)

However, these differences lessen when small size classes alone are considered. It is important to note that in the Prevost and Mauguio lagoons, Gilthead seabream consume no shellfish and fish make up 78% of the biomass ingested. The situation is certainly different in the Thau lagoon since this species causes devastation to mussel beds. This is also the case in the Mellah lagoon, where Gilthead seabream (15.7–61 cm TL) feed mainly on bivalve mollusks and teleost fish, which together with thallophytic plants constitute the majority of their diet (Table 4.18) (Chaoui et al., 2005). Ferrari and Chieregato (1981) indicate that the Gilthead seabream feed on polychaetes and gastropods in the Pô Delta. At sea, in Posidonia meadows in the Marseille region, they have a balanced diet comprising polychaetes and amphipods (Bell and Harmelin-Vivien, 1983). In the Gulf of Gabes (Tunisia), S. aurata (10.1–35 cm TL) feeds mainly on arthropods (Pinnotheridae, Dorippidae, Homolidae, Penaeidae) (RII = 51.71%) and mollusks (RII = 43.74%) (Hadj-Taieb et al., 2013b). Other dietary patterns are described at sea, in the Mediterranean and in the Atlantic (Xhuvelaj, 1959; Suau and Lopez, 1976; Chieregato et al., 1979; Ramos and Kobayashi, 1981; Pita et al., 2002), suggesting that Gilthead seabream is an opportunistic predator. Items Crustaceans Brachyura Cirripedia Amphipods Isopods Unspecified Caridea

Cn (%)

Cp (%)

F (%)

Q

< 0.5 0.5 20.1 4.5 < 0.5

1.4 < 0.5 0.5 < 0.5 4.1

2.0 5.7 14.0 9.3 1.3

0.5 < 0.5 11.1 0.5 0.8

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

Mollusks Bivalves Gastropods

20.6 18.8

23.5 1.9

35.5 10.7

485.6 36.0

Fish

10.0

26.1

59.4

262.3

Polychaetes

4.3

3.81

15.4

16.6

< 0.5 1.3

0 < 0.5

1.34 2.01

0 < 0.5

7.9 2.2

22.1 0.5

36.9 14.0

176.3 1.1

Echiurans

< 0.5

1.3

2.0

0.5

Sponges

< 0.5

< 0.5

0.6

< 0.5

Anthozoans

4.0

2.3

8.0

9.3

Unidentified prey

3.1

9.9

19.4

-

Echinoderms Echinoids Ophiuroids Plants Thallophytes Macrophytes

Table 4.18. Qualitative and quantitative composition of S. aurata diet in Mellah lagoon (Chaoui et al., 2005)

Dietary variations and patterns: Tancioni et al. (2003) compared the feeding of juveniles, subadults and adults of S. aurata in two adjacent lagoons in the Tyrrhenian Sea (Fogliano and Caprolace). In addition to the intralagunal variations in diet as a function of the fish growth; there is also evidence of interlagoon differences, but with the exception of juveniles that feed on nematodes, copepods, ostracods and polychaete larvae in both cases. Indeed, in Fogliano the adult diet is composed of bivalves and Carcinus aestuarii, while in Caprolace prey are more diverse (15 vs. 10) and include C. aestuarii, polychaetes (errant and sedentary), amphipods and other decapod crustaceans; the consumption of bivalves is very small. Feeding activity of the Gilthead seabream S. aurata in the Mellah lagoon (Algeria) has monthly fluctuations that highlight a seasonal feeding pattern, characterized by intense trophic activity in fall and a short period of fasting in winter. These events largely determine the monthly changes in the K coefficient condition. The latter shows significant differences between juveniles and adults, especially after reaching first sexual maturity (Chaoui et al., 2005). In the Gulf of

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Gabes, the t mean annuual stomach vacuity v index x is 56.81% and a varies signnificantly with tim me. The qualittative and quuantitative anaalyses of the diet reveal siignificant variationns according too sex, size andd seasons (Haadj-Taieb et all., 2013b). Russo et al. (20007) distinguuished morph hological staages during ontogeny correspoonding to diffe ferent trophic stages. Accorrding to ecom morphological analysis, the earlyy stages of deevelopment arre characterizeed by organoggenesis of sennsory and respiratoory organs, mouth m enlargeement and caaudal fin devvelopment, whhile later stages are a optimizedd to allow feeding on hard prey, improving sw wimming performaance and reduucing predationn risk (Figure 4.52).

Figure e 4.52. Link be etween morph hological stage es and trophicc stages in S. aurata: (•) recen ntly hatched la arvae, ( ) you ung larvae, (○)) preflexion la arvae, (-) flexio on larvae, (∆) older larvae („) young juve eniles, (#) juve eniles, (¤) sub badults and ad dults. Changes in diet are ind dicated by arro ows (Russo ett al., 2007)

4.4.1.6. Reproductio on and repro oductive beha avior Sexuaality: A descrription of the gonads is giv ven by Zohar et al. (1984). Gilthead seabream m are protanndric hermapphrodites (D D’Ancona, 19941; Pasqualli, 1941; Reinbothh, 1962; Ariass, 1980; Chaouui et al., 2006 6; Hadj-Taieb et al., 2013a).. The size frequenccy distributionn according to t the differeent sexual staates (juvenilees, males, females)) is bimodal, males havingg the smallest sizes and a sex s ratio in thheir favor (Figure 4.53). 4

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Fisshes in Lagoonss and Estuaries in the Mediterra anean 3B

Figure 4.53. 4 Frequenccy of the different sexual sttages accordin ng to the totall length of S. aurata a in the Mella ah lagoon duriing the month hs of Novembe er and Decem mber. The first line of numbers at a the top of th he table show ws the numberr of individualss (Chaoui et al., 20 006)

In caaptivity, Zoharr et al. (1978) monitored go onad developm ment up to twoo years of age. For individuals up u to eight moonths, the gon nad is bisexuall with a prepoonderance of the ovvarian componnent in the doorsal position. On reaching their first reproductive season (end ( of the first f year), the testicular component, c inn the ventral position, proliferaates and form ms a mature teesticle. At thee end of the first breedingg season, sexual innversion begins to occur in all indiviiduals. At 177 months, one of two situationns occur: in abbout 80% of individuals, i th he process off sexual inverssion ends and givees rise to femaales; in the rem maining indiv viduals (20%),, the inversionn remains incompleete and development continnues as male.. A similar sccenario is desccribed by Ben-Tuvvia (1979) in the t Bardawil Lagoon. L This author reportss the case of a Gilthead seabream m caught in February F on its i return mig gratory route, at the entrannce to the lagoon, with w traces off both mature sperm s and ooccytes in the goonads. Firstt sexual maturity: The sizee of males at first sexual maturity is reeached at 32.6 cm m TL in the Mellah M lagoonn (Algeria), i.e. i at an agee of about 188 months (Chaoui et al., 2006). In the Ebro Delta D (Spain),, males are tw wo years old (Suau and Lopez, 1976). 1 Femalees in the Beym melek Lagoon n (Turkey) are mature at 28.5 cm TL

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(Emre et al., 2009). In the Gulf of Gabes (Tunisia), 50% of males are mature at 17.63 cm (Hadj-Taieb et al., 2013a). Sexual inversion usually begins one year after the onset of sexual activity in males (D’Ancona, 1941; Lasserre, 1976), but D’Ancona (1941) and Bruslé-Sicard and Fourcault (1997) consider the possibility of a later sexual inversion. Chaoui et al. (2006) confirm this hypothesis, since only 40% of Mellah lagoon specimens change sex at the end of the second year, from size class 43–45 cm (Figure 4.53). In the Beymelek Lagoon (Turkey), sexual inversion occurs in the size range 24–26 cm TL and all individuals larger than 34 cm are female (Emre et al., 2009). In the Cadiz Estuary, all individuals aged one and two years (21–36 cm) are male. The latter represent 84.3% and 12.1%, respectively, at three and four years. Beyond this, up to seven years (50.3–57 cm), all the Gilthead seabream are female (Arias, 1980). On the Catalan coast, all fish between 14 and 21 cm are male; beyond 46 cm they are exclusively female (Suau and Lopez, 1976). In the Gulf of Gabes, 50% of males undergo sexual inversion at 18.75 cm TL (Hadj-Taieb et al., 2013a). Spawning site and period: Spawning is coastal, but the sites have not yet been properly identified. S. aurata females are known to not spawn in the Cadiz estuary (Arias 1980). The maturation of their gonads remains blocked at stage IV (maturation). The author questions the temperature and salinity conditions of their environment. In both the Mediterranean and the Atlantic, spawning takes place at sea from October to January–February. The maximum GSI values upon exit of the lagoons are reached in December–January for Gilthead seabream in the Thau, Prévost (Lasserre, 1976), Mellah (Chaoui et al., 2006) and Beymelek (Emre et al., 2009) lagoons, Cadiz estuary (Arias, 1980) and Gulf of Gabès (Hadj-Taieb et al., 2013a). It extends from November to February for the Bardawil lagoon (Ben-Tuvia, 1979). Dimitriou et al. (2007) suspect successful reproduction of captive Gilthead seabream at the entrance to the Messolonghi-Etoliko lagoon in Greece. Having not yet been marketed, these fish remain in cages where they will have reached sexual maturity and spawned; spawning in certain lagoons thus cannot be excluded. Fecundity: We did not find data on the fecundity of Gilthead seabream in the wild. In captivity, Zohar et al. (1984) state that its relative value can reach (1,222 million eggs per kilogram of female. Reproductive behavior: Gilthead seabream spawning seems to be influenced by the lunar cycle. Saavedra and Pousao-Ferreira (2006) monitored two females reared in the lagoon for four months, from January to May 2003. During this period, a peak

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in egg emission is observed during the full moon. Out of a total of 8,644 g and 5,653 g of eggs released by each female, respectively, 4,535 g corresponds to the full moon and 2,882 g to the new moon. Meiri et al. (2002) have shown that the suppression of males in spawning lagoons causes atresia of the oocytes in females and the continuous but infrequent emission of small quantities of eggs for seven weeks. In these females, a decrease in the level of GnRHs and βLH was observed compared to controls in the company of males. In contrast, βFSH levels were higher. This implies the existence of an endocrine response to sociosexual stimuli during reproduction. Eggs, larvae and ontogenesis: Lo Bianco (1909), Bounhiol and Pron (1916), Ranzi (1930, 1933) and Vodyanitzky and Kazanova (1954) provide information on eggs and larvae of S. aurata. Ranzi (1933) summarizes current research at the time and shows the development of postlarvae between 13 and 98 mm in length. The eggs are spherical and pelagic, less than 1 mm in diameter, and contain a single oil globule. Kamaci et al. (2005) monitored the stages of embryonic development in this species from egg fertilization (Figure 4.54(a)) to hatching (Figure 4.54(b)), incubated at 18.5 °C, with a salinity of 36.6–37.4‰ and an oxygen content of between 6.6 and 7.8 mg/L. The first cell division takes place 1.5 h after fertilization and the morula stage is reached after 4.15 h. The gastrula stage is determined after 12 h and after 16 h the neurula stage is clearly apparent. The embryo is visible after 18 h and becomes pigmented after 21 h. Thirty-two hours later, the primordial fin begins to form, and after 51 h, the larvae hatch. The average size on hatching is 2.68 ± 0.27 mm (n = 62; 2.41–3.06 mm) at 17–19°C and 37‰ (Saka et al., 2008). The planktonic larval stage lasts around 50 days at 17–18°C (Crosetti et al., 2014).

Figure 4.54. (a) Fertilized egg after 1 h 15 and (b) larva at eclosion of captive S. aurata (Kamaci et al., 2005)

Russo et al. (2007) describe the evolution in the body shape of captive S. aurata, from hatching to adulthood (4–461 days post-hatching; 3.50–235.6 mm TL). They differentiate the morphological stages during ontogenesis. The evolution in body shape is rapid in small individuals and decreases when growth reaches stability at 70 mm TL.

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4.4.1.7. Economic importance Marketed fresh, chilled or frozen, Gilthead seabream is very popular. It is used for semi-industrial, artisanal or recreational fishing using beach seines and sliding seines, trawls, gillnets, bottom longlines, traps, lines and dams in the case of lagoons. The quantity fished overall is between 5,123 and 9,564 tons between 1985 and 2007. Mediterranean captures accounted for 65% (4,794 tons) of the total production in 2007, which amounted to 7,361 tons. The main producing countries are Egypt (1,367 tons), Spain (955 tons), Turkey (759 tons) and Tunisia (695 tons). The natural mortality values (M = 0.91) and fishing (F = 0.35) coefficients, determined for the Mellah lagoon Gilthead seabream population, gave an exploitation rate of E = 0.28, indicating an underexploitation of the present stock (Chaoui and Kara, 2011). Also, a drop in the yield of Gilthead seabream was found in this lagoon between 1999 (160 kg/ha/year) and 2003 (29 kg/ha/year). A more restricted connection with the sea may explain this trend (Chaoui and Kara, 2011). According to Hadj Taieb et al. (2014), the biomass of Gilthead seabream from the Gulf of Gabes (about 850 tons) is overexploited (E = 0.61), which is also the case (E = 0.69) in Güllük Bay in the Aegean Sea (Akyol and Gamsiz, 2011). In the Italian lagoons of Fogliano and Caprolace, the Gilthead seabream represent 75% and 43% of the Sparidae caught (Mariani, 2006) and 92.2% in the Beymelek lagoon in Turkey (Emre et al., 2009). In this lagoon, it amounts to 38% of total catches (Balik et al., 2011) and 15% in the Ghar El Melh lagoon in Tunisia (Kraiem et al., 2009). In the Homa lagoon (Turkey), the annual production of Gilthead seabream is about 25 tons per year (Cataudella and Ferlin, 1984). In the Messolonghi lagoon (Greece), cage culture induced an 80% increase in the yield of Gilthead seabream fishing in this environment over five years (Dimitriou et al., 2007). This increase is certainly due to the high escape rate from intralagoon farms and perhaps the fact that the captive, non-commercialized individuals have reached the age and size required for sexual maturity and have been able to spawn. This untimely rearing has led to an increase in the population density within the lagoon, resulting in a decrease in the average size of individuals less than one year old (trophic competition) (Dimitriou et al., 2007). Today, Gilthead seabream is produced extensively, semi-intensively in lagoons and intensively in lagoons and cages. It is traditionally the subject of semi-extensive farming in the Italian valli north of the Adriatic and in Egyptian hosha. The repopulation of these habitats was based on wild larvae and juveniles that were subject to special fishing conditions. The deficiency in this resource for the development of intensive farms has led to the development of hatcheries. Currently, it is the latter that provide fry to farms and some lagoons. Since 1994, more than

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1,100,000 juveniles have been introduced in different Greek lagoons (Dimitriou, 2000). In the Orbetello lagoon (central Italy), restocking with hatchery fry began in 1995 and production multiplied by nine between 1995 and 20003. The overall production of farmed Gilthead seabream has evolved rapidly from 564 tons in 1985 to 125,355 tons in 2007, 101,000 tons of which was from the Mediterranean at the time. The main producing countries are Greece (50,000 tons), Turkey (33,500 tons) and Italy (8,200 tons). Extensive and semiextensive traditional fishing persist, but have a small impact on the markets. In 2007, lagoon production totaled 2,282 tons, of which nearly 50% (1,181 tons) came from Italy. Greece and Tunisia also contribute to this production. 4.4.1.8. Protection status and conservation According to the European Union legislation, dated December 21, 2006, the capture of any individual less than 20 cm or 23 cm in France (JO 06/11/2012) is prohibited, regardless of the technique used. – IUCN Global Red List: LC. – IUCN Mediterranean Red List: LC. 4.5. Bibliography ABECASIS D., ABECASIS A.R.C., “ First report of cleaning behavior in white seabream (Diplodus sargus) ”, Marine and Freshwater Behavior and Physiology, 48 (1): 71–75, 2015. ABECASIS D., AFONSO P., ERZINI K., “Changes in movements of white seabream (Diplodus sargus) during the reproductive season”, Estuarine, Coastal and Shelf Science, 167: 499–503, 2015. ABELLAN E., GARCIA-ALCAZAR A., “Pre-growout and growout experiences with white seabream (Diplodus sargus sargus, Linnæus, 1758) and sharpsnout seabream (Diplodus puntazzo, Cetti, 1977)”, Cahiers Options Méditerranéennes, 16: 57–63, 1995. ACARLI D., KARA A., BAYHAN B., “Length–weight relation for 29 fish species from Homa lagoon, Aegean Sea, Turkey”, Acta Ichthyologica et Piscatoria, 44 (3): 249–257, 2014. AKAZAKI M., “Specific divergence of spariform fishes when considered from their geographical distribution”, Honyuruikagaku, 20–21: 131–146, 1970. 3 See http://genimpact.imr.no/data/page/7650/gilthead_seabream.pdf.

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AKYOL O., GAMSIZ K., “Age and growth of adult gilthead seabream (Sparus aurata L.) in the Aegean Sea”, Journal of the Marine Biological Association of the United Kingdom, 91 (6): 1255–1259, 2011. ALARCÓN J.A., MAGOULAS A., GEORGAKOPOULOS T., ZOUROS E., ALVAREZ M.C., “Genetic comparison of wild and cultivated European populations of the gilthead seabream (Sparus aurata)”, Aquaculture, 230 (1–4): 65–80, 2004. ALKALIN S., “Izmir Körfezi’nde isparoz baliğinin (Diplodus annularis L., 1758) beslenme rejimi üzerine arastirmalar”, Y.L. Tezi, Izmir, Turkey, 1996. ALONSO-FERNÁNDEZ A., ALÓS J., GRAU A., DOMINGUEZ-PETIT R., SABORIDOREY F., “The use of histological techniques to study the reproductive biology of the hermaphroditic Mediterranean fishes Coris julis, Serranus scriba, and Diplodus annularis”, Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science, 3 (1): 145–159, 2011. ALÓS J., CABANELLAS-REBOREDO M., MARCH D., “Spatial and temporal patterns in the movement of adult two-banded seabream Diplodus vulgaris (Saint-Hilaire, 1817)”, Fisheries Research, 115: 82–88, 2012. ALÓS J., PALMER M., ALONSO-FERNÁNDEZ A., MORALES-NIN B., “Individual variability and sex-related differences in the growth of Diplodus annularis (Linnæus, 1758)”, Fisheries Research, 101: 60–69, 2010. ALTIN A., ÖZEN O., AYYILDIZ H., AYAZ A., “Feeding habits and diet overlap of juveniles of two sparids, Diplodus puntazzo (Walbaum, 1792) and Diplodus vulgaris (Geoffroy Saint-Hilaire, 1817), from the North Aegean Sea of Turkey”, Turkish Journal of Zoology, 39: 80–87, 2015. AMANIEU M., “Écologie et exploitation des étangs et lagunes saumâtres du littoral français”, Annales de la Société royale zoologique de Belgique, 103 (1): 79–94, 1973. AMANIEU M., LASSERRE G., “Stock et biomasse des daurades 0+ de l’étang du Prévost à Palavas (Hérault, France)”, Bulletin d’écologie, 4 (2): 132–143, 1973. AMANIEU M., LASSERRE G., “Biomasse et taux de charge des daurades juvéniles. Comparaison entre étangs atlantiques et méditerranéens”, Bulletin UOF, 6 (2): 29–34, 1974. ANATO C.B., KTARI M.H., “Reproduction de Boops boops (Linné, 1758) et de Sarpa salpa (Linnè, 1758), poissons téléostéens, sparidés du golfe de Tunis”, Bulletin de l’Institut national scientifique et technique d’océanographie et de pêche, Salammbô, 10: 49–53, 1983.

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ANATO C.B., KTARI M.H., KAMOUN M.N., “La bogue et la saupe dans les pêcheries tunisiennes”, Bulletin de l’Institut national scientifique et technique d’océanographie et de pêche, Salammbô, 10: 99–106, 1983. ANTOLIC B., SKARAMUCA B., SPAN A., MUSIN D., SANKO-NJIRE J., “Food and feeding habits of a herbivore fish Sarpa salpa (L.) (Teleostei, Sparidae) in the Southern Adriatic (Croatia)”, Acta Adriatica, 35 (1–2): 45–52, 1994. ARCULEO M., LO BRUTTO S., SIRNA-TERRANOVA M., MAGGIO T., CANNIZZARO L., PARRINELLO N., “The stock genetic of two Sparidae species, Diplodus vulgaris and Lithognathus mormyrus, in the Mediterranean Sea”, Fisheries Research, 53: 339–347, 2003. ARIAS A., “Crecimento, regimen alimentarion y reproduccion de la dorada (Sparus aurata L.) y del robalo (Dicentrarchus labrax L.) en los esteros de Cádiz”, Investigacion Pesquera, 44: 59–83, 1980. ARIAS E., MORALES E., “Estudio electroforético comparative de las proteinas del sarcoplasma de Sarpa salpa y Boops boops”, Investigacion Pesquera, 44 (1): 35–41, 1980. ARNAL J., ALCAZAR A.G., ORTEGA A., “Observaciones sobre el crecimento de la dorada (Sparus aurata L.) en el Mar Menor (Murcia)”, Boletín del Instituto Español de Oceanografía, 221–222: 1–17, 1976. ATHANASSOPOULOU F., PRAPAS T., RODGER H., “Diseases of Puntazzo puntazzo Cuvier in marine aquaculture systems in Greece”, Journal of Fish Diseases, 22: 215–218, 1999. AUDOUIN J., “La daurade de l’étang de Thau Chrysophrys aurata (Linné)”, Revue des travaux de l’Institut des pêches maritimes, 26 (1): 105–126, 1962. AYYILDIZ H., OZEN O., ALTIN A., “Growth, mortality and hatch-date distributions of striped seabream Lithognathus mormyrus inhabiting the Canakkale Strait, Turkey”, Journal of the Marine Biological Association of the United Kingdom, 94 (3): 607–613, 2014. AYYILDIZ H., OZEN O., ALTIN A., Daily growth rates and hatch date distributions of common two-banded seabream, Diplodus vulgaris inhabiting the Canakkale shallow waters of Turkey”, Journal of the Marine Biological Association of the United Kingdom, 95 (1): 185–191, 2015. BALART E.F., PÉREZ-URBIOLA J.C., CAMPOS-DÁVILA L., MONTEFORTE M., “On the first record of a potentially harmful fish, Sparus aurata in the Gulf of California”, Biological Invasions, 11: 547–550, 2008.

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BALIK I., EMRE Y., SUMER C., TAMER F.Y., “Spatial and temporal variations and assemblage structure of fish species in Beymelek lagoon, Turkey”, Journal of Applied Ichthyology, 27 (4): 1023–1030, 2011. BÂNÂRESCU P., Fauna republicii populare romine (Pisces-Osteichthyes), Editura Academiei Republicii Populare Române, Bucharest, 1964. BARGELLONI L., ALARCON J.A., ALVAREZ M.C., PENZO E., MAGOULAS A., REIS C., PATARNELLO T., “Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic–Mediterranean divide”, Journal of Evolutionary Biology, 16: 1149–1158, 2003. BARGELLONI L., ALARCO J.A., ALVAREZ M.C., PENZO E., MAGOULAS A., PALMA J., PATARNELLO T., “The Atlanto–Mediterranean transition: dicordant genetic patterns in two seabream species, Diplodus puntazzo (Cetti) and Diplodus sargus (L.)”, Molecular Phylogenetics and Evolution, 36: 523–535, 2005. BASAGLIA F., MARCHETTI M.G., “A comparative study of some soluble proteins of the genus Diplodus (Sparidae: Teleostei) (1990)”, Comparative Biochemistry and Physiology – Part B: Biochemistry and Molecular Biology, 95 (4): 653–656, 1990. BASAGLIA F., MARCHETTI M.G., SALVATORELLI G., “Genetic, developmental and comparative analysis of LDH, MDH and GPI isozymes in the sheepshead bream (Diplodus puntazzo GM)”, Comparative Biochemistry and Physiology – Part B: Biochemistry and Molecular Biology, 96 (2): 257–266, 1990. BAUCHOT M.L., “Poissons osseux”, in W. FISCHER, M.L. BAUCHOT, M. SCHNEIDER (eds), Fiches FAO d’identification des espèces pour les besoins de la pêche. Méditerranée et mer noire – Zone de pêche 37, vol. 2. Vertébrés, p. 891–1421, FAO-CEE, Rome, 1987. BAUCHOT M.L., HUREAU J.C., “Sparidae”, in P.J.P. WHITEHEAD, M.L. BAUCHOT, J.C. HUREAU, J. NIELSEN, E. TORTONESE (eds), Fishes of the North-Eastern Atlantic and the Mediterranean (FNAM), Paris, 2: 883–907, 1986. BAUCHOT M.L., HUREAU J.C., “Sparidae”, in J.C. BY, J.C. QUERO, J.C. HUREAU, C. KARRER, A. POST, L. SALDANHA (eds), Checklist of the Fishes of the Eastern Tropical Atlantic, Catalogue des poissons de l’Atlantique tropical oriental (Clofeta), Paris, 31: 790–812, 1990. BAUCHOT M.L., PRAS A., Guide des poissons marins d’Europe, Delachaux and Niestlé, Paris, 1980. BAYHAN B., KARA A., “Length–weight and length–length relationships of the Salema Sarpa salpa (Linnæus, 1758) in Izmir Bay (Aegean Sea of Turkey)”, Pakistan Journal of Zoology, 47 (4): 1141–1146, 2015.

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BELL J.D., HARMELIN-VIVIEN M.L., “Fish fauna of French mediterranean Posidonia oceanica seagrass meadows. 2. Feeding habits”, Tethys, 11 (1): 1–14, 1983. BELLASSOUED K., HAMZA A., ABDELMOULEH A., MAKNI F.A., VAN PELT J., ELFEKI A., “Toxicity assessment of dreamfish Sarpa salpa from the gulf of Gabes (Tunisia, Eastern Mediterranean Sea)”, Journal of Food Agriculture and Environment, 10 (2): 1308–1313, 2012a. BELLASSOUED K., HAMZA A., VAN PELT J., ELFEKI A., “Evaluation of cytotoxic compounds in different organs of the seabream Sarpa salpa as related to phytoplancton consumption: an in vitro study in human liver cell lines HepG2 and WRL68”, In Vitro Cellular & Developmental Biology – Animal, 48 (8): 528–534, 2012b. BELLASSOUED K., MAKNI-AYADI F., VAN PELT J., ELFEKI A., “Hepatotoxicity in rats induced by the poisonous dreamfish (Sarpa salpa)”, Toxicology Mechanisms and Methods, 24 (2): 151–160, 2014. BELLASSOUED K., VAN PELT J., ELFEKI A., “Neurotoxicity in rats induced by the poisonous dreamfish (Sarpa salpa)”, Pharmaceutical Biology, 53 (2): 286–295, 2015. BEN SLIMEN H., GUERBEJ H., BEN OTHMEN A., OULD BRAHIM I., BLEL H., CHATTI N., EL ABED A., SAID K., “Genetic differentiation between populations of gilthead seabream (Sparus aurata) along the Tunisian coast”, Cybium, 28 (1): 45–50, 2004. BEN-TUVIA A., “Studies of the population and fisheries of Sparus aurata in the Bardawil lagoon, Eastern Mediterranean”, Investigacion Pesquera, 43 (1): 43–67, 1979. BENCHALEL W., DERBAL F., KARA M.H., “Régime alimentaire du sar commun Diplodus sargus sargus (Sparidae) des côtes de l’Est algérien”, Cybium, 34 (3): 231–242, 2010. BENCHALEL W., KARA M.H., “Biométrie et dimorphisme sexuel du sar commun Diplodus sargus sargus (Sparidae) des côtes de l’Est algérien”, Bulletin de la Société zoologique de France, 135 (3–4): 149–162, 2010. BENCHALEL W., KARA M.H., “Age, growth and reproduction of the white seabream Diplodus sargus sargus (Sparidae) off eastern coast of Algeria”, Journal of Applied Ichthyology, 29: 64–70, 2013. BESSEAU L., Étude histo-cytologique de la structure sexuelle d’une population de Lithognathus mormyrus (L.) (téléostéen sparidé), Report, Commission internationale pour l’exploration scientifique de la mer Méditerranée (CIESM), 32: 262, 1990.

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BESSEAU L., “Sex-inversion in a protandric hermaphrodite Lithognathus mormyrus (L 1758) (Teleostei, Sparidae). Histo-cytological peculiarities”, Proceedings of the Fourth International Symposium on the Reproductive Physiology of Fish, University of East Anglia, Norwich, United Kingdon, 1991. BIAGI F., GAMBACCINI S., ZAZZETTA M., “Settlement and recruitment in fishes: the role of coastal areas”, Italian Journal of Zoology, 65: 269–274, 1998. BINI G., “Atlante dei pesci delle coste italiane”, Mondo Sommerso, 9 (8): 58–75, Sirio Edizioni, Rome, 1968. BIZSEL C., KARA M.H., POLLARD D., YOKES B., GOREN M., FRANCOUR P., “Diplodus vulgaris”, The IUCN Red List of Threatened Species, 2014–3, available at: www.iucnredlist.org, accessed 23 November 2014. BODINGTON P., “Enterprise experiences in the culture of new sparids”, in B. BASURCO, M. PEDINI (eds), Cahiers Options Méditerranéennes. Marine Aquaculture Finfish Species Diversification, CIHEAM, 47: 135–139, Zaragoza, 2000. BODINIER C., SUCRE E., LECURIEUX-BELFOND L., BLONDEAU-BIDET E., CHARMANTIER G., “Ontogeny of osmoregulation and salinity tolerance in the gilthead seabream Sparus aurata” , Comparative Biochemistry and Physiology – Part A: Molecular & Integrative Physiology, 157 (3): 220–228, 2010. BOUNHIOL J.B., PRON L., “La précocité sexuelle et les conditions thermiques de la ponte chez quelques Sparidés communs d’Algérie”, Comptes rendus des séances de la Société de biologie et de ses filiales, Paris, 79: 140–143, 1916. BRADAI M.N., Diversité du peuplement ichtyque et contribution à la connaissance des sparidés du golfe de Gabès, Science PhD thesis, Université de Sfax, 2000. BREDER C.M., ROSEN D.E., “Modes of reproduction in fishes”, American Museum of Natural History, New York, 462: 85, 1966. BRUSLÉ-SICARD S., FOURCAULT B., “Recognition of sex-inverting protandric Sparus aurata: ultrastructural aspects”, Journal of Fish Biology, 50: 1094–1103, 1997. BUEN F. DE, “Formas ontogenicas de peces (nota primera)”, Notas y resúmenes – Instituto Español de Oceanografía, 2 (57): 38, 1932. CABALLERO C., CASTRO-HDEZ J.J., “Effect of competitor density on the aggressiveness of juvenile white seabream (Diplodus sargus cadenati de la Paz, Bauchot and Daget, 1974)”, Aggressive Behavior, 29: 279–284, 2003. CASTRO J.J., SANTIAGO J.A., “The influence of food distribution on the aggressive behaviour of juvenile white-seabream (Diplodus sargus cadenati de la Paz, Bauchot and Daget, 1974)”, Aggressive Behavior, 24: 379–384, 1998.

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CATAUDELLA S., FERLIN P., “Aspects of simple technology in the management of fishery resources and the development of aquaculture in lagoons”, Management of Coastal Lagoon Fisheries, Études et Revues de la FAO/CGPM, 61 (2): 568–591, 1984. CATAUDELLA S., PERIN-RIZ P., SOLA L., “A chromosome study of eight Mediterranean species of Sparidae (Pisces, Perciformes)”, Genetica, 54: 155–159, 1980. CEBRIAN J., DUARTE C.M., MARBA N., ENRIQUEZ S., GALLEGOS M., OLESEN B., “Herbivory on Posidonia oceanica: magnitude and variability in the Spanish Mediterranean”, Marine Ecology Progress Series, 30: 147–155, 1996. CETINIĆ P., SOLDO A., DULČIĆ J., PALLAORO A., “Specific method of fishing for Sparidae species in the eastern Adriatic”, Fisheries Research, 55 (1–3): 131–191, 2002. CHAINE J., “Recherches sur les otolithes des poissons”, Actes de la Société linnéenne de Bordeaux, 89: 1–252, 1937. CHANET B., DETTAI A., “Presence of juvenile Diplodus sargus on the seashore of North Brittany (France)”, Cybium, 32 (4): 339–340, 2008. CHAOUCH H., BEN ABDALLAH-BEN HADJ HAMIDA O., GHORBEL M., JARBOUI O., “Reproductive biology of the annular seabream, Diplodus annularis (Linnæus, 1758), in the Gulf of Gabes (Central Mediterranean)”, Journal of Applied Ichthyology, 29 (4): 796–800, 2013. CHAOUCH H., BEN ABDALLAH-BEN HADJ HAMIDA O., GHORBEL M., JARBOUI O., “Feeding habits of the annular seabream Diplodus annularis (Linnæus, 1758) (Pisces; Sparidae), in the Gulf of Gabes (Central Mediterranean)”, Cahiers de Biologie Marine, 55 (1): 13–19, 2014. CHAOUCH H., BEN ABDALLAH-BEN HADJ HAMIDA O., GHORBEL M., JARBOUI O., “Diet composition and food habits of Diplodus puntazzo (Sparidae) from the Gulf of Gabes (Central Mediterranean)”, Journal of the Marine Biological Association of the United Kingdom, 93 (8): 2257–2264, 2013. CHAOUI L., L’ichtyofaune de la lagune du Mellah. Biologie, génétique et exploitation de la daurade Sparus aurata (L., 1758), PhD thesis, Université d’Annaba, 2007. CHAOUI L., DERBAL F., KARA M.H., QUIGNARD J.P., “Alimentation et condition de la dorade Sparus aurata (Teleostei : Sparidae) dans la lagune du Mellah (Algérie nord-est)”, Cahiers de Biologie Marine, 46: 221–225, 2005. CHAOUI L., GAGNAIRE P.A., GUIGNAND B., QUIGNARD J.P., KARA H., BONHOMME F., “Microsatellite length variation in candidate genes correlates with habitat in the gilthead seabream Sparus aurata” , Molecular Ecology, 21: 5497–5511, 2012.

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CHAOUI L., KARA M.H., “Évaluation et diagnostic par l’approche structurale de la population de daurades Sparus aurata (L. 1758) dans la lagune du Mellah”, Revue d’écologie – la Terre et la Vie, 66: 135–144, 2011. CHAOUI L., KARA M.H., FAURE E., QUIGNARD J.P., “Growth and reproduction of the gilthead seabream Sparus aurata in Mellah lagoon (Algeria north-eastern)”, Scientia Marina, 70 (3): 545–552, 2006. CHAOUI L., KARA M.H., QUIGNARD J.P., FAURE E., BONHOMME F., “Forte différenciation génétique de la daurade Sparus aurata (L., 1758) entre les deux rives de la Méditerranée occidentale”, Comptes Rendus Biologies, 332: 329–335, 2009. CHAOUI L., QUIGNARD J.P., KARA M.H., Différenciation morphologique de deux populations marine et lagunaire de daurade Sparus aurata (Linné, 1758), Report, Commission internationale pour l’exploration scientifique de la mer Méditerranée (CIESM), 36: 37, 2001. CHAUVET C., Comparaison de la croissance de huit populations méditerranéennes de la daurade Sparus aurta L. 1758 (Pisces, Sparidae), Report, 27 (5): 197–108, 1981. CHAUVET C., LASSERRE G., BACH P., BESSAU L., “Résultats d’une expérience de marquage de trois espèces de poissons côtiers du Golfe du Lion : Dicentrarchus labrax, Sparus aurata et Liza aurata”, Cybium, 16 (1): 3–11, 1992. CHEVALDONNE P., “Ciguatera and the saupe, Sarpa salpa (L.) in the Mediterranean: a possible misinterpretation”, Journal of Fish Biology, 37: 503–504, 1990. CHIBA S.N., IWATSUKI Y., YOSHINO T., HANZAWA N., “Comprehensive phylogeny of the family Sparidae (Perciformes: Teleostei) inferred from mitochondrial gene analyses”, Genes & Genetic Systems, 84: 153–170, 2009. CHIERAGATO A.R., FERRARI I., ROSSI R., “Il regime alimentare degli stadi giovanile di orata, branzino botolo e lotregano nella sacca di scardovari”, Atti della Società Toscana di Scienze Naturali, 86, 1979. CHRISTENSEN M.S., “Trophic relationships in juveniles of three species of sparid fishes in the South African marine littoral”, Fishery Bulletin, 76: 389–401, 1978. ÇOBAN D., SUZER C., YILDIRIM S., SAKA S., FIRAT K., “Morphological development and allometric growth of Sharpsnout Seabream (Diplodus puntazzo) larvae”, Turkish Journal of Fisheries and Aquatic Sciences, 12: 883–891, 2012. CRAIG G., PAYNTER D., COSCIA I., MARIANI S., “Settlement of gilthead seabream Sparus aurata L. in a southern Irish Sea coastal habitat”, Journal of Fish Biology, 72: 287–291, 2008.

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SAKA S., COBAN D., KAMACI H.O., SUZER C., FIRAT K., “Early development of cephalic skeleton in hatchery-reared gilthead seabream, Sparus aurata”, Turkish Journal of Fisheries and Aquatic Sciences, 8: 341–345, 2008. SALA E., BALLESTEROS E., “Partitioning of space and food resources by three fish of the genus Diplodus (Sparidae) in a Mediterranean rocky infralittoral ecosystem”, Marine Ecology Progress Series, 152 (1–3): 273–283, 1997. SALEKHOVA L.P., “Hermaphrodisme chez Diplodus annularis”, Trudy Sevastopol’skoi Biologicheskoi Stantsii Station, 14: 257–268, 1961. SALEKHOVA L.P., “Composition d’âge des populations de Diplodus annularis”, Soviet Journal of Marine Biology, 38: 46–55, 1976. SÁNCHEZ-JEREZ P., GILLANDERS B.M., RODRIGUEZ-RUIZ S., RAMOS-ESPLA A.A., “Effect of an artificial reef in Posidonia meadows on fish assemblage and diet of Diplodus annularis”, ICES Journal of Marine Science, 59: S59–S68, 2002. SÁNCHEZ-VELASCO L., NORBIS W., “Comparative diets and feeding habits of Boops boops and Diplodus sargus larvae, two sparid fishes co-occurring in the northwestern Mediterranean”, Bulletin of Marine Science, 61 (3): 821–835, 1997. SANTIC M., PALADIN A., ELEZ G., “Diet of striped seabream Lithognathus mormyrus (Sparidae) from eastern central Adriatic Sea”, Cybium, 34 (4): 345–352, 2010. SANZ ECHEVERRIA J., “Datos sobre el otolito, sagitta de los peces de España”, Boletín de la Real Sociedad Española de Historia Natural, 26 (1): 145–160 fig. 71, 1926. SANZ ECHEVERRIA J., “Investigacones sobre otolitos de peces de espana”, Boletín de la Real Sociedad Española de Historia Natural, 30 (3): 174–178, 1930. SANZ ECHEVERRIA J., “Notas sobre otolitos de peces procedentes de la costas del Sahara. I/Fam. Sparidae”, Notas y resúmenes – Instituto Español de Oceanografía, 2: 114, 1–51, 1943. SARÀ M., FAVALORO E., MAZZOLA A., “Comparative morphometrics of sharpsnout seabream (Doplodus puntazzo Cetti, 1777), reared in different conditions”, Aquacultural Engineering, 19: 195–209, 1999. ŠEGVIĆ-BUBIĆ T., LEPEN I., TRUMBIĆ Ž., LJUBKOVIĆ J., SUTLOVIĆ D., MATIĆSKOKO S., GRUBIŠIĆ L., GLAMUZINA B., MLADINEO I., “Population genetic structure of reared and wild gilthead seabream (Sparus aurata) in the Adriatic Sea inferred with microsatellite loci”, Aquaculture, 318: 309–315, 2011. SELLAMI A., BRUSLE J., “Contribution à l’étude de la sexualité de la saupe Boops salpa Linnæus 1758 (Téléostéen Sparidae) des côtes de Tunisie”, Vie et Milieu, 23A (2): 261–276, 1975.

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TAIEB A.H., GHORBEL M., HAMIDA N.B., JARBOUI O., “Reproductive biology of Diplodus vulgaris (Teleostei, Sparidae) in the southern Tunisian waters (Central Mediterranean)”, Acta Adriatica, 53 (3): 437–446, 2012. TAIEB A.H., GHORBEL M., HAMIDA N.B., JARBOUI O., “Reproductive biology, age and growth of the two-banded seabream Diplodus vulgaris (Pisces: Sparidae) in the Gulf of Gabes, Tunisia”, Journal of the Marine Biological Association of the United Kingdom, 93 (5): 1415–1421, 2013a. TANCIONI L., ,MARIANI S., MACCARONI A., MARIANI A., MASSA F., SCARDI S., CATAUDELLA S., “Locality-specific variation in the feeding of Sparus aurata L.: evidence from two Mediterranean lagoon systems”, Estuarine, Coastal and Shelf Science, 57: 469–474, 2003. TECAM, “Survey on Mediterranean marine finfish species diversification. Marine finfish species diversification: current situation and prospects in Mediterranean aquaculture”, Cahiers Options Méditerranéennes (Série B: Études et Recherches), 24: 169, 1999. TERLIZZI A., FELLINE S., LIONETTO M.G., CARICATO R., PERFETTI V., CUTIGNANO A., MOLLO E., “Detrimental physiological effects of the invasive alga Caulerpa racemosa on the Mediterranean white seabream Diplodus sargus”, Aquatic Biology, 12 (2): 109–117, 2011. TORTONÈSE E., Fauna d’Italia echinodermata, osteichthyes, Pesci Ossei (Parte Seconda), Calderini, Bologna, 1975. TOSONOGLU Z., AKYOL O., METIN G., TOKAC A., ÜNSAL S., “Research on the population characteristics of three Sparid species of Gülbahce gulf”, Ege Üniversitesi Su Ürünleri Dergisi, C 14: 127–143 (in Turkish), 1997. TROJETTE M., BEN FALEH A., FATNASSI M., MARSAOUI B., MAHOUACHI N.E.H., CHALH A., QUIGNARD J.P., TRABELSI M., “Stock discrimination of two insular populations of Diplodus aannularis (Actinopterygii: Perciformes: Sparidae) along the coast of Tunisia by analysis of otolith shape”, Acta Ichthyologica et Piscatoria, 45 (4): 363–372, 2015. TÜRKMEN M., AKYURT I., “Growth characteristics, sex inversion and mortality rates of striped seabream, Lithognathus mormyrus L., in Iskenderun Bay”, Turkish Journal of Zoology, 27: 323–329, 2003. TUSET V.M., LOMBARTE A., ASSIS C.A., “Otolith Atlas for the Western Mediterranean, north and central eastern Atlantic. CSCI, Barcelona”, Scientia Marina, 72, (S1): 203, 2008. VARAGNOLO S., “Calendario di comparse di uova pelagiche di Teleostei marini nel plancton di Chioggia”, Archivi di Oceanografia e Limnologia, 13 (2): 249–279, 1964.

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Glossary

Adelphophagy: The behavior of certain individuals who eat their siblings. Allomone: A substance produced and secreted by an organism, inducing a particular behavior in an individual of another species (attraction or repulsion), and thus able to be used as a means of defense. Anadromous: Characterizing fish that migrate from the sea and ascend rivers upstream. Androviviparous (androviviparity): A male organism that takes charge of the incubation of eggs placed into his care by one or more females, in a corporal structure that facilitates respiratory and metabolic exchanges between the pregnant male, the eggs and the embryos (the brood pouch of seahorses and syngnatids). Anoxia, anoxic: The state of a system deprived of oxygen (anoxic waters). Avifauna: All the bird species living in a given area. Biosphere: All living beings and their living environments, thus the totality of the ecosystems in the lithosphere, hydrosphere and atmosphere. Brood pouch: See marsupium. Chemoreception: An organism’s capacity to be sensitive to the chemical components in the environment (sense of smell, taste). Climax: Optimal ecological balance defined by environmental conditions.

Fishes in Lagoons and Estuaries in the Mediterranean 3B: Migratory Fish, First Edition. Mohamed Hichem Kara and Jean-Pierre Quignard. © ISTE Ltd 2019. Published by ISTE Ltd and John Wiley & Sons, Inc.

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Confinement: For Guelorget and Perthuisot, confinement is a complex notion, difficult to measure directly in situ. To simplify, it means the progressive exhaustion of the oligoelements of marine origin and the progressive reduction in potential nutrient input from water courses (nitrates, phosphates, etc.) according to the sea/land and land/sea gradients. The confinement parameter is therefore closely linked to hydrodynamics and particularly to the residence time of the water in the lagoon basin. Detritivore: An animal that feeds on organic debris. Dystrophy: An anomaly in water quality due to excessive production of organic matter, leading to increased mortality causing fermentations that produce anoxia, and production of toxic gases (H2S), conditions unfavorable for life (dystrophic crisis). Ecotone: Natural environment on the borders of two neighboring ecosystems. Ecotype: Individual characteristics (shape, color, etc.) of an organism in relation to its adaptation to a particular living environment. Edaphic: “Related to the soil”. Edaphic factors are abiotic factors specific to the nature of the ground (rock type, nature of sediment, etc.). Endemic (endemism): A species (or group of species) that exist only in a very clearly defined region and nowhere else. Endemism defines the natural presence of a species or biological group in a defined geographic region. Epiphyte: An organism that lives on plant matter using it only as a structural base, establishing no trophic relationship with it. Euryvalent (euryvalence): An organism’s capacity to support wide variations in environmental conditions (salinity, temperature, etc.). Eutrophication: From the Greek for “well nourished”, the enrichment of an environment in nutrient salts, leading to significant production of organic matter, the excess of which triggers dystrophic crises (see dystrophy). Fry propagation: Restocking the waters with very young fishes, usually sourced from aquaculture. Genesic: Pertaining to the establishment of a new generation.

Glossary

Gonopod: External appendage of the male to enable copulation (intromittent organ). Grau: An Occitanian word derived from the Latin word gradus, which means the natural or artificial channel linking a lagoon to the sea. Gynogenesis: Female genetic uniparental reproduction from one single active egg. Gynoviviparity: Female viviparity. Herculean: Pertaining to a plant or animal from the Atlantic entering the Mediterranean via Gibraltar (a reference to the Pillars of Hercules, the rocks of Gibraltar and Ceuta). Hermaphrodism: Characteristic of an organism capable of providing both male and female gametes. Heterozygosity: The state of a cell (or living being) possessing different alleles for a given gene on each homologous chromosome (opposite: homozygosity). Homing: An organism with the “homing instinct” has the capacity to find its way home, i.e. return to the place it lived previously. An example of this is salmon returning to the river where they were born after spending time in the sea. Hypolimnion: A deep part of a lake with little light and which is often poorly oxygenated. Interspecific: Between different species; between individuals belonging to different species. Intraspecific: Within one species; between individuals of the same species. Iteroparity: The condition of an animal that reproduces several times during its life. This is a different notion from “fragmented spawning” that describes, in teleosts, the action of a female emitting waves of ovocytes, at variable time intervals, during one single reproductive season (opposite: semelparity). Kairomone: A chemical molecule that acts interpecifically to the advantage of the recipient.

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“Lagunotrophic” migration: Marine animals paying regular visits to lagoons in order to feed. Lentic: A calm water environment that renews itself slowly (opposite: lotic). Lessepsian: A term used for Eritrean or Indo-Pacific plants and animals that reach the Mediterranean via the Suez canal (a reference to Ferdinand de Lesseps). Lido: The French term for a sandspit, the long, sandy geological formation that separates a lagoon from the sea (also called a barrier beach). Limivore: An organism that ingests mud to take nourishment from the dead or living organic matter contained in it. Often incorrectly spelled as “limnivore” (meaning “that eats calm waters”!). Limnogenic: Pertaining to spawning in lakes (limnogenic migrators are fishes that visit lakes to reproduce). Malaigue: An Occitanian word meaning “bad waters” used to denote anoxic or subanoxic waters rich in H2S, as a result of an overload of organic matter in a more or less advanced state of decomposition. Marker: A natural or artificial substance present in an organism that shows a physiological or behavioral activity in a given environment. Marsupium: A pouch located on the ventral side of the male in certain syngnathids into which females deposit their eggs which, after fertilization, continue to develop and emerge at a very advanced postlarval stage (subjuvenile). Messinian: The final age of the Miocene epoch, during which the Mediterranean dried up, between 5.96 and 5.33 million years ago (Messinian crisis). Micropyle: In teleosts and myxines, an orifice through which spermatozoa can reach the ovocyte (ovule) in order to fertilize it. Monogamous: Describes an animal that forms a stable pair bond lasting for at least one sexual cycle. Monogyne or monogamous male: A male that mates with only one female. Neonate: Synonym of newborn.

Glossary

Neuston: All the organisms that float on the water’s surface, between air and water. Nidification: Modifying a cavity or building a structure from plant or mineral matter for the purpose of reproduction or simply for protection. Ontogenesis: The development of an individual, from egg to adulthood. Ontogenic, ontogenetic: Pertaining to ontogenesis. Otolith: From the Greek term otos lithos, meaning “stone of the ear”, a piece of mineralized calcareous material located in the inner ear (fish have three pairs of otoliths, called asteriscus, lapillus and sagitta). Oviparous: An oviparous female lays eggs (i.e. ovocytes, ovules fertilized by spermatozoa in the genital passages of the female or hermaphrodite) that develop outside the “maternal” organism. Ovuliparous: An ovuliparous female emits her ovocytes or ovules into the water (external fertilization) or (in syngnatids) into the brood pouch of the male, where they are fertilized and become eggs. Panmictia, panmictic: See panmixia, panmixic. Panmixia: Random mating of individuals of a population (absence of barriers to genetic exchanges). Panmixic: Pertaining to panmixia. Paralic: A paralic environment denotes a coastal area in contact with the sea via a narrow communication channel, as is the case for lagoons. Synonym: “marginal continental system”. Paraviviparity: Incubating eggs in a way that has affinities with the viviparity practiced in the female genital passages. Male seahorses and syngnatids that incubate eggs in their “marsupium” are sometimes described as “paraviviparous”. Pheromone: A chemical message produced by an organism and picked up by the olfactory system of its fellows.

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Phylogeography: The study of the principles and processes governing the geographic distribution of genealogical lineages, especially at the intraspecific level. Phylogeographic: Studies and findings pertaining to phylogeography. Physoclist: A teleost that has no “pneumatic duct” connecting the air bladder to the oesophagus. Physostome: A teleost with a duct (“pneumatic duct”) connecting the air bladder to the oesophagus. Pleistocene: The geological epoch of the quaternary period lasting from around 2.6 million years ago to 12,000 years ago. Polyandric: Denotes a female that mates with a number of males during a single spawning season. Polyandry: The condition of females that mate with a number of males. Polygynandry: A method of reproduction where one female mates with a number of males, and one male with a number of females. Polygyny: A method of reproduction where the male reproduces with a number of females. Potamotoc: It denotes a fish that can live in the sea or in brackish lagoons, but that has to return to fresh water to reproduce. Protandrous or proterandric hermaphrodism: An animal that functions as a male in the early part of its sexual life, then as a female until its death (sexual inversion). Protogynous or proterogynous hermaphrodism: An animal that functions as a female in the early part of its sexual life, then as a male until its death (sexual inversion). Relict: Plants or animals whose existence in a given location can be explained by former climatic conditions (glacial relicts in the present-day Mediterranean: cold water species that have survived in the Mediterranean since the last ice age).

Glossary

“Rhapie”: Synonym of “ionic relationship”, relative ionic concentration (rhapic factor according to Por, 1980). Rock-dwelling: Denotes organisms that naturally live close to or in contact with rocks Semelparous: Denotes a fish that achieves just one sexual cycle during its life, but whose spawning can be fragmented throughout the duration of this single reproductive season (a separate notion from “fragmented spawning” which denotes the behavior of a female who emits waves of ovocytes at variable time intervals over one reproductive season). Sneaker: A furtive male that effects fertilizations to the detriment of males who have taken a mate (fertilization theft). Synomone: An allelochemical substance of value to the animals or plants that release it and receive it. Thalassogenic: A term relating to sea spawning (thalassogenic migration is the action of animals who migrate from a river or lagoon to the sea to spawn). Thalassogenic or thalassogenesic migration: Animals going to the sea in order to reproduce. Thalassotoc: Amphidromous animals capable of living in fresh and brackish water but which go to the sea to reproduce. Tidal range: The difference in water level between successive high and low tides. In the Mediterranean, the tidal range is low except in the Adriatic and the Gulf of Gabes. Trophic: Relating to feeding. Turbidity: The state of water that is clouded due to its content of suspended particles (sand, mud, humic acids). Valliculture: One of the most ancient forms of semi-intensive aquaculture in the Mediterranean, still used in the Po Delta. Viviparous (viviparity): Term used to denote an animal that practices internal fertilization and gives birth to living offspring (neonates).

279

Index

A, B, C

G, L

asymmetric flatfish, 76 annular gilthead, see also Sparus annularis, 135, 140 bar, 30 Charax puntazzo, 148 Chelon labrosus, 173 Chrysophrys aurata, 218

gilthead seab ream, see also, Sparus aurata, 45, 193, 218, 220, 222–224, 230, 232–237, 239 gobies, 90 Lithognathus, 194 mormyrus, 194

D Dicentrarchus labrax, 242, 247, 251, 272 Diplodus, 130, 132–135, 148, 151, 152, 155, 161–163, 173, 180, 182, 187, 193 annularis, 133, 135 puntazzo, 133, 148, 163 sargus sargus, 133, 161, 240, 244, 249, 253, 263 vulgaris, 133, 180, 187, 193, 214

F flesus, 59–66, 68, 70, 95 vulgaris, 60 flounder, see also pleuronec flesus, 60–62, 64, 65, 67, 70, 71, 73, 74, 112, 113, 124, 127

M Mugil cephalus, 173 mullet, 173 Mullidae, 1 Mullus, 1–5, 7, 10, 11, 13, 18, 23, 24, 26, 27, 32 barbatus barbatus, 4, 5, 13, 27 barbatus surmuletus, 23 ruber, 5 surmuletus, 1, 4, 23, 26, 32

P, R Pagellus lithognathus, 194 mormyrus, 194 Pegusa, 76–78, 79 Platichthys, 59, 60, 62, 63 rugosus, 59 Pleuronectidae, 59

Fishes in Lagoons and Estuaries in the Mediterranean 3B: Migratory Fish, First Edition. Mohamed Hichem Kara and Jean-Pierre Quignard. © ISTE Ltd 2019. Published by ISTE Ltd and John Wiley & Sons, Inc.

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Fishes in Lagoons and Estuaries in the Mediterranean 3B

pleuronectes, 59, 64 flesus, 60, 70 italicus, 60 luscus, 60 passer, 60 solea, 92 Puntazzo puntazzo, 148 right eyed flounder see also asymmetric flatfish, 59

S Salpa salpa, 206 Sargus, 130, 132–135, 137, 151, 153, 155, 161–180, 182, 187 annularis, 135 rondelettii, 161 salviani, 180 vetula, 161 vulgaris, 180 Sarpa, 206 salpa, 206, 210 salema, see also Sarpa salpa, 206, 209–211, 213–216 sea bass, 160 sole, 74, 75–82, 84–86, 91–110

Solea, 45, 75–82, 84–86, 91–110 aegyptiaca, 79, 81, 82, 84, 86, 97 melanochira, 85 senegalensis, 76, 81, 84–86, 109 solea, 78, 80, 86, 91, 92, 99 vulgaris aegyptiaca, 79 vulgaris typica, 92, 97 vulgaris, 77, 79, 80, 86, 92, 97 Soleidae, 75–77, 81 Sparidae, 129, 130 Sparus, 130, 135, 148, 161, 163, 179, 193, 194, 206, 217, 218, 233, 234 annularis, 130, 135 aurata, 163, 179, 193, 217, 218, 233, 234, 241, 242, 244–260, 262, 264, 265, 267–270, 272 mormyrus, 194 puntazzo, 148 salpa, 206 sargus, 161 surmullet, 1, 4, 24 Synapturichthys, 77

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