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Fishes in Lagoons and Estuaries in the Mediterranean V3A : Migratory Fish
 9781119597407, 1119597404, 9781786302465, 1786302462

Table of contents :
Content: Cover
Half-Title Page
Title Page
Copyright Page
Contents
Preface
Foreword
Introduction
Occupation of lagoons and migration phenology
Lifespan and growth
Other biological and behavioral traits
A strong contribution to fishery resources
Status and threats
Bibliography
1. Anguillidae Jordan and Evermann, 1896
1.1. Anguilla (Schrank, 1798)
1.1.1. Anguilla anguilla (Linnaeus, 1758)
1.2. Bibliography
2. Engraulidae Jordan and Evermann, 1896
2.1. Engraulis Cuvier, 1817
2.1.1. Engraulis russoi Dulzetto, 1947
2.2. Bibliography
3. Gobiidae Regan, 1911 3.1. Pomatoschistus Gill, 18643.1.1. Pomatoschistus minutus (Pallas, 1770)
3.2. Bibliography
4. Moronidae Jordan and Evermann, 1896
4.1. Dicentrarchus Gill, 1860
4.1.1. Dicentrarchus labrax (Linnaeus, 1758)
4.2. Bibliography
5. Mugilidae Günther, 1861
5.1. Chelon (Rose Walbaum, 1793)
5.1.1. Chelon labrosus (Risso, 1827)
5.2. Liza (Jordan and Swain, 1884)
5.2.1. Liza aurata (Risso, 1810)
5.2.2. Liza ramada (Risso, 1827)
5.2.3. Liza saliens (Risso, 1810)
5.3. Mugil Linnaeus, 1758
5.3.1. Mugil cephalus Linnaeus, 1758
5.4. Bibliography
Glossary
Index of Names
Index of Places

Citation preview

Fishes in Lagoons and Estuaries in the Mediterranean 3A

Series Editor Françoise Gaill

Fishes in Lagoons and Estuaries in the Mediterranean 3A 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

www.wiley.com

© 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: 2018967379 British Library Cataloguing-in-Publication Data A CIP record for this book is available from the British Library ISBN 978-1-78630-246-5

Contents

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

vii

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

ix

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

xi

Chapter 1. Anguillidae Jordan and Evermann, 1896 . . . . . . . . . . .

1

1.1. Anguilla (Schrank, 1798) . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1.1. Anguilla anguilla (Linnaeus, 1758) . . . . . . . . . . . . . . . . . . . 1.2. Bibliography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 6 60

Chapter 2. Engraulidae Jordan and Evermann, 1896 . . . . . . . . . . .

95

2.1. Engraulis Cuvier, 1817 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1. Engraulis russoi Dulzetto, 1947 . . . . . . . . . . . . . . . . . . . . . 2.2. Bibliography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

95 96 104

Chapter 3. Gobiidae Regan, 1911 . . . . . . . . . . . . . . . . . . . . . . . .

107

3.1. Pomatoschistus Gill, 1864 . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.1. Pomatoschistus minutus (Pallas, 1770) . . . . . . . . . . . . . . . . . 3.2. Bibliography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

108 109 121

Chapter 4. Moronidae Jordan and Evermann, 1896 . . . . . . . . . . . .

129

4.1. Dicentrarchus Gill, 1860 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.1. Dicentrarchus labrax (Linnaeus, 1758) . . . . . . . . . . . . . . . . . 4.2. Bibliography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

130 132 149

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Chapter 5. Mugilidae Günther, 1861 . . . . . . . . . . . . . . . . . . . . . . 5.1. Chelon (Rose Walbaum, 1793) . . . 5.1.1. Chelon labrosus (Risso, 1827) . 5.2. Liza (Jordan and Swain, 1884) . . . 5.2.1. Liza aurata (Risso, 1810) . . . . 5.2.2. Liza ramada (Risso, 1827) . . . 5.2.3. Liza saliens (Risso, 1810) . . . . 5.3. Mugil Linnaeus, 1758 . . . . . . . . . 5.3.1. Mugil cephalus Linnaeus, 1758 5.4. Bibliography . . . . . . . . . . . . . .

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164 165 180 181 195 215 230 231 256

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

291

Index of Names . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

299

Index of Places . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

301

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

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

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

xiii

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 gilt-head sea bream 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 gilt-head sea bream 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 gilt-head sea bream (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 autumn 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 sea breams visit the Mirna estuary in Croatia (Kraljević and Dulčić 1997),

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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 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

Introduction

xv

and juveniles born of good male and female begetters 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 gilt-head sea bream 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 gilt-head sea bream, 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 molluscs (sea breams), crustaceans, fish (sea bass) and plants for the S. salpa porgy, 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 gilt-head sea bream and the sea bass, but in different proportions depending on climatic and geographical zones. In the lagoons of the eastern Mediterranean, the eel 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 gilt-head sea bream 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, gilt-head sea breams, 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), gilt-head sea breams (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, gilt-head sea bream). In 2008, it reached 66,738 tons for the sea bass and 133,026 tons for the sea bream (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 larvae 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 Anguillidae Jordan and Evermann, 1896

Vernacular name: Eels. Etymology: Derived from the Latin, anguis (snake). Brief description: It has tiny scales. The mouth is terminal and the lower jaw is slightly protruding. The teeth are small in several rows on the jaws and the palate. The tongue is present, the lips are thick, the frontal bones are twinned and the palato-pterygoid arch is well developed. The gill slits, small and vertical, are located in front of the base of the pectoral. The lateral line, well developed, is complete. The pectoral fins are well developed and supported by seven to nine rays (more than 11 in juveniles). Dorsal anal fins are united to the caudal fin. The origin of the dorsal fin is located far behind the pectoral fin, but before the anus. The anal fin takes its origin a little behind the anus. The number of vertebrae is 100–119 (Nelson, 2006). Biogeography: Tropical, subtropical and temperate warm and cold seas, with the exception of the eastern Pacific and southern Atlantic. Habitat and bioecology: Adults live in fresh and brackish waters (estuaries and lagoons), spawn at sea and their larval stages are marine. Systematics and phylogeny: Recent studies have shown that Anguillidae have affinities with the “eels” of deep marine waters: Nemichthyidae and Serrivomeridae (Inoe et al., 2010). Biodiversity: Anguillidae are currently represented in the world by only one genus Anguilla (Nelson, 2006).

Fishes in Lagoons and Estuaries in the Mediterranean 3A: 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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1.1. Anguilla (Schrank, 1798) Type: Muraena anguilla Linnaeus, 1758 (named by Schrank, 1798, in Fauna Boica, 1(2): 304). Synonyms: None. Etymology: Anguilla, name derived from the Latin anguis (snake). Brief description: See box, “Brief description”. Biogeography: Species of the genus Anguilla are widely distributed in most tropical, subtropical and temperate areas of the world. They are present on all continents, except in Antarctica. The continental distribution of temperate species seems to be related to the subtropical circulation of the oceans, with a majority of species living along the western coasts of the Atlantic, Indian and Pacific oceans, except for Anguilla anguilla (Ege, 1939; Watanabe, 2003) (see Figure 1.1).

1 – A. anguilla 2 – A. australis australis 3 – A. australis schmidtii 4 – A. bicolor bicolor 5 – A. bicolor pacifica 6 – A. borneensis

7 – A. celebesensis 8 – A. dieffenbachii 9 – A. interioris 10 – A. japonica 11 – A. marmorata 12 – A. megastoma

13 – A. mossambica 14 – A. nebulosa labiata 15 – A. nebulosa nebulosa 16 – A. obscura 17 – A. reinhardtii 18 – A. rostrata

Figure 1.1. Geographical distribution of the genus Anguilla (bold lines) and possible dispersal routes of eel ancestors in the Atlantic Ocean (gray arrows). The regions where each species is present are indicated in numbers. The Anguilla marmorata (11) is the most widespread species and is found from the western Indian Ocean across the Indonesian archipelago, to southern Japan and all along the islands of the Southeast Pacific (according to Minegishi et al., 2005)

Anguillidae Jordan and Evermann, 1896

3

However, eels are absent from the eastern coasts of South America, despite the existence of the hot current of Brazil. On the basis of this geographical distribution, the Atlantic species (A. anguilla and Anguilla rostrata) are geographically separated from their counterparts in the Pacific and Indian Oceans. Habitat and bioecology: The genus Anguilla occupies a variety of habitats. Because of their euryhalinity, the species of this genus colonize inland waters, including estuaries, lagoons, rivers, lakes and marshes. All these catadromous species spawn in the tropical ocean and their larvae are distributed in fresh and brackish estuarine and lagoonal waters by warm subtropical currents (Schmidt, 1923, 1925; Tesch, 1977; Tsukamoto, 1992). Let us mention the recent discovery regarding ocean residents, which never enter freshwater. Three temperate species A. anguilla, A. rostrata, and Anguilla japonica seem to have a flexible life story (Tsukamoto et al., 1998; Tzeng et al., 1997; Tsukamoto and Arai, 2001; Jessop et al., 2002). By studying the Sr/Ca ratio in otoliths, these authors have highlighted the existence of permanent populations of yellow and silver eels in coastal marine waters. The stay in fresh water and can therefore be optional. Tsukamoto et al. (2002) consider that there are two ecophenotypes of eels: one estuarine, the other one, marine. All the species of the genus Anguilla are semelparous (they die after one laying). Biodiversity: The genus Anguilla is represented by 18 species in the world (Hastings et al., 2014), 16 Indo-Pacific and two Atlantic ones: the A. anguilla (AfroEuropean eel) and the A. rostrata (American eel) (Lecomte-Finiger, 2003). The six Indo-Pacific subspecies listed by Ege (1939) have been considered as invalid by Tsukamoto and Aoyama (1998). However, Minegishi et al. (2005) have not taken this revision into account in their work on the phylogeny and the evolution of the genus Anguilla. Only the A. anguilla lives in the Mediterranean. Systematics and phylogeny: The results of the studies carried out have not yet made it possible to know the most probable dispersal routes of the genus Anguilla nor the most “ancestral” species. On the basis of molecular phylogenetic analyses, Aoyama and Tsukamoto (1997) and Aoyama et al. (2001) were the first ones to propose the hypothesis according to which the founding species of Atlantic eels might have moved from its place of origin, Indonesia, and reached the future Atlantic via the Tethys, about 30 million years ago (Figures 1.1 and 1.2, Route A). However, Lin et al. (2001) have suggested an opposite dispersal direction based on phylogenetic molecular analyses and the estimation of eel divergence time. They have suggested that the original migration to the Atlantic took place via the Central American “Seaway”, closed for about 3 million years (Isthmus of Panama). This

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path is the only one possible since, according to these authors, the origin of the genus Anguilla is approximately 20 million years old (Figures 1.1 and 1.2, Route B).

Figure 1.2. Topologies of phylogenetic trees that support two different hypotheses concerning the eel entry route in the Atlantic Ocean. The numbers following the name of each species correspond to those in Figure 1.1.The asterisk on the tree by Lin et al. (2001) shows the first divergence that divides the 12 species into two large cladi. Cyt b: cytochrome b; 12S: 12S ribosomal RNA; 16S: 16S ribosomal RNA, IP: Indo-Pacific; O: Oceanic; A: Atlantic (according to Minegishi et al., 2005)

Although Ege (1939) considered that current eels derive from A. japonica, more recent studies (Aoyama et al., 1997) have shown that A. mossambica might be their common ancestor. Moreover, this viewpoint has been confirmed by the sequence analysis of the entire mitochondrial genome of 18 eel species and subspecies (Minegishi et al. 2005). These authors have suggested that A. mossambica is the species from which three geographical eel cladi (with the exception of Anguilla borneensis) originated: Atlantic (two species), Oceania (three species), Indo-Pacific (11 species) (Figure 1.3).

Anguillidae Jordan and Evermann, 1896

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Figure 1.3. Consensus tree of the 9,001 trees from the two independent Bayesian inference analyses of the 15,187 nucleotide positions unambiguously aligned for the Anguilla 18 species/subspecies and for the three species outside the group (according to Minegishi et al., 2005)

These same authors found that the age of the beginning of speciation in anguillids, estimated at 20 million years, has been underestimated. While the morphometric criteria described by Ege (1939) led to the proximity of the three temperate species, A. anguilla, A. rostrata and A. japonica, this relationship was not confirmed by mitochondrial DNA studies (Tagliavini et al., 1996; Aoyama et al., 1997; Tsukamoto and Aoyama, 1998; Ragauskas et al., 2011) or nuclear DNA (Lehmann et al., 2000; Liang et al., 2005). According to these studies, A. mossambica, A. australis, A. anguilla and A. rostrata belong to the same cladi from which A. japonica has been excluded (Figure 1.3). The genetic distance between A. anguilla and A. rostrata is 0.0115. This value is the lowest recorded between the various eels, indicating that the separation between these two species was recent (Tsukamoto and Aoyama, 1998).

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1.1.1. Anguilla anguilla (Linnaeus, 1758)

1.1.1.1. Nomenclature and systematics Type: Muraena anguilla, Linnaeus, 1758. Syst. Nat. Edit X: 245 (Habitat in Europa). One specimen named by Linnaeus is at the Natural History Museum in London: Linnaeus collection, no. 80. Synonyms: Thirty-three synonyms, according to Tesch (1991). Vernacular names1: Anguilla (DZ), hannash (EG), anguila (ES), anguille (FR), common eel (GB), chéli (GR), sallura (IS), anguilla, capitone (IT), noune (MY), zelofah (MT), hancha, sannour (TN), yilan (TR). Etymology: Anguilla is the diminutive of the Latin name Angius, which means snake. 1.1.1.2. Description 1.1.1.2.1. The larvae – “Leptocephalic” stage: The larva, called “leptocephalus”, from lepto (thin) and cephale (head) is morphoanatomically and chromatically different from later “postmetamorphic” and continental stages (Figure 1.4). Its length after hatching in the Sargasso Sea from a 1.2 mm diameter egg (Yamamoto et al., 1974) is about 3 mm (Yamamoto and Yamauchi, 1974). Its final size reached on the European continental shelf, after about 1–2.5 years of oceanic migration, is about 70 mm. Lecomte-Finiger et al. (2004) provided an update to the knowledge about this larva. Its body, shaped like a willow or an olive tree leaf, is crystalline or transparent and compressed laterally. The head is proportionally small compared to the rest of the body. The transparency of leptocephalic larvae (Figure 1.5) suggests their anatomy. 1 Short forms: (DZ) Algeria, (EG) Egypt, (ES) Spain, (FR) France, (GB) Great Britain, (GR) Greece, (IS) Israel, (IT) Italy, (MA) Morocco, (MT) Malta, (TN) Tunisia, (TR) Turkey.

Anguillidae Jordan and Evermann, 1896

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Figure 1.4. Metamorphosis of the Anguilla anguilla eel. Leptocephalic larvae (A, B, C and D), leptocephalic larvae undergoing metamorphosis (E and F)

Figure 1.5. Twelve-day-old Anguilla anguilla larvae ready to feed (photo J. Tomkiewicz, DTU Aqua)

The musculature consists of myotomes arranged in a V or W stripe. In the axial zone, we can find the spinal cord, the chord and the aortic artery. Leptocephali do not possess either red blood cells or hemoglobin. The heart and the circulatory system, with very thin and transparent walls, are difficult to observe. The olfactory lobes are well developed, as are the optical capsules (Rasquin, 1955). The structure

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of the eyes (Pfeiler 1989; Appelbaum and Riehl, 1993) is remarkable in relation to the way of life of these mesopelagic larvae (–600 m), with nyctohemeral rhythms at the surface at night (–30 m). Indeed, the photoreceptor layer of the retina is entirely made up of sticks rich in chrysopsin (Wood et al., 1992), which indicates an essentially nocturnal vision. The dentition is typical and, depending on the size of the planktonophagous larva, it comprises between 3 and 20 long and pointed teeth, projected forward (Bertin, 1951; Appelbaum and Riehl, 1993). Leptocephali are characterized by a development strategy of their own, called leptocephalus strategy (Pfeiler, 1986), different from other teleosts. This strategy consists of a long phase of larval growth or pre-metamorphic phase (phase I), followed by a rapid metamorphosis (phase II) during which the lepharocephalic larva will radically change its shape and acquire the definitive serpentiform shape and pigmentation that are characteristic of the larvae species. This metamorphosis begins when the leptocephalic larva reaches the continental shelf and measures 70– 80 mm. – Elver stage: The “larva” resulting from the metamorphosis of the leptocephalus is called an elver (or pibale), but some authors describe the larva as elver as soon as the metamorphosis of the leptocephalus begins at sea on the continental shelf (see ontogenesis). The larval stage that we are describing here corresponds to the end of the acquisition of the “anguilliform, serpentine” morph in the course of “metamorphosis” (Struberg’s stage V, 1913; Elie et al., 1982). This “larva” measures an average of 6 cm and weighs between 0.2 and 0.5 g. A staged classification according to pigment development was developed by Strubberg (1913). Many authors worked over this classification, either by simplifying it (Boetius, 1976, Charlon and Blanc, 1982) or by adding a stage (Elie et al., 1982). Except for pigmentation, the eel at the elver stage has reached its final morphological appearance (juvenile type). With regard to pigmentation, we can observe the presence of a spot of melanophores on the skull, another one at the end of the tail and some rostral pigments. Subsequently, melanophores develop along the body. In stage VI B, the strongly colored larva loses its transparency; this signals the end of the glass eel stage. At the following stage (stage VII), in addition to the black color, yellow pigments appear, and thus the “eel” stage is reached. Alongside the chromatic transformations, anatomical changes take place. At the level of the eyes, the cones appear and the retinal pigments change. Chrysopsin is thus replaced by rhodopsin, associated with porphyropsin (Wood et al., 1992).

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These changes show the transition to a new way of life. In fact, once pelagics, the larvae will become benthic. The gaseous bladder will appear in the glass eel at the end of its colonization migration from continental waters at the end of the pigmentation process (Hickman, 1981). We can observe the replacement of leptocephalic-type larval teeth by caniniform teeth (Bauchot, 1959). The glass eel stage is accompanied by a prolonged period of fasting, following the “partial or total” obstruction of the digestive tract by three valves (Monein-Lang, 1985) at the VB stage (continental transparent stage). The digestive tract is subsequently remodeled as follows: in addition to the teeth, the gastric glands appear and it becomes functional again through the suppression (stage VI A3) of the three valves that obstructed it (Monein-Langle, 1985). The glass eel becomes a carnivorous eel, with a diet based on benthic preys, and the growth process is resumed. 1.1.1.2.2. Juveniles and subadults Juvenile (yellow, green) and subadult (silver) eels have a very elongated, serpentiform, circular-shaped body, which is slightly compressed particularly close to the caudal end. The tail is rounded. The head is compressed, with a rather elongated snout, which is sometimes wide. The oral cleft extends to almost half of the eye. The mouth is terminal, with a prominent lower jaw. The jaws and the vomer are equipped with a series of teeth. The eye is round and represents between 1/8th and 1/12th of the length of the head. Its diameter varies throughout its development. It is bigger in the silvery eel than in the yellow eel in relation to the different visual abilities required for freshwater and for marine environments (Pankhurst, 1982a). The dorsal, caudal and anal fins are fused, forming a very long odd fin. Pelvic fins are absent. The skin is smooth and viscous, rich in mucus cells. This mucus, made up of glycoproteins containing sialic acid, contributes to the protection of the cutaneous barrier. The lateral line is clear. Numerical characters have been provided by different authors: – Berg et al. (1949): vert. 111–119 (normally 114-116), D. 245–275, A. 176– 249, C. 7–12, P. 15–21; – Wheeler (1969): vert. 112–117, D. 245–275, A. 205–235, P. 14–18 rays. The number of vertebrae enables a specific diagnosis (Boetius, 1980, see Figure 1.6).

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Figure 1.6. Differences in the number of vetebrae between American eels and European eels (according to Boetius, 1980)

– Yellow eel stage: When the pigmentation is fully developed, the “yellow eel” stage, also called “green eel”, is reached. The back varies from dark green or brown to black, depending on the habitat. Abnormal colors have been found (Lohnisky, 1982). These anomalies range from almost white eels (Walter, 1910) to mottled or mottled in black individuals. The yellow eel phase, called the “growth phase”, lasts for several years, depending on the sex and the environment. The black, brownish, greenish or yellowish colors, at the yellow eel stage, are related to the habitat (homochromy). The dark color of the integument and its changes (the chromatic adaptation to the environment) depend on the number and extent of the melanophores (melanophoric index); these pigment cells are under neuro-endocrine control (Fremberg and Olivereau, 1973), namely the pituitary hormone, the melanophore stimulating hormone (MSH), itself dependent on the hypothalamic nervous system: the cathecolamines, the MIF-1 (MSH-release inhibiting factor) and/or MRF (MSH-releasing factor). In fresh water, the yellow color depends on the extension of endocrine-induced xanthophores: the prolactin

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secretion (PRL) by hypothalamic controlled hypophysis, with the inhibition of prolactin hormonal synthesis in salt water (Olivereau, 1978). – Silver eel stage: The end of the “yellow/green eel” stage is marked by the appearance of a new skin, with a dark green to black back, flanked with silvery reflections and a whitish belly. Due to the presence of guanine and hypoxanthine in the skin, this “silvering” is the visible expression of a second metamorphosis which, linked to physiological and morphological changes, prepares fish for the oceanic reproductive migration toward the Sargasso Sea. Fontaine (1994) was the first to suggest that the simple distinction between “green-yellow eel/silver eel” does not correspond to reality and that it is necessary to subdivide this transformation into several stages. Feunteun et al. (2000) recognized three stages: yellow, silvery, yellow/silver. These stages are based on external variables (skin color, visibility of the lateral line, surface of the eye). In any case, the silver skin of eels at the time of their downstream migration is the most apparent external change, although the use of color for identifying migrating eels has been criticized (Pankhurst and Lythgoe, 1982). An increase in the eye size, the pigmentation of the lateral line and the darkening of the pectoral fins are also commonly used indicators in order to determine the “premigratory” stage of eels. However, the sequence of events leading to this stage and the factors that trigger silvering remain unknown. According to Durif et al. (2005), it is likely that the production of the growth hormone (GH) at the premigratory stage (stage III of the classification by these same authors) induces an important period of growth and triggers silvering. In migrating eels, the development of the gonads, the production of the gonadotropic hormone (GTH-II) and an increase in the surface of the eyes have been confirmed. Differences between sites involved the regression of the intestine, as well as the length of the pectoral fin. These variables appear to vary with the size of the watershed and the distance from the sea, which may indicate the time when an eel started its migration. The reversibility of silvering was pointed out by Svedäng and Wickstrom (1997). The latter concluded that silvering is much more flexible than has been predicted. Eels can stop their metamorphosis and start eating again if the chances of a successful migration are compromised. Coloring: See the chromatic characteristics of the various development stages in section 1.1.1.2, “Description”. Variations: The European eel shows variations in the width of the head: it is narrow and wide (Figure 1.7) (Torlitz, 1922; Thurow, 1958; Tesch, 1983).

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a)

b)

Figure 1.7. a) Narrow-headed eel. b) Broad-headed eel (according to Tesch, 1983)

These variations probably depend on environmental influences, including the type of available prey (Tesch, 1991; De Meyer et al., 2016). In silver eels, these variations are not so important (Muller, 1975). Cucherouss et al. (2011) have shown that, regardless of their size, individuals with a broader head occupy a higher trophic position than fish with a narrower head. The former consume more fish prey than invertebrates and occupy more distant habitats from the river banks than the latter. In addition, individuals with intermediate cephalic morphology display a less favorable condition than fish with extreme cephalic morphologies (broad and narrow), which might indicate the existence of disruptive selection, associated with individual specialization. However, the trophic determinism of cephalic dimorphism in eels is questionable, because “fasting” elvers are also concerned (De Meyer et al., 2015). Let us note that the two forms display a different predisposition toward parasitism in Anguillicola crassus, depending on whether they are more or less piscivorous (Pegget al., 2015). Yahyaoui (1988) found no correlation between the average number of vertebrae and the size of glass eels from two Mediterranean sites (the mouth of the Moulouya in Morocco and the Bages-Sigean lagoon in France), and a site in the Atlantic (Sebou estuary). Chromatic analyses (pigmentation), morphometrics (height– weight) and meristics (vertebrae) made by this author have confirmed the results of enzymatic polymorphism (Yahyaoui et al., 1983) and revealed a homogeneity between Mediterranean and near-Atlantic populations, arguing in favor of their common Atlantic origin.

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Sexual dimorphism: Anguilla anguilla is characterized by a clear sexual dimorphism that essentially concerns the size. For example, in two lagoons in the southern Adriatic (Lesina and Varano), males are small (30–45 cm maximum) and all the eels over 45–50 cm TL are females (Rossi and Villani, 1980) (Figure 1.8).

Figure 1.8. Size dimorphism in silver eels in two Italian lagoons from the Adriatic (according to Rossi and Villani, 1980)

There is little overlap between the two sexes, and therefore, sex determination via the “size method” is possible. It is accepted that yellow eels larger than 45 cm are females, but small females (about 37 cm TL) have also been reported (Tesch, 1991). Nordquist (1917) found that the pectoral fin, the eye and the head are broader in males. Holmgren and Wickstrom (1993) pointed out that in breeding males, the eyes are prominent in dorsal view.

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Osteology, otoliths and scales: In A. anguilla, the basephenoid bone, normally located at the base of the skull, above the parasphenoid, is absent. A symplectic, linking the quadratic of the lower jaw to the hyomandibule and thus to the skull, does not exist. The narrowness of the head also entailed an adjustment in the position of the branchial apparatus. The latter moved behind the skull. The odd fins (dorsal, anal, caudal) are confluent. However, as shown by the caudal part of the spine, the skeletal elements of the caudal fin (the hypural bones) are still present (Bertin, 1956). The scales are small and oval, deeply embedded in the skin. They appear rather late, according to a caudo-cephalic gradient, depending on the size, not on the age of the eel. As a result, these cannot be used for age assessment by scalimetry, because their appearance is late and their growth is irregular (Jellyman, 1979), hence the interest in otolithometry (Lecomte-Finiger, 1983a). The eel’s otoliths, and more particularly, the sagitta, have been the subject of many descriptions after Klein gave his own in 1740. In this area, GandolfiHornyold, who, between 1928 and 1937, devoted 16 notes to the otoliths of the European eel, was certainly the most prolific (Hureau and Monod, 1973). The otoliths from A. anguilla leptocephali and from glass eels are characteristic of eels (Hecht, 1977). The description of otoliths from leptocephalic to subadult stages was given by Appelbaum and Hecht (1978): in leptocephali and glass eels, the shape is circular, with a smooth border. The sulcus acusticus is open toward the front, closed behind, with a poorly individualized ostium and cauda. The collicula is homomorphic and relatively well developed. The upper and inner crista are well developed. The antiroster and the excisura ostii are absent; the rostrum is small, but present. The inner surface is flat; the lateral surfaces are strongly convex. The sagittae of larger individuals (>18 cm TL) differs from previous forms in that the antirostrend excisura ostii is absent and in that they have a more oval shape. In addition, the lateral edges become less convex. Capoccioni et al. (2011) examined intra- and interpopulation variations in the shape of otoliths in three eel stocks from different environments in Italy: two lagoons (Caprolace and Lesina) and one river (Tiber). In all three cases, the form evolved during ontogenetic development, presenting a better uniformity in small sizes than in larger ones. Depending on the environment, the otolith appeared as more elongated, with an accentuation of protrusions (rostrum and postrostrum) in both lagoons. Conversely, the shape of the otoliths appears as less elongated in the Tiber and does not seem to be subject to the influence of growth. Not only does the eel’s otolith serve as a growth marker and an age indicator, but it is also used as if it were the fish “black box”. Because of its microstructure and the

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values of its Sr/Ca, Sr/Si, O18/C13, etc., ratios, the otolith makes it possible to apprehend the biological past of the eel (leptocephalic larval life, metamorphosis, changes in glass eel environments, thermal or nutritional crises, etc.) and to retrospectively reconstruct its lifecycle (Lecomte-Finiger, 1999) (Figure 1.9).

Figure 1.9. Reading of an eel glass eel otolith making it possible to trace the stages of its larval life (according to Lecomte-Finiger and Yahyaoui, 1989)

In fact, Lin et al. (2011) showed that the Sr/Ca ratio differed in the yellow eel otoliths from three sites sampled along the Asi River (in southern Turkey), possibly reflecting regional peculiarities of water chemistry. On the other hand, by subjecting juvenile pigmented eels to different diets for 8 weeks, Marohn et al. (2009) proved that feeding has no influence on the chemical composition of otoliths (Na, Sr, Ba, Mg, Mn, Cu, Y). Karyology: 2n = 38 (Sick et al., 1962, 1967; Chiarelli et al., 1969; Cucchi and Moritu, 1970; Passakas and Tesch, 1980; Passakas, 1981). Other investigations have revealed the existence of a distinct pair of heteromorphous female chromosomes (Ohno et al., 1973; Kang, 1974; Passakas, 1976; Park and Kang, 1979).

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Figure 1.10. Anguilla anguilla (2n = 38) chromosomes: 1–5 metacentric, 6–10 submetacentric, 11–18 acrocentric and a heteromorphic pair female (ZW) (according to Passakas and Tesch, 1980)

Indeed, Figure 1.10 shows five metacentric pairs (1–5), five submetacentric pairs (6–10), eight acrocentric pairs (11–18) and a female heteromorphic pair. The latter is composed of two metacentric chromosomes, a large (Z) and a small (W) one. Males have two Z chromosomes. Wiberg (1983) has questioned the presence of sex chromosomes. Passakas and Tesch (1980) examined the relationship between gonadal sex and genotypic sex in yellow eels. They claimed that sexual differentiation is not entirely dependent on the genotype. The phenotypic sex also depends on the density of the population, nutrition and/or other factors, such as salinity. Protein specificity and genetic diversity: Sick et al. (1967) showed the protein monomorphism of the European eel’s hemoglobin, while that of the American eel A. rostrata is polymorphic. De Ligny and Pante-Louris (1973), Williams et al. (1973) and Rodino and Comparini (1978) found differences between the allelic frequencies for the malate dehydrogenase of these two species. Avise et al. (1986) also found differences in mitochondrial DNA. Larvae of both species from the Sargasso revealed genetic differences corresponding to differences in the number of myomers (Comparini and Schoth, 1982). Jacobsen et al. (2014) estimated the divergence time of the two species at 3.38 million years, coinciding with the closure of the Isthmus of Panama, which led to the strengthening of the Gulf Stream. The serum protein frequencies in the transferring group are different, both between Atlantic and Mediterranean specimens, and between the eastern and western Mediterranean populations of A. anguilla (Drilhon et al., 1966, 1967). A study of enzymatic polymorphism also highlighted the heterogeneity of the Mediterranean and near-Atlantic populations (Rodino and Comparini, 1978b). On

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the other hand, with the same differentiation technique, Yahyaoui (1983) and Yahyaoui et al. (1983) found these homogeneous and considered them as having originated from the same “Sargassian” egg-laying area. The genetic structure of the eel remains controversial (Maes and Volckaert, 2007; et al., 2009; Pujolar et al., 2009). The first genetic studies using mitochondrial DNA (Avise et al., 1986; Lintas et al., 1998) or allozymes (De Ligny and PanteLouris, 1973; Comparini et al., 1977) did not reveal the genetic structuring of the A. anguilla. The hypothesis of a panmictic population was not retained by Daemen et al. (2001), Wirth and Bernatchez (2001) nor by Maes and Volckaert (2002), who proved a large-scale genetic differentiation using various genetic markers. Wirth and Bernatchez (2001), as well as Maes and Volckaert (2002), suggested the existence of a population subdivided into three subpopulations: the Mediterranean, the Atlantic and the North Baltic, interconnected by a large gene flow. The results of these studies showed signals that were associated with the clinal variation of allele frequencies, or to the haplotypic diversity related to distance isolation (Daemen et al., 2001; Wirth and Bernatchez, 2001; Maes and Volckaert, 2002). These results are consistent with the ocean circulation patterns distributing eel larvae in Europe and a clinal variation in the number of vertebrae (Boëtius, 1980). The maintenance of such a large-scale stable geographical structure would require not only active migration routes and different breeding grounds for the three subpopulations, but also a restriction in the intermingling of larvae during the drift within the Gulf Stream (Andrello et al., 2011). Studies analyzing the genetic structure only using eels belonging to the same cohort have targeted genetic differentiation on a smaller scale. These studies have shown that the temporal genetic differences between groups of glass eels recruited on the same site during the same year may be greater than the large-scale spatial genetic differences of the same recruited cohort (Dannewitz et al., 2005; Maes et al., 2006, 2009; Pujolar et al., 2006, 2007, 2009). In agreement with these observations, such small-scale genetic differentiation of glass eel waves would result from independent mating events, involving small groups of spawners separated by space or time (Maes et al., 2006; Pujolar et al., 2009). By studying the polymorphism of the cytochrome C oxidase region of the COI gene, Hassab El-Nabi et al. (2017) identified 14 haplotypes specific to the Burullus lagoon and 11 features typical of the Rosetta estuary in Egypt. They suggested considering these two environments as separate conservation units for the A. anguilla. In this context and looking for the origin of the genetic structure of the A. anguilla, Andrello et al. (2011) found that: 1) even a very feeble intermingling during larval dispersal or adult migration is sufficient to completely eliminate any genetic differentiation between subpopulations;

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2) temporal differences in small-scale recruitment may occur if the broodstock is subdivided into separate breeding groups; 3) geographic differentiation may be overestimated when a limited number of temporary recruits is analyzed. Taking these considerations into account, and in the absence of results based on appropriate sampling, the eel continues to be considered a panmictic species. 1.1.1.3. Distribution These are the species with wide geographical distribution (Figure 1.11). Its distribution limits according to Ege (1939) are: – to the north: until the North Cape and the Barents Sea (22°–30° N); – to the east: to the eastern Mediterranean and the Black Sea (48°–65° E); – to the south: as far as the coasts of Morocco and the Canary Islands (30° N); – to the west: to Iceland, Madeira and the Azores (20° W).

Figure 1.11. Geographic distribution of the A. anguilla

The European eel was introduced in Japan for the first time in 1968 for aquaculture purposes (Tabeta et al., 1977). 1.1.1.4. Ecology Habitat: Within its wide range, the eel visits coastal waters (coastal areas, estuaries, lagoons) as well as continental waters (rivers, lakes, ponds, marshes, reservoirs). Glass eels are also able to flourish in very salty environments, such as

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the hypersaline lagoons (40 g/L) of Tunisia (Lake of Tunis), Egypt (Bardawil) and South Sardinia (up to 70 g/L) (Rossi and Cannas, 1984). Pelagic leptocephali live only in the ocean and are located in the near-surface water layer (50–100 m) (Tesch, 1980). However, some larvae perform nyhtohemeral migrations and dive as soon as the sun rises to the deeper layers of water (Tesch, 1980). Only the mainland phase of the eel’s life is well known. The marine phase, particularly the one concerning the transoceanic migratory stage of the silver eel, remains hypothetical: marine trawling catches are certainly exceptional (Ernst, 1975). Only a few rare pieces of data provided by images filmed because of the Alvin American submarine are available (Robins et al., 1979). The tagging and tracking of silver eels released west of the European continental shelf (Tesch, 1978), as well as in the Mediterranean (near Gibraltar) and in the Sargasso Sea (individuals treated with pituitary extracts) (Tesch, 1989), have shown that they dive up to 700 m during the day. During the dark hours, eels swim quite near the surface. The direction of the monitored individuals was west/southwest. In brackish coastal waters and in fresh continental waters, eels reach the bottom with appropriate substrates in order to dig burrows where they can easily hide and move, freely shifting forwards and backwards, as well. Its smooth integument is advantageous for endogenous cryptic behavior. The glass eels prefer a particle size of 0.25 mm for the burrows, but they also show a preference for gravel larger than 2 mm, with interstices where they can penetrate (Lecomte-Finiger, 1979). Observations have revealed that eels stay in burrows or in hiding places during the day, but swim around during dusk and at night. They show almost no bathymetric preference, although younger individuals can be found in shallower waters than those frequented by adults (Neveu, 1981). Multiple observations have led us to admit to the existence of a certain sexual segregation in the occupation of habitats: males probably remain in the downstream part of rivers and salt lagoons, whereas the females, perhaps more sensitive to population pressure, might seek less competitive habitats and occupy the upstream part of river basins (Svardson, 1976; Vollestad and Jonsson, 1988). Migrations, displacements: The eel is the only large amphihaline and thalassotoc migrant in the Mediterranean. Its lifecycle is particularly complex, characterized by several metamorphoses, which can either be preliminary or consecutive to largescale migrations (Figure 1.12): 1) transatlantic migration of leptocephalic larvae; 2) (mounted) anadromous migration of larval eels;

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3) conquest of (freshwater or brackish) continental environments by the elvers and then, by the yellow eels; 4) catadromous (descent) migration of silver eels; 5) transatlantic migration back to the nesting area: the Sargasso Sea.

Figure 1.12. Lifecycle of the European eel (according to Michaud, 1996)

A photophobe fish, the eel especially, displays nocturnal activity. Therefore, its movements are difficult to observe, but in rivers, lakes and estuaries these have been specified because of tracking through markings: either metallic markings (Gundersen, 1979), colored markings (Cantrelle, 1984) or radionuclides (bromine 82, iodine 125) (Kruger, 1979) and through biotelemetry (radiotracking by ultrasonic transmitters) at sea (Tesch, 1974, 1978). The possibility of glass eels and eels crawling out of water makes it possible to conquer watersheds and water bodies isolated from the river systems, and it is one of the means of overcoming obstacles during anadromous migration (Legault, 1988). LaBar et al. (1987) studied local eel movements in a small lake in southwestern Spain (Acebrón, 1.2 ha). Individuals evolved in a surface ranging between 2,700 and 1,300 m2 and cover a wider space at night than during the day. The individuals monitored during rainy and cloudy weather were more active during the day and used a larger area than those followed during the dry season or during more stable weather conditions.

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– Leptocephalic migration: Leptocephalic larvae of the two eel species present at the Sargasso Sea are separated: geographical segregation (McCleave and Kleckner, 1987; McCleave et al., 1987) (Figure 1.13) for hydrological reasons, toward the European continents for one species (A. anguilla) and toward the Americas for the other (A. rostrata).

Figure 1.13.The respective egg-laying areas of the European eel and the American eel in the western Atlantic from the leptocephalic collections by three authors (according to McLeave and Kleckner, 1987)

The migration of the A. anguilla larvae from the Sargasso Sea to the European and African coasts was studied at the beginning of the 20th Century by Schmidt (1925), and then by Boëtius and Harding (1985). Research concerning larval distribution in the nesting area and assumed migration routes to Europe was conducted in 1979 and 1981 (Tesch, 1982a, 1982b; Kracht and Tesch, 1981; Tesch and Wegner, 1990). Hatching in areas with weak currents, leptocephalic larvae (size starting at 5 mm: Schoth and Tesch, 1984) are pelagic (–50 to –150 m: Tesch, 1980 and up to –500 m: Tesch et al., 1986), and gradually driven north-east, toward the European continent, because of the current of the Gulf Stream and the NorthAtlantic drift. The migratory journey involves more than a simple horizontal drift and supposes the existence of active swimming (Tesch, 1983, 1991), favoring vertical displacements according to a nychthemeral rhythm (at 50–100 m, then 30– 70 m deep during the night and 100–150 m, then 250–300 m deep during the day) (Schoth and Tesch, 1982, 1984; Castonguay and McCleave, 1987). Several branches of the Gulf Stream and the North Atlantic drift might enable (Figure 1.14) the differentiation of three populations (Boetius, 1980):

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Fishes in Lagoons and Estuaries in the Mediterranean 3A

– a northern population, pointing toward Iceland and Norway; – a central population in the direction of the British Isles, the French coasts of the Atlantic, the North Sea and the Baltic; – a southern population toward the coasts of Portugal, Morocco and the Strait of Gibraltar, that is to say, all the Mediterranean basin. These three populations can be distinguished by their number of vertebrae (respectively, 114.46, 114.51 and 114.74) (Harding, 1985).

Figure 1.14. Migration pathways of the leptocephali of the European eel (vertical lines) and American eel (horizontal lines) (according to Boetius, 1980)

Following Schmidt’s work (1925), it seems clear that the migration of larvae from about 26° N–60° W to Europe takes about 2.5 years. Boëtius and Harding (1985) did not confirm this hypothesis and estimated this duration at around 11–18 months. It is unmistakable that the duration of leptocephalic migration has remained controversial to this day. This duration ranges between 7 and 9 months, estimated from the interpretation of otolith microstructures, and more than 2 years, determined from cohort analysis, otolith microstructures and numerical models (Figure 1.15).

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Figure 1.15. Interval and average values (circle) of the European eel’s migration duration, according to different studies (from Bonhommeau et al., 2010). For a color version of this figure, see www.iste.co.uk/kara/fishes3a.zip

A recent review of the work on this question tends to favor the hypothesis of a long migration period (Bonhommeau et al., 2010). In light of current knowledge, these authors have expressed their reservations about the hypothesis of an active and oriented swimming ability, which might enable leptocephalic larvae to cross the Atlantic Ocean in less than a year: (1) fish larvae are not known to carry out large scale active migrations; (2) the required high speed is unrealistic (six somatic lengths per second for 35 mm larvae assuming perfect orientation); (3) the eel larvae do not have the necessary red muscles, able to support such a swimming speed; what is more, energy costs would be difficult to cover, given what is known about larval feeding and the low productivity of the tropical Atlantic. As part of his hypothesis, Schmidt (1924) considered that the leptocephali coming from the Sargasso Sea penetrated the Mediterranean Sea, which was confirmed by harvesting leptocephalic larvae on both sides of the Strait of Gibraltar, as well as in the western and eastern basin of the Mediterranean. When they reach a size between 60 and 70 mm, the leptocephalic larvae metamorphose into glass eels on the continental shelf. This metamorphosis might effectively take place during the migration from west to east linked to the general circulation of marine currents

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Fishes in Lagoons and Estuaries in the Mediterranean 3A

along the coasts (Lacombe and Chernia, 1972). The migratory movement of glass eels toward the northern Mediterranean coast (Adriatic Sea, Tyrrhenian Sea, Gulf of Genoa, Gulf of Lion) might take place along the currents that move upwards from the coast of North Africa, along Sicily and Italy, and to a lesser degree Sardinia and Corsica (LecomteFiniger, 1984). These data definitively invalidate the hypothesis put forward by Mazzarelli (1914) and Grassi (1914), concerning the existence of a Mediterranean spawning area. These last authors based their argument on ecological considerations, particularly those concerning certain similarities between the Ionian and Tyrrhenian seas and the Sargasso, and those on the harvest of some leptocephalic larvae, ranging between 30 and 50 mm, which are much superior to the ones collected by Schmidt in the Sargasso Sea (5–15 mm). The orientation of the ocean navigation of glass eels might be influenced by electric fields (weak: 10–4 at 10–2 A/cm2), generated by ocean currents (McCleave and Power, 1978). It does not seem to be influenced by terrestrial geomagnetism (Zimmerman and McCleave, 1975) but appears to be more dependent on chemical signals (Sola and Tongiorgi, 1998). – Glass eel migration: Eels or pibales, measuring around 6 cm and weighing 0.2 g, whose digestive tract is non-functional, are transparent at first (glass-eels, see Figure 1.16). They enter the littoral waters where they can stay (stabling is more or less prolonged, depending on the sites and seasons). Sensitive to the influence of desalinated continental waters (brackish estuarine, deltaic or lagoonal waters) at the ocean-continent interface, they search for the mouths of rivers, as well as the inlets of Mediterranean lagoons, even if oversaturated. Part of the stock settles in the lagoon and estuarine waters, while the other party is involved in the colonization of inland waters. Nevertheless, using the Sr/Ca ratio as a tracer (Secor et al., 1995; Tzeng, 1996), the otolith microchemistry has shown that some individuals might carry out their entire growth phase at sea (Daverat et al., 2004), at least in Atlantic Canada.

Figure 1.16. European eel elvers. Source: http://www.migrateurs-loire.fr/ quest-ce-que-le-programme-de-repeuplement. For a color version of this figure, see www.iste.co.uk/kara/fishes3a.zip

Anguillidae Jordan and Evermann, 1896

25

In the Mediterranean, the entry of glass eels in continental waters is carried out according to a seasonal periodicity, especially in winter (December–March). Places and authors Egypt (Paget, 1923) Lake of Tunis (Heldt and Heldt, 1929) Arno River, Italy (Gandolfi et al., 1984) Tiber River, Italy (Ciccotti et al., 1995) Mex Channel, Alexandria, Egypt (Ezzat and El-Serafy, 1977) Sagiada Lagoon, Greece (Zampola et al., 2008) Alfios River, Greece (Zampola et al., 2008) Gozlen River, Turkey (Kucuk et al., 2005) Fourcade inlet, Camargue, France (Lefebvre et al., 2003) Fourcade inlet, Camargue, France (Crivelli et al., 2008)

J

F

M

A

×

×× ×× ××

M

J

J

×

×

×

×

×× ×× ××

×

×

×

×

××

×

×

×

××

×× ××

×

×

×× ×× ××

×

×

×

×

×× ××

×

××

×× ×× ×× ××

S

O

N

D ×

×× ×× ×× ××

×

A

×

×

×

×

×

×

××

×

×

×

×

×

×

× ×

×

×

×

×

×

×

×

×

×

Table 1.1. Seasonal appearance of glass eels on the Mediterranean coasts (×: appearance, ××: maximum appearance)

In the Atlantic, tidal currents carry glass eels toward the coasts and to the estuaries (passive rise) (Deelder, 1958; Creutzberg, 1961), while in the Mediterranean areas where there are no strong tides, the entry of glass eels in lagoons and estuaries is active and occurs mostly at night (Lecomte-Finiger, 1976). The size and the age structure of migrating glass eels vary during the lagoon recruitment season. For example, for the glass eels caught between November 2000 and May 2001 at the Fourcade inlet (linking the Camargue Imperial and the Vaccarès ponds of the Mediterranean), the maximum abundances took place in January–February and, to a lesser extent, in April (Lefebvre et al., 2003). Monitoring the monthly proportions of the different pigmentary stages (from VA to VI A4) suggested a general aging of glass eels recruited between November and March, followed by the arrival of a second stream of young glass eels in April. At the same time, there was a marked decrease in monthly average masses and lengths, and this even considering only a given pigmentary stage (in this case, VB). The comparative analysis of these data with those obtained by LecomteFiniger (1976) for the “population” of the Bages-Sigean lagoon showed a completely different

26

Fishes in Lagoons and Estuaries in the Mediterranean 3A

monthly pigment composition and revealed a significant decrease in the length of glass eels of around 5% in 25 years. Zompola et al. (2008) analyzed the temporal migration patterns of glass eels on the west coast of Greece (the Sagiada marsh and the Alfios river) and found that it takes place simultaneously on the Atlantic coasts of southwestern Europe following the same pattern. However, the migratory dynamic is characterized by marked short-term fluctuations (migratory waves of 5–40 days) related to environmental factors, such as water temperature, atmospheric pressure, precipitation and the lunar cycle. A similar pattern is described by Lecomte-Finiger and Razouls (1981) regarding the Gulf of Lion, and by Ciccotti et al. (1995) with regard to the Tiber’s estuary. The seasonal and even the daily variations of the anadromous migration of glass eels have shown a clear influence of environmental, hydroclimatic and hydrometeorological factors. Temperature seems to be the key factor in this migration. In the wild, as in the laboratory, glass eels choose the coolest temperatures in comparison with the ones they are acclimated to, and which are actually the ones they encounter in nature (Tosi et al., 1988, 1990). The long-term effects of global warming, linked to Global changes, are likely to modify their anadromous migration behavior (White and Knights, 1997). Several field studies have indicated that freshwater migration and recruitment are negatively correlated with temperature (Elie, 1979; Cantrelle, 1981; Gascuel 1986; Vollestad and Jonsson, 1988; McGovern and McCarthy 1992; Elie and Rochard 1994; Martin, 1995; Jessop, 2003). On the basis of experiments, Edeline et al. (2006) concluded that low temperatures might trigger the migration of glass eels and their recruitment into the river, due to a reduction in locomotor activity and their preference for freshwater. They suggested that the temperature might engage thyroid hormones. In addition to this, a drop in the condition of glass eels reduces the preference for freshwater and increases the preference for salt water. Depending on the condition, this behavioral plasticity might have an adaptive signification, limiting mortality by exhaustion, due to energy expenditure, induced by the passage to desalinated water. Desalination is also an inducing factor in the rise of glass eels in estuaries and the mouths of coastal rivers (Tosi et al., 1988, 1989). Under experimental conditions, glass eels show a clear preference for freshwater over brackish or salty water; this salt-related factor clearly guides their choice and is more important than the thermal factor itself (Tosi et al., 1990). Their ability to detect small differences in salinity (5 ppm) enables them to adopt a guided approach toward inland waters during recruitment. In addition, a clear influence of salinity (desalinated water at 2.5–3.5 g/l) on trophic activity, and therefore, on the growth of glass eels, has been experimentally proved (Yahyaoui, 1983). By combining several environmental parameters in the Italian lagoon of Fogliano (temperature, salinity, dissolved oxygen, lunar cycle, availability of benthic prey), Leone et al. (2016) proved the existence of a relationship between

Anguillidae Jordan and Evermann, 1896

27

the spatiotemporal dynamics of recruitment and the settlement of young individuals (glass eels, elvers, yellow eels) and the environmental characteristics of the host habitats. The most influential factors are temperature and salinity. While the tide mainly acts at the sea–lagoon interface and does not orient the eels which are already inside the lagoon, the availability of prey does not seem to attract more individuals. Cosmic factors also play an important role in migration: there is a nychthemeral rhythm; in fact, anadromous migration begins during the hours immediately following sunset (Gandolfi et al 1980, 1984; Lecomte-Finiger, 1976). However, no lunar influence was detected. Bardonnet et al. (2005) found that with age, the light sensitivity of glass eels decreased, and that light avoidance was less stressed in unpigmented glass eels than in pigmented ones. This sensitivity might condition their migration as well as their vertical distribution in the water column, with consequences on the estimation of their abundance depending on fishing depths (Creutzberg, 1961). At the Fourcade inlet, in connection with the Vaccarès lagoon, Crivelli et al. (2008) suggested that it is essential to let the lagoons receive rainwater runoff from their watersheds. The elevation of their levels in winter, associated with the Mistral wind, carries low salinity water toward the sea, which favors the recruitment of glass eels. Local factors also play a role: odors or odor bouquets (especially the odors of decaying plant debris) are likely to play an attractive role (Sorensen, 1986). Another attractive role comes from conspecific chemical signals, as shown by experimental studies (Tosi et al., 1990). These signals are epidermal pheromones emitted by yellow eels, established upstream of watercourses (Pesaro et al., 1981; Saglio, 1982). Transparent eels progressively become pigmented because of the development of cells enriched with melanic pigment (black), and thus become pigmented glass eels (elvers). In agreement with different authors, such metamorphosis ends with the completion of melanophore development (Elie et al., 1982). Other types of reorganization accompany this loss of transparency: (1) structural, with the development of teeth, the modification of the digestive tract (resorption of shutter valves) (Elie, 1979) and the settlement of trophic activity (Lecomte-Finiger, 1983); (2) anatomical, with the differentiation of musculature, through an increase in diameter and in the number of fibers of the lateral musculature (Willemse and Lieuwma-Noordanus, 1984); (3) sensory (visual and olfactory) and physiological, with a change in the level thyroid hormone production (Monaco et al., 1981, Yamano et al., 2007) and in osmotic control capabilities (Sasai et al., 2007). These changes continue during estuarine migration and at the beginning of lagoon life. The gaseous bladder remains non-functional during estuarine migration (Hickman 1981). After this first stage of subcontinental evolution, the scarcity of available studies does not allow us to provide details about the physiological, morphometric and behavioral changes that influence the migratory mode of river colonization.

28

Fishes in Lagoons and Estuaries in the Mediterranean 3A

– Relative sedentarization of glass eels and yellow eels: Young eels that have reached a suitable habitat tend to become sedentary, but they can make more or less, sometimes seasonal moves, depending on hydroclimatic conditions. The stay in brackish and even hyper-haline lagoon waters and in fresh continental waters may span between 3 and 12 years, and sometimes even 20 years. This favors a more or less rapid growth and an accumulation of energy-giving reserves (especially lipids), prior to the large reproductive migration back to the nesting area. The ecological preferences of the yellow eel, in terms of habitat, were specified by Pouilly (1994). An example was given by Rossi et al. (1987): three groups of yellow eels from the Po Delta (605 from Pila, 664 from Scardovari, 401 from Goro) were tagged and released 5 nautical miles offshore. Out of the 1670 tagged individuals (mean TL between 26.6 and 33.4 cm), 9.8% were fished over a 1-month period. Among the latter, 75% were caught in the nearest inland waters (9 km) from the release point and 8.6% at the mouth of the two branches of the Po River. However, there is no evidence that there is a real trend toward the homing of individuals, which previously adapted to brackish water. According to the authors, the massive return to the near-shore might only be a way of avoiding the relatively unfavorable conditions of the open sea. From the microchemical analysis of Sr/Ca ratios in otoliths of 56 individuals from three Italian transition environments at the same latitude, Caprolace lagoon (N = 21), Lesina lagoon (N = 20) and the Tiber estuary (N = 15), Capoccioni et al. (2014) showed that in all the sites considered, the fraction of resident eels is significant (between 60 and 85.7%), but that the proportion of nomadic individuals varies according to the environment. According to these authors, the user profile of different habitats is related to local ecological conditions: nomadic behavior seems to be affected by food availability rather than by the salinity gradient. This consideration reinforces the hypothesis that the “optional catadromy” of the eel at the Mediterranean and the trophic changes shown by this species depend on the productivity of the environment rather than on salinity. The movements of the yellow eel within its territory (home range) could be retraced because of various marking techniques. Through radiotelemetry, Baras and Jeandrain (1998) revealed a relative sedentarity of the eel, with a return to a diurnal place of residence corresponding to a highly structured cryptic habitat, with variable surface area (0.01–0.1 ha). As previously suggested, such fidelity to a given territory was interpreted as due to dependency on food resources and hunting strategies related to intraspecific competition. Motor activity responds to a nychthemeral cycle. It is essentially nocturnal; eels leave their habitats as soon as the sun sets. There is also a decrease in activity at temperatures below 13°C and an increase with increasing temperatures. In addition, there are variations related to the lunar cycle, with greater “agitation” during the full moon (Baras et al., 1998).

Anguillidae Jordan and Evermann, 1896

29

– Migration of silver eels: At a certain age and size, and this varying greatly depending on the site, immature yellow (green) eels undergo an anatomical and physiological evolution corresponding to the metamorphosis into silver eels (third metamorphosis: leptocephalus/glass eel, glass eel/yellow or green eel, yellow eel/silver eel with a pre-adaptation value (or anticipatory adaptation according to Fontaine, 1989) to a meso-bathypelagic marine life (–600 to –2,000 m). These transformations concern: - skin changes: (1) the skin becomes thicker, more elastic (rich in collagen fibers) and richer in mucus cells (Saglio et al., 1988). This mucus shows differences in the concentration and chemical composition of glycoproteins between yellow eels and silver eels (Saglio and Fauconneau, 1988): the concentration of free amino acids is higher in yellow eels and three of these amino acids (taurine, glycine and alanine) decrease with the evolution toward silver eels; these changes possess an intraspecific chemical communication (pheromone attractiveness); (2) a change in the color of the integument takes place. The back darkens (it becomes rich in melanophores), the flanks and belly become poor in xanthophores (yellow pigment) and turn silverywhite due to the extension of purine-enriched guanophores (guanine and hypoxanthine), which are responsible for silvering; - muscle modifications: an increase in muscular volume is due to muscle differentiation and reorganization (increase in the number and the size of the fibers of the white muscles because of hyperplastic and hypertrophic mechanisms). On the other hand, there is an increase in the volume of red muscles (due to an increase in the diameter of the fibers and their reorganization), which can range from 5% in the immature eel to >13% in the more sexually mature eel (Pankhurst, 1982b). These changes are coupled with a development of enzymatic glycolysis capabilities, all of which translates into an increase in their swimming abilities; - a certain involution of the digestive tract generating a strict fasting throughout the reproductive migration and until the end of the lifecycle. Some tissue and cell changes take place. These are unrelated to digestion, but to osmoregulation as a response to a demineralization situation, which is responsible for hypotonicity (Fontaine, 1994). On the one hand, there is a transformation of the oesophageal epithelium which, having been pluristratified and rich in mucus cells in the freshwater eel, becomes unistratified and poor in mucus cells in the marine eel. These tissue and cell changes favor the acquisition of a selective permeability to Na+ and Cl– ions as a part of a necessary regulation of the hydromineral balance (Laurent and Kirsch, 1975); - an osmotic balance, which is reached because of the absorption of water by the digestive tract, following water loss and an increase in ion concentration in the blood, after the passage to seawater. The intestine, kidneys and gills eliminate the

30

Fishes in Lagoons and Estuaries in the Mediterranean 3A

ions. Mucus is more abundant and the skin thickens in order to reduce water loss (Fontaine, 1975). A branchial specialization through the differentiation of many ionocytes or chloride cells makes osmoregulation possible because of Na+ and Cl– ion excretion mechanisms (Fountain et al., 1995). The development of these cells (Sargent et al., 1978), rich in mitochondria (ATP-producing) and in endoplasmic reticulum (synthesis of Na enzymes+-K- ATPases), and which have a pre-adaptation value (preparation for marine life), is controlled by the endocrine system (growth hormone or GH, thyroid hormones T3 and T4, cortisol). However, Aroua et al. (2005) concluded that the thyrotropic axis is not, or is only moderately, involved in silvering; - an increase in hematocrit values (Johansson et al., 1974) and vascular revisions, characterized by an increase (5×) in the capillary network or rete mirabilis, which enables an intensification of gas (Kleckner and Krueger, 1981) and pigmentary exchanges in the gas bladder (guanine enrichment that decreases gas conductance, that is to say, a reduction in diffusion losses). The physiology of the gaseous bladder, an organ intended to present a strong gas pressure at great depth, is based on the production made by the bladder’s epithelium, CO2 and lactic acid from glucose (anaerobic glycolysis) (Pelster and Scheid, 1991). Pelster (2015) gave a review of the functioning of the eel’s gas bladder during their oviposition migration; - a development of sensory abilities, with an increase in the diameter (5×) and the surface of the eye (Bertin, 1951; Stramke, 1972; Pankhurst, 1982b), a decrease in the number of cones in the retina due to degeneration (Pankhurst, 1982a) and changes in retinal pigments, related to the replacement of rhodopsin and porphyropsin by chrysopsin (Archer, 1998). The number of cone cells decreases and the number of rods increases (2×), varying from two to four layers (Es-Sounni et al., 1987), favoring a monochromatic and scotopic vision. The lateral line becomes visible and the number of sensory cells increases (Zacchei and Tavolaro, 1988). Pankhurst and Lythgoe (1983) and Sorensen and Pankhurst (1988) showed that olfactory cells and associated mucus cells degenerate in males and females after the hormonal induction of sexual maturation, which suggests that olfaction becomes less important. However, later during sexual maturation, the development of sensitivity to sex pheromones is probably involved in the expression of sexual behavior; - an accumulation of energy reserves to meet migratory needs (swimming) and gonadal development; these two functions mobilize 75% of stored energy. The reserves are essentially (80%) lipidic in the form of triglycerides, which are mainly accumulated in the muscle tissue (white muscle) and also in the liver; these deposits are then (partly) redistributed to the gonads. This accumulation of fat occurs specifically during the acquisition of silvering, since eels mainly accumulate glycogen (Barni et al., 1985); between these two stages, it increases by 8–28% (Bergersen and Klemetsen, 1988; Larsson et al., 1990). Lipids are in direct contact

Anguillidae Jordan and Evermann, 1896

31

with the muscles (Fontaine 1975, Pankhurst 1982a); they are also stored under the skin and in the liver. However, the silvering process and the moment of catadromic migration may not coincide with the acquisition of the optimum reserves; - progressive bone resorption due to osteoclast activity in vertebral tissues, favoring a Ca2+ recycling that benefits the ovary (as co-factor of vitellogenesis); - activation of the endocrine glands: the hypophysis (GH), the thyroid (T3 and T4), the interrenal (cortisol), as well as a correlative regression of the pituitary gland’s prolactin secretion (PRL) (Olivereau and Olivereau, 1977). On the other hand, the rate of pituitary gonadotropins (GtH) remains particularly low in immature eels (2– 100 ng/mg fresh hypophysis, 1,000 times lower than the rate of the Cyprinus carpio hypophysis carp), which reflects a shortfall in the gonadal stimulation by the pituitary gland during the continental lifelong phase (Dufour et al., 1983). On the other hand, the gonads show a weak development and the silver individuals remain sexually immature. Their gonadosomatic index (GSI) increases slightly (0.38–1.86), distant from the one reached during maturity (30 at least) (Fontaine, 1989). Maturation is not correlated with age, but rather with size, and is mostly related to growth and to the accumulation of energetic reserves, which are necessary for the genital maturation that will take place as soon as the earliest opportunity arises (Svedang et al., 1996). In males, differentiation takes place at the same time as silvering, whereas female gonads become different far earlier (Colombo et al., 1984; Durif et al., 2005). Although “yellow and silver” have been described as two separate stages, the silvering process is actually gradual. Durif et al. (2005) could distinguish five different stages in 1,188 females fished in six localities in France, corresponding to different types of hydrosystems. For each of the individuals examined, a profile had been previously defined based on morphological and physiological characters. Thus, the silvering process is described as follows: stages I and II correspond to the yellow stage, separating sexually undifferentiated individuals (stage I) from females (stage II). At these stages, eels have undeveloped gonads with a GSI of 0.5% at most. There is still no production of vitellogenin or gonadotropin. Silvering is initiated in stage III, when vitellogenin significantly increases (P < 0.05). The level of GH reaches a maximum at this stage, suggesting a high growth rate before or at the start of silvering. The GSI of these presilvered eels is about 0.8%. The diameter of the eye also increases significantly (P < 0.05) and the average eye index is 7.6. The silver migratory stage is reached at stages IV and V. The levels of vitellogenin and GtH-II reach their maximum, as during gonad development. The digestive tract regresses significantly (P < 0.05) and the fish probably stop feeding. The eye index is about 1.0. The length of the pectoral fin continues to increase between stages IV and V. However, GH decreases significantly as from stage IV, suggesting that at this stage eels stop investing in somatic growth in favor of sexual maturation.

32

Fishes in Lagoons and Estuaries in the Mediterranean 3A

At the silver stage, eels seek to migrate to the sea. Migration begins in late summer or fall, which might allow them to reach the Sargasso sea-spawning area by the following spring. Their swimming speed is 2 km/h. Migratory activity is more intense during the night, but especially during the first hours of darkness (Bertin, 1951, Bräutigam, 1961) and for several authors, it is exclusively nocturnal (Winter et al., 2005; Westerberg et al., 2007; Aarestrup et al., 2008; Billota et al., 2011). According to the fishing statistics of lunar months, it is also clear that the peak of activity takes place at the time of, or a few days after, the last quarter (Figure 1.17) (Renström, 1979).

Figure 1.17. Average frequency of silver eels fished in different environments during the lunar month (according to Renström, 1979)

Anguillidae Jordan and Evermann, 1896

33

The participation of Mediterranean silver eels’ egg-laying at the Sargasso Sea was questioned by Ekman (1932), who considered that the Mediterranean operates as “an eel trap”. No silver eel catch in the vicinity of Gibraltar has made it possible to contradict this hypothesis. However, the “Sargassian” migration of Mediterranean eels has been generally accepted (Lecomte-Finiger, 1984). Because of tagging, Anilhat et al. (2016) have recently been able to reveal that Mediterranean eels can cross the Strait of Gibraltar. By simulating the optimal spawning migration conditions of eight silver eels (five females and three males, 4–11 years) caught in the Strait of Sicily, Capoccioni et al. (2014) suggested that only a small quota of Mediterranean males could reach the Sargasso Sea, and that only females from the central and western Mediterranean were able to reach it and lay their eggs. – Sea migration: Transoceanic migration of future spawners might occur at depths ranging from 600–700 m to 2,000–3,000 m. Information on migratory routes and the behavior of silver eels after leaving continental waters is still rare. Two migratory routes toward the Sargasso have been suggested: a migratory route to the North via the central Atlantic Ocean (Tesch, 1986) and a route toward the South via the Azores current (Fricke and Kaese, 1995). In the latter case, the estimated duration of migration from simulation ranges between 4 and 6 months and is congruent with the period of departure of silver eels from Europe (September to November), and the first catches of the smallest larvae recorded in the Sargasso Sea range between February and June. The beginning of silver eel migration toward the sea has been studied by conventional tagging (Westin, 1990) and by telemetry (Tesch, 1989; Westerberg et al., 2007; Wysujack et al., 2015) in the Baltic Sea, the North Sea, the North-East Atlantic and the Mediterranean. In the western Mediterranean, Bianchini et al. (2009) reported the capture of seven silver eels in two localities in the Strait of Sicily, 500 km apart from each other, at a depth of between 300 and 650 m. The tracking of silver eels for 6 days after their release near Gibraltar has shown that they rise at dusk and go down at dawn, making a medium horizontal movement at a speed of 0.3 m/s, but no exit through Gibraltar has been recorded (Tesch, 1989). In contrast, out of eight silver females carrying pop-up satellite tags, released in the coastal waters of Roussillon (French Mediterranean), two crossed the Strait of Gibraltar in depth and were followed throughout the Atlantic for around 2,000 km from their point of departure, the duration of the trip having lasted for 6 months (Amilhat et al., 2016). In the North-East Atlantic, the average minimum migration speed is 1.5–17 km/day with vertical nychthemeral movements, which oscillate between 300 and 1,000 m (Wysujack et al., 2015). According to these authors, silver

34

Fishes in Lagoons and Estuaries in the Mediterranean 3A

eels released at the Sargasso Sea occupy greater depths and a wider range of temperatures than those at the Northeast Atlantic. The problems of orientation and navigation toward the Sargasso Sea remain unclear and various factors have been suspected: temperature (Westin and Nyman, 1977), light (Tesch et al., 1992), electric and terrestrial magnetic fields (Karlsson, 1985; Hanson et al., 1984), olfactory recognition, etc. Studies have suggested that there is a geomagnetic basis for the eel’s orientation during its long Atlantic crossing (Tesch, 1974; et al., 1992). Hanson et al. (1984) and Hanson and Westerberg (1986) measured the “magnetic” sensibility of the skull and spine. They concluded that the distribution and composition of the magnetic material in the fish is insufficient to justify magnetic orientation. In contrast, Moore and Riley (2009) proved the presence of biomagnetite in the mandibular canal region of the lateral line, which makes it suitable for a good magnetoreception. In addition, an imprint acquired during the leptocephalic transatlantic trip is suspected. In fact, silver eels deriving from transplanted glass eels for restocking and rearing are unable to find a proper return migration route (Westin, 1990). Whatever the factors of orientation toward the Sargasso, the duration of this transatlantic trip might last around 5 months, which would correspond to a maximum swimming speed of 40 km/d. This transatlantic migration ends at the Sargasso Sea, at the level of a thermal front located between 24° and 29° North latitude, in the vicinity of the subtropical convergence, a marine zone where temperature and salinity are constant. Van Ginneken and Van den Thillart (2000) provided the first estimate of the energy cost of oceanic eel migration. They concluded that energy reserves are sufficient for migration and reproduction. The displacement cost, deduced from various studies (Palstra and Van den Thillart, 2010), oscillated between 11.5 and 17.5 milligram of fat per kilogram of somatic weight and per traveled kilometer. The average energy cost of reproduction is estimated at 57 ± 22 g of fat per kilogram (Palstra 2006, Palstra and Van den Thillart 2010) for GSI of 60%. – Ecological valence: Eel larvae are among the most delicate organisms. In contrast, yellow and silver eels are comparatively more resistant to different environmental stresses. Their tolerance to salinity and their ability to survive exposed in the open air (Tesch, 1983) are well known. Glass eels tolerate low oxygen concentrations of approximately 2 mg/L at a temperature of 15°C (Gritzke, 1980). Silver eels can be stored in ponds at high densities for months. Mann (1960) stored fasting eels for 4 months in aquariums filled with fresh water. Boëtius and Boëtius (1967) kept silver eels that reached sexual maturity after a fasting period longer than 3 years. These same authors showed that the survival thermal amplitude

Anguillidae Jordan and Evermann, 1896

35

is between 0 and 30°C. Sadler (1979) reports a lethal temperature of 38°C for both yellow and silver eels. Fischer (1977) confirmed the eel’s ability to fast, while Gadeau De Kerville (1918) tested their resistance out of water (168 h at 6.5°C). – Size, lifespan and growth: The standard European eel usually measures up to 1 m (maximum 1.50 m) and weighs up to 3 kg (maximum 4 kg). An eel measuring 148.7 cm TL and weighing 5.54 kg, fished in a Croatian river in 2006, is considered the largest known specimen (Tutman et al., 2007). The age of the A. anguilla is limited by the fact that after laying eggs in the Sargasso Sea, its lifecycle is complete. However, if its migration is prevented, it may live to a fairly advanced age (Walter, 1910; Tesch, 1983). According to otolithometric observations, its lifespan can extend from 3 to 18–20 years (4–11 years in the Mediterranean). Males stay in the fresh, lagoonal waters between 3 and 15 years, whereas females stay there for up to 20 years. Cases of larger lifespan (24, 30, 37 years) have been observed in captive Atlantic eels. The age of 50 was reached in a Swiss lake without an outlet, whereas it was 55 years old in Denmark, 57 years old in Ireland (Poole and Reynolds, 1998) and even 85 years old, according to Feunteun et al. (2011). The question of whether spawners survive spawning remains unresolved. Schmidt admitted that the Sargasso Sea was both their cradle and their grave, but at the laboratory, experimentally induced maturation and spawning were followed by a survival of spawners (Delerue-Le-Belle et al., 1982). Because of direct (individual labeling with tetracycline at a natural pond in the Camargue) and indirect methods (observation of the marginal appearance of growth marks over time in the case of Languedoc and Camargue populations), Panfili and Ximénès (1994) validated estimates for the age of Mediterranean eels from otoliths: a broad opaque zone is mainly formed in the spring, a broad hyaline zone is deposited during the summer months and a chromophilic “growth stop line” corresponds to the winter period. Otolithometry techniques were also applied to glass eels (Lecomte-Finiger, 1983a, 1992b) and yellow eels (Lecomte-Finiger, 1992a) in the lagoons at the Gulf of Lion (Narbonnais and Roussillon). The microstructure of the glass eel’s otolith, analyzed by a scanning electron microscope (Lecomte-Finiger and Yahyaoui, 1989), revealed the history of larval life (hatching, first food intake, growth of the leptocephalus during the marine life phase, the metamorphosis to glass eels and the transition to continental life). The growth of glass eels is due to the resumption of food activity at the VIA3 stage (fully pigmented elver). It is faster during the summer months. Yahyaoui (1983) showed that this is closely related to temperature and desalination; the optimum growth might take place at 22–23°C (Sadler, 1979). Supernumerary stunting rings are visible in the otolith of samples captured in the Mediterranean lagoons in the Gulf of

36

Fishes in Lagoons and Estuaries in the Mediterranean 3A

Lionet and appear to be related to summer dystrophic crises (Lecomte-Finiger, 1985). Taking into account the inconsistencies between the nesting period determined from the larvae sampled at sea and the ones revealed through otolith analysis, McCleave (2008) questioned the value of daily growth streaks for determining the age of eel larvae. According to different authors, the metamorphosis age may vary between 159–212 days (Lecomte-Finiger, 1992; Désaunay et al. 1996a, 1996b; Arai et al., 2000) and 318–397 days (Wang and Tzeng, 2000). In the Mediterranean lagoons in the Gulf of Lion, eel growth is significant from April–May to October–November (Lecomte-Finiger, 1983a, 1985). A growth disharmony between the two sexes is classically observed, as shown by the example of the populations of the Adriatic lagoons of Lesina and Varano (Rossi and Villani, 1980) (Figure 1.8). Indeed, as suggested by Panfili et al. (1994) and Melia et al. (2006) in the Camargue lagoons, females reach larger sizes and generally grow faster than males. However, these differences are difficult to detect in the early stages of development of eels and yellow eels, because gonad differentiation takes place when they reach a size of 15–25 cm, and also due to the existence of precocious intersex (Colombo et al., 1984). Holmgren et al. (1997) observed a high rate of growth in females after the completion of sexual differentiation. Somatic growth showed large variations at different scales: interindividual variations within the same population, and geographical variations between different habitats (Panfili et al., 1994; Leo and Gatto, 1995). A classification based on 17 different eel populations revealed that growth is better in brackish water than in freshwater, but that latitude also has an influence (Ferandez-Delgado et al., 1989). Panfili and Ximenes (1994), Acou et al. (2003) and Melia et al. (2006) also showed that growth in brackish environments is significantly higher than in freshwater environments. Capoccioni et al. (2014) compared the growth of eels in three transition environments in Italy (Caprolace and Lesina lagoons, Tiber estuary), located at the same latitude. The annual growth rate is higher in Lesina and Tiber, which are relatively productive, in comparison with the oligotrophic lagoon of Caprolace. Melia et al. (2006) studied the growth of male and female glass eels in the Vaccarès and Impériaux lagoons (Camargue, France), using samples fished between 1993 and 2003. The average size of glass eels is between 60 and 65 mm, whereas in the case of adults (both sexes), it ranges between 200 and 400 mm TL. It appears that males are rarely larger than 400 mm, whereas females are significantly larger (Figure 1.18).

Anguillidae Jordan and Evermann, 1896

37

Figure 1.18. Distribution of the total length of 18,300 European eels fished between 1997 and 2003 at the Vaccarès and Impériaux lagoon systems: a) whole sample, b) by sex (undifferentiated represented by the dotted line, solid gray the males, and the females in continuous line), c) by stage of sexual maturity (yellow in continuous line, silver in solid gray). The frequency refers to the total number for each type of size (amplitude 30 mm) (according to Melia et al., 2006)

On the other hand, yellow eels are rarely bigger than 300 mm in size, whereas the silver eels have a bimodal distribution, with a first mode at 350 mm and a second one at 600 mm, respectively, corresponding to mature males and females. The age distribution of a sample of 291 eels fished between 1997 and 1998 is given in Figure 1.19 (Vaccarès and Impériaux).

38

Fishes in Lagoons and Estuaries in the Mediterranean 3A

Figure 1.19. Age distribution of 291 European eels sampled between 1997 and 1998 in the Vaccarès and Impériaux lagoon system: a) whole sample, b) differentiated by sex (undifferentiated dashed, male in solid gray, females in solid line). The frequency is relative to the total number in each size class (according to Melia et al., 2006)

The majority of eels undergo sexual maturation after 2–3 years of residence in the lagoon. Females remain in the lagoon for more than 5 years, whereas males do not stay there longer than 3 years. The growth parameters of the von Bertalanffy model, as well as those regarding the length–weight relationship obtained at the Mediterranean, are given in Table 1.2. In the Camargue, Melia et al. (2006) highlighted significant differences concerning relative growth between sexes and sexual maturation stages. In terms of size/mass relationships, silver eels have the lowest “a” and “b” values, which may indicate certain weight loss due to metamorphosis (gonad development and fasting). The value of “b” is higher in females, whereas the value of “a” is higher in males. These authors also showed interannual variations in “a” and “b” parameters. Parameter “a” has greater variability than “b” (variation coefficient VC = 39 and

Anguillidae Jordan and Evermann, 1896

39

2%, respectively). Parameters “a” and “b” are linked by a clear negative correlation (r = –0.95; P < 0.01). The value of “b” is also negatively correlated to the total length of eels for the same year (r = –0.58; P < 0.01), but it is positively correlated to the value of “a” (r = 0.40, P < 0.01). Analysis of the relationship between the length–weight of silver eels, following a latitudinal gradient (six countries: Denmark, Ireland, England, Belgium, France, Spain; 13 watersheds) showed significant differences between and among watersheds, probably implying differences in stoutness. This could suggest that the ability of eels to migrate and breed varies depending on the site (Boulenger et al., 2015). Places and authors

Sex or Age stage (years)

N

a

b

L∞ (cm)

K

to

Valle Nuova Lagoon, Italy (Rossi and Colombo, 1976)

-

10

100

-

-

87.2 0.1873

-

Comacchio Lagoon, Italy (Rossi and Colombo, 1976)

-

11

212

-

-

73.6 0.1290

-

Lagoon of Porto Pino, Sardinia (Rossi and Cannas, 1984) Monaci Lagoon, Italy (Ardizzone and Corsi, 1985) Kinneret Lake, Israel (Golani et al., 1988)

F M

10

110 3.3 × 10-4 3,405

72.8

0.336 –0.35

150

0.0242

2,299

50.1

0.337 –0.31

-

5

469

0.002

2.92

42.1

0.391

– 0.001

-

4

32

4.04 × 10-6

2,917

-

-

-

97.0

0.5–8.5 Camacchio Lagoon, Italy (Castaldelli et al., 2013)

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

4.5– 10.5

565 0.00026 3,491

0.157

-

2,780 125.97 0.124

-

Mixed

0.5– 10.5

925 0.00087 3,223 155.94 0.087

-

-

-

103

-

Yellow Silver

360

0.006

0.0006

3,266

-

-

Table 1.2. Absolute (L∞, K, to) and relative (a, b) growth parameters of the Anguilla anguilla in different Mediterranean lagoons

In addition to male- and female-specific growth patterns, for eels remaining at a sexually undifferentiated stage between 2 and 3 years, Melia et al. (2006) suggested

40

Fishes in Lagoons and Estuaries in the Mediterranean 3A

a third curve so as to describe the growth of undifferentiated eels. This curve takes into account in its mathematical expression the length and age during sexual differentiation. According to these authors, in the Camargue lagoons, the females are characterized by an asymptotic length, greater than that of males (580 ± 50 and 388 ± 13 mm respectively) and growing faster, while the growth rate is higher in males than in females (3.00 × 10–3 and 1.73 × 10–3, respectively). Sexual differentiation begins at 204 ± 38 mm, that is to say, at the end of the second year of life in the lagoon, well before the length at which macroscopic differentiation becomes possible (300 mm). Experimentally, Kuhlmann (1975) obtained optimal growth at a temperature of 26°C and Sadler (1979) at 22–23°C. Under breeding conditions, in Italy, Deelder (1981) found that males can grow 12 cm/year and females can grow 17 cm/year, and the silver stage being reached between 2 and 4 years. Then, their average size is 44.5 and 59.8 cm, respectively. – Structure and population dynamics: Studies on the dynamics of eel populations are rare. The recruitment of glass eels takes place later in the Mediterranean than in the Atlantic (Lecomte-Finiger, 1983). Interregional variations in recruitment depend not only on the arrival of leptocephali and their metamorphosis to elver on the continental shelf, but are directly related to local hydrological and hydrodynamic conditions. At the mouth of Moulouya (Morocco), the rise is the result of abundant fall season rains that cause a considerable increase in the river flow (Yahyaoui, 1983). Similarly, in Port-la-Nouvelle (Bages-Sigean lagoon), the outflow of a desalinated current, induced by northwesterly winds, is attractive for glass eels (Lecomte-Finiger, 1983). Nevertheless, elvers penetrate the lagoon all year round with a slowdown, or even a total stop, in summer (Finiger, 1976). At Mediterranean sites (Moulouya and Port-la-Nouvelle), the beginning of the recruitment season is characterized by the exclusive presence of transparent glass eels (from VA to VIA2, according to Elie et al., 1982). Pigmented elvers (VIA4-VIB) are only found at the end of recruitment; on the other hand, at the Atlantic (Sebou estuary), the two categories are simultaneously present, even at the beginning of recruitment (Yahyaoui, 1988). In the Sardinian lagoons of Porto-Pino, 60% of the fish caught are females and 90% of the sampled eels are at the silver stage, that is, around 5 years old (Rossi and Cannas, 1984). Silver males, aged 5.1 ± 0.5 years on average, measure 41.5 ± 2.6 cm and weigh 128 ± 21 g. Females, aged 6.4 ± 1.2 years, measure 58.5 ± 6.6 cm and weigh 370 ± 146 g. In the lagoon of Monaci (Italy), four age classes were identified (Ardizzone and Corsi, 1985). With regard to yellow undifferentiated eels, size frequency distribution (Figure 1.20) showed an average length of 25.35 ± 2.35 cm and 28.72 ± 2.22 cm for males and 40.37 ± 7 for females.

Anguillidae Jordan and Evermann, 1896

41

Figure 1.20. Size frequency distribution of silver and yellow eels at Monaci lagoon (according to Ardizzone and Corsi, 1985)

On average, silver eels measured 31.48 ± 2.57 cm. The sex ratio of yellow eels (undifferentiated individuals obviously being excluded, that is 53% of yellow eels) was 96.3% for males and 3.7% females. With regard to silver eels, males represented 95.8% and females represented 4.2%. Age structure showed a dominance of the 3-year olds for silver eels, as well as for undifferentiated individuals (26.1 ± 1.95 cm) and for males (28.6 ± 2.0 cm). A certain amount (11% out of the total number of yellow eels) in the undifferentiated group belonged to the 2-year-old group (23.1 ± 1.8 cm). Among silver eels, 3-year-old (30.8 ± 1.9 cm) and 4-year-old (33.6 ± 2.9 cm) males were the most frequent (Ardizzone and Corsi,

42

Fishes in Lagoons and Estuaries in the Mediterranean 3A

1985). In the Bages-Sigean and Canet-Saint-Nazaire lagoons, eels were between 1 and 12 years of age (15–97 cm TL) and 1 and 10 years of age (17–60 cm TL), respectively. Age group 3 dominated (34.2%) these two lagoons (Mallawa and Lecomte-Finiger, 1992). At the Vistonis (Greece) freshwater lake, the eel population was exclusively made up of silver females ranging from 68.7 to 113.8 cm in size (Macnamara et al., 2014). Table 1.3 provided a structure of eel populations in different regions of the Mediterranean.

Authors

Places

Rossi and Lesina and Varano Villani (1976) lagoons, Italy

Gatto and Rossi (1979)

Comacchio Lagoon, Italy

Total population Dominant age groups Dominant age Length Age Lengths groups Ages (cm) group (cm) (%) 1–5

28–47

I–III

1–14

Yellow eel I–III 26–80 Silver eel IV–VII

35–45

-

25–29 41–59

Ardizzone and Corsi (1985)

Poontin Lagoon, Italy

1–5

23–46.5

II–III

25–33

90

Purwanto (1981)

Piemanson, Camargue, France

1–4

17–49

I–II

17–21

-

GIS ARM (1986)

Languedoc, France: Mauguio lagoon Vic Lagoon Vaccarès lagoon

1–6 1–4 1–6

15–80

I–II I–II I–II

15–25 25–35 15–34 14–30

84–95 72 90 90

Mallawa (1987)

Narbonnais Roussillon, France: Bages-Sigean lagoon Canet lagoon

1–12 1–10

15–97 17–60

II–IV

23–34

75 80

Panfili (1988)

Languedoc, France: Vaccarès lagoon Mauguio lagoon Vic Lagoon

1–5 1–7 1–3

23–56 28–46 26–37

I–II

-

-

Table 1.3. Structure of eel populations in different Mediterranean regions (according to Mallawa and Lecomte-Finiger, 1992)

Anguillidae Jordan and Evermann, 1896

43

Predators: Eel predation is significant at the leptocephalic and glass eel stages. Predators are marine mammals such as whales (Vaillant, 1896), marine fishes such as myctophids and estuarine fish such as sticklebacks (Daniel, 1965). Predation is lower, but not negligible, at the elver and yellow eel stages by ictyophagous birds (cormorants, herons, grebes, seagulls, etc.) as well as by mammals (otters). According to Moriarty (1978), predation by the European conger Conger conger has a negative effect on eel stocks. The sea bass Dicentrarchus labrax not only competes with eels, but also feeds on glass eels and small yellow eels (Rossi and Cannas, 1984). 1.1.1.5. Food and eating behavior Diet: At the moment of hatching, the digestive tract is barely formed and the mouth is closed (Prokhorchick, 1986). The digestive tract of the leptocephali, as well as its associated organs, is set in place in the first days after hatching. According to some authors (Hulet, 1978; Kracht and Tesch, 1981; Moser, 1981), the digestive tract might not be functional in leptocephali in general. According to other authors (Westerberg, 1989, 1990; Mochioka et al., 1993; Mochioka and Iwamizu, 1996; Pfeiler et al., 1998), larvae feed on plankton. It was Westerberg (1989, 1990) who first hypothesized the consumption of zooplanktonic organisms belonging to large gelatinous plankton (hydromeduses, siphonophores, scyphomeduses, ctenophores, thalias and appendicularians), in relation to the possibility of a wide mouth opening. Currently, the diet of leptocephali is still little known; no planktonic prey has been identified in the digestive tract (Kracht and Tesch, 1981). Its trophic resources have also been assumed to be particulate organic matter, such as the fecal pellets of copepods, or on the appendages of larvaceans (Desaunay and Guerault, 1997). According to Rasquin (1955), the leptocephalic larva does not feed during the whole metamorphosis, but it is at the gelatinous matrix, rich in GAGs glycosaminoglicans, and from lipids that the leptocephali will find the necessary energy for such transformations. Then, the gelatinous matrix will gradually be replaced by muscles and bone tissue. Between 70 and 80% of the GAGs, rich and highly energetic molecules will be catabolized during the metamorphosis (Pfeiler, 1984). Considering that GAGs have the property of retaining water, their degradation leads to a considerable loss of water and mineral salts, particularly of NaCl. Around 80% of the energy required for this ontogenetic stage comes from lipids (Pfeiler, 1996). During metamorphosis, the composition of lipids changes, manifesting their catabolism. The fasting phase ends at the VIA3 elver stage (complete pigmentation) (Lecomte-Finiger, 1983), corresponding to the reopening of the gastrointestinal tract (Monein-Langle, 1985), reflecting a close relationship between structural and functional development.

44

Fishes in Lagoons and Estuaries in the Mediterranean 3A

Pigmented elvers first consume planktonic prey, and later, they progressively feed on larger benthic prey. Their olfactory and gustatory sensitivity (chemoreception) is considerable in relation to amino acids at very low concentrations (10–8 at 10–9 M) (Crnjar et al., 1992). Among the different pigmentary stages captured at a natural environment, the VIA4 stage (Elie et al., 1982) is the first to contain prey in significant amounts (Tesch, 1983). In the lagoons of the Gulf of Lion, the elver’s eating activity is only gradually established. Glass eels and those individuals at the beginning of pigmentation have no nutritional activity. Feeding begins only at stage V1A3 (according to the stages suggested by Elijah et al., 1982), when pigmentation begins to develop (Lecomte-Finiger, 1983). For stages VIA4, VIB and yellow eels, there is a relationship between prey size and the number and length of fish. In fish measuring between 6 and 20 cm, and as they grow, eels tend to consume larger prey (although they continue to feed on small prey). The relationship between the size of fish and that of prey is: Pl = 0.49 TL0.47 (r = 0.82). However, the average number of preys per stomach does not show significant variations with regard to fish size (6–20 cm) (Lecomte-Finiger, 1983). Yellow eels are voracious carnivores with a broad food spectrum. They consume great diversity of benthic prey, usually the most available according to the seasons: isopod crustaceans (Sphaeroma), amphipods (Gammarus), mysids, annelids, molluscs, insects (Diptera, ephemeroptera, etc.) and fish. Their piscivorous tendencies increase with age, but we should observe that the ichthyophagia reported by several authors (Moriarty, 1972; Tesch, 1977) most often corresponds to a strict form of cannibalism, in that elvers occasionally serve as prey to eels, as already pointed out by Sinha and Jones (1967) and Tesch (1977). In the Mediterranean lagoons, the diet is quite diversified and offers seasonal variations: crustaceans (copepods, amphipods, isopods, decapods), insect larvae, polychaete annelids, gastropods and fish (Atherina boyeri), which reveals an obvious trophic opportunism (Lecomte-Finiger, 1983b). This type of diet has been described in the Prévost (Bouchereau et al., 2006) and Mauguio lagoons (Bouchereau et al., 2009) for fish measuring 23–87 cm TL and 15.6–72 cm TL. At three brackish ponds in Roussillon (Lapalme, Salses-Leucate, Bourdigou), glass eels and elvers (6-25 cm TL) also feed on crustaceans, annelids, insects, molluscs and fish (Lecomte-Finiger, 1983). Crustaceans represent the basis of the diet for each environment. Variations occur at the level of the consumed species. Thus, gammarids dominate at Lapalme (71–87%), idotheae are the main prey at Salses-Leucate (66-100%), while corophids are the main prey at Bourdigou (almost 100%). The dietary regime of eels (25–61 cm TL) from the Manzalah Lake (Egypt) is composed of fish, insect larvae, crustaceans and molluscs (Table 1.4; Ezzat and El-Seraffy, 1977). These differences confirm the opportunistic eating behavior.

Anguillidae Jordan and Evermann, 1896

Food items

Number

%

Tilapia spp. Other fish Chironomidae (larvae) Shellfish

153 64

49.28 22.19

47

10.22

41

8.84

Odonata (larvae)

25

6.91

Shellfish

7

2.56

45

Table 1.4. Abundance and frequency of prey in the stomach of the A. anguilla at the Manzalah lagoon (from Ezzat and El-Seraffy, 1977)

The size of the prey consumed is correlated to the width of the eel’s head (Sivertsen, 1938, Micheler, 1967). Thus, broad-headed eels, which are generally large individuals (40–60 cm TL), eat more fish than those with narrow heads. It is probable for silver eels not to feed during their migration (Morović, 1970), as evidenced by the degeneration of the intestinal tract (Tesch, 1983). This degeneration is unlikely to be reversible (Fontaine et al., 1982). Eating behavior: As a nocturnal species, eels feed mostly during the night (Morović, 1970; Deelder, 1984). The feeding activity mostly depends on temperature, being reduced when temperatures are too hot (28–30°C) and being interrupted below 10°C. Although voracious and cannibal, the eel is able to withstand prolonged fasting (up to 460 days) during which it uses its liver lipid (triglyceride) reserves, and then, its glycogen reserves are stored in its liver (Larsson and Lewander, 1973). Three modes of food intake have been identified in yellow eels: sucking, cephalic shocks and body rotation (Helfman and Clark, 1986). The choice of each of these types of behavior is determined by the kind of prey (according to its consistency) and by the search for a ratio optimization between energetic costs and energetic benefits that these same prey may provide (Helfman and Clark, 1986). The existence of a regular plankton diet by eels, at various sizes, has been proven by parasitic infestations (for example Pseudodactylogyrus anguillae) because during the infestation cycle, planktonic copepods act as vectors for the parasite (Kennedy et al., 1992). The same happens with the A. crassus nematode (Blanc, 1994; Bruslé, 1996). Silver eels do not feed during their catadromic migration. They are considered anorexic and as their gut has receded, and their transoceanic migration is carried out because of the exclusive use of (mainly lipidic) energy reserves accumulated during the yellow eel stage.

46

Fishes in Lagoons and Estuaries in the Mediterranean 3A

Intraspecific competition seems to be limited due to the adoption of territorial behavior by elvers and yellow eels, which allows for benthic resources to be shared. In addition, the diversification of diet and a change in the trophic spectrum during growth (increasing the consumption of gammarids) might reduce the risks of intraspecific competition. The eel has been considered able to compete interspecifically with the Salmo trutta fario trout, although their respective eating behavior and their activity rhythms are quite different. Nevertheless, in France, the eel is still deemed as harmful in the salmon farming zone (first category), where it was systematically destroyed until 1984 (CSP, 1998). – Variations and food rhythms: In the brackish ponds of Roussillon (France), the values of the stomach vacuity coefficient are high in winter (50–95%) and in summer (60–78%), and seem to be related to water temperature fluctuations. Trophic activity is optimal between 15 and 25°C (Lecomte-Finiger, 1983). Similarly, in Lake Manzalah in Egypt, Ezzat and El-Seraffy (1977) revealed that feeding activity is active in spring and autumn, while it is very low in winter. In winter, eels only eat fish. In the Prévost (Bouchereau et al., 2006) and Mauguio lagoons (Bouchereau et al., 2009), the seasonal influence is manifested by a decrease in nutritional activity during the summer period, which reverses and increases at the following seasons. According to these authors, the seasonal variations observed reveal an opportunistic feeding behavior, characterized by the consumption of the most available benthic prey. Thus, the eel adapts its diet by adjusting it to the available energetic resources in the environment. As a result, this lagoon-resident is an indirect bioindicator of the trophic capacity and level of confinement present in the ecosystem. In the Roussillon lagoons, glass eels consume small prey (annelids, diptera), which are present at shallow depths, whereas elvers (>10 cm and particularly those close to 20 cm TL) feed on more voluminous prey (idoths and gammarids) from the aquatic plant habitats (Lecomte-Finiger, 1983). In Manzalah Lake, feeding also changes with the size of fish (Ezzat and El-Seraffy 1977). The young ( 33 TL, F:> 36 TL

3

M: 33–35 TL, F: 36–38 TL

4

> 33 TL

3

27 TL

3

F: 57 TL

2

Pantan Lagoon, Croatia (Morovic, 1963) Venice Lagoon, Italy (Morovic, 1954, 1957) Coast of Israel (Abraham, 1963) Tiberias Lake, Israel (Abraham, 1963)

Table 5.31. Mugil cephalus length and age of first sexual maturity in different regions in the Mediterranean (M: males, F: females, TL total length, SL: standard length)

Site and spawning period: Mullets breed in the littoral marine area (Lam Hoai, 1969; Cambrony, 1983), although adults may spend almost their entire lives in estuaries and/or lagoons (Cardona, 2000). Heldt (1948) showed the absence of mullet eggs in the plankton, observations made during four years in the north lake of Tunis, a lagoon which is rich in mullets. The organisms of this species require certain conditions for oviposition, other than those prevailing in deep Mediterranean and shallow lagoons. If mullets cannot go out at sea so as to finish the maturation of their genital products, these involute and laying does not take place (Abraham et al., 1966). Their oocytes remain at the stage of previtellogenesis. It is even possible that this inability to achieve reproductive migration could lead to the decline and massive

Mugilidae Günther, 1861

251

death of mullet populations. Such an event occurred in 1924 in Ichkeul (northern Tunisia), where tons of mullets were found. According to Heldt (1931, 1948b), this crisis was caused by the flooding of the wadis, which had delayed the entry of marine currents into the lagoon, in such a way that mullets not “receiving the call from the sea” remained inconveniently confined in the desalted lagoon. In Tunisia, it seems unlikely for the breeding migration to push mullets far away from the coast (Farrugio, 1975). In lakes, the gonads reach full maturity in males and a highly advanced stage in females. Similarly, mullets being fished along the coastline during the prelaying period have complete or nearly fully developed gonads. It is therefore plausible for these fish, whose laying is imminent, not to deviate far from the littoral zone. While diving at the time of the reproduction of M. cephalus, Farrugio (1975) observed groups of adults at the moment of laying. Some of these observations were made a few meters from the shore, others up to nearly 1 km from the coast, in the Gulf of Tunis, at depths oscillating between 15 and 25 m. In Israel, Abraham (1963) pointed out that oogenesis begins when water temperature is high (27°C in the sea and 30°C in the Tiberiade Lake), and that oocytes ripen when the temperature begins to decrease. He suggested that in warmer waters, this species can lay twice a year. Yashuv and Berner-Samsonov (1970) showed that on the shores of Israel, temperatures below 22°C block the development of eggs, which eventually perish. In the Mediterranean, laying takes place essentially between July and October. Variations may be observed from one region to another (Table 5.32) and could be mainly explained due to the differences in temperature (Farrugio, 1975). Places and authors Adriatic Sea (Brunelli, 1916) Sardinia, Italy (Paolucci, 1917) Mar Menor Lagoon, Spain (Navarro, 1927) Corsican coast (De Caraffa, 1929) Messina, Italy (Sanzo, 1936) Egyptian coasts (Faouzi, 1938) Biguglia Lagoon , Corsica (Belloc, 1938) Mar Menor Lagoon, Spain (Lozano-Rey, 1947) Tunisian lakes (Heldt, 1948)

J

F M A M

J

J

A

S

O N

D

252

Fishes in Lagoons and Estuaries in the Mediterranean 3A

Coast of Croatia (Morovic, 1957) Istanbul, Turkey (Denizci, 1958) Bosphorus (Erman, 1959) Algeria coasts (Dieuzeide et al., 1959) Rivers, Israel (Bograd, 1961) Gulf of Marseille, France (Ezzat, 1963) Pantan Lagoon, Croatia (Morovic, 1963) Coast of Israel (Abraham, 1963) Berre Pond, France (Ezzat, 1965) Coasts of Israel (Abraham, 1966) Coasts of Israel (Thierberger-Abraham, 1967) Italian Coasts (De Angelis, 1967) Coasts of Israel (White and Abraham, 1968) Marseille, France (Leray, 1968) Coast of Israel (Yashuv, 1969) Coast of Israel (Yashuv and Berner-Samsonov, 1970) Bay of Algiers (Marinaro, 1971) Borullus Lagoon, Egypt (Hashem et al., 1973) Tunisia (Farrugio, 1975) Languedoc-Roussillon lagoons, France (Cambrony, 1983) Italian coasts (Ghittino, 1983)

Table 5.32. Spawning periods of Mugil cephalus in the Mediterranean

Fecundity: Absolute fecundity is generally calculated between 1.2 and 7 million eggs (see compilation in Bruslé, 1981). It usually increases with the size of females (Gandolfi et al., 1991). Ezzat (1965) and Nash and Shehadeh (1980) observed that M. cephalus is the most fertile among the mullet species (1,200–7,200 eggs/g of fish). On the northern coast of Tunisia, Farrugio (1975) calculated an absolute

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fecundity of 1.2–3.7 million eggs in females measuring between 33 and 42 cm, which correspond to an Rf of 2,200 and 2,850 eggs/g of fish, respectively. Reproductive behavior: There are still gaps in the knowledge of the egg-laying behavior, as this activity usually takes place at night, before dawn (Arnold and Thompson, 1958; Avanesov, 1972). It is generally accepted that small groups of three to six fish, consisting of a female with several males, swim close to the surface. The males, smaller and thinner than the female, stay a little behind it. When it lays, the males stay by its side and fertilize the oocytes as soon as they are emitted. The eggs are pelagic. Such behavior was documented by Farrugio (1975) in Tunisia. In general, the author observed these spawners on sandy areas, forming clearings within the plant beds; the female, visibly heavy and moving slowly, with the males around the female. The latter turn around, approaching her in turns, and touch their partners’ side with their ventral side. All the evidence suggests that this is the moment when spawning and fertilization take place. Egg, larva and ontogenesis: Eggs are spherical, transparent and smooth. The egg measures approximately 930 μm and is characterized by the presence of a single lipid globule with a uniform diameter of 330 μm (Kuo et al., 1973; Nash et al., 1974). The metric characteristics of eggs laid in different regions of the Mediterranean are as follows: 0.72 mm in Messina (Sanzo, 1938) and Biguglia lagoon (Belloc, 1938), 0.66–1.08 mm in Israel (Yashuv and Berner-Samsonov, 1970) and 0.72–0.78 mm in Algiers (Marinaro, 1971). Lipid globules have a diameter of 0.26–0.31 mm (Sanzo, 1938, Marinaro, 1971) and represent 36.1–40.8% of the egg’s diameter in Israel (Yashuv and Berner-Samsonov, 1970). Yashuv (1969) reported that some M. cephalus eggs founder toward the end of their incubation period (after 20 h); according to Kuo et al. (1973), these might be undeveloped or unfertilized eggs (lack of perivitelline space). Experimentally, Lee et al. (1992) and Tamaru et al. (1993) showed that egg fertilization is better in sea water (about 35‰) than in brackish water, and especially better than in freshwaters; this is probably due to the higher motility of spermatozoa. Egg hatching occurs after 34–65 h of incubation, depending on temperature (Nash and Konings-Berger, 1981; Chen, 1990). Kuo et al. (1973) reported the success of incubation between 22 and 24°C at 32‰ in well-aerated water. Temperatures equal to or greater than 25°C are usually lethal (Nash et al., 1974). The best survivals are obtained at 21–24°C, with an optimum at 22°C. Nash and Koningsberger (1981) pointed out that most authors prefer to work between 18 and 24°C. On the other hand, Yashouv and Berner-Samsonov (1970) found that temperatures below 22°C stop the embryonic development of eggs, which eventually perish. The egg and embryonic development were studied by several authors: Sanzo (1936, Italy), Pillay (1972, Italy, following Sanzo, 1936), Vialli

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(1937, Gulf of Naples), Burdak (1957, Black Sea), Kuo et al. (1973, Israel), Nash et al. (1974, Israel). This development is rapid and gastrulation is reached after 12 h postlaying (Nash et al., 1974). Yashuv and Berner-Samsonov (1970) gave a complete description of the eggs and larvae of five mugilid species in Israel, including M. cephalus. The size of larvae at hatching may vary: 2.2–2.4 mm (Sanzo, 1936; Vialli, 1937; Lumare and Villani, 1972, Italy), 3.4–3.6 mm (Yashuv, 1969, aquaculture, Israel). Depending on the environmental conditions, the larvae reach 2.5 mm after two days in Italy (Lumare and Villani, 1972) and 3.1 mm after eight days in Messina (Sanzo, 1936). Oral opening takes place at day 2. Larvae do not feed for the first 4 days, even when their mouth is open. They still use their vitelline reserves (Bruslé, 1981), which are over after 5 days. They are carnivorous in the early stages of development, becoming omnivorous soon after (Bruslé, 1981). Complete morphological descriptions of M. cephalus larvae were mainly made during the hormonal spawning induction operations in Israel (Yashouv, 1969; Yashouv and Berner-Samsonov, 1970). The ontogeny of juvenile stages was described by Anderson (1958) and Kuo et al. (1973). 5.3.1.7. Economic importance The worldwide fishing of M. cephalus ranged between 28,895 and 165,376 tons from 1985 to 2007. In the Mediterranean, this production evolved between 1,679 and 7,285 tons from 1985 to 2005. The main producing countries are Greece and Tunisia, with 98% of the total fished in 2005. The main fisheries of this species operate in lagoons and estuaries and play an important socioeconomic and cultural role at the regional level. This fishing is practiced with different types of gear: seine net, gill net, casting net, plaice, barrier net, capéchade, fyke, fishing weirs and other handcraft gear. The catches are spread over the whole year with the most frequent maxima in relation to certain migratory phases. So, Katselis et al. (2003, 2005) record two peaks in the catch of the bordigues installed in the lagoon complex of Messolonghi–Etoliko (Greece): the first (from the beginning of August to the end of October) corresponds to the reproduction migration of this species to the sea; the second (in November and December) coincides with his return to the lagoon. In this environment, the average annual M. cephalus production from 1988 to 2002 was about 14.9 tons (± 0.9 tons). In the Mellah lagoon (Algeria), mugilid catches may reach 75% of the amounts fished, with a dominance of M. cephalus from August to November. Most of the catches of this species are made at the “bordigue” in September and October (about 80%) (Chaoui et al., 2006). World aquaculture production of M. cephalus increased from 5,527 tons in 1985 to 264,383 tons in 2007. In 2007 (FAO-FishStat Plus), the main producing countries were Egypt (252,500 tons), Korea (4,921 tons), Taiwan (2,700 tons) and Israel

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(2,100 tons). Extensive and semiintensive breeding of this species has been practiced for several decades. It occupies an important place in Egyptian fish farming, where it is reared in the region of the Nile Delta in “hosha”. The fish larvae supply is based mainly on natural inputs, especially to the east and south of the Mediterranean. The induction of egg laying and the production of fish larvae are conducted experimentally and semicommercially in the United States and in Taiwan and, on a smaller scale, in Italy, Israel and Egypt. In Israel, 600,000 good quality fish larvae were produced in 2013. In many countries, fish larvae are used for restocking freshwater lakes and dams in order to improve their fisheries. This has been the case for lakes in the region of El Fayum in Egypt since the 1920s. In Egypt, the cost of hatchery-raised 10 g fish larvae is 0.3 USD, while it costs 0.1–0.12 USD when caught in lagoons or estuaries. Since the aquaculture of M. cephalus depends on the collection of fish larvae in the wild, it may have a negative impact on the exploitable stocks of this fish. Sarig (1981) reported that rearing M. cephalus at 1 fish/m2 produces an annual yield of 3,500 kg/ha, with a feed conversion rate (rice bran and peanut cake) 1.6:1. The same type of breeding in Israel with 2–3 fish/m2 yields from 3,600 to 8,900 kg/ha/year, with 25–50% of M. cephalus and L. ramada (Pruginin et al., 1975). In Egypt, the breeding of M. cephalus and L. ramada in ponds (hosha) at 3 fish/m2 yields around 6,000 kg/ha/year (Crosetti and Cataudella, 1994). Other breeding operations in Egypt produce yields of 100–2,500 kg/ha/year in polyculture and 3,500 kg/ha/year in monoculture (Crosetti and Cataudella, 1994). In the latter case, farms may include prefertilization ponds with 30–50 juveniles/m2. Traditional Italian valliculture consists of raising lagoons with 0.1–0.4 juvenile mullets (five species) per square meter in association with the bass, the sea bream and the eel (Crosetti and Cataudella, 1994). Yields achieved when net-capturing 3- to 5-year olds migrating to the sea range from 50 to 150 kg/ha (Crosetti and Cataudella, 1994). The same system applied in the marine swamps of Cadiz Bay makes it possible to obtain an average yield of 190–240 kg/ha, where mullets represent 60–80% of the production (Arias et al., 1984; Arias and Drake, 1993). In Italy, Ravagnan (1978, 1992) applied a mullet intensive breeding technique (especially M. cephalus and C. labrosus) in earth ponds, with a 1-year enlargement. This technique makes it possible to have an animal production of 250–300 g at the end of the second year. After a supplementary year of semiintensive breeding, the same species may reach a weight of 500–600 g. The commercial importance of mugilids depends on the country, ranging from highly esteemed in Tunisia and Egypt to low value in certain regions of Spain, Greece and France. M. cephalus is eaten mostly fresh, but also salty (in Egypt), dried or smoked. Its mature gonads are dried, salted and wrapped in wax film and

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sold under the name avgotaracho in Greece, as dried-salted caviar in Turkey and as bottarga in other Mediterranean countries (France, Italy, Maghreb). 5.3.1.8. Protection status, conservation – IUCN Global Red List: LC; – IUCN Mediterranean Red List: LC. 5.4. Bibliography ABDALLAH C., GHORBEL M., HAJJEJ G., JARBOUI O., “Reproductive biology of the leaping grey mullet Liza saliens, in the Gulf of Gabes (central Mediterranean, Tunisia)”, Cahiers de Biologie Marine, 54 (1): 11–17, 2013. ABDALLAH C., GHORBEL M., JARBOUI O., “Reproductive biology of the golden grey mullet Liza aurata (Risso, 1810) in the Gulf of Gabes (central Mediterranean, Tunisia)”, Mediterranean Marine Science, 14 (2): 409–415, 2013. ABDEL’MALEK S.A., “Some data on the distribution and biology of commercial fish in Lake Qarun, Egypt”, Voprosy Ikhtiologii, 21 (4): 616–622. 1981. ABRAHAM B., “A study of the oogenesis and egg resorption in the mullets Mugil cephalus and Mugil capito in Israël”, Global Council of the Mediterranean, 7: 435–453, 1963. ABRAHAM M., BLANC N., YASHOUV A., “Oogenesis in five species of grey mullets (Teleostei, Mugilidae) from natural and landlocked habitats”, Israel Journal of Zoology, 15: 155–172, 1966. ABRAHAM M., YASHOUV A., BLANC N., “Induction expérimentale de la ponte chez Mugil capito confiné en eau douce”, Comptes rendus de l’Académie des Sciences, Paris, 265 (11): 818–821, 1967. 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. ALBERTINI-BERHAUT J., VALLET F., “Utilisation alimentaire de l’urée chez les muges”, Tethys, 3(3): 677–680, 1972. ALBERTINI-BERHAUT J., “Biologie des stades juvéniles de téléostéens mugilidae Mugil auratus Risso 1810, Mugil capito Cuvier 1829 et Mugil saliens Risso, 1810”, Aquaculture, 2: 251–266, 1973. ALBERTINI-BERHAUT J., “Biologie des stades juvéniles de téléostéens mugilidae Mugil auratus R. 1810, Mugil capito C. 1829 et Mugil saliens R. 1810. II. Modifications du régime alimentaire en relation avec la taille”, Aquaculture, 4: 13–27, 1974.

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ARDIZZONE G.D., CATAUDELLA S., ROSSI R., “Management of coastal lagoon fisheries and aquaculture in Italy”, FAO Fisheries Technical Paper, 293: 1–103, 1988. AREFYEV V.A., “The application of the method of colchicines baths to studies of karyotypes of the young of two mullet species (Mugilidae) from the Black Sea”, in L.A. DUSHKINA (ed.), Early Life History of Marine Species, Sb. Nauchn. Tr. VNIRO, Moscow, 139–149, 1989. ARIAS A.M., DRAKE P., “Evolution of fish production in saltmarsh fish ponds of the bay of Cadiz (Spain), World Aquaculture 93 International Conference, 308, Torremolinos, Spain, 26–28 May 1993. ARIAS A.M., DRAKE P., RODRIGUES R.B., “Los esteros de las salinas de San Fernando (Cadiz, Espana) y el cultivo extensivo de peces marinos”, in G. BARNABÉ, R. BILLARD (eds), Colloque sur l’aquaculture du bar (loup) et des sparidés, Sète, France, 15 March 1983, Paris, 447–463, 1984. ARNE P., Contribution à l’étude de la biologie des muges du golfe de Gascogne, PV Report, Commission internationale pour l’exploration scientifique de la mer (CIESM), 11: 76–115. 1938. ARNOLD E.L., THOMPSON J.R., “Offshore spawning of the striped mullet, Mugil cephalus, in the Gulf of Mexico”, Copeia, 1958: 130–132, 1958. AURELLE D., BARTHELEMY R.M., QUIGNARD J.-P., TRABELSI M., FAURE E., “Molecular phylogeny of Mugilidae (Teleostei: Perciforms)”, The Open Marine Biology Journal, 2: 29–37, 2008. AUTEM M., Contribution à l’étude biologique des zones de dilution du littoral méditerranéen (estuaires et étangs lagunaires), I. Les estuaires languedociens et leurs poissons. II. Recherches sur les stratégies d’occupation de ces milieux par les poissons mugilidés. Différenciation, génétique, biologie, PhD thesis, USTL, Montpellier, 1979. AUTEM M., BONHOMME F., “Élements de systématique biochimique chez les mugilidés de Méditerranée”, Biochemical Systematics and Ecology, 8: 305–308, 1980. AVANESOV E.M., “Present spawning conditions of mullets (genus Mugil) in the Caspian Sea”, Journal of Ichthyology, 12: 419–5, 1972. BALIK I., EMRE Y., SUMER C., TAMER F.Y., OSKAY D.A., TEKSAM I., “Population structure, growth and reproduction of leaping grey mullet (Liza saliens Risso, 1810) in Beymelek lagoon, Turkey”, Iranian Journal of Fisheries Sciences, 10 (2): 218–229, 2011. BARDACH J.E., RYTHER J.H., MCLARNEY W.O., Aquaculture. The Farming and Husbandry of Freshwater and Marine Organisms, 385–312, John Wiley & Sons, New York,1972.

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BARTULOVIĆ V., DULČIĆ J., MATIC-SKOKO S., GLAMUZINA B., “Reproductive cycles of Mugil cephalus, Liza ramada and Liza aurata (Teleostei: Mugilidae) , Journal of Fish Biology, 78 (7): 2067–73, 2011. BARTULOVIĆ V., GLAMUZINA B., LUCIC D., CONIDES A., JASPRICA N., DULČIĆ J., “Recruitment and food composition of juvenile thin-lipped grey mullet, Liza ramada (Risso, 1826), in the Neretva River estuary (Eastern Adriatic, Croatia)”, Acta Adriatica, 48 (1): 25–37, 2007. BARTULOVIĆ V., MATIC-SKOKO S., LUCIC D., CONIDES A., JASPRICA N., JOKSIMOVIC A., DULČIĆ J., GLAMUZINA B., “Recruitment and feeding of juvenile leaping grey mullet, Liza saliens (Risso, 1810) in the Neretva River estuary (South-Eastern Adriatic, Croatia)”, Acta Adriatica, 50 (1): 91–104, 2009. BAUCHOT M.L., PRAS A., Guide des poissons marins d’Europe, Delachaux et Niestlé, Paris, 1980. BAUCHOT M.L., “Mugilidae”, in W. FISHER, M. SCHNEIDER, M.-L. BAUCHOT (eds), “Fiches FAO d’identification des espèces pour les besoins de la pêche. Méditerranée et mer Noire”, (37) 2: 1190–1194, FAO/CEE, Rome, 1987. BAUZA-RULLAN J., “Contribucion al estudio de los otolitos de peces”, Boletín de la Real Sociedad Española de Historia Natural, Sección biológica, 57, 1959: 89– 118, 1960. BAUZA-RULLAN J., “Nueva contribucion al conocimiento de los otolitosdo peces actuales”, Boletín de la Sociedad de Historia Natural de Baleares, 6: 49–61, 1960. BAYHAN B., KAYA M., ACARH D., “A fin anomaly in thinlip Mullet Liza ramada (Risso, 1810) caught from Homa lagoon (Izmir Bay, Aegean Sea)”, Pakistan Journal of Zoology, 42 (6): 830–833, 2010. BEBARS M.I., Étude biochimique sur les protéines solubles du cristallin des muges de la région du Languedoc-Roussillon, DEA Report, USTL, Montpellier,1976. BELLOC G., Biologie et pêche de l’étang de Biguglia, PV Report, Commission internationale pour l’exploration scientifique de la mer Méditerranée (CIESM), 11: 405–431, 1938. BEN KHEMIS I., GISBERT E., ALCARAZ C., ZOUITEN D., BESBES R., ZOUITEN A., MASMOUDI A.S., CAHU C., “Allometric growth patterns and development in larvae and juveniles of thick-lipped grey mullet Chelon labrosus reared in mesocosm conditions”, Aquaculture Research, 44 (12): 1872–1888, 2013. BEN KHEMIS I., ZOUITEN D., BESBES R., KAMOUN F., “Larval rearing and weaning of thick lipped grey mullet (Chelon labrosus) in mesocosm with semi-extensive technology”, Aquaculture, 259: 190–201, 2006. BEN-TUVIA A., “Mugilidae”, in P.J.P WHITEHEAD, M.L. BAUCHOT, J.C. HUREAU, J. NIELSEN, E. TORTONESE (eds), Fishes of the Northeastern Atlantic and the Mediterranean, 3: 1197–1204, Paris, 1986.

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BERG L.S., BOGDAROV A.S., KOJIA N.E., PASS T.A., Commercial Fishes of the USSR Food Industry, Moscow, 1949. BESBES R., BENSEDDIK A., BEN KHEMIS I., ZOUITEN D., ZAAFRANE S., MAATOUK K., EL ABED A., M’RABET R., “Comparative development and growth of the larvae of thick lipped mullet Chelon labrosus (Mugilidae) reared in intensive conditions: Green water and clear water”, Cybium, 34 (2): 145–150, 2010. BESBES R., FAUVEL C., GUERBEJ H., BENSEDDIK-BESBES A., EL OUAER A., KRAIEM M.M., EL ABED A., “Contribution à l’étude de la maturation et de la ponte en captivité du mullet lippu Chelon labrosus (Cuvier, 1829). Résultats préliminaires de pontes par stimulation hormonale”, Actes des 5e journées tunisiennes des Sciences de la mer, Ain Draham, Tunisia, 21–24 December 2002, Bulletin de l’INSTM, 7: 40–43, 2003. BLANC-LIVNI N., ABRAHAM M., “Aspects endocriniens de la reproduction chez Mugil (Teleostei) en relation avec l’habitat d’eau douce et d’eau de mer”, Verhandlungen des Internationalen Verein Limnologie, 17: 625–629, 1969. BLEL H., CHATTI N., BESBES R., FARJALLAH S., ELOUAER A., GUERBEJ H., SAID K., “Phylogenetic relationships in grey mullets (Mugilidae) in a Tunisian lagoon”, Aquaculture Research, 39: 268–275, 2008. BLEL H., PANFILI J., GUINAND B., BERREBI P., SAID K., DURAND J.D., “Selection footprint at the first intron of the Prl gene in natural populations of the flathead mullet (Mugil cephalus, L. 1758)”, Journal of Experimental Marine Biology and Ecology, 387: 60–67,2010. BOGLIONE C., BERTOLINI C., RUSSIELLO M., CATAUDELLA S., “Embryonic and larval development of the thick-lipped mullet (Chelon labrosus) under controlled reproduction conditions”, Aquaculture, 101: 349–359, 1992. BOGLIONE C., COSTA C., GIGANTI M., CECCHETTI M., DI DATO P., SCARDI M., CATAUDELLA S., “Biological monitoring of wild thicklip grey mullet (Chelon labrosus), golden grey mullet (Liza aurata), thinlip mullet (Liza ramada) and flathead mullet (Mugil cephalus) (Pisces: Mugilidae) from different Adriatic sites: meristic counts and skeletal anomalies”, Ecological Indicators, 6: 712– 732, 2006. BOGRAD L., “Occurrence of Mugil in the rivers of Israel”, Bulletin of the Research Council of Israel, 9b: 169–191, 1961. BOISSEAU J., LASSERRE P., GALLIS J.L., CASSIFOUR P., “Aspects écophysiologiques de l’osmorégulation et de l’évolution génitale de poissons mugilidés en milieu lagunaire”, The Journal of Physiology, 70: 669–670, 1975. BORAEY F.A., Biological study in the family Mugilidae in Lake Quarun, PhD thesis, Ain Shams Université, Cairo, Egypt,1974. BOUGIS P., “La croissance des poissons méditerranéens. Océanographie méditerranéenne. Journées d’études du laboratoire Arago”, Science and Industry Research Act, 1187: 118–146, 1952.

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BOURIGA N., MILI S., BOUYAZBECK E., LAOUER H., QUIGNARD J.-P., TRABELSI M., FAURE E., “Identification et caractérisation des alevins de muges ensemencés dans les retenues de barrages en Tunisie”, Bulletin de la Société zoologique de France, 137(1–4): 229–243,2012. BOURQUARD C., BENHARRAT K., “La colonisation des lagunes du Golfe du Lion par les stades jeunes de Soleidae, Mugilidae et Sparidae”, Actes du 110e Congrès national des Sociétés savantes, Montpellier 1985, Section Sciences, fasc. II: 127– 138, Montpellier, France, 1985. BREDER C.M., “The spawning of Mugil cephalus on the Florida West Coast”, Copeia, 1940: 139, 1940. BRULHET J., “Situation et perspectives des pêcheries du mulet jaune de Mauritanie”, La pêche maritime, 1159: 702–706, 1974. BRULHET J., “Observations on the biology of Mugil cephalus ashenteensis and the possibility of its aquaculture on the Maurianian coast”, Aquaculture, 5: 271–281, 1975. BRUNELLI G., “Ricerche sul novellame dei muggini con osservazioni e considerazioni sulla mugginicoltura”, Regio Comitato Talassografico Italiano, 54: 1–45, 1916. BRUSLÉ J., CAMBRONY M., “Les lagunes méditerranéennes: des nurseries favorables aux juvéniles de poissons 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: 193–205, 1992. BRUSLÉ J., “Food and feeding in grey mullets”, in O.H. OREN (ed.), Aquaculture of Grey Mullets, Cambridge, Cambridge University Press, 185–212, 1981a. BRUSLÉ J., “Sexuality and biology of reproduction in grey mullets”, in O.H. OREN (ed.), Aquaculture of Grey Mullets, 99–114, Cambridge University Press, Cambridge, 1981b. BRUSLÉ S., BRUSLÉ J., “Intersexualité testiculaire chez les muges méditerranéens Mugil cephalus et Mugil ramada”, Bulletin de la Société zoologique de France, 100: 249, 1974. BULLO G.S., Pescicoltura marina, stima della coltivazione in acqua salsa, Prosperini, Padua, 1891. BURDAK V.D., “Peculiarities in the ontogenetic and phylogenetic relationship in Black Sea mullet (Mugil saliens, M. auratus, M. cephalus)” Trudy Sevastopol’skoi Biologicheskoi Stantsii, 8: 243–272 (in Russian),1957. CAIN R.L., DEAN J.M., “Annual occurrence, abundance and diversity of fish in a South Carolina intertidal creek”, Marine Biology, 36: 369–379, 1976.

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WIMPENNY R.S., “Eggs and larval stages of Mugil capito Cuv. From lake Qarun, Egypt”, Annals and Magazine of Natural History, 17: 405–412, 1936. XIMENES M.C., Observations sur les faunes ichtyologiques des étangs corses: Biguglia, Diana et Urbino (inventaire, alevinage, croissance et démographie de certaines espèces, Centre technique du génie rural des eaux et forêts, Division ALA, Montpellier, 1979–1980. YANG W.T., KIM U.B., “A preliminary report on the artificial culture of grey mullet in Korea”, Proceedings - Indo-Pacific Fisheries Council, 9 (2/3): 62–70, 1962. YASHOUV A., “Preliminary report on induced spawning of Mugil cephalus L. reared in captivity in fresh water ponds”, Bamidgeh, 21 (1): 19–24, 1969. YASHOUV A., BERNER-SAMSONOV E., “Contribution to the knowledge of eggs and early larval stages of mullets (Mugilidae) along the Israeli coast”, Bamidgeh, 22 (3): 72–89, 1970. YASHOUV A., BERNER-SAMSONOV E., HINES R., REICH K., “A hybrid of a female Mugil cephalus and male Liza ramada M. capito”, Bamidgeh, 21: 114–116, 1969. YERLI S.V., “Köyceğiz Lagǘn Sistemindeki L. ramada (Risso. 1826) stoklari ǘ zerine Yncelemeter”, Doğa Turkish Journal of Veterinary and Animal Sciences, 16: 103–120, 1991. YOUSSEF S.F., Studies of the biology of family Mugilidae in lake Manzala, MSc thesis, Faculty of Science, Cairo University, 1973. ZAKY-RAFAIL S., “Investigations of mullet fisheries by beach seine on the UAR Mediterranean coast”, Études et Revues de la FAO/GFCM, 35: 1–19, 1968. ZAOUALI J., “Données biologiques sur les mugilidés, anguillidés et Cyprinidae du lac Kelbia”, 25e Congrès Assemblée Pleinière, CIESM, Split, October, 1976. ZHUTENEV A.N., KALINICH D.S., ABEYEV Y.I., “Embryonic and larval development of the leaping grey mullet, Mugil saliens”, Journal of Ichthyology, 16 (1): 63–67, 1976. ZISMANN L., “Means of identification of grey mullet fry for culture”, in O.H. OREN (ed.), Aquaculture of grey mullets, Cambridge University Press, Cambridge, 26: 17–63, 1981. ZISMANN L., BERDUGO V., KIMOR B., “The food and feeding habits of early stages of grey mullets in the Haïfa Bay region”, Annual Report of Israel Oceanographic and Limnological Research Institute, Haïfa Laboratory, 72–73, 1974. ZISMANN L., BERDUGO V., KIMOR B., “The food and feeding habits of early stages of grey mullets in the Haïfa Bay region”, Aquaculture, 6: 59–75, 1975. ZOUITEN D., BEN KHEMIS I., BESBES R., CAHU C., “Ontogeny of the digestive tract of thick lipped grey mullet (Chelon labrosus) larvae reared in ‘mesocosms’”, Aquaculture, 279: 166–172, 2008.

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.

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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).

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Index of Names

A anchovy, 95, 98, 100, 102, 144 white, 96 Anguilla, 1–3, 5–7, 13, 14, 16–18, 21, 35, 39, 45, 47, 50, 56, 57

B, C bourgette, 110 buhotte, 110 Centropomus lupus, 132 Chelon labrosus, 160, 164, 165, 174, 175, 178, 186, 199, 233, 235 Clupea encrasicolus, 95

D Dicentrarchus, 130, 132, 137, 264 labrax, 43, 130, 132, 148, 264 lupus, 132

E eel, 10, 12, 31, 45, 53, 59 Engraulis, 95 albidu, 96 encrasicolus, 95–103 russoi, 96

F, G flathead gray mullet, 231 Gobiidae, 107, 111, 151 Gobius elongatus, 110 minutus, 108, 109 grande mougne, 110 gray mullet, thick-lipped, 165, 179 thin-lipped, 195

L Labrax, 130–146, 149 labrax, 132 lupus, 132 leaping mullet, 215 Liza, 159–161, 168, 179–184, 190, 192, 194, 195, 199, 206, 213, 215, 218, 223, 228, 230, 233, 235 (Protomugil) saliens, 215 aurata, 152, 160, 168, 179, 180, 181, 184, 190, 192, 194, 233 ramada, 161, 195, 206, 213, 235 saliens, 161, 180, 215, 223, 228

Fishes in Lagoons and Estuaries in the Mediterranean 3A: 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 Morone labrax, 130, 132 Mugil (Liza) auratus, 181 capito, 180, 195 cephalus, 160, 175, 230, 231, 235, 245, 252 cephalus cephalus, 231 chelo, 164, 165 labeo, 165 labrosus, 165 maderensis, 181 provensalis, 165, 231 ramada, 195 mullets, 144, 159, 160, 164, 166, 168, 169, 176, 179–182, 186, 197, 201, 214, 230, 234, 235, 241, 242, 246, 248–250, 252, 255

saliens, 215, 256, 257 Mugilidae, 159, 218 Muraena anguilla, 2, 6

N, P, R Ninnia, 108 Ninnigobius, 108 Perca labrax, 130, 132 Pomatoschistus, 108–117, 121–128 minutus, 109, 110–114, 116 Roccus labrax, 132

S, W sea bass, 43, 113, 129, 130, 132–135, 138, 140, 141–144, 147–149, 153, 154, 156, 157 sea bream, 255 white perch, 129

Index of Places

A, C Algeria Mellah, 54, 55, 99, 133–135, 143, 145, 169, 171, 179, 247, 254 Croatia Mirna, 187, 188, 243 Neretva, 201, 202, 206, 208, 210, 213, 221, 243, 244 Pantan, 173, 243, 244, 250, 252

E, F Egypt Bardawil, 19, 204, 232, 236, 245 Burullus, 213, 242 Edku, 170, 185, 206, 207, 213, 221, 222, 228, 239 Manzalah, 44, 46, 213, 228 Qarun, 212, 222, 225, 228, 237 France Bages-Sigean, 12, 55, 60 Berre, 115, 178, 185, 187, 189, 192, 205, 207, 213, 221, 222, 225, 228, 243, 245, 252 Camargue, 25, 36, 42, 96, 114, 115, 117, 118, 119 Fourcade, 25 Impériaux, 36

Malagroy, 115, 117–119 Mauguio, 111, 114–118 Rhône, 200 Saint-Nazaire, 55 Thau, 173, 187, 228, 244

G, I Greece Agiasma, 168 Alfios, 25, 26 Eratino, 168 Messolonghi-Etoliko, 144, 185, 225, 240, 254 Porto-Lagos, 170, 179, 185, 202, 206, 207, 213, 221, 222 Rihios, 185, 243 Sagiada, 25 Strymon, 185, 243 Vassova, 168 Vistonis, 42, 51, 176, 185, 196, 203, 206, 207, 221, 222 Italy Arno, 25, 170, 185, 221, 239 Burano, 54, 56 Caprolace, 14, 36 Comacchio, 39, 42, 56 Faro, 96, 98–100, 102

Fishes in Lagoons and Estuaries in the Mediterranean 3A: 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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Fiumicino, 139, 233 Fogliano, 26 Ganzirri, 96, 98–100, 102, 103 Lesina, 14, 36, 42 Monaci, 39, 40, 55 Muravera, 139 Orbetello, 245 Paola, 173, 175–178 Pila, 28 Porto-Pino, 40, 55 Sacca di Goro, 166, 182, 197, 199, 218, 233 Scardovari, 28, 171 Tiber, 14, 25, 36 Ugento, 139 Valle Bertuzzi, 199, 218 Valle Nuova, 39, 55 Varano, 42 Venice, 98, 110–112, 114, 115, 117, 120, 185, 220, 224, 226–229, 241, 243, 244, 250

M Montenegro Bojana, 200 Jaska, 200 Sutorina, 200

Morocco Moulouya, 12, 40 Nador, 55 Sebou, 12, 40

S, T Spain Mar Menor, 192, 237, 243, 251 San Fernando, 176, 248 Tunisia Bizerte, 172, 220 El Bibane, 55 Ghar El Melh, 54, 55 Ichkeul, 54, 98, 99, 172, 200, 206, 207, 240, 251, Medjerda, 183 North Tunis, 220 Porto-Farina, 172, 220 South Tunis, 220 Turkey Akgol-Paradeniz, 210, 248, 250 Beymelek, 139, 223–226, 228 Homa, 39, 175, 188, 189, 197, 207, 210, 223, 225, 243

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