Fish Invasions of the Mediterranean Sea

FISH INVASIONS of the

MEDITERRANEAN SEA Change and Renewal

Edited by

Daniel Golani & Brenda Appelbaum-Golani

Fish Invasions of the Mediterranean Sea: Change and Renewal 1

Fish Invasions of the Mediterranean Sea: Change and Renewal

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Fish Invasions of the Mediterranean Sea: Change and Renewal 3

FISH INVASIONS of the MEDITERRANEAN SEA: Change and Renewal Edited by Daniel Golani and Brenda Appelbaum-Golani

Sofia–Moscow 2010

4 Fish Invasions of the Mediterranean Sea: Change and Renewal Fish Invasions of the Mediterranean Sea: Change and Renewal Edited by Daniel Golani and Brenda Appelbaum-Golani

On the front cover: Plotosus lineatus (photo by M. Mendelson) On the back cover: Apogon pharaonis and Sargocentron rubrum (photos by Dr. D. Barchana)

First published 2010 ISBN 978-954-642-526-3 Pensoft Series Faunistica No 91 ISSN 1312-0174

© PENSOFT Publishers All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior written permission of the copyright owner.

Pensoft Publishers Geo Milev Str. 13a, Sofia 1111, Bulgaria e-mail: [email protected] www.pensoft.net

Printed in Bulgaria, February 2010

Fish Invasions of the Mediterranean Sea: Change and Renewal 5

Contents 7

Preface

11

Contributors

13

F.D.Por The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect

35

F. Ben Rais Lasram, F. Guilhaumon and D. Mouillot Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion and spatial congruence with endemic species

57

J. Belmaker, E. Brokovich, V. China, D.Golani and M. Kiflawi Introduction rate of Lessepsian fishes into the Mediterranean

71

G. Bernardi, D. Golani and E. Azzurro The genetics of Lessepsian bioinvasions

85

A. Diamant Red-Med immigration: a fish parasitology perspective, with special reference to the Myxosporea

99

E. Azzurro Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection

6 Fish Invasions of the Mediterranean Sea: Change and Renewal

127

P. Francour, L. Mangialajo and J. Pastor Mediterranean marine protected areas and non-indigenous fish spreading

145

D. Golani Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration

189

M. Bilecenoglu Alien marine fishes of Turkey – an updated review

219

M. Corsini-Foka Current status of alien fishes in Greek seas

255

B. Dragičević and J. Dulčić Fish invasions in the Adriatic Sea

267

L. Orsi Relini Non native marine fish in Italian waters

293

E. Massutí, M. Valls and F. Ordines Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization

313

G. Minos, A. Imsiridou and P.S. Economidis Liza hematocheilus (Pisces, Mugilidae) in the northern Aegean Sea

Fish Invasions of the Mediterranean Sea: Change and Renewal 7

Preface BACKGROUND Invasive species that have entered new ecosystems due to human intervention are considered to be one of the major factors causing an ongoing world-wide process of homogeneity of fauna and flora. A plethora of articles and books have been published on the subject of invasive species; of particular note was the pioneer work of Elton, The Ecology of Invasions by Animals and Plants, in 1958. Most of these older studies described taxonomic groups in various areas of the world. In this volume we chose to concentrate on one particular taxonomic group, namely, fishes, in one specific area, namely, the Mediterranean Sea. The advantages of studying fishes, as opposed to other taxonomic groups, are numerous; commercial fisheries supply ready access to sampling, which allows a constant reappraisal of the quantitative and qualitative status of fish species and populations. In addition, the taxonomy of fish is clearer than that of other taxa. Concerning the invasion of the Mediterranean, the level of interest is far above and beyond the relative size of this enclosed sea. However, the geographic location of the Mediterranean touches upon Europe, Africa and Asia Minor and allows close observation of changes and processes. The most dramatic invasions of the Mediterranean have been by Red Sea species via the Suez Canal which have changed significantly the composition of the fauna and flora of the Mediterranean, especially in its eastern basin, thus leading to the designation of the Eastern Levant as a distinct zoogeographic region, often called the “Lessepsian Province”. Nevertheless, in this volume we also discuss the effects of fish invasions from the Atlantic Ocean via Gibraltar and from the Black Sea via the Dardanelles. The inspiration for this edited volume on fish invasions of the Mediterranean Sea came from a symposium on Invasive Fish Species in the Mediterranean Sea, led by the editors of this volume, at the international scientific conference, the XII European Congress of Ichthyology, held in September 2007 in Cavtat (Dubrovnik), Croatia. Many of the chapters in this book were first presented at that conference, although they have been rewritten and updated, while other chapters are entirely new and were commissioned especially for this book.

8 Fish Invasions of the Mediterranean Sea: Change and Renewal

TERMINOLOGY Throughout this volume we have endeavored to maintain a serious and rational approach to the issues surrounding the scientific study of invasive species. It is unfortunate that in some other publications there are authors who have written on this subject in a more emotional mode, occasionally taking a high moral tone, as reflected in the vocabulary they use. Words and labels such as “alien” or “exotic” or “colonizing” when applied to species may hint of something insidious, perhaps even evil regarding natural phenomena of migration, immigration and invasion. The use of the expression “worst alien species” may suggest the necessity of a “war against invasive species”. Even such common topics as biodiversity may be ambiguous and even controversial, in the absence of a clear and universally accepted definition. Literature reveals no clear consensus as to the reason why biodiversity is such a critical issue; authors vary in their arguments, from stressing its importance to humanity on one hand and its inherent value on the other. There seems to be a spillover from sociological concepts such as “multiculturalism” to “biodiversity”. Oftentimes there are hidden agendas, presuppositions and unwritten subtexts in such papers. For example, there may be some researchers who believe that commercial fishery and fishermen constitute “the enemy”, although such radical suppositions are rarely if ever stated explicitly. Although it is beyond the boundaries of this volume to discuss at length the practical policy implementations of the conclusions reached by the researchers who have contributed to this edited book, we the editors can clearly state that we believe that there must be a trade-off between commercial and conservation interests in any effective monitoring policy regarding invasive fish species. In the growing scientific literature on invasive species there are varying approaches to their origin, dispersion and impact on recipient communities. Some authors place great importance on the role of climate change and global warming, particularly regarding invasions from the tropical Red Sea into the more temperate eastern Mediterranean. Other researchers maintain that an actual recent temperature rise of a fraction of a degree cannot be the main factor for the massive influx of Red Sea species into the Mediterranean. Even the term for this influx is in dispute; this phenomenon has been called “Lessepsian” or occasionally “Erythrean” as well as “Red-Med”. In this book we did not take a stand regarding terminology; we granted freedom of expression to all the contributors and allowed them to use such terms as they saw fit. This approach may have led to a certain lack of standardization between chapters. In some cases, a contributor may have considered a certain species to be exotic in the Mediterranean, while another may believe that this status may be unjustified. Therefore, it should be emphasized that the opinions expressed by the various authors are their own and not necessarily those of the editors.

Fish Invasions of the Mediterranean Sea: Change and Renewal 9

STRUCTURE OF THE BOOK The first seven chapters of this volume discuss different general aspects of fish invasions in the Mediterranean. The geological history of the Mediterranean Sea and its ichthyofauna are presented by Por who argues that from the perspective of geological ages, the current so-called colonization by Red Sea species can be considered a reuniting of species all originating from the ancient Tethys Sea. Ben Rais Lasram et al. and Belmaker et al., discuss the rate of dispersal, distribution and colonization of the allochthonous fish of the Mediterranean; the former present data correlating this phenomenon to climate change while the latter analyzes the rate of increase with an increased rate of ichthyological research. Bernardi et al. summarizes the contribution of genetic research to the understanding of the phenomenon of the invasion of Red Sea fishes into the Mediterranean. Genetic results revealed, as expected, that the source and colonizing populations are essentially identical genetically and, with the exception of the recent colonizer the Bluespotted cornetfish Fistularia commersonii, there has been no reduction of genetic variability or bottleneck effect. The question whether Red Sea fishes colonizing the Mediterranean did so passively as drifting eggs and larvae or rather actively as swimming adults was discussed by Diamant. The study of the parasitofauna of Siganus rivulatus in both the Red and Mediterranean Seas reveals that some of the parasite species were carried by their adult hosts into the Mediterranean. Detection of invasive species from their initial stage of entry and population establishment in their new region is surveyed by Azzurro who presents examples from monitoring programs in Italy and the central Mediterranean basin. Francour presents the role played by marine protected areas, particularly in southern France, in protecting indigenous Mediterranean fishes and in slowing the spread and establishment of invasive species. The second part of the book covers regional aspects of fish invasions in the Mediterranean. Golani presents an historical and current overview of the invasion of Red Sea fish species into the Mediterranean and discusses their distribution and possible impact on indigenous ichthyofauna. The current status of invasive fish in the Mediterranean waters of Turkey, Greece, the Adriatic and Italy are presented by Bilecenoglu, Corsini-Foka, Dragicevic and Dulčić and Orsi-Relini, respectively. Fish introduction in the western basin of the Mediterranean, primarily from the Atlantic Ocean via Gibraltar, and their integration with the local ichthyofauna is described by Massutí et al. Last but definitely not least, Minos et al. focuses on reproductive aspects of the grey mullet Liza haemitochilus which was introduced from the Far East for aquaculture and stocking purposes into the Azov and Black Seas and spread via the Sea of Marmara into the Mediterranean Sea. We the editors are thankful to all the contributors who are renowned marine biologists from both the northern and southern shores of the Mediterranean and are intimately

10 Fish Invasions of the Mediterranean Sea: Change and Renewal

familiar both with their own country’s marine ecosystems as well as the wider issues affecting the entire Mediterranean. We would also like to acknowledge the following people: the organizers of the Cavtat conference, especially M. Mrakovcic, I. Buj and L. Zanella, from Zagreb University. Special thanks go to Ronald Fricke of the Staatliches Museum für Naturkunde, Stuttgart, for his help with the literature. Finally we wish to thank our children for their patience, understanding and inspiration.

Fish Invasions of the Mediterranean Sea: Change and Renewal 11

Contributors Brenda Appelbaum-Golani – Mt. Scopus Library, The Hebrew University of Jerusalem, 91905 Jerusalem, Israel. E-mail: [email protected] Ernesto Azzurro – ISPRA, High Institute for Environmental Protection and Research, Laboratory of Milazzo, Via dei Mille 44, 98057 Milazzo (ME), Italy. E-mail: [email protected]; [email protected]. Jonathan Belmaker – Interuniversity Institute of Marine Sciences, Eilat, Israel and Department of Life Sciences, Ben-Gurion University, Be’er Sheva, Israel. E-mail: [email protected] Frida Ben Rais Lasram – Laboratoire Ecosystèmes Lagunaires, UMR CNRS-IFREMERUM2 5119, Université Montpellier 2, cc 093, place Eugène Bataillon, 34095 Montpellier Cedex 5, France and Laboratoire Ecosystèmes et Ressources Aquatiques, Institut National Agronomique de Tunisie, 43 avenue Charles Nicolle, 1082 Tunis, Tunisie. E-mail: Frida. [email protected] Giacomo Bernardi – Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, CA 95060, USA. E-mail: bernardi@biology. ucsc.edu Murat Bilecenoglu – Department of Biology, Faculty of Arts & Sciences, Adnan Menderes University, 09010 Aydin, Turkey. E-mail: [email protected] Eran Brokovich – Interuniversity Institute of Marine Sciences, Eilat, Israel and Department of Evolution, Systematics and Ecology, The Hebrew University of Jerusalem, 91904 Jerusalem, Israel. E-mail: [email protected] Victor China – Interuniversity Institute of Marine Sciences, Eilat, Israel and Department of Life Sciences, Ben-Gurion University, Be’er Sheva, Israel. E-mail: [email protected] Maria Corsini-Foka – Hellenic Center for Marine Research/Hydrobiological Station of Rhodes, Cos Street, 85100 Rhodes, Greece. E-mail: [email protected] Ariel Diamant – National Center for Mariculture, Israel Oceanographic and Limnological Research Institute, Eilat 88112, Israel. E-mail: [email protected] Branko Dragičević – Laboratory of Ichthyology and Coastal Fishery, Institute of Oceanography and Fisheries, Setliste I. Mestrovica 63, 21 000 Split, Croatia. E-mail: [email protected]

12 Fish Invasions of the Mediterranean Sea: Change and Renewal

Jakov Dulčić – Institute of Oceanography and Fisheries, 21000 Split, Croatia. E-mail: dulcic@ izor.hr Panos S. Economidis – Karakasi 79, GR-54453, Thessaloniki, Greece. E-mail: [email protected] Patrice Francour – Nice University, Sciences Faculty, EA 4228 ECOMERS, Parc Valrose, 06108 Nice, France. E-mail: [email protected] Daniel Golani – Department of Evolution, Systematics and Ecology, The Hebrew University of Jerusalem, 91904 Jerusalem, Israel. E-mail: [email protected] Francois Guilhaumon – Laboratoire Ecosystèmes Lagunaires, UMR CNRS-IFREMER-UM2 5119, Université Montpellier 2, cc 093, place Eugène Bataillon, 34095 Montpellier Cedex 5, France. E-mail: [email protected] Anastasia Imsiridou – ATEI Thessalonikis, Department of Aquaculture & Fisheries Technology, P.O. Box: 157, GR-63200, Nea Moudania, Greece. E-mail: [email protected] Moshe Kiflawi – Interuniversity Institute of Marine Sciences, Eilat, Israel and Department of Life Sciences, Ben-Gurion University, Be’er Sheva, Israel. E-mail: [email protected] Luisa Mangialajo – Nice University, Sciences Faculty, EA 4228 ECOMERS, Parc Valrose, 06108 Nice, France. E-mail: [email protected] Enric Massutí – IEO- Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma, Spain. E-mail: [email protected] George Minos – ATEI Thessalonikis, Department of Aquaculture & Fisheries Technology, P.O. Box: 157, GR-63200, Nea Moudania, Greece. E-mail: [email protected] David Mouillot – Laboratoire Ecosystèmes Lagunaires, UMR CNRS-IFREMER-UM2 5119, Université Montpellier 2, cc 093, place Eugène Bataillon, 34095 Montpellier Cedex 5, France. E-mail: [email protected] Francesc Ordines – IEO- Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma, Spain. E-mail: [email protected] Lidia Orsi Relini – Laboratori di Biologia Marina ed Ecologia Animale, Via Balbi 5, 16126 Genova, Italy. E-mail: [email protected] Jérémy Pastor – Nice University, Sciences Faculty, EA 4228 ECOMERS, Parc Valrose, 06108 Nice, France. E-mail: [email protected] Francis Dov Por – Hebrew University of Jerusalem, Edmund Safra Campus, Jerusalem 91904, National Collections of Natural History, Department of Evolution, Systematics and Ecology. E-mail: [email protected] María Valls – IEO- Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma, Spain. E-mail: [email protected]

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 13 D. Golani & B. Appelbaum-Golani (Eds.) 2010 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 13-33. © Pensoft Publishers Sofia–Moscow

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect Francis Dov Por

Abstract A historical framework and forecast are given for the  recent biological tropicalization of the Mediterranean. The Eastern basin in particular is increasingly settled by tropical species, especially Lessepsian migrants, but also Senegalian newcomers are increasingly reported from the Western basins. A new Tethys situation is evolving. Recent changes, especially in the ichthyofauna, are compared with the Neogene fossil documents (mainly from the Tortonian, Piacenzian and Eemian stages). The number of newly recorded tropical fish approaches 100 and that of the other biota is assumed to be in the thousands. This is a new episode in the geological history of the Mediterranean, in which the presence of tropical biota was interrupted only briefly during the Pleistocene.   With a continuing warm climate and the rapid increase in the number of tropical re-settlers, the Mediterranean will again become  a subtropical-tropical sea, albeit  devoid of coral reefs and associate fauna because of distributional barriers.

INTRODUCTION For the past few decades, the Mediterranean has been the stage for the most important biogeographic event in the contemporary globe. The “Legacy of Tethys” (Por and Dimentman, 1989) is alive and a new Tethyan biogeographic pattern is presently being re-established. Although contact with the Cretaceous-Paleogene Neotethys was interrupted 15 million years ago, tropical species of Tethyan ascendancy survived in a warm Mediterranean until the late Pliocene glaciations started, less than 3 million years ago, and exterminated almost all of them. After this short geological interval, tropical biota are now returning in numbers and, in their modern guise, to their old haunts.

14 Francis Dov Por

Surface temperatures in the Mediterranean have increased by 1.1°C during the last 27 years. Sará et al. (2006) even speak of an increase of 3.0°C in the main sea level temperature of the Mediterranean during the last 10 years, i.e. from 20-21°C to 23-24°C. There is a unique opportunity to see such changes of geological proportions in our lifetime and on our doorsteps. First of all, Lessepsian migration (Por, 1969, 1978), but also increased tropical influx through Gibraltar and the recent climate optimum go hand in hand resulting in a tropicalization of the Mediterranean biota (Francour et al., 1994; Bianchi, 2007). This trend is expressed in all the wide taxonomic array of marine fauna and flora. New reports of tropical species, chiefly of Indo-Pacific origin appear almost weekly, although the whole process is inadequately and unequally monitored and many taxa go sorely uninvestigated. It is a safe assumption that the number of the newly arrived tropical species already runs, or will soon run, into the thousands. By the time this review goes to press, the number of immigrant fish species will certainly have reached 100, about 90% of them Lessepsian migrants. Some 30 species of symbiont-bearing warm water Foraminifera have already established themselves in the Mediterranean (Hyams et al., 2002; Langer, 2008). According to these authors, most of the species have entered through the Suez Canal, although establishment in the warming Mediterranean may have occurred also through the Atlantic portal or even by introduction through ship ballast. These Foraminifera supply stratigraphic documentation for an as yet, unnamed geological episode that began in our days. The additions to the Mediterranean ichthyofauna have been the most accurately and best studied (Golani et al., 2002; Golani et al., 2006) Moreover, the fishes have a good palaeontological documentation. Therefore, for this non-ichthyologist author, the fate of the fish fauna can be seen as an example of the general historical context in which the radical changes are occurring in the Mediterranean. NO ROGUE ALIEN INVADERS A preliminary analysis of the changes in the Mediterranean fish fauna reveals that we are not dealing with a phenomenon comparable to the issue of the anthropic invasive species worldwide. There are many well documented cases of invasive fish species, all of them in fresh waters, or at least in estuarine waters, but scarcely any cases of marine fish invading alien seas. At best, there are a few cases of area increase. In the Mediterranean though, there is the isolated appearance of the Brazilian sandperch Pinguipes brasilianus Cuvier, possibly brought in by ballast water (Orsi Relini, 2002). Actually, the Mediterranean is singularly resistant to invasion by “classical” invasive species (Por and Dimentman, 2006). As a rule, there are a number of typical, geographically rather limited, cases of typical invasive records of invertebrates in the northern Adriatic, a relatively cool and

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 15

less oligotrophic extension of the main Mediterranean, or mainly around aquaculture sites and harbors. Therefore, I always made a clear distinction between natural migration of whole biota and isolated invasions by rogue species, even if, as in the case of Lessepsian migration, the causation was a man-made seaway, the Suez Canal. The natural seaway of the Dardanelles, 450 m wide at the narrowest point is not significantly larger than the 300 m wide modern Suez Canal (Fig. 1). The Canal is an artificial replica of seaways resulting from tectonic changes. As with several other anthropic changes, such as for instance the increased emission of greenhouse gasses, the results are equifinal with natural events of geologic emissions of such gasses. Passive transport through the Suez Canal by fouling or in ship ballast most probably contributes to the present enrichment of the Mediterranean with tropical species of some plant and animal taxa. However, presumably, all the newcomer Lessepsian immigrant fishes in the Mediterranean migrated actively through the waters of the Suez Canal and its lakes and established their populations in the new marine environment by natural means. They gradually widened their range, and, often competitively, acquired their new niches. They did not disrupt pest-like, existing ecosystems, neither did they cause economic harm, nor did they lead to extinctions. They do not deserve the value-loaded sobriquet of “worst invasive species”. Likewise, the newly arrived West African tropical fish species are “Senegalian immigrants” through the Gibraltar seaway and not invasive aliens. There has always been an exchange with the Atlantic through the Straits of Gibraltar, since it opened. What is happening now is a new phase in the geological history of the Mediterranean fish fauna. The Mediterranean is regaining its tropical biota, lost when the Tethys Sea closed in the upper Miocene and especially after the Pleistocene cooling put a final touch to this. We have the unique chance of witnessing this process of re-colonization. By downgrading this phenomenon to a collection of “invasive species”, a modern scientific catchword, we are not only missing the point, but side-tracking the required research effort. Calls for hand-picked elimination of migrant organisms, or even for physical blocking of the Suez Canal to further migration cannot Fig. 1. The northern stretch of the Suez be taken seriously. Canal before the last widening

16 Francis Dov Por

A CRADLE OF THE MARINE TELEOSTS The Mediterranean had the most extreme and eventful geological history of any known oceanic water body. After the break-up of Pangea, our area was flooded by the sea. Marine historical biogeography of today has its beginnings in this tropical Tethys Ocean, the cradle of the modern marine biota. Geologists separate an older Paleotethys from this newer Triassic-Cenozoic Neotethys (see for example Makhlouf, 2006). Initially an oceanic gulf of the Mesozoic “Semail Ocean” (roughly today’s Arabian Sea), it opened to the nascent Atlantic only subsequently (Fig. 2) When dealing with the marine fishes, the lower Cretaceous was the high day of the teleost re-invasion and diversification in the oceans. The Mediterranean segment of Neotethys is seen as the cradle of the marine teleost fauna. Cavin et al. (2007) consider that the central Tethys might have been a centre of origin for the Cretaceous fishes, like the IndoWest Pacific of today, which is the evolutionary centre for the recent tropical fish fauna. The Levantine Basin of the Eastern Mediterranean is an authentic residual oceanic basin of the Mesozoic Tethys. It is perhaps not entirely incidental that the rich Cretaceous fish beds of Lebanon, Hakel, Hajula and Namoura, contain the most important information about the Mesozoic origins of the modern bony fish in the Tethys (Calvin et al., 2006). En Yabrud in the Palestine territory also yielded lithographic plates with important findings, such as the saber-toothed herring genus Enchodus Agassiz (Chalifa, 1989) (Fig. 3). By the Eocene, a fully -fledged fauna of tropical fishes inhabited the Mediterranean, as best documented in the Italian Lagerstat of Monte Bolca. This is considered to be by far the largest and best preserved fossil assemblage of teleost fish fauna. Bellwood (1995) mentioned the predominance of Holocentridae pine cone fishes there and considered that the fauna was typical for coral reefs. Robertson (1998) disagreed, mentioning that not all the fish species considered today to be “reef fishes” are necessarily dependent on corals. This is a consideration which we will take into account later in our discussion. It should be also mentioned that the rich Monte Bolca thanatocenose indicates perhaps

Fig. 2. A reconstruction of the late Cretaceous Tethys Sea

Fig. 3. Enchodus sp. (Chalifa, 1989)

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 17

the occurrence of a very extreme environmental happenings, possibly related to active tectonics and volcanism or to a sudden estuarine crisis (Bellwood, 1998). After the climatic maximum and the optimal development of the palaeo-Mediterranean tropical fauna during the Oligocene, the northward movement of the Indian plate and of the Arabian-African plate obstructed the Tethys Ocean. The severance in the Mesopotamian region was gradual. For some time a supposedly hypersaline “Mesopotamian Trough” persisted. The Terminal Tethyan Event (Adams et al., 1983), i.e. the final separation of the Mediterranean from the Semail Ocean, the nascent Indian Ocean, occurred 13.65 million years ago at the base of the Miocene Serravallian (Harzhauser et al., 2007). Subsequently the tropical centre of speciation of fishes, corals, mollusks and echinoderms shifted to the Indo-West Pacific. There is very little knowledge of the Mediterranean fish fauna of the later Miocene. Fish assemblages of the Tortonian are known for instance also from Gavdos (Gaudant, 2002). The codlet †Bregmaceros albyi (Sauvage) was the dominant fish (Gaudant et al., 2005). The presence of the Indo-West Pacific round herring Spratelloides gracilis (Temminck and Schlegel) in the Tortonian fish fauna led Gaudant (2002) to question if there was a total separation from the Indian Ocean. There is however no geological proof for such a resilient contact. The nascent Red Sea was indeed in contact with the Mediterranean since the early Miocene. However, during the Tortonian this basin lost both its connection to the Mediterranean and to the Indian Ocean, and became hypersalineevaporitic (Bosworth et al., 2005). SURVIVING THE MESSINIAN CRISIS Contact between the Mediterranean and the Atlantic Ocean started to be difficult some 7.1 million years ago and then was interrupted altogether. The result was the Messinian Salinity Crisis, which lasted till 5.32 million years ago. At its discovery, it was assumed that the Mediterranean became hypersaline or a dry playa basin in its entirety. Today, the ideas are different (see Briand, 2008). Repeated incursions of Atlantic water furnished the enormous salt deposits of the evaporitic Messinian phase. During a period of a few tens of thousands of years, between 5.6- 5.5 million years ago, there was the short climax of the crisis. During the whole range of the Messinian Crisis, shallow marginal water bodies with brackish, marine to hypersaline environments existed, which were not necessarily adverse to marine life. The initial idea that marine life disappeared altogether from the hypersaline Mediterranean basin during the Messinian Salinity Crisis does not hold anymore (Por and Dimentman, 2006). The Persian Gulf, with its Pleistocene history and wide range of elevated salinity values, would be a kind of small-scale comparison with the Messinian Mediterranean. The re-connection of the Mediterranean with the Atlantic Ocean, an event which marks the start of the Pliocene, has been precisely dated at 5.32 my ago, however the

18 Francis Dov Por

exact time of the opening of the Red Sea to the Indian Ocean which supposedly happened at around the same time, is not known. The fish fauna of the Salinity Crisis period was represented by the widely present killifish †Aphanius crassicaudatus (Agassiz) and also by some brackish to freshwater species, especially during the Italian “Lago Mare” brackish phase of the late Messinian (Gaudant, 2002). But marine fauna survived in marginal basins. As to the Messinian Mediterranean marine fishes, Sorbini and Tirapelle-Rancan (1980) mention the dragonet Callionymus pusillus Delaroche and a cornetfish Fistularia. L. Sorbini (1988) reported marine fishes from the evaporitic Messinian in the Italian Monte Castellaro fish beds, among them a scorpion fish Scorpaena sp., a false herring Harengula sp., and most important, the above mentioned Spratelloides gracilis and the typically Indo-West Pacific razor fish Centriscus strigatus Wheeler (Fig. 4). Sorbini attributed “temperatures more or less tropical or subtropical” to the Messinian marine areas. Based on fossil otolith studies, Landini and Sorbini (2005) also confirm the continuity of some tropical Indo-West Pacific fish taxa during the Messinian crisis. They assume the existence of hypothetical “Lazarus taxa” that survived the Salinity Crisis unnoticed as fossils, then reappearing in the Pliocene. Perhaps they survived in the Eastern Mediterranean where, according to these authors, the effects of the salinity crisis were weaker. The authors conclude that “a significant part of the fish fauna remained in the basin, minimizing the effects of the Messinian crisis”(Landini and Sorbini, 2005). It is worthwhile mentioning that shallow marine environments existed during the Messinian evaporative phases in the area of the Nile Delta (Ottes et al., 2008). According to Griffin (2002) the salt deposits in the Gulf of Suez are of Tortonian age, i.e. not coeval with the Mediterranean salt deposits. In the Gulf of Suez and in the Northern Red Sea it was the successive humid Zeit formation, with marine deposits which was coeval with the Messinian salinity crisis in the Mediterranean. The significance of these normal salinity conditions in the Nile Delta and in the neighboring Red Sea for the history of the Messinian fish fauna has still to be elucidated. A major problem is the fact that there is no precise chronology for the closing of the Red Sea to the Mediterranean and its opening to the Indian Ocean. As mentioned, the incipient Red Sea lost its contact with the Mediterranean and with the Indian Ocean around 10 million years ago in Tortonian times, when the initial rifting stopped its northward advance and turned 45 0 eastward, resulting in the Aqaba-Dead Sea slip movement transform. As a result, the Gulf of Suez area was compressed and the Isthmus of Suez formed. The Fig. 4. Centriscus strigosus Pliocene of Marecchia

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 19

Red Sea reopened to the Indian Ocean approximately 5 million years ago (Bosworth et al., 2005). The marine normalization events of the Mediterranean and of the Red Sea were most probably not concomitant. Much could have happened during the tens of thousands of years of asynchrony between the two normalization events. Unfortunately, there is no information about the living world of the Pliocene Red Sea and most specifically of its fishes. THE PIACENZIAN CLIMATIC OPTIMUM The Zanclian, the first Pliocene phase after the opening of the Gibraltar, starting 5.3 million years ago, saw a massive influx of temperate and cool water species, including also fishes (Landini and Sorbini, 2005). This faunistic element is still dominant in the present Mediterranean fish fauna. Around 3 my ago, during the Piacenzian phase, a marked climatic optimum occurred, with average yearly sea surface temperatures 50 C higher than today and with sea levels rising to 35 m above present sea level. The climate was also less seasonal and wetter, with 400-1000 mm/year more precipitations (Haywood et al., 2000). Emig and Geistdoerfer (2004) consider that the conditions of the early Pliocene were warm-temperate right from the start, similar to the Piacenzian. There are numerous records of tropical fish in the Piacenzian Mediterranean, some with Indo-West Pacific affinities, like those from the classical Marecchia site in Italy (Sorbini, 1988; Sorbini and Tyler, 2001; Landini and Sorbini, 2005). These include several Monacanthidae, among them the filefishes Stephanolepis cf. diaspros Fraser-Bruner (Fig. 5) and Alutera sp., the above mentioned Centriscus, Spratelloides as well as the spotted halfbeak Hemiramphus cf. far (Forsskål), the red-eye round herring Etrumeus teres (Dekay), † Bregmaceros albyi and the red squirrelfish Sargocentron cf. rubrum (Forsskål). Two alternative or complementary hypotheses can explain this outburst of tropical fish species. Either they survived the Messsinian and the relatively cold-water phase of the early Pliocene Zanclian and flourished again on site, or they resettled from the Red Sea. For instance, †Bregmaceros albyi, a dominant species earlier, in the Tortonian of the island of Gavdos (see above) could be such a survivor. The second hypothesis is plausible too, since at the high Piacenzian sea levels, the Isthmus of Suez which separated the Mediterranean from the Red Sea could have been flooded and possibly a normal marine connection Fig. 5. Stephanolepis diaspros (photo D. Darom)

20 Francis Dov Por

between the two seas might have existed. Sorbini (1988) even compared the settlement of the Indo-West Pacific Pliocene fishes along the shores of Pliocene Northern Italy, to the present influx of Lessepsian fishes. The Piacenzian mollusk fauna of Italy also contained several species of cowry shells and auger shells as well as many other mollusk species which disappeared in the recent Mediterranean. The cowry shell Lurida lurida (L. ) is the only cowry that survives today in this sea. Coral reefs of Porites did not survive in the Pliocene Mediterranean and if indeed aquatic contact with the Red Sea across the Isthmus of Suez was established, it might have been impracticable on edaphic or hydrographic grounds for the influx of Indo Pacific coral species. This, obviously, should not have hindered the arrival of several “coral reef fish” species, a situation reminiscent of the current Lessepsian historical phase (see below). Checconi et al. (2007) mention the absence of coral reefs and the low representation of the symbiont-bearing foraminifer Amphistegina d’Orbigny in the Mid-Pliocene Tyrrhenian Sea and reach the conclusion that the sea temperatures there were warmtemperate and not tropical. Foraminifera of this genus do not withstand temperatures below 140 C (Langer and Hottinger, 2000), which means that winter temperatures in the Tyrrhenian Sea were warmer than today. The Mid-Pliocene optimum is considered by some authors as a possible model for the presumed “Hyper-Interglacial” of the warming globe of today. The Piacenzian warm climax lasted possibly only for a few hundreds of thousands years. At the beginning of the Gelasian, the third Pliocene phase, 2.6 my ago, the glaciation cycles started and cold water conditions developed, gradually phasing into the cold Pleistocene. There was a renewed influx of cold water Atlantic fishes and the last surviving populations of Indo-West Pacific fishes died out. THE LEVANTINE PLEISTOCENE WARM CUL-DE-SAC During the lower Pleistocene, most of the Mediterranean behaved like a temperate oceanic water body, even with a certain number of deep-sea fishes (Girone et al., 2006). According to these authors, the contact with the Atlantic via Gibraltar must have become subsequently gradually shallower and the Mediterranean evolved towards its present peculiar hydrography, with a very limited deep sea ichthyofauna. At the low glacial sea levels, the contact with the world ocean was more difficult. In its turn, the Eastern Mediterranean became even more isolated from the Western Mediterranean than today. The complex of Boreal mollusks, the “Arctica islandica fauna”, which characterizes the glacial Mediterranean apparently did not reach the shores of the Levant. Some of the boreal fishes, like the European hake Merluccius merluccius (L), the European sprot Sprattus sprattus (L) and the hagfish Myxine glutinosa (L), survive in the colder parts of the Mediterranean. They too did not reach or survive in the Levantine basin. An indication

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 21

though for colder temperatures there is given by the rather isolated finding of the Boreal foraminiferan Hyalinea baltica (Schröter) in Pleistocene boreholes on the Israeli coast (Moshkovitz and Ehrlich, 1980). In the nearly enclosed water body of the Mediterranean the sea surface temperatures varied widely, especially during the cold and low sea level glacial conditions. During the glaciations a very low annual temperature range of 7-150C was calculated for the Western Mediterranean and 8-220 C for the Aegean Sea. However, according to Thunell (1979), during the glacial periods the sea surface temperatures in the Levant Sea and along the North African shores remained probably broadly similar to those of today. During the repeated climate pulsations, the Levant remained more or less stable, with minimum winter temperatures slightly oscillating at or around 17°C. The temperature gradient between the Western Mediterranean and the Levantine basin must have been therefore much steeper than today. As shown by Stewart Grant (2005), the genetic indicators of the Mediterranean and Black Sea populations of the anchovy Engraulis encrasicolus (L) testify for repeated extinctions in the Mediterranean and repeated re-colonization from the Atlantic. Influx of warm, sub-tropical Atlantic fish fauna into the Mediterranean was possible during the short interglacials (Girone and Varola, 2001). In a very sketchy way, there were probably several interglacial pulses of sub-tropical Senegalian fauna alternating with the pulsations of Boreal fauna (Por, 1975). The period which has been investigated the best is the last interglacial, the Eemian interglacial, dated between ca 125, 000 -110, 000 years ago, corresponding to the Marine Isotopic Substage MIS 5e, when temperatures were 2-30C higher than today. This entire warm episode, which lasted only for 14, 000 years or so, was subdivided further into two warm phases by van Kolfschoten et al. (2003). Tropical species of mollusks, the so-called “ Strombus bubonius fauna”, penetrated the Mediterranean from tropical West Africa during these short warm intervals but disappeared partially afterwards during the last glacial, even in the warmest south-Eastern Mediterranean. An earlier Interglacial, corresponding to MIS11, had a longer duration than the Eemain (lasting between 425.000-375.000 years ago), with temperatures warm and similar to those of today (de Vernal and Hillaire-Marcel, 2008). This must have been another opportunity for West-African tropical species to enter the Mediterranean. Some mollusks and crustaceans belonging to these tropical influxes survive to this day, for instance the ghost crab Ocypode cursor (L), and others, which have today a disjunct Senegalian –south-Eastern Mediterranean distribution. Among fishes, the Haifa grouper Epinephelus haifensis Ben Tuvia, described more than 50 years ago (Ben Tuvia, 1953), the Madeiran sardinella Sardinella maderensis (Low) as well as the African hind Cephalopholis taeniops (Valenciennes), recently reported from the largely uninvestigated Libyan coast (Ben Abdallah et al., 2007), have a similar southeast Mediterranean-Senegalian disjoint distribution. The damsel fish Chromis chromis (L), a lone representative of its large family of reef fishes, is considered also to be a warm water relic in the Mediterranean.

22 Francis Dov Por

The cold Canaries Current along the Mauritanian and Atlantic Moroccan coasts interposes an oceanographic barrier between the tropical African fauna and the Gibraltar. The fluctuating regime of this current, along with the North Atlantic current, has probably offered opportunities from time to time to tropical species, especially to fish, to pass Gibraltar (Emig and Geistdoerfer, 2004), reaching and surviving in the sub-tropical enclave of the south-Eastern Mediterranean. Such might have been the case in the postglacial warm episodes, even several hundreds of years ago, during the Medieval Warm Period. Gibraltar probably served also as an alternating two-way movement. Remaining always warmer than the Atlantic ocean outside, the Mediterranean could also serve as a refuge for some warm-water fishes like the ornate wrasse Thalassoma pavo (L), which according to Domingues et al. (2008) repeatedly re-colonized the Macaronesian Islands in the East Atlantic. During the whole of the Pleistocene there were no opportunities to breach the barrier separating the Mediterranean from the Indo-West Pacific fauna of the Red Sea and there were most likely no instances of Eastern tropical fishes reaching the Mediterranean cul-de-sac. As shown above, the Gulf of Suez was initially part of the Eocene-Oligocene rifting process of the Red Sea. However, in the Pleistocene the tectonism moved eastward to the Gulf of Aqaba. The Gulf of Suez remained a shallow basin and was repeatedly dry or hypersaline during the low glacial sea levels. At these worldwide low sea levels the gap separating the Mediterranean from the Red Sea was repeatedly much broader than today. The highest elevation on the Isthmus of Suez 23 m. is at El Guisr. Therefore, even at the Eemian high sea levels of + 3-5 m ( Jedoui et al., 2002), there existed no open seaway through the Isthmus. This was still the situation, even if the Eemian sea level reached + 8 m, as inferred by Emig and Geistdoerfer (2004). The land gap was narrowed to perhaps only 20 km, instead of the 150 km. today (Fuchs, 1878). Under the influence of the Nile, however, the Isthmus was always dotted with a series of fresh to hypersaline lakes and lagoons and was even cut across by ancient Nile delta branches (Por, 1971). No marine fish could have crossed this hydrographic barrier during all the duration of the Pleistocene. The waters of the Isthmus of Suez probably remained the exclusive domain of the killifish Aphanius dispar (Rüppell) (Fig. 6). A possible exception though is the roving gray mullet Liza carinata (Valenciennes) from the Red Sea, which could have managed to overcome the natural hurdles of Fig. 6. Aphanius dispar dispar (from Fish Base).

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 23

the Isthmus even in pre-Lessepsian times (Por, 1978). Phylogeographic analysis of the populations on both sides of the isthmus should check this conjecture. The digging of the Suez Canal by Lesseps in 1869 was therefore an event of geological significance. It re-established the tropical Tethyan contact of the Mediterranean, which was lost some 15 million years ago, perhaps with the exception of the short interlude in the Piacenzian. This allowed, and allows now, the re-colonization of the Mediterranean by fish species, descendants of the Neotethyan fauna and by other tropical biota as well. GLOBAL WARMING AND LESSEPSIAN MIGRATION Had the Suez Canal have been built in the 17th century, in the middle of the “Little Ice Age”, following a recommendation by the mathematician and humanist Leibniz to Louis XIV, there would probably have been much less migration through the Canal. The warming of the Mediterranean as part of the climatic optimum which started in the 19th century has been and is coincidentally propitious to the immigration of tropical fishes through the modern Suez Canal (Fig. 7). For about 40 years after its opening, the hypersaline salinity barrier of the Bitter Lakes only allowed for some estuarine fish to inhabit the canal waters. Shortly after their flooding, Keller (1882) mentions Mediterranean estuarine species from there, such as the flathead gray mullet Mugil cephalus (L), the European sea bass Dicentrarchus labrax (L) and the corb Umbrina cirrosa (L) The only early Red Sea species mentioned in the Canal by Keller were the pony fish Leiognathus klunzingeri (Steindachner) and Reconstructed Temperature 0.6

2004

Temperature Anomaly (°C)

0.4

Medieval Warm Period

0.2 0 -0.2 -0.4 -0.6 -0.8

Little Ice Age

-1 0

200

400

600

800

1000 1200 1400 1600 1800 2000

Fig. 7. Temperature curves of the last two millenia.

24 Francis Dov Por

karenteen sea bream Crenidens creniden (Forsskål). Interestingly, 6 or 7 Mediterranean estuarine fishes, like those mentioned above, are till today the only “anti-Lessepsian” migrant fishes, that is, species that crossed the Canal in the opposite direction. They are present today only in the two northern Red Sea gulfs and did not advance farther south (Dor, 1984; Goren, 2008). By the turn of the 20th century, the salinity barrier had decreased to below 50 ppm, owing to the flushing out of the salt deposits in the Bitter Lakes. Tillier (1902) already reports a list of 14 Indo-West Pacific fish species from the Canal waters, all of them future Lessepsian migrants. Salinities, well in excess of 40 ppm, are usual for the marine Red Sea fishes but not for the Mediterranean ones. These are the marine metahaline salinity values (Por, 1972, 2008) which are common in the Red Sea but not in the Mediterranean. Even at present the Bitter Lakes resemble the Gulf of Suez and various inshore habitats of the Red Sea, with salinity levels around 44-45 ppm. Migration through the Suez Canal became unidirectional. The estuarine hardyhead silverside Atherinomorus lacunosus (Forster in Bloch and Schneider), as well as pony fish Leiognathus klunzingeri (Steindachner) (Fig. 8) were the first Indo-Pacific species to appear in the open Mediterranean (Tillier, 1902). By the 1920s the immigration was already progressing along the Levantine coasts (Steinitz, 1927). During World War II, with the rabbitfish Siganus rivulatus Forsskål, it reached Turkey and Rhodes. Interestingly, three of the Pliocene tropical fishes reported by Sorbini (1988), namely Hemiramphus, Stephanolepis and Sargocentron,, were in the first wave of immigrants to resettle the Mediterranean. After the stabilization of the salinity barrier at its present levels, another factor which contributed to the increase in Lessepsian migration has been the deepening and widening of the Suez Canal (see Galil, 2006). However, the most important agent in the recent amplification of the immigration is probably global warming as expressed recently in the Mediterranean (Fig. 9). There has been an increase in the number of immigrants over the last two decades and there is no sign of abatement nor of any case of attempted and failed immigration, though a few of the immigrants are still rare. In 1978 I raised the hypothesis that the Lessepsian migration was nearing a plateau. This has not been the case, although, as discussed below, there are still limitations to immigration and these will remain as such for the foreseeable future. I concluded also (Por, 1978), that the immigration seems to be mainly anti-clockwise, Fig. 8. Leiognathus klunzingeri (photo D. Darom)

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 25

along the Levantine and Anatolian coasts and lamented the lack of information from the Libyan coast. Information from there is still poor, but there are cases of westward, clock-wise migraTotal sea surface temperature changes in the Mediteranean tion of foraminifera Sea, 1982–2003 (Langer, 2008). Ben Rais Lasram et al. -1.0 -0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 (2008b) emphasize the prevalence of the Fig. 9. Sea surface temperature changes during the last two decades. anti-clockwise direction of the Lessepsian migration, reiterating the role of the dominant inshore current in the Levant basin. More recently (Por, 1990), I have defined the Mediterranean area occupied by the Suez Canal immigrants as a “Lessepsian Province”, the boundaries of which will expand or shrink according to the climatic evolution of the area. It is now evident that this area has been expanding since that date, mainly progressing along the Adriatic shores and pushing northward into the Aegean Sea. For some time the Straits of Sicily were considered to be the western limit of the Lessepsian migrants, the “crossroad between Atlantic and Indo-Pacific worlds” (Andaloro and Azzurro, 2004) but Castriota and Andaloro (2005) mention the presence of rabbitfish Siganus luridus (Rüppell) and of the bluespotted cornetfish Fistularia commersonii Rüppell from the Tyrrhenian Sea of the Western Mediterranean. The former species, a very successful herbivore, spread gradually since its first Mediterranean mention in 1964, whereas the latter was first reported in the Mediterranean only in 2000 (Golani, 2000) and spread at breakneck speed. Ben Rais Lasram et al. (2008b) define the area around the island of Rhodes and probably also off southern Tunisia, where mean surface temperature drops presently from a tropical 20.80C to a cooler 18.95 0C as critical for the advancing Lessepsian migrant fishes. Yet, Leiognathus klunzingeri and in sequence Siganus rivulatus, two of the early Lessepsian migrants, have already reached the southern Adriatic (Dulčić and Pallaoro, 2002; Dulčić and Pallaoro, 2004). In general, the early arrivers into the Mediterranean are also the ones that spread farther west. Among the mollusks, the small mussel Brachidontes pharaonis (Fischer) appeared at Port Said in 1882, reached the Israeli coast in the 1930’s, Eastern Sicily in the 1970’s and recently crossed into the Western Mediterranean (Sará et al., 2006). Sargocentron rubrum (Fig. 10) lived in the warm Pliocene Mediterranean (see above). It took an early opportunity to enter the Suez Canal and

26 Francis Dov Por

appeared in 1927 along the coast of Israel and reached today Sicily and Tunisia. This species is not an invasive alien; it is the emblematic Tethyan re-colonizer of the Mediterranean. Ben Rais Lasram and Mouillot (2009) count 63 Indo-Pacific species in a total of 664 Mediterranean fish species. The immigrant Lessepsian fish already represent 15% of the fish species diversity in the Eastern Mediterranean and 9% in Fig. 10. Sargocentron rubrum (photo: Maoz the Mediterranean as a whole (Mavruk and Fine) the emblematic Tethyan re-colonizer Avsar, 2007). These are not “invasive Erithrean aliens” as they are sometimes called, but repatriating species of old tropical Tethyan origin. They reached the Mediterranean swimming and expanding within this sea by their own natural means and did no need “direct transport.. as the main factor/corridor for introduction”(Rilov and Galil, 2009). CLOSING THE MEDITERRANEAN GAP At its best, the Neotethys was a world-spanning circumtropical biogeographic realm. In the words of Ekman (1967) “The Indo-West Pacific, the Mediterranean, the tropical Atlantic and the East Pacific faunas, were parts of one major unit, the Tethys fauna”. The modern Mediterranean represents the major gap in this once continuous tropical belt. There are indications that this gap is closing. As a matter of fact, the circumtropical distribution of many planktonic organisms was never interrupted. In the specific case of the Mediterranean, one can often find the same species of tropical planktonic species at both ends of the Isthmus of Suez without being able by classical taxonomic methods to establish if the Mediterranean population came the “Western way” from the Atlantic or through the Suez Canal (Steinitz, 1929). The actively migrating spinner shark Carcharhinus brevipinna (Müller and Henle), considered previously to be a Lessepsian migrant has also an unbroken circumtropical distribution (Por, 1978). Several sharks, included by Ben Rais Lasram et al. (2008a) in the category of the “neo-Atlantic colonizers”, also have a circumtropical distribution. Such is the case of the small-toothed sawfish Pristis pectinata Latham which was first reported in the Mediterranean in 1810 from the Israeli coast. Other newcomer Mediterranean sharks on the list, like the great hammerhead Sphyrna mokarram (Rüppell), or the milk shark Rhizoprionodon acutus (Rüppell) are circumtropical too, found both in the Atlantic and in the Red Sea. The oceanic puffer Lagocephalus lagocephalus (L. ) is a circumtropical species, first reported in the Mediterranean in 1893 (Ben Rais Lasram

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 27

et al., 2008a), but is unknown from the Red Sea proper and, so far, absent from the Eastern Mediterranean. Ben Rais Lasram et al. (2008a) designates as “neo-Atlantic colonizers” the tropical fishes which have entered the Mediterranean through Gibraltar during the last two centuries. The fact that during the last two centuries Senegalian species are entering the Mediterranean, instead of Boreal ones (Ben Rais Lasram et al., 2008a), is perhaps the most concrete indicator for the warm climate period which we are witnessing. The best colonizers are found today in the Alboran Sea and along the coasts of Spain and Algiers (Ben Rais Lasram, op. cit. ). Outstanding is the amberjack genus Seriola, a pelagic predator, which has three migrant species reported from the Tyrrhenian Sea. Some 8 neo-Atlantic species have already reached the shores of the Levant. The fangtooth moray Enchelycore anatina (Lowe) which has an easily drifting pelagic larval stage, made possibly its way straight to the shores of Israel (Golani et al., 2006). Another quick success is that of the smooth puffer Sphoeroides pachygaster (Müller and Troschel), which was first reported from Spain in 1980 and is presently already found along the Levantine coasts (Golani et al., 2006). The round herring Etrumeus teres, rightly considered to be a Lessepsian migrant, is also circumtropical, widespread in the warm Atlantic, though not along the west African shores. The round herring, as discussed above, was present in the Piacenzian material of Sorbini (1988). The codlet Bregmaceros atlanticus Goode and Bean, a widely circumtropical species, has recently been recorded in the Mediterranean by Yilmaz et al. (2004). †Bregmaceros albyi, as mentioned above was a dominant species in the pre-Messinian and in the Piacenzian fish fauna of the sea. The tropical Atlantic bastard grunt Pomadasys incisus (Bowdich) met the Indo-West Pacific striped piggy Pomadasys stridens (Forsskål) in the newly warm Mediterranean. In recent times there were no puffer fishes in the Eastern Mediterranean. By now, the Atlantic migrant Sphoeorides pachygaster meets there no less than four newcomer IndoWest Pacific puffer fish species (Golani et al., 2006). The restoration of the circumtropical species ranges with the disappearance of the Mediterranean gap is also a good indicator for the progressive return to Tethys conditions in this sea. INTRINSIC CHANGES IN THE MEDITERRANEAN A warming Mediterranean led also to shifts in the distribution of the autochthonous species. There are several instances of species hitherto restricted to the warm African sector of the Mediterranean that now appear in the northern basins. The best and most spectacular example among the fishes is that of the ornate wrass Thalassoma pavo (L). There are also several new reports of warm water fishes advancing northward in the Adriatic Sea, for instance of the white grouper Epinephelus aeneus (Geoffroy de SaintHilaire) (see Dullo et al., 2006). Among the invertebrates there is, for instance, the

28 Francis Dov Por

well-monitored expansion of the warm water coral Astroides calycularis (Pallas) to the Adriatic Sea (Grubelic et al., 2004). Ben Rais Lasram and Mouilot (2008), following other authors, fear for the fate of the endemic Mediterranean fish species facing the new immigrants. Nothing indicates such a negative effect, unlike the case of the introduced exotic invaders in the terrestrial or fresh water realms. We have no notice of any competitive extinction of local species. There seems to be an accommodation between the local species and the newcomers, like for instance a division of depth ranges, the Mediterranean species leaving the shallower waters for the Indo-Pacific ones. The shallow rocky bottoms and the deep waters, as shown below, are not yet impacted by newcomers. There will be however a continuing and gradual shift in the areas of distribution within the Mediterranean. Like in past climatic fluctuations (Por, 1975) the species with Boreal affinities will retreat further into their cold water refuges, along the Ligurian shores, the northern Adriatic Sea and northern Aegean Sea. The fauna of the Mediterranean will continue to be a mixture of the old and the newcomer species. In the long run it even might be possible that some Mediterranean species, among them endemic ones, will be eliminated. But such cases will not be caused by direct by claws-and-teeth competition with the tropical incomers, but rather due to a further warming of the Mediterranean waters. Such extinctions will be natural biogeographic and evolutionary phenomena, like everything which is happening now in the natural environments of the warming Mediterranean. TOWARDS A NEW TETHYAN ICHTHYOFAUNA? Analyzing the data base on invading species of the Mediterranean maintained by Argyro Zenetos and her colleagues, it appears, despite the incompleteness of our information, that the Lessepsian migrants make up around 75% and the Senegalian migrants around 15% of the newcomers. The remaining 10% are anthropic introductions or “cryptogenic” species, i.e. species with an uncertain previous record. Almost two decades ago, I defined a Lessepsian province in the Mediterranean (Por, 1990) as a possible embryo of a new Tethys. We can now test the prognostics of this process, i.e., how much Tethys-like will the Mediterranean biota become? The southeastern Mediterranean with winter surface temperatures never dropping below 18°C has already been re-settled by many symbiont-bearing Foraminifera (threshold 14°C) and could already have been potentially again inhabited by scleractinian reef building corals (threshold 15°C for individual colonies). But no Indo-Pacific scleractinian coral has actually settled the Mediterranean. As a consequence, there are still no butterfly fishes (Chaetodontidae), surgeon fishes (Acanthuridae) or angel fishes (Pomacanthidae) in the Mediterranean. There are other species considered to be coral fishes among the immigrants, but they can manage without corals.

The new Tethyan ichthyofauna of the Mediterranean – historical background and prospect 29

The fish fauna of the shallow rocky littoral along the Israeli coasts is still the original Mediterranean one, largely untouched by migrants (Golani et al., 2007). The successful migrant fishes are dwellers of shallow soft and mixed bottoms, algal feeders or outright pelagic fishes and powerful swimmers. More than half the number of fish species recorded from a sandy bottom in the Gulf of Aqaba-Eilat are also successful migrants through the Suez Canal (Golani, 1993). This cannot be said of the fishes of the coral reefs proper. Even without turning yet into a coral sea, the warming Mediterranean presents all the characteristics of a nascent new Tethys. The return of several tropical families of Tethyan origin is a qualitative phenomenon which is observed not only in the fish fauna, as above, but also in other major marine taxa. It is a phenomenon of geological dimensions which will reach its completion only with the eventual arrival of reef building corals to the Mediterranean. ACKNOWLEDGMENTS My thanks are due to my colleague Dr. Daniel Golani from the Hebrew University of Jerusalem, the organizer of this book, for his stimulus. He also commented and checked the purely ichthyological content of this article. I acknowledge also the preliminary exchange of ideas with Dr. Argyro Zenetos, Athens. For the foraminiferal and historical geological aspects, I am indebted to Dr Ahuva Almogi-Labin, Jerusalem. Dr. H. J. Bromley-Schnur is acknowledged for her stylistic help. REFERENCES Adams, C.G., A.W. Gentry and P.J. Whybrow. 1983. Dating the terminal Tethyan event. Utrecht Miocropaleontological Bullletin 30: 273-289. Andaloro, F. and E. Azzurro. 2004. The Sicily Channel, a crossroads between Atlantic and IndoPacific worlds. 13th International Congress on Aquatic Invasive Species. (Cited online 25.4.2006) www.icais.org/pdf/21Tuesday/B/tues_b_l_am/Franco_Andaloro.pdf Bellwood, D.R. 1995. The Eocene fishes from Monte Bolca: the earliest coral reef fish assemblage. Coral Reefs 15(1): 11-19. Bellwood, D.R. 1998. What are reef fishes? Comment on the report by D. R. Robertson: Do coral-reef faunas have a distinctive taxonomic structure? Coral Reefs 17: 187-189 Ben Abdallah, A., J. Ben Souissi, H. Mejri, C. Capapé and D. Golani. 2007. First record of Cephalopholis taeniops (Valenciennes) in the Mediterranean Sea. Journal of Fish Biology 71(2): 610-614. Ben Rais Lasram, F., J.A. Tomasini, M.S. Romdhane, T. Do Chi and D. Mouillot. 2008a. Historical colonization of the Mediterranean Sea by Atlantic fishes: do biological traits matter? Hydrobiologia 607: 51-62.

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Ben Rais Lasram, F., J.A. Tomasini, F. Guilhaumon, M.S. Romdhane, T. Do Chi and D. Mouillot. 2008b. Ecological correlates of dispersal success of Lessepsian fishes. Marine Ecology Progress Series 363: 273-286. Ben Rais Lasram, F. and D. Mouillot. 2009. Increasing southern invasion enhances congruence between endemic and exotic Mediterranean fish fauna. Biological Invasions 11(3): 697-711. Ben Tuvia, A. 1953. Mediterranean fishes of Israel. Bulletin of the Sea Fisheries Station, Haifa 8: 1-40. Bianchi, C.N. 2007. Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580: 7-21. Bitar, G. and H. Zibrowius. 1997. Scleractinian corals from Lebanon, Eastern Mediterranean, including a non-lessepsian invading species (Cnidaria: Scleractinia). Scientia Marina 61(2): 227-231. Bosworth, W., P. Huchon and K. McClay. 2005. The Red Sea and the Gulf of Aden Basins. Journal of African Earth Sciences 43: 334-378. Briand, F. 2008. Executive Summary. In: Briand, F. (ed.), The Messinian Salinity Crisis from megadeposits to microbiology – A consensus report. No. 33 in CIESM Workshop Monographs. Monaco. pp. 7-28. Briggs, J.C. 2004. The ultimate expanding earth hypothesis. Journal of Biogeography 31: 855-857. Carey, W.S. 1987. Tethys and her forebears. In: McKenzie, K.G. (ed.), Shallow Tethys 2. International Symposium on Shallow Tethys (2nd 1986 Wagga Wagga, N.S.W.) Rotterdam: A.A. Balkema. pp. 3-29. Cavin, L., P.L. Forey and Ch. Lecoyer. 2007. Correlation between environment and Late Mesozoic ray-finned fish evolution. Palaeogeography, Palaeoclimatology, Palaeoecology 245(3-4): 363-367. Castriota, L. and F. Andaloro. 2005. First record of lessepsian fish Siganus luridus (Osteichthyes: Siganidae) in the Tyrrhenian Sea. Journal of Marine Biological Association 2 – Biodiversity Records. Published online. http: //www.mba.ac.uk/jmba/pdf/5122.pdf. Cited 21.11.2006. Chalifa, Y. 1989. New species of Enchodus (Pisces: Enchodontoidea) from the lower Cenomanian of Ein Yabrud, Israel . Journal of Paleontology 63(3): 356-364. Checconi, A., D. Bassi, L. Passeri and R. Rettori. 2007. Coralline red algal assemblage from the Middle Pliocene shallow-water temperate carbonates of the Monte Cetona (Northern Apennines, Italy). Facies 53(1): 57-66. Domingues, V.S., M. Alexandrou, V.C. Almada, D.R. Robertson, A. Brito, R.S. Santos and G. Bernardi. 2008. Tropical fishes in a temperate sea: evolution of the wrasse Thalassoma pavo and the parrotfish Sparisoma cretense in the Mediterranean and the adjacent Macaronesian and Cape Verde Archipelagos. Marine Biology 154 (3): 465-474. Dor, M. 1984. Checklist of the Fishes of the Red Sea: CLOFRES. Jerusalem: The Israel Academy of Sciences and Humanities. 437pp. Dulčić, J. and A. Pallaoro. 2002. First record of the migrant Leiognathus klunzingeri (Pisces: Leiognathidae) from the Adriatic Sea. Journal of the Marine Biological Association of the UK 82: 523-524. Dulčić, J. and A. Pallaoro. 2004. First record of the marbled spinefoot Siganus rivulatus (Pisces: Siganidae) in the Adriatic Sea. Journal of the Marine Biological Association of the UK 84: 1087-1088. Dullo, J., P. Tutman and M. Caleta. 2006. The northernmost occurrence of the white grouper Epinephelus aeneus (Perciformes: Serranidae) in the Mediterranean area. Acta Ichthyologica et Piscatoria 36(1): 73-75. Ekman, S. 1967. Zoogeography of the sea. London: Sidgwick and Jackson. 417 pp.

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Por, F.D. 2008. Life at salinity beyond 41 ppm: Metahaline environments and anchialine pools in the Gulf of Aqaba-Eilat. In: Por.F.D. (ed.) Aqaba-Eilat, the improbable gulf: environment, biodiversity and preservation. Jerusalem: Magnes Press. 135-152. Por, F.D. and Ch. Dimentman. 1989. The legacy of Tethys: an aquatic biogeography of the Levant. Dordrect: Kluwer Academic Publishers. 214 pp. Por, F.D. and Ch. Dimentman. 2006. Mare Nostrum: Neogene and anthropic natural history of the Mediterranean basin with emphasis on the Levant. Sofia-Moscow: Pensoft. 349 pp. Robertson, D.R. 1998. Do coral-reef fish faunas have a distinctive taxonomic structure? Coral Reefs 17: 179-186. Rilov, G. and B. Galil. 2009. Marine biodiversity in the Mediterranean Sea – history, distribution and ecology. In: Rilov, G. and J.A. Crooks (eds.), Biological invasions in marine ecosystems. Ecological Studies 204. Berlin Heidelberg. Springer Verlag. pp. 549-575 Sará, G., G. Romano, and A. Mazzola. 2006. A new Lessepsian species in the Western Mediterranean (Brachidontes pharaonis, Bivalvia: Mytilidae): density, resource allocation and biomass. JMBA2- Biodiversity Records. 7 pp. Published online. http: //www.mba.ac.uk/ jmba/pdf/5087.pdf Sorbini, Ch. and J.C. Tyler. 2001. Review of the fossil filefish of the family Monacanthidae (Tetraodontiformes) from the Pliocene of Italy. VI European Workshop on Vertebrate Paleontology, Florence and Montevarchi, September 19-21 2001. Abstract volume p.56. Sorbini, L. 1988.Biogeography and climatology of Pliocene and Messinian fossil fish from Eastern Central Italy. Bolletino del Museo de Storia Naturale Venezia 14: 1-85. Steinitz, W. 1927. Beiträge zur Kenntnis der Küstenfauna Palästinas.I. Publicazzioni della Stazzione Zoologica di Napoli 13(1): 145-154. Steinitz, W. 1929. Die Wanderung indopazifischer Arten ins Mittelmeer seit Beginn der Quartärperiode. Internationale Revue der Hydrobiologie und Hydrographie 22(1-2): 1-90. Stewart Grant, W. 2005. A second look at mitochondrial DNA variability in European anchovy (Engraulis encrasicolus): assessing models of population structure and the Black Sea isolation hypothesis. Genetica 125: 293-309. Thunell, R.C. 1979. Climatic evolution of the Mediterranean Sea during the last 5.0 million years. Sedimentary Geology 23: 67-79 Tillier, J.B. 1902. Le Canal de Suez et sa faune ichthyologique. Mémoires de la Societée Zoologique de France 30: 129-131. Vernal, A.de and C. Hillaire-Marcel. 2008. Natural variability of Greenland climate, vegetation and ice volume during the past million years. Science 320: 1622-1625. Yilmaz, R., M. Bilecenoglu and B. Hossucu. 2004. First record of the Antenna Codlet Bregmaceros atlanticus Goode & Bean (Osteichthyes: Bregmacerotidae) from the Eastern Mediterranean Sea. Zoology of the Middle East 31: 111-112. Zenetos, A., S. Gofas, G. Russo and J. Templado. 2004. CIESM atlas of exotic species in the Mediterranean. Vol 3. Molluscs Briand, F. (ed.). Monaco: CIESM Publisher. 376 pp. www. ciesm.org/atlas/fishes.html

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Global warming and exotic fishes in&the Sea: introduction D. Golani B. Mediterranean Appelbaum-Golani (Eds.) 2010 dynamic, range expansion ... 35 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 35-56. © Pensoft Publishers Sofia–Moscow

Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion and spatial congruence with endemic species Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

INTRODUCTION The contemporary acceleration of biodiversity loss is now widely recognized by ecologists in both terrestrial (Thomas et al., 2004) and marine ecosystems (Roberts and Hawkins, 1999). There are a few major sources of ecological alterations that can be extracted from the long list of factors explaining this trend. For aquatic ecosystems, the most important factors are certainly climatic change and biotic exchanges (e.g. Olden et al., 2006). Indeed, biological invasions often cause ecological and economic damages to ecosystems (Crooks, 2002; Olden et al., 2004). For instance, when exotic species enter local communities and occupy part of native species niches, they can drive these latter to extinction by competitive interactions, by predation or simply by demographic stochasticity. They can, at the very least, reduce the abundance of native species, alter disturbance regimes and basic ecosystem processes, impose large economic costs, and introduce new pathogens to indigenous populations. At worst, these interactions may produce, in combination, a spiral towards extinction of native populations (Olden et al., 2006). Nowadays biological invasions are largely promoted by human domination on Earth through a direct way (human-driven introduction of species out of their native range) and an indirect way (range shift following climate change). Indeed, it appears that many species have recently shifted their area of distribution by extending polar-ward as a response to climate warming rather than adapting to warmer temperatures (e.g. Perry et al., 2005). Thus, we may expect that some “winner” species, which expand their geographical ranges, invade communities of “loser” species which do not spread while being under biotic pressure of exotic species (McKinney and Lockwood, 1999). This is

36 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

even more critical for hotspots of endemism because endemic species are restricted to an enclosed area and cannot escape and establish elsewhere when environmental (climate change) and biotic constraints (exotic species) increase in intensity. The Mediterranean Sea provides exceptional material for a case study, as it appears to be a hotspot for endemism (8.8% of the fish species are endemic (Quignard and Tomasini, 2000) while being a semi-closed receptacle for exotic species from the Red Sea and the Atlantic Ocean (see a review in Streftaris et al., 2005). Similar to many systems around the world, the Mediterranean Sea is currently becoming warmer and there are evidences of an increased presence of thermophilic marine species (Ben Yami, 1955; Chervinsky, 1959; Bianchi and Morri, 2000; Sabatés et al., 2006). Consequently, fundamental questions arise: is the Mediterranean Sea under increasing southern invasions? What are the spread rates of exotic species? Are hotspots of endemism experiencing an increasing spatial overlap with exotic species? The aim of our review was to quantify (i) the trend of sea surface warming since the beginning of the XXth century (ii) the trend of exotic introduction rate from the Red Sea and the Atlantic Ocean, (iii) the spread rate of some exotic species and (iv) the increasing spatial overlap between exotic and endemic Mediterranean fish fauna. A] GLOBAL WARMING IN THE MEDITERRANEAN SEA The analysis of regional averaging of terrestrial surfaces temperatures over the Mediterranean basin reveals an evolution concurrent with global trends (a decrease in temperatures during the period 1955-1975 followed by a strong increase since the 1980s, NOA 2001 available at http://www.climate.noa.gr). Similarly, despite a high inter-annual and regional variability characterizing Mediterranean waters, Diaz-Almela et al. (2007) detected a warming trend for the whole basin of 0.04°C.yr-1 using the maximum Sea Surface Temperatures (SSTmax) series (1982–2005) extracted from NCEP Reynolds Optimally Interpolated Sea Surface Temperature data sets (Reynolds et al., 2002). Behind this general warming, distinctive trends are identified for the western and eastern parts of the Mediterranean (NOA, 2001) as well as for the northern and southern parts. This said, local differences in the impact of global warming would shape differential spreads of introduced species and contrasting impacts on recipient communities. In order to visualize spatially the warming trend, we generated maps of the Mediterranean SST from 1982 to 2006 on a 0.1-degree grid representing the whole Mediterranean basin. Data were interpolated via ordinary kriging (Diggle and Ribeiro, 2007) on the basis of 1-degree gridded SST data from the NOAA Satellite and Information Service (National Climatic Data Center National Operational Model Archive and Distribution System Meteorological Data Server of the National Oceanic and Atmospheric Administration). For each cell of the 0.1-degree grid we used monthly SST data to calculate mean annual SST. To evaluate the evolution of SST over the studied period we calculated for

Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 37

each cell the trend (the slope of a linear regression of SSTs versus time) and the acceleration (the slope of a linear regression of differences in SST between two consecutive years versus time) of SSTs over the 1982-2006 period. The comparison of Figures 1 and 2, illustrating respectively mean SST values for the early 1980s and 2000s, reveals the general warming described by Diaz-Almela et al. (2007) and confirms the west-east and the north-south increasing SST gradients. On average, over a period of 20 years, the Mediterranean waters warmed by 0.68°C. The areas that warmed by more than 1°C are the Ligurian Sea, the Gulf of Gabes (southern Tunisia) and the coastal waters of southern Turkey. Despite these anomalies, the observed gradients remain stable over time. The Levantine Basin warmed by 0.74°C and the Alboran Sea by 0.63°C. These values seem weak but they are sufficient to cause ecological responses of some organisms (Tonn, 1990) and to enhance the spread of some exotic species. The Mediterranean Sea has not warmed homogenously: some areas warm faster than others while others become cooler. For example, the southern Aegean Sea is the area that warms the most quickly: the warming increase is about 0.05 to 0.06°C per year. The northern Levantine Basin, the southern Ionian Sea, as well as the Gulf of Gabes 0

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Fig. 1. Sea surface temperature of the Mediterranean during the early 1980’s (a) and the mid2000 (b)

38 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

and the Ligurian Sea appear also to be areas that warm drastically (about 0.04 to 0.05°C per year) (Fig. 2). An opposite trend appears in the northern Adriatic which displays a decrease in SST ranging from -0.02 to -0.01°C per year. Except for the northern Adriatic, the whole Mediterranean has become warmer, but in these last years, the warming increase, in terms of acceleration rate (°C.year-2), has been more important in some areas than in others. For example, the Gulf of Lion, the Catalan Sea and the transition area between the Tyrrhenian and the South Ionian Sea off Tunisia are the regions that are warming at an increasing rate (see: acceleration in Fig. 3). In contrast, in the Aegean Sea, the warming rate is decreasing (see: braking in Fig. 3), being more important in the past than nowadays (Fig. 3).

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Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 39

B] INTRODUCTION RATES OF EXOTIC SPECIES IN THE MEDITERRANEAN SEA Due to this warming, is the Mediterranean subject to increasing southern invasions? To try to answer this question we investigated the correlation between the introduction rate of exotic species and the sea surface temperature. B.1] Lessepsian introductions Since the opening of the Suez Canal, 70 Lessepsian species were recorded to date (Golani, this volume). The first record of a Lessepsian fish, Atherinomorus lacunosus, in the Mediterranean dates from 1902 by Tillier (1902) and the most recent one is Apogon smithi by Golani et al. (2008). As this study was conducted in 2006, we only took into account Lessepsian migrants that reached the Mediterranean Sea up to 2006, i.e. 63 species. Lessepsian species considered in this work belong to 45 families and 57 genera. The most represented family within the Lessepsian fish group is the Tetraodontidae family with 5 species, followed by the Clupeidae with 4 species and the Gobiidae and the Platycephalidae with 3 species each. Red Sea species migrating through the Suez Canal are inevitably from more southern latitudes than the Mediterranean. By reconstructing the Lessepsian invasion history through literature we observe a continuous increase in the number of new introduced species between the beginning of the 20th century and the 1950s (Fig. 4). Another period 2.5

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Fig. 4. Changes per decade in the Mediterranean Sea water temperature (A) and in the number of newly introduced Lessepsian fishes (B) (r = 0.77, p<0.05).

40 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

of increasing invasion by Lessepsian species has been observed, which started in the 1990s. Invasion rate has increased from 0.7 species per year on average in the 1990s to 2 species per year since 2000. Overall, the number of introduced Lessepsian fish species is correlated significantly and positively (Fig. 4) with the Mediterranean water temperature (r = 0.77, p<0.05). B.2] Atlantic introductions The Gibraltar Strait has contributed, since its opening 5.33 million years ago, to Mediterranean biodiversity by the introduction of Atlantic fauna and flora (Bianchi and Morri, 2000). Since there are no reliable records before the 19th century and since species introduced before that date are considered as full-fledged Mediterranean species with Atlantic origin, we restricted our study to the “neo-Atlantic colonizers”, i.e. introduced since 1800. Since 1810, 62 Atlantic species (45 families, 55 genera) invading the Mediterranean Sea were recorded up to 2006. The first records of Atlantic fishes in the Mediterranean Sea, Entelurus aequoraeus and Pristis pectinata, came out in 1810 (by Risso, 1810). The most recent one is Cyclopterus lumpus (by Dulčić and Golani, 2006). The most represented families within the Atlantic fish group colonizing the Mediterranean Sea are the Carcharinidae (5 species), the Soleidae (5 species), the Tetraodontidae (3 species) and the Syngnathidae (3 species). Conversely to the Lessepsian species, Atlantic species do not come necessarily from lower latitudes. Hence, if we assess their introduction rate by the number of species that migrated to the Mediterranean Sea, we cannot detect whether southern migrations are accelerating or not during a period of global warming. We overcome this limitation by estimating the maximum latitude of introduced Atlantic species in their original habitat. During a period of global warming we may expect decreasing latitude of Atlantic species entering the Mediterranean if the climate has an impact on fish geographic ranges and invasion process. Once we plotted the latitude of Atlantic species entering the Mediterranean against the temperature, we observed that Atlantic fish invading the western Mediterranean basin have lower maximum latitudes over time, and were thus more thermophilic. The maximum latitudes of the Atlantic species that occur in the Mediterranean Sea are correlated significantly and negatively with the Mediterranean surface water temperature (r = -0.60, p<0.05) (Fig. 5). Since the 1980s, no species whose maximum latitude exceeds 42.35° has entered via the Gibraltar strait and has become established successfully (Fig. 5). Taken together, our results, although descriptive, suggest that southern invasions from the Red Sea and from the Atlantic accelerate with global warming. This indicates that the Mediterranean Sea is under an increasing trend of southern fish invasions which has accelerated recently.

Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 41 19.6

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Fig. 5. Changes per decade in the Mediterranean Sea water temperature (A) and in the average maximum latitude for the Atlantic species introduced in the Mediterranean Sea (B) (r = -0.60, p<0.05)

C] SPREAD RATE OF SOME EXOTIC SPECIES A very dense literature reporting locations and dates of exotic new records is available. The most complete reference is certainly the CIESM Atlas of Golani et al. (2002) and also the list of Quignard and Tomasini (2000). Using these compilations, we mapped Lessepsian and Atlantic exotic fish richness before and after evidence of global warming, thanks to Geographical Information Systems. First, we digitized the geographical distributions of Lessepsian species during the eighties, i.e. before evidence of global warming and we have updated these maps until 2006, i.e. after evidence of global warming. Second, this set of maps was overlaid on a regular grid to obtain the number of species per cell. A cell grid of 0.1° latitude x 0.1° longitude seems adequate in order to avoid the overestimation of species richness. The same procedure was applied to exotic species coming from the Atlantic and, finally, we obtained maps showing the dynamic of invasion density (Fig. 6). During the 1980’s there were 43 Lessepsian species in the Mediterranean. The highest richness was for the Israeli coasts with 37 species per cell of 0.1° by 0.1°. During that period, only four species reached the western basin: Pomadasys stridens identified by Torchio in the Gulf of Genoa (Italy) in 1969, Stephanolepis diaspros identified by Chakroun in 1966, Siganus luridus identified by Ktari Chakroun in 1971 and Siganus rivulatus identified by Ktari and Ktari in 1974 in Tunisia. Adriatic Sea, northern Tunisia, Sicily and a large part of Libyan coasts were not yet colonized (Fig. 6). By 2006, 63 Lessepsian species were identified in the Mediterranean. The Israeli coasts are the most invaded with 59 species by cell at the maximum. Some Lessepsian species reached the northern

42 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

Adriatic Sea (Epinephelus coioides by Parenti and Bressi in 2001), the northern Tunisia and Sardinia (Fistularia commersonii by Pais et al. in 2007). During the eighties, there were 21 Atlantic species in the Mediterranean. Only three species reached marginally the eastern basin: Pristis pectinata (by Ben-Tuvia, 1953; Quignard and Tomasini, 2000), Arius parki (by Golani and Ben Tunia, 1986) and Enchelycore anatina (by Ben Tuvia and Golani, 1984) in Israel. In 2006, 62 Atlantic species are present in the Mediterranean and many other species reached the Levantine Basin (Fig. 6): Acanthurus monroviae, Carcharhinus altimus and Sphoeroides pachygaster were identified in Israel in 1996 by Golani and Sonin for the former and by Golani for the latter. If we consider the increasing geographic range size of each species separately, we can classify Lessepsian and Atlantic exotic species into three categories according to their ability to disperse over the Mediterranean Sea (Fig. 7): - Absence of dispersal, for the species that were recorded once and that have never been recorded since that first record: this category includes 12 Lessepsian species and 34 Atlantic species; - Weak dispersal, for species that were not able to spread past the biogeographical boundaries of the Levantine basin (i.e. the Island of Rhodes (northern side) and the Egypto-Libyan boundary (southern side) for the Lessepsian species and past the biogeographical boundaries of the Alboran Sea (i.e. the Nao Cape 0

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Fig. 6. Lessepsian and Atlantic invasion dynamics in the Mediterranean Sea in terms of species richness per cell of 0.1° by 0.1° between the eighties and 2006

Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 43

-

(northern side) and the Arzew Gulf (southern side)) for Atlantic species: this category includes 32 Lessepsian species and 9 Atlantic species; Strong dispersal, i.e. for species observed beyond the two above boundaries: this category includes 19 Lessepsian species and 19 Atlantic species.

Since very recent introduced species (after 2002) are unlikely to have already spread over the Mediterranean coasts, the classification above is not suitable for them. Overall, 30% of the Lessepsian species and 33% of the Atlantic ones succeeded in dispersing over the Mediterranean Sea. The frequencies of dispersal rate on the northern and the southern sides of the Mediterranean are not similar, neither for the Lessepsians nor for the Atlantics. Thus, we cannot compare the dispersal on both sides statistically since fishing effort and scientific investigation are not comparable between the two sides. As we can find the year and the location of exotic species records in the literature, we were able to estimate the dispersal speed of these species: using GIS software, we digitized the distribution area of each exotic fish and calculated the distance separating two successive records. Since it is not likely that dispersal is achieved by swimming along 0

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Fig. 7. Dispersal of some Lessepsian and Atlantic exotic species defining three classes

44 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

the entire coast, we did not include the coastline in bays and along islands (in the Aegean Sea and the Gulf of Taranto for example) in the distance covered by each species. After measuring the distance covered by each fish species during a period of time, we estimated their speeds. If we want to assess the temporal trend of these speeds, we have to limit the data set to the species recorded at least three times in order to provide a robust trend. This is possible only with Lessepsian species because they are better monitored than Atlantic species. Even if we only provide an approximation, our results generate some general trends. The study of Lessepsian species dispersal shows that the speed of dispersal increases over time for species restricted to the Levantine basin, (e.g. Apogon pharaonis (Fig. 8a),

Distance (km)

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Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 45

24.2 km.y-1

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Callionymus filamentus (Fig. 8i), Hemiramphus far (Fig. 8c), Herklotsichthys punctatus (Fig. 8d), Lagocephalus suezensis (Fig. 8e) and Petroscirtes ancylodon (Fig. 8f )). Conversely, for species that spread beyond the Levant limits towards the northern side of the Mediterranean Sea, the speed of dispersal decreased at transitional zones between basins (e.g. Leiognathus klunzingeri (Fig. 8k), Parexocoetus mento (Fig. 8l), Siganus luridus (Fig. 8n) and Siganus rivulatus (Fig. 8o)) when they reached the Adriatic and Tyrrhenian seas. For instance, the dispersal rate of Leiognathus klunzingeri (Fig. 8k) was 207.8 km.year-1 until the island of Rhodes and dropped to 31.6 km.year-1 between the island of Rhodes and the Greek eastern coast corresponding to the crossing of the Aegean Sea. Once

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46 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

this “barrier” is crossed, the speed increases up to 153.4 km.year-1 towards the Adriatic Sea. During the spread of Parexocoetus mento from the island of Rhodes to Albania, the dispersal speed dropped from 600.4 km.year-1 to 72.9 km.year-1. The same deceleration was observed for Siganus luridus during its transition from the Aegean Sea to the Adriatic Sea where the dispersal rate decreased by more than seven times (Fig. 8). It appears that the transition between different water bodies acts like a geographical barrier. We also observe that the transition between these water bodies corresponds to a shift in water temperature (Fig. 1) which may partly explain the difficulty to reach a cooler basin for some species coming from the South. Leiognathus klunzingeri (Fig. 8k), Parexocoetus mento (Fig. 8l), Saurida undosquamis (Fig. 8m and Fig. 9a), Siganus luridus (Fig. 8n), Siganus rivulatus (Fig. 8o) and Stephanolepis diaspros (Fig. 8p and Fig. 9b) have a logistic curve shape typical for invasive species (Hengeveld, 1989; Silva et al., 2002). The slow down near the inflexion in the curve happens around the island of Rhodes that appears critical for Lessepsian species. The island of Rhodes is at the transition between the warm Levant basin and the cooler western part of the Mediterranean Sea (Figures 1 and 2). Thus, we conclude that the island of Rhodes represents a thermal barrier, forcing the species to decelerate their dispersal rate. But since the Mediterranean waters are 0

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Fig. 9. Examples of species dispersal showing a logistic curve shape typical for invasive species: Saurida undosquamis (a) and Stephanolepis diaspros (b)

Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 47

becoming warmer (Somot et al., 2006), we expect this kind of threshold to be more easily crossable by invasive species. We conclude that crossing the Suez Canal or the Gibraltar strait does not guarantee the success of dispersal for fishes in the Mediterranean Sea. Indeed we observe a large variability in dispersal speed among exotic species which brings us to new questioning. Is species ecology a key determinant for dispersal? Are habitat characteristics important parameters to include in Mediterranean fish invasion? Ultimately, the goal of such research would be invasiveness prediction. For instance, recent studies show how some life history and ecological traits predispose certain fish species to establish, or to become invasive outside their native range (Ruesink, 2005). The identification of such biological traits would allow us to predict future colonizations and anticipate major changes in the Mediterranean fish fauna partly due to exotic pressure on endemics. D] INCREASING SPATIAL OVERLAP BETWEEN EXOTIC AND ENDEMIC MEDITERRANEAN FISH FAUNA Following the northward movement of exotic species into the Mediterranean, the overlap with endemic populations is expected to rise. Even if it remains impossible to predict the threat that this overlap will pose to endemic biota, we know that the intensity of interactions between exotic and endemic species is of major concern for the conservation of biodiversity worldwide (e.g. Olden et al., 2006). In addition to the rate of fish introduction, we suggest that attention should focus on the ratio of exotic species density to that of endemic species. Indeed, a higher density of exotic species has been shown to increase the impact of exotic species on endemic biota (Smith and Knapp, 2001). The introduction of fish from both the Atlantic Ocean and the Red Sea may increase the intensity of interactions between the exotic and endemic fish faunas. However, the rate of spread of exotic species towards higher latitudes in the Mediterranean Sea has been neglected. Here we propose to estimate the trend of spatial overlap between exotic and endemic species by comparing the maps of exotics and those of endemics before and after the global warming. To do so we had to merge the maps of Lessepsian and Atlantic species to obtain an exotic species richness map. We also generated an endemic species richness map but since endemic species did not alter their geographical ranges significantly over the last 20 years, we generated only one map for them (Fig. 10a). The key published works that we used were the FNAM atlas (Fishes of the North-eastern Atlantic and the Mediterranean) (Whitehead et al., 1986) and the list of endemic species compiled by Quignard and Tomasini (2000). According to these works, there are 79 endemic species in the Mediterranean. The spatial distribution of endemic species richness (n = 79) is heterogeneous. The greatest endemic species richness was found in the Adriatic Sea, the Gulf of Lion and

48 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

along the western coast of Italy. The richness of endemic species tends to be lower in the Levantine basin. The highest endemic richness was found to be 44 species, while the lowest value was one species, per cell (Fig. 10a). The spatial distribution of all exotic species shows a coastal pattern, especially in the eastern basin. During the 1980s, 64 exotic fish species were identified in the Mediterranean Sea. The highest exotic species richness was found along the eastern coast of the Levantine basin, which had a maximum of 38 species per cell 0.1° by 0.1°. Conversely, the coast of Italy, the Ionian Sea coast of Greece, and the major part of the Libyan coast were not colonized at all by exotic species (Fig. 10b). Since the 1980s, most of exotic species have moved northwards in the Mediterranean Sea by an average of 3.5° (approximately 300 km). In 2006, 125 exotic species were identified in the Mediterranean Sea, and the updated spatial distribution of richness of exotic fish shows that almost all Mediterranean coastal waters have been colonized, with the exception of the eastern and western coasts of the Italian peninsula. The highest richness of exotic species recorded in 2006 was 64 species per cell, an increase of more than 68 % over that observed during the 1980s. Some areas that were not colonized at all during the 1980s, such as the Ionian coast and the eastern Adriatic Sea, contained on average 3.5 exotic fish species per cell in 2006 (Fig. 10c). The early 2000’s experienced a particular dispersal: those of Fistularia commersonii. Indeed, this species was identified in the Mediterranean Sea for the first time in 2000 in Israel by Golani (2000). Two years later, it was recorded in Turkey by Gökoglu et al. (2002) and by Bilecenoglu et al. (2002) and around the Greek island of Rhodes by Corsini et al. (2002). In summer 2003, it was recorded in northern Aegean by Karachle et al. (2003). One year later, in 2004, it was recorded in Tunisia by Ben Souissi et al. (2004) and around the Italian island of Lampedusa by Azzurro et al. (2004). In 2005 it was recorded in Sardinia by Pais et al. (2007). This species is described as a “Lessepsian sprinter” by Karachle et al. (2003). The spatial overlap between exotics and endemics was assessed by evaluating the relative density of endemic species relatively to exotic species. This was carried out by calculating the ratio R = NEnd./ NEx. before and after the apparent global warming, where NEnd. and NEx. are respectively the number of endemic species and of exotic species per cell. It appears that between the 1980s and 2006, the number of cells in which exotic species were more numerous than endemic species, i.e. a ratio inferior to 1, increased by 56.5%. The number of exotic species in the Mediterranean is now 98.4% higher than it was 20 years ago: the number of invasive species has risen from 64 in the 1980s to 127 in 2006. This observation is supported by the finding of an increase of 56.5% in the number of cells in which exotic species were more numerous than endemic species between the 1980s and 2006, i.e. a ratio inferior to 1. In the 1980s there were 21 cells with a ratio equal to 1; in 2006 this number rose by a factor of eight, to 166.

Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 49

Overall, it appears that in twenty years the balance between exotic and endemic species richness has been reversed. Exotic species have extended their geographical range towards endemic hotspots, have colonized new areas, have become more numerous than endemic species in some areas and reached the coldest areas of the Mediterranean, for example the Adriatic Sea, which is a major hotspot of endemism (Fig. 10).

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50 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

Although we are unable to demonstrate a causal relationship between exotic invasion and the risk of extinction for endemic species, we expect that species replacement will be more likely to occur in the future. Indeed, many species have succeeded in colonizing the Mediterranean Sea, and then can exert competitive pressure on Mediterranean endemic species, which consequently are prone to decline in number. At least, we can say that global warming enhances the gradual replacement of endemic species by exotic populations, which contributes to the breakdown of the regional distinctiveness of the Mediterranean from the Atlantic and the Red Sea, a process termed “biotic homogenization” (Vitousek et al., 1997; McKinney and Lockwood, 1999) as illustrated in Fig. 11. CONCLUSIONS Since the 1980s the rate of introduction of Lessepsian species from the Red Sea to the Mediterranean has increased. In parallel, new fish introductions from the Atlantic Ocean involve species from more southerly latitudes. During the period 2000-2006, eleven new Lessepsian fish species were identified in the Mediterranean Sea, namely Fistularia commersonii (by Golani, 2000), Hippocampus fuscus (by Golani and Fine, 2002), Plotosus lineatus (by Golani, 2002), Heniochus intermedius (by Gökoglu et al., 2003), Scarus ghobban (by Goren and Aronov, 2001), Lagocephalus

T. Kurtz

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Fig. 11. The Mediterranean Sea under southern invasions contributing to the biotic homogenization worldwide

Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 51

sceleratus (by Filiz and Er, 2004), Tylerius spinosissimus (by Corsini et al., 2005), Nemipterus randalli (by Golani and Sonin, 2006), Iniistius pavo (Corsini et al., 2006), Apogon queketti (Eryilmaz and Dalyan, 2006) and Decapterus russelli (Golani, 2006). Six new Atlantic fish species have also been identified in the Mediterranean, namely Seriola carpenteri (by Pizzicori et al., 2000), Seriola rivoliana (by Castriota et al., 2002), Pinguipes brasilianus (by Orsi Relini, 2002), Cheilopogon furcatus (by Ben Souissi et al., 2004), Sphoeroides spengleri (by Reina Hervas et al., 2004) and Cyclopterus lumpus (Dulčić and Golani, 2006). The rate of introduction of Lessepsian fish during 2000–2006 was three times higher than during the preceding decade, and represents the highest value since the opening of the Suez Canal. The average maximum latitude of residence of the five new species from the Atlantic Ocean is 24.23°; this value is the lowest observed since the beginning of the 19th century. These values are associated with the highest temperatures recorded since 1810: in 2006, the temperature was 0.36°C higher than during the 1990s. Moreover, the role of global warming in this phenomenon is supported by evidence that some fish, especially Lessepsian species, have succeeded in invading the western basin of the Mediterranean Sea. Such fish include Fistutlaria commersonii (by Azzuro et al., 2004; Ben Souissi et al., 2004), Stephanolepis diaspros (by Chakroun, 1966; Catalano and Zava, 1993), Siganus rivulatus (by Ktari and Ktari, 1974; Dulčić and Pallaoro, 2004), Siganus luridus (by Ktari Chakroun and Boualal, 1971; Azzurro and Andaloro, 2004) and Parexocoetus mento (by Ben Souissi et al., 2004). The success of these species may be linked to warmer climatic conditions, which enable these thermophilic exotic fishes to colonize areas of higher latitude. Consequently, comparison of the two maps that correspond to exotic species richness distribution, one representing the situation before and the other after global warming, reveals a clear modification in the pattern of distribution of exotic fish species (Fig. 10). In conclusion, our results highlight the fact that endemic fish species are facing the invasion of an increasing number of exotic species which may lead to a reduction in the abundance of endemic populations. Endemic species are more vulnerable than other species because they are restricted to the Mediterranean Sea and cannot escape or establish elsewhere. Although we are unable to demonstrate a causal relationship between exotic invasion and the risk of extinction for endemic species, we expect that species replacement will be more likely to occur in the future. As many exotic species have succeeded in colonizing the Mediterranean Sea, they then likely to exert competition on Mediterranean endemic species, which consequently are prone to decline in number. In a different context, Olden et al. (2006) demonstrated that fish invasions led to the extirpation of native species occupying the same niche in the Colorado River Basin. Generally, a more diverse assemblage of exotic species is more likely to affect native species, due to a combination of specific negative effects and higher demographic pressure (Smith and Knapp, 2001). Due to the increasing rate of invasion of Lessepsian fish species we expect major changes in the fish populations of the Mediterranean Sea to occur in the future, such as a gradual replacement of endemic species by exotic fish.

52 Frida Ben Rais Lasram, François Guilhaumon and David Mouillot

Gradual replacement of endemic species by exotic populations in semi-closed regional biota, which are usually important hotspots of biodiversity and endemism, contributes to the breakdown of the regional distinctiveness of the Earth’s biota, a process termed “biotic homogenization” (Vitousek et al., 1997; McKinney and Lockwood, 1999). There is a threat that the “Mediterranean character” of the ichthyofauna will progressively disappear. However, the dynamics of the process and its ecological consequences are challenging to predict. It is unlikely that the true geographical distribution of exotic species is at equilibrium. Instead, according to the “colonization lag” hypothesis (Menendez et al., 2006), we expect that the climatic warming already observed in the Mediterranean Sea is sufficient to promote changes in species assemblages for decades, because invasion lags behind climate change. It can reasonably be hypothesized that global warming may lead to an increase in the progression of tropical Atlantic species along the African coast towards the latitude of the Strait of Gibraltar. Such species are potential invaders of the Mediterranean Sea even without accidental introduction. In addition, because Lessepsian fishes represent only 5.7% of the Red Sea fish fauna, we predict that the risk of future invasion by fish from the Red Sea is potentially very high, and the magnitude of the phenomenon may accelerate with sea surface warming. The prediction of such phenomena and the identification of fish species from the Red Sea that are more likely to invade the Mediterranean are critical areas for further research. Understanding the global geographical distribution of extinction risk is a key challenge in conservation biology. Our results underline the importance of a global perspective on the mechanisms that drive spatial patterns of extinction risk, and the key role of climate warming in the current extinction crisis. The observational design of our study does not enable us to determine whether the increasing presence of exotic fish species has increased the likelihood that endemic fish species will become extinct. However, our study has clearly demonstrated that the Mediterranean Sea, a hotspot of endemism, is under increasing southern exotic species invasions that have benefited from global warming by expanding their range northwards. Since invasion ecology aims to understand a system we need to provide predictions and scenarios about the future of fish assemblages in the Mediterranean Sea under increasing southern pressure. Two new approaches deserve our attention to go one step further in understanding invasion processes and their consequences. First, we would need to predict the ability to invade using species life-history traits. It appears that fish species introduced in the Mediterranean have not the same invasion potential with some spreading far from their introduction area while some others do not spread. A useful issue would be the finding of common traits to “winner” species in order to anticipate the new invasions. Second we suggest using niche models based on climatic envelope to predict the dynamic of species geographic ranges under global warming (Thuiller, 2003; Thuiller, 2005). In turn such a modeling approach would allow the prediction of extinction risks and the range expansion of introduced species.

Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion ... 53

ACKNOWLEDGMENTS The authors wish to express their gratitude to the Cooperation and Cultural Action Services of the French Embassy in Tunisia, which funded this research by a PhD grant for the first author. This project was also supported by the Total Foundation. REFERENCES Azzurro, E. and F. Andaloro. 2004. A new settled population of the Lessepsian migrant Siganus luridus (Pisces : Siganidae) in Linosa Island – Sicily Strait. Journal of the Marine Biological Association of the United Kingdom 84: 819-821. Azzurro, E., P. Pizzicori and F. Andaloro. 2004. First record of Fistularia commersonii (Fistularidae) from the central Mediterranean. Cybium 28: 72-74. Ben-Tuvia, A. 1953. Mediterranean fishes of Israel. Bulletin of the Sea Fisheries Research Station, Haifa 8: 1-40. Ben Souissi, J., D. Golani, H. Mejri and C. Capape. 2005. On the occurrence of Cheilopogon furcatus in the Mediterranean Sea. Journal of Fish Biology 67: 1144-1149. Ben Souissi, J., J. Zaouali, M.N. Bradai and J.P. Quignard. 2004. Lessepsian migrant fishes off the coast of Tunisia. First record of Fistularia commersonii (Osteichthyes, Fistularidae) and Parexocoetus mento (Osteichthyes, Exocoetidae). Vie Et Milieu-Life and Environment 54: 247-248. Bianchi, C.N. and C. Morri. 2000. Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Marine Pollution Bulletin 40: 367-376. Bilecenoglu, M., E. Taskavak and K.B. Kunt. 2002. Range extension of three Lessepsian migrant fish (Fistularia commersoni, Sphyraena falvicauda, Lagocephalus suezensis) in the Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 82: 525-526. Castriota, L., S. Greco, G. Marino and F. Andaloro. 2002. First record of Seriola rivoliana Cuvier, 1833 in the Mediterranean. Journal of Fish Biology 60: 486-488. Catalano, E. and B. Zava.1993. Sulla presenza di Stephanolepis diaspros fr. Brunn. Nelle acque italiane (Osteichthyes, Monacanthidae). Supplemento alle Ricerche di Biologia della Selvaggina 21: 379-382. Chakroun, F. 1966. Captures d’animaux rares en Tunisie. Bulletin de l’Institut National Scientifique et Technique d’Océanographie et de Pêche de Salammbô 1: 75-79. Corsini, M., G. Kondilatos and P.S. Economidis. 2002. Lessepsian migrant Fistularia commersonii from the Rhodes marine area. Journal of Fish Biology 61: 1061-1062. Corsini, M., P. Margies, G. Kondilatos and P.S. Economidis. 2005. Lessepsian migration of fishes to the Aegean Sea: first record of Tylerius spinosissimus (Tetraodontidae) from the Mediterranean, and six more fish records from Rhodes. Cybium 29: 347-354. Corsini, M., P. Margies, G. Kondilatos and P.S. Economidis. 2006. Three new exotic fish records from the SE Aegean Greek waters. Scientia Marina 70: 319-323. Crooks, J.A. 2002. Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97: 153-166.

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Diaz Almela, E., N. Marba and C. Duarte. 2007. Consequences of Mediterranean warming events in seagrass (Posidonia oceanica) flowering records. Global Change Biology 13: 224-235. Diggle, P., J. and P.J. Ribeiro. 2007. Model-based geostatistics. New York: Springer, 230 pp. Dulčić, J. and D. Golani. 2006. First record of Cyclopterus lumpus L., 1758 (Osteichthyes: Cyclopteridae) in the Mediterranean Sea. Journal of Fish Biology 69: 300-303. Dulčić, J. and A. Pallaoro. 2004. First record of the marbled spinefoot Siganus rivulatus (Pisces : Siganidae) in the Adriatic Sea. Journal of the Marine Biological Association of the United Kingdom 84: 1087-1088. Eryilmaz, L. and C. Dalyan. 2006. First record of Apogon queketti Gilchrist (Osteichthyes: Apogonidae) in the Mediterranean Sea. Journal of Fish Biology 69: 1251-1254. Filiz, H. and M. Er. 2004. Akdeniz’in Yeni Misafiri (New guests in the Mediterranean). Deniz Magazin (Istanbul) 68: 52-54. Gökoglu, M., T. Bodur and H. Gulyavuz. 2002. The first record of the bluespotted cornetfish (Fistularia commersonii Ruppell, 1835) (fam: Fistulariidae) along the Turkish Mediterranean coast. Israel Journal of Zoology 48: 252-254. Gokoglu, M., T. Bodur and Y. Kaya. 2003. First record of the Red Sea bannerfish (Heniochus intermedius Steindachner, 1893) from the Mediterranean Sea. Israel Journal of Zoology 49: 324-325. Golani, D. 2000. First record of the bluespotted cornetfish from the Mediterranean Sea. Journal of Fish Biology 56: 1545-1547. Golani, D. 2002.The Indo-Pacific striped eel catfish, Plotosus lineatus (Thunberg, 1787), (Osteichthyes: Siluriformes) a new record from the Mediterranean. Scientia Marina 66: 321-323. Golani, D. 2004. First record of the muzzled blenny (Osteichthyes: Blenniidae: Omobranchus punctatus) from the Mediterranean, with remarks on ship-mediated fish introduction. Journal of the Marine Biological Association of the United Kingdom 84: 851-852. Golani, D. 2006. The Indian scad (Decapterus russelli ), (Osteichthyes: Carangidae) a new IndoPacific fish invader of the eastern Mediterranean. Scientia Marina 70: 603-605. Golani, D., B. Appelbaum-Golani and O. Gon. 2008. Apogon smithi (Kotthaus, 1970) (Teleostei: Apogonidae), a Red Sea cardinalfish colonizing the Mediterranean Sea. Journal of Fish Biology 72: 1534-1538. Golani, D. and A. Ben Tuvia. 1986. New records of fishes from the Mediterranean coast of Israel including Red Sea immigrants. Cybium 10: 285-291. Golani, D. and M. Fine. 2002. On the occurrence of Hippocampus fuscus in the eastern Mediterranean. Journal of Fish Biology 60: 764-766. Golani, D., L. Orsi Relini, E. Massuti and J.P. Quignard. 2002. CIESM Atlas of exotic species in the Mediterranean: Vol. 1. Fishes. Briand, F. (ed.). Monaco: CIESM. 254 pp Golani, D. and O. Sonin. 2006. The Japanese threadfin bream Nemipterus japonicus, a new IndoPacific fish in the Mediterranean Sea. Journal of Fish Biology 68: 940-943. Goren, M. and A. Aronov. 2002. First record of the Indo-Pacific parrot fish Scarus ghobban in the Eastern Mediterranean. Cybium 26: 239-240. Karachle, P.K., C. Triantaphyllidis and K.I. Stergiou. 2004. Bluespotted cornetfish, Fistularia commersonii Rüppell, 1868: a Lessepsian sprinter. Acta Ichthyologica et Piscatoria 34: 103-108. Ktari Chakroun, F. and M. Boualal. 1971. Capture de Siganus luridus (Rüppell) dans le golfe de Tunis. Bulletin de l’Institut National Scientifique et Technique d’Océanographie et de Pêche de Salammbô 2: 49-52.

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Ktari, F. and M.H. Ktari. 1974. Présence dans le golfe de Gabès de Siganus luridus (Rüppell, 1829) et de Siganus rivulatus (Forsskal, 1775) (Poissons, Siganidae) parasités par Pseudohaliotrematodides polymorphus. Bulletin de l’Institut National Scientifique et Technique d’Océanographie et de Pêche de Salammbô 3: 95-98. McKinney, M.L. and J.L. Lockwood. 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology and Evolution 14: 450-453. Melendez, R. and D.F. Markle. 1997. Phylogeny and zoogeography of Laemonema and Guttigadus (Pisces : Gadiformes : Moridae). Bulletin of Marine Science 61: 593-670. Olden, J.D., N.L. Poff and K.R.L. Bestgen. 2006. Life-history strategies predict fish invasions and extirpations in the Colorado River basin. Ecological Monographs 76: 25-40. Olden, J.D., N.L. Poff, M.R. Douglas, M.E. Douglas and K.D. Fausch. 2004. Ecological and evolutionary consequences of biotic homogenization. Trends in Ecology and Evolution 19: 18-24. Orsi Relini, L. 2002. Occurrence of the South American fish Pinguipes brasilianus in the Mediterranean. Cybium 26: 147-149. Pais, A., P. Merella, M.C. Follesa and G. Garippa. 2007. Westward range expansion of the Lessepsian migrant Fistularia commersonii (Fistulariidae) in the Mediterranean Sea, with notes on its parasites. Journal of Fish Biology 70: 269-277. Parenti, P. and N. Bressi. 2001. First record of the orange-spotted grouper, Epinephelus coioides (Perciformes : Serranidae) in the northern Adriatic Sea. Cybium 25: 281-284. Perry, A.L., P.J. Low, J.R. Ellis and J.D. Reynolds. 2005. Climate change and distribution shifts in marine fishes. Science 308: 1912-1915. Pizzicori, P., L. Castriota, G. Marino and F. Andaloro. 2000. Seriola carpenteri: a new immigrant in the Mediterranean from the Atlantic Ocean. Journal of Fish Biology 57: 1335-1338. Quignard, J.P. and J.A. Tomasini. 2000. Mediterranean fish biodiversity. Biologia Marina Mediterranea 7: 1-66. Reina Hervas, J.A., J.E.G. Raso and M.E. Manjon-Cabeza. 2004. First record of Sphoeroides spengleri (Osteichthyes : Tetraodontidae) in the Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 84: 1089-1090. Reynolds, R.W., N.A. Rayner, T.M. Smith, D.C. Stokes and W. Wang. 2002. An improved in situ and satellite SST analysis for climate. Journal of Climate 15: 1609-1625. Roberts, C.M. and J.P. Hawkins. 1999. Extinction risk in the sea. Trends in Ecology and Evolution 14: 241-246. Ruesink, J.L. 2005. Global analysis of factors affecting the outcome of freshwater fish introductions. Conservation Biology 19: 1883-1893. Sabates, A., P. Martin, J. Lloret and V. Raya. 2006. Sea warming and fish distribution: the case of the small pelagic fish, Sardinella aurita, in the western Mediterranean. Global Change Biology 12: 2209-2219. Silva, T., L.M. Reino and R. Borralho. 2002. A model for range expansion of an introduced species: the common waxbill Estrilda astrildin Portugal. Diversity and Distributions 8: 319-326. Smith, M.D. and A.K. Knapp. 2001. Size of the local species pool determines invisibility of a C-4 dominated grassland. Oikos 92: 55-61. Somot, S., F. Sevault and M. Déqué. 2006. Transient climate change scenario simulation of the Mediterranean Sea for the twenty-first century using a high-resolution ocean circulation model. Climate Dynamics 27: 851-879.

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Streftaris, N., A. Zenetos and E. Papathanassiou. 2005. Globalisation in marine ecosystems: the story of non-indigenous marine species across European seas. Oceanography and Marine Biology – an Annual Review 43: 419-453. Thomas, C.D., A. Cameron, R.E. Green, M. Bakkenes, L.J. Beaumont, Y.C. Collingham, B.F.N. Erasmus, M.F. De Siqueira, A. Grainger, L. Hannah, Hughes, L., B. Huntley, A.S. Van Jaarsveld, G.F. Midgley, L. Miles, M.A. Ortega-Huerta, A.T. Peterson, O.L. Phillips and S.E. Williams. 2004. Extinction risk from climate change. Nature 427: 145-148. Thuiller, W. 2003. BIOMOD: Optimising predictions of species distributions and projecting potential future shifts under global change. Global Change Biology 9: 1353-1362. Thuiller, W., S. Lavorel and M.D. Araújo. 2005. Niche properties and geographical extent as predictors of species sensitivity to climate change. Global Ecology and Biogeography 14: 347-357. Tonn, W.M. 1990. Climate change and fish communities: a conceptual framework. American Fisheries Society 119: 337-352. Torchio, M. 1969. Minacce per l’ittiofauna Mediterranea: le forme esotiche. Atti della Società Italiana della Scienze Naturali 109: 91-96. Vitousek, P.M., H.A. Mooney, J. Lubchenco and J.M. Melillo. 1997. Human domination of Earth’s ecosystems. Science 277: 494-499. Whitehead, P.J.P., M.L. Bauchot, J.C. Hureau, J. Nielsen and E. Tortonese. 1986. Fishes of the north-eastern Atlantic and the Mediterranean. Paris: UNESCO. Electronic references National Observatory of Athens: http: //www.climate.noa.gr National Oceanic and Atmospheric Administration: http: //ingrid.ldeo.columbia.edu/

rate of (Eds.) Lessepsian D. Golani & B. Introduction Appelbaum-Golani 2010fishes into the Mediterranean 57 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 57-69. © Pensoft Publishers Sofia–Moscow

Introduction rate of Lessepsian fishes into the Mediterranean Jonathan Belmaker, Eran Brokovich, Victor China, Daniel Golani and Moshe Kiflawi

INTRODUCTION In 1902, Tillier described the first record in the Mediterranean of a fish species of an otherwise Indo-Pacific distribution (Tillier, 1902). Since then, a total of 67 such species have been recorded (Golani et al., 2007); all of which presumably entered the Mediterranean through the Suez Canal. The discovery record of these Lessepsian migrants along the Israeli coastline (Fig 1A) shows a steady increase over the past 80 years, with several pronounced jumps following major scientific expeditions; predominantly those led by Ben Tuvia and coworkers (Ben Tuvia, 1966, 1978, 1985; Golani and Ben-Tuvia, 1995). But what does the discovery record have to teach us of the underlying introduction process? As ecologists, we are constantly reminded of the need to control for sampling effort when trying to estimate species richness (see: Gotelli and Colwell, 2001). However, it is only recently that researchers began developing the analytical tools needed to control for sampling effort when attempting to estimate species introduction rates (Costello and Solow, 2003; Solow and Costello, 2004; Belmaker et al., 2009). In this chapter, we outline the importance of estimating introduction rates and the reasons why these estimates should not be based on the discovery record. We proceed by outlining two approaches for obtaining sampling-effort independent estimates of the introduction rate and conclude with an analysis of the introduction process of Lessepsian-migrant fish species. THE IMPORTANCE OF ESTIMATING INTRODUCTION RATES Non-native species introduction is one of the most serious threats to global biodiversity. At a global scale, species introductions are leading to biotic homogenization and the

58 Jonathan Belmaker, Eran Brokovich, Victor China, Daniel Golani and Moshe Kiflawi

loss of endemic species (Grosholz, 2002; Sax and Gaines, 2003). Increasing awareness is motivating the incorporation of preventative measures in the management of many terrestrial and marine ecosystems although the latter has lagged behind (Bax et al., 2001; Grosholz, 2002). Determining the magnitude and temporal trends of biological invasions is the first step in controlling alien species (Bax et al., 2001) since a realistic appreciation of the introduction process is vital for decision makers to define priorities and develop efficient strategies. The opening of the Suez Canal in 1869 provided Indo-Pacific species a direct route into the Eastern Mediterranean. The ensuing “Lessepsian migration” (Por, 1971) offers a unique opportunity to study the consequences of a large-scale biotic exchange over relatively short time scales. Non-indigenous fish species contribute substantially to the richness of the Eastern Mediterranean fish biota (Golani et al., 2002). More than half of these species have established large populations in the Eastern Mediterranean (Golani et al., 2006), becoming economically important in the fishing industry: in some locations, migrants constitute 50–90 % of the fish biomass (Goren and Galil, 2005). Nevertheless, no attempt has been made so far to give a reliable estimate of the rate of migration and how it may be changing over time. Over 1200 fish species are currently known to occur in the Red Sea. Of these, 502 are known to occur in the Gulf of Suez, which forms the launching pad for Lessepsian migrants (Golani, 1999). These numbers place an upper limit on the number of potential future Lessepsian introductions. However, not all species may have the necessary capabilities to become successful migrants (Golani, 1993) and the fraction of this pool that could potentially invade is unknown. As we show below, reliable estimates of past and current introduction rates, together with a reasonable upper limit, can be used to predict future Lessepsian influx into the Eastern Mediterranean. WHY NOT USE THE NUMBER OF NEW SPECIES RECORDED? The number of newly recorded species per unit time necessarily underestimates the true number of introduced species. Species are rarely recorded at the moment of introduction. An introduced species may remain undiscovered for some time because: (1) it is rare, with population sizes so small as to preclude detection, (2) sampling effort has not been sufficient and/or (3) it has gone extinct before being discovered. Hence, for example, while 67 Red Sea fish species have been recorded in the Eastern Mediterranean (Golani et al., 2007), the actual number of species that have crossed the Suez Canal is most likely to be higher. Superficially, it may seem that temporal trends in the discovery record may mirror the underlying introduction process. This notion is wrong. As shown by Costello and Solow (2003), when detection probability is less than one, the discovery rate may accelerate even with a constant introduction rate and a constant sampling effort. For example, assume that species are introduced at a rate of 8 per year, and are discovered

Introduction rate of Lessepsian fishes into the Mediterranean 59

with a probability of 0.5 per year, regardless of the time elapsed since introduction. After the first year, four new species may be expected to be added to the discovery record (8×0.5=4). However, following the second year, the discovery record is expected to grow by 6 new species ((8+4)×0.5); suggesting an accelerating introduction rate, when it is in fact constant (see Costello and Solow, 2003). Another complication arises when sampling effort varies through time. Detection probability can change, for example, due to better sampling methods or more scientists actively looking for introduced species. This again can lead to an accelerating pattern in the discovery record that does not necessarily reflect changes in the underlying introduction rates. An accelerating discovery record may also emerge, despite a constant introduction rate, when introduced species have local survival probabilities smaller than 1 (Wonham and Pachepsky, 2006). In fact, Wonham and Pachepsky (2006) show that an exponentially increasing introduction rate can be considered a null model for introduction records. These studies make it clear that the discovery record has to be analyzed with relation to a model of the underlying processes/dynamics, if the introduction rate is to be inferred correctly. Unfortunately, this issue is still often neglected by studies that continue to use discovery rates as a surrogate for introduction rates (Ricciardi, 2001; Boudouresque and Verlaque, 2002; Wonham and Carlton, 2005). MODELING SOLUTIONS Solow and Costello (2004) were the first to treat the joint effects of the discovery and introduction processes. They did so by constructing a statistical model (hereafter, the ‘S&C model’) with two main components. First, the probability that a species introduced in year s is discovered in year t, allowing for a monotonic temporal trend in sampling effort and the effect of population size (which was assumed to follow exponential growth). Second, the introduction rate itself, which was also allowed to vary monotonically across time (see Appendix 1 for more details). The full S&C model contains 5 parameters, the maximum likelihood estimates of which are obtained numerically. Simpler models can be constructed by setting some of the parameters to zero, and their relative performance can be evaluated by comparing log likelihoods. More recently, Belmaker et al. (2009) proposed a hierarchical Bayesian approach to tackle the problem. Their model (hereafter, the ‘HB model’) uses the discovery record of native species to control for sampling effort when analyzing the coincident discovery record of the introduced species (note that over ecological time scales, the cumulative number of native species increases solely due to the effect of sampling). In this manner, sampling effort is not constrained to be constant or follow a monotonic trend, as in the S&C model, but can vary freely over time. The HB model capitalizes on the Bayesian framework’s ability to accommodate complex models with multiple sources of uncertainty, and combine different sources of information in a single analysis (Clark, 2005).

60 Jonathan Belmaker, Eran Brokovich, Victor China, Daniel Golani and Moshe Kiflawi

For example, by incorporating the size of the species pool at the source, the model can provide an estimate of both the maximum number of potential migrant species and the time of the first successful introduction (see Appendix 2 for details). The main advantage of the S&C model is its simplicity. It does not require specification of prior distributions, nor does it require the discovery record of the native species, which is needed for the HB model. In cases where such data does not exist, or when a system has been so heavily studied that the native discovery record has essentially reached a plateau, the S&C model remains the sole option. However, given an informative, coincident discovery records for natives, the HB model offers three important advantages. First, as mentioned above, it relaxes assumptions regarding temporal trends in sampling effort. Second, it provides estimates of potentially important parameters that are not accommodated in the S&C model – specifically, the maximum number of potential migrant species and the time of the first successful introduction. The model can then be used to estimate the total number of introduced species, which is unattainable using the S&C model. Finally, the Bayesian model offers great flexibility in implementing modifications. Such modifications may include post-introduction extinctions and among-species variation in introduction and extinction rates (Wonham and Pachepsky, 2006). Most importantly, the basic HB model assumes that native and introduced species are equally detectable and that the level of being detected remains constant over time. Violating this assumption can have considerable impact on parameter estimates. However, the model is easily modified to account for differences in the level of being detected (when this can be tested independently), or to conduct sensitivity analyses when differences are suspected but can not be quantified directly (see: Belmaker et al., 2009). Of further note, neither model can accommodate situations with multiple sources of introduction at varying rates. INTRODUCTION RATE OF LESSEPSIAN–MIGRANT FISH SPECIES The data set We used the S&C and HB models to analyze the complete and updated (to 2006) list of fish species recorded along Israel’s Mediterranean coastline over the past 80 years (Golani, 2005). This coastline has been subject to intensive and continuous ichthyological surveys since 1927 (e.g. Por, 1971; Diamant et al., 1986; Golani, 1996; Golani, 2005). It is close enough to the Suez Canal’s entry into the Mediterranean to guarantee the detection of early colonization of Lessepsian migrants; but far enough to make it unlikely new records are accidental observations of unestablished species. The latter makes it unnecessary to incorporate species survival rates into the model (see: Wonham and Pachepsky, 2006). To reduce variation caused by single years with no new records of either Lessepsian and/or native species (most likely due to low sampling effort), we pooled the data into two year intervals (Fig 1(A)).

400

A

140

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Cumulative number of species

Introduction rate of Lessepsian fishes into the Mediterranean 61

Med species Lessepsians species

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Fig. 1. (A) The cumulative number of indigenous Mediterranean and Lessepsian fish species observed in Israeli waters. Observations correspond to two-year intervals. (B) The cumulative number of Lessepsian species predicted by the HB temporally-invariant immigration probability model. The median and 95% credible intervals are shown. Reproduced with permission of the copyright owner from Belmaker et al (2009).

Results The S&C model with the highest log likelihood estimate was a reduced model with constant introduction rate and constant annual observation probability (β1 = γ1 = γ2 = 0; Table 1). The corresponding maximum likelihood estimates of the introduction rate was 0.71 species × year -1, with an annual observation probability approaching 1. The HB model that was best supported by the data invoked a temporally invariant probability of successful introduction (u, Table 2). The corresponding best estimate of the pool-size of potential migrants (i.e. the mode of the posterior distribution of R) was 170, albeit the credible intervals were large. With a fixed R and a constant u, we conclude that the introduction rate has been steadily, albeit slowly, declining ever since the first migrant has entered the Mediterranean (Fig. 1). Averaged over time, the model’s best estimate of the mean introduction rate is 0.72 species × year -1; which is similar to the constant rate inferred by the S&C model. Furthermore, the model suggests that crossing the Suez Canal became possible (i.e. u > 0) around 1911; 16 years before the first record and 42 years after the opening of the canal (see Belmaker et al., 2009 for details). Table 1. Maximum Likelihood (ML) estimates from the S & C model. Reproduced with permission of the copyright owner from Belmaker et al. (2009). Model Full γ1= γ2 = β1= 0

log Likelihood - 74.83 - 76.32

β0 -0.77 -0.34

β1 0.01 –

γ0 33.57 32.78

γ1 0.052 –

γ2 0.014 –

62 Jonathan Belmaker, Eran Brokovich, Victor China, Daniel Golani and Moshe Kiflawi

Table 2. Bayesian posteriors (modes and 95% credible intervals) of selected parameter. Reproduced with permission of the copyright owner from Belmaker et al. (2009). Parameter * R β0 β1 S0 z

Mode (95% CI) Constant u 170 (98 – 578) -4.9 (-6.0 – -3.5) – 18.5 (8.8 – 36.2) 8 (2.6 – 24.2)

Mode (95% CI) Varying u 140 (80 – 568) -5.3 (-6.7 – -3.5) 0.03 (-0.03 – 0.12) 20.5 (10.3 – 41.9) –

* R = pool of potential Red Sea migrants; logit(u)= β0 + β1× t, where u is immigration probability at the t’th time interval; S0 = number of introduced species before the first report in 1927; 1927- z ×2 = point in time in which dispersal through the canal became possible.

IMPLICATIONS It seems that, averaged over the past 80 years, new Lessepsian migrant fish species have successfully immigrated at a rate ~0.7 per year. The constant annual probability of crossing the Canal (u), predicted by the HB model, implies that the process is largely stochastic. This conclusion is supported by the lack of change, across time, in mean migrant traits such as size, habitat depth and number of closely related (taxonomically and ecologically) species (Belmaker et al., 2009). Moreover, barring major future changes in the factors that affect Lessepsian migration, the process of species introduction into the eastern Mediterranean is expected to continue for many more years, albeit at a decelerating rate (Fig 2). Indeed, major deviation from the expected trends could indicate to future researchers of changes in these factors. As noted above, the temporal invariance of u implies that migration and proliferation of those migrant species that have become established in the eastern Mediterranean is relatively independent of species-specific traits and is consistent with growing body of literature which suggests that inter-specific interactions are seldom a limiting factor in the successful establishment of introduced species (Bruno et al., 2005). Otherwise we would expect a decline of u with time. Nevertheless, species introduced into the Mediterranean are not a random sample from the pool of species in the Red Sea but instead correlated to certain life-history traits (Golani, 1993). In fact, the HB model predicts that just over a third of the 502 species known to occur in the Gulf of Suez (Golani, 1999) are potential candidates for successful introduction. Of these 170 candidate species, 67 are known to have established viable populations in the eastern Med. (Golani et al., 2007). This leaves an expected 100 species likely to cross and possibly be recorded. Why the majority of the species in the Gulf of Suez are not ‘destined’ to enter the Mediterranean is not clear. It seems likely that fishes closely associated with coral reefs

Introduction rate of Lessepsian fishes into the Mediterranean 63

Introduction rate (species * year-1)

0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 1900

S&C S & C - forecast Bayesian Bayesian - forecast 1950

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Year

Fig. 2. The rate of Lessepsian fish introduction into the Mediterranean (species * year-1) according the two models examined (S&C and the HB model). Model results are shown for year < 2006, while results for year > 2006 are future predictions. Predictions of future introduction shown in white symbols.

will not be able to survive in the coral-deprived waters of the Mediterranean. Indeed, many of the successfully introduced species live in shallow sandy or muddy habitats, both in their original and target areas (Golani, 1993). In addition, winter temperatures in the Mediterranean are lower than in the tropical Red Sea and Gulf of Suez. These low temperatures may lie below the minimum tolerable level of many of the tropical fish, thereby preventing their successful establishment. The time (~1911) at which crossing the Canal became possible, as estimated by the HB model, may seem unreasonably late since the Canal was opened some 42 years earlier. However, the Canal was cut through the hypersaline Great and Small Bitter Lakes, which had several meters of salt deposited at their bottom. After the construction of the Suez Canal, the salinity within these lakes is likely to have precluded the movement of either adults or larval fish to the Mediterranean. The salinity of the lakes was subsequently reduced by the influx of sea water from the Red Sea and the dissolution of the salt bed. The HB model’s estimation of 1911 coincides remarkably with the period of time that the salinity of the Bitter Lakes was sufficiently reduced so that it ceased being a barrier to dispersal (Por, 1971). It should be noted that a single species, Atherinomorus lacunosus, was collected off the coast of Egypt prior to this date (1902, see: Tillier, 1902), but may not have reached Israeli waters until 1911.

64 Jonathan Belmaker, Eran Brokovich, Victor China, Daniel Golani and Moshe Kiflawi

Caveat It is possible that what we call immigration probability has little to do with immigration through the Canal but rather more a function of the rate of population expansion in the Mediterranean (i.e., the probability of reaching the Israeli coast within a given time interval). Under this scenario, the Suez Canal would not have constituted a barrier to dispersal and most species would have crossed it relatively early. However, as species typically differ in their population growth rates, many would have remained rare and confined to the area close to the Canal’s opening. Under this alternative scenario, introduced species would have remained confined to the Gulf of Suez until several individuals managed to traverse the Canal and establish a viable population in the Mediterranean. These two scenarios probably represent extremes along a continuum, where for some species range expansion is limited by dispersal while for others it is limited by population size. Since the mechanism of fish introduction cannot be determined solely from the discovery record, resolving this issue requires detailed research on the population structure of Lessepsian fish. Although the exact process regulating the appearance of migrants along the eastern Mediterranean remains unknown, the distinction between the two scenarios need not affect our inferences regarding the dynamics followed by the process. CONCLUSIONS A cursory look at the discovery records of Lessepsian fish species (Fig 1) would lead us to believe that the rate by which these species are entering the eastern Mediterranean is increasing with time. The model-based approach for analyzing the discovery of the records of exotic species, as outlined above, shows that such is not the case. Moreover, it shows that much more information may be gleaned from these records than just the rate of introduction. Such model-based analyses are likely to facilitate the study of biotic exchange, which is central in determining contemporary patterns of diversity (Vermeij, 1991; Brown and Lomolino, 1998), as well as provide vital information in formulating conservation and management policies. The relative recentness of Lessepsian migration and the scope of the phenomenon make it an ideal system for studying the combined action of historical and ecological processes within an ecological timeframe.

Introduction rate of Lessepsian fishes into the Mediterranean 65

APPENDIX 1: THE SOLOW & COSTELLO MODEL Solow and Costello (2004) modeled the number of newly introduced species, per year, as dependent on two components. First, the annual probability that a species introduced in year s will be observed in year t (πst); which itself is a function of both sampling effort and the species abundance in year t:

π st =

exp[γ 0 + γ 1 ⋅ t + γ 2 exp(t − s )] 1 + exp[γ 0 + γ 1 ⋅ t + γ 2 exp(t − s )]

Eq. 1

γ0, γ1 and γ2 are unknown parameters, which allow a monotonic temporal trend in sampling effort (γ1× t ), and incorporates post-introduction growth in fish abundance (γ2 × exp(t-s)). A positive value of γ1 means sampling effort has been increasing, while a negative value means sampling effort has been decreasing. The probability πst is then used to calculate the probability that a species introduced in year s will be discovered in year t: t −1

pst = π st ∏ (1 −π sj ) j=s

Eq. 2

The second component is the mean introduction rate at time t, and is modeled as:

μt = exp(β 0 + β1 ⋅ t )

Eq. 3

where β0 and β1 are unknown parameters. When β1 is positive, the introduction rate is increasing through time and when it is negative, the introduction rate is decreasing. Theoretically, higher order relationships (quadratic functions, etc.) can be examined. However, in practice it is unlikely the data will be informative enough to allow reasonable estimation of these parameters. The number of species introduced in year t thus follows a Poisson distribution with a mean: t

λ t = ∑ μ spst s =1

Eq. 4

The Matlab© code used for this model can be found in Solow and Costello (2004). One can directly insert one’s own data into the text file (NumDis.txt), define the time period over which the samples were taken (the parameter T), and run the code. The model output provides Maximum Likelihood estimates for the five parameters: β0, β1, γ0, γ1 and γ2. From an ecological perspective, the main parameter of interest is μt – the expected unobserved introduction rate – which is directly derived from β0 and β1. To construct a reduced model, one should set the parameters to be eliminated to 0 in the vector “constr”.

66 Jonathan Belmaker, Eran Brokovich, Victor China, Daniel Golani and Moshe Kiflawi

APPENDIX 2: HIERARCHICAL BAYESIAN MODEL The model is separated into a processes model and a data model. The former describes the process of introduction. The latter relates the actual data and the latent state variables (the true number of introduced species). Since only the process model is of biological significance, the following will focus on its properties. A full description of the complete model can be found in Belmaker et al. (2009). The number of species introduced during the t’th time interval is considered a random variable drawn from a Poisson distribution: Lt ~ Poisson(ut․Rpt)

Eq. 5

whereRptis the number of potential migrants that have not yet been established in target system at the onset of the t’th interval: t −1

Rpt = R − So − ∑ Lt t =1

Eq. 6

R is the pool of species that can (potentially) migrate into the target system and S0 is the number of migrant species established in the target system by the onset of the first interval. The parameter ut is the probability with which each of the R species enters and becomes established in the target system during t’th interval. Equation 5 is the Poisson approximation of the binomial which we adopted due to programming limitation associated with direct use of the binomial. To test for the possibility of a monotonic dependence of u on time elapsed since the beginning of the time-series we set:

⎛ u ⎞ log ⎜ t ⎟ = β 0 + β 1⋅t ⎝ 1 − ut ⎠

Eq. 7

where b0 and b1 are unknown parameters (note that a positive/negative b1 implies an increasing/decreasing probability, whereas b1 = 0 implies a constant probability). The equation may be expanded to include any covariates that may affect u (e.g. number of ships or volume of ballast water). Assuming that u is constant through time, the accumulation of migrant species up to the time of the first reported introduction forms a geometric series of length z intervals; starting at a point in time after which dispersal became possible (u > 0). We can estimate this point in time by solving for z:

⎛ S ⎞ ln ⎜1 − 0 ⎟ R⎠ z= ⎝ −1 ln (1 − u )

Eq. 8

Introduction rate of Lessepsian fishes into the Mediterranean 67

(i.e. we can estimate how soon after the opening of the canal did the first Red Sea species become established in the Mediterranean). The Winbugs© code for this model can be found at Belmaker et al. (2009). Winbugs (Spiegelhalter et al., 2004) is a free software that facilitates easy Bayesian computation and can be downloaded from the Internet (http://www.mrc-bsu.cam.ac.uk/bugs/winbugs/ contents.shtml). It is recommended to consult the following resources for an introduction to Bayesian statistics before performing any serious inference (Gelman et al., 1995; Miller and Meyer, 2000; Wade, 2000; Ellison, 2004; Clark, 2005; Clark and Gelfand, 2006; McCarthy, 2007). In this model, ut , the per-species immigration probability, together with the pool-size of potential migrants, R, determines the actual introduction rates. ut is analogous to μt in the S&C model, and is similarly derived directly from β0 and β1. Nevertheless, ut refers to a species’ probability (per unit time) of crossing into the target system, while μt refers to the number (per unit time) of species that enter the target system for the first time. As with the S & C model, one can directly insert one’s own data to the model to obtain posterior distributions of the parameters of interest. This can be done by replacing the original data with the new data, which must include the number of sampling intervals (T), two vectors containing the number of new native and introduced species recorded at time t (new_species and new_species_L, respectively) and two vectors containing the cumulative number of native and introduced species recorded at time t (SM1 and SR1, respectively). It will probably be necessary to change the values of the initials before the model can run on a different data set. To construct a full model that allows for a linear monotonic trend in u through time, one can simply remove the # sign from the parameter “beta1” and replace the # signs between the two versions of logit(u[1]) and logit(u[i]). Note, that under the full model it is invalid to estimate z. REFERENCES Bax, N., J. T. Carlton, A. Mathews-Amos, R. L. Haedrich, F. G. Howarth, J. E. Purcell, A. Rieser, and A. Gray. 2001. The control of biological invasions in the world’s oceans. Conservation Biology 15: 1234-1246. Belmaker, J., Brokovich, E., China, V., Golani, D., and Kiflawi, M. 2009. Estimating the rate of biological introductions: Lessepsian fishes in the Mediterranean. Ecology 90(4): 1134-1141. Ben-Tuvia, A. 1966. Red Sea fishes recently found in the Mediterranean. Copeia 1966: 254-275. Ben-Tuvia, A. 1978. Immigration of fishes through the Suez Canal. Fishery Bulletin 76: 249-255. Ben-Tuvia, A. 1985. The impact of the Lessepsian (Suez Canal) fish migration on the eastern Mediterranean ecosystem. In: Moraitou-Apostolopoulo, M. and V. Kiortsis (eds.), Mediterranean marine ecosystems. New York: Plenum Press. pp. 367-375. Boudouresque, C. F., and M. Verlaque. 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 44: 32-38. Brown, J. H. and M. V. Lomolino. 1998. Biogeography, 2nd edition. Sinauer Associates, Sunderland, MA.

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Bruno, J.F., J.D. Fridley, K.D. Bromberg and M.D. Bertness. 2005. Insights into biotic interactions from studies of species invasions. In: Sax, D.F., J.J. Stachowicz and S.D. Gaines (eds.). Species invasions: insights into ecology, evolution, and biogeography. Sunderland, MA.: Sinauer. Clark, J. S. 2005. Why environmental scientists are becoming Bayesians. Ecology Letters 8: 2-14. Clark, J.S. and A.E. Gelfand. 2006. Hierarchical modelling for the environmental sciences : statistical methods and applications. Oxford, UK.: Oxford University Press. Costello, C. J. and A. R. Solow. 2003. On the pattern of discovery of introduced species. Proceedings of the National Academy of Sciences USA 100: 3321-3323. Diamant, A., A. Ben-Tuvia, A. Baranes and D. Golani. 1986. analysis of rocky coastal eastern Mediterranean fish assemblages and a comparison with an adjacent small artificial reef. Journal of Experimental Marine Biology and Ecology 97: 269-285. Gelman, A., J.B. Carlin, H.S. Stern and D.B. Rubin. 1995. Bayesian data analysis. London: Chapman and Hall. Golani, D. 1993. The sandy shore of the Red-Sea – launching pad for Lessepsian (Suez Canal) migrant fish colonizers of the Eastern Mediterranean. Journal of Biogeography 20: 579-585. Golani, D. 1996. The marine ichthyofauna of the Eastern Levant – history, inventory, and characterization. Israel Journal of Zoology 42: 15-55. Golani, D. 1999. The Gulf of Suez ichthyofauna – assemblage pool for Lessepsian migration into the Mediterranean. Israel Journal of Zoology 45: 79-90. Golani, D. 2005. Checklist of the Mediterranean fishes of Israel. Zootaxa 947: 3-90. Golani, D. and A. Ben-Tuvia. 1995. Lessepsian migration and the Mediterranean fisheries of Israel. In: Armantrout, N.B. (ed.), Conditions of the world’s aquatic habits, proceedings of the World Fishery Congress Theme 1. New Delhi: Oxford & IBH Pub. Co. Pvt. Ltd. pp. 279-289. Golani, D., L. Orsi-Relini, E. Massutí, and J.-P. Quignard. 2002. CIESM atlas of exotic species in the Mediterranean. Vol. 1. Fishes. F. Briand (ed.) Monaco: CIESM Publishers. 254 pp. Golani, D., B. Özturk, and N. Basusta. 2006. Fishes of the Eastern Mediterranean. Turkish Marine Research Foundation, Istanbul, Turkey. 259 pp Golani, D., B. Appelbaum-Golani and O. Gon. 2007. Apogon smithi (Kotthaus, 1970)(Teleostei: Apogonidae): a Red Sea cardinalfish colonizing the Mediterranean Sea. Journal of Fish Biology 72: 1534-1538 Goren, M. and B. S. Galil. 2005. A review of changes in the fish assemblages of Levantine inland and marine ecosystems following the introduction of non-native fishes. Journal of Applied Ichthyology 21: 364-370. Gotelli, N. J. and R. K. Colwell. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4: 379-391. Grosholz, E. 2002. Ecological and evolutionary consequences of coastal invasions. Trends in Ecology and Evolution 17: 22-27 McCarthy, M.A. 2007. Bayesian methods for ecology. Cambridge, Mass.: Cambridge University Press. Millar, R. B. and R. Meyer. 2000. Bayesian state-space modeling of age-structured data: fitting a model is just the beginning. Canadian Journal of Fisheries and Aquatic Sciences 57: 43-50. Por, F.D. 1971. One hundred years of Suez Canal – a century of Lessepsian migration. Systematic Zoology 20: 138-159. Ricciardi, A. 2001. Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes? Canadian Journal of Fisheries and Aquatic Sciences 58: 2513-2525.

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Sax, D.F. and S.D. Gaines. 2003. Species diversity: from global decreases to local increases. Trends in Ecology and Evolution 18: 561-566 Solow, A.R. and C.J. Costello. 2004. Estimating the rate of species introductions from the discovery record. Ecology 85: 1822-1825. Spiegelhalter, D., A. Thomas and N. Best. 2004. WinBUGS version 1.4.1 User Manual. Medical Research Council Biostatistics Unit, Cambridge. [http: //www.mrc-bsu.cam.ac.uk/bugs/ winbugs/contents.shtml] Tillier J.E. 1902. Le Canal de Suez et sa faune ichthylogique. Mémoires de la Société zoologique de France 15: 279-318 Vermeij, G. J. 1991. When biotas meet – understanding biotic interchange. Science 253: 1099-1104. Wade, P. R. 2000. Bayesian methods in conservation biology. Conservation Biology 14: 1308-1316. Wonham, M. J. and E. Pachepsky. 2006. A null model of temporal trends in biological invasion records. Ecology Letters 9: 663-672.

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The genetics D. Golani & B. Appelbaum-Golani (Eds.) 2010 of Lessepsian bioinvasions 71 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 71-84. © Pensoft Publishers Sofia–Moscow

The genetics of Lessepsian bioinvasions Giacomo Bernardi, Daniel Golani and Ernesto Azzurro

INTRODUCTION Bioinvasions are increasingly having an impact on ecological and economic balances in both terrestrial and marine habitats (Kolar and Lodge, 2001) and, as such, are becoming the focus of attention. At the same time however, invasive phenomena are increasingly seen as a unique opportunity to explore ecological (Lockwood et al., 2007) and evolutionary processes in the marine environment (Lee, 2002; Rice and Sax 2005; Wares et al., 2005). Much work has been dedicated to the understanding of the ecological consequences of introductions and resources have been allocated to prevent and control those invasions. Recently, genetic tools have been added to the approaches used to assess bioinvasions and together with those new results, theoretical predictions have been formulated. Genetic studies have been traditionally employed to answer a variety of questions such as to determine invasive patterns, to reconstruct the route, the source and the timing of invasion and to explore the historical biogeography, as evidenced by a growing amount of literature. Invasive species colonizing a new environment typically face new selective pressures. Following fundamental principles of population genetics, their genetic variability can be considered integral to their capability to adapt. Indeed empirical evidence supports the link between invasion success and genetic attributes, such as additive genetic variance, epistasis, hybridization, genetic tradeoffs, the action of small numbers of genes and, possibly, genomic rearrangements (see Lee, 2002 for review). Nevertheless, bioinvaders generally harbor a sub-set of the original genetic pool, due to founding effects, which are evidenced by a genetic bottleneck. With some exceptions (e.g. Tsutsui, 2000), a reduction in genetic variability is predicted to make populations vulnerable, especially in their capability to adapt to environmental conditions, in contrast to the general success of bioinvaders. The level of genetic loss during the colonization process will be determined by the propagule size and the diversity of founder individuals, which is related to the diversity

72 Giacomo Bernardi, Daniel Golani and Ernesto Azzurro

of the source population. In some cases, initial genetic bottlenecks can be dampened by multiple invasions, accompanied by high gene flow, that eventually allow invading populations to exhibit sustainable genetic diversity (Dlugosh and Parker, 2007). One of the major problems that plagued the study of bioinvasions derives from the fact that bioinvaders are usually observed a long time after their original invasion and only once they have successfully colonized the new habitat. This is a problem because, in most situations, it is difficult to determine when the invasion originally occurred and if it is the result of a single event or successive ones. Failed invasions tend also not to be accounted for. In that respect, the case of Lessepsian bioinvasions is quite unique. Lessepsian invaders are organisms originating from the Red Sea that entered the Mediterranean Sea via the Suez Canal, opened in 1869 under the supervision of the engineer Ferdinand de Lesseps. With more than 300 new species added to the Mediterranean (Galil, 2009), including 71 species of fishes (Bilecenoglu et al., 2008; Lipej et al., 2008; Golani, this volume), i.e., approximately a quarter to one half of the world’s marine fish invaders (Lockwood et al., 2007), the Lessepsian migration represents the ‘most important biogeographic phenomenon witnessed in the contemporary oceans’ (Por, 1978). It is an ongoing process with new species regularly entering every year and certainly a massive human-mediated ‘experiment’ (Féral, 2002), with unique opportunities to study rapid evolutionary changes. The vast majority of Indo-Pacific organisms that are currently present in the Mediterranean can be considered as resulting from Lessepsian migrations. Only few of them might possibly have a different origin, following two main hypotheses. Firstly, it has been suggested that Tethys Sea remnants may have been present in the Mediterranean during the Messinian Salinity Crisis (MSC). Approximately 5.5 Mya, a desiccation event dried up the Mediterranean (the MSC), which later refilled at the opening of the Strait of Gibraltar with the Atlantic Ocean (Bianco, 1990). Some authors have suggested that a few species, originally from the Red Sea (which was part of the Tethys Sea), may have been present in the Mediterranean and survived the desiccation period. In fact, this hypothesis is highly unlikely but needs to be kept in mind. A more likely scenario derives from the fact that a connection between the Red Sea and the Mediterranean has been tampered with for a very long time, starting in ancient Egyptian, and later, Roman times. Besides those extreme cases, the vast majority, if not all, of species with Red Sea affinities that are present in the Mediterranean did invade after 1869. Interestingly, the dates of Lessepsian invasion span a very long period. In the case of the species that will be presented here, the date of first invasion varies from the late 1900s to the present (Table 1). Because the time of invasion is variable for different Lessepsian invaders, a precise record of the first occurrence of invasion is of crucial importance to fully appreciate genetic data. This information is often available for Lessepsian species, together with a detailed spatio-temporal picture of their spread in the Mediterranean (Golani et al., 2002).

The genetics of Lessepsian bioinvasions 73

Therefore, Lessepsian migrants offer some definite advantages for scientists. Since the timing of invasion, the invasion route, and the invader’s geographic source are known, theoretical predictions seemed fairly simple. Some individuals from the Red Sea would enter the Mediterranean via the Suez Canal, and would later expand in the novel environment. This situation would predict a likely genetic bottleneck due to an invading sub-sample of the original populations, followed by a fast range expansion, a pattern that is consistent with other documented invasions (e.g. Sax et al., 2005). Our goal here is to review and compare genetic studies of Lessepsian migrants in order to determine if this unique bioinvasion follows some general patterns. We also want to assess if Lessepsian invasions can be used to test specific theoretical predictions. Specifically, we want to determine if (1) invasions were accompanied by bottlenecks, (2) success could be associated with genetic diversity, and if (3) bottlenecked populations displayed rapid population expansions. METHODS AND APPROACHES The genetic approaches used to study Lessepsian migrants reflect the general evolution of methodological toolboxes used in the field of molecular ecology and evolution. Early studies of Lessepsian invaders capitalized on the rapid, easy, and relatively cheap allozyme assays (e.g. Lavee and Ritte, 1994; Golani and Ritte 1999; Safriel and Ritte, 1986). These studies allowed the establishment of the bases of understanding for the genetic patterns displayed by marine bioinvaders. However, while genetic bottlenecks and their associated lowered genetic diversity were expected, these early studies showed that Lessepsian migrants did not show such genetic signatures. As for the rest of the field, criticisms of allozymic methods mostly focused on the lack of resolution and the potential for the presence of selective pressure. Therefore the logical next step was to use neutral DNA markers. The workhorse of population genetics being the use of mitochondrial DNA sequences, the second wave of studies used such markers. Unexpectedly, these studies confirmed previous results based on allozymes. Indeed, the surprising lack of bottlenecks in Lessepsian migrants was found not to be due to an artifact of the allozymic methods, but was real and confirmed by neutral mitochondrial markers (e.g. Bucciarelli et al., 2002; Hassan et al. 2003; but see Golani et al., 2007 for a bottleneck). It is clear that DNA sequences have provided some unique insight in the understanding of the genetics of Lessepsian bioinvaders, yet, it is also clear that more power could be gained by using larger datasets and more variable markers. Microsatellites and SNPs seem to be ideal candidates and the obvious choices for such approaches. They have not yet been used on Lessepsian migrants, but it is likely that they will soon be, and it is also likely that new light will then be shed on the Lessepsian system.

74 Giacomo Bernardi, Daniel Golani and Ernesto Azzurro

GENETIC STUDIES Electrophoretic analysis of Red Sea and Mediterranean populations are available for Aphanius dispar (Rüppell, 1829). This Teleost fish was considered for many years to be a Lessepsian migrant but in all probability was in fact present in the Mediterranean prior to the opening of the Suez Canal (Kornfield and Nevo, 1972) and hence it will be not included in our review. Genetic approaches focusing on bona-fide Lessepsian migrants started in 1994. Currently 14 species have been investigated (which is less than 5% of the known invaders) (Table 1). These 14 species include 1 marine angiosperm, Halophyla stipulacea, 6 invertebrates, and 7 fish species. In the field of Lessepsian invasion, molecular techniques have been mainly employed to contrast the levels of genetic diversity between native and invasive populations (Golani and Ritte, 1999; Bucciarelli et al., 2002; Karako et al., 2002; Bonhomme et al., 2003; Hassan et al., 2003; Azzurro et al., 2006) and to test for genetic structuring within invasive populations (Karako et al., 2002; Azzurro et al., 2006; Terranova et al., 2006). Genetic studies have been also used to explore demographic aspects within the Mediterranean (Azzurro et al., 2006; Iannotta et al., 2007), to support taxonomy (Golani and Ritte, 1999; Kasapidis et al., 2007) and to unveil cryptic sibling species (Bucciarelli et al., 2002) Many Lessepsian species tend to be quite cryptic (such as interstitial polychaetes and flatworms), and are likely to be overlooked for a long time before being recorded. However, the 14 species that were used in this analysis are large and conspicuous and are therefore likely to have been noticed very soon after their first occurrence in the Mediterranean. GENETICAL VARIABILITY IN LESSEPSIAN INVADERS Population bottleneck, often associated with a loss of genetic variability, seems to be a common feature of biological invasions (Allendorf and Lundquist, 2003). In this review, the presence of bottlenecks could be addressed for 12 out of 14 studied species. Noticeably, most of Lessepsian invaders (10 out of 12) did not display any sign of founder effect, with any apparent loss of genetic diversity from the Red Sea to the Mediterranean (see Table 1). Nevertheless, sampling was biased since it was conducted mostly in the areas of major abundances for these species (the Eastern Mediterranean). In addition, bias was also introduced in sampling the source populations, because specimens were mainly collected in the northern Red Sea, particularly Eilat (Israel). In the majority of the studied cases, the original invasion occurred a long time ago (Table 1). Older and successive waves of invaders might have added to incipient populations, making it difficult to detect specific signatures of single founding episodes. A chance to do away with these confounding effects was to focus on early invasive events, possibly

Estimated date of invasion 1895 (1)

Data type

* potential Lessepsian invader sampled along the whole length of the Suez Canal

Halophyla stipulacea

Species

Evidence of bottleneck

RAPD N/I ITS no Invertebrates Brachydontes pharaonis 1876 (2) alloz., SSCP, CO1 no Cerithium scabridum 1883 (11) alloz. n.d. Modiolus auriculatus early 1900 (2) alloz. no Lysidice collaris 1962 (3) ITS, CO1 N/I, but low diversity Asterina burtoni 1966 (4) RAPD yes Minona ileanae not yet* (10) ISSR no Fishes Siganus rivulatus 1927 (5) SSCP, RFLP, ISSR no Upeneus pori 1950 (6) alloz. no Upeneus moluccensis 1947 (12) alloz., n and m SSCP no Atherinomorus lacunosus 1902 (13) DL no Siganus luridus 1956 (7) SSCP, RFLP, ISSR, DL no Fistularia commersonii 2000 (8) DL yes Lagocephalus sceleratus 2003 (9) Cyt b N/I

Plants

Organism

yes yes yes no yes no no no no no no yes yes no

(1) (2) (3,4,5,16) (17) (3) (6) (7) (15) (8) (9) (9, 10) (11) (8, 12) (13) (14)

Reached Genetic study western basin

Genetic study 1. Procaccini et al., 1999; 2. Ruggiero and Procaccini, 2004, 3. Lavee and Ritte, 1994, 4. Safriel and Ritte, 1986, 5.Shefer et al., 2004, 16. Sirna Terranova et al., 2006, 17. Lavie and Nevo, 1986, 6. Iannotta et al., 2007, 7 Karako et al., 2002, 15. Lai et al., 2008., 8. Hassan et al., 2003, 9. Golani and Ritte, 1999, 10. Hassan and Bonhomme, 2005, 11. Bucciarelli et al., 2002, 12. Azzurro et al., 2006, 13 Golani et al., 2007, 14. Kasapidis et al., 2007.

Table 1. Date of invasion, 1. Fritsch, 1895, 2. Fuchs, 1878, 11. Keller, 1883, 3. Tenerelli, 1962, 4. Tortonese, 1966, 10. Lai et al., 2008, 5. Steinitz, 1927, 6. Kosswig, 1950, 12. Haas and Steinitz, 1947. 13. Tillier 1902, 7. Ben-Tuvia, 1964, 8. Golani, 2000 9. Akyol et al., 2005.

The genetics of Lessepsian bioinvasions 75

76 Giacomo Bernardi, Daniel Golani and Ernesto Azzurro

far from the source of invasion. In the last few years, three different papers (Azzurro et al., 2006; Terranova et al., 2006; Golani et al., 2007) presented such kinds of data, thus overcoming pragmatic difficulties in studying recently founded populations and making a step forward into the exploration of the Lessepsian invasive dynamics. In Brachidontes pharaonis, no difference in both haplotype and nucleotide diversity was detected between the youngest populations (of Sicily) and the oldest populations of the Eastern Mediterranean Sea (Terranova et al., 2006). Within the Mediterranean, some regional clustering and the existence of unique haplotypes have been evidenced for this species, but the input of larvae from ballast waters seemed to be the most likely explanation, with no reference to the Lessepsian process (Shefer et al., 2004). The absence of genetic differentiation between Mediterranean and Red Sea populations of B. pharaonis (Shefer et al., 2004; Terranova et al., 2006) and mostly of some fish species, i.e. the hardyhead silverside Atherinomorus lacunosus (Bucciarelli et al., 2002), the rabbitfishes Siganus luridus and S. rivulatus (Bonhomme et al., 2003; Hassan et al., 2003) and the goatfishes Upeneus pori and U. maluccensis (Golani and Ritte, 1999; Hassan and Bonhomme, 2005), contributed to develop the idea that Lessepsian migration involves many individuals since its early phases and continuous gene flow from the Red Sea. These findings were later confirmed by Azzurro et al. (2006), which showed no partitioning between the Mediterranean and the Red Sea populations of S. luridus. Importantly, mitochondrial diversity appeared to be preserved also in the youngest and westernmost population of Linosa, with no traces of founder events, suggesting that the genetic variability was ‘there’ from the very beginning of the process. This could indicate that recruitment processes occur “en masse” with relatively high levels of genetic diversity within a cohort. At the same time, these authors showed a weak but detectable structure between Red Sea and Mediterranean populations, with a slight lowering of the genetic diversity in the latter. These findings were based on a wider geographic sampling with respect to previous studies (Bonhomme et al., 2003; Hassan et al., 2003) and highlighted the importance to sample along the entire introduced range of Lessepsian invaders, not only close to their entry point. Many other marine invaders have showed little or no genetic erosion during the colonization process (Holland, 2001; Wares, 2005) and this was mainly due to very large propagule sizes or even to repeated introductions from different source areas. In contrast, the Blue-spotted cornetfish displayed very strong evidence of a genuine bottlenecking event, with only 2 haplotypes being present in the Mediterranean (Fig. 1), suggesting that a single invasion event by as few as two females had generated its invasion in the Mediterranean Sea (Golani et al., 2007). The Blue-spotted cornetfish, Fistularia commersonii, is now considered one of the 100 ‘worst’ invasive species of Europe (Daisie, 2008. http: //www.europe-aliens.org), as it only recently entered the Mediterranean (Golani, 2000) yet it is rapidly spreading through both the eastern and western basin. So far, no similar episodes are available for the Mediterranean Sea but the migration of Red Sea species in the form of a small number of individuals is likely to have occurred several times. In fact, several Lessepsian species have been tallied on the basis

The genetics of Lessepsian bioinvasions 77 F. petimba (Taiwan) F. tabacaria (Sao Tome)

TUR (1) SCI (1) LAM (6) RHO (19)

95/97

HAI (12) JAF (2) ASH (3)

Lessepsian migrants

MAL15 EIL8 EIL9 MOO1 EIL5 EIL1 EIL6 EIL17 EIL4

83/20

EIL29 EIL7 MOO3

86/88

LAM (5)

ASH HAI TUR

Ashdod, Israel Haifa, Israel Karaburnu, Turkey

RHO LAM

Rhodes, Greece Lampedusa, Italy

EIL MAL SEY MOO MUE

Eilat, Israel Marsa Alam, Egypt Seychelles Moorea, French Polynesia Baja California, Mexico

RHO (2)

2% Bay/NJ

95/33

EIL28 SEY2 EIL14 EIL13 MAL1 EIL27 MAL2 EIL11 MAL4 EIL23 MOO2 EIL2 EIL10 EIL15 EIL20 EIL26 SEY1 EIL25 EIL4 EIL21 EIL16 EIL19 EIL22

94/62

MUE 1

78/46 MUE 2 MAL5 MAL7 MAL12 MAL8 MAL14 MAL9 MAL6 MAL13 MAL10

58/66

MAL11 EIL1 EIL12 EIL18 MAL3

Fig. 1. Phylogenetic relationships of Fistularia commersonii samples based on mitochondrial control region sequences based on Bayesian and Neighbor-Joining reconstruction methods. Numbers next to the main nodes correspond to Bayesian consensus numbers (left figures) and NeighborJoining bootstrap support (right figures, 2000 replicates). Sample codes and sampling locality, and the two Mediterranean (Lessepsian) haplotypes are identified in the figure. Two outgroups were used, F. petimba, collected in Taiwan, and F. tabacaria, collected in Sao Tomé.

of only one or few specimens, with no further signs of population growth or expansion (Golani et al., 2002). In these cases, it is difficult to support the idea of a massive and continuous migration of individuals, since it would result in repeated sightings, or even in sustaining the incipient population during its establishment process.

78 Giacomo Bernardi, Daniel Golani and Ernesto Azzurro

Only one other Lessepsian species, the sea star Asterina burtoni (Karako et al., 2002) displayed a significant loss in genetic diversity, but this was attributed to differences in the reproductive mode adopted by this species in the Mediterranean and in the Red Sea (fissiparity vs. sexual reproduction). GENETIC DIVERSITY, TEMPORAL DYNAMICS AND INVASION SUCCESS Many invaders undergo variable periods of time between initial establishment and subsequent population growth and expansion. Such lags of time are a common feature in biological invasions (Kowarik, 1995) and it may have diverse ecological and demographic causes or even it may be determined by time needed for evolutionary adaptation to the new environment (Holt et al., 2005). As far as Lessepsians are concerned, genetic studies did not support any conclusion on their temporal dynamics and documented time lags have been justified on the basis of alternative ecological reasons. The only available examples are the case of the recently settled population of S. luridus in Linosa, which appeared three decades after its first settlement in the Sicily Channel (Azzurro and Andaloro, 2004; Azzurro et al., 2006), and of the mussel B. pharaonis, which underwent population explosion (massive formations of beds) after a lag of about 120 years since its first establishment in the Israeli coasts (Rilov et al., 2004). This lack of knowledge is not surprising among Lessepsians, since the role of evolutionary changes in the colonization process is seldom explored in invasive species (Sakai et al., 2001). The success of an exotic species, apparently not genetically adapted to its new environmental conditions, is always difficult to explain. All the analyzed studies deal with successful invaders but (after the case of F. commersonii) we have seen that their genetic variability may span between opposites, from the absence of genetic loss to severe bottlenek. The case of F. commersonii provides a clear example that an extreme bottleneck does not preclude population growth and rapid geographical expansion. This also draws attention to an emblematic paradox of invasion biology: “how bottlenecked populations that typically have low fitness can become invasive?” (Frankham, 2004). Actually, the observed contradiction between the decline in genetic diversity and invasive success seems to be a rule rather than an exception in introduced species (Dlugosh and Parker, 2007). The invasion success of F. commersonii, regardless of its genomic uniformity, also debunks the apparently coherent pattern in the dynamic of Lessepsian invasions, as probably expected from previous works (e.g. Golani and Ritte, 1999; Bonhomme et al., 2003; Hassan et al., 2003; Hassan and Bonhomme, 2005; Azzurro et al., 2006). To sum up, there is no apparent association between genetic diversity and invasive success in Lessepsian migrants and our findings reaffirm a well-known difficulty of predicting the success of new invaders on the basis of this information. Yet, it is

The genetics of Lessepsian bioinvasions 79

possible that neutral genetic markers were poor indicators of heritable variation in adaptive traits (McKay and Latta, 2002), but the discussion of this hypothesis goes far beyond the purposes of this paper. Alternatively, high genetic variability may have little significance for Lessepsians, as hypothesized by Golani and Ritte (1999) and ecological traits could much more important in determining the success of these organisms (Golani, 1993). During the establishment process, a plethora of biotic and abiotic variables, together with demographic and environmental stochasticity probably interplay their roles (Lockwood et al., 2007) making it difficult to rationalize the factors of success for invasive species. Considering the young history of the Lessepsian invaders, it is possible that some of them had had enough phenotypic plasticity (the ability to cope with a range of environmental conditions) to survive, reproduce and succeed in their novel environment, with ‘no need’ of evolutionary adaptation. This can be likely at least for those species for which there was no lag of time between the initial colonization and subsequent population explosion. According to Allendorf and Lundquist (2003) and to Sax and Brown (2000) some species may be intrinsically better competitors because they evolved in a more competitive environment. Hence, the possibility of a competitive superiority of these colonists coming from a species rich region (the Red Sea), should be also taken into appropriate account. It is equally true that successful Lessepsian migrants, which seem adapted or even ‘preadapted’ (Sakai et al., 2001) to the variety of the conditions of coastal Mediterranean habitats, might reasonably have some limits to their performances, with relation to biotic and abiotic variables, such as temperature (noteworthy are the mortalities which have been observed for F. commersonii during the coldest winter times: Azzurro, personal information). Ultimately, the new biotic and abiotic conditions encountered in the Mediterranean Sea represent new selective forces for Lessepsian migrants and selective effects are expected in these populations, even if the studies available up to date do not provide evidence of that. Selection might occur in response to environmental forces, such as temperature and photoperiod, or to biological variables such as competitors, predators, prey and parasites. RESEARCH PERSPECTIVES Molecular techniques represent a new approach in invasion biology and certainly much has to be done in this field. Moreover the Lessepsian phenomenon has a relatively young history with only a small fraction of the Red Sea species that have already established in the Mediterranean. For the majority of these colonists, we have no information on their genetic structure and we have already lost the opportunity to study their colonization from the beginning. Nevertheless, other species are currently still in the process of

80 Giacomo Bernardi, Daniel Golani and Ernesto Azzurro

invading the Mediterranean and many other organisms are extending their distribution range into the Mediterranean, thus offering new study opportunities. Genetic differences in invasive and source population might be masked by sampling biases. Therefore it is important to focus on the early phases of the invasive process and to sample the largest possible geographical area for comprehensive genetic studies. Marginal populations at the westernmost edge of the distribution range, and the study of the colonization at its earliest stages, turned out to be particularly informative (Azzurro, 2006; Terranova et al., 2006; Golani et al., 2007). Early settled populations are unique events that would allow to simplify theoretical work and help to determine the fundamental variables of the colonization process, such as the propagule size, one of the least documented aspect in invasion biology ( Lockwood et al., 2007). Our ability to detect the effects of founder events will also depend upon the measure that we use for genetic variation. Techniques such as microsatellites and SNPs have seldom been employed with Lessepsians and it is likely that they will yield new and exciting results. Clearly, genetic information on a great number of Lessepsians would give us a better and more comprehensive understanding of this phenomenon. Nevertheless, the monitoring of selected key species at the genetic level may be used to test directly our hypothesis. For instance, given the large contemporary size of the Mediterranean population of F. commersonii, new migrants from the Red Sea are predicted to have little effects in altering haplotype frequencies and this would deserve to be assessed in the future. CONCLUSIONS Our review certainly failed to reconstruct a uniform pattern for the genetic of Lessepsian invaders, which likely includes a variety of different invasive models. However we have enough information to conclude that the passage used by larvae and/or adults to enter the Mediterranean (the Suez Canal) had the potential to sustain great numbers of migrants and high gene flow, at least for most of these colonists. Interestingly, there is also a homogeneous phylogeographical pattern for the species that have migrated from the Atlantic Ocean into the Mediterranean during geological times (Patarnello et al., 2007). Thus, the biogeographical relationships between the Mediterranean and its oceanic connections remain somehow controversial at the genetic level. As far as Lessepsian migrants are concerned, beside spatial and temporal biases of previous studies, uncertainty may arise from the uniqueness of single species but also from the rapid environmental changes that are now happening in the Mediterranean Sea. The same Lessepsian pathway is far from steady in its function. In fact, the Suez Canal has changed much in the course of its history, having experienced drastic environmental modifications (e.g. the decline in salinity of the Bitter Lakes; see Golani, this volume) together with important human-inducted alterations, which occurred at the release areas

The genetics of Lessepsian bioinvasions 81

(i.e. the damming of the Nile). Therefore its capacity to act as a genetic barrier and to produce phylogeographical breaks between native and donor populations has significantly changed since its opening. Above all, the warming trend of the Mediterranean is providing more suitable ecological conditions for Lessepsian migrants (CIESM, 2008). These species, which have entered a temperate sea, are typically thermophilic, with tropical or subtropical origin (Golani et al., 2002) and their increasing number and success represent one of the most visible consequences of climate change within the Mediterranean realm (Bianchi, 2007; Azzurro, 2008 and references therein included). The occurrence of evolutionary adaptive processes in Lessepsian invaders highlights the fact that the Mediterranean environment may be changing towards the requirements of these tropical species, rather than the opposite. ACKNOWLEDGEMENTS We acknowledge the Euromediterranean Center for Climatic Changes and the Italian Ministry for the Environment and the Territory Ministry (Project: The impacts of biological invasions and climate change on the biodiversity of the Mediterranean Sea) for partially supporting the formulation of this review. REFERENCES Allendorf, F.W. and L.L. Lundquist. 2003. Introduction: population biology, evolution, and control of invasive species. Conservation Biology 17: 24-30. Akyol, O., V. Unal, T. Ceyhan and M. Bilecenoglu. 2005. First confirmed record of Lagocephalus sceleratus (Gmelin, 1789) in the Mediterranean. Journal of Fish Biology 66: 1183-1186. Azzurro, E. 2008. The advance of thermophilic fishes in the Mediterranean sea: overview and methodological questions. In: Briand, F. (ed.). Climate warming and related changes in Mediterranean marine biota. CIESM Workshop Monographs No. 35. pp. 39-46. Azzurro, E. and F. Andaloro. 2004. A new settled population of the lessepsian migrant Siganus luridus (Pisces: Siganidae) in Linosa Island – Sicily Strait. Journal of Marine Biological Association UK 84: 819-821. Azzurro, E., D. Golani, G. Bucciarelli and G. Bernardi. 2006. Genetics of the early stages of invasion of the Lessepsian rabbitfish Siganus luridus. Journal of Experimental Marine Biology and Ecology 333: 190-201. Ben-Tuvia, A. 1964. Two siganids fishes of Red Sea origin in the eastern Mediterranean. Bulletin of the Sea Fisheries Research Station, Haifa 37: 3-10. Bianchi, C.N. 2007. Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580 (1): 7-21. Bilecenoglu, M., M.B. Yokeş and A. Eryigit, 2008. First record of Vanderhorstia mertensi Klausewitz, 1974 (Pisces, Gobiidae) in the Mediterranean. Aquatic Invasions 3: 487-490.

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Bonhomme, F., A. Baranes, D. Golani and M. Harmelin-Vivien. 2003. Lack of mitochondrial differentiation between Red Sea and Mediterranean populations of the Lessepsian rabbitfish, Siganus rivulatus (Perciformes: Siganidae). Scientia Marina 67: 215-217. Bucciarelli, G., D. Golani and G. Bernardi. 2002. Genetic cryptic species as biological invaders: the case of Lessepsian fish migrant, the hardyhead silverside Atherinomorus lacunosus. Journal of Experimental Marine Biology and Ecology 273: 143-149. CIESM, 2008. Climate warming and related changes in Mediterranean marine biota. N° 35 in CIESM Workshop Monographs [F. Briand, Ed.] Monaco, 152 pp. http: //www.ciesm. org/online/monographs/Helgoland.html Frankham, R. 2005. Resolving the genetic paradox in invasive species. Heredity 94: 385. Fuchs, Th. 1878. Die geologische Beschaffenheit der Landenge von Suez. Denkschriften der Kaiserkichen Akademie der Wissenschaften, Mathematisch-Naturwissenschaftliche Classe 38: 25-42. Galil, B.S. 2009. Taking stock: inventory of alien species in the Mediterranean sea. Biological Invasions 11: 359-372. Garton, D.W. and W. R. Haag. 1991. Heterozygosity, shell length and metabolism in the European mussel, Dreissena polymorpha, from a recently established population in Lake Erie. Comparative Biochemistry and Physiology 99a (1/2): 45-48. Golani, D. 1993. The sandy shore of the Red Sea – launching pad for Lessepsian (Suez Canal) migrant fish colonizers of the eastern Mediterranean. Journal of Biogeography 20: 579-585. Golani, D. 2000. First record of the Bluespotted cornetfish from the Mediterranean. Journal of Fish Biology 56: 1545-1547. Golani, D. and U. Ritte. 1999. Genetic relationship in goatfishes (Mullidae: Perciformes) of the Red Sea and the Mediterranean, with remarks on Suez Canal migrants. Scientia Marina 63: 129-135. Golani, D., L. Orsi-Relini, E. Massutí and J.P. Quignard. 2002. CIESM atlas of exotic species in the Mediterranean, Vol.1, Fishes. Briand F. (ed.). Monaco: CIESM Publishers. 254 pp. Golani, D., E. Azzurro, M. Corsini-Foka, M. Falautano, F. Andaloro and G. Bernardi. 2007. Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant. Biology Letters 3: 541-545. Golani, D., B. Appelbaum-Golani and O. Gon. 2008. Apogon smithi (Kotthaus, 1970) (Teleostei: Apogonidae), a Red Sea cardinalfish colonizing the Mediterranean Sea. Journal of Fish Biology 72: 1534-1538. Haas, G. and H. Steinitz. 1947. Erythrean fishes on the Mediterranean coast of Palestine. Nature 160: 28. Hassan, M. and F. Bonhomme. 2005. No reduction in neutral variation of mitochondrial and nuclear genes for a Lessepsian migrant, Upeneus moluccensis. Journal of Fish Biology 66: 865-870. Hassan, M., M. Harmelin-Vivien and F. Bonhomme. 2003. Lessepsian invasion without bottleneck: example of two rabbitfish species (Siganus rivulatus and Siganus luridus). Journal of Experimental Marine Biology and Ecology 291: 219-232. Hawley, D.M., D. Hanley, A.A. Dhondt and I.J. Lovette. 2006. Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Molecular Ecology 15: 263-275. Holland, B.S. 2000. Genetics of marine bioinvasions. Hydrobiologia 420: 63-71. Holland, B.S. 2001. Invasion without a bottleneck: microsatellite variation in natural and invasive populations of the brown mussel Perna perna (L). Marine Biotechnology 3: 407-415.

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Holt, J., M. Barfield and R. Gomulkiewicz. 2005. Theories of niche conservatism and evolution: could exotic species be potential tests? In: Sax, D.F., J.J. Stachowicz and S.D. Gaines (eds.), Species invasions: insights into ecology, evolution, and biogeography, Sunderland: Sinauer. pp. 259-290. Iannotta, M.A., F.P. Patti, M. Ambrosino, G. Procaccini and M.C. Gambi. 2007. Phylogeography of two species of Lysidice (Polychaeta, Eunicidae) associated to the seagrass Posidonia oceanica in the Mediterranean Sea. Marine Biology 150: 1115-1126. Karako, S., Y. Achituv, R. Perl-Treves and D. Katcoff. 2002. Asterina burtoni (Asteroidea; Echinodermata) in the Mediterranean and the Red Sea: Does asexual reproduction facilitate colonization? Marine Ecology Progress Series 234: 139-145. Kasapidis, P., P. Peristeraki, G. Tserpes and A. Magoulas. 2007. First record of the Lessepsian migrant Lagocephalus sceleratus (Gmelin, 1789) (Osteichthyes: Tetraodontidae) in the Cretan Sea (Aegean, Greece). Aquatic Invasions 2(1): 71-73. Keller, C. 1882. Die Fauna im Suez Kanal und die Diffusion de mediterranen und erythräischen Tierwelt. Neue Denkschriften der allgemeinen Schweizerischen Gesellschaft für die gesammten Naturwissenschaften 28(3): 1-39. Kolar, C.S. and D.M. Lodge. 2001. Progress in invasion biology: predicting invaders. Trends in Ecology and Evolution 16: 199-204. Kornfield, I.L. and E. Nevo. 1976. Likely pre-Suez occurrence of a Red Sea fish, Aphanius dispar, in the Mediterranean. Nature 264: 289-291. Kosswig, C. 1950. Erythräische Fische im Mittelmeer und an der Grenze der Ägais. Syllegomena Biologica. Festschrift Kleinschmidt. Leipzig: Akademie Verlag. pp 203-212 Kowarik, I. 1995. Time lags in biological invasions with regard to the success and failure of alien species. In: Pylek, P., K. Prach, M. Rejmanek and M. Wade (eds.). Plant invasions – general aspects and special problems. Amsterdam (The Netherlands): SPB Academic Publishers, pp. 15-38. Lai, T., M. Curini-Galletti and Casu, M. 2008 Genetic differentiation among populations of Minona ileanae (Platyhelminthes: Proseriata) from the Red Sea and the Suez Canal. Journal of Experimental Marine Biology and Ecology 362(1): 9-17. Lavee, D and U. Ritte. (1994). Genetic variability and success in colonization in two intertidal mussels. In: Beaumont, A. R. (ed.), Genetic and evolution of aquatic organisms. New York: Chapman & Hall. pp. 168-176. Lavie, B. and E. Nevo. 1986. Genetic diversity of marine gastropods: contrasting strategies of Cerithium rupestre and C. scabridum in the Mediterranean Sea. Marine Ecology Progress Series 28: 99-103. Lee, C.E., 2002. Evolutionary genetics of invasive species. Trends in Ecology and Evolution 17: 386-391. Lipej, L., B. Mavrič, V. Žiža and J. Dulčić, 2008. The Largescaled terapon Terapon theraps: a new Indo-Pacific fish in the Mediterranean Sea. Journal of Fish Biology 73: 1819-1822. Lockwood, J. L., M. F. Hoopes and M. P. Marchetti. 2007. Invasion Ecology. Malden: Blackwell Publishing. 304 pp. Nevo, E., A. Beiles and R. Ben-Shlomo. 1984. The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In: Mani, G.S. (ed.), Evolutionary dynamics of genetic diversity. Berlin: Springer-Verlag. pp. 13-213. Por, F.D., 1978. Lessepsian migration – the influx of Red Sea biota into the Mediterranean by way of the Suez Canal. Berlin: Springer-Verlag. 228 pp.

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Rice, W. R. and D. Sax. 2005. Testing fundamental evolutionary questions at large spatial and demographic scales: Species invasions as an underappreciated tool. In: Sax, D.F., J.J. Stachowicz and S.D. Gaines (eds.), Species invasions: insights into ecology, evolution and biogeography. Sunderland: Sinauer Associates. pp. 291-308 Rilov, G., Y. Benayahu and A. Gasith. 2004. Prolonged lag in population outbreak of an invasive mussel: a shifting-habitat model. Biological Invasions 6: 347-364. Patarnello, T., F.A.M.J. Volckaert and R. Castilho. 2007. Pillars of Hercules: is the AtlanticMediterranean transition a phylogeographical break? Molecular Ecology 16: 4426-4444. Sakai, A.K., F.W. Allendorf, J.S. Holt, D.M. Lodge, J. Molofsky, K.A. With, S. Baughman, R.J. Cabin, J.E. Cohen, N.C. Ellstrand, D.E. McCauley, P. O‘Neil, I.M. Parker, J.N. Thomson and S.G. Weller. 2001. The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305-332. Safriel, U.N., A. Gilboa and T. Felsenburg. 1980. Distribution of rocky intertidal mussels in the Red Sea coasts of Sinai, the Suez Canal and the Mediterranean coast of Israel, with special reference to recent colonizers. Journal of Biogeography 7: 39-62. Sax, D. F. and J.H. Brown. 2000. The paradox of invasion. Global Ecology and Biogeography 9: 363-371. Shefer, S., A. Abelson, O. Mokady and E. Geffen. 2004. Red to Mediterranean Sea bioinvasion: natural drift through the Suez Canal, or anthropogenic transport? Molecular Ecology 13: 2333-2343. Sneh, A., T. Weissbrod and I. Perath. 1975. Evidence for an ancient Egyptian frontier canal. American Scientist 63 (5): 542-548. Steinitz, W. 1927. Beiträge zur Kenntnis der Küstenfauna Palästinas. I. Pubblicazioni della Stazione Zoologica di Napoli 8(3-4): 311-353. Terranova, M.S., S. Lo Brutto, M. Arculeo and J.B. Mitton. 2006. Population structure of Brachidontes pharaonis (P. Fisher, 1870) (Bivalvia, Mytilidae) in the Mediterranean Sea, and evolution of a novel mtDNA polymorphism. Marine Biology 150: 89-101. Tillier, J.E. 1902. Le Canal de Suez et sa faune ichthylogique. Mémoires de la Société zoologique de France 15: 279-318. Tsutsui, N.D., A.V. Suarez, D.A. Holway and T.J. Case. 2000. Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences of the U.S.A. 97: 5948-5953. Wares, J.P., A.R. Hughes and R.K. Grosberg. 2005. Mechanisms to drive evolutionary change: insights from species introductions and invasions. In: Sax D.F., J.J. Stachowicz and S.D. Gaines (eds.) Species invasions: insights into ecology, evolution and biogeography. Sunderland, Mass.: Sinauer Associates. pp. 229-257.

Red-Med immigration: a fish¶sitology perspective, (Eds.) with special D. Golani B. Appelbaum-Golani 2010 reference to the Myxosporea 85 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 85-97. © Pensoft Publishers Sofia–Moscow

Red-Med immigration: a fish parasitology perspective, with special reference to the Myxosporea Ariel Diamant INTRODUCTION The Suez Canal is viewed as a “filter” or “bottleneck” through which only a small fraction of the Red Sea fauna has managed to successfully pass and colonize the Mediterranean (“Red-Med” or “Lessepsian” immigration) (Por, 1978; Galil, 2000). The canal offers ecologists a unique opportunity to study invading marine organisms on a large-scale, biogeographical level. There are many unanswered questions regarding this phenomenon. Virtually all free living fish and invertebrates have parasites associated with them. Not much is known about the parasites naturally associated with immigrant Red Sea species and whether they are affected by the Red-Med “filter”. Few investigations have studied their fate following their host’s invasion and the factors governing their survival in their host’s new environment. What do we really know about the parasitological aspects of Red-Med fish immigration? In this short paper, we will briefly present the current knowledge on this fascinating aspect of the Suez Canal and present some new findings based on recent observations. DISCUSSION Parasites carried into a new environment are typically exposed to different, often unfavorable conditions and are likely to be as affected as their hosts. However, documented reports of parasites invading marine environments are relatively scarce (Torchin et al., 2003). Invading species typically ‘escape’ specific natural enemies (such as predators, or specific parasites), leaving them behind. It has been reasoned that in the new environment, a newly established population will be less burdened by their natural (old) enemies

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in the new habitat. This means they are less regulated and their competitiveness will be increased accordingly (Polyanski, 1961; Paperna, 1972). This is the basis for the so-called “enemy-release hypothesis” (Torchin et al., 2003), which has yet to be substantiated. The information currently available on the parasite fauna associated with Red-Med invertebrate species concerns only one species, the rhizocephalan Heterosaccus dollfusi that parasitizes the Red-Med portunid crab Charybdis longicollis (Galil and Innocenti, 1999). Invading fish hosts have been studied more thoroughly (see Paperna, 1972; Fischthal, 1980, 1982; Maillard and Raibaut, 1990; Pais et al., 2007). The most comprehensive parasitological data available on Red-Med immigrants is that of the rabbitfish, genus Siganus (family Siganidae) (Paperna, 1972; Ktari and Ktari, 1974; 1989b; Diamant, 1985; Diamant et al., 1999; Pasternak et al., 2007). The tendency of Red-Med immigrant fish to lose certain elements of their natural parasite fauna in the Mediterranean was observed by Paperna (1972) and Diamant (1989b, 1998). This process was thought to be regulated by the Suez Canal “filter” or “bottleneck”, (Por, 1978). How does this work? Does the canal in itself promote loss of parasites during the immigration process, or are they lost in the new environment? What is the restricting mechanism that enables only a subset of the original parasite assemblage to survive in the Mediterranean? Consider an invading fish population carrying its parasites into a new environment. We may envision the following hypothetical scenarios (Fig. 1); A. Loss of all parasites, yielding a “parasite free” host population; B. Loss of some of the parasites, maintaining a subset of the original parasite fauna; C. Retaining the entire (or nearly so) natural parasite assemblage; D. Acquiring autochthonous (local) parasites while maintaining a subset of the original parasite fauna, yielding a mixed assemblage; and E. Loss of entire original parasite fauna and acquisition of local species, producing a purely autochthonous parasite assemblage. The currently available data indicates that Siganus spp. have maintained a subset of their Red Sea parasites as well as acquired some autochthonous parasites (scenario D) (Diamant, 1989b; Diamant et al., 1999). As will be discussed in the next pages, rabbitfish in the Mediterranean essentially lost their Red Sea Digenea, Acanthocephala and Nematoda, while acquiring gnathiid isopods, the ciliate Cryptocaryon irritans and the the ciliate Cryptocaryon irritans and the digenean Hemiurus appendiculatus (see Fischthal, 1980; Diamant, 1989b; Diamant, 1999). What is the nature of the Suez Canal “filter” with regard to its effect on fish parasites? Clearly, the parasites are capable of surviving the passage through the canal together with their hosts. It may be expected that the effect on ectoparasites living in the mouth, gills, skin and other external surfaces will be more pronounced than on endoparasites, since the former would be equally exposed to any harsh extreme ambient conditions that their hosts encounter along the Canal. Endoparasites, on the other hand, have the advantage of living in the sheltered environment of the fish and are likely to be “buffered” from the external milieu to a much greater extent. Upon arrival of the host in the Mediterranean,

Red-Med immigration: a fish parasitology perspective, with special reference to the Myxosporea 87

A

Red Sea

B Mediterranean

C

D

E

Fig. 1. Schematic presentation of five theoretical scenarios resulting from an adult Red-Med immigrant fish population carrying its parasite assemblage into the Mediterranean. A. Gradual loss of all parasites, yielding a parasite free host population; B. loss of some of the parasites, but persisting with a reduced Red Sea parasite fauna; C. Maintaining the full (or nearly complete) Red Sea parasite assemblage; D. Shift in parasite composition to a mixed Red Sea/Mediterranean parasite assemblage; and E. Losing all Red Sea parasites and adopting purely autochthonous parasite species.

the key factors governing survival of its parasites seem to involve the degree of complexity of the parasitic life cycle. A parasite with a simple, monoxenous (single host) life cycle, i.e., requiring only a suitable fish for survival, is more likely to survive in the long run. Conversely, heteroxenous parasites possessing multiple-host life cycle strategies and thus requiring in addition to the fish at least one or more hosts (normally invertebrates) are clearly at a disadvantage. As only a small percentage of Red Sea organisms have in fact immigrated into the Mediterranean, a heteroxenous parasite’s requirement for a series of hosts would be a distinct disadvantage. This fundamental difference in the natural history of the parasitic development has great significance in terms of parasite capacity to co-establish in its host’s new biogeographic region. Generally speaking, monoxenous fish parasites are usually ectoparasitic, predominantly infecting the skin and gills of their hosts (e.g. monogeneans and most parasitic crustaceans). On the other hand, heterox-

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enous fish parasites tend to be endoparasitic, inhabiting internal organs, body cavities and tissues (e.g. gut helminths and myxosporeans). Nevertheless, some internal forms are monoxenous (e.g. gut Protozoa). Rabbitfish are medium-sized, tropical marine species, inhabiting coral reefs and shallow sandy habitats. In the Red Sea, these fish are amongst the few herbivorous reef fish living in the coastal ecosystems (Bouchon-Navaron and Harmelin-Vivien, 1981). Two of the four Red Sea rabbitfish species, Siganus rivulatus and S. luridus, have been immensely successful in colonizing the eastern Mediterranean. S. rivulatus has for decades been one of Israel’s most common inshore fish, while S. luridus is less common, abounding mainly in the country’s northern coast (Golani et al., 2002). In a recent study, the mitochondrial cytochrome-b marker between Mediterranean and Red Sea Siganus populations was compared. The results showed that the genetic structure of the populations was identical. The authors concluded that immigration of these fish is either an ongoing, continuous process or that invasion of the Mediterranean initially involved a large number of colonist individuals (Bonhomme et al., 2003; Azzurro et al., 2006). Using parasitological data, Diamant (1998) concluded that invasion of the Mediterranean by Siganus spp. had to involve grown fish, probably actively swimming individuals (rather than passively swept planktonic larvae). Analyses of the parasite assemblages of Mediterranean populations of S. rivulatus and S. luridus have shown that with the exception of one group (Myxosporea, dealt with in more detail later on), predominantly monoxenous parasite species occur on these fish in their newly adopted biogeographic region (Diamant, 1989b; Diamant et al., 1999). In the Red Sea, rabbitfish harbor a rich, diverse parasite fauna that includes skin, gill, muscle and a variety of internal parasites. These include Microsporidia, Apicomplexa, Ciliophora, Sarcodina, Mastigophora, Myxosporea, Monogenea, Copepoda, Isopoda and Hirudinea, (Diamant, 1985). Eight species of Digenea, Acanthocephala and Nematoda have been recorded from the alimentary tract of Eilat rabbitfish: Opisthogonoporoides hanumanthai, Opisthogonoporoides sp., Hexangium sigani, Gyliauchen sp., Prosorchis sp., Sclerocollum rubrimaris, Procamallanus elatensis and Cucullanus sigani. Some of these have been studied in detail (Diamant and Paperna, 1985; 1992; Diamant, 1989a; Diamant et al., 1999; Dzikowski et al., 2003). However, it should be emphasized that the life cycle details of these heteroxenous species are still unknown. All are noticeably absent from the Mediterranean rabbitfish (Diamant, 1985; Diamant, 1989b; Diamant et al., 1999). I would like to shift focus now to the Myxosporea, a parasite group which is found on immigrant rabbitfish and is particularly intriguing. This parasitic class contains species which are common parasites of fish and have been shown to possess heteroxenous life cycles. Surprisingly, representatives of the group occur also in Mediterranean rabbitfish. Who are these curious parasites that do not conform to the heteroxenous/monoxenous Red-Med “filter” assumption? Myxosporeans are microscopic organisms which until 20 years ago were classified as protists. The class Myxosporea belongs to the phylum Myxozoa, a group of 62 genera

Red-Med immigration: a fish parasitology perspective, with special reference to the Myxosporea 89

and 2180 known species, parasites of aquatic hosts, mainly fish (Lom and Dykova, 2006). While most are innocuous, some are highly pathogenic in cultured and wild fish stocks. Accordingly, the group has significance in aquaculture and catch fisheries. As a result of a milestone discovery made by Wolf and Markiw (1984), the first full life cycle of a myxosporean, Myxobolus cerebralis, was elucidated. In M. cerebralis, a parasite of rainbow trout, a requirement was demonstrated for an oligochaete host for completion of the parasitic life cycle. The developmental stage in the annelid host was found to “belong” to a group of animals previously known as Actinosporea and considered a distinct protist group. Of course, the genetic link between the two groups and the observation that they are in fact two stages in the life cycle of the same organism was a significant step forward in the understanding of the biology of these parasites. Subsequently, using SSU sequence analysis, 30 additional freshwater species of piscine myxosporeans were shown to include in their development a non-piscine (actinosporean) stage of the parasite, thus elucidating their full life cycles. In all cases, the invertebrate host was an annelid (usually an oligochaete), and as a result, the two “classes”, Myxosporea and Actinosporea have been relocated into the same Phylum, Myxozoa (Kent et al., 2001). Recently, a similar life cycle scheme was demonstrated also in a marine myxosporean species, involving a goby (Gobiidae) and polychaete worm (Køie et al., 2004). The Myxosporea, by definition, are categorized as heteroxenous parasites, possessing a multiple-host life cycle. It should be noted that, to date, the precise phylogenetic position of the Myxozoa, albeit related to the Cnidaria, remains inconclusive. Accurate identification of Myxozoan species is limited by the relative simplicity of spore morphology features, and such characteristics usually cannot be applied to actinosporean developmental stages of the same species (Kent et al., 2001). As a result, molecular phylogeny analyses are being increasingly employed to advance the taxonomy and evolution of the group (Holzer, 2004; Fiala, 2006). The application of molecular probes in in situ hybridization protocols has also enabled tracking of the route of infective stages of Myxosporea from port of entry to their target organs in the fish (e.g. Holzer et al., 2003). At least 4 Myxosporean species are known to infect Red Sea rabbitfish. Three are coelozoic, i.e. invade body cavities in their host: Zschokkella icterica (Figs. 2, 3) parasitizes the hepatic bile ducts and gall bladder: Ceratomyxa spp. (Figs. 4, 5) parasitize the gall bladder; and Ortholinea sp. (Figs. 6-8) parasitizes the urinary bladder. A fourth species, Kudoa iwatai, is histozoic, i.e., invading a variety of tissues, including muscle, brain, eye and visceral organs (Fig. 9) (see Diamant, 1985; Diamant and Paperna, 1992; Diamant et al., 1999; Diamant et al., 2005). The first three species Ceratomyxa sp., Z. icterica and Ortholinea sp. have been detected in Mediterranean rabbitfish (Diamant, 1985; Diamant 1989b; Diamant et al., 1999). Among these, Ceratomyxa sp. is by far the commonest (Diamant et al., 1999), while Kudoa iwatai has so far not been detected in the Mediterranean. It should be noted that this parasite is common in gilthead sea bream (Sparus aurata) introduced and cultured in the Red Sea (see Diamant et al., 2005), but it has not yet been recorded from gilthead sea bream cultured in the Mediterranean,

90 Ariel Diamant

3

2

4

5

Figs. 2-3. Zschokkella icterica paraffin section of liver of Siganus luridus from the Gulf of Eilat, Red Sea. Fig. 2. Dilated hepatic bile ducts packed with polysporous plasmodia (P); L – Liver parenchyma; Gram stain, Bar = 100μm. Fig 3. Higher magnification of the same slide, showing bipolar spores (H – host biliary endothelium). Bar = 30μm. Figs. 4-5. Ceratomyxa sp. in fresh bile from the gall bladder of Siganus rivulatus from the Gulf of Eilat, Red Sea. Fig. 4, plasmodia; Fig 5. spores; Both Nomarski interference microscopy; Bars = 20μm.

which could well happen in the future (i.e., parasite introduction through transfer of mariculture stocks). The necessity of passing through the actinosporean stage for completion of the life cycle means that such stages must occur. Although actinosporeans are known to occur both in marine oligochaetes (Roubal et al., 1997; Hallett et al., 1998) and nereid

Red-Med immigration: a fish parasitology perspective, with special reference to the Myxosporea 91

polychaetes (Køie, 2000; Køie et al., 2004), they have not yet been found in the Red Sea, despite considerable search efforts carried out during 2002-2005 (EU-FP5 MYXFISHCONTROL, unpublished data). This is quite amazing, in view of the great abundance of myxosporean infections in the Red Sea (see Diamant et al., 1999; Diamant et al., 2004; Diamant et al., 2007) and a rich, diverse fauna of polychaetes and oligochaetes that may act as their potential intermediate hosts. Myxozoa have hitherto been largely overlooked as invading parasites and not been duly investigated. For example, in a recent chapter covering the topic of introduced marine parasites (Torchin and Kuris, 2005), the phylum is not even mentioned. Nevertheless,

6

8

7

9

Figs. 6-8. Ortholinea sp. in the urinary bladder of S. rivulatus in the Gulf of Eilat, Red Sea (H – host urinary bladder endothelium). Spores are spherical, with a diameter of approximately 8 μm. Fig. 6, Paraffin section, Gram stain, Bar = 10μm; Figs. 7 and 8, Nomarski interference microscopy, Bars = 10μm. Fig. 9. Kudoa iwatai spores released from a plasmodium lodged in the cranial adipose tissue of S. rivulatus in the Gulf of Eilat, Red Sea. Nomarski interference microscopy; Bar = 10μm.

92 Ariel Diamant

these small organisms are important ecological indicators. But, how certain are we that we are dealing with the same myxosporean species found in rabbitfish of both seas? Zschokkella icterica and Ortholinea sp. display high host specificity and have never been documented in any other fish hosts. In fact, both are specific to such a degree that they have a high affinity to particular species of Siganus (Z. icterica to S. luridus and Ortholinea sp. to S. rivulatus). As the SSU r-DNA genes of both species have been sequenced from Red Sea rabbitfish in our lab (Z. icterica, 1907 bp, Genbank DQ333434; Ortholinea sp., 1950 bp, Genbank DQ333433), a comparison with parasite samples sequenced from Mediterranean-collected rabbitfish could provide a fairly conclusive answer; however, this comparison has yet to be conducted. As far as Ceratomyxa is concerned, this is a ubiquitous genus with numerous undescribed species and the Genus is regarded as having overall low specificity. Thus, Ceratomyxa infections observed in Mediterranean rabbitfish may easily include locally acquired autochthonous species. Nevertheless, we have conducted a comparison of SSU r-DNA sequences of Ceratomyxa collected from Mediterranean S. rivulatus with those from Red Sea S. rivulatus and the results suggest that they are identical (Ceratomyxa sp., 1705 bp, Genbank DQ 333429 + one non-submitted sequence of isolate found in S. rivulatus in both Mediterranean and Red Sea, as well as in 4 additional wild Red Sea hosts) (A. Diamant and A. Lipshitz, unpublished data). It is interesting to note here another phenomenon that is associated with the rabbitfish and its myxosporean parasites. This regards the occurrence of a hyper-parasite, Nosema ceratomyxae (Order Microsporida) that invades the plasmodia of Ceratomyxa sp. in the gall bladder of S. rivulatus in the Red Sea (Fig. 10) (Diamant and Paperna, 1985, 1989). This species has been found repeatedly to hyperparasitize Ceratomyxa in S. rivulatus in the Mediterranean (Figs.11, 12), which would suggest that it co-invaded the Mediterranean together with both rabbitfish and myxosporean hosts. The nature of the myxosporean-rabbitfish relationship is still largely obscure. The specific life cycle details of the myxosporean parasites of rabbitfish parasites have not been elucidated. Ceratomyxa sp. infections are detected in the gall bladders of juvenile rabbitfish living in shallow Red Sea coastal waters, very early on in their development (Diamant, 1985). The demersal nature of the fish brings them in close contact with benthic invertebrates. Infection levels are high, with Ceratomyxa sp. prevalence in the Gulf of Eilat (Red Sea) approaching 100% (Diamant et al., 1999). Concurrent infections of two and even three of the myxosporean species in the same host fish individual have been observed (A. Diamant, unpublished data). When and how the initial Myxosporean-host contact takes place is unknown. The question remains: how is the presence on Mediterranean rabbitfish of not one, but three Red Sea myxosporeans, consistent with the putative heteroxenous life cycle of the parasite? Is it possible that the intermediate hosts of these species (presumably annelids) have co-invaded the Mediterranean? Alternatively, are the myxosporeans perhaps employing autochthonous (annelid?) species as intermediate hosts? Either way, an assumed heteroxenous life cycle could be completed.

Red-Med immigration: a fish parasitology perspective, with special reference to the Myxosporea 93

10

11

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Figs. 10-12. Nosema ceratomyxae in S. rivulatus gall bladder. Fig. 10 shows developing stages of the hyperparasite (arrows) in plasmodia (P) of Ceratomyxa attached to the biliary endothelium (H) of gall bladder in fish from the Red Sea (Eilat). Transmission electron micrograph, uranyl acetate and lead citrate stain, Bar = 5μm. Figs. 11 and 12 show live spores in fresh bile in an individual from the Mediterranean (Ashdod Harbor); Nomarski interference microscopy; Bars = 10μm.

94 Ariel Diamant

An alternative explanation could be that the myxosporeans are reproducing in the Mediterranean without intermediate hosts, i.e. by transmitting directly from fish to fish. Fish-to-fish transmission in Myxosporea has been demonstrated in at least 3 species (Diamant, 1997; Redondo et al., 2002; Yasuda et al., 2002) and suspected in an additional one (Swearer and Robertson, 1999). In other parasite taxa, studies have shown that truncation of the life cycle by eliminating one or more hosts from a heteroxenous life cycle, is possible (Poulin and Cribb, 2002; Levsen and Jakobsen, 2002). Indeed, the ability to transmit directly from one fish to another could well be an indispensable preadaptation for successful fish parasite colonization of a newly encountered habitat. Thus, the Red-Med immigrant myxosporeans may theoretically represent a case of parasite survival through life cycle truncation. However, since we have no hard evidence to support any of the above speculative scenarios, they must remain theoretical and we await evidence from future studies. CONCLUSIONS We are only beginning to comprehend the complex effects of Red-Med immigration on the Mediterranean ecosystem. As parasites are abundant and constitute a key component of natural marine communities, natural parasites associated with immigrant fish are likely to have considerable ecological impact. At present, there is still very limited hard data available in this area. Thus it is impossible to make any comprehensive statements. Additional research is needed to evaluate what factors govern the composition and infection levels of parasites in Red-Med immigrant fish, and how these affect local communities. A possible explanation for the unexpected colonization success of RedMed immigrant fish parasite species belonging to the class Myxosporea, despite their putative complex life cycles, is discussed. As a rule of thumb, the currently available data suggests that parasites with complex requirements, e.g. possessing a heteroxenous life cycle, are likely to have diminished chances of successful persistence on a host population in a newly adopted environment, and thus, it is predicted that, as a group, monoxenous parasite species will have significantly more ecological impact on the Mediterranean in the foreseeable future. ACKNOWLEDGEMENTS I thank Asaf Lipshitz, Yariv Shtupler and Sharon Ram, who during different periods in the lab assisted in collecting, processing, analyzing and discussing Myxozoan parasites in wild and cultured fish.

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REFERENCES Azzurro, E., D. Golani, G. Bucciarelli and G. Bernardi. 2006. Genetics of the early stages of invasion of the Lessespian rabbitfish Siganus luridus. Journal of Experimental Marine Biology and Ecology 333: 190-201. Bonhomme, F., A. Baranes, D. Golani and M. Harmelin-Vivien. 2003. Lack of mitochondrial differentiation between Red Sea and Mediterranean populations of the Lessepsian rabbitfish, Siganus rivulatus (Perciformes: Siganidae). Scientia Marina 67: 215-217. Bouchon-Navarro, Y. and M. L. Harmelin-Vivien. 1981. Quantitative distribution of herbivorous reef fishes in the Gulf of Aqaba (Red Sea). Marine Biology 63: 79-86. Diamant, A. 1985. Biology of the parasites of Siganus spp. (Teleosti: Siganidae) from the Northern Red Sea and Eastern Mediterranean coasts of Israel. PhD Thesis presented to the Senate of the Hebrew University of Jerusalem (in Hebrew, English summary).160 pp. Diamant, A. 1989a. Ecology of the acanthocephalan Sclerocollum rubrimaris Schmidt and Paperna, 1978 (Rhadinorhynchidae: Gorgorhynchinae) from wild populations of rabbitfish (Genus Siganus) in the northern Red Sea. Journal of Fish Biology 34: 387-398. Diamant, A. 1989b. Lessepsian migrants as hosts: a parasitological assessment of rabbitfish Siganus luridus and Siganus rivulatus (Siganidae) in their original and new biogeographical regions. In: Spanier, E., Y. Steinberger and M. Luria. (eds.), Environmental quality and ecosystem stability, Vol. IV-B, Environmental Quality. Jerusalem, ISEEQS Pub., pp. 187-194. Diamant, A. 1997. Fish to fish transmission of a marine myxosporean. Diseases of Aquatic Organisms 30: 99-105. Diamant, A. 1998. Parasitological aspects of Red-Med fish migration. In: Actes du Colloque Scientifique, Proceedings of the International Colloquium. OCEANOS. Montpellier (April 11-12, 1996). pp. 175-178. Diamant, A. and I. Paperna. 1985. The development and ultrastructure of Nosema ceratomyxae sp. nov. (Microsporidae), a hyperparasite of the myxosporean Ceratomyxa sp. from siganid fishes in the Red Sea. Protistologica 21: 249-258. Diamant, A. and I. Paperna. 1989. Cytopathology of Ceratomyxa sp. (Myxosporea) hyperparasitized by the microsporidan Nosema ceratomyxae. Diseases of Aquatic Organisms 6: 75-79. Diamant, A. and I. Paperna. 1992. Zschokkella icterica sp. nov. (Myxozoa, Myxosporea) a pathogen of wild rabbitfish Siganus luridus (Ruppell, 1829) from the Red Sea. European Journal of Protistology 28: 71-79. Diamant, A., A. Banet, I. Paperna, H. von Westernhagen, K. Broeg, G. Kruener, W. Koerting and S. Zander. 1999. The use of fish metabolic, pathological and parasitological indices in pollution monitoring. II. The Red Sea and Mediterranean. Helgoland Marine Research 53: 195-208 Diamant, A., C. M. Whipps and M.L. Kent. 2004. A new species of Sphaeromyxa (Myxosporea: Sphaeromyxina: Sphaeromyxidae), in Devil Firefish, Pterois miles (Scorpaenidae), from the northern Red Sea: morphology, ultrastructure and phylogeny. Journal of Parasitology 90: 1434-1442. Diamant, A., M. Ucko, I. Paperna, A. Colorni and A. Lipshitz. 2005. Kudoa iwatai (Myxosporea: Multivalvulida) in wild and cultured fish in the Red Sea: re-description and molecular phylogeny. Journal of Parasitology 91: 1175-1189.

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Diamant, A., A. Lipshitz and M.Ucko. 2007. Phylogeny of Coccomyxa (Myxosporea: Myxidiidae) spp. from littoral fish in Eilat, northern Red Sea, with the description of a new species. Folia Parasitologica 54: 109-116. Dzikowski, R., I. Paperna and A. Diamant. 2003. Transitions in parasite communities of the rabbitfish (Siganus rivulatus) in a changing Red Sea coastal environment – a long-term perspective. Helgoland Marine Research 57: 228-235. Fiala, I. 2006. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36: 1521-1534. Fischthal, J.H. 1980. Some digenetic trematodes of marine fishes from Israel’s Mediterranean coast and their biogeography, especially those from Red Sea immigrant fishes. Biologia Scripta 9: 11-23. Fischthal, J. H. 1982. Additional records of digenetic trematodes of marine fishes from Israel’s Mediterranean coast. Proceedings of the Helminthological Society, Washington 49: 34-44. Galil, B.S. 2000. A sea under siege –alien species in the Mediterranean. Biological Invasions 2: 177-186. Galil, B. S. and G. Innocenti. 1999. Notes on the population structure of the portunid crab Charybdis longicollis Leene parasitized by the rhizocephalan Heterosaccus dollfusi Boschma, off the Mediterranean coast of Israel. Bulletin of Marine Science 64: 451-463. Golani, D., L. Orsi-Relini, E. Massuti and J.-P.Quignard. 2002. CIESM atlas of exotic species in the Mediterranean. Vol. 1. Fishes. Briand, F. (ed.), Monaco: CIESM Publishers. 254 pp. Hallett, S.L., P.J. O’Donoghue and R.J.G. Lester. 1998. Structure and development of a marine actinosporean Sphaeromyxon ersei n. sp. (Myxozoa). Journal of Eukaryotic Microbiology 45: 142-150. Holzer, A.S., C. Sommerville and R. Wootten. 2003. Tracing the route of Sphaerospora truttae from the entry locus to the target organ of the host, Salmo salar L., using an optimized and specific in situ hybridization technique. Journal of Fish Diseases 26: 647-55. Holzer A.S., C. Sommerville and R. Wootten. 2004. Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal for Parasitology 34: 1099-111. Kent, M.L., K.B. Andree, J.L. Bartholomew, M. El-Matbouli, S.S. Desser, R.H. Devlin, S.W. Feist, R.P. Hedrick, R.W. Hoffmann, J. Khattra, S.L. Hallett, R.J.G. Lester, M. Longshaw, O. Palenzeula, M.E. Siddall and C.X. Xiao. 2001. Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48: 395-413. Køie, M. 2000. First record of an actinosporean (Myxozoa) in a marine polychaete annelid. Journal of Parasitology 86: 871-872. Køie, M., C.M. Whipps and M.L. Kent. 2004. Ellipsosoma gobii (Myxozoa: ceratomyxidae) in the common goby Pomatoschistus microps (Teleostei: Gobiidae) uses Nereis spp. (Annelidae: Polychaeta) as invertebrate hosts. Folia Parasitologica 51: 14-18 Ktari, F. and M.H. Ktari. 1974. Presence dans le golfe de Gabes de Siganus luridus (Rüppel, 1829) et de Siganus rivulatus (Forsskal, 1775). (Poissons, Siganidae), parasites par Pseudohaliotrematoides polymorphus. Bulletin de l’Institute et Technique d’Oceanographique et de Peche de Salammbô 3: 95-98. Levsen, A. and P.J. Jakobsen. 2002. Selection pressure towards monoxeny in Camallanus cotti (Nematoda, Camallanidae) facing and intermediate host bottleneck situation. Parasitology 124: 625-629.

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Lom, J. and I. Dyková. 2006. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53: 1-36. Maillard, C. and A. Raibaut. 1990. Human activities and modification of ichthyofauna of the Mediterranean Sea: effect on parasitosis. In: di Castri, E., A.J. Hansen and M. Debussche (eds.), Biological invasions in Europe and the Mediterranean basin. Dordrecht: Kluwer Academic Publishers. pp. 297-305. Pais, A., P. Merella, M.C. Follesa and G. Garippa. 2007. Westward range expansion of the Lessepsian migrant Fistularia commersonii (Fistulariidae) in the Mediterranean Sea, with notes on its parasites. Journal of Fish Biology 70: 269-277. Paperna, I. 1972. Parasitiological implications of fish migration through interoceanic canals. 17e Congrèss International de Biologie (Monte-Carlo 25-27 Septembre 1972). Theme Nº 3: Les consequences biologiques des canaux inter-océans. 9 pp. Pasternak, Z., A. Diamant and A. Abelson. 2007. Co-invasion of a Red Sea fish and its ectoparasitic monogenean, Polylabris cf. mamaevi into the Mediterranean: observations on the oncomiracidium behavior and infection levels in both seas. Parasitology Research 100: 721-727. Polyanski, Y.I. 1961. Ecology of parasites in marine fishes. In: Dogiel, V.A., G.K. Petrushevski, Y.I. Polyanski (eds), Parasitology of fishes, Edinburgh: Oliver and Boyd. pp. 230-245. Por, F.D. 1978. Lessepsian migration: the influx of Red Sea biota into the Mediterranean by way of the Suez Canal. Ecological Studies, 23. Berlin: Springer-Verlag. 228 pp. Poulin R. and T.H. Cribb. 2002. Trematode life cycles: short is sweet? Trends in Parasitology 18: 176-183. Redondo, M. J., O. Palenzuela, A. Riaza, A. Macias and P. Alvarez-Pellitero. 2002. Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. Journal of Parasitology 88: 482-488. Roubal, F.R., S.L. Hallett and R.J.G. Lester. 1997. First record of Triactinomyxon actinosporean in a marine oligochaete. Bulletin of the European Association of Fish Pathologists 17: 83-85. Swearer S.E. and D.R. Robertson. 1999. Life history, pathology, and description of Kudoa ovivora n. sp (Myxozoa, Myxosporea): An ovarian parasite of Caribbean labroid fishes. Journal of Parasitology 85: 337-353 Torchin, M.E., K.D. Lafferty, A.P. Dobson, V.J. McKenzie and A.M. Kuris. 2003. Introduced species and their missing parasites. Nature 421: 628-630. Whipps, C.M., G. Grossel, R.D. Aadlard, H. Yokoyama, M.S. Bryant, B.L. Munday and M.L. Kent. 2004. Phylogeny of the Multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. Journal of Parasitology 90: 618-622. Wolf, K. and M.E. Markiw. 1984. Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225: 1449-1452 Yasuda, H., T. Ooyama, K. Iwata, T. Tun, H. Yokoyama and K. Ogawa. 2002. Fish-to-fish transmision of Myxidium spp. (Myxozoa) in cultured tiger puffer suffering from emaciation disease. Fish Pathology 37: 29-33.

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UnusualD.occurrences ofAppelbaum-Golani fish in the Mediterranean Golani & B. (Eds.) Sea: 2010an insight into early detection 99 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 99-126. © Pensoft Publishers Sofia–Moscow

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection Ernesto Azzurro

INTRODUCTION Field observations and records of new and “rare” fishes are intensifying in the Mediterranean Sea, as well as in other marine systems. These unusual occurrences may testify to substantial extensions of species’ geographical ranges and this has been demonstrated for several exotic fishes that have already established themselves in the Mediterranean and are now spreading further in their new environment. Changes in the distributional patterns are also exemplified by a number of native species with tropical or subtropical affinity which are moving towards the northern and colder sectors of the Mediterranean. These changes in the distributional patterns of both exotic and indigenous Mediterranean fishes have recently astonished the scientific community due to their speed and increasing importance. In most cases the direct and indirect consequences of climate variation have been cited as causative factors of this phenomenon that appears to favor the movements and the success of the warm-water biota, especially of marine fishes. The observation of a new species in a new area represents the first (and sometimes the only) opportunity to follow and to study the dynamics of colonization. Obviously it is important to know, even approximately, when and where the propagules arrive and if and when colonization starts, but the chances of a newcomer to be discovered rapidly depends on a number of factors and, at the beginning, research opportunities are usually limited. Monitoring the spread of what we will define as “unusual occurrences” is crucial to understand how a new species arrives, what are its movements and developments and the impact that it may have. This knowledge is particularly necessary to face the problem of exotic fishes but, up to now, information on the biology and the ecology of these newcomers (if available) is limited to those geographical sectors where the species has historically settled. In contrast, information regarding marginal populations, reaching or even trespassing their specific distribution ranges, is scarce and particularly difficult to obtain.

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Concern has been expressed at the lack of monitoring, coordination, and study in relation to the discovery of new exotic species and of their subsequent spread. In this regard, early monitoring of colonizing populations and even sporadic captures of pioneering individuals constitute a valuable and underexploited opportunity for the sake of biological invasion research. Therefore, this chapter focuses on how to detect and to report these observations in an attempt to ameliorate our capacity to keep informed about the changing biodiversity. A primary aim is to give some insights on the difficulties and perspectives of the study of exotic fishes from a multidisciplinary approach. Special focus is placed on the early stages of invasion and, of course, to the Mediterranean system. Multifaceted views of this phenomenon are considered and some practical suggestions on how detection of these early invaders could be conceived, planned and organized are proposed here, by taking into account some case studies. Perspectives of study are then explored by considering empirical evidence and the theoretical context. Contemporary trends of change in Mediterranean fish biodiversity cover large geographical scales, beyond the limits of any single nation state and involving an increasing number of scientists from different disciplines. For this reason, the chapter is mainly intended for those researchers that approach this phenomenon for the first time and have the opportunity to document it. In many cases, the “story” begins when an “uncommon” fish, never captured before, find its way in the hands of a specialist or even of a non-specialist, who is simply interested in it. A CHANGING ICHTHYOFAUNA Current patterns of change The recent breaching of some major biogeographical and ecological barriers combined with modern climate change are reshuffling the geographic distributions of plant and animal species world-wide (Parmesan and Yohe, 2003), enhancing the spreading of new species into new environments (Mearns, 1988; Perry et al., 2005). The acceleration and magnitude of this phenomenon is well illustrated within the Mediterranean system (Galil, 2007; Bianchi, 2007), especially by fish communities (Quignard and Tomasini, 2000; Azzurro, 2008; Ben Rais Lasram and Mouillot, 2009). Within the Mediterranean, two general and wide-scale phenomena can be recognized today (Fig. 1): (A) The incoming of new exotic species; (B) The change of species distributions. Clearly the first process is ultimately linked with the second one since the incoming of a new species in a new area represents itself a change in its geographical range. Moreover, once arrived and established in a certain location, the same species is expected to expand its distribution. As far as the incoming of exotic fish is concerned, this is a non-stop, ongoing process which today has reached the recorded number of 116 non-native fish species (see

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 101

CIESM web atlas at: http://www.ciesm.org/atlas/appendix1.html), constituting more than 16% of the entire Mediterranean ichthyofauna. The influx of these species is linked to two main routes: Atlantic waters provide new species to the Mediterranean through the Straits of Gibraltar, continuing an historical process started during the interglacial phases of the Quaternari, while Red Sea species are entering through the Suez Canal, giving shape to the Lessepsian phenomenon (Por, 1978).These two routes of migration act on very different time scales, but both are thought to have enormously accelerated in the last two decades, with an increase of 20% within only four years (Golani et al., 2007a). Other invasion pathways linked to direct human activity such as ship-mediated transport and mariculture are considered of minor importance for fish species. After entering the Mediterranean, exotic fishes may establish self-maintaining populations and subsequently spread into other sectors, possibly altering the structure and the ecology of indigenous communities. Recent substantial range extensions have been summarized by Golani et al. (2007a). According to this review, a number of Lessepsian species are extending westwards, whilst other Atlantic invaders such as Seriola fasciata are moving into the opposite direction, reaching the eastern basin. Considering that nearly all the exotic species that enter the Mediterranean are of tropical origin, various authors have defined the process of entrance and spread of these organisms as ‘tropicalization’ (Andaloro and Rinaldi, 1998; Bianchi and Morri, 2004; Bianchi, 2007). Another definition that has been used is “demediterranization”(Quignard and Tomassini, 2000), if we want to put the emphasis on the process of biotic homogenization of the Mediterranean1 Sea. The geographical expansion of these species has been often explained by the direct or indirect effects of climatic variation (e.g. Astraldi et al., 1995; Bianchi and Morri, 2004; Francour et al., 1994; Dulčić et al., 1999; Dulčić and Grbec, 2000; Bianchini and Ragonese, 2007) being the linkage between climate change and distribution shifts in marine fishes more and more evident today (Perry et al., 2005). Climate change may directly influence individuals, populations and communities through the individuals’ physiological and behavioral responses to environmental changes. Fish are particularly sensitive to temperature, in fact water temperature warming may alter metabolism, behavior, patterns of resource use, reproductive success and generate active movement and migratory patterns (Roessig et al., 2004). On the other hand, indirect effects, mediated by changing currents, are extremely important and may affect larval dispersal, retention and recruitment (Bianchi and Morri, 2004). Exotic species are not the only species showing rapid geographical expansion2. In the last decade the northward spread of indigenous fishes of tropical and subtropical affinity has been a noticeable trend as well (Azzurro, 2008). The counterpart is represented by the process of regression of fish species with boreal affinity (Quignard and Tomassini, 2000). Climate variation is apparently modifying the distribution patterns of Mediterranean Sea biodiversity (Bianchi, 2007 and references therein included) favoring the occurrence and 1 2

.. which is leading to the loss of its faunistic identity. The counterpart is represented by the process of regression of fish species with boreal affinity (Quignard and Tomassini, 2000)

102 Ernesto Azzurro

establishment of warm-water species, whether exotic or native. For this reason some authors include in the concept of tropicalization also the movements of indigenous species (Bianchi, 2007) which are largely illustrated by a series of new presence records (Francour et al., 1994). Species as the parrotfish Sparisoma cretense (Guidetti and Boero, 2001) and the wrasse Thalassoma pavo (Vacchi et al., 1999, 2001; Guidetti et al., 2002; Sara and Ugolini, 2001), are the most cited examples. However there are also many other species, typical of the southern sectors of the Mediterranean, that have been recently recorded in the northern and colder sectors of the Mediterranean. By reviewing the relevant literature of the last 15 years, Azzurro (2008) listed 51 species occurring northwards with respect to their known distribution limits in the Mediterranean Sea. Among them, 34 native and 17 exotic (6 Atlantic and 11 Lessepsian) fish were counted and nearly all have been

B

A

Fig. 1. Current patterns of change in the Mediterranean fish biodiversity are here exemplified by two key species: A. “Tropicalization” or even “demediterranization” is the process caused by the incoming and spread of exotic species with tropical or subtropical origin such as the Dusky Spinefoot, Siganus luridus. Some authors are inclined to include within the concept of “tropicalization” also the concept of “Meridionalization” B. “Meridionalization” is the northward spread of Mediterranean indigenous thermophilic species (against the recession of boreal ones). This is the case of the Mediterranean parrotfish, Sparisoma cretense which is typical of the southern sectors of the Mediterranean. (Photo by E. Azzurro)

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 103

categorized as thermophilic. As a matter of fact, many of these north-expanding fish have extended their distribution margins also in other marine areas of the world, showing an astonishing coherence in their spread. This is the case of species such as Epinephelus marginatus; Caranx crysos; Balistes capriscus; Pseudocaranx dentex; Solea senegalensis; Sphyraena spp. Other warm water fishes such as the Round Sardinella, Sardinella aurita are increasing in abundance (Sabates et al., 2006) and species that had difficulty reproducing in the north, such as the Dusky Grouper Epinephelus marginatus and the Ornate Wrasse Thalassoma pavo (Francour et al., 1994; Sara and Ugolini, 2001) are now established and seasonal recruitment occurs in these areas. This success and geographical expansion of native warm water biota has been called by some authors “meridionalization” (Bianchi and Morri, 1993, 1994; Riera et al., 1995), since the main participants of this phenomenon are “meridional” species, typical of the southern sectors of the Mediterranean (Fig. 1). As a result of these complex phenomena of biodiversity changes, an increasing number of “unusual” fishes, both of native and exotic origin, are now appearing in new sectors of the Mediterranean, stressing the need for specific studies and ongoing monitoring. The arrival of new species in these areas raises obvious concern on the ecological and economic impact that such migrants may have and solicits the need of knowledge. Up to now the research on exotic fish species in the Mediterranean has been limited to those areas where the species have historically established and where they occur in high abundance. If we look at the Lessepsian fishes, it is clear that these invaders have been studied almost exclusively in the Levantine Sea. With some exceptions (i.e. Azzurro et al., 2006, 2007a, b; Kalogirou et al., 2007) the colonization fronts are poorly known and all we know about the exotic fishes along their marginal areas is limited to mere presence records. PRESENCE RECORDS The “unusual” fish According to Schreck and Moyle (1990), the process of research should be “a systematic and orderly process by which new knowledge or information is obtained in accordance with specified objectives”. As pointed out by the Authors, the definition excludes sole reliance on casual observation and chance discovery. However, in the field of biological invasions, there are circumstances in which discovery is offered by casualty and accessible information does not extend beyond the descriptive stage. This is the case of the accidental captures of organisms outside of their natural range. Commonly, after being captured, these specimens may find their way into a museum, in fishery magazines, in a newspaper (Fig. 2) or even in a web page, but in some cases their capture is considered so extraordinary as to deserve a scientific publication. Scientific journals contains a vast array of records of “unusual” fishes and other organisms. These records can be defined as single observation of one or more specimens

104 Ernesto Azzurro

Fig. 2. On the left, a newspaper reporting the “unusual” capture of Spheroides pachigasters in Sicilian waters. On the right, presence records published in peer reviewed journals.

of a single species at a single date and location (Mearns, 1988) and appear usually in the form of notes or brief articles (Fig. 2). Records may be focused on exotic organisms, on deep or rare species or even on individuals characterized by particular attributes, such as extreme sizes or albinism. Being interested on exotic fishes and in distributional changes, our attention will be restricted to those records of organisms which have been found outside of their natural range. In this case, it is not the specimen itself that is rare (in fact, it is usually abundant elsewhere), rather it is its occurrence at a particular place and time to be noteworthy. To detect and to report these observations is a primary challenge of bio invasion research. If by chance one of these rare captures crosses our path, we should keep in mind that this episode could represent a first opportunity to document the occurrence of a new invasive phenomenon or to give evidence of some relevant geographical expansion. Now, it will be important to ask what these fortuitous observations can tell us. Species records and the provided information Following the capture of an “unusual specimen” we may feel that this episode is something that deserves scientific attention. In this case, our first task will be to identify the individual and to provide unquestionable proof that it belongs to a certain species. Generally, a voucher specimen has to be examined to allow taxonomical identification since records based on a sole picture or video are rarely considered. In view of the absence of specific guidelines on how to prepare a “presence record”, some uncertainties may exist on what

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 105

kind of information do we have to provide and what scientific standards to follow. In order to better respond to these questions, a sample of 130 published records out of 28 different journals was randomly chosen from an existing comprehensive database and then analyzed. Analyzed papers ranged from 1945 to 2007 and accounted for 67 species and 11 Mediterranean countries. For each paper, data such as: “species”, “type of record” (discriminating between “first record” and subsequent ones), “journal”, “year”, “area of observation” were recorded, as well as the presence/absence of a series of information such as “taxonomic characters of the voucher specimen”, “general morphological description”; “depth of capture”; “picture” 1; “destination of voucher specimen”, “ habitat characteristics”, “water temperature”, “sex”, “gonad maturity”, “stomach content”, “age” and “parasites”. The results of this screening are summarized in Fig. 4.

Fig. 3. The dusky spinefoot Siganus luridus and the bluespotted cornetfish Fistularia commersonii in a drawing of L. Valdéz. (Published by The Journal of Marine Biological Association UK 84, p. 819 and by Cybium 28, p. 72). 100% 80% 60%

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Fig. 4. Relative frequency (presence/absence) of some fields of observation included in the records of Mediterranean exotic fishes, based on the analysis of 130 published records from 1945 to 2007. 1

In some cases a scientific drawing is also welcome (Fig.3)

106 Ernesto Azzurro

Starting with some obvious evidences, we can see that every first record presented an accurate description of the specimens and this is usually provided through a detailed documentation of morphological characters. Subsequent records, aimed to confirm the establishment of the species in the area, or even to testify some geographical extension, can be compiled also without reporting these details, being based on the confirmation of previous identifications. Other significant information such as “picture”, “depth” and the “final destination of the voucher specimens” seems to follow the same general rule: needed when the fish is recorded for the first time, optional in subsequent records. Actually, what seems to be “optional” or not, regardless of the biogeographical importance of the capture, are ecological and biological information associated to the discovered specimen, such as: habitat characteristics, water temperature, sex, gonad maturity, stomach content, age and parasites. As showed in Fig. 4, in the analyzed presence records, all these fields appear with a frequency lower than 5%, demonstrating that very few papers reported this information. In large part this depends on the author’s subjectivity and in some few cases from the status of conservation of the voucher specimen. Clearly, it is true that the main objective of a presence record is to provide evidence that “a certain species has been observed in a certain place in a certain time” and this would explain the scarce attention given to the other “optional” information. Instead, some biological observations can be easily conducted on these specimens and it can be of great interest for our purposes (Ruiz-Carus et al., 2006). To cite some Mediterranean examples, Pais et al. (2007) on the basis of a single capture of F. commersonii, showed the occurrence of a post-spawning ovarian stage in Sardinia waters, supporting the hypothesis of successful reproductive events. These authors also highlighted the concurrent invasion of new parasites species in the Mediterranean and endorsed the hypothesis that the migration of Fistularia from the Red Sea was by actively swimming individuals rather than by passive planktonic larvae. Similarly, Romeo et al. (2006) found a single specimen of the wahoo, Acantocybium solandri, in the Straits of Messina. The wahoo is not considered as “exotic” but the analysis of associated parasites supported hypothesis on its provenience. Pizzicori et al. (2000) recorded for the first time S. carpenteri in the Mediterranean and concluded that the species reaches final gonad maturation in the area on the basis of the observation of post ovulatory follicles that are good evidence of previous spawning events. All these biological observations can be relevant, even if associated to single captures. As a matter of fact, adding relevant biological information to a presence record may render the record itself more interesting and suitable for the scientific community. In this manner some captures with “minor” biogeographical relevance can be suitable for international peer reviewed journals, as showed in some of the above mentioned examples. At the end of this paragraph, I think is the right time to shift our attention to what is actually the major gap in the formulation of presence records: the actual discovery of the presence of exotic species themselves. Therefore, our first task will be to detect exotic species as soon as possible and, subsequently, to provide adequate sampling for our study.

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 107

In the next paragraph we will see how these “unusual” fishes are usually detected. How we usually find new exotic fishes. Analysis of published presence records may give us some cues to discuss the chief argument of this paragraph. According to Fig. 5a, the fishing methods which provided most of the exotic captures in the Mediterranean are trawl fishing (33%) and the trammel net (27%) but a diverse array of artisanal methods, ranging from handfishing to longlines, have also provided voucher specimens. In teleost fishes, adults are easier to collect and also to identify than juveniles. This may provide a reasonable explanation why the provided specimen is commonly an adult, whilst only in rare episodes the juvenile stage was found first (e.g. Parenti and Bressi, 2001). One other relevant bit of information is revealed by examining the “collectors”, the ones who personally discover the specimen (Fig. 5a). In most cases (62%) the collector turned out to be a fisherman who caught or found something he can’t identify and reports it to a laboratory or to a biologist. In 23 % of the cases, it was the author or some scientific personnel who detected the fish and in 15% of the cases this information was not reported in the publication. These results may help us understand that the discovery of a new exotic fish species in the Mediterranean is usually an empiric, not a planned episode1 and what usually happen is that we wait until these species are found by chance. In the next paragraphs we will see that some simple activities and procedures can be of valuable help to intercept exotic fishes and to provide the biological samples needed for our studies.

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Fig 5. A) Relative frequency of the fishing methods which provided voucher exotic fishes in the Mediterranean Sea. B) Relative frequency of the collectors who provided the specimens. (Based on analysis of 130 published records from 1945 to 2007).

1

This approach is considered of high risk.

108 Ernesto Azzurro

Some practical suggestions to prepare your “first record” The writing of a new presence record is considered a simple task and, for some researchers (including the author of this chapter), it has been the way to publish their first papers. Although no specific literature exist in how to prepare such contributions, the taxonomic analysis of the specimen should follow some conventional procedures that are not always followed. This will be important to avoid misidentifications that seems to be nothing but unusual in the history of Mediterranean records (see references included in Golani et al., 2002). In order to provide the details of identification, it would be enough to present just the key taxonomical characters that are needed to provide an unequivocal identification, but it is a common practice to present a detailed list of the meristic1 and morphometric2 characters, plus a general description of the specimen. Conventional morphometric measurement can be taken with dial or Vernier calipers on the specimen. Photograph, radiograph, camera lucida drawing and videocamera pictures can be also used if needed. The only requirements are that the image be taken at the zenith of the plan and that a standard measure is placed in the picture. By convention, the left side of the body is used for recording numeric characters. The right one may be used if bilateral counts are requested or if the left is damaged. Gill rakers are counted on the first arch on the left side of the body. All rudiments are counted, so the arch must be carefully dissected for accuracy. If counts of rakers on the upper and lower limbs are reported, the upper count is given first, separated from the lower count by a plus sign (e.g. 7+12). Conventionally, a raker that lies directly on the angle of the arch is reported with those on the lower limb. The use of skeletal elements in species identification is seldom needed for our purposes. Taxonomically important skeletal features include vertebrae, pharingeal teeth and the morphology of cranial bones. Otoliths are useful for identification as well as for age determination. However otoliths dissolve in formalin in a matter of days, so they must be carefully preserved (eventually, buffered formalin can be used). Conventionally, all the meristic characters can be summarized in the Meristic formula. The explanation of the formula can be found in many basic ichthyological books. Once the meristic and morphometric data have been collected, the method of analysis depends on our purposes. If our objective is limited to the fish identification, we may express the counts with the help of a table and the meristic formula. When 1

2

Meristic characters are the body segments and other features such as myomeres, fin rays, vertebrae, scales that once, in the evolutionary history corresponded to the body segmentation. Other enumerable characters such as piloric caeca or cephalic pores are sometimes referred to as meristic even though they have no correspondence with the myomeres. Countable characters vary within and among species and are useful in describing or identifying fishes. The evaluation of countable characters can be subjective so that published accounts should mention the criteria used in making counts. Morphometric characters: characters that can be measured and expressed by a numerical value, e.g. head length.

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 109

more than a few specimens are recorded, meristic data can be presented in frequency tables accompanied by statistics such as mean and standard deviations (e.g. Azzurro and Andaloro, 2004). Retrieving critical information about the distribution of exotic fishes has always been difficult because much of this information is buried in different magazines, in obscure documents or in technical reports (“grey literature”) that are not widely accessible. Inventories are usually based on the analysis of the icthyological knowledge available for a certain country, fishery surveys and to visits to the main landings points. Following these observations and single presence records, published and unpublished observation can be gathered to prepare inventories and check lists. One of the first and most remarkable lists of exotic fishes in the Mediterranean is without doubt the well-polished article of Haas and Steinitz, published in Nature on the 5th of July, 1947, at the beginning of the study of the Lessepsian phenomenon1. Many international scientific journals are interested in publishing biodiversity records. Following the increasing number of submitted records and the growing interest in these contributions, recently some new online journals have been created for this specific purpose. CAN WE IMPROVE OUR CAPABILITY TO DETECT EXOTIC FISHES? Need for an early detection system? As highlighted in the previous paragraph, invasive fishes spreading in the Mediterranean are usually found by chance and specific procedures for their detection are lacking in this area, as well as in most marine systems (Wittenberg and Cock, 2001). Nevertheless, some extra-Mediterranean countries have developed national strategies to manage marine biological incursions and ongoing monitoring is considered an important component. For example, in Australia (Sutton and Hewitt, 2004; Wittenberg and Cock, 2001), California (http://www.elkhornslough.org/invader.htm) and Hawaii (http://www8.nos.noaa. gov/nccos/npe/projectdetail.aspx?id=69&fy=2006), marine invasive species are the object of ongoing monitoring projects and community-based “detection kits” have been developed with the aim to widely disseminate information about potential invaders to target communities2. These kits include protocols to detect macroscopic invasive species, usually easy to be identified in the field, and may describe the method, season, sampling duration and timing best suited for detecting these organisms. Then, local communities are asked to provide reports of invasions and networks of scientific experts work together 1 2

Actually the term Lessepsian was proposed only in 1972 by Por A broad range of people using or acquainted with the natural environment, including divers, fishers, boaters, marine naturalists, surfers, beachcombers, but also tourists and school groups may be targeted by these projects.

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with administrative organizations to implement the most appropriate rapid response strategy. Specific procedures have been also specifically planned for fishes, especially in freshwater systems (Koehn and Mackenzie, 2004). It has to be said that these systems have been developed with the aim to manage harmful species and that many exotic fishes in the Mediterranean can not be properly considered as “pests” (Galil, 2007). In any case, the primary goal of every monitoring program is to provide early detection. Early detection in the form of surveys may focus on a species of concern or on a specific site and species-specific surveys can be designed, adapted or developed for a specific situation. The development of systems for early detection is specifically encouraged by the European Strategy on Invasive Alien Species (Shine, 2007) as well as the building of public awareness and the collection and sharing of information. New strategies and actions should be built up to detect Mediterranean fish introductions, in cooperation with the fishery sectors and local communities. This is not a simple task but it presents some definite point of advantage. With respect to other groups of organisms, the study of fishes has some advantages since commercial fishery exploitation may provide data, information and samples. In addition, the taxonomy of fishes is relatively clear and this is of obvious help for their detection. As we will see in the next paragraphs, members of local communities could play a vital role in this regard, since their broad geographic distribution and familiarity with natural environment. Awareness raising, information, management, education and training are essential areas to address and standards procedures should be developed, both at the national and international and national level. A pilot early system for early detection in the Sicily Strait: the “alien fish alert” In one recent endeavor to ameliorate our capability to detect exotic fishes and to provide adequate sampling to support biological investigations, an experimental early detection system has been developed in the area of the Sicily Strait. The system was aimed to involve local communities, especially people which could notice new aliens in the course of their activities, i.e. fishermen and divers. There are many ways to develop capability and awareness which might include activities such as: media promotion, field guides, personal interactions, displays of preserved specimens, preparation of school materials, posters etc. Our awareness campaign was mainly based on a simple media promotion, posters (Fig. 6) and personal interactions, in the Pelagie Islands. Given the familiarity of fishermen with local species, no training on taxonomy was considered necessary and no black list was proposed. We aimed to receive reports of all “unusual occurrences”. Here is the slogan of the campaign: “..there is no need of any expertise in identifying alien species – those familiar with our sea will immediately recognize a ‘strange’ fish that they have never seen before – it is such records that we are after!”.

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 111

Fig. 6. “Alien fish alert”: Copies of these signs were posted at various locations in the Pelagie islands to advertise the campaign.

Besides the awareness campaign, active monitoring was conducted by underwater visual census and, when possible, by controls to landing points. In Fig 7 this early detection system is summarized in a synthetic self explanatory chart. Dark blocks represent the three possibilities of detection: fortuitous sightings, active monitoring and the awareness campaign. In grey are highlighted the expected results: community awareness, new reports (personal communication of unusual captures to be verified); new records (confirmed capture of exotic species) and new biological samples, suitable for research purposes. Our experience was employed to validate specimens and reports and to evaluate the effectiveness of the program. The campaign was conducted in 2007. Overall, we received reports of 6 valid alien species: Fistularia commersonii; Siganus luridus; Seriola fasciata; Seriola carpenteri; Sphoeroides pachigaster and Stephanolepis diaspros, recorded for the first time in the Pelagie Island. Other reported captures included some uncommon species in the area, such as Lobotes surinamensis, Pseudocaranx dentex and Sygnathus typhle. Other species such as Oxinotus centrina, Lepidopus caudatus, Dactylopterus volitans, Remora remora, Naucrates ductor, Balistes capriscus, Gobius auratus have been also reported, being considered as “unusual” by some fishermen or divers. Doubtful observations, not supported by a preserved specimen or photographic proof were considered as unidentified specimens. Fig. 8 shows the relative frequency of reports of these categories according to fishermen, divers and scientific personnel. Fishermen, and obviously scientific personnel, were particularly helpful in the detection of exotic fishes, both for the high frequency of validated records and for providing biological samples. It is interesting to note that, in the case of fishermen, most

112 Ernesto Azzurro AWARENESS CAMPAIGN

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Fig. 7. Self explanatory chart summarizing the pilot early warning system for the detection of exotic fishes in the Sicily Strait. Dark blocks represent the three possibilities of detection; white blocks research activities and grey blocks the expected results. The management block is with interrupted line because it was not part of the realized actions. 100 90

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Fig. 8. Relative frequency of reports of “unusual fishes”, according to fishermen (113 reports), divers (61 reports) and scientific personnel (23 reports). (Based on the experimental campaign on “alien fish alert” in the Pelagie Island and a total number of 197 different reports).

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 113

of the reports (97%) were attributable to personal interactions whilst only 3% to media promotion. Information reported by divers were also quite important for our purposes. Generally a crucial task of early detection is also to determine the action to be taken when an alien species is found. This would generate timely control responses that are more likely to succeed than action after a species has become established. However, wild fishes unlike other invasive animals and plants are extremely difficult to manage. Eradication, which is quite a desperate solution in freshwater environments (see for example Stokstad, 2003), is considered not feasible in open marine systems where consistent management measures are seldom applied. Nevertheless, research is a priority for exotic species and a timely base of information is needed to track and to understand the phenomenon. The system is intended to work on a local scale but international research networks can be very helpful for exchange of expertise and also biological samples. The “alien fish alert” campaign created a direct link for two-way flow of information on non-native fishes between researchers and the community at-large. Future developments of this experimental system for early detection should include the building of a well coordinated network of monitoring, in order to develop a national and transnational capability for the detection of distributional changes of both native and exotic species. THE STUDY OF THE EARLY STAGES OF COLONIZATION A few words on invasive dynamics The development of a new population is a dynamic process involving different stages. The beginning of that process is represented by the arrival of invasive propagules that in the case of fishes may be represented by drifting larvae or by active swimming individuals. Following dispersal to a new environment, propagules have to face a host of filters i.e. environment survival, reproduction and subsequent recruitment, that may preclude (or not) the establishment of a self maintaining population. Once successfully established, these populations may disperse new propagules to nearby habitats and extend their distribution, according to a series of sequential invasion called “meta-invasion” (Davies et al., 1999), which basically proceed through three subsequent phases: initial dispersal, establishment of self-sustaining populations and spreading to nearby habitats (Puth and Post, 2005). In most cases, the geographical expansion of exotic fish species in the Mediterranean should be considered as a secondary (at least) invasion event, since the likely source populations were themselves established as part of the primary invasion (Azzurro et al., 2006). The temporal succession of these stages can be highly variable and unpredictable; much time may be needed for the invasion to proceed further. Such “time lags” are a common feature of biological invasion (Sakai et al., 2001; Lee, 2002) and exotic fishes in the Mediterranean present a wide array of examples. Two different and opposite cases are the ones of the dusky spinefoot, S. luridus which has been recorded in Tunisia in

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1969 (Ktari-Chakroun and Bouhlal, 1971) with no subsequent evidence of geographical expansion until 2002 (Azzurro et al., 2004) and the bluespotted cornetfish, F. commersonii, which showed an unprecedented rapid expansion (Azzurro et al., 2007) immediately after its first sighting in 2000 (Golani, 2002). Why study early invasions? In the previous paragraph we have seen that invasions proceed in multiple steps: initial dispersal, establishment and spreading. All these phases can be the subject of study but the initial stages are thought to deserve special attention since the other stages are contingent upon it. It is clear that early settled populations must reproduce at a rate that exceeds its mortality to continue the invasion process. Nevertheless, local density of individuals in newly colonized areas is typically low at early stages of invasion and, according to the “Allee effects” (Allee, 1938), reproductive impairments may occur at such low density. As a result, early invasive populations, with density below a certain threshold, may decline in abundance despite living in a basically favorable environment. On the other hand, the process of gonad maturation in teleost fish is a very susceptible phase and suboptimal conditions1 of a new environment may affect the final stages of ovarian maturation (Nagahama, 1983; Hunter and Macewicz, 1985). For these reasons, the study of reproductive biology of early settled populations is thought to be particularly informative. This knowledge is also needed to assess whether a given exotic species has managed to establish a self-maintaining population or if it is maintained by migratory fluxes. Up to now, this information has been considered too difficult to obtain and “established” species have been arbitrarily defined as those having at least three distinct published records, well separated in time and space, in the Mediterranean (Golani et al., 2002). This gap in the knowledge of the reproductive status of early migrants make it difficult to assess the status of invasive phenomena (Roll et al., 2007) with consequent uncertainness on the invasive dynamics and potentialities. Another matter of concern regards concurrent invaders such as parasites and pathogens that may be transported into a new environment by an invasive host with unforeseeable effects upon local communities (Wurtsbaugh and Tapia, 1988). In that situation, the parasite is thought to be more damaging to the new host because the host and parasite have not had the evolutionary time to reach an equilibrium relationship. Actually, the possibility that the exotic parasite could cross onto native hosts has been seldom considered in the Mediterranean context and very few studies on parasites associated to exotic fishes exist (i.e. Fischthal, 1980; Diamant, 1989; 1998; Pasternak et al., 2007; Pais et al., 2007). Here it is worthwhile to reaffirm that exotic fishes should be checked for their biotic associations as soon as the first individuals are detected. 1

e.g. low water temperature, variation in nutritional state, stress, inappropriate photoperiod

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Other important studies are those dealing with the feeding habits of early invaders. This information can be used as a feasible first step in evaluate the potential impact of these migrants on the native food web, as recently shown for early F. commersonii by Kalogirou et al. (2007). Particularly relevant are the studies aimed to compare the trophic niche of both invasive species and their ecological analogues because they may help us understand the level of competition between species. One reason to approach these comparisons as soon as possible is to allow investigation of an invasive phenomenon before its disturbance of native communities (Puth and Post, 2005). The history of Lessepsian invasions is rich in examples in which ecological shifts, species replacements, displacements and changes in structure and abundances have been hypothesized but, surprisingly, specific studies are very rare (Golani et al., 2007a). Instead, ecological studies performed at the beginning of colonization, when interaction between native and exotic species is minimal, would allow us to better define the “fundamental” niches and, obviously, to follow any subsequent ecological shift (Golani, 1994; Azzurro et al., 2006). Genetic studies, even if seldom applied in the Mediterranean context, are thought to offer insights into the mechanisms of invasions and its dynamics. Recent investigations considered early settled populations at the current margins of their Mediterranean distribution, thus highlighting some advantages in their study (Azzurro et al., 2006; Golani et al., 2007b). The exact beginning of colonization can be often determined in these populations and the analysis of the genetic structure of “colonization front lines” can be particularly informative to understand how invasion proceeds. Looking at the cases of historical invaders such as Atherinomorus lacunosus and Siganus luridus (Golani and Ritte, 1999; Bucciarelli et al., 2002; Hassan et al., 2003; Hassan and Bonhomme, 2005), colonization seemed to have occurred by a large number of individuals or by multiple colonization events, or a combination of both. This was also the case of the early settled population of S. luridus in Linosa, which showed no traces of founder events (Azzurro et al., 2006). On the contrary, the recent invasion of F. commersonii was determined to be founded from a very small number of individuals which underwent a severe population bottleneck (Golani et al., 2007b). It is clear that the invasive dynamics of Lessepsian fishes have shown no coherent pattern and this reflects a general lack of unified theories in both terrestrial and marine bio-invasions. These arguments are treated in more detail in the chapter by Prof. G. Bernardi et al. One of the major requirements in assessing colonizer impact is the information on native communities before the onset of an invasion or even within a short period after colonization (Golani, 1994). The onset of invasion is the appropriate time to start the monitoring of invasive populations and of the host community in order to appropriately follow temporal changes at the community level. The lesson of the eastern Mediterranean teaches us that this information is of paramount importance to assess the impact of invasive fish, otherwise, the lack of historical series of data on local communities renders any conclusions on this subject of a speculative nature only (Golani et al., 2007a). Finally, in a management context, it is during the initial stages, when populations are small, that management efforts can prevent or control unwanted colonization and spread

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of exotic species. In terrestrial systems early detection and rapid response are often the best way to successful, cost-effective eradication of a new invasive species (McNeely et al., 2001). However, as already mentioned, fishes are difficult to eradicate and in most cases the establishment of an exotic fish in the open sea is considered as irreversible. In Table 1 are summarized some of the advantages and difficulties of the study of the early stages of invasion. Why it is difficult to study early stages of invasions Despite their importance, information on the early stages of invasions is rarely reported and we have seen that studies in recently colonized areas, at the margin of species distribution ranges are very rare in the Mediterranean Sea. This lack of information on the Table 1. A summary of the advantages and constraints for the study of early invasive fish populations Why study early invasions? “Species border”: those populations residing at the current margins of species distribution are important for the progression of invasion. “Before ecological shifts”: it is possible to perform ecological studies when presumably there is slight interaction between native and exotic species. “Mechanisms of dispersal”: early invasive phenomena may offer insight into their dynamics. Molecular markers and the study parasites can be used. “Follow up studies”: the onset of invasion is the appropriate time to start monitoring of invasive populations and of the host community in order to appropriately follow temporal changes at the community level. “Measure and observe impacts”: ecological shifts, species replacements, displacements, changes in structure and abundances can be followed and described if the studies are timely and appropriate. “Management”: management measures are far more effective if directed to the early stages of invasion. Even if marine fishes are considered to be difficult to manage and fairly impossible to control, prompt scientific information is necessary to assess the importance of invading events and to give timely insight as to how to manage the same.

The difficulties “Hard to detect”: the early stages of invasions often occur over large spatial and temporal scales. “Small samples”: early invaders typically occur as few and isolated individuals or small assemblages. “Lack of temporal and spatial replication”: the shortage of samples renders it difficult to incorporate spatial and temporal variability in our studies. Some suggestions:  Single observations, such as on gonad maturity or parasites, can be of interest, even if few specimens are considered.  The formulation of simple key questions may facilitate our task.  Methods of study which need few or no temporal or spatial replication are suited.  Severe experimental design can be used to overcome the shortage of samples.  Caution is required when drawing conclusions.

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initial stages of invasion reflects a general pattern, common in both marine and terrestrial habitats (Puth and Post, 2005). As a matter of fact, the study of early invasive episodes is not a simple task, both because it is composed of rare events that are hard to detect and because these often occur over large spatial and temporal scales. Biological and ecological questions can be answered if appropriate sampling is available and sampling is representative if it is representative of the natural variability. Instead, the initial stages of invasion are typically represented by widely scattered and isolated individuals and pragmatic constraints arise. In most cases, the shortage of samples and observations renders it impossible to incorporate such spatial and temporal variability into our study. However the quality of our sampling will depend also on our objectives of study. For this reason, the formulation of simple key questions may facilitate our task and it can help us in our approach to early colonizing episodes. For instance, an early settled population of S. luridus, in Linosa Island at the current borders of species distribution in the Mediterranean has been recently the object of several studies, based on a very limited set of samples (Azzurro, 2006; Azzurro et al., 2006; Azzurro et al., 2007a,b). The first question to solve was “if early colonizers attain final gonad maturation stages and have the potential for successful reproduction”. The authors (Azzurro et al., 2007a) concentrated sampling during the reproductive season, in order to analyze the most critical stages of the reproductive cycle. One other way of overcoming the shortage of samples is to use methods of study which need few or no temporal or spatial replication and to adopt severe experimental designs. The simultaneous capture of fish and their similar size range enabled Azzurro et al. (2007b) to perform a direct comparison of diets between early invasive S. luridus and the native herbivorous Salpa salpa and Sparisoma cretense based on gut-contents analysis. Given the impossibility to incorporate temporal and spatial variation, this information was integrated with stable isotope analyses which yield information on what is actually assimilated and provided relatively long-term and time-integrated measurements of feeding preferences, being less subject to temporal bias (Pinnegar and Polunin, 2000). We have stressed repeatedly the importance of studying early settled populations and of overcoming the difficulty to incorporate temporal and/ spatial variation. It is clear that extreme caution must be utilized when planning our investigations and drawing conclusions. Watch locally – think globally Up to now we have stressed the importance of early detection, exploring some possibilities of the study of the early stages of colonization, as soon as a newcomer arrives in a new locality. To act or even to “watch” at a local scale is imperative if we wish to detect, to monitor and eventually to manage these invasions. We have also seen that the spread of exotic species and the concurrent changes of marine fish biodiversity are wide scale processes that extend beyond the limits of communities, ecosystems and nationals

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borders and this would widen the perspectives of study. Here the first goal of research is to understand how the sum of single observations may be used to explore patterns and processes of which they are part but this is a rather difficult and debated issue (Galil, 2007). Following the establishment of a new species, novel assemblages are formed and new functional and structural elements are added to the host ecosystems. In the case of Mediterranean fishes, no extinction of native species has been recorded, as well as for the other Mediterranean marine taxa (Boudouresque, 2004). Thus the incoming of new species usually results in increasing diversity1, and this can be perceived as favorable by many people. However we should consider that biological diversity is changing in fundamentally different ways at different spatial scales (Gray, 1997). Thus, when local boundaries are crossed and more than one habitat or community is considered, things may be different. In this case, the movement of species may result in a lowering of diversity2, more precisely in a lowering of the number of taxa that are unique to each of the ecosystems. If we take for instance the spread of S. luridus from African coasts to adjacent Sicily, one of the results was an increase in similarity between these two areas in terms of species identity. This process is even more evident at an even larger geographical scale3 and this has been recently stressed in an overview of the whole Mediterranean fish community (Quignard and Tomassini, 2000), which resulted in the paradox of gaining species but losing diversity. This process is commonly referred to as biotic homogenization (Vitousek et al., 1997), one of the most prominent forms of biotic impoverishment worldwide. Another field of “global debate” is the theoretical arena. Following the publication of the Ecology of Invasions by Animals and Plants by C. Elton (1958), biological invasions emerged as an important focus of ecological research and today their study can be considered one of the most exciting areas of interplay between theoretical and observational work in ecology. From a certain point of view, a new invasive phenomenon can be viewed as a natural experiment and in some cases this episode can be capitalized for the understanding of theoretical questions. Nevertheless, despite the large amount of studies and observations, no unified theories have emerged and the debate is still controversial. Recent attempts at developing generalizations for invasion ecology have focused on predicting the driven factors that promote the successful establishment of an introduced species (Kolar and Lodge, 2001) and invasions have been considered from a variety of viewpoints. Historically, the success of biological invasions has been related to both the intrinsic attributes of the invaders (e.g. the propagule pressure, tolerance to 1

2

3

We focus on Alpha diversity (α-diversity) which is the biodiversity within a particular area, community or ecosystem, and is measured by counting the number of taxa (distinct groups of organisms) within the ecosystem (eg. families, genera, species). We focus on Beta diversity (β-diversity) which is a measure of biodiversity which works by comparing the species diversity between ecosystems or along environmental gradients. This involves comparing the number of taxa that are unique to each of the ecosystems. When we consider the Gamma diversity (γ-diversity) i.e. the total biodiversity over a large area or region

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abiotic factors, genetic variability, reproductive capacity, wideness of ecological niche…) and to the characteristics of the recipient community (e.g. stability, species richness, prior disturbance; available resources and the release from natural controls including predators, competitors and parasites natural biotic constraints). Considering the complexity of these issues and the large amount of literature, a comprehensive argumentation on the theoretical debate would go beyond the purposes of this chapter. In any case one may recall some recent examples in which an early approach to an invasive phenomenon proved to be advantageous for theoretical work. An important area of theoretical debate concerns the concept of “niche”. Ecological niches are defined by the relationships between organisms and their physical and biological environment and in the context of exotic species the concept of ‘niche opportunity’ has been often used to define conditions that promote invasions. Niche opportunities vary naturally between communities (Shea and Chesson, 2002) and the Mediterranean Sea, owing to its recent history, can be considered a system where many ecological spaces are still “available’’ (Oliverio and Taviani, 2003). For these reasons the idea of “unsaturated”, “empty” or “vacant” niches” is a theory that has been often used to explain the success of exotic fishes in the Mediterranean (e.g. Por, 1978; Ben-Tuvia, 1985). Actually, in the last few decades, the concept of ‘vacant niche’ has been the subject of considerable controversy and today it is rejected by many ecologists simply because if the niche is a property of a species, it does exist only when the species is present. Besides this necessary clarification, very few studies focused on the degree of niche partitioning between exotic species and their native analogues (see Golani, 1994 and references therein included; Azzurro et al., 2007b) and further efforts are needed to explore the ecological basis of the success of exotic species in the Mediterranean Sea. As already discussed in the previous paragraph, fishes have the capability to switch ecologically if “disturbed” by species with overlapping requirements. Thus niche partitioning among historically settled exotic and native species could be the result of an ecological shift. In this sense, the timely studies, at the early phases of invasion, have the advantage to avoid this bias and to get information when presumably there is slight interaction between native and exotic species. Another important theoretical field concerns the role of propagule pressure and the effects of natural control agents. Propagule pressure (i.e. the number of individuals introduced and the number of introduction attempts) is not easily measurable directly, but genetic studies can give us an idea of the genetic flow between the source and the recipient community. In this regard, early settled populations can turn into a unique study opportunity. If we look at the case of F. commersonii, Mediterranean populations were found to be generated by a single invasion event and by bottlenecked populations founded by a very small number of individuals (Golani et al., 2007b), reaffirming a well-known dilemma in invasion biology (Frankham, 2005) (for more details see the chapter of G. Bernardi et al.). Finally it is worth to recall, even if briefly, another theory that in recent times has received increasing attention, the “enemy release hypothesis” (Elton, 1958). According to this hypothesis, introduced species may flourish because they manage to escape the effects

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of natural control agents such as predators or parasites (Torchin et al., 2002; Colautti et al., 2004). This hypothesis should be tested in the Mediterranean environment and specific studies are needed to compare the parasitofauna of exotic fishes in their native and introduced range. In this context, early settled populations provide unique opportunities to understand the effects of host range expansion on parasite communities, whose study can give details on both the host movements and the migration process itself. CONCLUSIONS This entire chapter has been motivated by an increasing awareness and concern about the rapid change that is now facing Mediterranean biodiversity. In this matter we have tried to recognize the significance of what we called “unusual occurrences” and their exploitability for research purposes. We did not refer to those exotic populations that have been historically established in the Mediterranean, but rather to those species that are currently finding their way out of their contemporary distribution ranges. Considering the sporadic nature of these observations, a series of methods, suggestions and “tricks” to facilitate their detection and study has been given, with the aim of extracting as much information as we can from these rare episodes that are always difficult to observe. Having the lucky chance to have crossed paths with one unusual occurrence, we should keep in mind that this episode could represent a first chance to document a new invasive phenomenon or even an opportunity to obtain evidence of some relevant biogeographical changes. Therefore, it has been suggested to do our best to document the new arrivals and to capitalize our possibilities to provide biological information, even if few observations and/or samples are available. When a new exotic species is found in a new area, timely information is needed to understand “what’s going on” and to assess the stage or status of the invasion. To answer these questions we need to acquire basic information on the biology and demography of these early invaders. It is therefore suggested that researchers and scientific journals continue to take into appropriate consideration the unusual incidence of organisms present outside their expected range and publish them with sufficient detail so that future research will have the possibility to explore the offered opportunities. Often our research will not go beyond the descriptive stage and extreme caution is necessary when drawing conclusions, but the sum of the information that we can get from all these episodes may have some role in deciphering trends of environmental changes in the Mediterranean Sea. The short time-period of samples and the spatially and temporally sporadic nature of the initial stages of colonization render research extremely difficult, even if not precluding completely their study. To choose the appropriate experimental scale and to recognize the limits of extrapolation from this scale may be helpful advice if we want to conduct research in this field, but it is necessary to do it in time. The example of Lessepsian fish invasion in the eastern Mediterranean represents a powerful lesson in lost opportunities

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for research at very early stages of an invasion. In fact, it is now difficult to understand how and to what extent the eastern Mediterranean and its biological communities have changed since the onset of Lessepsian invasions, if historical data are lacking. Therefore, one other important challenge will lie in our capability to follow the dynamics of both exotic populations and recipient communities by means of long-term monitoring programs. Patterns and processes that govern biological invasions are complex and a multifaceted approach is required in order to face the different questions that are raised by a new invasive episode. A single question may require different disciplines and a single discipline may respond to different questions, but research opportunities are clearly underexploited. Future efforts will be directed to improve our capabilities to detect and study early invasive events by multidisciplinary approaches and coordinated regional and international monitoring. This represents the ultimate and pragmatic challenge facing us simultaneously at both the regional and global level at this time. ACKNOWLEDGEMENTS I would like to express my gratitude to the people who significantly contributed to the “alien fish alert” campaign, which has been partially funded by the project MonItaMal, Interreg III A Italia-Malta: Dr. Alfonso Scarpato and to Dr. Raffaella Piermarini of the High Institute for Environmental Protection and Research; Dr. Gaetano Vassallo and Dr. Alessandro Cento of the Parco Scientifico e Tecnologico della Sicilia; Dr. Peppino Sorrentino of the Marine Protected Area of the Pelagie Islands; Dr. Federica Celoni, Dr. Gabriella La Manna, Dr. Simona Clò and the Centro Turistico Studentesco for their valuable help. A special thanks to all the fishermen and divers of the Pelagie Islands, especially to Pizzicotto and Pillino, who provided some of the most important reports. REFERENCES Allee, W.C. 1938. The social life of animals. New York: Norton. 293 pp. Andaloro, F. and A. Rinaldi. 1998. Fish biodiversity change in Mediterranean Sea as tropicalisation phenomenon indicator. In: Enne, G., M. D’Angelo. and C. Zanolla (eds.), Indicators for assessing desertification in the Mediterranean. Rome: A.N.P.A. pp. 201-206. Astraldi, M., C. N. Bianchi, G.P. Gasparini and C. Morri. 1995. Climatic fluctuations, current variability and marine species distribution: a case study in the Ligurian Sea (north-west Mediterranean). Oceanologica Acta 18: 139-149. Azzurro, E. 2006. Fish biodiversity changes in the Mediterranean Sea: cases of study. PhD Thesis, Università Politecnica delle Marche, Ancona, Italy. 238 pp. Azzurro, E. 2008. The advance of thermophilic fishes in the Mediterranean sea: overview and methodological questions. In: Briand, F. (ed.) Climate warming and related changes in Mediterranean marine biota. N° 35 CIESM Workshop Monographs. Monaco. pp 39-46.

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Azzurro, E. and F. Andaloro. 2004. A new settled population of the Lessepsian migrant Siganus luridus (Pisces: Siganidae) in Linosa Island – Sicily Strait. Journal of Marine Biological Association UK 84: 819-821. Azzurro, E., P. Pizzicori and F. Andaloro. 2004. First record of Fistularia commersonii (Fistularidae) from the Central Mediterranean. Cybium 28(1): 72-74. Azzurro, E., D. Golani, G. Bucciarelli and G. Bernardi. 2006. Genetics of the early stages of invasion of the Lessepsian rabbitfish Siganus luridus. Journal of Experimental Marine Biology and Ecology 333: 190-201. Azzurro, E., O. Carnevali, M. Bariche, F. Andaloro. 2007a. Reproductive features of the non-native Siganus luridus (Teleostei, Siganidae) during early colonization at Linosa Island (Sicily Strait, Mediterranean Sea). Journal of Applied Ichthyology 23: 640-645. Azzurro, E., E. Fanelli, E. Mostarda, M. Catra and F. Andaloro. 2007b. Resource partitioning among early colonizing Siganus luridus and native herbivorous fishes in the Mediterranean: an integrated study based on gut-content analysis and stable isotope signatures. Journal of the Marine Biological Association of the UK 87: 991-998. Ben Rais Lasram, F. and D. Mouillot. 2009. Increasing southern invasion enhances congruence between endemic and exotic Mediterranean fish fauna. Biological Invasions 11: 697-711. Ben-Tuvia, A. 1985. The impact of the Lessepsian (Suez Canal) fish migration on the eastern Mediterranean ecosystem. In: Moraitou-Apostolopoulou, M. and V. Kiortis (eds.). Mediterranean marine ecosystems. New York: Plenum Press. pp 367-375. Bianchi, C. N. 2007. Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580: 7-21. Bianchi, C. N. and C. Morri. 1993. Range extension of warm-water species in the northern Mediterranean: evidence for climatic fluctuations? Porcupine Newsletter 5 (7): 156-159. Bianchi, C. N. and C. Morri. 1994. Southern species in the Ligurian Sea (northern Mediterranean): new records and a review. Bollettino dei Musei e degli Istituti Biologici dell’Università di Genova 58-59: 181-197. Bianchi, C. N. and C. Morri. 2004. Climate change and biological response in Mediterranean Sea ecosystems – a need for broad-scale and long-term research. Ocean Challenge 13(2): 32-36. Bianchini, M.L. and S. Ragonese. 2007. Presenze di specie ittiche esotiche come possibili indicatori di cambiamenti climatici: il caso dello Stretto di Sicilia. Available online at: http: //www. dta.cnr.it. Boudouresque, C.F. 2004. Marine biodiversity in the Mediterranean: status of species, populations, and communities. Scientific Report of Port-Cros Natural Park, France 20: 97-146. Bucciarelli, G., D. Golani and G. Bernardi. 2002. Genetic cryptic species as biological invaders: the case of a Lessepsian fish migrant, the hardyhead silverside Atherinomorus lacunosus. Journal of Experimental Marine Biology and Ecology 273: 143-149. Colautti, R., A. Ricciardi, I.A. Grigorovich and H.J. Macisaac. 2004. Is invasion success explained by the enemy release hypothesis? Ecology Letters 7: 721-733. Davies, N., Villablanca, F.X. and G.K. Roderick. 1999. Determining the source of individuals: multilocus genotyping in nonequilibrium population genetics. Trends in Ecology and Evolution 14: 17-21. Diamant, A., 1989. Lessepsian migrants as hosts: a parasitological assessment of rabbitfish Siganus luridus and S. rivulatus (Siganidae) in their original and new zoogeographical regions. In:

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marine protected areas and non-indigenous fish spreading 127 D.Mediterranean Golani & B. Appelbaum-Golani (Eds.) 2010 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 127-144. © Pensoft Publishers Sofia–Moscow

Mediterranean marine protected areas and non-indigenous fish spreading Patrice Francour, Luisa Mangialajo and Jérémy Pastor

INTRODUCTION Ecosystem biodiversity is being altered worldwide by species loss due to extinction from human activities and species gain through intentional and accidental introductions (Sala et al., 2000). At the regional level, the gain of species most often equals or outpaces the losses due to extinction, suggesting that extinctions and invasions might offset one another with little net change in diversity (Sax and Gaines, 2003). However, because different processes drive extinctions and invasion (e.g. overfishing versus ballast water transport), the types of species being gained and lost might differ (Byrnes et al., 2007). The combined effect of these two processes is altering the structure of coastal marine food webs since most extinction events occur at high trophic levels, while most invasions are by species from lower trophic levels (Byrnes et al., 2007). The Mediterranean Sea is currently facing dramatic changes, including change in native species distribution due to climatic modification (Francour et al., 1994; Bianchi, 2007), harmful algal blooms linked to increasing eutrophication (Heisler et al., 2008), fishing activity (Farrugio et al., 1993), habitat fragmentation and destruction (see Airoldi and Beck, 2007) and non-indigenous species (NIS) invasion (Galil, 2008). Consequently, Mediterranean food webs are considered to be in an advanced state of ecological degradation (Coll et al., 2008). To reduce these impacts, biodiversity management policies have been proposed throughout legislative regulation of human activities (Francour and Bellan-Santini, 2007), and creation of marine protected areas (Francour et al., 2001). Prevention measures could be potentially effective in fighting against invasions related to aquaculture and aquarium escapees. However, it appears actually very utopian to effectively prevent introductions due to two very important vectors, ballast waters and inter-ocean channels. Consequently, is the spreading of NIS into the Mediterranean from the Atlantic Ocean or the Red Sea ineluctable? Some

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communities appear to be more resistant to invasion than others; however, a great deal of uncertainty regarding site- and community-specific resistance to invasion remains (Klinger et al., 2006). The effect of reserves and protected areas on invaders success is generally not known. While terrestrial reserves are often highly invaded, they tend to be substantially less invaded than areas outside reserves (Lonsdale, 1999). We know far less about the frequency and fate of NIS in marine reserves and protected areas but it is apparent that marine reserves are not immune to biological invasion (Byers, 2005; Klinger et al., 2006). The marine protected areas (MPAs) in the Mediterranean Sea have been well studied and ecological consequences of protection, at least in no-take areas, are well known (Francour et al., 2001; Guidetti, 2006, 2007). Will MPAs, as oases of biodiversity, serve as the last rampart against these invasive species? In this chapter we briefly review the main characteristics of the so-called reserve effect. Secondly, we discuss how and why marine protected areas could be effective tools in limiting invasive species from spreading. Most of Mediterranean MPAs (and especially the oldest ones) are located in the north-western basin (Fig. 1), where Erythrean/Lessepsian species are still rare. So, the conclusions brought to light herein are mainly theoretical and not yet tested throughout the Mediterranean Sea. MARINE PROTECTED AREAS (MPAS) The expectation in the creation of Marine Protected Areas (MPAs) for biodiversity and resources conservation implies the regulation of local human activities, especially fishery. However such regulation policies could never counteract human disturbances of more global scale, such as climate change or atmospheric agents impacts (e.g., acid rain and fallout), those linked with basin-scale dynamics (e.g., wastewater discharge in surrounding areas or other pollutant inputs) (Terlizzi et al., 2004) or catastrophic events occurring on a regional scale (i.e., hurricanes and oil spills; see: Allison et al., 2003). We cannot therefore expect that MPA establishment will prevent invasive species settlement (Simberloff, 2000) but indirect effects of protection may hinder the establishment of NIS and/or their spreading. Fishing is now widely recognized as one of the most significant human impacts on marine systems, with the direct potential to reduce the abundance of target species (Pauly et al., 1998; Steneck et al., 2004). Fishing can also cause cascading ecosystem effects (sensu Pinnegar et al., 2000) due to alterations in the extent of top-down regulation of grazers’ density and/or assemblage structure (Pauly et al., 1998; Tegner and Dayton, 2000). The establishment of MPAs partially alleviates this impact (Côté et al., 2001; Guidetti and Sala, 2007). By returning areas under protection to nearly un-fished states, MPAs provide a reference allowing the quantification of fishing effects (e.g. Guénette et al., 1998; Tegner and Dayton, 2000; Seytre and Francour, 2008).

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2

3

1 4

1 – Natural Reserve of Medes Island (Spain) 2 – Natural Reserve of Banyuls-sur-mer (France) 3 – Natural Park of Port-Cros (France) 4 – Natural Reserve of Scandola (France)

– creation before 1990 – creation after 1990

Fig. 1. Map of the Mediterranean Sea MPAs. Triangles indicate MPAs created before 1990 while circles represent MPAs created after 1990 (adapted from http://www.medpan.org; consulted online 27/04/2009). Arrows indicate the four MPAs considered in this study.

Few studies have attempted to quantify changes in entire fish assemblages (e.g. Francour, 1994), focusing rather on target species (e.g. Harmelin et al., 1995; Seytre and Francour, 2009). As a general rule, target species have been found to increase in size and abundance following protection, with an overall increase in the abundance of larger fishes (e.g. Francour, 1994; Jennings and Blanchard, 2004; Guidetti, 2006; Barrett et al., 2007; Ojeda-Martinez et al., 2007). Other observed effects include changes to life history characters such as size at maturity and size of sex change (Buxton, 1993). Empirical and theoretical studies also suggest that changes in predatory fish abundance can cause ecosystem-wide changes such as trophic cascades (Sala et al., 1998; Pinnegar et al., 2000; Shears and Babcock, 2002; Guidetti, 2006). Natural trophic balances may take several decades to be restored (Shears and Babcock, 2002, 2003; Barrett et al., 2007; Guidetti and Sala, 2007) however, if an MPA is established, some changes may be observed, even after only a few years (Halpern and Warner, 2002; Seytre and Francour, 2008, 2009). A critical issue concerning trophic balance restoration in Mediterranean MPAs is related to the level and the endurance of enforcement measures: Guidetti et al. (2008) showed that positive responses to protection in fish assemblages were observed only in those Italian MPAs characterized by a high level of enforcement (only 20 % of the studied MPAs). Therefore, eventual indirect effects of MPAs to hinder NIS establishment and/or spreading can only be expected by effective enforcement of Mediterranean MPAs.

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NON INDIGENOUS SPECIES (NIS) One of the many unintended consequences of global trading has been the translocation of countless plants and animals to new regions, continents and oceans (e.g. Sala et al., 2000; Galil, 2008; Levine, 2008). NIS have colonized almost every habitat on Earth and modern ecosystems are now constituted to a great extent by species originating from geographically distinct regions (e.g. Simberloff, 2000; Occhipinti-Ambrogi and Savini, 2003; Streftaris et al., 2005; Byrnes et al., 2007). Even Cape Horn, Chile, at the southernmost point of South America, which is considered to be one of the world’s most pristine wilderness areas, has become prone to the spreading of invasive species (see: http://www.chile.unt.edu/ rec/invasive_species.html) . In this extremely remote area, characterized by low human population density and vast tracts of undisturbed land, Anderson et al. (2006) noted the domination of exotic species in several terrestrial vertebrate groups. Successful establishment by NIS outside their natural range is a highly probabilistic outcome dependant upon the coincidence between delivery of the species to the new location and suitable conditions for establishment, including the absence of enemies and the availability of resources (e.g. Galil, 2008; Levine, 2008). Both the supply characteristics (i.e. propagule pressure) and opportunity for establishment (i.e. niche opportunity) are likely to be highly variable in space and time in marine systems. Inglis et al. (2006) reported several studies supporting the hypothesis of a greater success of NIS on islands than on continental areas, at least for continental biota. However, according to them, there is no evidence that native marine biota of islands are any more or less susceptible to invasion, or that they are more severely affected by NIS, than that observed for continental biota. Regarding the Mediterranean, Ben Rais Lasram et al. (2008) concluded that crossing the Suez Canal does not guarantee successful invasion and widespread dispersal of fish populations. Although consideration of the hydrological conditions in both the western and eastern Mediterranean basins is important in understanding the successful spreading of many Lessepsian fish (Mavruk and Avsar, 2008), species ecology is a key determinant for dispersal success as well: overall, only 30% of the Lessepsian species have succeeded in establishing colonizing populations in the Mediterranean Sea (Ben Rais Lasram et al., 2008). The impact and distribution of NIS today is a major topic of scientific interest and conservation concern (e.g. Sala et al., 2000; Meinesz, 2007; Galil, 2007, 2008; Levine, 2008). Together with habitat fragmentation (Hoffmeister et al., 2005) and global warming (Francour et al., 1994; Bianchi, 2007), species introductions constitute a principal cause of current global ecological change (Chapin et al., 2000; Simberloff, 2000; Sala et al., 2000; Galil, 2007; Hellmann et al., 2008). Accidental or intentional introduction of non-indigenous organisms continues to threaten terrestrial (e.g. Lonsdale, 1999; Levine, 2008) and marine ecosystems worldwide (e.g. Occhipinti-Ambrogi and Savini, 2003; Streftaris et al., 2005).

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Given the sizable ecological and economic costs of species invasions (Levine, 2008), understanding the regulating environmental factors has become a major goal for basic and applied ecologists (Occhipinti-Ambrogi and Savini, 2003; Bulleri et al., 2008). Yet there is no general theoretical framework predicting which NIS species will become an invader or to assess invasibility of ecosystems (Lonsdale, 1999; but see Ben Rais Lasram et al., 2008 regarding Mediterranean fish). However, one of the major and primary hypotheses is the relationship between native species richness and exotic species ability to colonize new habitats, i.e. the community “invasibility” (Byers and Noonburg, 2003; Stachowicz et al., 2002; Dunstan and Johnson, 2004; Stachowicz and Byrnes, 2006; Bulleri et al., 2008). This concept implies that habitats with high levels of diversity are difficult to invade. In contrast, species-poor communities, or stressed ecosystems, are arguably more prone to invasion, primarily due to lack of biotic resistance (Occhipinti-Ambrogi and Savini, 2003). This is because, in theory, a more diverse assemblage of plants or animals utilizes its resources more efficiently than a less diverse community, thus increasing competition intensity and making it more difficult for new species to become established (Bampfyle and Lewis, 2007). Occhipinti-Ambrogi and Savini (2003) reviewed marine bioinvasions using examples taken from the Mediterranean and Black Sea regions. They emphasized that stressed environments are easily colonized by alien species and concluded that understanding the links between human and natural disturbances and the massive phenomenon of NIS will help to prevent future marine bioinvasions that are already favored by global oceanic trade (but see Zaiko et al., 2007). Conflicting results have emerged between small-scale experimental studies, which have typically found a negative relationship between native and non-native species richness, and large-scale observational studies, which have frequently found the opposite in nature (Kennedy et al., 2002; Byers and Noonburg, 2003; Stachowicz and Byrnes, 2006). On a local scale, Dunstan and Johnson (2004) showed that the probability of invasion of patches subject to similar environmental conditions is determined largely by the specific properties of component species and their local interactions, rather than being an inherent function of local species richness. Consequently, on a local level, for a given propagules availability, invasion resistance is inextricably and intricately related to the particular patterns of mortality, growth and inter-specific interactions. Depending on these features, invasion rates may decrease (Kennedy et al., 2002; Stachowicz et al., 2002; Yonekura et al., 2004; France and Duffy, 2006) or increase (Dunstan and Johnson, 2004; Zaiko et al., 2007). In the Mediterranean, Klein et al. (2005) presented unclear relationships between native and non-indigenous species richness, probably due to the lack of a truly rich and undisturbed reference site in their sampling design. All the sampling stations were areas close to big harbors in highly urbanized areas (i.e., Marseille and Toulon); the authors considered then that the very high rate of introductions in the Mediterranean and the great success of introduced macrophytes along the French coast may have resulted from human-made changes on the coastal environment over several decades.

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There is also growing evidence that facilitation, i.e. positive species interactions, plays an equally important role in shaping communities and ecosystems (Bruno et al., 2003; Stachowicz and Byrnes, 2006; Bulleri et al., 2008). For example, on Mediterranean rocky reefs, both encrusting and turf forming algae facilitate the anchoring of stolons of the exotic algae Caulerpa racemosa by providing a more complex substratum than bare rock (Bulleri and Benedetti-Cecchi, 2008; Klein and Verlaque, 2008). Similarly, in British waters, Tweedley et al. (2008) suggested that the presence of Zostera marina beds may actually enhance Sargassum muticum colonization of soft sediments, trapping drifting fragments and allowing viable algae to settle on the seagrass matrix in an otherwise unfavorable environment. Bulleri et al. (2008) considered that facilitation is a scale dependent process, because the larger the area over which the observation or manipulation is conducted, the larger the number of native species (and potential facilitating traits) that are included. Indirect effects involve more than two species and are defined as how one species alters the effect that another species has on a third (Paine, 1980). These complex interactions are often overlooked in studies of interactions between NIS and native species. Their influence on biological invasions has been rarely considered and their inherent unpredictability is challenging (White et al., 2006). A mathematical approach of invasibility degree suggested that invasion resistance is a matter of scaling up, varying between complete resistance to partial resistance (Hewitt and Huxel, 2002). These findings indicate that the inoculation density of the non-indigenous species has a greater influence on its invasion success than the number of simultaneous invaders. However, in the model developed by Hewitt and Huxel (2002) when two species were allowed to invade per time step, invasion resistant states did not occur in any of the 20 simulated communities, even after 10,000 invasion events. Thus, as human activities and transport mechanisms continue to reduce the isolation of regional biota from one another, the numbers of species and inoculation densities of invaders will increase and result in higher susceptibilities to invasion in recipient regions and communities. CAN MPAS HINDER NIS INVASION? The degree of invasibility by NIS is either directly or indirectly related to several community parameters such as species richness, habitat complexity, interactions between species and parameters related to NIS characteristics such as propagule pressure, ability to spread or to be transported by a vector (e.g. vessels, currents, etc.). A degraded ecosystem seems to be more sensitive to invasion than a pristine one, at least at the first step of invasion. In literature, few papers tested this hypothesis in marine reserves (Byers, 2005; Klinger et al., 2006; see also Simberloff, 2000 for a general review). Byers (2005) studied a system of intertidal reserves in northern Puget Sound, Washington, in the northwestern U.S. and addressed the issue of NIS in marine reserves.

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Specifically, he focused on non-indigenous clam species and the resultant impact of these species on native clams within and outside of reserves throughout the archipelago. Marine reserves substantially augmented the density, biomass, and size structure of the heavily harvested NIS. In contrast, the two non-indigenous clams with little to no harvest pressure demonstrated no consistent pattern in abundance with reserve status. Native clams in general, including harvested native species, also exhibited no significant pattern between reserves and non-reserves. Byers (2005) concluded that the NIS’ shallow burial depth, and not its non-indigenous status per se, best explains why it so heavily benefited from the reserve status (protection from human harvesting) as compared to the native clam. Marine reserves in the San Juan Archipelago were found to contain higher densities of two very different invaders, a sub-tidal seaweed (Sargassum muticum) and an intertidal oyster (Crassostrea gigas), than comparable unprotected areas outside reserves (Klinger et al., 2006). These findings suggest either that the communities within these reserves are less resistant to invasion, or that intrinsic characteristic(s) of these reserve sites facilitate the two NIS’ invasion. Fish or invertebrate grazers that can regulate the abundance of adult S. muticum remain unknown in this region and elsewhere. Similarly, predators of the oyster have never been recorded in the archipelago. Although Klinger et al. (2006) did not yet identify the causal mechanisms, differential rates of human harvest do not appear to be responsible for the patterns observed. They provisionally suggested that physical or biological aspects of the reserves themselves may directly or indirectly facilitate biological invasion. Consequently, they concluded that marine reserves offer a promising management tool for protection of native marine biodiversity, but on their own they do not afford protection against biological invasion, which threatens to erode gains in biodiversity conservation made through the establishment of reserves. These two papers dealing with NIS ecology within MPAs highlighted unexpected findings and the greater susceptibility of MPA to invasion. Are these results applicable to the Mediterranean MPAs? Byers (2005) and Klinger et al. (2006) monitored intertidal or sub-tidal species. Within the Mediterranean, a sea almost without tides, most of the positive MPA effects concern infralittoral or circalittoral ecosystems: Posidonia oceanica seagrass beds, photophilic algal community and coralligenous formations (Francour et al., 2001). We previously showed that one of the main characteristics of marine MPAs (at least older MPAs) is the modification of the trophic structure with an increase of the top-predators biomass. These recoveries of top-predator and consequent trophic changes overtake probably modifications observed within intertidal protected ecosystems. We can then hypothesize different outcomes within Mediterranean MPAs. POSSIBLE CONTROLS OF NIS WITHIN A MPA Invasion biologists typically consider the susceptibility of a NIS species to native predators as a fortuitous condition that increases biotic resistance to invasion (Noonburg and

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Byers, 2005). Within the MPAs, the significant increase of abundance and biomass of the predator functional group allow restoration of a top-down regulation; examples are increasingly being identified in a range of marine ecosystems (Sala et al., 1998; Pinnegar et al., 2000; Tegner and Dayton, 2000; Shears and Babcock, 2003). In a very interesting study, Steneck et al. (2004) used archaeological, historical, ecological and fisheries data to identify three distinct and sequential phases in the trophic structure of kelp forests in the western North Atlantic’s Gulf of Maine. Phase 1 is characterized by vertebrate apex predators and persisted for more than 4,000 years. Phase 2 is identified by herbivorous sea urchins and lasted from the 1970s to the 1990s. Phase 3 is dominated by invertebrate predators such as large crabs and has developed since 1995. They showed that each phase change resulted directly or indirectly from fisheries-induced trophic-level dysfunction. Similarly, in the central Pacific, Stevenson et al. (2007) showed that on coral reefs with limited fishing pressure, large apex predators (groupers, sharks, snappers and jacks larger than 50 cm in length) accounted for 56% of total fish biomass on average, but only 7 and 3% on similar fished areas. It is clear that a complete ban of fishing activity inside a no-take area will not produce a fast recovery of top or apex predators, which characterized Phase 1 as highlighted (see above) by Steneck et al. (2004). Several decades are necessary (Shears and Babcock, 2002, 2003; Barrett et al., 2007; Guidetti and Sala, 2007; but see Palumbi et al., 2008 for the recovery processes). However, the results of fish assemblage monitoring inside the oldest north-western Mediterranean MPAs show a clear increase of ichthyophagous predator biomass (Table 1). We can then hypothesize that this top-down regulation inside MPA could allow control of NIS spreading inside the MPA, at least for fish species. In the most traditional sense, keystone species are top predators which maintain community diversity by preying selectively on competitively superior prey taxa, thereby preventing the exclusion of relatively weak competitors (Paine, 1980). Surprisingly, it is unknown if keystone predators play a similarly important role in invaded communities (Smith, 2006). This author suggested through an experimental design involving tadpoles that a keystone species can significantly modify the competitive hierarchy of the invaded tadpole assemblage and reduced the impacts of a competitively superior invasive species. Predation is not the only eventual NIS regulating ecological process. Interspecific interactions include also competition. The combination of these two processes is known as intraguild predation (IGP), defined as the killing or eating of species that use similar, often limiting, resources and are thus potential competitors (Polis and Holt, 1992). IGP can be observed in many interactions between exotic and native species, as reviewed by Bampfylde and Lewis (2007). Their mathematical model allows highlighting a control of the invasive species by a predator. However, they only considered the interaction between one predator species and one consumer (invasive) species. Consequently, with IGP occurring across multiple trophic levels the outcomes can be unexpected. Most frequently, in multiple trophic levels systems, the higher predator is a generalist and will consume

Mediterranean marine protected areas and non-indigenous fish spreading 135

Table 1. Proportions (biomass) of ichthyophagous species at different level of protection in North Western Mediterranean MPAs.

Status of the site is assessed as a function of the level of protection. R: reserves where some professional fishery activities are allowed; NT: no-take areas (total ban of fishery); OR: sites outside the reserve with no particular regulation of human activities). Predators: only ichthyophagous species are considered; Labrus merula, Labrus viridis, Scorpaena scrofa, Dicentrarchus labrax, Epinephelus marginatus, Serranus cabrilla, Serranus scriba, and Dentex dentex. Source A: recalculated from Ganteaume A., J.G. Harmelin, P. Lelong, J. Rancher and P. Robert (unpublished data). Source B: recalculated from Francour P. (unpublished data). Source C: recalculated from Lenfant P. and J. Pastor (unpublished data). Source D: recalculated from data published in Macpherson et al. (2002) Marine Protected Area (country)

Date of creation

National Park of Port-Cros (France)

1963

Natural Reserve of Banyuls-sur-mer (France)

1974

Natural Reserve of Scandola (Corsica, France)

1975

Natural Reserve of Medes Island (Spain)

1983

Station (status) Gabinière (NT) La Galère (R) Montrémiant (R) Rederis (NT) Cap Abeille (R) North (OR) South (OR) Palazzu (NT) Punta Nera (R) South (OR) North (OR) Protected 1 (NT) Protected 2 (NT) Unprotected 1 (OR) Unprotected 2 (OR)

Proportion of predators (% of total fish biomass) 33.4 16.5 7.5 28.8 24.5 5.8 2.3 44.5 5.0 11.0 13.0

Source; Year of data acquisition A; 2004 B; 2006 B; 2006 C; 2008 C; 2008 C; 2008 C; 2008 B; 2000 B; 2000 B; 1997 B; 1997

14.2 46.8 3.4 1.5

D; 1998 D; 1998 D; 1998 D; 1998

both the intermediate predator and the consumer. The result for biological control may be the reduction of the intermediate predator, while the invasive species population may increase. Further consideration of multiple species interactions and trophic levels in the model framework are required to investigate this problem (Bampfylde and Lewis, 2007; Bulleri et al., 2008). In addition, predation on NIS is a coupled interaction: every invader consumed also enhances the predator population. These predators probably also consume native species.

136 Patrice Francour, Luisa Mangialajo and Jérémy Pastor

Then the invader’s indirect effect via predators could be more harmful to natives than the effect of resource competition from the NIS (Noonburg and Byers, 2005). DOES PARASITE BURDEN MATTER? Parasites are becoming a major concern in conservation biology because of their ability to evolve rapidly and are now recognized as playing an important role not only in aquaculture but also in natural systems (Altizer et al., 2003). During the transfer of a species to a new habitat (as for aquaculture purposes), one of the biggest problems is to anticipate the possible effects of parasites accidentally introduced with the transfer of the host species. Sasal et al. (2004) highlighted that, due to the potential local adaptation of the host and parasite, the re-colonization of a host with its parasites in a protected area may induce changes: 1) in the parasite community of local populations and 2) in the parasite community of the re-colonizing population. Similarly, several examples of unwanted introduction of parasites and their dramatic effects on natural populations have been reported (see the references listed by Sasal et al., 2000, 2004). For example, the nematoda Anguillicola crassus introduced in Europe from Japan is highly virulent to the European eel Anguilla anguilla and has become in just a few years a major contributor to the depletion of this commercial species (Kennedy, 2007). A prominent hypothesis explaining the success of introduced species is that they are relatively free of the effects of natural enemies, the classic “enemy release hypothesis”. Most notably, they may encounter fewer parasites in their introduced range as compared to their native range (Torchin et al., 2002). Recent studies have demonstrated that exotic plant species have less pathogen in their introduced range as compared to their place of origin. This reduced parasite biota gives potentially exotic plants an advantage in comparison to native plants (Agrawal and Kotanen, 2003). In MPAs, very few studies have considered the potential effects of protection on parasite communities (Sasal et al., 1996, 2000, 2004). These studies have shown that parasite species diversity and abundance are higher in MPAs than in non-protected areas. This increase of parasite burden with respect to protection has been related to an increase in the biomass and density of hosts in marine reserves. Sasal et al. (2004) observed no modification in the global parasite community linked with the protection of the host populations. However, the most abundant and less specific parasite species increased their abundance in the protected area. These authors also found a significant relationship between parasite host range (as the number of host species where the parasite species has already been found; i.e. the inverse of the specificity) and the percentage of infected hosts. But are the parasites able to mediate marine invasions? Even though this point has been rarely examined (see Torchin et al., 2002 and Diamant, this book), we could hypothesize that a NIS would be more easily parasitized in a MPA than outside, mainly due to lack of resistance to local parasites. In addition, the vector of introduction of NIS is important to

Mediterranean marine protected areas and non-indigenous fish spreading 137

consider (Torchin et al., 2002). Those species presumably introduced via ballast water tend to have the fewest parasites in the introduced range. On the other hand, species introduced as biological contaminants or for food typically harbor a subset of the parasite species present in their native range. In a MPA, a non indigenous fish, such as Lessepsian fish, will then be facing both its own subset of parasites and the abundant naïve local parasites. However, if infected hosts invade a new area and their parasites become established, these invasive parasites may impact native species if they can recruit novel hosts. Often forgotten in studies on the ecosystem functioning, the parasite burden of a MPA could be an excellent regulator of invasive species by exercising a control similar to the predator top-down control. As we have seen, MPAs are conducive to the development of parasites, notably fish parasites. In a protected environment, they take advantage of the largest and most numerous hosts, facilitating transfers from host to host (Sasal et al., 1996, 2000, 2004). However, not enough studies are currently available that examined the links of protection-parasites and invasion-parasites to know the extent of parasitism impact on NIS invasion within a MPA. CONCLUSIONS At present, a relevant part of the long list of alien fish recorded in the Mediterranean is represented by occasional records (see the other chapters of this book). In the eastern Mediterranean, several new populations of Lessepsian species are exploited by fisheries. Currently such fisheries are sustainable probably due to the lack of “natural” predator species able to play this role of regulation (Harmelin-Vivien et al., 2005; Galil, 2007). Classically, Lessepsian species were expected to be limited to the eastern Mediterranean basin, due to hydrological conditions (Mavruk and Avsar, 2008), but the spread to the western basin is now a reality. So far, only a few Lessepsian fish species have been observed in the western Mediterranean basin: Abudefduf vaigiensis (Pomacentridae), Siganus luridus (Siganidae), and Fistularia commersonii (Fistularidae). This latter is probably the fastest-spreading species in the Mediterranean: since the first record in Mediterranean ten years ago, F. commersonii is now reported more or less in the whole Mediterranean (Table 2). The modification of the main current circulation experienced by the Mediterranean during the last few decades could deeply modify the exchanges of water between the western and eastern basins (Lascaratos et al., 1999) and some models permit the possibility of an additional surface salt content in many regions of the western basin (Gasparini et al., 2005). These new oceanographic conditions, associated with the present warming of the western basin (Francour et al, 1994; Bianchi, 2007; but see also Olita et al., 2007) could facilitate the spreading of Lessepsian species within the western basin. The very recent records of F. commersonii and S. luridus in the north western Mediterranean could then be the hint of future extensive spreading of Lessepsian species.

138 Patrice Francour, Luisa Mangialajo and Jérémy Pastor

Table 2. Records of three Lessepsian fish species in the western basin of the Mediterranean Species (Family) Abudefduf vaigiensis (Pomacentridae)

References close to Naples and in Ligurian Sea (Vacchi and Chiantore, 2000) Croatia, Adriatic Sea (Dulčić and Pallaoro, 2004); north-east of Tunisia (Charfi-Cheikhrouha, 2004); island of Linosa, the Siganus luridus (Siganidae) Sicily Strait (Azzurro and Andaloro, 2004); Cape d’Orlando, northern Sicily (Castriota and Andaloro, 2005); close to Marseille, France (Daniel et al., 2009) Eastern Mediterranean basin (e.g. Galil, 2007); southwestern Adriatic Sea (Dulčić et al., 2008; Joksimovic et al., 2008); northern Sicily (Pipitone et al., 2004); Sardinia (Pais et al., 2007); central (Psomadakis et al., 2008) and northern Fistularia commersonii Tyrrhenian Sea (Micarelli et al., 2006; Ligas et al., 2007); (Fistularidae) Ligurian Sea (Gabribaldi and Orsi Relini, 2008; OcchipintiAmbrogi and Galil, 2008); Iberian Peninsula (Sanchez-Tocino et al., 2007); eastern and central Algeria (Kara and Oudjane, 2008); Tunisia (Charfi-Cheikhrouha, 2004)

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Colonization of the Mediterranean Red Sea fishes via (Eds.) the Suez Canal – Lessepsian migration 145 D. Golani & B.byAppelbaum-Golani 2010 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 145-188. © Pensoft Publishers Sofia–Moscow

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration Daniel Golani

BRIEF HISTORY AND DESCRIPTION OF THE SUEZ CANAL History The idea of excavating a canal connecting the Mediterranean and the Red Sea originated in ancient times. In the 7th and 6th centuries B.C.E. during the reign of Pharoah Nehco II a canal was dug connecting the Nile River and the Bitter Lakes. This canal was widened and reinforced during the next few centuries. The final renovation of this canal was executed by the Roman Emperor Trajan in 98-117 C.E. The aspiration of establishing a direct sea route between the Mediterranean and Red Sea was discussed in the 16th century during the rule over Egypt of the Ottoman Empire. The Ottomans had a commercial interest in enabling their fleet to reach the Red Sea in order to facilitate trade with India and other countries bordering the Indian Ocean. The Turks also desired a shorter route for their Moslem pilgrims making the Haj to Mecca. In 1671 the German scientist and philosopher Gottfried Wilhelm Leibnitz delivered a memorandum entitled “Consilium Aegyptiacum” to the French emperor Louis XIV, demonstrating the feasibility and benefits of a canal between the Mediterranean and Red Sea. When Napoleon invaded Egypt in 1798-1801 the matter of digging a canal was raised once again. But the plan was dealt a blow by the conclusion reached by Napoleon’s chief engineer Le Père who believed that the higher sea level of the Red Sea (reaching 10 m during high tide) would cause massive floods in Lower Egypt if a canal were built. But nearly half a century later, a group of prominent diplomats and scientists from England, France, Germany and Austria, led by the Austrian Alois Nigrelli, concluded that the differences in sea level between the Red Sea and the Mediterranean were actually much less than previously thought and that a canal could be feasible.

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The decisive thrust toward actualizing the dream to dig the Suez Canal came in 1852 when the French diplomat Ferdinand de Lesseps submitted a detailed plan to Abbas Pasha, then governor of Egypt. Two years later, following the death of Abbas Pasha and the succession by Said Pasha in 1854, de Lesseps received the concession to excavate the Suez Canal. An additional five years of diplomatic negotiating and financial division of rights between shareholders passed prior to the actual commencement of the project on 25 April 1859. It took over ten years of massive digging by hand by Egyptian fellahs and prisoners with the aid of a few machines imported from Europe before the Suez Canal was finally completed on 15 August 1869 (Fig. 1). The official ceremony celebrating the opening of the Canal connecting the Mediterranean and Red Seas was held some three months later with the participation of international diplomats, royalty and nobility. In honor of the great event, the composer Josepa Verdi wrote the opera Aïda which was first performed in 1871. Description of the Suez Canal The Suez Canal has been described as a narrow and shallow capillary connecting the Red Sea and the Mediterranean Sea, which are two major bodies of water with fundamentally different fauna. The length of the Suez Canal is 162.5 km. Nearly 70 km of the Suez Canal were excavated through dry land while the remainder of the Canal passed through the existing waters of the Timsah and Bitter Lakes and the swampy areas of Lake Menzaleh and Lake Ballah (Fig. 2). The Canal was deepened and widened in consequent years and the

Fig. 1. Illustration of the construction of the Suez Canal (Source: E. Riou in Fontane, 1869)

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Fig. 2. Map of the Suez Canal

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Egyptian government plans to deepen and widen it further in order to allow the passage of larger ships (Table 1). The high level of salinity is considered one of the most important factors determining the rate of biota influx into the Suez Canal. The northern lakes of Manzaleh, Ballah and Timsah had a periodic connection with the Nile Delta System which created a brackish oligohaline environment with considerable seasonal fluctuations in salinity levels. In October 1871, two years following the opening of the Canal, Tissot (1872) (as sited by Morcos, 1972, 1980) reported salinity levels of close to 70‰ in the Great Bitter Lake; there are some doubts as to the preciseness of his calculations, due to limitations in the instruments used for measurement at that time. Only 3-4 months later in February 1872 salinity levels dropped by almost 10‰ (Morcos, 1972, 1980). This sharp drop could be due to seasonal fluctuations. However, the general trend was one of fast water dilution and sharp lower levels of salinity, leading Fox (1929) to predict that the salt beds of the Bitter Lakes would be dissolved by the end of the 20th century. In 1934 Ghazzawi (1939) reported salinity values of 44.4-47.5 ‰ at depths of 5 m and two decades later, the salinity of the Bitter Lakes was recorded as 40-45‰; other areas of the Canal, including at its two openings in the north and south, were measured and showed quite similar levels of salinity (Morcos, 1980). The temperature regimes in the Suez Canal resemble those measured at the shores of the Eastern Mediterranean and in the northern Gulf of Suez (Oren, 1969). Temperatures rise to 29-30o C during July-September and drop to 14-15o C during the height of the winter in January and February. However, in some shallow lagoons and swamps, temperatures can reach extreme values above and below those measured in the main body of the Canal. The currents regime in the Suez Canal is influenced by several factors such as differences in sea level at both entrances to the Canal, tidal regimes, local winds and variations in levels of evaporation. Measurements taken at the Canal (see: Por, 1978; Galil, 2008) concur with results of computer simulations of hydraulic models (Agur and Safriel, 1981) in showing that the prevailing currents in the Canal are of low velocity. During most of the year (October-June) they are of a northward direction while during the height of the summer and the beginning of the autumn they flow in the opposite

Table 1. Enlargement of the Suez Canal (width and depth) in meters Year 1869 1958 1972 1999 2010 (est.)

Width 59-98 125 250 300-365 400

Depth 8 13 14.7 17.7 25

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direction (Agur and Safriel, 1981). It is quite likely that the planned widening of the Suez Canal will intensify the strength of the Canal’s currents. BIOGEOGRAPHY OF MIGRATION OF LESSEPSIAN ORGANISMS TO THE MEDITERRANEAN As a result of the opening of the Suez Canal, both the Red Sea and the Mediterranean Sea were exposed to the possibility of invasive species from each other. Yet it soon became clear that the main movement of migrant organisms has been from the Red Sea to the Mediterranean; only a small number of species have migrated from the Mediterranean to the Red Sea. This phenomenon of migration of Red Sea biota to the Mediterranean via the Suez Canal has been named “Lessepsian migration” in honor of Ferdinand de Lesseps, the chief promoter of the Suez Canal (Por, 1969, 1971). In order for a species to migrate from the Red Sea into the Mediterranean it must successfully pass through substantial obstacles in the Suez Canal (Ben-Yami and Glazer, 1974). The higher the level of difficulty in overcoming barriers, the greater the part that chance plays in successfully arriving to the target area (Ehrlich, 1986; Mollison, 1986); regarding the Suez Canal, these physical and ecological obstacles include the shallowness of the Canal, its narrowness, its high salinity, its lack of rocky substrate that could serve as refuge areas and pollution from maritime activity. Golani (1998) maintained that the element of chance constitutes an important factor in determining the crossing of the Canal and entering the Mediterranean. However, once a Lessepsian migrant has arrived into the Mediterranean and established a sustainable population, there are no significant physical barriers preventing their dispersal westward (see below for more on distribution of Lessepsian migrants). Por (1973) summarized the data from various sources comprising an inventory of Red Sea species that were recorded in the Mediterranean in the first century after the opening of the Suez Canal. In his later work (Por, 1978) he expressed the view that “Lessepsian migration is eventually approaching a plateau”. It is now recognized that the situation is quite the opposite. Fig. 3 illustrates the dramatic changes in number and percentages of the various taxa of Lessepsian migrants. However one should take into account that the increase in the number of known species is also a result of the scientific effort exerted in research on various taxa. One prominent example of the contribution of increased scientific efforts in discovering new Lessepsian migrants is that of Foraminifera. Little was known about this class of small benthic organisms in the Levant until recent studies revealed more than 30 species of Red Sea origin in the Mediterranean (Meriç et al., 2006). Mollusks have increased dramatically in number and percentage of Lessepsian migrant species; this increase may be attributed to the tremendous rise in collection activity, both by scientists and especially by amateurs. In addition, most mollusks have

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M

O L 41 LU .1 SC % S

S OD AP % C DE 14.1

A

ER NIF MI RA 9.2%

FO

F 20 ISH .1 %

POL YCH A 8.6% ETS

OTHER 1.2%

Fig. 3. Percentages of Lessepsian migrant species by taxa; inner circle from Por (1971) representing the situation at the end of the first century following the opening of the Suez Canal; outer circle by the author, representing the current percentage of number of species per taxa

hard shells which remain after their death and allow detection of abortive colonization attempts, which is not the case in fish and other taxa. The scientific study of fishes has an advantage over other groups since commercial fishery exploitation provides extensive quantitative and qualitative data by means of “samples” from the local environment. In addition, the taxonomy of fishes is relatively clear, thus facilitating the documentation of new records and the verification of new species in the target area. LESSEPSIAN FISH SPECIES – HISTORY AND RATE OF INVASION More than 30 years after the opening of the Suez Canal, the first Red Sea fish Atherinomorus forskali was found in the Mediterranean Sea near the port of Alexandria, Egypt, by Tillier (1902) (as Atherina forskalii). Another 25 years passed before the report by Prof. W. Steinitz (1927) from British Mandatory Palestine of an additional four Red Sea fish species in the vicinity of Haifa: Hemiramphus far (as Hemiramphus marginatus), Alepes djedeba (as Caranx calla), Siganus rivulatus (as Teuthis sigana) and Stephanolepis diaspros (as

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 151

Monacanthus setifer). In that same year Norman (1927) recorded Hyporhamphus affinis (as Hyporhamphis dussumieri), Liza carinata (as Mugil sehli) and Corygalops ochetica (as Gobius ocheticus) from Egypt and the northern Mediterranean shores of the Sinai Peninsula. By the middle of the 20th century, an additional ten Red Sea fish species were recorded from the Mediterranean, all as sporadic records or as part of lists of commercial fishes. In the first comprehensive study of the ichthyofauna of Israel, conducted by BenTuvia (1953a), and in his subsequent papers and short notes (Ben-Tuvia,1953b, 1955), another six Lessepsian fish species were added, reaching 24 species. Most of the newly recorded Lessepsian migrant fish from the 1960’s were sporadic records of species that failed to establish large populations in the Mediterranean, with the exception of Etrumeus teres. The case of E. teres is of great interest. A single specimen was collected in October 1961 in purse seine catch in Haifa Bay, Israel (Whitehead, 1963). During the next three decades, not a single specimen of this species was recorded in the Mediterranean. In the early 1990’s it reappeared in large numbers in the commercial catch in Egypt (El Sayad, 1994), Israel and Cyprus (Golani, 2000a) and in Turkey (Başusta et al., 1997). Soon its rapid population increase was followed by a rapid westward distribution enlargement and it reached Crete (Kasapidis et al., 2007) and Lampedusa Island in the central Mediterranean (Falautano et al., 2006). It can be postulated that the earlier record represented an abortive attempt of colonization while its reappearance and subsequent success at establishing a sustainable population were the result of a second invasion event. Alternatively, it is possible that the species was very rare in its new habitat and therefore not collected in the interim period. From the 1970’s onward, the rate of recorded new arrivals of Lessepsian migrant fish rose sharply, with new species being added nearly every year. LIKELIHOOD OF LESSEPSIAN MIGRANTS BEING RECOGNIZED A number of factors affect the chances of a new Lessepsian migrant being discovered and recorded. This issue is related to the question, when does colonization of a particular migrant begin and when does that species become established in the target area. Clearly the chances of a species being caught and recorded grow with its population growth in its new area. Another important factor is the appearance of the particular fish; striking colors or unusual structural formations may facilitate its differentiation from indigenous species. For example, the Lionfish Pterois miles (Bennett, 1803) (Golani and Sonin, 1992) and the Red Sea Bannerfish Heniochus intermedius Steindachner, 1893 (Gokuglu et al., 2003) were easily spotted in the Mediterranean due to there conspicuous appearance, even though only one specimen of each has been recorded there so far. But when a species has a superficial resemblance to an existing indigenous species, it may be discovered only after some time has passed by an expert ichthyologist who is able to recognize the significant, albeit small, distinguishing characteristics. Another factor affecting the chance

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of discovery is the type of habitat. If a migrant species inhabits a particular habitat that is sampled infrequently, it may go undetected for years. POPULATION GROWTH OF LESSEPSIAN MIGRANT FISHES The general pattern of population growth of Lessepsian fish in the Mediterranean is hypothesized to be initiation by a small founder group that gradually expands its population size. Although monitoring of the population dynamics of Lessepsian migrants in their new habitat has been limited, quantitative studies allow us a good estimation of these processes. A classic example is provided by the Red Squirrelfish Sargocentron rubrum. The first specimen of S. rubrum was recorded along the coast of Israel in the late 1940’s (Haas and Steinitz, 1947). Two decades later, it was still considered rare (Ben-Tuvia, 1966). By the 1980’s S. rubrum became common (Golani and Ben-Tuvia, 1985) and ten years later it was the most abundant species in the artificial reef and in experimental trammel net catch near Haifa, Israel (Spanier, 2000). Another case in point is that of the Narrow-Barred Spanish Mackerel Scomberomorus commerson. This species was first recorded in the Mediterranean by Hornell (1935). It remained rare for some time; Ben-Tuvia (1953a, 1966) did not include it among Israeli ichthyofauna. In the late 1970’s it was considered rare (Ben-Tuvia, 1978). By the end of the 1990’s S. commerson became the most common species among the large scombrids and has been caught in large numbers in trammel nets and longline along the Mediterranean coast of Israel. Bahkoum (2007) reported the recent increase in Egypt of the catch of this species, reaching an annual catch of 1,300 ton. The Red Sea Tonguesole Cynoglossus sinusarabici was first recorded in the Mediterranean as a rare species by Ben-Tuvia (1953a). In a later work (Ben-Tuvia, 1966) it was described as being “found quite frequently among trawl fishes”. A decade later, Ben-Tuvia (1978) designated it as common. At present this species is very common and found in large numbers in trawl catches at depths of 20-50 m. However there are many cases of migrant species whose population exploded almost immediately following the initial colonization event. The best documented case of population explosion is that of the Brushtooth Lizardfish Saurida undosquamis. The first specimens were found in the Mediterranean in 1952 and after only two years, it became a major commercial species whose catch increased steadily during the next four years, reaching close to 400 tons in 1960, constituting ca. 20% of the Israeli trawl catch (Ben-Yami and Glaser, 1974; Golani and Ben-Tuvia, 1995). Other cases of Lessepsian fish species undergoing a population explosion shortly after invasion are concentrated in two distinct five-year periods. The Whiting Sillago sihama was first recorded from Lebanon in 1977 (Mouneimne, 1977) and one year later the Sweeper Pempheris vanicolensis was found in the same region (Mouneimne, 1979).

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 153

Within a matter of months both species became very common in the Eastern Mediterranean, the former on sandy substrate in shallow waters and the latter in shallow waters of caves and grottos. The Peter’s Goby Oxurichthys petersi was first found in 1982 in the Mediterranean (as O. papuensis) as a well established large population (Ben-Tuvia, 1983). The second wave of Lessepsian population explosions occurred from 2000 to 2005. The Bluespotted Cornetfish Fistularia commersonii was first recorded in the Mediterranean in January 2000 in the vicinity of Ashdod, Israel (Golani, 2000b). A few months later, very large populations of F. commersonii were observed in various locations in the Eastern Mediterranean. Within two years this species was recorded from the Island of Rhodes (Corsini et al., 2002) and it took only another two years for it to reach the central Mediterranean (Azzurro et al., 2004). A year later F. commersonii was found in Sardinia (Pais et al., 2007) and Spain (Sánchez-Tocino et al., 2007) , making it the first Lessepsian migrant to reach the western basin of the Mediterranean and earning it the titles “Champion of the Lessepsian Fishes” and “The Lessepsian Sprinter” (Karachlė et al., 2004). In November 2001 the venomous Striped Eel Catfish Plotosus lineatus was first found in large numbers in trawl catch near Ashdod, Israel (Golani, 2002). This fish is currently very common on soft bottom substrates at depths of 20-40 m, as well as in the vicinity of rocky habitats. It appears in large numbers in trawl catches and has caused some fishermen to be severely injured, in some cases even hospitalized (Gweta et al., 2008). An additional case of population explosion just subsequent to colonization is that of the Elongated Puffer Lagocephalus sceleratus which was first found in the Mediterranean in Gokova Bay, Turkey (Filiz and Er, 2004). An earlier record of Mouneimne (1977) of this species was based on a misidentification of Lagocephalus suezensis (see: Golani, 1996). This poisonous fish spread rapidly throughout the Eastern Mediterranean (Golani and Levy, 2005). Being an attractive, large bodied and relatively common fish, it is often caught by amateur fishermen who unwittingly consume its flesh and inner organs and then often suffer severe poisoning and hospitalization (Eisenman et al., 2008; Bentur et al., 2008). Two Lessepsian fish that were recorded recently for the first time in the Mediterranean and soon became essential components of the commercial catch along the Israeli coast are the Threadfin Bream and the Indian Scad. In February 2005 Golani and Sonin (2006) reported from Haifa Bay, Israel, the first record in the Mediterranean of Randall’s Threadfin Bream Nemipterus randalli (erroneously reported as N. japonicus). In December 2005 several specimens of the Indian Scad Decapterus russelli were found by Golani (2006) among purse seine catch, also in Haifa Bay. Both species have already spread westward to Turkey (Bilencennoglu and Russell, 2008; Gokuglu et al., 2008) and north to Lebanon (Lelli et al., 2008). The issue of the phenomenon of population explosions among Lessepsian fish species soon after their initial colonization is part of a wider area of study concerning the causes of different degrees of success of these migrant species in establishing large, sustainable populations in the target area. Several explanations have been presented in

154 Daniel Golani

literature concerning Lessepsian migrants. One of the models maintains that Lessepsian fish originated from a rich and diverse tropical or sub-tropical ecosystem and therefore possess a superior competitive advantage over indigenous Mediterranean species from a poorer temperate region (Ben-Tuvia, 1978; Por, 1978). Another model emphasizes the nature of the target area, i.e., the Mediterranean. According to this model, Lessepsian migrants succeed in inhabiting “unsaturated” or “empty niches”, whether bathymetrical or trophic or diurnal. Examples given to illustrate this model are the massive successes of the two siganids Siganus rivulatus and S. luridus in their new environment. Golani (1993b) and Lundberg and Golani (1995) explain the success of these siganids by noting that indigenous Mediterranean fish originated mainly from the temperate Atlantic Ocean which lacks herbivores, due to the low temperatures prevailing throughout long periods of the year which hinder or prevent digestion of plants. Therefore the herbivorous siganids of tropical origin had an advantage in the sub-tropical environment over indigenous species which enable to adapt to their new Mediterranean environment by exploiting presumably an unsaturated niches. Similarly, the success of several nocturnal species such as Apogon pharaonis, Apogon smithi, Sargocentron rubrum and Pempheris vanicolensis can be attributed to the paucity of Mediterranean indigenous species in this underexploited temporal niche. The ultimate cause or causes for sudden increases in population among Lessepsian fish in the Mediterranean, whether occurring just after initial colonization or many years later, may be difficult to determine and in many cases remains speculative. One of the cases still under study is that of the sudden and remarkable increase in population of the Goldband Goatfish Upeneus moluccensis in Israeli fishing grounds in 1955 (Ben-Yami, 1955; Oren, 1957); these authors claimed that the increased population of U. moluccensis was a direct result of the slightly higher temperatures (a rise of 1-1.5 °C in the winter months). If this is indeed the ultimate reason for the sudden population explosion, one may ask why only U. moluccensis was affected but not other presumably thermophilic Lessepsian fish species that were known to be in the same areas of the eastern Mediterranean at that time. Furthermore, there are records of other periods (1977-1982 and 2000-2006) during which many Lessepsian species experienced population explosions despite the winter temperatures being no higher than normal. So far no clear correlation between temperature and population explosion of Lessepsian fishes has been found. Figure 4 shows a clear correlation between the year of first record of particular Lessepsian species in the Mediterranean and that species’ current abundance along the Israeli Mediterranean coast. The general trend is that those species that were recorded earlier are currently more abundant. Although date of first record is not necessarily identical with the moment in time when the species first arrived to the Mediterranean, it is logical to presume that the chance that a species will be collected and recorded increases with the growth of its population following its arrival to the target area (see Table 2). Therefore, we can use the date of first record as a baseline for initiation of a species’ colonization. This correlation may be explained as follows: Firstly, the more time

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 155

80 very rare rare prevalent common very common

Number of species

60

40

20

0 1900

1920

1940

1960 Years

1980

2000

2020

Fig. 4. Cumulative number of Lessepsian fish migrants and their current abundance in the Mediterranean

elapsed since colonization, the better the opportunity to establish a large, flourishing population. In addition, the species may adapt further to its new habitat during these first years. Secondly, the species may possess superior colonizing and adapting abilities that gave them a competitive edge over other species, allowing them to arrive first and closely thereafter establish a population. In addition, the increase in ichthyological studies in the last few decades may have led to more first records, some of which were detected primarily due to the use of intensive ichthyological research methods. DISTRIBUTION OF LESSEPSIAN MIGRANT FISH Observation and monitoring of the distribution of Lessepsian fish species reveals a clear east-west gradient of the number of species that spread into the new region (Fig. 5). There are numerous factors that affect the extent that a Lessepsian fish species disperses westward, including timing, inherent pre-adaptive characteristics and the characteristics of the local indigenous ichthyofauna.

Common Name

Guitarfishes Halavi Guirarfish Stingrays Forsskål’s Stingray Sardines Rainbow Sardine Red-eye Round Herring Spotted Herring Delicate Round Herring Conger eels Trewavas’ Conger Eel Pike congers Daggertooth Pike Conger Lizardfishes Brushtooth Lizardfish

Family; Species

RHINOBATIDAE Glaucostegus halavi (Forsskål, 1775) DASYATIDAE Himantura uarnak (Forsskål, 1775) CLUPEIDAE Dussumieria elepsoides Bleeker, 1849 Etrumeus teres (DeKay, 1842) Herklotsichthys punctatus (Rüppell), 1837 Spratelloides delicatulus (Bennett, 1831) CONGRIDAE Rhynchoconger trewavasae Ben-Tuvia, 1993 MURAENESOCIDAE Muraenesox cinereus (Forsskål, 1775) SYNODONTIDAE Saurida undosquamis (Richardson, 1848)

Table 2. List of Lessepsian fish migrants

Ben-Tuvia, 1955 Whitehead, 1963 Bertin, 1943

Israel, 1949

Ben-Tuvia, 1953

Israel, 1952

Indo-Pacific

Golani and Indo-Pacific Ben-Tuvia, 1982

Israel, 1979

Red Sea

Ben-Tuvia, 1993

Indo-Pacific

Red Sea

Cosmopolitan

Indo-Pacific

Indo-Pacific

Indo-Pacific

Original distribution

Israel, 1987

Israel, before 1943 Israel, 1973 Ben-Tuvia, 1978

Ben-Tuvia, 1955

Israel, 1954

Israel, 1961

Ben Souissi, et al. 2007

References

Tunis, 2004

1st record and location

Rhodes/Libya

Israel

Israel

Israel

Crete/ Lampedusa Isl Turkey/Egypt

Turkey/Egypt

Turkey/Egypt

Tunis

Single record

Single record

Single record

Mediterranean Remarks distribution: North/southern coasts

156 Daniel Golani

Eel Catfishes Striped Eel Catfish Flying fishes African sailfin Flyingfish Needlefishes Red Sea Needlefish Halfbeaks Spotted Halfbeak Tropical Halfbeak Silversides Forsskål’s Hardyhead Silverside Squirrelfishes Red Squirrelfish Pipefishes & Seahorses Sea Pony

PLOTOSIDAE Plotosus lineatus (Thunberg, 1787) EXOCOETIDAE Parexocoetus mento (Valenciennes, 1846) BELONIDAE Tylosurus choram (Rüppell, 1837) HEMIRAMPHIDAE Hemiramphus far (Forsskål, 1775) Hyporhamphus affinis (Günther, 1866) ATHERINIDAE Atherinomorus forsskali (Rüppell, 1838)

Hippocampus fuscus Rüppell, 1838

HOLOCENTRIDAE Sargocentron rubrum (Forsskål, 1775) SYNGNATHIDAE

Common Name

Family; Species

Indo-Pacific

Red Sea

Steinitz, 1927

Israel, 1927 Northern Sinai, Norman, 1927 1924 Alexandria, Egypt, 1902

Haas and Steinitz, 1947

Golani and Fine, 2002

Israel, 1945

Israel, 1994

Tillier, 1902

Indo-Pacific

Parin, 1967

Lebanon, 1962

W. Indian Ocean

Indo-Pacific

Indo-Pacific

Indo-Pacific

Bruun, 1935

Israel, 1935

Indo-Pacific

Original distribution

Golani, 2002

References

Israel, 2001

1st record and location

Israel/Antalya, Turkey

Dodecanese /Libya

Dodecanese /Tunisia

Lebanon/N. Sinai

Rhodes/Libya

Lebanon

Albania/Libya

Israel

Two records only

Two records only

Mediterranean Remarks distribution: North/southern coasts Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 157

Cornetfishes Bluespotted Cornetfish

Scrpionfishes Lionfish, Turkeyfish Flatheads Mentacled Flathead

FISTULARIDAE Fistularia commersonii Rüppell, 1835

SCORPAENIDAE Pterois miles (Bennett, 1828) PLATYCEPHALIDAE Papilloculiceps longiceps (Eherenberg in Valenciennes, 1829) Platycephalus indicus (Linnaeus, 1758) Sorsogona prionota (Sauvage, 1873) SERRANIDAE Epinephelus coioides (Hamilton, 1822) Epinephelus malabaricus (Bloch & Schneider, 1801) TERAPONIDAE Pelates quadrilineatus (Bloch, 1790)

Terapons Fourline Terapon

Indian Flathead Halfspine Flathead Groupers Orange-spotted Grouper Malabar Grouper

Common Name

Family; Species

Ben-Tuvia and Lourie,1969 Ben-Tuvia and Lourie,1969

Israel, 1966

Israel, 1969

Israel, 1966

Golani and Ben- W. Indian Tuvia, 1990 Ocean

Israel, before 1946

Lourie and Ben- Indo-Pacific Tuvia, 1970

Indo-Pacific

Indo-Pacific

Ben-Tuvia, 1953 Indo-Pacific

Israel, 1953

Golani and Ben- W. Indian Tuvia, 1990 Ocean

Israel, 1986

Indian Ocean

Indo-Pacific including E. Pacific

Original distribution

Golani and Sonin, 1992

Golani, 2000b

References

Israel, 1991

Israel, 2000

1st record and location

Iskenderun, Turkey/Egypt

N. Adriatic Sea/ Israel Israel

Israel

Lebanon/Egypt

Israel

Israel

Gibraltar/ Tunisia

Single record

Single record

Single record

Mediterranean Remarks distribution: North/southern coasts

158 Daniel Golani

CARANGIDAE Alepes djedaba (Forsskål, 1775)

Jacks, Scades Shrimp’s Scade

Cardinalfishes Broad-banded Cardinalfish Bullseye Cardinalfish Signal Cardinalfish Smith’s Cardinalfish Sillagos Silver Sillago, Whiting Cobia Cobia

Israel, 1927

Steinitz, 1927

Indo-Pacific

Golani and Ben- Cosmopolitan Tuvia, 1986 in warm water (except w. America

Israel, 1978

Indo-Pacific

W. Indian Ocean W. Indian Ocean Indo-Pacific

Indo-Pacific

Mouneimne, 1977

Goren et al. 2009 Haas and Steinitz, 1947 Eryilmaz and Dalyan, 2006 Golani et al., 2008

Lebanon, 1977

Israel, before 1946 Iskenderun, Turkey, 2004 Israel, 2007

Israel, 2008

N. Sinai, Egypt, Ben-Tuvia, 1977 Indo-Pacific 1973 Piran, Slovenia, Lipej et al, 2008 Indo-Pacific 2007

Spiny-cheeked Terapon Largescaled Terapon

Original distribution

Terapon puta (Cuvier, 1829) Terapon theraps Cuvier & Valenciennes, 1829 APOGONIDAE Apogon fasciatus (White, 1790)* Apogon pharaonis Bellotti, 1874 Apogon queketti Gilchrist, 1903 Apogon smithi Kotthaus, 1970 SILLAGINIDAE Sillago sihama (Forsskål, 1775) RACHYCENTRIDAE Rachycentron canadum (Linnaeus, 1766)

References

1st record and location

Common Name

Family; Species

Aegean Sea/ Egypt

Israel

Aegean Sea/ Egypt

Iskenderun, Turkey/Israel Iskenderun, Turkey/Israel

Rhodes/Israel

Israel

Piran, Slovenia

Single record

Single record

Mediterranean Remarks distribution: North/southern coasts Lebanon/Egypt Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 159

Upeneus moluccensis (Bleeker, 1855) Upeneus pori Ben-Tuvia & Golani, 1989

Nemipterus randalli Russell, 1986 MULLIDAE

Gruvel, 1931

Mouneimne, 1979

Golani and Sonin, 2006

Haas and Steinitz, 1947 Kosswig, 1950

Syria, 1931

Lebanon, 1977

Israel, 2005

Israel, before 1946 Turkey, 1942

Dalyan and Eryilmaz, 2009

Iskenderun, Turkey, 2004

Ponyfishes Klunzinger’s Ponyfish Snappers Mangrove Red Snapper Thredfin Breams Randall’s Threadfin Bream Goatfishes, Red Mullet Goldband Goatfish Por’s Goatfish

Golani, 2006

Israel, 2005

Indian Scad Arabian Scad

Decapterus russelli (Rüppell, 1830) Trachurus indicus Nekrasov, 1966 LEIOGNATHIDAE Leiognathus klunzingeri (Steindachner, 1898) LUTJANIDAE Lutjanus argentimaculatus (Forsskål, 1775) NEMIPTERIDAE

References

1st record and location

Common Name

Family; Species

Red Sea and the Gulf of Oman

Indo-Pacific

W. Indian Ocean

Indo-Pacific

W. Indian Ocean

W. Indian Ocean

Indo-Pacific

Original distribution

Aegean Seae/ Libya Rhodes/Tunisia

Antalya Bay, Turkey/Israel

Lebanon

Lampedusa Isl./ Egypt Single record

Mediterranean Remarks distribution: North/southern coasts Iskenderun, Turkey/Israel Iskenderun, Two Turkey specimens

160 Daniel Golani

POMACENTRIDAE Abudefduf vaigiensis (Quoy and Gaimard, 1824) CHAETODONTIDAE Heniochus intermedius Steindachner, 1893

Crenidens crenidens (Forsskål, 1775) Rhabdosargus haffara (Forsskål, 1775) PEMPHERIDAE Pempheris vanicolensis Cuvier, 1831 EPHIPPIDAE Platex teira (Forsskål, 1775)

SPARIDAE

Butterflyfishes Red Sea Bannerfish

Demselfishes Sergean major

Batfishes Teira

Seabreams, Porgies Kerenteen Sea Bream Haffara sea bream Sweepers Sweeper

Grunts, Sweetlips Striped Grunt

Haemulidae

Pomadasys stridens (Forsskål, 1775)

Common Name

Family; Species

References

Original distribution

Indo-Pacific

Bilecenoglu and Indo-Pacific Kaya, 2006

Mouneimne, 1979

Antalya Bay, Turkey, 2002

Gökoglu et al., 2003

W. Indian Ocean

(Gulf of Naples, (Tardent, 1959), Indo-Pacific 1959), Israel, Goren and 1997 Galil, 1998

Bodrum, S. Aegean Sea, 2006

Lebanon, 1978

N. Sinai, Egypt, Lourie and Ben- W. Indian 1970 Tuvia, 1970 Ocean Israel, 1991 Golani, 1992 W. Indian Ocean

(Gulf of Genoa, (Torchio, 1969); W. Indian Ben-Tuvia, 1977 Ocean 1969); Israel, 1971

1st record and location

Antalya/ Lebanon

Israel, Italy(?)

Bodrum, S. Aegean Sea

Dodecaneses/ Tunisia

Israel

Israel/Libya

Lebanon/Egypt

Two records

The Italian records are questionable

Single record

Mediterranean Remarks distribution: North/southern coasts Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 161

Gray mullets Roving Gray Mullet Barracudas Obtuse Barracuda Yellowtail Barracuda Wrasses Peacock Razorfish Sideburn Wrasse Parrotfishes Bluebarred Parrotfish Blennies Arabian Fangblenny Gobies

MUGILIDAE Liza carinata (Valenciennes, 1836) SPHYRAENIDAE Sphyraena chrysotaenia Klunzinger, 1884 Sphyraena flavicauda Rüppell, 1838 LABRIDAE Iniistius pavo Valenciennes, 1840 Pteragogus pelycus Randall, 1981 SCARIDAE Scarus ghobban Forsskål, 1775 BLENNIIDAE Petroscirtes ancylodon Rüppell, 1838 GOBIIDAE Coryogalops ochetica (Norman, 1927) Oxyurichthys petersi (Klunzinger, 1871)

Peter’s Goby

Common Name

Family; Species

Goren and Galil, 1989 Norman, 1927

Israel, 1988

Port Said, Egypt, 1924 Israel, 1982

Red Sea

W. Indian Ocean

Indo-Pacific

W. Indian Ocean

Indo-Pacific

Ben-Tuvia, 1983 Red Sea

Goren and Aronov, 2002

Israel, 2001

Israel, 1991

Corsini et al., 2006 Golani and Sonin,1992

Indian Ocean

Golani, 1992

Rhodes, 2004

Indo-Pacific

Spicer, 1931

Israel, before 1931 Israel, 1991

W. Indian Ocean

Original distribution

Norman, 1929

References

Port Said, 1924

1st record and location

Mersin, Turkey/ Israel

Northern Sinai

Rhodes/Israel

Lebanon/Israel

Rhodes/Israe

Rhodes, 2004

Rhode/Israel

Malta/Tunisia

Iskederun/ Egypt

Singe record

Mediterranean Remarks distribution: North/southern coasts

162 Daniel Golani

Rastrelliger kanagurta (Cuvier, 1816)

SCOMBRIDAE

Siganus rivulatus (Forsskål, 1775)

Siganus luridus (Rüppell, 1828)

Rabbitfishes, Spinefoots Israel, 1955 Dusky Rabbitfish, Squaretail Spinifoot Israel, 1927 Marbled Rabbitfish, Rivulated Spinefoot Tunas, Mackerels Indian Mackerel Israel, 1967

Indo-Pacific Ben-Tuvia, 1953, Tortonese, 1953

Israel, before 1953

SIGANIDAE

Miller and Fouda, 1986 Bilecenoglu et al., 2008

Northern Sinai, 1979 Fethiya Bay, Turkey, 2008

Egyptian Goby Merten’s Shrimpgoby Dragonet Filamentous Dragonet Fethiya Bay, Turkey

Indo-Pacific

Collette, 1970

Indo-Pacific

Israel

Ionian Sea Greece/Tunisia

Steinitz, 1927

Red Sea and the Gulf of Aden

Marseille, France/Tunisia

Ben-Tuvia, 1964 W. Indian Ocean

Rhodes/Israel

Israel/Egypt

Two records

Mediterranean Remarks distribution: North/southern coasts Northern Sinai Single record

Red Sea

Indo-Pacific

Northern Sinai, Kovačić and 1978 Golani, 2008

Blackgill Goby

Original distribution

Papillogobius melanobranchus (Fowler, 1934) Silhouettea aegyptia (Chabanaud, 1933) Vanderhorstia mertensi Klausewitz, 1974* CALLIONYMIDAE Callionymus filamentosus Valenciennes, 1837

References

1st record and location

Common Name

Family; Species

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 163

Common Name

Scomberomorus commerson Lacepède, 1800

Narrow-barred Spanish Mackerel CYNOGLOSSUS Tonguesoles Cynoglossus sinusarabici Red Sea (Chabanaud, 1931) Tonguesole MONACANTHIDAE Filefishes Stephanolepis diaspros Lozenge Fraser-Brunner, 1940 Filefish OSTRACIIDAE Boxfishes Tetrosomus gibbosus Thornback (Linnaeus, 1758) Trunkfish TETRAODONTIDAE Pufferfishes Lagocephalus sceleratus Elongated (Gmelin, 1789) Pufferfish Lagocephalus spadiceus Pufferfish, (Richardson, 1844) Blassop Lagocephalus suezensis Suez Pufferfish Clark & Gohar, 1953 Torquigener flavimaculosus Yellowspotted Hardy & Randall, 1983 Pufferfish Tylerius spinosissimus Spiny Pufferfish (Regan, 1908)

Family; Species

Filiz and Er, 2004 Kosswig, 1950

Gokova Bay, Turkey, 2004 Iskanderun Bay, Turkey, 1950 Lebanon, 1977

Rhodes, 2004

Israel, 1987

Spanier and Goren, 1988

Israel, 1987

Corsini et al., 2005

Mouneimne, 1977 Golani, 1987

Steinitz, 1927

Israel, 1927

Turkey/Egypt

W. Indian Ocean Indo-Pacific

Red Sea

Indo-Pacific

Indo-Pacific

Indo-Pacific

Gokova Bay/ Israel Rhodes

Gokova Bay/ Egypt Dodecaneses/ Marmara/Israel Rhodes/Israel

Israel

Single record

Mediterranean Remarks distribution: North/southern coasts Dodecaneses/ Tunisia

Red Sea and the Sicily/Tunisia Arabian Gulf

Ben-Tuvia, 1953 Red Sea

Israel, before 1953

Indo-Pacific

Original distribution

Hornell, 1935

References

Israel, 1935

1st record and location

164 Daniel Golani

* Recent migrants that are not included in Figs 4-7.

Porcupinefishes Yellowspotted Israel, 1992 Burrfish

DIODONTIDAE Cyclichthys spilostylus (Leis & Randall, 1982)

1st record and location

Common Name

Family; Species

Golani, 1993b

References

Indo-Pacific

Original distribution

Israel

Single record

Mediterranean Remarks distribution: North/southern coasts Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 165

166 Daniel Golani

Fig. 5. Number of Lessepsian fish species in various regions of the Mediterranean

Since the late 1970’s there has been an increase in the amount of ichthyofaunistic studies documenting this westward movement of Lessepsian fish species: from Lebanon (Mouneimne, 1977), from Greece (Papaconstantinou, 1987, 1988; Zenethos et al., 2005; Corsini et al., 2005; Corsini-Foka and Economidis, 2007), from Egypt (El-Sayad, 1992), from Turkey (Gücü et al., 1994; Bilecenoglu et al., 2002; Fricke et al., 2007; Mavruk and Avsar, 2007), from Syria (Saad, 1995), Tunisia, (Bradai et al., 2004) and from Israel (Golani, 1996, 2005). Consequently we now have a greater understanding of the distribution of Lessepsian fish species in the Mediterranean. From 67 species in the Israeli-Lebanese coast, the gradient extends westward fairly evenly along the northern and southern coastlines of the eastern Mediterranean, with the number of species gradually decreasing as one moves westward to the coasts of Sicily and Tunisia. Forty species have been recorded from the southern coast of Turkey from Iskandarun Bay to Antalya (Fricke et al., 2007) and 32 from Egypt (El-Sayad, 1992). The Dodecanese Islands and Gokova Bay at the southeastern Aegean Sea have become the subject of intensified research in the last decade (Corsini-Foka and Economides, 2007, Bilecenoglu et al., 2002; Fricke et al., 2007), revealing 25 Lessepsian fish species. According to Por, this region constitutes the western boundary of the heavy influence of Lessepsian migration, which has its parallel in the Egyptian coastline to Libya; Por proposed calling this region the “Lessepsian Province” (Por, 1990). Very few ichthyological studies were conducted along the Libyan coast until the end of the 20th century. However, new studies conducted in the last decade (Ben-Abdallah et al., 2005; Shakman and Kinzelbuch, 2006, and others) have enumerated 16 Lessepsian fish species along the Libyan coasts and added significantly to our knowledge of Lessepsian fish species distribution along the southern shores of the Mediterranean.

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 167

Eight species were found in the southern Adriatic Sea, most of which are still rare (see: Dragičević and Dulčić in this book). There are two surprising records of single specimens of Lessepsian fish from the northern tip of the Adriatic Sea, Epinephlus coioides (by Parenti and Bressi, 2001) was recorded near Trieste, Italy and Terapen theraps (by Lipej et al., 2008) near Piran, Slovenia. The old record (from 1896) from Rijeka of a single specimen of the Silver Pomfret, Pampus argenteus (by Dulčić et al., 2004) should be considered as a vagrant rather than a Lessepsian migrant since it is not known to inhabit the Red Sea (Last, 2001). The shores of the larger islands in the eastern basin of the Mediterranean (e.g., Cyprus and Crete) are surprisingly low in the number of Lessepsian fish species recorded, namely, 17 and 5, respectively. Therefore these islands are seen as having a paucity of Lessepsian species, especially considering their location along the east-west gradient. This paucity may be explained by the cold temperature regime in the waters surrounding these islands’ coasts, the reduced continental shelf and the relatively large distance from the shores, which are the main routes westward of the advancing Lessepsian migrants (Por, 1978). As of publication, eight Lessepsian fish species have reached the central Mediterranean, off the shores of Tunisia (Bradai et al., 2004; Ben-Souissi et al., 2007) and that of southern Italy (Azzuro et al., 2006 ) and two Lessepsian species Siganus luridus and Stephanolepis diasperos have been recorded from the Tyrrhenian Sea (Castriota and Andoloro, 2005). The Bluespotted Cornetfish (Fistularia commersonii) has invaded the western basin of the Mediterranean; it has been recorded from the island of Sardinia (Pais et al., 2007) and off the eastern and southern coast of Spain (Sánchez-Tocino, 2007). Another Lessepsian migrant, the Dusky Rabbitfish Siganus luridus, also extended its distribution to the western basin; Castriota and Andaloro (2005) reported a small population from the Tyrrhenian Sea and Daniel et al. (2009) collected two specimens from the vicinity of Marseille. However, the increase in the distribution of Lessepsian fish is so rapid that almost each month brings a record in a new area, such that any published list, including in this book, will soon need updating. Those Lessepsian fish species that have been found only along the Israeli-Lebanese (Fig. 6) coast are rare and usually recent invaders. Thus, time is of primary importance as a factor determining westward expansion. However, there are a number of notable examples of Lessepsian migrant fish, such as Sargocentron rubrum and Lagocephalus spadiceus, reported by Laskaridis (1948) and Upeneus moluccensis, reported by Serbetis (1947), that reached the coastal waters of Greece over 60 years ago yet ceased moving westward. At the present time, there is no conclusive explanation why some species continue westward while others do not. Since there is no physical barrier preventing further westward dispersal of Lessepsian fish, the answer to this question must reside in the biotic and/or abiotic levels. The most important abiotic factor affecting dispersal of Lessepsian species is temperature (Por, 1978; Ben-Tuvia and Golani, 1995). It has been demonstrated that

168 Daniel Golani 80

Number of species

60

40

20

0 1900

1920

1940

1960 Years

1980

2000

2020

Fig. 6. Cumulative number of Lessepsian fish migrants in four sections of the Mediterranean

the range of temperatures in which reproduction can occur is defined and limited due to physiological constraints (Wootton, 1992); it is of high probability that individuals of certain fish species may be able to survive in cooler temperatures but they may not necessarily be able to produce offspring in such an extreme temperature regime. In other words, Lessepsian fish species must maintain ontogenic continuity in the region they occupy in order to successfully colonize it. In this matter of temperature regime, Golani (1998) suggested a correlation between the early commencement of spawning season in the Mediterranean, i.e., March or April, when temperatures reach 17-18 o C (Oren and Hornung, 1972), and western extension of distribution. Biotic factors are more complicated and need further study. MacArthur (1972) argued that there is an inverse relationship between the ability of a colonizing species to penetrate an area and the degree of species richness and diversity in that area. Several researchers have shown that the indigenous ichthyofauna of the Mediterranean becomes richer and more diverse as one moves westward (Fredj and Maurin, 1987; HarmelinVivien and Harmelin, 1990; Golani, 1996; Quignard and Tomasini, 2000). Due to the complexity and multiplicity of biotic factors, such as food availability, competition with indigenous species for food and habitats, exposure to local pathogens and searching for

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 169

suitable substrate, it is difficult to rank the importance of these factors and to determine which will most influence the westward movement of Lessepsian fish species. IMPACT OF INVASION OF LESSEPSIAN MIGRANT FISH Biological invasions and the subsequent establishment of alien species in a new geographical region have increased dramatically in the last few decades, and with them, a dramatic rise in controversy as to their long-term impact. This phenomenon has been recognized as a major source of biotic homogenization. One may ask whether fish invasions necessarily pose a significant threat to the well-being of indigenous marine communities. Some have argued that the main impact of biological invasions is a considerable decrease in species diversity in the target area. Unlike many regions of the world which are suffering from a noted decrease in biodiversity, the marine environment of the eastern Mediterranean is experiencing an increase in its biodiversity due to the influx of Red Sea organisms. A total of 73 Lessepsian fish species are known in the eastern Mediterranean, constituting 14.9% of the 471 species enumerated by Golani et al. (2006) for this region. These species represent 44 families (Table 2), of which 18 families are new arrivals to the Mediterranean; in another 11 families, Lessepsian migrants constitute 50% or more of the number of species in those families (Fig. 7). No less interesting is the category of the low percentage (ca. 19%) of Lessepsian migrants in their families in the Mediterranean, reflecting colonization by invasive spe-

5 spp. 4 spp. 3 spp. 2 spp. 1 spp.

18 16

no. of families

14 12 10 8 6 4 2 0 <19

20–49

55–90

100

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Fig. 7. Percentage of Lessepsian migrant species in their families in the Mediterranean; breakdown according to number of Lessepsian species per family

170 Daniel Golani

cies belonging to a family of multiple indigenous species (<5). Lessepsian colonization has occurred in not less than 13 families with more than 5 con-familial “native” species. This finding is in direct opposition to the prediction that multi-species families with many species with similar ecological requirements will hinder colonization. The massive colonization of the eastern Mediterranean by Red Sea fish species has potentially an enormous impact on the recipient niche. However the importance of Lessepsian fish on the biodiversity of the eastern Mediterranean is much greater than their proportion of the fish inventory in this critical region. Golani and Ben-Tuvia (1995) demonstrated that nearly 50% of the Israeli trawl catch consisted of Lessepsian migrants. Spanier et al. (2000) found that their experimental trammel net was dominated by the Red Sea invaders. Gücü and Bingal (1994) reported that Lessepsian demersal fish made up to 70% of the biomass of the trawl catch in the Marsin Bay and the Gulf of Iskenderun. Biology and ecology of migrant fish were studied, especially that of commercial species (see Table 3) but the data obtained was not compared to that of closely related indigenous species in order to assess the possible impact. It is in fact rather surprising that there have been so few studies that directly tackle this important issue. One would expect that there would be a number of studies comparing biological and ecological characteristics of Lessepsian fish to those of indigenous Mediterranean species sharing the same ecological niche since the logical assumption is that these species are potential competitors. Some researchers have inferred from current conditions that Lessepsian species have displaced indigenous species, without any clear evidence for this far-reaching conclusion and without detailed knowledge of the situation prior to colonization. Table 3. Biological and ecological studies of Lessepsian migrant fishes in the Mediterranean Etrumeus teres General biology: Yilmaz and Hoşsucu, 2003. Saurida undosquamis General biology: Golani, 1993a; Işmen, 2002. Feeding: Bograd-Zismann, 1965; Golani, 1993b Growth rate: Mouneimne, 1978 Reproduction: Shenouda and Wadie, 1990; Işmen, 2003; El-Greisy, 2005a; El-Greisy, 2005b. Parasitology: Paperna, 1972; Fischthal, 1980; Ramadan et al., 1990 Fishery: Oren et al., 1971; Ben-Yami and Glaser, 1974; Golani and Ben-Tuvia, 1995 Atherinomorus forskalii General biology: Ben-Tuvia and Golani, 1993; Feeding: Golani, 1993b Growth rate: Mouneimne, 1978 Genetics: Bucciarelli et al., 2002 Parasitology: Paperna, 1972; Fischthal, 1980

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Sargocentron rubrum General biology: Golani and Ben-Tuvia, 1985; Golani, 1993b Feeding: Ben-Eliahu et al., 1983; Golani et al., 1983 Growth rate: Mouneimne, 1978 Artificial reefs: Spanier et al., 1996; Spanier, 2000. Fistularia commersonii Feeding: Kalogirou et al., 2007; Bariche et al., 2009 Genetics: Golani et al., 2007. Sillago sihama Feeding: Golani, 1993b Parasitology: Fischthal, 1980 Physiology: Chervinski, 1986 Alepes djedaba Parasitology: Fischthal, 1980 Leiognathus klunzingeri Growth rate: Mouneimne, 1978 Reproduction: Özütok and Avşar, 2003 Pomadasys stridens Parasitology: Fischthal, 1980 Crenidens crenidens Parasitology: Paperna, 1972 Upeneus moluccensis General biology: Laskaridis, 1948; Golani, 1994b; Kaya et al., 1999 Feeding: Ben-Eliahu and Golani, 1990; Golani and Galil, 1991; Golani, 1993b Growth rate: Mouneimne, 1978; Işmen, 2005; Genetics: Golani and Ritte, 1999; Hassan and Bonhomme, 2005; Turan, 2006 Parasitology: Paperna, 1972 Fishery: Gottlieb and Oren, 1957; Gottlieb, 1960b; Oren et al., 1971; Golani and Ben-Tuvia, 1995; Sonin et al., 1996 Upeneus pori General biology: Golani, 1994b; Cicek et al., 2002. Feeding: Ben-Eliahu and Golani, 1990; Golani and Galil, 1991; Golani, 1993b Growth rate: Mouneimne, 1978; Işmen, 2006 Fishery: Golani and Ben-Tuvia, 1995 Genetics: Golani and Ritte, 1999; Turan, 2006 Pempheris vanicolensis General biology: Golani and Diamant, 1991 Feeding: Golani, 1993b Behviour: Bilecenoglu and Taşkavak, 1999 Callionymus filamentosus Growth rate: Mouneimne, 1978 Parasitology: Fischthal, 1980 Silhouettea aegyptia General biology: Miller and Fouda, 1986

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Siganus luridus General biology: Popper and Gundermann, 1975; Bariche et al., 2004 Feeding: Golani, 1993b; Stergiou, 1988; Lundberg and Golani, 1995; Lundberg et al., 1999; Lundberg et al., 2004; Bariche, 2006 Growth rate: Mouneimne, 1978; Bariche, 2005, Shakman et al., 2008 Reproduction: George, 1972; Lahnsteiner and Patzner, 1999; Azzurro and Andaloro, 2004; Bariche et al., 2003 Parasitology: Paperna, 1972; Fischthal, 1980; Diamant, 1989; Diamant, 1998 Genetics: Azzurro et al. 2006; Hassan et al., 2003 Siganus rivulatus General biology: Popper and Gundermann, 1975; Bariche et al., 2004 Feeding: Lndberg, 1980; Lundberg, 1981; Lundberg, 1989; Golani, 1993b; Lundberg and Lipkin, 1993b; Lundberg and Golani, 1995; Lundberg et al., 1999; Lundberg et al., 2004; Bariche, 2006 Growth rate: Mouneimne, 1978; Yeldan and Avşar, 1998; Bilecenoglu and Kaya, 2002; Bariche, 2005; Shakman et al., 2008 Reproduction: George, 1972; Popper et al., 1973; Lahnsteiner and Patzner, 1999; Yeldan and Avşar, 2000 Bariche et al., 2003 Genetics: Bonhomme et al., 2003; Azzurro et al., 2006; Hassan et al., 2003 Parasitology: Paperna, 1972; Fischthal, 1980; Diamant, 1989; Diamant, 1998; Diamant et al., 1999 Sphyraena chrysotaenia Feeding: Golani, 1993b Growth rate: Mouneimne, 1978; Zouari-Ktari et al., 2007 Parasitology: Fischthal, 1980 Fishery: Golani and Ben-Tuvia, 1995 Scomberomorus commerson Feeding: Bakhoum, 2007 Stephanolepis diaspros Feeding: Zouari-Ktari et al., 2008 Torquigener flavimaculosus Behavior: Bilecenoglu, 2005

At present only a few studies have attempted to gauge the direct impact of Lessepsian migrants on their new habitat. Golani (1994) studied resource partitioning between the two Lessepsian goatfish, the Goldband Goatfish (Upeneus moluccensis) and Por’s Goatfish (Upeneus pori) and the two indigenous goatfish, the Red Mullet (Mullus barbatus) and the Striped Red Mullet (Mullus surmuletus) along the coast of Israel. All four species were found to have remarkably similar feedings habits (Golani and Galil, 1991); all fed mainly on macrurid crustaceans and therefore there were high values of diet overlap. Niche partitioning was observed mainly on the bathymetric distribution axis, with the Lessepsian migrants inhabiting shallower waters of 20-30 m while the indigenous species occupied deeper grounds at 55-90 m. The opposite situation was

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 173

observed by Golani (1993a) concerning lizardfish: the Lessepsian migrant Brushtooth Lizardfish (Saurida undosquamis) was found to inhabit slightly deeper grounds than its confamilial indigenous relative, the Atlantic Lizardfish (Synodus saurus). Bariche et al. (2004) studied the temporal settlement of two herbivorous Lessepsian migrants, the Dusky Rabbitfish (Siganus luridas) and the Marbled Rabbitfish (Siganus rivulatus), and compared it to that of the two indigenous herbivores the Salema (Sarpa salpa) and the Parrotfish (Sparisoma cretense) and discovered that the colonizers were much more abundant. The authors postulated that the colonizers replaced the indigenous S. salpa. However, a major shortcoming to this conclusion by the authors is that they relied on a description of pre-colonization abundance from an old report of Gruvel (1931) who was not an ichthyologist and could have easily confused Sarpa salpa with the externally similar and still quite abundant Bogue (Boops boops). The suspicion that Gruvel erred is even greater when one considers that it is generally not captured by trawl as described by Gruvel (1931) in his report. Moreover, the assumption that the two siganids are better competitors than the indigenous species vis-à-vis resources cannot be considered correct until it is proven that trophic resources constitute the most important limiting factor, algae having been observed to be quite abundant along the eastern Mediterranean coast (Lipkin and Safriel, 1971; Lundberg, 1980; Lundberg and Golani, 1995). The paucity of comparative studies between Lessepsian migrants and their closely related Mediterranean indigenous species, combined with the lack of data on eastern Mediterranean fish biodiversity prior to colonization, has led to the publication of numerous papers of a speculative nature. The observation of bathymetrical partitioning between colonizer and indigenous goatfishes has been used as “proof ” of displacement by colonizers and the forcing of native species to deeper waters (Fishelson, 2000; Goren and Galil, 2005; Galil, 2006, 2007). Since Mullus spp. distribution prior to colonization of Lessepsian migrants is not thoroughly documented, such conclusions are speculative at best. A similar situation exists regarding research of the invasive lizardfish Saurida undosquamis which was shown to inhabit shallower waters than its possible competitor the indigenous Hake (Merluccius merluccius) by Ben-Yami and Glaser (1973), who thereby concluded that the former colonizing species competitively displaced the indigenous species. However, there was no clear evidence to support this conclusion, particularly in the absence of studies of local bathymetric distribution of the Hake prior to the lizardfish’s invasion of the eastern Mediterranean. The case of the disappearance of the indigenous killifish Striped Tooth-Carp Aphanius fasciatus, allegedly due to the “sudden” appearance of the Dispar Tooth-Carp Aphanius dispar as reported by Goren and Galil (2005) and Galil (2006) is yet another example of a too hasty and unsupported conclusion. Aphanius dispar occurred in the eastern Mediterranean much before the opening of the Suez Canal (see: Kornfield and Nevo, 1976) and therefore it is not considered as a Lessepsian migrant (see: Golani et al., 2002 p. 223 and Table 2 of this article). The fact that it was first collected in the Mediterranean waters of Israel in 1943-44 (Mendelsohn, 1947) does not prove that it

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had just arrived to that area; during those years only 35% of indigenous species had been documented from that region. This species is still rare along the Israeli coast with the exception of the artificial salt pool adjacent to Atlit. The claim of alleged disappearance of one closely-related species by the other is further complicated by the possibility of hybridization; both killifish are known to co-exist and partially hybridize in the northern Sinai lagoon of Bardawil (Villwock, 1987; Lotan and Ben-Tuvia, 1996) as well as in other locations in the Mediterranean. CHARACTERISTICS OF SUCCESSFUL COLONIZERS Can successful colonizers be identified by certain common traits or characteristics? This question has been discussed often in scientific literature (Parsons, 1983; Kolar and Lodge, 2001; Fagan et al., 2002; García-Berthou, 2007; Nentwig, 2007). Safriel and Ritte (1980, 1983) studied Lessepsian migration in order to formulate universal criteria for successful colonizers, such as life history strategy, genetic variability and exploitation of trophic niches. Golani (1993, 1998) examined the applicability of Safriel and Ritte’s theories on the Lessepsian migrants of the Goatfish family (Mullidae) and concluded, following Ehrlich (1986), that universal criteria that would be viable in all ecosystems and to all known taxonomic groups could not be formulated. It was discovered that the trait that could be considered the most common in Lessepsian fish is their pre-adaptation to colonization of the Mediterranean by being well adapted to the most vulnerable niche in their target area, namely, shallow sandy or muddy substrates. Predicting whether an invasive fish species will succeed or fail in colonizing its new habitat depends on examining a number of factors. A prerequisite to success for any colonizing species is some degree of similarity regarding biotic and abiotic conditions between the target area and the source area, assuming that any degree of difference is still within the colonizing fish’s physiological and biological tolerance levels, particularly regarding differences in water temperature and salinity. Success will also depend on appropriate sources of food in the recipient community. For example, the two very successful Lessepsian migrant Rabbitfish Siganus luridus and Siganus rivulatus feed upon the same algal resources in both the source (Red Sea) and the target (Mediterranean) areas (Lundberg, 1980; Lundberg and Golani, 1995). New migrants have a great chance of success when there are few species in the target area with their particular ecological demands. Another factor signifying success in colonization is species with high mobility and schooling. The “pioneer” group of colonizers is usually small; a school of migrants has a better chance of reproducing in the target area than a solitary migrant. For example, the second most specious Lessepsian fish family in the Mediterranean is Clupeidae (sardines) which are active schooling fish with 4 representatives in the Mediterranean. Schooling species form the majority of the most successful Lessepsian fish species. The most outstanding examples of successful schooling Lessepsian migrants are

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration 175

Sphyraenia chrysotaenia, Atherinomorus forsskali, Upeneus moluccensis, Upeneus pori, Plotosus lineatus and Alepes djedaba. Territorial species have been less successful colonizers; most of them have been recorded by a single record or by very few individuals; some examples of these are Pterois miles, Epinephelus coioides, E. malabaricus, Lutjanus argentimaculatus, Abudefduf variegatus, Heniochus intermedia and Iniistius pavo. Two territorial Lessepsian species, Hippocampus fuscus and Stephanolepis diaspros, are exceptions to the rule mentioned above; they have established large populations in well-defined areas of the Mediterranean. The nocturnal species Sargocentron rubrum, Pempheris vanicolensis and the three cardinalfishes Apogon spp. are territorial but only during the daytime. With the exception of the most recent arrival Apogon queketti, all nocturnal species are very well established, probably due to their wider territorial activity during the nighttime. EXCLUSION OF DOUBTFUL LESSEPSIAN MIGRANTS Many fish species that were earlier reported as Lessepsian migrants have been consequently excluded from the official list of Lessepsian migrants. Golani et al. (2002) compiled a detailed annotated list of these excluded species. The main reasons for exclusion were misidentifications, unclear taxonomy, lack of preserved material necessary to confirm records and erroneous designation of species indigenous to the Mediterranean as Lessepsian migrants. Since the publication of Golani et al. (2002), several additional cases have been published including a new category of species whose presence in the Mediterranean was based only upon underwater photographs. Öztürk (2005) reported the occurrence of Carangoides bajad (Forsskål, 1775), Çinar et al. (2006) reported Parupeneus forsskali (Fourmanoir and Guézé, 1976) and Bilecenoglu (2007) reported Monotaxis grandoculis (Forsskål, 1775) from the Mediterranean coast of Turkey. Despite the high probability that these species will be collected from this new area in the future, it is currently best to refrain from including them in the official list of Mediterranean ichthyofauna. Similarly, Goren and Galil (2006) reported Bregmaceros atlanticus Goode and Bean, 1886 from the Mediterranean coast of Israel and postulated that it is a Lessepsian migrant; however, this speculation is apparently not correct since this species is known in the western Mediterranean (see D’Ancona and Cavinato, 1965) and it is not found in the Red Sea (Belyanina, 1974). The identification of Carcharhinus amboinensis (Müller and Henle, 1839) based on the finding of a jaw in 2003 off Crotone, Italy in the northwest Ionian Sea led De Maddalena and Della Rovere (2005) to conclude that this species “must be considered a Lessepsian migrant”. This conclusion is improbable since this species is not known from the Red Sea (Compagno, 1984; Compagno et al., 2004).

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Alien marine fishes of Turkey – an updated review Murat Bilecenoglu

INTRODUCTION Modification of the Mediterranean ecosystem by non-indigenous species has become much more evident in the last decades. The picture drawn by a growing number of specific research have revealed the presence of hundreds of alien species – whether established or not, in this oligotrophic sea. The word “hundreds” should be perceived symbolical, attributing to the still unclear diversity of the alien biota, i.e. Zenetos et al. listed 745 alien species during 2005, which has increased to 903 within a few years (Zenetos et al., 2008). It is obvious that there will never be an exact inventory, since the influx of nonindigenous organisms is continuous with an increasing trend, seemingly to slow down only if the relevant niche and habitats becomes saturated. The eastern basin of the Mediterranean Sea is much more prone to invasions than the western basin and Turkey is among the most influenced countries for a variety of reasons. Concisely, the combination of two main factors make Turkey more susceptible to the establishment of alien organisms – proximity to the Suez Canal and dense maritime traffic occurring through the Dardanelles and Bosphorus Straits (Cinar et al., 2005). Despite the increasing effort in alien species documentation, bioecological studies are still very scarce in Turkey, thus delaying potential governmental precautions that need to be taken. Fishes are probably the most studied taxa among all alien marine organisms, mainly due to their contribution to local fishery activities. The presence of alien fish in the Mediterranean Sea was mentioned only a few decades after the opening of the Suez Canal (Por, 1978), but it was not until the 1940’s that documentation studies at the Anatolian coasts began. Erazi (1943), who recorded Leiognathus klunzingeri from Iskenderun Bay, is considered to be the pioneering study, followed by Kosswig (1950, 1956) and Akyüz (1957). The 1960’s represent the “period of realization” of the commercial alien species (for example, Upeneus moluccensis and Saurida undosquamis) at bottom trawling grounds along the northeast Levant (Aasen and Akyüz, 1956; Ben-Tuvia, 1966). No papers on

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non-native fishes were published during the 1970’s by Turkish scientists. The first efforts to determine biological characters of some abundant aliens were conducted during the 1980’s and 1990’s, including data on the main components of the local trawl fishery (see Bingel, 1981; Anonymous, 1983; Bingel, 1987; Gücü et al., 1994). Today, we have a more or less complete picture of the non-native fishes inhabiting Turkey, mostly based on inventory studies compiled by Bilecenoglu et al. (2002) and Cinar et al. (2005). In this chapter, an updated review is presented, together with available biological data (i.e. age, growth, reproduction etc.) published until now, which may be useful in forming a basis for further studies and identifying the gaps yet to be filled. INVENTORY OF ALIEN FISH The data presented herein was compiled from a variety of sources, including gray literature (i.e. theses, reports etc.) and previously unpublished observations of the author. However, the backbone of the review is based on Cinar et al. (2005), updated by recent information and taxonomical revisions. Emphasis was placed on the current distribution ranges of alien fishes at Turkish coasts, which may help to improve the maps of Golani et al. (2002). Moreover, available data on the population dynamics parameters of studied species are included. As of April 2009, there were a total of 49 valid alien fishes reported from Turkey, corresponding to one new species added to the local ichthyofauna every 0.75 years. This time span has decreased to 2.4 species per year since 2000 to date (Fig. 1), a general trend observed also throughout the Mediterranean Sea. 55 50 Number of Species

45 40 35 30 25 20 15 10 5 0 1940

1950

1960

1970

1980

1990

2000

Years

Fig. 1. Rate of introduction of alien fishes along the Turkish coast. Black bars indicate the number of recorded species for the given period and the line represents the cumulative number of species.

Alien marine fishes of Turkey – an updated review 191

When the actual distribution ranges of the fishes are examined, a clear decrease in number of species can be seen from Iskenderun Bay towards the west (Fig. 2). The highest alien fish diversity (41 species) in the northeast Levant is not surprising due to its closeness to the Suez Canal. The northwest Levant region including Antalya city coasts and Fethiye Bay, has a similar alien fauna, which drops to 28 and 9 species in the southern and northern Aegean Seas, respectively. The only alien species inhabiting the Black Sea is Pilengas mullet (Liza haematocheilus), which is also in the Sea of Marmara together with the recently recorded pufferfish, Lagocephalus spadiceus (Tuncer et al., 2008). The species accounts are given below, under three subheadings – casual, established and questionable aliens. A casual species is identified as having been recorded no more than twice from Turkey, while fishes recorded three or more times are considered as established. Casual Aliens Carcharhinidae Carcharhinus altimus (Springer, 1950): The Bignose shark is known by two records in the Levantine basin. After its first report from the Levant Sea (Golani, 1996), a 64.3 cm total length specimen was captured from a depth of 20 m in Iskenderun Bay (Basusta and Erdem, 2000). Identification of C. altimus is often confused with other sharks, so a wider distribution range can be expected in the Mediterranean Sea (Golani et al., 2006). 24°

27°

30°

33°

36°

39°

42°

45°

1 42°

2 9

39°

28 38

41

36°

33°

Fig. 2. Number of alien fish species at Turkish coasts.

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Dasyatidae Himantura uarnak (Forsskål, 1775): A prevalent species with a stable population in the southeastern Levant (Golani et al., 2002), but apparently very rare in Turkey, since only a few specimen-based records are available. Ben-Tuvia (1966) mentioned a large H. uarnak with 120 cm disc length, captured by bottom trawlers near Mersin. On September 1996, a small sized individual (ca. 40 cm disc width) was observed at a depth of 18 m during a scuba dive off Tasucu coasts, Mersin (M. Bilecenoglu, pers. obs.). One male specimen with a 45.9 cm disc width was captured from Iskenderun Bay on May 1997 (Basusta et al., 1998), which represents the last valid observation of the species along Turkish coasts. Current distribution of the species along the eastern Levant coasts of Turkey is restricted to a small area between Iskenderun Bay and Tasucu – Mersin. Chirocentridae Chirocentrus dorab (Forsskål, 1775): During ichthyoplankton samplings carried out at the northeast Levant on May 1999, yolk-sac larvae (6.35 mm in length) of the Dorab Wolf herring were collected from a depth of 100 m, but this sample remained unexamined until now (Yesim Ak Orek, pers. comm.). Four eggs and four larvae of C. dorab were again collected from Iskenderun Bay and Mersin (off Erdemli and Tasucu) during 2007, representing a first record of the species from the Mediterranean Sea (Ak Orek, 2008). Status and mode of introduction of C. dorab is not clear at the moment, however, considering its first observation almost a decade ago, we may assume that the species is relatively rare. Further samplings of adult specimens will doubtless provide more data. Carangidae Trachurus indicus Nekrasov, 1966: Two specimens of the Arabian scad were captured from Iskenderun Bay during October 2004 (Dalyan and Eryilmaz, 2009), which have likely entered to the Mediterranean via the Suez Canal. It was probably an overlooked species in previous studies, due to clear morphological similarities with native Trachurus spp. Although Smith-Vaniz (1984) mentioned that no occurrence records of T.indicus are available at waters colder than 20°C, there are several cases of alien fish successfully adapted to significantly different environmental conditions of the Mediterranean Sea. We should currently assume the species as rare, until additional information is provided from Turkish coasts and rest of the Levantine basin. Lethrinidae Monotaxis grandoculis (Forsskål, 1775): A single sub-adult individual was observed during a scuba dive at Antalya Bay (Bilecenoglu, 2007) and no further information exists. Its origin is not clear at the moment, but the possibility of a ship-mediated introduction should not be rejected, in addition to a possible dispersal through the Suez Canal.

Alien marine fishes of Turkey – an updated review 193

Chaetodontidae Heniochus intermedius Steindachner, 1893: Two specimens of the Red Sea bannerfish were observed in Antalya Bay, one of which was captured and recorded as a new alien in the Mediterranean Sea (Gökoglu et al., 2003). No further observations are available for this unmistakable species since then. Mullidae Parupeneus forsskali (Fourmanoir and Guézé, 1976): The first observation of P. forsskali was made during 2000 at Mersin coasts, which was later photographed at the same locality (Cinar et al., 2006). Despite extensive bottom trawlings made along the area, no specimens could be captured until now. The species is likely to exist also in Malta, where Sciberras and Schembri (2007) concluded that a specimen obtained in Gozo during 1979 was described well enough to be identified as P. forsskali. Champsodontidae Champsodon nudivittis (Ogilby, 1895): One specimen (11.4 cm TL) of the Indo West Pacific originated nakedband gaper was recently captured from Iskenderun Bay, at a depth of 50 m (Cicek and Bilecenoglu, 2009). The species is still unrecorded from the Red Sea and the northwest Indian Ocean, which indicates a probable ship-mediated introduction. However, knowledge on the Red Sea gapers is far from being complete, so the possibility that C.nudivittis is an overlooked species in the area should not be neglected. Blenniidae Petroscirtes ancylodon Rüppell, 1835: This species has long been considered as a rare alien of the eastern Mediterranean, since only two records were available from Israel and Turkey, respectively (Taskavak et al., 2000). Recent findings from Gokova Bay (Okus et al., 2006) indicate a range expansion of the species through the Anatolian coasts to southern Aegean Sea, as far as Rhodes (Corsini et al., 2005). Ephippidae Platax teira (Forsskål, 1775): One specimen with 38.9 cm standard length was captured by a speargun from Bodrum (southern Aegean Sea), which represents the single record of the species throughout the Mediterranean Sea (Bilecenoglu and Kaya, 2006). Since many Platax species (especially juveniles) are commercially traded worldwide by aquarists, a release from an aquarium is suspected.

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Established Aliens Muraenidae Enchelycore anatina (Lowe, 1838) (Fig. 3): The occurrence of the Fangtooth moray in Turkey was first mentioned by Yokes et al. (2002), based on specimens observed at Antalya Bay. It was later recorded at various localities along the Datca Peninsula (southern Aegean Sea) (Okus et al., 2004) and Mersin coasts (Can and Bilecenoglu, 2005). A popular magazine article by Altan (1998) has recently been available to the author, where a specimen of E. anatina was photographed from Sarigerme (Fethiye Bay). Therefore, it seems highly probable that the Fangtooth moray is an overlooked species in previous studies. Although Golani et al. (2002) regarded the species as very rare in the Mediterranean Sea, underwater observations from Turkey indicate widespread and locally abundant populations. Clupeidae Dussumieria elopsoides Bleeker, 1849: Reported first by Ben-Tuvia (1953, as D. productissima) from Iskenderun Bay and Mersin coasts, which was followed by several successive records along the Levantine coasts of Turkey. Previous identifications of the species as D. acuta are erroneous (Whitehead, 1985). Although mentioned as occurring in the Aegean Sea (Geldiay, 1969), it was not accepted as a valid occurrence record (Bilecenoglu et al., 2002). Distribution of the species covers the entire coastline from Iskenderun Bay to Fethiye Bay, whose abundance is clearly higher at the northeastern Levant and reducing westwards.

Fig. 3. Fangtooth moray from Kalkan, Antalya (Photograph: Tahsin Ceylan).

Alien marine fishes of Turkey – an updated review 195

There are no existing specific studies on the contribution of D. elopsoides to Turkish regional fishery activities, but all those captured are marketed mixed with native clupeoids. According to the results of an experimental fishery survey, specimens with fork lengths and weights ranging 9.0 to 16.5 cm and 5 to 45 g, respectively, appear in the catches along the Mersin coast (Anonymous, 1968). Length-weight relationship of the species was given by Taskavak and Bilecenoglu (2001). Etrumeus teres (Dekay, 1842): The Round herring first occurred along the Turkish coast possibly during the early 1990’s, based on interviews made by the local fishermen (M. Bilecenoglu, unpublished data). Worldwide distribution map of the species given by Whitehead (1985) included Mediterranean coasts of Turkey, but this information seems to be erroneous. A valid record of E. teres was given during 1997 from Iskenderun Bay (Basusta et al., 1997), where it was already abundant in the local commercial fish catches. The species is currently very common along the northern Levantine coast, which expanded its distribution to Datca Peninsula of southern Aegean Sea coasts (Okus et al., 2004). A single specimen was recently observed in a purse seine catch at Kusadasi Bay, which may be a sign of step-by-step expansion towards northern parts of the Aegean Sea. Unlike other alien clupeids, the Round herring is generally marketed separately, under the commonly used local name “Akdeniz hamsisi – Mediterranean anchovy”. Its proportion within the total clupeid catch of purse seiners is unknown, but Cicek (2006) mentioned that E. teres is also captured by bottom trawlers in small quantities, representing only 0.2% of the total alien fish biomass. Length-weight relationship of the species was given in two studies (Taskavak and Bilecenoglu, 2001; Yilmaz and Hossucu, 2003). The single study on the growth of Round herring indicated a short life span (3 years) based on otolith readings (Yilmaz and Hossucu, 2003), however, the von Bertalanffy growth parameters estimated seems to be erroneous (i.e. L∞= 33.8 cm, k= 0.20 years-1 and t0= -1.63 years for pooled samples) – such a low “k” value is unexpected for a fast growing species, which maybe due to biased sampling strategy. Herklotsichthys punctatus (Rüppell, 1837): No detailed information exists concerning the species, except for a few papers dealing with its distribution (Bilecenoglu et al., 2002). It may be regarded as prevalent in Iskenderun Bay, whose abundance peaks during summer months (Baki Yokes, pers. comm). The westernmost occurrence of H.punctatus along the Turkish Mediterranean coasts is Antalya Bay, where the abundance of the species is distinctly very rare. Synodontidae Saurida undosquamis (Richardson, 1848): The Brushtooth lizardfish was rather an uncommon species in the Mediterranean Sea until 1955, which then started to appear in large quantities in bottom trawl catches. It was already abundant by 1956 at Mersin coasts and Iskenderun Bay, during its first record from Turkey (Ben-Tuvia, 1966). Current distribution of S. undosquamis covers the entire Levantine coast of Turkey and the southern Aegean Sea, where its abundance clearly decreases westwards of Antalya Bay.

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Due to its commercial importance and high abundance, the Brushtooth lizardfish was subjected to several biological studies. The value of exponent “b” of the length-weight relationship was reported to range between 2.879 and 3.240 (Bingel, 1981; Türeli and Erdem, 1997; Cicek, 2006; Cicek et al., 2006; Sangün et al., 2007; Akyol et al., 2007). Maximum age was determined as 7 years from otolith readings (Ismen, 2002), and as 6 years from results of length frequency analysis (Gokce et al., 2007). Growth parameters estimated until now are not in accordance, probably due to methods used or the sampling strategy (Table 1); however, reported life spans should indicate a relatively fast growth. The available catch per unit effort (CPUE) data reveals a distinct decrease in the population of the species, i.e. CPUE was ca. 16 kg/hr during 1984 and ca. 4 kg/hr during the 2002-2003 fishing season (Cicek, 2006), which clearly indicates overfishing throughout the area. Stomach content analyses based on percentage numerical abundance show that S. undosquamis primarily feeds on teleosts (40.1% Mullidae, 13.5% Sparidae, 12.4% Leiognathus klunzingeri and 7.4% S. undosquamis) and benthic invertebrates to a lesser extent (such as cephalopods and penaeid shrimps) (Bingel and Avsar, 1988). Piscivorous feeding habits of the species was also noted by Gücü (1995), who reported that the diet consists mainly of Sardinella aurita and Engraulis encrasicholus (39.6%), Spicara flexuosa (16.4%), Mullus barbatus (15.6%) and other teleosts in smaller quantities, using percentage weight of prey items. According to the reproductive biology studies, S.undosquamis may spawn throughout the year, with two distinct peaks in gonadosomatic index values (April-July and September-November) (Bingel, 1981; Ismen, 2003). Length at first sexual maturity was given as 12.5 cm by Türeli and Erdem (1997) and 16.0 – 16.5 cm by Ismen (2003). Bregmacerotidae Bregmaceros atlanticus Goode and Bean, 1886: The status of the Antenna codlet in the Mediterranean Sea has long been a matter of dispute, due to its previous doubtful record from the Straits of Sicily (see Goren and Galil, 2006). In this respect, the recent reports of B. atlanticus from Antalya Bay (Yilmaz et al., 2004) and Kusadasi Bay (Filiz et al., 2007) deserves special interest, since the sudden occurrence of the species in the eastern Mediterranean raises a question mark on its origin. Such a distinctive species is hardly Table 1. A review of von Bertalanffy growth parameters of Saurida undosquamis from Turkey. L∞ (cm) 46.70 45.60 42.80 22.43 42.00 38.05 42.00

k (year-1) 0.133 0.185 0.420 0.597 0.178 0.124 0.510

t0 (year) - 0.160 - 0.007 - 1.365 - 1.229 - 1.680 - 0.290

n 333 602 275 4711

Locality Göksu Delta Tirtar NE Levant Iskenderun Bay Iskenderun Bay Iskenderun Bay Iskenderun Bay

Reference Bingel (1981) Bingel (1981) Gücü (1995) Türeli and Erdem (1997) Ismen (2002) Cicek (2006) Gokce et al. (2007)

Alien marine fishes of Turkey – an updated review 197

to be overlooked in previous studies, thus Goren and Galil (2006) suspected of a shipmediated introduction of B. atlanticus. The Antenna codlet is currently very common at Iskenderun Bay and is also in the southern Aegean Sea coasts. It is possible to observe the species in large schools during night dives, even in very shallow waters. The genus Bregmaceros urgently requires a revision, so a change in taxonomy and distribution of some species can be expected. Atherinidae Atherinomorus lacunosus (Forster, 1801): Little data is available concerning this species, expect for those on its distribution (Bilecenoglu et al., 2002). It is widespread throughout the Levantine coast of Turkey and locally abundant populations can be observed at the southern Aegean. The species have a minor commercial value, which is sometimes marketed locally. Hemiramphidae Hemiramphus far (Forsskål, 1775): The Blackbarred halfbeak is among the first alien fishes reported from Turkey. It may be regarded as a prevalent species along all the entire northern Levantine coasts as far as the southern Aegean Sea. Aasen and Akyüz (1956) reported that H. far was one of the most common species captured by beach seines in Iskenderun Bay, especially at depths shallower than 10 m. Beach seines are currently forbidden for use in Turkey but large sized individuals (i.e. > 30 cm total length) caught by fishing rods are marketed fresh in some fishery ports. Exocoetidae Parexocoetus mento (Valenciennes, 1846): Information on this species is very limited, similar to other flying fishes of the Mediterranean. It sometimes forms very large schools especially in Iskenderun Bay (possibly with a thousand individuals or more), observed leaping out of the water. Two specimens captured from the northern Cilician basin had total lengths of 12.8 and 13.5 cm, slightly over the maximum length (12 cm) mentioned by Golani et al. (2002). The distribution of P.mento extends as far as Kusadasi Bay in the southern Aegean Sea. Holocentridae Sargocentron rubrum (Forsskål, 1775): A common species reported first by Kosswig (1950) from Iskenderun Bay. Typically inhabits caves and crevices, generally at depths down to 40 m (Golani et al., 2002), but scuba observations at greater depths (50 – 60 m) were also made at several localities (M. Bilecenoglu, pers. obs.). It is currently distributed along the northern Levantine coasts and the southern Aegean Sea. Although the species is not commercially fished, it sometimes appears as a bycatch in gill-net fisheries and may be marketed fresh in local ports. There are no detailed data on its bioecology or fisheries, except for its length-weight relationship given by Taskavak and Bilecenoglu (2001).

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Fistulariidae Fistularia commersonii Rüppell, 1838 (Fig. 4): The Bluespotted cornetfish is among the most rapidly spreading aliens in the Mediterranean Sea. Following its first record in 2000 from the Israeli coast, specimens were subsequently collected from Antalya and Gökova Bays (Bilecenoglu et al., 2002). Underwater observations reveal that the species can occupy a variety of habitats, including seagrass beds, rocky substrates and even sandy bottoms, generally in small schools of up to 20 individuals. It is common along the Levantine and southern Aegean coasts of Turkey while its abundance distinctly decreases towards the northern Aegean Sea. Fistularia commersonii is caught as a bycatch in artisanal fisheries and marketed fresh in some local ports. Syngnathidae Hippocampus fuscus Rüppell, 1838: The Sea pony was known by a single specimen reported from Antalya Bay (Gokoglu et al., 2004) but recent findings from the same locality indicate that H. fuscus is an established alien in Turkey (Zenetos et al., 2008). There is currently no sign of a westwards range expansion of the species. Terapontidae Pelates quadrilineatus (Bloch, 1790): All records of the Fourlined terapon are confined to the northeastern Levant (from Iskenderun Bay to Mersin coasts) (Bilecenoglu et al., 2002). Field observations indicate that P.quadrilineatus is much more common in the vicinity of estuaries, in agreement with the habitat description of Golani et al. (2002) for

Fig. 4. A Bluespotted cornetfish individual over sandy substrate (Photograph: Tahsin Ceylan)

Alien marine fishes of Turkey – an updated review 199

the species. Bottom trawl studies conducted between 1983 and 1989 indicate a prevalent population in Iskenderun Bay (CPUE ranges from 21.3 to 1091.8 g/h) and a relatively rare population along Mersin coasts (maximum CPUE was 3.7 g/h) (Gücü et al., 1994). The species is not of interest to local fisheries due to its small size. Apogonidae Apogon pharaonis Bellotti, 1874: The species has long been known only from the Levantine coasts of Turkey since its first record by Mater and Kaya (1987). Recently it has penetrated to Datca peninsula in the southern Aegean Sea (Okus et al., 2004). It is commonly captured by bottom trawlers, especially in Iskenderun Bay, but always discarded. Apogon queketti Gilchrist, 1903: This is the second alien apogonid recorded from Turkey by Eryilmaz and Dalyan (2006) who collected two specimens (one with ripe gonads) at depths of 55 – 60 m from Iskenderun Bay. Its recent record from the Israeli coasts indicates that the Spotfin cardinal has successfully established breeding populations in the eastern Mediterranean Sea (Goren et al., 2008). A wider distribution range can be expected for A. queketti, which will be examined in further studies. Apogon smithi (Kotthaus, 1970): Seven specimens with total lengths ranging 96 to 110 mm were collected off Iskenderun Bay (Goren et al., 2008), only one year after its first record in the Mediterranean Sea (Golani et al., 2008). The sudden introduction of A. smithi is likely to be followed by a further westward range expansion. Sillaginidae Sillago sihama (Forsskål, 1775): A prevalent species at Iskenderun Bay and Mersin coasts, known since 1983 (Gücü et al., 1994). Only a few specimens were collected from Antalya Bay and an exceptional individual from Datca peninsula (southern Aegean Sea) (Bilecenoglu, 2004). Although it was stated to be very common at the eastern Mediterranean Sea (Golani et al., 2002), S. sihama forms only a minor proportion of the local commercial fishery catch with a maximum CPUE of 131.2 g/h (Gücü et al., 1994). It is sometimes marketed fresh in local fishing ports. Carangidae Alepes djedaba (Forsskål, 1775): The Shrimp scad was first recorded from Iskenderun Bay (as Caranx kalla) by Akyüz (1957). It later reached the Aegean Sea coasts (Geldiay, 1969). Local fishermen capture A. djedaba sometimes in high quantities (depending on the season), but it is not generally regarded as a very common species, contrary to other parts of the eastern Mediterranean. Except for its length-weight relationship (Taskavak and Bilecenoglu, 2001), no further biological data exists from Turkish coasts. Some recent observations revealed that A. djedaba can also enter estuaries and lagoons; a single specimen was caught in brackish water during 2006 (M.Bilecenoglu, pers. obs.).

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Leiognathidae Equulites klunzingeri (Steindachner, 1898): The Silverbelly is the first Red Sea immigrant fish species ever reported from the Anatolian coast, under the name of Leiognathus mediterraneus by Erazi (1943). It is probable that the Silverbelly reached Turkish coasts much earlier, with reference to previous records from Rhodes (see Golani et al., 2002). Current distribution of the species extends as far as the southern Aegean Sea; its abundance clearly decreases northwest of Fethiye Bay. It is a non-commercial fish due to its small size, forming a significant portion of the discard of the eastern Mediterranean trawl fisheries. Golani et al. (2002) stated that the taxonomy of the genus Leiognathus is unsettled, requiring revision. A phylogeny was recently generated for Leiognathidae, using several characters derived from seven mitochondrial genes. Although a tissue sample was lacking for L.mediterraneus, Sparks et al. (2005) tentatively placed the species in the newly described genus Photoplagios, based on external morphology and light organ comparisons. However, Kimura et al. (2008) proposed Equulites Fowler, 1904 as a senior synonym of Photoplagios Sparks, Dunlap and Smith 2005 (in accordance with the principle of priority), since the type species (Photoplagios elongatus) share diagnostic characters of the former genus. Biological information on E. klunzingeri from the Turkish coast is limited to a few studies. CPUE values along the Iskenderun Bay and Mersin coastlines ranged from 465 to 12861 g/h, depending on the locality and season (Gücü et al., 1994). Ageing studies indicate that the species is moderately long lived, with a maximum age of 6 for both sexes (Ozütok and Avsar, 2004). Growth parameters were estimated from samples obtained in two different localities in Iskenderun Bay (Table 2). The silverbelly has a short spawning season (from July to September); length at first maturity is 5.5 and 5.8 cm for females and males, respectively, corresponding to an age of 2 – 3 years (Ozutok and Avsar, 2003). Two spawning periods (April – May and August – September) were mentioned by Bingel (1987), which requires confirmation. According to length-weight relationships calculated, the exponent “b” ranges from 2.93 to 3.27 (Bingel, 1987; Taskavak and Bilecenoglu, 2001; Ozutok and Avsar, 2004; Cicek et al., 2006; Sangün et al., 2007). Nemipteridae Nemipterus randalli Russell, 1986: After first being recorded in the Mediterranean Sea by Golani and Sonin (2006), N. randalli rapidly spread westwards, forming abundant populations in Lebanon (Lelli et al., 2008) and Turkey (Bilecenoglu and Russell, 2008). It is potentially a commercial species, extending as far as Antalya Bay (Gokoglu et al., 2008), but no individuals have yet penetrated the southern Aegean Sea. Table 2. A review of von Bertalanffy growth parameters of Equulites klunzingeri from Turkey. L∞ (cm) 10.28 11.51

k (year-1) t0 (year) 0.290 - 0.420 0.262 - 0.841

n 440 724

Locality Yumurtalik Karatas

Reference Ozutok and Avsar (2004) Ozaydin and Leblebici (2008)

Alien marine fishes of Turkey – an updated review 201

Mullidae Upeneus moluccensis (Bleeker, 1855): The Goldband goatfish is among the most successful colonizers in the Mediterranean Sea, forming a remarkable portion of the commercial trawl catches for decades. Only a few years after its first record from Iskenderun Bay (Kosswig, 1950), U. moluccensis became a main catch of bottom trawlers (Aasen and Akyüz, 1956). There are distinctive fluctuations in the abundance of the species during the last two decades, which may be related to overfishing. A recent study pointed out that only 3% of the total alien fish biomass was formed by U. moluccensis (Cicek, 2006). The species may be regarded as a common alien along the northeast Levant and a rare fish at the southern Aegean Sea. Observations from the central Aegean are limited to a few individuals captured by bottom trawlers, not indicating a well established population in the area. The “b” values of the length-weight relationship ranged between 2.86 and 3.56 (Anonymous, 1983; Kaya et al., 1999; Ismen, 2005; Sangün et al., 2007). Age estimates from Antalya Bay resulted with a maximum age of 4 (mean fork length = 16.2 cm) (Anonymous, 1983), while Kaya et al. (1999) determined 6 years (mean fork length = 17.5 cm). In a recent study, Ismen (2005) reported a specimen with 7 years of age at a total length of 20.5 cm. There are clear differences in growth parameter estimates (Table 3), likely to be due to sampling strategy (i.e. lack of small sized fish in the sample because of trawl net selectivity) or methods used to construct growth curves (otolith readings vs. length-frequency analysis). Diet of the species from Antalya Bay included Mollusca, Crustacea, Polychaeta and Teleost juveniles, but no quantitative data exists (Anonymous, 1983). Examination of several specimens captured between Iskenderun and Fethiye Bays revealed that U. moluccensis prefers Decapod crustaceans as its main food (51.87%), followed by Copepoda (17.29%) and Mysidacea (14.12%) (Kaya et al., 1999). All previous studies indicate that the spawning season begins in June and lasting possibly through September (Anonymous, 1983; Kaya et al., 1999; Ismen, 2005). Upeneus pori (Ben-Tuvia and Golani, 1989) (Fig. 5): First recorded as Upenoides tragula from Iskenderun Bay (Kosswig, 1950), it has currently reached Gokova Bay (Akyol et al., 2006). The species was less abundant throughout the northern Levant than its congeneric U. moluccensis (see Gücü et al., 1994), but recent studies indicate a distinct population increase. Cicek (2006) estimated a biomass of 36.7 kg/km2 and CPUE value of 4.5 kg/h (at depths not exceeding 20 m) for the 2002-2003 fishing season, where the species ranked as the most abundant alien fish within the bottom trawl catch. Table 3. A review of von Bertalanffy growth parameters of Upeneus moluccensis from Turkey. L∞ (cm) 25.60 25.60 25.98 25.20

k (year-1) 0.621 0.430 0.110 0.197

t0 (year) - 0.270 - 3.770 - 1.002

n 711 418

Locality NE Levant NE Levant Northern Levant Iskenderun Bay

Reference Bingel et al. (1993) Gücü (1995) Kaya et al. (1999) Ismen (2005)

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There are three studies on the age and growth of U. pori from Turkey (Table 4), all ow which mention a maximum age of 5. It should be noted that a higher “k” value is expected for such a small sized fish with such a relatively short life span. The gonadosomatic index values remained high between April and June, however the occurrence of mature individuals during September may indicate a prolonged spawning season (Ismen, 2006). The parameter “b” of the length-weight relationship ranges between 2.95 and 3.26 (Taskavak and Bilecenoglu, 2001; Cicek et al., 2002; Ismen, 2006; Cicek, 2006). Pempheridae Pempheris vanicolensis Cuvier, 1831: An immediate population explosion was observed for the Vanikoro sweeper following its introduction to the Mediterranean Sea in 1979 (Golani et al., 2002). It was commonly observed in small schools at Mersin coasts during 1983 Table 4. A review of von Bertalanffy growth parameters of Upeneus pori from Turkey. L∞ (cm) 22.54 21.94 19.10

k (year-1) 0.190 0.194 0.360

t0 (year) - 1.690 - 1.168 - 0.812

n 957 247 616

Locality Iskenderun Bay Iskenderun Bay Iskenderun Bay

Reference Cicek et al. (2002) Cicek (2006) Ismen (2006)

Fig. 5. Upeneus pori specimens from the shallow waters of Iskenderun Bay (specimen total lengths ca. 10 cm) (Photograph: Alp Can).

Alien marine fishes of Turkey – an updated review 203

and 1984 (Gücü et al., 1994). The presence of P. vanicolensis at the Dodecanese islands was indicated by Papaconstantinou (1988), who stated that the species has reached the area by following the main current along the Asia Minor. Vanikoro sweeper is currently common at inshore caves throughout the northern Levantine coasts as far as Bodrum peninsula but has not yet expanded its range towards the northern Aegean Sea. It is probably a highly adaptive species that can tolerate a wide range of physico-chemical conditions. Bilecenoglu and Taskavak (1999) reported a population of P. vanicolensis inhabiting the brackish water caves in Antalya Bay, where the seasonal salinity ranged between 0.6 and 5‰. The species is generally caught by gill-nets but often discarded since it has no commercial value. Mugilidae Liza carinata (Valenciennes, 1836): The Keeled mullet is confined to the northeastern Levant coasts of Turkey, seemingly not even expanding to Antalya Bay since its introduction during the late 1950’s. All previous records from the southern Aegean Sea are probably erroneous (Bilecenoglu et al., 2002). Although its proportion among the local native mullet catch is remarkably low, L. carinata is sometimes of interest to artisanal fishermen but with minor commercial value due to its small size. Liza haematocheilus (Temminck and Schlegel, 1845): Among all alien fishes of Turkey, Pilengas mullet represents an exceptional case because of its origin. The species was anthropogenically introduced to the Azov and Black Seas for aquaculture purposes and subsequently penetrated to Turkish coasts (Unsal, 1992) and then to the Sea of Marmara and the central Aegean Sea (Kaya et al., 1998). Taxonomy of this species is complicated. According to Parin (2003), previous records from various localities as Mugil soiuy (or M. so-iuy) refers to Liza haematocheila. In a phylogenetic study of mugilids from Greece using mtDNA sequence analysis, the close relationship between genera Chelon and Liza was demonstrated (Papasotiropoulos et al., 2007), providing support to earlier revisions that consider Chelon haematocheilus as a valid name for the Pilengas mullet (Chang et al., 1999). In contrast, the species was clustered together with the native Mugil cephalus by Turan et al. (2005), who used allozyme electrophoresis to examine phylogenetic relationships between nine mullets inhabiting Turkey. At this stage, the use of L. haematocheilus should be preferred until mugilid taxonomy is settled. The species became so abundant that large quantities were fished during the late 1990’s and marketed in several cities at cheap prices. There is a distinct annual fluctuation in the population of L. haematocheilus, which generally provides catches during the early summer and autumn. Unlike the very common occurrence of the species in the Black Sea, a relatively rare population can be observed in the northern and central Aegean Sea. To the best available knowledge, no further specimens have been captured from Homa Lagoon in Izmir Bay since 1998. Population dynamics of this species was studied by Okumus and Bascinar (1997) who obtained a maximum specimen length of 66.7 cm (corresponding to 6 years of age)

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and the following growth parameters were estimated: L∞ (cm) = 71.9, W∞ (g) = 3412.7, k= 0.26 year−1, t0 = −1.57 years. (See: Minos et al. in this book for reproduction and other aspects of this species). Labridae Pteragogus pelycus Randall, 1981 (Fig. 6): A prevalent species along the Turkish coast, reported from Iskenderun (Taskavak et al., 2000) and Gokova Bays (Bilecenoglu et al., 2002). Studies have shown that P. pelycus is more common in the vicinity of Rhodes, but relatively rare elsewhere (Golani et al., 2002). This small sized non-commercial wrasse is not of interest to fisheries. Callionymidae Callionymus filamentosus Valenciennes, 1837 : Observed during 1983 for the first time at the trawl grounds of Iskenderun Bay, Mersin and Anamur, with decreasing abundance towards the west (Gücü et al., 1994). It is currently distributed along the entire northern Levant coasts but not in the Aegean Sea. It is a common species in the bottom trawl catch and is usually discarded. Except for its length-weight relationship (Taskavak and Bilecenoglu, 2001) no further data is available. Gobiidae Oxyurichthys petersi (Klunzinger, 1871): This Red Sea endemic goby was first found off Mersin coasts (as O. papuensis by Kaya et al., 1992), almost a decade after its introduction to the Mediterranean Sea. Commonly captured by bottom trawlers and always discarded since it is a non-commercial fish. There is a clear abundance gradient for O. petersi along the Turkish coast while becoming relatively rare towards Fethiye Bay. Although the spe-

Fig. 6. A juvenile Pteragogus pelycus from Fethiye Bay (specimen total length ca. 5 cm) (Photograph: Melih E. Cinar).

Alien marine fishes of Turkey – an updated review 205

cies was presented by Akyol et al. (2006) as a new record from the Aegean Sea, it was previously recorded from the area by Benli et al. (1999). Vanderhorstia mertensi Klausewitz, 1974 (Fig. 7): The Shrimp-goby is the most recent alien fish in the Mediterranean Sea, first recorded from Fethiye Bay (Bilecenoglu et al., 2008). Sandy and muddy substrates at depths ranging 2 to 52 m were strikingly invaded by V. mertensi, which was generally found in association with the Alpheid shrimps, although in smaller quantities, the species also inhabits burrows close to seagrass beds. Since it was observed only at a single locality that is very far from the Suez Canal, its mode of introduction is unclear at the moment. A wider distribution range in the eastern Mediterranean can be expected. Siganidae Siganus luridus (Rüppell, 1829): A common species at Turkish coasts, known since the 1970’s. Despite its commercial value and widespread distribution along the northern Levant and the southern Aegean Sea, no biological studies have been carried out in Turkey until now. Artisanal fishermen capture the species with a variety of fishing gears, but the other congeneric S. rivulatus is much preferred commercially. According to scuba observations, adults may form very large schools of up to 500 or more individuals during late spring (M. Bilecenoglu, pers. obs.). Siganus rivulatus Forsskål, 1775: The Marbled spinefoot is among the most abundant alien fishes of the northern Levant shores, whose distribution extends as far as Candarli Bay in the northern Aegean Sea. It is captured generally by trammel nets in large quantities and by trawlers to a lesser extent. In several bays, S.rivulatus is a target species of artisanal fishermen. Total annual catch remains a question mark, however it is likely to be included in official fishery statistics together with Sarpa salpa (Bilecenoglu and Kaya, 2002).

Fig. 7. A presumed female (left) and male (right) specimen of Vanderhorstia mertensi from Fethiye Bay (specimen total lengths about 7 – 8 cm) (Photographs: Serdar Sozen and Alper Dogan).

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Despite its commercial importance and abundance, biological information on S.rivulatus from Turkey is scarce. A maximum age of 8 was determined using posterior body scales and growth parameters estimated as: L∞ (cm) = 22.3, W∞ (g) = 137.9, k= 0.28 year−1, t0 = −0.50 years (Bilecenoglu and Kaya, 2002). In a recent study from Lebanon, Bariche (2005) indicated that ageing of the Marbled spinefoot by scales does not seem to be an accurate method and he found larger individuals with smaller corresponding ages (i.e. 26.7 cm / 6 years) by otolith readings. According to results of the length-weight relationship, the value “b” ranges between 3.13 and 3.22, indicating a positive allometric growth (Bilecenoglu and Kaya, 2002). The species’ spawning season begins in July and continues until the end of August (Yeldan and Avsar, 2000). Sphyraenidae Sphyraena obtusata Cuvier, 1829: Only a single record of the Obtuse barracuda (as S.flavicauda) by Bilecenoglu et al. (2002) exists from Turkey, based on two specimens collected off Antalya Bay. In recent taxonomical revisions based on morphological (Doiuchi and Nakabo, 2005) and molecular characteristics (Doiuchi and Nakabo, 2007) of the “S. obtusata” group, S. flavicauda Rüppell, 1838 was considered as a synonym of S. obtusata. Unlike its alien congeneric S. pinguis, the species did not form an abundant population along the northeastern Mediterranean but a wider distribution range can be expected. Recent findings from Rhodes (Corsini et al., 2005) revealed that S. obtusata was most probably overlooked in previous studies. Sphyraena pinguis Günther, 1874: This species is commonly observed in the northern Levant since the late 1950’s. The species name S. chrysotaenia was widely used previously in literature and is currently considered a synonym of S. pinguis (Doiuchi and Nakabo, 2005, 2007). Contribution of this species to trawl catch composition is limited; maximum CPUE was 99.5 g/h during 1983 along Mersin coasts (Gücü et al., 1994) and formed only 0.48% of the total alien fish biomass (Cicek, 2006). Larger quantities are generally fished with purse seiners. Current distribution of this species includes the entire northern Levant and up to Izmir Bay in the central Aegean Sea. Scombridae Scomberomorus commerson (Lacepède, 1800): Since the early 1980’s, the Narrow-barred Spanish mackerel has become abundant in the eastern Mediterranean Sea almost five decades since its first record (Golani et al., 2002). Gücü et al. (1994) obtained two specimens from Mersin coasts by gill-nets during 1981 and indicated its increasing commercial importance in the local fisheries. By 1994 the species reached Gokova Bay, providing a catch of up to 200 individuals per day (Buhan et al., 1997). On a few occasions, S. commerson was also observed off the Cesme peninsula (central Aegean Sea). It is currently considered a prevalent species along the Levantine and southern Aegean Sea coasts, becoming common only during the late autumn and winter. Available data on the species include only its length-weight relationship and condition factor from Gokova bay (Buhan et al., 1997).

Alien marine fishes of Turkey – an updated review 207

Cynoglossidae Cynoglossus sinusarabici (Chabanaud, 1931): Although this species is one of the earliest alien fishes of Turkey (Akyüz, 1957), it has a limited distribution between Iskenderun Bay and Mersin coasts, not extending westwards. Said to be common in the eastern Mediterranean (Golani et al., 2002), but relatively less abundant in northeastern Levant, with a proportion of 1.2% in the total alien fish biomass (Cicek, 2006). Often discarded from the trawl catch due to its non-commercial value and small size. The “b” value of the length-weight relationship ranges between 2.41 and 2.96 (Cicek et al., 2006; Sangün et al., 2007). Length at first maturity is 6.8 – 6.9 cm for males and females, respectively; spawning takes place in two seasons (May – July and September – December) (Yeldan et al., 2006). The authors also determined ages, with a maximum of 5 years for a 15.1 cm length specimen. Monacanthidae Stephanolepis diaspros Fraser and Brunner, 1940: The Reticulated filefish was an early colonizer of Anatolian coasts, dispersing to Kusadasi Bay in the southern Aegean Sea. The species is commonly observed in the bottom trawl catch composition, having no commercial value and usually discarded. It seems to present a spawning aggregation during late autumn and winter, since its biomass within the total of alien fishes increases two or three folds in November and December (Cicek, 2006). No detailed biological information is available from Turkey, except for some few data on the length-weight relationship (Taskavak and Bilecenoglu, 2001; Sangün et al., 2007). Two specimens of S. diaspros collected from Antalya and Iskenderun Bays had total lengths of 21.5 and 22.0 cm (M. Bilecenoglu, unpub. data), slightly higher than the value reported by Golani et al. (2002). Tetraodontidae Lagocephalus spadiceus (Richardson, 1844): This species is distributed along the northern Levant coasts and the southern Aegean Sea, being common at Iskenderun and Antalya Bays, but less abundant elsewhere. A recent paper reports a single specimen of L. spadiceus from the Sea of Marmara, representing the first occurrence of a Red Sea originated fish in the area (Tuncer et al., 2008). Bottom trawlers of the northeast Levant capture the species frequently, generally in small quantities that are always discarded. Similar to its confamilial members, L. spadiceus is potentially a lethal fish with several toxic organs (Golani et al., 2002). Lagocephalus suezensis Clark and Gohar, 1953: Only a few occurrence records are available from the eastern Mediterranean Sea, however, the species is currently the most abundant pufferfish of the northern Levant (together with L. sceleratus). Although it was first recorded a decade ago by Avsar and Cicek (1999) (misidentified as Sphoeroides cutaneus), L. suezensis was probably introduced to Anatolian coasts much earlier. It is possible to see the species in every bottom trawl catch, including very small sized specimens with lengths

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between 4 – 6 cm. The current distribution of L. suezensis includes the entire northern Levant shores and the southern Aegean Sea (Bilecenoglu et al., 2002). During night dives, several individuals can be observed resting on the sandy grounds of inshore waters (Fig. 8). Lagocephalus sceleratus (Gmelin, 1789): This species can be regarded as one of the “worst alien fishes” of the entire Mediterranean Sea; harmful to both human health and fishing gears. Only a single individual from Gokova Bay was known until 2004, followed by successive records throughout a large coastline covering the entire northern Levant, southern and central Aegean Seas (Bilecenoglu et al., 2006). In terms of biomass, L. sceleratus is currently the most common pufferfish at Turkish coasts. Due to its large size, the species was marketed in some fishing ports and some cases of poisonings have been observed especially at the northeast Levant shores (see Eisenman, 2008 and Bentur et al., 2008). The Turkish Ministry of Agriculture and Rural Affairs has recently banned the fishing and marketing of L. sceleratus in Turkey. In addition to its toxic nature, this species has powerful jaws that can easily cut bottom longlines; complaints of local fishermen on this matter have been published several times in newspapers. A hobby fishing attempt in Fethiye Bay resulted with three broken fishing lines, ten missing hooks and one L.sceleratus caught (slightly over 1 kg), just within five minutes (Fig. 9). Sphoeroides pachygaster (Müller and Troschel, 1848): The Blunthead puffer has penetrated the Mediterranean Sea via Gibraltar and then reached the Levant Sea (Golani et al., 2002). Recorded from only a few localities along the Turkish coasts, it is possibly absent from the coastline between Iskenderun Bay to Mersin; however, some specimens were obtained from Antalya Bay, Gokova Bay (M. Bilecenoglu, unpub. data) and Saros Bay (northern Aegean Sea) (Eryilmaz et al., 2003).

Fig. 8. A Lagocephalus suezensis specimen (total length ca. 15 cm) observed during a night time scuba dive at Fethiye Bay (Photograph: Melih E. Cinar).

Alien marine fishes of Turkey – an updated review 209

Torquigener flavimaculosus Hardy and Randall, 1983: Since its first record in the eastern Mediterranean Sea, the Dwarf blaasop have been reported only from a few localities. Despite extensive surveys along the northern Levant coasts, T. flavimaculosus can only be observed in Turkey in Fethiye Bay (Fig. 10), where the population is regarded

Fig. 9. Lagocephalus sceleratus is a nuisance alien species, harmful to human health and small scale fisheries. The photograph shows a specimen caught by a fishing line from Fethiye Bay (Photograph: Betil Ergev).

Fig. 10. The Dwarf blaasop – the most abundant pufferfish of Fethiye Bay (specimen total length ca. 10 cm) (Photograph: Melih E. Cinar).

210 Murat Bilecenoglu

as common. In a single paper related to its biology, its burrowing behavior was observed, which is apparently a strategy for predator avoidance or an adaptation to increase foraging success (Bilecenoglu, 2005). QUESTIONABLE ALIENS There are several cases of fish species previously reported from Turkey where essential information is not available to support their occurrence. In the checklist of Turkish marine fishes, Bilecenoglu et al. (2002) listed 45 doubtful records, including the following 10 alien species: Hyporhamphus affinis (Günther, 1866), Tylosurus choram (Rüppell, 1837), Platycephalus indicus (Linnaeus, 1758), Epinephelus tauvina (Forsskål, 1775), Pomadasys stridens (Forsskål, 1775), Crenidens crenidens (Forsskål, 1775), Parupeneus barberinus (Lacepède, 1801), Rastrelliger kanagurta (Cuvier, 1816), Bothus pantherinus (Rüppell, 1828) and Diodon hystrix Linnaeus, 1758. No specimens of the above mentioned species have yet been collected from the region and they should not be treated as a part of the local ichthyofauna until a relevant individual specimen has been provided. A further species, Solea senegalensis Kaup, 1858, listed from the Sea of Marmara and the Aegean and Levantine coasts of Turkey during 1942 should also be considered as doubtful (Cinar et al., 2005). The actual distribution range of S. senegalensis is confined to the western Mediterranean Sea and no data of even a single occurrence is available from the eastern basin (Golani et al., 2002). The recent report of Boreal-Atlantic originated Syngnathus rostellatus Nilsson, 1855 from Antalya Bay (Gokoglu et al., 2004) seems to be based on a misidentification. In the photograph presented, the elevated median dorsal postorbital region is conspicuous and the long snout is clearly seen. According to Dawson (1986), the head is not elevated in S. rostellatus and the snout length is less than half head length. Moreover, the total length of the Antalya Bay specimen (187 mm) is longer than the maximum length of S. rostellatus reported to date (170 mm; Dawson, 1986). Finally, Carangoides bajad (Forsskål, 1775) was recorded by Ozturk (2005) from a photograph presumed to be taken from Fethiye Bay but is clearly erroneous (Golani, 2006). CONCLUSIONS The influx of alien species to the Mediterranean is a continuous phenomenon, with an increasing trend. A total of 33 non-native fish was reported by Bilecenoglu et al. (2002) from Turkey, within the next six years the number increased to 49. It is almost certain that several species have already arrived to Anatolian coasts, waiting to be recognized and recorded. There are 10 casual aliens versus 39 established ones. Although suitable ecological conditions (i.e. unsaturated habitats, sufficient food resources etc.) do not guarantee a suc-

Alien marine fishes of Turkey – an updated review 211

cessful establishment for an alien species, several fish species seem to carry out step-by-step colonization over time. Some species previously regarded as rare have now prevalent or common populations, but there is always a possibility that they could have been overlooked. At least a dozen fish species can be listed among the commercial aliens, some of which are treated as a target species since the 1970’s. Although official capture fish statistics may provide a good basis in demonstrating the impact of non-native fishes, lack of species-specific landing data of Turkey is a big gap for the relevant analysis. Only a few studies on the contribution of non-native species to trawl fisheries of the northeastern Levant was published and fishery related status of aliens along rest of the Anatolian coast is still a question mark. Life history parameters of alien fishes deserve special interest, in order to understand their biological characteristics and role in local food webs. Published papers on the subject are few, dealing generally with commercial species such as Upeneus spp., S. undosquamis and E.teres. Discrepancies in growth parameters as mentioned above are good indicators of the necessity for more detailed and meticulous studies. Except for a single attempt to provide a model of northeastern Mediterranean fisheries (Gücü, 1995), no ecological models were constructed until now. Such models can serve to demonstrate predator-prey relationships and provide essential information for regulation and management of local fisheries. ACKNOWLEDGEMENTS I am grateful to Prof. Dr. Melih E. Cinar, Tahsin Ceylan, Prof. Dr. Alp Can, Serdar Sozen, Alper Dogan and Betil Ergev for the photographs. Some observations mentioned in the text were carried out during the TUBITAK project no. 104Y065 and the Fethiye Bay marine biodiversity project (Ministry of Environment and Forestry, Republic of Turkey). REFERENCES Aasen, O. and E. Akyüz. 1956. Some data concerning the fisheries in Iskenderun Bay. Fishery Research Center Reports, Meat and Fish Office, Marine Research Series 1 (4): 5-20. Ak Orek, Y. 2008. The first Mediterranean record of eggs and yolk-sac larvae of Indo-Pacific Chirocentrus dorab (Forsskål, 1775) (Teleostei: Chirocentridae). 32nd Annual Larval Fish Conference, August 4-7, 2008, Kiel, Germany (abstract). Akyol, O., V. Unal and T. Ceyhan. 2006. Occurrence of two Lessepsian migrant fish, Oxyurichthys petersi (Gobiidae) and Upeneus pori (Mullidae), from the Aegean Sea. Cybium 30(4): 389-390. Akyol, O., H.T. Kinacigil and R. Sevik. 2007. Longline fishery and length-weight relationships for selected fish species in Gokova Bay (Aegean Sea, Turkey). International Journal of Natural and Engineering Sciences 1: 1-4 Akyüz, E. 1957. Observations on the Iskenderun red mullet (Mullus barbatus) and its environment. GFCM Proceedings and Technical Papers 4(38): 305-326.

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Altan, H. 1998. Ege’nin dibinde bir hayal alemi: Sarigerme. Gezi, National Geographic Traveler 1 (5): 60-75. Anonymous. 1968. Dogu Akdeniz trawl sahalarinda 1968 Subatinda yapilan calismalar. Hidrobiyoloji Arastirma Enstitusu Yayinlari, Istanbul, 38 pp. Anonymous, 1983. Antalya Korfezi’nde ekonomik degere haiz su ürünlerinin avlanmalarina iliskin üreme periyotlarinin tespiti projesi. Tarım ve Koyisleri Bakanligi Su Urünleri Daire Baskanligi: Antalya, 34 pp. Avsar, D. and E. Cicek, E. 1999. A new species record for the central and eastern Mediterranean; Sphoeroides cutaneus (Günther, 1870) (Pisces: Tetraodontidae). Oebalia 25: 17-21. Bariche, M. 2005. Age and growth of Lessepsian rabbitfish from the eastern Mediterranean. Journal of Applied Ichthyology 21: 141-145. Basusta, N. and U. Erdem. 2000. Iskenderun Korfezi baliklari üzerine bir arastirma. Turkish Journal of Zoology 24: 1-19. Basusta, N., U. Erdem and M. Kumlu. 1998. Two new fish records for the Turkish seas: round stingray Taeniura grabata and skate stingray Himantura uarnak (Dasyatidae). Israel Journal of Zoology 44: 65-66. Basusta, N., U. Erdem and S. Mater. 1997. Iskenderun Korfezi’nde yeni bir Lesepsiyen gocmen balik türü; kizilgozlü sardalya, Etrumeus teres (Dekay, 1842). Akdeniz Balikcilik Kongresi, Izmir, pp. 921-924. Benli, H.A., B. Cihangir and K.C. Bizsel. 1999. Ege Denizi’nde bazi demersal balikcilik kaynaklari üzerine arastirmalar. Istanbul Üniversitesi Su Urünleri Dergisi, 301-369. Bentur, Y., J. Ashkar, Y. Lurie, Y. Levy, Z. Azzam, M. Litmanovich, B. Gurevych, D. Golani and A. Eisenman. 2008. Lessepsian migration and tetrodotoxin poisoning due to Lagocephalus sceleratus in the eastern Mediterranean. Toxicon 52: 964-968. Ben-Tuvia, A. 1953. Mediterranean fishes of Israel. Bulletin of the Sea Fisheries Research Station, Haifa 8: 1-40. Ben-Tuvia, A. 1966. Red Sea fishes recently found in the Mediterranean. Copeia 2: 254-275. Bilecenoglu, M. 2004. Occurrence of the Lessepsian migrant fish, Sillago sihama (Forsskål, 1775) (Osteichthyes: Sillaginidae), from the Aegean Sea. Israel Journal of Zoology 50: 420-421. Bilecenoglu, M. 2005. Observations on the burrowing behaviour of dwarf blaasop, Torquigener flavimaculosus Hardy & Randall, 1983 (Osteichthyes: Tetraodontidae) along Fethiye Coasts, Turkey. Zoology in the Middle East 35: 29-34. Bilecenoglu, M. 2007. First record of Monotaxis grandoculis (Forsskål, 1775) (Osteichthyes, Lethrinidae) in the Mediterranean Sea. Aquatic Invasions 2 (4): 466-467. Bilecenoglu, M. and M. Kaya. 2002. Growth of marbled spinefoot Siganus rivulatus Forsskål, 1775 (Teleostei: Siganidae) introduced to Antalya Bay, eastern Mediterranean Sea (Turkey). Fisheries Research 54: 279-285. Bilecenoglu, M. and E. Taskavak. 1999. Some observations on the habitat of the Red Sea immigrant sweeper, Pempheris vanicolensis, on the Mediterranean coast of Turkey. Zoology in the Middle East 17: 67-70. Bilecenoglu, M. and M. Kaya. 2006. A new alien fish in the Mediterranean Sea – Platax teira (Forsskål, 1775) (Osteichthyes: Ephippidae). Aquatic Invasions 1 (2): 80-83. Bilecenoglu, M., E. Taskavak, S. Mater and M. Kaya. 2002. Checklist of the marine fishes of Turkey. Zootaxa 113: 1-194.

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Bilecenoglu, M., M. Kaya and S. Akalin. 2006. Range expansion of silverstripe blaasop, Lagocephalus sceleratus (Gmelin, 1789), to the northern Aegean Sea. Aquatic Invasions 1(4): 289-291. Bilecenoglu, M., M.B. Yokes and A. Eryigit. 2008. First record of Vanderhorstia mertensi Klausewitz, 1974 (Pisces, Gobiidae) in the Mediterranean Sea. Aquatic Invasions 3(4): 475-478. Bingel, F. 1981. Erdemli – Icel bolgesi balikciligi gelistirme projesi kesin raporu. T.C. Basbakanlik Devlet Planlama Teskilati: Ankara. 154 pp. Bingel, F. 1987. Dogu Akdeniz’de kiyi balikciligi av alanlarinda sayisal balikcilik projesi kesin raporu. T.C. Basbakanlik Devlet Planlama Teskilati: Ankara. 312 pp. Bingel, F., E. Ozsoy and U. Unluata. 1993. A review of the state of the fisheries and the environment of the northeastern Mediterranean (Northern Levantine Basin). Studies and Reviews, General Fisheries Council for the Mediterranean, No. 65. Rome: FAO. 74 pp. Buhan, E., H. Yilmaz, Y. Morkan, E. Büke and A. Yüksek. 1997. Güllük ve Gokova Korfezleri icin yeni bir av potansiyeli: Scomberomorus commerson (Lacepède, 1800) (Pisces – Teleostei). Akdeniz Balikcilik Kongresi, Izmir, p. 937-944. Can, A. and M. Bilecenoglu. 2005. Türkiye denizleri’nin dip baliklari atlasi. Arkadas Yayinevi: Ankara. 224 pp. Chang, C.W., C.S. Huang and W.N. Tzeng. 1999. Redescription of redlip mullet Chelon haematocheilus (Pisces: Mugilidae) with a key to mugilid fishes in Taiwan. Acta Zoologica Taiwanica 10(1): 37-43. Cicek, E. 2006. Karatas (Adana) aciklarinda dip trolleriyle avlanan ekonomik potansiyele sahip türlerin incelenmesi. Cukurova Universitesi Fen Bilimleri Enstitüsü, Doktora Tezi, Adana, 146 pp. Cicek, E. and M. Bilecenoglu. 2009. A new alien fish in the Mediterranean Sea: Champsodon nudivittis (Actinopterygii: Perciformes: Champsodontidae). Acta Ichthyologica et Piscatoria 39: 67-69. Cicek, E., D. Avsar, H. Yeldan and M. Ozutok. 2006. Length–weight relationships for 31 teleost fishes caught by bottom trawl net in the Babadillimani Bight (northeastern Mediterranean). Journal of Applied Ichthyology 22: 290-292. Cinar, M.E., M. Bilecenoglu, B. Oztürk, T. Katagan and V. Aysel. 2005. Alien species on the coasts of Turkey. Mediterranean Marine Science 6(2): 119-146. Cinar, M.E., M. Bilecenoglu, B. Oztürk and A. Can. 2006. New records of alien species on the Levantine coast of Turkey. Aquatic Invasions 1(2): 84-90 Corsini, M., P. Margies, G. Kondilatos and P.S. Economidis. 2005. Lessepsian migration of fishes to the Aegean Sea: First record of Tylerius spinosissimus (Tetraodontidae) from the Mediterranean, and six more fish records from Rhodes. Cybium 29(4): 347-354. Dalyan, C. and L. Eryilmaz. 2009. The Arabian scad Trachurus indicus Nekrasov, 1966, a new Indo-Pacific in the Mediterranean Sea. Journal of Fish Biology 74: 1615-1619. Dawson, A. 1986. Syngnathidae. In: Whitehead, P.J.P., M.L. Bauchot, J.C. Hureau, J. Nielsen and E.Tortonese (eds.), Fishes of the North-eastern Atlantic and the Mediterranean. Vol. 2. Paris: UNESCO. pp.628-639. Doiuchi, R. and T. Nakabo. 2005. The Sphyraena obtusata group (Perciformes: Sphyraenidae) with a description of a new species from southern Japan. Ichthyological Research 52(2): 132-151. Doiuchi, R. and T. Nakabo. 2007. Molecular evidence for the taxonomic status of three species of the Sphyraena obtusata group (Perciformes: Sphyraenidae) from East Asia. Ichthyological Research 54(3): 313-316. Eisenman, A., V. Rusetski, D. Sharivker, Z. Yona and D. Golani, 2008. An odd pilgrim in the Holyland. American Journal of Emergency Medicine. (electronic) 26: 383.e3-e6

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Erazi, R.A.R. 1943. Leiognathus mediterraneus nov. sp.. Compte rendu annuel et archives de la Société Turque des Sciences Physiques et Naturelles 10: 49-53. Eryilmaz, L. and C. Dalyan. 2006. First record of Apogon queketti Gilchrist (Osteichthyes: Apogonidae) in the Mediterranean Sea. Journal of Fish Biology 69: 1251-1254. Eryilmaz, L., M. Ozulug and N. Meric. 2003. The Smooth pufferfish, Sphoeroides pachygaster (Müller & Troschel, 1848) (Teleostei: Tetraodontidae), new to the northern Aegean Sea. Zoology in the Middle East 28: 125-126. Filiz H., S.C. Akcinar, E. Ulutürk, B. Bayhan, E. Taskavak, T.M. Sever, G. Bilge and E. Irmak. 2007. New records of Bregmaceros atlanticus (Bregmacerotidae), Echiodon dentatus (Carapidae), and Nemichthys scolopaceus (Nemichthyidae) from the Aegean Sea. Acta Ichthyologica et Piscatoria 37 (2): 107-112. Geldiay, R. 1969. Izmir Körfezinin baslica baliklari ve muhtemel invasionlari. Ege Üniversitesi Fen Fakültesi Monografileri, Izmir, 135 pp. Gokce, G., L. Sangün, H. Ozbilgin and M. Bilecenoglu. 2007. Growth and mortality of the brushtooth lizardfish (Saurida undosquamis) in Iskenderun Bay (eastern Mediterranean Sea) using length frequency analysis. Journal of Applied Ichthyology 23: 697-699. Gokoglu, M.,T. Bodur and Y. Kaya. 2003. First record of the Red Sea bannerfish (Heniochus intermedius Steindachner, 1893) from the Mediterranean Sea. Israel Journal of Zoology 49: 324-325. Gokoglu, M., T. Bodur and Y. Kaya. 2004. First records of Hippocampus fuscus and Syngnathus rostellatus (Osteichthyes: Syngnathidae) from the Anatolian coast (Mediterranean Sea). Journal of the Marine Biological Association of the UK 84 (5): 1093-1094. Gokoglu, M., O. Güven, B.A. Balci, H. Colak and D. Golani. 2008. First records of Nemichthys scolopaceus and Nemipterus randalli and second record of Apterichthus caecus from Antalya Bay, Southern Turkey. JMBA2 – Biodiversity Records 6234: 1-3. Golani, D. 1996. The marine ichthyofauna of the eastern Levant – history, inventory and characterization. Israel Journal of Zoology 42: 15-55. Golani, D. 2006. The Indian scad (Decapterus russelli), (Osteichthyes: Carangidae), a new IndoPacific fish invader of the eastern Mediterranean. Scientia Marina 70(4): 603-605. Golani, D., B. Appelbaum-Golani and O. Gon. 2008. Apogon smithi (Kotthaus, 1970) (Teleostei: Apogonidae), a Red Sea cardinalfish colonizing the Mediterranean Sea. Journal of Fish Biology 72: 1534-1538. Golani, D., L. Orsi-Relini, E. Massutí and J.P. Quignard. 2002. CIESM Atlas of exotic species in the Mediterranean. Vol.1. Fishes. F.Briand (ed.), Monaco: CIESM. 254 pp. Golani, D., B. Oztürk and N. Basusta. 2006. Fishes of the eastern Mediterranean. Turkish Marine Research Foundation, Publication No. 24, Istanbul: TUDAV. 259 pp. Golani, D. and O. Sonin. 2006. The Japanese threadfin bream Nemipterus japonicus, a new IndoPacific fish in the Mediterranean. Journal of Fish Biology 68: 940-943. Goren, M. and B.S. Galil. 2006. Additional records of Bregmaceros atlanticus in the eastern Mediterranean – an invasion through the Suez Canal or in ballast water? JMBA2 – Biodiversity Records 5459: 1-2. Goren, M., M.B. Yokes, B.S. Galil and A. Diamant. 2008. Indo-Pacific cardinal fishes in the Mediterranean Sea – new records of Apogon smithi from Turkey and A.queketti from Israel. JMBA2 – Biodiversity Records 6417: 1-5. Gücü, A. 1995. A box model for the basic elements of the northeastern Mediterranean Sea trawl fisheries. Israel Journal of Zoology 41: 551-567.

Alien marine fishes of Turkey – an updated review 215

Gücü, A.C., F. Bingel, D. Avsar and N. Uysal. 1994. Distribution and occurrence of Red Sea fish at the Turkish Mediterranean coast – northern Cilician Basin. Acta Adriatica 34(1/2): 103-113. Ismen, A. 2002. Age, growth, sex ratio and spawning season of lizardfish (Saurida undosquamis Richardson, 1848) in the Iskenderun Bay, eastern Mediterranean. Workshop on Lessepsian Migration Proceedings, Turkish Marine Research Foundation Publications 9: 108-115. Ismen, A. 2003. Maturity and fecundity of lizardfish (Saurida undosquamis Richardson, 1848) in Iskenderun Bay (Eastern Mediterranean). Turkish Journal of Zoology 27: 231-238. Ismen, A. 2005. Age, growth and reproduction of the goldband goatfish, Upeneus moluccensis (Bleeker, 1855), in Iskenderun Bay, the Eastern Mediterranean. Turkish Journal of Zoology 29: 301-309. Ismen, A., 2006. Growth and reproduction of Por’s goatfish (Upeneus pori Ben-Tuvia & Golani, 1989) in Iskenderun Bay, the Eastern Mediterranean. Turkish Journal of Zoology 30: 91-98. Kaya, M., S. Mater and H.A. Benli. 1992. A new Indo-Pacific gobiid fish Oxyurichthys papuensis (Val., 1837) for eastern Mediterranean coasts of Turkey. Rapports et Procès-Verbaux des Réunions Commission Internationale pour L’Exploration Scientifique de la Mer Méditerranée 33: 298. Kaya, M., S. Mater and A.Y. Korkut. 1998. A new grey mullet species «Mugil so-iuy Basilewsky” (Teleostei: Mugilidae) from the Aegean coast of Turkey. Turkish Journal of Zoology 22: 303-306. Kaya M., H.A. Benli, T. Katagan and O. Ozaydin. 1999. Age, growth, sex-ratio, spawning season and food of golden banded goatfish, Upeneus moluccensis Bleeker (1855) from the Mediterranean and south Aegean Sea coasts of Turkey. Fisheries Research 41: 317-328. Kimura, S., H. Motomura and Y. Iwatsuki. 2008. Equulites Fowler 1904, a senior synonym of Photoplagios Sparks, Dunlap and Smith 2005 (Perciformes: Leiognathidae). Ichthyological Research 55: 204-205. Kosswig, C. 1950. Erythräische fische im Mittelmeer und an der grenze der Ägais. Syllegomena Biologica, Festschrift Kleinschmidt, 203-212. Kosswig, C. 1956. Facts and problems offered by the Erythrean invaders into the Mediterranean. Balik ve Balikcilik 4(9): 31-37. Lelli, S., F. Colloca, P. Carpentieri and B.C. Russell. 2008. Establishment of the threadfin bream Nemipterus randalli Russell, 1986 (Perciformes: Nemipteridae) in the eastern Mediterranean Sea. Journal of Fish Biology 73(3): 740-745. Mater, S. and M. Kaya, M. 1987. Türkiye’nin Akdeniz sularinda yeni kaydedilen üc balik türü, Sudis hyalina Rafinesque, Pelates quadrilineatus (Bloch), Apogon nigripinnis Cuvier (Teleostei), hakkinda. Doga-Türk Zooloji Dergisi 11(1): 45-49. Okumus, I. and N. Bascinar. 1997. Population structure, growth and reproduction of introduced Pacific mullet, Mugil so-iuy, in the Black Sea. Fisheries Research 33: 131-137. Okus E., H.I. Sur, A. Yüksek, I.N. Yilmaz, A. Aslan-Yilmaz, S.U. Karhan, M.I. Oz, N. Demirel, S. Tas, A. Altiok, A.E. Müftüoglu, C. Gazioglu and Z.Y. Yücel. 2004. Datca-Bozburun Ozel Cevre Koruma Bolgesinin Denizsel ve Kiyisal Alanlarinin Biyolojik Cesitliliginin Tespiti Projesi. T.C. Cevre ve Orman Bakanligi Ozel Cevre Koruma Kurumu Baskanligi, Ankara. 698 pp. Okus E., A. Yüksek, I.N. Yilmaz, A. Aslan-Yilmaz, S.U. Karhan, N. Demirel, V. Demir, S. Zeki, S. Tas, H.I. Sur, H. Altiok, A.E. Müftüoglu, N.Balkis, A. Aksu, E. Dogan and C. Gazioglu. 2006. Gokova Ozel Cevre Koruma Bolgesinin Kiyi ve Deniz Alanlarinin Biyolojik Cesitliliginin Tespiti Projesi. T.C. Cevre ve Orman Bakanligi Ozel Cevre Koruma Kurumu Baskanligi, Ankara. 504 pp.

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Ozaydin, O. and S. Leblebici. 2008. Karatas onünde yasayan (dogu Akdeniz) eksi baligi’nin (Leiognathus klunzingeri Steindachner, 1898) büyümesi üzerine bir on calisma. Journal of Fisheries Sciences 2(5): 672-676. Ozturk, B. 2005. Marine life of Turkey in the Aegean and Mediterranean seas. Istanbul: TUDAV. 200 pp. Ozütok, M. and D. Avsar. 2003. Yumurtalik Koyu’ndaki (Adana) eksi baliklarinda (Leiognathus klunzingeri Steindachner, 1898) üreme. Turkish Journal of Veterinary and Animal Sciences 27: 1383-1389. Ozütok, M. and D. Avsar. 2004. Preliminary estimation of growth, mortality and the exploitation rates of the silverbelly (Leiognathus klunzingeri Steindachner, 1898) population from the Yumurtalık Bight, northeastern Mediterranean coast of Turkey. Turkish Journal of Fisheries and Aquatic Sciences 4: 59-64. Papaconstantinou, C. 1988. Check-list of marine fishes of Greece. Fauna Graeciae IV. Athens: Hellenic Zoological Society. 257 pp. Papasotiropoulos, V., E. Klossa-Kilia, S.N. Alahiotis and G. Kilias. 2007. Molecular phylogeny of grey mullets (Teleostei: Mugilidae) in Greece: evidence from sequence analysis of mtDNA segments. Biochemical Genetics 45: 623-636. Parin, N.V. 2003. Liza haematocheila: a correct name for pilengas mullet – M. soiuy (Mugilidae). Journal of Ichthyology 43(4): 322-323. Por, F.D. 1978. Lessepsian migration – the influx of Red Sea biota into the Mediterranean by way of the Suez Canal. Berlin: Springer. 228 pp. Sangün, L., E. Akamca and M. Akar. 2007. Weight-length relationships for 39 fish species from the north-eastern Mediterranean coast of Turkey. Turkish Journal of Fisheries and Aquatic Sciences 7: 37-40. Sciberras, M. and P.J. Schembri. 2007. A critical review of records of alien marine species from the Maltese Islands and surrounding waters (central Mediterranean). Mediterranean Marine Science 8(1): 41-66. Smith-Vaniz, W. F. 1984. Carangidae. In: Fischer, W. and G. Bianchi (eds.), FAO species identification sheets for fishery purposes. Western Indian Ocean (Fishing Area 51), Vol. I., Rome: FAO. Sparks, J.S., P.V. Dunlap and W.L. Smith. 2005. Evolution and diversification of a sexually dimorphic luminescent system in ponyfishes (Teleostei: Leiognathidae), including diagnoses for two new genera. Cladistics 21(4): 305-327. Taskavak, E., M. Bilecenoglu, N. Basusta and S. Mater. 2000. Occurrence of Pteragogus pelycus Randall, 1981 (Teleostei: Labridae) and Petroscirtes ancylodon Rüppell, 1838 (Teleostei: Blennidae) in Turkish Mediterranean waters. Acta Adriatica 41(2): 53 – 58. Taskavak, E. and M. Bilecenoglu. 2001. Length-weight relationships for 18 Lessepsian (Red Sea) immigrant fish species from the eastern Mediterranean coast of Turkey. Journal of the Marine Biological Association of U.K. 81: 895-896. Tuncer, S., H. Aslan Cihangir and M. Bilecenoglu. 2008. First record of the Lessepsian migrant Lagocephalus spadiceus (Tetraodontidae) in the Sea of Marmara. Cybium 32(4): 347-348. Turan, C., M. Caliskan and H. Kücüktas. 2005. Phylogenetic relationships of nine mullet species (Mugilidae) in the Mediterranean Sea. Hydrobiologia 532(1): 45-51. Türeli, C. and U. Erdem. 1997. Adana ili kiyi bolgesinde ekonomik oneme sahip balik türlerinden barbunya (Mullus barbatus Linnaeus, 1758) ve iskarmoz (Saurida undosquamis Richardson,

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1848) baliklarinin büyüme ozellikleri (Iskenderun Korfezi, Türkiye). Turkish Journal of Zoology 21: 329-334. Unsal, S. 1992. Türkiye denizleri icin yeni bir kefal baligi türü: Mugil so-iuy Basilewsky. Turkish Journal of Veterinary and Animal Sciences 16: 427-432. Whitehead, P.J.P. 1985. FAO species catalogue. Clupeoid fishes of the world (Suborder Clupeoidei). An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, anchovies and wolf-herrings. Part I – Chirocentridae, Clupeidae and Pristigasteridae. FAO Fisheries Synopsis, Vol.7., Rome: FAO, 303 pp. Yeldan, H. and D. Avsar. 2000. A preliminary study on the reproduction of the rabbitfish (Siganus rivulatus (Forsskål, 1775)) in the northeastern Mediterranean. Turkish Journal of Zoology 24: 173-182. Yeldan, H., D. Avsar, M. Ozütok, E. Cicek and C.E. Ozyurt. 2006. Kuzeydogu Akdeniz’deki (Mersin) sivrikuyruk dil baligi’nin (Cynoglossus sinusarabici Chabanaud, 1931) üreme donemi ve ilk üreme boyunun belirlenmesi üzerine bir on calisma. E.U. Su Urünleri Dergisi 23 (1/3): 519-522. Yilmaz, R. and B. Hossucu. 2003. Some biological parameters of round herring, Etrumeus teres (De Kay, 1842) in the Gulf of Antalya (Mediterranean Sea). E.U. Su Urünleri Dergisi 20 (1-2):1-8. Yilmaz, R., M. Bilecenoglu and B. Hossucu. 2004. First record of the antenna codlet, Bregmaceros atlanticus Good & Bean, 1886 (Osteichthys: Bregmacerotidae), from the eastern Mediterranean. Zoology in the Middle East 31: 111-112. Yokes, B., R. Dervisoglu and B. Karacik. 2002. Likya kiyilarinda denizel biyolojik zenginlik arastirmasi. Sualti Bilim ve Teknoloji Toplantisi Bildiriler Kitabi, Istanbul, 166-181. Zenetos, A., M.E. Cinar, M.A. Pancucci-Papadopoulou, J.G. Harmelin, G. Furnari, F. Andaloro, N. Bellou, N. Streftaris and H. Zibrowius. 2005. Annotated list of marine alien species in the Mediterranean with records of the worst invasive species. Mediterranean Marine Science 6 (2): 63-118. Zenetos, A., E. Meric, M. Verlaque, P. Galli, C.F. Boudouresque, A. Giangrande, M.E. Cinar and M. Bilecenoglu. 2008. Additions to the annotated list of marine alien biota in the Mediterranean with special emphasis on Foraminifera and Parasites. Mediterranean Marine Science 9 (1): 119-165.

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Current D. Golani & B. Appelbaum-Golani (Eds.)status 2010of alien fishes in Greek seas 219 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 219-253. © Pensoft Publishers Sofia–Moscow

Current status of alien fishes in Greek seas Maria Corsini-Foka

INTRODUCTION The Hellenic seas consist of the Aegean and the Ionian Seas; their general assessment in coastal and open areas, both from oceanographic and biological points of view, is provided in Papathanassiou and Zenetos (2005). The Mediterranean specific biodiversity includes a total of 664 fish species (Quignard and Tomasini, 2000) and in the Eastern Mediterranean 470 species have been recently listed (Golani et al., 2006). Among the Mediterranean ichthyofauna, more than 100 exotic fish species have been described (14% approximately), 30 or more of Atlantic origin and more than 65 of Indo-Pacific origin (Golani et al., 2002, 2006b; Reina-Hervás et al., 2004; Zenetos et al., 2005; Ben Souissi et al., 2005a, 2007; Dulčić and Golani, 2006; Eryilmaz and Dalyan, 2006; Golani and Sonin, 2006; Dulčić and Kraljevic, 2007; Ben Abdallah et al., 2007; Ben Rais Lasram and Mouillot, 2008; Lipej et al., 2008; Golani et al., 2008). In the Greek waters of the Aegean and Ionian seas, 447 species of fishes have been listed (Economidis, 1973; Papaconstantinou, 1988), this number increased to at least 480 by alien and native species recorded in the last decade (Golani et al., 2002, 2006b; Megalofonou et al., 2005; Mytilineou et al., 2005; Pancucci-Papadopoulou et al., 2005a, b; Corsini-Foka et al., 2006; Corsini-Foka and Economidis, 2007a, b; CorsiniFoka and Kalogirou, 2008; Corsini-Foka, unpublished data). Due to the temperate climate and the temperature ranges of the Greek marine coastal environment, which are 10oC-18oC in winter and 14oC-30oC in summer, the Hellenic ichthyofauna considered in its whole is typically temperate (Papaconstantinou et al., 2007), showing a higher percentage of thermophylic species in the warmer South Aegean Sea, including the Dodecanese continental shelf, as compared with the North Aegean Sea (Tortonese, 1947a; Papaconstantinou, 1988; Labropoulou, 2007) (Fig. 1). The distribution of the number of demersal fish species found during experimental trawl surveys decreases from the north and west to the south-east Aegean Sea (Labropoulou,

220 Maria Corsini-Foka

Fig. 1a. Typical winter surface temperature Fig. 1b. Typical summer surface temperature (above) and salinity (below) in the Greek seas (above) and salinity (below) in the Greek seas (www.poseidon.ncmr.gr). (www.poseidon.ncmr.gr).

2007), a region strongly subjected to influx of biota from the Eastern Mediterranean. The species inhabiting Hellenic seas may be classified into a) endemic, b) Atlantic origin, including also new colonizers, c) introduced by human activity and d) Indo-Pacific origin, as in the rest of the Mediterranean Sea (Corsini-Foka and Economidis, 2007a, b). According to Pancucci-Papadopoulou et al. (2005a), up to 2005, alien marine biota in Hellenic waters (phytoplankton, zooplankton, zoobenthos, phytobenthos, fishes) consisted of 126 species, the majority of which were represented by zoobenthos (63 species) followed by fish (32 species) and macroalgae (16 species). As assessed by the same authors, there has been an evident increase of chronological trends in the last two decades, while the main pathways of invasion were from the Suez Canal opening (60%), followed by accidental transportation via shipping (25%) and invasion via Gibraltar (5%). A bulk of 69 species was recorded in the SE Aegean Sea, where 90% of the alien biota was repre-

Current status of alien fishes in Greek seas 221

sented by Indo-Pacific species (Pancucci-Papadopoulou et al., 2005b). Recent updates added more than 30 alien species to the Hellenic marine biota, with a relative increased contribution of shipping and aquaculture as invasion pathways and a slight decrease of invasion via the Suez Canal (Pancucci-Papadopoulou et al., 2007; Elnais, 2008). Currently there are 34 non-native fish species in Greek seas (7% approximately of the total Greek marine ichthyofauna) while the occurrence of other species, mainly in estuaries, still needs to be confirmed (Corsini-Foka and Economidis, 2007b). Nonnative fishes belong to the last three groups mentioned above, i.e., (1) new colonizers of Atlantic origin, (2) human introduced species, mainly through aquaculture activities but other ways not to be excluded such as ship ballasts and (3) alien species of Indo-Pacific origin (variously called Lessepsian immigrants, allochthonous, Erythrean or Red Sea species), which have entered the Mediterranean via the Suez Canal. The manner and chronicle of invasive species in Hellenic waters, the spreading of these more or less recent colonizer fishes, some of which are truly invasive, and their impact on the native marine ecosystem structure, function, biodiversity and fishery are hereby discussed. NEW COLONIZERS OF ATLANTIC ORIGIN According to Corsini and Economidis (2007b), since the origin of Mediterranean ichthyofauna is prevalently Atlantic through its uninterrupted communication and exchanges via the Gibraltar Strait with this ocean, it is not appropriate to consider the newly recorded species originating from the Atlantic as true “aliens” for the Mediterranean. Some of them may be named vagrant or visitors, with rare or periodic appearance (Golani et al., 2002); others could be called new colonizers, their spread enhanced by changes in currents and temperature. Among the 30 and more Atlantic immigrants recorded in the Mediterranean, three species have been recorded in Greek waters, Sphoeroides pachygaster, Enchelycore anatina and Seriola fasciata, while the consideration of the deep water Gaidropsarus granti as a new colonizer continues to be questionable (Golani et al., 2002; Corsini-Foka and Economidis, 2007b; Pais et al., 2008) (Table 1). S. pachygaster is well established in all the Mediterranean (Golani et al., 2002, 2006b). In Greek waters it was first recorded from the SE Aegean Sea by Zachariou-Mamalinga and Corsini (1994) and since then its population has evolved and established in the area, resulting in frequent records so far (Rhodes, Symi, Karpathos: Author, pers. comm.). It has been recorded furthermore in the South Aegean (Peristeraki et al., 2006; Peloponnese, 2008, Author, unpublished data) and in the Central Aegean and Ionian Sea as well (Zenetos et al., 2007). Being distributed also along the NE Aegean coasts of Greece (Lesvos, 2007, Author, unpublished data) and Turkey (Eryilmaz et al., 2003), it may be concluded that this tetraodontid has successfully colonized all of the Aegean Sea, particularly in recent years. Although the species is generally considered a recent immigrant of Atlan-

222 Maria Corsini-Foka

Table 1. List of allochthonous and vagrant fishes in Greek seas. ES: Establishment, E: Established, C: Casual, Q: Questionable, FR: Area of first record, ST: Subtropical; T: Tropical Species Atlantic origin Sphoeroides pachygaster (Müller and Troschel, 1848) Gaidropsarus granti (Regan, 1903) Enchelycore anatina (Lowe, 1839) Seriola fasciata (Bloch, 1793) Aquaculture introduced Liza haematocheila (Mugil soiuy) Basilewsky, 1855 Indo-Pacific origin Siganus rivulatus Forsskål, 1775 Hemiramphus far (Forsskål, 1775) Stephanolepis diaspros Fraser-Brunner, 1940 Upeneus moluccensis (Bleeker, 1855) Sargocentron rubrum (Forsskål, 1775) Leiognathus klunzingeri (Steindachner, 1898) Parexocoetus mento (Valenciennes, 1847) Lagocephalus spadiceus (Richardson, 1845) Alepes djedaba (Forsskål, 1775) Siganus luridus (Rüppell, 1828) Saurida undosquamis (Richardson, 1848)

Family

ES FR

First published record

Tetraodontidae

E Rhodes

ST

Gadidae

Q Rhodes

Muraenidae

C Elafonissos Island C Rhodes

Zachariou-Mamalinga and Corsini, 1994 Zachariou-Mamalinga, 1999 See Golani et al., 2002 Corsini et al., 2006

Mugilidae

E Thracian Sea

Koutrakis and Economidis, 2000

TE

Siganidae

E Rhodes

ST

Hemiramphidae

E Rhodes

Monacanthidae

E Rhodes

Mullidae

E Rhodes

Holocentridae

E Rhodes

Brunelli and Bini, 1934 Tortonese, 1946, 1947a, b Tortonese, 1946, 1947a, b Serbetis, 1947; Laskaridis, 1948a Laskaridis, 1948b

Leiognathidae

E Rhodes

Kosswig, 1950

T

Exocoetidae

E Rhodes

Kosswig, 1950

T

Tetraodontidae

E Samos

Ananiadis, 1952

ST

Carangidae

Bini, 1960

ST

Siganidae

C Aegean Sea E Tilos

Kavalakis, 1968

ST

Synodontidae

E Naxos

Ondrias, 1971

ST

Carangidae

Climate*

T ST ST

ST T ST ST

Current status of alien fishes in Greek seas 223

Species

Family

Atherinomorus lacunosus (Forster, 1801) Pempheris vanicolensis Cuvier, 1831

Atherinidae

Fistulariidae

First published Clirecord mate* C Rhodes Quignard and Pras, ST 1986 E Kastellori- Papaconstantinou T zon and Caragitsou, 1987 E Symi Corsini and Econo- ST midis, 1999 E Rhodes Corsini and Econo- ST midis, 1999 E Rhodes Corsini et al., 2002 T

Pteragogus pelycus Randall, 1981 Sphyraena chrysotaenia Klunzinger, 1884 Fistularia commersonii (Rüppell, 1838) Apogon pharaonis Bellotti, 1874 Tylerius spinosissimus (Regan, 1908) Upeneus pori Ben-Tuvia and Golani, 1989 Callionymus filamentosus Valenciennes, 1837 Sphyraena flavicauda Rüppell, 1838 Etrumeus teres De Kay, 1842

Labridae

Apogonidae

E Rhodes

Corsini et al., 2004

T

Tetraodontidae

C Rhodes

Corsini et al., 2005

T

Mullidae

E Rhodes

Corsini et al., 2005

ST

Callionymidae

E Rhodes

Corsini et al., 2005

ST

Sphyraenidae

E Rhodes

Corsini et al., 2005

T

Clupeidae

E Rhodes, Cyclades

Tetraodontidae

E Rhodes

Corsini et al., 2005; ST Kallianiotis and Lekkas, 2005 Corsini et al., 2005 T, ST

Lagocephalus suezensis Clark and Gohar, 1853 Petroscirtes ancylodon Rüppell, 1835 Tylosurus crocodilus (Péron and Lesueur, 1821) Iniistius pavo (Valenciennes, 1840) Lagocephalus sceleratus (Gmelin, 1789) Torquigener flavimaculosus Hardy and Randall, 1983 Scomberomorus commerson (Lacepède, 1800)

Blennidae

E Rhodes

Corsini et al., 2005

Belonidae

Q Chalkidiki Sinis, 2005

T

Labridae

C Rhodes

Corsini et al., 2006

T

Tetraodontidae

E Rhodes

Corsini et al., 2006

T

Tetraodontidae

E Rhodes

Corsini-Foka et al., 2006

T

Scombridae

C Rhodes

Corsini-Foka and Kalogirou, 2008

T

Pempheridae

Sphyraenidae

* Based on Froese and Pauly (2008)

ES FR

T

224 Maria Corsini-Foka

tic origin, Psomadakis et al. (2007), after reviewing all available data, did not exclude the possibility of Lessepsian migration of the smooth puffer, which has a worldwide geographical distribution (Golani et al., 2002; Froese and Pauly, 2008), or even a more ancient unrecorded presence in the Mediterranean. The occurrence of both Enchelycore anatina and Seriola fasciata in Greek waters is based only on single records. E. anatina has been reported from Elafonissos (Peloponnesus coasts), accompanied by only other two local records along the Mediterranean coasts, in Israel and South Turkey (Golani et al., 2002, 2006b; Yokes et al., 2002). According to Corsini-Foka and Economidis (2007a, b), the spread of this species could be explained by passive dissemination of the leptocephali larvae and/or via transport in ship ballast. Concerning S. fasciata, a single young specimen has been reported from Rhodes (Corsini et al., 2006). This species is considered to be an Atlantic immigrant (Golani et al., 2002), with a wide western Mediterranean distribution, from the Balearic Islands to Malta and Tunisia (Bradai et al., 2004; Andaloro et al., 2005). The significant biomass it has achieved in the last years in this area leads Andaloro et al. (2005) to suppose that it may be not a recent colonizer. Since the local record of the Lesser Amberjack in Rhodes waters in 2004, so far from its actual known geographical distribution area, was not followed by other records in the eastern Mediterranean, as was the case with S. pachygaster, it may be considered a casual finding so far. HUMAN INTRODUCED SPECIES The only one confirmed record of non native fish species introduced by human activities in Greek waters is the Indo-Pacific Grey Mullet Liza haematocheila (Mugil soiuy). This species was introduced by humans for aquaculture in the Sea of Azov and the Black Sea (Golani et al., 2002) and after the collapse of fish farms (Starushenko and Kazansky, 1996) entered the Turkish Aegean Sea (Gulf of Smyrna: Kaya et al., 1998) and the Thracian Sea (Koutrakis and Economidis, 2000) (see also Harrison, 2004) (Table 1). Actually, it forms fished populations in various Thracian and Macedonia lagoons and appears frequently in the fish markets of North Greece (Minos et al., 2007, and in this volume). As discussed in Corsini-Foka and Economidis (2007b), other species, suspected to have been introduced in the wild by humans due to aquaculture activities, have been reported in the Greek estuaries, based on pictured and/or preserved specimen, but information has not been yet published. LESSEPSIAN IMMIGRANTS The movement of various marine organisms from the Red Sea to the Mediterranean via the Suez Canal was named by Por (1969) “Lessepsian migration”, also called today “Erythrean

Current status of alien fishes in Greek seas 225

migration”. According to Galil and Zenetos (2002), the Eastern Mediterranean, open to the Atlantic, Pontic and Erythrean biota, is particularly prone to invasions. Concerning fish, the Lessepsian species in the Mediterranean are real alien species because they belong to another ecological status (thermophilous) (see Galil, 2006) and to a different biogeographical zone (Indo-Pacific), and the Mediterranean is out of their native distribution. Establishment in Greek waters: the Dodecanese “refuge” The Lessepsian fish migrants in the Mediterranean are two cartilaginous fish species and more than 65 bony fish species as of this publication (Golani et al., 2002, 2004, 2006b; Gokoglu et al., 2003; Corsini et al., 2005; Akyol et al., 2005; Golani and Sonin, 2006; Corsini et al., 2006; Bilecenoglu and Kaya, 2006; Çinar et al., 2006; Golani, 2006; Erylmaz and Dalyan, 2006; Galil, 2006; Golani and Sonin, 2006; Ben Souissi et al., 2007; Lipej et al., 2008; Golani et al., 2008), while the Atlantic or Indo-Pacific origin of the alien fish Zenopsis conchifera, recently recorded in Tunisian waters, is to be evaluated, according to Ragonese and Giusto (2007). Upon arrival into the Mediterranean Sea through the Suez Canal, these species move either westward to the African coasts or, more frequently, eastward first and then northward, following mainly the Asiatic continental shelf. It has been suggested that they establish, fast or slow, dense or scarce populations, in the Eastern Mediterranean where they may influence or even modify the composition, structure and function of the local marine ecosystems (Goren and Galil, 2005). Further colonization of the Mediterranean mainly follows the Asia Minor Mediterranean coasts. Distribution then extends up to the water masses around the Dodecanese Islands, considered to be the most important gates for entering and establishing in the Aegean Sea and the main pathway of further westward spreading (Pancucci-Papadopoulou et al., 2005a, b; Corsini-Foka and Economidis, 2007a, b; Zenetos et al., 2007). According to Masseti (2002), “due to their geographical location, most of the islands of the Dodecanese fall within the biogeographical and paleogeographical range of Anatolia, to which they were joined by land-bridges at various different times during the Pleistocene glacial episodes”. The coastal zone of the marine area especially around Rhodes is characterized by a sub-tropical open-sea environment and is influenced essentially by the neighboring Levantine basin, since the island is hugged by the warm Asia Minor current through the strait of Rhodes in the north and the straits of Kassos and Karpathos in the south (Pancucci-Papadopoulou et al., 1999). Salinity at Rhodes coastal areas ranges from 39.1‰ at the surface to 39.2‰ at 50 m during winter, while it ranges from 39.3‰ at the surface to 39‰ at 50m in the summer (Kondoyannis et al., 2005). Temperature measurements obtained in the last decade during the stratified and the mixed period at the NE coast of Rhodes Island showed that the average temperature during the year at all depths considered ranged from 16.35 oC to 28.1 oC, while it was from 20.6 oC to 28.1 oC during the stratified period and from 16.4 oC to 20.9 oC during the mixed period, in the first 20m

226 Maria Corsini-Foka

layer (Table 2) (Fig. 2). It should be noted that measurements carried out in September 2007 gave a different profile of the temperature as compared with previous years, showing the presence of the thermocline at 35-60 m of depth, significantly deeper than that usually observed at 25-35 m of depth. This apparent warming revealed a temperature of about 25 o C at 50m of depth (Fig. 2) and was probably a consequence of the three extremely hot and prolonged periods observed repeatedly during summer 2007. A deeper formation of the thermocline was also observed in September 2008, after a long, uninterrupted and windless warm period. Due to these characteristics which are similar to those of the rest of the eastern Mediterranean coasts (Mavruk and Avsar, 2007), the Dodecanese continental shelf was classified long ago as part of the biogeographic “Lessepsian province” of the Mediterranean (Por, 1990), since it offers suitable environmental conditions for the establishment of thermophilous organisms, including tropical or sub-tropical Indo-Pacific species. The evolution of the Eastern Mediterranean Transient (EMT) (Theocharis and Lascaratos, 2000; Galil and Kevrekidis, 2002) and other factors, mainly vacant niches and the Mediterranean warming as discussed in Bianchi and Morri (2003) and Bianchi (2007) and the Aegean Sea warming as described in Theocharis (2008) and Raitsos et al. (2008) provide favorable conditions for the maintenance and spread of Erythrean migrant species and may explain the increase of Red Sea exotic species being recorded there (Elnais, 2008). As mentioned above (Pancucci-Papadopoulou et al., 2005a, b) the majority of nonindigenous species listed from Hellenic waters have been recorded in the south-eastern Aegean Sea, particularly in Rhodes and along the other Dodecanese Islands’ continental shelf, where about 90% of the alien biota is of Indo-Pacific origin, particularly for fishes. The number of Lessepsian immigrant fishes species having entered Greek waters is 29, where Tylosurus crocodilus could be considered questionable. As noted in Corsini-Foka

All depths and periods

Table 2. Temperatures from a station along the NE coasts of Rhodes Island (1996-2007) (Data: “Mediterranean Pollution Program-Monitoring of the coastal water quality of Rhodes Island” and Hydrobiological Station of Rhodes Archive). Avg: Average, SD: Standard deviation, Min: Minimum, Max: Maximum

Stratified period

0-20 0-40 2 m 20 m m m Avg 21.04 25.45 23.75 25.27 24.73 SD 3.18 2.04 2.94 2.15 2.43 Min 16.35 20.61 17.24 21.80 20.62 Max 28,09 28.09 28.09 28.05 27.86

Mixed period

40 m

0-20 0-40 2 m 20 m m m 19.90 19.93 19.95 19.80 19.73 2.75 1.32 1.30 1.58 1.61 17.24 16.48 16.47 16.62 16.49 26.49 20.87 20.87 20.87 20.85

40 m 19.65 1.58 16.47 20.74

Current status of alien fishes in Greek seas 227

Rhodes 26 23 21 N 28 16 12 E 15

16

17

18

Temperature (Deg. C) 19

20

21

22

23

24

25

26

27

28

29

0 10 20 30

Depth (m)

40 50 60 70 80 90 100

11/08/96 26/08/97 27/08/98 28/08/01 06/09/07 27/07/99 10/06/04 08/10/04 12/07/05 28/11/96 02/12/98 01/12/99 05/12/00 04/12/01 25/02/05

110 120

Fig. 2. Temperature profiles obtained with a CTD at a station located at the NE coasts of Rhodes Island.

and Economidis (2007b), the first record for the Mediterranean of Tylosurus crocodilus in Chalkidiki Peninsula is based on a single dead fish found in Gerakini beach (Sinis, 2005). Further investigation is needed concerning the status of the specimen. Lessepsian fish species belong to 21 families, seven of which are new to the Hellenic ichthyofauna, namely Siganidae, Hemiramphidae, Fistulariidae, Holocentridae, Leiognathidae, Pempheridae and Monacanthidae; other aliens increased the species number of 14 families that were already represented (Economidis, 1973; Bauchot, 1987; Papaconstantinou, 1988; Whitehead et al., 1984-1986) (Table 1). As observed in Corsini-Foka and Economidis (2007b), Tetraodontidae deserves particular attention. Until 1994 only the autochthonous Lagocephalus lagocephalus, the Lessepsian Lagocephalus spadiceus and the allochthonous Sphoeroides pachygaster from the Atlantic were known in the area. A rapid increase of records in the last years added four more tetraodontid species, all of Indo-Pacific origin: Tylerius spinosissimus, Lagocephalus suezensis, Lagocephalus sceleratus and Torquigener flavimaculosus (Table 1). According to Vacchi et al. (2007), including Ephippion guttiferum, Sphoeroides marmoratus and Sphoeroides spengleri, this family is actually represented by ten species in the Mediterranean Sea.

228 Maria Corsini-Foka

Until 1990 the number of Lessepsian fish in Hellenic waters amounted to thirteen species. An evident increase of records has been observed in the last decade with the addition of 16 other such species (see Table 1). It is interesting to note that among the first thirteen immigrants in Greek waters, 9 were subtropical and 4 were tropical species, while among the last sixteen immigrants, 5 were subtropical and 11 tropical species (Table 1). The lastest record of a Lessepsian fish in Hellenic waters was the narrow-barred Spanish mackerel Scomberomorus commerson (Corsini-Foka and Kalogirou, 2008). Another three Erythrean fish species have been observed in the Turkish waters of the south-eastern corner of the Aegean Sea, Liza carinata (by Zaitsev and Öztürk, 2001) and, more recently, Oxyurichthys petersi in Gökova Bay (Akyol et al., 2006) and Sillago sihama in Datça peninsula (Bilecenoglu, 2004), but not yet detected in Greek waters. The two species Leiognathus klunzingeri and Alepes djedaba, reported in the past from Greek waters (Table 1), are regularly caught in Turkish waters, along the Anatolian coasts of the SE Aegean Sea (Öğretmen et al., 2005; Oz et al., 2007). There is a direct relation between environmental conditions and the speed of spreading and adaptation of new settlers (Mavruk and Avsar, 2007). Several Erythrean fishes were reported in the Dodecanese almost simultaneously in the coasts of Israel, such as Siganus rivulatus, Upeneus moluccensis, Sargocentron rubrum, Pteragogus pelycus, Fistularia commersonii and Lagocephalus sceleratus, while in other cases, such as Sphyraena chrysotaenia, Apogon pharaonis, Etrumeus teres and others, their advance along the Anatolian coasts was gradual, the immigrants reaching this area only after a relatively long time (Golani et al., 2006b; Galil, 2006; see references in Table 1). The rate of spreading depends on biotic and/or abiotic factors, such as temperature regime, substrate, currents, extension of the continental shelf, thermal tolerance of the colonizing species, food availability, competition with indigenous species, local pathogens, extension of the spawning season, behaviour of the new species and their food habits and the availability of free niches already existing or created by overfishing of local species (Golani, 1998a; Mavruk and Avsar, 2007; Corsini-Foka and Economidis, 2007a, b). Consequently, once they reached the continental shelf of the Dodecanese islands, they usually did not advance any further. The increased number of records listed for the Hellenic waters beyond the Dodecanese continental shelf in recent years may be a first indication of a change in the previously known situation. On the other hand, many Lessepsian immigrants quite common in the Levant have not been recorded in the SE Aegean Sea, probably due to difficulties in overcoming one or more of the above factors. In comparison, along the Turkish territorial waters of the Aegean and East Mediterranean, 38 species of bony fishes of Red Sea origin have been recorded (Golani et al., 2006b; Bilecenoglu et al., 2002; Çinar et al., 2005, 2006; Bilecenoglu and Kaya, 2006; Akyol et al., 2006). With the exception of the local records of Iniistius pavo and Tylerius spinosissimus, considered as first records for the Mediterranean and discussed below, and of the questionable Tylosurus crocodilus, the remaining 26 species (Table 1) are also in Turkish waters. Several species already diffused along the Turkish coasts are highly expected to arrive at Aegean Hellenic waters, especially Dussumieria elopsoides,

Current status of alien fishes in Greek seas 229

Herklotsichthys punctatus, Pelates quadrilineatus, Cynoglossus sinusarabici, Liza carinata, Oxyurichthys petersi and Sillago sihama. A single specimen of Tylerius spinosissimus, was collected at deeper depths than usual for Lessepsian migrant fishes in the SE Aegean Sea, but lower than those used in its tropical habitat (Corsini et al., 2005), showing probably that new colonizers are able to occupy unexploited niches, as already discussed in Corsini-Foka and Economidis (2007b). Concerning the manner of invasion, its spreading may have followed unusual ways, as observed in the case of Tetrosomus gibbosus (by Spanier and Goren, 1988) but other vectors different from usual pathways (ship ballast, aquaculture or aquaria purposes transport) have to be evaluated, as observed in Greek waters for other taxa (Pancucci-Papadopoulou et al., 2005a, 2006; Elnais, 2008). The finding of the spiny pufferfish could indicate that a certain population of the species is already established in the eastern Mediterranean, but not detected or neglected being a fish of very small size. A similar discussion may be needed for the local single record of Iniistius pavo (Corsini et al., 2006), caught by hand-net in very shallow waters of Rhodes, not supported by other findings until now in the rest of the Mediterranean. Spreading of Lessepsian fishes in the Aegean Sea The Aegean Sea, due to the complexity and variety of morphological features, bathymetry, hydrological and hydrodynamic features (Papathanassiou and Zenetos, 2005), offers a unique opportunity for monitoring the spreading of tropical colonizer fishes in various environmental conditions. As mentioned above, Lessepsian migrant species, once having reached the SE Aegean Sea, Dodecanese and/or Asia Minor continental shelf, generally reveal difficulties spreading to the rest of the Aegean Sea, especially in the north, or continuing their expansion westward and southward, as observed by Papaconstantinou (1990). According to Mavruk and Avsar (2007), concerning Red Sea fishes, “an important factor that influences establishment in a new ecosystem is their adaptation ability”. Many of the successful migrants are eurytherm and euryaline, which may explain those species spreading from the SE Aegean coasts and overcoming environmental and/or biological impediments. Looking at the 31 Erythrean fishes which have reached the southeastern Aegean coasts of Turkey and Greece so far (Table 3), most have already been established in the Levantine waters west and northeast of the Suez Canal (Golani et al., 2006a, b), fourteen have enlarged their distribution toward the central Aegean Sea: ten of these species expanded their populations northward along the eastern coasts and also westward into the central Aegean, while the distribution of Atherinomorus lacunosus, Lagocephalus spadiceus, Sargocentron rubrum and Scomberomorus commerson seems to remain restricted to the eastern coasts of the central Aegean, until today (Table 3). The Cretan continental shelf is located in the south Aegean Sea in a rather warm water zone, consequently one would expect that Lessepsian immigrants would settle

NA SEA Cr CA I AD Li Tu CMED SSi/ TY Sp References* /Ma StSi *See References in Table 1 +? + + + + + + + + + + *; Tingilis et al., 2003 ; Karachlè et al., 2004; Azzurro et al., 2004 ; Ben Souissi et al., 2004; Çinar et al., 2005; Micarelli et al., 2006; Milazzo et al., 2006; Golani et al., 2006b; Golani et al., 2007; Kalogirou et al., 2007; Oz et al., 2007 ; Pais et al., 2007; Corsini-Foka and Economidis, 2007b; Sciberras and Schembri, 2007; Shakman and Kinzelbach, 2007; Zenetos at al., 2007; Psomadakis et al., 2008 ; Sánchez-Tocino et al., 2008 ; Dulčić et al., 2008; Present work. Stephanolepis + + + + + + + + + + *; Economidis and Bauchot, 1976; Catalano and Zava, 1993; Zaitsev and diaspros Öztürk, 2001; Golani et al., 2002, 2006b; Dulčić et al., 2003; Çinar et al., 2005; Öğretmen et al., 2005; Bradai et al., 2004; Öziç and Yilmaz, 2006 ; Oz et al., 2007; Shakman and Kinzelbach, 2007; Corsini-Foka and Economidis, 2007b; Sciberras and Schembri, 2007; Present work. Siganus luridus + + + + + + + + + *; Ondrias, 1971; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; Azzurro and Andaloro, 2004; Bradai et al., 2004; Castriota and Andaloro, 2005; Öğretmen et al., 2005; Corsini-Foka and Economidis, 2007b; Oz et al., 2007; Sciberras and Schembri, 2007; Shakman and Kinzelbach, 2007; Present work. Siganus + + + + + + + + *; Geldiay, 1969; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; rivulatus Tigilis et al., 2003; Dulčić et al., 2003; Bradai et al., 2004; Çinar et al., 2005; Öğretmen et al., 2005; Peristeraki et al., 2006; Oz et al., 2007; Sciberras and Schembri, 2007; Shakman and Kinzelbach, 2007; CorsiniFoka and Economidis, 2007b; Present work. Sphyraena + + + + + *; Lanfranco, 1993; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; chrysotaenia Dulčić et al., 2003; Çinar et al., 2005; Öğretmen et al., 2005; Shakman and Kinzelbach, 2007; Sciberras and Schembri, 2007; Rim et al., 2007; Corsini-Foka and Economidis, 2007b; Present work. Alepes djedaba + + + *; Zaitsev and Öztürk, 2001; Golani et al., 2002; Oz et al., 2007; Shakman and Kinzelbach, 2007; Sciberras and Schembri, 2007.

Indo-Pacific Species Fistularia commersonii

Table 3. Lessepsian fish species reported from the South Eastern Aegean coasts and their distribution in other regions northward and westward. SEA: South-eastern Aegean Sea, Cr: Crete, CA: Central Aegean Sea; NA: North Aegean Sea, I: Ionian Sea, AD: Adriatic Sea, Li: Libyan coasts, Tu: Tunisian coasts, CMED/Ma: Central Mediterranean Sea/Malta, SSi/StSi: South Sicily/Strait of Sicily, TY: Tyrrhenian Sea, Sp: Spain coasts.

230 Maria Corsini-Foka

+

Sphyraena flavicauda

+

+

Hemiramphus far

+

+

+

+

+

+

+

Sargocentron rubrum

+

+

+

+

Saurida undosquamis

+

+

+

+

+

+

+

Scomberomorus commerson

+

+

+

+

+

+

+

+

+

`

Pempheris vanicolensis

+

+

+

+

+

+

+

Upeneus pori

?

Leiognathus klunzingeri Parexocoetus mento Atherinomorus lacunosus

Etrumeus teres

+

+

+

+

+

+?

+

*; Falautano et al., 2006; Kasapidis et al., 2007a; Zenetos et al., 2007; Corsini-Foka and Economidis, 2007b; Present work. *; Papaconstantinou, 1988, 1990; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; Dulčić et al., 2003 ; Galil, 2006. *; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; Dulčić et al., 2003; Bradai et al., 2004. *; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; Corsini-Foka, 2004, pers. comm.; Ben Souissi et al., 2006a; Shakman and Kinzelbach, 2007. *; Zaitsev and Öztürk, 2001; Tingilis et al., 2003; Bradai et al., 2004; Shakman and Kinzelbach, 2007; Corsini-Foka and Economidis, 2007b; Present work. *; Ben Souissi et al., 2005b; Öğretmen et al., 2005; Akyol et al., 2006; Shakman and Kinzelbach, 2007; Corsini-Foka and Economidis, 2007b; Present work. *; Buhan et al., 1997; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; Öğretmen et al., 2005; Çinar et al., 2005  ; Ben Souissi et al., 2006b; Oz et al., 2007; Shakman and Kinzelbach, 2007. *; Ondrias, 1971; Tsimenidis et al., 1991; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; Dulčić et al., 2003; Öğretmen et al., 2005 ; Öziç and Yilmaz, 2006; Oz et al., 2007; Shakman and Kinzelbach, 2007; Corsini-Foka and Economidis, 2007b. *; Zaitsev and Öztürk, 2001; Golani et al., 2002, 2006b; Crete, Tingilis, 2003, pers. comm.; Çinar et al., 2005; Oz et al., 2007; Öziç and Yilmaz, 2006; Zenetos et al., 2007; Corsini-Foka and Economidis, 2007b; Present work. *; Torcu and Mater, 2000; Golani et al., 2002, 2006b; Shakman and Kinzelbach, 2007; Dulčić et al., 2003; Corsini-Foka and Economidis, 2007b; Present work. *; Shakman and Kinzelbach, 2007. Current status of alien fishes in Greek seas 231

Lagocephalus spadiceus Pteragogus pelycus Apogon pharaonis Tylerius spinosissimus Callionymus filamentosus Lagocephalus suezensis Petroscirtes ancylodon Iniistius pavo Torquigener flavimaculosus Sillago sihama Oxyurichthys petersi

Lagocephalus sceleratus

Liza carinata

Indo-Pacific Species Upeneus moluccensis

*; Corsini-Foka and Economidis, 2007b; Present work. * *; Bilecenoglou et al., 2002; Çinar et al., 2005; present work. *; present work. * * Bilecenoglu, 2004. Akyol et al., 2006.

+

+

+

+

+ +

+ +

NA SEA Cr CA I AD Li Tu CMED SSi/ TY Sp References* /Ma StSi *See References in Table 1 + + + + + *; Kaspiris, 1976; Kaya et al., 1999; Zaitsev and Öztürk, 2001; Torcu and Mater, 2000; Golani et al., 2002, 2006b; Öziç and Yilmaz, 2006; Peristeraki et al., 2006; Zenetos et al., 2007; Oz et al., 2007; Corsini-Foka and Economidis, 2007b; Present work. + + + Zaitsev and Öztürk, 2001; Shakman and Kinzelbach, 2007. L. carinata is not listed for the Aegean Sea in Çinar et al., 2005. + + + + *; Akyol et al., 2005; Bilecenoglu et al., 2006; Kasapidis et al., 2007b; Koutsoubas et al., 2007; Corsini-Foka and Economidis, 2007b; Peristeraki, 2007; Corsini-Foka, 2007; Zenetos et al., 2007; Elnais, 2008  ; Present work. + + *; Zaitsev and Öztürk, 2001; Çinar et al., 2005; Corsini-Foka and Economidis, 2007b; Present work. + + *; Oz et al., 2007; Crete, 2005, Sterioti, pers. comm.; Öğretmen et al., 2005. + *; Golani et al., 2006b; Oz et al., 2007.

232 Maria Corsini-Foka

Current status of alien fishes in Greek seas 233

more easily in the coastal waters of this island. However, unfavorable factors seemed to have prevented their large scale settlement there, since only eleven fish species have been recorded, two prior to 2002, Stephanolepis diaspros and Saurida undosquamis, and another nine in the last five years: Siganus luridus, Fistularia commersonii, Siganus rivulatus, Pempheris vanicolensis, Lagocephalus sceleratus, Etrumeus teres, Sargocentron rubrum, Pteragogus pelycus and Upeneus moluccensis (Table 3), a number rather low when compared to that in the SE Aegean waters. This rather slow process of colonization may be due to the deep waters which surround the continental shelf of Crete (Corsini and Economidis, 2007b). Even if recent increased scientific interest is considered, the number of records of Red Sea fish species concentrated along the coasts of Crete in the last few years, accompanied by the population establishment of some of them (Peristeraki et al., 2006), may suggest that some environmental factors have favoured their spreading there. The colonization of the north Aegean Sea, defined as the sea north of a line connecting the south Eubia Island in the west and the Menderes region in Asia Minor (approximately Izmir) in the east (Papaconstantinou, 1990; Sakellariou and Alexandri, 2007), appears to be a very difficult challenge. Only three of the Lessepsian migrant fishes (listed in Table 3) have been recorded there: Liza carinata along the Turkish northeastern Aegean coasts and, very recently, Fistularia commersonii and Lagocephalus sceleratus. After recent verifications, the presence of the species Siganus luridus, Siganus rivulatus, Saurida undosquamis and Upeneus moluccensis in the north Aegean Sea has been excluded, contrary to previous work (see Corsini-Foka and Economidis, 2007b), their distribution reaching the limits between these two regions of the Aegean, according to the definition given above. Concerning Lejognathus klunzingeri, probably some misunderstanding has occurred concerning its distribution in all of the north Aegean Sea (see Golani et al., 2006b): Papaconstantinou and Tortonese (1980) assessed that “immigrants from the Red Sea have not reached Thermaikos Gulf till now” and Papaconstantinou (1990) did not report this Lessepsian species in the north Aegean. The occurrence of Sphyraena chrysotaenia could also be expected in the northern Aegean Sea, since the yellowstrip barracuda has been sighted within the offshore zone of the south-western Crimea (Boltachev and Yurakhno, 2002). The Blue Cornetfish occurs in the northeastern Aegean Sea (see Golani et al., 2007b), while the record of Fistularia commersonii in the northwestern Aegean Sea is based, until today, on an adult specimen collected at Chalkidiki peninsula during the summer of 2003 (Karachlé et al., 2004). Since then no indications concerning the occurrence of the blue cornetfish in that area have been collected, consequently the above finding may be considered as part of an incursion probably due to favorable currents and warm surface waters of the summer. The quick expansion of the invader Lagocephalus sceleratus in the southeastern, south and central Aegean Sea in all seasons (Table 3), combined with its occurrence along the north-eastern Aegean coasts at Lesvos Island in February 2007 (Peristeraki, 2007) and March 2007 (Koutsouba et al., 2007) and also summer 2008 (Author, pers. knowledge), shows that this tropical species was able to adapt and occupy in an exceptionally

234 Maria Corsini-Foka

reduced time all the Aegean coastal waters between the isotherm of 16.25o C and 15o C and to enter also a part of the region limited by the isotherm of 14o C (see Bianchi, 2007). The species has been in fact sighted along the northwestern Aegean coasts in the area of Kavala in September 2007 (Peristeraki, 2007). Probably, and perhaps similarly to F. commersonii, it was able to explore that area of the Aegean under favorable summer conditions (Fig. 1b). One of the factors which could be associated with the population explosion of L. sceleratus during summer 2007 may be the exceptionally high temperature events observed in that period throughout Greece and the consequent creation of unusually deeper warm water niches, similarly to those observed for Rhodes Island (Fig. 2). Migration to deeper niches with warmer waters may also be considered for possible establishment of immigrants in various Mediterranean areas, as assessed by Mavruk and Avsar (2007). Taking into account that the L. sceleratus invasion is very recent, further information is needed to ascertain that the elongated puffer has successfully colonized also the coldest part of the northwestern Aegean Sea. Each alien species, on the other hand, responds to new environmental conditions in different ways and times, according to its biological characteristics and capacity of adaptation. A sudden accidental decrease of water temperature from 20o C to the environmental winter temperature of 12o C in a closed system tank of 100 liters at Rhodes Aquarium, caused the death of two juvenile L. sceleratus specimens, while three juvenile S. diaspros and an adult A. pharaonis in the same aquarium, were able to survive. A similar negative effect of a decrease of water temperature from 20o C to 12o C was observed in the past regarding the survival of Pteragogus pelycus in an aquarium (Corsini and Stamatellos, 1998). Although sudden changes of physical parameters in captivity conditions do not usually occur in nature, these observations may suggest that winter water temperatures around 12 oC may constitute a fatal minimum limit for survival of some Erythrean species also in the natural environment. Lessepsian fishes in SE Aegean Sea and their occurrence westward in the Mediterranean: affinities and difference in distribution Regarding the 31 Erythrean fishes occurring in the SE Aegean coasts of Turkey and Greece (Table 3), it can be observed that three of these species have succeeded in crossing the Strait of Sicily, namely Fistularia commersonii, Siganus luridus and Stephanolepis diaspros; the first, a recent Lessepsian pioneer reaching the Iberian Peninsula (Sánchez-Tocino et al., 2007) and the Western Ligurian Sea (Garibaldi and Orsi Relini, 2008; Occhipinti-Ambrogi and Galil, 2008), as discussed below. Ten of these species occur also along the Tunisian coasts, where also Hyporhamphus affinis was recently recorded (Kinzelbach, 2007), and seven in the Central Mediterranean. Among the Erythrean fishes present in the SE Aegean coasts, as many as 17 species are also along the Libyan coasts, where other Indo-Pacific species are also present, such as Herklotsichthys punctatus and Crenidens crenidens (see Golani et al., 2002, 2006b; Shakman and Kinzelbach, 2007). Furthermore, six of these species

Current status of alien fishes in Greek seas 235

have been recorded in the Greek part of the Ionian Sea and already eight are colonizing the coasts of the Adriatic Sea, where also another three Indo-Pacific species have been recorded, namely, Epinephelus coioides (by Parenti and Bressi, 2001), Pampus argenteus (by Dulčić et al., 2004) and Terapon theraps (by Lipej et al., 2008) (Table 3). Concerning the remaining 12 species, their westward population expansion from the Levant seems today confined to the Aegean Sea, in particular to its southeastern waters. Habitat Most Erythrean alien invertebrates occupy the Mediterranean littoral and infralittoral zones to a depth of approximately 50 m, and are hardly found in deeper waters, according to Galil and Zenetos (2002). This is also true for the Lessepsian fish species, which are mainly coastal littoral species, dwelling in rather shallow sandy (Golani, 1993) and/ or muddy habitats, often covered by sea-grass, while their presence on rocky shores is more limited (Golani et al., 2007a). This has been observed also in Rhodes and other Dodecanese coastal areas, where the majority of Erythrean fish are collected by trawlers and purse seine, sometimes also by net and fishing lines, at depths up to 50 m. In some cases, they may be captured in deeper waters, such as Tylerius spinosissimus, caught at 80 m (Corsini et al., 2005) or Lagocephalus sceleratus, recently caught (Rhodes, February 2008) at 70-80 m (Author, unpublished data). Generally they dwell on sandy and/or sandy-muddy bottom, covered by well-developed Chlorophyceae beds (Caulerpa prolifera and Caulerpa racemosa) and Phanerogames prairies, mainly Posidonia oceanica and Halophila stipulacea (by Corsini and Economidis, 1999; Corsini et al., 2005, 2006; Kalogirou et al., 2007), as for example S. luridus, S. rivulatus, F. commersonii, L. sceleratus, L. suezensis, S. chrysotaenia, S. flavicauda, A. pharaonis, S. diaspros, P. pelycus, U. moluccensis, U. pori, S. rubrum. Schools of juvenile Shyraena chrysotaenia, juveniles and adults of F. commersonii (Fig. 3) and adults of L. sceleratus as well are encountered also on sandy-rocky bottom while schools of Pempheris vanicolensis inhabit caves in Rhodes, Symi and Kastellorizon. Abundance The abundance of some Lessepsian immigrant fishes has assumed economical importance in the south-eastern Levantine and Anatolian fisheries (Gücü et al., 1994; Torcu and Mater, 2000; Golani et al., 2002; Çicek and Asvar, 2003; Harmelin-Vivien et al., 2005). In the Levantine Basin, the Erythtrean invaders “comprise 50-90% of the fish biomass and have altered the native food web”, according to Goren and Galil (2005). Populations of Lessepsian fishes throughout the coastal waters of the Dodecanese continental shelf have established there a population large enough to be detectable (Cor-

236 Maria Corsini-Foka

Fig. 3. Fistularia commersonii in the wild (Rhodes) (Photo by Stefanos Kalogirou).

sini et al., 2005). Many of these species have been present in fishery catches since their first record in the region (Corsini-Foka et al., 2004), except for the single casual records of Tylerius spinosissimus and Iniistius pavo (see also Zenetos et al., 2005). Among the established species listed in Table 1, the majority are caught regularly in local fishery of Rhodes and adjacent islands, where Hemiramphus far, Upeneus moluccensis, Sargocentron rubrum and Apogon pharaonis are caught less than Stephanolepis diaspros and Pteragogus pelycus. Other species are encountered less frequently: the occurrence of Atherinomorus lacunosus in Rhodes was ascertained in 2004 (Author, unpublished data), Pempheris vanicolensis is difficult to be caught by usual local fishing methods, being a nocturnal species; Saurida undosquamis is caught but rarely; a large specimen of Lagocephalus spadiceus (TL 43 cm, weight 1.55 Kg) caught at 40 m of depth, has been reported from Cos in October 2007 as well as a smaller one (TL 18 cm) from Rhodes in August 2008, while other findings of the recently recorded Petroscirtes ancylodon, Callionymus filamentosus, Torquigener flavimaculosus and Scomberomorus commerson from Rhodes in summer 2008, confirm their quick establishment (Author, pers. knowledge). Other species are common; since their successful establishment long ago (Table 1), they have acquired stable commercial importance, i.e. Siganus luridus, S. rivulatus and Sphyraena chrysotaenia; the last being often confused with the two indigenous species S. sphyhraena and S. viridensis coexisting in the same coastal area and also with the new Erythrean colonizer S. flavicauda (Corsini and Economidis, 1999; Corsini et al., 2005; Corsini-Foka and Economidis, 2007a, b). The recent colonizer of Greek waters Etrumeus teres is already contributing to fishery in the Dodecanese (Fotaki, M., 2007, pers. comm.), in the Cyclades Islands (Kallianiotis and Lekkas, 2005) and in Crete (Kasapidis et al.,

Current status of alien fishes in Greek seas 237

2007a) as has been observed also in Israel, Cyprus and Turkey (Golani et al., 2002; Çicek and Avsar, 2003). Other alien fishes are abundant nowadays but without commercial importance and consequently discarded, such as Fistularia commersonii and the two recent invasive tetraodontids Lagocephalus suezensis and L. sceleratus, which pose danger for public health. Of the above species, Stephanolepis diaspros (Fig. 4), Sargocentron rubrum, Pteragogus pelycus, Apogon pharaonis, S. luridus and S. rivulatus are regularly present in the Aquarium of Rhodes exhibition, maintained with common sparids, labrids and serranids (see Corsini and Stamatellos, 1998), while also L. sceleratus of small and medium size (Fig. 5) and L. suezensis specimens are hosted in experimental tanks.

Fig. 4. Stephanolepis diaspros in the Aquarium of the Hydrobiological Station of Rhodes (Photo by Bruno Zava).

Fig. 5. Lagocephalus sceleratus in the Aquarium of the Hydrobiological Station of Rhodes.

238 Maria Corsini-Foka

Impact of recent invasions Local indigenous fishes, especially the small sized and fry, similar to invertebrates, cephalopods, crustaceans and algal vegetation, are prone to remarkable predation pressure by invaders. Furthermore several invaders and native species may be involved in competition. Consequently, the impact, both on ecosystem composition, structure and function and on the local exploited populations, by Lessepsian immigrants may be serious and increasing in some cases. Moreover, little information is known in the area about predation on alien invaders by native species or by aliens on aliens (Kalogirou et al., 2007). Warmer local niches, the lack of native predators, man included, and probably the absence of competitors, combined with reproductive success, food availability, body features and other favorable factors for successful establishment, may support population expansion or explosion of recent invaders such as Fistularia commersonii, Lagocephalus sceleratus and L. suezensis or of the earlier colonizer Upeneus moluccensis. An exceptional population explosion of this last species was observed in the area during the 1940’s (Laskaridis, 1948a), followed by a dramatic crash shortly thereafter, so that nowadays this species is rarely found in the area, as mentioned above. A deeper study of this matter is needed. Several Erythrean invaders may have found unexploited ecological niches without competing with local native species. For example, Siganus luridus and S. rivulatus became well established in the Levantine basin initially and then invaded the Central Mediterranean, aided by the absence of many herbivorous competitors and/or the existence of abundant available food (Lundberg and Golani, 1995; Goren and Galil, 2005; Galil, 2007). These two alien siganids are quite important in local Dodecanese fishery, where the herbivorous native Sparisoma cretensis is still abundant, while the occurrence of Sarpa salpa is apparently decreasing (unpublished data), as observed along the Lebanese coasts (Bariche et al., 2004). Schools of native and alien sphyraenids of similar size are also captured, as mentioned above, and recent studies indicate competition for food between the native S. viridensis and the alien S. chrysotaenia (unpublished data). Furthermore, Upeneus moluccensis is sometimes present but it does not seem to dominate Mullus barbatus, while the population of the new migrant U. pori seems to have gain in importance recently and may be occasionally confused with native or allochthonous confamilial species. Saurida undosquamis is very rare in Greek waters compared to the native confamilial Synodus saurus. Also, Apogon pharaonis is regularly caught in purse seine nets as well as its indigenous confamilial Apogon imberbis, while Pteragogus pelycus occurs with other labrid species of similar size (for example Symphodus spp., Coris julis, Thalassoma pavo), mainly on Posidonia beds. No local fish species has been recorded as disappeared in the Rhodes marine area, as assessed for the rest of the Eastern Mediterranean (Golani, 1998b), but monitoring of the situation and studies on changes in abundance of native species should be increased in this region.

Current status of alien fishes in Greek seas 239

In terms of impact, the recent invading Blue Cornetfish, Fistularia commersonii, caught since its first appearance in the Rhodes marine area in 2001, usually by trawlnets and purse seine from very shallow waters up to 50 m, has established an important population and it is considered one of the most successful invasive fish species in the Mediterranean Sea (Streftaris and Zenetos, 2006). This species presented not only a very fast expansion along the coasts of the Levantine basin and up to the north Aegean Sea and to the northern coasts of Crete, but also westward to the Central Mediterranean and Thyrrenian Sea, reaching the extremity of the Western Mediterranean coasts of Spain (Golani et al., 2006b; see references in Table 3). The phenomenon is alarming because this fish, despite the genetic bottleneck determined in its Mediterranean population (Golani et al., 2007b), reproduces and grows very rapidly, reaching a large size and showing a unique ability of adaptation that allowed it to invade all the Mediterranean in just a few years, crossing from the east to the west as well as four decreasing winter isotherms (Bianchi, 2007). Fistularia commersonii is subjected to a very low fishing pressure, as already observed (Corsini-Foka and Economidis, 2007a, b), while predation on its large specimens appears limited to the invaded coastal area, leaving it free to form large populations. It is an active piscivorous species with a clear aggressive behavior when in schools which may seriously affect native species economically and ecologically. The Blue Cornetfish feeds mainly on small fish, gobiids and several native fish, particularly Spicara smaris, Mullus spp. and Boops boops (Corsini et al., 2002; Kalogirou et al., 2007). Furthermore, the body features of F. commersonii, such as its dorsal-ventral flattened body and its tubular mouth, allow large sized specimens to reach very shallow waters and to suck young fishes and small decapods in large quantities. Among the most recent alien tetraodontids colonizers (Table 1), the population of the large sized invasive species Lagocephalus sceleratus, which should not be marketable because it may be a source of food poisoning, is increasing rapidly along the Levantine coasts, invading in just a few years almost all the South and Central Aegean coasts, even reaching the North Aegean Sea (Golani and Levy, 2005; Golani et al., 2006b; References in Tables 1 and 3). Today, along the coasts of Rhodes, Symi, Cos and Kalymnos, specimens of all sizes, from small to juvenile and adults reaching up to 70 cm in total length and 3.5-4 kg in weight, are caught regularly, sometimes in exceptional abundance, in the habitats described above. Based on preliminary studies in the area of Rhodes, the species shows an isometrical growth, as observed in New Caledonia (Kulbicki et al., 2005), while there are first indications that its spawning season is during the summer months (unpublished data). Adult specimens of L. sceleratus dwell near the bottom and feed mainly on cephalopods, such as Sepiidae, but also on crustaceans and benthic fishes as Synodontidae, while young specimens feed prevalently on small benthic invertebrates found searching food into the sand (Kalogirou, pers. comm.).Lagocephalus suezensis (Table 1), another recent invader of smaller size than the previous species, occurs in the area of Rhodes, sometimes in large quantity as already noted (Corsini-Foka and Economidis,

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2007b) and often caught together with L. sceleratus. Due to similarities and to the fact that its juvenile and adult sizes resemble the small and juvenile sizes of L. sceleratus, the two species may be confused in the nets. A survey carried out by purse seine in November 2007 along the SE coats of Rhodes, sandy bottom, 8-40 m of depth, described the extreme situation produced in some cases in local fishery by these new invaders. The same number of specimens of L. sceleratus and L. suezensis was counted, with similar total length (8-20 cm in both species) and weight (Table 4): the Lessespian fishes represented 43% in number and 38% in weight of the total catch (Fig. 6) (Kalogirou, pers. comm.) giving an image similar to situations common in the Eastern Mediterranean fishery (Mavruk and Avsar, 2007). On the other hand, during a survey carried out later in February 2008, by purse seine in a fishing ground adjacent to that in the previous study, the native species of economical value Boops boops, Spicara maena and S. smaris exceeded 90% in number and weight of the total catch (unpublished data), as observed previously (Kalogirou et al., 2007). It should be considered that, while the new incursor Fistularia commersonii is the only species of the family Fistulariidae to successfully be established due to its exceptional capacity of adaptation in the area (F. petimba occurs only at the western extremity of the Mediterranean), and consequently free from confamilial competition, the two new invasive demersal species, L. suezensis and L. sceleratus, belong to a family well represented in the Mediterranean by native and allochthonous species, as already mentioned. Consequently, Table 4. Results of a boat seine catch carried out on November 2007 at Haraki, SE coasts of Rhodes Island, sandy bottom (n: number of specimens). Species Lagocephalus sceleratus Lagocephalus suezensis Pagrus pagrus Bothus podas Trachinus draco Synodus saurus Stephanolepis diaspros Trigla lyra Mullus barbatus Fistularia commersonii Upeneus pori Scomber japonicus Xyrichthys novacula Rajidae Zeus faber Total

n 47 47 40 40 35 28 22 9 9 8 7 6 5 3 1 307

Weight (g) 1977.5 2300.2 631.6 1056.1 1048.7 1900.3 790.1 721.0 62.8 775.0 44.7 473.5 95.2 3500.0 46.4 15423.1

Current status of alien fishes in Greek seas 241

25 %n %W

20

%

15 10 5

Fistularia commersonii

Lagocephalus suezensis

Lagocephalus sceleratus

Rajidae

Mullus barbatus

Upeneus pori

Synodus saurus

Bothus podas

Stephanolepis diaspros

Scomber japonicus

Zeus faber

Trachinus draco

Xyrichthys novacula

Trigla lyra

Pagrus pagrus

0

Species

Fig. 6. Composition of a boat seine catch, at Haraki, SE coast of Rhodes Island, sandy bottom (November 2007) (% n: percentage in number, % W: percentage in weight).

it is reasonable to suppose the existence of possible competition, firstmost with other confamilial species. None of the previously recorded tetraodontids occurs or occurred in such large quantities in local fishery as these two last invaders (with the possible exception of the demersal S. pachygaster which is more frequent, but not as abundant since it is caught almost exclusively by fishing lines). Since L. lagocephalus is a pelagic species, L. spadiceus benthopelagic and S. pachygaster generally inhabits deeper waters, the two new invaders have occupied prevalently the shallow sandy shore of the region, a habitat free of both confamilial and interspecific competitors, probably free of predators as well (Table 4) and, for the moment, with abundant food for sustaining the growth of both invaders at similar size. CONCLUSIONS Although only one allochthonous species, Liza haematocheila, has been introduced in Greek waters by uncareful release or escape from aquaculture installations, according to Corsini-Foka and Economidis (2007a, b) there are indications that the number of alien species introduced in the wild through aquaculture activities may contribute in the future

242 Maria Corsini-Foka

to the increase of the xenodiversity (Leppäkoski and Olenin, 2000) in Greek waters, mainly estuarine. Precautions and stricter control must be applied to prevent their escape from fish farms in the future in order to avoid their establishment in nature. The number of colonizer fishes of Atlantic origin occurring in Greek waters is limited to four species, of which Gaidropsarus granti is questionable. The only one well established is the tetraodontid Sphoeroides pachygaster, which hase expanded in recent years its distribution area from the SE Aegean waters to of all the Aegean Sea and is one of the 100 most successful invasive species in the Mediterranean, potentially threatening biodiversity and affecting the socio-economic value of the area by impact on fishery and public health (Streftaris and Zenetos, 2006). Allochthonous fishes of Indo-Pacific origin in Greek waters number 29 species, more than half of them recorded in the last decade. The majority of these invaders are well established; half of them are included in the list of the 100 most successful alien species of the Mediterranean, all possibly threatening biodiversity, while one species, the tetraodontid L. sceleratus, affects also human health (Zenetos et al., 2005; Streftaris and Zenetos, 2006). Based on more recent knowledge, the alien invasive species F. commersonii, L. sceleratus and L. suezensis may have a serious negative socio-economic effect on the area: they have no commercial value and their large populations are mainly sustained by intensive feeding on native fish and invertebrate stocks, locally exploited and economically important in fisheries. Furthermore, small sized specimens of the last two species, the elongated and the Suez puffers, are frequently caught in large quantities together with marketable species of similar size, in particular Spicara smaris and Boops boops, depending on season and fishing area. Consequently, since the pufferfishes are rejected due to their toxicity, a negative economic effect is also greatly increased for the effort required to clean fishing gear (see Streftaris and Zenetos, 2006). Siganus luridus and S. rivulatus have achieved commercial importance since the time of their appearance and establishment, but there is indication that the population of the native herbivorous Sarpa salpa is decreasing. Schools of Sphyraena chrysotaenia and, less frequently, S. flavicauda, are caught with the native S. viridensis and S. sphyraena of similar size, and unpublished data indicate possible competition for food between native and alien confamilial species. The recent colonizer Etrumeus teres already contributed to fishery in the central and south Aegean Sea, while the recent invasive alien Upeneus pori occurs actually often in fishery activities of Rhodes Island. Among the 31 Indo-Pacific fishes reported from the southeastern Aegean Sea, 48 % have spread to the central and south Aegean Sea considered together, 45% toward the central Aegean and 35% toward the south Aegean (Crete). Very difficult impediments obstruct easy colonization of the north Aegean Sea, in particular its western coasts, where only the recent invaders F. commersonii and L. sceleratus were recorded during summer. Liza carinata and L. sceleratus have been reported along the northeastern Aegean coasts, which probably present more suitable environmental conditions for the settlement of these two tropical species.

Current status of alien fishes in Greek seas 243

At the present time, about 55% of the Lessepsian fish species which have reached the SE Aegean Sea are the same species present also along the Libyan coasts, showing high adaptation ability during their advance in colonizing successfully the eastern Mediterranean, by various pathways; 38% of them are in common furthermore with Tunisia and Central Mediterranean considered together, at the limit between the east and west Mediterranean, and many of these species are early introductions into the Mediterranean (Galil, 2008). In conclusion, the westward spread of such alien species is continuing via various pathways along the Mediterranean coasts (Streftaris et al., 2005), showing an acceleration in the last few years enhanced by a combination of factors, such as the Suez Canal expansion in depth and width, increase in shipping, climate changes and the rise in water temperature, fisheries over-exploitation and other factors (Galil, 2006; Galil et al., 2007; Bianchi, 2007; Galil, 2008). According to Galil (2006), the Erythrean invasion is not limited to the Eastern Mediterranean, but is showing a significant expansion of its geographic limits, previously assumed to be east of Sicily, south of the Aegean and Adriatic Seas, known as the "Lessepsian Province" (Por, 1990). The dynamics of invasions and extension of the distribution of alien species obviously demand continuous update. A rearrangement of the ecosystem structure has already appeared in the eastern basin and monitoring procedures of the increasing southern exotic species invasions of the Mediterranean are carried out and should be intensified in the entire Mediterranean and in the countries along its coasts (Golani et al., 2004, 2006b; Zenetos et al., 2005; Pancucci-Papadopoulou et al., 2005a, b; 2006; Çinar et al., 2006; Elnais, 2008) for the assessment of the situation, for the conservation of biodiversity and for fishery management (Ben Rais Lasram and Mouillot, 2008; CIESM, 2008). REFERENCES Akyol, O., V. Ünal, T. Ceyhan, and M. Bilecenoglu. 2005. First confirmed record of Lagocephalus sceleratus (Gmelin, 1789) in the Mediterranean Sea. Journal of Fish Biology 66: 1183-1186. Akyol, O., V. Ünal and T. Ceyhan. 2006. Occurrence of two Lessepsian migrant fish, Oxyurichthys petersi (Gobiidae) and Upeneus pori (Mullidae), from the Aegean Sea. Cybium 30: 389-390. Ananiadis, C. 1952. On the appearance of the fish Tetrodon spadiceus (Rich.) in Greek seas. Praktika of Hellenic Hydrobiological Institute 6: 73-74. Andaloro, F., M. Falautano, M. Sinopoli, F. M. Passarelli, C. Pipitone, P. Addis, A. Cau and L. Castriota. 2005. The lesser amberjack Seriola fasciata (Perciformes: Carangidae) in the Mediterranean: A recent colonist? Cybium 29: 141-145. Azzurro, E. and F. Andaloro. 2004. A new settled population of the lessepsian migrant Siganus luridus (Pisces: Siganidae) in Linosa Island- Sicily Strait. Journal of the Marine Biological Association United Kingdom 84: 819-821. Azzurro, E., F. Pizzicori and F. Andaloro. 2004. First record of Fistularia commersonii (Fistularidae) from the Central Mediterranean. Cybium 28: 72-74.

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Micarelli, P., M. Barlettani and R. Ceccarelli. 2006 First record of Fistularia commersonii (Rüppel, (sic), 1838)  (Fistulariidae, Pisces) in the north Tyrrhenian. Biologia Marina Mediterranea 13 (1): 887-889. Milazzo, A., B. Barraco, A. M. Beltrame, L. Cannizzaro, M. Puleo, P. Rizzo, G. Salvo and S. Vitale. 2006. Capture of Fistularia commersonii (Rüppel, (sic), 1835) (Pisces, Fistularidae) in the coastal waters of Selinunte (S-W Sicily). Biologia Marina Mediterranea 13: 890-891. Minos, G., A. Imsiridou and P. S. Economidis, 2007. Liza haematochilus (Pisces, Mugilidae) in northern Aegean Sea: new records and gonad structure. XII European Congress of Ichthyology: Cavtat (Dubrovnik), Croatia, 9-13 September 2007. Book of Abstacts, p. 243. Minos, G., A. Imsiridou, and P. S. Economidis. Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea (in this volume). Mytilineou, C., C.-Y. Politou, C. Papaconstantinou, S. Kavadas, G. D’Onghia and L. Sion. 2005. Deep-water fish fauna in the Eastern Ionian Sea. Belgian Journal of Zoology 135: 229-233. Occhipinti-Ambrogi, A. and B. S. Galil. 2008. The northernmost record of the blue-spotted cornetfish from the Mediterranean Sea. Mediterranean Marine Science 9 (2): 127-129. Öğretmen, F., F. Yilmaz and H. Torcu Koç. 2005. An investigation on fishes of Gökova Bay (Southern Aegean Sea). Journal of Science and Technology of Balikesir University 7 (2): 19-36. Ondrias, I. C. 1971. A list of the fresh and sea water fishes of Greece. Hellenic Oceanology and Limnology10: 23-96. Oz, M. I., E. Okuş and A. Yüksek. 2007. Notes on the Erythrean alien fishes of Datça-Bozburun Peninsula- A specially protected area in the South eastern Aegean Sea (Turkey). Rapport de la Commission Internationale pour l'Exploration Scientifique de la mer Méditerranée 38: 563. Öziç, F. and F. Yilmaz. 2006. An investigation of demersal fishes of Gökova Bay in Aegean Sea. Ekoloji 15 (58): 16-20. Pais, A., P. Merella, M. C. Follesa and G. Garippa. 2007. Westward range expansion of the Lessepsian migrant Fistularia commersonii (Fistulariidae) in the Mediterranean Sea, with notes on its parasites. Journal of Fish Biology 70: 269-277. Pais, A., P. Merella, M. Cristina Follesa, G. Garippa and D. Golani. 2008. New data on Gaidropsarus granti (Regan, 1903) (Gadiformes: Lotidae) from the Mediterranean Sea, with emphasis on its parasites. Scientia Marina 72(3): 461-468. Pancucci-Papadopoulou, M.A., A. Simboura, A. Zenetos, M. Thessalou-Legaki and A. Nicolaidou. 1999. Benthic invertebrate communities of NW Rodos (Rhodes) Island (SE Aegean Sea) as related to hydrological regime and geographical location. Israel Journal of Zoology 45: 371-393. Pancucci-Papadopoulou, M.A., A. Zenetos, M. Corsini-Foka and Ch. Politou. 2005a. Update of marine alien species in Hellenic waters. Mediterranean Marine Science 6/2: 147-158. Pancucci-Papadopoulou, M.A., K. Kevrekidis, M. Corsini-Foka and N. Simboura. 2005b. Changes in species: invasion of exotic species. In: Papathanassiou E. and A. Zenetos (eds.), State of the Hellenic marine environment (SoHelME). Athens: HCMR Publications. pp. 336-342 Pancucci-Papadopoulou, M.A., A. Zenetos and M. Corsini-Foka. 2006. Aliens in Hellenic Seas: emphasis on introductions in ports. Communication presented at ICES/IOC/ IMO Working Group on ballast and other ship vectors. Oostende, Belgium, 13-15 March, 2006. p. 65. Pancucci-Papadopoulou, M.A., M. Corsini-Foka and A. Zenetos. 2007. Alien species in Hellenic marine waters. Record and monitoring of the phenomenon. 1st Panhellenic Meeting for the invasion of alien aquatic species in the Eastern Mediterranean. Heraklion, Crete, 5-6

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Tingilis, G., A. Anezaki, E. Valla, P. Lymberakis, A. Kapatangakis, S. Biyiakis and S. Kauri. 2003. First records of Lessepsian fish fauna migrants from the Crete marine area. Proceedings of the 11th Panhellenic Congress of Ichthyologists, Preveza, 10-13 April 2003. pp. 47-50. Torcu, H. and S. Mater. 2000. Lessepsian fishes spreading along the coasts of the Mediterranean and the Southern Aegean Sea of Turkey. Turkish Journal of Zoology 24: 139-148. Tortonese, E. 1946. On some fishes from the Eastern Mediterranean (Island of Rhodes). Annals and Magazine of Natural History 13: 710-715. Tortonese, E. 1947a. Ricerche zoologiche nell’isola di Rodi (Mar Egeo). Pesci. Bollettino di Pesca Piscicoltura e Idrobiologia 23 (2): 143-192. Tortonese, E., 1947b. Biological investigations in the Aegean Sea. Nature 159: 887-888. Tsimenidis, N., G. Tserpes, A. Machias and A. Kallianiotis. 1991. Distribution of fishes on the Cretan shelf. Journal of Fish Biology 39: 661-672. Vacchi, M., S. Bussotti, A. M. Miglietta and P. Guidetti. 2007. Presence of the Guineian puffer Sphoeroides marmoratus (Lowe, 1838) in the Mediterranean Sea. Journal of Fish Biology 71: 1215-1219. Whitehead, P.J.P., M.-L. Bauchot, J.-C. Hureau, J. Nielsen and E. Tortonese (eds.). 1984-1986. Fishes of the North-eastern Atlantic and the Mediterranean. Vol. I, II, III. Paris: UNESCO. 1473 pp. Yokes, B., R. Dervisoglu and B. Karacilk. 2002. An investigation of the marine biological diversity along Likya shores. Sualti Bilim ve Teknoloji Toplantisi Bildiriler Kitabi. Istanbul. 2000. pp. 166-181. (in Turkish). Zachariou-Mamalinga, H. 1999. The occurrence of the Atlantic fish Gaidropsarus granti in the Mediterranean Sea (South-eastern Aegean Sea, Dodecanese, Greece, Eastern Mediterranean). Annales Musei Goulandris 10: 261-266. Zachariou-Mamalinga, H. and M. Corsini. 1994. The occurrence of the fish Sphoeroides pachygaster in the south-eastern Aegean Sea (Greece). Annales Musei Goulandris 9: 479-483. Zaitsev, Y. and B. Öztürk (eds.). 2001. Exotic species in the Aegean, Marmara, Black, Azov and Caspian Seas. Istanbul: TUDAV. 265 pp. Zenetos, A., M. E. Çinar, M. A. Pancucci-Papdopoulou, J. G. Harmelin, G. Furnari, F. Andaloro, N. Bellou, N. Streftaris and H. Zibrowius. 2005. Annotated list of marine alien species in the Mediterranean with records of the worst invasive species. Mediterranean Marine Science 6 (2): 63-118. Zenetos, A., V. Vassilopoulou, M. Salomidi and D. Poursanidis. 2007. Additions to the marine alien fauna of Greek waters (2007 update). Journal of the Marine Biological Association of the United Kingdom, JMBA2 – Biodiversity Records, 5928. (Published online) http://www.mba. ac.uk/jmba/jmba2biodiversityrecords.php

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Invasions in the Adriatic Sea 255 D. Golani & B. Appelbaum-Golani (Eds.)Fish 2010 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 255-266. © Pensoft Publishers Sofia–Moscow

Fish Invasions in the Adriatic Sea Branko Dragičević and Jakov Dulčić

INTRODUCTION The Adriatic Sea is a semi-enclosed area of the Mediterranean Sea and is connected to the Ionian Sea and the rest of the Mediterranean basin via the Otrant gate. Being the northernmost part of the Mediterranean Sea, it is characterized by some significantly different physical aspects than those of the rest of the Mediterranean Sea, especially the eastern Mediterranean. Even in its southernmost part, but to a lesser extent, these characteristics still affect the properties of the Adriatic. Historically it has been generally divided into three geographic regions: the Northern, Middle and Southern Adriatic. With the shelf constituting as much as 74% of the sea bed, it is considered to be a rather shallow sea. The Northern Adriatic is very shallow and to a great extent influenced by the freshwater influx from the Po River. The Middle Adriatic is deeper, reaching 280 m at the Jabuka Pit and is separated from the Southern Adriatic by Palagruža Sill (180 m depth). The South Adriatic pit, at 1333 m of depth, is the deepest part of the Adriatic Sea ( Jardas, 1996). Even in the deepest water layers of Adriatic, temperatures usually do not fall below 10°C. During the summer, the temperature of the open sea surface waters rises to 22-25°C, although extremes can be observed in the range from 3° to 29°C (Zore-Armanda et al., 1999). As would be expected, the southern Adriatic is generally warmer than its central and northern part during the winter, usually by 8-10°C. Horizontal temperature distribution is more uniform during other seasons, although generally, the open sea is warmer than the coastal waters. Decreases of temperature are evident through the depth gradient and thermocline occurs at 10-30 m depth during warmer season (Zore-Armanda et al., 1999). The Adriatic is a basin of relatively high salinity. At an average of 38.3 ‰, it is somewhat lower in salinity than the Eastern Mediterranean, but still higher than that of the Western (Buljan and Zore-Armanda, 1971). As previously mentioned the freshwater influx from the Po River is the reason for lower and varying salinity values in the

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Northern Adriatic. Measurements have shown a continuous salinity increase as one moves towards the coastal and open waters of the Middle and Southern Adriatic basins (Grbec et al., 1998). There is a constant exchange between Adriatic and Mediterranean waters. Surface and bottom layer currents run from the Adriatic into the Mediterranean, while salinityrich Mediterranean water enters the intermediate layer of the Adriatic (Zore-Armanda, 1963). Due to the distribution of a large pressure center over the Mediterranean region, the horizontal air pressure varies between the northern and the southern Adriatic, influencing the intensity of the water exchange between the Adriatic and the eastern Mediterranean (Dulčić et al., 1999). Probably the most significant event occurring in an unpredictable pattern is the intensification of the inflow of Mediterranean waters, particularly Ionian water, which increases the salinity in the Middle Adriatic and the water temperature accordingly (Grbec et al.,1998). This phenomenon is called Adriatic Ingression and the influence of these ingressions can be observed in almost all periodic fluctuations of biotic and abiotic parameters such as salinity, temperature, transparency as well as primary production (Dulčić et al., 1999). Ingressions vary greatly from yearto-year; some years are characterized by extremely high water influx which consequently changes the hydrographic properties of the Adriatic. All these characteristics may be altered by climate change effects and should be taken into account as factors affecting biodiversity, and especially ichthyofauna, in the case of the Adriatic. BIODIVERSITY STATUS OF THE ADRIATIC ICHTHYOFAUNA It is worth mentioning that Adriatic ichthyofauna, in comparison to other Mediterranean regions, exhibits quite a high rate of biodiversity. The last extensive checklist of Adriatic fishes by Jardas (1996) enumerated 407 fish species inhabiting this area which, from a biogeographical standpoint, belong mainly to the Mediterranean and AtlantoMediterranean group of species. This list included indigenous and frequent species as well as sporadically occurring and rare or very rare species. Later revisions raised this number to at least 432 (Dulčić et al., 2004); the main reason for this increase is that a number of new exotic species have been encountered during the last few decades, the majority of which are Lessepsian migrants. The most important reason for the increase in perceived biodiversity of the Adriatic ichthyofauna is probably the discovery of a large number of species outside their usual area of distribution. During the last decade, several papers reported the occurrence of new fish species in the Adriatic Sea and a few possible reasons for these new findings can be distinguished. Lack of knowledge, for example; it is unclear if some fish species are only occasional visitors or are indigenous inhabitants of Adriatic, but rarely found (e.g., Regalecus glesne, Lophotus lacepedei, etc.). In regard to this issue, it can be noted that the Southern

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Adriatic basin is still insufficiently explored and a few new species have been recorded during last few years such as Lepidion lepidion, Caelorinchus mediterraneus, Cataetyx alleni, Valenciennellus tripunctulatus etc. (Lipej and Dulčić, 2004). There are also some unsolved systematic (taxonomic) and status issues; certain fish species were collected and wrongly identified years ago and received their proper identification only recently, leading to inclusion of such species in the Adriatic ichthyofauna checklist (e.g., Vanneaugobius dollfusi (see Pallaoro and Kovačić, 2000), Pampus argenteus (see Dulčić et al., 2004)). Implementation of new techniques and increasing research efforts have contributed greatly to the discovery of new species and led to a change of biodiversity status in general. The advance of non-destructive methods such as visual censuses has enabled insight to habitats previously inaccessible by fishing gear. This is most evident in assessment of benthic habitats, and especially in the case of some cryptobenthic fishes such as gobiids. Better surveys and monitoring programs have led to change in status of some fish species in the Adriatic, such as the Sandbar shark Carcharhinus plumbeus which was believed to be rare, but now should be considered a common species due to its recent findings (Lipej and Dulčić, 2004). Finally, temperature-related factors, influencing atmospheric and consequently oceanographic parameters have led to a increase of thermophilic species in the Adriatic. Numerous new records of such species as well as their increased abundance in some areas, has significantly altered fish diversity in the Adriatic. BIOLOGICAL INVASIONS DUE TO WATER WARMING EFFECTS There seem to be a number of areas in the land-ocean-atmosphere system at which regional climate changes reflect events on a global scale. The case of the Mediterranean Sea, due to its specific oceanographic conditions, can be of global importance (Dulčić et al., 1999). Considering this, conditions that occur in the Mediterranean Sea, are consequently reflected in those of the Adriatic. Incoming Mediterranean water into the Adriatic carries nutrient-rich water which affects primary and secondary production so the climate change, via its oceanographic influence, can play an important role in Adriatic ecosystems. The incoming Mediterranean water, with its higher salinity, is also warmer and many warm water fish species are moving toward higher latitudes (Dulčić and Grbec, 2000). Various studies have associated changes in ichthyofauna with climatic and oceanographic changes (Mearns, 1988; Stephens et al., 1988; Cushing, 1990; Francour et al., 1994). These changes could be reflected by new occurrences of thermophilic species, but also by relatively increased abundance of species that are rare or very rare in the area. The general conclusion regarding the occurrences of fish species in the Adriatic over the last 25 years is that the number of thermophilic species has been increasing (Dulčić and Grbec, 2000). It is indicative that through the periods of 1985-1987 and 1990-1995 when the mean sea surface temperatures for the Middle Adriatic showed

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anomalies of +0.15°C and +0.30°C respectively, many records of rare and new fish were produced (Dulčić et al., 1999). Several phases of the northward spreading of southern species can be distinguished according to Francour et al. (1994). Only single specimens appear in the first phase. Subsequently, more adult individuals are observed in the area. The next phase is characterized by the occurrences of larval stages and finally, southern species achieve the status of a new settler. The Eastern Adriatic, for example, has produced frequent records of some larvae and juveniles of warm water species in the last 15 years, only to name a few, larva of Trachipterus trachypterus (by Dulčić, 1996) and Balistes carolinensis (by Dulčić et al., 1997a) and juvenile of Trachinotus ovatus (by Dulčić et al., 1997b). All these findings may be connected with climatic and hydrographic parameters that were present in the area at a time. Records of species like Lagocephalus lagocephalus lagocephalus, Sphoeroides pachygaster, Plectorhinchus mediterraneus and Mycteropterca rubra were new for the Adriatic. These species probably extended their distribution from the southern areas to the north due to water warming, but whether those findings represent an abortive or a successful attempt of colonization of northern areas is yet to be evaluated through successive records of those species. The finding of Epinephelus aeneus in the middle-eastern Adriatic in 2006 represents the northernmost occurrence of this species in the Mediterranean and, along with two other records for the Adriatic, this could be a sign that this species is in the process of colonization of new areas, particularly Adriatic, as a consequence of water warming (Glamuzina et al., 2000, Dulčić et al., 2006). It has also been shown that some species, previously considered rare or uncommon, have begun to occur more commonly or even experience population boom. One interesting case worth mentioning is the unusual catch of a 1.5 kg of Pomatomus saltatrix in Tarska Cove in Northern Adriatic in winter of 2003. This species was not even recognized by local fishermen since its occurrence in Adriatic was sporadic and limited only to southern areas. Its presence in large numbers could very easily be attributed to oceanographic changes (Adriatic ingressions) augmented by feeding migration (Dulčić et al., 2005). A remarkable change in population structure was observed recently with three species: Thalassoma pavo, Balistes carolinensis and Sparisoma cretense. These species were observed only rarely in the past, mostly in southern part of Adriatic, but today they represent an established part of rocky coastal ichthyofauna of the entire Adriatic (Dulčić et al., 2006). During the last few years, a number of Lessepsian fish species were also reported in the Adriatic. More than 67 Erythrean fish species of Indo-Pacific origin have entered Mediterranean Sea via the Suez Canal since its opening (CIESM, 2008). Most of these species, named Lessepsian migrants, established populations in Levantine waters where they made a tremendous impact on the ecosystem and dozens of these have become important components of commercial fisheries (Golani et al., 2002). Temperature is the most important factor in determining the dispersal of Lessepsian fish (Ben-Tuvia and Golani, 1995; Pallaoro and Dulčić, 2001) and therefore the presence of Lessepsian migrants in the Adriatic could be in correlation with the previ-

Fish Invasions in the Adriatic Sea 259

ously described Adriatic ingressions rather than a consequence of species adaptation to a new environment. A key argument for this conclusion is the fact that we still do not have any data that those species have established their populations in the Adriatic Sea (with the possible exception of Fistularia commersonii, but this is yet to be confirmed). Therefore, it is difficult to perform any ecological analyses based on sporadic and rare records. Furthermore, established populations of some Lessepsian migrants in the Eastern Mediterranean Sea, especially those with higher colonizing potential, could provide “recruits” capable of establishing populations in the northern areas. Alien species are an increasing problem in aquatic systems and the consequences for indigenous species, especially those of economic importance, are poorly understood (Kalogirou et al., 2007). There are quite a few cases in the Levantine Sea where Lessepsian migrants may have affected populations of native fishes. Herbivorous migrants Siganus luridus and S. rivulatus may have out competed the only native herbivorous fish Sarpa salpa and reduced its abundance (Galil, 2007); Upeneus moluccensis may have displaced native Mullus barbatus to deeper waters (Golani, 1994) and other invasive species may cause future major shifts in community composition. LESSEPSIAN FISH MIGRANTS IN THE ADRIATIC The catch of Terapon theraps in 2007 (Lipej et al., 2008) brought the number of Lessepsian fish migrants that were recorded in the Adriatic Sea to 11 (Fig. 1). A specimen of T. theraps, a species previously unrecorded in the Mediterranean, was caught in the Piran Bay in Slovenia, Northern Adriatic. This species was found a great distance from its normal geographical distribution and it is possible that it has extended its distribution from an established population from the Red Sea. This hypothesis could be supported by the fact that juveniles of T. theraps were observed with floating weeds, often far offshore (Kuiter and Tkamasa Tonozuka, 2001), and there is a possibility that they could enter the Adriatic Sea, probably during Adriatic ingressions. The occurrence of T. theraps is of particular interest since its record was the first for the Mediterranean; furthermore, it was found a great distance from its usual distribution area. Similar are the cases of Pampus argenteus and Epinephelus coioides. The latter was considered rare and a recent invader and its presence in the Mediterranean was acknowledged only from the coast of Israel, hence its presence in the northernmost part of the Adriatic is rather surprising. One specimen of 12 cm long E. coioides was caught with a fishing net in the Gulf of Trieste in the summer of 1998 and this record represents the northernmost record of this species in the Mediterranean (Parenti and Bressi, 2001). Considering the record of P. argenteus, one specimen was caught in 1896 in front of Rijeka (Fig. 2) and was initially identified as Stromateus fiatola, but later revision yielded its proper identification (Dulčić et al., 2004). This is the only record of this species in the Mediterranean; hence its presence is even more surprising. It is possible

260 Branko Dragicevic and Jakov Dulcic

6 - 11

1 N W

E S

1. Pampus argenteus 2. Hemiramphus far 3. Paraexocoetus mento 4. Saurida undosquamis 5. Sphyraena chrysotaenia 6. Epinephelus coioides 7. Leioghathus klunzingeri 8. Stephanolepis diaspros 9. Siganus rivulatus 10. Fistularia commersonii 11. Terapon theraps

7

9 - 10

5 8

2 3

4

10

Fig. 1. Records of Lessepsian migrants in the Adriatic Sea

Fig. 2. Pampus argenteus caught in 1896 off Rijeka, northern Adriatic (specimen is preserved in the collection of the Zoological Museum in Zagreb)

Fish Invasions in the Adriatic Sea 261

that this specimen penetrated in the Mediterranean following slow boats or associated with pelagic jellyfishes, floating wrecks or drifting algae. Nevertheless, this record could represent the first confirmed Lessepsian fish migrant in the Mediterranean Sea. Furthermore, one specimen of Hemiramphus far was recorded at the entrance of the Adriatic Sea, along the Albanian coast in 1986 (Colette and Parin, 1986). This early invader, recorded in the Mediterranean for the first time in 1927 by Steinitz (1927) in the Eastern Levantine Basin (Mavruk and Avsar, 2007) spread successively in the waters off Syria, Rhodes and Egypt (Golani et al., 2002). In the same year, one specimen of Parexocoetus mento was also recorded in Albanian coastal waters (Parin, 1986). This species is, like H. far, frequent in the Eastern Levantine Basin (Golani et al., 2002) and after being recorded there for the first time in 1935 (Bruun, 1935), records followed successively in the waters of Rhodes and Libya (Golani et al., 2002). Albanian coastal waters yielded another record of Lessepsian fish. In 1995 a single 28 cm long specimen of Saurida undosquamis was caught with a deep sea trawl (Rakaj, 1995). This species’ first Mediterranean record was from the waters of Israel (Ben-Tuvia, 1953) and it was successively recorded in the waters of Cyprus, Turkey, Greece, Libya and Egypt (Golani et al., 2002). In the summer of 2000, another visitor was recorded in the Adriatic. One 123 mm long specimen of Sphyraena chrysotaenia was caught in the Bay of Gornji Molunat in the southern Adriatic at a depth of 6 m (Pallaoro and Dulčić, 2001). This species’ Mediterranean distribution ranges from waters of Israel, Lebanon and Egypt to Turkish waters, Eastern Aegean Sea and Ionian Sea. It was also recorded in the Italian and Tunisian coastal waters (Golani, 1998). In the summer of the same year, an 85 mm a specimen of Leiognathus klunzingeri was captured by beach seine near the island of Mljet in the Southern Adriatic at a depth of 4 meters. This Lessepsian species is very abundant in the Eastern Mediterranean and this record represents its northernmost occurrence in the Mediterranean Sea where it was recorded for the first time in Syria (Gruvel, 1931) and successively in the waters of Israel, Rhodes, Turkey, Lampedus island, Egypt and Greece (Golani et al., 2002). Another migrant, very abundant and frequent in the Eastern Mediterranean – Stephanolepis diaspros, has been recorded in the Adriatic in the summer of 2002. A 77 mm long specimen of this species was caught in the coastal waters of Montenegro in Southern Adriatic. It was found on the local fish market, and according to local fishermen it was caught with a beach seine at a depth of about 20 m. It is the northernmost record for this species in the Mediterranean and is also the first occurrence of a member of this family (Monacanthidae) for the Adriatic Sea (Dulčić and Pallaoro, 2003). After being recorded in the Eastern Levantine Basin for the first time in the Mediterranean, this species was successively detected in the waters of Syria, Cyprus, Greece and Italy (Golani et al., 2002). Two specimens of Siganus rivulatus were captured by beach seine near the islet Bobara (southern Adriatic, Croatian coast) in the autumn of 2000 at a depth of 15 m (Fig. 3). This is also the northernmost occurrence of this species in the Mediterranean

262 Branko Dragicevic and Jakov Dulcic

Sea. It was first recorded in the Eastern Levantine Basin (Steinitz, 1927) and successively in the waters of Syria, Cyprus, Aegean Sea, Libya, Tunisia and Ionian Sea (Golani et al., 2002). This species, beside Siganus luridus, is an extremely successful colonizer due to lack of competition from indigenous Mediterranean species, specifically, a lack of herbivorous species (Golani, 2002). In 2006 Fistularia commersonii, of which two specimens were recorded, occurred in the Adriatic (Dulčić et al., 2008). One specimen was caught in the waters of Tricase Porto (southwestern Adriatic, Italy) and the other off Sveti Andrija (southeastern Adriatic, Croatia). Additionally, a third specimen of this species was caught near the Montenegrin coast in the winter of 2007 (Fig. 4). This record suggests that F. commersonii has succeeded in colonizing the Adriatic Sea and it is possible that this species will establish a self-sustaining population in the near future. Furthermore, this is the only Lessepsian migrant with an additional record in the Adriatic so far. F. commersonii has

Fig. 3. Siganus rivulatus caught near the islet Bobara, southern Adriatic

Fig. 4. Fistularia commersonii, washed up on the shore in Bar (Montenegran coast, southern Adriatic)

Fish Invasions in the Adriatic Sea 263

been nicknamed the “Lessepsian sprinter” referring to its fast range increase through the Mediterranean area (Karachle et al., 2004), having experienced a population explosion along the coast of Israel and subsequently spreading northward to the waters of Turkey and Greece (CIESM, 2008) and westward reaching the shores of Southern Italy (Azzurro et al., 2004) eventually reaching the Tyrrhenian Sea (Psomadakis et al., 2008) and southern Spain (Sánchez-Tocino et al., 2007). CONCLUSIONS Although no thorough studies have been conducted to evaluate the impact of the colonizing fishes on local communities in the Adriatic, some observations taken by local fishermen should be emphasized. The most significant is the case of Pomatomus saltatrix which endangered the community of mullet species in the estuarine area of the Neretva river in the eastern Adriatic. These mullets are of great importance to local commercial fisheries but lately there has been a decrease in their catch: furthermore there is an increasing number of mutilated fishes, most likely severed by this voracious and aggressive predator (Cervigón, 1993). The presence of Fistularia commersonii in the Adriatic is far from alarming, but it should be noted that Kalogirou et al. (2007) found that most abundant prey by weight of F. commersonii in the Mediterranean were Spicara smaris, Boops boops and Mullidae spp. Since these species are of a great importance to local fisheries and considering the fast spreading rate of F. commersonii followed by rapidly increasing abundance, there is a possibility of negative effects on the local fish communities. As water warming continues, one might expect a further increase in abundance of some thermophilic species. There is a possibility that species like Balistes carolinensis, Spheroides pachygaster or Sparisoma cretense could out-compete some indigenous species in specific areas. This scenario could be augmented by the fisheries pressure on local species, while such pressure on exotic species is absent. However, it would be very interesting to see whether such species may become commercially important. For example B. carolinensis is considered a high priced species and its flesh is of excellent quality (Froese and Pauly, 1994), but local fishermen usually discard it believing it is inedible or of a poor flesh quality. There are many indications that climate change on a global scale has influenced and changed the assemblage of Adriatic ichthyofauna in a more or less significant manner in regard to new species present in the area. The hypothesis of northward movement of thermophilic species and changes in marine biodiversity is supported by numerous records of fish species previously characteristic to more southern areas. The Adriatic Sea is apparently becoming a northward distribution path for Lessepsian migrants and it will be very interesting to observe this invasion on a larger time scale especially in the context of the response of such species to their new environment.

264 Branko Dragicevic and Jakov Dulcic

We conclude that biological invasions have not yet affected Adriatic ichthyofauna in an amount which could have extremely negative consequences on indigenous fish species. However, increasing abundance of some thermophillic species could potentially shift ecological balance in unpredictable directions. In any case, we emphasize the need for further research and evaluation of migrant species status on a continuous basis. REFERENCES Azzurro E., F. Pizzicori and F. Andaloro. 2004. First record of Fistularia commersonii (Fistularidae) from the central Mediterranean. Cybium 28: 72-74. Ben-Tuvia, A. 1953. Mediterranean fishes of the Israel. Bulletin of the Sea Fishery Research Station, Haifa 8: 1-40. Ben-Tuvia, A. and D. Golani. 1995. Temperature as the main factor influencing the Lessepsian migration. In: Quignard, J.-P., P. Beaubrun and M. Bertrand (eds.) Proceedings of International Colloqium Maison Environment Montpellier, Montpellier: Maison de l’Environnement de Montpellier. pp. 159-162. Cervigón, F., 1993. Los peces marinos de Venezuela. Volume 2. Caracas: Fundación Científica Los Roques. 497 p.  Dulčić, J. 1996. First record of ribbon fish larva, Trachipterus trachypterus, from the eastern Adriatic. Cybium 20: 101-102 Dulčić, J., M. Kraljević, F. Kršinić and A. Pallaoro. 1997a. Occurrence of fingerlings of grey triggerfish, Balistes caroliensis Gmelin 1789 (Pisces: Balistidae), in the eastern Adriatic. Annales. Annals for Istrian and Mediterranean Studies 11:271-276. Dulčić, J., A. Pallaoro and M. Kraljević. 1997b. First record of pompano fingerling, Trachinotus ovatus (Linnaeus, 1758) (Pisces: Carangidae), in the Eastern middle Adriatic. Natura Croatica 1: 61-65. Dulčić, J., B. Grbec and L. Lipej. 1999. Information on Adriatic ichthyofauna – effect of water warming? Acta Adriatica 40: 33-43. Dulčić, J. and B. Grbec. 2000. Climate change and Adriatic ichthyofauna. Fisheries Oceanography 9(2): 187-191. Dulčić, J. and A. Pallaoro. 2003. First record of the filefish, Stephanolepis diaspros(Monacanthidae), in the Adriatic Sea. Cybium 27:321-322.  Dulčić, J. and A. Pallaoro. 2004. First record of the marbled spinefoot Siganus rivulatus (Pisces: Siganidae) in the Adriatic Sea. Journal of Marine Biological Association of the United Kingdom 84: 1087-1088. Dulčić, J., L. Lipej, A. Pallaoro and A. Soldo. 2004. The spreading of lessepsian fish migrants into the Adriatic Sea: a review. Rapports Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 37: 349. Dulčić, J., M. Kraljević, A. Pallaoro and B. Glamuzina. 2005. Unusual catch of bluefish Pomatomus saltatrix (Pomatomidae) in Tarska cove (northern Adriatic). Cybium 29: 207-208. Dulčić, J., P. Tutman and M. Ćaleta. 2006. Northernmost occurrence of the White Grouper, Epinephelus aeneus (Perciformes: Serranidae), in the Mediterranean Area. Acta Ichthyologica et Piscatoria 36: 73-75

Fish Invasions in the Adriatic Sea 265

Dulčić, J., G. Scordella and P. Guidetti. 2008. On the record of the Lessepsian migrant Fistularia commersonii (Rüppell,1835) from the Adriatic Sea. Journal of Applied Ichthyology 24: 101-102. Francour, P., C.F. Boudouresque, J.G. Harmelin, M. Harmelin-Vivien and J.P. Quignard. 1994. Are the Mediterranean waters becoming warmer? Information from biological indicators. Marine Pollution Bulletin 28:523-526. Froese, R. and D. Pauly (eds.). 2008. FishBase. World Wide Web electronic publication. www. fishbase.org – version (01/2008). Galil, B.S.  2007.  Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Marine Pollution Bulletin 55(7-9):314-322 Glamuzina, B., P. Tutman, A.J. Geffen, V. Kozul, and B. Skaramuca. 2000. First record of white grouper, Epinephelus aeneus (Serranidae) in the south eastern Adriatic. Cybium 24: 306-308 Golani, D. 1998. Impact of Red Sea fish migrants through the Suez Canal on the aquatic environment of the eastern Mediterranean. Yale School of Forestry and Environmental Studies Bulletin 103: 375-387. Golani, D. 1998. Distribution of Lessepsian migrant fish in the Mediterranean. Italian Journal of Zoology 65 (Suppl.): 95-99. Golani, D. 2002. Lessepsian fish migration – characterization and impact on the eastern Mediterranean. In: Őztürk, B. and N. Basusta (eds.) Proceedings of the Workshop on Lessepsian Migration. Istanbul: Turkish Marine Research Foundation, 9: 1-9. Golani D., L. Orsi Relini, E. Massutí and J.P. Quignard. 2002. CIESM atlas of exotic species in the Mediterranean. Vol. 1. Fishes. Briand, F. (ed), Monaco: CIESM Publisher. 254 pp. Grbec, B., M. Morović and M. Zore-Armanda. 1998. Some new observations on the long-term salinity changes in the Adriatic Sea. Acta Adriatica 39 (1): 3-12. Gruvel, A. 1931. Les Etats de Syrie. Richesses marines et fluviales. Exploitation actuelle. Paris: Avenir Société d’Editions Géographiques, Maritimes et Coloniales. 453 pp. Jardas, I. 1996. Jadranska ihtiofauna. Zagreb: Školska knjiga. 552 pp. (in Croatian). Kalogirou, S., M. Corsini, G. Kondilatos and H. Wennhage. 2007. Diet of the invasive piscivorous fish Fistularia commersonii in a recently colonized area of the eastern Mediterranean. Biological Invasions 9: 887-896. Karachle P.K., C. Triantaphyllidis and K.I. Stergiou. 2004. Fistularia commersonii Rüppell, 1838: A Lessepsian sprinter. Acta Ichthyologica et Piscatoria 34: 103-108. Koutrakis E. T. and A.C. Tsikliras. 2003. Length-weight relationships of fishes from three northern Aegean estuarine systems (Greece). Journal of Applied Ichthyology 19: 258-260. Kuiter, R. H. and Takamasa Tonozuka. 2001. Pictorial guide to Indonesian reef fishes. Part 1. Eels- Snappers, Muraenidae – Lutjanidae. Seaford, Victoria : Zoonetics. 302 pp. Lipej, L. and J. Dulčić, J. 2004. The current status of Adriatic fish biodiversity. In: Griffiths,H.I., B. Krystufek and J. M. Reed (eds.) Balkan biodiversity: pattern and process in the European hotspot. Amsterdam: Kluwer. pp. 291-306. Lipej, L., B. Mavrič and J. Dulčić. 2008. The largescaled terapon Terapon theraps: an Indo-Pacific fish new to the Mediterranean Sea. Journal of Fish Biology 73: 1819-1822 Mavruk S. and A. Dursun. 2008. Non-native fishes in the Mediterranean from the Red Sea, by way of the Suez Canal. Reviews in Fish Biology and Fisheries 18: 251-262. Mearns, A. J. 1988. The odd fish: unusual occurrences of marine life as indicators of changing ocean conditions. In: Soule, D.F. and G. S. Keppel (eds). Marine organisms as indicators. Berlin: Springer. pp. 137-173.

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Pallaoro, A. and M. Kovačić. 2000. Vanneaugobius dollfusi Brownell, 1978 a rare fish new to the Adriatic Sea. Journal of Fish Biology 57: 255-257. Pallaoro A. and J. Dulčić. 2001. First record of the Sphyraena chrysotaenia (Klunzinger, 1884) (Pisces, Sphyraenidae) from the Adriatic Sea. Journal of Fish Biology 59: 179-182. Parenti, N. and P. Bresi. 2001. First record of the orange-spotted grouper, Epinephelus coioides (Perciformes: Serranidae) in the Northern Adriatic Sea. Cybium 25: 281-284. Parin, N.V., 1986. Hemiramphidae. In: Whitehead, P.J.P., M.L. Bauchot, J.C. Hureau, J. Nielsen and E. Tortonese (eds.), Fishes of the North-Eastern Atlantic and the Mediterranean Vol. 2. Paris: UNESCO. pp. 967-973. Psomadakis, P.N., U. Scacco, I. Consalvo, M. Bottaro, F. Leone and M. Vacchi. 2008. New records of the lessepsian fish Fistularia commersonii (Osteichthyes: Fistulariidae) from the central Tyrrhenian Sea: signs of an incoming colonization? JMBA 2 Biodiversity Records. Published online (www.mba.ac.uk/jmba/pdf/6123.pdf ). Cited 12 February 2008. Rakaj, N. 1995. Iktiofauna e Shqipërisë [Ichthyofauna of Albania]. Tiranë: Shtëpia Botuese “Libri universitar”. (in Albanian). 700 pp. Sánchez-Tocino, L., F. Hidalgo Puertas and M. Pontes. 2007. Primera cita de Fistularia commersonii Ruppell, 1838 (Osteichtyes: Fistulariidae) en aguas mediterráneas de la Península Ibérica. Zoologica Baetica 18: 79-84. Steinitz W., 1927. Beitrage zur Kenntnis der Kustenfauna Palestinas. I. Pubblicazioni della. Stazione Zoologica di Napoli 8(3-4): 311-353. Stephens, J. S., Jr., J. E. Hose and M. S. Love. 1988. Fish assemblages as indicators of environmental change in nearshore environments. In: Soule, D.F. and G. S. Keppel (eds.) Marine organisms as indicators. Berlin: Springer. pp. 91-105. Zore-Armanda, M. 1963. Les masses d’eau de la mer Adriatique. Acta Adriatica 10: 5-88. Zore-Armanda, M. 1969. Temperature relations in the Adriatic Sea. Acta Adriatica 13: 1-50. Zore-Armanda, M., B. Grbec and M. Morović. 1999. Oceanographic properties of the Adriatic Sea – A point of view. Acta Adriatica 40 (Suppl.): 39-54.

native D. Golani & B. Appelbaum-GolaniNon (Eds.) 2010marine fish in Italian waters 267 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 267-292. © Pensoft Publishers Sofia–Moscow

Non native marine fish in Italian waters Lidia Orsi Relini

INTRODUCTION About thirty species of non native marine fish appeared in Italian waters during the last fifty years, a consistent fraction of the total number recorded in the same period in the whole Mediterranean by the CIESM Atlas of Exotic Fish (Golani et al., 2002, 2004, 2007 plus online updating 2005, 2008). This number represents an approximation because abundant material is still waiting to be studied. In the present notes I take into account a sample (Table 1) hopefully sufficient to characterize different groups, in order to separate casual events from those which have ecological significance. In the Mediterranean, evaporation processes surpass river inputs and rainfall, so the prevailing surface currents enter both from the western (Gibraltar Strait) and the eastern (Suez Canal) side. Recent climatic trends (Fig. 1) indicate an increase in temperatures and rainfall reduction, both of which contribute to increase the influx toward this basin. It is therefore easy to envisage a continuous inward flow of marine species, mainly in planktonic phases, but also during other life stages, which enriches the Mediterranean; on the other side the Mediterranean is not only a destination, but also a point of departure of fish species, a fact which testifies its vitality (Quignard and Tomasini, 2000). Fish transported by currents can be larvae, postlarvae and juveniles living in surface waters; we can add all those species which live in association with flotsam and large pelagic cnidarians, or adult fish using large pelagic vectors, such as remoras. Other passive ways to enter the Mediterranean are related to human activities such as the maritime traffic and aquaculture. Carlton (1985, 2001) described ships as biological isles bearing hundreds of marine species and their routes as conveyor-belts on which huge numbers of marine organisms are continuously transported. To these basic aspects, fishes add autonomous displacement ability, reaching top performances in some species of Scombridae and Carangidae; in fact, recent satellite

268 Lidia Orsi Relini

Table 1. Non native fish species recorded in Italian waters in recent times (1959-2008). Chondrichthyes

Origin

Where

How many

Category

circumtropical

Ligurian Sea, Sicily ?

1

vagrant

(Peron & Le Sueur, 1822)

circumtropical

Ionian Sea

1

vagrant

(Rüppell, 1837)

circumtropical

Ionian Sea

1

vagrant

circumtropical

Ligurian Sea

1

vagrant

Indopacific

Tyrrhenian Sea, Ligurian Sea

2

ship transported

Atlantic

Ligurian Sea

3

colonizer?

Chaunax suttkusi Caruso, 1989

Atlantic

Sicily Strait

2

moving North

Diodon hystrix Linnaeus, 1758

circumtropical

Ionian Sea

1

vagrant

Indopacific

Ionian Sea

1

ship transported

Indopacific

Adriatic Sea

1

ship transported

Indopacific

Sicily Strait

1

erythrean colonizer ?

Indopacific

All Italian seas

tens

erythrean colonizer

Atlantic

Sardinia channel

1

moving North

Indopacific

Ligurian Sea

1

vagrant

South Atlantic Ligurian Sea, Ionian Sea

2

ship transported

Atlantic

Sicily Strait, Tyrrhenian Sea

3

moving North colonizer?

Indopacific

Ligurian Sea

1

ship transported

Atlantic

Ionian Sea, Sardinia

3

drift fish unclassified

Atlantic

Sicily Strait, South Tyrrhenian

tens

colonizer

Carcharhinus falciformis Galeocerdo cuvier

Rhizoprionodon acutus

(Müller & Henle, 1839)

Sphyrna mokarran (Rüppell, 1837) Osteichthyes (Quoy & Gaimard, 1825)

Abudefduf vaigiensis

Lowe, 1934

Beryx splendens

Elates ransonnettii (Steindachner, 1876) (Hamilton, 1822)

Epinephelus coioides

Etrumeus teres (Dekay, 1842) Rüppell, 1835

Fistularia commersonii Halosaurus ovenii

Johnson, 1863

Makaira indica (Cuvier,1832) Cuvier & Valenciennes, 1829

Pinguipes brasilianus

Pisodonophis semicinctus

(Forsskål, 1875)

Pomadasys stridens

Lutken, 1880

Psenes pellucidus Seriola fasciata

(Richardson, 1848)

(Bloch, 1793)

Seriola carpenteri

Mather, 1971

Seriola rivoliana Cuvier, 1833 Siganus luridus (Rüppell, 1829) Sphoeroides marmoratus

(Lowe, 1838)

Sphoeroides pachygaster

(Müller & Troschel, 1848)

Stephanolepis diaspros Synagrops japonicus Zenopsis conchifer

Fraser-Brunner, 1940 (Doderlein, 1884)

(Lowe, 1852)

Atlantic

Sicily Strait

hundreds

moving North colonizer

Atlantic

Sicily Strait

1

moving North

Indopacific

Sicily Strait, Tyrrhenian tens sampled Sea

erythrean colonizer

Atlantic

Ionian Sea

1

unclassified

circumtropical

All Italian seas

hundreds

moving North colonizer

Indopacific

Ionian Sea, Sicily Strait, South Tyrrhenian Sea

3

erythrean unclassified

Indopacific

Ligurian Sea

1

ship transported

Atlantic

Sicily Strait

1

moving North

Non native marine fish in Italian waters 269

Fig. 1. a) Winter NAO index oscillations and general trends in the last half century. In the Mediterranean, high values of NAO are associated with high temperatures and reduced rainfall: b and c are examples of these relationships in the Ligurian area (Orsi Relini et al., 2006). NAO oscillations influence currents both in NE Atlantic (Pingree, 2002) and in the Mediterranean (Gasparini and Astraldi, 2002). Background: inflow of Atlantic surface waters in the Gibraltar Strait.

270 Lidia Orsi Relini

tuna tagging experiments showed that a large bluefin can cross the Atlantic in four weeks (Block et al., 2005). Thus the present Italian alien fish data set can, in my opinion, be divided into the following categories: a) Vagrant b) Ship transported fish c) Drift fish d) Atlantic fish enlarging their distribution northward, including Mediterranean colonizers e) Erythrean colonizers, i.e. those species which have established population units in the Mediterranean (also named Lessepsian sensu Por, 1978). Not all listed fish are known well enough to be properly allocated. The present sample (Table 1), in terms of geographic origin includes 10 Indo-Pacific, 11 Atlantic and 6 circumtropical species: this balanced ratio between fish coming from East and West is probably due to the central position of the Italian peninsula and its surrounding seas. In fact, a similar pattern was observed in Tunisian waters, where 6 Lessepsian and 6 Atlantic species were recorded (Bradai et al., 2004); while in the adjacent west coast of Libya, the Erythrean species are 8 but, in the east coast of the same country, their number rises to 16 (Shakman and Kinzelbach, 2007). In Italian waters (Table 1) 6 species are clearly stragglers or vagrant fish, at least 6 have been introduced by ships, 7 are Atlantic species extending their distribution northward due to ocean warming, 2 (possibly 3) are Erythrean colonizers and only one belong to the poorly known category of drift fish. Other species, listed in Table 1, present some uncertainties linked to their distributions and cannot be properly allocated in one of these groups. VAGRANT FISH In the literature of the Mediterranean many cases of vagrant organisms can be found, mainly represented by the largest members of offshore nekton. Marine mammals (e.g. Megaptera novaeangliae, see Frantzis et al., 2004), perciform fish, sharks and large cephalopods (e.g. Architeuthis see Gonzales et al., 2000) are the more outstanding alien species. Generally isolated specimens were observed and their records were casual and unpredictable. Apparently such rare events had a very limited (if any) impact on Mediterranean natural ecosystems, if compared to their large mediatic success. In Italian waters, a large hammerhead shark Sphyrna mokarran (Boero and Carli, 1977) and an adult male of Makaira indica (Orsi Relini and Costa, 1987) were caught by the small tuna trap of Camogli (Ligurian Sea), in 1969 and 1987 respectively, while one individual of the Charcharinid shark Rhizoprionodon acutus was captured in the Gulf of Taranto (Ionian Sea) (Pastore and Tortonese, 1985); these 3 records are unique till now for the whole Mediterranean. Regarding the Tiger shark, Galeocerdo cuvieri, one specimen was fished in July 1998 by a swordfish driftnet in the Messina Strait (Sicily) (Celona, 2000); only another specimen of this species had been previously caught in Mediterranean waters, in the Alboran Sea (Pinto della Rosa, 1994). More generally,

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catches of uncommon sharks have been several times mentioned, especially from Sicily, but they are still waiting to be verified. This aspect is related to the possibility of preserving study material, a necessary step to assure the reliability of the records. One of these cases is represented by the Charcarhinid shark Carcharhinus falciformis, reported as present in southern Italian waters, but so far documented only by a specimen of the Ligurian Sea. Dyodon hystrix is also considered to be a vagrant (Table 1) because only one record (Torchio, 1963) occurred in the last fifty years. Other vagrants can be tracked in the old literature: the Rainbow Runner Elagatis bipinnulata was fished in the Gulf of Genoa in a small group (Sassi, 1846); specimens are preserved in three different Italian museums (Tortonese, 1975). Acanthocybium solandri and Scomberomorus tritor were recorded in Sicily at the end of 1800; the former reappered in Sicily after the passing of more than one century (Romeo et al., 2005). In rarer cases, the vagrant was a large mesopelagic fish: Alepisaurus ferox was mentioned first by Bonaparte (1846); laterDoderlein (1878-1879) listed this species in the ichthyofauna of Sicily, but no further records exist for Italian seas and the whole Mediterranean. SHIP TRANSPORTED FISH Some non native species have a such remote origin that is impossible to hypothesize a natural displacement to the locality where they are found; generally these fishes appear not far from large harbors, making maritime traffic the most likely cause of their presence. In the present sample (Table1), six species can clearly be ascribed to this group: Abudefduf vaigiensis was observed in the Gulf of Naples in September 1957, during a dive in shallow water (Tardent, 1959): it was a young specimen (8.5 cm), outstanding for its yellow and black color, apparently associated with a school of indigenous fish (Chromis and Thalassoma). This fish was then caught few days later; at the Zoological Station of Naples, Tardent made a comparison of Atlantic and Red Sea materials, which led him to the conclusion that it was the first case of a Red Sea species caught in the Western Mediterranean. Given the great distance from Suez, he considered the possibility of an eggs/larvae transport on board a ship. Ben Tuvia (1966) accepted this interpretation “since there are no records of this fish from the Suez Canal or from the Eastern Mediterranean, this is probably an instance of a single specimen having been transported in Italy”. As a matter of fact, only about 40 years later this species appeared in the Levant (Goren and Galil, 1998). Curiously, during August 1998, the same underwater observations of Tardent were repeated in the Ligurian Sea, with another young fish of the same size (Vacchi and Chiantore, 2000), which resulted the third specimen recorded in the Mediterranean. Pomadasys stridens was the second Red Sea fish found in the Western Mediterranean. It was caught by a trammel net at a depth of 45 m not far from the harbor facilities of Savona

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– Vado Ligure (Torchio, 1969). The same author had previously collected a specimen of Cephalopholis cfr. miniatus (Finale Ligure, near Savona, August 1968) and received for study a specimen of Chaetodon cfr. hoeflery (Torchio, 1968), but he refused to add these two species to any official list, since he was doubtful as to their occurrence by natural causes. In other words, he suspected that defrosted fish could have been illegally added to the products of the local artisanal fishery (personal communication). So, different opinions arose concerning the record of exotic species in the Western Ligurian Riviera, casting doubts on previous records as well. In fact Tortonese (1958) described the capture of a large specimen of the Atlantic fish Anarhichas lupus at Varazze (near Savona), but not all his colleagues accepted the addition of this species to the Italian ichthyofauna. Torchio considered of paramount importance the necessity of a trust-worthy person for the collection of study material; this was the same position held by Soljan (1975) regarding the intriguing Adriatic record of Pampus argenteus, caught in 1896 near the port of Fiume (today Rijeka). In April 1987 a specimen of Synagrops japonicus (an Indo-Pacific species widely distributed from South Africa to Hawai’i) was caught by trawl on epibathyal fishing grounds (250-450 m) of the Gulf of Genoa (Orsi Relini, 1990). Given that this species apparently is not present in the Red Sea, a transport in ballast water was hypothesized; a possible alternative is the existence in the Mediterranean of this species of Acropomidae, perhaps till now confused with bathyal Apogonid fishes belonging to the genus Epigonus. The fourth case of transported species is represented by two specimens of the South American fish Pinguipes brasilianus, the first one collected at Messina in March 1990, photographed, but not preserved, and the second one sampled in the Ligurian Sea in October of the same year. This latter specimen, included by Torchio in the collection of the Civica Stazione Idrobiologica of Milan, allowed the study of the two cases (Orsi Relini, 2002). These records occurred not only at a great distance from their possible origin, South American waters, but also in two different localities of the Mediterranean about 900 km apart, both important in terms of maritime traffic. A small specimen (12 cm) of the Orange Spotted grouper Epinephelus coioides was captured in the Gulf of Trieste in May 1998 and maintained alive at the civic Marine Aquarium of Trieste. After three years it measured more than 50 cm (Parenti and Bressi, 2001). The authors suggested an occasional transport from the Eastern Mediterranean, given that previous records were found only in the coast of Israel. Probably in this case the survival and growth of this tropical species was assured by its life in captivity, because during winter the sea temperatures of the North Adriatic are the most severe of the Italian Seas (see Fig. 5). Other Indo-Pacific species recorded far from natural distribution with only one specimen, besides the already mentioned Pampus argenteus, are Elates ransonnettii found in the Gulf of Taranto (Mastrototaro et al., 2007) and Terapon therapes (Lipej et al., 2008), caught alive North of Piran, in the Gulf of Trieste. This fish, found in Slovenian waters, is mentioned here because the traffic of the near harbor of Trieste is the most probable reason for its presence, as well as for the case of Epinephelus coioides.

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At present the records of Indo-Pacific fish in the Adriatic number 11 species, 9 of which were recorded on the basis of only one specimen (Dulčić and Pallaoro, 2003; Lipey et al., 2008; Ungaro et al., 2004). Records occurred mainly on the eastern coast, where the main current flows northward from the Greek Ionian Sea. In all Greek waters, Erythrean fish number 28 species, 10 of which are considered casual (Corsini – Foka and Economidis, 2007). In the Adriatic, the three species appeared near Istrian ports and are clearly separated from the others, as shown by the map of the records (Dulčić and Pallaoro, 2003). The introduction of fish species by maritime traffic is particularly evident where ichthyologists have the chance to observe marine life inside a large port, in particular at the dry docks (Relini Orsi and Mori, 1979). This problem was faced about one century ago by Parona, at the University of Genoa, where a docker brought a smooth trunkfish Lactophrys triqueter (Fig. 2) collected inside the harbour. After an exhaustive study of the available literature, Parona (1909) excluded the Ostraciidae from the Mediterranean fauna (as a matter of fact they appeared in 1988, with an Erythrean species, Tetrosomus gibbosus, see Golani et al., 2002) and linked the presence of the fish to a ship transport, reporting similar findings at Nice, where Risso (1826), obtained his specimens “aprés l’apparition d’un vaisseau de commerce dans nos parages”. So the problem appeared at least another century ago, during the age of sailing navigation, but, at the same time, this could be true also for more ancient periods. In fact, the port of Genoa, as many others in the Mediterranean, has at least 3000 years of active life: it is interesting to recall that botanists are able to relate the distribution of relevant

Fig. 2. Lactophrys triqueter: specimen collected inside the port of Genoa on 12 February 1909 and studied by Parona (1909).

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plant species (both marine and terrestrial) to the routes of ancient Phoenician and Greek vessels. In contrast to plants, however, the present six species of ship transported fish (Table 1) have had no impact on Mediterranean ecosystems. Since then, many exotic fish species (and of course other taxa) have been found inside Italian harbors, but generally they were not taken into account as a subject eligible for deeper studies. This approach was possibly suggested by the fact that life expectancy of exotic species was assumed to be short, only a few months at best. At present, in the name of biodiversity, the approach to NIS (Non Indigenous Species) has changed and frequently the risk is to assign them roles they cannot perform. If someone used scraped fouling (from an Australian vessel!) to list alien species in the Mediterranean (Galil, 2008), the risks of confusions and misunderstandings are relevant. DRIFT FISH Species of the families Centrolophidae and Nomeidae are poorly known and their presence in the Mediterranean may be undervalued. These fish present very peculiar life histories, with a juvenile phase in offshore surface waters, lasting several months to more than one year; thereafter the fish reaches the bottom, frequently in rocky areas at great depths (canyons and sea mounts) where it grows to size of about 80-100 cm (at what age is scarcely known). The juvenile is associated with flotsam or to cnidarians and a feeding on macroplankton, especially on jellyfish, is characteristic of all phases of life. The name “medusafish” (Haedrich, 2002) expresses these characteristics. Haedrich (1986) determined the following distributions: Schedophilus ovalis: all of the Mediterranean; Centrolophus niger: Western and Central Mediterranean; Schedophilus medusophagus and Cubiceps gracilis: Western Mediterranean. Similarly, in the CIESM Exotic Fish Atlas (Golani et al., 2002) Psenes pellucidus was reported as an Atlantic invader, appearing in the waters of Algeria, Morocco, Spain and France. This species was mentioned also in Italian waters at Messina (East Sicily) albeit in local journals (Costa and Fanara, 1994; Berdar et al., 1995). More recently it was found in Sardinia (Follesa et al., 2006) and another time near Messina (Navarra et al., 2007). Generally the records are represented by young fish, but one of the most recent, a specimen of 38 cm TL caught at 600 m,, shows an adult profile (Follesa et al., 2006). In general, recent studies have largely expanded the distributions of drift fishes in the Mediterranean. Karrer (1986) ascertained that a small fish, collected near Marseille and described by Moreau (1881) with the name Centrolophus valenciennesi, was Hyperoglife perciformis (Mitchell, 1815), a species found on the east coast of North America, from Florida to Nova Scotia. Given that Centrolophidae are characterized by fast growth, she noted that the fish, of only 15 cm TL, the smallest found in European waters, could not be interpreted as a stray from the Western Atlantic, but it was probably native in the area. The same remark could be said also of P. pellucidus. Is this species a recent colonizer?

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Having explored worldwide collections, including that of the Natural History Museum of Genoa, Karrer (1986) confirmed also the correct identification of a very large specimen (1.07 m) of Cubiceps found at Alassio (Western Liguria Riviera) as Cubiceps capensis (Fig. 3), according to the statement of Ariola (1912) who had described the record. Was this fish a deep sea straggler? Due to such uncertainties and difficulties of regular sampling, the group of drift fishes remains hard to classify. FISH ENLARGING THEIR DISTRIBUTION IN THE NORTH ATLANTIC IN RELATION TO OCEAN WARMING AND MEDITERRANEAN COLONIZERS Since the 1960’s a series of fish inhabiting a tropical-subtropical belt of the Eastern Atlantic have begun to appear in European waters, advancing northward from Portugal (Saldanha, 1968 – Fig. 4; Costa and Reiner, 1978) to northern Spain (Banon Diaz and Casas Sanchez, 1997; Banon Diaz et al., 1997; Banon et al., 2002; Banon and Garazo, 2006), to the Bay of Biscay and northern France (Du Buit and Quero, 1993; Quero and Laborde, 1996; Quero et al., 1997) and to the British Isles (Wheeler et al., 1985; Wheeler, 1986). Quero (1998) reviewed thirty years of observations, assembling 123 records belonging to at least 18 different species and mapped the distribution of the main species, observing the times of their displacements. Available hydrological data failed to cover the complete extension of the new geographical distributions of the studied fishes. However, there are indications of a warming process of surface waters, mainly in the Bay of Biscay; moreover they showed a very important increase of temperature (2 °C during a 20 years period, from 1972 to 1992) in the current which flows from South to North along the upper slope. Fishes were assigned to three ecological groups. Species living on

Fig. 3. Cubiceps capensis: the specimen collected at Alassio, Western Ligurian Riviera, studied by Ariola (1912).

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the upper slope, between 200 and 600 m (Zenopsis conchifer, Cyttopsis roseus, Chaunax spp., Sphoeroides pachygaster) were the most abundant, with 68.3 % of the specimens. Species living in surface waters, generally at depth less than 200 m (Tarpon atlanticus, Seriola dumerili, S. rivoliana, S. carpenteri (only one record), Lichia amia, Pomatomus saltator, Aluterus monoceros and Pisodonophis semicinctus) constituted 19.5% of the studied group. The third ecological category included five species living on the mid-slope between 900 and 1300 m: these species (Hoplostethus cadenati, Allocyttus verrucosus, Dibranchus atlanticus, Diretmoides parini, Lamprogrammus niger) reached the most northerly latitudes, surpassing northern Scotland. Seven non native species recorded in Italian waters (Table 1) belong to the groups listed by Banon-Diaz et al. (1997) and Quero (1998): Halosaurus ovenii (by Cau and Deiana, 1979); Sphoeroides pachygaster (by Vacchi and Cau, 1985-1986; Barletta and Torchio, 1986); Chaunax suttkusi (by Ragonese and Giusto, 1997; Ragonese et al., 2001); Pisodonophis semicinctus (by Insacco and Zava, 1999; Ragonese and Giusto, 2000; Serena, 2001); Seriola carpenteri (by Pizzicori et al., 2000); Seriola rivoliana (by Castriota et al., 2002); Zenopsis conchifer (by Ragonese and Giusto 2007). These records in Italian seas occurred throughout a long period (1979-2007); their times of appearance, in Italian waters generally do not correspond to those of the NE Atlantic, probably indicating the casualness of the introduction of these fishes from

5 cm

Fig. 4. Young specimen of Zenopsis conchifer, found in 1966 in Portuguese waters (Saldanha, 1968). This record represents the first documentation of the long northward displacement of this species (Quero, 1998).

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Gibraltar. Moreover they are very different in terms of specimens involved (Table 1): in fact, among species represented by one or two specimens, there are two species whose records reach hundreds of individuals, indicating a successful invasion. In particular, 148 specimens of Seriola carpenteri were caught in September 1997 during a research survey onboard commercial vessels, at night, at 20 m depth on the African shelf, about 42 nautical miles east of Lampedusa. All specimens, dark pink in color, were adults in their reproductive phase (running gametes). Fishermen reported a similar daytime capture of 20 individuals in August 1996 (Pizzicori et al., 2000); thus, this species can be considered established in the Mediterranean. Sphoeroides pachygaster was found in all Italian seas (Vacchi and Cau, 1985; Barletta and Torchio, 1986; Fiorentino and Zamboni, 1990; Ragonese et al., 1992; Tursi et al., 1992; Bello, 1993; Arculeo et al., 1994; Bedini, 1998, Ligas et al., 2007) in the majority of cases with single individuals. The first records in Italian waters were in both northern and southern locations, Sardinia and Sicily Strait (Vacchi and Cau, 1985, 1986) and the Ligurian Sea (Barletta and Torchio, 1986). Moreover, a collection of 403 specimens of S. pachygaster was assembled in the period 1990-1994 by trawling in the Sicily Strait (Ragonese et al., 1997). Such numbers suggest that the Smooth Puffer probably arrived in the Sicily Strait prior to the date of the first record in the Mediterranean by Oliver (1981) at Balearic Islands (Ragonese et al., 1992). Older Italian literature mentions a puffer fish, very abundant on the coast of Egypt (Salviani, 1558): in the dedicated table the fish presents strong similarities with S. pachygaster. If the figured fish was really S. pachygaster, we can suppose at least recurrent invasions, related to climatic oscillations (Relini and Orsi Relini, 1995) or, alternatively a permanent presence in the southern Mediterranean. On the other hand, a displacement of this species from west to east in the Mediterranean seems very clear (Golani et al., 2002; Psomadakis et al., 2006) and in the eastern Atlantic a latitudinal range of 16° was covered by this species in a very short time (Quero, 1998). Other Atlantic immigrants could be associated with the same Atlantic warming, such as Seriola fasciata and Sphoeroides marmoratus. However, S. fasciata was never mentioned in the pool of species moving northward and its distribution remains unclear due to possible confusion with S. carpenteri (Smith-Vaniz, 1986); the hypothesis of a restricted distribution East Atlantic (Madeira) – Mediterranean was also mentioned at the occasion of the first record (Massutì and Stefanescu, 1993); the fish could have been native, but went unrecognized given its great similarity to other species of Seriola. At present, S. fasciata is considered established in the Mediterranean, with records from Spain, France, Italy, Tunisia and Greece. Sphoeroides marmoratus is placed among unclassified species (see below). Another Atlantic species, living in deep water, could be a new invader; it is not listed in the above mentioned group because it is fished normally from Macaronesia to the Bay of Biscay, namely Beryx splendens. In the Macaronesian area B. splendens is fished together with Beryx decadactilus, the only species of the same genus previously

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found in the Western Mediterranean (Maul, 1986), with very rare and old records in Spain, France and Italy. B. splendens was recently found in the Ligurian Sea three times. The first specimen was fished in Nice and not preserved, but a series of photographs allowed its identification (Gavagnin et al., 1992); the second was caught in 1993 by trawl at 630-640 m, on red shrimps fishing grounds near Portofino (Orsi Relini et al., 1995); the third, unpublished, has the same origin as the latter. This author was also informed of the capture of another specimen in Calabrian waters. On the basis of such records, the species could be considered as established in the Italian Seas, where however it remains uncommon. ERYTHREAN COLONIZERS Having left aside questionable cases (Torchio, 1968) and all fish found inside dry docks, ten Indo-Pacific fish species appeared in Italian waters (Table 1); paying attention to numbers of specimens mentioned in Italian literature, it is clear that Fistularia commersonii and Siganus luridus are Erythrean colonizers for certain; a third species, Etrumeus teres, may be added soon, while a fourth one, in part recorded by photographs, remains unclassified (see below). Fistularia commersonii represents the most intriguing case among the exotic fish listed in Table 1 and in the Mediterranean in general. In fact, it first appeared in January 2000 in Israel (Golani, 2000) and by November-December 2007 it was recorded as present both in northern and southern Spanish waters (Sanchez-Tocino et al., 2007) having travelled the entire Mediterranean. In particular, the observation of several individuals in Berenguel Bay, near Gibraltar, suggests the possibility that at present, i.e. during 2008, it may have reached the Atlantic. In Italian waters it was recorded south of Lampedusa in November 2002 (Fiorentino et al., 2004) and in the coastal waters of this island in December 2002 (Azzurro et al., 2004). Only a few months earlier several individuals were collected in Tunisian waters (Ben Souissi et al., 2004). The Tyrrhenian Sea was reached in 2003 (Pipitone et al., 2004), the north Tyrrhenian in 2004 (Micarelli et al., 2006); the western Tyrrhenian in 2005 (Pais et al., 2007) while tens were sampled on the east side of the same sea (Psomadakis et al., 2008); the Adriatic in 2006 (Dulčić et al., 2008) and the Ligurian Sea in 2007 (Garibaldi and Orsi Relini, 2008). Apparently main surface water circulation of the western Italian Sea, the Tyrrhenian and the Ligurian Sea, could be related to the progression of this invader (Garibaldi and Orsi Relini, 2008): however at present the great number of specimens found in Algeria, where F. commersoni is the only Indo-Pacific fish recorded (Kara and Oudjane, 2008), suggests the ability of this species to move also against the main currents, probably taking advantage of coastal countercurrents. Given the wealth of available material, F. commersonii was the object of studies of general value about fish invasions. Golani et al. (2007b) comparing specimens caught in Israel, Turkey, Greece and Italy with fish of the natural range, from the Pacific Ocean to

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the Red Sea, found that the Mediterranean invaders presented a genetic bottleneck, which proves that the invasion resulted from the reproductive success of very few individuals; it seems that all the fish sampled in the period 2003-2006 could be related to only two females. Pais et al. (2007), studying the parasites of a specimen caught in Sardinia during 2005, found the genus specific trematode Allolepidapedon fistulariae; this worm has a very complex life history in terms of larval stages, so the record seemed to suggest displacements of adult fish instead of those of eggs and larvae. F. commersonii is a noxious invader. In the Greek isle of Rhodes it appeared in 2001 and developed an important population in only a few years, so that recently any trawl net operation, generally at 20-25 m depth, catches 5 to 20 specimens (Corsini-Foka and Economidis, 2007). The species presents an extreme feeding activity and a clear aggressive behavior when in schools. It mainly feeds on valuable native fish (Spicara smaris, Mullus sp. and Boops boops), being itself of no or little commercial value (Corsini-Foka and Economidis, 2007; Kalogirou et al., 2007). To the best of this author’s knowledge, at present in Italian waters the presence of Fistularia in the form of a local population, consisting of both adults and young fish, is located and limited to the Strait of Sicily, which is the locality of its first appearance, in the autumn of 2002. The second successful Erythrean invader is the rabbitfish Siganus luridus (see: Azzurro and Andaloro, 2004) an herbivorous species deeply studied and monitored in the Eastern Mediterranean (Golani et al., 2002). Tens of individuals were sampled in 2003 for study at the isle of Linosa (Pelagie Islands, in the Sicily Strait). Both juveniles and adult fully mature individuals were available and were used to study reproductive aspects, feeding habits and genetic diversity (Azzurro, 2006; Azzurro et al., 2006; Azzurro et al., 2007a and b). This fish’s presence was also recorded at the neighboring isle of Lampedusa. More recently, a single specimen was recorded in northern Sicily (Tyrrhenian Sea) (Castriota and Andaloro, 2005). At Linosa the fish was not present in the summer of 1999, when the invasive crab Percnon gibbesi was observed for the first time in Italian waters (Relini M. et al., 2000; personal communication). Thus, the colonization of the rocky shores of this small vulcanic isle by the rabbitfish is considered to have commenced later. At the time of the above mentioned sampling, Siganus luridus was abundant, but in a secondary position vis-a-vis the local herbivorous fish species, Sarpa salpa and Sparisoma cretense (Azzurro, 2006). Now that five years have elapsed, a new check of the relationship among these species should be of great interest, given that in rocky habitats of the Israeli Mediterrnean coastline, the two species of rabbitfish (S. luridus and S. rivulatus) represent a third of the total fish biomass (Goren and Galil, 2005). In all of the Levant, rabbitfish constitute a portion of the captures by trammel net and purse seines; in Greek waters as well, rabbitfish have acquired commercial importance (Corsini-Foka and Economids, 2007). A single specimen of Etrumeus teres was recorded off Lampedusa Island in September 2005 (Falautano et al., 2006); the authors could not ascertain if other specimens

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of this species were present in the purse seine catch. Given that the dynamics of little pelagic fish are rapid and this species is gaining commercial interest in Greek waters (Kasapidis et al., 2007) we can expect that Etrumeus teres may soon become established in the southern Italian waters. OTHER UNCLASSIFIED FISH OF TABLE 1 Sphoeroides marmoratus Only one specimen was caught in 1977 off Gallipoli (Ionian Sea). The fish was preserved in the Marine Biology Station of Porto Cesareo, misidentified as Lagocephalus lagocephalus, and only recently was recognized as S. marmoratus (Vacchi et al., 2007). Another two records of this species occurred recently (2004 and 2005) in southern Spain, but the presence of the fish in the Mediterranean remains occasional, especially if compared with the quick diffusion of S. pachygaster. Stephanolepis diaspros This species is quite common in all of the Levant Sea and in Tunisia, but has been found less frequently around Sicily and in the north Ionian Sea (Golani et al., 2002): Bradai et al. (2004) reported a capture of 133 specimens by trawl in the Gulf of Gabes during December 1998. Three records of this species occurred in Italian waters: two specimens were fished at Porto Cesareo (Ionian Sea), one of which studied by Tortonese (1967); another two in the Gulf of Palermo (South Tyrrhenian) in July 1983 (Catalano and Zava, 1993); in the same paper B. Zava reports the underwater observation of a young individual that occurred at Lampedusa in September 1986, while, more recently, a large fish was photographed at Pantelleria (Pipitone and Badalamenti, pers. comm., 2001). Even if other occasional observations by divers are reported, the distribution of this fish in South Italy, after so many years after the first occurrence, remains unclear. Other difficulties derive form the fact that the Atlantic species Stephanolepis hispidus is scarcely distinguished from the present one (Tortonese, 1986). DISCUSSION The appearance and establishment of alien species in the Mediterranean is considered to be part of global changes, in which human activities and climatic events are interlaced (Occhipinti-Ambrogi, 2007). Climatic trends of the last decades have already been mentioned (Fig. 1). Maximum increases of temperature registered in the Mediterranean are about 1° C in the last 30 years at surface, 0.2° C in the period 1970-92 in intermediate water and 0.13° C

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in 35 years in deep waters (Bethoux and Gentili, 1996), the latter clearly less than those indicated by Quero (1998) for warming in the eastern Atlantic. In the up-to-date debate about changes in Italian seas, between the two main factors related to NAO oscillations, namely, increase in temperature and decrease of rainfall, the latter appears to be the more important, particularly in the Adriatic, where the input of the Po river in the last few years has noticeably decreased, causing modifications in the sea water chemistry. As far as fish are concerned, several studies were addressed to species living in surface coastal waters which have been considered biological indicators of global warming (Francour et al., 1994) and/or “tropicalization” of the sea (Andaloro and Rinaldi, 1998; Bianchi and Morri, 2003; Bianchi, 2007). In French marine protected areas of the Ligurian Sea (Port-Cros National Park, Natural Reserve of Scandola, Corsica) there was evidence of the increased presence of Thalassoma pavo, Epinephelus marginatus, Balistes carolinensis (= B. capriscus), Pomadasys incisus, Sphyraena sphyraena (in the author’s opinion, probably S. viridensis), as well as, in the Gulf of Lion, the appearance of uncommon species in the local fishery products, such as Diplodus cervinus cervinus, Pomatomus saltator, Solea senegalensis, and Sphoeroides pachygaster (Francour et al., 1994). Parallel observations occurred in the Italian waters of the Ligurian Sea with the record of Sphoeroides pachygaster (Barletta and Torchio, 1986) and Pomadasys incisus (Gavagnin et al., 1993). A specific study was addressed to Sphyraena spp. in order to clarify if native or alien species were involved (Relini and Orsi Relini, 1997). In the last decade in Italy several studies were dedicated to T. pavo (Vacchi et al., 1999; Guidetti, 2002; Guidetti et al., 2002; Sara et al., 2005) and Sparisoma cretense (Guidetti and Boero, 2001), mainly to study recruitment processes in the extended latitudinal range. The monitoring of coastal fisheries in the Gulf of Genoa at the end of the 1990’s, thanks to the survival of a tuna trap of ancient Liguro-Provençal type at Camogli (see box, below), allowed to compare recent data with those of 40 years earlier (Relini M., 2001). These data are quantitative, representing total catches per fishery season (AprilSeptember), i.e. CPUE, that are a proxy of abundance indices. The unprecedented success of Seriola dumerili (this species was not placed in the first top ten in the past, yet it reached the first position by the end of the 1990’s), the remarkable increase of Trachurus spp. of the same family (Carangidae), the regression of Scomber scombrus, a temperate boreal species (recorded also in the Adriatic, see Dulčić et al., 1999), its replacement by Scomber japonicus, a temperate-tropical species, are all manifestations (and also measures) of the changes occurring in the coastal fish assemblages of the Ligurian Sea (Relini M., 2001). To what extent does the study of exotic fish species contribute to our understanding of such processes? In a relatively small sample of alien fish species (N=27) found in Italian waters, this author has tried to establish categories useful for identifying the most significant occurrences. If we set apart vagrant fish (N=6), ship transported fish (N=6),

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and some poorly known species, we remain with the species which are responding to large scale climatic events. Some of these species are colonizing the Italian Seas. In fact, we face at least three species of tropical Atlantic origin, S. pachygaster, S. fasciata and S. carpenteri, which are becoming established in Italian waters. In the same manner we find two established Erythrean species, Fistularia commersonii and Siganus luridus, and the clupeid Etrumeus teres which could be the next successful colonizing species. So, the balance between West and East is maintained. These established species represent, in the most direct way, the tropicalization of the central Mediterranean; in the Levant the process is so advanced that half of the fishery products consist of Erythrean species (Golani and Ben-Tuvia, 1995; Goren and Galil, 2005). However, the tropicalization of the Italian Seas, in terms of the establishment of an exotic ichthyofauna, with both benthic and pelagic components, has been recorded in a very limited area of sea water surrounding Lampedusa and Linosa. Why there? First of all, the Sicily Strait is directly reached by Atlantic waters entering the Mediterranean from Gibraltar; moreover, after Cape Bon the main surface current, given the sudden enlargement of space, slows down and break up in numberless veins of variable direction (Poulain and Zambianchi, 2007). These characteristics seem very favorable to species coming from the west. On the other side, winter temperatures of the Strait of Sicily on the African coast are higher than those of the northern section of the Strait (Millot, 2005; see Fig. 5) and therefore favorable to all tropical species, independent of their origin. Looking at the main geomorphological characteristics of the Pelagie islands (Lampedusa, Linosa, Lampione with an area of about 20, 5 and 1 km2 respectively), Linosa is very different form the other two, being the top of a volcanic complex born about 300.000 years ago on the margin of the African platform (Massoli-Novelli, 2004).

Fig. 5. Winter temperatures in the Mediterranean (Millot, 2005).

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Changes in coastal fish assemblages The Ligurian Sea has an excellent observation post for the monitoring of changes in coastal fish assemblages: the tuna trap of Camogli, at present located in the Marine Protected Area of Portofino. The trap is a “tonnarella” i.e. a type of gear which some centuries ago in the LiguroProvencal basin was used to target bluefin of the age one-four years, typical of this area. This trap, the last surviving in the NW Mediterranean, is active from April to September and at present catches several coastal species (about 40 of them form an annual commercial landing of about 50 tons) but not bluefin. The total annual catches of the peAnnual catches a Tons riod 1956-1960 and Tons 80 those of 1996-2000 70 are shown in Fig. a. 60 The annual fish50 ery product appear 40 30 increased in recent 20 times, probably indi10 cating an amelioration 0 of fishing technics. 1956 1957 1958 1959 1960 1996 1997 1998 1999 2000 The composition of Top ten species the catches (limited b to the ten top species) Seriola is shown in Fig. b: dumerili Seriola dumerili, absent Auxis rochei in the past top ten, at the end of the 1990’s Trachurus gains the first position spp. and other carangids Scomberesox fish (Trachurus spp.) saurus shows a very large inBoops boops crease; the temperate1956-1960 boreal Scomber scom1996-2000 Sarda sarda brus is replaced by the temperate-tropical S. Scomber japonicus japonicus.The two species of sparids Sarpa Mola mola salpa and Boops boops show a moderate inSarpa salpa crease and decrease respectively, accordScomber scombrus ing to their major or minor tropical affinity 0 2 4 6 8 10 12 14 16 18 (Relini M., 2001). Tons

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Given its fertile soil, this isle is “green” compared to the others; we can assume that marine plants also take advantage of a young fertile substratum. Two alien herbivorous species, the invasive atlantic crab Percnon gibbesi (Galil et al., 2002) and Siganus rivulatus settled their new Italian populations here, the former finding the launching pad for the conquest of a large part of the Mediterranean. Lampedusa is located about 200 km from Sicily and only 120 km from Tunisia. It is part of the African platform, where water depths do not surpass 120 m. These waters are famous for the abundance of fish and canning industries are present on the isle. The exotic and F. commersonii apparently found here a convenient piscivorous species of Seriola setting. Such successful invasions appear to be in some way equilibrated, including both primary and secondary consumers. Future concern based on Greek experiences (Corsini Foka and Economidis, 2007) may be in regard to F. commersonii, but the increased native as well as exotic piscivorous fish may also be able to take advantage of new prey. In conclusion, large scale climatic factors are changing fish distribution: we do not know yet if the changes are only oscillations or if the process is irreversible. Seen from the Levant and ignoring the role of new Atlantic species, the diffusion of Erythrean fish seems to be part of a dramatic sequence of events, mainly of anthropic origin, which is threatening the Mediterranean identity (Galil, 2008); seen from the majority of the Italian seas, till now the combat between Atlantic and Indo-Pacific colonizers appears to be a skirmish played only far south on the edge of the African shelf. ACKNOWLEDGEMENTS I would like to thank Dr. Fulvio Garibaldi and Dr. Luca Lanteri for their help in the preparation of the text and search for literature. Having reported some anedoctal facts and opinions of many years ago, I gratefully remember my teachers of ichthyology when I was a first year biology student, Giuseppe Scortecci and Enrico Tortonese, as well as Menico Torchio, who was not only my teacher but also a brotherly friend of my family; I also thank the Editors for improving my manuscript. REFERENCES Andaloro, F. and A. Rinaldi. 1998. Fish biodiversity change in Mediterranean Sea as tropicalisation phenomenon indicator. In: Enne G., M. D’Angelo and C. Zanolla. (eds.) Indicators for assessing desertification in the Mediterranean. Rome: Agenzia Nazionale per la Protezione dell’Ambiente pp. 201-206. Arculeo, M., S. Riggio and G. D’Anna. 1994. First record of Sphoeroides pachygaster (Tetraodontidae) in the South Tyrrhenian (N/W Sicily). Cybium 18 (2): 208-209. Ariola, V. 1912. Nuovo pesce abissale del Golfo di Genova (Cubiceps capensis Smith). Rivista Mensile di Pesca e Idrobiologia, Pavia 7: 185-192 .

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Azzurro, E. 2006. Fish biodiversity changes in the Mediterranean sea: cases of study. PhD Thesis, Università Politecnica delle Marche, Ancona, Italy. 238 pp. Azzurro, E. and F. Andaloro. 2004. A new settled population of the lessepsian migrant Siganus luridus (Pisces: Siganidae) in Linosa Island – Sicily Strait. ). Journal of the Marine Biological Association of the United Kingdom 84: 819-821. Azzurro E., E. Fanelli, E. Mostarda, M. Catra M. and F. Andaloro. 2007a. Resource partitioning among early colonizing Siganus luridus and native herbivorous fishes at Linosa Island. Evidence from gut-content analysis and stable isotope signatures. Journal of the Marine Biological Association of the United Kingdom 87: 1-8. Azzurro E., O. Carnevali, M. Bariche and F. Andaloro. 2007b. Reproductive condition in the non-native Siganus luridus (Teleostei, Siganidae) during early colonization at Linosa Island (Sicily-Strait, central Mediterranean Sea). Journal of Applied Ichthyology 23: 640-645. Azzurro E., D.Golani, G. Bucciarelli and G. Bernardi. 2006. Genetics of the early stages of invasion of the Lessepsian rabbitfish Siganus luridus. Journal of Experimental Marine Biology and Ecology 333: 190-201. Azzurro, E., F. Pizzicori and F. Andaloro. 2004. First record of Fistularia commersonii (Fistulariidae) from the Central Mediterranean. Cybium 28: 72-74. Bañón, R., J.D. Del Rio, C. Piñeiro and M. Casas. 2002. Occurrence of tropical affinity fish in Galician waters, north-west Spain. Journal of the Marine Biological Association of the United Kingdom 82: 877-880. Bañón, R. and A. Garazo. 2006. Presencia de medregal negro Seriola rivoliana Valenciennes, 1833 y barracuda Sphyraena sphyraena (Linnaeus, 1758) (Perciformes) en la costa de Galicia. Nova Acta Científica Compostelana. Bioloxía 15: 95-97. Banon Diaz, R. and J.M. Casa Sanchez. 1997. Primera cita de Caranx crysos (Mitchill, 1815) en aguas de Galicia. Boletin del Instituto Espanol de Oceanografia 13 (1-2): 79-81. Banon Diaz, R., J.M. Casa Sanchez, C.G. Pineiro Alvarez and M. Covel. 1997. Capturras de peces de afinidades tropicales en aguas atlanticas de Galicia (noroeste de la penisula Iberica). Boletin del Instituto Espanol de Oceanografia 13 (1-2): 57-66. Barletta, G. and M. Torchio. 1986. Segnalazione di Bathypterois Gunther e di Sphoeroides Lacepède in acque imperiesi (Mar Ligure) (Osteichthyes). Quaderni della Civica Stazione Idrobiologica di Milano 13: 31-34. Bedini, R, 1998. First record of Sphoeroides pachygaster (Tetraodontidae) from the northern Tyrrhenian Sea. Cybium 22: 94-96. Bello, G. 1993. Il pesce palla Sphoeroides cutaneus nel mare Adriatico. Memorie di Biologia Marina e di Oceanografia 18: 75-77. Ben Souissi, J., J. Zaouali, M.N. Bradai and J.P. Quignard. 2004. Lessepsian migrant fishes off the coast of Tunisia. First record of Fistularia commersonii (Osteichthyes, Fistulariidae) and Parexocoetus mento (Osteichthyes, Exocoetidae). Vie et Milieu 54: 247-248. Ben-Tuvia, A. 1966. Red Sea fishes recently found in the Mediterraenan. Copeia (1966) 2: 254-275. Berdar, A. D. Capecchi, F. Costa, D. Giordano, G. Mento and B. Spalletta. 1995. Pesci parassiti e pseudoparassiti dei mari italiani. [Fish parasites and pseudoparasites of Italian seas.] Rivista di parassitologia 12: 454-465. Bethoux, J.P. and B. Gentili. 1996. The Mediterranean Sea, coastal and deepsea signatures of climatic and environmental changes. Journal of Marine Systems 7: 383-394.

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Dulčić, J. and A. Pallaoro. 2003. Lessepsian fish migrants reported in the Eastern Adriatic Sea: an annotated list. Annales, Series historia Naturalis 13 (2): 137-144. Dulčić, J., B. Grbec and J. Lipej. 1999. Information on the Adriatic ichthyofauna-effect of water warming? Acta Adriatica 40 (2): 33-43. Dulčić, J., G. Scordella and P. Guidetti, P. 2008. On the record of the Lessepsian migrant Fistularia commersonii (Rüppell, 1835) from the Adriatic Sea. Journal of Applied Ichthyology 24: 101-102. Falautano, M., L. Castriota and F. Andaloro. 2006. First record of Etrumeus teres (Clupeidae) in the Central Mediterranean Sea. Cybium 30: 287-288. Fiorentino, F. and A. Zamboni. 1990. Ritrovamento di Epigonus constanciae (Giglioli, 1880) e nuove catture di Sphoeroides cutaneus (Günther, 1870) in Mar Ligure. Oebalia (Supplemento) 16: 659-661. Fiorentino, F., G.B. Giusto, G. Sinacori and G. Norrito. 2004. First record of Fistularia commersonii (Fistulariidae, Pisces) in the Strait of Sicily (Mediterranean). Biologia Marina Mediterranea 11: 583-585. Follesa, M.C., S. Cabiddu, A. Sabatini and A. Cau. 2006. First record of Psenes pellucidus (Perciformes, Actinopterygii) in the Sardinian waters (Central Western Mediterranean). Acta Ichthyologica et Piscatoria 36 (1): 77-79. Francour, P., C.F. Boudouresque, J.-G. Harmelin, M.L. Harmelin-Vivien and J.P. Quignard. 1994. Are the Mediterranean waters becoming warmer? Information from biological indicators. Marine Pollution Bulletin 28: 523-526. Frantiz, A., O. Nikolaou, J.M. Bompar and A. Camedda. 2004. Humpback whale (Megaptera novaeangliae) occurrence in the Mediterranean Sea. Journal of Cetacean Research and Management 6: 25-28. Galil, B.S., 2008. Alien species in the Mediterranean Sea – which, when, where, why? Hydrobiologia 606:105-116. Galil, B., C. Froglia and P. Noël. 2002. CIESM Atlas of exotic species in the Mediterranean. Crustaceans: Decapods and Stomatopods Vol. 2, Briand F. (ed.). Monaco: CIESM Publishers. 192 pp. [available at ]. Garibaldi, F. and L. Orsi Relini. 2008. Record of the bluespotted cornetfish Fistularia commersonii Rüppel, 1838 in the Ligurian Sea (NW Mediterranean). Aquatic Invasions 3 (4): 359-362. Gasparini, G.P. and M. Astraldi. 2002. Experimental evidence of the interannual variability of currents in two Mediterranean straits: the Straits of Sicily and the Corsica Channel. In: CIESM, Workshop Series no 16. Tracking-long-term hydrological change in the Mediterranean Sea, Monaco. 134 pp. Gavagnin, P., F. Garibaldi, L. Orsi Relini and G. Palandri. 1992. Cattura di un raro pesce bericiforme nelle acque profonde del Mar Ligure. Oebalia 17 (2 supplemento): 57-60. Gavagnin, P., M. Relini and F. Garibaldi. 1993. Segnalazione di Pomadasys incisus (Bowdich) (Haemulidae, Osteichthyes ) in acque italiane. Biologia Marina Mediterranea 1 (1): 285-286. Golani, D. 2000. First record of the bluespotted cornetfish from the Mediterranean Sea. Journal of Fish Biology 56: 1545-1547. Golani, D. and A. Ben-Tuvia. 1995. Lessepsian migration and the Mediteranean fisheries of Israel. In: Armantrout, N.B. (ed.) Conditions of the world’s aquatic habits. Proceedings of the World Fisheries Congress. Theme I. New Delhi: Oxford & IBH Publication Co. Pvt. Ltd. pp. 279-289. Golani, D., L. Orsi Relini, E. Massutí and J.-P. Quignard. 2002. CIESM Atlas of exotic species in the Mediterranean. Vol. I. Fishes. F. Briand (ed.). Monaco: CIESM Publisher. 254p.

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Golani D., L. Orsi Relini, E. Massutí and J.-P. Quignard. 2004. Dynamics of fish invasions in the Mediterranean: update to the CIESM fish atlas. Rapport du 37e Congrès de la Commission Internationale pour l’Exploration scientifique de la mer Méditerranée 37: 367. Golani, D., L. Orsi Relini, E. Massutí, J.-P. Quignard and J. Dulčić, 2007a. Fish invasion of the Mediterranean – retrospective and prospective. Rapport du38e Congrès de la Commission Internationale pour l’exploration scientifique de la mer Méditerranée 38: 10. Golani, D., E. Azzurro, M. Corsini-Foka, M. Falautano, F. Andaloro and G. Bernardi. 2007b. Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant. Biology Letters 3: 541-545. Gonzales, M., M. Fernandez-Casado, M. Pila Rodriguez, A. Segura and J.J. Martin. 2000. First record of the giant squid Architeuthis sp. (Architeuthidae) in the Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 80: 745-746. Goren, M. and B.S. Galil. 2005. A review of changes in the fish assemblages of Levantine inland and marine ecosystems following the introduction of non native fishes. Journal of Applied Ichthyology 21: 364-370. Guidetti, P. 2002. Temporal changes in density and recruitment of the Mediterranean ornate wrasse Thalassoma pavo (Pisces, Labridae). Archive of Fishery and Marine Research 49: 259-267. Guidetti, P. and F. Boero. 2001. Occurrence of the Mediterranean parrotfish Sparisoma cretense (Perciformes: Scaridae) in south-eastern Apulia (south-east Italy). Journal of the Marine Biological Association of the United Kingdom 81: 717-719. Guidetti, P., C.N. Bianchi, G. La Mesa, M. Modena, C. Morri, G. Sara and M. Vacchi. 2002. Abundance and size structure of Thalassoma pavo (Pisces: Labridae) in the western Mediterranean Sea: variability at different spatial scales. Journal of the Marine Biological Association of the United Kingdom 82 (3): 495-500. Haedrich, R.L. 1986. Centrolophidae. In: Whitehead, P.J.P., M.L. Bauchot, J.C. Hureau, J. Nielsen and E. Tortonese E.(eds.) Fishes of the north-eastern Atlantic and Mediterranean. Vol.3. Paris: UNESCO. pp. 1177-1182. Haedrich, R.L. 2002. Centrolophidae. Medusafishes (ruffs, barrelfish). In: K.E. Carpenter (ed.) FAO species identification guide for fishery purposes. The living marine resources of the Western Central Atlantic. Vol. 3: Bony fishes part 2 (Opistognathidae to Molidae), sea turtles and marine mammals. American Society of Ichthyologists and Herpetologists. Special Publication No. 5 and Rome: Food and Agriculture Organization of the United Nations. pp. 1867-1868. Insacco, G. and B. Zava. 1999. First record of the saddled snake eel Pisodonopis semicinctus (Richardson, 1848) in Italian waters (Osteichthyes, Ophichthidae). Atti della Società Italiana di Scienze naturali e del Museo Civico di Storia Naturale in Milano 140: 283-286. Kalogirou, S., M. Corsini, G. Kondilatos and H. Wennhage. 2007. Diet of the invasive piscivorous fish Fistularia commersonii in a recently colonized area of the eastern Mediterranean. Biological Invasion 9: 887-896. Kara, M.H. and F. Oudjane. 2008. First observations of the Indo-Pacific bluespotted cornetfish Fistularia commersonii (Fistulariidae) from Algerian coasts. Journal of the Marine Biological Association of the United Kingdom, JMBA 2 – Biodiveristy Records: published online. Karrer, C. 1986. Occurrence of the barrelfish, Hyperoglyfe perciformis (Teleostei, Perciformes, Stromateoidei) in the Mediterranean Sea and off Portugal. Cybium 10 (1): 77-83.

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Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization Enric Massutí, María Valls and Francesc Ordines

INTRODUCTION During the second half of the 20th century up to 38 new fishes were reported in the western Mediterranean. Almost all of these exotic species entered naturally through the Strait of Gibraltar, being mainly of sub-tropical and tropical Atlantic origin. It is difficult to ascertain if some of these species have established self-maintaining populations in the area. In contrast, others populations of exotic species already established seem to be expanding north- and eastwards. The indigenous ichthyofauna of the western Mediterranean has also shown some changes in its population dynamics during the last decades. In the north-western part of this area, thermophilic species have increased their populations, while boreal species have become rare, as reflected in the landings of commercial fisheries. The possible effects of these changes on the ichthyofauna of the western Mediterranean are discussed, taking into account the acceleration of changes caused by the current phenomenon of global warming. The Mediterranean Sea is located in the temperate zone of the northern hemisphere. Its biodiversity is high: although constituting only ca. 0.7% of the world’s ocean surface area, more than 7% of the described marine species are present in this area. One of the reasons for its high biodiversity is the coexistence of Atlantic and Indo-Pacific species (Fredj, 1974), being also a vast import-export system. Thus both species of subtropical and tropical affinity are found in the Mediterranean, mainly in the eastern and southern areas, where water temperatures are higher than average, while cold-temperate species tend to inhabit the northern areas where water temperatures are colder. The Mediterranean ichthyofauna reflects this high diversity and distinct biogeographic origin, acquired after the Messinian crisis and characterized by a mixture of temperate and subtropical elements (Fredj and Maurin, 1987; Quignard and Tomasini, 2000). Fish species richness and diversity in the western basin was considered higher

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than that in the eastern basin (Quignard and Tomasini, 2000), but new data for the eastern basin has demonstrated that this hypothesis is unjustified (e.g. Golani, 1996; Papaconstantinou et al., 1994, 1997). Moreover, the increase in fish diversity in the Mediterranean documented mainly since the middle of the 20th century, which mainly affects the eastern basin since the influence of the Suez Canal (Golani et al., 2002), tends to minimize these differences, increasing the faunistic divergence between the eastern and western basins, towards an Indo-Pacific and Atlantic fashioned fish fauna, respectively. However, the role of the Strait of Gibraltar should not be underestimated in the colonization of the Mediterranean by non indigenous fishes. The reports of Atlantic species in the western basin, some of them settled, and the sporadic presence of Atlantic vagrants have increased during the recent decades (Quignard and Tomasini, 2000; Golani et al., 2002). A northern extension of distribution areas and biomass increase of thermophilic fishes and recession of boreal ones have also been observed (e.g. Quignard and Raibaut, 1993; Grau and Riera, 2001). These changes have often been considered as a consequence of global warming. In the present chapter, we review and summarize those changes observed in the ichthyofauna of the western Mediterranean during the last decades and we discuss their ramifications and effect on its biodiversity. MATERIALS AND METHODS Study area The western Mediterranean basin is located in the temperate zone of the northern hemisphere. It is delimitated by two relatively shallow (300-400 m depth) and narrow (14 km wide) passages: the Strait of Gibraltar in the west, connecting it with the Atlantic Ocean and the Sicily channel in the east, separating Tunisia from Italy and connecting it with the eastern Mediterranean basin. It can be divided into six sub-basins: Alboran, Algerian, Balearic, Gulf of Lions, Liguro-Provençal and Tyrrhenian (Fig. 1). The Atlantic surface waters flow into the Mediterranean through the Strait of Gibraltar and they circulate from the Alboran Sea along the coast of Africa (Millot, 1999). In the area of Sicily, the water current is divided into two branches, one running north along the Tyrrhenian and Liguro-Provençal sub-basins to the Gulf of Lions and the Iberian coast before returning to the Alboran Sea, while the second one enters the eastern Mediterranean basin. The surface waters of the western Mediterranean show high seasonal variations of temperature, with a uniform temperature (13-15ºC) during winter, but reaching temperatures as high as 20-25ºC in the summer. Below depths of 200 m, the western Mediterranean is characterized by a high environmental stability, with a temperature of 13ºC (Hopkins, 1985). Within the global context of climate change, the Mediterranean Sea has been well documented as especially sensitive to atmospheric forces and anthropogenic influence due

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46

44

42

40

38

Algerian

36

34 -5

0

5

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Fig. 1. General view of the western Mediterranean, between the Strait of Gibraltar and the Sicily channel, showing its six sub-basins: Alboran, Algerian, Balearic, Gulf of Lions, LiguroProvençal and Tyrrhenian.

to its location between continents and its reduced dimensions. The western Mediterranean has been observed as being in a process of warming and increased salinity since at least the middle of the 20th century in the upper (0.1-0.5ºC), intermediate (0.05-0.2ºC 83 and 0.030.09 for salinity) and deep (0.03-0.1ºC and 0.05-0.06 for salinity) layers (Bethoux et al., 1990, 1998; Rohling and Bryden, 1992; Rixen et al., 2005; Vargas-Yáñez et al., 2005, 2008). Data source The presence and range extensions of non indigenous fishes in the Mediterranean during the 20th century has been already compiled by the CIESM Atlas of Exotic Species in the Mediterranean (Golani et al., 2002, 2004, 2007), as updated from time to time in the CIESM website: http://www.ciesm.org/atlas. Much of the data used in this chapter comes from the information compiled in these reviews, considering as regards only the western Mediterranean basin, from the Strait of Gibraltar to the Sicily channel. This information has been augmented by data from other reports published in literature. The increment or rarefaction of indicator species in the western Mediterranean, as well as possible changes in their life cycles (e.g. reproduction and recruitment), has been analyzed from the review of available bibliographic information at different areas of this basin.

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We have also amplified this information by adding historical data series of annual landings and fishing efforts (in number of fishing vessels), obtained from the monitoring of two artisanal fisheries developed in Mallorca (Balearic Islands), targeted to fishes of different bio-geographic origins: e.g. (i) the epi-pelagic oceanic species Coryphaena hippurus, distributed in tropical and subtropical waters of all the oceans (Massutí and Morales-Nin, 1995); (ii) and the neritic species Aphia minuta, distributed in the northeastern Atlantic, from the Baltic Sea to the coasts of Morocco (La Mesa et al., 2005). This information has allowed us to estimate the annual catch per unit of effort, used as a proxy for abundance of these species. We have also added information of landings in the Balearic Islands (statistics from the central fish auction wharf of Mallorca) and in the western part of the Mediterranean (from FAO FISHSTAT Fisheries Statistical Database, regarding landings reported by France, Spain, Morocco and Algeria) for other possible species, with distinct bio-geographic origin. RESULTS Non indigenous species Since the middle 20th century, up to 38 new fishes have been reported for the first time in the western Mediterranean (Table 1). Almost all of these exotic species have entered naturally, with only two cases that were probably introduced via direct human activity, such as ship-mediated transport (ballast waters). The natural entrance of exotic fishes into the western Mediterranean has been continuous, with 70% of the new reports occurring since 1980 (Fig. 2). Most of them came through the Strait of Gibraltar from sub-tropical and tropical Atlantic regions (27 fishes), 6 are Indo-Pacific species, entering into the Mediterranean via the Suez Canal and only 3 are boreal Atlantic species (Fig. 3). Some of the exotic Atlantic fishes in the western Mediterranean have been reported only a few times and from a small number of specimens, thus making it difficult to know if they have established self-maintaining populations in the area. This is the case of Halosaurus ovenii, Gephyroberyx darwini, Scorpaena stephanica, Centrolabrus exoletus, Pseudupeneus prayensis, Beryx spendens, Chaunax suttkusi, Fistularia petimba, Seriola rivoliana, Zenopsis conchifera and Sphoeroides spengleri. The large pelagic migratory fishes Sphyrna mokarran, Carcharhinus falciformis, Galeocerdo cuvieri and Makaira indica could be considered vagrant, entering occasionally into the Mediterranean. A third group corresponds to fishes reported a few times, but possibly belonging to already established populations. This could be the case of: (i) the benthic species with limited swimming capacity Syngnathus rostellatus and Solea boscanion, who have been captured at different localities and times; (ii) Gymnammodytes semisquamatus, only reported in the northeastern Iberian coast, where it is exploited in commercial fishery, together with the other co-generic endemic species (G. cicerelus); (iii) and also of the pelagic fish Seriola carpenteri. This species has been captured only in

Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization 297

Table 1. New species reported in the western Mediterranean during the second half of the 20th century. Areas or sub-basins (see Fig. 1) where first recorded and other areas where presence has been documented (ALG: Algerian; ALB: Alboran; BAL: Balearic; GOL: Gulf of Lions; LIG. LiguroProvençal; TYR: Tyrrhenian; SIC: Sicily channel; EMED: eastern Mediterranean; CMED: central Mediterranean), the possible origin (TATL: sub-tropical and tropical Atlantic; IP: Indo-Pacific; B-ATL: boreal Atlantic; WATL: western Atlantic) and via for entrance (G: strait of Gibraltar; S: Suez Canal), as well as the bibliographic references which support this information (1: Golani et al., 2002, and references cited therein; 2: Bradai et al., 2004a, 2004b; 3: Mercader-Bravo, 2002; 4: Golani et al., 2004, and references cited therein; 5: Golani et al., 2007, and references cited therein; 6: Castriota et al., 2004; 7: Reina-Hervás et al. 2004; 8: Azzurro et al., 2004; 9: Fiorentino et al., 2004; 10: Pais et al., 2007; 11: Ragonese et al., 2007; 12: Sánchez-Tocino et al., 2007) are indicated. Year Species 1955 Psenes pellucidus 1958 Pisodonophis semicinctus 1959 Abudefduf vaigiensis 1960 Pagellus bellottii 1960 Synaptura lusitanica 1962 Trachyscorpia cristulata 1963 Halosaurus ovenii 1963 Gephyroberyx darwini 1969 Pomadasys stridens 1971 Siganus luridus 1977 Sphyrna mokarran 1981 Syngnathus rostellatus 1981 Scorpaena stephanica 1981 Diplodus bellottii 1981 Centrolabrus exoletus 1981 Sphoeroides pachygaster 1983 Carcharhinus altimus

First report ALG ALG

Other reports

Origin

Via

References

ALB, BAL & GOL GOL, TYR, SIC & CMED LIG & EMED

T-ATL T-ATL

G G

1 1, 2

IP

S

1

ALB & ALB ALG ALG BAL & CMED

T-ATL

G

1

T-ATL

G

1

ALB

ALB, BAL & SIC

T-ATL

G

1

ALG ALG

TYR –

T-ATL T-ATL

G G

1 1

LIG

EMED

IP

S

1

SIC LIG ALB

CMED & EMED – –

IP T-ATL B-ATL

S G G

1 1 1

BAL

–

T-ATL

G

1

ALB ALB

ALB –

T-ATL B-ATL

G G

1 1

BAL

whole sub-basin, CMED & EMED ALG & EMED

T-ATL

G

1

T-ATL

G

1

TYR

ALB

298 Enric Massutí, María Valls and Francesc Ordines

Year Species 1984 Microchirus hexophthalmus 1987 Carcharhinus falciformis 1987 Pseudupeneus prayensis 1987 Acanthurus monroviae 1987 Makaira indica 1990 Gymnammodytes semisquamatus 1990 Synagrops japonicus 1993 Stephanolepis diaspros 1993 Seriola fasciata 1994 1995 1997 1997 2000 2002

Galeocerdo cuvieri Beryx spendens Chaunax suttkusi Fistularia petimba Seriola carpenteri Pinguipes brasilianus 2002 Seriola rivoliana 2002 Solea boscanion 2004 Sphoeroides spengleri 2004 Fistularia commersonii 2006 Scomberomorus commerson 2007 Zenopsis conchifera

First report BAL

Other reports

Origin

Via

References

GOL

T-ATL

G

1

ALB

ALG & CMED

T-ATL

G

1, 2

ALB

BAL

T-ATL

G

1, 3

ALB

EMED & ALG

T-ATL

G

1, 4

TYR* BAL

LIG –

T-ATL B-ATL

G* G

1 1

LIG

–

IP

Sb

1

SIC

TYR, CMED & EMED SIC, CMED & EMED CMED – SIC – – CMED

IP

S

1, 2

T-ATL

G

1, 2, 5

T-ATL T-ATL T-ATL T-ATL T-ATL WATL

G G G G G Gb

1 1 1 1 1 1

SIC SIC ALB & – ALG ALB –

T-ATL T-ATL

G G

4, 6 4

T-ATL

G

7

SIC

IP

S

SIC

TYR, ALB, BAL, CMED & EMED CMED & EMED

IP

S

1, 4, 5, 8, 9, 10, 12 1, 5

SIC

–

T-ATL

G

11

BAL ALB LIG SIC ALB SIC LIG

(∗): probably; (b): ballast waters.

Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization 299

40

Number of species

35 30 25 20 15 10 5 0 1950

1960

1970

1980

1990

2000

2010

Years

Fig. 2. Cumulative reports of new fish fauna in the western Mediterranean during the second half of the 20th century. (see also Table 1). 17%

8%

75% Indo-Pacific Boreal Atlantic Subtropical or Tropical Atlantic

Fig. 3. Bio-geographic composition of the new fish fauna reported in the western Mediterranean during the second half of the 20th century. (see also Table 1).

300 Enric Massutí, María Valls and Francesc Ordines

the Sicily channel, but during different years and also with great amount of specimens and whose reproductive conditions suggest their establishment in the area. Lastly, there are some species that could be considered as recent colonizers, whose presence is well documented from different sites. Within this group, we can include: (i) the Diplodus bellottii and Pagellus bellottii, reported at the Maghrebin and Iberian coasts of the Alboran Sea, being occasionally captured by commercial fisheries; (ii) Pisodonophis semicinctus, reported at different locations north, south and east of the western Mediterranean; (iii) and Microchirus hexophthalmus and Synaptura lusitanica, that, although being confused with other soleids, which could explain its few records (Matallanas, 1984), are known along the Iberian Peninsula and even in the Gulf of Lions and in the central Mediterranean, respectively. Other recent colonizers seem to be expanding north- and eastwards. The clearest cases are those of Sphoeroides pachygaster (by Ragonese et al., 1992, 1997), Seriola fasciata (by Andaloro et al., 2005), Trachyscorpia cristulata echinata (by Ragonese and Giusto, 1999) and Psenes pellucidus (Fig. 4). Other species 46

46

T. cristulata echinata

S. pachygaster 44

44

5

42

42

2

40

40

1

38

4 6

3

36

4

38 S Adriatic S Tunisia SE Aegean E Levant

34

36

1 2

5

6

3

34 -5

0

5

10

15

20

46

-5

0

5

10

15

20

15

20

46

S. fasciata

P. pellucidus

44

44

2

42

4

40

40

3

3

1

38

4

42

4

36

38 Ionian S Tunisia E Levant

34

5

1 2

36 34

-5

0

5

10

15

20

-5

0

5

10

Fig. 4. Records of some subtropical and tropical Atlantic fishes that entered into the western Mediterranean during recent decades and seem to be in expansion: Sphoeroides pachygaster (1: Oliver, 1981; 2: Cerro and Portas, 1984; 3: Crespo et al., 1986; 4: Vacchi and Cau, 1986; 5: Barletta and Torchio, 1986; 6: Ragonese et al., 1992, 1997); Trachyscorpia cristulata echinata (1: Maurin, 1962; 2: Crespo et al., 1976; 3-5: Massutí et al., 1993; 6: Ragonese and Giusto, 1999); Seriola fasciata (1: Massutí and Stefanescu, 1993; 2: Quignard and Tomasini, 2000; 3: Andaloro et al., 2002; 4: Andaloro et al., 2005); Psenes pellucidus (1: Dieuzeide and Roland, 1955; 2: Maurin, 1962; 3: Riera et al., 1995; 4: Quignard and Tomasini, 2000; 5: Follesa et al., 2006). Other areas of the central and eastern Mediterranean where these species have been reported are also indicated.

Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization 301

such as Carcharhinus altimus and Acanthurus monroviae, that were documented first in the Alboran Sea and afterwards in the eastern Levant (Golani, 1996), could also be considered as extending their distribution. Within the exotic Indo-Pacific species, Pomadasys stridens was reported for the first time in the western Mediterranean and then it was known in the eastern basin, where it is common. The case of Abudefduf vaigiensis could be similar, but it has been reported only three times in the Mediterranean. By contrast, Siganus luridus, Stephanolepis diaspros, Fistularia commersonii and Scomberomorus commerson were first reported in the eastern Mediterranean, where they are well known and even common and could be considered as recent colonizers of the western basin, as a result of their expansion westwards. Demographic observations The indigenous ichthyofauna of the western Mediterranean has also shown some changes in its population dynamics during the last decades. In the Balearic Islands, Riera et al. (1995) and Grau and Riera (2001) reported that 6 septentrional species became rare during the last decades, while 24 thermophilic species increased their populations (Table 2). This categorization is based on sporadic observations carried out by these and other authors. However, similar trends can also be observed from more standardized data, obtained during the monitoring of fisheries developed in the area. The annual catch per unit effort of the circum-tropical Coryphaena hippurus during the last decades shows an increasing trend (Fig. 5). By contrast, this information for the north-eastern Atlantic Aphia minuta confirms a decrease in abundance reported by the previous authors (Fig. 5). During more recent years, an increasing trend can also be observed from annual landings of the thermophilic fishes Sardinella aurita, Seriola dumerili, Epinephelus marginatus and Balistes carolinensis (Fig. 6) captured as a by-catch of some artisanal fisheries. Table 2. Faunistic and demographic modifications in the ichthyofauna of the Balearic Islands, during the period 1975-2000 (from Riera et al., 1995 and Grau and Riera, 2001). Species in progress: Pteromylaeus bovinus, Tylosurus acus imperialis, Epinephelus aeneus, Epinephelus caninus, Epinephelus costae, Epinephelus marginatus, Caranx chrysos, Caranx rhonchus, Seriola fasciata, Lobotes surinamensis, Pomadasys incisus, Kyphosus spectator, Katsuwonus pelamis, Pontinus kuhli, Scorpaena maderensis, Tetrapterus albidus, Tetrapterus belone, Parablennius pilicornis, Scartella cristata, Schedophilus medusophagus, Schedophilus ovalis, Psenes pellucidus, Balistes carolinensis and Sphoeroides pachygaster Species in regression: Squatina spp., Scyliorhinus stellaris, Squalus acanthias, Sprattus sprattus, Argyrosomus regius and Aphia minuta mediterranea

302 Enric Massutí, María Valls and Francesc Ordines 6000

kg/boat

5000

C. hippurus

4000 3000 2000 1000 0 1980

1985

1990

1995

2000

2005

2010

Years 2500

A. minuta kg/boat

2000 1500 1000 500 0 1980

1985

1990

1995

2000

2005

2010

Years

Fig. 5. Annual catch per unit effort of Coryphaena hippurus and Aphia minuta for two artisanal fisheries developed in Mallorca (Balearic Islands) during the period 1981-2007.

In the Gulf of Lions, Quignard and Raibaut (1993) have reported the presence of 6 fishes, not previously documented, most of them sub-tropical or tropical species, and another 4 species of similar origin, already known in the area but considered very rare or exceptional (Table 3). They also indicated that 11 fishes, most of them thermophilic Table 3. Faunistic and demographic modifications in the ichthyofauna of the Gulf of Lions (from Quignard and Raibaut, 1993). New species: Rhinoptera marginata, Pomatomus saltator, Seriola dumerili, Diplodus cervinus cervinus, Thalassoma pavo and Sphoeroides pachygaster New reports of species considered as rare or exceptional: Mobula mobular, Pomadasys incisus, Epinephelus guaza and Coryphaena hippurus Species in progress: Carcharodon carcharias, Sardinella aurita, Sphyraena sphyraena, Sarpa salpa, Oblada melanura, Pagrus pagrus, Dentex dentex, Puntazzo puntazzo, Balistes carolinensis, Dactylopterus volitans and Solea senegalensis Species in regression: Sprattus sprattus and Platichthys flesus

Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization 303 400

S. aurita

Landings (kg; x103)

350 300 250 200 150 100 50 0 1970

1975

1980

1985

1990

1995

2000

2005

2010

1995

2000

2005

2010

1995

2000

2005

2010

1995

2000

2005

2010

Years

Landings (kg; x103)

120

S. dumerili

100 80 60 40 20 0 1970

1975

1980

1985

1990 Years

7000

E. marginatus

Landings (kg)

6000 5000 4000 3000 2000 1000 0 1970

1975

1980

1985

1990 Years

600

Landings (kg)

500

B. carolinensis

400 300 200 100 0 1970

1975

1980

1985

1990 Years

Fig. 6. Annual landings of Sardinella aurita, Seriola dumerili, Epinephelus marginatus and Balistes carolinensis between 1979 and 2007, captured as by-catch of artisanal fisheries in the Balearic Islands (statistics from the central fish auction wharf of Mallorca)

304 Enric Massutí, María Valls and Francesc Ordines

species, increased their populations, while 2 boreal ones were in regression. Francour et al. (1994) also reported that Thalassoma pavo, scarce in the north-western basin, arrived to Corsica in 1988. Since then, its concentration has increased by a factor of ten and juveniles have been observed since 1991. In the western basin of the Mediterranean, the landings of the boreal species Sprattus sprattus between 1970 and 2005 reveal two different periods: before 1990, when catches of this species were reported, and after 1990, with no catches (Fig. 7). According to Quignard and Raibaut (1993), this species was captured regularly by the commercial fishing fleet in the Gulf of Lions, but since 1985 its catches are very scarce. This marked decline has also been observed further south in the Iberian coast, where during 1950-60s this species supported commercial exploitation (Vives and Suau, 1956). Observations from experimental surveys indicate that it was still fairly common in the 1980s, but has become extremely scarce during the 1990s (P. Abelló, personal communication). By contrast, noticeable catches of the sub-tropical species Seriola dumerili can be observed after 1995, with no reported catches before this year (Fig. 7). For the other thermophilic species Sardinella aurita, Sabatés et al. (2006) have reported a gradual increase in abundance from the southern to the northern Iberian coast during 1989-2004, associated with the increment in sea water temperature. They also revealed a marked increase in its larval abundance during the last decades and the recent appearance of larvae in the 2000

Landings (tons)

S. sprattus 1500

1000

500

0 1970

1975

1980

1985

1990

1995

2000

2005

1995

2000

2005

Years 1400

Landings (tons)

1200

S. dumerili

1000 800 600 400 200 0 1970

1975

1980

1985

1990 Years

Fig. 7. Annual landings of Sprattus sprattus and Seriola dumerili between 1970 and 2005 in the western part of the Mediterranean (Source: FAO FISHSTAT Fisheries Statistical Database, regarding landings reported by France, Spain, Morocco and Algeria).

Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization 305

northernmost coast, where they did not occur 20 years ago, which indicates the successful reproduction of this species in the northern part of the Mediterranean, to which where it has expanded and confirms its establishment in the area. A similar trend has been observed for Parablennius pilicornis, which shows a progressive expansion throughout the western Mediterranean (Fiorentino et al., 2004). Similar observations have been also made for nektobenthic fishes. According to Francour et al. (1994), the population of Thalassoma pavo in the French Mediterranean coast has clearly increased since 1988, with an important recruitment for the first time in 1992. In the same manner, young individuals of Diplodus cervinus, almost unknown in the north-western Mediterranean until 1980, are now fairly common. In the Balearic Islands, Riera et al. (1995) have also reported abnormal recruitments of Epinephelus alexandrinus and Epinephelus marginatus from 1989 to 1992 and annual recruitments of Epinephelus caninus, not known in the area since the 1980s. More recently, two juveniles of Epinephelus aeneus, a species documented in the area only from a single specimen, have been also reported, jointly with 25 adults (Mas et al., 2006). DISCUSSION AND CONCLUSIONS The biological invasions, and the subsequent alteration of biodiversity, are particularly important in the sensitive area of the Mediterranean, with its high biodiversity and colonized by flora and fauna of different biogeographic origin. Numerous taxonomic groups have been affected, mainly by the influence that human activity has exerted over several centuries and through different ways: e.g. navigation, commercial shellfish transfers, etc. (Zibrowius, 1991). However, this impact has increased in the 20th century: firstly, by the opening of the Suez Canal, thus allowing the colonization of Indo-Pacific species; secondly, by the threat of global warming during the last decades and its effects on the oceanographic conditions of the Mediterranean, with a significant increment in average temperature of the waters and possible consequential influence on Mediterranean biota, in particular fishes whose abundance and distribution can be adversely affected by rising water temperatures (McFarlane et al., 2000; Genner et al., 2004) through the speciesspecific physiological thresholds of tolerance to this parameter. The preference of fishes for a certain range of temperatures implies that thermal characteristics of water masses can determine the habitat extension of species (Murawski, 1993). Our results suggest that in the western Mediterranean, where a clear increment in temperature and salinity of the water masses have been observed during the second half of the 20th century, global warming has also influenced the composition of the ichthyofauna. During this period, the entrance of 38 new species has been reported, mainly from the adjacent Atlantic through the Strait of Gibraltar Strait. This impact has not been as relevant as the one observed in the eastern Mediterranean, from the colonization of Indo-Pacific species entering through the Suez Canal (Golani, 1998; Golani et al.,

306 Enric Massutí, María Valls and Francesc Ordines

2007), but the entrance of exotic fish in the western basin, mainly of sub-tropical and tropical Atlantic origin, has also been important. It has produced the so-called effect of “tropicalization”, which tends to increase fish biodiversity. This phenomenon has expanded geographically, reaching the eastern basin. Thus, the Atlantic species Carcharhinus altimus, Acanthurus monroviae and Seriola fasciata, recently entered into the Mediterranean through the Strait of Gibraltar, have already reached the eastern Levant. By contrast, the Indo-Pacific species Siganus luridus, Stephanolepis diaspros, Fistularia commersonii and Scomberomorus commerson, which some years ago entered into the Mediterranean through the Suez Canal, have expanded westwards, even crossing the Sicily Channel. As it is also a continuous phenomenon, which has accelerated during the last decades, in the following years other Indo-Pacific species, such as Upeneus pori, Pempheris vanicolensis, Sphyraena chrysotaenia and Siganus rivulatus, which have been already reported in the central Mediterranean (Bradai et al., 2004; Ben Souissi et al., 2006), could be the next colonizers of the western basin through the Sicily channel. The only report of an Indo-Pacific species in the more westernmost part of the Mediterranean (e.g. Algerian, Alboran, Balearic and Gulf of Lions sub-basins) has been made very recently. It corresponds to Fistularia commersonii, which has been already observed off south-eastern and north-eastern Iberian Peninsula (Sánchez-Tocino et al., 2007). The population of this species has clearly expanded westwards, being firstly reported in Israel (Golani, 2000) and then in Rhodes (Corsini et al., 2002), southern Tyrrhenian (Azzurro et al., 2004), Sicily channel (Fiorentino et al., 2004), northern Tyrrhenian (Micarelli et al., 2006) and Sardinia (Pais et al., 2007). Moreover, it has been observed that the increment in the water temperature also produces the northern extension of the distribution areas and biomass increase of thermophilic species and the recession of boreal ones. This effect could tend to homogenize the fish fauna, being identified as “meridianization”. This process has not only had an impact on the faunistic composition of fish assemblages but also on the fisheries industry, being detected in the commercial fishing landings. The impact of the “tropicalization” effect has not been detected yet on the fisheries of the western Mediterranean, in contrast to the colonization of the eastern Mediterranean by Indo-Pacific species, which has been widely reflected in the fisheries landings (e.g. Galil, 2000). In the western basin, only a few species appear regularly in the catches of some fisheries. That could be the case of Solea senegalensis, the first sub-tropical invader species, whose presence in the western Mediterranean was recorded in 1920 off the Iberian coast. Since then, its distribution area has extended to Tunisia and the Gulf of Lions, and actually it is frequent in Alboran Sea and of growing importance in northern Tunisian, where in some fisheries it represents around 25% of soleids captured (Golani et al., 2002). More recently, Seriola fasciata, reported in 1993 for the first time in the western Mediterranean, has also increased progressively in importance in the fisheries of the Sicily channel area (Andaloro et al., 2005). In any case, the impact of these species in the fisheries seems to be lower than that of the Lessepsian fishes.

Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization 307

The “meridianization” affects not only the abundance and distribution of species but also their population dynamics. As example, the lack of juveniles of sub-tropical and tropical groupers in the northern part of the Mediterranean (over 41º5’N), and the dominance of very large individuals, suggested that these populations were not self-recruiting, being renewed by migratory movements of adult fishes (Chauvet, 1991). However, recruits of E. marginatus and E. alexandrinus have been observed since the 1990s (Francour and Finelli, 1991; Harmelin and Robert, 1992), which brought the evidence, corroborated in 1996 by visual observations (Zabala et al., 1997), that reproduction now occurs in this area. Invasive species can alter the evolutionary pathway of native species, by competitive exclusion, niche displacement, predation, and other ecological and genetic mechanisms (Mooney and Cleland, 2001). However, the lack of monitoring programs collecting standardized information and ecological studies makes it difficult to formulate a comprehensive interpretation of the dynamics of the establishment or/and the expansion of new and thermophilic species in the western Mediterranean. In the eastern basin, where this phenomenon has been studied intensely, the question of replacement of some native species and niche partitioning (e.g. in depth) between native and invasive species has been suggested (Golani, 1993, 1994; Bariche et al., 2004). The ecological role of the new species within the western Mediterranean ecosystems, and their impact on local populations, should be one of the most important objectives for future research. Another important tool to be addressed should be the comparison of settlement rate in the area of the species of sub-tropical and tropical Atlantic and the Indo-Pacific fishes. Up to now, with the exception of Sphoeroides paghygaster, the newcomers into the Mediterranean from the Red Sea seem to have higher capability of invasion than those from the Atlantic. In conclusion, both “tropicalization” and “meridianization” of the ichthyofauna, considered as biological responses to global warming, have been claimed for different areas of the western Mediterranean, as well as in the Adriatic (Dulčić et al., 1999) and in the adjacent Atlantic waters (Bañón et al., 1997; Quéro, 1998; Quéro et al., 1998). They have opposite effects, because they tend to increase the fish diversity of these areas and to homogenize their fish community, respectively. Their ecological and economic implications should require further studies, especially within the current context of global climatic changes, which could accelerate these processes. In any case, these biological events, which in the western Mediterranean are happening in a relatively short time and spatial scale, are liable to reduce the unique identity of the Mediterranean ichthyofauna, acquired progressively after the Messinian crisis and the last glaciation. ACKNOWLEDGEMENTS We would like to thank Dr. Pere Abelló (CSIC- Institut de Ciències del Mar), for the information on Sprattus sprattus and Carlos Barceló, for his assistance in the laboratory.

308 Enric Massutí, María Valls and Francesc Ordines

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Liza haematocheilus (Pisces, Mugilidae) D. Golani & B. Appelbaum-Golani (Eds.) 2010in the northern Aegean Sea 313 Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 313-332. © Pensoft Publishers Sofia–Moscow

Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea George Minos, Anastasia Imsiridou and Panos S. Economidis

INTRODUCTION The Mugilidae family consists around the world of more than 72 species from 17 fish genera (Nelson, 2006), with a worldwide distribution. Eight of these species are found in the Mediterranean Sea: Mugil cephalus (Linnaeus, 1758), Chelon labrosus (Risso, 1826), Oedalechilus labeo (Cuvier, 1829), Liza aurata (Risso, 1810), Liza ramada (Risso, 1826), Liza saliens (Risso, 1810), Liza haematocheilus (Temminck and Schlegel, 1845) and Liza carinata (Ehrenberg, 1836). The first six species are native while the last two are exotic in the Mediterranean. Especially, Liza haematocheilus (Redlip Mullet or Haarder), is a euryhaline species inhabiting both freshwater and marine environments. It has confirmed its high ecological plasticity and adaptability to waters considerably differing in both salt content and ion composition so that it can reproduce there and the eggs can be fertilized in the salinity range from 3 to 45‰ (Matishov and Luzhnyak, 2007). This fish can endure the water-dissolved oxygen deficiency (less than 1.0 mg/l), and temperature oscillations from -0.5 to 30 oC (Abrosimova and Abrosimov, 2002), thus being able to winter in cold freshwater (Starushenko and Kazansky, 1996). It has been introduced from seas of the Far East as suitable for aquaculture in the Azov and the Black Seas where the local mullets have suffered greatly from extreme water temperatures and salinities (Starushenko and Kazansky, 1996). Following eight (1972-1980) and six years (1978-1984) of translocations into lagoons of the Black and Azov Seas respectively, together with three years (1984, 1987 and 1989) of releases of fry produced from induced spawning stock, a self-reproducing population has been established (Starushenko and Kazansky, 1996). After collapse in the early 1990’s, live fish were released in these installations to the free water. Some of these specimens crossed the Bosporus, the Sea of Marmara and the Dardanelles and appeared soon after in the Mediterranean (e.g., the Gulf of Smyrna in Turkey (Kaya et al., 1998) and the Thracian Sea in Greece (Koutrakis and Economidis,

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2000). During the last few years it has spread progressively and been recorded in several other localities in the northern Aegean Sea (mainly in the Strymon and Nestos estuaries). However, there is no clear evidence that it has established a self-sustaining population. According to Corsini and Economidis (2007), the species introduced via aquaculture form a new category of allochthonous species which is gradually increasing in almost all of the Mediterranean, mainly due to rearing of exotic species in cages, of careless management in various sea fish farms, the lack of laws or of the enforcement of existing laws and of international rules. In fact, there are some unverified records of the presence in free waters of several such exotic fish and crustacean species such as the fishes Pagrus major ( Japanese bream), Liza carinata (Roving grey mullet), various Acipenser species (see Koutrakis and Economidis, 2006), the shrimp Marsupenaeus japonicus or fry of native Mediterranean fish, such as Dicentrarchus labrax and Sparus auratus, reared elsewhere, and exotic eel fry (Anguilla japonica and/or A. rostrata). SYNONYMY AND TAXONOMY Redlip mullet or Primorskiy redlip or haarder was and is still known under various names: Liza haematocheila (Temminck and Schlegel, 1845); Chelon haematocheilus (Temminck and Schlegel, 1845); Mugil so-iuy Basilewsky 1855; Liza lauvergnii (Eydoux and Souleyet, 1841) and Liza menada Tanaka, 1916. All these names should be placed in synonymy under the generally accepted as valid Liza haematocheilus (Temminck and Schlegel, 1845). Actually, Harrison (2004), after an analysis of nomenclature, used the name Liza haematocheila which Bogutskaya and Naseka (2004) replaced by the more correct Liza haematocheilus. Another key point is the taxonomy of the species, i.e. the genus under which Liza haematocheilus should be classified. According to Harrison (2003), the two genera Chelon and Liza, having both as types the Mediterranean species Chelon labrosus and Liza ramada, share many anatomical and molecular characters, but for various reasons it is not expedient to consider them as synonyms at present. The genus Liza, which is a specious but probably non-monophyletic assemblage (Harrison and Howes, 1991) and should be split (Ghasemzadeh, 1998), is however kept for nomenclatural stability as adapted by Eschmeyer’s Catalog of Fishes (online) and FishBase. It seems as if they are using the name Chelon, for haematocheilus, based on the opinion of Senou (2002). REDLIP MULLET IN THE SEAS OF THE FAR EAST This species is native to the Primorskiy Territory of Russia (brackish waters of the Sea of Japan), distributed at the north-eastern Asian coasts, from Peter the Great Bay (Vladivostok, Sedanka R., Suifan upstream to Voroshilov, Tumen’-ula, and other rivers) as far

Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea 315

north as the Amur Liman; through the Korean Peninsula; in Bo Sea, northern China (Fig. 1), to Macao in the south (Berg, 1949; Thomson, 1997; An et al., 2006). In Peter the Great Bay, the Redlip mullet occurs during the summer in large numbers in near-shore shoals, in estuaries and near river mouths where fish rear and spawn. In the fall, it migrates into rivers and settles down into pits for wintering (Serkov, 2003). In the Amur Bay (Fig. 1), the spawning of this species proceeds from June until the middle of July (maximum reached by the end of June) at water temperatures of 15.8-20.7 °C, salinity 31.5-32.8 ‰, at depths of 10-35 m. (Mizyurkina, 1984). Furthermore, eggs were recorded at depths from 5 to 20 m at water temperatures of 14-15.8 o C, salinities of 24-33‰ (Mizyurkina, 1984) while the egg diameter varied from 0.85 to 1.05mm (average 0.95mm) and the diameter of the oil drop from 0.35 to 0.55mm (average 0.44mm) (Chesalina, 2000). Redlip mullet is quite common in the rivers emptying into Peter the Great Bay together with M. cephalus (Fig. 1) entering fresh waters while large concentrations of fry (30-60 mm) have been encountered in the mouths of the rivers in August (Berg, 1949). Developing eggs appeared in the beginning of July above the depths of 23-29 m

Fig. 1. Schematic map of the native waters of the Redlip mullet and enlargement of the Primorskiy region. (1) Tesnaya river; (2) Razdol’naya river; (3) Artemovka river.

316 George Minos, Anastasia Imsiridou and Panos S. Economidis

at a surface water temperature of 16.6-17.1 °C. The egg diameter varied from 0.83 to 1.01 mm (average 0.93 mm) and the diameter of the oil drop from 0.34 to 0.54 mm (average 0.44 mm) (Dekhnik, 1951). In the shores of China the egg diameter has found to vary from 0.84 to 1.09 mm and the diameter of the oil drop from 0.38 to 0.51mm (Sha et al., 1986). The pelagic larvae of Redlip mullet are typically found in near-shore waters and post-larvae migrate to inshore waters and shallow estuaries (Li, 1992: cited after Liu et al., 2007). According to Omelchenko et al. (2004) Primorskiy Redlip mullet is represented by four local subpopulations differing in wintering localities and possibly in spawning sites. The extent of isolation or genetic exchange among subpopulations is unknown. The largest subpopulation winters in Tesnaya rivers and spawns in the sea in the southern Khasanskii region of Primorskiy (Fig. 1). The Razdol’naya subpopulation winters in the Razdol’naya River flowing in the northern Amur Bay and spawns in Peter the Great Bay in the vicinity of Russkii Island (Fig. 1). The Artemovka subpopulation presumably spawns in the same bay, wintering in rivers of the Ussuri Bay (Fig. 1). The Kievka subpopulation winters in the Kievka River (southeastern coast of the Sea of Japan); the locality of its wintering is unknown. As was reported by Omelchenko et al. (2004) the Far Eastern Primorskiy populations appeared to be genetically homogenous. This can be explained by 1) the absence of strict isolation between them and 2) the similar levels of salinity in the spawning localities of the Sea of Japan, about 30‰. Redlip mullet originates from an area (Sea of Japan) that experienced extreme changes in water level, especially during the Pleistocene glacial cycles. The Sea of Japan is a semi-enclosed marginal sea, which is distinguished from the other marginal seas of the Western Pacific by its extremely shallow sills. It was closed with long-term isolation from the Pacific Ocean and the East China Sea during glaciation events due to its shallow ledges (< 135 m) and became a freshwater body at least twice (Liu et al., 2007). The population of Redlip mullet could have become isolated in this area and adapted to the great variation of salinity. Adaptation to such changes included hibernation in river depressions during winters, thanks to its ability to store fat (Starushenko and Kazansky, 1996). REDLIP MULLET IN THE AZOV AND BLACK SEAS The Azov and Black Seas populations of Redlip mullet started being established after its introduction for aquaculture purposes in the Black Sea in 1972 and in the sea of Azov in 1978 (Starushenco and Kazansky, 1996). The initial population was formed by juveniles captured in the mouth of the Sukhodol (Kangauz) river and in the Ussuri Bay in the Sea of Japan, near Vladivostok (Fig. 1), and transported by airplane to Odessa (Starushenko and Kazansky, 1996). The reason for this introduction was the drastic decrease of the abundance of the valuable local commercial fish species (mainly grey mullets) and the

Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea 317

ineffective artificial propagation attempts in the early 1970s (Zaitsev and Starushenko, 2000; Omelchenko et al., 2004). Since 1984, coastal lagoons of Molochny, Shabolatsky and Burnassk, began to be stocked with fish produced from artificial propagation. It seems that from these lagoons Redlip mullet escaped to the free waters of the Azov and the Black Seas (Starushenko and Kazansky, 1996). During sampling in the Azov and Black Seas mature or ready to spawn individuals were found but never developing eggs (Chesalina, 2000). Initial data confirming the natural spawning were obtained during June 1989, when in the Molochny estuary (Azov Sea) young individuals were collected at the stage of the laying of scales (Chesalina, 2000) and in 1990 fertilized eggs and larvae were found (Luzhnyak, 2007). However, the first information about the presence of eggs of Redlip mullet in the Black Sea was in 1996 (Chesalina, 1997; Kideys et al., 2000) and proved that this species which was introduced into the northern lagoons during 1972–1986 now spawns along the coasts of the Black Sea. The acclimatization of the species in these seas (Fig. 2) was completed at the end of the 1980s – beginning of the 1990s – by the formation of a self-reproducing population (Chesalina, 2000). In 1992, Redlip mullet was included into the Inventory of Edible Fishes of the Sea of Azov/Black Sea Basin and in 1993 it was officially permitted to

Fig. 2. Schematic map of distribution of Redlip mullet in the Azov and Black Seas and recorded migration paths (→) to the Aegean Sea where the populations appeared. ∅ = the areas where individuals were released into the Azov and Black Seas; ▲ = places where individuals were captured in the Aegean Sea.

318 George Minos, Anastasia Imsiridou and Panos S. Economidis

catch it commercially (Matishov and Luzhnyak, 2007). At present, the increase in the abundance of the Redlip mullet population throughout the Azov and Black Seas basins has resulted its occurrence in many lagoons, river mouths and coastal areas of Romania, Bulgaria, the Ukraine, Russia, Georgia and Turkey (Fig. 2) and made it one of the most important and common commercial fish, reaching first place in catches of grey mullets, providing a total catch of 12,430 t in 2006 (Abrosimova and Abrosimov, 2002; Anonymous, 2002; Pianova, 2005) and successfully replacing the depleted stocks of the three local mullets (Starushenko and Kazansky, 1996). It is worth mentioning that in native waters (Primorskiy Bay) it did not exceed 500 t. (Sabodash and Semenenko, 1995). Actually, recently in the Turkish coasts of Black Sea remarkable quantities of catches of this fish have been recorded. This fact suggests that the fish should be abundant all along the coast line of the Turkish Black Sea, perhaps even up to the Bosporus channel (Fig. 2). Normally developing eggs in different stages were found during June in the Sevastopol region (Black Sea) at water temperatures of 18-20 °C, salinity of 17.6-18 ‰, above the depths of 20-100 m (Chesalina, 2000). In the Southern Black Sea (Okumuş and Başçinar, 1997) Redlip mullet enter shallow waters for feeding and spawning from mid May, where the spawning season extends from the end of May to the middle of July. In the Azov Sea species spawn in water temperatures ranging from 10.5 to 24.0 o C and salinity from 12 to 17 ‰ (Abrosimova and Abrosimov, 2002), during evenings and night (Chesalina, 2000). The spawning period lasts from April to July. After first spawning in April-May the next oocytes group matures and since the vitellogenesis of mullet is fast, at the end of July they are able to spawn for a second time (Pianova, 2005). According to Matishov and Luzhnyak (2007) Redlip mullet switched its spawning standards after its acclimation in the Azov Sea and not only winters but also reproduces into rivers and streams with low salinity. This capability to perform spawning migrations to rivers and to reproduce into them has not been previously recorded either in water bodies of the Primorskiy or in the Azov–Black Sea basin (Luzhnyak, 2007). Why did the species adopt so quickly a different reproduction strategy, leaving the open sea for inland waters, while the native mullet species (L. aurata, L. saliens and M. cephalus) did not? Perhaps the answer to this question is an ecological adaptation of Redlip mullet into the new and changing environment, following a lower level of predation by the alien ctenophore Mnemiopsis leidyi. Precisely on the onset (see above) of the Redlip mullet reproduction, in the Azov Sea the pelagic ctenophore M. leidyi appeared which was accidentally introduced from the Atlantic Ocean. This ctenophore was present all over the Azov Sea, inhabiting the water column and feeding on plankton, eggs and larvae of pelagic fish. This was very damaging to the Azov Sea fishery, leading to a collapse of anchovy (Engraulis encrasicolus) and seriously affecting the kilka (Clupeonella cultriventris) population (see Starushenko and Kazansky, 1996). It appeared that the reproduction of Redlip mullet in the Azov Sea was not affected and continued to be successful and adapted to a different spawning environment so that the eggs are not affected from ctenophore predation (Starushenko and Kazansky, 1996).

Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea 319

What about the physiology of this species? Is it able to successfully go through fertilization, incubation of the eggs and survival of the larvae into fresh water? It is known (Bulli, 1994) that the eggs of Redlip mullet may be fertilized in a salinity range of 3 to 45 ‰ but no fertilization occurs in fresh water. Also larvae are capable of adapting to fresh and saline water at the earliest stages of development, since six-day old individuals with swim bladders filled with gas survive direct transfer from seawater (17-19 ‰) to brackish water (5‰), and safely endure the subsequent transfer a day later to fresh (1‰) water (Bulli and Kulikova, 2006). Is there any evidence that the Redlip mullet reproduces in freshwater? In the eastern part of the Gulf of Taganrog (North-eastern Azov Sea) Redlip mullet reproduces at a water salinity of at least 5.3-6.4 ‰ and in the Don River, Manych River and Ust’Manych Reservoir from the middle of May to late June in lower salinity levels, between 1.7 to 2.7 ‰ (Matishov and Luzhnyak, 2007). Spawning occurred in the daytime, with the participation of one female and two to three males, at a temperature of 21-22o C in the surface layer of water with a slow or backward current, reaching highest intensity towards 11 a.m.(Matishov and Luzhnyak, 2007; Luzhnyak, 2007). According to Pianova (2005) Redlip mullet in the Azov and Black Seas presents a protogenic hermaphroditism, since individuals are originally females, two years old juveniles are hermaphrodite and later some fish become males. Histological examinations indicated the absence of male among one-year old fish and that hermaphroditism begins to appear in the gonads of two-year old fish (Mikodina and Pyanova, 2001). Testes of two-year old individuals had a few cytoplasmic oocytes among the spermatogoniums (Pianova, 2005). Most of the above conclusions are based on samples from cooling ponds of a nuclear power station (Kursk). The Azov and Black Sea Redlip mullet is an intermittent and asynchronous spawner, able to produce multiple portions (usually two batches) of eggs under good environmental conditions. If the food supply is poor, the second batch of oocytes is resorbed, thus giving a better chance to the first batch (Starushenko and Kazansky, 1996; Pianova, 2005). The eggs of Redlip mullet are spherical and pelagic, bearing one large oil drop. The shell of eggs is thin and is transparent and the yolk homogeneous, and a light yellow color. They are developed on surface water by oil drop upwards. In the Azov Sea, the egg diameter varies from 0.83 to 0.95 mm (average 0.87 mm) and the diameter of the oil drop from 0.41 to 0.47 mm (average 0.44 mm) while in the Molochny estuary (Azov Sea), the place for the initial acclimatization of species and subsequently of its mass spawning, there are (in water salinity of 16-17‰) eggs characterized by greater sizes (0.94 mm) and large oil drops (0.52 mm) (Chesalina, 2000). In the Black Sea (Sevastopol region) the egg diameter varies from 0.87 to 0.97 mm (average 0.92 mm) and the diameter of the oil drop from 0.42 to 0.50 mm (average 0.46 mm) (Chesalina, 1997). Fry usually winter in freshwater streams with a slow current near the mouth, where the wintering sites are usually set by the first frost in November (Matishov and Luzhnyak, 2007). Juveniles, yearlings, two-year-olds and some of three-year-olds in summer mainly feed in

320 George Minos, Anastasia Imsiridou and Panos S. Economidis

the shallow coastal seawaters and in near-by estuaries. In autumn, as the water temperature decreases to 10o C, juveniles begin wintering migration into fresh waters, entering the mouth and the lower courses of shallow rivers with a slow current. The wintering takes place in water temperatures of 1.5 to 4.5o C and when the temperature reaches the threshold of 8o C, wintering areas are abandoned as feeding activity commences (Starushenko and Kazansky, 1996). Aged specimen move to the sea for wintering. In general, the mullet groups of mature age feed throughout the Azov Sea area and in the estuaries, going for winter to the central part of the sea (Omelchenko et al., 2004). In spring a considerable part of spawners migrate for reproduction to the saltier Black Sea through the Kerch Strait while the rest remain in the Azov Sea, moving to spawn either to open seawaters or to warm fresh-water areas, such as Khanskoe Lake and Taganrog Bay (Omelchenko et al., 2004; Matishov and Luzhnyak, 2007). Growing in the new more favorable environment (Azov and Black Seas) the species reached a larger size (up to 80 cm), a rise in weight from 0.96±0.10 kg to 3.56±0.23 kg, fecundity at 22% and a growth rate three times greater than in its area of origin (Sea of Japan). Furthermore, maturity appeared one year earlier, spawning began 1-1.5 months earlier and lasted longer than in the Far Eastern seas. The vitellogenic oocyte diameters increased by 48.2% on the average while a reduction appeared in the diameter of the egg with a relative increase in the size of oil drop, which increases the buoyancy of the egg and contributes to the reproduction of species in waters with lower salinity (Starushenko and Kazansky, 1996; Chesalina, 2000; Pianova, 2005; Diripasko, 2007). Such an invader species seems to have more influence on the local mullet populations and environmental disturbances in general. We should take into account seriously the parasite fauna carried by any exotic species which may probably affect progressively the local closely related species. Regarding Redlip mullet, the Azov and Black Sea populations being in contact or found in mixed schools with M. cephalus, L. aurata and L. saliens could eventually infect them with Ligophorus (Dmitrieva et al., 2007), a gill parasite of Mugilidae family. REDLIP MULLET IN THE AEGEAN SEA The following information on Redlip mullet biology is based on a collection of 28 individuals (43-74.4 cm) sampled from 2003 to 2008 between May and February in the northern Aegean Sea (Fig. 2). Morphology. The species is easily distinguished from other native mullets in the Aegean Sea by its rather emarginated to slight forked caudal fin and the large scales (Fig. 3). These scales and the head shape resemble a carp and this similarity led Greek fishermen to give it the recent common name “sazanokefalos”, which means “carp-shaped mullet”. Additionally, it also has short pectoral fins, a rather small head pointed and flattened dorsally, a yellow iris and six pyloric caeca of approximately equal length.

Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea 321

Fig. 3. Individual of Redlip mullet Liza haematocheilus from the northern Aegean Sea.

The lengths, fork length (FL), standard length (SL), head length (HL), distance of the first (D1) and second (D2) dorsal fin together with the parameters of the estimated linear equations between each morphometric character in relation to the total length (TL), are given in Table 1. A detailed morphometric analysis on Aegean grey mullets is given by Minos et al. (1995) for adults and by Katselis et al. (2006) for fry. The R-squared values (R2) showed that there is a strong correlation between each morphometric character and total length (>0.98) except for HL (=0.8). Reproduction. Information on maturity and reproduction period is based on 28 individuals collected from 2003 to 2008 between May and February in the northern Aegean Sea. Summer samples were collected at the entrances of lagoons and across the coast line during a westward migration but each year after October the samples were found only in freshwater bodies that connect to the sea. Female individuals (7) ranged between 47 to 74.4 cm TL, while males (20) from 43 to 74 cm TL. It is worthy to mention that this size (74.4cm) is closest to the longest record up to now, being 80.0 cm TL (Novikov et al., 2002). Table 1. Parameters from TL=a + bX for each morhometric character (n=22). FL SL HL D1 D2

a -0.021 -1.535 -1.329 1.254 1.025

b 1.031 0.873 5.077 2.534 1.539

R2 0.997 0.982 0.807 0.989 0.991

322 George Minos, Anastasia Imsiridou and Panos S. Economidis

All the above individuals were ripening, the gonadosomatic index (GSI), being usually <1, while in July of 2006 (Fig. 4) two more ripe individuals (male and female) were caught (GSI: 11.2 and 15.5 respectively), indicating the eventuality of a self-reproducing population. The values of the gonadosomatic index for both sexes (Table 2) varied strongly for the same month each year. The highest value for the females was 15.46 and appeared in late July of 2007, while the lowest value 0.35 appeared in September of 2003. Similar values were recorded in the Black Sea while in the Azov Sea and in the native waters of the Primorskiy region the values were much higher, 26.4±3.5 and 35.2 respectively (Okumuş and Başçinar, 1997; Pianova, 2005). For males, GSI values in the Aegean Sea were 11.19 in late July of 2007, while the lowest values 0.13 appeared in the same month of 2004. In conformity with our results, in the Azov and Black seas the highest GSI values were about the same (Okumuş and Başçinar, 1997; Pianova, 2005). Consequently, reproduction of the species in the Aegean Sea apparently takes place in the summer from May to September with a peak around July. During fall, individuals full of fat move for wintering into inland fresh waters.

Fig. 4. Ripe male (upper) and female (lower) individuals of Redlip mullet Liza haematocheilus from the northern Aegean Sea.

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Table 2. Monthly variation of gonadosomatic index (GSI) for males and females from 2003 to 2008. Date September 2003 July 2004 May 2005 August 2005 October 2005 July 2006 September 2007 October 2007 November 2007 December 2007 January 2008 February 2008

n 1 3 1 6 2 2 2 2 2 2 3 1

GSI Male 0.397±0.26 1.849 0.198±0.02 0.722 11.187 0.282±0.0005 2.007±0.08 1.477±0.4 2.002±0.34 3.053±0.742

Female 0.350 0.733 0.920.09 1.093 15.457

2.898

Age structure. For ageing, 21 individuals were used. Annuli of at least three scales from each individual were counted under a light microscope (Leica MZ6). The age composition of the population was found to vary from 3 to 7, the dominant age groups were 4+ (33.3%) 3+ (28.6%) and 5+ (23.8%) years. It is worthy to note that in the sample there were no young individuals (age groups 1 and 2). The scales showed relatively clear annual rings (Fig. 5), allowing accurate aging for the first 7 years of fish.

Fig. 5. Scale of Redlip mullet Liza haematocheilus from the northern Aegean Sea with five visible growth rings.

324 George Minos, Anastasia Imsiridou and Panos S. Economidis

Growth. The calculated length-weight relationship from 28 individuals was: W=0.0002TL3.9446 (R2: 0.96, SEb: 0.156), demonstrating an allometric growth (P<0.05). Weight ranged from 824 to 5,495 g, this last being greater than the up to now heaviest recorded individual which was 5,000 g (Novikov et al., 2002). Relationships between total scale radius (Rn) and total length (TL) were determined with regression analysis. Back-calculated lengths at the estimated age (L1-L7) of individual fishes were estimated from the total length-scale radius regression (R2=0.8) and are as follows: L1 = 11.28; L2 = 24.03; L3 = 37.13; L4 = 46.33; L5 = 55.37; L6 = 63.30; L7=68.65. It appears that growth is continuous throughout the fish’s life. The von Bertalanffy growth equation (VBGE) was adjusted to back-calculated length at age data using the Levenberg-Marquardt method for non-linear regression analysis. The parameters of VBGE for sexes combined are shown in Table 3 while the data set appeared welladjusted (R2=99.94; SE=0.626). The ratio of Lmax/L∞ was 0.69 and the parameter ∅’ (Munro and Pauly, 1983) was 3.260. In studies in the Black sea (Okumuş and Başçinar, 1997), the age determination was estimated to have a smaller L∞ and a greater k and t0 value, since the von Bertalanffy values were for sexes combined L∞=71.8 cm, k=0.257 year-1 and t0=-0.562 and for females L∞=97.3 cm, k=0.136 year-1 and t0=-1.250, while the parameters ∅’ were 5.123 and 5.110, respectively. The negative t0 (age at zero length) values from the Black Sea Redlip mullet indicate that juveniles grow more quickly than the predicted growth curve for adults, and the positive t0 values from the Aegean Sea population indicate that juveniles grow more slowly (King, 2003). In fact, in the Black Sea samples all age classes were present while from the Aegean Sea young individuals were absent which affected the estimation of the VBGF parameters. Furthermore if this is not due to the lack or low number of young specimen, the alternative explanation could be that in the Mediterranean waters there is not yet successful reproduction. As mentioned above, the species store fat in their guts and this also observed in the Aegean Sea samples, since all the individuals caught from October till February were full of fat in the guts. This deposition of fat (during autumn and winter) in its body cavity allows a rapid maturation in the spring.

Table 3. von Bertalanffy growth parameters for Liza haematocheilus in Aegean Sea. Parameter L∞ K t0

Estimate

Std. Error

106.67 0.16 0.30

5.81 0.01 0.06

95% Confidence Interval Lower Upper 90.54 122.81 0.12 0.20 0.14 0.47

Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea 325

GENETIC STRUCTURE Azov population. Genetic studies of the species L. haematocheilus are few. Omelchenko et al. (2004) conducted a comparative population genetic analysis of the Redlip mullet from the Sea of Japan basin and the Azov Sea basin ranges. The genetic characteristics of the six populations were studied using electrophoretic analysis of fifteen enzymes, encoded by twenty one loci. The aims of this study were the following: a) the genetic characterization of the Far Eastern population, b) the comparison of genetic parameters of the Far Eastern donor and the new Azov populations, in order to detect genetic changes caused by acclimatization and adaptation of the new range and c) the study of genetic differentiation that may have appeared within the Azov population, due to local differences in spawning conditions. The genetic differences between the Far Eastern and the Azov sample groups was found to be highly significant (Gst = 0.9%). The mean heterozygosity per locus was equal in the native and new ranges but a 1.9 fold reduction in the percentage of polymorphic loci and a 1.5 fold reduction in the mean number of alleles per locus was found in the Azov populations. The reduction of these parameters in the introduced mullet may be explained by transplantation of only a part of the original gene pool. Apparently the Azov populations have passed through a dramatic decrease in the effective size (bottleneck effect), which primarily affects the allele number. In the native range, no genetic differentiation among the mullet samples from different areas was found (Gst = 0.42%), whereas in the Azov Sea basin, the samples from spatially isolated populations (ecological groups) exhibited genetic differences (Gst = 1.38%). The genetic homogeneity of the Far Eastern populations may be explained not only by the absence of strict isolation between them but also by the similar levels of salinity in the spawning localities of the Sea of Japan, which are close to the ocean one (reaching 30‰). On the other hand, the genetic divergence of the subpopulations and the excess of heterozygotes at some loci in the Azov population suggest selection processes that formed genetically divergent groups associated with the areas of different salinity in the new range. It is likely that water salinity at the sites of spawning and the egg development may be the major factor of direct or indirect selection providing this divergence. Another study conducted later by Salmenkova et al., (2007a,b) also investigated the genetic variation of native and acclimatized fish by using Restriction Fragment Length Polymorphism analysis (RFLP) of a mitochondrial DNA fragment containing the cytochrome b gene and the D-Loop. The study had been focused on five out of fifteen endonucleases detected polymorphic sites. In the samples of native and acclimatized Redlip mullet only five common haplotypes were found, whereas ten and three “unique” haplotypes were found respectively in the Far Eastern and the Azov populations. The haplotype mtDNA diversity was lower in the Azov Sea (μ = 6.35 ± 0.27) than in the Far Eastern populations (μ = 9.14 ± 0.55), which is in good accordance with the decrease in the number of polymorphic loci and the mean number of alleles per locus

326 George Minos, Anastasia Imsiridou and Panos S. Economidis

found in the previous allozyme analysis of these populations. Yet, the reduction of these parameters estimated from the allozyme markers is in accordance with the lower number of haplotypes (three unique haplotypes) and the lower proportion of rare mtDNA haplotypes found for the Azov samples in the RFLP analysis. The mtDNA study demonstrates once again that the Azov populations did pass through a bottleneck, which caused a considerable reduction in the effective population size. In contrast to protein marker data, which showed association with salinity of the spawning localities in the new range, the results of the mtDNA study did not reveal any adaptive character of mtDNA variation in the Azov Redlip mullet. Turan et al. (2005) studied the phylogenetic relationships of nine mullet species in the Mediterranean Sea by using allozyme analysis and found that M. cephalus and M. soiuy (=L. haematocheilus) clustered together. These are clearly isolated from Liza, Chelon and Oedalechilus genera the highest genetic distance value detected between M. soiuy and L. aurata. These results, placing M. cephalus and L. haematocheilus close together, need more confirmation because they suggest a new taxonomical rearrangement which is not justified by other investigations. For instance, Semina et al. (2007) investigating the mitochondrial DNA divergence and phylogenetic relationships in mullets of the sea of Japan (L. haematocheilus and M. cephalus) and the Azov Sea (L. aurata and M. cephalus), using PCR – RFLP analysis of three mitochondrial DNA fragments which include 12S/16S rRNA and ND3/ND4L/ND4 genes, found that L. haematocheilus and L. aurata are clustered together, whereas M. cephalus was the most genetically distinct species. Aegean population. The steady presence of the species in the European seas suggests that it should be recognized and identified among other native mullet. For this purpose a DNA methodology was developed to distinguish fry of six Mugilidae species found in the Mediterranean, namely M. cephalus, L. haematocheilus, C. labrosus, L. aurata, L. ramada and L. saliens (Imsiridou et al., 2007). In higher eukaryotes the 5S rDNA repeats consist of 120 bp highly conserved coding sequences, which are separated from each other by a nontranscribed spacer (NTS) that shows an accentuated length variation (Pendas et al., 1994). The above unit is tandemly repeated, it is located to different chromosome pairs in fish and normally it is species specific (Martins and Galetti, 2001; Martins et al., 2002). The fact that the organization of 5S rDNA presents no intraspecific polymorphism and on the other hand high interspecific variability makes it a very good candidate for comparison of closely related species. For this reason Polymerase Chain Reaction (PCR) amplification of the 5S rDNA gene was used for the identification of the above six species. Thirty individuals of fry (total length range 20-35 mm) of each of the five most common Mugilidae species (M. cephalus, C. labrosus, L. aurata, L. ramada and L. saliens) were collected from the coast of Nea Moudania, Northern Aegean Sea, Greece. For the species L. haematocheilus, 20 of the individuals mentioned above (sampled from 2003 to 2007 between May and November in northern Aegean Sea), were analyzed. In total 170 individuals of the above six species were analyzed with the PCR technique. The 5S

Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea 327

Fig. 6. Electrophoretic analysis on 1.5% agarose gel of the 5S rDNA gene PCR products, obtained from the six Mugilidae species (M. cephalus, L. haematocheilus, C. labrosus, L. aurata, L. saliens and L. ramada – two different individuals per species). The size of the PCR products was checked against a 100 bp DNA ladder.

rDNA gene was amplified successfully in all six species. As shown in Fig. 6, two out of six species revealed species – specific patterns. L. haematocheilus gave a pattern of three bands: a band of approximately 280 bp, a band of 600 bp and one of 620 bp. L. saliens gave a pattern of one band the size of which was approximately 220 bp. The other four species (M. cephalus, C. labrosus, L. aurata and L. ramada) gave a pattern of two bands the sizes of which were around 220 bp and 440 bp. No intraspecific polymorphism was detected, as all the individuals of each species revealed the same PCR pattern. So L. haematocheilus can be discriminated with a simple PCR reaction from the rest of the species, as it reveals a unique PCR pattern. CONCLUSIONS Redlip mullet is a highly adaptable, euryhaline fish tolerant of low water temperatures. Usually spawning in lagoons and inshore waters at salinities of 12 to 15‰, it makes

328 George Minos, Anastasia Imsiridou and Panos S. Economidis

wintering migrations into rivers. In contrast to the other mullet species it can withstand colder waters. It appears to have a remarkably fast growth rate, especially at high water temperatures of 29° to 32°C, making it a very suitable fish for culturing also in warm water. Furthermore, the species have successful adaptation in the Black Sea estuarine complex since: 1) it has a wide range of salinities and/or water temperatures which do not bar this species, 2) the wintering and spawning areas do not coincide with those of the indigenous mullets and 3) within any one estuary, most mullet species avoid interspecific feeding competition by selecting particles of different size (Mariani et al., 1987) or different species present distinct distribution patterns (Almeida, 2003) together with the ability to exploit different eutrophic substrates through their complex pharyngobranchial structure (Capanna et al., 1974). Growing in the new environment (Azov and Black Seas), considerable adaptive changes were recorded in species biology as compared to the native range. The diet spectrum widened, the rate of growth increased by factors of 1.5–2.0, the size and weight of individuals rose, the time of reaching sexual maturity decreased by a year, spawning began 1-1.5 months earlier and lasted longer, the sizes of the egg and of the oil globule changed and fecundity increased. Redlip mullet population actually is a commercial species and maintains first place in catches of grey mullets in Azov-Black Sea basin, with a total annual yield of 12,430 t in 2006. Obviously the species presents the character of a true invader with its typical population explosion (invader effect). At the moment it is too early to judge whether this population explosion, as expressed by the high catch, will continue or stabilize. Similar phenomena are appearing in smaller scale in the northern Aegean Sea, where other mullet species are clearly in decline. Salinity level of spawning sites and subsequent egg development is the most probable factor differentiating local selection during rapid adaptation and naturalization of the acclimatized Redlip mullet population in the Azov Sea providing the genetic divergence of the subpopulations. Since invader species have more influence on the local populations, parasite fauna carried by the Redlip mullet can progressively affect local closely related species (M. cephalus, L. aurata and L. saliens) who are in contact with this species, possibly infecting them with a gill parasite of the Mugilidae family such as Ligophorus. Starushenko and Kazansky (1996) suggested that the oceanic salinity of water and mild climate of the Mediterranean probably do not pose an obstacle for this species, which might continue to expand its area of distribution towards the Strait of Gibraltar and even beyond, after flooding the Mediterranean. However the westward spreading of the species seems to be not so fast. Maybe there are problems in reproduction; this supposition is reinforced by the lack from the Aegean population of fry and/or juveniles. The species has appeared in the Aegean Sea since 1998 and it is estimated that it is not yet very abundant. The species appears in coastal areas near estuaries from May to November. During the fall, individuals move into inland waters for the winter (records

Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea 329

were obtained in winter from Lake Vistonis). During this period, the species seems to store fat in its gut, thus making possible a rapid maturation in the spring. The fact of relatively few and large individuals caught and the lack of fry and juveniles of the species across the Aegean Sea indicates that so far it has not been established a self-sustaining population and probably that it is adults who frequent this area for feeding. Finally, this new invader species in the Black Sea-Mediterranean environment represents an unpredictable prospect. The more negative result would be the successful adaptation of the species in the Mediterranean and the replacement of all or several native mullet. But for this perspective there is not any serious evidence at the moment. REFERENCES Almeida, P.R. 2003. Feeding ecology of Liza ramada (Risso, 1810) (Pisces, Mugilidae) in a southwestern estuary of Portugal. Estuarine, Coastal and Shelf Science 57: 313-323 Abrosimova, N.A. and S.S. Abrosimov. 2002. Mugil so-iuy Basilewske as a new object of aquaculture. European Aquaculture Society, Special Publication No. 32: 105-106. An, L., J. Hu, Z. Zhang and M. Yang. 2006. Quantitative real-time RT-PCR for determination of vitellogenin mRNA in so-iuy mullet (Mugil soiuy). Analytical and Bioanalytical Chemistry 386: 1995-2001. Anonymous, 2002. State of the environment of the Black Sea. Pressures and Trends 1996-2000. Commission on the protection of the Black Sea against pollution. 4.48-4.52. Berg, L. S. 1949. Mugilidae. In: Fresh-water fishes of the U.S.S.R. and adjacent countries. Vol. III. English translation, Jerusalem, 1965, Israel Program for Scientific Translations. pp. 58-70. Bogutskaya, N.G. and A.M. Naseka. 2004. Catalogue of agnathans and fishes of fresh and brackish waters of Russia with comments on nomenclature and taxonomy. Moscow: KMK Scientific Press Ltd. 387 pp. (In Russian). Bulli, L. I. 1994. Some specific features of early ontogenesis of haarder from brood stocks and natural populations. Trudy Yuzhnogo Nauchno-Issledovatel’skogo Instituta Morskogo Rybnogo Khozyaistva i Okeanografii (YUGNIRO) 40: 111-114. Bulli, L.I. and N.I. Kulikova. 2006. Adaptive capability of larvae of the haarder Liza haematocheila (Mugilidae, Mugiliformes) under decreasing salinity of the environment. Journal of Ichthyology 46(7): 534-544. Capanna, E., S. Cataudella and G. Monaco. 1974. The pharyngeal structure of Mediterranean mugilidae. Monitore Zoologico Italiano-Italian Journal of Zoology 8: 29-46. Chesalina, T.L. 1997. On the spawning of pilengas (Mugil so-iuy) in the Black Sea. Journal of Ichthyology 37 (5): 717-718. (In Russian). Chesalina, T.L. 2000. Some data on spawning of haarder (Mugil so-iuy) in the Azov-Black Sea region. Ecology of the Sea 53: 72-76. (In Russian). Corsini-Foka, M. and P. S. Economidis. 2007. Allochthonous and vagrant ichthyofauna in Hellenic marine and estuarine waters. Mediterranean Marine Science 8:67-89. Dekhnik, T. V. 1951. Roe of pilengas and its development. Izvestiya TINRO 34: 262-266. (In Russian). Diripasko, O.A. 2007. Population structure of haarder Liza haematocheila (Mugiliformes, Mugilidae) acclimatized in the Sea of Azov basin. Journal of Ichthyology 47(7): 486-493.

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