Fish Invasions of the Mediterranean Sea 9546425265, 9789546425263

Table of contents :
Contents
Preface
Contributors
The new Tethyan ichthyofauna of the Mediterranean– historical background and prospect
Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion and spatial congruence with endemic species
Introduction rate of Lessepsian fishes into the Mediterranean
The genetics of Lessepsian bioinvasions
Red-Med immigration: a fish parasitology perspective, with special reference to the Myxosporea
Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection
Mediterranean marine protected areas and non-indigenous fish spreading
Colonization of the Mediterranean by Red Sea fishes via the Suez Canal – Lessepsian migration
Alien marine fishes of Turkey – an updated review
Current status of alien fishes in Greek seas
Fish Invasions in the Adriatic Sea
Non native marine fish in Italian waters
Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization
Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea

Citation preview

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

2 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