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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

SofiaMoscow
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
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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. Dragievi and J. Duli


Fish invasions in the Adriatic Sea

267

L. Orsi Relini
Non native marine fish in Italian waters

293

E. Massut, 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 Duli 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 Massut 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 countrys 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 fr 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: brendag@savion.huji.ac.il
Ernesto Azzurro ISPRA, High Institute for Environmental Protection and Research, Laboratory of Milazzo, Via dei Mille 44, 98057 Milazzo (ME), Italy. E-mail: eazzurr@tin.it;
e.azzurro@icram.org.
Jonathan Belmaker Interuniversity Institute of Marine Sciences, Eilat, Israel and Department
of Life Sciences, Ben-Gurion University, Beer Sheva, Israel. E-mail: belmakej@bgu.ac.il
Frida Ben Rais Lasram Laboratoire Ecosystmes Lagunaires, UMR CNRS-IFREMERUM2 5119, Universit Montpellier 2, cc 093, place Eugne Bataillon, 34095 Montpellier
Cedex 5, France and Laboratoire Ecosystmes et Ressources Aquatiques, Institut National
Agronomique de Tunisie, 43 avenue Charles Nicolle, 1082 Tunis, Tunisie. E-mail: Frida.
Lasram@univ-montp2.fr
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: mbilecenoglu@yahoo.com
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: eran.brokovich@mail.huji.ac.il
Victor China Interuniversity Institute of Marine Sciences, Eilat, Israel and Department of Life
Sciences, Ben-Gurion University, Beer Sheva, Israel. E-mail: china@bgu.ac.il
Maria Corsini-Foka Hellenic Center for Marine Research/Hydrobiological Station of Rhodes,
Cos Street, 85100 Rhodes, Greece. E-mail: mcorsini-foka@hsr-ncmr.gr
Ariel Diamant National Center for Mariculture, Israel Oceanographic and Limnological
Research Institute, Eilat 88112, Israel. E-mail: diamant@agri.huji.ac.il
Branko Dragievi Laboratory of Ichthyology and Coastal Fishery, Institute of Oceanography
and Fisheries, Setliste I. Mestrovica 63, 21 000 Split, Croatia. E-mail: brankod@izor.hr

12 Fish Invasions of the Mediterranean Sea: Change and Renewal

Jakov Duli Institute of Oceanography and Fisheries, 21000 Split, Croatia. E-mail: dulcic@
izor.hr
Panos S. Economidis Karakasi 79, GR-54453, Thessaloniki, Greece. E-mail: psecon@bio.auth.gr
Patrice Francour Nice University, Sciences Faculty, EA 4228 ECOMERS, Parc Valrose, 06108
Nice, France. E-mail: francour@unice.fr
Daniel Golani Department of Evolution, Systematics and Ecology, The Hebrew University of
Jerusalem, 91904 Jerusalem, Israel. E-mail: dgolani@cc.huji.ac.il
Francois Guilhaumon Laboratoire Ecosystmes Lagunaires, UMR CNRS-IFREMER-UM2
5119, Universit Montpellier 2, cc 093, place Eugne Bataillon, 34095 Montpellier Cedex
5, France. E-mail: francoisguilhaumon@gmail.com
Anastasia Imsiridou ATEI Thessalonikis, Department of Aquaculture & Fisheries Technology,
P.O. Box: 157, GR-63200, Nea Moudania, Greece. E-mail: imsiri@otenet.gr
Moshe Kiflawi Interuniversity Institute of Marine Sciences, Eilat, Israel and Department of
Life Sciences, Ben-Gurion University, Beer Sheva, Israel. E-mail: mkiflawi@bgu.ac.il
Luisa Mangialajo Nice University, Sciences Faculty, EA 4228 ECOMERS, Parc Valrose, 06108
Nice, France. E-mail: Luisa.MANGIALAJO@unice.fr
Enric Massut IEO- Centre Oceanogrfic de les Balears, Moll de Ponent s/n, 07015 Palma,
Spain. E-mail: enric.massuti@ba.ieo.es
George Minos ATEI Thessalonikis, Department of Aquaculture & Fisheries Technology, P.O.
Box: 157, GR-63200, Nea Moudania, Greece. E-mail: gminos@aqua.teithe.gr
David Mouillot Laboratoire Ecosystmes Lagunaires, UMR CNRS-IFREMER-UM2 5119,
Universit Montpellier 2, cc 093, place Eugne Bataillon, 34095 Montpellier Cedex 5,
France. E-mail: mouillot@univ-montp2.fr
Francesc Ordines IEO- Centre Oceanogrfic de les Balears, Moll de Ponent s/n, 07015 Palma,
Spain. E-mail: xisco.ordinas@ba.ieo.es
Lidia Orsi Relini Laboratori di Biologia Marina ed Ecologia Animale, Via Balbi 5, 16126
Genova, Italy. E-mail: largepel@unige.it
Jrmy Pastor Nice University, Sciences Faculty, EA 4228 ECOMERS, Parc Valrose, 06108
Nice, France. E-mail: Jeremy.PASTOR@unice.fr
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: fdpor@netvision.net.il
Mara Valls IEO- Centre Oceanogrfic de les Balears, Moll de Ponent s/n, 07015 Palma, Spain.
E-mail: maria.valls@ba.ieo.es

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
SofiaMoscow

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 100and that of the other
biota is assumed to be inthe 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 therapid 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 1.1C during the


last 27 years. Sar et al. (2006) even speak of an increase of 3.0C in the main sea
level temperature of the Mediterranean during the last 10 years, i.e. from 20-21C to
23-24C.
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 todays 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 (Forsskl), the red-eye round herring Etrumeus teres
(Dekay), Bregmaceros albyi and the red squirrelfish Sargocentron cf. rubrum (Forsskl).
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 dOrbigny 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 (Schrter) 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 17C. 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 (Rppell) (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 (Forsskl). 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 Forsskl, 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, 19822003
(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 (Rppell) and
of the bluespotted cornetfish Fistularia commersonii Rppell 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 (Duli and Pallaoro,
2002; Duli 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 1930s, Eastern Sicily in the 1970s and recently crossed into the Western Mediterranean (Sar 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 (Mller 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 (Rppell),
or the milk shark Rhizoprionodon acutus (Rppell) 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 (Mller 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 (Forsskl) 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 18C
has already been re-settled by many symbiont-bearing Foraminifera (threshold 14C)
and could already have been potentially again inhabited by scleractinian reef building
corals (threshold 15C 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.
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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
SofiaMoscow

Global warming and exotic fishes in the


Mediterranean Sea: introduction dynamic, range
expansion and spatial congruence with
endemic species
Frida Ben Rais Lasram, Franois 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, Franois 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; Sabats 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 0.04C.yr-1 using the maximum Sea
Surface Temperatures (SSTmax) series (19822005) 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 0.68C.
The areas that warmed by more than 1C 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 0.74C and the Alboran Sea by 0.63C. 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 0.06C per year.
The northern Levantine Basin, the southern Ionian Sea, as well as the Gulf of Gabes
0

15

30

45

45

Mean SST (C)

30

30
0

15

30

15

30

45

45

30

30
0

15

16.15 16.95
16.95 17.67
17.67 18.39
18.39 19.10
19.10 19.82
19.82 20.53
20.53 21.25
21.25 21.96
21.96 22.68

30

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

38 Frida Ben Rais Lasram, Franois Guilhaumon and David Mouillot

and the Ligurian Sea appear also to be areas that warm drastically (about 0.04 to 0.05C
per year) (Fig. 2). An opposite trend appears in the northern Adriatic which displays a
decrease in SST ranging from -0.02 to -0.01C 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).

15

30
45

45

Warming trend
(C.year-1)
-0.02 -0.01
-0.01 0
0 0.01
0.01 0.02
0.02 0.03
0.03 0.04
0.04 0.05
0.05 0.06

30

30
0

15

30

Fig. 2. Warming trend of the Mediterranean Sea surface waters


0

15

30
45

45

Warming rate
(C.year-2)

30

30
0

15

30

Fig. 3. Warming rate acceleration of the Mediterranean Sea surface waters

-0.009 -0.007
-0.007 -0.005
-0.005 -0.003
-0.003 -0.001
-0.001 0
0 0.004
0.004 0.006
0.006 0.008

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

19.6

19.2
19

1.5

18.8
18.6

18.4
18.2

0.5

Number of Lessepsian
species per decade

Temperature (C)

19.4

18

0
1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000

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, Franois 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 Duli 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

60

19.2

50

19

40

18.8
30

18.6

20

18.4

Latitude (degree)

Temperature (C)

19.4

70

10

18.2

18
1810 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000

Decade

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 1980s 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, Franois 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

15

30

15

30

45

45 45

45

30

30 30

30

0
0

15
15

30
30

0
0

15
15

30
30

45

45 45

45

30

30 30

30

15

30

15

30

Number of species per cell


1
18 - 25

2-3
26 - 37

4-9
38 - 44

10 - 13
45 - 49

14 - 17
50 - 59

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

15

30

15

30

45 45

45

45

30 30

30

15

30
30
15
0
Pseudupeneus prayensis: an Atlantis species that has not dispersed

30
15
0
Sorsogona prionota: a Lessepassian spesies that has not dispersed
30

15

30

45 45

45

30

45

30 30
15
0
Terapon puta: a Lessepassian spesies with weak dispersal
0

15

30
30
15
0
Microchirus hexophtalmus: an Atlantis species with weak dispersal

30

30

15

30

45 45

45

30

45

30 30
30
0
15
Siganus luridus: a Lessepassian spesies with strong dispersal

30
30
15
0
Sphoeroides pachygaster: an Atlantis species with strong dispersal

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

44 Frida Ben Rais Lasram, Franois 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)

55.27 km.y-1
1000
27.5 km.y-1

Year

0
1940
1950
Palestine
1974

1960
1970
Cyprus
1969

1980
1990
Turkey
1987

Hemiramphus far
3000
-1

300 km.y
1500

124 km.y

-1

Year

0
1925

1930

1935

Palestine
1927

Syria
1931

1940

Rhodes
1937

Distance (km)

Etrumeus teres
3000
1500

1000 km.y-1
29.4 km.y-1

Herklotsichthys punctatus
80 km.y-1
500

10.3 km.y-1

0
1940

1990

2010

Aegean sea
2002

Lebanon
1977

2000

Rhodes
2005

Distance (km)

Distance (km)

Year
1980

53.7 km.y-1
13.6 km.y-1
1980

Palestine
1935

Lebanon Turkey
1965
1981

Turkey
1984

0
1985

Year

1990
Greece
1997

Year
1990

1995

Israel
1989

2000

2005

Turkey
2000

Rhodes
2005

2010

Atherinomorus lacunosus

50.6 km.y

1960

1990

66.7 km.y-1

-1

1930

1980

171 km.y-1

1000

Distance (km)

Distance (km)

1000
0

1970

Lebanon
1977

2000

Scomberomorus commerson
2000

Year
1960

Petroscirtes ancylodon

32 km.y-1

0
1970

1950

Palestine
1937

335 km.y-1

1000

Year

1000

Lagocephalus suezensis
2000

66.6 km.y-1

1960
1990
2000
2005
Israel Turkey Greece Lampedusa
2004
2005
1963 1997

Distance (km)

Distance (km)

Apogon pharaonis
2000

2000
1000

33.7 km.y-1
8.7 km.y-1

0
1900

1930

Egypt Israel
1902 1927

43.4 km.y-1
1950
Turkey
1950

Year
1990

Lebanon
1986

Fig. 8. Dispersal of 16 Lessepsian species recorded at least 3 times in the northern Mediterranean.
Location of new records and average speed (km yr-11) are indicated below the x-axis and within
the curves, respectively. The shaded speed values indicate a deceleration.

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

24.2 km.y-1

1000

-1

27.2 km.y
0
1965
1945
Israel
Lebanon
1953
1964

29.5 km.y-1

Year

1985
Turkey
1994

2005
Rhodes
2005

Distance (km)

Leiognathus klunzingeri
153.4 km.y-1
3000

307.8 km.y-1

Syria
1931

1940

1960

Rhodes
1937

Year
1980

Sphyraena flavicauda
2000
1000

2000

Greece
1980

2020

Adriatic sea
2002

1990
Israel
1992

3000

45.3 km.y-1

0
1940
1920
1960
Palestine
Rhodes
1935
1938

Israel
1953

Year

49.8 km.y-1
1960
1980
Turkey
1956

1990

Greece
1984

Albania
1995

Distance (km)

Siganus rivulatus

3000
0
1920

21.4 km.y-1

329 km.y-1
279 km.y-1
1940

Palestine Syria
1927
1929

Fig. 8. Continued

1960

Year
1980

Aegean sea
1934

2000

Distance (km)

1950

2005
Rhodes
2005

600.4 km.y-1

Year
2000
1980
Albania
1986

25 km.y-1
3000

n
Distance (km)

Distance (km)

244.6 km.y-1

2000
Turkey
2002

Siganus luridus

312.2 km.y-1

2000

Year

Saurida undosquamis
4000

116.3 km.y-1
131.6 km.y-1

Parexocoetus mento

31.6 km.y-1

0
1920

Distance (km)

Callionymus filamentus
2000

Distance (km)

Distance (km)

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

2020

Adriatic sea
2004

-1

100 km.y-1
388.5 km.y-1

45.4 km.y
Year
0
1940
1960
1980
2000
2020
Israel Lebanon Ionian sea Tyrrhenian sea
1995
1964
1976
2004
Stephanolepis diaspros
3000

107 km.y-1
81.6 km.y-1
283 km.y
63.6 km.y-1
0
1920 1930 1940 1950 1970

1500

-1

Palestine Syria Cuprus Rhodes Italy


1927
1929 1935
1946
1967

Year

46 Frida Ben Rais Lasram, Franois 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

15

30

45

45
1953 Israel
1956 Turkey
1962 Cyprus
1982 Libya
1984 Rhodes
1991 Crete
1994 Egypt
1995 Albania

30

30
0

15

30

15

30

45

45

30

30
0

15

1927 Palestine
1929 Syria
1935 Cyprus
1946 Rhodes
1966 Tunisia
1967 Italy
1976 Crete
1993 Sicily
2003 Montenegro

30

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, Franois 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 2000s 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 Gkoglu 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).

15

30

45

45

30

30
0

15

30

15

30

Number of species
45 per cell

45

1
23
47
8 15
16 25
30

30

26 38
39 44

15

30

45 55
56 64

Fig. 10. Spatial patterns of exotic species richness during the eighties (a), exotic species richness
in 2006 (b) and endemic species richness (c)

50 Frida Ben Rais Lasram, Franois 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 Gkoglu et al., 2003), Scarus ghobban (by Goren and Aronov, 2001), Lagocephalus

T. Kurtz

D. Daron

1 Psenes pellucidus
2 Seriola fasciata

3 Epinephelus coioides
4 Siganus rivulatus

D. Daron

F. Riera

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 (Duli
and Golani, 2006).
The rate of introduction of Lessepsian fish during 20002006 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 0.36C 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; Duli 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, Franois 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 Earths 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.
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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
SofiaMoscow

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 5090 % 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
(80.5=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
frameworks 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 LESSEPSIANMIGRANT 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 Israels 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 Canals 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

140

Cumulative number of species

Cumulative number of species

Introduction rate of Lessepsian fishes into the Mediterranean 61

Med species
Lessepsians species

300

200

100

120

1945

1965
1985
Year

2.5%
Median
97.5%

100
80
60
40
20

1925

1925

2005

1945

1965

1985

2005

Year

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 (1 = 1 = 2 = 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 models 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
1= 2 = 1= 0

log Likelihood
- 74.83
- 76.32

0
-0.77
-0.34

1
0.01

0
33.57
32.78

1
0.052

2
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
0
1
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)= 0 + 1 t, where u is immigration probability


at the tth 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

2000

2050

2010

2150

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 models 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 Canals 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 (st); which itself is a function of both sampling effort
and the species abundance in year t:

st =

exp[ 0 + 1 t + 2 exp(t s )]
1 + exp[ 0 + 1 t + 2 exp(t s )]

Eq. 1

0, 1 and 2 are unknown parameters, which allow a monotonic temporal trend in


sampling effort (1 t ), and incorporates post-introduction growth in fish abundance
(2 exp(t-s)). A positive value of 1 means sampling effort has been increasing, while a
negative value means sampling effort has been decreasing. The probability st is then used
to calculate the probability that a species introduced in year s will be discovered in year t:
t 1

pst = st (1 sj )
j=s

Eq. 2

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

t = exp( 0 + 1 t )

Eq. 3

where 0 and 1 are unknown parameters. When 1 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

t = spst
s =1

Eq. 4

The Matlab code used for this model can be found in Solow and Costello (2004).
One can directly insert ones 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: 0, 1, 0, 1 and
2. From an ecological perspective, the main parameter of interest is t the expected
unobserved introduction rate which is directly derived from 0 and 1. 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 tth time interval is considered a
random variable drawn from a Poisson distribution:
Lt ~ Poisson(utRpt)

Eq. 5

whereRptis the number of potential migrants that have not yet been established in
target system at the onset of the tth 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 tth 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 = 0 + 1t
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 t in the S&C model, and is similarly derived directly from 0
and 1. Nevertheless, ut refers to a species probability (per unit time) of crossing into
the target system, while t 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 ones 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.
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70 Jonathan Belmaker, Eran Brokovich, Victor China, Daniel Golani and Moshe Kiflawi

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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
SofiaMoscow

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 worlds
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 (Fral, 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 invaders 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 (Rppell, 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 Tom.

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.
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Red-Med immigration:
a fish&parasitology
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
SofiaMoscow

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 hosts invasion and the factors governing their survival in their
hosts 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

86 Ariel Diamant

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

Red Sea

B
Mediterranean

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 parasites 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 hosts 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-

88 Ariel Diamant

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 Israels most common inshore fish, while S. luridus is less common,
abounding mainly in the countrys 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 (Kie 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

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 = 100m. Fig 3. Higher magnification of the same slide, showing
bipolar spores (H host biliary endothelium). Bar = 30m.
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 = 20m.

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 (Kie, 2000; Kie 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,

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 m. Fig. 6, Paraffin section, Gram stain, Bar = 10m; Figs. 7 and 8, Nomarski interference
microscopy, Bars = 10m.
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 = 10m.

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

12

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 = 5m. Figs. 11 and 12 show live spores in fresh bile in an individual
from the Mediterranean (Ashdod Harbor); Nomarski interference microscopy; Bars = 10m.

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.

Red-Med immigration: a fish parasitology perspective, with special reference to the Myxosporea 95

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Pais, A., P. Merella, M.C. Follesa and G. Garippa. 2007. Westward range expansion of the
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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
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98 Ariel Diamant

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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
SofiaMoscow

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.

100 Ernesto Azzurro

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; Duli et al., 1999; Duli 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 sh species with boreal afnity (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

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. Valdz. (Published by The Journal of Marine Biological Association UK 84, p.819
and by Cybium 28, p. 72).
100%
80%
60%

not reported

40%

reported

20%

h
ac

e
ra

si

te

Ag

om

Pa

en

co

nt

ur
at
m

ad
on

ity

x
Se

tu
ra

pe
m

Te

St

re

t
ita

n
io
at

ab
H

e
ur

tin

ct
D

es

Pi

ep

tio
ip
cr

es

s
er
ct
ra
D

ha
C

th

0%

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 authors 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 cant 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.

2%
2%
2%

7%

7%

N.D.

N.D.

15%

Trawl

Author or scientist

Trammelnet

5%

Longline
33%

9%

Fisherman

Purse seine
Spear
Trap

6%

23%
62%

Beam-trawl
By hand
27%

Others

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).

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

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.

110 Ernesto Azzurro

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

COMMUNITY
AWARENESS

FORTITUOUS
SIGHTINGS

ACTIVE
MONITORING

NEW REPORTS

REPORTS
VERIFICATION

NEW SAMPLES
RESEARCH
DISCARDED
REPORTS

NEW RECORDS

KNOWLEDGE

MANAGEMENT

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

Fishermen

80

Divers

70

Scientific personnel

60

% 50
40
30
20
10
0
Exotic

Native
uncommon

Native common

Unidentified

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

114 Ernesto Azzurro

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

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 115

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

116 Ernesto Azzurro

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.

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 117

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

118 Ernesto Azzurro

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

We focus on Alpha diversity (-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 (-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 (-diversity) i.e. the total biodiversity over a large area or
region

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 119

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

120 Ernesto Azzurro

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 whats 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

Unusual occurrences of fish in the Mediterranean Sea: an insight into early detection 121

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 Cl 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.
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Pensoft Publishers
SofiaMoscow

Mediterranean marine protected areas and


non-indigenous fish spreading
Patrice Francour, Luisa Mangialajo and Jrmy 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

128 Patrice Francour, Luisa Mangialajo and Jrmy Pastor

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 (Ct 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. Gunette
et al., 1998; Tegner and Dayton, 2000; Seytre and Francour, 2008).

Mediterranean marine protected areas and non-indigenous fish spreading 129

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.

130 Patrice Francour, Luisa Mangialajo and Jrmy Pastor

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 worlds 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).

Mediterranean marine protected areas and non-indigenous fish spreading 131

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.

132 Patrice Francour, Luisa Mangialajo and Jrmy Pastor

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.

Mediterranean marine protected areas and non-indigenous fish spreading 133

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

134 Patrice Francour, Luisa Mangialajo and Jrmy Pastor

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 Atlantics 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)
Gabinire (NT)
La Galre (R)
Montrmiant (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 Jrmy Pastor

Then the invaders 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 nave 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 Jrmy 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 (Duli and Pallaoro, 2004); north-east
of Tunisia (Charfi-Cheikhrouha, 2004); island of Linosa, the
Siganus luridus (Siganidae) Sicily Strait (Azzurro and Andaloro, 2004); Cape dOrlando,
northern Sicily (Castriota and Andaloro, 2005); close to
Marseille, France (Daniel et al., 2009)
Eastern Mediterranean basin (e.g. Galil, 2007); southwestern Adriatic Sea (Duli 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)

The oldest and most efficient Mediterranean MPAs are located in the western
basin (Francour et al., 2001). The fish monitoring related to MPAs showed a modified
trophic web, with a steady dominance of top-predators. The food webs are then widely
affected by trophic cascade and top-down control (Guidetti and Sala, 2007). According
to the reviewed literature, we can then hypothesize that within these old MPAs a new
non indigenous fish will be controlled by predation, although numerous intraguild predations within a complex trophic web could impair this control. In addition, MPAs appear
as privileged sites for early NIS detection through periodic and long term monitoring.
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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
SofiaMoscow

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 Napoleons chief engineer Le Pre 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.

146 Daniel Golani

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 Ada 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)

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal Lessepsian migration 147

Fig. 2. Map of the Suez Canal

148 Daniel Golani

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

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal Lessepsian migration 149

direction (Agur and Safriel, 1981). It is quite likely that the planned widening of the
Suez Canal will intensify the strength of the Canals 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 (Meri 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

150 Daniel Golani

O
L
41 LU
.1 SC
% S

S
OD
AP %
C
DE 14.1

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 1960s 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 1990s it reappeared in large numbers in the commercial catch in Egypt (El Sayad,
1994), Israel and Cyprus (Golani, 2000a) and in Turkey (Bausta 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 1970s 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

152 Daniel Golani

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 1940s (Haas
and Steinitz, 1947). Two decades later, it was still considered rare (Ben-Tuvia, 1966). By
the 1980s 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 1970s it was considered rare (Ben-Tuvia, 1978). By the end of
the 1990s 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 Peters 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 (Snchez-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
(Karachl 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 Randalls 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
Forsskls
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
(Forsskl, 1775)
DASYATIDAE
Himantura uarnak
(Forsskl, 1775)
CLUPEIDAE
Dussumieria elepsoides
Bleeker, 1849
Etrumeus teres
(DeKay, 1842)
Herklotsichthys punctatus
(Rppell), 1837
Spratelloides delicatulus
(Bennett, 1831)
CONGRIDAE
Rhynchoconger trewavasae
Ben-Tuvia, 1993
MURAENESOCIDAE
Muraenesox cinereus
(Forsskl, 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
Forsskls
Hardyhead
Silverside
Squirrelfishes
Red
Squirrelfish
Pipefishes &
Seahorses
Sea Pony

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

Hippocampus fuscus
Rppell, 1838

HOLOCENTRIDAE
Sargocentron rubrum
(Forsskl, 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
Rppell, 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
(Forsskl, 1775)

Jacks, Scades
Shrimps
Scade

Cardinalfishes
Broad-banded
Cardinalfish
Bullseye
Cardinalfish
Signal
Cardinalfish
Smiths
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
(Forsskl, 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
Klunzingers
Ponyfish
Snappers
Mangrove
Red Snapper
Thredfin
Breams
Randalls
Threadfin Bream
Goatfishes, Red
Mullet
Goldband
Goatfish
Pors
Goatfish

Golani, 2006

Israel, 2005

Indian
Scad
Arabian Scad

Decapterus russelli
(Rppell, 1830)
Trachurus indicus
Nekrasov, 1966
LEIOGNATHIDAE
Leiognathus klunzingeri
(Steindachner, 1898)
LUTJANIDAE
Lutjanus argentimaculatus
(Forsskl, 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
(Forsskl, 1775)
Rhabdosargus haffara
(Forsskl, 1775)
PEMPHERIDAE
Pempheris vanicolensis
Cuvier, 1831
EPHIPPIDAE
Platex teira
(Forsskl, 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
(Forsskl, 1775)

Common
Name

Family; Species

References

Original
distribution

Indo-Pacific

Bilecenoglu and Indo-Pacific


Kaya, 2006

Mouneimne,
1979

Antalya Bay,
Turkey, 2002

Gkoglu 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
Rppell, 1838
LABRIDAE
Iniistius pavo
Valenciennes, 1840
Pteragogus pelycus
Randall, 1981
SCARIDAE
Scarus ghobban
Forsskl, 1775
BLENNIIDAE
Petroscirtes ancylodon
Rppell, 1838
GOBIIDAE
Coryogalops ochetica
(Norman, 1927)
Oxyurichthys petersi
(Klunzinger, 1871)

Peters 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
(Forsskl, 1775)

Siganus luridus
(Rppell, 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
Mertens
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, Kovai 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
Lacepde, 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 1970s 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 (Gc 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: Dragievi and Duli 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 Duli 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 (Snchez-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

2049

5590

100

Percent Lessepsian migrants in family

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. Gc 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 Hosucu, 2003.
Saurida undosquamis
General biology: Golani, 1993a; Imen, 2002.
Feeding: Bograd-Zismann, 1965; Golani, 1993b
Growth rate: Mouneimne, 1978
Reproduction: Shenouda and Wadie, 1990; Imen, 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

Colonization of the Mediterranean by Red Sea fishes via the Suez Canal Lessepsian migration 171

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: ztok and Avar, 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; Imen, 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; Imen, 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 Takavak, 1999
Callionymus filamentosus
Growth rate: Mouneimne, 1978
Parasitology: Fischthal, 1980
Silhouettea aegyptia
General biology: Miller and Fouda, 1986

172 Daniel Golani

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 Avar, 1998; Bilecenoglu and Kaya,
2002; Bariche, 2005; Shakman et al., 2008
Reproduction: George, 1972; Popper et al., 1973; Lahnsteiner and Patzner, 1999;
Yeldan and Avar, 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
Pors 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--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 lizardfishs
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

174 Daniel Golani

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; Garca-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 Rittes 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 fishs 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. ztrk (2005) reported the occurrence
of Carangoides bajad (Forsskl, 1775), inar et al. (2006) reported Parupeneus forsskali
(Fourmanoir and Guz, 1976) and Bilecenoglu (2007) reported Monotaxis grandoculis
(Forsskl, 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 DAncona and Cavinato, 1965) and it is not found in
the Red Sea (Belyanina, 1974).
The identification of Carcharhinus amboinensis (Mller 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).

176 Daniel Golani

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Alien marine
fishes
of Turkey an updated review 189
D. Golani & B. Appelbaum-Golani
(Eds.)
2010
Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 189-217.
Pensoft Publishers
SofiaMoscow

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 1940s 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 Akyz
(1957). The 1960s 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 Akyz, 1956; Ben-Tuvia, 1966). No papers on

190 Murat Bilecenoglu

non-native fishes were published during the 1970s by Turkish scientists. The first efforts
to determine biological characters of some abundant aliens were conducted during the
1980s and 1990s, including data on the main components of the local trawl fishery (see
Bingel, 1981; Anonymous, 1983; Bingel, 1987; Gc 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.

192 Murat Bilecenoglu

Dasyatidae
Himantura uarnak (Forsskl, 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 (Forsskl, 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 20C, 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 (Forsskl, 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 (Gkoglu et al., 2003). No further observations are available
for this unmistakable species since then.
Mullidae
Parupeneus forsskali (Fourmanoir and Guz, 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 Rppell, 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 (Forsskl, 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.

194 Murat Bilecenoglu

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 1990s, 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 (Rppell, 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.

196 Murat Bilecenoglu

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; Treli and
Erdem, 1997; Cicek, 2006; Cicek et al., 2006; Sangn 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 Gc (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 Treli 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
Gksu Delta
Tirtar
NE Levant
Iskenderun Bay
Iskenderun Bay
Iskenderun Bay
Iskenderun Bay

Reference
Bingel (1981)
Bingel (1981)
Gc (1995)
Treli 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 (Forsskl, 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 Akyz (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 (Forsskl, 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).

198 Murat Bilecenoglu

Fistulariidae
Fistularia commersonii Rppell, 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 Gkova
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 Rppell, 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) (Gc 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 (Forsskl, 1775): A prevalent species at Iskenderun Bay and Mersin coasts,
known since 1983 (Gc 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 (Gc et al., 1994). It
is sometimes marketed fresh in local fishing ports.
Carangidae
Alepes djedaba (Forsskl, 1775): The Shrimp scad was first recorded from Iskenderun Bay (as Caranx kalla) by Akyz (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.).

200 Murat Bilecenoglu

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 (Gc et al., 1994). Ageing
studies indicate that the species is moderately long lived, with a maximum age of 6 for
both sexes (Oztok 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; Sangn 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 Akyz, 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; Sangn 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 Gc 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)
Gc (1995)
Kaya et al. (1999)
Ismen (2005)

202 Murat Bilecenoglu

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 (Gc 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 1950s. 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
1990s 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)

204 Murat Bilecenoglu

and the following growth parameters were estimated: L (cm) = 71.9, W (g) = 3412.7,
k= 0.26 year1, 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 (Gc 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 (Rppell, 1829): A common species at Turkish coasts, known since the
1970s. 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 Forsskl, 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).

206 Murat Bilecenoglu

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
year1, 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 Rppell, 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 Gnther, 1874: This species is commonly observed in the northern
Levant since the late 1950s. 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 (Gc 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 (Lacepde, 1800): Since the early 1980s, the Narrow-barred
Spanish mackerel has become abundant in the eastern Mediterranean Sea almost five
decades since its first record (Golani et al., 2002). Gc 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 (Akyz, 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; Sangn 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; Sangn 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

208 Murat Bilecenoglu

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 (Mller 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 (Gnther, 1866), Tylosurus choram (Rppell, 1837),
Platycephalus indicus (Linnaeus, 1758), Epinephelus tauvina (Forsskl, 1775), Pomadasys
stridens (Forsskl, 1775), Crenidens crenidens (Forsskl, 1775), Parupeneus barberinus (Lacepde, 1801), Rastrelliger kanagurta (Cuvier, 1816), Bothus pantherinus (Rppell, 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 (Forsskl, 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 1970s. 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 (Gc, 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).
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218 Murat Bilecenoglu

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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
SofiaMoscow

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-Hervs
et al., 2004; Zenetos et al., 2005; Ben Souissi et al., 2005a, 2007; Duli and Golani, 2006;
Eryilmaz and Dalyan, 2006; Golani and Sonin, 2006; Duli 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
(Mller 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
Forsskl, 1775
Hemiramphus far
(Forsskl, 1775)
Stephanolepis diaspros
Fraser-Brunner, 1940
Upeneus moluccensis
(Bleeker, 1855)
Sargocentron rubrum
(Forsskl, 1775)
Leiognathus klunzingeri
(Steindachner, 1898)
Parexocoetus mento
(Valenciennes, 1847)
Lagocephalus spadiceus
(Richardson, 1845)
Alepes djedaba
(Forsskl, 1775)
Siganus luridus
(Rppell, 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

Exocoetidae

E Rhodes

Kosswig, 1950

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
(Rppell, 1838)
Apogon pharaonis
Bellotti, 1874
Tylerius spinosissimus
(Regan, 1908)
Upeneus pori Ben-Tuvia
and Golani, 1989
Callionymus filamentosus
Valenciennes, 1837
Sphyraena flavicauda
Rppell, 1838
Etrumeus teres
De Kay, 1842

Labridae

Apogonidae

E Rhodes

Corsini et al., 2004

Tetraodontidae

C Rhodes

Corsini et al., 2005

Mullidae

E Rhodes

Corsini et al., 2005

ST

Callionymidae

E Rhodes

Corsini et al., 2005

ST

Sphyraenidae

E Rhodes

Corsini et al., 2005

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
Rppell, 1835
Tylosurus crocodilus
(Pron and Lesueur,
1821)
Iniistius pavo
(Valenciennes, 1840)
Lagocephalus sceleratus
(Gmelin, 1789)
Torquigener flavimaculosus Hardy and Randall,
1983
Scomberomorus commerson
(Lacepde, 1800)

Blennidae

E Rhodes

Corsini et al., 2005

Belonidae

Q Chalkidiki Sinis, 2005

Labridae

C Rhodes

Corsini et al., 2006

Tetraodontidae

E Rhodes

Corsini et al., 2006

Tetraodontidae

E Rhodes

Corsini-Foka et al.,
2006

Scombridae

C Rhodes

Corsini-Foka and
Kalogirou, 2008

Pempheridae

Sphyraenidae

* Based on Froese and Pauly (2008)

ES FR

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; inar 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 ztrk, 2001)
and, more recently, Oxyurichthys petersi in Gkova Bay (Akyol et al., 2006) and Sillago
sihama in Data 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 (retmen 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; inar 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; Karachl et al., 2004; Azzurro et al., 2004; Ben
Souissi et al., 2004; inar 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; Snchez-Tocino et al., 2008;
Duli et al., 2008; Present work.
Stephanolepis
+
+ + + + + +
+
+
+
*; Economidis and Bauchot, 1976; Catalano and Zava, 1993; Zaitsev and
diaspros
ztrk, 2001; Golani et al., 2002, 2006b; Duli et al., 2003; inar et
al., 2005; retmen et al., 2005; Bradai et al., 2004; zi 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 ztrk, 2001; Golani et al., 2002, 2006b;
Azzurro and Andaloro, 2004; Bradai et al., 2004; Castriota and Andaloro, 2005; retmen 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 ztrk, 2001; Golani et al., 2002, 2006b;
rivulatus
Tigilis et al., 2003; Duli et al., 2003; Bradai et al., 2004; inar et al.,
2005; retmen 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 ztrk, 2001; Golani et al., 2002, 2006b;
chrysotaenia
Duli et al., 2003; inar et al., 2005; retmen 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 ztrk, 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 ztrk, 2001; Golani et al.,
2002, 2006b; Duli et al., 2003; Galil, 2006.
*; Zaitsev and ztrk, 2001; Golani et al., 2002, 2006b; Duli et al.,
2003; Bradai et al., 2004.
*; Zaitsev and ztrk, 2001; Golani et al., 2002, 2006b; Corsini-Foka,
2004, pers. comm.; Ben Souissi et al., 2006a; Shakman and Kinzelbach,
2007.
*; Zaitsev and ztrk, 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; retmen et al., 2005; Akyol et al., 2006;
Shakman and Kinzelbach, 2007; Corsini-Foka and Economidis, 2007b;
Present work.
*; Buhan et al., 1997; Zaitsev and ztrk, 2001; Golani et al., 2002,
2006b; retmen et al., 2005; inar et al., 2005 ; Ben Souissi et al.,
2006b; Oz et al., 2007; Shakman and Kinzelbach, 2007.
*; Ondrias, 1971; Tsimenidis et al., 1991; Zaitsev and ztrk, 2001;
Golani et al., 2002, 2006b; Duli et al., 2003; retmen et al., 2005;
zi and Yilmaz, 2006; Oz et al., 2007; Shakman and Kinzelbach, 2007;
Corsini-Foka and Economidis, 2007b.
*; Zaitsev and ztrk, 2001; Golani et al., 2002, 2006b; Crete, Tingilis,
2003, pers. comm.; inar et al., 2005; Oz et al., 2007; zi 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; Duli 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; inar 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 ztrk, 2001; Torcu and
Mater, 2000; Golani et al., 2002, 2006b; zi and Yilmaz, 2006; Peristeraki et al., 2006; Zenetos et al., 2007; Oz et al., 2007; Corsini-Foka and
Economidis, 2007b; Present work.
+
+
+
Zaitsev and ztrk, 2001; Shakman and Kinzelbach, 2007.
L. carinata is not listed for the Aegean Sea in inar 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 ztrk, 2001; inar et al., 2005; Corsini-Foka and
Economidis, 2007b; Present work.
+
+
*; Oz et al., 2007; Crete, 2005, Sterioti, pers. comm.; retmen 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 (Karachl 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 (Snchez-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
Duli et al., 2004) and Terapon theraps (by Lipej et al., 2008) (Table3). 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 (Gc et al., 1994; Torcu and
Mater, 2000; Golani et al., 2002; icek 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; icek
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 1940s (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,

240 Maria Corsini-Foka

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

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 (Leppkoski 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; inar 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).
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Caspian Seas. Istanbul: TUDAV. 265 pp.
Zenetos, A., M. E. inar, 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
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ac.uk/jmba/jmba2biodiversityrecords.php

254 Maria Corsini-Foka

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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
SofiaMoscow

Fish Invasions in the Adriatic Sea


Branko Dragievi and Jakov Duli

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 Palagrua 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
10C. During the summer, the temperature of the open sea surface waters rises to 22-25C,
although extremes can be observed in the range from 3 to 29C (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 8-10C. 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

256 Branko Dragicevic and Jakov Dulcic

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 (Duli 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 (Duli 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 (Duli 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

Fish Invasions in the Adriatic Sea 257

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 Duli, 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 Kovai, 2000), Pampus argenteus (see Duli 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 Duli, 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 (Duli
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 (Duli
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
(Duli 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

258 Branko Dragicevic and Jakov Dulcic

anomalies of +0.15C and +0.30C respectively, many records of rare and new fish were
produced (Duli 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 Duli, 1996) and Balistes carolinensis (by Duli et al., 1997a)
and juvenile of Trachinotus ovatus (by Duli 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, Duli 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 (Duli 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 (Duli 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 Duli, 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 (Duli 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

9 - 10

5
8

2
3

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 Duli, 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 (Duli 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 (Duli 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 (Snchez-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 (Cervign, 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.
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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
SofiaMoscow

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 ?

vagrant

(Peron & Le Sueur, 1822)

circumtropical

Ionian Sea

vagrant

(Rppell, 1837)

circumtropical

Ionian Sea

vagrant

circumtropical

Ligurian Sea

vagrant

Indopacific

Tyrrhenian Sea, Ligurian


Sea

ship transported

Atlantic

Ligurian Sea

colonizer?

Chaunax suttkusi Caruso, 1989

Atlantic

Sicily Strait

moving North

Diodon hystrix Linnaeus, 1758

circumtropical

Ionian Sea

vagrant

Indopacific

Ionian Sea

ship transported

Indopacific

Adriatic Sea

ship transported

Indopacific

Sicily Strait

erythrean
colonizer ?

Indopacific

All Italian seas

tens

erythrean
colonizer

Atlantic

Sardinia channel

moving North

Indopacific

Ligurian Sea

vagrant

South Atlantic Ligurian Sea, Ionian Sea

ship transported

Atlantic

Sicily Strait, Tyrrhenian


Sea

moving North
colonizer?

Indopacific

Ligurian Sea

ship transported

Atlantic

Ionian Sea, Sardinia

drift fish
unclassified

Atlantic

Sicily Strait, South


Tyrrhenian

tens

colonizer

Carcharhinus falciformis
Galeocerdo cuvier

Rhizoprionodon acutus

(Mller & Henle, 1839)

Sphyrna mokarran (Rppell, 1837)


Osteichthyes
(Quoy & Gaimard, 1825)

Abudefduf vaigiensis

Lowe, 1934

Beryx splendens

Elates ransonnettii (Steindachner, 1876)


(Hamilton, 1822)

Epinephelus coioides

Etrumeus teres (Dekay, 1842)


Rppell, 1835

Fistularia commersonii
Halosaurus ovenii

Johnson, 1863

Makaira indica (Cuvier,1832)


Cuvier & Valenciennes, 1829

Pinguipes brasilianus

Pisodonophis semicinctus

(Forsskl, 1875)

Pomadasys stridens

Lutken, 1880

Psenes pellucidus
Seriola fasciata

(Richardson, 1848)

(Bloch, 1793)

Seriola carpenteri

Mather, 1971

Seriola rivoliana Cuvier, 1833


Siganus luridus (Rppell, 1829)
Sphoeroides marmoratus

(Lowe, 1838)

Sphoeroides pachygaster

(Mller & 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

moving North

Indopacific

Sicily Strait, Tyrrhenian


tens sampled
Sea

erythrean
colonizer

Atlantic

Ionian Sea

unclassified

circumtropical

All Italian seas

hundreds

moving North
colonizer

Indopacific

Ionian Sea, Sicily Strait,


South Tyrrhenian Sea

erythrean
unclassified

Indopacific

Ligurian Sea

ship transported

Atlantic

Sicily Strait

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,

Non native marine fish in Italian waters 271

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

272 Lidia Orsi Relini

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 Hawaii) 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.

Non native marine fish in Italian waters 273

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 (Duli 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 (Duli
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 aprs lapparition dun 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).

274 Lidia Orsi Relini

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?

Non native marine fish in Italian waters 275

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 1960s 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).

276 Lidia Orsi Relini

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).

Non native marine fish in Italian waters 277

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 (Massut 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

278 Lidia Orsi Relini

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 (Duli 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

Non native marine fish in Italian waters 279

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 authors 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 fishs 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

280 Lidia Orsi Relini

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 1C in the
last 30 years at surface, 0.2C in the period 1970-92 in intermediate water and 0.13C

Non native marine fish in Italian waters 281

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 authors 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 1990s,
thanks to the survival of a tuna trap of ancient Liguro-Provenal 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 1990s), 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 Duli
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),

282 Lidia Orsi Relini

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).

Non native marine fish in Italian waters 283

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 1990s
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

284 Lidia Orsi Relini

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.
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ichthyofauna: signs(Eds.)
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and meridianization 293
D.Mediterranean
Golani & B. Appelbaum-Golani
2010
Fish Invasions of the Mediterranean Sea: Change and Renewal, pp. 293-312.
Pensoft Publishers
SofiaMoscow

Changes in the western Mediterranean ichthyofauna:


signs of tropicalization and meridianization
Enric Massut, Mara 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 worlds 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

294 Enric Massut, Mara Valls and Francesc Ordines

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-Provenal 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-Provenal 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 (13-15C) during
winter, but reaching temperatures as high as 20-25C in the summer. Below depths of
200 m, the western Mediterranean is characterized by a high environmental stability,
with a temperature of 13C (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

Changes in the western Mediterranean ichthyofauna: signs of tropicalization and meridianization 295

46

44

42

40

38

Algerian

36

34
-5

10

15

20

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, LiguroProvenal 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 (0.1-0.5C), intermediate (0.05-0.2C 83 and 0.030.09 for salinity) and deep (0.03-0.1C and 0.05-0.06 for salinity) layers (Bethoux et al.,
1990, 1998; Rohling and Bryden, 1992; Rixen et al., 2005; Vargas-Yez 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.

296 Enric Massut, Mara Valls and Francesc Ordines

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 (Massut 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. LiguroProvenal; 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-Hervs et al. 2004; 8: Azzurro et al., 2004; 9: Fiorentino et al.,
2004; 10: Pais et al., 2007; 11: Ragonese et al., 2007; 12: Snchez-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

ALB & ALB


ALG
ALG
BAL & CMED

T-ATL

T-ATL

ALB

ALB, BAL & SIC

T-ATL

ALG
ALG

TYR

T-ATL
T-ATL

G
G

1
1

LIG

EMED

IP

SIC
LIG
ALB

CMED & EMED

IP
T-ATL
B-ATL

S
G
G

1
1
1

BAL

T-ATL

ALB
ALB

ALB

T-ATL
B-ATL

G
G

1
1

BAL

whole sub-basin,
CMED & EMED
ALG & EMED

T-ATL

T-ATL

TYR

ALB

298 Enric Massut, Mara 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

ALB

ALG & CMED

T-ATL

1, 2

ALB

BAL

T-ATL

1, 3

ALB

EMED & ALG

T-ATL

1, 4

TYR*
BAL

LIG

T-ATL
B-ATL

G*
G

1
1

LIG

IP

Sb

SIC

TYR, CMED &


EMED
SIC, CMED &
EMED
CMED

SIC

CMED

IP

1, 2

T-ATL

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

SIC

IP

SIC

TYR, ALB, BAL,


CMED & EMED
CMED & EMED

IP

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

SIC

T-ATL

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 Massut, Mara 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

42

42

40

40

38

4
6

36

38
S Adriatic
S Tunisia
SE Aegean
E Levant

34

36

1 2

34
-5

10

15

20

46

-5

10

15

20

15

20

46

S. fasciata

P. pellucidus

44

44

42

40

40

38

42

36

38
Ionian
S Tunisia
E Levant

34

1
2

36
34

-5

10

15

20

-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: Massut et al., 1993; 6: Ragonese and Giusto, 1999); Seriola
fasciata (1: Massut 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 Massut, Mara 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 Massut, Mara 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. Abell, 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, Sabats 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 Massut, Mara 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 (Snchez-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 415N), 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 (Duli et al., 1999) and
in the adjacent Atlantic waters (Ban et al., 1997; Quro, 1998; Quro 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 Abell (CSIC- Institut de Cincies del Mar), for the
information on Sprattus sprattus and Carlos Barcel, for his assistance in the laboratory.

308 Enric Massut, Mara 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
SofiaMoscow

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 1990s, 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,

314 George Minos, Anastasia Imsiridou and Panos S. Economidis

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 Eschmeyers 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
15.8-20.7C, 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 23-29m

Fig. 1. Schematic map of the native waters of the Redlip mullet and enlargement of the Primorskiy
region. (1) Tesnaya river; (2) Razdolnaya 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
1.01mm (average 0.93mm) and the diameter of the oil drop from 0.34 to 0.54mm
(average 0.44mm) (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 Razdolnaya subpopulation winters in the
Razdolnaya 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 duri