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1. Introduction
The introduction of species from one biogeographic region to another has been
recognized as a major threat to ecosystems, with a set of ecological and evolutionary
consequences from species to ecosystem levels (Grosholz, 2002; Ehrenfeld, 2010).
Introduced species have different degree of impacts in the recipient area and can be
classified as established, casual and invasive alien species according to their success of
establishment and invasive potential (Zenetos et al., 2005). Invasive alien species that are
capable of overcoming biotic and abiotic barriers in their new environments and have
noticeable ecological and economic impacts are accepted one of the most serious threats
to the conservation of natural resources (Lodge, 1993).
The Mediterranean Sea is considered as one of the hot-spot areas in terms of the
alien species diversity (inar, 2013) and almost 1000 alien species have been reported
from the region up to date, with the eastern basin being more prone to invasion than the
western basin as it has more than one pathway for the introduction of the species (Zenetos
et al., 2010). The most important pathway through which alien species have been
continuously entering into the Mediterranean without any decisive filtering mechanism
is the corridor, called Suez Canal. The majority of alien species (more than 70%-80%)
reported from the eastern part of the Mediterranean Sea have been introduced into the
area via the Suez Canal (called as Lessepsian species/invaders, inar et al., 2011; Zenetos
et al., 2012). In July 2015, the Suez Canal has been greatly enlarged with the construction
of a new canal paralleled to the older one. It was foreseen that this enlargement initiative
would facilitate the entrance of more (so-called double) Lessepsian invaders to the
Mediterranean Sea that might cause major, irreversible ecological and economic
consequences in the region (Galil et al., 2015).
Having a great habitat richness and different environmental conditions between its
northern and southern points, the Aegean Sea offers a suitable area for a variety of living
forms and acts as a crossroad for the thermophilic and psychrophilic marine species
(Kocata and Bilecik, 1992). Its interaction with the Levantine Sea and Black Sea through
different current systems, it represents a complex and dynamic ecosystem with additions
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of Indo-Pacific species predominantly drifting to the area by means of the Asian Minor
current. inar et al., (2011) estimated that 58% of total number of alien species reported
from the eastern Aegean Sea were the species first entered into the Mediterranean via the
Suez Canal and expanded their distributional ranges to the Aegean Sea by natural
dispersal processes.
This paper focuses on the alien species diversity along the eastern Aegean Sea coast
and their actual impacts on the native biota.
2. History of studies on alien species in the area
The first alien species in the eastern Aegean Sea was reported by Quatrefages
(1865), who reported the invasive serpulid species, Hydroides dianthus (cited as Serpula
uncinata) in zmir Bay. The other alien speciess reports in the region were begun after
the mid-20th century with the studies focusing on fishes by Tortonese (1947), Kosswig
(1950), Ben-Tuvia (1966) and Geldiay (1969). After 1970, alien species other than fish
were begun to be reported. Between 1970 and 1975, 5 algae, 2 crustaceans and 3 fish
were recorded from the area. By the year 1975, the eastern Aegean Sea coast included 29
alien species (Figure 1). After 10 years later, the total number was increased to 40, mainly
thanks to the studies by Marinopoulos (1979) and Zeybek et al. (1986). Almost a similar
number of alien species (ca. 19 species) was reported along the Aegean coast at ten years
intervals between 1965 and 1995. The first sharp increase in the number of recorded alien
species was detected between 1995 and 2005, when the cumulative number of species by
1996 was doubled, bringing the number of species known from the area to 123. The main
contributors (>4 species reports) within this interval were Meri et al. (2004) and Oku
et al. (2004). During the last ten years (2005-2015), 99 new alien species (3 algae, 22
protozoans, 65 invertebrates and 9 fish) were reported from the Aegean coast of Turkey.
Figure 1. Yearly and cumulative changes in the number of new records of alien
species along the eastern Aegean Sea.
637
638
Table 1. The new additions of alien species to the inventory of the Aegean coast of
Turkey after the study by inar et al. (2011) and their first year of observations (FYO).
ES: Establishment Success (E: Established, C: Casual, Cr: Cryptogenic), O: Origin (IP:
Indo-Pacific, RS: Red Sea, EA: Eastern Atlantic; AT: Atlantic, WA: Western Atlantic,
IO: Indian Ocean, PO: Pacific Ocean, CT: Circumtropical, Co: Cosmopolitan) MI= Mode
of Introduction (Su: Suez Canal, S: Shipping, Aq: Aquaculture), H: Habitat [Hs: Hard
Substratum (including algae and sponges), Ss: Soft Substratum (including
phanerogames), P: pelagic, Pz: parasite], DR: Depth Range (I: 010 m, II: 1150m, III:
51100 m).
Alien Species
ALGAE
Chlorophyta
Caulerpa taxifolia (M.Vahl) C.Agardh, 1817
Codium parvulum (Bory de Saint Vincent ex
Audouin) P.C.Silva, 2003
Codium taylorii P.C.Silva, 1960
PROTOZOA
Foraminifera
Acervulina inhaerens Schulze, 1854
Cymbaloporetta squammosa (d'Orbigny, 1826)
Iridia diaphana Heron-Allen & Earland, 1914
Polymorphina fistulosa (Cushman, 1914)
Spiroloculina cf. angulata Cushman, 1917
Ciliata
Leprotintinnus nordqvistii Brandt, 1906
Rhizodomus tagatzi Strelkow & Wirketis, 1950
CNIDARIA
Hydrozoa
Eudendrium merulum Watson, 1985
Sertularia marginata (Kirchenpauer, 1864)
Clytia linearis (Thorneley, 1900)
Filellum serratum (Clarke, 1879)
Scyphozoa
Cassiopea andromeda (Forsskal, 1775)
Phyllorhiza punctata Lendenfeld, 1884
Rhopilema nomadica Galil, Spanier & Ferguson,
1990
Anthozoa
Diadumene lineata (Verrill, 1869)
POLYCHAETA
Prosphaerosyllis longipapillata (HartmannSchrder, 1979)
Ceratonereis mirabilis Kinberg, 1866
Glycinde bonhourei Gravier, 1904
Diopatra marocensis Paxton, Fadlaoui & Lechapt,
1995
FYO
ES
MI
20101
PO
Hs/Ss
I,II
20122
PO
Su
Hs
20113
WA
Hs
20044
20025
20086
20127
20044
E
E
E
E
E
IP
IP
IP
IP
IP
?S
?Su
?S
?S
Su
Ss
?
?
Ss
?
I
I
I
I
I,II
20078
20078
E
E
?AT
?AT
S
S
P
P
I
I
20009
197710
197710
197710
E
E
E
C
CT
CT
CT
CT
?Su
?Su
?Su
?Su
Hs
Hs
Hs
Hs
I
I
I
I
201111
201112
E
C
RS/IP
RS
Su
Su
Ss,P
P
I
I
201113
RS/IP
Su
199714
AT
Hs
200415
PO
Ss
I,II
201116
200917
200518
E
E
E
RS/IP
RS/IP
AT
Su
Su
?S
Ss
Ss
Ss
III
I
I,II
639
CRUSTACEA
Alien Species
Copepoda
Calanopia elliptica (Dana, 1849)
Labidocera pavo Giesbrecht, 1889
Pseudocalanus elongatus (Boeck, 1865)
Amphipoda
Elasmopus pectenicrus (Bate, 1862)
Monocorophium sextonae (Crawford, 1937)
Tanaidacea
Paradoxapseudes intermedius (Hansen, 1895)
Decapoda
Alpheus lobidens de Haan, 1849
MOLLUSCA
Gastropoda
Alvania dorbignyi (Audouin, 1826)
Rissoina bertholleti Issel, 1869
Crepidula fornicata (Linnaeus, 1758)
Retusa desgenettii (Audouin, 1826)
Pyrunculus fourierii (Audouin, 1826)
Monotygma lauta (Adams, A., 1853)
Odostomia lorioli (Hornung & Mermod, 1924)
Chelidonura fulvipunctata Baba, 1938
Cylichnina girardi (Audouin, 1826)
Elysia tomentosa Jensen, 1997
Bivalvia
Arcuatula senhousia (Benson in Cantor, 1842)
Malleus regula (Forsskl in Niebuhr, 1775)
Spondylus spinosus Schreibers, 1793
Crassostrea gigas (Thunberg, 1793)
ECHINODERMATA
Diadema setosum (Leske, 1778)
TUNICATA
Phallusia nigra Savignyi, 1816
Microcosmus exasperatus Heller, 1878
PISCES
Ostorhinchus fasciatus (White, 1790)
Rachycentron canadum (Linnaeus, 1766)
Nemipterus randalli Russell, 1986
Champsodon nudivittis (Ogilby, 1895)
Champsodon vorax Gnther, 1867
Callionymus filamentosus Valenciennes, 1837
Platax teira (Forsskl, 1775)
Cynoglossus sinusarabici (Chabanaud, 1931)
Torquigener flavimaculosus Hardy & Randall, 1983
FYO
ES
MI
199919
199919
200020
?E
E
Cr
WA
IP
EA
S
Su
S
P
P
P
I
I
I
199521
199521
C
E
CT
PO
Su
S
Hs
Hs/Ss
I
II
197622
AT
?S
Hs, Ss I,II
201423
IP/RS
Su
Ss
200024
200125
201226
200227
200227
201428
199529
200430
199631
200232
Cr
E
E
E
E
E
C
E
E
E
Co
RS/IO
AT
RS/IP
RS/IP
RS/IP
RS
IP
IP
?IP
?
Su
S
Su
Su
Su
?Su
?Su
Su
?Su
Ss
Ss
Ss
Ss
Ss
Pz
Ss
Ss
Ss
Hs
I
I
I,II
I
I
I,II
I,II
I,II
II
I,II
201233
200232
200232
2001
E
E
E
E
IP
RS/IP
RS/IP
PO
S
Su
Su
Aq
Ss
Hs
Hs
Hs
I
I
I,II
I
201435
RS/IP
Su
Hs
201111
200436
E
E
RS/IP
RS/IP
Su
Su
Hs
Hs
I,II
I
201137
201338
201137
201039
201440
201041
200642
201441
201441
E
C
E
E
C
C
C
C
C
RS/IP
CT
RS/IP
IP/IO
IP/IO
RS/IP
RS/IP
RS/IP
RS/IP
Su
Su
Su
?Su
?Su
Su
Su
Su
Su
Ss
P
Ss
Ss
Ss
Ss
Hs
Ss
Ss
I,II
II,III
I,II
II,III
III
II
II
II
II
1. Turan et al., 2011; 2. Aydoan and Takn, 2015; 3. Takn and Aydoan, 2012; 4.
Meri et al., 2008a; 5. Meri et al., 2008b; 6. Meri et al., 2010; 7. Meri et al., 2012; 8.
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Yurga, 2012; 9. Marques et al., 2000; 10. Marinopoulos, 1979; 11. Gozceliolu, 2011;
12. Gulahin and Tarkan, 2012; 13. Gulahin and Tarkan, 2011; 14. Sar et al., 2001; 15.
inar et al., 2014a; 16. inar and Dagli, 2012; 17. inar et al., 2012; 18. inar et al.,
2014b; 19. Aker, 2002; 20. Benli et al., 2001; 21. Doan et al., 2008; 22. Kocata, 1976;
23. Bakir et al., 2015; 24. Erol-zfuucu et al., 2003; 25. Koak and Kataan, 2005; 26.
Doan et al., 2014; 27. Crocettaand Tringali, 2015; 28. ztrk et al., 2014; 29. ztrk et
al., 2013; 30. Oku et al., 2006; 31. Buzzurro and Greppi, 1996; 32. Oku et al., 2004;
33. Doan et al., 2014; 34. Doan et al., 2007; 35. Yapici et al., 2014; 36. Ramos-Espla
et al., 2013; 37. Bilecenolu and Yoke, 2013; 38. Akyol and nal, 2013; 39. Filiz et al.,
2013; 40. Aydn and Akyol, 2015; 41. Bilecenolu et al., 2014; 42. Bilecenolu and Kaya,
2006.
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Figure 4. The origins of alien species reported from the eastern Aegean Sea. IP/RS:
Indo-Pacific/Red Sea, AT: Atlantic, CT: Circumtropical.
Being a neighbor on the Levantine Sea, the Aegean Sea receives high number of
alien species that were entered into the Mediterranean Sea from the Red Sea via the Suez
Canal (Lessepsian invaders). A total of 136 Lessepsian invaders (61% of total number of
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alien species) were found along the eastern Aegean Sea (Figure 5). Species introduction
via shipping comprised 35% of total number of alien species in the area. The introductions
of three species (Crassostrea gigas, Ruditapes philippinarum and Liza haematocheila)
were attributed to escapes from the aquaculture facilities. They extended their
distributional ranges to other Mediterranean and Black Sea environments later on. It is a
requisite to re-evaluate if the eastern Atlantic species that were entered into the
Mediterranean Sea via Gibraltar are alien species, as no anthropogenic vectors are
involved in their introductions. Two fish (Enchelycore anatina and Sphoeroides
pachygaster) and one decapod crustacean (Processa macrodactyla) species were claimed
to have been introduced to the Mediterranean via Gibraltar. As E. anatina solely occurs
in the eastern Mediterranean, Gibraltar as a pathway (corridor) for the introduction of this
species seems to be unlikely, but an anthropogenic vector such as shipping or aquarium
release could be incorporated with the introduction of this species to the eastern part of
the Mediterranean. However, S. pachygaster and P. marcodactyla, which are distributed
along the eastern Atlantic coasts, might have been naturally entered into the
Mediterranean Sea and expanded their distributional range within the basin, so they could
be accepted as native rather than alien species. Their first reports came from the Alboran
Sea, suggesting their entrance to the Mediterranean by means of natural dispersal
mechanism. However, we kept these species in the list at time being and will re-evaluate
their alien status in the future.
Figure 5. The relative importance of pathways for the introduction of alien species
to the eastern Aegean Sea.
The percentages of Lessepsian invaders vary among the taxonomic groups. For
instance, Lessepsian invaders comprised 100% of total number of species in
Echinodermata; 93% in Pisces; 88% in Cnidaria; 65% in Foraminifera. Ship-mediated
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species are important in polychaetes and algae, accounted for up to 70% and 55% of total
number of alien species, respectively.
5. Habitat and depth preferences of alien species
The highest number of alien species were encountered on soft (83 species, 37% of
total number of species) and hard substrata (65 species, 29%). Twenty-nine alien species
were common on hard and soft substrata. All jellyfish and copepods, and some fish (nine
species) occurred in the pelagic environment. Two pyramidellid gastropods (Monotygma
fulva and M. lauta) are known to be parasite on some echinoderms and bivalves (ztrk
et al., 2014). The habitats of 23 alien species (mainly foraminiferans) were unknown.
Majority of alien species were found in association with shallow water-benthic
habitats (0-50 m) (Figure 6). Thirty-three species were found at depths deeper than 100
m. Fourteen alien species were capable of occurring at depths between 101 and 200 m.
Sphoeroides pachygaster has the widest depth distributional range, inhabiting depths
from 0 to 400 m.
Figure 6. The depth preferences of alien species along the eastern Aegean Sea.
6. Invasive alien species and their impacts
According to the Zenetoss (2012) classification of invasive alien species in the
Mediterranean Sea, the species list of the eastern Aegean Sea included a total of 71
invasive or potentially invasive species. Majority of these species have become highly
invasive along the Levantine coast of Turkey, but a few number of them have sustained
a proliferated population and become invasive species in habitats of the Aegean Sea.
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Higher numbers of invasive species (mainly polychaetes) were reported from the polluted
inner part of Izmir Bay, where 6 polychaete (Streblospio gynobranchiata, Polydora
cornuta, Prionospio pulchra, Pseudopolydora paucibranchiata, Hydroides elegans and
H. dianthus), 1 crustacean (Metapenaeus affinis) and 1 mollusc (Anadara transversa)
species invaded the soft and hard substrata in the area. The invasive polychaetes
comprised more than 90% of total zoobenthic populations in the majority of samples
collected at some sites near Alsancak Harbour (inar et al., 2006; Dal and inar, 2008;
Dal et al., 2011). The population densities of H. elegans and S. gynobranchiata reached
up to 111,000 ind.m-2 and 61,000 ind.m-2 in the area, respectively (inar et al., 2006;
2008).
High number of individuals of the jinga shrimp Metapenaeus affinis were caught
with a trammel net set in a muddy bottom at depths 812 m in the inner part of Izmir Bay
in 2008 (Aydn et al., 2009). As its distribution was only confined to Alsancak Harbour
and its vicinity, its introduction to the area via ballast water of ships was hypothesized.
Although the inner part of Izmir Bay is banned for any fishing activity, illegal fishing of
this shrimp in the area is still continuing and it coasts ca. 35 /per kg in the market. As
the shrimp is highly demanded by local consumers, it was said that local fishermen had
translocated it outside zmir Bay (Aliaa) to fish it outside the banned area, but no
documented report is available regarding its presence outside the inner part of Izmir Bay
yet.
Anadara transversa is a dominant component of benthic communities in the inner
and middle parts of the zmir Bay (inar et al., 2006). The identification of this species
in the area has a long story. It was begun when Dr. Ahmet Kocata (Ege University, zmir)
sent a large number of the arcid specimens to Dr. Muzaffer Demir (stanbul University,
stanbul) in spring 1978, who was the expert of this group in Turkey at that time. After a
long examination, he quoted it could be either Arca (Scapharca) transversa Say, 1822 or
Arca (Scapharca) amygdalum Philippi, 1847. However, I was not able to decide which
one it was and then he sent some specimens to Dr. B. Metivier at Museum dHistoire
Naturelle (Paris) and he finally identified them as A. (S.) amygdalum (Demir, 1977).
However, this species name for the Mediterranean population of the species was used for
a short time. A new name Scapharca demiri was proposed for Arca amygdalum since this
name was pre-occupied for other species of Arca (Piani, 1981). Thanks to molecular tools,
Albano et al. (2009) postulated that the specimens previously identified as S. demiri in
the Adriatic, Greece and Turkey in fact belonged to A. transversa, a common species of
the eastern coasts of North America. Scapharca demiri then became a junior synonym of
A. transversa. This species prefers inhabiting semi-polluted bottom of zmir Bay. Demir
(1977) reported that it occurred dominantly in gray-muddy bottom (300 ind.m-2) and
became scarce in areas where sediment colour was turned into black because of high
organic inputs (30 ind.m-2). inar et al. (2006) found a high density of this species (580
ind.m-2) near the boundary between the middle part and inner part of zmir Bay.
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The invasive green alga Caulerpa cylindracea is one of the invasive species that has
a wide distributional range along the eastern Aegean Sea, occurring throughout the
coastline from Dalaman River to the entrance of anakkale Strait (inar et al., 2005), but
it covers large benthic areas at some localities such as Ildr Bay, where intense fish
farming activities take place. It has invaded both soft and hard substrata and extended to
depths from shallow water down to 40 m. Not only does it cover many habitats (such as
Posidonia oceanica meadows, bare sand, rocks) like a carpet, but also it blocks pores of
many sponge species with its elongated stolons and rhizoids, eventually resulting in mass
deaths or local necrosis (personal observation ME, Figure 7). Ulas et al. (2012) found
that biomass of C. cylindracea increased with increasing depth in zmir Bay and its
biomass (635 g.m-2) estimated at 25 m depth were five times higher than those at 5 m
depth.
646
the Aegean Sea by Turan et al. (2011). This species was found in summer 2010 in Yolluca
Social Facility Command belonging to the Turkish Navy Forces located near emealt
Port and covered an area of 35 m2. The morphology of this species is similar to Caulerpa
taxifolia var. distichophylla, which were first reported in skenderun Bay within the
Mediterranean Sea (evik et al., 2007). However, it was claimed that the alga found in
zmir Bay belonged to the western Mediterranean strain of C. taxifolia (G. Turan, pers.
comm.). We do not know at this stage if it still occurs in the area or has a potential to
invade the benthic habitats like in the western Mediterranean. For this, a monitoring study
is urgently required.
The phanerogame Halophila stipulacea is one of the successful invaders in the
Aegean Sea. It forms dense beds in some areas like Ildr Bay (ME, personal
observation) and extended its northern limit around Dikili (Akal and Cirik, 2007). Its
impact on the native biota has not been a subject of study in the eastern Aegean Sea.
Hot water springs along the coast of Kuadas attracts dense settlements of some
alien foraminiferan species. Amphistegina lobifera formed a dense population density
near the spring (1954 specimens per 5 g of sediment) and its density sharply decreased
when moving away from the spring (Meri et al., 2010). This species also covered
coralligenous habitats in Ildr Bay (personal observation, ME). It has a wide
distributional range in the area and also occurs in the Sea of Marmara (inar et al., 2011).
A single specimen of Rhopilema nomadica, which constitutes great swarms almost
in each summer in the Levantine Sea, was recently reported from Gkova Bay (Gulsahin
and Tarkan, 2011). One specimen of this species was also captured in the inner part of
zmir Bay in 2003 (ME, unpublished record). Though it is an invasive species along the
Levantine coasts and has great impacts on human health and fisheries by obstructing
fishing nets and covering catches with their stinging mucous, it can be classified as a
casual alien species along the eastern Aegean Sea at the time being. We do not know if it
will form a massive bloom in the colder water of the Aegean Sea in the future. The other
jellies such as Cassiopea andromeda and Phyllorhiza punctata were also represented by
a few number of specimens along the Aegean Sea (Gzceliolu 2011; Gulsahin and
Tarkan 2012). The former species extended its distributional range to Gllk Bay (zgr
zbek and ztrk 2015).
The siganids Siganus rivulatus and S. luridus were reported from the southeastern
Aegean Sea more than 40-60 years ago, but they have not formed dense populations in
the area. It is possible to observe siganid schools (both species) from Marmaris to entire
Data coasts up to Bodrum (personal observations, ME+MB), which swiftly decrease
towards Kuadas. It was only S. rivulatus that extended its distribution to northern
Aegean Sea (andarl Bay) (Bilecenolu, 2010).
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653
Edited by
Tuncer KATAAN Ege University
Adnan TOKA Ege University
kr BEKTEPE Dokuz Eyll University
Bayram ZTRK Istanbul University
Publication No: 41
Istanbul 2015
Bu kitabn btn haklar Trk Deniz Aratrmalar Vakfna aittir. zinsiz baslamaz, oatlamaz.
Kitapta bulunan makalelerin bilimsel sorumluluu yazarlara aittir.
All right are reserved. No part of this publication may be reproduced, stored in a retrieval system,
or transmitted in any form by any means without the prior permission from the Turkish Marine
Research Foundation (TDAV). Authors are responsible for their articles conformity to scientific
rules.
Editor and Publisher cannot be held responsible for errors or any consequences arising from the
use of the information contained in this book; the views and opinions expressed do not necessarily
reflect those of Editors and Publisher.
Copyright: Trk Deniz Aratrmalar Vakf (Turkish Marine Research Foundation)
ISBN-978-975-8825-33-2
Citation:
Kataan, T., Toka, A., Beiktepe, ., ztrk, B. (Eds.) (2015). The Aegean Sea
Marine Biodiversity, Fisheries, Conservation and Governance. Turkish Marine
Research Foundation (TUDAV), Publication No: 41, Istanbul, TURKEY.
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