Harmful algal blooms (HABs) and mucilage formations in the Sea of Marmara

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THE SEA OF MARMARA
MARINE BIODIVERSITY,
FISHERIES, CONSERVATION
AND GOVERNANCE
Edited by
Emin ÖZSOY- Middle East Technical University
M. Namık ÇAĞATAY- Istanbul Technical University
Neslihan BALKIS – Istanbul University
Nuray BALKIS– Istanbul University
Bayram ÖZTÜRK – Istanbul University
Publication No: 42
Istanbul 2016

ii
THE SEA OF MARMARA
MARINE BIODIVERSITY, FISHERIES,
CONSERVATION AND GOVERNANCE
Bu kitabın bütün hakları Türk Deniz Araştırmaları Vakfı’na aittir. İzinsiz basılamaz, çoğatılamaz.
Kitapta bulunan makalelerin bilimsel sorumluluğu yazarlara aittir.
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or transmitted in any form by any means without the prior permission from the Turkish Marine
Research Foundation (TÜDAV). Authors are responsible for their articles’ conformity to scientific
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reflect those of Editors and Publisher.
Copyright: Türk Deniz Araştırmaları Vakfı (Turkish Marine Research Foundation)
ISBN 978-975-8825-34-9
Citation: Özsoy, E., Çağatay, M.N., Balkıs, N., Balkıs, N., Öztürk, B. (Eds.) (2016). The Sea of
Marmara; Marine Biodiversity, Fisheries, Conservation and Governance. Turkish Marine Research
Foundation (TUDAV), Publication No: 42, Istanbul, TURKEY.
Cover page: Yazın ÖZTÜRK
Turkish Marine Research Foundation (TUDAV)
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HARMFUL ALGAL BLOOMS (HABs) AND MUCILAGE FORMATIONS
IN THE SEA OF MARMARA
Seyfettin TAŞ1*, Halim Aytekin ERGÜL2 and Neslihan BALKIS3
1Institute of Marine Sciences and Management, Istanbul University
2 Faculty of Sciences and Arts, Department of Biology, Kocaeli University
3Department of Biology, Faculty of Science, Istanbul University
*stas@istanbul.edu.tr
1. Introduction
Photosynthetic algae support healthy aquatic ecosystems by forming the base of
the food web, fixing carbon and producing oxygen. Under certain circumstances, some
species can form high-biomass and/or toxic proliferations of cells (or “blooms”), there-
by causing harm to aquatic ecosystems, including plants and animals, and to humans via
direct exposure to water-borne toxins or by toxic seafood consumption (Kudela et al.
2015). Microalgae that may have a deleterious effect on other aquatic species or humans
are termed 'harmful algae'. This encompasses a number of different algae taxa such as
diatoms, dinoflagellates, haptophytes and cyanobacteria (Kraberg et al. 2010).
Algal blooms may appear yellow, brown, green, blue or milky in color,
depending upon the causative organisms. Most water discolorations are caused by
motile or strongly buoyant species. Dense algal concentrations are most strongly
developed under stratified stable conditions, at high temperatures and following nutrient
input from land run-off after heavy rains and/or domestic discharges in coastal marine
ecosystems. Most of these algal blooms appear to be harmless events, but under
exceptional conditions, non-toxic bloom-formers may become so densely concentrated
that they constitute anoxic conditions that cause fish and invertebrates kills in sheltered
bays. The essential problem for algal blooms is the production of toxins by certain
species (especially dinoflagellates). In this case, even low densities of toxic algae in the
water column may be sufficient to cause illnesses in humans as Paralytic Shellfish
Poisoning (PSP), Amnesic Shellfish Poisoning (ASP), Neurotoxic Shellfish Poisoning
(NSP), Diarrhetic Shellfish Poisoning (DSP), Ciguatera Fish Poisoning (CFP) and
Azaspiracid Poisoning (AZP). PSP can result from eating either shellfish, and
planktivorous, while, DSP, NSP, AZP and ASP are caused by eating shellfish, ciguatera
by eating tropical fish. Another group of toxins (Ichthyotoxins) selectively kill fish by
inhibiting their respiration (Hallegraeff 2002).
Proliferations of microalgae in marine or brackish waters can cause massive fish
kills, contaminate seafood with toxins, and alter ecosystems. A broad classification of

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harmful algal blooms (HABs) distinguishes two groups of organisms: the toxin
producers, which can contaminate seafood or kill fish, and the high-biomass producers,
which can cause anoxia. Many coastal region of the world is affected by HABs
commonly called red tides. HABs are most common in coastal marine ecosystems as
well as brackish and freshwater ecosystems. Most HAB events are caused by blooms of
microalgae, including certain cyanobacteria (blue-green algae). HAB events are
typically associated with rapid proliferation of toxic or otherwise noxious microalgae at
the sea surface or in the water column. Even low cell numbers of highly toxic
planktonic species or accumulations of cells on benthic substrates may cause problems.
Certain HAB species can directly release compounds that are not toxins and non-toxic
HABs cause damage to ecosystems (Anderson et al. 2012). Ecosystem damage by high-
biomass blooms may include, for instance, disruption of food webs, fish-killing by gill
damage, oxygen depletion after bloom degradation. Some species also produce potent
natural chemicals (toxins) that can persist in the water or enter the food web, leading to
illness or death of aquatic animals and/or human seafood consumers (Kudela et al.
2015). The most damaging HABs are those caused by toxin-producing microalgae
species. The number of species that normally or perhaps only under specific
environmental conditions, contain toxins is quite low (~100). Toxins produced by HAB
can be transferred within aquatic food chains. Their toxin content varies depending on
the N and P concentrations in the water. Intracellular toxin content in HAB species has
been shown to increase when the cells grow under nitrogen and/or phosphorus
unbalanced conditions (Granéli 2004).
In recent years, red tide events in coastal waters of the Sea of Marmara have
been frequently observed particularly in spring and summer. In the previous studies on
phytoplankton have been found a certain number of harmful species (Balkis 2003;
Aktan et al. 2003, 2005; Tas and Okus 2004; Tas et al. 2006, 2009, 2011; Turkoglu
2008; 2010a, b; 2013; Deniz and Tas 2009; Turkoglu and Oner 2010; Turkoglu and
Erdogan 2010; Kucuk and Ergul 2011; Balkis and Toklu-Alicli 2014; Tas 2015; Tas and
Yilmaz 2015; Tas and Lundholm 2016). Studies on harmful algal blooms including
cyanobacteria showed that water discoloration, light attenuation, supersaturated
dissolved oxygen (Tas and Okus 2011; Ergul et al. 2014, 2015; Tas 2015; Tas and
Yilmaz 2015) and mucilage formations (Aktan et al. 2008; Tüfekci et al. 2010; Balkis
et al. 2011) were major effects on the ecosystem. A study investigated the influence of
Noctiluca scintillans, a well-known red tide dinoflagellate species, on the abundance,
diversity, and community structure of meso-zooplankton in the Sea of Marmara
(Yilmaz et al. 2005).
In the recent years, studies on dinoflagellate cysts in sediment conducted in the
Sea of Marmara. In one of these studies, cysts belonging to the Cochlodinium genus,
which are toxic and not observed in Turkish Seas, have been detected (Balkis et al.
2016). In a recent study, a bio-toxin caused by microalgae, domoic acid (DA), a

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neurotoxin produced by the diatom genus Pseudo-nitzschia, which caused to Amnesic
Shellfish Poisoning (ASP) was detected in the Sea of Marmara (Dursun et al. 2016).
There is also some non-toxic but potentially harmful species, i.e., bloom forming
species which can reach very high abundances can cause discoloration of water and
light attenuation. Non-toxic bloom formers can generate anoxic conditions that cause
kills of fish and invertebrates at the bottom during decay of the algal bloom.
The main goal of this review study is to summarize the distribution of harmful
algae, algal blooms, mucilage events and harmful effects in the Turkish Strait Systems
in the light of the studies made so far.
2. Potentially harmful microalgae and HAB events in the Sea of Marmara
The Sea of Marmara is located between the Black Sea and Aegean Sea, where
saline lower layer originating from Mediterranean Sea is overlaid with brackish waters
from the northwestern Black Sea. The system is permanently stratified together with the
Straits (İstanbul and Çanakkale) and the coastal embayment, and changes from meso- to
eutrophic conditions depending on the location and the season (Tufekci et al. 2010).
İzmit Bay is located at the northeastern edge of the Sea of Marmara and is a 50
km length. The Bay is divided into 3 regions: western, central and eastern. The eastern
part is 6 km wide and 11 km long on average and a maximum depth of 40 m. The
central part is the widest (up to 12 km) and the longest (up to 25 km) in the Bay and the
deepest point is 208 m. The Western Basin is connected to the Sea of Marmara. It is a
12 km long and up to 11 km wide basin deepening towards the West (Kuscu et al.
2002).
During last 40 years, industrial development and intense urbanization have
occurred around İzmit Bay. Consequently, extensive water, air, and soil pollution has
occurred. Many major sources of pollution are located around the coast, carrying
domestic waste together with effluents from industrial plants such as petroleum
refineries, and shipyard, cement, fertilizer, chlor-alkali, metal, pesticides, detergent, dye
etc. factories. In addition, the Bay is also under pressure from heavy shipping activities
(Tufekci et al. 2010). The situation mentioned above influences the water quality and
cause to the eutrophication in İzmit Bay. As a consequence, the appropriate conditions
for bloom events in some certain species mainly dinoflagellates may occur in this area.
The previous studies on phytoplankton community carried out in İzmit Bay showed that
some potentially harmful and/or bloom-forming species have been commonly observed
(Artuz and Baykut 1986; Tas and Okus 2004; Aktan et al. 2005, 2008; Tufekci et al.
2010, Kucuk and Ergul 2011; Ergul et al. 2014; Ergul et al. 2015). The first HAB event
in the İzmit Bay caused by Noctiluca scintillans (reported as N. miliaris) was reported
by Artuz and Baykut (1986).

771
In a phytoplankton study performed in İzmit Bay between 1999 and 2000
reported that a dense bloom caused by dinoflagellate Prorocentrum scutellum occurred
in the east part of İzmit Bay. In this bloom event was suggested that the abundance of P.
scutellum reached 2.4×106 cells L-1 and a strong discoloration was observed. As a result
of this study, it is highlighted that highly eutrophication particularly in the eastern İzmit
Bay stimulates the phytoplankton blooms mainly in dinoflagellates (Tas and Okus
2004). In another study performed between February 1999 and September 2000, it was
suggested that the İzmit Bay was characterized by intensive dinoflagellate (mainly
Prorocentrum spp.) dominated bloom in all sampling period (Aktan et al. 2005). In
September 1999, it has been reported that P. scutellum was the dominant and reached
~410×103cells L-1 at the east part of the Bay. Other common Prorocentrum species were
P. micans and P. cordatum (reported as P. minimum), which are known potentially
harmful species and during the study 14 toxic and harmful species were recorded in
İzmit Bay. Authors also reported that red tides caused by Prorocentrum species were
observed in some periods, but other noxious algal blooms were not recorded during the
study period (Aktan et al. 2005). In the recent studies, the dense dinoflagellate blooms
were reported from the İzmit Bay. Prorocentrum micans formed dense blooms in March
2014 and in May 2015 and caused to brownish-red water discoloration. At the same
area, the bloom of Noctiluca scintillans occurred in mid-April 2014, with the pale red
water discoloration (Ergul et al. 2014; 2015). It was clearly observed the water
discoloration in the red tide events caused by Noctiluca scintillans in the Sea of
Marmara (Figure 1).
The influence of a heterotrophic dinoflagellate (N. scintillans) on zooplankton
community structure has been investigated in the Sea of Marmara, a highly stratified
basin (Yilmaz et al. 2005). They reported that enhanced abundance, year-round
occurrence, and high condition of Noctiluca scintillans population indicated that
optimum conditions had been achieved for explosive development of the species in the
Sea of Marmara. Increasing dominance of Noctiluca scintillans in the Sea of Marmara
shows that the species could have a stronger effect on zooplankton in the following
years and interrupt trophic pathways by reducing fodder zooplankton biomass. The
highest concentration was encountered in May 2002 as 217 cells L-1 (Yilmaz et al.
2005).
The bloom of the diatom Nitzschia longissima from the north-eastern Sea of
Marmara was reported by Deniz and Tas (2009). The abundance of N. longissima was
found 1.28×106 cells L-1 in February 2000, and also raphidophyte Heterosigma cf.
akashiwo was first recorded in the same study. Deniz and Tas (2009) reported 25
potentially harmful species in the north-eastern Sea of Marmara. The first study on
coccolithophorids in the Sea of Marmara was done by Aubert et al. (1990) and a bloom
of coccolithophorid Emiliana huxleyi (1.44×106 cells L-1) has been reported from the
Sea of Marmara.

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Figure 1. Red-tide of the dinoflagellate N. scintillans observed in the Sea of
Marmara.
2.1. Golden Horn Estuary
The Golden Horn Estuary (GHE) located southwest of the Istanbul Strait, served
as a fishery ground, recreational area, and, after the 1950s, as an industrial ground to the
inhabitants of Istanbul. Golden Horn Estuary, extending in northwest–southeast
direction, is a 7.5 km length and 200–900 m width and covers about 2.6 km2. The
maximum depth is around 40 m in the lower estuary and it rapidly decreases to 14 m in
the mid-estuary, and to <5 m in the upper estuary. As a result of unplanned urbanization
and heavy industrialization, the GHE has been polluted since the 1950s and has become
the most significant environmental problem in Istanbul. In 1990s, the estuarine life was
limited to the surrounding of Galata and Atatürk Bridges, and the upper estuary had
hypoxia and heavy sedimentation together with wastewater discharges. In 1997, the
Golden Horn Rehabilitation Project was initiated. The surface discharges were
gradually taken under control, connected to collector systems, and discharged into the
lower layer of the İstanbul Strait from two deep discharge systems. As the most
important step, 4.25×106 m3 anoxic sediment was removed from the completely filled
upper estuary and at least 5 m depth was gained in this region. The turning point for the
Golden Horn ecosystem was the opening of the floating Valide Sultan Bridge and
release of freshwater in the following week from a dam on Alibey Stream due to
maintenance studies at the end of May 2000. This resulted in rapid renewal and
oxygenation of anoxic and highly polluted waters trapped at the upper estuary (Tas et
al. 2009).
The previous studies on phytoplankton carried out in the GHE before its
rehabilitation demonstrated that insufficient water circulation, extreme pollution and
light limitation limited the growth of phytoplankton, particularly at the upper part of the
estuary (Uysal and Unsal 1996; Tas and Okus 2003; Tas et al. 2009). However, the

773
blooms of a cyanobacterium Microcystis cf. aeruginosa occurred in the GHE before
rehabilitation and this bloom conditions was studied from 1998 to 2000. The blooms
were recorded at the upper part of estuary in winter in the very low salinity conditions
due to high precipitation (<5). The highest abundances of Microcystis cf. aeruginosa
were detected as 1.4×106 cells mL-1 in December 1998 and 2.7×106 cells mL-1 in
February 1999. During these blooms, DO concentration increased considerably (~7 mg
L-1) at the upper part of estuary, where it was normally below 1 mg L-1. A remarkable
increase in the eukaryotic phytoplankton abundance following the rehabilitation of the
GHE occurred, while the Microcystis cf. aeruginosa abundance remained below bloom
level (Tas et al. 2006).
Following improving water quality by the rehabilitation project, phytoplankton
composition changed rapidly and consecutive blooms observed in the GHE. Increased
phytoplankton activity resulted in super saturated dissolved oxygen. The first bloom
following the rehabilitation efforts occurred by Skeletonema marinoi (reported as S.
costatum) (5×106 cells L-1) in June 2000. The densest bloom (70×106 cells L-1) was
caused by dinoflagellate Prorocentrum cordatum (reported as P. minimum) in July
2000. Subsequent diatom blooms were caused by S. marinoi (~8×106 cells L-1) in March
2001 and Thalassiosira allenii (4×106 cells L-1) in June 2001. A dense bloom of P.
cordatum (~36×106 cells L-1) was observed in July 2001, and dissolved oxygen
concentration reached super-saturation levels (19.9 mg L-1). Dense blooms continued
until the end of 2001. At times, different groups such as euglenophytes dominated the
phytoplankton; e.g. Eutreptiella sp. had the highest abundance (~3×106 cells L-1) in
February 2001 (Tas et al. 2009).
The prolonged red tide of dinoflagellate Heterocapsa triquetra and
phytoplankton succession were investigated in the GHE in 2007 (Tas 2015). Red tide of
H. triquetra was observed with an orange-brownish water discoloration at the upper part
of estuary from January to April and the highest cell density reached 19.2×106 cells L-1
in April 2007, when DO concentration was 20.4 mg L-1. Successive blooms continued
with dinoflagellate Prorocentrum cordatum (reported as P. minimum) in May,
euglenophyte Eutreptiella marina and raphidophyte Fibrocapsa sp. in summer (Tas
2015).
In the recent study, the distribution of potentially harmful microalgae and algal
blooms were investigated in the GHE during one year between 2009 and 2010 (Tas and
Yılmaz 2015). A total number of 23 potentially harmful and/or bloom-forming
microalgae (14 dinoflagellates, 4 diatoms and 5 phytoflagellates) were identified
throughout this study period, of which nine taxa have been confirmed to be toxic and
nine taxa formed dense and successive algal blooms causing water discoloration. Dense
algal blooms observed in this study belonged to diatoms Skeletonema marinoi (54×106
cells L-1) and Pseudo-nitzschia spp. (2.8×106 cells L-1), cryptophyte Plagioselmis

774
prolonga (7.8×106 cells L-1) and euglenophyte Euglena viridis (1.3×106 cells L-1) in
April and May, P. prolonga (7.5×106 cells L-1), S. marinoi (37×106 cells L-1),
prasinophyte Pyramimonas cf. grossii (1.2×106 cells L-1) and raphidophyte Heterosigma
akashiwo (14×106 cells L-1) in June, Scrippsiella trochoidea (2.3×106 cells L-1) in
August, Thalassiosira sp. (16×106 cells L-1) and H. akashiwo (1.6×106 cells L-1) in
September (Tas and Yılmaz 2015). Temporal and spatial variability of the potentially
toxic Pseudo-nitzschia spp. was studied in the GHE between 2009 and 2010. Two
blooms caused by Pseudo-nitzschia spp. were observed in January and May. Two
species, P. calliantha and P. pungens, were identified based on the SEM examination
and P. calliantha was the first record for the Sea of Marmara (Tas and Lundholm 2016).
Most harmful microalgae were observed in spring and summer, particularly in
the middle and upper part of estuary. Water discolorations from orange-brown
(Scrippsiella trochoidea), to greenish-brown (cryptophyte Plagioselmis prolonga), to
green (Euglena viridis) were observed during these blooms. At time, DO values
increased considerably and oversaturated sometimes, e.g. DO concentration reached
17.6 mg L-1 during the Skeletonema marinoi bloom in July (Tas and Yilmaz 2015).
Figure 2. Number of bloom-forming species (A) and potentially harmful species
(B) in the GHE during the period of 30 years between 1985 and 2014.
The number of the bloom-forming species and potentially harmful species in the
GHE increased gradually between 1998 and 2014 and it is obvious that there is a
significant increase in HAB events between 2010 and 2014 (Tas and Yilmaz 2015; Tas
2016) (Table 1 and Figure 2). Most of the bloom-forming species is composed of
phytoflagellates (5 taxa) and diatoms (4 taxa), while dinoflagellates were represented by
one taxon. However, most of the potentially harmful species is composed of
dinoflagellates (15 taxa), while diatoms were represented by two taxa. Water
1985
1986
1987
1995
1998
1999
2000
2001
2007
2010
2014
0
4
8
12
16
20
Number of bloom-forming species
1985
1986
1987
1995
1998
1999
2000
2001
2007
2010
2014
0
4
8
12
16
20
Number of potentially harmful species
AB

775
discolorations depending on the bloom-forming species were clearly observed in
surface of the GHE (Figure 3).
Table 1. List of HAB species in eukaryotic phytoplankton observed in the GHE
during the period of 30 years between 1985 and 2014.
1985-1987 1995 1998-2001 2007 2010-2014
Bacillariophyceae Bacillariophyceae Bacillariophyceae Bacillariophyceae Bacillariophyceae
Pseud o-nitzschia
delicatissima
Pseud o-nitzschia
delicatissima
Pseud o-nitzschia
delicatissima
Pseud o-nitzschia
delicatissima
Pseud o-nitzschia
calliantha
P. pungens P. seriata P. pungens P. pungens P. delicatissima
P. seriata
P. pungens
Dinophyceae Dinophyceae Dinophyceae Dinophyceae Dinophyce ae
Dinophysis
acuminata
Akashiwo sanguinea Akashiwo sanguinea Alexandrium sp.
D. caudata Dinophysis acuminata Dinophysis caudata Dinophysis acuminata
Noctulica scintillans D. acuta Heterocapsa triquetra D. acuta
Tripos furca D. caudata Noctiluca scintillans D. caudata
Tripos fusus D. sacculus
Phalachroma
rotundatum
D. fortii
Heterocapsa triquetra Prorocentrum micans D. tripos
Gymnodinium. catenatum P. cordatum Heterocapsa triquetra
Noctulica scintillans Scrippsiella trochoidea
Lingulodinium
polyedrum
Phalachroma rotundatum Tripos furca Noctulica scintilla ns
Prorocentrum micans Tripos fusus
Phalachroma
rotundatum
P. cordatum Prorocentrum micans
Scrippsiella trochoidea
P. cordatum
Tripos furca
Protoperidinium
crassipes
Tripos fusus
Scrippsiella trochoidea
Tripos furca
Tripos fusus
Raphidophyceae Raphidophyceae Raphidophyceae
Fibrocapsa sp. Fibrocapsa sp. Heterosigma akashiwo

776
Figure 3. Algal blooms causing water discoloration in the GHE.
(1): diatom Skeletonema marinoi, (2): cryptophycean Plagioselmis prolonga,
(3): raphidophycean Heterosigma akashiwo (4): euglenophycean Euglena viridis
(Photo: S. Tas).
2.2. İstanbul and Çanakkale Straits
There are a few studies on HABs performed in the İstanbul and Çanakkale
Straits, which have strong current systems. One of them was the study performed by
Aktan et al. (2003) on the coast of the Istanbul Strait (Bosphorus) between May 1997
and August 1998. A total of five species of coccolithophorids were determined and a
bloom was observed during May 1997, and total density of coccolithophorids was
detected as 2.34×106 cells L-1 dominating by Calyptrosphaera species (Aktan et al.
2003).
In the study carried out by Turkoglu (2008) in the Çanakkale Strait (Dardanelles)
between 7 June and 11 July 2003 has been reported a bloom of P. micans reaching
3.3×106 cells L-1 and also other dinoflagellates Tripos spp. (as reported Ceratium spp.
containing C. furca var. furca and C. fusus var. seta) reached up to 1.05×106 cells L-1 in
the Sea of Marmara. In the same study performed, it has been investigated the
synchronous blooms of the coccolithophoride Emiliana huxleyi and three dinoflagellates
in the Çanakkale Strait between 7 June and 11 July 2003. In the time-sequence of Sea
WiFs images the regions with the highest coccolith accumulations has been observed in
the turquoise colour. The algal bloom was first observed in İzmit Bay in early June then
quickly spread through the Sea of Marmara and lasted until mid-July. During the bloom
period, cell density of E. huxleyi reached up to 2.55×108 cells L-1 (Turkoglu 2008).
Following a summer bloom of coccolithophoride Emiliana huxleyi in 2003, a winter

777
bloom has been observed for the first time between December and January in the
Çanakkale Strait (Turkoglu 2010a). This winter bloom started middle December 2003
(7.86×106 cells L-1) and then peaked (5.03×107 cells L-1) in early January 2004.
Moreover, Turkoglu (2010a) suggested that the bloom started flourishing after diatom
and dinoflagellate blooms under nitrogen depletion and moderate light, temperature and
salinity conditions.
In the another study, the blooms of coccolithophoride Emiliana huxleyi were
observed in early December 2004 (2.36×106 cells L-1) and late February 2005 (1.57×106
cells L-1) in Kepez harbor in the Çanakkale Strait (Turkoglu and Oner 2010). Turkoglu
(2013) has been investigated red tides of the dinoflagellate Noctiluca scintillans
associated with eutophication between March 2001 and January 2004 in the Çanakkale
Strait and reported that March-June and October-December periods were bloom periods
of N. scintillans. During bloom periods the density of N. scintillans reached 2.2×103
cells L-1 and the bloom of N. scintillans was associated not only eutrophication, but also
with stable temperatures and salinities (Turkoglu 2013).
3. Mucilage events in the Sea of Marmara
Mucilage formation in the seas is the aggregation in large amounts of
extracellular organic substances producing by various marine organisms under special
environmental and trophic conditions (Innamorati et al. 2001; Mecozzi et al. 2001). It
has been stated that diatoms produce extracellular organic substances (Rinaldi et al.
1995), and bacteria were reported to participate in this information (Herndl et al. 1999;
Azam and Long 2001), and dinoflagellates also produce extracellular mucilages
(MacKenzie et al. 2002). Mucilage formation in the Sea of Marmara began to be
observed firstly in İzmit Bay in October 2007 (Aktan et al. 2008; Tufekci et al. 2010)
and in Büyükada Island in the Sea of Marmara (Balkis et al. 2011).
Aktan et al. (2008) investigated the mucilage event associated with diatoms and
dinoflagellates at nine sampling stations in the Sea of Marmara during the bloom period
(September 2007- March 2008). During the first days of this bloom, diatom species
(Proboscia alata, Rhizosolenia sp., Pseudosolenia calcar-avis) were most abundant in
the phytoplankton community and their total abundance was more than 107 cells L-1. In
February 2008 simultaneously with the diatom bloom, the dinoflagellate Gonyaulax
fragilis became abundant in the mucilage, but its density did not reach high numbers
(36×103 cells L-1). Furthermore, a significant increase of coccolithophores (especially
Emiliana huxleyi) was observed during the mucilage event (Aktan et al. 2008).
In another study, the composition and abundance of phytoplankton together with
environmental conditions have been investigated during the mucilage event observed in
the Sea of Marmara from October 2007 to February 2008 (Tufekci et al. 2010). The

778
most abundant species were Gonyaulax fragilis, Skeletonema costatum, Ceratoneis
closterium (reported as Cylindrotheca closterium) and Thalassiosira rotula in the
mucilage formation. G. fragilis reached 83.6×103 cells L-1 in November 2007 in İzmit
Bay, and T. rotula was the most abundant diatom species, with 131×103 cells L-1 in the
same period. The highest abundance of G. fragilis was 96.3×103 cells L-1 in dense
mucilage-containing water samples collected from İzmit Bay in January 2008, and C.
closterium was the dominant diatom species (161.3×103 cells L-1) in the same sample
(Tufekci et al. 2010).
Balkis et al. (2011) has been investigated the role of single-celled organisms and
bacteria in mucilage formation on the shores of Büyükada Island in the Sea of Marmara
between January and June 2008. They stated that mucilage formation was very dense in
January and February and diatoms Ceratoneis closterium (reported as Cylindrotheca
closterium), Pseudo-nitzschia sp., Skeletonema costatum, Thalassiosira rotula and
dinoflagellate Gonyaulax fragilis were the dominant species in mucilage formation.
Moreover, it is suggested that bacteria play an important role in the mucilage
formations. The highest abundance of G. fragilis was 18.2×103 cells L-1 and C.
closterium was 114×103 cells L-1. As known that a few thousand G. fragilis cells release
the same amount of carbohydrate as that produced by tens of millions of C. closterium
cells (Pompei et al. 2003). In April, the effect of mucilage began to decline and in June,
the mucilage event lost its effect considerably (Balkis et al. 2011). Dense mucilage
aggregations were observed both in surface and on the sediment of the Sea of Marmara
(Figure 4).
Figure 4. Mucilage aggregations observed in surface waters of the İzmit Bay
(at left) in December 2007 (Photo: S. Tas) and on the sediment in the coast of
Erdek Bay (at right) in February 2008 (Photo: N. Balkis).
Although there are many studies on phytoplankton community in the Sea of
Marmara as mentioned above, there is only one study on biotoxins caused by
microalgae (Dursun et al. 2016). In this recent study, domoic acid (DA), a neurotoxin
produced by the diatom genus Pseudo-nitzschia, which caused to Amnesic Shellfish
Poisoning (ASP), from plankton net samples collected in the Sea of Marmara has been

779
firstly investigated in December 2010 and February 2011. In this study, the biotoxin
concentrations in samples from coastal waters were detected between 0.96 and 5.25 µg
DA/mL in the Sea of Marmara (Dursun et al. 2016).
A list of HAB species, which are noxious or toxic and/or bloom-forming species,
observed in the Sea of Marmara, has been given in Table 2. A total of 35 taxa were
determined as bloom-forming and/or potentially harmful in the phytoplankton
community of the Sea of Marmara. Moreover, Aktan and Aykulu (2003) reported three
toxic cyanobacteria not included in this Table 2, Lyngbya spp., Planktothrix sp. and
Pseudoanabaena sp., from the littoral sediments of İzmit Bay.
Table 2. List of potentially harmful and/or bloom-forming microalgae observed
in the Turkish Straits System.
Species
Harmful effect
Most
abundant
period
Most
abundant
area
Max. density
(cells L-1)
Cyanophyceae
Anabaena sp.
Toxic7
Aug
NE-SM
400×10³
Microcystis cf. aeruginosa*
Toxic7
Dec, Feb
GHE
2.7×108
Oscillatoria sp.
Toxic7
-
GHE
-
Bacillariophyceae
Nitzschia longissima*
Discoloration?
Feb
NE-SM
1.28×106
Pseudo-nitzschia calliantha*
Toxic, ASP1
Jan, May
GHE
1.2×106
Pseudo-nitzschia delicatissima
Toxic, ASP1
Jan
GHE
250×10³
Pseudo-nitzschia pungens
Toxic, ASP1
Jan, May
GHE
5.8×105
Skeletonema marinoi* (reported as S.
costatum)
Discoloration
April
GHE
54×106
Thalassiosira sp.*
Discoloration
Sep
GHE
15.6×106
Thalassiosira allenii*
Discoloration
June
GHE
4×106
Dinophyceae
Akashiwo sanguinea*
Ichtyotoxic?6,10
May
GHE
59.5×10³
Dinophysis acuminata
Toxic, DSP1
May
GHE
1.3×10³
Dinophysis acuta
Toxic, DSP1
May, Sep
GHE
2.6×10³
Dinophysis caudata
Toxic, DSP1
Sep
GHE
2.6×10³
Dinophysis fortii
Toxic, DSP1
May
GHE
-
Dinophysis sacculus
Toxic, DSP1
June
GHE
5.0×102
Phalacroma rotundatum
Toxic, DSP1
May
GHE
1.3×10³
Gonyaulax fragilis
Mucilage formation2,3,11,12
Dec, Jan
E-SM
96.3×10³
Gymnodinium catenatum
Toxic, PSP1
Jan
GHE
4.5×10³
Heterocapsa triquetra*
Discoloration/Fish kills4,5
April
GHE
19.2×106

780
Table 2. (continued)
Species
Harmful effect
Most
abundant
period
Most
abundant
area
Max. density
(cells L-1)
Lingulodinium polyedrum
Toxic6
May
GHE
-
Noctiluca scintillans*
Discoloration/Ammonia6
May
D
2.2×105
Prorocentrum micans*
Discoloration/Fish kills5
Sep
D
3.3×106
Prorocentrum cordatum* (reported as
P. minimum)
Discoloration/Toxic to
marine fauna6
July
GHE
70×106
Prorocentrum scutellum*
Discoloration
Oct
E-SM
2.4×106
Scrippsiella trochoidea *
Discoloration/Fish kills5,6
Aug
GHE
2.3×106
Tripos furca (reported as Ceratium
furca)
Fish kills5
June
GHE
5.2×10³
Tripos fusus (reported as Ceratium
fusus)
Fish kills5
March
E-SM
106×10³
Tripos spp. (reported as Ceratium
spp.: C. furca and C. fusus)
Fish kills5
July
D
1.05×106
Raphidophyceae
Heterosigma akashiwo*
Ichthyotoxic/Fish kills1,8
June
GHE
13.9×106
Fibrocapsa sp.
Ichthyotoxic/Fish kills7
Nov.
GHE
288×10³
Cryptophyceae
Plagioselmis prolonga*
Discoloration
May
GHE
7.8×106
Prymnesiophyceae
Emiliana huxlei
Discoloration
July
D
2.55×108
Prasinophyceae
Pyramimonas cf. grossii *
Discoloration
June
GHE
1.6×106
Euglenophyceae
Euglena viridis*
Discoloration
July
GHE
11.4×106
Eutreptiella marina*
Discoloration
July
GHE
3.4×106
Abbreviations: ASP: Amnesic Shellfish Poisoning; DSP: Diarrethic Shellfish Poisoning; GHE:
Golden Horn Estuary; SM: Sea of Marmara; E-SM: Eastern Sea of Marmara; NE-SM: North-eastern Sea of
Marmara; D: Dardanelles; The symbol (*) indicates the bloom-forming species; The numbers (x) indicates the
references related to the harmful effects of species: 1Moestrup et al. 2009; 2Pompei et al. 2003; 3Pistocchi et
al. 2005; 4Tas 2015; 5Lu and Hodgkiss 2004; 6Hallegraeff 2002; 7Hallegraeff et al. 2003; 8 Heil et al. 2005;
9Koray 2004; 10Zingone et al. 2006; 11Tufekci et al. 2010; 12Balkis et al. 2011.
4. Discussion
There was no study on HABs events before 2000s. The studies focusing on
HABs have increased in the Sea of Marmara particularly in the GHE, İzmit Bay and
Çanakkale Strait. The lack of HABs data before 2000 makes it difficult to compare with
the present situations and better understanding the dynamics of HAB events. A few
harmful species were reported in the GHE in the period of 1985-1987, because of the
one study covering only diatoms. The results obtained from the studies on

781
phytoplankton and HABs performed in the Sea of Marmara showed that there are 35
bloom-forming and potentially harmful species in the Sea of Marmara, as shown in
Table 2. Cyanobacteria were represented with 3 species, while diatoms were 7 species,
dinoflagellates were 18 species and other marine flagellates were 7 species.
Several species formed successive and dense blooms in the GHE in late spring
and summer, particularly between 2010 and 2014. Although neither fish-kill events nor
human health problems were witnessed during these blooms, anoxia and light
attenuation due to discoloration was observed. But, more harmful effects may occur in
the future since the GHE is a potential risk area for future HABs with increase in the
number of potentially harmful species and magnitude of blooms in response to rapidly
changing environmental conditions (Tas and Yilmaz 2015).
High phytoplankton density in the Çanakkale Strait showed that eutrophication
due to high terrestrial discharges coming from Black Sea was the most important factor
(Turkoglu and Oner 2010; Turkoglu and Erdogan 2010). High phytoplankton densities
in the Çanakkale Strait are generally controlled by smaller forms in size and having
generally a short life cycles, such as coccolithophorid Emiliana huxleyi, dinoflagellate
Prorocentrum spp. and diatoms Dactyliosolen fragilissimus and Leptocylindrus spp.
(Turkoglu 2010a). The studies on coccolithophorid Emiliana huxleyi indicated that this
species came from the Black Sea through the Sea of Marmara and the Çanakkale Strait
under favorable conditions. These conditions may be due to climate changes because
this species formed not only extensive summer blooms but also winter blooms in the sea
of Marmara, in addition to the dramatic eutrophication of the system since 1980s
(Turkoglu 2008; 2010a). Bloom of coccolithophorids in the İstanbul Strait may
probably be occur because of the hydrodinamics of the Istanbul strait and entry of
intensive sources of nutrients from rivers, sewage, industry, heavy marine traffic (Aktan
et al. 2003).
The bloom of dinoflagellate Noctiluca scintillans was associated not only with
eutrophication, but also with stable temperatures and salinities. Very excessive blooms
of N. scintillans caused to gelatinous water and changes in water colour in some
recreational swimming areas during late spring and early summer (Turkoglu 2013).
Enhanced abundance, year-round occurrence, and high condition of Noctiluca
population indicated that optimum conditions have occurred for explosive development
of the species in the Sea of Marmara (Yılmaz et al. 2005). In recent years, brownish-red
water discoloration caused by Prorocentrum micans and pale red water discoloration
caused by Noctiluca scintillans were commonly observed in the İzmit Bay (Ergul et al.
2014).
During mucilage observations in the Sea of Marmara, neither hypoxia/anoxia nor
fish kills have been recorded (Aktan et al. 2008), but the large quantity of mucilage

782
aggregates affected fishing activities and fishing associations were highly sensitive to
this matter (Aktan et al. 2008; Tufekci et al. 2010; Balkis et al. 2011) and extensive
benthic mucilage aggregates were observed on the sediments and mussels (Aktan et al.
2008). Moreover, the presence of high dissolved organic carbon (DOC) content in the
waters surrounding the aggregate indicate that the vicinity of the material produced was
5-10 times richer in organic material than the usual organic carbon content of the sea
(Tufekci et al. 2010). In the recent years, the studies on dinoflagellate cysts are very
important to monitor the blooms might be in the future caused by these species (Balkis
et al. 2016). Therefore, the number of these studies should be increased.
In conclusion, as shown in the results, there are significant increases both in algal
blooms and the number of potentially harmful species in the Sea of Marmara in recent
years. We can assume that nutrient enrichment human induced lead to eutrophication
and climate change caused by global warming are the main factors supporting many
algal blooms. The resulting stress conditions accelerate the competition among species
and promote the reproduction of certain microalgae species particularly in competitive
and tolerant species. Considering the increasing algal blooms and harmful species in
recent years, it appears clearly that the studies on HABs and their impacts on the
ecosystem should be increase and the water quality monitoring studies should be
conducted at regular intervals.
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