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2014 and in May 2015 and caused to brownish-red water discoloration. At the same area, the ..... human health problems were witnessed during these blooms, anoxia and light attenuation due to ... Istanbul University, Centre for Environmental.
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

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. 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 (TÜDAV). Authors are responsible for their articles’ conformity to scientific rules. Editors 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: 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) P.O. Box: 10, Beykoz / Istanbul, TÜRKİYE Tel: +90 216 424 07 72 Belge geçer: +90 216 42407 71 E-mail: [email protected] www.tudav.org

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HARMFUL ALGAL BLOOMS (HABs) AND MUCILAGE FORMATIONS IN THE SEA OF MARMARA Seyfettin TAŞ1*, Halim Aytekin ERGÜL2 and Neslihan BALKIS3 2

1 Institute of Marine Sciences and Management, Istanbul University Faculty of Sciences and Arts, Department of Biology, Kocaeli University 3 Department of Biology, Faculty of Science, Istanbul University * [email protected]

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”), thereby 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 highbiomass 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).

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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