Ecologica Montenegrina 19: 130-151 (2018) This journal is available online at: www.biotaxa.org/em

Assessments of environmental variables affecting the spatiotemporal distribution and habitat preferences of living Ostracoda (Crustacea) species in the Enez Lagoon Complex (Enez-Evros Delta, )

SELÇUK ALTINSAÇLI1, FERDA PERÇIN PAÇAL*2, SONGÜL ALTINSAÇLI3

1 Merdivenköy Mahallesi, Ortabahar Sok. No: 20/4, , Kadıköy, Turkey, e-mail: [email protected] 2 İstanbul University, Aziz Sancar Institute of Experimental Medicine, Department of Genetics, TR, Şehremini, İstanbul, Turkey e-mail: [email protected] 3 İstanbul University, Department of Biology, Faculty of Science, Vezneciler, İstanbul-Turkey, e-mail: [email protected] Corresponding author: Selçuk Altınsaçlı

Received 10 October 2018 │ Accepted by V. Pešić: 5 December 2018 │ Published online 14 December 2018.

Abstract The present study analyzed the spatiotemporal changes of Ostracoda fauna in eight coastal lagoons in the Enez-Evros delta (Tuzla Lake 1, Tuzla Lake 2, Tuzla Lake 3, Taz, Işık, Dalyan, Kuvalak, and Taşaltı), located along the northern coastline of Turkey. Recent ostracod samples collected from the eight lagoons were analyzed, and 16 living ostracod species (belonging to 14 genera) were identified during the sampling periods. The most abundant species were found to be Cyprideis torosa and Loxoconcha elliptica. C. torosa, a cosmopolitan and opportunistic species of Ostracoda, was found in all the studied coastal lagoons. All ostracod species determined in the lagoons were grouped into three assemblages: Group 1: halophilic continental freshwater species (F. fabaeformis, C. vidua, D. stevensoni, E. virens, H. salina, I. biplicata, I. bradyi, L. inopinata, and S. aculeata); Group 2: euryhaline and typical brackish water species (C. torosa and L. elliptica); Group 3: marine (coastal: A. convexa, L. rhomboidea, C. elongata, and X. communis) and brackish (lagoonal: L. lacertosa) water species. These species of Ostracoda were shown to be affected by environmental conditions. Analyses with the physicochemical variables and species (Spearman’s rank correlation coefficient and Canonical Correspondence Analysis) confirmed that ostracod distribution in the Enez lagoons are controlled by seawater–freshwater inputs and by salinity. The purpose of this work is about to present data about of the Enez lagoons, and analyze the diversity of ostracods of them.

Key words: Ostracoda, Evros Delta, Lagoon, Ecology, Turkey.

Introduction

According to Kjerfve (1994), coastal lagoons are usually positioned parallel to the coast, separated from the sea by a sand barrier and connected to the sea by one or more linking channels or inlets with shallow waters. Coastal lagoons are one of the most common and known coastal wetland types, occupying 13% of the world’s coastlines (Barnes 1980). Lagoons help to stabilize regional climates by storing heat energy, prevent

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floods by accumulating water, and prevent erosion through the accumulation of sediments. Lagoons salinity values vary from freshwater (or low salt concentration levels in mouths of creeks/river mouth) to brackish water (in connected sections of it’s to sea) Turkey is a rich country with regard to the types and the number of wetlands. Turkey’s wetlands are located on important bird-migration routes, and close to 420 bird species find refuge in Turkey’s wetlands, with about 110 species visiting in the summer to nest (Şişman & Özyavuz 2010). Twenty-one bird species were observed in eight lagoons in this study, showing how the eight lagoons and the area of the Evros delta located in Turkey form an important biological area for many bird species in regard to their breeding, feeding, and sheltering. Lake Gala and the Enez lagoons in this Evros delta are ecological units of international importance for their rarity and sensitivity (Şişman & Özyavuz 2010). Wetlands are habitats that have high biological diversity and dynamic structures, and thus need to be protected as they have both economic and ecological importance. According to Yaşar (2010), environmental threats affecting the eight lagoons of Enez are: a) the erosion of shore arrows separating two lagoons, Dalyan and Işık, from the sea, b) increasing shoaling areas in the Dalyan and Işık lagoons, c) increasing water pollution in the Dalyan and Işık lagoons, d) shrinking of the lakes of Enez-Tuzla (former saltpans), e) incorrect location selection for the building of the Enez Yacht Harbor and Fisherman’s Shelter, f) environmental problems caused by summer cottages. Nowadays, the most important anthropogenic activity in the Dalyan, Taşaltı, and Işık lagoons is fishing. Fish species of both economic and non-economic importance live a part of their life cycle in coastal lagoons (Kapetsky 1984). Invertebrate species such as ostracods play an important role in the feeding of juvenile fish in lagoons; indeed, this study determined ostracod samples in the stomachs of juvenile fish. Ostracods are small bivalved aquatic invertebrates (0.3–5 mm long) (Meisch 2000), a group of microcrustaceans that inhabit all aquatic environments, from fresh to hypersaline waters and from continental to abyssal ocean zones (Martínez-García et al. 2013). They are very common in marine or marine-connected environments such as seas, lagoons, and estuaries (Athersuch et al. 1989) and non-marine environments such as lakes, ponds, springs, creeks, troughs, seas (Meisch 2000). Ostracods show specific responses and tolerances to the different environmental variables of aquatic bodies (Benson 1990) and are important in determining and assessing past environments due to their well-fossilized valves. This present study is a comprehensive field study performed on ostracods in the Enez lagoon complex. The ostracod species reported in the literature from Turkey were collected to investigate the relationships between ostracod species and different physicochemical variables, to determine spatiotemporal distributions of ostracod species, and determine the habitat preferences of living ostracod species in the shallow Enez lagoons. The secondary objective of this study was to analyze the positive and negative effects of anthropogenic activities. The results and conclusions drawn are useful for the future management and conservation practices of the lagoon-complex environment.

Material and Methods

Site description: The Meriç river (, Evros) waters flow to the Aegean Sea via two channels at present (Alpar et al. 1998). One of these is a western branch located within the boundaries of Greece and other is the eastern branch along the political border between Turkey and Greece (Alpar et al. 1998). The study area consists of lagoons and former saltpans that are separated from in the northeastern Aegean Sea and other lagoons by a sandy barrier. The Enez lagoon complex is located in the western part of the district, in the center of Enez (Turkey). This lagoon complex consists of eight shallow coastal lagoons (Dalyan, Işık, Kuvalak, Tuzla Lake 1, Tuzla Lake 2, Tuzla Lake 3, Taşaltı, and Taz), whose salinity ranges vary from fresh to hypersaline waters (Figure 1). The lagoonal system (lagoon, saline- and freshwater marshes, river, canals) of the Evros delta is located on the border between Greece and Turkey (its southern part in Turkey, northern part in Greece). The South branch of the Evros (Maritsa, Meriç) river is divided into sections by the Evros (Meriç, Maritsa) delta. Enez was originally a marine harbor; it was separated from the Aegean Sea due to the dominant marine currents and the deposits of river sediments, and it was later a brackish coastal lagoon complex, from Roman times until the 18th century (Alpar et al. 1998). The Enez lagoon complex is a second-grade natural protected area (Anonymous 2016). The Enez district features an average rainfall of 551 mm and an average temperature of 14 ºC (Şişman & Özyavuz 2010). Ecologica Montenegrina, 19, 2018, 130-151 131

SPATIOTEMPORAL DISTRIBUTION AND HABITAT PREFERENCES OF OSTRACODA IN THE ENEZ LAGOONS

Fig. 1. Map of the eight studied coastal lagoons. Selected sampling sites at Tuzla Lake 1 (St-1), Tuzla Lake 2 (St-2), Tuzla Lake 3 (St-3), Taz (St-4), Işık (St-5), Dalyan (St-7, 8, and 9), Kuvalak (St-10), and Taşaltı (St-11 and 12) were used for comparisons of the lagoons. The sampling sites are indicated by red circles; the red arrows show the direction of water currents.

The many of lagoon call as "lake" in the Turkey. Likewise, the Enez lagoons were called as the lake in many Turkish publications.

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Tuzla (Saltpan) Lake 1: Located 1321 m east of the Enez district center, a stabilized road passes through a narrow sandy barrier between this lake and Taşaltı Lagoon. This lagoon is fed only with rainwater. Tuzla Lake 1 (formerly a saltpan) is not connected to the Taşaltı end of Dalyan Lagoon. As freshwater input into this lagoon comes mainly from rainwater in the wet seasons, the lagoon’s salinity decreases during these times. The first sampling site was in this lagoon.

Tuzla (Saltpan) Lake 2: Is located 1729 m east of the Enez district center. Tuzla Lake 2 (formerly a saltpan) is not connected to Taşaltı Lagoon, Tuzla Lake 1, Tuzla Lake 3, or Dalyan Lagoon. As freshwater input into this lagoon comes mainly from rainwater in the wet seasons, the lagoon’s salinity decreases during these times. The second sampling site was in this lagoon.

Tuzla (Saltpan) Lake 3: Located 2050 m southwest of Enez district center, Tuzla Lake 3 (formerly a saltpan) is not connected to Taşaltı Lagoon, Tuzla Lake 1, Tuzla Lake 2, or Dalyan lagoon. This lagoon is fed only by rainwater in the wet seasons. It is accepted as a freshwater lake according to the salinity classification of brackish water (Venice System criteria). The third sampling site was in this lagoon.

Taz Lagoon: Located 3200 m southwest of the Enez district center, this lagoon connects to Dalyan Lagoon in the rainy seasons but not in the dry season. Freshwater input to this lagoon comes mainly from rainwater in the wet seasons. The fourth sampling site was in this lagoon.

Işık (Bücürmene, Üzmene) Lagoon: This shallow coastal lagoon covers an area of 71 ha and is characterized by an average depth of around 0.4 m and a maximum depth of around 1 m. Located 2 km southwest of the Enez district center, this lagoon is a system of choked coastal lagoons in northwest Turkey. The mean depth of the lagoon system is 40 cm. The lagoon is connected to the sea by a small channel, in the western part. While marine water flows into the lagoon through this canal, lagoon water also flows out to the sea through this channel. The lagoon is only temporarily connected to the sea through this single one narrow inlet because, after economic-relevant fish species have entered through this channel, it is closed by the fishery cooperative. Strong, high waves could destroy the sandy barrier between Işık lagoon and the sea during stormy weather. Freshwater input is taken from falling rain. The rainy seasons comprise autumn, winter, and spring months, with the summer being dry. The fifth and sixth sampling sites were in this lagoon.

Dalyan (Peso) Lagoon: Located 100 m southwest of the Enez district center, the lagoon is temporarily connected to the sea via two narrow inlets. When economic-relevant fish species have entered these channels, they are closed by the fishery cooperative. The seventh, eighth, and ninth sampling sites were situated in this lagoon.

Kuvalak Lagoon: Located 1800 m southwest of the Enez district center, this lagoon does not connect to the Dalyan or Işık lagoons. Freshwater input into this lagoon comes mainly from rainwater in the wet seasons. A sandy barrier, located in the eastern section of this lagoon, separates it from Dalyan Lagoon, but the lagoon’s water flows into Dalyan Lagoon when the sandy barrier between the lagoons is eroded by floodwater. The tenth sampling site was located in this lagoon.

Taşaltı Lagoon: Located 180 m southwest of the Enez district center, a motorway passes through a narrow sandy barrier between this lagoon and Dalyan Lagoon. Taşaltı Lagoon connects to Dalyan Lagoon via a narrow channel, which passes under the motorway. Taşyarma Canal discharges freshwater from Lake Gala into Taşaltı Lagoon. The eleventh and twelfth sampling sites were in this lagoon.

Sampling and Measuring

Samples were collected from a total of 12 sampling sites selected from Tuzla Lake 1 (formerly a saltpan), Tuzla Lake 2 (formerly a saltpan), Tuzla Lake 3 (formerly a saltpan), and the Taz, Işık, Dalyan, Kuvalak, and Taşaltı lagoons. Samples were taken from seven sites with a hand net (mesh size of 100 μm) in January, March, May, July, September, and November 2016. At each site, about 200 g of surface sediment was collected, fixed in 70% ethanol in situ, and placed in polyethylene jars (250 ml). The samples were brought Ecologica Montenegrina, 19, 2018, 130-151 133

SPATIOTEMPORAL DISTRIBUTION AND HABITAT PREFERENCES OF OSTRACODA IN THE ENEZ LAGOONS to the laboratory, where the sediment was washed out under pressurized tap water and separated into four grain-size fractions using standardized sieves (2.0, 1.5, 0.5, 0.25, and 0.125 mm mesh size). Ostracods and other invertebrates were sorted under a stereomicroscope and fixed again and preserved in 70% ethanol. The retained material was transferred to a petri dish. Ostracod specimens were picked out of the sediment under a stereomicroscope and the soft body parts dissected in lactophenol solution for taxonomic identification. The number of adult individuals belonging to each identified ostracod species was counted under a stereomicroscope. A light microscope was used for taxonomic identification. The juvenile stages of some ostracod species were observed at all sampling sites. The ostracods were handpicked and species identified using the keys developed by Bonaduce et al. (1975), Athersuch et al. (1989), Meisch (2000), and Fuhrmann (2013), with taxonomy and nomenclature following the latter. Seven physicochemical variables commonly used in studies were measured in January, March, May, July, September, and November of 2016. The redox potential (ORP [Mv]), pH, percentage of oxygen saturation (Sat [%]), dissolved oxygen (DO [mg L-1]), electrical conductivity (EC [µS/cm]), salinity (psu), and water temperature (Tw [ºC]) were measured in situ using electronic probes (WTW 340i multimeter) at each of the 12 sampling sites. Air temperature (Ta, °C) and atmospheric pressure (ATP, Mbar) were measured using a handheld digital thermometer and barometer, respectively. The coordinates for each sampling site were determined using a handheld Global Positioning System (GPS) receiver. GPS coordinates and other identifiable characteristics of each sampling site are given in Table 1. During this study, a total of 109 species in addition to ostracods were recorded; they comprised 44 invertebrate (in 34 genera), 44 vertebrate (in 36 genera), and 25 macrophyte (in 21 genera) from the eight lagoons (see Table 2). A list of other animal and plant species that were collected together with the ostracods from the eight lagoons is given in Table 2. Various invertebrate and vertebrate animal species and macrophyte species in addition to the ostracod species were identified to the lowest possible taxon (see Table 2). These data were not used for the statistical analysis.

Statistical Analysis

Binary (presence/absence) data was used to show the similarity between the sampling stations and the clustering of ostracod species using Jaccard’s coefficient test of unweighted pair group mean averages (UPGMA) provided by the program Multi-Variate Statistical Package (MVSP) Version 3.22 (Kovach 2013). Jaccard’s coefficient test was used to display the clustering of the five sampling sites and eight species. To examine seasonal differences in ostracod species composition, we calculated the Shannon– Weaver diversity index (H') for each site in four seasons by using Biodiversity Pro software package (McAleece et al. 1997). The Shannon–Weaver diversity index was calculated by using the formula from Legendre & Legendre (1983). A two-tailed Spearman rank correlation test was used to examine the relationships between seven environmental variables (temperature, electrical conductivity, salinity, oxidation-reduction potential, pH, dissolved oxygen, and percent oxygen saturation) and the abundance of eight ostracod species collected during the study. Canonical correspondence analysis (CCA) was also used to analyze species–environment relationships in order to identify those environmental factors potentially influencing ostracod assemblages (Ter Braak 1986). Data were analyzed using the Multi-Variate Statistical Package (MVSP), version 3.22 (Kovach 2013).

Results

72 samples taken from 12 sampling stations contained 39,796 individuals belonging to 16 ostracod species (Table 3, Table 4). The percentage rates of prevalence and abundance values for each ostracod species found in four sampling stations are given in Table 3.

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Table 1. Coordinates and other identifiable characteristics of each sampling sites (SSN: sampling site number).

SSN Sampling sites Coordinates Substrata Sampling Mean Surface Trophic Salinity Water Lagoon-sea connections Name Depth (m) Depth area class classification type (m) (ha) St-1 Tuzla Lake 1 40° 42' 30.47"N Sandy mud 0.4 0.8 31 Mesotrophic Poly to hyperhaline NaCl isolated from the sea 26° 05' 06.98"E St-2 Tuzla Lake 2 40° 42' 17.84"N Sandy mud 0.4 0.8 8 Mesotrophic α-oligohaline NaCl isolated from the sea 26° 04' 45.61"E St-3 Tuzla Lake 3 40° 42' 12.36"N Sandy mud 0.4 0.8 1 Mesotrophic Freshwater NaCl isolated from the sea 26° 04' 42.17"E St-4 Taz Lagoon 40° 41' 48.27"N Sandy mud 0.4 0.6 16.5 Mesotrophic Poly to euhaline NaCl isolated from the sea 26° 03' 22.95"E St-5 Işık Lagoon 40° 42' 01.67"N Sandy mud 0.4 1 Mesotrophic Poly to euhaline NaCl Communicated 26° 03' 25.43"D 71 with the sea St-6 Işık Lagoon 40° 42' 24.32"N Sandy mud 0.4 1 Mesotrophic Poly to euhaline NaCl Communicated 26° 03' 45.97"E with the sea St-7 Dalyan Lagoon 40° 42' 50.67"N Sandy mud 0.4 1 Mesotrophic α-mesohaline to NaCl Communicated 26° 03' 11.84"E 449 polyhaline with the sea St-8 Dalyan Lagoon 40° 43' 27.31"N Sandy mud 0.4 1 Mesotrophic α-mesohaline to NaCl Communicated 26° 04' 05.40"E polyhaline with the sea St-9 Dalyan Lagoon 40° 42' 30.92"N Muddy sand 0.4 1 Mesotrophic α-mesohaline to NaCl Communicated 26° 04' 53.01"E polyhaline with the sea St-10 Kuvalak lagoon 40° 42' 40.44"N Sandy mud 0.4 0.6 17.5 Mesotrophic euhaline NaCl isolated from the sea 26° 03' 26.70"D St-11 Taşaltı Lagoon 40° 42' 43.53"N Muddy sand 0.4 0.9 Meso-eutrophic α-mesohaline NaCl Communicated 26° 05' 05.04"E 62 with the sea St-12 Taşaltı Lagoon 40° 43' 14.94"N Muddy sand 0.4 0.9 Meso-eutrophic β-oligohaline NaCl Communicated 26° 05' 32.91"E with the sea

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Table 2. Species list of other animals and plants collected together with ostracods from 12 sampling sites in the eight lagoons.

TAXA 1 2 3 4 5 6 7 8 TAXA 1 2 3 4 5 6 7 8 FORAMINIFERA Idotea balthica (Pallas, 1772) X X X

Ammonia beccarii (Linnaeus, 1758) X X X X X X X Exosphaeroma pulchellum Colosi, 1921 X X X

Ammonia tepida (Cushman, 1926) X X X X X Sphaeroma serratum (Fabricius, 1787) X X X

Ammonia parkinsoniana (d'Orbigny, 1839) X X X X X TANAIDECEA

Elphidium limbatum (Chapman, 1907) X X X X X Araphura filiformis (Lilljeborg, 1864) X X X

Haynesina germanica (Ehrenberg, 1840) X X X X X AMPHIPODA

Haynesina depressula (Walker and Jacob, 1798) X X X X X Corophium orientale Schellenberg, 1928 X X X X X X

Spiroloculina angulata (Cushman, 1917) X X X X X Gammarus aequicauda (Martynov, 1931) X X X X X X

Spiroloculina ornata (d’Orbigny, 1839) X X X X X Gammarus crinicornis Stock, 1966 X X X X X X

Siphonaptera aspera (d’Orbigny, 1826) X X X X X Gammarus subtypicus Stock, 1966 X X X X X X

Quinqueloculina laevigata (d’Orbigny, 1839) X X X X X Microdeutopus gryllotalpa Costa, 1853 X X X X X X

GASTROPODA Monocorophium insidiosum (Crawford, 1937) X X X X X X

Haminoea navicula (da Costa, 1778) X X X Monocorophium sextonae (Crawford, 1937) X X X X X X

Hydrobia acuta (Draparnaud, 1805) X X X X X DECAPODA

Cerithium vulgatum Bruguière, 1792 X X X X X Carcinus aestuarii Nardo, 1847 X X X

Ecrobia ventrosa (Montagu, 1803) X X X X X Crangon crangon (Linnaeus, 1758) X X X

Tritia neritea (Linnaeus, 1758) X X X Palaemon elegans Rathke, 1837 X X X

BIVALVIA Penaeus kerathurus (Forskål, 1775) X X X

Abra segmentum (Récluz, 1843) X X X X X X INSECTA

Cerastoderma glaucum (Bruguière, 1789) X X X X X X X X Chironomus salinarius Kieffer, 1915 X X X X X X X X Loripes orbiculatus Poli, 1791 X X PISCES

Ruditapes decussatus (Linnaeus, 1758) X X X Anguilla anguilla (Linnaeus, 1758) X X X X

POLYCHAETA Atherina boyeri Risso, 1810 X

Capitella capitata (Fabricius, 1780) X X X Aphanius fasciatus (Valenciennes, 1821) X X X X

Capitella giardi (Mesnil, 1897) X X X Chelon (Liza) ramada (Risso, 1827) X X X

Hediste diversicolor (Muller, 1776) X X X Chelon (Liza) aurata (Risso, 1810) X X X

Scolelepis tridentate (Southern, 1914) X X X Chelon (Liza) saliens (Risso, 1810) X X X

Spio decorata Bobretzky, 1870 X X X Cyprinus carpio Linnaeus, 1758 X X X

Streblospio shrubsolii (Buchanan, 1890) X X X Dicentrarchus labrax (Linnaeus, 1758) X X X

MYSIDACEA Knipowitschia caucasica (Berg, 1916) X

Mesopodopsis slabberi (Van Beneden, 1861) X X X Lithognathus mormyrus (Linnaeus, 1758) X X X

ISOPODA Mugil cephalus Linnaeus, 1758 X X X

…continued on the next page

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TABLE 2. TAXA 1 2 3 4 5 6 7 8 TAXA 1 2 3 4 5 6 7 8 Mullus barbatus Linnaeus, 1758 X FLORA

Pomatomus saltatrix (Linnaeus, 1766) X X X Ammophila arenaria (L.) Link X X X X X X X X

Pomatoschistus marmoratus (Risso, 1810) X X Bolboschoenus maritimus (L.) Palla X X X X X X X X

Sarpa salpa (Linnaeus, 1758) X X X Carex divisa Huds. X X

Silurus glanis Linnaeus, 1758 X X Ceratophyllum demersum L. X X

Sparus aurata Linnaeus, 1758 X X X Cyperus capitatus Vandelli X X X X X X X X

Solea solea (Linnaeus, 1758) X X X Elymus farctus (Viv.) Runemark ex Melderis X X X X X X X

Syngnathus acus Linnaeus, 1758 X X X Juncus acutus L. X X X X X X X X

Umbrina cirrosa (Linnaeus, 1758) X X X Juncus maritimus Lam. X X X X X X X X

AMPHIBIA Imperata cylindrica (l.) rausch X

Pelophylax ridibundus (Pallas, 1771) X X Nymphoides peltata (S.G. Gmel.) Kuntze X

REPTİLIA Myriophyllum spicatum L. X X

Natrix natrix (Linnaeus, 1758) X X X X X X X Quercus sp. X X X X X X X X

Natrix tessellata (Laurenti, 1768) X X X X X X X X Phragmites australis (Cav.) Trin. ex Steud. X X X X X X X X AVES Ruppia maritima Linnaeus, 1753 X X X X X X

Ardea alba Linnaeus, 1758 X X X X X X X Scirpoides holoschoenus (L.) Soják, X X

Ardea cinerea Linnaeus, 1758 X X X X X X X X Ulva intestinalis Linnaeus, 1753 X X X

Ardea purpurea Linnaeus, 1766 X X X X X X X X Salicornia europaea Linnaeus X X X X X X X X Ardeola ralloides (Scopoli, 1769) X X X X X X X X Salvinia natans L. X X

Botaurus stellaris (Linnaeus, 1758) X X X X X X X X Stuckenia pectinata (L.) Börner, 1912 X X X X

Charadrius alexandrinus Linnaeus, 1758 X X X X X X X X Tamarix sp. X X X X X X X X Cygnus cygnus Linnaeus, 1758 X X X X Typha angustifolia L. X X X X Cygnus olor (Gmelin, 1789) X X X Typha domingensis Pers. X X

Egretta garzetta (Linnaeus, 1766) X X X X X X X Typha latifolia L. X X X X

Fulica atra Linnaeus, 1758 X X X X X X X X Ulva intestinalis Linnaeus, 1753 X X X

Himantopus himantopus (Linnaeus, 1758) X X X X X X X X Ulva rigida C.Agardh, 1823 X X X

NycticoraX nycticorax (Linnaeus, 1758) X X X X X X X X Larus michahellis J. F. Naumann, 1840 X X X X X X X X Phalacrocorax carbo (Linnaeus, 1758) X X X X X X

Phoenicopterus roseus Pallas, 1811 X X X X X

Pelecanus onocrotalus Linnaeus, 1758 X X X X X

Platalea leucorodia Linnaeus, 1758 X X X X X X X Plegadis falcinellus (Linnaeus, 1766) X X

Recurvirostra avosetta Linnaeus, 1758 X X X X X X X X Sterna hirundo Linnaeus, 1758 X X X X X X X X Sterna albifrons Pallas, 1764 X X X X X X X X

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Table 3. The abundance and frequency of each identified living ostracod species.

Number of sampling sites in Species Frequency Species Number of Individual which ostracod species were Frequency (%) code (%) collected Aurila convexa (Baird. 1850) AC 152 0.37 2 16.6 Fabaeformiscandona fabaeformis (Fischer. 1851) FF 42 0.1 1 8.3 Cyprideis torosa (Jones. 1850) CT 28075 70.55 11 91.6 Cypridopsis vidua (O.F. Muller) CV 1437 3.61 2 16.6 Cushmanidea elongata (Brady. 1868) Puri. 1958 CE 104 0.25 2 16.6 Darwinula stevensoni (Brady & Robertson. 1870) DS 224 0.56 2 16.6 Eucypris virens (Jurine. 1820) EV 55 0.13 2 16.6 Heterocypris salina (Brady. 1868) HS 973 2.44 2 16.6 Ilyocypris biplicata (Koch. 1838) IBI 1051 2.65 3 25 Ilyocypris bradyi G.O. Sars. 1890 IBR 1118 2.83 3 25 Limnocythere inopinata (Baird. 1843) LI 2346 5.89 3 25 Leptocythere lacertosa (Hirschmann. 1912) LL 131 0.33 2 16.6 Loxoconcha elliptica Brady. 1868 LE 3753 9.44 9 75 Loxoconcha rhomboidea (Fischer. 1855) LR 70 0.17 2 16.6 Sarscypridopsis aculeata (Costa. 1847) SA 217 0.56 2 16.6 Xestoleberis communis (Müller. 1894) XC 48 0.12 2 16.6 39796 100 12 100

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Table 4. The individual numbers of ostracod species by station.

Sampling sites AC CE CT CV DS EV HS FF IBI IBR LI LE LR LL SA XC Total St-1 Tuzla lake 1 4180 770 4950 St-2 Tuzla lake 2 2232 308 337 1623 4500 St-3 Tuzla lake 3 559 116 483 372 393 392 100 2415 St-4 Taz lagoon 616 174 790 St-5 Işık lagoon 70 48 447 159 30 63 27 844 St-6 Işık lagoon 4045 654 4699 St-7 Dalyan lagoon 82 56 404 190 40 68 21 861 St-8 Dalyan lagoon 3778 494 4272 St-9 Dalyan lagoon 3717 473 4190 St-10 Kuvalak lagoon 4453 376 4829 St-11 Taşaltı lagoon 4159 463 4622 St-12 Taşaltı lagoon 44 878 108 55 490 42 371 388 331 117 2824 Total 152 104 28075 1437 224 55 973 42 1051 1118 2346 3753 70 131 217 48 39796

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Table 5. Maximum, minimum, mean and standard deviations values of the environmental variables determined at each sampling site. Abbreviations: SD: standard deviations, SSN: sampling site number, Ta (air temperature, °C), Tw (water temperature, °C), Sal. (salinity, PSU), EC (electrical conductivity, mS/cm), ORP (oxidation-reduction potential, mV), DO (dissolved oxygen mg L-1), Sat. % (saturation), and AP (atmospheric pressure, Mbar).

Ta Tw pH ORP DO Sat. PSU EC AP St-1 Min-Max 10-28 9-26 7.89-8-25 -61- -64 7.21-10.79 75.8-101.2 24-41.2 38.8-65.-9 1009-1012 St-1 Mean±SD 17.8±6.79 15.65±6.37 8.11±0.13 -62.1±1.06 9.1±1.3 87.12±9.99 27.27±6.24 43.98±9.81 1009.5±1.11 St-2 Min-Max 10-28 9.2-27 8.11-8.78 -46- -53 9-11.8 99.8-106.5 1.9-2.8 3.9-6.7 1009-1012 St-2 Mean±SD 17.8±6.79 14.91±6.36 7.139±0.22 -40.8±2.4 9.301±1.05 88.53±2.21 1.98±0.35 4.24±1.05 1009.5±1.11 St-3 Min-Max 10-28 11-26.5 7.55-7.89 -23 - -26 7.1-8.53 78.1-102.4 0.2.-03 0.88-1.1 1009-1012 St-3 Mean±SD 17.8±6.79 13±9.33 6.44±3.08 -19.8 ±1.03 6.81±3.09 80.47±36.97 0.18±0.09 0.77±0.35 1009.5±1.11 St-4 Min-Max 10-28 9.5-26 7.32-8.71 -28 - -48 6.91-9.61 75.2-98.8 22.2-40 35.1-64.6 1009-1012 St-4 Mean±SD 17.8±6.79 13.22±8.67 6.497±2.94 -27.8±14.14 6.62±3.07 70.08± 23.77±32.2 37.25±9.18 1009.5±1.11 St-5 Min-Max 10-28 9.1-26.4 7.78-8.51 -69- -74 7.21-7.71 78.5-85.8 25.1-34 37.3-56.3 1009-1012 St-5 Mean±SD 17.8±6.79 16.2±6.46 8.25±0.25 -71.16±1.77 7.54±0.17 83.42±1.56 27.8±3.14 43.05±6.61 1009.5±1.11 St-6 Min-Max 10-28 8.9-26.7 7.45-8.71 -64 - -79 6.61-7.64 69.5-88.7 24.6-33 37.1-54.2 1009-1012 St-6 Mean±SD 17.8±6.79 16.1±6.81 8.059±0.52 -71.5±4.72 7.167±0.33 78.63±7.03 27.55±2.86 42.8±5.88 1009.5±1.11 St-7 Min-Max 10-28 9.1-26.7 8.48-8.76 -82 - -87 7.32-7.78 83.2-96.8 17.1-18.2 27.3-29.3 1009-1012 St-7 Mean±SD 17.8±6.79 17.27±661 8.61±0.10 -83.3±1.80 7.61±0.15 92.48±4.47 17.38±0.38 27.75±0.71 1009.5±1.11 St-8 Min-Max 10-28 9.2-26.5 8.48-9.11 -90- -96 7.33-7.86 87.1-98.2 16.5-19.1 28.2-31.3 1009-1012 St-8 Mean±SD 17.8±6.79 16.55±6.45 8.76±0.22 -92.167±1.95 7.55±0.21 89.6±3.92 17.58±1.03 29.2833±1.03 1009.5±1.11 St-9 Min-Max 10-28 9.1-27 7.67-8.86 -81 - -85 7.42-7.78 85.2-88.2 16.1-19.2 25.8-32.7 1009-1012 St-9 Mean±SD 17.8±6.79 16.48±6.55 8.25±0.45 -82.5±1.80 7.52±0.12 86.1±1.04 17.15±1.162 27.7±2.43 1009.5±1.11 St-10 Min-Max 10-28 9.3-26.5 7.56-9.21 -62- -78-0 6.1-7.82 61.5-70.3 30-36 45.2-48.6 1009-1012 St-10 Mean±SD 17.8±6.79 13.5±8.68 6.79±3.09 -56±25.6 5.73±2.61 50.7±29.3 27.3±12.46 39.43±17.7 1009.5±1.11 St-11 Min-Max 10-28 9.1-26.7 8.11-8.82 -77- -83 7.21-7.71 81.2-85.6 12.9-15.1 20.1-25.2 1009-1012 St-11 Mean±SD 17.8±6.79 16.5±6.73 8.47±0.25 -79.3±2.32 7.47±0.21 83.87±1.71 13.45±0.75 21.62±1.69 1009.5±1.11 St-12 Min-Max 10-28 9.3-25.6 7.45-7.91 -24- -26 8.11-9.52 91.5-98.5 1.6-2.4 2.5-4.9 1009-1012 St-12 Mean±SD 17.8±6.79 15.97±6.18 7.7±0.17 -25.5±0.76 9.03±0.53 95.8±2.80 2.03±0.31 3.37±0.86 1009.5±1.11

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According to these results, the dominant species were Cyprideis torosa, Loxoconcha elliptica, Limnocythere inopinata, Cyridopsis vidua, Ilyocyris bradyi, Ilyocypris biplicata, and Heterocypris salina, representing 70.55%, 9.44%, 5.89%, 3.61%, 2.83%, 2.65%, and 2.44%, respectively, of the total number of individuals (38,753, 94.76 %) collected from all the sites (Table 3). The most widespread species was C. torosa, which was found in 11 (91.6 %) of the sampling sites, followed by L. elliptica, found in 9 (75%) of the sampling sites. The maximum, minimum, and mean values and standard deviations of the environmental variables determined at the 12 sampling sites are presented in Table 5. Water temperature can vary daily since it can be dependent on the influence of daily air temperature. The water temperature values of eight lagoons varied depending on the air temperature. The highest water temperature was measured as 27 ºC at sampling site 9 in July and the lowest was 8.9 ºC at sampling site 6 in January. The salinity values of the eight waterbodies varied seasonally. The highest salinity was measured as 41.2 psu at sampling site 1 in September and the lowest 0.2 psu at sampling site 3 in January, March, May, and November. All the measured salinity values indicate that each waterbody has a different salinity range of (varying from nearly freshwater to hypersaline). We recorded that the surface salinity rate changes ranged from 30 to 35 psu of the Aegean Sea on the coast of Enez. The highest pH was measured as 9.21 at sampling site 10 in July and the lowest 7.32 at sampling site 4 in November, indicating that the lagoon and lake waters had a quite a wide pH range, from slightly alkaline to very alkaline levels. The highest dissolved oxygen values were measured as 11.8 mg L-1 at sampling site 2 in July and the lowest 6.1 mg L-1 at sampling site 10 in November, indicating the waters were well oxygenated. According to results of Jaccard coefficient test, UPGMA dendrogram showings three clustering groups (I-III) for the ostracod species (Fig. 2a). The first cluster consisted of nine species (F. fabaeformis, C. vidua, D. stevensoni, E. virens, H. salina, I. biplicata, I. bradyi, L. inopinata, and S. aculeata) (see Fig. 2a), all of which are halophilic continental freshwater species, and thus Therefore, all of them are allochthonous species. It should be mentioned that these species were the most abundant in the inner part of the lagoon complex. The second cluster consisted of euryhaline, opportunistic, and typical brackish water species (C. torosa and L. elliptica) (see Fig. 2a), found commonly and at high abundance. These species, too, are autochthonous. The third cluster was composed of four coastal marine species (A. convexa, L. rhomboidea, C. elongata, and X. communis) and one brackish (lagoonal: L. lacertosa) water species. While four marine ostracod species are allochthonous species, L. lacertosa is an autochthonous ostracod species. Based on species binary (presence/absence) data, the Jaccard’s coefficient dendrogram shows three main clusters among the 12 sampling sites (see Fig. 2b). The first cluster comprised three sampling sites (sampling sites 12, 2 and 3), the second cluster two sampling sites (sampling sites 5 and 7), and the third cluster seven sampling sites (sampling sites 1, 4, 6, 8, 9, 10, and 11). According to the results of the Jaccard’s coefficient, the lakes and lagoons are divided into three main clusters with regards to the similarity of species assemblages that exist in the lagoons (see Fig. 2c). The first cluster included two lagoon (Taşaltı Lagoon (Brackish-freshwater) and Tuzla Lake 3 (freshwater)), the second cluster was made up of one lagoon (Tuzla Lake 2), and the third cluster comprised three lagoon (Dalyan, Işık, Kuvalak, Taz, and Tuzla Lake 1). Faunal similarities between the sampling sites were computed using Jaccard’s coefficient test. The typical brackish water community of the Dalyan, Işık, and Taşaltı lagoons appears to be colonized by euryhaline and eurythermal ostracod species. The lagoons were classified on the basis of their mean values of salinity according to the Venice System (1958, 1959). All of the Enez lagoons can be characterized as shallow, alkaline, mostly saline (varying from freshwater to polyhaline), and oxygen-rich water according to the measured physicochemical properties. The species diversity for each sampling site was estimated using the Shannon–Weaver index (H’). The highest diversity was recorded at sampling site 12 (0.935) in September 2016 and the lowest (0.066) at sampling site 10 in March 2016 (see Table 6). The species diversity value is given as zero for both sampling sites 3 (Tuzla Lake 3) and 4 (Taz Lagoon) due to the dryness of the lagoons in September 2016.

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Figure 2. Jaccard’s coefficient similarity dendrograms showing the faunal similarity among the 12 sampling sites (based on presence/absence of species) and clustering relationships among the 16 ostracod species. (Species codes are given in Table 3.)

Table 6. Shannon–Weaver diversity index (H') values for all sampling sites.

Sampling ST- 1 ST- 2 ST- 3 ST- 4 ST- 5 ST- 6 ST- 7 ST- 8 ST- 9 ST- 10 ST-11 ST-12 Date/Station Jan. 2016 0.194 0.367 0.759 0.224 0.724 0.179 0.716 0.185 0.189 0.192 0.219 0.672 Mar. 2016 0.191 0.352 0.812 0.265 0.717 0.183 0.741 0.188 0.169 0.066 0.123 0.874 May. 16 0.181 0.473 0.784 0.267 0.565 0.153 0.638 0.134 0.136 0.112 0.133 0.785 July 2016 0.169 0.489 0.77 0.197 0.526 0.174 0.568 0.14 0.142 0.125 0.136 0.812 Sept. 2016 0.224 0.501 0* 0* 0.595 0.196 0.585 0.172 0.173 0.113 0.132 0.935 Nov. 2016 0.227 0.417 0.707 0.216 0.719 0.224 0.751 0.212 0.207 0.219 0.231 0.754

Relationships among the seven environmental variables and ostracod species were analyzed using Spearman’s rank correlation coefficient test. The results are given in Table 7.

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Table 7. Spearman’s rank correlation coefficient showing the correlation between environmental variables and the 16 living ostracod species (levels of significance: *0.05 (2-tailed); **0.01 (2-tailed).

Ta Tw pH ORP DO Sat Sal. EC AP AC CE CT CV DS EV HS FF IBI IBR LI LE LR LL SA XC Ta 1 ,795** ,423** n.s n.s n.s n.s n.s ,651** n.s n.s ,315** n.s n.s n.s n.s n.s n.s n.s n.s ,320** n.s n.s n.s n.s Tw ,795** 1 ,621** -,296* ,325** ,325** n.s n.s ,646** n.s n.s ,348** n.s n.s n.s n.s n.s n.s n.s n.s ,358** n.s n.s n.s n.s pH ,423** ,621** 1 -,769** n.s n.s ,251* ,263* ,332** ,260* ,263* ,513** -,352** -,340** -,392** -,281* -,282* -,254* ,542** ,260* ,268* -,279* ,248*

ORP n.s -,296* -,769** 1 n.s n.s -,355** -,357** n.s -,315** -,315** -,503** ,525** ,500** ,307** ,558** ,295* ,606** ,606** ,594** -,631** -,316** -,316** ,418** -,303** DO n.s ,325** n.s n.s 1 ,835** -,248* -,245* n.s n.s n.s n.s ,307** ,287* ,284* ,331** ,283* ,566** ,566** ,582** n.s n.s ,243* n.s

Sat n.s ,325** n.s n.s ,835** 1 -,431** -,414** n.s n.s n.s n.s ,359** ,351** ,245* ,376** ,234* ,606** ,607** ,622** -,242* n.s n.s ,269* n.s PSU n.s n.s ,251* -,355** -,248* -,431** 1 ,991** n.s ,236* ,238* ,389** -,502** -,477** -,258* -,534** -,247* -,644** -,643** -,639** ,570** ,237* ,245* -,395** ,251* EC n.s n.s ,263* -,357** -,245* -,414** ,991** 1 n.s n.s n.s ,430** -,519** -,493** -,282* -,550** -,271* -,645** -,645** -,638** ,598** n.s n.s -,414** n.s AP ,651** ,646** ,332** n.s n.s n.s n.s n.s n.s n.s n.s ,283* n.s n.s n.s n.s n.s n.s n.s n.s ,275* n.s n.s n.s n.s AC n.s n.s ,260* -,315** n.s n.s ,236* n.s n.s 1 ,998** -,294* n.s n.s n.s n.s n.s -,244* -,244* -,244* n.s ,997** ,989** n.s ,989** CE n.s n.s ,263* -,315** n.s n.s ,238* n.s n.s ,998** 1 -,294* n.s n.s n.s n.s n.s -,244* -,244* -,244* n.s ,997** ,989** n.s ,992** CT ,315** ,348** ,513** -,503** n.s n.s ,389** ,430** ,283* -,294* -,294* 1 -,557** -,529** -,305** -,589** -,293* -,413** -,412** -,377** ,797** -,295* -,289* -,446** -,295* CV n.s n.s -,352** ,525** ,307** ,359** -,502** -,519** n.s n.s n.s -,557** 1 ,955** ,666** ,960** ,637** ,752** ,751** ,691** -,515** n.s n.s ,855** n.s DS n.s n.s -,340** ,500** ,287* ,351** -,477** -,493** n.s n.s n.s -,529** ,955** 1 ,682** ,918** ,649** ,729** ,727** ,666** -,485** n.s n.s ,891** n.s EV n.s n.s n.s ,307** ,284* ,245* -,258* -,282* n.s n.s n.s -,305** ,666** ,682** 1 ,624** 1** ,494** ,488** ,440** -,318** n.s n.s ,733** n.s HS n.s n.s -,392** ,558** ,331** ,376** -,534** -,550** n.s n.s n.s -,589** ,960** ,918** ,624** 1 ,600** ,774** ,773** ,715** -,544** -,188 -,188 ,821** n.s FF n.s n.s n.s ,295* ,283* ,234* -,247* -,271* n.s n.s n.s -,293* ,637** ,649** 1** ,600** 1 ,483** ,478** ,426** -,312** -,108 -,108 ,733** n.s IBI n.s n.s -,281* ,606** ,566** ,606** -,644** -,645** ,060 -,244* -,244* -,413** ,752** ,729** ,494** ,774** ,483** 1 1** ,994** -,707** -,244* -,244* ,669** -,244* IBR n.s n.s -,282* ,606** ,566** ,607** -,643** -,645** n.s -,244* -,244* -,412** ,751** ,727** ,488** ,773** ,478** 1** 1 ,994** -,707** -,244* -,244* ,662** -,244* LI n.s n.s -,254* ,594** ,582** ,622** -,639** -,638** n.s -,244* -,244* -,377** ,691** ,666** ,440** ,715** ,426** ,994** ,994** 1 -,707** -,244* -,244* ,601** -,244* LE ,320** ,358** ,542** -,631** n.s -,242* ,570** ,598** ,275* n.s n.s ,797** -,515** -,485** -,318** -,544** -,312** -,707** -,707** -,707** 1 n.s n.s -,422** n.s LR n.s n.s ,260* -,316** n.s n.s ,237* n.s n.s ,997** ,997** -,295* n.s n.s n.s n.s n.s n.s -,244* -,244* n.s 1 ,985** n.s ,994** LL n.s n.s ,268* -,316** n.s n.s ,245* n.s n.s ,989** ,989** -,289* n.s n.s n.s n.s n.s n.s -,244* -,244* n.s ,985** 1 n.s ,985** SA n.s n.s -,279* ,418** ,243* ,269* -,395** -,414** n.s n.s n.s -,446** ,855** ,891** ,733** ,821** ,733** ,669** ,662** ,601** -,422** n.s n.s 1 n.s XC n.s n.s ,248* -,303** n.s n.s ,251* n.s n.s ,989** ,992** -,295* n.s n.s n.s n.s n.s -,244* -,244* -,244* n.s ,994** ,985** n.s 1

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According to the Spearman correlation coefficient results (see Table 7), the most significantly positive correlations (1,000) are between I. biplicata and I. bradyi, E. virens and H. salina, and F. fabaeformis and E. virens. There was a significantly positive correlation between the typical lagoonal species L. elliptica and C. torosa (0.797), but they correlated negatively with the other ostracod species. These two species exhibited a positive correlation with salinity, the most important determining factor. There were significantly positive correlations between seven halophilic species (C. vidua, D stevensoni, E. virens, H. salina, F. fabaeformis, I. biplicata, I. bradyi, L. inopinata, and S. aculeata) originating from continental freshwater. All of these species exhibited a negative correlation with salinity, the most important determining factor. Significantly positive correlations (at a 0.05 significance level) were observed between the marine-lagoonal species A. convexa, C. elongata, L. rhomboidea, X. communis, and L. lacertosa. In contrast, there was a strong positive correlation between L. elliptica and C. torosa and all of the salinity. Figure 3 shows the results of the Canonical Correspondence Analysis (CCA).

Figure 3. CCA showing the relationship between 16 species (red triangles) and 9 environmental variables (red arrows). See Tables 2 and 4 for an explanation of abbreviations and variables.

In addition to these findings, along with the Ostracoda species, the following 10 foraminiferal species, some of which have been categorized as typical lagoonal, were determined in Enez lagoon complex: Ammonia beccarii (Linnaeus 1758), Ammonia tepida (Cushman 1926), Ammonia parkinsoniana (d’Orbigny 1839), Elphidium limbatum (Chapman 1907), Haynesina germanica (Ehrenberg 1840), Haynesina depressula (Walker and Jacob 1798), Spiroloculina angulata (Cushman 1917), Spiroloculina ornata (d’Orbigny 1839), Siphonaptera aspera (d’Orbigny 1826), and Quinqueloculina laevigata (d’Orbigny 1839). Of the marine ostracod species synchronically collected from the coasts of the Enez district of the Aegean Sea during this present lagoonal study, the determined species were: Aurila convexa (Baird 1850), Tenedocythere prava (Baird 1850), Buntonia giesbrechtii (Mueller 1894), Bosquetina dentata (Mueller 1894), Carinocythereis carinata (Roemer 1838), Sagmatocythere littoralis (Mueller 1894), Semicytherura

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sulcata (Mueller 1894), Loxoconcha agilis (Ruggieri 1967), Loxoconcha bairdi (Mueller 1912), Loxoconcha rhomboidea (Fischer 1855), Loxoconcha tumida (Brady 1869), Xestoleberis communis (Mueller 1894), Xestoleberis cornelii (Caraion 1963), and Xestoleberis dispar (Mueller 1894) Phytoplankton bloom was observed during September 2016 at sampling site 3.

Discussion

Twelve sites (three in Dalyan Lagoon, two each in the Işık and Taşaltı lagoons, and one each in Kuvalak Lagoon, in Taz Lagoon, in Tuzla Lake 1, in Tuzla Lake 2, and in Tuzla Lake 3) from the Enez lagoon complex were selected for sampling, and a total of 16 ostracod species were determined from these sampling sites. The highest number of ostracod individuals (4,950 individuals) was found at sampling site 1 (see table 4) and the highest number of ostracod species (seven species) was also found at sampling site 1.

Evaluation of the Relationships between Sampling Sites Structure and Ostracod Assemblages Sampling site 1, at Tuzla Lake 1, featured only two euryhaline ostracod species (Cyprideis torosa and Loxoconcha elliptica). The most dominant species was C. torosa (84%), with L. elliptica at 16%. In the past, when this lake was used as a salt mine, the Dalyan and Taşaltı lagoons were connected to this lake, but today, they are separated. According to the salinity classification at this site, the lagoon’s salinity varied from polyhaline (24 psu in January) to euhaline (41.2 psu in September). This finding shows that precipitation/evaporation ratios determine the shape of the physicochemical parameters within the lagoonal ecosystem. Sampling site 2, at Tuzla Lake 1, featured one euryhaline ostracod species (Cyprideis torosa) and three halophilic freshwater species (L. inopinata, I. biplicata, and I. bradyi). The most dominant species was C. torosa (50%), followed by L. inopinata (36%), I. biplicata (7%), and I. bradyi (7%). Today, this lake is separated from Dalyan Lagoon, Tuzla Lake 1, and Tuzla Lake 3. This lagoon is slightly less affected by saltwater intrusion because it is located further from the other bodies. According to the salinity classification (Venice System, 1958 and 1959), the lagoon salinity was oligohaline (1.9–2.8 psu), this results are showing that there is more precipitation than evaporation. Sampling site 3, at Tuzla Lake 3, featured seven halophilic freshwater species (C. vidua, D. stevensoni, H. salina, I. biplicata, I. bradyi, L. inopinata, and S. aculeata). The most dominant species was C. vidua (23%); other dominant ostracod species were: H. salina (16%), I. bradyi (16%), L. inopinata (16%), I. biplicata (16%), D. stevensoni (5%), and S. aculeata (4%). Separated from Dalyan Lagoon and Tuzla Lake 2, this lake is slightly less affected today by saltwater intrusion because it is located further from the other water bodies. According to the salinity classification, Tuzla 3 is a freshwater lake (0.2–0.3 psu), which shows that this lake is fed only by rainwater. The diversity and richness of macrophyte species reveal this lake’s freshwater wetland features (see Table 2). Slightly higher electrical conductivity and salinity values are indicators of slightly saltine environments; determining the halophilic ostracod species also confirms this. Sampling site 4, at Taz Lagoon, featured two euryhaline ostracod species (Cyprideis torosa and Loxoconcha elliptica). The most dominant species was C. torosa (78%), with L. elliptica at 22%. According to the salinity classification, the lagoon varied from polyhaline (22.2 psu in January) to euryhaline (40 psu in July). During the rainy seasons, the shallow Taz Lagoon connects to Işık Lagoon; during the dry season, whoever, this connection is lost due to evaporation. Since, even at the end of the season in September, Taz Lagoon is completely dry, environmental variables could not be measured. Sampling site 5, at Işık Lagoon, featured two euryhaline ostracod species (Cyprideis torosa and Loxoconcha elliptica) and five marine species (A. convexa, C. elongata, L. rhomboidea, L. lacertosa, and X. communis). According to the salinity classification, this lagoon’s salinity varied from polyhaline (25.1 psu in January) to euryhaline (34 psu in September). This sampling site was located in a connecting canal between Işık Lagoon and the Aegean Sea, which is why three marine ostracods species (L. rhomboidea, L. Ecologica Montenegrina, 19, 2018, 130-151 145

SPATIOTEMPORAL DISTRIBUTION AND HABITAT PREFERENCES OF OSTRACODA IN THE ENEZ LAGOONS lacertosa, and X. communis) were determined at this site. Finding marine ostracods at this site, where there is an inflow of seawater, is an expected result. Seawater inflow, rainwater, and evaporation all influence the salinity in this lagoon. However, sampling site 6 at this lagoon featured two euryhaline ostracod species (Cyprideis torosa and Loxoconcha elliptica). According to the salinity classification, the lagoon’s salinity varied from α-mesohaline (24.6 psu in January) to euryhaline (33 psu in September) as seawater did not strongly influence this sampling site. However, the present sandy barrier between Işık Lagoon and the Aegean may be damaged during excessive precipitations. The most dominant species was C. torosa (81%) at both sampling sites. Other dominant ostracod species were: L. elliptica (15%), A. convexa (1%), L. lacertosa (1%), C. elongata (1%), L. rhomboidea (0.52%), and X. communis (0.48%). Sampling site 7, at Dalyan Lagoon, featured two euryhaline ostracod species (Cyprideis torosa and Loxoconcha elliptica) and five marine species (A. convexa, C. elongata, L. rhomboidea, L. lacertosa, and X. communis). According to the salinity classification, salinity varied from α-mesohaline (17.1 psu in January) to polyhaline (18.2 psu in September). The sampling site was located in a connecting canal between Dalyan Lagoon and the Aegean Sea, similar to sampling site 5. Consequently, seawater inflow, rainwater, and evaporation influenced the salinity rates at this sampling site, too. Seawater flows in from the sea to this lagoon, while brackish water flows out from the lagoon to the sea, and this too strongly influenced this sampling site. Dalyan Lagoon connects to Taşaltı Lagoon via a man-made concrete canal under the roadway. Also, fresh water from Lake Gala flows into Taşaltı Lagoon via Taşyarma Canal. Sampling sites 8 and 9, at Dalyan Lagoon, featured two euryhaline ostracod species (Cyprideis torosa and Loxoconcha elliptica). According to the salinity classification, the lagoon’s salinity varied from alfa mesohaline (16.1 psu) to polyhaline (19.2 psu). These sampling sites located far from the sea connecting canals. Seawater inflow influenced these sampling sites less than sampling site 7, and fresh water from Taşyarma Canal and from rain enters Dalyan Lagoon, especially in rainy periods. The most dominant species was C. torosa (85%), with other dominant ostracod species as follows: L. elliptica (12%), A. convexa (1%), L. lacertosa (0.76%), C. elongata (0.64%), L. rhomboidea (0.42%), and X. communis (0.22%). Sampling site 10, at Kuvalak Lagoon, featured two typical euryhaline ostracod species (Cyprideis torosa and Loxoconcha elliptica). The most dominant species was C. torosa (92%), with L. elliptica at 8%. According to the salinity classification, the lagoon varied from polyhaline (30 psu in January) to euhaline (36 psu in July). The present sandy barrier between the Dalyan and Kuvalak lagoons may be damaged during excessive precipitations. Water from Kuvalak Lagoon flows into Dalyan Lagoon. However, by the end of dry season, this lagoon is completely dry. Sampling site 11, at Taşaltı Lagoon, featured two euryhaline ostracod species (Cyprideis torosa and Loxoconcha elliptica). According to the salinity classification, salinity is α-mesohaline (12.9-15.1 psu). This lagoon is located far from the sea, and the inflow of brackish water from Dalyan Lagoon influenced this sampling site more than sampling site 12, also at Taşaltı Lagoon. Sampling site 12 featured a euryhaline and typical brackish ostracod species (Cyprideis torosa) and nine halophilic freshwater species (C. vidua, D. stevensoni, E. virens, H. salina, F. fabaeformis, I. biplicata, I. bradyi, L. inopinata, and S. aculeata). According to the salinity classification, salinity here is β-oligohaline (1.6-2.4 psu). The most dominant species was C. torosa (56%), followed by C. vidua (12%), H. salina (7%), L. elliptica (6%), I. bradyi (5%), I. biplicata (5%), L. inopinata (4%), S. aculeata (2%), D. stevensoni (1%), E. virens (1%), and F. fabaeformis (1%). The brackish water from this sampling site was more influenced by the fresh water of Taşyarma Canal than sampling site 11. In rainy periods, fresh waters of Taşyarma Canal reach to Taşaltı Lagoon through flowing on the organic-rich sediments of this canal, as the macrophyte species richness and diversity indicates to this proves (see Table 2).

Analysis of the Dominant Ostracod Species Cyprideis torosa and Other Species C. torosa is a typical brackish water species that tolerates a wide salinity range from 0.5 to 150 psu (De Deckker 1981; Gasse et al. 1987; Meisch 2000; Neale 1988). It reproduces in waters up to 60 psu (Meisch 2000). In accordance with these data, this species was found in over 50 psu salinity in shallow tectonic playa Lake Acıgöl (Altınsaçlı & Mezquita 2008). This cosmopolitan species is an ideal indicator for 146

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determining changes in salinity values in the past. As in this study, C. torosa is one of the most reliable species for assessing lagoonal environments due to its higher abundance compared with other ostracod species in lagoons, and that it is more easily differentiated from other ostracod species, and is an important indicator species for define to relationships between the ostracod species and environmental variables. The ostracod assemblages at the Enez lagoon complex were mainly represented by C. torosa (70.5%; dominant in seven lagoons), followed by L. elliptica (9.44%). Studies by Altınsaçlı (2004, 2014) and Perçin-Paçal et al. (2017) indicated that individual numbers of C. torosa are always higher than L. elliptica, as was also the case in the present study. Loxoconcha elliptica has frequently been found in salinity ranges between 18 and 30 psu typical of shallow coastal brackish water habitats such as lagoons, river mouths, and salt marshes (Altınsaçlı 2004; Athersuch et al. 1989; Besonen 1997; Bonaduce et al. 1975; Mischke et al. 2012; Pascual & Carbonel 1992). This typical lagoonal species has previously been determined in lagoons in Turkey (Altınsaçlı 2004; Altınsaçlı 2014; Perçin-Paçal 2017). As well as Loxoconcha elliptica being able to tolerate high salinity (up to 65 psu) like C. torosa (Zaninetti 1982; 1984). As confirmed in the present study, L. elliptica is the second-most dominant species in lagoonal environments and is generally found together with Cyprideis torosa. Heterocypris salina and Sarscypridopsis aculeata occur most commonly in mesohaline coastal habitat (Meisch 2000). H. salina has been recorded in some coastal brackish wetlands in Turkey by Altınsaçlı (2004) and Perçin-Paçal et al. (2015). Only found in Taşaltı Lagoon in this study, S. aculeata is a relatively rare species compared to other species found in the Enez lagoons. Limnocythere inopinata is a cosmopolitan species, occurring in deep freshwater lakes as well as in brackish coastal water bodies (Curry et al. 2016; Meisch 2000). According to Curry et al. (2016), in the Mediterranean region, its range of salinity tolerance ranges from 0.75 to 42.5 psu with an optimum of 7 psu. This species was found in both a continental lake (salinity range varying from freshwater to β oligohaline) and two β-mesohaline coastal wetlands (Altınsaçlı et al. 2014). It can also tolerate low salinities (Meisch, 2000). Results of from the Enez lagoons showed that L. inopinata, while less common and abundant, was present in Tuzla Lake 3 and Taşaltı Lagoon and, more abundantly, in Tuzla Lake 2. Ilyocypris biplicata is accepted as a junior synonym of I. gibba. Ilyocypris gibba is oligohaline (Meisch 2000). Our findings generally strongly confirm the data of Altınsaçlı (2015) concerning ostracods found in seven karstic springs. Ilyocypris biplicata prefers living environments like springs, rivers, streams, ditches, canals, and rice fields (Meisch 2000), environments with muddy or sandy bottoms (Bronshtein 1947; Klie 1938). Cypridopsis vidua is one of the most abundant freshwater ostracods on the earth’s surface, both in terms of numbers as well as its percentage occurrence among water habitats (Curry et al. 2016). According to Curry et al. (2016), it can be found in water bodies with salinities ranging from 0.14 to 2.2 psu in the Mediterranean region. In this study, the species was determined in Tuzla Lake 3 (freshwater) and Taşaltı Lagoon (oligosaline). The species accounts for 3.61% of the total counted in both study’s ostracod records. Darwinula stevensoni is a cosmopolitan mesohalophilic species that lives in water with salinity as high as 15 psu (Hiller 1972). It is an opportunistic species that quickly populates potential sites. D. stevensoni was recorded in oligosaline (0.7–4.6 psu) conditions of Sarısu Lagoon located on the coast (Altınsaçlı et al. 2014) and an oligosaline spring located on the Aegean Sea coast (Altınsaçlı et al. 2015). The present study again indicated this species can tolerate varying levels of salinity Loxoconcha rhomboidea was recorded at water depths varying between 1 and 57 m in the Mediterranean Sea (Montenegro et al. 1998). This ostracod species is common in marine and phytal environments (Athersuch et al. 1989) and has been commonly found in littoral and sublittoral zones in the seas of Turkey (Perçin-Paçal 2011; Perçin-Paçal et al. 2015) Aurila convexa is known as a common species in the Mediterranean Sea (Bonaduce et al. 1975) and was also recorded in the northern Aegean Sea (Stambolidis 1985). This polyhaline species was determined in brackish water systems of the Black Sea (Schornikov 1969). A. convexa is a common species in littoral and shallow sublittoral environments, living on algae and sand substrates of Turkey Ecologica Montenegrina, 19, 2018, 130-151 147

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(Perçin-Paçal et al. 2015). Distribution of this species in littoral and sublittoral zones of Turkish seas has been reported (Perçin-Paçal 2011; Perçin-Paçal et al. 2015.) C. vidua in 39, C. torosa in 14, D. stevensoni in 19, E. virens in 14, H. salina in 40, F. fabaeformis in 19, I. bradyi in 36, I. biplicata in 8, L. elliptica in 5, and L. inopinata in 19 of 63 major wetlands (including lakes, marshes, lagoons, springs, and streams) in Turkey have been recorded (Altınsaçlı 2004). Typical marine species A. convexa, C. elongata, L. rhomboidea, X. communis, and L. lacertosa were reported in the seas and lagoons of Turkey (Perçin-Paçal 2015). Salinity has been shown to be one of the major controlling factors affecting the distribution of Ostracoda in the Enez lagoons (see Figure 4).

Figure 4. Salinity tolerance diagram of Ostracoda determined in the Enez lagoons.

Marine species and typical brackish water species show a distribution over a wider salinity range, while continental halophilic species show a distribution over a narrow salinity range (see Figure 4). Seawater and freshwater entrances to the lagoon cause fluctuations in the salinity. Clear significant correlations were found between the salinity level and the diversity of ostracods. Specifically, while the presence of marine ostracod assemblages indicate a marine influence, the presence of typical lagoonal ostracod assemblages indicate a restricted fauna in brackish or hypersaline water, which is evidence of the above correlation. A combination of low salinity and brackish water is a common feature of lagoons in areas of high rainfall. According to the results of CCA analyses, the longest arrows belong to salinity and electrical conductivity variables; this indicates these variables are effective in the environment (see Fig. 3). However, the euryhaline and eurytherm species C. torosa and L. elliptica were not significantly affected by changes since they have a wide tolerance for environmental variables. According to the results of CCA analyses, the longest arrows belong to salinity and electrical conductivity variables; this indicates these variables are effective in the environment (see Fig. 3). However, the euryhaline and eurytherm species C. torosa and L. elliptica were not significantly affected by changes since they have a wide tolerance for environmental variables. These results are once again confirmed to characteristics of each two species. However, as expected, the euryhaline species C. torosa was not found at sampling site 3, which had more input of fresh water. Approximately 75.73% of the relationships between the species and environmental

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variables are expressed by the first two CCA axes in Figure 3. The clustering of ostracod species to ecological characteristics is clearly reflected in the CCA diagram. In contrast to the freshwater, brackish water and euryhaline ostracod species determined in the Enez lagoons show a high adaptability to a variety of water temperatures, a factor that is highly variable within the environment. The species living in shallow lagoons do not survive in this habitat due to the quick changes of water temperature, which depend on the air temperature. Salinity is one of the major controlling factors affecting the distribution of Ostracoda (Amorosi et al. 2014; Gliozzi & Mazzini 1998; Marco-Barba et al. 2013), as in this study. The Enez lagoons are characterized by the high dominance of opportunistic species such as Ammonia tepida, Ammonia parkinsoniana, and Cyprideis torosa. In this study, species diversity was significantly lower in typical lagoonal sites but significantly higher in freshwater-inflow sites. The distribution of ostracod specimens is affected by environmental stress, which can be of natural origin (e.g., lower salinity due to freshwater input) or caused by anthropogenic activities (e.g., sewage outfall, and agricultural or water activities). The results of this study show that marine ostracod species found in lagoons are transported to other lagoonal environments through established sea connections. Temperature, salinity, pH, and dissolved oxygen values increased during the dry season but decreased in the rainy seasons. Freshwater enters Taşaltı Lagoon mainly via Taşyarma Canal and other drainage channels. Rainwater is a major freshwater source for the other water bodies studied, too. Strong winds blow from the north and northeast in this area, and we observed that micro-tidal currents and winds are important factors affecting the water circulation of lagoons. Salinity causes a seasonal alteration, with high values at the end of summer (higher evaporation,) and lower values in winter (lower evaporation, higher rainfall). Although brackish environments are characterized by strong fluctuating salinities, they are very important habitats due to the diversity of plants and animal species. The rich biodiversity levels of the Enez lagoons are at remarkable levels (see Table 2). We indicate that the diversity and distribution of Ostracoda assemblages in these studied lagoons and former saltpan environments depend on the effects of increased or decreased salinity. Finally, the lagoons have less salinity than normal marine salinity, and the fluctuation of salinity produces a lower specific diversity in the Dalyan, Işık, Taşaltı (except sampling site 12), Taz, and Kuvalak lagoons, and the species dominance of C. torosa and L. elliptica in these lagoons is because they adapt to strong oscillations in salinity. This study confirms that benthic Ostracoda are useful indicators for understanding impacts of abiotic variables on brackish and transitional environments. This research into the Ostracoda fauna of the Enez lagoons has ensured important data for future benthic research. What is sure already is that the substantial agricultural activity (with high fertilization intensity and pesticides used) in the surroundings has certainly impacted the Enez lagoon ecosystem. Residential, industrial, and agricultural pollutants were determined in the study area. Touristic activities, too, have led to the overexploitation of the lands surrounding the lagoons, and we are likely to see a decrease in the site’s biodiversity in the coming years.

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