Indian Journal of Geo Marine Sciences Vol. 47 (11), November 2018, pp. 2296-2304

Soft bottom mollusc assemblages (-bivalvia) in marine shallow waters of the western turkey coast

Mehmet Culha*, Ozlem Aksoy & Gozde Ekin Tatarhan

Department of Hydrobiology, Faculty of Fisheries, Izmir Katip Celebi University, Balatcık, Cigli, Izmir/Turkey *[E.mail: [email protected]]

Received 27 April 2017; revised 24 July 2017

The most dominant family was found to be with 10 . Of the 105 species obtained stations, the most dominant species was Bittium reticulatum (26%) with 2226 specimens, followed by Mytilus galloprovincialis (11%) with 1022 specimens and membranacea (8%) with 713 specimens, respectively. Shannon-Weaver’s Diversity Index (H'), Pielou’s Evenness Index (J’), Soyer’s Frequency Index (F), Bray-Curtis Similarity Index and Pearson's Correlation Analysis were applied to the benthic mollusc fauna. Diversity index values (between 1.71 and 4.43) and evenness index values (between 0.38 and 0.82) were determined in the area. According to Bray Curtis similarity analysis there were 3 distinct species assemblages in the area. The number of individuals, diversity index value, gastropoda and bivalvia species were also positively correlated with temperature.

[Keywords: Gastropods, Bivalves, , communities, Candarlı bay, Aegean Sea] Introduction organisms in the water column. They are important The phylum Mollusca is one of the largest and most food sources, especially for demersal fish9. well-studied groups in the kingdom (about Because of its location, geomorphological structure 50,000 marine living species belonging to 8 classes)1. and hydrographical and ecological characteristics, the Among the classes, Gastropods and Bivalves are the Aegean Sea comprises an important part of the most interesting groups of molluscs. they have Mediterranean ecosystem. Biologically, the Aegean attracted amateurs, businessmen, ecologists and Sea can be divided into two subregions (northern and scientists from around the globe for centuries2. In southern). The ecological features of these two basins addition, these classes, which are economically very show great variety10, 11. The coasts of Turkey have important, are widely cultivated2. They also play been subject to many studies for over two centuries. importante roles in structure of the ecosystem and The first available information about the Turkish maintenance of the biodiversity3. Furthermore, some coast is from Forsskål12. This study was followed by molluscs have been widely used in monitoring studies Forbes13 in the Aegean Sea, Ostroumov14 in the of various contaminants worldwide because of their Marmara Sea and Colombo15 in the Dardanelles. economic and ecological significance4. In soft bottom Investigations of the Mollusca fauna (Gastropods– sediments of the marine ecosystem, knowledge about Bivalves) in the Aegean Sea coastal waters of Turkey the spatial and temporal distribution of species is have been conducted by many researchers. However, quite important for understanding biotic and abiotic until recently, there has been a limited number of mutual effect5. Hydrographical, sediment structure studies in Candarlı Bay that involve the species of and biological varieties are most likely to be temporal mollusca. These studies were carried out in Candarlı controlling agents of the benthic group in marine Bay and its vicinity16, 17, 18, 19, 20, 21, 22, 23. shallow waters6, 7. Present study consists the information on the molluscan Benthic molluscs have been used as descriptors of biodiversity in the area and the factors governing the the sublittoral soft-bottom benthic association with coastal ecosystems distributions in Candarlı Bay. their ecological relationship to water quality 3, 4, 8 Materials and Methods variations in the . Furthermore, Collection and evaluation of the study material according to dietary diversity, benthic organisms can The present study was carried out with the aim of supply a link between substratum and living determining the species of Mollusca (Gastropods and CULHA et al.: SOFT BOTTOM MOLLUSC ASSEMBLAGES (GASTROPODA-BIVALVIA) 2297

Bivalves) distributed in the coastal ecosystem of Pearson’s correlation analysis was applied to verify Candarlı Bay (Fig 1). The benthic samples was collected existing relationships (the physicochemical at 9 stations in depths from 0.5 to 5 m between the years parameters with number of individuals, diversity 2013 and 2014 by using sampling gears such as the index, evenness index and number of species). dredge, hand dredge, spatula and quadrat. Information Statistical analysis was performed using SPSS v21. about the study stations are given in Table 1. Sediment particle (grain) size analysis was carried The collected material was fixed in 4% formalin out to understand the sea-bed inhabited by living solution and examined in the laboratory. Material was organisms. No single analytical method covers the washed through a sieve with 0.5 mm and 1 mm mesh entire size range of sediment particles. For many sizes, with the help of pressurized water, and was then purposes, including benthic ecology, sedimentology stored in 70% alcohol. Molluscan specimens were and evaluation of chemical contaminant data, sieves classified into groups using a stereomicroscope are the most practical option for describing gravel and (Olympus SZ61), and species were identified. sand sizes down to 63 μm. Also for this purpose, Identification was performed according to shell Wentworth interval sieves were used38. Sediment characteristics and several references, including24, 25, samples were taken from the each stations. And then, 26, 27, 28, 29, 30, 31. The methods of Sabelli et al.29, 30, a series of Wentworth interval sieves were used to Ozturk et al.1 and the Check List of European Marine Mollusca32 were followed for the systematic status of the species (Table 2). Furthermore, various statistical analyzes were carried out to establish the distributional and ecological characteristics of those species and individuals. Results of Soyer’s Frequency Index formula33, Bellan-Santini’s Dominance Index Formula34, Shannon-Wiener’s Diversity Index35 (H'), Pielou’s Evenness Index36 (J') and Bray-Curtis’s Similarity Index 37 were displayed in graphical form. Additionally, the physicochemical parameters of the sampling stations were measured in-situ seasonally from the surface to a depth of approximately 2 m, using a WTW Multi 3420 water quality meter probe. Fig. 1 — Research area and sampling stations Table 1 — Information related to the study stations Station No Coordinates Depth (m) Biotope Sampling Equipment 1(Barınak) 38°48'12'' N 0,5-1 Sand, Rocky&Sandy, Cystoseira spp. Quadrat, Spatula, Hand dredge 26°57'46'' E 2 (Iskele) 38°48'26'' N 0,5-2 Sand, Rocky&Sandy, Stony&Sand Quadrat, Spatula, Hand dredge 26°58'31'' E 3 (Tabakcı) 38°49'35'' N 0,5-3 Sand Quadrat, Spatula, Hand dredge 26°58'59'' E 4 (Arka plaj) 38°50'46'' N 0,5- 3,5 Sand, Sandy mud, Cystoseira spp. Quadrat, Spatula, Hand dredge 26°58'14'' E 5 (Pınarcık) 38°51'24'' N 0,5- 1,5 Sand&Rocky Quadrat, Spatula, Hand dredge 27°00'37' 'E 6 (Sakran) 38°53'11'' N 0,5- 1,5 Sand&Rocky Quadrat, Spatula, Hand dredge 27°03'40'' E 7 (Candarlı-Adaburnu) 38°56'19'' N 1- 4 P. oceanica, Muddy, Sand Dredge 26°56'28 '' E 8 (Candarlı-Bakırcay) 38°55'46'' N 1- 4,5 P. oceanica, Muddy, Sand Dredge 26°56'25'' E 9 (Aliaga) 38°50'54'' N 1- 5 P. oceanica, Muddy, Sand Dredge 26°59'29'' E 2298 INDIAN J. MAR. SCI., VOL. 47, NO. 11, NOVEMBER 2018

determine percentages of sand, silt and clay (particle Ecological and biological assessment size analysis) at the laboratory39. As a result of evaluating the samples, 105 species and 8668 individuals belonging to 53 families were Results and Discussion encountered during the course of this study (Table 2). Physicochemical assessment Among these, gastropoda presented the maximum To provide information about the region and number (62 taxon and 6444 individuals) of species and stations, some physicochemical parameters were individuals, while bivalvia presented the minimum measured in situ at the stations. At shallow-water number (43 taxon and 2224 individuals) of species and stations (0.5-5m), these varied between; 15.3 °C individuals. The number of species in the previous (winter, St.2) and 26.6 °C (summer, St.2) for surface studies were differed from each other. These were water temperature; 6.18 mg/l (summer, St.6) and 10.9 because of different depths, biotopes and stations; using mg/l (autumn, St.6) for dissolved oxygen; 8.11 different sampling material such as dredge, gravity (winter, St.8) and 8.32 (summer, St.9) for pH; 34.2‰ corer, grab etc. Considering prior studies, most of the (winter, St.8) and 38.9‰ (summer, St.6) for salinity; species found in the present study are common and well- and 50.4 μS cm-1 (winter, St.4) and 58.7 μS cm-1 known species near the Turkish coasts. 43 (autumn, St.9) for conductivity. Basaran and Arslan In this study at Candarlı bay, the Rissoidae family 21 et al. also measured some physicochemical was found to have the highest number of species with parameters at Candarlı Bay. They found values close 10 species, dominance value of 9%, followed by to the parameters found in this study. Trochidae with 8 species (dominance value of 8%) The physicochemical parameters of the study area and then Mytilidae and Veneridae families with 7 were related to the number of individuals, diversity species each (dominance value of 7%). In terms of the index (Hꞌ), evenness index (Jꞌ) and number of species. number of individuals, the Cerithiidae family Among all physicochemical values, there was only a presented the highest number of individuals with 3243 correlation with temperature. According to the and a dominance value of 37%, followed by Rissoidae Pearson's correlation analysis, a positive correlation as the second highest with 1686 individual and a (p<0.05) was determined with temperature between dominance value of 19% (Fig 3). This situation can be number of individuals (r=0.436), diversity index value explained as a result of their species being the (r=0.375), gastropoda (r=0.426) and bivalvia species dominant which can create an enormous populations (r=0. 362), respectively. The evenness value both in terms of depth and various biotopes. (r= -0.334) was negative correlated with temperature. When the results of distribution of these species Marine mollusks are influenced by substrate according to the stations and seasons were evaluated, 40 characteristics, depths and hydro-dynamics . The the highest number of species was observed in the substrate characteristics and hydrodynamic forces spring period at the st. 9 (36 species) but the least have been considered to be two of the principal value was in the autumn period at the st. 5 (7 species) factors governing the community structures in the (Fig 4). In terms of the number of individuals, the shallow water benthic environments of the Aegean highest number of individuals was observed in the 41 Sea . Particle (grain) size analysis (as % value) of spring period in st. 7 (828 ind.) but the lowest value sediment belonging to nine stations was made to was in the winter period in st. 2 (40 ind.) (Fig 5). demonstrate the ecological status of the sea-bed inhabited by living organisms. The order of the three groups (Sand, Silt, Clay) is as follows; max 92.56% (st. 4)–min 36.47% (st. 8) for Sand, max 55.71% (St. 8) – min 3.94% (st. 4) for Silt, max 8.67% (St. 1) – min 0.73% (St. 3) for Clay. Sand was the dominant component of the sediment at all stations, except for st. 8. Silt content varied between 3.94% and 55.71%. Finaly, Clay was the minimum compenent at all the stations (Fig. 2). Generally, while the sediment structure consists of sand and gravel materials in Dikili canal, in Candarlı Bay, sandy, silty, clayey and 42 muddy materials were observed . Fig. 2 — Sediment particulate size analysis belonging to the stations CULHA et al.: SOFT BOTTOM MOLLUSC ASSEMBLAGES (GASTROPODA-BIVALVIA) 2299

Table 2 — List of mollusca species were encountered and their total number of individuals as well as their dominance (%D) and frequency (%F) results Stations Species 1 2 3 4 5 6 7 8 9 %D %F rustica Linnaeus, 1758 6 2 1 1.1 33.3 Patella ulyssiponensis Gmelin, 1791 2 0.02 11.1 nubecula (Linnaeus, 1758) 3 2 0.06 22.2 Gibbula adansonii (Payraudeau,1826) 10 27 23 10 45 29 4 4 7 1.85 100 Gibbula albida (Gmelin, 1791) 2 11 10 6 47 41 9 9 8 1.66 100 Gibbula divaricata (Linnaeus, 1758) 1 13 9 0.27 33.3 Gibbula rarilineata (Michaud, 1829) 1 5 0.07 22.2 Jujubinus exasperatus (Pennant, 1777) 5 6 14 21 19 0.76 55.6 Jujubinus striatus (Linnaeus, 1758) 2 0.02 11.1 Phorcus articulatus (Lamarck, 1822) 14 17 0.36 22.2 Phorcus turbinatus (Born, 1778) 60 13 1 128 41 2.83 55.6 Calliostoma laugieri (Payraudeau, 1826) 2 1 2 0.06 33.3 pullus pullus (Linnaeus, 1758) 3 12 6 31 54 17 13 23 1.85 88.9 Tricolia speciosa (Megerle von Mühlfeld, 1824) 1 9 1 0.13 33.3 Smaragdia viridis Linnaeus, 1758 8 4 0.14 22.2 Bittium latreillii (Payraudeau, 1826) 2 18 25 25 13 68 119 3.14 77.8 Bittium reticulatum (da Costa, 1778) 366 201 75 17 178 325 283 489 292 25.91 100 Bittium scabrum (Olivi,1792) 59 78 25 13 51 98 94 123 133 7.85 100 Cerithium vulgatum Bruguiere, 1792 3 3 13 1 8 18 27 0.85 77.8 Potamides conicus (de Blainville, 1829) 26 0.30 11.1 Turritella communis Risso, 1826 1 0.01 11.1 Marshallora adversa (Montagu, 1803) 1 0.01 11.1 Monophorus erythrosoma (Bouchet & Guillemot, 2 0.02 11.1 1978) Monophorus perversus Linnaeus, 1758 2 4 1 0.08 33.3 Cerithiopsis tubercularis (Montagu, 1803) 1 1 0.02 22.2 Epitonium clathrus (Linnaeus, 1758) 1 1 1 1 2 0.07 55.6 Melarhapne neritoides (Linnaeus, 1758) 7 4 0.13 22.2 cimex (Linnaeus,1758) 20 1 3 3 26 14 15 13 29 1.44 100 Alvania discors (Allan, 1818) 7 8 0.17 22.2 Alvania lactea (Michaud, 1822) 2 0.02 11.1 Rissoa auriscalpium (Linnaeus, 1758) 9 35 51 1.11 33.3 Rissoa membranacea (Adams J., 1800) 15 5 22 88 120 301 89 73 8.30 88.9 Rissoa monodonta Philippi, 1836 5 4 0.10 22.2 Rissoa similis Scacchi,1836 4 32 12 67 37 1.77 55.6 Rissoa splendida Eichwald, 1830 4 8 40 5 101 132 80 118 72 6.52 100 Rissoa variabilis (Von Muehlfeldt, 1824) 2 4 0.07 22.2 Rissoa violacea Desmarest, 1814 6 4 0.12 22.2 Truncatella subcylindrica (Linnaeus, 1767) 1 1 0.02 22.2 Vermetus triquetrus Bivona-Bernardi,1832 1 0.01 11.1 Calyptraea chinensis (Linnaeus, 1758) 1 0.01 11.1 Natica hebraea (Martyn, 1784) 1 0.01 11.1 Bolinus brandaris (Linnaeus, 1758) 10 0.12 11.1 Hexaplex trunculus (Linnaeus, 1758) 20 6 2 26 10 15 0.92 66.7 Gibberula philippii (Monterosato, 1878) 1 0.01 11.1 Vexillum ebenus (Lamarck, 1811) 7 6 0.15 22.2 cornea (Linnaeus, 1758) 3 1 0.05 22.2 (contd.) 2300 INDIAN J. MAR. SCI., VOL. 47, NO. 11, NOVEMBER 2018

Table 2 — List of mollusca species were encountered and their total number of individuals as well as their dominance (%D) and frequency (%F) results (contd.) Stations Species 1 2 3 4 5 6 7 8 9 %D %F Pisania striata (Gmelin, 1791) 5 1 3 0.10 33.3 Cyclope neritea (Linnaeus, 1758) 5 2 3 4 7 0.24 55.6 Nassarius mutabilis (Linnaeus, 1758) 1 2 0.03 22.2 Nassarius reticulatus (Linnaeus,1758) 2 6 18 6 8 112 27 27 2.40 88.9 Columbella rustica (Linnaeus, 1758) 2 30 3 4 0.45 44.4 Mitrella gervillii (Payraudeau, 1826) 21 0.24 11.1 Fusinus syracusanus (Linnaeus, 1758) 1 0.01 11.1 Conus mediterraneus Hwass in Bruguiere, 1792 2 1 1 1 0.06 44.4 Bela nebula (Montagu, 1803) 5 1 0.07 22.2 Mangelia costulata Risso, 1826 2 1 11 0.16 33.3 Megastomia conoidea (Brocchi, 1814) 1 1 2 0.05 33.3 Turbonilla pusilla (Philippi, 1844) 1 0.01 11.1 Ringicula auriculata (Ménard de la Groya, 1811) 1 0.01 11.1 Weinkauffia turgidula (Forbes, 1844) 1 1 1 0.03 33.3 Roxania utriculus (Brocchi, 1814) 3 0.03 11.1 Nucula nucleus (Linnaeus, 1758) 2 1 1 0.05 33.3 Anadara transversa (Say, 1822) 2 2 1 0.06 33.3 Arca noae Linnaeus,1758 1 1 0.02 22.2 Striarca lactea (Linnaeus, 1758) 4 2 1 0.08 33.3 Gregariella petagnae (Scacchi, 1832) 2 3 2 0.08 33.3 Lithophaga lithophaga (Linnaeus,1758) 6 0.07 11.1 Modiolus barbatus (Linnaeus, 1758) 17 26 12 10 19 60 27 14 2.15 88.9 Mytilaster lineatus (Gmelin, 1791) 4 26 5 0.41 33.3 Mytilaster marioni (Locard, 1889) 1 0.01 11.1 Mytilaster minimus (Poli, 1795) 16 76 1.07 22.2 Mytilus galloprovincialis Lamarck, 1819 279 115 20 433 28 112 13 4 18 11.90 100 Pinna nobilis Linnaeus, 1758 3 0.03 11.1 Aequipecten opercularis (Linnaeus, 1758) 2 4 0.07 22.2 Mimachlamys varia (Linnaeus, 1758) 16 16 2 1 3 11 5 6 0.70 88.9 Pecten jacobaeus (Linnaeus, 1758) 3 1 3 4 5 0.19 55.6 Anomia ephippium Linnaeus, 1758 2 3 0.06 22.2 Limaria hians (Gmelin, 1791) 16 7 18 7 16 17 14 1.11 77.8 Ostrea edulis Linnaeus, 1758 3 9 1 3 1 1 0.21 66.7 Ostrea stentina Payraudeau, 1826 3 2 0.06 22.2 Neopycnodonte cochlear (Poli, 1795) 1 0.01 11.1 Cardita calyculata (Linnaeus, 1758) 3 0.03 11.1 Glans trapezia (Linnaeus, 1758) 1 2 0.03 22.2 Loripes lucinalis (Lamarck, 1818) 1 2 2 6 5 0.19 55.6 Acanthocardia echinata (Linnaeus, 1758) 4 1 3 11 10 0.34 55.6 Acanthocardia paucicostata (Sowerby, G.B. II, 1841) 1 1 0.02 22.2 Acanthocardia tuberculata (Linnaeus, 1758) 3 0.03 11.1 Papillicardium papillosum (Poli, 1795) 1 13 2 6 11 14 80 1.48 77.8 Mactra stultorum (Linnaeus, 1758) 3 0.03 11.1 Spisula subtruncata (da Costa, 1778) 2 15 31 48 3 1.15 55.6 Tellina tenuis da Costa, 1778 1 12 1 5 0.22 44.4 Donax trunculus Linnaeus, 1758 10 5 15 13 1 0.51 55.6 Abra alba (Wood W., 1802) 1 0.01 11.1 (contd.) CULHA et al.: SOFT BOTTOM MOLLUSC ASSEMBLAGES (GASTROPODA-BIVALVIA) 2301

Table 2 — List of mollusca species were encountered and their total number of individuals as well as their dominance (%D) and frequency (%F) results (contd.) Stations Species 1 2 3 4 5 6 7 8 9 %D %F Callista chione (Linnaeus, 1758) 1 0.01 11.1 Irus irus (Linnaeus, 1758) 1 0.01 11.1 Pitar rudis (Poli,1795) 3 3 0.07 22.2 Polititapes aureus (Gmelin, 1791) 5 1 21 14 19 0.70 55.6 Ruditapes decussatus (Linnaeus, 1758) 3 5 1 2 13 12 27 28 1.06 88.9 Venus casina Linnaeus, 1758 1 0.01 11.1 Venus verrucosa Linnaeus, 1758 25 16 32 0.85 33.3 Corbula gibba (Olivi, 1792) 4 4 0.09 22.2 Solen marginatus Pulteney, 1799 1 0.01 44.4 Ensis minor (Chenu, 1843) 1 2 0.03 22.2 Hiatella arctica (Linnaeus, 1767) 11 6 5 1 29 2 1 0.64 77.8

Fig. 3 — Number of species of each families Among the 105 species of mollusca, B. reticulatum transportation and wastewaters discharged in the bay18. was found to have the highest dominance value with The other dominant mollusca species were R. 2226 ind. (26%). The second most dominant species membranacea (713 ind., 8%), B. scabrum (674 ind., in the area is M. galloprovincialis (1022 ind., 11%). 8%), R. splendida (560 ind., 7%), B. latreillii (270 ind., This species lives by clinging to byssus strands and 3%), Phorcus turbinatus (243 ind., 3%), Nassarius hard substratums in mediolittoral and infralittoral reticulatus (206 ind., 2%), respectively (Fig 6). zones. They can also create intensive populations in The frequency index value (F) was calculated for the semi-dirty zones11. The species, known as pollution 105 Mollusca species identified at the stations based on indicator, was also intensively encountered the Aliaga the formula suggested by Soyer’s index and it was found marine ecosystem. that 53 species showed a rare distribution, 32 species The reason for this situation is that the area contains showed a continuous distribution and 20 species showed various industrial and shipyard activities, marine a common distribution. Gibbula adansonii, G. albida, 2302 INDIAN J. MAR. SCI., VOL. 47, NO. 11, NOVEMBER 2018

Fig. 4 — Number of species of the stations and seasons

Fig. 5 — Number of individuals of the stations and seasons B. reticulatum, B. scabrum, Alvania cimex, R. splendida and M. galloprovincialis as continuous species were the most common species with a rate of 100% in the mollusca (Fig 7). The biodiversity of the species and the distribution rates were determined by using diversity (H') and evenness index (J') values. According to the seasons and stations, for the diversity values of species, min value was obtained as st. 4 (1.71), max value was obtained as st. 3 (4.43). For the, evenness index values, min value was obtained as st. 4 (0.38), max value was obtained as st. 3 (0.82). Fig. 6 — Dominance values (%) of the mollusca species According to the Bray-Curtis similarity index, 3 important groups were seen among the stations; group A: st. 1, st. 5 and st. 6; group B: st. 2 and st. 3; group C: st. 7, st. 8 and st. 9. Some stations had the closest similarity to each other. These were st. 5 and st. 6 with 68% rate, st. 2 and st. 3 with 59% rate, st. 8 and st. 9 with 76% rate. These groupings is based on the fact that some biotopes show similarity. However, due to being in the mouth of the river, station 4 shows a distinct type of species composition (Fig 8). Fig. 7 — Frequency index values (%) of mollusca species CULHA et al.: SOFT BOTTOM MOLLUSC ASSEMBLAGES (GASTROPODA-BIVALVIA) 2303

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