Turkish Journal of Zoology Turk J Zool (2018) 42: 541-556 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1801-13

Seasonal variation and taxonomic composition of mesozooplankton in the southern (off Sinop) between 2005 and 2009

1 , 1 2 Funda ÜSTÜN *, Levent BAT , Erhan MUTLU  1 Department of Hydrobiology, Faculty of Fisheries, Sinop University, Sinop, Turkey 2 Faculty of Fisheries, Akdeniz University, Antalya, Turkey

Received: 09.01.2018 Accepted/Published Online: 13.08.2018 Final Version: 17.09.2018

Abstract: The monthly and long-term fluctuations of mesozooplankton abundance, biomass, and taxonomic composition in the Sinop inner harbor (southern Black Sea) between 2005 and 2009 are presented in the present study. In total, 31 mesozooplankton taxa were identified during the study. The recorded average mesozooplankton abundance and biomass were 34,323 ± 7580 ind.–2 m and 1208 ± 460 mg m–2 in 2005, 95,063 ± 31,434 ind m–2 and 1787 ± 604 mg m–2 in 2006, 97,626 ± 12,141 ind m–2 and 1034 ± 20 mg m–2 in 2007, 91,918 ± 10,476 ind m–2 and 775 ± 121 mg m–2 in 2008, and 146,918 ± 19,671 ind m–2 and 1955 ± 437 mg m–2 in 2009, respectively. The highest abundance values of mesozooplankton were encountered in March 2006 (299,110 ind m–2) with the contribution of Copepoda nauplii (167,000 ind m–2) particularly. Meanwhile, the mesozooplankton biomass was highest in October 2005 (5852 mg m–2), due to setosa (3695 mg m–2). The heterotrophic dinoflagellate Noctiluca scintillans was a major component of samples in the Sinop region, presenting its highest values in April 2005. Mesozooplankton abundance values showed significant differences (except 2007–2009 and 2008–2009) during the 5-year sampling period. Since the middle of 2006, an increase in abundance, biomass, and biodiversity of mesozooplankton has been detected. Many mesozooplanktonic species/groups showed seasonality in the study (especially Cladocera species). This seasonality was determined to be based on temperature changes.

Key words: Mesozooplankton, Black Sea, Turkey, abundance, biomass, coastal area, long-term

1. Introduction the abundance of nonindigenous species has increased The Black Sea is the world’s largest closed water system (Kovalev et al., 1999; Kideys et al., 2000; Oguz 2005a, that exhibits characteristics specific to itself. The Black 2005b). Zooplankton, a very important energy transfer link Sea, completely isolated except for the weak interchange in the sea, has been the first to respond to these changes provided by the Turkish straits system from the world’s (Shiganova et al., 1998). oceans, also contains the world’s largest oxygen-free water Zooplankton is the main link between primary mass with an anoxic water layer starting from ~200 m. One producers and high consumers. Zooplanktonic organisms of the most prominent and basic oceanographic features of play a key role in the pelagic nutrient network in terms the Black Sea is that the upper layer waters have a cyclonic of controlling phytoplankton production and shaping the flow system. The oceanography of the Black Sea basin is pelagic ecosystem. In addition, the dynamics, reproductive controlled by the river entrances, thermohaline factors, the and developmental cycles, and survival rates of zooplankton exchange in the Turkish straits system, and the bathymetric populations are the most important factors that affect fish structure (Oguz et al., 1993; Sur et al., 1996; Özsoy and stocks because they are important nutrients for fish larvae Ünlüata, 1997). (Lenz, 2000). Since many zooplankton species have a short The Black Sea fauna has been extensively influenced lifecycle and high growth potential, they react to changes in by many factors over the last 30 years and it has been the environmental conditions in terms of biodiversity and experiencing temporal and spatial changes such as abundance (Gajbhiye, 2002). In this respect, zooplankton excessive nutrients and pollutant influx, excessive fishing, should also be followed closely besides other biological the introduction of new species, and climate changes. As parameters to gain information about the ecosystem’s status. a result of these changes, some species have disappeared Current periodical qualitative and quantitative studies or their numbers have dropped dramatically; however, on a certain region in the southern Black Sea are very few * Correspondence: [email protected] 541

This work is licensed under a Creative Commons Attribution 4.0 International License. ÜSTÜN et al. / Turk J Zool

(Ünal, 2002; Özdemir and Ak, 2012; Deniz and Gönülol, biomass transformations were based on wet individual 2014; Üstün et al., 2016). This study has contributed weights according to Petipa (1957) and the taxa of to the understanding of the long-term changes, the Cladocera, Copepoda, Appendicularia, and seasonal variation, and the species composition of the were identified at species level. All other taxa were mesozooplankton fauna with formation of long-term identified to phylum, class, or order levels. zooplankton data in the southern Black Sea. The main references used for the identification of the major zooplanktonic groups were Zhong (1988), Bradford 2. Materials and methods Grieve et al. (1999), and Conway et al. (2003). Systematic classification and the nomenclature of zooplankton species 2.1. Study area were according to WoRMS Editorial Board (2017). The The Sinop Peninsula is located on the Boztepe Peninsula, abundance and biomass results were given in ind m–2 and extending to the northern shores of the southern Black mg m–2. Sea. Sinop’s inner harbor area, where the study was carried 2.3. Statistical analysis out, has characteristics of a natural harbor. This feature protects the area from the northern and eastern winds The relations among mesozooplankton abundance and (Sinop Valiliği Çevre ve Şehircilik İl Müdürlüğü, 2011). biomass, environmental parameters, and N. scintillans Sinop and its surroundings, located at the junction of abundance were investigated by Spearman correlation eastern and western currents (Oguz et al., 1993), are some analyses (SPSS 21, IBM Corp., Armonk, NY, USA). For of the most important transition regions and spawning assessing the community structure, a similarity matrix was grounds of migratory species, such as , horse prepared using the Bray–Curtis similarity coefficient over mackerel, and bluefish. Because of that, this region is an log-transformed zooplankton abundance and biomass data important fishing center. and mapped with MDS and cluster analysis. Differences in Other important features of the region are the low the mesozooplankton community among the years were population density and the underdeveloped industry, tested statistically by PERMANOVA. The Bray–Curtis which results in less pollution. dissimilarity matrix of the log10-transformed abundance data was applied to the nonparametric PERMANOVA. In 2.2. Sampling and laboratory studies order to interpret the mesozooplankton quantitative data, The study took place in the coastal zone off Sinop, the Shannon–Weaver diversity index (H’) and number of Turkey (southern Black Sea; Figure 1). Samples were species were applied to the species abundance data using ′ ″ obtained monthly from a sampling station (42°00 21 N, PRIMER 5 software. 35°09′32″E) situated 1.6 km offshore at a depth of 50 m from January 2005 to December 2009 (excluding October and December 2006 and June 2009). 3. Results The temperature and salinity values of the seawater During the sampling period, the sea water temperature were measured using an YSI 6600 brand CTD. (at 10 m depth) fluctuated from 7.2 °C (February) to Mesozooplankton sampling was carried out from 50 m 24.9 °C (August) in 2005 (mean: 15.56 ± 1.97 °C), 7.1 to 0 m (sea surface) via vertical tows aboard the Araştırma °C (March) to 22 °C (June) in 2006 (mean: 13.28 ± 1.97 I research vessel. All zooplankton samples were obtained °C), 7.8 °C (March) to 21.8 °C (August) in 2007 (mean: during daytime with a single vertical haul using a standard 13.36 ± 1.91 °C), 8.1 °C (January and February) to 24.9 plankton net (50 cm diameter mouth opening and a 210 °C (July) in 2008 (mean: 15.14 ± 1.7 °C), and 8.5 °C µm mesh size in 2005 and January and February 2006; (March) to 23.9 °C (July) in 2009 (mean: 15.43 ± 1.82 50 cm diameter mouth opening and 112 µm mesh size °C). The minimum and maximum sea water salinity values (at 10 m depth) were 17‰ (November) and in 2006, 2007, 2008, and 2009). Following the vertical 17.83‰ (July) in 2005 (mean: 17.5 ± 0.09‰), 17.3‰ tow, the contents of the cod ends were filtered using a 2 (July) and 18.7‰ (September) in 2008 (mean: 17.93 mm sieve to retain gelatinous organisms. Samples were ± 0.12‰), and 17.5‰ (July) and 18.02‰ (December) preserved in borax-buffered formalin solution (final in 2009 (mean: 17.7 ± 0.06‰), respectively (Figure 2). concentration 4%) until laboratory analysis. Subsamples There were no salinity data in 2006 or 2007. of 1 mL (two replicates) taken with a Stempel pipette were used for analysis. For species that did not appear during 3.1. Abundance and biomass of overall subsampling and for rare groups (such as Chaetognatha mesozooplankton and Decapod larvae), all samples were analyzed. The mesozooplankton abundance and biomass off Sinop Samples were analyzed under a stereomicroscope displayed remarkably different patterns between years. with a zooplankton counting apparatus and the results The total annual abundance of mesozooplankton was in were averaged and extrapolated to the whole sample. The the range of 12,890 (September) to 101,300 (October)

542 ÜSTÜN et al. / Turk J Zool ind m–2 in 2005, 14,005 (June) to 299,110 (March) ind 218.8 (June) to 1558.7 (August) mg m–2 in 2008, and m–2 in 2006, 57,850 (September) to 201,460 (July) ind 185.95 (May) to 4879.9 (September) mg m–2 in 2009 m–2 in 2007, 31,847 (June) to 154,520 (December) ind (Figure 3). m–2 in 2008, and 31,425 (May) to 266,840 (April) ind The annual abundance and biomass cycles of m–2 in 2009 (Figure 3). mesozooplankton (excluding the dinoflagellate The annual total biomass of mesozooplankton was Noctiluca scintillans) in the Sinop region for 2005–2009 in the range of 221.6 (September) to 5852 (October) mg showed a clear seasonal pattern and was characterized m–2 in 2005, 389.9 (February) to 5664.6 (August) mg by two peaks (autumn and summer) in 2005, three m–2 in 2006, 391.5 (May) to 3093 (July) mg m–2 in 2007, peaks (spring and summer) in 2006, three peaks

Figure 1. Study area and sampling station location.

Figure 2. The monthly change in seawater temperature (°C) and salinity (‰) at 10 m depth during 2005–2009 in the Sinop coastal area.

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Figure 3. Annual pattern of mesozooplankton abundance (ind m–2) and biomass (mg m–2) (excluding Noctiluca scintillans) off Sinop for 2005–2009.

(summer, autumn, and spring) in 2007, and four peaks for 2005, 9,835–293,325 ind m–2 (February–March) in (autumn, spring, and winter) in 2009. In 2008, abundance 2006, 37,215–140,700 ind m–2 (September–July) in 2007, was characterized by three peaks (winter, autumn, and 17,627–131,972 ind m–2 (June–December) in 2008, spring) and biomass was characterized by one peak and 19,195–229,050 ind m–2 (May–April) in 2009. The (summer) (Figure 3). minimum and maximum biomass values of In terms of both abundance and biomass, the highest were in range of 145.08–2024.61 mg m–2 (July–October) values were recorded in October (101,300 ind m–2 and in 2005, 217.4–2920 mg m–2 (June–May) in 2006, 241.34– 5852 mg m–2) and August 2005 (696,700 ind m–2 and 2374.23 mg m–2 (October–July) in 2007, 77.20–829.57 2595.6 mg m–2); March (299,110 ind m–2 and 2139.3 mg mg m–2 (June–October) in 2008, and 75.58–3368.26 mg m –2), August (100,220 ind m–2 and 4849.4 mg m–2), and m–2 (May–April) in 2009 (Figure 5). Nine Copepoda May 2006 (252,215 ind m–2 and 5664.6 mg m–2); and July species were identified in this study (Acartia (Acartiura) (201,460 ind m–2 and 3093.3 mg m–2) and November clausi, Acartia (Acanthacartia) tonsa, Calanus euxinus, –2 –2 2007 (139,060 ind m and 1149.6 mg m ). In terms of Centropages ponticus, Paracalanus parvus, Pontella abundance the highest values were in December (154,520 mediterranea, Pseudocalanus elongatus, Oithona davisae, –2 –2 ind m ) and October 2008 (139,305 ind m ) and April and Oithona similis). We only observed A. tonsa in one –2 –2 (266,840 ind m ) and November 2009 (210,325 ind m ). subsample in August 2006 and September 2006. A. In terms of biomass, the highest values were in August clausi was present throughout all years, reaching higher –2 –2 (1558.7 mg m ) and October 2008 (1263.1 mg m ) and abundances and biomass values in summer and autumn, –2 September (4879.9 mg m ) and April 2009 (3804.1 mg while C. euxinus, P. elongatus, O. similis, and P. p ar v u s –2 m ) (Figure 3). were more pronounced in colder months. C. ponticus The mean abundance and biomass values of all was the most important contributor to the Copepoda mesozooplankton groups and their identified species are community in late summer and early autumn. In terms presented in Tables 1 and 2. of abundance, A. calusi (59,220 ind m–2 and 972 mg m–2 3.2. Abundance and biomass of each mesozooplankton in October 2005), P. elongatus (72,500 ind m–2 and 1321 group and species mg m–2 in March 2006), P. p ar v u s (67,000 ind m–2 and 341 Copepods dominated the mesozooplankton composition mg m–2 in November 2007; 95,250 ind m–2 and 538 mg over all 5 years. The highest percentages of m–2 in December 2008; 58,275 ind m–2 and 372 mg m–2 in abundance were observed in May 2005 (96.4%), March December 2009) were determined as the most abundant 2006 (98.07%), January 2007 (90.82%), December copepod species. In terms of biomass P. elongatus (13,440 2008 (85.44%), and January 2009 (87.23%); the highest ind m–2 and 435 mg m–2 in March 2005), C. euxinus (3350 copepod biomasses were observed in May 2005 (99.46%), ind m–2 and 2026 mg m–2 in May 2006; 13,150 ind m–2 and April 2006 (97.7%), January 2007 (90.06%), December 1349 mg m–2 in July 2007; 7000 ind m–2 and 1880 mg m–2 in 2008 (77.08%), and April 2009 (88.54%) (Figure 4). The April 2009), and A. clausi (56,000 ind m–2 and 643 mg m–2 minimum and maximum abundance values of copepods in October 2008) were found to make high contributions –2 was in the range of 6,780–91,710 ind m (July–October) (Figure 5).

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Table 1. The annual mean abundances of mesozooplankton groups during this study (standard error values given after ±).

Species Abundance (ind m–2)

2005 2006 2007 2008 2009

APPENDICULARIA (Vexillaria) dioica Fol, 1872 1606.7 ± 558.5 5062.5 ± 2354 7052.1 ± 2000 5245.8 ± 1246.8 12,659.1 ± 1764.5 CLADOERA Evadne spinifera P.E.Müller, 1867 7.9 ± 5.3 50 ± 33.3 1604.2 ± 1293.5 466.7 ± 457.7 Penilia avirostris Dana, 1849 6500.8 ± 4687 9687.5 ± 8140.7 968.8 ± 479.5 5358.3 ± 3343.1 6772.7 ± 3998.5 Pleopis polyphemoides (Leuckart, 1859) 159.2 ± 149.4 450 ± 271.4 44.2 ± 41.5 3622.1 ± 1368 474.6 ± 270.4 Pseudevadne tergestina (Claus, 1877) 52.9 ± 49.8 1932.5 ± 1924.2 62.5 ± 62.5 13.5 ± 12.4 420.5 ± 315.5 Cladocera Total 6721 ± 4892 12,120 ± 10,369 2679 ± 1876 9460 ± 5181 7667 ± 4584 CHAETOGNATHA Parasagitta setosa (Müller, 1847) 435 ± 290.1 540.5 ± 288.5 115.8 ± 29.1 294.4 ± 70.7 3599.1 ± 2759.2 COPEPODA Acartia sp. Dana, 1846 11,437.5 ± 5134.9 0 Acartia (Acartiura) clausi Giesbrecht, 1889 11,100 ± 4509 9212.5 ± 5003.8 16,381.3 ± 4484.9 14,356.3 ± 4326.5 15,488.6 ± 3473.4 Acartia (Acanthacartia) tonsa Dana, 1849 775 ± 747.6 Calanus euxinus Hulsemann, 1991 465.8 ± 216.2 1038.5 ± 371.9 1827.1 ± 1039.8 409.6 ± 139.6 1000 ± 613.3 Centropages ponticus Karavaev, 1895 93.8 ± 57.6 190 ± 138 2145.8 ± 1798 55.6 ± 29.7 570.5 ± 369.3 Oithona davisae Ferrari F.D. & Orsi, 1984 8636.4 ± 6531 Oithona similis Claus, 1866 637.5 ± 162.1 2337.5 ± 572.5 7875 ± 2205.7 2203 ± 477.6 5813.6 ± 1490.6 Paracalanus parvus (Claus, 1863) 4612.9 ± 1660.6 4200 ± 1193 19,639.6 ± 5488.6 17,010.4 ± 8098.5 36,938.6 ± 6331.3 Pontella mediterranea (Claus, 1863) 0.21 ± 0.2 Pseudocalanus elongatus (Boeck, 1865) 6226.7 ± 1415 17,520 ± 7424 10,056.3 ± 2556 4761.5 ± 622.2 12,279.6 ± 6002.6 Unidentified Copepoda 3.8 ± 2.1 27.5 ± 24.9 86.7 ± 46.5 129.8 ± 73.8 42.3 ± 16.3 Copepoda egg 2750 ± 1715 11,468.8 ± 1357.4 3341.7 ± 1109 2988.6 ± 1192 Copepoda nauplii 641.7 ± 289.5 23,137.5 ± 16,156 1125 ± 460.8 14,814.6 ± 2095.3 22,818.2 ± 6514.5 Copepoda Total 23,782 ± 8312 72,626 ± 38,482 70,605 ± 19,437 57,083 ± 16,972 106,576 ± 32,534 FORAMINIFERA 1.7 ± 1.7 3.1 ± 3.1 5.5 ± 3.1 TINTINNIDA 41.7 ± 32 291.7 ± 189.8 102.3 ± 80.5 MEROPLANKTON Actinotroch larvae 21.3 ± 20.8 1.3 ± 0.7 Ascidiacea larvae 1.7 ± 1.7 65 ± 62.3 9 ± 5 0.5 ± 0.5 Bivalvia larvae 1545.8 ± 678.2 1800 ± 655.3 13208.3 ± 3905.4 17,425 ± 3808.8 14,545.5 ± 2307.7 Bryozoa larvae 0.83 ± 0.8 25 ± 22.6 Cirripedia larvae 91.3 ± 58.2 74.5 ± 48.8 298.3 ± 207.3 508 ± 136 126 ± 44.2 Decapoda larvae 50 ± 29.1 85.5 ± 54.6 14.6 ± 6.4 32.9 ± 13 44.6 ± 28.2 Gastropoda larvae 53.3 ± 24.2 275 ± 120.5 3197.9 ± 1875 1144.6 ± 405.3 743.2 ± 220.5 Medusae planula larvae 0.4 ± 0.4 2375 ± 2223.8 18.8 ± 11.2 191.7 ± 134.1 22.7 ± 22.7 Microniscus sp. 4.6 ± 2.9 7 ± 5.2 44.2 ± 41.5 14 ± 8.3 3.2 ± 1.6 Polychaeta larvae 7.9 ± 2.4 92 ± 40.9 251.7 ± 123.4 205.4 ± 63.1 764.1 ± 423 Fish egg 4.6 ± 2.5 1 ± 0.7 8.8 ± 6.10 5.4 ± 5.4 24.1 ± 13.7 Fish larva 16.3 ± 5.8 4 ± 2.2 2.9 ± 2.1 2.3 ± 2.3 9.6 ± 4.8 Meroplankton Total 1776 ± 806 4714 ± 3151 17,132 ± 6261 19,539 ± 4581 16,308 ± 3089 Total mesozooplankton average m–2 34,323 ± 7580 95,063 ± 31,434 97,626 ± 12,141 91,918 ± 10,476 146,918 ± 19,671 Total mesozooplankton average m–3 703.28 ± 154.27 1937.59 ± 640.69 1989.83 ± 247.70 1873.28 ± 213.58 2994.52 ± 400.93 DINOFLAGELLATA Noctiluca scintillans (Macartney) 40,365 ± 13,598.4 28,162.5 ± 14,234.6 2364.6 ± 596.7 5108.8 ± 1739.5 7625 ± 3062.7 Kofoid & Swezy, 1921

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Table 2. Annual mean biomasses of mesozooplankton groups during this study (standard error values given after ±).

Species Biomass (mg m–2) 2005 2006 2007 2008 2009 APPENDICULARIA Oikopleura (Vexillaria) dioica Fol, 1872 39 ± 15.6 114.1 ± 60 101.7 ± 32 51.1 ± 13 198.7 ± 25 CLADOERA Evadne spinifera P.E.Müller, 1867 0.03 ± 0.02 0.2 ± 0.1 0.3 ± 0.3 1.9 ± 1.8 Penilia avirostris Dana, 1849 200 ± 143 271.3 ± 228 44.9 ± 36.2 150 ± 93.6 189.6 ± 112 Pleopis polyphemoides (Leuckart, 1859) 1.4 ± 1.3 4.1 ± 2.4 8.7 ± 4.3 32.6 ± 12.3 4.3 ± 2.4 Pseudevadne tergestina (Claus, 1877) 0.2 ± 0.2 7.7 ± 7.7 0.2 ± 0.2 0.05 ± 0.05 1.7 ± 1.3 Cladocera Total 202 ± 144 283 ± 238 54 ± 41 185 ± 108 196 ± 116 CHAETOGNATHA Parasagitta setosa (Müller, 1847) 377.3 ± 303.9 317.3 ± 137.1 31.2 ± 6.6 42.9 ± 10.1 534.8 ± 277.7 COPEPODA Acartia sp. Dana, 1846 71.7 ± 36.4 Acartia (Acartiura) clausi Giesbrecht, 1889 215.1 ± 90.8 242.5 ± 131.4 199 ± 56.5 161.7 ± 49.6 174.7 ± 38.5 Acartia (Acanthacartia) tonsa Dana, 1849 18.9 ± 18.1 Calanus euxinus Hulsemann, 1991 116.3 ± 57.8 326.7 ± 192.9 213.6 ± 108.3 37.6 ± 9 251 ± 169.4 Centropages ponticus Karavaev, 1895 2 ± 1.5 6.2 ± 4 18.5 ± 12.4 1.92 ± 1.04 16.2 ± 11.8 Oithona davisae Ferrari F.D. & Orsi, 1984 17.3 ± 12.7 Oithona similis Claus, 1866 2.8 ± 0.7 7.6 ± 2.4 22.4 ± 6 7 ± 1.5 18.5 ± 4.9 Paracalanus parvus (Claus, 1863) 45 ± 16.5 28 ± 7.7 106.6 ± 29.8 92.84 ± 47 190 ± 37.3 Pontella mediterranea (Claus, 1863) Pseudocalanus elongatus (Boeck, 1865) 192.7 ± 48.2 309.6 ± 126.5 159.4 ± 45.7 57 ± 11.7 214.3 ± 102.5 Unidentified Copepoda 0.06 ± 0.03 0.9 ± 0.8 2.7 ± 1.4 2.2 ± 0.9 1.3 ± 0.5 Copepoda nauplii 0.7 ± 0.3 23.1 ± 16.2 11.5 ± 1.4 18.1 ± 2.7 22.8 ± 6.5 Copepoda egg 2.5 ± 1.5 1.01 ± 0.41 3.1 ± 1.01 2.7 ± 1.07 Copepoda Total 575 ± 216 1038 ± 538 735 ± 262 381 ± 124 909 ± 385 FORAMINIFERA 0.01 ± 0.1 0.01 ± 0.01 TINTINNIDA 0.04 ± 0.03 0.3 ± 0.2 0.1 ± 0.08 MEROPLANKTON Actinotroch larvae Ascidiacea larvae 0.02 ± 0.02 0.91 ± 0.87 0.21 ± 0.08 0.006 ± 0.01 Bivalvia larvae 7.7 ± 3.4 9 ± 3.3 66 ± 19.5 87.1 ± 19.04 72.7 ± 11.5 Bryozoa larvae 0.03 ± 0.03 Cirripedia larvae 3.3 ± 2.4 1.6 ± 1.06 4.8 ± 3.2 8.7 ± 2.3 3.7 ± 1.8 Decapoda larvae 3.1 ± 1.8 5.3 ± 3.4 0.90 ± 0.4 2.04 ± 0.8 2.8 ± 1.8 Gastropoda larvae 0.6 ± 0.3 3 ± 1.31 34.9 ± 20.4 12.5 ± 4.4 8.1 ± 2.4 Medusae planula larvae 14.7 ± 13.3 0.11 ± 0.07 1.2 ± 0.8 0.14 ± 0.14 Microniscus sp. 0.23 ± 0.14 0.35 ± 0.26 2.21 ± 2.07 0.7 ± 0.41 0.16 ± 0.08 Polychaeta larvae 0.23 ± 0.1 1.3 ± 0.6 2.5 ± 1.2 2.05 ± 0.6 29 ± 16.1 Fish egg Fish larva Meroplankton Total 15 ± 8 35 ± 23 112 ± 48 114 ± 28 117 ± 34 Total mesozooplankton average m–2 1208 ± 460 1787 ± 604 1034 ± 204 774 ± 121 1955 ± 437 Total mesozooplankton average m–3 24.62 ± 9.39 36.43 ± 12.3 21.08 ± 4.16 15.99 ± 2.46 39.84 ± 8.92 DINOFLAGELLATA Noctiluca scintillans (Macartney) 4217.8 ± 1386 2478.3 ± 1252.6 208.1 ± 52.5 449.6 ± 153.1 671 ± 269.5 Kofoid & Swezy, 1921

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Figure 4. Percentage composition of the main mesozooplankton groups in terms of abundance and biomass off Sinop for 2005–2009.

In terms of both abundance and biomass, the maximum and early autumn with values of up to 82,250 ind m–2 and values of cladocerans were recorded in August 2005, 2006, 2303 mg m–2 in August 2006. E. spinifera was not observed 2007, and 2008 and July 2009 (52,685 ind m–2 and 1585 mg in subsamples of zooplankton in 2009 (Figure 6). m–2; 103,250 ind m–2 and 2394 mg m–2; 17,000 ind m–2 and During both spring and winter periods, meroplanktonic 441 mg m–2; 40,600 ind m–2 and 1127 mg m–2; 39,250 ind forms also contributed notably to the mesozooplankton m–2 and 1003 m m–2, respectively). The highest values were abundance and biomass (Figure 7). The maximum reached in August 2006 (103,250 ind m–2 and 2394 mg m–2), abundance and biomass values of meroplankton were seen while the minimum values of cladocerans were recorded in February 2005 and 2006 (8450 ind m–2 and 42.8 mg m–2; in March 2005 (10 ind m–2 and 0.2 mg m–2), November 22,775 ind m–2 and 137.2 mg m–2), April and July 2007 2006 (500 ind m–2 and 11.6 mg m–2), April 2007 (125 ind (50,050 ind m–2 and 253 mg m–2; 35,310 ind m–2 and 338 m–2 and 1.1 mg m–2), December 2008 (12.5 ind m–2 and 0.1 mg m–2), January 2008 (44,882 ind m–2 and 226 mg m–2), mg m–2), and February 2009 (75 ind m–2 and 0.7 mg m–2) and September 2009 (30,545 ind m–2 and 341 mg m–2) (Figure 6). Four cladoceran species were identified in the (Figure 7). Bivalve larvae dominated the meroplankton; present study (Penilia avirostris, Evadne spinifera, Pleopis the highest peaks in both the abundance and biomass polyphemoides, and Pseudevadne tergestina). Among the values of bivalve larvae occurred in April 2007 (49,625 ind cladocerans, P. av iro str i s was dominant during summer m–2 and 248 mg m–2, respectively), followed by January

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Figure 5. Annual cycle in abundance (ind m–2) and biomass (mg m–2) for Copepoda and Copepoda species off Sinop for 2005–2009.

2008 (44,700 ind m–2 and 224 mg m–2), February 2009 remarkable existence being recorded in October 2005 (3585 (26,000 ind m–2 and 130 mg m–2), February 2005 (8400 ind m–2 and 3695 mg m–2) and September 2009 (30,875 ind m–2 and 42 mg m–2), and July 2006 (5750 ind m–2 and ind m–2 and 2593 mg m–2). Chaetognatha constituted a 29 mg m–2). The next most abundant of the meroplankton significant part of the plankton community biomass in groups were identified as larvae belonging to cirripeds, October 2005, with a share of 63.15% (Figure 8). polychaetes, and gastropods (Figure 7). The heterotrophic dinoflagellate Noctiluca scintillans The highest peaks in appendicularian abundance and was a major component of plankton samples in the region –2 biomass were observed in November 2005 (6300 ind m off Sinop, attaining the highest values in April 2005 –2 –2 and 167 mg m ), May 2006 (22,000 ind m and 586 mg (131,160 ind m–2 and 14,306 mg m–2); this species was not –2 –2 m ), July and November 2007 (22,000 ind m and 310 present in samples from June 2007 (Figure 8). –2 –2 –2 mg m ; 17,750 ind m and 339 mg m ), November 2008 Most mesozooplankton groups exhibited evident (11,588 ind m–2 and 155 mg m–2), and July and November –2 –2 –2 seasonality in the Sinop region. This was particularly 2009 (23,250 ind m and 317 mg m ; 18,500 ind m and apparent for cladocerans and chaetognaths, which occurred 324 mg m–2) with the lowest occurring in March 2005 (20 in summer–autumn, and for meroplankton, which were ind m–2 and 0.3 mg m–2), January and June 2006 (125 ind more important during winter. m–2 and 1.8 mg m–2; 375 ind m–2 and 8.7 mg m–2), August 2007 (750 ind m–2 and 5.1 mg m–2), June 2008 (603 ind m–2 3.3. The relationship of environmental variables with and 6.2 mg m–2), and May 2009 (3875 ind m–2 and 56 mg mesozooplankton community structure and N. scintillans m–2) (Figure 8). The lowest number of species was recorded in January 2005 The contribution of Chaetognatha was virtually and April 2005 (9 species/groups) and the highest values negligible throughout the 5-year study period, the only in September 2006, October 2007, September 2008, and

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Figure 6. Annual cycle in abundance (ind m–2) and biomass (mg m–2) for Cladocera and Cladocera species off Sinop for 2005–2009.

August 2009 (23 species/groups). The maximum Shannon Copepoda nauplii (2005–2007, 32%; 2005–2009, 34.68%), diversity index was found in September 2008 (3.31). The Copepoda eggs (2005–2008, 34.81%), and Cirripedia minimum Shannon diversity index was determined in larvae (2007–2008, 23%) (SIMPER). September 2005 (1.19). This decrease in diversity was due The relation among temperature, salinity, and N. to numerical dominance of A. clausi (Figure 9). scintillans is shown in Table 4 for species/groups. During In terms of abundance values, there was no significant the 5-year study period, a positive correlation was found difference detected in terms of months and years (R = 0.36, between N. scintillans and copepod eggs in 2007, and P = 0.001, ANOSIM). It was determined that there was a a negative correlation was found between N. scintillans similarity of more than 60% in terms of abundance values. and copepod nauplii in 2008. A positive correlation was In terms of abundance values, the community of 2005 was found between salinity and C. ponticus in 2005, and a dominated by A. clausi, P. parvus, P. elongatus, and Bivalvia negative correlation was determined between salinity and larvae; the community of 2006 was dominated by A. clausi Copepoda, Copepoda nauplii, and Bivalvia larvae in 2005 and P. parvus; the community of 2007 was dominated by and P. ployphemoides in 2009. Cladocera and its species (C. Copepoda nauplii, A. clausi, P. parvus, and Bivalvia larvae; ponticus, O. similis, P. setosa) and Gastropoda larvae had the community of 2008 was dominated by Copepoda a positive correlation with temperature, whereas Bivalvia nauplii, Bivalvia larvae, A. clausi, and P. elongatus; and larvae, copepod nauplii and eggs, C. euxinus, P. elongatus, the community of 2009 was dominated by P. parvus, and P. parvus had a negative correlation with temperature Copepoda nauplii, Bivalvia larvae, O. dioica, and A. clausi (Table 4). (SIMPER) (Figure 10). PERMANOVA showed that mesozooplankton abundance values had significant differences (except 4. Discussion 2007–2009 and 2008–2009) among the 5 years studied (P As it forms an epipelagic zone surface layer and is in < 0.05; Table 3). The lowest abundance was determined in constant contact with the atmosphere, the water displays 2005 (34,323 ind m–2) and the highest value was in 2009 variable characteristics. In the Black Sea, significant (146,918 ind m–2) (Table 1). The species that caused these seasonal changes are observed in the physicochemical dissimilarities were Acartia sp. (2005–2006, 35.32%; 2006– properties of water mass over 50–70 m, which creates the 2007, 31.26%; 2008–2006, 30.93%; 2006–2009, 33.23%), upper part of epipelagic and the mesopelagic regions. In

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Table 3. PERMANOVA on log-transformed [log10(X+1)] and biomass were 64% and 54% in Sinop in 1999, 46% abundance values and Bray–Curtis dissimilarities. in Trabzon in 2007–2008 (no data biomass), 75% and 74% in Samsun in 2012–2013, 66% and 50.65% in Years P(perm) Sinop in 2002, 70% and 65.8% in Sinop in 2003, and 75.6% and 52.6% in Sinop in 2004, respectively (Ünal, 2005, 2006 0.0432 2002; Özdemir and Ak, 2012; Deniz, 2013; Üstün et al., 2005, 2007 0.0078 2016). It has been determined that its contribution to 2005, 2008 0.0079 total mesozooplankton abundance ranges from 62% to 2005, 2009 0.0119 76% and the contribution of biomass varies between 2006, 2007 0.0451 47% and 71% in this study. A. clausi and P. elongatus were dominant in the Sinop region in both abundance 2006, 2008 0.0305 and biomass, while A. clausi and P. p ar v u s were most 2006, 2009 0.0408 abundant in the Samsun region (Ünal, 2002; Deniz, 2007, 2008 0.0438 2013; Üstün et al., 2016). In the present study, copepod 2007, 2009 0.133 P. p ar v u s ranks first in terms of abundance, and C. 2008, 2009 0.0666 euxinus is at the forefront in terms of biomass. In 2005 and 2006, A. clausi and P. elongatus were dominant in the environment, but after 2007, it was observed that P. parvus became the most dominant species by increasing particular, the changes in coastal zones and ecological its dominance in the environment (28% in 2007, 30% characteristics differ (Sivri, 1999). in 2008, and 35% in 2009). It has been determined In the Black Sea, the monthly temperature change that P. p ar v u s reaches the highest values in terms of in the surface waters is quite variable depending on abundance and biomass on the south Black Sea coast the season. In spring and early summer, the water in autumn and on the northeastern Black Sea coast in temperature rises parallel to the heating of the air, winter (Ünal, 2002; Deniz and Gönülol, 2014; Yıldız which gets warm first. On the other hand, in autumn and Feyzioğlu, 2014; Lebedeva et al., 2015; Üstün et and winter, the seawater temperature is higher than the al., 2016). In the present study, the highest values were air temperature, and the water cools down more slowly. observed in the autumn season. Additionally, it has In the Black Sea, it is known that the temperature drops been determined that it peaked in the winter season in starting from September and it reaches the lowest 2005, 2008, and 2009. C. euxinus is the largest copepod values in January and February. Following a significant species in the Black Sea (Ergün, 1994; Beşiktepe, 1998) increase towards spring, the highest surface water and therefore the contribution of mesozooplankton to temperatures are reported in July and August (Ivanov biomass is high. Maximum abundance and biomass and Beverton, 1985). In a study carried out by Oguz et values in coastal waters were observed in winter and al. (2008) in the internal regions of the Black Sea basin, spring (Ünal, 2002; Üstün et al., 2016). In the present they reported that the surface water temperature varied study, C. euxinus abundance and biomass peaks were between 6 and 7 °C in the cold periods of the year and determined in spring, summer, and autumn, and second between 22 and 26 °C in the hot periods. When the high values were observed in autumn and winter. The change in the temperature measurements made during cyclopoid copepod O. davisae originating from the the study period was analyzed according to months, western Pacific Ocean (Razouls et al., 2017), which has they found that the surface seawater temperature varied just entered the Black Sea, was first seen in September between 7.1 °C (March 2006) and 24.9 °C (August 2005 2009 in the current work, and it was the dominant and July 2008). type of the environment in November. While there is a Zooplankton within different communities in the very low abundance of O. davisae, a eurythermal (Uye ecosystem are the main grazers in aquatic environments. and Sano, 1995; Mihneva and Stefanova, 2013) and This role enables them to transmit the energy from euryhaline species (Svetlichny and Hubareva, 2014), the first producers (phytoplankton) to consumers at in winter and spring in the Black Sea, it reaches high higher nutrient levels such as fish and marine mammals abundance values in autumn and summer (Gubanova (Richardson, 2008). and Altukhov, 2007; Selifonova, 2009; Altukhov et al., In the present study, Copepoda was found to be the 2014). most dominant group, similar to other studies in the The temporal distribution of Cladocera, which is same and different coastal regions of the Black Sea. Its the second most dominant group of mesozooplankton contribution to the total mesozooplankton abundance in the coastal marine environment after copepods,

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Figure 7. Annual cycle in abundance (ind m–2) and biomass (mg m–2) for meroplankton and meroplankton groups off Sinop for 2005–2009.

Figure 8. The annual cycle in abundance (ind –2m ) and biomass (mg m–2) for Appendicularia, Chaetognatha, and Noctiluca scintillans off Sinop for 2005–2009.

551 ÜSTÜN et al. / Turk J Zool N. scintillans ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns * Salinity ns ns ns ns ns ns ns ns ns ns ns –0.659 ns ns ns ns ns ns * ** * ** ** ** ** * ** Temperature ns ns 0.799 ns –0.846 –0.627 ns ns –0.873 ns .801 ns 0.720 0.853 0.832 ns ns –0.691 2009 * N. scintillans ns ns ns ns –0.650 ns ns ns ns ns ns ns ns ns ns ns ns ns Salinity ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns * ** Temperature ns ns ns 2008 ns ns –0.599 ns ns 0.717 ns ns ns ns ns ns ns ns ns * N. scintillans ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns 0.703 * ** ** * ** Temperature ns ns 0.746** 2007 ns –0.626 0.792 ns ns –0.854 ns 0.752 ns ns ns ns 0.604* 0.683 ns ns ns ns N. scintillans ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns Temperature 2006 ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns N. scintillans ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns ** * ** * –0.718 ns ns ns Salinity ns ns ns ns ns ns ns ns ns –0.803 0.579 ns –0.648 ns * ns ns 0.810* Temperature 2005 ns ns ns 0.761** ns 0.686* 0.640* 0.650* ns ns 0.705* ns ns ns –0.702 Abundance Biomass Cladocera C. euxinus P. p ar v u s elongatus P. abundance; mesozooplankton Abundance: Nonsignificant; ns: (2-tailed). atthe 0.05 level is significant (2-tailed).at 0.01 level * the Correlation significant is ** Correlation biomass. mesozooplankton Biomass: Gastropoda larvaeGastropoda P. setosa P. P. av iro str i s tergestina P. E. spinifera polyphemoides P. Copepoda C. ponticus similisO. Copepoda nauplii Copepoda egg larvaeBivalvia , and mesozooplankton abundance, biomass, and species/groups of mesozooplankton. of species/groups and biomass, abundance, mesozooplankton , and N. scintillans salinity, between temperature, measured results correlation 4. Spearman Table

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Figure 9. Temporal fluctuation of Shannon diversity index (H′) and the number of species.

Figure 10. Defined groups by the cluster and MDS analysis based on mesozooplankton abundance values. is interrupted, and it is known that high abundance and autumn P. av irostr i s is dominant, whereas around values are reached from the beginning of spring to the September P. polyphemoides increases its dominance and end of summer. It is followed by a rapid decline and maintains it during the winter-spring period (Ünal, 2002; disappearance from the plankton during the winter Lebedeva et al., 2015; Üstün et al., 2016). The findings that (Isinibilir, 2009; Özdemir and Ak, 2012; Kurt Terbıyık and we have obtained are consistent with the literature. Polat, 2014). In this study, Cladocera formed the second It has been found that a new generation joins the P. most important group of mesozooplankton after copepods. setosa population, the most important species of food While its contribution to the total mesozooplankton in zooplankton in terms of biomass, in the Black Sea in terms of abundance ranges from 3% to 20%, it has been September. The reproductive period is more intense determined that its contribution to biomass is 5%–24%. from June to November, and the abundance values are Within this group, two types are in the foreground: especially high in the summer months (Niermann et al., P. av iro str i s and P. polyphemoides. Until midsummer 1998; Besiktepe and Unsal, 2000; Ünal, 2002). In this study

553 ÜSTÜN et al. / Turk J Zool carried out in the Sinop inner harbor area in 2005–2009, abundance, whereas its contribution to biomass is 1%– its contribution to the total mesozooplankton abundance 28%. In the study, Bivalvia larvae (38%–89% in terms of was calculated as 0.1%–2.4%, and its contribution to the abundance, 25%–76% in terms of biomass) constituted biomass was calculated as 3%–31%. In this study, which the most dominant group, followed by Gastropoda larvae, was carried out in the coastal area, the findings obtained Cirripedia larvae, and Polychaeta larvae. While Bivalvia regarding the seasonality of the P. setosa species are larvae cause the increase in the abundance and the biomass consistent with previously conducted studies. values of the meroplankton in winter, spring, and autumn, In the Black Sea Oikopleura dioica is abundant in winter gastropod larvae cause the increase in summer. and early spring in the plankton, and even at the beginning It has been determined that the first increase of of spring and the beginning of summer, it is abundant Noctiluca scintillans, a heterotrophic dinoflagellate species, during phytoplankton bloom. At the beginning of summer occurs in March–June in the northwest Black Sea and and beginning of autumn, it has been found that it reaches the second increase occurs in November–December. the highest levels of abundance along with warm-water The lowest values are seen between July and September species (Shiganova, 2005). It has been determined that (Porumb, 1992). In the northeastern Black Sea, the its contribution to the total mesozooplankton abundance highest abundance values have been observed in the first ranges from 5% to 9%, whereas its contribution to the half of May and June (Mikaelyan et al., 2014). However, content of biomass varies between 3% and 10%. The in the present study, no regularity was observed in the findings we obtained regardingO. dioica, which has been seasonality of N. scintillans. Peak values were determined reported to be the highest in abundance at the beginning at different periods each year (Figure 8). In this study, of spring and autumn, are compatible with the findings of in the 2005–2008 period, the peak values were observed Ünal (2002), Üstün et al. (2016), and Shiganova (2005). In in spring and summer, while maximum values were addition to these studies, it was also determined that this observed in winter in 2009. Nonphotosynthetic species species reached peak values during the summer period. (not containing chloroplasts) feed on a wide spectrum of Meroplankton, or temporary plankton, largely consist nutrients, from phytoplankton to zooplankton larvae and of larval stages of benthic, littoral, and nektonic organisms. eggs, organic detritus, and bacteria (Quevedo et al., 1999; Meroplanktonic larvae disperse in the plankton for a Nikishina et al., 2011). In previously conducted studies, period ranging from 1 week to 1 month. During this time, it was pointed out that during the peak season of N. the meroplankton forms an important part of the pelagic scintillans, there was an extreme decrease in zooplankton community. The timing of the release of the larvae to the abundance (Elbrächter and Qi, 1998; Ünal, 2002; Yılmaz water column differs from species to species and various et al., 2005; Isinibilir, 2009; Özdemir and Ak, 2012). factors such as temperature, nutrient availability, and The same situation was observed in the present study. It meteorological factors can stimulate egg production and was observed that the abundance and biomass values of larval release (Belgrano et al., 1995; Byrne, 1995). This may mesozooplankton organisms decreased in April and May lead to a difference between regions in the distribution and 2005, the most abundant period for N. scintillans species. seasonality of the meroplanktonic larvae. Meroplankton In conclusion, the present study provides information on is an important component of mesozooplankton in the qualitative and quantitative state of mesozooplankton the coastal waters of the Black Sea. In the northeastern in the Sinop sea region, which has a specific current coastal areas of the Black Sea, meroplankton larvae have system. It has been found that the seasonality of been identified in the plankton from May to September. mesozooplankton in the region is similar to that of other In spring and autumn, Bivalvia larvae dominated, while studies. Mesozooplankton abundance and biomass values in summer, gastropod and Bivalvia larvae dominated the started to increase with the increase of Copepoda nauplii environment (Selifonova, 2006, 2012, Lebedeva et al., and Bivalvia larvae from the middle of 2006, and the 2015). In the present study, it was determined that the first values reached the maximum level due to the addition of peak in terms of both abundance and biomass was seen in copepod O. davisae to the environment in September 2009. winter, and the second peak was seen in spring or autumn. No relation was determined between the total abundance The present finding is consistent with studies conducted and biomass values of mesozooplankton and temperature, in 1999 (Ünal, 2002) and 2002–2004 (Üstün et al., 2016) salinity, and N. scintillans (the predator of zooplanktonic in the same region. In addition, it was determined that the organisms such as copepod nauplii and Bivalvia larvae). meroplankton abundance and biomass values increased Like our sample area, coastal ecosystems are dynamic in July in this study. Üstün et al. (2016) recorded the environments influenced by many physical factors, such as maximum values in August 2004. It has been determined wind, waves, and currents. In order to better interpret the that the contribution of meroplankton to the total results of future studies, it would be useful to investigate mesozooplankton varies from 5% to 21% in terms of biological factors, such as chlorophyll a or phytoplankton,

554 ÜSTÜN et al. / Turk J Zool as well as physical factors. In addition, the continuity of Acknowledgments these studies is crucial in determining how the species that This work was carried out at the Sinop University Fisheries newly entered the area, such as O. davisae, will affect the Faculty, Department of Hydrobiology, during 2005–2009. current situation and future predictions. We thank the staff of the RV Arastırma-1, Dr Fatih Şahin and Dr Zekiye Birinci Özdemir for their assistance on the cruises, and the referees for their valuable contributions.

References

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