seasonal distribution of zooplankton in the gulf of erdek

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Jun 5, 2014 - collected from 3 sampling stations using WP-2 zooplank- ton net (200µm mesh size). During the study, 2 holoplank- ton, 7 meroplankton groups ...
© by PSP Volume 23 – No 12. 2014

Fresenius Environmental Bulletin

SEASONAL DISTRIBUTION OF ZOOPLANKTON IN THE GULF OF ERDEK (THE MARMARA SEA) AND THE IMPACT OF ECOLOGIAL VARIABLES Benin Toklu Alıçlı1,*, Neslihan Balkıs1 and Muharrem Balcı2 Istanbul University, Faculty of Science, Department of Biology 34134 Vezneciler, Istanbul, Turkey Istanbul University, Institute of Science, 34134 Vezneciler, Istanbul, Turkey

Presented at the 17th International Symposium on Environmental Pollution and its Impact on Life in the Mediterranean Region (MESAEP), September28 - October 01, 2013, Istanbul, Turkey

ABSTRACT The aim of this study is to characterize the seasonal variation of zooplankton and the impact of some ecological variables on zooplankton distribution. The study was conducted seasonally in the Gulf of Erdek between November 2006 and August 2008. Zooplankton samples were collected from 3 sampling stations using WP-2 zooplankton net (200µm mesh size). During the study, 2 holoplankton, 7 meroplankton groups, 12 Copepoda, 3 Cladocera, 1 Ctenophora and 1 Cnidaria species were found in the study area. Acartia clausi (401 ind/m3 in May 2008), Paracalanus parvus (139 ind/m3 in February 2007) which belong to Copepoda, Penilia avirostris (610 ind/m3 in August 2008) which belong to Cladocera and Liriope tetraphylla ( 270 ind/m3 in August 2007) which belong to Cnidaria were the important species of this study since they are abundant in total zooplankton identified. In addition, temperature (6.5-25.5 ºC), salinity (22.4-38.8 ppt), dissolved oxygen (3.78-14.96 mg L-1), chlorophyll-a (0.12.83 µg L-1), NO2+NO3-N (0.11-4.93 µg-at N L-1), PO4-P (0.09-2.11 µg-at P L-1) and SiO4-Si (0.28-21.62 µg-at Si L-1) of seawater were recorded on each sampling occasion.

KEYWORDS: Gulf of Erdek, Marmara Sea, Zooplankton, Ecological variables

1. INTRODUCTION The zooplankton serves as the primary consumer and secondary producer in the marine food chain. Most zooplanktonic organisms convert vegetable protein into animal protein and, thereby, constitute the essential food for vertebrates and invertebrates that feed on animal protein. Therefore, the abundance of animal organisms depends on * Corresponding author

the abundance of zooplankton in an aquatic ecosystem. In other words, the fish abundance in an aquatic ecosystem highly depends on the zooplankton abundance in the same ecosystem. Zooplanktonic organisms are affected by the possible changes in the environment, which means that the distribution and abundance of zooplankton very much depend on the ecological changes. Located in the northwest of Turkey, the Marmara Sea is a small basin (surface area :11,500 km2, the maximum depth: 1390 m) and has always been the passageway between the Black Sea and the Aegean Sea through the Bosphorus and the Dardanelles Straits [1-3]. The lower-layer flow of the Mediterranean Sea origin with a salinity of about 38 ppt is directed to the north towards the Sea of Marmara through the Dardanelles. In contrast, the upper-layer water of the Black Sea origin with a salinity of about 17.6 ppt flows in the opposite direction to the Marmara Sea through the Bosphorus. Approximately at 25 m depth, there is a halocline between the two separate water layers, which are not mixed into each other due to the density differences [2, 4]. Water exchange and oceanographic conditions in the Marmara Sea are controlled by the two straits. While the salinity is higher in the bottom water, dissolved oxygen is lower. Oxygen transfer from the surface layer to the lower-layers is impeded by the halocline. The oxygen consumption by biogenic particles in the lower-layer is another factor to decrease oxygen content [2, 5]. The fauna and flora of the Marmara Sea, which include both brackish water and typical sea water, are also rich. The oceanographic characteristics of the Gulf of Erdek, which is the study area, are similar to that of the Marmara Sea and the water column has a two-layer structure. The human population and industrial activities in Gulf of Erdek are lower comparing to the other locations around Marmara Sea. The Biga River and the Gönen River flow into the Gulf of Erdek. Studies on zooplankton were conducted in various parts of the Marmara Sea [6-21]. However, there is little data about the zooplankton in the Gulf of Erdek [22, 23].

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FIGURE 1 - Sampling stations in the Gulf of Erdek [24]

The aim of this study is to assess the composition and distribution of zooplankton seasonally between November 2006 and August 2008 and determine the impact of some ecological variables on them.

2. MATERIALS AND METHOD This study was carried out in order to identify the zooplankton species that live in the neritic waters of the Gulf of Erdek, determine their seasonal distribution and the effect of some ecological factors on their distribution. Zooplankton samples were collected from three stations with a depth of 30 m seasonally (November, February, May, August) for two years between November 2006 and August 2008. The maximum depths of the stations ranged between 28 and 38 meters. Water samples for detecting temperature, salinity, dissolved oxygen (DO), chlorophyll a and nutrients were collected at different depths (0.5, 15, 30 m) on each sampling occasion. Zooplankton samples were collected horizontally from surface and vertically from 30m depth to surface, by a zooplankton net with a mesh size of 200 µm and a diameter of 57 cm., at between 08:00-12: 00 am. The samples were fixed in 4% borax buffered formaldehyde. The samples were analyzed in a Bogorov counting chamber using a stereomicroscope. Sub-samples were taken (at least twice) using a Stempel pipette and quantitative analyses were performed. The samples were identified as species or groups. Temperature was measured with the thermometer on the water sampler, salinity following the Mohr-Knudsen method [25], dissolved oxygen following Winkler method [26], visibility with a Secchi disk, Nitrate+nitrite (NO3+NO2N) concentration was analyzed by cadmium reduction

method using a Seal Analytical continuous-flow autoanalyzer 3 [27], chlorophyll-a, silicate (SiO4-Si) and Phosphate (PO4-P) concentration following the method of Parsons et al. [28] at all sampling stations and different depths. The relationship between species and ecological variables was investigated with a canonical correspondence analysis (CCA), applied with Monte Carlo permutation test for statistical significance (p< 0.05) was used to test ecological variables [29]. Spearman’s rank correlation coefficient Siegel [30] was used to detect any correlation among the ecological variables and zooplankton abundance.

3. RESULTS AND DISCUSSION The average profiles of the three stations are given in Fig 2. The highest (25.5 °C) temperature was measured at the depth of 0.5 m at all stations in August 2007 (mean value 25.3±0.29, 0.5 m) and lowest (6.5 °C) at depth of 15 m at the all stations in February 2008 (mean value 6.5±0.00, 15m) in the Gulf of Erdek . In 2006-2007 autumns, 2007-2008 winters and 2007 spring temperature values were stable because of vertical mixtures in the water column. On the other hand, in summer 2007-2008 and spring 2008, the temperature was higher at surface layer comparing the lower layer, with the effect of atmosphere. The thermocline prevented mixing of the two layers in these seasons, thus caused the difference in temperatures. The temperature change was remarkable at depths deeper than 15. The highest salinity value (38.6 ppt) was determined at the depth of 30 m at Station 3 in November 2006 (mean value 37.37±1.1, 30m) and Station 2 in February 2007 (mean value 37.93±0.58, 30m) and lowest (22.4 ppt) at the depth of 0.5m at Station 2 in May 2007

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(a)

(b)

(c) FIGURE 2 - (a-c) Seasonal variations of temperature (ºC), salinity (ppt) and dissolved oxygen (mg L-1) along the water column in the Gulf of Erdek. Data are reported as averages of the sampling stations.

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(mean value 24.87±4.19, 0.5m) in the area. Halocline was detected at 15m depth and a remarkable increase in salinity was noticed at 30m, with the effect of Mediterranean. The highest dissolved oxygen (DO) value (14.96 mg L-1) was measured at the depth of 0.5 m at Station 2 in November 2006 (mean value 14.49±0,4, 0,5m) and the lowest (3.78 mg L-1) at the depth of 30 m at Station 3 in August 2008 (mean value 3.96±0.16, 30m). A decrease in oxygen level was observed when the samples were taken from deeper layers. The high oxygen levels at shallow depths were attributed atmospheric interactions. The bacterial activity decreased the oxygen level at lower layers. For chlorophyll-a concentration, the highest value (2.83 μg L-1) was determined at the depth of 15 m at Station 3 in February 2008 and the lowest value at the depth of 30 m (0.10 μg L-1) at Station 3 in May 2008. While the highest NO2+NO3-N value (4.93 µg-at N L-1) was measured at the depth of 30 m at Station 3, the lowest value (0.11 µg-at N L-1) was measured at 15 m at Station 2 in May 2007. The highest PO4-P value (2.11 µg-at P L-1) was measured at 30 m depth, at Station 3 in November 2007 and the lowest (0.09 µg-at P L-1) value measured at the depth of 30 m at Station 1 in February 2008. We measured the highest (21.62 µg-at Si L-1) and the lowest (0.28 µg-at Si L-1) SiO4-Si values at the depth of 30 m at Station 2, in May 2007, and at the depth of 0.5 m at Station 3, in May 2008 respectively [31]. In the Gulf of Erdek, different zooplankton species and groups were identified in different seasons between 2006 and 2008. In autumn 2006, 2 copepod species, Liriope tetraphylla which belongs to Cnidaria, 1 holoplankton group and 2 meroplankton groups were found. In winter 2007, 7 copepod species, Liriope tetraphylla which belongs to Cnidaria, Pleurobrachia pileus which belongs to Ctenophora, 1 holoplankton group and 4 meroplankton groups were found. In spring 2007, 5 copepod species, 1 cladoceran species, Pleurobrachia pileus which belongs to Ctenophora, 2 holoplankton groups and 4 meroplankton groups were found. In summer 2007, 2 copepod species, Liriope tetraphylla which belongs to Cnidaria, 1 holoplankton group and 2 meroplankton groups were found. In autumn 2007, 7 copepod species, 2 cladoceran species and 2 meroplankton groups were found. In winter 2008, 2 copepod species and 1 meroplankton group were found. In spring 2008, 10 copepod species, 3 cladoceran species, Pleurobrachia pileus which belongs to Ctenophora, 2 holoplankton groups and 5 meroplankton groups were found. In summer 2008, 4 copepod species, 1 cladoceran species, 2 holoplankton groups and 6 meroplankton groups were found. The seasonal distributions of the species and groups among stations were determined as; in autumns 6 copepoda, 1 cladocera, Liriope tetraphylla, 1 holoplankton and 2 meroplankton groups at the Station 1, 6 copepoda, 1 cladocera, Liriope tetraphylla, 1 holoplankton and 1 meroplankton groups at the Station 2, 4 copepoda, 2 cladocera, Liriope tetraphylla, 1 holoplankton and 2 meroplankton groups at the Station 3; in winter 6 copepoda, 2 cladocera, Liriope tetraphylla, Pleurobrachia pileus , 1 holoplankton and 1 meroplankton groups at the Station 1, 5 copepoda,

Liriope tetraphylla, Pleurobrachia pileus, 1 holoplankton and 2 meroplankton groups at the Station 2, 5 copepoda Liriope tetraphylla, Pleurobrachia pileus, 1 holoplankton and 4 meroplankton groups at the Station 3; in spring 6 copepoda, 2 cladocera, 1 holoplankton and 4 meroplankton groups at the Station 1, 5 copepoda , 2 cladocera, Pleurobrachia pileus,2 holoplankton and 4 meroplankton groups at the Station 2, 6 copepoda, 2 cladocera, Pleurobrachia pileus, 2 holoplankton and 2 meroplankton groups at the Station 3; in summer 2 copepoda, 1 cladocera, Liriope tetraphylla, 1 holoplankton and 3 meroplankton groups at the Station 1, 3 copepoda, 1 cladocera, Liriope tetraphylla, 1 holoplankton and 6 meroplankton groups at the Station 2, 4 copepoda, 1 cladocera, Liriope tetraphylla, 2 holoplankton and 6 meroplankton groups at the Station 3.When we investigated the abundance of the species Paracalanus parvus (139 ind/m3), Oithona nana (44 ind/m3) Oncea spp. (26 ind/m3), L. tetraphylla (270 ind/m3) and Acartia clausi (401 ind/m3) were dominant species at station 2. In the study, a total of 12 copepod species which belong to the orders of Calanoida, Cyclopoida and Harpactoida were found. Of these species, Acartia clausi and Paracalanus parvus which belong to the order of Calanoida and Oithona nana which belong to the order of Cyclopoida were the species that were frequently observed during the two years. P. parvus was observed in every season (Table 1). Similar results were obtained in the studies conducted in different parts of the Marmara Sea [6, 9, 10, 32, 19]. Besides, in a study which was conducted in the same part as the present study, Isinibilir [22] found the copepods Calanus euxinus, Centropages ponticus, Euterpina acutifrons, Pseudocalanus elongatus and the cladocerans Pleopis polyphemoides and Penilia avirostris. Similarly, in the present study these species were identified. In a study conducted in the Gulf of Erdek and in the studies conducted in other parts of the Marmara Sea, Acartia clausi was again reported to be abundant [22,15]. In our study, the copepod Acartia clausi (401 ind/m3) constituted 66.18% of zooplankton abundance in the study area in spring 2008 (Table 1). Besides, this species was observed to be more abundant in the spring of the previous year. A. clausi is found in contaminated parts since it has a high tolerance to contamination. The increase in phytoplankton also caused an increase in A. clausi in this period due to nutrition as in other zooplankton species. In addition, the mucilage event that is observed more intensively in the region in 2007 affected the species. Of Cyclopoid copepoda, Oncea spp. was not common in the present study. The reason for this could be low salinity values in the study area. Indeed, Svetlichny et al. [15] argued that the subsurface of the Marmara Sea with lower salinity is not favorable to the survival of Oncea spp. Although Liriope tetraphylla is a common species in the Mediterranean Sea, it was not recorded in the Marmara Sea before September 2005. It reached a high level of

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TABLE 1 - Percentage contribution of zooplankton species and groups in terms of abundance (%) in sampling periods.

Paracalanus parvus Claus, 1863 Pseudocalanus elongatus Boeck, 1872 Calanus euxinus Hulsemann, 1991 Acartia clausi Giesbrecht, 1889 Centropages ponticus Karavaev, 1894 Centropages typicus Kröyer, 1849 Anomalocera patersoni Templeton, 1837 Oithona nana Giesbrecht, 1892 Oithona similis Claus, 1863 Oncea spp. Corycaeus spp. Euterpina acutifrons Dana, 1852 Liriope tetraphylla Otto,1823 Pleurobrachia pileus O.F.Müller, 1776 Evadne spinifera P.E. Müller, 1867 Pleopis polyphemoides Leuckart, 1859 Penilia avirostris Dana, 1852 Appendicularia Chaetognatha Decapoda larvae Polychaeta larvae Bivalvia larvae Gastropoda larvae Echinodermata larvae Cirripedia larva Fish larvae

Autumn 06

Winter 07

Spring 07

Summer 07

Autumn 07

Winter 08

Spring 08

Summer 08

68.42

30.28

28.99

12.58

16

26.32

3.18

1.65

0

7.27

0

0

0

0

0.09

0

0

13.19

0

0

8

0

1.20

0

0

1.75

26.57

0

1

0

66.18

0.34

0

1.21

0

0

9

0

0.34

0

0

0

0

0

0

0

0.52

0.96

0

0

0

0

0

0

0.09

0

1.64

12.25

6.28

3.71

7

0

0.34

0

0

0

1.93

0

0

0

0.69

0

0 0

0 0

12.56 0

0 0

10 16

0 21.05

1.98 0

0.62 0

0

0.54

0

0

0

0

0

0

23.03

7.94

0

73,91

0

0

0

0

0

10.09

4.83

0

0

0

1.98

0

0

0

2.42

0

0

0

6.20

0

0

0

0

0

1

0

0.34

0

0

0

0

0

3

0

0.69

88,22

2.30 0 0 0 1.32 0 3.29 0 0

6.46 0 0.54 0.54 4.98 0 0 0 2.96

9.66 1.93 0.48 1.93 0.48 0 0 0 1.93

8.48 0 0 0 0.13 0 1.19 0 0

0 0 0 4 0 0 25 0 0

0 0 0 0 0 0 0 0 52.63

9.47 0.34 2.5 0 0.09 0 0.77 1.89 1.12

0.69 0.28 0.41 0 3.58 1.86 0.07 1.10 0.21

abundance in the Gulf in October 2006 and March 2007 [22]. In the present study, L. tetraphylla (270 ind/ m3) constituted 73.91% of zooplankton abundance in August 2007 (Table 1). In addition, this species caused the change of zooplankton structure in the Marmara Sea [33]. In a previous study, it was reported that L .tetraphylla which was observed in all seasons reached the maximum level of abundance in August [34]. Isinibilir [22] reported that Penilia avirostris, which is a moderate temperature species, reached a high level of abundance in summer. Also in the present study, the species was observed abundantly (610 ind/m3) in summer (August 2008) and constituted 88.22% of total zooplankton abundance (Table 1). The disappearance of P. avirostris can be explained by negative effects of lower water temperature in winter [35]. Furthermore, cladocerans, which are circannual organisms, were not present in the winter because winter is the period when they rest their eggs on the sea bed [36]. This result is in accordance with our study. Ramirez and Perez [36] argued that the occur-

rence and abundance of cladocerans are determined by the warming and stability of upper water levels. Also, Svetlichny et al.[15] mentioned that cladocerans show successful development in the Marmara Sea and, their larvae can survive in the black sea originated low saline upper layers because of the their spawning type. Isinibilir [22] reported the existence of the holoplankton appendicularia and chaetognatha, and the meroplankton echinoderm, poliket, bivalvia, gastropod and cirriped larvae in the Gulf of Erdek. In the present study, similar results were obtained; however, the percentage of these species in the total zooplankton abundance was recorded to be low (Table 1). The results of Spearman’s rank order correlation were employed to explain the relationship between the ecological variables and zooplankton abundance in the Gulf (Table 2). In the Gulf of Erdek, there was highly positive correlation (p