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Decapod Crustaceans in the Marmara Island (Marmara Sea) and Ecological Characteristics of Their Habitats.

INTRODUCTION

The Archipelago in the Sea of Marmara consisting of small and large islands located southwest of the Sea of Marmara and the northwest of the Kapidag Peninsula are referred to as the Islands of Marmara. With an area of 120 [km.sup.2], the Marmara Island is the largest of these islands in the Sea of Marmara. The Marmara Island extends to 18 km in the east-west direction and has coastline of 10 km in the north-south. Deep-water pink shrimp and rock lobster are target species for commercial fishing activities in the area (1).

The Marmara Island has similar water characteristics to the Sea of Marmara; the upper water layer is the Black Sea and the lower water layer is the Mediterranean Sea. The Black Sea water (low salinity: 18) and the Mediterranean water (high salinity: 38) do not mix with each other due to different densities of salinity, but form a salinity intermediate water (halocline) at 25 m depth of the Sea of Marmara (2).

There is a rich body of literature on the biodiversity of the Sea of Marmara. However, the number of studies conducted on the Marmara Island is relatively small. The first study at the island was carried out by Ostroumoff (3,4) followed by studies by Okus (5), Yuksek (6) and Balkis (7).

MATERIALS AND METHODS

Sample Collection

Samplings were performed at the coastal waters of the Marmara Island in May and November months of 2008 year. Specimens of decapod crustaceans were captured from 12 sites at the depths between 0 and 60 m. The sampling stations are shown in Figure 1. Samples were hand-picked or collected using a hand-held scoop while the offshore samples were collected using a beam trawl with a mesh size of 18 mm.The samples were preserved in 5% formalin and species were stored in 70% ethanol.

Sample Identification

Specimens of decapoda were identified using the criteria as previously described by Bouvier (8), Zariquiey Alvarez (9,10), Demir (11), Holthuis (12-15), Geldiay and Kocatas (16,17), Ingle (18,19) and Balkis (20). The names of the species were updated according to WORMS (21).

Measurements and Analysis

During the study, sea water variables such as temperature, were measured in situ. The temperature was measured using the thermometer on the sampling flask. The salinity was measured using silver nitrate titration using the Mohr-Knudsen method (22). The amount of dissolved oxygen was measured using a sodium thiosulfate titration according to the Winkler method (23).

Soyer's (24) Frequency index (Fs) was used to determine the frequency of the decapod species in the coastal zones of the study field. The results were analysed in three groups according to calculated Fs values as 'constant' (Fs[greater than or equal to]50%), 'common' (50%>Fs[greater than or equal to]25%) and 'rare' (Fs<25%). The Dominance Index Formula was used to determine the dominance of the decapod species in the coastal zones of the study field (25).

Bray-Curtis similarity index and (MDS) analyses were performed in the Primer v6 program to determine the similarity between the sampled stations (26). For these analyses, firstly, log (x+1) conversion was applied on raw information. Using the composition of the number of species and the number of individuals at the sampling stations Shannon-Weaver Diversity Index (H') was performed.

RESULTS

Environmental Variables

The ecological variable such as temperature ([degrees]C), salinity (%o) and dissolved oxygen (mg [L.sup.-1]) at the sampling stations in the littoral zone of the Marmara Island were presented in Table 1.

The temperature varied between 14.3 [degrees]C and 18.0 [degrees]C in the two sampling periods. The temperature lowered with depth. The salinity values ranged from 21.2 % to 35.7 %. As a natural feature of the two-layered water system of the Sea of Marmara, the salinity increased with depth. The highest dissolved oxygen value (12.98 mg [l.sup.-1]) was obtained in May from station 2 and the lowest value (5.65 mg [l.sup.-1]) was obtained in May from station V at the depth of 50 m.

Faunistic Data

A total of 17 species of decapod crustaceans were reported (Table 2). Table 2 shows 10 species out of 17 species found from the onshore sampling while 7 from the offshore sampling studies. Pink shrimp Parapenaeus longirostris, Majid crab Maja squinado and Portunid crab Liocarcinus depurator observed from the offshore were found at the depths of 40, 50 and 60 m, respectively. Pandalid shrimp Plesionika heterocarpus, Crangonid shrimp Aegaeon lacazei and Norway lobster Nephrops norvegicus were reported only at the depth of 60 m, and brachyuran crab Dromia personata at the depth of 40 m. No common species was detected both from the shore and the deep water.

A total of 10 species were obtained during the onshore sampling (Table 3). While the highest number of species was observed with 6 species at site 5 in May, the lowest value (2 species) was recorded at site 4. In November, the highest number of species (6) was found at station 4 and the lowest (2 species) at station 1. Among these species found during offshore samplings, only brachyuran crab X. poressa is constant species in both seasons. The common species in spring are Paguroid D. pugilator, Portunid crab C. aestuarii, Anomuran P. bluteli, and Paguroid C. erythropus. In autumn, P. bluteli and Pisidia longimana are constant species while C. erythropus, C. aestuarii and P. hirtellus are common species. Dominance index values show that, D. pugilator and X. poressa are dominant species in spring and in autumn, respectively.

A total of 7 decapod crustaceans were found at the offshore sampling stations (Table 4). In May and November, the highest number of species (4) was found at station II while the lowest (2) at station I. Out of these 7 species, A. lacazei was caught only in November while N. norvegicus and D. personata were found only in May. No samples could be collected at stations IV, V and VI in November. The general distribution of the species indicates that P. longirostris (429 individuals) and L. depurator (362 individuals) were collected from all the offshore sampling stations both in May and November.

(H') values for grab samples collected from Marmara a Island are presented in Table 5. When (H') values of the studied sites were analyzed, site 4 in autumn was found to have the highest H' value.

The similarities between the stations were evaluated according to the distributions of the species obtained from the onshore sampling stations.

The results of the Bray-Curtis similarity index and MDS methods applied at the onshore sampling stations in the spring and autumn are shown in Figure 2.

Figure 2 shows that there is a similarity between stations 1, 4 and 3 in the spring, while there is a similarity between stations 1 and 2, and between stations 5 and 6 in the autumn.5.

DISCUSSION

The zoogeographical characteristics of the species were presented according to d'Udekem d'Acoz (27) and in compliance with Stevcic (28). Accordingly 12 species reported here (P. longirostris, P. heterocarpus, N. norvegicus, P. longimana, P. platycheles, C. erythropus, D. personata, C. aestuarii, L. depurator, L. vernalis, X. poressa and P. hirtellus) are Atlanto-Mediterranean originated, therefore, 3 species (P. elegans, A. lacazei and D. pugilator) are Cosmopolitan and the remaining two (P. bluteli and M. squinado) are Mediterranean Endemic.

Previous studies on the Turkish Strait System' decapods have examined the first records provided by Forskal (29) showing the presence of 2 crab species in Istanbul [Nepinnotheres pinnotheres (Linnaeus 1758); Eriphia verrucosa (Forskal 1775)]. Then Bakir et al. (30) reported 144 and Balkis et al. (31) reported a total of 140 decapod crustaceans from the area.

Researchers who previously studied on the Marmara Island and the species they identified are shown in Table 6.

Ostroumoff (3,4) reported 14 species of decapod crustaceans in the littoral zone of the Marmara Island. Presence of the Liocarcinus holsatus is not very clear in this study so we accept the presence of 13 species as reported in the study. Okus (5) reported the presence of 25 decapod Crustacea species in the littoral zone of the Marmara Island. However, 2 of these species were reported only at the level of genus and Liocarcinus depurator was specified twice in the study as Macropipus depurator and Liocarcinus depurator. Therefore, Okus (5) reported 22 decapod species. Yuksek (6) reported the presence of 20 decapod species from the southern coasts of the Marmara Island. However, having reported 7 species only at the level of genus, she reported 13 decapod Crustacea species. Balkis (7) carried out a study on the macrobenthos of the Marmara Island and reported 9 decapod species. Xantonid crab Xantho incicus and Caridean shrimp Hippolyte longirostris species reported by Balkis were not found in the Sea of Marmara in previous studies. Therefore, presence of these species is not validated. Current literature indicates there are a total of 36 decapod crustaceans present in the littoral of the Marmara Island to the date.

The similarity percentage of the stations are so different in the spring and autumn as indicated by their similarity percentages. Many environmental factors, such as temperature and food, control zoogeographical distribution of decapod crustaceans (33). Algal vegetation increases in the spring and D.pugilator and X. poressa species are abundant living in algae to protect and feed themselves. Specimens hidden under the stone are more common in the autumn with limited vegetation.

Because samples obtained from the offshore sampling stations were collected using two beam trawls, the dominance, frequency and similarity indices were not calculated. The species identified onshore and offshore are completely different from each other which is thought to be due to the significant effect of depth and sediment type on the distribution of decapods (33).

Nine of the species (P. longirostris; P. elegans, P. heterocarpus, C. erythropus, M. squinado, C. aestuarii, L. depurator, X. poressa and P. hirtellus) in this study have been reported before while the remaining 8 species (A. lacazei, N. norvegicus, P. bluteli, P. longimana, P. platycheles, D. pugilator, D. personata and L. vernalis) have been reported in the littoral zone of Marmara Island for the first time in this study. Including these species, the number of decapod Crustacea species found in the littoral zone of Marmara Island has increased to 44.

This study was conducted in spring and autumn and hence 8 more species have been added to the decapod crustaceans reported to be living in the littoral zone of Marmara Island. In addition, some ecological factors of the habitats of these species have been revealed. This study will also contribute to the further systematic and ecological studies on decapod crustaceans in the region.

Acknowledgements

This study was supported by (the Research Fund of Istanbul University (project number: 1389).

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Begum Ayfer, Husamettin Balkis, Aysegul Mulayim (*)

Istanbul University, Faculty of Science, Department of Biology, Istanbul, Turkey

Address for Correspondence: Aysegul Mulayim

Received: 05.05.2017

Accepted: 28.05.2017

E-mail: aysegulm@istanbul.edu.tr

DOI: 10.5152/EurJBiol.2017.1704
Table 1. Coordinates of sampling stations on the Marmara Island and
physicochemical data of seawater

                                  SPRING
Station  Depth (m)  Temperature   Salinity  Dissolved
                    ([degrees]C)  (%o)      Oxygen ([mg.l.sup.-1])

1        0.5        18.0          21.3      11.54
2        0.5        17.5          21.7      12.98
3        0.5        17.5          21.2      10.63
4        0.5        17.0          21.8      11.73
5        0.5        17.0          21.3      11.89
6        0.5        17.0          21.9      10.11
I         50        14.5          35.3       6.97
II        60        14.5          35.1       6.22
III       40        14.5          35.6       6.28
IV        60        14.3          35.0       6.26
V         50        15.0          34.4       5.65
VI        40        14.8          33.8       6.75

                       AUTUMN
Station  Temperature   Salinity  Dissolved
         ([degrees]C)  (%)       Oxygen ([mg.l.sup.-1])

1        15.0          24.2      10.43
2        15.0          23.9       9.26
3        14.9          23.7       9.44
4        15.0          23.7       9.13
5        15.1          24.4       9.97
6        14.9          23.4       8.92
I        16.9          35.7      10.18
II       16.0          34.8       9.27
III      16.2          35.1       8.25
IV       -             -          -
V        -             -          -
VI       -             -          -

Table 2. Species collected in the littoral zone of Marmara Island

                                            Depths (m)
                                            0-1  40  50  60

Order DECAPODA
Suborder DENDROBRANCHIATA
Parapenaeus longirostris (Lucas, 1946)           +   +   +
Suborder PLEOCYEMATA
Infraorder CARIDEA
Aegaeon lacazei (Gourret, 1887)                          +
Palaemon elegans Rathke, 1837               +
Plesionika heterocarpus (A. Costa, 1871)                 +
Infraorder ASTACIDEA
Nephrops norvegicus (Linnaeus, 1758)                     +
Infraorder ANOMURA
Clibanarius erythropus (Latreille, 1818)   +
Diogenes pugilator (Roux, 1829)            +
Pisidia bluteli (Risso, 1816)              +
Pisidia longimana (Risso, 1816)            +
Porcellana platycheles (Pennant, 1777)     +
Infraorder BRACHYURA
Carcinus aestuarii Nardo, 1847             +
Dromia personata (Linnaeus, 1758)                +
Liocarcinus depurator (Linnaeus, 1758)           +   +   +
Liocarcinus vernalis (Risso, 1827)         +
Maja squinado (Herbst, 1788)                     +   +   +
Pilumnus hirtellus (Linnaeus, 1761)        +
Xantho poressa (Olivi, 1792)               +

Table 3. Decapod crustacean species collected onshore, numbers of
individuals, Frequency (f %) and dominancy (Di)

                                 Shore Stations
                                 Spring

Species                 1   2  3   4    5  6   f%    Di %
Palaemon elegans                                0     0
Pisidia bluteli                         2  2   33.3   1.4
Pisidia longimana                               0     0
Porcellana platycheles                     1   16.6   0.3
Clibanarius erythropus         2       35      33.3  13.1
Diogenes pugilator      51  4  20  74   4      83.3  54.26
Carcinus aestuarii       2  3           5      50     3.5
Liocarcinus vernalis                    1      16.6   0.3
Xantho poressa          17  5  11   6  27  10  100   26.95
Pilumnus hirtellus                                    0

                        Shore Stations
                                        Autumn

Species                 1  2  3  4   5  6    f%     Di %
Palaemon elegans           1                  16.6   0.89
Pisidia bluteli               1  8   3  2     66.7  12.5
Pisidia longimana          2  1  4      3     66.7   8.93
Porcellana platycheles           8            16.6   7.14
Clibanarius erythropus           3   5        33.3   7.14
Diogenes pugilator                             0     0
Carcinus aestuarii      6  2                  33.3   7.14
Liocarcinus vernalis                           0     0
Xantho poressa          7  5  8  13  10 18   100    54.46
Pilumnus hirtellus            1  1            33.3   1.79

Table 4. List of decapod crustaceans collected using beam trawls

                          Beam Trawl Stations
                          Spring

Species                   I   II   III  IV  V   VI
Parapenaeus longirostris  21  74   49   71  28  54
Plesionika heterocarpus    1             1
Aegaeon lacazei
Nephrops norvegicus            1
Maja squinado                       2        1
Dromia personata                                 1
Liocarcinus depurator     19   3   16   47   3  101

                          Beam Trawl Stations
                          Autumn

Species                   I   II  III  IV  V  VI
Parapenaeus longirostris  33  61  37   -   -  -
Plesionika heterocarpus    2
Aegaeon lacazei                1
Nephrops norvegicus
Maja squinado                     1
Dromia personata
Liocarcinus depurator     57  65  51

Tablo 5. Shannon-Weaver Diversity Index (H') values of the grab
stations

             H' Values
Stations  Spring  Autumn

1         0.2318  0.9957
2         1.555   1.761
3         1.2111  1.278
4         0.3843  2.267
5         1.757   1.415
6         0.9913  0.9665

Table 6. Crustacean species in Marmara Island

Order DECAPODA
Suborder DENDROBRANCHIATA
Parapenaeus longirostris (Lucas, 1846)       6, This study
Penaeus kerathurus (Forskal, 1775)           7
Suborder PLEOCYEMATA
Infraorder CARIDEA
Aegaeon lacazei (Gourret, 1887)              This study
Alpheus glaber (Olivi, 1792)                 5
Athanas nitescens (Leach, 1813)              5, 7
Crangon crangon (Linnaeus, 1758)             5
Hippolyte holthuisi Zariquiey Alvarez, 1953  5
Palaemon adspersus Rathke, 1837              5
Palaemon elegans Rathke, 1837                32, 5, 6, This study
Pandalina brevirostris (Rathke, 1843)        5, 7
Plesionika heterocarpus (A. Costa, 1871)     32, This study
Processa canaliculata Leach, 1815            5, 6
Processa edulis edulis (Risso, 1816)         32
Typton spongicola O.G. Costa, 1844           32
Infraorder ASTACIDEA
Homarus gammarus (Linnaeus, 1758)            7
Nephrops norvegicus (Linnaeus, 1758)         This study
Infraorder ANOMURA
Clibanarius erythropus (Latreille, 1818)     5,This study
Diogenes pugilator (Roux, 1829)              This study
Galathea nexa Embleton, 1834                 32
Galathea squamifera Leach, 1814              5
Munida rugosa (Fabricius, 1775)              32
Pagurus cuanensis Bell, 1846                 32
Pisidia bluteli (Risso, 1816)                This study
Pisidia longicornis (Linnaeus, 1767)         5, 6
Pisidia longimana (Risso, 1816)              This study
Porcellana platycheles (Pennant, 1777)       This study
Infraorder BRACHYURA
Carcinus aestuarii Nardo, 1847               5, 6, 7, This study
Dromia personata (Linnaeus, 1758)            This study
Ebalia cranchii Leach, 1817                  32
Eriphia verrucosa (Forskal, 1775)            5
Eurynome aspera (Pennant, 1777)              32, 5
Inachus leptochirus Leach, 1817              32
Inachus thoracicus Roux, 1830                6
Liocarcinus depurator (Linnaeus, 1758)       32, 5, 6, 7, This study
Liocarcinus navigator (Herbst, 1794)         5, 6, 7
Liocarcinus vernalis (Risso, 1827)           This study
Macropodia longirostris (Fabricius, 1775)    5, 6
Macropodia rostrata (Linnaeus, 1761)         5, 6
Maja crispata Maja crispata Risso, 1827      5
Maja squinado (Herbst, 1788)                 5, 6, This study
Monodaeus couchii (Couch, 1851)              32
Pilumnus hirtellus (Linnaeus, 1761)          5, 6, This study
Pisa tetraodon (Pennant, 1777)               32
Xantho poressa (Olivi, 1792)                 5, 6 This study
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Title Annotation:RESEARCH ARTICLE
Author:Ayfer, Begum; Balkis, Husamettin; Mulayim, Aysegul
Publication:IUFS Journal of Biology
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Date:Jun 1, 2017
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