ORIGINAL ARTICLE

Temporal changes of soft-bottom zoobenthic communitiesin and around Alsancak Harbor (Izmir Bay, Aegean Sea),with special attention to the autecology of exotic speciesMelih Ertan Cinar, Tuncer Katagan, Bilal Ozturk, Ozdemir Egemen, Zeki Ergen, Ahmet Kocatas,Mesut Onen, Fevzi Kirkim, Kerem Bakir, Guley Kurt, Ertan Dagli, Asli Kaymakci, Sermin Acik, AlperDogan & Tahir Ozcan

Department of Hydrobiology, Faculty of Fisheries, Ege University, Bornova, Izmir, Turkey

Problem

Anthropogenically introduced alien species are one of the

major factors affecting biodiversity. The number and diver-

sity of non-native species (exotics) vary both at regional

and global scales according to the complex combination of

differences in history, timing, and diversity of transport

vectors, traits of the introduced species, abiotic and biotic

features of the invaded environment, and sampling strat-

egies (Wonham & Carlton 2005). A study performed in

San Francisco Bay indicated that the rate of invasions

increased from an average of one new species established

every 55 weeks from 1851 to 1960, to an average of one

species every 14 weeks from 1961 to 1995 (Cohen & Carl-

ton 1998). Species-poor communities, such as those inha-

biting polluted or physically degraded environments, are

more vulnerable to invasion than are other communities

(Elton 1958). Shea & Chesson (2002) demonstrated that a

weakening of a species fundamentally important in a native

ecosystem structure or those in inherently unstable and

variable environments often result in multiple introduc-

tions. Native species might not be adapted to the altered

Keywords

Community structure; exotics; Izmir Bay;

Mediterranean Sea; pollution; temporal

variation; zoobenthos.

Correspondence

Melih Ertan Cinar, Department of

Hydrobiology, Faculty of Fisheries, Ege

University, 35100 Bornova, Izmir, Turkey

E-mail: melih.cinar@ege.edu.tr

Accepted: 15 June 2006

doi:10.1111/j.1439-0485.2006.00102.x

Abstract

Temporal and spatial variation in soft-bottom benthic communities following

recovery from a pollution episode were studied between January and Septem-

ber 2004 in and around Alsancak Harbor, located in the polluted part of Izmir

Bay (Aegean Sea, eastern Mediterranean). Samples were collected at seven sta-

tions by van Veen grab. Three additional stations were sampled by means of a

beam trawl to take into account large mobile animals and for a better estimate

of the local biodiversity. A total of 231 species belonging to 10 zoobenthic

groups were found. Polychaetes contributed 90% of the total faunal popula-

tions and mollusks 87% of the total biomass in the area. Community parame-

ters varied significantly among stations and sampling periods; number of

species ranged from 2 to 79 per 0.1 m2 grab sample; density from 20 to

81,720 indÆm)2; biomass from 0.1 to 4190 gÆm)2; Shannon–Wiener diversity

index (log2 base) from 0.4 to 4.4; and Pielou’s evenness index from 0.11 to 1.0.

Collections indicate that a number of species, including those sensitive to pol-

lution, have colonized the area where azoic conditions had been previously

reported. A total of six exotic species, Streblospio gynobranchiata, Polydora cor-

nuta, Hydroides dianthus, Hydroides elegans, Anadara demiri and Fulvia fragilis,

probably transferred to the area via ballast water or hull fouling, dominated

soft or hard substrata in and near Alsancak Harbor. The first two species

accounted for more than 70% of the total population in the area, while

A. demiri contributed the most to the biomass (93%, at station 7).

Marine Ecology. ISSN 0173-9565

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 229

environmental conditions, lessening their ability to reduce

resource availability uniformly in time and space, and thus

providing resource opportunities for invaders. Invaders

that alter ecosystem processes such as primary production,

decomposition, hydrology, geomorphology, nutrient

cycling and/or disturbance regimes do not simply compete

with or consume native species – they change the rules of

existence for all species (Vitousek et al. 1997).

The inner part of Izmir Bay, where Alsancak Harbor is

located, has been subjected to various pollution discharges

since the 1960s and is considered to be one of the most pol-

luted environments of the Mediterranean Sea over the last

two decades. The main pollutants affecting the bay water

quality are organic matter, suspended matter, hydrocar-

bons, metals, and pathogenic organisms, all derived mainly

from domestic and industrial wastes (50%), rainfall (15%),

rivers and streams (10%), agricultural sources (10%) and

others (15%) (UNEP 1994). Intense marine transportation

around Alsancak Harbor also contributes to pollution in

the area. According to the statistical data maintained by the

Alsancak Harbor Authority in 2003, a total of 3640 vessels

approached the harbor for loading or unloading. The

majority of the vessels came from Mediterranean countries

but almost 2% came from outside of the Mediterranean.

Because of intense pollution and degradation, azoic condi-

tions together with intense odor have previously been

reported from the area (Muezzinoglu et al. 2000; Dogan

et al. 2005).

Environmental instability and maritime traffic make the

area more susceptible to invasion by exotics. Previous stud-

ies have reported a total of seven exotic species in the inner

part of Izmir Bay: Pseudonereis anomala, Streblospio gyno-

branchiata, Polydora cornuta, Hydroides dianthus, Hydroides

elegans, Anadara demiri, and Fulvia fragilis. Hydroides dian-

thus has been known from the area for more than a century

(Quatrefages 1865) and Ergen (1976) first reported H. ele-

gans from the polluted part of Izmir Bay. These two species

are considered as the primary fouling organisms in the

Mediterranean Sea (Kocak et al. 1999), derived from the

northern Atlantic (H. dianthus) and the tropical/subtrop-

ical region (H. elegans) by shipping (Zibrowius 1971). The

other well-known exotic species from Izmir Bay is A. dem-

iri, which was first reported in Izmir Bay (Demir 1977) and

subsequently from the Greek and Adriatic coasts (Zenetos

1994; Morello & Solustri 2001). This species was possibly

introduced into the area from the Indian Ocean by ship-

ping (Zenetos et al. 2003). More recently, Cinar et al.

(2005) found dense populations of two spionid polycha-

etes, S. gynobranchiata and P. cornuta, around Alsancak

Harbor, and emphasized that they were exotic species ori-

ginated from the South Atlantic coast of the US (type local-

ity of S. gynobranchiata) and the northern Atlantic (P.

cornuta). Cinar & Ergen (2005) reported the Lessepsian

species (i.e. Red Sea species migrated to the Mediterranean

through the Suez Canal) P. anomala on mussels attached to

the piles of Alsancak Harbor and rocks. Another Lessepsian

species, F. fragilis, was found to build up a dense popula-

tion on the polluted soft bottom of Izmir Bay (Ozturk &

Poutiers 2005).

A sudden increase in the number of exotics reported

from the inner part of Izmir Bay coincided with the

improvement in the water quality of the area after the

establishment of ‘The Grand Canal Project’ in February

2000. The project treated wastewater being discharged

into the bay. A recovery in the sediment and water qual-

ity was observed and no azoic conditions have been

detected in the area since 2002 (Ergen et al. 2006). The

disappearance of azoic conditions may create empty

niches for both opportunistic and exotic species. How-

ever, no detailed study regarding this situation has been

carried out within the area.

The objectives of the present study were (i): to investi-

gate the spatial and temporal patterns of soft-bottom ben-

thic communities after an episode of severe pollution and

the establishment of a wastewater treatment plant in the

area, (ii) to examine the possible recovery in water and

sediment quality in the area, (iii) to assess the environ-

mental factors affecting the structure of benthic commu-

nities in the area, and (iv) to determine the importance

of previously known exotic species within the communi-

ties and their spatio-temporal patterns in the area.

Material and Methods

Soft sediments were collected in various periods between

January and September 2004 by a van Veen grab (samp-

ling an area of 0.1 m)2) at seven stations located in and

around Alsancak Harbor (Fig. 1). At each station, three

Fig. 1. Map of the investigated area with the location of sampling

sites. The numbers 1–7 indicate stations sampled with a van Veen

grab, while B1, B2, and B2 are beam-trawl hauls.

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

230 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

grab replicates were taken for benthic community analysis

and an additional sample was collected for chemical and

granulometric analyses of sediments. Stations 1–5 were

selected near Alsancak Harbor, station 6 in Pasaport Har-

bor and station 7 off Inciralti, distant from the Alsancak

Harbor. To better estimate the local biodiversity in the

area, three additional stations were selected near Alsancak

Harbor and sampled by means of a beam trawl to capture

large, mobile animals such as crabs and shrimps that can-

not be sampled by using the grab. A presence–absence

matrix was constructed for species found in the beam-

trawl samples, but was not used for further community

analyses (Table 2). The depths and sediment features of

each station are presented in Table 1.

To determine the possible recovery of water and sedi-

ment quality in the area and its relationship to species

abundance data, 10 surface water samples and one sedi-

ment sample were taken at each station. Granulometric

analyses were performed according to Erguvanli (1995).

Surface water samples were taken by using a Nansen bot-

tle at each grab station during the sampling period. Tem-

perature, dissolved oxygen concentration, and visibility

(Secchi disk depth) were determined in the field. Water

samples for analyzing salinity, pH, nitrite, nitrate, ammo-

nium, phosphate phosphorus, and silicate were poured

into the bottles after pre-filtration, freezing and then

transferred to the laboratory immediately. Salinity, pH,

and nutrients were analyzed by using the Mohr-Knudsen

method, pH meter, and spectrophotometer, respectively

(Parsons et al. 1984). The percentage of carbon in each

sediment sample was estimated according to the modified

Walkley Black titration method (Gaudette et al. 1974).

On board the R/V EGESUF, benthic samples were

sieved with a 0.5-mm mesh and the retained fauna were

put in jars containing 10% seawater–formalin solution. In

the laboratory, the material was sorted according to major

taxonomic groups under a stereomicroscope and pre-

served in 70% ethanol. The specimens were then identi-

fied and counted, and the total wet weight of each species

was estimated by using a balance of 0.0001 sensitivity.

Several specimens of exotic species were dissected to

observe their gametes, and egg diameter (n ¼ 15–20) was

measured with an ocular micrometer. The material was

deposited at the Museum of Faculty of Fisheries, Ege Uni-

versity (ESFM).

Community parameters such as the number of species,

the number of individuals, Shannon–Wiener’s diversity

index (log2 base) (H¢), Pielou’s evenness index (J¢) and

the total biomass value (wet weight) were calculated for

each station in each sampling period. The temporal trends

at each station were tested using both one-way and two-

way ANOVA. To better determine temporal distribution

patterns, the abundance data of all stations in each samp-

ling period were pooled and were analyzed using cluster

and multidimensional scaling (MDS) techniques, based

on the Bray–Curtis similarity (group-average technique),

using the PRIMER package (Clarke & Warwick 2001).

Pair-wise analysis of similarities (ANOSIM) was carried

out to test differences in the benthic assemblages in time.

SIMPER analysis was performed to identify the percent-

age contribution of each species to the overall similarity

(dissimilarity) within each of the groups identified from

the cluster analysis. Spearman rank and Pearson’s correl-

ation analysis were used to assess relationships between

environmental variables and community parameters.

Results

Physico-chemical analyses

Water and sediment features are shown in Fig. 2. Salinity

was usually high in September (max. 39.8 psu), tempera-

ture (max. 26 �C) and phosphate phosphorus [max.

4.5 lgatÆl)1 (except station 7)] were usually high in June,

while dissolved oxygen (max. 9.6 mgÆl)1), pH (max. 8.4),

nitrite (max. 2.4 lgatÆl)1), nitrate [max. 1.17 lgatÆl)1

[except station 3)], ammonium [max. 20.5 lgat l)1

(except stations 5 and 7)], silicate [max. 23.8 lgat l)1

(except stations 2 and 7)] and Secchi disk depth [max.

6.2 m (except stations 3 and 5)] were usually high in

January. The percentage of carbon in sediment was usu-

ally high at station 6.

Faunistical and ecological analysis

The analysis of grab (seven stations) and beam-trawl sam-

ples (three stations) revealed a total of 231 benthic species

Table 1. Depth and granulometric features of sediment taken at

each station.

stations depth [m]

granulometric analysis

silt (%) clay (%) sand (%)

Grab samples

1 7 63.0 22.4 14.7

2 9 69.5 26.9 3.6

3 11 67.3 28.6 4.2

4 6 56.8 40.8 2.5

5 9 69.8 25.4 4.8

6 9 64.7 30.8 4.5

7 9 65.0 30.8 4.2

Beam-trawl samples

B1 8 63.0 22.4 14.7

B2 9 56.8 40.8 2.5

B3 6 67.3 28.6 4.2

Source: Cinar et al. (2005).

Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik, Dogan & Ozcan Zoobentos and exotics in

Alsancak Harbor

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 231

Table 2. List of species collected by van Veen grab and beam-trawl (BT) during the study and their total number of individuals per station (on

grab samples), dominance (D%) and frequency values (F%).

Grab statıons

D% F% BT1 2 3 4 5 6 7

ACTINARIA

*Aiptosiogeton comatus (Andres, 1881) ) ) ) ) ) ) ) ) ) +

*Paranthus rugosus (Andres, 1881) 3 1 ) 1 1 1 ) ** 7.4 +

*Edwardsia claparedeii (Panceri, 1869) 30 1 3 1 17 ) 13 ** 21.4 +

TURBELLARIA

Turbellaria (sp. 1) ) ) ) ) ) ) 2 ** 1.2 +

Turbellaria (sp. 2) ) ) ) ) ) ) 1 ** 1.2 +

Turbellaria (sp. 3) ) ) ) 1 ) ) ) ** 1.2 +

NEMERTINI

*Cerebratulus cf. urticans (Muller, 1854) ) ) ) ) ) ) 4 ** 2.4 )Heteronemertea sp. 11 3 6 11 14 4 21 ** 22.6 +

*Tubulanus cf. polymorphus Renier, 1804 7 3 2 4 8 3 28 ** 31 +

Lineus cf. ruber Muller, 1771 11 ) ) 16 11 3 3 ** 19 +

Nemertini (sp. 1) 1 ) ) 1 ) ) ) ** 2.4 )Nemertini (sp. 2) 2 ) ) ) ) ) ) ** 2.4 )Nemertini (sp. 3) ) ) ) ) 1 ) 3 ** 3.6 )Nemertini (sp. 4) ) ) ) ) ) ) 3 ** 2.4 )NEMATODA

*Enoplus meridionalis Steiner, 1921 3 11 ) ) 124 1156 1 0.99 28.6 )OLIGOCHAETA

*Tubificoides swirenkowi Jaroschencko, 1937 ) ) ) ) ) ) 10 ** 4.8 )*Thalassodrilides gurwitschi (Hrabe, 1971) 35 2 7 55 23 100 25 0.19 49 )POLYCHAETA

Adyte assimilis (McIntosh, 1874) ) ) ) ) ) ) 1 ** 1.2 )Harmothoe imbricata (Linne, 1767) ) ) ) ) 2 ) ) ** 2.4 )Harmothoe sp. ) ) ) ) ) ) 2 ** 1.2 )Polynoidae (sp.) ) ) ) ) ) ) 1 ** 1.2 )Eumida sanguinea Oersted, 1843 15 9 2 25 30 16 11 ** 37 +

Eteone picta (Quatrefages 1865) ) 4 ) 2 2 ) ) ** 6 +

Phyllodoce mucosa Oersted, 1843 ) ) 1 ) ) ) ) ** 1.2 )*Phyllodoce rosea (McIntosh, 1877) 2 12 ) 1 2 ) ) ** 9.5 +

Phyllodoce sp. ) ) ) ) ) ) 1 ** 1.2 )Ophiodromus flexuosus (Delle Chiaje, 1825) 1 ) ) 4 4 11 4 ** 16.7 )Ophiodromus pallidus (Claparede, 1864) 5 9 3 10 8 1 24 ** 33.3 +

Podarkeopsis galangaui Laubier, 1961 27 49 17 41 49 22 63 0.21 69 +

Sigambra tentaculata (Treadwell, 1941) 9 14 3 9 18 2 104 0.12 48.8 +

Syllidia armata Quatrefages 1865 11 30 5 23 37 27 34 0.13 53.6 +

Exogone naidina Oersted, 1845 ) ) ) ) ) ) 1 ** 1.2 )Syllis garciai (Campoy, 1982) ) ) ) ) 1 ) ) ** 1.2 )Eunereis longissima (Johnston, 1840) ) ) ) ) ) ) 1 ** 1.2 )Neanthes caudata (Delle Chiaje, 1828) 27 6 1 ) 2 4 ) ** 15.5 +

Neanthes succinea (Frey & Leuckart, 1847) 6 22 2 42 6 3 8 ** 41.7 +

Nereis falsa Quatrefages 1865 ) ) ) ) 1 ) ) ** 1.2 )Micronepthys maryae San Martin, 1982 6 5 ) 3 5 4 40 ** 26.2 )Nepthys hombergi Savigny, 1818 10 7 2 112 14 2 7 0.12 34.5 +

Nepthys incisa Malmgren, 1865 ) 1 ) ) 4 ) 13 ** 11.9 )Glycera alba (O. F. Muller, 1776) 2 7 5 ) 3 4 6 ** 22.6 +

Glycera fallax Quatrefages, 1850 4 7 5 7 10 1 53 ** 31 +

Glycera tridactyla Schmarda, 1861 3 ) ) 4 3 7 ) ** 13 +

Glycera unicornis Savigny, 1818 5 8 2 ) 13 4 8 ** 21.4 +

Glycinde nordmanni (Malmgren, 1865) ) 1 ) ) ) ) 1 ** 2.4 )Eunicidae (sp.) ) ) ) ) ) ) 1 ** 1.2 )Diopatra neapolitana Delle Chiaje, 1841 ) 5 1 3 5 1 7 ** 21.4 )Lumbrineris gracilis (Ehlers, 1868) ) 1 ) ) ) ) 106 ** 9.5 )

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

232 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

Table 2. Continued.

Grab statıons

D% F% BT1 2 3 4 5 6 7

Lumbrineris latreilli Audouin & M. Edwards, 1834 ) ) ) ) ) ) 4 ** 3.6 )Schistomeringos rudolphii (Delle Chiaje, 1828) 67 9 30 7 6 3 12 0.11 34.5 +

Drilonereis filum (Claparede, 1868) ) 1 ) ) ) ) ) ** 1.2 )Aonides oxycephala (Sars, 1862) ) ) ) ) ) ) 4 ** 3.6 )Laonice cirrata (Sars, 1851) ) ) ) ) ) ) 1 ** 1.2 )Malacoceros fuliginosus (Claparede, 1868) 4 ) 13 ) ) 5 ) ** 15.5 )Polydora coeca (Oersted, 1843) ) ) ) ) ) ) 10 ** 2.4 )Polydora cornuta Bosc, 1802 203 256 106 247 304 141 8 0.97 69 +

Polydora sp. 1 ) ) ) ) 2 ) 4 ** 5.6 +

Polydora sp. 2 ) ) ) ) ) ) 1 ** 1.2 +

Prionospio fallax Soderstrom, 1920 62 135 26 127 83 198 265 0.68 67.9 +

Prionospio multibranchiata Berkeley, 1927 308 1452 398 893 620 951 1688 4.84 91.7 +

Prionospio sp. ) ) ) 7 ) ) ) ** 2.4 )Pseudopolydora antennata (Claparede, 1870) 653 1102 77 2343 1925 1441 15 5.8 66.7 +

*Pseudopolydora pulchra (Carazzi, 1895) 5 23 2 2 9 2 ) ** 21.4 +

Spio decoratus Bobretzky, 1870 105 92 37 378 187 123 7 0.71 48.8 +

Streblospio gynobranchiata Rice & Levin 1998 17956 15678 14151 13572 16765 6337 1069 66 95.2 +

Aricidea fragilis mediterranea Laubier & Ramos, 1974 ) 6 ) ) 14 ) 37 ** 20.2 +

Aricidea suecica meridionalis Laubier & Ramos, 1974 ) 1 1 ) 2 ) 43 ** 15.5 )Cirrophorus furcatus (Hartman, 1957) 1 ) ) ) 15 ) 26 ** 11.9 )Paradoneis lyra (Southern, 1914) 3 ) ) ) 4 ) 17 ** 11.9 )Poecilochaetus sp. ) ) ) ) 2 ) 1 ** 3.6 )Spiochaetopterus costarum (Claparede, 1870) ) ) ) ) ) ) 17 ** 9.5 )Magelona alleni Wilson, 1958 ) ) ) ) ) ) 2 ** 2.4 )Magelona minuta Eliason, 1962 ) ) ) ) ) ) 11 ** 7.1 )Capitella capitata (Fabricius 1780) 1963 217 359 310 827 1114 61 3.72 71.4 +

Heteromastus filiformis (Claparede, 1864) 1269 729 79 1086 1284 314 782 4.26 78.6 +

Mediomastus fragilis Rasmussen, 1973 ) 1 ) 12 274 ) 871 0.89 16.7 +

Mediomastus sp. 8 ) ) 1 ) ) 2 ** 7.1 )Notomastus latericeus Sars, 1851 ) ) ) ) ) ) 2 ** 2.4 )Ctenodrilus serratus (Scmidt, 1857) ) ) ) ) ) 148 ) 0.11 3.6 )Aphelochaeta spp. ) ) ) ) ) ) 64 ** 7.1 )Caulleriella bioculata (Keferstein, 1862) ) ) ) ) ) ) 3 ** 2.4 )Chaetozone gibber Woodham & Chambers, 1994 1 ) ) ) 1 ) 18 ** 11.9 +

Chaetozone sp. 1 ) ) ) ) ) ) 15 ** 7.1 )Chaetozone sp. 2 ) ) ) ) ) ) 2 ** 2.4 )Cirriformia cf. tentaculata (Montagu, 1808) 1 ) ) ) ) ) 29 ** 7.1 )*Dodecaceria cf. sextentaculata (Delle Chiaje, 1822) ) ) ) ) ) ) 10 ** 1.2 )Dodecaceria sp. ) ) ) ) ) ) 1 ** 1.2 )Monticellina dorsobranchialis (Kirkegaard, 1959) ) ) ) ) ) ) 5 ** 2.4 )Monticellina heterochaeta Laubier, 1961 ) ) ) ) ) ) 24 ** 4.8 )Monticellina sp. ) ) ) ) ) ) 1 ** 1.2 )Protocirrineris sp. ) ) ) ) ) ) 1 ** 1.2 )Timarete sp. ) ) ) ) ) ) 53 ** 3.6 )*Ophelina modesta Stop)Bowitz, 1958 16 26 18 6 29 4 14 ** 25 +

Polyophthalmus pictus (Dujardin, 1839) ) ) ) ) ) ) 1 ** 1.2 )Cossura soyeri Laubier, 1963 ) ) ) ) ) ) 29 ** 8.3 )Owenia fusiformis Delle Chiaje, 1842 1 ) ) ) ) 2 5 ** 5.6 )Lagis koreni (Malmgren, 1866) 1 13 8 ) 77 2 8 ** 26.2 +

Sabellaria alveolata (Linne, 1767) ) ) ) ) ) ) ) ) ) +

*Sabellaria alcocki Gravier, 1906 ) ) ) 1 ) ) 21 ** 3.6 +

Sabellaria spinulosa Leuckart, 1849 ) ) ) ) ) ) 1 ** 1.2 )Melinna palmata Grube, 1870 ) ) ) ) ) ) 19 ** 10.7 )Lanice conchylega (Pallas, 1766) ) 2 1 13 25 ) ) ** 19 +

Terebella lapidaria Linne 1767 1 ) ) ) ) ) 52 ** 6 +

Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik, Dogan & Ozcan Zoobentos and exotics in

Alsancak Harbor

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 233

Table 2. Continued.

Grab statıons

D% F% BT1 2 3 4 5 6 7

Polycirrus sp. ) ) ) ) ) ) 61 ** 7.1 )Chone filicaudata Southern, 1914 ) ) ) ) ) ) 1 ** 1.2 )Demonax brachychone (Claparede, 1870) ) ) ) 1 ) ) ) ** 1.2 )Demonax tenuicollaris (Grube, 1870) ) ) ) ) ) ) 2 ** 2.4 +

*Demonax cf. langerhansi Knight)Jones, 1983 ) ) ) ) ) ) 1 ** 1.2 +

Demonax sp. ) ) ) 1 ) ) ) ** 1.2 )Euchone rosea Langerhans, 1884 ) ) ) ) ) ) 20 ** 3.6 )*Myxicola infundibulum (Renier, 1804) ) ) ) ) ) ) 2 ** 1.2 )Hydroides dianthus (Verrill, 1873) 11 2 ) 25 1 ) 83 ** 15.5 +

Hydroides elegans (Haswell, 1883) ) 2 ) 12 1 3 10 ** 16.7 +

Spirobranchus polytrema (Philippi, 1844) ) ) ) ) ) ) 4 ** 1.2 )Vermiliopsis infundibulum (Gmelin, 1788) ) ) ) ) ) ) ) ) ) +

PHORONIDA

Phoronis cf. muelleri Selys-Longchamps, 1903 ) 10 ) 1 11 ) 28 ** 22.6 +

Phoronis sp. 1 ) ) ) ) ) 140 0.11 6 +

CRUSTACEA

Balanus amphitrite (Darwin, 1854) ) ) ) ) ) ) ) ) ) +

Balanus eburneus Gould, 1841 ) ) ) ) ) ) ) ) ) +

Ampelisca pseudosarsi B Santini&K Malka, 1977 ) ) ) ) ) ) 45 ** 3.6 )Ampelisca sarsi Chevreux, 1888 ) ) ) ) ) ) 2 ** 2.4 )Corophium acherusicum Costa, 1851 ) 2 ) ) ) ) ) ** 2.4 +

Corophium acutum Chevreux, 1908 ) 6 ) 14 30 1 ) ** 15.5 +

Elasmopus affinis (Della Valle, 1893) ) 1 ) ) ) 1 ) ** 2.4 )Elasmopus rapax A.Costa, 1853 ) ) ) 5 ) ) 2 ** 2.4 +

Erichthonius brasiliensis (Dana, 1855) ) ) ) ) ) ) 141 0.11 3.6 +

Jassa marmorata Holmes, 1903 ) ) ) ) ) ) ) ) ) +

Leucothoe serraticarpa Della Valle, 1893 ) ) ) ) ) ) 34 ** 3.6 )Maera grossimana Montagu, 1808 ) ) ) ) ) ) 11 ** 2.4 )Maera inaequipes (Costa, 1857) ) ) ) ) ) ) 19 ** 2.4 )Maera hamigera Haswell, 1880 ) ) ) ) ) ) ) ) ) +

Maera shiecki Karaman & Ruffo, 1971 ) ) ) ) ) ) 12 ** 2.4 )Microdeutopus gryllotalpa (Costa, 1853) ) ) ) ) ) ) 7 ** 2.4 )Microdeutopus sp. 1 ) ) ) ) ) ) ** 1.2 +

Pereinotus testudo (Montagu, 1808) ) ) ) ) ) ) 1 ** 1.2 )Phtisica marina Slabber, 1749 16 61 ) 10 149 9 6 0.19 23.8 +

Synchelidium haplocheles (Grube, 1864) ) ) ) ) ) ) 9 ** 7.1 )Synchelidium longidigitatum Ruffo, 1947 ) ) ) ) ) ) 5 ** 2.4 )Cymodoce tuberculata Costa in Hope, 1851 ) ) ) ) ) ) 4 ** 1.2 +

Gnathia vorax (Lucas 1849) ) ) ) ) ) ) 26 ** 3.6 )Leptochelia savignyi (Kroyer, 1842) ) ) ) ) ) ) 30 ** 2.4 )Iphinoe serrata Norman, 1867 2 4 7 5 1 ) 13 ** 15.5 )Iphinoe tenella (G. O. Sars, 1878) ) ) 1 ) 1 ) 5 ** 6 )Mesopodopsis slabberi (P. J. Van Beneden, 1861) ) 2 ) ) ) ) ) ** 2.4 )Paramysis helleri (G. O. Sars, 1877) ) ) ) 4 ) ) 4 ** 3.6 )Mysis sp. ) ) ) ) ) ) 1 ** 1.2 +

Squilla mantis Linne, 1758 ) ) ) ) ) ) ) ) ) +

Crangon crangon (Linne, 1758) ) ) ) ) ) ) ) ) ) +

Palaemon adspersus (Rathke, 1837) ) ) ) ) ) ) ) ) ) +

Melicertus kerathurus (Forskal, 1775) ) ) ) ) ) ) ) ) ) +

Sicyonia carinata (Brunnich, 1768) ) ) ) ) ) ) ) ) ) +

Galathea cenarroi (Zariquiey Alvarez, 1968) ) ) ) ) ) ) ) ) ) +

Upogebia pusilla (Petagna, 1792) ) ) ) ) ) ) 1 ** 1.2 )Brachynotus sexdentatus (Risso, 1827) 5 16 ) 12 3 ) 9 ** 32.1 +

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

234 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

Table 2. Continued.

Grab statıons

D% F% BT1 2 3 4 5 6 7

Carcinus aestuarii Nardo, 1847 ) ) ) ) ) ) ) ) ) +

Polybius vernalis (Risso, 1827) ) ) ) ) ) ) ) ) ) +

Pisidia bluteli (Risso, 1816) ) ) ) ) ) ) 1 ** 1.2 +

MOLLUSCA

Cerithium vulgatum Brugiere, 1792 ) ) ) ) 3 ) ) ** 1.2 )Bittium latreillii (Payraudeau, 1826) ) 2 ) ) 1 ) ) ** 3.6 )Bittium reticulatum (Da Costa, 1778) ) 48 1 ) 26 ) 13 ** 16.7 +

Bittium scabrum (Olivi, 1792) ) 1 ) ) ) ) ) ** 1.2 +

Skeneopsis sp. 3 1 3 ) 1 ) ) ** 4.8 )Alvania geryonia (Mardo, 1847 ex Chiereghini) ) 21 1 1 7 ) ) ** 10.7 )Crisilla semistriata (Montagu, 1808) ) ) ) ) 1 ) ) ** 1.2 )Pusillina lineolata (Michaud 1832) 5 5 3 ) 2 20 3 ** 21.4 +

Ventrosia ventrosa (Montagu, 1803) ) 1 ) ) ) ) ) ** 1.2 )Hyala vitrea (Montagu, 1803) ) ) ) ) ) ) 1 ** 1.2 )Aporrhais pespelecani (Linne, 1767) ) ) ) ) ) ) 2 ** 1.2 )Calyptraea chinensis (Linne, 1758) ) ) ) ) ) ) 1 ** 1.2 )Euspira guillemini (Payraudeau, 1826) ) 1 ) ) ) ) ) ** 1.2 )Euspira pulchella (Risso, 1826) ) ) ) ) ) ) 1 ** 1.2 )Monophorus perversus (Linne, 1758) ) 2 ) ) ) ) ) ** 2.4 )Cerithiopsis tubercularis (Montagu, 1803) ) 3 ) ) ) ) ) ** 1.2 )Epitonium commune (Lamarck, 1822) ) 1 ) ) 1 ) ) ** 2.4 )Eulima glabra (Da Costa, 1778) ) 7 ) ) ) ) ) ** 6 )Hexaplex trunculus (Linne, 1758) ) 3 ) ) ) ) ) ** 2.4 +

Cyclope neritea (Linne, 1758) ) ) ) ) ) ) ) ) ) +

Nassarius incrassatus (Stroem, 1768) ) 3 ) ) ) ) ) ** 1.2 )Nassarius pygmaeus (Lamarck, 1822) ) 58 ) 1 9 3 7 ** 19 +

Nassarius reticulatus (Linne, 1758) 2 2 ) ) ) 1 1 ** 7.1 +

Bela brachystoma (Philippi, 1844) 1 5 ) ) ) ) 1 ** 6 )Bela nebula (Montagu, 1803) 2 3 ) ) ) ) 1 ** 6 )Mangelia attenuata (Montagu, 1803) ) 4 ) ) ) ) 1 ** 2.4 )Mangelia nuperrima (Tiberi, 1855) ) 1 ) ) ) ) ) ** 1.2 )Mangelia unifasciata (Deshayes, 1835) ) 14 ) 1 3 ) 1 ** 11.9 )Acteon tornatilis (Linne, 1758) ) ) ) ) 1 ) ) ** 1.2 )Ringicula conformis (Monterosato, 1877) ) 1 ) ) ) ) ) ** 1.2 )Weinkauffia turgidula (Forbes, 1844) ) ) ) ) 1 ) ) ** 1.2 )Philine aperta (Linne 1767) 6 ) ) 1 ) ) ) ** 3.6 +

Nucula nitidosa Winckworth, 1931 1 2 ) ) 3 ) ) ** 6 )Lembulus pellus (Linne, 1758) ) 22 1 ) 5 ) ) ** 9.5 )Anadara demiri (Piani, 1981) 5 85 3 22 21 1 110 0.19 46.4 +

Mytilus galloprovincialis (Lamarck, 1819) 3 1 ) 2 2 3 2 ** 9.5 +

Modiolus barbatus (Linne, 1758) 3 ) 6 ) 2 ) ) ** 7.1 +

Modiolus adriaticus (Lamarck, 1819) ) ) ) ) ) 1 ) ** 1.2 )Modiolarca subpicta (Cantraine, 1835) ) ) ) ) ) ) ) ) ) +

Anomia ephippium Linne, 1758 1 14 ) 158 37 2 21 0.18 25 +

Mimachlamys varia (Linne, 1758 ) ) ) ) ) ) 1 ** 1.2 )Ctena decussata (Costa, 1829) ) 1 ) ) ) ) ) ** 1.2 )Lucinella divaricata (Linne, 1758) ) ) ) ) ) 1 ) ** 1.2 )Anadontia fragilis (Philippi, 1836) ) ) ) ) ) ) 2 ** 2.4 )Mysella bidentata (Montagu, 1803) 9 ) 5 78 4 17 99 0.16 20.2 +

Acanthocardia paucicostata (Sowerby, 1841) 6 ) 2 9 7 9 11 ** 25 +

Parvicardium exiguum (Gmelin, 1791) 1 3 ) 8 ) ) 1 ** 4.8 +

Cerastoderma glaucum (Poiret, 1789) 4 1 2 40 3 16 1 ** 27.4 +

Fulvia fragilis (Forsskal, 1775) ) ) ) 1 4 ) 2 ** 6 +

Spisula subtruncata (Da Costa, 1778) 5 1 2 27 13 11 9 ** 25 +

Tellina nitida Poli, 1791 ) 2 ) 3 1 ) ) ** 4.8 +

Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik, Dogan & Ozcan Zoobentos and exotics in

Alsancak Harbor

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 235

belonging to Actinaria (three species, 72 individuals),

Turbellaria (three species, four individuals), Nemertini

(eight species, 184 individuals), Nematoda (one species,

1295 individuals), Oligochaeta (two species, 257 individu-

als), Polychaeta (98 species, 116,991 individuals), Phoron-

ida (two species, 191 individuals), Crustacea (40 species,

757 individuals), Mollusca (62 species, 10,432 individu-

als), Echinodermata (five species, 48 individuals), and Tu-

nicata (seven species, 12 individuals). Grab samples

included more species (211 species) than beam-trawl sam-

ples (107 species) (Table 2). A total of 80 species were

found both in grab and beam-trawl samples. This study

added 17 new records to the inventory of the marine

fauna inhabiting the coasts of Turkey (see Table 2).

Polychaeta accounted for 90% of the total number of

specimens, followed by Mollusca (8%). The dominant

species in the area were Streblospio gynobranchiata (66%

of total individuals), Corbula gibba (6.6%), Pseudopolydo-

ra antennata (5.8%), Prionospio multibranchiata (4.8%),

Heteromastus filiformis (4.3%) and Capitella capitata

(3.7%), all comprising 92% of total specimens (Table 2).

The most frequent species (all belonging to Polychaeta)

in all grab samples were S. gynobranchiata (present in

95% of the samples), P. multibranchiata (92%), H. filifor-

mis (79%), Polydora cornuta (69%), Podarkeopsis galan-

gaui (69%), Prionospio fallax (68%) and P. antennata

(67%) (Table 2).

Mollusca accounted for 87% of the total biomass

(1891 g) in grab samples, followed by Polychaeta (4%)

and Tunicata (4%). The species with the highest individ-

ual biomass were A. demiri (38% of total biomass), Ceras-

toderma glaucum (16%), Anomia ephippium (15%) and C.

gibba (12%).

Temporal variations in number of individuals, num-

ber of species, biomass, and diversity and evenness val-

ues at all stations are presented in Figs 3 and 4. The

mean number of individuals encountered at all stations

was always high in April. Stations 1 and 2 showed the

highest number of individuals. Except at station 7,

community parameters at all stations varied significantly

between sampling periods (P < 0.01, see Figs 3 and 4,

and Table 3). However, temporal changes in diversity

values at stations 1, 3, and 7 were not statistically sig-

nificant (P > 0.05). No difference was found in the

value of biomass between time and the combined effect

of time and station (Table 3).

Table 2. Continued.

Grab statıons

D% F% BT1 2 3 4 5 6 7

Tellina pulchella Lamarck, 1818 ) 2 ) ) 1 1 6 ** 7.1 +

Abra alba (Wood, 1802) 74 9 36 28 34 47 32 0.2 41.7 +

Abra prismatica (Montagu, 1808) 8 2 7 9 5 1 14 ** 26.2 +

Gouldia minima (Montagu, 1803) ) ) ) ) ) ) 1 ** 1.2 +

Dosinia exoleta (Linne, 1758) ) 1 ) ) 1 ) 2 ** 3.6 )Dosinia lupinus (Linneaus, 1758) 1 10 ) 3 7 1 4 ** 19 )Pitar rudis (Poli, 1795) ) 1 ) ) ) 1 ) ** 2.4 )Paphia rhomboides (Pennant, 1777) 2 13 ) 18 20 19 18 ** 38 +

Sphenia binghami Turton, 1822 ) ) ) ) ) 1 3 ** 2.4 )Corbula gibba (Olivi, 1792) 1749 266 396 719 1567 3624 311 6.63 86.9 +

Dentalium inaequicostatum Dautzenberg 1891 ) 48 1 ) 10 1 5 ** 21.4 +

ECHINODERMATA

Astropecten spinulosus (Philippi, 1837) ) ) ) ) ) ) ) ) ) +

Amphipholis squamata (Delle Chiaje, 1829) ) ) ) ) ) ) 3 ** 1.2 )Brissopsis lyrifera (Forbes, 1841) ) ) ) ) ) ) 42 ** 9.5 )Psammechinus microtuberculatus (Blainville, 1825) ) ) ) ) ) ) 2 ** 1.2 )Holothuroidea (sp.) ) ) ) ) ) ) 1 ** 1.2 )TUNICATA

Ascidia mentula O. F. Muller, 1776 ) ) ) ) ) ) 4 ** 1.2 )Ciona intestinalis (Linne, 1767) ) ) ) ) ) ) ) ) ) +

Botryllus schlosseri (Pallas, 1766) ) ) ) ) 1 1 ) ** 2.4 )Phallusia mammilata (Cuvier, 1815) ) ) ) ) ) ) 1 ** 1.2 )*Pyura dura Heller, 1877 ) ) ) ) ) ) ) ) ) +

*Styela canopus Stimson, 1852 ) ) ) ) ) ) 1 ** 1.2 )*Styela plicata (Lesueur, 1823) ) ) ) 2 ) ) 2 ** 2.4 +

*Species that represent new records for the Turkish fauna; **species with a dominance value lower than 0.10%.

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

236 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

The highest biomass values were generally found at sta-

tions 4 and 7, because of the presence of C. glaucum

(max. 1138 gÆm)2 at station 4 in April) and Anadara

demiri (max. 3330 gÆm)2 at station 7 in April). The lowest

biomass values were encountered at stations 1 and 3,

which were dominated by small-sized polychaete species.

The highest number of species, and the highest diver-

sity and evenness were found at station 7, the lowest at

stations 1 and 3 (Fig. 4). The diversity value was always

higher than 3 at station 7, showing a relatively undis-

turbed or recovering condition. There were large differ-

ences in these variables among sampling periods, with

September having generally lower and April higher num-

ber of species.

Based on Bray–Curtis similarity values higher than

50%, five groups of stations (A–E) can be recognized

(Fig. 5). Six species were the most responsible for the

similarity between groups, which correspond quite well to

different sampling periods (Table 4). The density of S. gy-

nobranchiata was the main factor affecting the similarity

or dissimilarity of the samples taken in the whole area

(Table 4). ANOSIM detected a significant difference

Fig. 2. Sediment and water characteristics for each grab station during the various sampling periods.

Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik, Dogan & Ozcan Zoobentos and exotics in

Alsancak Harbor

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 237

(P < 0.05) between September and April, and June and

April (Table 5).

Spearman’s rank correlation analysis between the mean

scores of community parameters and the environmental

variables indicated that the number of species was posi-

tively (P < 0.05) correlated with the Secchi disk depth

(qr ¼ 0.40) and negatively with the percentage of carbon

in sediment (qr ¼ )0.40); the diversity index negatively

with the ammonium concentration (qr ¼ )0.38).

A total of six exotic species, all previously known from

the area, were collected. These were S. gynobranchiata, P.

cornuta, Hydroides dianthus, H. elegans, A. demiri, and

Fulvia fragilis. The importance of these exotic species in

terms of the number of individuals and biomass at all sta-

tions and in all sampling periods is shown in Fig. 3. The

majority of individuals collected at stations near Alsancak

Harbor belonged to these species (e.g. station 3 with 92%

of the individuals). There was a weak positive correlation

between the total density of exotic species and that of

native ones (Pearson’s correlation r ¼ 0.33, P < 0.05). A.

demiri occurred patchily in the area, reaching its highest

density at station 7 (580 indÆm)2) in April and station 2

(520 indÆm)2) in January. However, weights of specimens

of A. demiri found at station 7 were higher than those

found at station 2, accounting for 93% of the mean total

biomass at station 7 in January. The contribution of exo-

tic species to total biomass values at stations 1 and 6 was

negligible (Fig. 3), except for samples taken in September

at station 6 where exotics comprised 97% of the total bio-

mass. The correlation between the total biomass value of

exotics versus natives was positive and significant,

although low (qr ¼ 0.29, P < 0.05).

The density and biomass values of the exotics at all sta-

tions and in all periods are shown in Fig. 6. The mean

Fig. 3. Temporal fluctuations in the mean

faunal densities (number of individuals per

0.1 m)2) and biomass (g wet weight per

0.1 m2) with +1 standard error. Dark bars

show the mean density and biomass of exotic

species, and white bars those of native ones.

The percentage of exotics in the total faunal

density and biomass estimated at each station

is indicated on the bars. One-way ANOVA

was used to find out if the mean scores for

density and biomass are significant or not

with regard to sampling time at each station

(*P < 0.01, **P < 0.001, ns ¼ not

significant). Ja ¼ January; A ¼ April; J ¼June; S ¼ September.

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

238 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

density and biomass values of S. gynobranchiata and P.

cornuta attained their maximum levels in April at stations

1 and 2, and gradually diminished with increasing dis-

tance from the harbor (from station 1 to 7). As station 6

is located in Pasaport Harbor, the species also had high

abundance and biomass. The other exotic polychaetes, H.

dianthus and H. elegans, occurring at all stations, except

station 3, were found on living or dead bivalve shells

embedded in muddy substrates. They were abundant at

stations 7 and 4 where shells of large bivalves A. demiri

and A. ephippium occurred. There were two density and

biomass peaks for A. demiri at stations 2 (520 indÆm)2;

680 gÆm)2 in January) and 7 (580 indÆm)2; 3330 gÆm)2 in

April). Fulvia fragilis was found only at stations 4, 5, and

Fig. 4. Temporal fluctuations in the mean

number of species, diversity index and

evenness index at each station, with +1

standard error. One-way ANOVA was used to

find out if the mean values of these

parameters are significant according to

sampling time at each station (*P < 0.01,

**P < 0.001, ns ¼ not significant).

Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik, Dogan & Ozcan Zoobentos and exotics in

Alsancak Harbor

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 239

7, with the highest density and biomass at stations 5

(20 indÆm)2, 2.5 gÆm)2 in April) and 7 (20 indÆm)2,

0.1 gÆm)2 in June).

Spearman’s rank correlation between abundances of the

six exotic species and abiotic variables indicated that the

number of individuals of P. cornuta was significantly

(P < 0.05) and negatively correlated with pH (qr ¼)0.42) and positively correlated with the silicate concen-

tration (qr ¼ 0.43); S. gynobranchiata was negatively cor-

related with the salinity (qr ¼ )0.39), and positively with

ammonium (qr ¼ 0.50) and silicate (qr ¼ 0.63) concen-

trations; A. demiri was negatively correlated with the per-

centage of carbon in sediment (qr ¼ )0.39).

No correlation was estimated between densities of each

exotic species and those of natives while abundance of H.

dianthus was well correlated with that of A. demiri (qr ¼0.63, P < 0.05), and abundance of H. elegans with that of

A. ephippium (qr ¼ 0.65, P < 0.05).

The reproductive periods of S. gynobranchiata and P.

cornuta occurred throughout the year, with maximum

oocyte diameter being calculated as 120 lm (mean ± SE ¼91 lm ± 2.89, n ¼ 15) in January for S. gynobranchiata

and as 60 lm (53 lm ± 1.05, n ¼ 20) for P. cornuta.

Oocytes within coelomic cavities of H. dianthus (max.

diameter ¼ 65 lm, mean ± SE ¼ 56 lm ± 1.35, n ¼ 15)

Table 3. Result of two-way ANOVA of the community parameters.

sources of variation df

number of

species

(C ¼ 0.346**)

number of

individuals

(C ¼ 0.361***)

evenness

index (J¢)(C ¼ 0.323***)

diversity

index (H¢)(C ¼ 0.152*)

biomass

(C ¼ 0.811***)

MS P MS P MS P MS P MS P

stations 6 1408.3 *** 3,119,553 *** 0.099 *** 6.83 *** 7092.4 *

post hoc test All 7 7 3, 7 7

sampling periods 3 1844.1 *** 40,452,695 *** 0.093 *** 1.03 *** 5196.8 ns

post hoc test All A A, S J, S ns

stations · periods 18 67.3 ns 2,153,805 *** 0.122 *** 1.43 *** 2122.6 ns

residual 56 38 618,929 0.010 0.14 2445.4

*P < 0.05; **P < 0.01; ***P < 0.001.

MS ¼ mean square; df ¼ degrees of freedom; C ¼ Cochrane’s test; ns ¼ not significant.

Post hoc test (Tukey’s HSD) shows the stations and sampling periods which determine statistical differences.

Fig. 5. Multidimensional scaling plot showing the similarity among

temporal samples. Associations were determined according to the

results of Bray–Curtis similarity analysis (each association has a similarity

higher than 50%). Ja ¼ January; A ¼ April; J ¼ June; S ¼ September.

Table 4. Species contributing to similarity among sampling periods,

and their average similarity.

average similarity

September June April January

29 MD 32 MD 50 MD 40 MD

Prionospio

multibranchiata

10 1220 4 1160 5 4300 12 2320

Pseudopolydora

antennata

– – 12 4340 5 5820 – –

Streblospio

gynobranchiata

70 9270 45 10770 72 74390 78 27730

Heteromastus

filiformis

11 1420 19 4690 – – – –

Capitella capitata – – – – 4 4940 – –

Corbula gibba – – 12 2030 6 8730 – –

Bold numbers indicate the highest score of species contribution in

each assemblage.

MD ¼ mean density (individuals Æm)2).

Table 5. The result of ANOSIM testing for differences among samp-

ling periods.

months R-value P-value

September versus June 0.07 ns

September versus April 0.43 *

September versus January 0.09 ns

June versus April 0.36 *

June versus January 0.16 ns

April versus January 0.23 ns

*P < 0.05; ns ¼ not significant.

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

240 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

and H. elegans (max. diameter ¼ 50 lm, mean ± SE ¼40.4 lm ± 0.96, n ¼ 15) were only found in June. No

reproductive individuals of A. demiri and F. fragilis were

observed.

Discussion

Analysis of benthic samples showed that the investigated

area has a diverse benthic fauna with a total number of

231 species. The innermost part of Izmir Bay was previ-

ously known to be one of the most polluted regions in

Turkey (Geldiay & Ergen 1972; Ergen 1979; Geldiay et al.

1979; Kocatas et al. 1987; Kocak et al. 1999). Azoic condi-

tions (Dogan et al. 2005; based on the material collected

in 1995 and 1996) and odorous biogenic sulfurous gases

(Muezzinoglu et al. 2000) were reported in the area in

the 1980s and 1990s. The muddy bottom of the area was

previously dominated only by opportunistic species such

as Capitella capitata, Malacoceros fuliginosus, Prionospio

fallax, and Ophiodromus pallidus (Ergen 1979; Dogan

et al. 2005). However, an improvement in the environ-

mental quality of the bay was anticipated once a new

wastewater treatment plant came into operation in early

2000. Ergen et al. (2006) examined the benthic materials

collected periodically in the area between 1997 and 2002

and showed such an improvement in 2002. In this year,

no azoic condition occurred in the area, even in summer,

and polychaetes other than pollution indicators were also

encountered. The present study also observed several spe-

cies such as Syllis garciai, Owenia fusiformis, Squilla man-

tis, Melicertus kerathurus, and Amphipholis squamata in

and around Alsancak Harbor, which are sensitive to

Fig. 6. Temporal fluctuations of the mean values of density and biomass of exotic species found at stations with +1 standard error (Ja ¼ January;

A ¼ April; J ¼ June; S ¼ September).

Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik, Dogan & Ozcan Zoobentos and exotics in

Alsancak Harbor

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 241

intense pollution. The number of species near Alsancak

Harbor (stations 1–5) ranged between seven (station 3, in

September) and 70 (station 2, April). The station farthest

from Alsancak Harbor (station 7) had a rich faunal com-

ponent, comprised of 107 species in April. Kocatas et al.

(1987) reported that 20 zoobenthic species inhabited the

area surrounding Alsancak Harbor in 1974; however, only

nine species were recorded in 1983. Ergen et al. (2006)

found azoic conditions near Alsancak Harbor (station 5

in the present study) every summer (except for 2002).

The number of species found at this station in our study

ranged from 17 (January) to 41 (April). In this survey, we

reported 231 soft-bottom benthic organisms in the inner

part of Izmir Bay, whereas only 21 species were reported

by Kocatas (1980), 23 species by Palaz (1989), 14 poly-

chaete species by Ergen (1992) and nine species by Dogan

et al. (2005). This result clearly shows that there has been

an environmental improvement, possibly because of the

beneficial effect of the treatment plant in reducing pol-

lution and making the area more favorable, even in sum-

mer, for the settlement of benthic organisms.

The chemical analyses of water and sediment samples

during this study also showed that there was a decline in

the concentrations of nitrite, nitrate, and ammonium over

time, especially after the establishment of the wastewater

treatment plant in 2000. The concentration of ammo-

nium in surface water, which was the dominant nitrogen

source in the area, was reported to reach maximum levels

of 42.4 lgatÆl)1 in 1987 (Uysal & Yaramaz 1987),

65.7 lgatÆl)1 in 2000 (Kaymakci et al. 2000), 50 lgatÆl)1

in 2001 (Kontas et al. 2004) and 20.5 lgatÆl)1 (mean ± -

SE ¼ 3.3 ± 0.8 lgatÆl)1) in 2004 (this study). However,

the concentration of phosphate phosphorus, which is an

important source of eutrophication in the bay (Kucuksez-

gin et al. 2001), remained relatively unchanged over the

years, possibly because of the effects of the polluted

creeks’ discharge into the area; max. 5.58 lgatÆl)1 in 1987

(Uysal & Yaramaz 1987), 10 lgatÆl)1 in 2001 (Kontas

et al. 2004) and 5.9 lgatÆl)1 in 2004 (this study). Simi-

larly, Kontas et al. (2004) pointed out that the capacity of

the wastewater plant was sufficient for removal of nitro-

gen from wastes, whereas it was inadequate for the

removal of phosphate. Similar results were also seen in

terms of the percentage of carbon in sediments in that

the highest levels were found in this present study (max.

27%) when compared with the previous study undertaken

by DEU (1997) (7%). The main reason for this difference

might be that in this study, the harbor environment

where the water circulation is weaker and the sedimenta-

tion is higher was also sampled.

In the present study, a clear temporal trend in the

abundance of benthic organisms, with peaks during April,

followed by a striking decline throughout June and

September was determined. At all stations (except for sta-

tion 7), the mean values of community parameters varied

significantly, showing the effects of sampling time, especi-

ally in the more polluted areas. In April, the benthic

assemblages were characterized by having a high number

of juveniles and a high percentage of reproducing speci-

mens belonging to the dominant species such as Streblos-

pio gynobranchiata, Capitella capitata, Pseudopolydora

antennata, Prionospio multibranchiata, and Corbula gibba.

Sarda et al. (1999) found a similar result in the abun-

dance and biomass of macroinfaunal assemblages at sub-

littoral stations of the Bay of Blanes, with peaks during

spring, and concluded that the reproductive cycle of most

species was the main factor affecting density fluctuations

in time. The temporal dynamics of the benthic fauna was

reported to be influenced by the availability of food and

the presence of predators (Sarda et al. 1995). However,

Oug (2000) examined the soft-bottom macrofauna from

fjords of northern Norway during 1979–1982 and repor-

ted that species number and densities varied stochastically

with peak values occurring at different times of the year.

He concluded that the lack of a temporal pattern was

mainly because of the stable physical conditions and the

irregular nutrient input in the fjord basin. This assump-

tion could also be applied to this study because of the

fact that community parameters show significant tem-

poral differences at stations in or around Alsancak Har-

bor (stations 1–6), where marked fluctuations in

environmental variables were observed in time. In con-

trast, the community parameters at station 7, which is

relatively far from pollution sources, did not show any

significant differences. In addition, the mean score for the

diversity index was always <3 at stations 1–6 (except for

station 2 in January), whereas it was always >3 at station

7. Low values of the diversity index indicate that the

majority of the study area could still be considered as an

impacted environment.

The community parameters were also affected by the

environmental factors. For example, the number of spe-

cies was negatively correlated with percentage of carbon

in sediment and positively correlated with transparency

(Secchi disk depth). A negative correlation was found

between diversity values and the ammonium concentra-

tion, which had higher values in January at stations near

Alsancak Harbor. Bourget et al. (2003) clearly showed

that water temperature and transparency, plus in some

cases primary production, were the variables having a sig-

nificant influence on the total biomass of epibenthic

assemblages in the Gulf of St. Lawrence. Je et al. (2003)

showed the importance of DDT, low aromatic hydrocar-

bons, lindane and grain size in the distribution of benthic

organisms in Vancouver Harbor. Similarly, pollution gra-

dient and granulometric parameters were reported to be

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

242 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

the main factors affecting polychaete distribution in a

harbor at Ceuta located in the Strait of Gibraltar (Guerra-

Garcıa & Garcıa-Gomez 2004). In the present study, the

significant difference in community parameters between

sampling periods and stations suggests that benthic com-

munities occurring in and near Alsancak Harbor were

dynamic and greatly affected by both environmental fac-

tors, and biological and ecological features of organisms.

Soft sediments in and around Alsancak Harbor have

been exposed to an intense invasion by two spionid poly-

chaetes, S. gynobranchiata and Polydora cornuta, which

were previously known from the area (Cinar et al. 2005).

The morphological, biometric, and reproductive features

of populations of these two species in this area were given

by Cinar et al. (2005). The importance of these two spe-

cies was high, they constituted more than 90% of faunal

populations in the majority of samples collected at sta-

tions 1–5. However, their biomass was low because of

their small body sizes (largest 8.3 mm long). Streblospio

gynobranchiata was previously reported not only from the

western Atlantic Ocean in muddy sand at a depth of 1 m,

but also in estuarine areas (Rice & Levin 1998). The first

appearance of this species in the inner part of Izmir Bay

was in 2002 when the azoic conditions disappeared. The

population density of this species was reported to be very

low in its type locality; while its density in this survey

reached up to 60,480 indÆm)2 at station 1 in April.

Organically polluted sediments of the inner part of Izmir

Bay seem to provide a suitable habitat for settlement and

growth. The reproductive period for the species in the

area continued throughout the year. This species together

with P. cornuta, Anadara demiri and Fulvia fragilis might

have been introduced to the area via ballast water. Evi-

dence for this includes: (i) a huge gap in their distribu-

tional patterns, (ii) their absence from previous material

taken from the area, which has been continuously monit-

ored since the 1970s, and (iii) the extensive maritime traf-

fic present from different parts of the world.

Polydora cornuta, which is apparently a cosmopolitan

species (Radashevsky 2005), was first reported from the

Valencia Harbor (Spain) in the Mediterrranean Sea (Tena

et al. 1991), and subsequently from Izmir Bay (Cinar

et al. 2005) and the Black Sea (Radashevsky 2005). Previ-

ous studies performed in the Mediterranean Sea cited P.

ciliata as one of the dominant species from polluted envi-

ronments (Ergen 1979; Magni et al. 2004). As taxonomic

confusion exists for species of Polydora, some previous

records of P. ciliata from the polluted soft sediments of

the Mediterranean Sea might indeed be P. cornuta. This

species was also one of the dominant species in the area

near Alsancak Harbor and reproduced continuously

throughout the year, suggesting that it has acclimatized

well in the region.

Hydroides dianthus and H. elegans were found to be

encrusted on shells of the bivalves A. ephippium and A.

demiri, and reached their maximum densities at station 7

where these bivalve species occurred. They dominate arti-

ficial hard substrates in polluted environments of the

Mediterranean Sea (Kocak et al. 1999).

The exotic bivalve A. demiri has been known from

Izmir Bay since the 1970s (Demir 1977). It was previously

found at densities of 300 indÆm)2 on gray mud,

30 indÆm)2 on black mud (Demir 1977), and 180 indÆm)2

in the polluted bottom of Thessaloniki Bay at 15–22 m

(Zenetos 1994). Our findings showed that this species

preferred semi-polluted bottoms and was negatively cor-

related with the percentage of carbon in sediment (qr ¼)0.39).

Fulvia fragilis, which is a Lessepsian bivalve, was

recently reported from Izmir Bay (Ozturk & Poutiers

2005) and is known both in the eastern and western

Mediterranean Sea (Ozturk & Poutiers 2005). These

authors emphasized that its introduction into Izmir Bay

was most probably via ballast waters, and found a dense

population at station 4 collected using a beam trawl in

July 2003.

The impact of exotics on benthic community structure

in the inner part of Izmir Bay was clear, contributing to

the majority of specimens and biomass in all sampling

periods. Streblospio gynobranchiata is the key species

responsible for the similarity/dissimilarity levels of benthic

samples in all periods. The occurrence and abundance of

this species do not seem to interfere with the pattern of

distribution and abundance of other species. Ranasinghe

et al. (2005) outlined a similar finding in a southern Cali-

fornia embayment in that abundance of exotics was posi-

tively correlated with the abundance and richness of other

species and that exotics did not have a negative impact

on the overall community, possibly because of the bio-

genic structures built by them. The wealth of detritus

material in the inner part of Izmir Bay might hinder any

possible competition between species and the still pol-

luted conditions restrict the settlement of pollution-sensi-

tive species, which have greater competitive abilities. This

was more evident at station 7, where exotic spionids had

very low abundances as they were probably out-competed

from the area by the natives.

Extreme anthropogenic disturbance may create a mis-

match between the traits of native species and their

environment, so that some invading species are as well

adapted to the altered environment as are the compet-

ing native species (Byers 2002). These disturbances

increase invasion success not only by creating new

microhabitats, introducing propagules, and decreasing

the populations of native species that can resist inva-

sion, but also by weakening the ‘per capita’ ability of

Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik, Dogan & Ozcan Zoobentos and exotics in

Alsancak Harbor

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 243

native biota to resist invaders (Kocak et al. 1999; Byers

2002). A recent study of macrofouling organisms dis-

covered many more species in a polluted rather than a

non-polluted marina, and that the exotic serpulid H.

elegans, which made up 65% of the population in the

polluted marina, was occasionally found in the non-

polluted marina (Kocak et al. 1999). A healthy pristine

community represents a natural barrier to bio-invasion

and thus environmental conservation plays a fundamen-

tal role in preventing further spread of non-indigenous

species (Occhipinti-Ambrogi & Savini 2003). Holeck

et al. (2004) also demonstrated that previous introduc-

tions of exotics can facilitate the introduction and suc-

cess of subsequent arrivals. Therefore, halting the

introduction of any one exotic (e.g. through control of

ballast water discharge and other vectors) can inhibit a

potentially larger number of other invaders whose suc-

cess and impact are magnified by that species.

The present study shows that the pollution intensity in

the area greatly diminished after the establishment of a

wastewater plant, facilitating the settlement of many

native and exotic species in the area. The exotics invaded

the soft sediments near Alsancak Harbor and played an

important role in the benthic community structure.

Conclusions

The soft-bottom samples collected from several stations

(seven with van Veen grab and three with beam trawl)

in and around Alsancak Harbor, in various periods

between January and September 2004, included a total

of 231 zoobenthic species, 17 of which are new records

for the Turkish coast. The collection included six exotic

species: Streblospio gynobranchiata, Polydora cornuta,

Hydroides dianthus, H. elegans, Anadara demiri and Ful-

via fragilis which were previously known from the area.

The area was also highly colonized by opportunistic

species such as Capitella capitata and Corbula gibba. In

general, polychaetes were the dominant benthic compo-

nents in the area, accounting for 90% of the total

faunal populations, followed by mollusks (8%). The

most dominant species in the area was the exotic spe-

cies S. gynobranchiata (66% of the total individuals),

which contributed extensively to the similarity or dissi-

milarity of stations in time. Community parameters

varied significantly between periods and stations. April

was characterized by relatively high species richness and

dense populations of some species. The importance of

exotics in benthic fauna diminished when the distance

from the harbor increased. Community and chemical

analyses showed that, where azoic conditions had been

previously reported, recovery had occurred after the

establishment of a wastewater treatment plant in the

area in 2000. However, relatively low values of diversity

(H¢ < 3) at stations near Alsancak Harbor indicated

that the area still suffers from the pollution impact.

Acknowledgements

We are much indebted to Dr. Christer Erseus (Sweden)

for the identification of oligochaetes, to Dr. Dimitris Vaf-

idis (Greece) for the identification of actinarians, to Drs.

Juan Junoy (Spain) and Jon L. Norenberg (USA) for the

identification of nemerteans, to Dr. Duane Hope (USA)

for the identification of the nematode Enoplus meridional-

is, to Dr. Alfonso Ramos (Spain) for the identification of

ascidian species, to two anonymous referees for their con-

structive comments on the manuscript, and to personnel

of R/V EGESUF for their help in collecting the benthic

material. This work has been financially supported by Sci-

entific Research Projects of Ege University (Project num-

ber: 03 SUF 005).

References

Bourget E., Ardisson P.-L., Lapointe L., Daigle G. (2003) Envi-

ronmental factors as predictors of epibenthic assemblage

biomass in the St. Lawrence system. Estuarine, Coastal and

Shelf Science, 57, 641–652.

Byers J.E. (2002) Impact of non-indigenous species on natives

enhanced by anthropogenic alteration of selection regimes.

Oikos, 97, 449–458.

Cinar M.E., Ergen Z. (2005) Lessepsian migrants expanding

their distributional ranges; Pseudonereis anomala (Polychaet-

a: Nereididae) in Izmir Bay (Aegean Sea). Journal of the

Marine Biological Associations of the United Kingdom, 85,

313–321.

Cinar M.E., Ergen Z., Dagli E., Petersen M.E. (2005) Alien spe-

cies of spionid polychaetes (Streblospio gynobranchiata and

Polydora cornuta) in Izmir Bay, eastern Mediterranean. Jour-

nal of Marine Biological Associations of the United Kingdom,

85, 821–827.

Clarke K.R., Warwick R.M. (2001) Change in marine communi-

ties: an approach to statistical analysis and interpretation, 2nd

edition. PRIMER–E, Plymouth.

Cohen A.N., Carlton J.T. (1998) Accelerating invasion rate in

a highly invaded estuary. Science, 279, 555–557.

Demir M. (1977) On the presence of Arca (Scapharca) amygd-

alum Philippi, 1847 in the harbour of Izmir, Turkey. Istan-

bul Universitesi Fen Fakultesi Mecmuasi Serisi, 42, 197–202.

DEU (1997) Izmir Korfezi 1994–1995 Deniz Arastirmalari Yillik

Raporu. Deniz Bilimleri ve Teknolojisi Enstitusu Projesi, In-

ciralti: 98 pp.

Dogan A., Cinar M.E., Onen M., Ergen Z., Katagan T. (2005)

Seasonal analysis of soft bottom zoobenthic communities in

polluted and unpolluted areas of Izmir Bay (Aegean Sea).

Senckenbergiana Maritima, 35, 133–145.

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

244 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

Elton C.S. (1958) The ecology of invasions by animals and

plants. The University of Chicago Press, Chicago: 181 pp.

Ergen Z. (1976) Izmir Korfezi ve civari poliketleri uzerine tak-

sonomik ve ekolojik arastirmalar. Ege Universitesi Fen Fakul-

tesi Ilmi Raporlar Serisi, 209, 1–73.

Ergen Z. (1979) _Izmir Korfezi’nin Pollusyonunun Poliket

(Polychaeta-Annelida) Populasyonunun Dagilimi Uzerine

Etkileri. TUJJB Yayinlari, 11, 77–82.

Ergen Z. (1992) The latest status of Polychaeta in the soft sub-

strate of Izmir Bay. Rapport de la Commission International

Exploration de la Mer Mediterranee, 33,36.

Ergen Z., Cinar M.E., Dagli E., Kurt G. (2006) Seasonal

dynamics of soft-bottom polychaetes in Izmir Bay (Aegean

Sea, eastern Mediterranean). Scientia Marina, in press.

Erguvanli K. (1995) Muhendislik Jeolojisi. Sec Yayin Dagitim, 4.

Baski, _Istanbul: 590 pp.

Gaudette H.E., Flight W.R., Toner L., Folger W. (1974) An in-

expensive titration method for the determination of organic

carbon in recent sediments. Journal of Sedimentary Petrology,

44, 249–253.

Geldiay R., Ergen Z. (1972) Deniz biyolojisi arastirma labo-

ratuvari onundeki bentik poliket faunasi uzerinde on musa-

hedeler. Ege Universitesi Fen Fakultesi _Ilmi Raporlar Serisi,

134, 1–10.

Geldiay R., Ergen Z., Kocatas A. (1979) Some effects of

pollution on the benthic communities of the soft subtrate in

the Gulf of Izmir (Turkey). Rapport de la Commission

International Exploration de la Mer Mediterranee, 25/26,

193–194.

Guerra-Garcıa J.M., Garcıa-Gomez J.C. (2004) Polychaete

assemblages and sediment pollution in a harbour with two

opposing entrances. Helgolander Marine Research, 58, 183–

191.

Holeck K.T., Mills E.L., McIsaac H.J., Dochoda M.R., Colautti

R.I., Ricciardi A. (2004) Bridging troubled waters: biological

invasions, transoceanic shipping, and the Laurentian Great

Lakes. BioScience, 54, 919–929.

Je J.G., Belan T., Levings C., Koo B.J. (2003) Changes in ben-

thic communities along a presumed pollution gradient in

Vancouver Harbour. Marine Environmental Research, 57,

121–135.

Kaymakci A., Sunlu U., Egemen O. (2000) Assessment of

nutrient pollution caused by land based activities in Izmir

Bay, Turkey. Meeting on Interdependency between Agriculture,

Urbanization: Conflicts on Sustainable Use of Soil, Water,

Tunisia: 41–49.

Kocak F., Ergen Z., Cinar M.E. (1999) Fouling organisms and

their developments in a polluted and an unpolluted marina

in the Aegean Sea (Turkey). Ophelia, 50, 1–20.

Kocatas A. (1980) Evolution cyclique du Benthos dans les zones

de pollution du golfe d’Izmir (Turquie). Ves Journees Etude

Pollutions. Rapport de la Commission International Explora-

tion de la Mer Mediterranee, Cagliari: 643–648.

Kocatas A., Ergen Z., Katagan T. (1987) Changes in the

benthic communities due to various pollutants in Izmir Bay

(Turkey). FAO Fisheries Report Number, 352(Suppl.), 112–

122.

Kontas A., Kucuksezgin F., Altay O., Uluturhan E. (2004)

Monitoring of eutrophication and nutrient limitation in

Izmir Bay (Turkey) before and after wastewater treatment

plant. Environmental International, 29, 1057–1062.

Kucuksezgin F., Kontas A., Altay O., Uluturhan E. (2001) Eutro-

phication in Izmir Bay (eastern Aegean): nutrient limitation

and monitoring of long-term effects. Rapport de la Commission

International Exploration de la Mer Mediterranee, 36, 397.

Magni P., Micheletti S., Casu D., Floris A., De Falco G., Cas-

telli A. (2004) Macrofaunal community structure and distri-

bution in a muddy coastal lagoon. Chemistry and Ecology,

20, 397–409.

Morello E., Solustri C. (2001) First record of Anadara demiri

(Piani, 1981) (Bivalvia: Arcidae) in Italian waters. Bollettino

Malacologico, 37, 231–234.

Muezzinoglu A., Sponza D., Koken I., Alparslan N., Akyarli A.,

Ozture N. (2000) Hydrogen sulfide and odour control in

Izmir Bay. Water, Air and Soil Pollution, 123, 245–257.

Occhipinti-Ambrogi A., Savini D. (2003) Biological invasions

as a component of global change in stressed marine ecosys-

tems. Marine Pollution Bulletin, 46, 542–551.

Oug E. (2000) Soft-bottom macrofauna in the high-latitude

ecosystem of Balsfjord, northern Norway: species composi-

tion, community structure and seasonal variability. Sarsia,

85, 1–13.

Ozturk B., Poutiers J.-M. (2005) Fulvia fragilis (Bivalvia:

Cardiidae): a Lessepsian mollusk species from Izmir Bay

(Aegean Sea). Journal of Marine Biological Associations of the

United Kingdom, 85, 351–356.

Palaz M. (1989) _Izmir Korfezi’nin ic bolgesindeki zoobentozun

dinamikleri. Yuksek Lisans Tezi, 9 Eylul Universitesi: 37 pp.

Parsons T.R., Matia Y., Lalli C.M. (1984) A manual of chemical

and biological methods for seawater analysis. Pergamon Press,

New York: 173 pp.

Quatrefages A. (1865) Histoire naturelle des Anelees d’eau

douce et marin. Paris, 1, 1–588.

Radashevsky V.I. (2005) On adult and larval morphology of

Polydora cornuta Bosc, 1802 (Annelida: Spionidae). Zootaxa,

1064, 1–24.

Ranasinghe J.A., Mikel T.K., Velarde R.G., Weisberg S.B.,

Montagne D.E., Cadien D.B., Dalkey A. (2005) The

prevalence of non-indigenous species in southern Califor-

nia embayments and their effects on benthic macroinver-

tebrate communities. Biological Invasions, 7, 679–686.

Rice S.A., Levin L.A. (1998) Streblospio gynobranchiata, a

new spionid polychaete species (Annelida: Polychaeta)

from Florida and the Gulf of Mexico with an analysis of

phylogenetic relationships within the genus Streblospio.

Proceedings of the Biological Society of Washington, 111,

694–707.

Sarda R., Martin D., Pinedo S., Dueso A., Cardell M.J. (1995)

Seasonal dynamics of shallow soft-bottom communities in

western Mediterranean. In: Eleftheriou A., Ansell A.D.,

Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik, Dogan & Ozcan Zoobentos and exotics in

Alsancak Harbor

Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd 245

Smith C.J. (Eds), The biology and ecology of shallow coastal

waters. Olsen and Olsen, Fredensborg: 191–198.

Sarda R., Pinedo S., Martin D. (1999) Seasonal dynamics of

macroinfaunal key species inhabiting shallow soft-bottoms

in the Bay of Blanes (NW Mediterranean). Acta Oecologica,

20, 315–326.

Shea K., Chesson P. (2002) Community ecology theory as a

framework for biological invasions. Trends in Ecology and

Evolution, 17, 170–176.

Tena J., Capaccioni-Azzati R., Porras R., Torres-Gavila F.J.

(1991) Cuatro especies de poliquetos nuevas para las costas

Mediterraneas en los sedimentos del antepuerto de Valencia.

Miscellania Zoologica, 15, 29–41.

UNEP (1994) Integrated management study for the area of

Izmir. MAP Technical Reports Series No. 84, United

Nations Environmental Programme, Split: 1–130. pp.

Uysal H., Yaramaz O. (1987) Izmir Korfezi’nin farkli

bolgelerinde bazi polluantlarin mukayeseli olarak

arastirilmasi. CEVRE 87 Symposium, EBSO, Izmir.

Vitousek P.M., D’Antonio C.M., Loope L.L., Rejmanek M.,

Westbrooks R. (1997) Introduced species: a significant com-

ponent of human-caused global change. New Zealand Jour-

nal of Ecology, 21, 1–16.

Wonham M.J., Carlton J.T. (2005) Trends in marine biolo-

gical invasions at local and regional scales: the Northeast

Pacific Ocean as a model system. Biological Invasions, 7,

369–392.

Zenetos A. (1994) Scapharca demiri (Piani, 1981): first finding

in the North Aegean Sea. La Conchiglia, 271, 37–38.

Zenetos A., Gofas S., Russo G.F., Templado J. (2003) CIESM

atlas of exotic species in the Mediterranean. Volume 3. Mol-

luscs. CIESM Publishers, Monaco: 376 pp.

Zibrowius H. (1971) Les especes Mediterraneennes du genre

Hydroides (Polychaete Serpulidae) remarques sur le preten-

du polymorphisme de Hydroides uncinata. Tethys, 2, 691–

745.

Zoobentos and exotics in Alsancak Harbor Cinar, Katagan, Ozturk, Egemen, Ergen, Kocatas, Onen, Kirkim, Bakir, Kurt, Dagli, Kaymakci, Acik,

Dogan & Ozcan

246 Marine Ecology 27 (2006) 229–246 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd