Assessment of marine pollution in Izmir Bay: Nutrient, heavy metal and total hydrocarbon concentrations

Environment International 32 (2006) 41 – 51 www.elsevier.com/locate/envint

Assessment of marine pollution in Izmir Bay: Nutrient, heavy metal and total hydrocarbon concentrations F. KucuksezginT, A. Kontas, O. Altay, E. Uluturhan, E. DarNlmaz Dokuz Eylul University, Institute of Marine Sciences and Technology, InciraltN, 35340-Izmir, Turkey Received 15 December 2004; accepted 13 April 2005 Available online 1 July 2005

Abstract Izmir Bay (western Turkey) is one of the great natural bays of the Mediterranean. Izmir is an important industrial and commercial centre and a cultural focal point. The main industries in the region include food processing, oil, soap and paint production, chemical industries, paper and pulp factories, textile industries and metal processing. The mean concentrations showed ranges of 0.01 – 0.19 and 0.01 – 10 AM for phosphate, 0.10 – 1.8 and 0.12 – 27 AM for nitrate + nitrite, and 0.30 – 5.8 and 0.43 – 39 AM for silicate in the outer and middle – inner bays, respectively. The TNOx /PO4 ratio is significantly lower than the Redfield’s ratio and nitrogen is the limiting element in the middle – inner bays. Diatoms and dinoflagellates were observed all year around in the bay and are normally nitrogen limited. Metal concentrations ranged between Hg: 0.05 – 1.3, Cd: 0.005 – 0.82, Pb: 14 – 113 and Cr: 29 – 316 Ag g 1 in the sediments. The results showed significant enrichments during sampling periods from Inner Bay. Outer and middle bays show low levels of heavy metal enrichments except estuary of Gediz River. The concentrations of Hg, Cd and Pb in the outer bay were generally similar to the background levels from the Mediterranean. The levels gradually decreased over the sampling period. Total hydrocarbons concentrations range from 427 to 7800 ng g 1 of sediments. The highest total hydrocarbon levels were found in the inner bay due to the anthropogenic activities, mainly combustion processes of traffic and industrial activities. The concentrations of heavy metals found in fish varied for Hg: 4.5 – 520, Cd: 0.10 – 10 and Pb: 0.10 – 491 Ag kg 1 in Izmir Bay. There was no significant seasonal variation in metal concentrations. An increase in Hg concentration with increasing length was noted for Mullus barbatus. A person can consume more than 2, 133 and 20 meals per week of fish in human diet would represent the tolerable weekly intake of mercury, cadmium and lead, respectively, in Izmir Bay. Heavy metal levels were lower than the results in fish tissues reported from polluted areas of the Mediterranean Sea. D 2005 Elsevier Ltd. All rights reserved. Keywords: Heavy metals; Nutrients; Total hydrocarbons; Sediment; Fish; Bioaccumulation; Izmir Bay

1. Introduction Izmir Bay (western Turkey) is one of the great natural bays of the Mediterranean. The main urban conurbation around the bay is the Izmir Metropolitan Municipality, covering 88,000 ha. Izmir is an important industrial and commercial centre and a cultural focal point. The bay has a total surface area of over 500 km2, water capacity of 11.5 billion m3, a total length of 64 km and opens in the Aegean Sea. The depth of water in the outer bay is about * Corresponding author. Tel.: +90 232 278 55 65; fax: +90 232 278 50 82. E-mail address: [email protected] (F. Kucuksezgin). 0160-4120/$ - see front matter D 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.envint.2005.04.007

70 m and decreases towards to the Inner Bay. The bay has been divided into three sections (outer, middle and inner) according to the physical characteristics of the different water masses. The middle bay is separated from the inner bay by a 13 m deep sill the Yenikale Strait. The Gediz River, which flows to the northern part of the bay, is the second biggest river along the eastern Aegean coast. Gediz River is densely populated and includes extensive agricultural lands and numerous manufacturing, food and chemical industries. The streams and hundreds of small domestic discharge outlets, flow to the bay. The main industries in the region include food processing, beverage manufacturing and

42

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51

bottling, tanneries, oil, soap and paint production, chemical industries, paper and pulp factories, textile industries, metal processing and timber processing. Nutrient oligotrophic or eutrophic conditions have been characterized as the principal factors affecting the marine ecosystem (Ryther and Dunstan, 1971). Several studies in the past have associated oligotrophy with the absence of measurable concentrations of a nutrient (McCarty and Goldman, 1979; Ignatiades et al., 1992; Kucuksezgin et al., 1995) and have defined eutrophication as a qualitative parameter referring simply to nutrient or organic matter enrichment from external sources and resulting in high biological productivity (Ignatiades et al., 1992). The inner bay is heavily polluted by nutrients and organic material, but metal concentrations were not high enough to indicate heavy metal pollution. Industrial fluxes of Cr, Cd and Hg to the bay are 6700, 20 and 70 kg year 1, respectively. Data are not available on fluxes of heavy metal due to domestic discharges. 105,000 m3 day 1 of industrial and 308,000 m3 day 1 of domestic wastewater were discharged to the bay without significant treatment (UNEP, 1993) until 2000. In early 2000, the wastewater treatment plant (WTP) began to treat domestic and industrial wastes. Eutrophication of the inner bay is a serious problem throughout the year and red tide events are becoming more frequent (UNEP, 1993; IMST, 1988; IMST, 1991; Kontas et al., 2004). Heavy metals, as defined by Nieboer and Richardson (1980), are normal constituents of the marine environment. At least 11 are known to be essential to marine organisms: Fe, Cu, Zn, Co, Mn, Cr, Mo, V, Se and Ni (Bryan, 1979). These metals always function in combination with organic molecules, usually proteins. Metals occur normally at low concentrations yet are capable of exerting considerable biological effects even at such levels (Rainbow, 1992). All metals are toxic above some threshold bioavailable level. Ag, Hg, Cu, Cd and Pb are particularly toxic (Bryan, 1979). The elucidation of the comparative pollution of aquatic environments by heavy metals is possible by analysis of water, sediments and members of indigenous biota, i.e. biomonitors (Phillips and Rainbow, 1993). Sediments are composite materials consisting of inorganic components, mineral particulates and organic matter in various stages of decomposition. It is well known that they are sensitive indicators between natural and anthropogenic variables (Salamons, 1995; Calmano et al., 1996). Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous organic contaminants of marine coastal sediments (NOAA, 1988; Raoux et al., 1999). PAHs show a marked hydrophobic character, resistance to biodegradation (Soclo et al., 2000) and adverse effects on health (carcinogenic and/or mutagenic activity) (Henner et al., 1997; Singh et al., 1998) and ecosystem (Varanasi et al., 1985; Long et al., 1995). Metal pollution of the sea is less visible and direct than other types of marine pollution but its effects on

marine ecosystems and humans are intensive and very extensive. As an indirect measure of the abundance and availability of metals in the marine environment, the bioaccumulation of metals by the tissues of marine organisms is studied. The bioaccumulation studies led to the adoption of the bio-indicator concept (Langston and Spence, 1995). Fish are widely used as bio-indicators of marine pollution by metals (Evans et al., 1993). A number of studies have been carried out on the concentrations of nutrients and heavy metals in the bay for 1 year periods (Demirkurt et al., 1990; Parlak and Demirkurt, 1990; Kucuksezgin and Balci, 1994; Balci et al., 1995; Kucuksezgin, 1996; Kucuksezgin et al., 2002), but no long-term and seasonal data are available. No published data are available on petroleum hydrocarbon concentrations in the sediments from the Izmir Bay. The main aim of this study was to monitor levels, temporal variability and distribution of nutrients, heavy metals in edible fishes and sediments of Izmir Bay before and after installation of a wastewater treatment plant. This is the first time that the total petroleum hydrocarbon data has been collected (November 2000), quantified and evaluated in the bay. 2. Materials and methods Nutrient and heavy metal data were collected during cruises of R/V K. Piri Reis during 1996 – 2003 at sampling stations. The study area and the positions of the sampling stations located between the longitudes 26-30V– 27-08VE and latitudes 38-41V– 38-21VN are shown in Fig. 1. Seawater samples were collected with General Oceanic Go-Flo Rosette bottles attached to the CTD system from the following depths: 0, 10, 20, 30, 40, 50 and 60 m. Nutrient analysis was carried out within 1 week of the completion of the cruise, using a Skalar (two-channel) Autoanalyzer. Intercalibration of seawater samples (from QUASIMEME, Plymouth Marine Laboratory, Round 22) was used as a control for the analytical methods of nutrients. The colorimetric methods adopted were similar to those described by Stricland and Parsons (1972) and Grasshoff et al. (1983). Water samples for chlorophyll-a (Chl-a) were collected from water column and were filtered through GF/F filters, Chl-a were measured, using a Sequoia-Turner Fluorometer (Stricland and Parsons, 1972). Sediment samples were taken using Van-Veen Grab from surface sediments. Samples were digested in microwave digestion system (Milestone 1200) with a HNO3 – HF – HClO4 – HCl acid mixture for heavy metals (UNEP, 1985b,c,d,e). Mullus barbatus, being bottom dwellers to a certain extent, are species that tend to concentrate contaminants to a higher degree than other species due to high mobility. For this reason, it was recommended by FAO/UNEP (1993) as monitoring species. Solea vulgaris was also selected as monitoring species because it is important commercially and commonly consumed by humans. Samples were collected from Foca, Mordogan and Gediz River estuary in the outer part of the bay. Tissues were homogenised in a blender; approximately 5 – 7 g of homogenate was then digested with 5:1 HNO3/HClO4 in a microwave oven (UNEP, 1982, 1984, 1985a). All analyses were performed by flame (Cr), cold vapour

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51

43

42°

38.7°° 1

2

3

5

6

4

Foca Gediz River

41°

GREECE

40°

7

38°

38.6°

8

9

10 12

11

14 17

Mordogan

36°

13 Uzun ada

15

16

18

19

20

25

26

AEGEAN SEA

37°

35° 22°

38.5° Outer Bay III

38.4°

TURKEY

39°

23°

24°

25°

Middle Bay 21

22

26°

27°

28°

Inner Bay 23

24

28

27

Outer Bay II

Harbour

Outer Bay I 26.5°

26.6°

26.7°

26.8°

26.9°

27.0°

27.1°

Fig. 1. Location of stations in the Izmir Bay.

(Hg) and graphite furnace (Cd, Pb) AAS (Varian Spectraa-300 plus), using the manufacturer’s conditions and with background correction. The detection limits for heavy metals are Hg: 0.05 Ag l 1, Cd: 0.10 Ag l 1, Pb: 0.10 Ag l 1 and Cr: 0.06 mg kg 1. Intercalibration sediment (SD-MEDPOL-1/TM) and fish (MAMEDPOL-1/TM) samples (from the International Laboratory of Marine Radioactivity, IAEA, Monaco) were used as a control for the analytical methods. Surface sediments were collected at 16 locations in November 2000 for hydrocarbon analysis. Hydrocarbon samples were also collected using with a Van-Veen grab sampler and stored frozen at 20 -C for subsequent analysis. Before extraction, the samples were freeze-dried for 48 h and sieved through 125 Am in a stainless steel sieve. Samples were extracted in a soxhlet apparatus for 8 h, using n-hexane and dichloromethane, according to UNEP (1991). High-resolution gas chromatography was conducted on a CHROMPACK gas chromatograph, equipped with a split/splitless capillary injection system and flame ionization detector (FID). The detection limits of petroleum hydrocarbons ranges between 0.12 and 2.9 ng g 1. Intercalibration sediment sample (IAEA-432) was used as reference material to test the validity of the entire method. Nutrient, heavy metal and hydrocarbon results were statistically evaluated using two-way ANOVA and cluster analysis.

3. Results and discussion 3.1. Nutrients The average concentrations from all depths in the outer bay ranged between 0.01 and 0.19 AM, 0.10 and 1.8 AM, 0.30 and 5.8 AM, and 0.01 and 4.3 Ag l 1 for o.phosphate – phosphorus (oPO4 – P), (nitrate + nitrite) – nitrogen (TNOx – N), silicate [Si(OH)4 – Si] and chlorophyll-a (Chl-a), respectively (Table 1). The seasonal variations of o-PO4 – P, TNOx – N, [Si(OH)4 – Si] and chlorophyll-a concentrations are illustrated in Fig. 2. In the periods of 1996 – 2003, during autumn and winter, TNOx – N levels were generally higher than those in spring and summer

periods. o-PO4 – P concentrations were similar to those of nitrate + nitrite concentrations. Maximum values were recorded during autumn and winter because of low consumption by phytoplankton. In the winter periods, high chlorophyll-a concentrations were measured in the outer bay due to Gediz River. The Gediz River is known to be under contamination menace by wastes derived from industrial sources, sewage and agricultural activities. The Gediz River discharges 295,000 tons of total suspended solid, 4900 tons of nitrogen each year. Amounts of pollutants discharged by Gediz River are higher than total amounts by other streams in the bay (UNEP, 1993). In the middle – inner bays, the ranges of nutrient and chlorophyll-a concentrations were 0.01 – 10, 0.12 – 27, 0.43 – 39 AM and 0.10 – 26 Ag l 1 for o-PO4 – P, TNOx – N, [Si(OH)4 – Si] and Chl-a, respectively (Table 1). Concentrations were comparatively higher in the middle and inner bays than the outer part of the bay. Maximum levels of phosphate and nitrate + nitrite values were observed during summer and autumn due to bacterial degradation in the inner bay, respectively. The observed phosphate concentrations in the inner bay were higher than values observed in clean waters, a clear indication of the role of domestic waste in Izmir Bay. Higher chlorophyll-a values were determined in spring and autumn periods in the water column. As expected, the transparency of seawater (secchi disk depth) decreases towards the inner bay depending on the productivity and the amount of terrestrial solid materials in the water. It reached a maximum value (29 m) in the outer bay in winter and autumn, minimum value (0.3 m) in the inner bay in summer as a result of increase in primary production. The secchi disk depth, an indicator of relative primary production and pollution levels in the marine environment, was comparatively high and independent of season in the outer bay. The atomic ratio of TNOx to phosphate ranges 1.8 – 27 in the outer bay, while the range at stations in the middle and inner bays is 0.02 – 54 owing to different characteristics of the seawater (Table 1). The water column in Izmir Bay has a two-layer temperature structure during summer as a result of radiant heating of the surface. In winter, the water column is almost homogenous due to surface cooling and vertical mixing induced by winds. Maximum temperature and salinity values were observed in summer periods

44

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51

Table 1 Range, mean values of nutrient (AM) and chlorophyll-a (Ag l

o.PO4 – P

T.PO4 – P

TNOx – N

NO2 – N

NH4 – N

Si

TNOx /PO4

Chl-a

a b

Period

Outer bay

96 – 98 2000 2001 2002 2003 2000 2001 2002 2003 96 – 98 2000 2001 2002 2003 96 – 98 2000 2001 2002 2003 96 – 98 2000 2001 2002 2003 96 – 98 2000 2001 2002 2003 96 – 98 2000 2001 2002 2003 96 – 98 2000 2001 2002 2003

0.01 – 0.19 0.01 – 0.11 0.02 – 0.10 0.01 – 0.19 0.01 – 0.16 0.06 – 0.85 0.11 – 0.61 0.12 – 0.66 0.10 – 0.69 0.11 – 1.8 0.11 – 1.0 0.18 – 0.90 0.10 – 1.4 0.10 – 1.4 0.01 – 0.23 0.01 – 0.14 0.01 – 0.16 0.01 – 0.11 0.01 – 0.24 0.10 – 0.96 0.10 – 0.69 0.10 – 0.79 0.10 – 0.68 0.10 – 0.69 0.30 – 4.1 0.38 – 2.8 0.48 – 1.7 0.72 – 4.8 0.80 – 5.8 3.0 – 27 1.8 – 14 5.8 – 17 5.2 – 18 3.0 – 18 0.02 – 4.3 0.08 – 1.1 0.02 – 0.69 0.02 – 0.41 0.01 – 0.94

1

) in the Izmir Bay, Aegean and Mediterranean Seas Middle – inner bays

0.06 T 0.001 0.05 T 0.003 0.04 T 0.002 0.05 T 0.005 0.05 T 0.004 0.32 T 0.02 0.28 T 0.01 0.32 T 0.01 0.32 T 0.01 0.48 T 0.01 0.44 T 0.02 0.40 T 0.02 0.48 T 0.03 0.46 T 0.04 0.03 T 0.001 0.04 T 0.003 0.04 T 0.003 0.04 T 0.002 0.04 T 0.006 0.30 T 0.02 0.21 T 0.01 0.32 T 0.02 0.23 T 0.01 0.22 T 0.02 1.5 T 0.02 1.2 T 0.05 0.94 T 0.03 1.69 T 0.08 2.1 T 0.12 9.8 T 0.13 8.3 T 0.27 11 T 0.37 11 T 0.32 11 T 0.40 0.48 T 0.03 0.34 T 0.02 0.24 T 0.02 0.15 T 0.01 0.22 T 0.03

0.01 – 10 0.13 – 3.8 0.14 – 2.9 0.14 – 4.4 0.32 – 4.5 0.52 – 6.9 0.20 – 3.0 0.38 – 4.8 0.28 – 5.9 0.13 – 27 0.15 – 18 0.29 – 16 0.26 – 6.7 0.12 – 8.6 0.01 – 18 0.02 – 12 0.02 – 4.3 0.01 – 6.1 0.01 – 1.0 0.10 – 21 0.13 – 34 0.11 – 50 0.10 – 6.7 0.21 – 2.4 0.50 – 39 0.43 – 20 1.2 – 18 1.0 – 26 2.6 – 32 0.02 – 54 0.10 – 7.3 0.10 – 7.5 0.13 – 9.8 0.06 – 17 0.10 – 26 0.46 – 18 0.38 – 7.8 0.13 – 3.7 0.24 – 2.6

0.83 T 0.06 1.3 T 0.13 0.95 T 0.19 1.2 T 0.20 1.6 T 0.26 2.5 T 0.26 1.3 T 0.19 1.9 T 0.24 2.3 T 0.34 2.6 T 0.25 2.5 T 0.40 3.1 T 0.91 1.7 T 0.35 1.9 T 0.62 0.53 T 0.09 1.1 T 0.34 0.76 T 0.27 0.68 T 0.27 0.32 T 0.08 2.5 T 0.18 3.4 T 0.67 5.8 T 2.8 1.5 T 0.29 0.89 T 0.14 4.2 T 0.28 5.1 T 0.49 4.5 T 0.89 6.8 T 1.1 14 T 1.6 6.7 T 0.40 2.2 T 0.21 3.7 T 0.55 2.6 T 0.48 3.8 T 1.2 4.6 T 0.49 4.3 T 0.63 2.2 T 0.45 1.2 T 0.19 1.3 T 0.17

Aegeana

NE Meditb

0.01 – 0.30

0.01 – 0.24

–

–

0.10 – 3.0

0.05 – 6.0

–

–

–

–

0.30 – 3.0

1.0 – 11

13.6 – 36.8

0.1 – 0.8

0.01 – 0.15

Stirn (1988) and Kucuksezgin et al. (1995). Salihoglu et al. (1990).

while minimum salinities are measured near freshwater inputs. The observed mean N/P ratio was significantly lower than the assimilatory optimal (N/P= 15:1) in conformity with Redfield’s ratio N/P= 16:1 in the bay. The vertical distribution of phytoplankton abundance was determined in the framework of Izmir Bay Project (IMST, 1996 – 2003) over the sampling periods. With regard to the proportion of the phosphorus relative to nitrogen (the N/P ratio), it may vary markedly (diatoms: 5 – 12, dinoflagellates: 9 – 41, natural plankton: 17) (Bougis, 1976). Phytoplankton abundance clearly showed a spring maximum (i.e. spring bloom). Diatoms (Bacillariophyceae) were observed all year around and increased during the spring bloom. Dinoflagellates (Dinophyceae) were found in summer, autumn and winter together with Bacillariophyceae. Cyanobacteria (Cyanophyceae) abundance increased only during the spring bloom. Diatoms and dinoflagellates are normally nitrogen limited and N/P ratios also indicate Nlimitation, but cyanobacteria may be phosphorus limited in summer.

A two-way ANOVA was used to compare the nutrient concentrations among seasons and sampling stations. The nutrient concentrations significantly varied among seasons and sampling stations in the bay. The relationships between o.PO4 – P and TNOx – N concentrations were significant (R = 0.62 for 1996 – 1998, R = 0.83 for 2000 – 2001, R = 0.65 for 2002, R = 0.78 for 2003, p < 0.05) in the outer bay. Correlation coefficients were calculated in the middle and inner bays (R = 0.44 for 1996 – 98, R = 0.48 for 2000 – 2001, R = 0.61 for 2002, R = 0.61 for 2003, p < 0.05). Table 2 shows typical phosphate and nitrate concentrations in different areas of the Mediterranean (Adriatic Sea and Saronikos Bay) and Izmir Bay. The nutrient concentrations are always measurable in Izmir Bay and keep photosynthetic production over the natural level of the marine environment. Izmir wastewater treatment plant was constructed in the scope of Great Channel Project in the beginning of 2000. It works on the principle of phosphorus and nitrogen treatment with activated

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51

OUTER BAY

Table 2 Typical concentrations of nutrients in the Adriatic Sea, Saronikos and Izmir Bays

µ

3 2,5

0,12

2

0,09

1,5

µ

0,06

1 0,03

0,5 0

0 3 4 1 2 3 4 1 2 3 4 2 3 4 1 2 3 4 1 2 3 4 1 2 3 98 00 01 02 03 96 97

µ

MIDDLE AND INNER BAYS 2,4

20

2

15

1,6

0,8

5

µ

10

0,4

0

0

3 4 1 2 3 4 1 2 3 4 2 3 4 1 2 3 4 1 2 3 4 1 2 3 96 97 98 00 01 02 03

o.PO4-P

Reac.Si

o.PO4 – P (AM)

(NO3) – N (AM)

Southern Adriatic (extremely oligotrophic)a Mid-Adriatic (oligotrophic)a NW Adriatic (eutrophic)a W Adriatic (hipertrophic)a Saronikos Bay (offshore water)b Saronikos Bay (inshore water)b Outer bay (this study) Middle – inner bays (this study)

0.03 0.05 0.30 >0.15 0.01 – 3.50 0.01 – 13.72 0.01 – 0.19 0.01 – 10

1.0 0.5 5.0 >8.0 0.01 – 15.04 0.01 – 24.11 0.10 – 1.8 0.12 – 27

b

1,2

TNOx-N

Typical areas

a

25

45

Chl-a

Fig. 2. Seasonal variations of nutrient and chlorophyll-a concentrations in the Izmir Bay (1: winter, 2: spring, 3: summer, 4: autumn).

sludge processes. The concentrations of NH4 – N have been reduced after wastewater biological treatment plant, while increases were recorded for the mean levels of o.PO4 – P in the middle – inner bays (Table 1). The capacity of wastewater plant has not been found enough for the phosphate. High phosphate values were observed after WTP in the middle – inner parts of the bay due to microbial activity (IMST, 2000) and lower N/P ratios occurred in this period. Low Chl-a values were recorded because of primary production after WTP in the bay. 3.2. Heavy metals in sediment Minimum and maximum concentrations of heavy metals (Hg, Cd, Pb and Cr) determined in the sediments are presented in Table 3. The highest concentrations of metals were found in the inner part of the bay where intensely industrialized (mainly iron, paper and pulp factories, antifouling paints, chlorine-alkali plants, chemical industries, textile industries, metal processing, timber processing, cement factories, food processing, beverage manufacturing and bottling, tanneries, oil, soap and a very busy harbour) compared to the middle and outer parts of the bay. The concentrations of mercury range between 0.05 and 0.99 Ag g 1 in the outer bay, while the range at stations in the middle and inner bays is 0.11 – 1.3 Ag g 1 during 1997 – 2002. The maximum level of Hg (1.3 Ag g 1 dry wt.) was measured at harbour in 2000 (Fig. 3). High levels of mercury were also found in the outer bay due to old centre of mercury mining in the NW part of the bay (station 8). The Hg concentrations at stations 11 and 15 were found higher than the other sampling stations in the outer bay due to the Gediz River.

UNESCO, 1990 (No. 34). Ignatiades et al. (1992).

The highest concentration of cadmium (0.82 Ag g 1 dry wt.) was found at station 24 in the inner part of the bay in 1997 (Fig. 3). The concentrations of cadmium measured in sediments varied, ranging from 0.005 to 0.33 Ag g 1 in the outer bay and 0.02 to 0.82 Ag g 1 in the middle – inner bays. High levels of Hg and Cd were measured at the estuary of Gediz River. Gediz River drains a basin of 15,616 km2, with annual discharge 40 – 70 m3 s 1 (EIE, 1984). Gediz River is densely populated and includes extensive agricultural lands and numerous manufacturing, food and chemical industries. Lead is quite high (44 – 103 Ag g 1 dry wt.) in the sediments of middle and inner parts of the bay. The main source of lead is probably the traffic, since the great majority of the cars have no catalytic converters and burn leaded fuel. The concentration of lead ranges between 14 and 90 Ag g 1 in the outer bay (Fig. 3). High levels of lead were measured at stations 15 and 17 in 2002 due to Gediz River and rainfall, respectively. The concentrations of chromium range between 29 and 199 Ag g 1 dry wt. in the outer bay. The highest chromium values were observed in the middle and inner parts of the bay, ranging from 116 Table 3 Minimum and maximum values of heavy metals in sediments during 1997 – 2002 from Izmir Bay (Ag g 1 dry wt.) Heavy metal

Period

Outer bay

Middle and inner bay

Hg

1997 1998 2000 2001 2002 1997 1998 2000 2001 2002 1997 1998 2000 2001 2002 1997 1998 2000 2001 2002

0.24 – 0.96 0.19 – 0.70 0.26 – 0.99 0.41 – 0.62 0.05 – 0.27 0.07 – 0.23 0.08 – 0.33 0.04 – 0.09 0.03 – 0.05 0.005 – 0.07 14 – 70 32 – 90 48 – 71 25 – 73 14 – 76 29 – 157 67 – 157 41 – 172 38 – 199 40 – 147

0.41 – 0.99 0.25 – 0.86 0.36 – 1.3 0.38 – 0.82 0.12 – 0.51 0.29 – 0.82 0.15 – 0.42 0.12 – 0.38 0.05 – 0.55 0.02 – 0.36 69 – 103 68 – 100 47 – 113 61 – 110 44 – 73 143 – 281 140 – 155 122 – 183 171 – 295 116 – 316

Cd

Pb

Cr

46

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51

1.4

Hg (µg/g dry wt)

from the Mediterranean and Aegean Seas except chromium (MAP, 1987; UNEP, 1978; Whitehead et al., 1985; Friligos et al., 1998; Batki et al., 1999). The levels of metals are lower in the inner bay than polluted areas of Mediterranean Sea (Zvonaric and Odzak, 1998; Ujevic et al., 1999). Analysis of covariance (ANCOVA) was used to compare the regional differences in the heavy metal concentrations of sediments, with metal concentrations as the dependent variable, sampling site as the independent variable and sampling time as the covariate (Table 4). In consequences, the comparison of metal concentrations demonstrates that there are significant ( p < 0.05) regional variations during 1997 – 2002. To evaluate spatial and temporal differences among samples studied, data obtained from the Izmir Bay as before and after waste water treatment plant were analyzed statistically. A cluster analysis of the data obtained from the five sampling cruise allowed the authors to differentiate four groups: group 1 (G1) includes samples from inner part of the bay (24, harbour); group 2 (G2) and group 3 (G3) include mainly samples collected in 2000 (3, 6, 11, 13, 20), 2001 (10, 11, 13, 15, 22, 23) and 2002 (3, 6, 11, 13, 22, 23) after wastewater treatment plant; group 4 (G4) includes a mixture of some samples (12, 17, 26) collected in all sampling periods from the southwestern part of the outer bay (Fig. 4).

1.2 1 0.8 0.6 0.4 0.2 0 1

Cd (µg/g dry wt)

0.8 0.6 0.4 0.2 0 120

Pb (µg/g dry wt)

3.3. Petroleum hydrocarbons in sediment

100 80 60 40 20 0 350

Cr (µg/g dry wt)

300 250 200 150 100 50 0 3

6

07/1997

8

11

12

01/1998

13

15

17

11/2000

20

22

23

08/2001

24 Harbour

11/2002

Fig. 3. Distribution of Hg, Cd, Pb and Cr concentrations during 1997 – 2002 in the Izmir Bay sediments. (The locations of sampling stations were cited in Fig. 1.)

to 316 Ag g 1 (Fig. 3). Until 1994, the leather tanning plants, which use large quantities of Cr in the tanning procedure, discharged wastes directly into the inner bay. Maximum levels of Cr were observed at stations 11, 13 and 15 due to Gediz River. As clearly seen in Fig. 3, heavy metal concentrations generally decreased in 2002 at all sampling stations. The concentrations of heavy metals in the outer bay were generally similar to the background levels and mean concentrations

In terms of total hydrocarbons (Table 5), concentrations range from 427 to 7800 ng g 1 dry wt. of Izmir Bay sediments. In ‘‘unpolluted’’ intertidal and estuarine sediments, concentration generally ranges from sub-Ag g 1 to approximately 10 Ag g 1 (Volkman et al., 1992; Bouloubassi and Saliot, 1993). Readman et al. (2002) have reported similar levels of total hydrocarbons (2.1 – 6.6 Ag g 1) in sediments from the Coastline – Ukraine – Black Sea; on the other hand, Readman et al. (2002) have reported the levels of total hydrocarbons in sediments from the Bosphorus – Turkey – Black Sea (12 – 76 Ag g 1). The highest total hydrocarbon levels were found in the inner bay (7800 ng g 1 dry wt.). These levels of total hydrocarbon suggest that the bottom sediments of the inner bay received a fair amount of petroleum containing waste material due to the industries and urban areas. Total extractable organic matter (EOM) in the sediments from the Izmir Bay ranged from 0.99 to 7.1 mg g 1 dry wt. in the outer bay, from 1.7 to 11 mg g 1 in the middle and inner bays and 84 mg g 1 in the harbour (Table 5). Total hydrocarbon (R 2 = 0.1582) concentrations in sediment showed no relation to EOM. According to Neff (1979), hydrocarbons in sediments are mainly associated with organic matter. Thus, a regression analysis was completed to investigate the relationship between the concentration of total hydrocarbon and the percentage of organic matter. The linear regressions between these parameters show

Table 4 Results of analysis of covariance for the significant differences in the metal concentrations of sediment among sampling sites in Izmir Bay, with year as the covariate Metal

df

F

p level

Hg Cd Pb Cr

35 35 35 35

3.07 2.19 3.08 6.87

0.0001 0.0046 0.0001 0.00001

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51

significant correlation coefficients, at the 99% confidence levels for total hydrocarbon (R = 0.7467). The cluster analysis results (hierarchical clustering) of the sampling sites are shown in Fig. 5. Three big clusters could be interpreted divided into two subgroups: the first contains several sites from Gediz River estuary (11, 10) and mainly northern part of the bay (6, 13, 17); the second one indicates less polluted areas of the bay; the third one represents heavily polluted sites from middle bay to the inner part of the bay (23, 24, harbour). 3.4. Heavy metals in fish The concentrations of heavy metals found in M. barbatus varied, with Hg ranging from 14 to 520, Cd from 0.10 to 10 and Pb from 2.6 to 478 Ag kg 1 wet weight in the bay. The highest levels of metals were measured as Hg: 520 Ag kg 1, Cd: 10 Ag kg 1 and Pb: 478 Ag kg 1 in M. barbatus in 2002, 2001 and 1998, respectively (Table 6). The concentrations of heavy metals found as Hg: 16 – 200 Ag kg 1, Cd: 0.57 – 4.5 Ag kg 1 and Pb: 40 – 207 Ag kg 1 in the Aegean Sea (IMST, 1995, 1997; Kucuksezgin et al., 2001), and the levels are lower than the values of Izmir Bay. The ranges of heavy metal concentrations in the bay were: Hg: 4.5 – 212, Cd: 0.10 – 3.5 and Pb: 1.0 – 491 Ag kg 1 in S. vulgaris. Hg and Cd levels were significantly lower in S. vulgaris than M. barbatus. The highest levels were found as Hg: 212, Cd: 3.5 and Pb: 491 Ag kg 1 in S. vulgaris in 1998, 2002 and 2001, respectively. The order of heavy metal concentrations found in M. barbatus and S. vulgaris was Pb > Hg > Cd. The mean concentrations of Cd and Pb in M. barbatus decreased, while Hg levels increased in 2003. In 1998, low levels of Cd were obtained, since most of the samples were collected from Mordogan located in the outer bay. The mean Cd and Pb concentrations were lower in 2002 than the other sampling periods

47

Table 5 Concentrations of total hydrocarbons (T.Hc), organic matter and extractable organic matter (EOM) for Izmir Bay sediments Station no.

T.Hc (ng/g)

EOM (mg/g)

Organic matter (%)

3 6 8 10 11 12 13 15 17 25 20 26 22 23 24 Harbour

427 1165 980 1929 1769 794 1460 1041 1233 662 2992 876 1350 3120 7800 5139

6.9 0.99 2.2 1.8 3.4 7.1 2.4 2.4 1.9 1.0 5.1 2.2 11 2.4 1.7 84

2.8 2.8 1.9 3.4 3.4 1.7 3.5 3.6 3.8 5.5 3.6 4.0 4.6 6.7 8.0 15

in S. vulgaris. These data are summarised in Figs. 6 and 7 for M. Barbatus and S. Vulgaris, respectively. Regression between Hg concentrations and the fish length was statistically significant ( p < 0.05). The relationships between Hg concentration and fish length in M. barbatus and S. vulgaris were given in Table 7. An increase in Hg with increasing length was noted for M. barbatus, in good agreement with results from the Aegean Sea (Kucuksezgin et al., 2001). Mercury concentration increases with increasing size of the sample and the accumulation is associated with its food and feeding habits. It is known that the position of the fish in food chain is an important factor determining its mercury content (Bernhard, 1988). Cd and Pb concentrations in muscle tissue were not related to fish

90

94

96

98

100

02-Harbour 97-24 01-24 97-Harbour 01-Harbour 00-24 98-Harbour 97-23 00-Harbour 98-20 98-22 01-10 01-22 01-13 01-11 01-15 02-15 98-13 98-12 02-10 97-20 02-20 97-11 00-3 98-15 00-6 98-3 98-6 97-22 98-23 97-15 98-24 00-20 00-23 00-13 00-11 01-6 01-23 02-24 97-6 00-10 00-15 00-22 97-3 97-13 02-11 02-13 02-6 02-22 02-23 98-10 02-3 01-12 97-26 98-17 01-17 98-11 98-26 02-12 02-26 00-12 00-17 02-17

Similarity

92

G1

G2

G3

G4

Fig. 4. Hierarchical dendogram for heavy metals at sampling points during different cruises in Izmir Bay.

48

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51 Table 6 Minimum and maximum concentrations of heavy metals in fish (Ag kg wet wt.)

length. ANCOVA was used to compare metal concentrations among seasons and no significant differences were detected. Maximum concentrations of mercury permitted in marine organisms are similar in the majority of Mediterranean countries, ranging between 500 and 700 Ag kg 1 (FAO, 1984). The maximum value of mercury 520 Ag kg 1 indicated for the edible parts of M. barbatus. The consumption of 0.156 mg week 1 of this fish in the human diet would represent the maximum tolerable consumption of mercury (300 Ag mercury week 1 60 kg man 1). Similarly, the provisionally tolerable weekly intake of Cd has been estimated to be 400 – 500 Ag person 1 week 1 (UNEP, 1985a). The maximum value of Cd in this study was 10 Ag kg 1 and a person could, therefore, consume more than 133 meals of fish per week. The maximum concentration of Pb in fish observed was 491 Ag kg 1. Consumption of 20 meals per week of this fish represents the tolerable weekly intake of lead (3000 Ag lead/60 kg human; UNEP, 1985a). Heavy metal concentrations found in this study were higher than those from clean areas of Aegean and Mediterranean Seas (Aydogdu et al., 1982; IMST, 1995, 1997; Kucuksezgin et al., 2001), and are likely due to natural and industrial inputs to Izmir Bay. On the other hand, metal concentrations in Izmir Bay are considerably lower than those found in polluted areas of Mediterranean Sea, such as Tyrrhenian Sea and Saronikos Gulf (Taliadouri-Voutsinou, 1980; Barghigiani and De Ranieri, 1992).

Period

Organism

Hg

Cd

Pb

1996

Mullus barbatus Solea vulgaris Mullus barbatus Solea vulgaris Mullus barbatus Solea vulgaris Mullus barbatus Mullus barbatus Solea vulgaris Mullus barbatus Solea vulgaris Mullus barbatus

182 – 259 17 – 159 66 – 399 5.2 – 95 27 – 285 11 – 212 14 – 355 18 – 276 4.5 – 91 34 – 520 10 – 113 101 – 209

0.13 – 2.4 0.44 – 2.2 0.53 – 5.7 1.1 – 2.3 0.77 – 1.6 1.2 – 3.5 0.38 – 9.4 1.1 – 10 1.8 – 2.1 0.10 – 10 0.10 – 3.5 0.83 – 2.2

2.6 – 125 46 – 388 29 – 349 110 – 364 8.0 – 478 2.0 – 341 16 – 241 36 – 303 90 – 491 17 – 300 1.0 – 218 15 – 103

1997 1998 2000 2001 2002 2003

0.12– 2.0 and NH4 – N: 0.10– 0.95 AM. Nutrient concentrations were relatively high at the surface layers of Gediz River estuary. The mean atomic ratio of TNOx to phosphate ranges 8.3– 11 in the outer bay, while the range at stations in the middle and inner bays is 2.2 – 6.7. Diatoms and dinoflagellates are normally nitrogen limited and N/P ratios also indicate N-limitation in the bay. Nutrient levels found in this study in the middle –inner bays were higher than those from Adriatic Sea, Northeastern Mediterranean and Aegean Seas. On the other hand, nutrient concentrations in this part of the bay are similar to the inshore water of Saranikos Gulf. The wastewater treatment plant treated the wastes about 60% capacity between 2000 and 2001 and full capacity after 2001. The quality of the marine environment in the middle and inner parts of the bay has not yet noticeably improved. Although the capacity of wastewater plant is sufficient for removal of nitrogen from the wastes, it is inadequate for removal of phosphate. This is also in accordance with the decreasing TNOx /PO4 ratios observed during 2000 –2003 (after WTP)

4. Conclusions Nutrient and chlorophyll-a concentrations have been determined during 1996– 2003 cruises in the Izmir Bay and compared with the similar regions in the Mediterranean Sea. Pollution in the outer bay is not significant, but eutrophication of the inner bay has already begun and might be spreading progressively to the outer part of the bay. The nutrient concentrations in the outer bay ranged between DIP: 0.01 – 0.40, DTP: 0.08 – 0.85, TNOx – N:

90

G1

G2

G3

Fig. 5. Hierarchical dendogram for sampling points in sediments from Izmir Bay.

Harbour

24

23

26

12

15

8

25

22

13

17

6

11

10

95

3

Similarity

85

100

1

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51 200

320 Mean±1.96*SE Mean; Mean±1.00*SE

160 Hg (µg/kg wet weight)

Hg (µg/kg wet weight)

280 240 200 160 120

Mean±1.96*SE Mean; Mean±1.00*SE

120 80 40 0

80 40

49

-40

1996

1997

1998

2000

2001

2002

2003

1996

1997

1998

2001

2002

1996

1997

1998

2001

2002

1996

1997

1998

2001

2002

4,0

5,5

3,5 3,0

Cd (µg/kg wet weight)

Cd (µg/kg wet weight)

4,5 3,5 2,5 1,5

2,5 2,0 1,5 1,0 0,5

0,5 -0,5

0,0 -0,5

1996

1997

1998

2000

2001

2002

2003 600

350

500 Pb (µg/kg wet weight)

Pb (µg/kg wet weight)

300 250 200 150 100 50 0

300 200 100 0

-50 -100

400

-100

1996 1997 1998 2000 2001 2002 2003

Year

Year

Fig. 6. Means T standard error and confidence intervals (1.96j) in Mullus barbatus.

in the middle and inner bays. The stations in the outer bay have an average ratio of TNOx to phosphate 9.8 for 1996 – 1998 and 10 for 2000 –2003, while the average ratio at stations in the middle and inner bays is 6.7 for 1996 –1998 and 3.1 for 2000– 2003 owing to the different characteristics of the seawater. The concentration of heavy metals in sediments was generally similar to the background levels from the Mediterranean and Aegean Seas, except delta of Gediz River in the outer bay. Gediz River is the major source of anthropogenic input into the outer bay. The high concentration of heavy metals is observed in the inner part of the bay. The levels of metals are lower in the inner bay than polluted areas of Mediterranean. The levels of heavy metals gradually decreased over the sampling period.

Fig. 7. Means T standard error and confidence intervals (1.96j) in Solea vulgaris.

Total petroleum hydrocarbon values measured in outer bay indicate that this area is not heavily polluted (except the estuary of Gediz River), while the considerable concentrations of hydrocarbons in some sediment sampled in the Table 7 Regression analysis between Hg concentration and fork length of Mullus barbatus and Solea vulgaris from Izmir Bay ( p < 0.05) Period

Organism

Sex

Correlation coefficients

1996 – 1998 1996 – 1998 2000 2000 2001 2002 2002

Mullus barbatus Solea vulgaris Mullus barbatus Mullus barbatus Mullus barbatus Mullus barbatus Solea vulgaris

Female + male Female + male Female Male Female Female + male Female + male

R = 0.59038 R = 0.69211 R = 0.82489 R = 0.79304 R = 0.57961 R = 0.41066 R = 0.97148

(n = 170) (n = 45) (n = 99) (n = 30) (n = 68) (n = 120) (n = 31)

50

F. Kucuksezgin et al. / Environment International 32 (2006) 41 – 51

area of the middle and inner bays highlight not negligible anthropogenic inputs. High levels of total petroleum hydrocarbon results were found in the inner bay due to the anthropogenic activities, mainly combustion processes of traffic and industrial activities. The hydrocarbon concentrations range from 427 to 7800 ng g 1, which substantiates from a relatively low to moderate hydrocarbon pollution compared to other urbanized Turkish coastal areas (Readman et al., 2002). The levels of heavy metals in the muscle tissue of M. barbatus and S. vulgaris in the Izmir Bay were measured. In 2003, the mean concentration of Hg in M. barbatus increased, while Cd and Pb levels decreased. Hg and Cd concentrations are higher than the reported mean values of heavy metals in fish organisms from the Aegean Sea and Mediterranean. Lead concentrations are similar to those reported in fish from Mediterranean countries. The metal levels were significantly lower in S. vulgaris than M. barbatus. The order of heavy metal concentrations found in M. barbatus and S. vulgaris was Pb > Hg > Cd. A person can consume more than 2, 133 and 20 meals per week of fish in human diet would represent the tolerable weekly intake of mercury, cadmium and lead, respectively, in Izmir Bay.

Acknowledgments This study has been supported by Izmir Metropolitan Municipality within the framework of the Izmir Bay Marine Research Project. We thank two anonymous reviewers for their helpful comments and suggestions for improving the manuscript. We also express our deep gratitude to the scientists and crew of the R/V Koca Piri Reis during the cruises.

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