Dredging related metal bioaccumulation in oysters

Marine Pollution Bulletin 58 (2009) 832–840

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Dredging related metal bioaccumulation in oysters L.H. Hedge *, N.A. Knott, E.L. Johnston Evolution and Ecology Research Centre, School of Biological Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW 2052, Australia

a r t i c l e Keywords: Saccostrea Sediments Bioavailability Resuspension BACI

i n f o

a b s t r a c t Bivalves are regularly used as biomonitors of contaminants in coastal and estuarine waters. We used oysters to assess short term changes in metal availability caused by the resuspension of contaminated sediments. Sydney Rock Oysters, Saccostrea glomerata, were deployed at multiple sites in Port Kembla Harbour and two reference estuaries for 11 weeks before dredging and for two equivalent periods during dredging. Saccostrea experienced large increases in accumulation of zinc, copper and tin during dredging in the Port relative to oysters deployed in reference estuaries. Lead and tin were found to be permanently elevated within Port Kembla. We present a clear and un-confounded demonstration of the potential for dredging activities to cause large scale increases in water column contamination. Our results also demonstrate the usefulness of external reference locations in overcoming temporal confounding in bioaccumulation studies. Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction Ports and harbours act as sinks for effluent from surrounding industry and urbanization, therefore inheriting a legacy of contamination (Cundy et al., 2003). Metals released into our waterways rapidly bind to particulates and sink to the seafloor (Cundy et al., 2003; Petersen et al., 1997). Invariably, in areas with high levels of industrialisation and urbanization, this has led to sediments with extremely high concentrations of contaminants (Birch, 1996; Luoma, 1989). Past research has emphasized the effects of this contamination on sediment infauna (Bryan and Langston, 1992; Hatje et al., 2006), with the view that most of this contamination is trapped within this habitat (see Birch, 2000). Numerous natural and anthropogenic disturbances, causing resuspension of contaminated sediment can, however, act to transfer contaminants from the sediment to the water column, possibly releasing contaminants from the particulate material (Eggleton and Thomas, 2004; van den Berg et al., 2001). In this way, sites with existing sediment contamination still pose a real hazard to organisms in other habitats (sensu Larsson, 1985). While direct measurements of metals in the water column and sediment have been made during dredging events (Kwon and Lee, 1998; van den Berg et al., 2001), the observed concentrations of metals vary according to different chemical, hydrographical and geological processes. It has been argued that direct measurements of metal concentrations in the sediment and surrounding waters

* Corresponding author. Tel.: +61 2 9385 3447; fax: +61 2 9385 1558. E-mail address: [email protected] (L.H. Hedge). 0025-326X/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2009.01.020

do not represent the metal loads actually available to biota (Bryan and Langston, 1992; Hatje et al., 2003). The use of bivalves to assess accumulation of metals is a relatively simple way of inferring metal bioavailability and assessing metal levels over both long and short periods of time (see reviews by Phillips, 1977; Rainbow, 2006). Studies of long term trends of contamination using metal accumulation in bivalves are common (Goldberg, 1975; Tripp et al., 1992), however studies to assess bioaccumulation during more transient disturbances, such as dredging, have been limited (for examples see Bellas et al., 2007; Lewis et al., 2001). While some of these studies infer effects of dredging, based on elevations in metal concentrations in the study organisms, most of these studies only sample the area directly disturbed by dredging. The accumulation of metals can, however, vary through time, mainly due to changes in physico-chemical variables, such as water temperature and salinity (Abbe et al., 2000; Bryan and Langston, 1992). Hence, studies that only sample metal accumulation at the disturbed location, or at reference locations too close to the disturbance, may infer an effect of resuspended sediment that is simply the result of a larger scale biotic or abiotic interaction (Boening, 1999; Eggleton and Thomas, 2004). Lincoln-Smith and Cooper (2004), however, used reference sites at varying distances from a potentially disturbed location (PIL) in order to establish an un-confounded link between a point source of contamination and estuary wide metal loads. Such study analyses are commonly referred to as BACI designs (Before After Control Impact) (Downes et al., 2002; Keough and Mapstone, 1995 and citations therein, Underwood, 1994). While BACI designs are the most appropriate method for the detection of anthropogenic disturbances, there remains a paucity of these designs in the bioaccumulation literature.

L.H. Hedge et al. / Marine Pollution Bulletin 58 (2009) 832–840

A ‘beyond BACI’ (Underwood, 1992) design utilizing an asymmetrical ANOVA, contrasting a potentially impacted location against the references before and after a perturbation, is often regarded as the ideal analysis for testing for impacts. For this analysis to be appropriate, however, multiple sampling times prior to the disturbance are needed. In many instances, including the current study, insufficient warning of potential environmental impacts means little time for sampling, prior to the perturbation, can be carried out. Often this can result in only a single sampling period prior to a potential impact. In such instances, an asymmetrical design lacks power (Weins, 1996) and becomes inappropriate, and a factorial treatment-control (or ‘reference’) style analysis is arguably more suited. The current study tests for the effects of resuspending contaminated sediment on the accumulation of several metals by the Sydney Rock Oyster, Saccostrea glomerata. We use a BACI style design (Downes et al., 2002; Keough and Mapstone, 1995; Underwood, 1994), utilizing external reference estuaries, to test whether sediment resuspension in a contaminated harbour leads to elevations in several metals within organisms suspended in the water column. S. glomerata is a suitable metal biomonitor for this study, due to its broad distribution within the study region, and its ability to accumulate various compounds, through both particulate and dissolved phases ( Edgar, 2000; Hayes et al., 1998; Rainbow, 2006). The resuspension of sediment in the current study was the result of a large scale dredging program in the highly industrial harbour of Port Kembla, Australia.

2. Materials and methods 2.1. Dredging program and sampling locations Port Kembla is a small estuary with over 70 years of use by heavy industry. It consists of an inner and outer harbour (Fig. 1) with two main tributaries draining urban and industrial catchments directly into the inner harbour. The large scale industry surrounding Port Kembla has led to elevations of several metal contaminants in the sediment of the harbour (Table 1 and He and Morrison (2001)). A dredging program in Port Kembla commenced in February 2007 to remove approximately 325,000 m3 of sediment from the inner harbour seabed and adjacent land to create extra shipping berths. Approximately 60% of this sediment is unsuitable for disposal at sea (ANZECC, 2000; Patterson Britton and Partners Pty Ltd. Consulting Engineers, 2005). Approximately 27,348 m3 of highly contaminated estuarine clay from these areas was placed in a deposition site within the inner harbour (Fig. 1). A further 163,000 m3 of moderately contaminated clay and slag was placed in a large deposition site in the outer harbour (Fig. 1), while 132,000 m3 of relatively uncontaminated alluvial sandstone and clay was deposited 8 km offshore. Dredging was completed in October 2007. 2.2. Assessment design As dredging activities were occurring in the several sections of the inner harbour, and dredge-spoil dumping was occurring within the outer harbour, they were considered separate potentially impacted locations (PIL). Potential increases in accumulation of metals in oysters was assessed by comparing changes in accumulation in the inner and outer harbours of Port Kembla before and during dredging, relative to changes at two reference locations, Botany Bay and Port Hacking. The reference estuaries, Port Hacking and Botany Bay are located approximately 70 km north of Port Kembla (Fig. 1). While Port Hacking is only moderately urbanized (Scanes and Roach, 1999), Botany Bay does have a catchment dominated by the great-

833

er Sydney metropolis. Metal levels in the sediment are elevated in some parts of Botany Bay, however they are still considerably lower than in Port Kembla (He and Morrison, 2001; Scanes and Roach, 1999). Importantly, these reference estuaries do not represent ‘pristine’ waterways, but instead provide a comparison to assess any potential changes in the accumulation of oysters along the coast that may occur coincidentally with dredging activities, allowing us to rule out any temporal confounding in our study. Both reference estuaries were substantially larger than Port Kembla Harbour, so smaller reference areas were selected within each estuary (Fig. 1) that had similar water quality conditions (salinity, pH, turbidity, DO and temperature) to Port Kembla prior to dredging (unpublished data). 2.3. Field deployment Oysters were deployed at four sites within each reference area and four sites within both the inner and outer harbours of Port Kembla. Exact site positions varied through time (random variable) but were always separated by a minimum of 50 m. Oysters were deployed three times at each site; once prior to, and twice during the dredging operations. Oysters were all from the same source population and commercially acquired. Commercially acquired oysters were used so that the size, age and history of the oysters were similar. All oysters were similar in length (60–85 mm) and weight (35–45 g) prior to deployment. 10 oysters were deployed within a single plastic cage approximately 30  15  15 cm at a depth of approximately 2 m at each site. The use of cages does not affect the accumulation of metals by organisms (Cain and Luoma, 1985). Oysters were left in the field for 11 w for each sampling period. Oyster deployment prior to dredging (‘Before’ sampling period) took place between 20th October 2006 and 24th December 2006, while the deployments during the dredging operations (‘During 1 and 2’ sampling periods) took place between 20th February 2007 and 24th July 2007. After 11 w, oysters were collected from each site and immediately placed into plastic bags and stored on ice in an insulated container while transported to the laboratory. In the laboratory, oysters from each site were depurated separately for 72 h on plastic racks in a plastic container with 10 L of aerated filtered seawater (Chan et al., 1999). Seawater for depuration was collected from Clovelly Bay (33°540 49S 151°160 00E), a coastal inlet isolated from any major sources of contamination. After depuration, oysters were frozen at 80 °C until analyses. The size of the oysters and the numbers that survived deployment was recorded. This enabled us to assess whether growth and mortality were directly affected by the dredging operations and whether any such effects may confound our conclusions regarding bioaccumulation. 2.4. Sample analysis Three oysters of the initial ten were randomly selected from each site, at each time, for analysis of metal accumulation. In preparation for analysis, the shell from each oyster was removed and the soft tissues rinsed in Milli QÒ water to remove any residual shell fragments. All instruments were acid washed (10% HNO3 for 24 h) plastic or stainless steel. Each oyster was then placed into individual 70 ml sample vials and freeze-dried for a period of 72 h then weighed. The tissue from each freeze-dried oyster was ground separately using a mortar and pestle and 0.40 g of each oyster sample was placed into a 100 ml Teflon polytetraflouroacetate (PFA) digestion vessel with 5 ml of Milli QÒ water, 3 ml of Nitric Acid (2% conc., Aristar Grade) and 3 ml of hydrogen peroxide. Each sample was microwave digested (Milestone Ethos) at 100 °C for 10 min then at 200 °C for 10 min. Milli QÒ water was then added to dilute each sample up to 30 ml.

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L.H. Hedge et al. / Marine Pollution Bulletin 58 (2009) 832–840

Botany Bay

SYDNEY-WOLLONGONG COAST

Reference Area

North

5km

Port Hacking

20km

Reference Area

Port Kembla

3km

Inner Harbour depostion Site

Dredge Sites

Inner Harbour Outer Harbour Outer Harbour Deposition Area

1km

Fig. 1. Sampled estuaries along the mid New South Wales coast; inner and outer harbours of Port Kembla (34°270 00S, 150°540 00E), Port Hacking (34°040 00S, 151°070 00E) and Botany Bay (33°590 00S, 151°110 00E). Shaded areas indicate where four oyster deployment sites were haphazardly placed at each sampling time within the reference estuaries. Four oyster sites were deployed randomly at each sampling time at many potential locations within the entire inner and outer harbours of Port Kembla, and all potential sites in the port are omitted for clarity.

Each sample was analyzed for arsenic, cadmium, cobalt, copper, iron, nickel, manganese, lead, tin and zinc simultaneously by ICPMS (Elan 6100). Due to high concentrations of zinc and copper in some samples, these two metals were reanalyzed using ICP-OES. A quality control program was run concurrently, with Standard (Certified) Reference Material NIST 1556b Oyster Tissue routinely digested in the same manner and analyzed to determine the recovery rate of metals. Reagent blanks were digested and analyzed every 20 samples and no contamination of the reagents was indicated. Recoveries were generally within 90–110% of expected, indicating an appropriate level of accuracy for these analyses.

2.5. Statistical analysis Prior to analysis, heterogeneity of variance was tested using a Cochran’s test and all metal concentrations were ln(x) transformed to meet homogeneity of variance assumptions for ANOVA. Transformation was not necessary for oyster dry weights or mortality rates Analyses of the effects of the dredging activities in Port Kembla Harbour on accumulation of the metals and the mortality and growth of oysters were tested using analysis of variance (ANOVA). Estuary was a fixed orthogonal factor with 3 levels: 1 potentially

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L.H. Hedge et al. / Marine Pollution Bulletin 58 (2009) 832–840 Table 1 Metal concentrations (mg kg1dry weight) in excavated sediments from the dredging areas within the inner harbour of Port Kembla. Reprinted with permission from Port Kembla Port Corporation. Metal

Disposal location Inner harbour

Cadmium Chromium Copper Lead Nickel Zinc

Outer harbour

East dredge site (silt and clay) (mg kg1dw)

West dredge site (silt and clay) (mg kg1dw)

(Sand and slag) (mg kg1dw)

2.2 90 76 160 0.24 977

3.6 254 80 260 33 1848

0.25 250 19a 19a 15a 148

a Indicates value is below maximum levels for safe disposal at sea (ANZECC 2000).

impacted estuary (PIE) and 2 reference estuaries (REF’s). Time was a random orthogonal factor with three levels: one ‘before’ dredging and two ‘during’ dredging times. Sites were random and nested within each estuary and sampling time. Student–Newmans–Keuls (SNK) tests were used to compare means for significant factors or interactions. An effect of the dredging activity was defined as any change in metal accumulation of the oysters within the dredged port from before to during the dredging, relative to the reference estuaries. 3. Results 3.1. Inner harbour Dredging, and the resultant resuspension of dredged material, substantially affected the accumulation of several trace metals in

the deployed oysters. In particular, zinc, copper and tin all showed greater concentrations in the oysters transplanted to the inner harbour during the dredging operations, than those placed in the reference estuaries during the same period (Table 2, Fig. 2). Before dredging, the accumulation of zinc was similar within the inner harbour and the reference estuaries, but with the commencement of dredging activities the accumulation of zinc increased by approximately 100% at Port Kembla. Concentrations of zinc either decreased or remained similar in the reference estuaries throughout the three sampling periods (Fig. 2). In the second ‘During’ round of sampling (‘During 2’; Table 2, Fig. 2) the concentration of zinc in the inner harbour oysters increased by over 200% from pre dredge levels. Similarly, copper concentrations were alike for all estuaries prior to dredging, yet were elevated by approximately 100% in the inner harbour oysters for both ‘During’ periods of sampling (Table 2, Fig. 2). Tin and lead concentrations in the oysters transplanted to the inner harbour were greater than those transplanted into the reference estuaries even before dredging commenced. Tin concentrations also increased in oysters deployed within the inner harbour during the dredging program, above that which was already present prior to dredging (Table 2, Fig. 2). Conversely, lead did not show this increase in accumulation above that which was already present before the dredging program (Table 2, Fig. 2). Elevations in the concentration of iron and cobalt in oysters deployed to the inner harbour were also observed (Table 2, Fig. 2). These elevations were not as great as zinc, copper, and tin and were only apparent during the first ‘during’ period of sampling (Fig. 2). While elevations in cadmium and nickel concentrations were also seen in oysters deployed to the inner harbour, oysters deployed to the reference sites also showed these general increases (Table 2, Fig. 2). This indicates that observed increases cannot be directly attributable to the resuspension event. Measured

Table 2 Analysis of variance to test for the effects of metal accumulation within S. glomerata in response to dredging activities within the inner harbour of Port Kembla. Bold indicates significant term at p < 0.05. Results of Student–Newman–Keuls (SNK) tests for differences between means for significant terms are presented below. T1,T2,T3: Sampling period 1, 2 and 3; BB: Botany Bay, PH: Port Hacking, PK: Port Kembla. Source

Estuary Time Est  Time Si(Es  Ti) Residual Total SNK Analysis

Source

Estuary Time Est  Time Si(Es  Ti) Residual Total SNK Analysis

df

2 2 4 27 72 107

Zn

Cu

2 2 4 27 72 107

Fe

Sn

p

MS

p

MS

p

MS

p

MS

p

4.918 6.389 1.584 1.560 0.096

0.153 <0.001 <0.001 0.052

6.153 1.295 2.251 0.41 0.201

0.178 0.059 <0.01 <0.01

35.321 0.522 1.910 0.176 0.079

<0.01 0.069 <0.001 <0.01

1.030 1.085 0.337 0.100 0.074

0.157 <0.001 <0.05 0.157

35.923 1.560 0.996 0.364 0.203

<0.01 <0.05 <0.05 <0.05

T1: BB = PK > PH T2: BB < PH < PK T3: BB = PH < PK BB: T2 < T1 = T3 PH: T1 = T2 < T3 PK: T1 = T2 < T3 df

Pb

MS

Co

T1: BB = PH = PK T2: BB < PH < PK T3: BB = PH < PK BB: T2 < T1 = T3 PH: T1 = T2 = T3 PK: T1 = T2 = T3 Cd

T1: BB = PH < PK T2: BB = PH < PK T3: BB > PH < PK BB: T1 = T2 = T3 PH: T1 > T2 > T3 PK: T1 < T2 = T3 Mn

T1: BB > PH = PK T2: BB = PH < PK T2: BB = PH,PK > PH, BB = PK BB: T1 = T2 = T3 PH: T1 = T2 = T3 PK: T1 < T2 = T3 As

T1: BB = PH < PK T2: BB < PH < PK T3: BB = PH < PK BB: T1 = T2 = T3 PH: T1 = T2 > T3 PK: T1 = T2 = T3 Ni

MS

p

MS

p

MS

p

MS

p

MS

p

2.291 0.621 0.481 0.070 0.047

0.211 <0.01 <0.001 0.090

3.357 20.557 0.765 0.388 0.051

0.098 <0.01 0.127 <0.001

0.437 20.629 0.641 0.457 0.462

0.556 <0.001 0.259 0.496

0.432 2.624 0.097 0.065 0.047

0.096 <0.01 0.229 0.145

1.141 3.514 1.011 0.601 0.045

0.409 <0.01 0.183 <0.001

T1: BB > PK = PH T2: BB = PH < PK T3: BB = PK > PH BB: T1 > T2,T1 = T3, T2 = T3 PH: T1 = T2 = T3 PK: T18T2 = T3

T1 < T3 < T2

T1 = T2 > T3

T3 < T1 < T2

T1 < T2 = T3

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L.H. Hedge et al. / Marine Pollution Bulletin 58 (2009) 832–840 0.75

1500

7500

Copper

Zinc

750

3750

0

1 Before

2 Time

During

3

8

0.375

0

1 Before

mg kg -1 d.w

Time

During

3

2 Time

During

3

8

0

1 Before

2

During

Time

3

2

During

0

1 Before

3

0

3

2 Time

During

3

15

Arsenic

Nickel

15

Time

During

Cobalt

30

4

2 Time

0.145

Cadmium

1 Before

1 Before

0.9

150

1 Before

0

Iron

4

0

2

300

Lead

0

Tin

7.5

1 Before

2 Time

During

3

0

1 Before

2 Time

During

3

60

Manganese

Reference Estuary- Botany Bay Reference Estuary- Port Hacking PIL- Inner Harbour, Port Kembla PIL- Outer Harbour, Port Kembla

30

0

1 Before

2 Time

During

3

Fig. 2. Mean (±SE) tissue concentrations of metals within S. glomerata transplanted to the inner and outer harbour of Port Kembla and 2 reference estuaries; Port Hacking and Botany Bay. PIL: Potentially Impacted Location. Concentrations in mg kg1 dry weight.

concentrations of the other metals did not display and clear trends related to the resuspension (Table 2, Fig. 2). The dry weight and mortality rate of S. glomerata from the inner harbour of Port Kembla showed no effects of the dredging operations (Table 3, Fig. 3). 3.2. Outer harbour The resuspension of contaminated sediment caused by dredging activities in Port Kembla Harbour substantially affected the accumulation of several metals in oysters transplanted to the outer harbour (Table 4, Fig. 2). The elevations in concentrations of metals

in the deployed oysters, however, were not as great as those observed in the inner harbour. The effects of dredging were clearest for copper (Table 4, Fig. 2). The dredging activities had a large effect in the second ‘during’ period of sampling when the accumulation of copper increased by approximately 150% in the outer harbour, while remaining relatively stable in the reference estuaries (‘During 2’, Table 4, Fig. 2). This increase was even greater than that observed in the inner harbour. Zinc also showed an increase in accumulation related to the dredging activities (Table 4, Fig. 2). Tin concentrations were over 100% higher in the oysters transplanted to the outer harbour of Port Kembla than those

L.H. Hedge et al. / Marine Pollution Bulletin 58 (2009) 832–840 Table 3 Analysis of variance to test for effects of dumping dredged sediment on dry weight and Mortality in S. glomerata transplanted to the outer and inner harbour of Port Kembla and 2 reference estuaries, Botany Bay and Port Hacking. Bold indicates significant term at p < 0.05. Results of Student–Newman–Keuls (SNK) tests for differences between means for significant terms are presented belowa. T1,T2,T3: Sampling period 1,2 and 3; BB: Botany Bay, PH: Port Hacking, PK: Port Kembla. Dry weight df Outer harbour comparison Estuary 2 Time 2 Es  Ti 4 Si(Es  Ti) 27 RES 108 SNK*

Inner harbour comparison Estuary 2 Time 2 Es  Ti 4 Si(Es  Ti) 27 RES 108

Mortality

MS

p

df

MS

p

0.51 3.17 0.87 0.85 0.16

0.56 0.13 0.41 <0.01

2 2 3

102.30 62.60 193.35

0.63 0.35 <0.05

35

65.46 T1: BB = PH = PK T2: BB = PK < PH T3: BB = PK = PH

0.44 6.39 1.3 1.06 0.15

0.67 0.08 0.32 <0.001

2 2 4

305.67 125.91 137.82

27

62.68

0.22 0.72 0.09

*

Only mortality rate in each estuary, as a function of time, is presented for clarity. No clear patterns were observed for each Time period, in each estuary.

4

i. Dry Weight

g

3

2

1

0

1 Before

2

During

Time 35

Estuary Reference Estaury- Botany Bay Reference Estruary- Port Hacking PIL- Inner Harbour, Port Kembla PIL- Outer Harbour, Port Kembla

ii. Mortality

30 25

%

3

20 15 10 5 0

1 Before

2

During

3

Time Fig. 3. Mean (±SE) (i) dry weights (g d.w.) and (ii) mortality rates (% of original 10 alive) of S. glomerata transplanted to both Outer and inner harbours of Port Kembla and two reference estuaries; Port Hacking and Botany Bay.

transplanted into the reference estuaries. Again, this elevation was seen before dredging had commenced (Table 4, Fig. 2). This indicates that, akin to the inner harbour, elevated accumulation of this metal was already occurring in the outer harbour prior to dredging operations. Concentrations of tin also increased in magnitude during the dredging program (Fig. 2). Lead concentrations were also substantially higher (i.e. over 300%) in oysters from the outer harbour than at the reference estuaries. This difference did not, however, increase with the onset of the dredging activities.

837

While iron, cobalt, cadmium, nickel increased in concentration during the dredging operations in Port Kembla, these changes are also seen in the reference estuaries, indicating that they were not affected by the dredging activities. (Table 4, Fig. 2). Dry weights of oysters showed site variation, both within the reference estuaries and the outer harbour of Port Kembla, however no higher level factors were detected (Table 3, Fig. 3). Mortality rates also showed no clear patterns (Table 3, Fig. 3).

4. Discussion The accumulation of several metals in oyster tissue increased substantially with the commencement of dredging activities in Port Kembla, compared to reference estuaries. Effects were large, with some metals showing over 100% increases in concentrations in both the inner and outer harbours. These patterns of metal accumulation clearly indicate that the resuspension of contaminated sediments can expose organisms in the water column to substantial amounts of metal contaminants. Despite these large elevations in metal accumulation, there were no effects on the growth or mortality of S. glomerata within Port Kembla. The excellent survival of these oysters clearly confirms their usefulness as a ‘biomonitor’ of metal contamination during anthropogenic disturbances (Rainbow, 2006; Robinson et al., 2005). Moreover, the similar growth and survivorship of oysters among estuaries means that our analyses of accumulation were not confounded by differences in these variables. Oyster metal levels during the dredging in Port Kembla not only exceeded our reference estuary concentrations but were greater than levels recorded in previous bioaccumulation studies conducted in nearby estuaries. Robinson et al. (2005) found copper concentrations ranging from 50–100 lg g1 in three year old S. glomerata from several estuaries in New South Wales (cf. 400 lg g1 in the current study). They also found zinc concentrations of approximately 1000–2000 lg g1 (Robinson et al., 2005), well below the 6000 lg g1 found in oysters deployed to the inner harbour during dredging. These results suggest that the resuspension of contaminated sediments caused increases in metal accumulation in the deployed oysters, greater than the natural accumulation of metals in nearby estuaries. The accumulation of metals by S. glomerata can occur via both dissolved and particulate pathways. The remobilization of copper, zinc and tin can occur when anoxic sediment is disturbed and oxidation of previously metal sulfide species takes place. This releases bioavailable metal ions into the water column that are subsequently adsorbed through the gills of marine organisms (Förstner et al., 1989; Simpson et al., 1998). Additionally, uptake of metals can also occur via an oysters diet (Wang and Fisher, 1999). The importance of each route of uptake is highly species specific and can vary dramatically with environmental factors (Allison et al., 1998; Ke and Wang, 2002; Luoma, 1989; Wang and Fisher, 1999). Metal uptake via diet has been shown to be an important factor in accumulation by many other invertebrate species (Luoma, 1995) and can be usefully studied using radio-labelled tracers and biokinetic modeling (Rainbow, 2006). It is important to note that using filter feeding organisms, such as oysters, will give an ‘overall’ measurement of the accumulation caused by both particle ingestion and membrane transport ( Rainbow, 1995; Rainbow, 2006). In the assessment of metal availability following an anthropogenic disturbance, it can be argued that this form of total measurement is a useful indicator for management and port authorities. Lead and tin concentrations in the transplanted S. glomerata from Port Kembla were much greater than either Botany Bay or Port Hacking at all times. This indicates an ongoing chronic disturbance within the Port for these metals. While inorganic tin has

838 Table 4 Analysis of variance to test for the effects of metal accumulation within S. glomerata in response to dredging activities in the outer harbour of Port Kembla. Bold indicates significant term at p < 0.05. Results of Student–Newman–Keuls (SNK) tests for differences between means for significant terms are presented below. T1,T2,T3: Sampling period 1,2 and 3; BB: Botany Bay; PH: Port Hacking; PK: Port Kembla. Source

2 2 4 27 72 107

Source

df

Estuary Time Est  Time Si(Es  Ti) Residual Total SNK analysis

2 2 4 27 72 107

Zn

Cu

Sn

Pb

Fe

MS

p

MS

p

MS

p

MS

p

MS

p

1.288 9.500 1.310 1.610 0.098

0.450 <0.001 <0.001 0.052

7.948 4.977 2.275 0.503 0.153

0.132 <0.001 <0.01 <0.001

23.486 0.471 1.387 0.224 0.088

<0.05 0.142 <0.001 <0.05

27.304 1.716 1.180 0.426 0.216

<0.001 <0.05 <0.05 <0.001

0.820 0.544 0.078 0.106 0.075

<0.05 <0.05 0.574 0.127

T1: BB > PK = PH T2: BB < PH = PK T3: BB = PH < PK BB: T1 = T3 > T2 PH: T1 = T2 < T3 PK: T1 > T2 < T3 Co

T1: BB = PH = PK T2: BB < PH = PK T3: BB = PH < PK BB: T1 = T3 > T2 PH: T1 = T3 = T2 PK: T1 = T2 < T3 As

T1: BB = PH < PK T2: BB = PH < PK T3: BB > PH < PK BB: T1 = T3 = T2 PH: T1 > T2 > T3 PK: T1 = T2 < T3 Mn

T1: BB = PH < PK T2: BB = PH < PK T3: BB = PH < PK BB: T1 = T3 = T2 PH: T1 > T3,T1 = T2, T2 = T3 PK: T1 = T3 = T2 Cd

T1 < T3,T1 = T2,T2 = T3

BB = PK > PH

Ni

MS

p

MS

p

MS

p

MS

p

MS

p

2.076 0.290 0.481 0.080 0.064

0.100 <0.05 <0.05 0.228

0.328 2.402 0.171 0.069 0.051

0.261 <0.001 0.067 0.160

0.502 24.586 0.379 0.498 0.511

0.362 <0.001 0.561 0.516

3.402 12.263 0.694 0.566 0.061

<0.01 0.084 0.323 <0.001

0.553 2.145 0.843 0.588 0.046

0.400 0.190 0.250 <0.001

T1: PH < PK < BB T2: BB = PK = PK T3: BB = PK < PH BB: T1 > T2,T1 = T3, 3 = T2 PH: T1 = T2 = T3 PK: T1=T2 < T3

T3 < T1 < T2

T1 = T2 > T3

T1 = T3 < T2

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Estuary Time Est  Time Si(Es  Ti) Residual Total SNK analysis

df

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been shown to have few toxic effects (Eisler, 1989), organotins are the source of many adverse effects on marine invertebrates including oysters ( Champ, 2000; Hoffman et al., 2002; Huggett et al., 1992). Our analyses did not measure different classes of tin. In light of the current results, further assessment of organotins in oysters in Port Kembla may be warranted. Lead, however, has been shown to be deleterious to many marine organisms (Hoffman et al., 2002). Lead enrichment in the region has been attributed to airborne pollution from surrounding industry (Gillis and Birch, 2006), however, a study in the nearby Lake Illawarra found little evidence of this (Gillis and Birch, 2006). Gillis and Birch, (2006) hypothesized that estuarine sediments in Lake Illawarra (adjacent Port Kembla) were enriched with lead (also copper, cadmium, and zinc) from urban outflows from Wollongong, whose runoff also flows into Port Kembla. The elevations in lead concentrations, independent of any sediment resuspension does suggest dissolved uptake from the water column. This design, however, does not test for the source of lead, and the larger temporal scale of this contamination may be due to a variety of processes. It is concerning that high concentrations of lead and tin were observed in deployed oysters independently of dredging and further investigation on these contaminant inputs into Port Kembla may be warranted. The effect of resuspended sediment on the accumulation of metals was different between the Outer and inner harbours of Port Kembla. This could be attributable to the nature of the dredging activities in the two harbours, the greater flushing of the outer harbour or a combination of both factors. Only moderately contaminated clay and slag were deposited in the outer harbour deposition site (Table 1), while highly contaminated finer sediment was deposited within the inner harbour. Low energy dredging and dumping techniques were used in both harbours (cutter dredging, silt curtains), however, the resuspension of a portion of each type of sediment is inevitable. While resuspended sediment and remobilized metals from the outer harbour can be flushed through the nearby harbour entrance easily, the highly contaminated material from the inner harbour is retained within the basin for much longer. Thus the distribution and contaminant loads of dredged material and the abiotic influences of the waterway mediate the level of contamination affecting accumulation in the oysters. It is clear from the observed changes in metal accumulation within the references estuaries, that substantial changes to metal availability may occur in the absence of obvious anthropogenic disturbance (for example a 250% change in cadmium and 100% in zinc accumulation between Port Hacking Times 1 and 2). This highlights the temporal variation in metal availability in many estuarine systems. Due to these temporal changes in bioaccumulation, without the use of the external references a conclusive finding on a ‘‘dredging” effect would have been difficult. Sampling, for example, just the potentially disturbed locations in Port Kembla would have indicated that there were effects in the outer harbour for iron, cadmium, nickel and manganese, however by using reference locations we were able to identify these changes as a large scale perturbation in accumulation that occurred along the entire coast coincidently with the onset of dredging. Studies that only sample one disturbed location risk inferring an effect of anthropogenic disturbance that is simply the result of natural, seasonal, or other confounding factors. In this study we show that historical contamination of habitats from past industrial practices, pose a real and contemporary threat to ecosystems. We used a novel design, for a bioaccumulation study, which included suitable reference locations. This enabled a clear link between the resuspension of metal contaminated sediment and increases in the accumulation of metals by marine organisms in the water column. Dredging activities clearly have the potential to cause large scale increases in water column contamination.

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