The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia)

Marine Pollution Bulletin xxx (2014) xxx–xxx

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia) G.F. Birch a,⇑, A. Melwani b, J.-H. Lee a, C. Apostolatos a a b

Environmental Geology Group, School of Geosciences, The University of Sydney, NSW, Australia Department of Biological Sciences, Macquarie University, NSW, Australia

a r t i c l e

i n f o

a b s t r a c t

Keywords: Metals Saccostrea glomerata Bioaccumulation Sydney estuary Sediments Tissue

The current study aimed to examine the relationship between metals in sediments and metal bioaccumulation in oyster tissue in a highly-modified estuary (Sydney estuary, Australia). While extensive metal contamination was observed in surficial sediments, suspended particulate matter and oyster tissue, a significant relationship between these media could not be established. No relationship was determined between sediment quality guidelines and oyster size or weight, nor with human consumption levels for metals in oyster tissue. Moreover, oyster tissue metal concentrations varied greatly at a single locality over temporal scales of years. Oyster tissue at all 19 study sites exceeded consumptions levels for Cu. Bioaccumulation of metals in oyster tissue is a useful dynamic indicator of anthropogenic influence within estuaries, however oysters cannot be used in Sydney estuary as a valid biomonitor due to overriding internal regulation (homoestasis) by the animal, or by external natural (sediment resuspension) and anthropogenic (sewer/stormwater discharges) pressures, or both. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction

1995; Tanabe et al., 2000; Monirith et al., 2003; Thébault et al., 2008). Bivalve molluscs are favoured as environmental monitors due to their sessile nature, cosmopolitan abundance and their ability to concentrate contaminants while maintaining a high tolerance (Farrington and Tripp, 1995; O’Connor and Lauenstein, 2006; Lewis et al., 2010). Many studies have been conducted in Australia on uptake of contaminants by oysters (Mackay et al., 1975; Batley et al., 1992; Brown and McPherson, 1992; Peerzada and Kozlik, 1992; Hardiman and Pearson, 1995; Scanes, 1996; Scanes and Roach, 1999; Robinson et al., 2005), though only two studies have included Sydney estuary. Scanes and Roach (1999) measured the concentration of trace metals in Saccostrea glomerata from 20 estuaries on the east-coast of New South Wales (NSW) to determine background metal concentrations. Oysters in Sydney estuary (3 sites) were found to be enriched in most metals, particularly Cu, Zn and Pb, with the latter element elevated by a factor of 13 times above mean background concentrations. Dafforn et al. (2012) measured ecological response to chemical indicators (metals and polycyclic aromatic hydrocarbons) of anthropogenic stress in benthic sediment, suspended material and oyster tissue from seven NSW estuaries. Sydney estuary was included as an example of a heavily modified estuary. Sydney estuary is a deep-water, drowned valley, located on the east coast of Australia comprising several harbours (Sydney Harbour, Middle Harbour, Port Jackson), bays and tributaries

Bottom sediment and water column chemistry have been used extensively to characterise the health of estuarine environments (Birch and Taylor, 1999; Hatje et al., 2001; Simpson et al., 2005). However, these data are of limited value as these parameters fail to provide meaningful information regarding the amount of anthropogenic chemicals being transferred to the biological (flora and fauna) system. Only a fraction of sedimentary contaminants are taken up by benthic plants and animals and it is important therefore that the ‘bio-available’ fraction of sediment-bound materials be established to adequately assess estuarine health (Rainbow, 1995). Establishing a correlation between metals in sediments and uptake in biota is important to adequately interpret the impact of sedimentary contaminants on the food chain in estuarine environments. Oysters have been widely used to assess contamination of aquatic environments (Cantillo, 1998; Anstat et al., 2007). The mussel watch program, primarily a North American initiative, which monitors organic and inorganic contaminants concentrating in both mussels and oysters, has been implemented in several regions around the world, including the Mediterranean, Asia-Pacific and Central and South America (Claisse, 1989; Farrington and Tripp, ⇑ Corresponding author. Tel.: +61 2 9351 2911; fax: +61 9351 2442. E-mail address: [email protected] (G.F. Birch). 0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

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G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

(approximate area 50 km2) (Birch and Taylor, 2004). The estuary catchment is highly urbanised (86%) and was once the primary location of heavy industry within NSW. Consequently, bottom sediment in many areas of the estuary contains high levels of legacy organic and inorganic contaminants (Birch and Taylor, 1999). However, the major source of temporary contamination is stormwater discharge (Birch and Taylor, 2004; Birch and McCready, 2009). The Sydney rock oyster, S. glomerata (Gould, 1850) – formerly S. Saccostrea commercialis – is a native inhabitant of Sydney estuary. S. glomerata is a sessile organism that attaches to rocks and other hard substratum in intertidal zone throughout the estuary. Sediment metal concentrations have been widely reported for Sydney estuary (Irvine and Birch, 1998; Birch and Taylor, 1999), however the effect on local fauna is not well documented. The current study aimed to: determine the temporal variance in oyster tissue concentrations over the medium term (3 years); establish the concentrations of metals in oyster tissue throughout Sydney estuary and to compare these levels to concentrations in various size fractions of ambient bottom sediment; determine whether metals have bioaccumulated in tissue of S. glomerata to concentrations which posed a human health risk; and determine whether sediment quality guidelines were appropriate for these animals.

the surface (upper 2 cm) of the sample and stored in metal-free plastic bags. Approximately 15 oysters (S. glomerata) were gently removed from the mid-tide zone using a stainless steel pick at each site. Water samples were collected in 3 L polyethylene bottles that had been soaked in nitric acid for 24 h then washed in detergent and ultrapure water in the laboratory. Before water collection, bottles were rinsed three times with ambient water and samples were taken from under the surface of the water to avoid floating debris. All samples were taken from within close proximity to each other (5 m), and were kept on ice until transported back to the laboratory where the sediment and water samples were stored at <4 °C and the oysters frozen (<20 °C). For the temporal study, the same number of oysters was taken at Site 1 (Iron Cove, Fig. 1) as described above, over two time periods spanning a total of 30 months. The first sampling period was between June, 2005 and June, 2006, where repeated sampling of oysters occurred at random times each month in June 2005, August–September 2005, December 2005, February–April 2006, and June 2006. The second sampling period occurred between January and December, 2008, where repeated sampling occurred at random times in each month.

2. Materials and methods 2.2. Laboratory techniques 2.1. Field techniques Nineteen locations (Fig. 1) throughout Sydney estuary were sampled for oysters, sediment and suspended particulate matter (SPM) for analysis of metal concentration. Locations were chosen based on availability of oysters and included a wide range of sediment compositions and metal concentrations. Sediment (500 g), obtained using a stainless steel grab, was scraped from

Four similar sized (approximately 6 cm long, 4 cm wide and 2 cm high) oysters were selected from each of the 19 sites and for each temporal sampling. Oysters were shucked into a polyethylene vial and freeze dried for 24 h. Length, breadth and depth measurements were made of the shell and both wet- and dry-tissue weights were recorded. Tissue samples of oysters in excess of the four selected for individual analysis were pooled to create a

Fig. 1. Location of sample sites for oyster and sediment sampling.

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

blended sample for each site. Oyster tissue samples were homogenised using a stainless steel blender. For digestion, 0.3 g of tissue sample was weighed into a Teflon digestion vessel to which 5 ml of 65% HNO3 was added. Each batch (n = 20) of tissue samples, including one blank, one International Reference Material (NIST 1566b) and one internal oyster standard, was placed into a microwave digester, following a modified US EPA method 3052 and heated for 5 min from room temperature to 130 °C, then maintained at this temperature for a further 15 min, before being allowed to cool. Vessels were rinsed with ultrapure water into a 100 ml volumetric flask and made up to volume. Sediment samples were wet sieved using a 62.5 lm mesh and the fine (<62.5 lm) fraction was analysed for metals to reduce the confounding effects of variable grain size (Birch, 2003). For digestion, 0.3 g of fine sediment, 10 ml ultrapure water, 2 ml HCl and 2 ml HNO3 were heated at 120 °C for 2 h (modified US EPA method 200.8 Rev 4.4). For total sediment, 0.7 g of material was used for analysis due to reduced metal concentrations. Hydrochloric acid (HCl) digests were undertaken to estimate the bioavailability of metals in sediments (Weimin et al., 1992; Clark et al., 2000). Five grams of sediment and 25 ml of 1 M HCl were added to a centrifuge tube and these tubes were then shaken for two hours. The tubes were placed in a centrifuge for 10 min at 3200 revolutions/min and the solute was poured into sample tubes. Each batch (n = 20) of sediment samples included one blank and an International Reference Material (AGAL-10, an estuarine sediment). Interim sediment quality guidelines (ISQGs) (ANZECC/ARMCANZ, 2000) were used to identify sediments that were likely to cause adverse biological affects (Simpson et al., 2005). Two values, ISQG-L (low) and ISQG-H (high) are provided for each chemical. The lower level (ISQG-L) denotes the concentration below which adverse biological effects are seldom observed and the upper value (ISQG-H) above which adverse biological effects are expected to occur frequently. Concentrations between the two guidelines indicate an intermediate, often irregular biological response. The ANZECC/ARMCANZ (2000) guidelines are based on SQGs developed for North America (Long and MacDonald, 1998). The ISQGs low and high values are 65 and 270 lg g 1 for Cu, 50 and 220 lg g 1 for Pb and 200 and 410 lg g 1 for Zn, respectively. Sediment quality guidelines are based upon total sediment chemistry. The water samples were filtered through pre-weighed filter papers (0.45 lm cellulose nitrate filters) that were dried and reweighed before undergoing digestion to determine SPM. The filter paper was digested with 10 ml ultrapure water, 5 ml HCl and 5 ml HNO3 at 120 °C for 2 h and made up to 15 ml with ultrapure water. Sediment and tissue samples were analysed by Inductively Coupled Plasma Atomic Emission Spectra (ICP-AES) for Ca, Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb and Zn (Tables 1 and 5). However, concentrations of Cd, Co, Cr and Ni were low (1 lg g 1) and frequently below detection levels in oyster tissue, while Ca, Fe and Mn are not recognised in Sydney estuary as anthropogenic elements. The current work thus focused on the metals Cu, Pb and Zn. Accuracy for sediment analyses, expressed as percent recovery, for Cu, Pb and Zn was 95%, 101% and 98%, respectively, while precision, stated as percent relative standard deviation (RSD = standard deviation/ mean*100) was 0.8%, 1.1% and 0.7%, respectively (Table 1). Accuracy for oyster tissue for Cu, Pb and Zn was 93%, 125% and 99%, respectively and precision was 14%, 6.9% and 17% RSD, respectively. Precision calculated using an internal standard was16%, 59% and 18% RSD, respectively. A relatively high RSD for Pb was due to low concentrations for this metal (0.31 lg g 1) in the oyster standard and internal standard (8.5 lg g 1). Blank concentrations were below detection limits of 0.02 lg g 1, 0.05 lg g 1 and 0.005 lg g 1 for Cu, Pb and Zn, respectively.

3

2.3. Statistical techniques Linear regression analysis was used to examine relationships of metal concentration (Cu, Pb, and Zn) between sediment (total sediment, fine sediment, bioavailable fine sediment and SPM) concentrations and average individual oyster tissue concentrations across 19 stations in the estuary using R Statistical Software (version 2.15). Each sediment variable was analysed separately. Prior to statistical analysis, concentrations below the detection limit were substituted with half the detection limit and log10 transformed (except for Pb in oyster tissue) to meet assumptions of normality and variance homoscedasticity of residuals. Linear regressions were also performed to examine the relationship between average individual oyster tissue concentrations and oyster physical measurements (length, height, width, and weight), with the same treatment of the tissue data as described above. Additionally, the size and weight of oysters were compared among sites that exceeded the ISQG-L to those that did not for each metal using the non-parametric Mann Whitney test. Principal Component Analysis (PCA) was undertaken in an attempt to identify whether groups of locations exhibited relationships across the three metals. However, variability among sampling points was too large and no meaningful results were obtained. Therefore, the correlative relationship between metals was simply compared using Spearman’s Rank correlation of un-transformed concentrations. Linear models were assembled to examine the variation in oyster tissue concentrations due to sampling date and climatic parameters at Site 1. Since the oyster temporal sampling effort was irregular, occurring over two different sample frequencies and with a large gap in sampling; separate analyses were performed for each dataset (2005–6 and 2008). Climatic measurements of temperature, rainfall, wind speed, and wind direction were obtained from the Bureau of Meteorology (BOM 2012). Wind data represent measurements taken at Station #066022 (Fort Denison), while precipitation and temperature data were from Station #066062 (Observatory Hill). Data for each timeframe of interest were averaged by month to match with the frequency that oyster tissue sampling occurred. Tissue concentrations below the detection limit were substituted with half the detection limit and log10 transformed to meet assumptions of normality and variance homoscedasticity of residuals. Linear models were then developed using the generalized least square function in R Statistical Software (version 2.15). Potential model terms included sampling date (categorical), mean maximum air temperature, mean precipitation, mean wind velocity, and mean wind direction. Model parameters were retained based on statistical significance. Temporal autocorrelation in any significant final models was considered by examining the correlation structure of error terms with sampling month. Statistical significance in all analyses was assessed at p < 0.05.

3. Results 3.1. Surficial sediment metal concentrations Total sediment metal concentrations varied significantly throughout Sydney estuary due to the influence of variable grain size and distance from contaminant source. Areas containing significant quantities of coarse-grained material (e. g., Sites 11, 13, 14 and 19 – all with over 98% coarse-grained sediment) recorded low concentrations for all metals for total sediment, whereas Site 5 (Homebush Bay) with 96% fine-grained sediment contained the highest concentrations of Pb and Zn (Table 2). The highest concentration of Cu (180 lg g 1) was at Site 12 (Long Bay), which had an

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

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G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

Table 1 International reference materials and internal standards. Ca

Co

Cr

Cu

Fe

Mn

Ni

Pb

Zn

International reference material oyster tissue SRM 1566b Mean (n = 12) (dw) 788 2.4 SD 107.2 0.9 RSD 13.6 36.2

2.4 3.2 135.1

bd na na

67 9.3 14.0

161 131.1 81.7

18 2.6 14.4

1.7 1.6 89.1

0.4 2.7 6.9

1412 241.3 17.1

SRM 1566b Doc Val (mean) Recovery %

2.5 96

na na

na na

71.6 93

205.8 78

18.5 96

1.04 168

0.31 125

1424 99

3.5 0.3 9.2

0.4 0.1 32.5

bd na na

774 127.1 16.4

378 72.3 19.1

5.9 0.7 12.2

1 0.3 33.1

8.5 5.0 59.1

7454 1320.4 17.7

International reference material sediment AGAL-10 Mean (n = 10) 1871.0 9 SD 22.1 0 RSD 1.2 5

9 1 6

88 1 1

22.1 0.2 0.8

17,653 95 1

248.0 7.6 3.1

19 1 3

40.7 0.4 1.1

55.8 0.4 0.7

AGAL-10 Doc val (mean) SD Recovery %

9.2 1.1 94

82 11.0 107

23.2 1.9 95.0

20,000 1170 88

241 10.5 103.0

17.8 2.7 107

40.4 2.7 101.0

57.0 4.2 98.0

na na

Internal oyster tissue standard Mean (n = 11) (dw) 6166 SD 1011.8 RSD 16.4

2060 140 91.0

Cd

9.3 0.6 95

SD = standard deviation; RSD = relative standard deviation; n = number of samples. Doc val = documented value; na = not available; dw = dry weight; Bd = below detection.

even mixture of course and fine-grained sediment, but was close to a contaminant source. Fine sediment metal concentrations were most elevated at the end of bays, particularly in the south, central estuary (Sites 1 and 9) and in Middle Harbour (Site 12), whereas fine sediment metal concentrations were lowest close to the mouth of Sydney estuary (Site 14). Mean metal concentrations of bioavailable fine sediment were marginally lower than that contained in the fine fraction sediment for Cu, Pb and Zn (82%, 99% and 90%, respectively). The bioavailable fraction of fine sediment metal concentrations correlated closely with fine sediment concentrations (R2 > 0.96 for all metals). Total sediment Cu, Pb and Zn concentrations exceeded ANZECC ISQG-L at eleven sites in the Sydney estuary for at least one metal (Sites 1, 2, 5, 6, 7, 9, 10, 12 and 20, 21, 22), however only one site (Site 5 in Homebush Bay) exceeded ISQG-H (for Zn).

3.2. Suspended particulate matter (SPM) metal concentrations The highest concentration of metals in SPM was in water samples taken from Rozelle Bay (Site 9) in the central docklands area and the lowest concentrations were at Site 11 in Middle Harbour adjacent to an extensive bushland (Table 3). Limited SPM load was found at several sites (Sites 7, 14, 20 and 22), which resulted in inaccurate analyses and have been excluded from the data set. 3.3. Oyster size and weight Mean length, width and height of oysters sampled were 6.1 ± 1.5 cm, 4.0 ± 1.3 cm, and 1.9 ± 0.6 cm, respectively (n = 92), whereas mean shell weight was 32.9 ± 28.7 g and tissue weights (wet and dry) were 5.6 ± 4.2 g and 0.8 ± 0.7 g, respectively (n = 92) (Table S1).

Table 2 Bioavailable fine sediment, fine and total sediment metal concentrations in Sydney estuary (%RSD) (lg g Site

C1 C2 C3 C5 C6 C7 C9 C10 C11 C12 C13 C14 C15 C17 C19 C20 C21 C22 C23 ISQG-L ISQG-H

1

).

% Fines

Cu Bio-available fine sediment

Fine sediment

Total sediment

Pb Bio-available fine sediment

Fine sediment

Total sediment

Zn Bio-available fine sediment

Fine sediment

Total sediment

46 21 7.1 96 58 4.8 11 52 1.1 53 1.6 1.7 3.4 5.9 1.3 14 22 18 0.4

222 (3.7) 186 (7.2) 144 (3.8) 116 (1.7) 96 (4.0) 181 (5.9) 276 (2.7) 256 (47.8) 109 (15.7) 314 (2.7) 142 (18.1) 52 (10.6) 303 (18.2) 101 (24.9) 150 (2.4) 96 (13.5) 117 (5.3) 221 (26.4) 84 (3.7)

280 (2.3) 250 (4.1) 202 (3.7) 156 (2.2) 137 (0.5) 236 (4.4) 316 (4.8) 207 (1.4) 137 (10.3) 358 (1.6) 181 (4.6) 73 (16.5) 302(4.8) 140(18.2) 206 (3.3) 117 (6.7) 163 (5.0) 243 (8.5) 118 (5.3)

102 (33.4) 90 (12.1) 18 (58.0) 112 (14.9) 54 (53.5) 21 (19.6) 62(23.9) 129 (24.4) 3 (36.6) 180 (47.9) 8 (23.7) 4 (21.4) 27 (39.9) 6 (58.7) 5 (18.1) 22 (31.8) 31 (31.5) 86 (34.8) 9.1 (61.3) 65 270

506(3.6) 428 (5.1) 331 (7.0) 248 (1.8) 203 (5.2) 351 (6.9) 562 (5.7) 468 (42.6) 149 (10.6) 390 (8.8) 178 (21.9) 91 (6.6) 344 (14.9) 224 (11.7) 337 (4.8) 262 (9.0) 296 (3.4) 328 (27.5) 219 (5.9)

523 459 364 266 218 347 544 329 162 332 192 116 326 225 333 222 301 337 208

190 (30.7) 143 (16.4) 40 (20.7) 200 (13.7) 95 (41.7) 50 (30.1) 115 (17.0) 190 (33.2) 11 (34.0) 183(33.1) 15 (24.0) 11 (18.7) 39 (29.3) 19 (34.2) 13 (12.1) 54 (18.1) 59 (44.5) 97 (35.4) 25 (38.8) 50 220

897 (5.0) 840 (6.3) 550 (5.7) 601 (3.4) 636 (3.2) 626 (2.7) 979 (4.5) 695 (18.1) 264 (7.0) 572 (15.3) 327 (10.6) 176 (2.1) 344 (10.0) 420 (7.8) 544 (3.2) 474 (6.7) 511.6 (2.5) 489 (62.4) 385 (12.6)

1006 (2.7) 971 (3.2) 686 (4.4) 708 (2.6) 781 (2.8) 715 (2.9) 1076 (5.7) 671 (1.3) 294 (3.9) 611 (2.6) 375 (6.9) 217 (3.3) 401 (2.3) 479 (8.7) 620 (3.0) 428 (1.5) 611 (2.7) 475 (4.9) 412 (5.3)

390 (32.0) 281 (15.0) 55 (50.8) 495 (18.6) 321 (35.2) 56 (38.3) 197 (26.6) 263 (30.7) 12 (31.9) 355(53.0) 18 (20.2) 15 (20.0) 36 (26.1) 22 (55.7) 15(29.6) 70 (31.7) 90 (52.4) 138 (41.5) 31 (48.1) 200 410

(2.6) (3.3) (5.7) (2.2) (1.4) (3.3) (6.1) (2.5) (4.8) (2.9) (7.6) (5.0) (3.8) (8.3) (5.3) (3.2) (4.4) (6.4) (7.1)

ISQG-L = Interim sediment quality guideline – Low; ISQG-H = Interim sediment quality guideline – High. n = 4 at each site; RSD = relative standard deviation.

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

5

G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

3.4. Metal oyster tissue concentrations A summary of mean metal concentrations (dry weight) in oyster tissue are presented in Table 4 for individual animals (n = 4) and for blends (up to 15 animals). The data presented in Table 5 are mean oyster tissue concentrations (dry and wet weight) Table 3 Suspended particulate metal matter concentrations in Sydney estuary (lg L

1

).

Site

Cu

Pb

Zn

C1 C2 C3 C5 C6 C9 C11 C12 C13 C15 C17 C19 C21

43 167 84 46 39 430 50 333 139 202 70 121 90

179 424 189 181 88 718 38 267 116 191 118 231 156

185 687 315 301 212 700 54 655 174 206 173 259 233

n = 1 at each site.

Table 4 Metals in sediments (<62.5 lm) and oyster tissue for individual animals and blends (lg g Ca

with relative standard deviations for each site. Mean concentrations (dw) of Cu, Pb and Zn were 1418 lg g 1 (174–4605 lg g 1), 8.9 lg g 1 (1.3–18 lg g 1) and 6518 lg g 1 (2157–13,552 lg g 1), respectively for individual analyses with similar concentrations for pooled samples. Oyster tissue metal concentrations were spatially irregular throughout Sydney estuary with no single site having consistently high metal concentrations for all three metals in the current study (Table 5 and Figs. 2 and 3). Oysters from Long Bay (Site 12) contained the highest Cu tissue concentrations (3151 lg g 1 dw), oysters in Double Bay (Site 19) had the highest concentrations of Pb (24 lg g 1 dw), while the highest concentrations of Zn in oyster tissue were in Rozelle Bay (Site 9; 12,197 lg g 1 dw). The Australian food standards code (FSANZ, 2006) maximum concentration of metals in food for human consumption is provided on a wet weight basis (Table 5). The guideline concentration for Pb in mollusc tissue is 2.0 lg g 1 ww and oyster tissue exceeded this concentration at two sites (Sites 1 and 19), i. e. in Iron Cove and Double Bay (Although not reported here, the guideline for Cd is also 2.0 lg g 1 ww and this concentration was not exceed anywhere in the estuary). The current food standards code does not set maximum concentrations for Cu and Zn, however the previous code (ANZFA, 1998) set levels for Cu and Zn at 70 and

1

dw).

Cd

Co

Cr

Cu

Fe

Mn

Ni

Pb

Zn

Sediments (<62.5 lm) (n = 90) Mean 1677 Max 19,002 Min 15

24,268 101,386 Bd

4.1 14 Bd

56 234 3.7

117 286 47

12,270 48,588 103

29,029 50,461 109

168 777 23

128 536 13

489 1031 185

Individual oysters (n = 90) Mean 11,877 Max 55,766 Min 1252

2.5 7.5 Bd

0.3 0.8 Bd

1.2 3.6 Bd

1419 4606 174

275 784 91

7.2 19.7 2.6

2.8 6.2 Bd

8.9 18.0 1.3

6518 13,552 2157

Oyster blends (n = 23) Mean 10,758 Max 44,315 Min 7945

2.9 5.9 Bd

0.3 0.5 Bd

1.3 3.8 Bd

1419 2985 290

273 653 95

6.3 7.2 5.8

1.8 4.4 Bd

7.7 17.5 2.4

6991 13,897 2876

Bd = Below detection.

Table 5 Dry and wet weight oyster tissue concentrations (lg g Site

C1 C2 C3 C5 C6 C7 C9 C10 C11 C12 C13 C14 C15 C17 C19 C20 C21 C22 C23 Guidelines Backgrounda

1

) (%RSD).

Dry weight

Wet weight

Cu

Pb

Zn

Cu

Pb

Zn

681 (7.5) 763 (49.7) 1043 (5.6) 661 (19.5) 751 (50.6) 1179 (18.1) 1147 (46.6) 1314 (15.7) 1114 (18.0) 3151 (6.4) 1248 (41.8) 1205 (11.9) 1412 (23.2) 1369 (33.9) 1606 (12.5) 1437 (26.2) 1687 (28.1) 2962 (40.4) 1273 (23.5)

12.1 (26.4) 8.1 (24.1) 5.7 (19.0) 1.8 (1.2) 7.7 (0.5) 8.0 (49.8) 11.0 (20.4) 9.0 (18.7) 3.4 (56.2) 16 (Bd) 3.9 (Bd) Bd 5.1 (46.6) 13.7 (43.7) 23.8 (16.9) 10.5 (60.4) 7.8 (29.3) 11.2 (40.5) 3.8 (20.8)

5137 (19.1) 5230 (45.7) 5934 (13.6) 7840 (12.1) 8649 (50.4) 4650 (20.8) 12,197 (15.7) 6827 (15.0) 4402 (12.9) 6862 (23.5) 5365 (40.7) 6869 (25.3) 6119 (22.6) 6038 (33.4) 6630 (13.3) 7567 (37.8) 5161 (33.1) 5812 (41.2) 6697 (11.7) 70 21.6

138 (17.5) 103 (73.5) 172 (4.5) 132 (15.9) 107 (55.3) 176 (21.2) 141 (29.7) 176 (46.0) 148 (10.0) 311 (15.1) 202 (37.5) 183 (38.8) 213 (51.6) 162 (30.4) 162 (26.5) 208 (62.6) 213 (26.3) 460 (56.5) 171 (21.2) 2.0 0.085

2.5 (44.8) 1.3 (29.6) 1.0 (10.0) 0.4 (2.7) 1.1 (1.8) 1.2 (55.4) 1.5 (34.6) 1.3 (44.2) 0.5 (69.7) Bd 0.6 (13.5) Bd 0.8 (69.5) 1.6 (56.4) 2.4 (28.6) 1.2 (62.6) 0.9 (33.8) 1.8 (40.6) 0.5 (48.1) 1000 277

1071 (38.8) 700 (72.6) 978 (12.6) 1575 (15.1) 1232 (55.0) 689 (21.2) 1314 (12.5) 988 (66.9) 592 (14.7) 734 (26.0) 867 (36.1) 845 (25.9) 892 (51.6) 705 (20.7) 662 (20.8) 840 (35.5) 681 (33.3) 888 (58.7) 919 (22.9)

n = 4 at each site; RSD = relative standard deviation; Bd = below detection. Guidelines: Cu – FSANZ, 2006; Pb and Zn – ANZFA, 1998. a Scanes and Roach, 1999.

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

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1000 lg g 1 ww, respectively. These levels were exceeded at every site for Cu and at four sites for Zn (Iron Cove, Site 1; Homebush Bay, Sites 5, 6; and Rozelle Bay, Site 9). 3.5. Temporal variance in tissue metal concentrations at Iron Cove Metal concentrations measured at irregular times each month at Iron Cove (Site 1) between June 2005 and June 2006, and January–December, 2008 varied substantially (Tables S2 and S3 and Fig. 4). Across the entire temporal dataset, Cu, Pb and Zn in oyster tissue ranged from 463–2947 lg g 1, 4.0–43 lg/g and 3018– 19,851 lg g 1 dw, respectively, which is similar to the variance exhibited by the spatial tissue dataset, i.e. 174–4606 lg/g, 1.3– 28 lg g 1 and 993–13,552 lg g 1 dw for Cu, Pb and Zn, respectively. Standard deviations for the spatio-temporal data sets were also similar for the three metals (Table 6 and Figs. 3 and 4). Temporal variance for the fine fraction of the sediment over the entire sampling period at Iron Cove was considerably smaller than for the oyster tissue, i. e. 220–278 lg g 1, 425–501 lg g 1 and 888– 1152 lg g 1 for Cu, Pb and Zn, respectively (Table 6). The RSDs for oyster tissue for the 30 months of sampling were 40%, 47% and 34% for the oyster tissue and 5.1%, 3.8% and 7.7% for Cu, Pb and Zn in the fine sediment, respectively. Generalized linear models constructed to examine the relationship of oyster concentrations at Site 1 (Iron Cove) only revealed a significant effect of sampling date. Neither of the metals exhibited a statistically significant model with climate data in either the 2005–6 or 2008 sampling and no temporal autocorrelation remained in the final models (all correlation coefficients were <0.1). Differences in Cu and Zn concentrations due to sampling date were evident for certain months; however these differences did not appear to follow a consistent pattern (Fig. 5). In 2005–6 sampling, Zn was significantly lower in April 2006 (p = 0.002) relative to other months. Copper was significantly lower in August 2005

(p = 0.02) and April 2006 (p < 0.001), and significantly higher in March (p = 0.005) and June 2006 (p = 0.006). During 2008 sampling, Cu and Zn were highly variable in December and lower in July and August. Lead concentrations did not significantly differ by sampling date. Visually, Pb concentrations appeared to be relatively stable during 2008, but exhibited high degree of variation in 2006. 3.6. Regression analysis 3.6.1. Relationship between total/fine sediment and SPM concentrations and oyster tissue concentrations Lead concentrations in oyster tissue exhibited the strongest relationships to sediment concentrations with significant regressions using total sediment (R2 = 0.323, p = 0.006), the bioavailable fraction of the fine sediment (R2 = 0.437, p < 0.001) and fine fraction (R2 = 0.359, p = 0.003) (Table 7 and Fig. 5). Zinc tissue concentrations were weakly (R2 = 0.307, p = 0.049) related with the suspended particulate fraction of Zn. Copper tissue concentrations were not statistically correlated with any sediment size fraction. A close relationship was observed between the metal content of SPM and the fine fraction (Cu R2 = 0.812, p < 0.0001; Pb R2 = 0.812, p < 0.0001 and Zn R2 = 0.603, p0.0001), as well as for the bioavailable fraction of fine sediment Pb (R2 = 0.673, p < 0.0001) and Cu (R2 = 0.632, p = 0.0001). 3.6.2. Relationship between animal size and tissue concentration Regression analysis showed significant relationships between size (length and width) and weight with Cu tissue concentrations (Table S4). The amount of variation explained in tissue Zn concentrations was relatively weak when regressed against shell length (R2 = 0.310, p = 0.006) and width (R2 = 0.212, p = 0.027). Lead did not relate to any size/weight variable. Size/weight variables were also highly correlated with each other.

Fig. 2. Bar graphs of Cu, Pb and Zn in oyster tissue (dry weight) at 19 sites in Sydney estuary. Sites where oyster tissue wet weight Pb concentrations exceed consumption guidelines (>2 lg g 1 wet weight) are marked with a black triangle and where wet weight Zn exceed consumption guidelines (>1000 lg g 1 wet weight) are marked with a star. Oyster tissue Cu concentrations (ww) exceed guidelines (70 lg g 1 ww) at all sites.

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

7

Fig. 3. Box plot of (a) Cu, (b) Pb and (c) Zn in oyster tissue (dry weight) for 19 sites in Sydney estuary. Horizontal line is the mean, lower/upper bounds of boxes are the 25th and 75th percentiles, respectively, and dots indicate outliers.

3.6.3. Relationship between oyster size/weight and sediment quality guidelines The size and weight of oysters from sites which exceeded ISQGL were no different to oysters from sites where sediment metal concentrations did not exceed these levels. 4. Discussion 4.1. Oyster tissue metal concentrations Metal tissue concentrations in the current study are high (Hunter et al., 1995; Jaffe et al., 1998; Frias-Espericueta et al., 1999; Abbe et al., 2000; Han et al., 2000; Soto-Jimenez et al., 2001) in comparison to other global studies (Table 8). In a world-wide study

Cantillo (1998) found mean oyster tissue concentrations to be 160 lg g 1, 2.5 lg g 1 and 1600 lg g 1 dw for Cu, Pb and Zn, respectively, i.e. considerably lower than the average for Sydney estuary (1419 lg g 1, 8.9 lg g 1 and 6518 lg g 1 dw for Cu, Pb and Zn, respectively). However, significantly higher concentrations of Cu and Pb (5110 lg g 1 and 14.5 lg g 1 dw, respectively) have been reported in Japan (Szefer et al., 1997). Most studies conducted in Australia have reported considerably lower metal concentrations in oyster tissue than in the current study (Mackay et al., 1975; Batley et al., 1992; Brown and McPherson, 1992; Hardiman and Pearson, 1995; Spooner et al., 2003) (Table 8). Exceptions are the Tamar River, Tasmania where high levels of Cu and Zn have been reported in oyster tissue, i.e. 372–1527 lg g 1 dw and 2200–14,700 lg g 1 dw, respectively

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

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G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

Fig. 4. Bivariate plots of (a) oyster Pb (ww) vs fine (<62.5 m) sediment Pb (dw) (R2 = 0.374), and (b) oyster Pb (ww) vs bioavailabe fine (<62.5 m) sediment Pb (dw) (R2 = 347). Grey region is the 95% confidence interval of the regression line.

Table 6 Variance in temporal and spatial data for oyster tissue and sediment. Cu Temporal tissue data from site 1 (n = 96) Mean 1424 Std Dev 575 RSD (%) 40 Max 2947 Min 463

Pb

Zn

15.2 7.1 47 43 4.0

8959 3010 34 19,851 3018

Spatial tissue data for individual animals for all 20 sites (n = 80) Mean 1419 8.9 SD 748 5.4 RSD (%) 53 61 Max 4606 28 Min 174 1.3

6518 2318 36 13,552 993

Temporal fine (<62.5 lm) sediment data from site 1 (n = 28) Mean 255 472 SD 13 18 RSD (%) 5.1 3.8 Max 278 501 Min 220 426

1027 80 7.7 1152 888

(Ayling, 1974) and exceptionally high concentrations of Pb (17–83 lg g 1 ww) in Darwin Harbour, Northern Territory compared to Sydney estuary (0.4–2.5 lg/g ww) (Peerzada and Kozlik, 1992). In the other investigations of oyster tissue metal concentrations in Sydney estuary, Scanes and Roach (1999) recorded levels of Cu, Pb and Zn at 149–160, 0.85–1.11 and 861–1176 lg g 1 ww, respectively, i.e. lower than the present study (103–460 lg g 1, 0.4–2.5 lg g–1 and 592–1575 lg g 1 ww, respectively). Maximum enrichment over background concentrations (Scanes and Roach, 1999) (on a wet weight basis) was 21, 29 and 6 for Cu, Pb and Zn, respectively. Daffron et al. (2012) recorded mean tissue concentrations of 263, 3 and 1449 lg g 1 dw for Cu, Pb and Zn, respectively, considerably lower than the present study (1419, 8.9 and 6518 lg g 1 dw, respectively). 4.2. Temporal variance in oyster tissue concentrations The magnitude of variance in concentrations of metals in oyster tissue at a single location (Site 1) over a 30-month period was considerably greater than variance exhibited by metals in fine sediment at the same location over the same time, i. e. RSDs between 34% and 47% for oyster tissue compared to between 4% and 8% RSDs for fine sediment over the same time (Table 6). Minor temporal variance for metals in low energy estuarine environments has been reported previously where RSDs of 12%, 3.7% and 5.0%,

respectively were obtained over a period of 75 months (Birch et al., 2001). Relationships were examined between tissue concentrations and climatic parameters to determine their influence on the magnitude and kinetics of metal uptake and bioaccumulation. Sydney estuary is prone to extensive resuspension of bottom sediment, especially in shallow parts of embayments during summer months (up to 67% of the total area of the estuary is estimated to be affected by suspension, Taylor, 2000) when north-easterly winds frequently blow in excess of 30 kts. Site 1, where the long-term temporal study of oyster tissue was undertaken, receives the full force of these winds for extended durations and resuspension is frequently observed at this location. Site 1 in Iron Cove is also in close proximity to two large stormwater canals, which during episodic high-precipitation events, may deliver large quantities of polluted catchment water to the upper parts of the embayment (e. g. Apeti et al., 2011). Tissue metal concentrations can vary substantially during November and February when spawning occurs, due to export of contaminants by sperm and eggs (e. g. Chen and Chen, 2003). Metal variation in oyster tissue was examined for possible relationships to time of year, as well as wind velocity and direction (resuspension), rainfall (polluted stormwater runoff), and temperature. Although, Zn and Cu were visually higher and more variable during summer 2008, no consistent pattern of statistically higher concentrations during summer sampling could be established. Similarly, no significant relationships between tissue concentrations and climatic variables were found. 4.3. Correlation between the concentration of metals in oyster tissue and bottom sediment For metals in bottom sediment to be a major source of metals in the tissue of filter-feeding animals, there would have to be a close relationship of metals in the fine fraction of surficial material and SPM. Similarities in metal concentrations between SPM and the fine fraction, as well as for the bioavailable fine fraction indicate suspended sediment is being derived from the fine fraction of ambient bottom sediments in some locations in the Sydney estuary. However, the correlation between the two phases was weak at several locations (Iron Cove, Middle Harbour) possibly due to the introduction of sediments to the estuary via runoff from the surrounding catchment, or sediment remobilisation (Birch and O’Hea, 2007; Birch and McCready, 2009). Lead concentrations (dw) in oyster tissue exhibited a moderate relationship (R2 = 0.437, p 6 0.001) to Pb sediment concentrations

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

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Fig. 5. Box plot of (a) Cu, (b) Pb and (c) Zn in oyster tissue (dry weight) at site 1 for the periods June, 2005 to June, 2006 and January, 2008 to December, 2008. Horizontal line is the mean, lower/upper bounds of boxes are the 25th and 75th percentiles, respectively, and dots indicate outliers.

in the bioavailable fraction of the fine sediment (Table 7). On wet weight basis, Pb concentrations were weakly related to both fine fraction (R2 = 0.374, p = 0.004) and the bioavailable fraction (R2 = 0.347, p = 0.006). Zinc tissue concentrations were very weakly correlated to Zn in SPM (R2 = 0.307, p = 0.049) and Cu tissue concentrations were not statistically correlated with Cu in any sediment size fraction. The poor correlation between metal concentrations in oyster tissue and total and fine sediment, as well as with SPM found in the present study suggests that for Sydney estuary, sediment metal concentrations are not a good predictor of metals in oyster tissue. A similar study of the relationship of oyster tissue concentrations and metals in these sedimentary phases by Birch and Hogg

(2011) found a significant relationship between Cu and Zn in fine sediments and oyster tissue. A strong correlation was found between Cd and Pb in oyster tissue and total sediment in San Andreas Lagoon, Mexico, but a similar relationship was not observed for Zn. This was explained by Zn being an essential element and was therefore regulated by the animal (Vazquez-Sauceda et al., 2011). A strong relationship was also found in the Persian Gulf (Iran) between Cd, Cu and Zn in oyster tissue and ambient fine (<62.5 lm) sediment (Chaharlang et al., 2012), but not for Pb due to Pb being accumulated in the shell. The poor correlation found in the current study may be due to a number of factors, including natural and anthropogenic processes and internal regulation (homoestasis) of metals by the animal.

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

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G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

Table 7 Sediment–tissue relationships (both dw). Metal

Physical variable

R2

p-Value

Cu

Total sediment Fine sediment Bioavailable fine sediment Suspended sediment

0.001 0.059 0.058 0.29

0.881 0.278 0.278 0.071

Pb

Total sediment Fine sediment Bioavailable fine sediment Suspended sediment⁄

0.323 0.359 0.437 0.171

0.006 0.003 <0.001 0.161

Zn

Total sediment Fine sediment Bioavailable fine sediment Suspended sediment

0.105 0.062 0.016 0.307

0.142 0.265 0.573 0.049

Concentrations were log transformed for all except Pb with ⁄ where only sediment was log transformed; tissue results based on mean of individual analyses; Bold values are significant.

Although ingestion of particulate matter in the water column by filter-feeding estuarine animals is an uptake pathway for contaminants (Maher et al., 1999), which may result in a relationship between metal concentrations in bottom sediment and oyster tissue, the process is complex. Anthropogenic activities, e. g. urbanization of the catchment and maritime activities result in increased concentrations of metals in coastal shellfish (Thébault et al., 2008). Natural processes, e.g. upwelling of deep oceanic water (e. g. Besada et al., 2011), run-off from volcanic regions has resulted in passive adaption and elevation of metal tissue concentrations in molluscs (Kamenev et al., 2004). Homoestasis (irregular internal regulation) of metals by marine molluscs may confound the relationship between metal concentrations in the sediment and in the organism (Fasulo et al., 2008). Sequestration of metal cations in insoluble granules and cellular metal detoxication/redistribution may result in enhanced accumulation (Viarengo and Nott, 1993; Irato et al., 2003). Internal regulation by the animal and external natural and anthropogenic pressures may confound or interrupt the relationship between metals in oyster tissue and surficial sediment. The magnitude of variance in concentrations of Cu, Pb and Zn at a single location (Site 1) over a period of 30 months, i. e. intra-site variance, renders establishing a meaningful distinction between the concentration of metals in oyster tissue on a spatial basis (inter-site variance) difficult. High temporal variance in oyster tissue metal concentrations further confounds the ability to detect any

Table 8 Mean concentrations of Cu, Pb and Zn in oyster tissue (lg g

a

spatial pattern between tissue and ambient bottom sediment. However, there appears to be a process(es) that strongly disrupts this relationship in Sydney estuary. Sediments in Chowder Bay (Site 23) are coarse and metal concentrations are low (25 lg g 1, 31 lg g 1 and 118 lg g 1 for Cu, Pb and Zn in the total sediment, respectively), but oyster tissue concentrations are high (1273 lg g 1 and 8897 lg g 1 dw for Cu and Zn, respectively). These tissue concentrations are greater than that for oysters in Iron Cove (681 lg g 1 and 5137 lg g 1 dw for Cu and Zn, respectively) (Site 1) where surficial sediment concentrations are amongst the highest in the estuary (102 lg g 1 and 390 lg g 1 dw for Cu and Zn, respectively), i.e. 10 times greater than in Chowder Bay. Many other sites in the estuary show similar disconnects between oyster tissue and bottom sediment metal concentrations. Perhaps this estuary is too complex to support such a relationship. Numerous stormwater and sewer overflow discharge points, extensive and prolonged resuspension (Wainwright, 1990), in situ-generated biological material and internal regulation by the animal itself has disrupted any relationship between metals in bottom sediment and in oyster tissue. Detailed research is ongoing into key processes controlling bioaccumulation of metals in filter-feeding animals in this estuary. 4.4. Sediment quality guidelines and human consumption of oyster tissue Recommendations of maximum concentrations of metals in sea foods are not only important for assessing risk for human consumption (Hardiman and Pearson, 1995), but stress resulting from contamination has also been shown to adversely affect the immune system of filter-feeding animals, which may trigger outbreaks of disease in aquatic organisms (Ringwood et al., 1998; Lacoste et al., 2001). Metal concentrations in oysters are therefore used to establish potential threats to human health, as well as to identify the risk of disease in the animal (Huang et al., 2007; Cevik et al., 2008; Cayir et al., 2012). Human consumption guidelines are based on wet weight tissue concentrations and SQGs are provided on a total sediment basis. The concentrations of Cu in oyster tissue exceed human consumption levels in all parts of Sydney estuary, although only 56% and 4% of bottom sediments exceed the ISQG-L and -H, respectively (Birch and Taylor, 2002a,b and c). The highest tissue Cu concentration (460 lg g 1 ww and 6.6 times the human consumption guideline value) was in oysters from Mosman Bay (Site 22) where total bottom sediment concentrations were low (86 lg g 1).

1

).

Oyster species

Location

Dry/wet wt.

Cu

Pb

Zn

Reference

Saccostrea commercialis

Port Jackson (NSW), Australia

Wet wt

Georges River (NSW), Australia Georges River (NSW), Australia Georges River (NSW), Australia Hawkesbury River (NSW), Australia Darwin Harbour (NT), Australia Tamar River (Tas), Australia Punta Cerritos, Mexico Kaneohe Bay, USA Kyushu Island, Japan Mazatlan Bay, USA World Sydney estuary

Wet wt Dry wt Wet wt Wet wt Wet wt Dry wt Dry wt Dry wt Dry wt Dry wt Dry wt Dry wt

1.2 0.9–1.1 0.3–0.7 0.4

949 861–1176 552–1970 2600 440–760 170–650 804–1139 2200–14,700 443 854

Scanes and Roach (1999)

Saccostrea commercialis Saccostrea commercialis Saccostrea commercialis Saccostrea commercialis Saccostrea sp. Crassostrea gigas Crassostrea iridescens Crassostrea gigas Crassostrea gigas Crassostrea iridescens Oyster sp. Saccostrea Glomerataa

Sydney estuary

Wet wt

193 149–175 14–93 170 19–89 20–85 24–74 372–1527 24 165 5110 42–142 160 1419 (174–4606) 193 (104–460)

0.02–0.06 17.3–83 0–4 3.1 0.6 14.5 0.9–4.6 2.5 8.9 (1.3–18) 1.2 (Bd-2.5)

370–1905 1600 6518 (2157–13,552) 949 (592–1946)

Brown and McPherson (1992) Spooner et al. (2003) Batley et al. (1992) Hardiman and Pearson (1995) Peerzada and Kozlik (1992) Ayling (1974) Frias-Espericueta et al. (1999) Hunter et al. (1995) Szefer et al. (1997) Soto-Jimenez et al. (2001) Cantillo (1998) This work This work

Formerly S. commercialis; single values are mean concentrations; Bd = below detection.

Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005

G.F. Birch et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

Copper tissue concentrations exceeded the human consumption level (70 lg g 1 ww) in areas of the waterway where total sediment Cu concentrations were SQG-L and 36% >ISQG-H for Pb, only oysters from two sites in the estuary exceeded the human consumption guideline for Pb. Total sediment mantling an estimated 63% of Sydney estuary exceeds the ISQG-L and 40% exceeded ISQG-H for Zn, however tissue Zn concentrations in only four sites exceed the human consumption guideline for Zn (1000 lg g 1 ww). Sediment quality guidelines do not predict metal tissue concentrations in oysters and do not assist in risk assessment for human consumption of oysters in Sydney estuary. 4.5. Sediment quality guidelines and oyster size and weight Total sediment metal concentrations exceeded ANZECC ISQG-H for Zn (410 lg g 1) in Homebush Bay (Site 5) (495 lg g 1) indicating elevated risk of adverse biological effects in this area of this bay due to Zn. Guidelines suggest minor risk of adverse effects in areas where sediment is consistently greater than ISQG-L guidelines (Sites 1, 2, 5, 6, 12 and 22) for at least one metal, i. e. predominately within the upper parts of Iron Cove, Homebush Bay and Long Bay (Birch and Taylor, 2002a,b and c). However, no statistically significant influence was evident on the size or weight of oysters in areas where metal concentrations in the sediment exceeded guidelines (low and high). 5. Conclusions Oyster tissue in Sydney estuary was found to be highly enriched in Cu and Zn however, the concentration of these metals was highly variable at both intra- and inter-site spatial scales throughout the estuary. Similarly, SPM and surficial sediment contain high Cu, Pb and Zn concentrations, especially at the ends of embayments in the south, central estuary. Metal concentrations in various sediment phases (total, fine, bioavailable fine and SPM) were poorly correlated with metal concentrations in oyster tissue and thus sedimentary metals were not a good predictor of metals in oyster tissue in this estuary. Oyster size and weight were not related to sediment quality, nor did these guidelines predict areas where oyster tissue exceeded human consumption levels for Cu, Pb and Zn. Further research is required to determine the processes controlling bioaccumulation of metals in oysters in Sydney estuary. Acknowledgements We thank Tom Savage and Tim Hogg for laboratory assistance and chemical analyses and Marco Olmos and Tim Gunns for GIS support. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.marpolbul.2013. 12.005.

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Please cite this article in press as: Birch, G.F., et al. The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2013.12.005