Selenium in sediments, pore waters and benthic infauna of Lake Macquarie, New South Wales, Australia

Marine Environmental Research 47 (1999) 491±508

Selenium in sediments, pore waters and benthic infauna of Lake Macquarie, New South Wales, Australia G.M. Peters a, W.A. Maher b,*, F. Krikowa b, A.C. Roach c, H.K. Jeswani a, J.P. Barford a, V.G. Gomes a, D.D. Reible d a

Chemical Engineering Department, University of Sydney, Sydney 2006, Australia b Applied Ecology, University of Canberra, Canberra ACT 2601, Australia c New South Wales Environment Protection Authority, Bankstown 2200, Australia d South/South West Hazardous Substances Research Center, Baton Rouge, LA 70803, USA Received 1 April 1998; received in revised form 5 December 1998; accepted 20 December 1998

Abstract Measurements of selenium in sediments and benthic infauna of Lake Macquarie, an estuary on the east coast of Australia, indicate that sediments are a signi®cant source of selenium in the lake's food web. Analysis of sur®cial sediment samples indicated higher selenium concentrations near what are believed to be the main industrial sources of selenium to the lake: a smelter and a power station. Sediment cores taken from sediments in Mannering Bay, near a power station at Vales Point, contained an average of 12 times more selenium in sur®cial sections than sediment cores from Nord's Wharf, a part of the lake remote from direct inputs of selenium. The highest selenium concentration found in Mannering Bay sediments (17.2 mg/g) was 69 times the apparent background concentration at Nord's Wharf (0.25 mg/g). Pore water concentrations in Mannering Bay were also high, up to 5 mg/l compared to those at Nord's Wharf which were below detection limits (0.2 mg/l). Selenium concentrations in muscle tissues of three benthic-feeding ®sh species (Mugil cephalus, Platycephalus fuscus, Acanthopagrus australis) were signi®cantly correlated ( p < 0:05) with sur®cial sediment selenium concentration. Selenium concentrations in polychaetes and molluscs of Mannering Bay were up to 58 times higher than those from Nord's Wharf. Two benthic organisms, the eunicid polychaete Marphysa sanguinea and the bivalve mollusc Spisula trigonella, were maintained at di€erent densities in selenium-spiked sediments. Both animals accumulated selenium from the spiked sediment, con®rming that bioaccumulation from contaminated sediments occurs. Collectively, * Corresponding author. Tel.: +61-6-201-2531; fax: +61-6-210-5305; e-mail: maher@science. canberra.edu.au 0141-1136/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved. PII: S014 1-1136(99)0002 7-6

492

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

these data suggest that benthic food webs are important sources of selenium to the ®sh of Lake Macquarie. # 1999 Elsevier Science Ltd. All rights reserved. Keywords: Selenium; Lake Macquarie; Estuary; Sediments; Pore water; Biota; Bioaccumulation

1. Introduction Selenium contamination of aquatic ecosystems has been shown to cause ®sh and bird mortality (Gillespie & Baumann, 1986; Ohlendorf, Ho€man, Saiki, & Aldrich, 1986). Sublethal e€ects are also prevalent in animals exposed to high selenium concentrations and for ®sh these include oedema, reduced hematocrit and heamoglobin levels, swollen gill lamella with extensive vacuolation, degeneration of ovarian follicles and liver, myocardial and pericardial damage and chromosomal aberrations (Krishnaja & Rege, 1982; Sorensen & Bauer, 1983; Sorensen, Cumbie, Bauer, Bell, & Harlan, 1984; Gillespie & Baumann, 1986; Saiki, 1990). Concern about selenium contamination of Lake Macquarie became public after the release of reports (Roberts, 1994; Maher, Deaker, Jolley, Krikowa, & Roberts, 1997) of concentrations of selenium in mullet (Mugil cephalus) and silverbiddy (Gerres subfasciatus) that were up to 12 times the acceptable limit for human consumption (1 mg/g wet wt). The ®sh analysed in these studies were taken from areas close to coal-®red power stations. Subsequently, the Hunter Public Health Unit conducted a study in which mullet, luderick (Girella tricuspidata), trumpeter whiting (Sillago maculata), yellow®n bream (Acanthopagrus australis) and dusky ¯athead (Platatycephalus fuscus) were caught from most parts of Lake Macquarie and trace metal concentrations measured (Wlodarczkyk & Beath, 1997). The results obtained by these studies, when compared to the selenium concentrations of Australian ®sh from unpolluted locations (Maher, Baldwin, Deaker, & Irving, 1992), showed that, on average, ®sh from Lake Macquarie contained six times the selenium concentration of those taken from unpolluted areas. In the case of mullet, the average selenium concentrations in ®sh from Lake Macquarie were found to be fourteen times higher than the national average. It has been shown in previous studies (e.g. Fowler & Benayoun, 1976a; Lui, Yang, Hu, Harrison, & Price, 1987; Zhang, Hu, Huang, & Harrison, 1990) that food chain accumulation is the major route of selenium bioaccumulation in marine animals. Selenium concentrated in organic detritus in sediments is thought to be more important than that dissolved in water in contaminating food webs (Canton and Van Derveer, 1997). High concentrations of selenium in Lake Macquarie sediments have been reported. Batley (1987) measured a selenium concentration of 14 mg/g in a single sediment core from Cockle Bay at the northern end of Lake Macquarie (Fig. 1), which receives discharges from smelting operations. Carroll, Nobbs, and Smith (1996) measured selenium concentrations in sur®cial sediments of up to 1.94 mg/g at Bennet Park (northeast Lake Macquarie) and up to 1.8 mg/g from the southern perimeter of Cockle Bay and adjacent to the coal-®red power station at Vales Point. Crawford et al. (1976) showed that approximately 20±40% w/w of

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

493

Fig. 1. Lake Macquarie and the Vales Point area showing sampling sites.

sediments in Wyee Bay were composed of ¯y ash. Davies and Linkson (1991) subsequently reported that ¯y ash from Eraring and Vales Point power stations contained 21±22 mg/g of selenium. The chemical forms of selenium present in sediments are unknown. Selenium from smelting operations may be entering the lake as selenite, selenate or elemental

494

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

selenium. Fly ash and vapour phase selenium from power generation activities is probably elemental selenium (Andren, Klien, & Talmi, 1975). Elemental selenium is rapidly converted to selenite on oxidation (Masscheleyn, Delaune, & Patrick, 1990). In aerobic sediments selenium will exist as an oxyanion in the form of selenite, selenate or biselenite (Masscheleyn, Delaune, & Patrick, 1991a) while under reducing conditions selenium will exist as elemental selenium or metal selenides (Masscheleyn & Patrick, 1993). Selenite and selenate are readily taken up by bacteria (Carroll et al., 1998) while selenite is preferred by phytoplankton (Price, Thompson, & Harrison, 1987). Bacteria and phytoplankton probably contain selenocysteine and selenomethionine (Wrench, 1978; Doran, 1982; Bottino et al., 1984) and form the base of food chains. It was expected that high concentrations of selenium exist in sediments near power generation and smelting activities in Lake Macquarie, that benthic infauna are accumulating selenium and that contamination of ®sh is occurring in areas with contaminated sediments, i.e. via benthic food chains. In order to examine the ®rst two hypotheses we measured selenium concentrations in sur®cial sediments around the lake to identify contaminated locations. To determine if any link existed between selenium concentrations in sediment and ®sh, these values were regressed. We then focussed on a contaminated area near one of the power stations, Mannering Bay, comparing sediment, pore water and infaunal selenium concentrations with those from Nord's Wharf, a relatively uncontaminated location. Bioaccumulation experiments using Marphysa sanguinea, an omnivorous polychaete worm, and a ®lterfeeding bivalve Spisula trigonella which lives in sediment, were then conducted to con®rm that bioaccumulation of selenium from contaminated sediments would occur in these common species. 2. Study area Lake Macquarie is a large estuarine barrier lake near the city of Newcastle, New South Wales. The lake extends approximately 22 km in a north±south direction, from Cockle Creek to Chain Valley Bay. Lake Macquarie has a maximum width of about 10 km and a maximum depth of approximately 11 m, with an average depth of 8 m (Maunsell & Partners, 1974). The lake catchment occupies an area of approximately 622 km2. The lake is separated from the ocean by a narrow entrance channel and sand-bars at Swansea. The tidal range in Lake Macquarie is small with the spring tidal range being estimated to be 0.15 m at the western end of the tidal channel (Stone, 1964, cited in Roy & Peat, 1976), decreasing with distance from the entrance to 0.06 m. Despite this poor tidal exchange, the lake is marine-dominated because of minimal freshwater dilution from the two main ¯uvial inputs. Tidal currents are non-existent in the lake with the exception of the tidal channel at Swansea; winds are considered to produce larger changes in water levels in the lake than do tides (Roy & Crawford, 1984). Shallows between Swansea and Wangi Wangi Point e€ectively bar deepwater movement within the lake, therefore resulting in a division of the lake into north and south segments about this latitudinal axis. As

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

495

such, water movements in the two portions of the lake are essentially independent (Spencer, 1959). Urban development is extensive on the northern shore of the estuary while the southern shore is less developed, but urban areas have increased in the last decade. Industrial development in the north is extensive with a lead±zinc smelter, a fertiliser plant, a steel foundry, collieries and sewage treatment works. The lead±zinc smelter commenced operation in 1897, resulting in the contamination of Cockle Creek and the northern reaches of Lake Macquarie with copper, lead, zinc and cadmium (SPCC, 1983). The southern part of the estuary has two coal-®red power stations near the lake. Electric power is generated by burning coal at Eraring and Vales Point, and was previously generated at Wangi Wangi. The combined output of the two currently operating stations is 3960 MW, a large part of New South Wales' generating capacity. Over¯ow from ash dams and stack emissions associated with the coal-®red power stations are contributing trace metals to the lake (Davies and Linkson, 1991). 3. Methods 3.1. Sampling Sediment sampling sites are shown in Fig. 1. Sur®cial sediments were collected from below seagrass beds using a stainless steel shovel, and only the top 30 mm retained for analysis. This sediment was placed in acid-washed polyethylene vials and frozen until analysis. Sediment cores were collected at Mannering Bay and Nord's Wharf using acid-washed polycarbonate tubes. Capped cores were kept cool during transport to the laboratory where they were frozen prior to sectioning for sediment analysis. Four sediment cores were also taken from Mannering Bay and from Nord's Wharf for pore water analysis. Benthic animals were collected by hand or by sieving of grab sediment samples and frozen until analysed. Attempts were made to collect the same organisms from both locations but not all species were present at each site. 3.2. Bioaccumulation experiments Sediments from Nord's Wharf were sieved through a 2-mm nylon mesh and 24 l of sediment (<2 mm) was rolled in a 60-l drum for 36 h to ensure homogeneity. 8 l of sediment was removed to be used as uncontaminated experimental controls. The remainder was rolled for a further 48 h after addition of seawater spiked with selenite to raise the selenium concentration in the sediment to 12 mg/g dry mass and then decanted immediately into the mesocosm cells. Sediments were spiked with selenite as this is the major chemical form expected in aerobic sediments (Masscheleyn et al., 1990, 1991a) and will be converted to elemental selenium or insoluble metal selenides under reducing conditions (Masscheleyn & Patrick, 1993).

496

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

A recirculating aquarium system was built in which water was puri®ed by passage through a shell grit ®lter. Mesocosm cells (1.4 l) were placed within this system and 1 l of sediment added to each cell. The ®nal sediment/water ratio in mesocosms was 0.3 v/v. Experiments using the polychaete Marphysa sanguinea (Eunicidae) and the mactrid bivalve Spisula trigonella (Mactridae) were conducted to determine the accumulation of selenium from selenium-spiked sediments. Marphysa sanguinea is a deposit feeder whereas Spisula trigonella is a suspension feeder. Animals were added to the sediment mesocosm cells after a 3-day settling period which allowed the sediments to revert to their normal redox pro®les. Redox potential was measured using a platinum electrode and an Ag/AgCl reference electrode. The sediment cores were aerobic in the top 5 mm and anaerobic below this zone. Marphysa sanguinea were added to three selenium-spiked and non-spiked cells: at densities of 1899/m2. Spisula trigonella were similarly added to three selenium-spiked and non-spiked cells at densities of 506/m2. The population densities were chosen to re¯ect the range of their natural abundances. A total of 30 Spisula trigonella and 18 Marphysa sanguinea were exposed to spiked sediment. Animals were exposed for 20 days and selenium concentrations determined only in live organisms. Composite samples (n ˆ 2) from each of the 12 mesocosm cells were analysed. The number of living animals were counted at the end of each experiment and percent mortality calculated. 3.3. Analysis 3.3.1. Chemical Sur®cial sediment samples were wet-sieved to collect the <100 mm fraction. Freeze-dried sediment (0.5±0.6 g) was digested with 5 ml of 15 M Aristar nitric acid in a microwave oven at 90 C for 20 min. Selenium was determined in the digests by electrothermal atomic absorption spectroscopy using a palladium±magnesium nitrate modi®er (Deaker & Maher, 1995). The marine sediment reference material NIST 1646 was digested and analysed along with the sur®cial sediment samples. The mean result was 0.70‹0.14 mg/g (n ˆ 10; non-certi®ed value, 0.6 mg/g). The sediment core samples were digested using the ®nal step of the European Community Bureau of Reference sequential extraction method described in Ure, Quevauviller, Muntau, and Griepink (1993). Selenium was determined in the digests by atomic absorption spectrophotometry (Fio & Fujii, 1990). The National Research Council of Canada marine standard reference material PACS-1, was digested and analysed with sediment core material. The mean result was 0.86‹0.26 mg/g (n ˆ 10) and was consistent with the certi®ed value of 1.09‹0.11 mg/g. For pore waters, the top 30 mm of each core was sectioned into 10-mm sections in a nitrogen glove box on arrival at the laboratory and centrifuged to separate the water. It was not possible to collect pore waters in sucient quantities to analyse individual sediment core sections; thus, combined extracts of the same section from two adjacent cores were analysed. Selenium was determined in the pore water samples by atomic absorption spectrophotometry (Fio & Fujii, 1990).

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

497

Animals were placed in seawater and allowed to purge their gut contents for at least 12 h prior to freeze drying. Approximately 0.1 g of sample was analysed by microwave digestion using 15 M nitric acid as described by Deaker and Maher (1997) and selenium determined by electrothermal furnace atomic absorption spectroscopy using a palladium±magnesium nitrate modi®er (Deaker & Maher, 1995). Analysis of two reference materials NIST 1566 oyster tissue (2.08‹0.20 mg/g) and NRCC Tort 1 lobster hepatopancreas (6.88‹0.40 mg/g), were in agreement with certi®ed values (2.2‹0.20 and 7.0‹0.30 mg/g, respectively). 3.3.2. Statistical All statistical analyses were performed using SAS (SAS, 1989). Data was tested for homogenity of variance and log-transformed where required. A one-way analysis of variance (ANOVA) followed by a Student Newman Keuls (SNK) test was used to determine if there was a signi®cant di€erence in sur®cial sediment selenium concentration between sites and to order sites from highest to lowest selenium concentration. t-tests were used to determine if there were signi®cant di€erences in selenium concentration of individual and classes (polychaetes, molluscs) of benthic organisms between sites. A two-way ANOVA (organism and sediment selenium concentration as factors) was used to determine if signi®cant bioaccumulation of selenium by Spisula trigonella and Marphysa sanguinea from spiked sediments had occurred. 4. Results Sediment data (sur®cial, cores, pore water) indicate much higher selenium concentrations at Mannering Bay than Nord's Wharf. A similar pattern exists for ®sh and benthic invertebrates even though the invertebrate taxa from the two sites were di€erent. 4.1. Sur®cial sediments, sediment cores and pore water Selenium concentrations in sur®cial sediment samples ranged from 0.1 to 12 mg/g dry mass (Table 1). Analysis of variance followed by a SNK test showed that the selenium concentrations were signi®cantly di€erent between sites (F ˆ 14:05, p < 0:0001, df 54). The highest average concentration of selenium was found at Mannering Bay (8.8‹2.0 mg/g) followed by the sediments located just east of the Vales Point Power Station in Chain Valley Bay (5.6‹3.1 mg/g) then Warners Bay (4.9‹2.0 mg/g), Swansea (4.6‹0.4 mg/g) and Wyee Bay (3.4‹0.3 mg/g). All other sites had lower selenium concentrations and were not signi®cantly di€erent (0.4±2.5 mg/g). Analysis of the core pro®les showed that the highest mean selenium concentration in the Mannering Bay cores (10.5‹3.4 mg/g) occurs between 40 and 50 mm below the surface (Fig. 2), and the mean selenium concentration falls to <3 mg/g below a depth of 200 mm. The highest selenium concentration found in an individual

498

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

Table 1 Selenium in sur®cial Lake Macquarie sediments Site

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

Location

Wyee Bay Bonnells Bay Dora Creek Myuna Bay Wangi Wangi Bay Kilaben Bay Fennell Bay Cockle Bay Warners Bay Croudace Bay Belmont Bay Swansea Nord's Wharf Chain Valley Bay Mannering Bay

Selenium (mg/g dry mass) Range

n

Mean‹SD

3.3±4.0 1.5±3.0 0.6±2.1 1.0±1.5 1.0±1.7 0.1±1.0 1.4±1.9 2.0±3.3 4.3±6.7 0.1±1.7 0.4±1.0 4.2±5.1 0.3±1.1 1.5±10 5.0±12

5 5 3 3 3 3 3 3 6 3 3 3 4 4 9

3.4‹0.3 2.2‹0.6 1.5‹0.6 1.2‹0.6 1.5‹0.6 0.4‹0.8 1.7‹0.2 2.5‹0.6 4.9‹2.0 0.8‹0.7 0.7‹0.2 4.6‹0.4 0.7‹0.2 5.6‹3.1 8.8‹2.0

15 14 9 12 1 8 2 7 5 3 4 10 11 13 6a ± ±±±±±±±±±± ±±±±±±±±±± ±±±±±±±±± ±±±±±±±±±±±±±±±±±±±±±±±± a Sites are arranged in order of decreasing selenium concentration as obtained by the Student Newman Keuls test with underlined values not signi®cantly di€erent ( p < 0:05) from one another.

sediment core at Mannering Bay was 17.2 mg/g between 30 and 40 mm below the surface. At Nord's Wharf (Fig. 3) the highest mean selenium concentration (1.71‹0.37 mg/g) was found between 180 and 200 mm depth and the selenium concentration falls to 0.25 mg/g at 250 mm. The maximum selenium concentration measured in an individual sediment core at Nord's Wharf was 2.7 mg/g, found at a depth of 140 mm. Selenium pore water concentrations in the top 25 mm of sediments in Mannering Bay were in the range of 0.3 to 5.0 mg/l (Fig. 3). Selenium concentrations in pore waters progressively decreased with sediment depth. Selenium concentrations in sediment pore waters from Nord's Wharf were all below the detection limit (<0.20 mg/l). 4.2. Fish and benthic infauna Using the sediment and ®sh data from the studies of Roberts (1994), and Wlodarczkyk and Beath (1997), we calculated the correlations between the sur®cial sediment and ®sh muscle selenium concentrations for each site (Table 2). There was a signi®cant relationship between the mean concentration of selenium in the muscle tissue and sediments for the benthos-feeding ®sh mullet, ¯athead and bream, but not whiting or ludrick.

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

499

Fig. 2. Selenium concentrations of core sediment pro®les (means‹SD, n ˆ 4).

Fig. 3. Selenium in Mannering Bay sediment pore waters (means‹SD, n ˆ 2).

Selenium concentrations in polychaetes and molluscs from Mannering Bay were all signi®cantly higher ( p < 0:005) than those collected from Nord's Wharf. The mean concentration of selenium in polychaetes and molluscs were, respectively, 11 and ®ve times higher at Mannering Bay than at Nord's Wharf (Table 3).

0.21±0.32 (0.28)

na

0.35

Luderick (Girella tricuspidata)

Tarwhine (Rhabdosargus sarba)

Averagec 1.52

0.3±4 (0.96)

na

0.46±12 (1.6)

1.19

na

0.47±1.68 (0.97)

na

0.45±3.44 (1.49)

0.80±1.90 (1.35)

0.33±3.47 (1.03)

0.81±1.93 (1.13)

Lake Macquarie (Wlodarczkyk & Beath, 1997)

Average concentrations are in parentheses. na, not available; ns, not signi®cant ( p ˆ 0:05). a Maher, unpublished data. b Uses Roberts (1994) and Wlodarczkyk and Beath (1997) data. c Uses all data in each publication.

na

0.10±0.60 (0.35)

Yellow®n bream (Acanthopagrus australis)

Silverbiddy (Gerres subfasciatus)

na

0.10±0.33 (0.21)a

Dusky ¯athead (Platycephalus fuscus) na

0.30±13 (2.0)

0.1±0.3 (0.14)

Mullet (Mugil cephalus)

na

Lake Macquarie (Roberts, 1994)

0.26±0.49 (0.37)

Background (Maher et al., 1992)

Selenium concentration (mg/g wet mass)

Trumpeter whiting (Sillago maculata)

Species

r2 ˆ 0:3097 ns

y ˆ 0:12x ‡ 1:2, r2 ˆ 0:3980, ( p ˆ 0:01)

y ˆ 0:11x ‡ 1:1, r2 ˆ 0:5622, ( p ˆ 0:05)

y ˆ 0:13x ‡ 0:8, r2 ˆ 0:7399, ( p ˆ 0:05)

r2 =0.1875 ns

Selenium in muscle tissues and sur®cial sedimentsb

Correlation

Table 2 Selenium in Lake Macquarie ®sh compared with other Australian data and correlation with sur®cial sediment selenium concentration

500 G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

501

Table 3 Selenium concentrations in benthic fauna. Organism

Selenium (mg/g dry mass) Nord's Wharf

Molluscs Tellina deltoidalis Laternula tasmanica Anadara trapezia Trichamya hirsuta Ostrea angasi Tapes watlingi All molluscs Polychaetes

Mannering Bay

n

Range

Mean‹SD

11 120 15 8 6 160

0.9±6.0 1.3±11.0 2.2±7.5 3.0±9.9 3.3±8.5 0.9±11.0

2.9‹1.7 4.4‹1.5 3.7‹0.3 5.1‹1.6 4.6‹0.8 4.1‹0.8

15

2.1±9.0

3.8‹1.6

n

Range

Mean‹SD

16 20 6 9

12±52 14±44 7.3±20 8±17

32‹19 30‹11 14‹6.4 12‹2

51

7.3±52

22‹11

11

16±70

41‹23

4.3. Bioaccumulation experiments Marphysa sanguinea and Spisula trigonella both accumulated signi®cantly more selenium (F ˆ 27:9, p < 0:0005) from the selenium-spiked sediment (Fig. 4). The concentration of selenium in both organisms was not signi®cantly di€erent before exposure (F ˆ 1:84, p ˆ 0:19; 2.5‹1.4 and 3.4‹0.8 mg/g, respectively) and contained approximately three times the amount of selenium after exposure (7.2‹1.9 and 8.9‹3.2 mg/g, respectively). Spiking the sediments resulted in pore water selenium concentrations (<10 mg/l) that were well below those known to impair bacteria or phytoplankton growth (Price et al., 1987; Zhang et al., 1990; Carroll et al., 1998). Organisms had enough food to sustain them throughout the period of the study as the selenium concentrations in the control animals did not decrease with time. Fifty-®ve of the Spisula trigonella (92%) survived to the end of the experiment. For Marphysa sanguinea, 61% of the animals survived until the end of the experiment. All the control animals, both worms and bivalves, survived the full 20 days in the non-spiked sediment. 5. Discussion 5.1. Sur®cial sediments, sediment cores and pore waters Analysis of selenium concentrations in sur®cial sediments from around the lake showed that sediments in close proximity to the Boolaroo lead±zinc smelter (Site 9) and Vales Point Power Station (Sites 1, 14 and 15) have signi®cantly higher sediment selenium concentrations than other sites. Site 8 in Cockle Creek near the lead±zinc smelter had the next highest selenium concentration. This was expected as these industries are known to release selenium into Lake Macquarie. Data for selenium concentrations in comparable uncontaminated sediments are not available; however,

502

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

Fig. 4. Selenium bioaccumulation in Marphysa sanguinea and Spisula trigonella (means‹SD, n ˆ 6).

all but one sur®cial sample contained selenium concentrations greater than 0.25 mg/g of selenium, the approximate background concentration as indicated by analysis of sediment cores (Fig. 2). Thus the entire lake appears to be contaminated with selenium, suggesting atmospheric deposition or rapid pelagic mixing. The high concentration of selenium in sediments close to the Swansea Channel (Site 12) was unexpected. Dredging in the Swansea Channel occurred from 1975 to 1981 to allow barges carrying heavy equipment for the power stations to enter into the lake (AWACS, 1995) and intermittently since then to allow commercial ®shing boats to enter the lake. Sediment core pro®les from a relatively unpolluted location show sub-surface maxima for selenium (Fig. 2). It is possible that during dredging, sediment containing higher sub-surface concentrations of selenium was dumped near Swansea and mixed with less contaminated sur®cial sediment resulting in higher apparent sur®cial selenium concentrations at this site. Seagrass detritus also accumulates at this location (and in Warners Bay, Site 9) because of the prevailing winds and currents. Seagrasses from this location contain 0.47‹0.12 mg/g dry mass (n ˆ 12) so detritus is not likely to cause an enrichment of selenium at this site. Selenium concentrations in the Mannering Bay sediment cores were much higher and closer to the surface than in the Nord's Wharf sediments (Fig. 2). This indicates more recent deposition of selenium or selenium-contaminated sediments. Given the proximity between Mannering Lake ash dam and Mannering Bay it is likely that the ash dam is the source of selenium, with particulate selenium released from the dam being deposited in Mannering Bay by gravitational settling. Selenium found in Nord's Wharf sediments has probably come from atmospheric emissions or settled in detritus after bioaccumulation. Even at Nord's Wharf, the selenium concentrations measured in the top 250 mm are above background concentrations (Fig. 2) indicating that selenium contamination is probably lake-wide to some degree. Average selenium concentrations in sediment cores from Mannering Bay diminish from a maximum of 11 mg/g at 45 mm depth to less than 1 mg/g at 350 mm. Batley

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

503

(1987) found a similar maximum concentration (14 mg/g) near the mouth of Cockle Creek in northern Lake Macquarie but a `plateau value' of 4 mg/g at a depth of 350±400 mm, in a 450-mm core. This apparent background concentration is much higher than that found at Nord's Wharf in this study, but this may be explained by the longer period of selenium contamination and, hence, depth of contamination at Cockle Creek, which has been occurring since smelting operations started in 1897. The highest selenium concentrations measured in the Mannering Bay sediment cores are well within the typical bioturbation zones of common invertebrates such as callianassids and large polychaetes (100±200 mm; Reineck & Singh, 1986). Bioturbation is known to cause a variety of changes in sediments, including the acceleration of pore water exchange, physical mixing and localised oxidation of sediments (Aller, 1982; Peters, Maher, Barford, Gomes, & Reible, 1996). The mobility of selenium is highly dependent on its redox state. Reducing conditions, expected in sediments below the redox discontinuity level, the depth at which a sudden decrease in redox potential occurs, results in selenium solubility being controlled by the formation of elemental selenium or insoluble metal selenides such as FeSe (Masscheleyn & Patrick, 1993; Peters, Maher, Barford, & Gomes, 1997). These forms of selenium can be expected to remain immobilised in anoxic sediments (Elrashidi, Adriano, Workman, & Lindsay, 1987). Release of selenium into pore water can be expected when selenides and elemental selenium are oxidised to selenate and selenite. As reducing conditions and high concentrations of selenium are present in super®cial sediments below about 20 mm, the potential for this selenium to be remobilised via oxygenation of sediments during bioturbation exists. The pore water selenium concentrations measured at Mannering Bay are much higher than the pore water concentrations in the sediments from Nord's Wharf. The average in the top 30 mm was 1.86‹1.5 mg/l compared with <0.20 mg/l at Nord's Wharf. Selenium concentrations in pore waters are still well below aqueous selenium concentrations that have been shown to be toxic to freshwater ®sh communities (Crane, Flower, Holmes, & Watson, 1992) and marine microalgae (Hollibaugh, Seibert, & Thomas, 1980; Wong & Oliveira, 1991a, b) or to cause the elimination of aquatic species (Davis, Maier, & Knight, 1988; Besser, Gan®eld, & La Point, 1993). 5.2. Fish and benthic in fauna Signi®cant correlations between selenium concentrations in ®sh muscle tissue and sur®cial sediments were found for mullet, ¯athead and bream (Table 2). Mullet mainly consume benthic microalgae and consume detritus-rich mud as a consequence of this diet. Flathead and bream are predators, feeding not only on small ®sh but crustaceans and polychaetes, i.e. sediment-dwelling organisms (Kailola et al., 1993). The sediment-related selenium concentrations for these species are consistent with the work of Fowler and Benayoun (1976a) and Zhang et al. (1990) which showed that selenium bioaccumulation was most likely to occur through food chains. Given that these ®sh have a degree of mobility in the lake and were sampled throughout the bay forming each site while the sediment samples were taken from within the seagrass zone, the correlations are surprisingly good. Each of these

504

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

factors would be expected to mask correlations between sediment and ®sh muscle selenium concentrations. Whiting also eat polychaetes, crustaceans and molluscs (Kailola et al., 1993) but no signi®cant relationship of selenium concentration in muscle tissue and sur®cial sediments was found. Adult luderick are predominantly herbivorous, feeding on seagrasses and ®lamentous algae (Kailola et al., 1993). Juveniles are omnivorous, but these were not sampled in any of the studies. Again a poor correlation with sediment selenium concentration was found. At this time we can only speculate as to why whiting and luderick selenium concentrations are not correlated to the selenium concentrations in sediments. These species may feed on organisms that are low in selenium. Seagrasses typically only contain selenium concentrations of 0.2±0.9 mg/g dry mass (Maher, unpublished data). Whiting tend to move into deep water as they grow older (Kailola et al., 1993); these sediments are further from known selenium sources, more sandy and sediments and benthic organisms are likely to have lower selenium concentrations. Variations in sources of selenium and metabolism have been shown to a€ect the uptake and retention of trace metals within and between marine species. (Cossa, Bourget, Pouliot, Piuze, & Chanut, 1980). There may also be di€erent metabolic requirements for selenium between species. As selenium concentration in organisms is a product of net uptake minus net elimination, i.e. net retention (Fowler & Benayoun, 1976b), interspecies di€erences in uptake, retention and elimination will cause di€erences in selenium concentration. Clearly molluscs and polychaetes are accumulating more selenium at Mannering Bay than at Nord's Wharf (Table 3). This is consistent with the ®ndings of other studies that have shown that if sediment is contaminated with selenium, benthos will have higher selenium concentrations than those considered to be background or unpolluted (Johns, Luoma, & Elrod, 1988). The selenium concentrations found in Trichamya hirsuta and Anadara trapezia from Nord's Wharf (3.7 and 4.4 mg/g dry mass, respectively) are similar to those reported by Batley (1987) for hairy mussels and cockles (3.3 and 6.4 mg/g dry mass, respectively) from Fennell Bay (near Site 7) which has a similar sur®cial sediment selenium concentration. Background concentrations in invertebrates sampled from uncontaminated areas are usually between 1 and 3 mg/g of selenium dry mass (Maher, 1983; Johns et al., 1988; Maher et al., 1992; Goede, Wolterbeek, & Koese, 1993). Selenium concentrations found in molluscs from Nord's Wharf have an average selenium concentration of 4.4‹0.8 mg/g which is above this range. Selenium concentrations of some individual organisms are much higher than the average (up to 1.3 to 11 mg/g) supporting the sur®cial sediment data that indicated that sediments throughout the lake are contaminated with selenium. 5.3. Bioaccumulation experiments Analysis of animal tissues clearly showed that both the polychaete Marphysa sanguinea and the bivalve Spisula trigonella accumulated signi®cant amounts of selenium from the contaminated environment to which they were exposed (Fig. 4).

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

505

Marphysa sanguinea are deposit feeders and it was expected that they would accumulate selenium from the sediments or associated pore waters. In this experiment, the bioaccumulation of selenium by Marphysa sanguinea may have involved dermal absorption from pore waters or have resulted from absorption of selenium from contaminated sediments in the polychaetes' digestive tracts. Alkaline conditions, as can be expected in invertebrate digestive tracts, can result in increased solubilisation of selenium (Masscheleyn, Delaune, & Patrick, 1991b). The bioaccumulation of selenium by Spisula trigonella, a ®lter feeder, is likely to have occurred via a number of pathways involving the ingestion of water, algae, microorganisms and sediment particles. It is known that benthic bivalves can directly accumulate selenium from sediment particles (Luoma et al., 1992). We know that Anandara trapezia, another ®lter-feeding bivalve which accumulates selenium (Table 3; Maher et al., 1997), bioaccumulates trace elements via dissolved or suspended phases (Scanes, 1993). This indicates the possible signi®cance of dissolved selenium in pore waters for the accumulation of selenium by ®lter-feeding bivalves. Pore water selenium concentrations were high in the selenium-spiked contaminated mesocosm sediments (10 mg/l). It is likely that the Spisula trigonella in this experiment accumulated selenium directly or indirectly from pore waters. Marphysa sanguinea had a relatively high death rate compared with Spisula trigonella. Being entirely di€erent phyla they may have a di€erent tolerance to selenium pollution. It should be noted that the sediments from which the Marphysa sanguinea were obtained were relatively uncontaminated with trace metals while Spisula trigonella were obtained from a site contaminated with trace metals but not selenium. Survival may have also been related to pre-exposure to trace metalcontaminated sediments. 6. Conclusions Analysis of selenium concentrations in sur®cial sediments from around the lake showed that sediments in close proximity to the Boolaroo lead±zinc smelter (Warners Bay, Cockle Creek) and Vales Point Power Station (Mannering Bay, Wyee Bay, Chain Valley Bay) have higher sediment selenium concentrations. Higher selenium concentrations were found in pore waters, benthic invertebrates and ®sh associated with highly contaminated sediments. Bioaccumulation experiments con®rm that sediment-dwelling organisms accumulate selenium from contaminated sediments. Collectively, these data suggest that the benthic food webs are important sources of selenium to the ®sh of Lake Macquarie. Acknowledgements The researchers gratefully acknowledge the ®nancial support of the Australian Research Council, Lake Macquarie City Council and Power Coal.

506

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

References Aller, R. C. (1982). The e€ects of macrobenthos on chemical properties of marine sediment and overlying water. In P. L. McCall, & M. J. S. Tevesz (Eds.), Animal±Sediment Relations. (pp. 53±102). New York: Plenum Press. Andren, A. W., Klien, D. H., & Talmi, Y. (1975). Selenium in coal ®red steam plant emissions. Environmental Science and Technology, 9, 856±858. AWACS (1995). Lake Macquarie estuarine process study (AWACS Report 94/25). Australian Water and Coastal Studies Pty Ltd, Manly Vale, NSW, Australia. Batley, G. E. (1987). Heavy metal speciation in waters, sediment and biota from Lake Macquarie, New South Wales. Australian Journal of Freshwater Research, 38, 591±606. Besser, J. M., Gan®eld, T. J., & La Point, T. W. (1993). Bioaccumulation of organic and inorganic selenium in a laboratory food chain. Environmental Toxicology and Chemistry, 12, 57±72. Bottino, N. R., Banks, C. H., Irgolic, K. J., Micks, P., Wheeler, A. E., & Zingaro, R. A. (1984). Selenium containing amino acids and proteins in marine algae. Phytochemistry, 23, 2445±2452. Canton, S. P., & Van Derveer, W. D. (1997). Selenium toxicity to wildlife: an argument for sediment based water quality criteria. Environmental Toxicology and Chemistry, 16, 1255±1259. Carroll, B. I., Peters, G. M., Barford, J. P., Nobbs, D. M., Maher, W. A., & Chapman, P. (1998). Microbial and redox dependent aspects of selenium biogeochemistry in a selenium contaminated lakeÐ Lake Macquarie, NSW. Proceedings of the 2nd International Conference on Environmental Management (pp. 221±228). Wollongong, 10±13 Feb. Oxford: Elsevier. Carroll, B. I., Nobbs, D. M., & Smith, G. (1996). Characterisation of selenium bioavailability by two sequential extraction methods in sediments from an estuarine lake subject to anthropogenic selenium input. Proceedings of the Asia Paci®c Conference on Sustainable Energy and Environmental Technology, 19±21 June. World Scienti®c Publishing Company, Singapore, pp. 72±79. Cossa, D., Bourget, E., Pouliot, D., Piuze, J., & Chanut, J. P. (1980). Geographical and seasonal variations in the relationship between trace metal content and body weight in Mytilus edulis. Marine Biology, 58, 7±14. Crane, M., Flower, T., Holmes, D., & Watson, S. (1992). The toxicity of selenium in experimental freshwater ponds. Archives of Environmental Contamination and Toxicology, 23, 440±452. Crawford, E. A., Roy, P. S., Brooks, K., Zamberlain, A., Scott, T., MacKay, N. J., & Chvojka, R. (1976). Heavy metals in bottom sediments and ®sh from Lake Macquarie (Report GS1976/283). Geological Survey of New South Wales, NSW Dept. of Mineral Resources, St Leonard, NSW, Australia. Davies, W. A., & Linkson, P.B. (1991). Selenium discharge from power station ash dams: Eraring, Vales point. Quantity, speciation and strategies for control. Department of Chemical Engineering, University of Sydney, Sydney. Davis, E. A., Maier, K. J., & Knight, A. (1988). The biological consequences of selenium in aquatic ecosystems. California Agriculture, 1, 18±20. Deaker, M., & Maher, W. (1995). Determination of selenium in seleno compounds and marine biological tissues using electrothermal atomisation atomic absorption spectroscopy. Journal of Analytical Atomic Spectroscopy, 10, 423±431. Deaker, M., & Maher, W. (1997). Low volume microwave digestion for the determination of selenium in marine biological tissues by graphite furnace atomic absorption spectroscopy. Anal. Chimica Acta, 350, 287±295. Doran, J. W. (1982). Microorganisms and the biological cycling of selenium. In K. C. Marshall (Ed.), Advances in microbial ecology (Vol. 6, pp. 1±32). New York: Plenum Publishing Corporation. Elrashidi, M. A., Adriano, D. C., Workman, S. M., & Lindsay, W. L. (1987). Chemical equilibria of selenium in soils: a theoretical development. Soil Sci., 144, 141±152. Fio, F. L., & Fujii, R. (1990). Selenium speciation methods and application to soil saturation extracts from San Joaquin Valley, California. Soil Science Society of America Journal, 54, 363±369. Fowler, S. W., & Benayoun, G. (1976a). Selenium kinetics in marine zooplankton. Marine Science Communications, 2, 43±67. Fowler, S., & Benayoun, G. (1976b). In¯uence of environmental factors on selenium ¯ux in two marine invertebrates. Marine Biology, 37, 59±68.

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

507

Gillespie, R. B., & Baumann, P. C. (1986). E€ects of high tissue concentrations of selenium on reproduction by bluegills. Transactions of the American Fisheries Society, 115, 208±213. Goede, A. A., Wolterbeek, H. T., & Koese, M. J. (1993). Selenium concentrations in the marine invertebrates Macoma balthica, Mytilus edulis, and Nereis diversicolor. Archives of Environmental Contamination and Toxicology, 25, 85±89. Hollibaugh, J. T., Seibert, D. L. R., & Thomas, W. H. (1980). A comparison of the acute toxicities of ten heavy metals to phytoplankton from Saanich Inlet, B.C., Canada. Estuarine and Coastal Marine Science, 10, 93±105. Johns, C., Luoma, S. N., & Elrod, S. N. (1988). Selenium accumulation in benthic bivalves and ®ne sediments of San Francisco Bay, the Sacramento±San Joaquin Delta and selected tributaries. Estuarine and Coastal Shelf Science, 27, 381±396. Kailola, P., Williams, M. J., Stewart, P. C., Reichelt, R. E., McNee, A., & Grieve, C. (1993) Australian ®sheries resources. Bureau of Resource Sciences and the Fisheries Research and Development Corporation, Commonwealth of Australia, Canberra. Krishnaja, A. P., & Rege, M. S. (1982). Induction of chromosomal aberrations in ®sh Boleophthalmus dussumerieri after exposure in vivo to mitomycin C and heavy metals mercury, selenium and chromiun. Mutation Research, 102, 71±82. Lui, D. L., Yang, Y. P., Hu, M. H., Harrison, P. J., & Price, N. M. (1987). Selenium content of marine food chain organisms from the coast of China. Marine Environmental Research, 22, 151±165. Luoma, S. N., Johns, C., Fisher, N. S., Steinberg, N. A., Oremland, R. S., & Reinfelder, J. R. (1992). Determination of selenium bioavailability to a benthic bivalve from particulate and solute pathways. Environmental Science Technology, 26, 485±491. Maher, W. A. (1983). Selenium in marine organisms from St Vincent Gulf. South Australia. Marine Pollution Bulletin, 14, 35±36. Maher, W., Baldwin, S., Deaker, M., & Irving, M. (1992). Characteristics of selenium in Australian marine biota. Applied Organometallic Chemistry, 6, 103±112. Maher, W., Deaker, M., Jolley, D., Krikowa, F., & Roberts, B. (1997). Selenium occurrence, distribution and speciation in the cockle Anadara trapezia and the mullet Mugil cephalus. Applied Organometal Chemistry, 11, 313±326. Masscheleyn, P. H., & Patrick, W. H. (1993). Biogeochemical processes a€ecting selenium cycling in wetlands. Environmental Toxicology and Chemistry, 12, 2235±2243. Masscheleyn, P. H., Delaune, R. D., & Patrick, W. H. (1990). Transformations of selenium as a€ected by sediment oxidation±reduction potential and pH. Environmental Science and Technology, 24, 91±96. Masscheleyn, P. H., Delaune, R. D., & Patrick, W. H. (1991a). Biogeochemical behaviour of selenium in anoxic soils and sediments an equilibrium thermodynamic approach. Journal of Environmental Science and Health, 26A, 555±573. Masscheleyn, P. H., Delaune, R. D., & Patrick, W. H. (1991b). Arsenic and selenium chemistry as a€ected by sediment redox potential and pH. Journal of Environmental Quality, 20, 522±527. Maunsell, & Partners (1974). Lake Macquarie foreshore study. Report for the Department of Public Works, New South Wales. Ohlendorf, H. M., Ho€man, D. J., Saiki, M. K., & Aldrich, T. W. (1986). Embryonic mortality and abnormalities of aquatic birds: apparent impacts of selenium from irrigation drainwater. Science of the Total Environment, 52, 49±63. Peters, G. M., Maher, W. A., Barford, J. P, Gomes, V. G., & Reible, D. D. (1996). Bioturbation e€ects on selenium mobility. Proceedings of the Interactions Between Sediments and WaterÐ7th International Symposium on Sediment Water Science, 22±25 September, Baveno, Italy, p. 151. Peters, G. M., Maher, W. A., Barford, J. P., & Gomes, V. G. (1997). Selenium associations in estuarine sediments: redox e€ects. Journal of Water, Air and Soil Pollution, 99, 275±282. Price, N. M., Thompson, P. A., & Harrison, P. J. (1987). Selenium: an essential element for the growth of the coastal marine diaton Thalassiosira pseudonana. Journal of Phycology, 23, 1±9. Roberts, B. (1994). The accumulation and distribution of selenium in sea mullet (Mugil cephalus) from Lake Macquarie, NSW, Australia. Honours thesis, University of Canberra, Canberra. Roy, P. S., & Peat, C. (1976). Bathmetry and bottom sediments of Tuross Estuary and Coila Lake. Records, Geological Survey of New South Wales, 18, 103±134.

508

G.M. Peters et al. / Marine Environmental Research 47 (1999) 491±508

Roy, P. S., & Crawford, E. H. (1984). Heavy metals in a contaminated Australian EstuaryÐDispersion and accumulation trend. Estuarine and Coastal Science, 19, 341±358. Saiki, M. K. (1990). Elemental concentrations in ®shes from the Salton sea, south eastern California. Water, Air and Soil Pollution, 52, 41±56. SAS (1989). SAS/STAT User's guide (Version 6, 4th Edition, Vol. 2). Cary, NC: SAS Institute. Scanes, P. (1993). Trace metal uptake in cockles Anadara trapezium from Lake Macquarie New South Wales. Marine Ecology Progress Series, 102, 135±142. Sorensen, E. M. B., & Bauer, T. L. (1983). Heaematological dyscrasia in telost chronically exposed to selenium-laden e‚uent. Archives of Environmental Contamination and Toxicology, 12, 135±141. Sorensen, E. M. B., Cumbie, P. M., Bauer, T. L., Bell, J. S., & Harlan, C. W. (1984). Histopathological, haematological, condition factor and organ weight changes associated with selenium contamination in ®sh from Belews Lake, North Carolina. Archives of Environmental Contamination and Toxicology, 13, 153±162. SPCC (1983). Environmental audit of Lake Macquarie. State Pollution Control Commission (now Environmental Protection Authority), New South Wales, Australia, Spencer, R. S. (1959). Some aspects of the ecology of Lake Macquarie, NSW, with regard to the alleged depletion of ®sh II. Hydrology. Australian Journal of Marine and Freshwater Research, 3, 279±296. Ure, A. M., Quevauviller, P. H., Muntau, H., & Griepink, B. (1993). Speciation of heavy metals in soils and sediments. An account of the improvement and harmonization of extraction techniques undertaken under the auspicies of the BCR of the Commission of the European Communities. International Journal of Environmental and Analytical Chemistry, 51, 135±151. Wlodarczkyk, J., & Beath, K. (1997). Heavy metals in seafood in Lake Macquarie: a cross-sectional survey (Report to the Hunter Public Health Unit). University of Newcastle Research Association, Callaghan NSW and John Wlodarczyk Consulting Services, New Lambton, New South Wales. Wong, D., & Oliveira, L. (1991a). E€ects of selenite and selenate on the growth and motility of seven species of marine microalgae. Canadian Journal of Fisheries and Aquatic Science, 48, 1193±1200. Wong, D., & Oliveira, L. (1991b). E€ects of selenite and selenate toxicity on the ultrstructure and physiology of three species of marine microalgae. Canadian Journal of Fisheries and Aquatic Science, 48, 1201±1211. Wrench, J. J. (1978). Selenium metabolism in the marine phytoplankters Tetraselmis tetrathele and Dunaliella minuta. Marine Biology, 49, 231±236. Zhang, G. H., Hu, M. H., Huang, Y. P., & Harrison, P. J. (1990). Selenium uptake and accumulation in marine phytoplankton and transfer of selenium to the clam Puditapes philippnmarium. Marine Environmental Research, 25, 179±190. Reineck, H. E., & Singh, I. B. (1986). Depositional sedimentary environments. Berlin: Springer.