Accumulation of trace metals in grey mangrove Avicennia marina fine nutritive roots: The role of rhizosphere processes

Marine Pollution Bulletin 79 (2014) 284–292

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Accumulation of trace metals in grey mangrove Avicennia marina fine nutritive roots: The role of rhizosphere processes Punarbasu Chaudhuri a,b, Bibhash Nath a,⇑, Gavin Birch a a b

School of Geosciences, University of Sydney, Sydney, NSW 2006, Australia Department of Environmental Science, University of Calcutta, Kolkata 700 019, West Bengal, India

a r t i c l e

i n f o

Keywords: Mangrove – Avicennia marina Rhizosphere Fine nutritive roots Trace metals Sydney estuary

a b s t r a c t Mangrove sediment has long been recognized as being important in restricting the mobility of contaminants in estuarine environments. To investigate the role of rhizosphere processes in the accumulation of trace metals in mangrove fine nutritive roots, the mangrove sediments and associated fine nutritive roots are collected from five major embayments of Sydney estuary (Australia) for geochemical studies. In this estuary Avicennia marina sediments are accumulating large quantities of trace metals due to presence of abundant fine sediment (<62.5 lm) and organic matter as well as anthropogenic input. Accumulation of trace metals in fine nutritive roots responds to total sediment chemistry mainly due to rhizosphere sediment geochemical processes resulting in a strong linear correlation between metal concentrations in fine nutritive roots vs. total and bio-available contents in sediments. Accumulation of trace metals in fine nutritive roots is almost always exceeds rhizosphere total sediment metal concentrations. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction Mangroves form a unique group of intertidal ecosystems that dominate over large extents of shorelines and estuaries in tropical and subtropical regions (e.g., Harbison, 1986; Lacerda et al., 1988; MacFarlane et al., 2003; Marchand et al., 2011; Wang et al., 2013) protecting coastlines from the devastating effects of erosion, storm surges and flooding (Das and Vincent, 2009; Zhang et al., 2012). Currently, mangroves are increasingly threatened due to anthropogenic chemicals sourced from uncontrolled agricultural runoff, urban and industrial effluent and wastewaters, as well as with urbanization and population growth (MacFarlane et al., 2007; Vane et al., 2009; Polidoro et al., 2010). Among contaminants effecting mangroves, trace metals and/or metalloids contribute a significant role (Wang et al., 2013). Although mangrove rhizosphere sediments have a large potential to sequester trace metals and assist in protecting coastal marine environments from pollution (Harbison, 1986; Lacerda et al., 1988; Clark et al., 1998), changes in physico-chemical conditions may trigger release of accumulated trace metals to the sediment–water interface (Marchand et al., 2006; Keene et al., 2010; Nath et al., 2013). Avicennia marina has a complex root system, including four types of roots, i.e., cable roots, aerial roots (or pneumatophores), fine nutritive roots (or feeding roots) and anchor roots (Purnobasuki and Suzuki, 2005). These root systems are mainly encountered ⇑ Corresponding author. Tel.: +61 2 93516706. E-mail addresses: [email protected], [email protected] (B. Nath). 0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2013.11.024

within the upper 20 cm of the rhizosphere, however, the density of root systems is greater in the upper 10 cm of the sediment profile (Otero et al., 2006). Root systems, especially aerial roots, create a pathway that allows gas exchange between the atmosphere and rhizosphere sediments (Lacerda et al., 1993; Purnobasuki and Suzuki, 2005; Marchand et al., 2011). This process results in strong pore-water redox stratifications within the rhizosphere and creates an oxidized upper rhizosphere and much reduced lower rhizosphere (Lacerda et al., 1993; Clark et al., 1998; Zhou et al., 2011). Oxidation of the upper rhizosphere leads to precipitation of Fe-oxyhydroxides and formation of iron plaques around root surfaces and ultimately results in significant accumulation of trace metals in these zones (Lacerda et al., 1993; Otte et al., 1995; Zhou et al., 2011). There are two contrasting scientific understandings of the effects of Avicennia marina rhizosphere processes on the biogeochemistry of trace metals: (i) oxidation of the rhizosphere, due to root activity, strongly increases the mobility of trace metals due to the breakdown of metal sulfides (e.g., Clark et al., 1998), and (ii) precipitation of Fe-oxyhydroxides and formation of iron plaques around root surfaces, although increases metal accumulation, actually decreases mobility and uptake of trace metals by plants (Otte et al., 1995; Mortimer and Rae, 2000). Accumulation of trace metals in mangroves mostly take place in the root zone and together with iron plaque formation results in limited translocation of metals to aerial parts of the plant, i.e., leaves, bark and flowers (Silva et al., 1990; Chiu and Chou, 1991; MacFarlane et al., 2003; Machado et al., 2005). This understanding is reflected in the reported observation of higher bio-concentration factors (BCFs) for trace metals (i.e., ratio of metal concentrations in

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tissues and sediments) in root tissues than that of aerial parts, and in most cases metal concentrations in roots exceeds that of ambient sediment (Rao et al., 1991; Saenger et al., 1991; Thomas and Fernandez, 1997; Che, 1999; Tam and Wong, 1999; MacFarlane et al., 2003). Mangrove forests are one of the important vegetations of Sydney estuary and are dominated by Avicennia marina (Burchett et al., 1984). MacFarlane et al. (2003) reported that Cu, Pb and Zn accumulation in fine nutritive root tissues of Avicennia marina are higher than that of rhizosphere sediments in Newington wetlands. Beside this work, no other studies have been carried out on the accumulation of trace metals by fine nutritive root tissue of Avicennia marina in Sydney estuary. As one of the critically polluted estuaries of the globe (Birch, 2000), an extensive study of Sydney estuary is required to understand the role of rhizosphere processes in the accumulation of trace metals in Avicennia marina fine nutritive roots. The present study is therefore aimed to determine the concentrations of different trace metals in grey mangrove Avicennia marina fine nutritive roots under a range of contaminant conditions in sediments for an entire estuary (Sydney estuary, Australia). We further assess the magnitude of metal uptake by fine nutritive roots and the role of this activity in protecting surrounding environments from pollution. 2. Materials and methods 2.1. Study area Sydney estuary is located on the south-eastern coastal plain of New South Wales, Australia (Fig. 1) and is a 30-km long drowned

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river valley draining an area of approximately 500 km2 (Birch, 2000). The estuary is situated in the center of the Sydney Metropolitan region and supports a livelihood of 4.6 million inhabitants (approximately one-fifth of the total Australian population). A large number of shallow, contaminated bays adjoin the main channel of the estuary. Approximately 86% of the catchment area is urbanized and industrialized (Birch and Taylor, 2000) and the estuary is popular for recreational boating and water sports. The estuary is divided into five parts, Upper, Central and Lower Estuary, and Middle and North Harbor (Fig. 1). Sydney estuary is dominated by intertidal mangrove habitats of the Avicennia marina variety along the coastal intertidal fringes of major embayments (Burchett et al., 1984; McLoughlin, 2000). 2.2. Sampling of mangrove rhizosphere sediments and fine nutritive roots Mangrove rhizosphere sediments and fine nutritive roots were collected from five major embayments (i.e., Homebush Bay, Hen and Chicken Bay, Iron Cove, Lane Cove and Middle Harbor) of Sydney estuary (Fig. 1). Sampling was conducted during June 2012. In each of five embayments, three representative sites were selected for sampling based on concentration gradients (i.e., high, moderate and low levels of metal contaminants in total sediments) established during prior studies (Birch et al., 2013). In each site (n = 15), a mature mangrove tree (i.e., Avicennia marina) of similar size and health condition was selected for sampling. At the base of each mangrove tree, four equally-spaced intact sediment cores (20 cm depth) were retrieved using a plastic push-corer (Birch et al., 2011). Sediment cores were taken about 1 m apart within a square plot with the mangrove tree at the centre of the plot.

Fig. 1. Map of the study area showing locations of sampling sites (n = 15) in five major embayments (i.e., Homebush Bay, Hen and Chicken Bay, Iron Cove, Lane Cove and Middle Harbor) of Sydney estuary. Three sites in each embayment were chosen for sediment coring and collection of fine nutritive roots of Avicennia marina mangroves.

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Immediately upon collection, the intact sediment cores were transferred to an ice box and taken to the laboratory and refrigerated at 4 °C until further processing.

2.3. Sample processing in the laboratory In the laboratory, intact sediment cores were extruded from the tubes and sampled at 5 cm intervals to establish a profile of rhizosphere metal concentrations. Additionally, samples from each depth interval were pooled for a representative bulk sample for each core (n = 60 samples from 15 locations). The recovered sediment samples were air-dried at 25 °C for 48 h and ground to fine powder with a mortar and a pestle for ‘near-total’ metal extractions. In addition, a portion of the sediment sample was wet-sieved using 62.5 lm nylon mesh for the determination of metal contents in the fine fraction (Birch, 2003; Birch and Snowdon, 2004). Fine sediment fractionation (size normalization) was undertaken to reduce the confounding effects introduced by variable grain size and to produce compatible metal data and consistent spatial metal distributions (Birch, 2011, 2013). Fine nutritive roots attached to rhizosphere sediments (both profile and pooled samples) were recovered after washing in nylon mesh with milliQ water. The recovered fine nutritive root tissues were dried at 60 °C and homogenized for chemical analysis. Only fine nutritive root tissue was considered for sampling, while larger roots, such as cable and aerial roots were discarded.

2.4. Laboratory chemical analysis Dried and ground sediment (both total and fine fractions) samples weighing 0.4 g were digested with 4 ml aqua regia solution (1:1 HNO3:HCl) and 10 ml ultra-high purity water (Birch et al., 2011). Samples together with aqua regia were heated in a block digestion system at 120 °C for approximately 2.5 h, or until a near-dry condition (modified USEPA method 200.8 Rev 4.4 methods; US EPA, 1994). Digested samples were air-cooled to room temperature and made up to 30 ml with ultra-high purity water (18.2 mX cm 1). Solutions were shaken and left to settle overnight. The solute was transferred to 10 ml polypropylene tubes and stored at 4 °C until analysis. Powdered fine nutritive roots weighing 0.2 g were poured into a test tube for a step digestion procedure using 5 ml HNO3. Initially, the test tube containing samples and HNO3 were left at room temperature in a fume hood overnight for a slow digestion, followed by heating in a block digestion system at 80 °C for 1 h and then at 120 °C for approximately 2 h or until a near-dry condition. The digested samples were air-cooled to room temperature and made up to 30 ml with ultra-high purity water (18.2 mX cm 1). Solutions were filtered into 10 ml polypropylene tubes through Sartorius RC 0.45 lm syringe filter and stored at 4 °C until analysis. Metal bio-availability was determined in pooled sediments using 1M HCl solution which targets metals associated with poorly crystalline Fe-oxides/hydroxides, carbonates and organic fractions (Weimin et al., 1992; McCready et al., 2003). Approximately 2 g of dried and ground sediment samples (dry weight) were mixed with 30 ml 1M HCl. Mixtures were thoroughly shaken on a spinning wheel for 2 h and left to settle overnight. The HCl extract was recovered through centrifugation (3500 rpm for 15 min) and transferred to 10 ml polypropylene tubes for chemical analysis. Organic carbon was determined on air-dried and powdered samples by loss-on-ignition (LOI; at 550 °C for 2 h) following Dean (1974).

2.5. Data quality Trace elements (As, Cd, Co, Cr, Cu, Ni, Pb, Zn and Fe) were analyzed in sediments (total, fine fractions and bio-available) and fine nutritive roots using a Varian Vista AX CCD simultaneous ICP-OES. One blank, a reference material (AGAL-10 for sediments and AGAL6 for fine nutritive roots) and triplicates of an unknown sample per batch of 20 samples were used to measure laboratory contamination, analytical accuracy and precision, respectively. Analytical accuracy, reported as recovery, was 95–105% and precision was <5% relative standard deviation for all measured elements. No procedural contamination was detected.

2.6. Data analysis Statistics on metal concentrations in sediments (total, fine fractions and bio-available) and fine nutritive root tissues is provided as minimum, maximum and mean values. The percentiles (25th, 50th and 95th) of the data were also provided due to asymmetrical data distribution (Birch et al., 2011). Australian interim sediment quality guidelines (ISQG)-Low and -High values are included (ANZECC and ARMCANZ, 2000) to provide a broader picture of the status of metal contamination in Sydney estuary. Metal enrichment factors (EFs) in sediments are also given to show the magnitude of human-induced change in Sydney estuary sediments (Birch et al., 2013). Enrichment factors in sediments were calculated as the ratio of metal concentrations in fine fractions (<62.5 lm) over background (i.e., pre-anthropogenic) levels obtained from the core data described in Birch et al. (2013). Bio-concentration factors (BCFs) in mangrove fine nutritive roots were calculated using a ratio of total metals in root tissues to total and bio-available (1 M HCl extractable) metals in sediments to provide an estimate of the degree of metal accumulation in fine nutritive root tissues from ambient sedimentary environments (MacFarlane et al., 2007).

3. Results 3.1. Mangrove rhizosphere sediment quality, metal enrichments and metal bio-availability The percentage of fine fraction in the mangrove rhizosphere sediment varies between 1.4% and 98% (mean: 29%). The organic matter from loss-on-ignition (LOI) varies between 1.2% and 48% (mean: 8.5%). The rhizosphere sediments (total) show high concentrations of Cr, Cu, Pb and Zn with low to moderate concentrations of As, Cd, Co and Ni (Table 1a). Total sediment metals (As, Cd, Co, Cr, Ni, Pb and Zn), with the exception of Cu, show moderate to strong linear correlations (R2 > 0.41 and p values <0.005) with fine fractions (Supplementary Fig. S1). However, the level of total sediment metals increases strongly at higher fine fractions (> 60%). Arsenic, Cd, Cr, Cu, Ni, Pb and Zn exceed ISQG-Low values in 10–45% of the samples, however, Pb and Zn concentrations exceed ISQG-High values in 12% and 10% samples, respectively. These data indicate a potential risk to estuarine ecosystems for a range of trace metals (ANZECC and ARMCANZ, 2000), the most notable of these metals are Pb and Zn. No guideline values are available for Co and this element is in low concentrations (mean 4.6 mg/kg). Chromium, Cu, Pb and Zn are in higher concentrations in fine fractions compared with other elements. High enrichment factors (EFs) are observed for Cu, Pb and Zn (i.e., mean EFs > 12), while other metals, except As (mostly at background levels, mean EFs of 1.1), show mean EFs between 2.1 and 3.3 (Table 1b). These data indicate significant anthropogenic modification of sediments in this estuary due to catchment activities (Birch et al., 2013).

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Table 1 Trace metal concentrations in intertidal mangrove sediments in Sydney estuary (Australia): (a) total, (b) fine fractions and (c) bio-available content. Australian Interim Sediment Quality Guidelines (ISQG) and local background concentrations are given. Parameters (pooled samples, n = 60)

As

Cd

Co

Cr

Cu

Ni

Pb

Zn

(a) Total Minimum Maximum Mean 25th percentile 50th percentile 95th percentile

0.52 35 8.1 3.5 5.9 26

bdl 3.5 0.59 0.17 0.3 2.7

0.2 23 4.6 1.4 2.3 18

1.3 199 30 6.6 13 150

1 206 42 13 24 126

0.66 48 9.5 3.1 4.9 40

4.9 534 95 28 48 417

9.3 668 156 51 89 613

ISQG-Lowa % of samples > ISQG-Low ISQG-Higha % of samples > ISQG-High

20 17 70 None

1.5 10 10 None

na na na na

80 12 370 None

65 22 270 None

21 12 52 None

50 45 220 12

200 23 410 10

(b) Fine fractions Minimum Maximum Mean 25th percentile 50th percentile 95th percentile

5.4 58 27 21 28 41

0.17 3.9 1.5 0.55 1.2 3.6

2.6 29 12 6.6 9.7 24

18 212 98 45 75 199

22 662 194 81 146 504

7.4 53 27 17 24 51

52 839 329 147 276 683

47 1602 611 272 596 1535

Backgroundb EFs (mean)

24 1.1

0.5 3

5 2.4

30 3.3

10 19

13 2.1

20 17

50 12

(c) Bio-available content Minimum Maximum Mean 25th percentile 50th percentile 95th percentile

0.43 19 3.8 1.2 2.1 13

bdl 2.5 0.39 0.07 0.09 2.3

0.09 12 2 0.41 0.8 9.3

0.31 61 7.8 1.2 2.2 51

0.62 149 29 8.5 15 105

0.17 28 3.6 0.75 1.3 21

3.6 576 87 24 40 454

5.8 580 127 28 74 532

Bio-available fractions (mean %)c

47

66

44

26

69

38

92

81

Note: All concentrations are in mg/kg (dry weight); bdl – below detection limit; na – not available; values in italics are % of samples greater than respective guidelines; EFs = enrichment factors. a Interim Sediment Quality Guidelines (ANZECC and ARMCANZ, 2000). b Birch et al. (2013). C Relative to total concentrations.

Copper, Pb and Zn are not only highly bio-available (mean > 69% for these metals) but also in higher concentrations (mean > 29 mg/ kg for these metals) than other metals, i.e., As, Cd, Co, Cr and Ni, which show low to moderate bio-availability (mean ranging between 26% and 66%) and low to moderate in concentrations (mean ranging between 0.39 and 7.8 mg/kg) (Table 1c). 3.2. Trace metal concentrations in Avicennia marina fine nutritive roots The highest metal concentrations in fine nutritive roots are observed for Cu, Pb and Zn with a mean of 153, 189 and 378 mg/kg, respectively. Arsenic, Cr and Ni are also enriched with a mean concentration of 16, 21 and 11 mg/kg, respectively, while, Cd and Cr have accumulated in low concentrations in fine nutritive root tissues (Table 2). All trace metals (As, Cd, Co, Cr, Ni, Pb and Zn), except Cu, present in the rhizosphere sediments (total content) are strongly correlated (R2 > 0.65 and p values <0.005) with metals accumulated in fine nutritive roots (Fig. 2). Cobalt, Cr and Ni in the sediment fine fraction (<62.5 lm) show a moderate correlation (R2 from 0.35 to 0.48 and p values <0.005) with metal concentrations in fine nutritive roots, whereas no such correlation is observed for As, Cd, Cu, Pb and Zn (Supplementary Fig. S2). Similar to trace metals in total sediments, the bio-available contents (1M HCl) of all metals, except As and Cu, are strongly correlated (R2 > 0.61 and p values <0.005) with metal concentrations in fine nutritive roots (Supplementary Fig. S3). The mean BCF values (total content) are greater than unity for all elements, except Cr, which is 0.96. However, the BCFs calculated

using bio-available contents are higher than the BCF calculations using total sediment metals (Fig. 3). 3.3. Profile of trace metals in rhizosphere sediments and fine nutritive roots Depth profile of the Homebush Bay core (profile-1, sampling site 1) shows sedimentary environments with a greater fine fraction (i.e., <62.5 lm, ranging between 85% and 98%) and higher organic matter (LOI ranging between 18% and 20%) and an overall increasing trend in trace metal concentrations in total sediments with depth (Fig. 4). However, trace metal concentrations in fine nutritive root tissues show some variations, e.g., (i) decreasing trend of As, Co, Cu, Pb, Zn and Fe with depth and (ii) increasing trend of Cd, Cr, Ni with depth. Profile of the Hen and Chicken Bay core (profile-2, sampling site 5) shows a gradual increase in trace metal concentrations in total sediments and fine nutritive root tissues towards the surface consistent with an increase in fine fraction (ranging between 3.6% and 17%) and organic matter (LOI ranging between 1.2% and 9.1%) (Fig. 5). Profile of the Middle Harbor core (i.e., a site in Sydney estuary which is relatively undisturbed, profile-3, sampling site 13) shows moderate levels of fine fraction (ranging between 13% and 33%) and organic matter (LOI ranging between 3.2% and 9.3%), and trace metal concentrations are low, except for major elements, e. g., Fe (Supplementary Fig. S4). Overall, trace metal concentrations in total sediments appears to decrease toward the surface which is consistent with a decrease in fine sediment and organic matter content, however, metals in fine nutritive root tissues show increasing trend, except

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Table 2 Trace metal concentrations in Avicennia marina fine nutritive roots in Sydney estuary (Australia). Parameters (pooled samples, n = 60)

As

Cd

Co

Cr

Cu

Ni

Pb

Zn

Minimum Maximum Mean 25th percentile 50th percentile 95th percentile

1.6 47 16 8.5 14 34

0.09 7.6 1.5 0.51 1.1 4.0

0.37 22 4.9 2.2 3.4 15

1.8 124 21 4.7 10 71

15 447 153 57 123 428

0.88 92 11 3.7 6.8 32

6.0 751 189 62 142 561

33 1108 378 166 324 844

Note: All concentrations in mg/kg (dry weight).

Fig. 2. Correlation between trace metal concentrations in Avicennia marina fine nutritive roots vs. total sediments. Full black line is showing y = x.

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Fig. 3. Metal bio-concentration factors (BCFs; mean ± standard deviation, 1r) in fine nutritive roots (n = 60) of Avicennia marina (Forsk.) Vierh., collected from Sydney estuary. BCFs were calculated as the ratio of metal concentrations in fine nutritive roots to total (BCF-total) and bio-available (BCF-bioavailable) concentrations in sediments.

Cr, until 10 cm depth followed by a sharp decrease toward the surface (Supplementary Fig. S4). 4. Discussion 4.1. Metal accumulation pattern in the rhizosphere sediment profile and in fine nutritive roots The rhizosphere profiles indicate a strong control exerted by the fine sediment fraction and organic matter content on the

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accumulation of trace metals in the mangrove sediments. However, trace metal accumulation in fine nutritive roots mainly responds to total sediment chemistry as evidenced through the strong positive linear correlation between metals in total sediments and fine nutritive roots (Fig. 2). Avicennia marina root systems (especially aerial roots) are known for their ability to diffuse oxygen into the substrate, resulting in oxidation of the rhizosphere (e.g., Machado et al., 2005; Marchand et al., 2011). Therefore, high concentrations of As, Co, Cu and Zn in fine nutritive root tissues in the upper rhizosphere zone, especially in Homebush Bay (site 1, Fig. 4), may be attributed to re-adsorption of these metals released during sulfidic oxidation onto organic matter and/or coprecipitation with Fe-oxyhydroxides (Lacerda et al., 1993; Marchand et al., 2011). High metal accumulations in fine nutritive roots in the upper rhizosphere horizon (i.e., <10 cm depth) of Hen and Chicken Bay (profile-2) may be attributed to large surface areas and high density of the root system (Lacerda et al., 1992; Otero et al., 2006). Generally, root activity in the upper rhizosphere is so intense that it leads to a dominant oxidation process and formation of iron plaque around root surfaces, favoring large metal accumulations (Lacerda et al., 1992; Machado et al., 2005; Otero et al., 2006). McLaughlin et al. (1985) and Machado et al. (2005) reported that 98% and >80% of total ‘root’ iron is associated with iron plaques, respectively, while between 45% and 90% of total ‘root’ Zn is associated with iron plaques (Machado et al., 2005). A positive correlation of Fe in total sediments and metals in fine nutritive root tissues (Supplementary Fig. S5) supports the possible formation of iron plaque and accumulation of these metals in iron plaques (Che, 1999). The dynamic state of redox zonation in the rhizosphere, i.e., fluctuation in the oxic upper rhizosphere and anoxic lower rhizosphere boundary, may contribute to the availability of certain trace

Fig. 4. Depth distribution of LOI, fine fractions and total metals in Avicennia marina rhizosphere sediments. The profile also shows metal concentrations in fine nutritive roots (profile-1, sampling site 1 in Homebush Bay).

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Fig. 5. Depth distribution of LOI, fine fractions and total metals in Avicennia marina rhizosphere sediments. The profile also shows metal concentrations in fine nutritive roots (profile-2, sampling site 5 in Hen and Chicken Bay).

metals (especially Cu, Pb and Zn) in the Avicennia marina sediments observed in the current study (Lacerda et al., 1993). Effect-based numerical sediment quality guidelines are used to assess the sediment contamination levels (ANZECC and ARMCANZ, 2000) for the entire estuary to demonstrate the level of sediment contamination and its likely consequences on the magnitude of trace metal accumulation in fine nutritive roots. The data indicates a high adverse risk potential to coastal estuarine ecosystems for a range of trace metals. The most notable of these metals are Pb and Zn, which exceed ISQG-Low in large number of samples, while exceed ISQG-High in 12% and 10% samples, for Pb and Zn, respectively (Table 1a). The magnitude of anthropogenic contributions is evident from enrichment factors of metals which show ‘severe/ very severe’ enrichment in Cu, Pb and Zn (EF 12–19 times background concentrations) together with ‘minor/moderate’ enrichment (1.1–3.3 times background) for the remaining metals (Table 1b). 4.2. Magnitude of trace metal accumulations in Avicennia marina fine nutritive roots All metals analyzed in the present investigation accumulated substantially in fine nutritive roots of the mangrove Avicennia marina, except Cd and Co (Table 2). Arsenic, Cd, Cu, Pb and Zn accumulated in fine nutritive roots with concentrations mostly exceeding total sediment concentrations, while Co, Cr and Ni accumulated in concentrations similar to total sediment. Peng et al. (1997) observed greatest accumulation of metals in root tissues compared with other tissue types (such as leaves, flower and aerial roots)

and suggested that the adsorbed metals may reside in the outer cortex of fine roots. A similar accumulation pattern was reported by MacFarlane et al. (2003) for Cu, Pb and Zn in Avicennia marina root tissues based on a spatially-limited, site-specific study in Newington wetland of Sydney estuary. Accumulation of trace metals in fine nutritive root tissue follows a strong linear relationship with total sediment metal concentrations, except for Cu. This indicates that, with increasing total sediment metals, the metal accumulations in fine nutritive roots also increases (MacFarlane et al., 2003). MacFarlane and Burchett (2002) were able to replicate the above findings in the laboratory for the same species, especially for Pb and Zn. However, they found an exponential relationship of Cu accumulation in between sediments and fine nutritive root tissues, i.e., the accumulation pattern was linear at low sediment concentrations and reached a plateau at concentrations >200 mg/kg of sediments. Baker (1981) suggested that Cu accumulation in mangrove tissues at low sediment concentrations was mainly due to physiological requirements; however, at higher sediment concentrations, an exclusion or saturation mechanism may have prevailed, resulting in low accumulation of metals in fine nutritive roots (Baker, 1981; MacFarlane and Burchett, 2002). This may explain the lack of observed strong linear relationship between Cu in total sediments and fine nutritive roots under field conditions (Fig. 2). A similar correlation is observed for bio-available metals and accumulated metals in fine nutritive roots in the present work, suggesting a strong influence of metal bio-availability in trace metal accumulation in root tissues (Lacerda and Rezende, 1987; John and Leventhal, 1996). This strong correlation between total (and bio-available) sediment metals and

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root metals is maintained even though the samples were collected over a wide spatial scale with significant variations in fine sediment fractions and organic matter contents. However, metals in fine nutritive root tissue do not reflect concentrations in the fine sediment fractions as indicated through a weak correlation between these materials (Supplementary Fig. S2). This suggests that metal accumulation in fine nutritive root tissues is mainly responding to processes associated with the total sediment chemistry and that no confounding is imposed by varying proportion of fine fractions in the sediment. The mean BCFs exceed unity (for total and bio-available fractions) in fine nutritive roots for all metals, indicating that fine nutritive roots can accumulate metals in greater concentrations than that observed in sediments (MacFarlane and Burchett, 2002; MacFarlane et al., 2003) and even though the sediments have diverse physicochemical constituents (e.g., Birch et al., 2013). The BCF values obtained in the present study are comparable to studies reported from elsewhere in the world and locally within Australia, however, Sydney estuary BCF values are slightly higher (Supplementary Table S1), due possibly to a greater range of metal concentrations (especially Cr, Cu, Pb and Zn) in total sediments. In addition, our mean BCF values are typically within the laboratory replicated range for Cu and Zn, but are higher than that reported for Pb (MacFarlane and Burchett, 2002) suggesting stronger potential for Pb accumulations in mangrove tissues under field conditions. The accumulation pattern of trace metals in rhizosphere sediments and fine nutritive roots supports the understanding that Avicennia marina mangrove habitats are acting as both physical and biogeochemical barrier to contaminant mobility and that these plants have shown low toxic effects from range of contaminants (e.g., MacFarlane and Burchett, 2002; Lewis et al., 2011). Likewise, these plants have been extensively used for estuarine management to protect coastal marine habitats from pollution (e.g., Zhou et al., 2010). Keene et al. (2010) and Nath et al. (2013) observed release of trace metals to surrounding environments due to anthropogenic disturbances of sulfidic mangrove sediments. Therefore, protection of these ecosystems are necessary to avoid risks of being significant estuarine pollution of these accumulated metals to the water column. 5. Conclusion The present study has demonstrated the strong role of Avicennia marina fine nutritive roots in accumulating trace metals from a highly modified estuarine system and by doing so that these plants have the potential to protect estuarine ecosystems if not disturbed. Trace metal concentrations in rhizosphere sediments are mainly controlled by the percentage of fine sediments and organic matter content, while metal accumulation in fine nutritive roots is responding to processes exerted by total sediment metals, i.e., the possible formation of iron plaques around root surfaces and precipitation of Fe-oxyhydroxides. The observed strong linear relationship between metal concentrations in fine nutritive roots and ambient sediments (especially total contents) and that root BCFs > 1 provides indication of metal accumulation capability of Avicennia marina fine nutritive roots. Acknowledgements This research was supported by the University of Sydney postdoctoral research fellowship scheme. We thank Tom Savage, Mahsa Safari and Md. Shaike for technical assistance. PC thanks Endeavour Australia for research fellowship. We also thank anonymous reviewers for their insightful comments that essentially improved the manuscript.

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