Concentration of 7 Heavy Metals in Sediments and Mangrove Root Samples from Mai Po, Hong Kong

Concentration of 7 Heavy Metals in Sediments and Mangrove Root Samples from Mai Po, Hong Kong

PII: Marine Pollution Bulletin Vol. 39, Nos. 1±12, pp. 269±279, 1999 Ó 1999 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-3...

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PII:

Marine Pollution Bulletin Vol. 39, Nos. 1±12, pp. 269±279, 1999 Ó 1999 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-326X/99 $ - see front matter S0025-326X(99)00056-9

Concentration of 7 Heavy Metals in Sediments and Mangrove Root Samples from Mai Po, Hong Kong R. G. ONG CHE* Department of Applied Science, Hong Kong Technical College, Chai Wan, Hong Kong, People's Republic of China Concentration of 7 heavy metals, Zn, Fe, Cu, Cr, Cd, Pb and Ni in mud¯at sediments, mangrove root sediments and root tissues of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel from the Mai Po Nature Reserve, Northwest Hong Kong, were measured. Metal concentrations in the upper 0±10 cm of the sediment cores from the mud¯at were 4±25% higher than those found in the bottom 21±30 cm. Relative Topsoil Enrichment Index approximated 1.0 for all the metals. Mud¯at sediment concentrations of Fe, Ni, Cr, Cd and Cu were greater than those found in the mangrove sediments. Except for Fe, concentrations of the other 6 heavy metals were more elevated in the mangrove root sediments than in the corresponding root samples. Higher concentration factors for Zn, Fe and Cu may indicate bioaccumulation. Mean metal concentrations in both mud¯at and mangrove sediments decreased in the order Fe > Zn > Pb > Ni > Cu > Cr > Cd. Mangrove root tissues also showed the same pattern except that Pb > Cu > Ni Ó 1999 Elsevier Science Ltd. All rights reserved.

Introduction The Mai Po Marshes (22° 300 N, 114° 020 E) is one of the six Sites of Special Scienti®c Interest bordering Deep Bay, Hong Kong, China. It comprises 381 ha of dwarf mangrove, shrimp ponds (gei wais) and ®sh ponds. Because of its high productivity, it is an important habitat for both resident birds and migratory water fowl like the Little Egret (Egretta garzette) and the Chinese Pond Heron (Ardeola bachus) (Melville and Morton, 1983). The Deep Bay/Mai Po area was declared a wetland of international importance under the Ramsar Convention in 1995 in order to protect the wide range of natural and man-made habitats contained in the area. These include one of the largest and most diverse mangrove communities along the south China coast and a large expanse of intertidal mud¯at. Both the mangroves and the mud¯at *Present address: The Swire Institute of Marine Science, The University of Hong Kong, Cape d'Aguilar, Sheko, Hong Kong, China.

are important feeding, nesting and staging grounds for some 67,000 birds belonging to 270 species, including some rare and endangered ones such as the Black-faced Spoonbill (Platalea minor) (Young and Melville, 1993). Inspite of the international recognition accorded to the ecological importance of this wetland habitat, environmental pressures from increased urban and industrial development in the surrounding areas continue to pose a threat (Kueh and Chui, 1996). Deep Bay receives discharges from 3 major rivers : the Pearl River from the northwest, the Shenzhen River from the northeast, and the Yuen Long River from the southeast. The Pearl River drains an area of about 442,440 km2 , covering the city of Guangdong and the hinterlands of southern China. The Shenzhen River which lies along the border between Hong Kong and the Shenzhen Special Economic Zone receives sewage e‚uent from Shek Wu Hui and the Northern New Territories of Hong Kong. The Yuen Long River is a 60 km long water course with a catchment area of highly intensive livestock rearing and industrial activities. Due to the growing rate of urbanization and industrialization in the areas surrounding Deep Bay, there is a growing concern about the pollution impact, especially that of heavy metal contamination, on this Ramsar site. However, there is not enough information available to determine the extent of contamination (Wu, 1988; Young and Melville, 1993). Ong Che and Cheung (1998) reported upon the levels of Cr, Pb, Fe and Zn in the sediments and tissues of Metapenaeus ensis and Eriocheir sinensis collected from the gei wais at Mai Po. Studies on the biomonitoring potential for coastal trace metals of barnacles, amphipods (Rainbow, 1992; Rainbow and Smith, 1992) and oysters (Phillips, 1979; Phillips and Yim, 1981; Phillips et al., 1982) have provided some data on the Mai Po area. Some further information is also available from the routine monitoring of sediment heavy metal concentrations at 66 sites around Hong Kong carried out by the Environmental Protection Department, Hong Kong Special Administrative Region Government (EPD, 1997). This study presents data on the concentrations of 7 heavy metals (Zn, Fe, Pb, Ni, Cd, Cu Cr) in the mud¯at 269

Marine Pollution Bulletin

sediments, in the root tissues of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel and in the sediments between the roots of these 3 mangrove species. The information reported here can add to the database and may be of use for the conservation and management of Mai Po.

Materials and Methods Sampling and analyses Mud¯at sediments, mangrove roots and sediments between mangrove roots were sampled in November 1997 from the Mai Po Nature Reserve, Hong Kong. Ten sediment cores were collected from the open mud¯at area close to the bird-watching hide. Mud¯at sediments were sampled at 2 depths : 0±10 and 20±30 cm to provide an indication of the rate of contamination within the soil pro®le. Live roots of 3 individual plants each of Acanthus ilicifolius, Aegicerus corniculatum, and Kandelia candel were collected from the mangroves close to the boardwalk and  1 km from the open mud¯at area. A root was de®ned as live if it was white and attached to the above ground portion of the plant. Plant roots were dug out with a lump of soil remaining around the roots. Sediments between the roots of the sampled mangrove plants were also collected. Root samples were washed with deionized water before storage. All samples were packed into plastic bags, and kept frozen until analysis. Sediment and root samples were dried at 105°C to constant weight. Dried samples were ground, then passed through a sieve of 250 lm mesh. Two replicates of 1 gm of dried and sieved sediments were digested in a Kjeldahl Digester with 1 ml of concentrated nitric acid and 10 ml of concentrated sulfuric acid at 270°C. Two replicates of 200 mg of ®nely ground root samples were ashed at 450°C for 3 h. The ashed sample was dissolved in 5 ml of 5M Hydrochloric acid and 1 ml of concentrated nitric acid. Digests or dilutions were analysed for 7 metals, chromium, iron, lead, zinc, copper, nickel and cadmium, by ¯ame atomic absorption spectrophotometry on a Perkin Elmer (Model 3110) AA spectrophotometer with continuous background correction. All metal concentrations are expressed as lg metal gÿ1 dry weight. Sediment organic matter was determined by ashing 4 g of dry soil for 4 h at 525°C. Sediment texture was determined using a hydrometer and the percentages of sand, silt and clay was calculated following Carter (1993). Statistical analyses The mean, standard deviation, range and coecient of variation of the heavy metal concentrations were calculated. Di€erences among metal concentrations in mud¯at sediments, mangrove root tissues and sediments between roots were tested by analyses of variance and post-hoc Newman±Keuls multiple range tests. Pearson product correlation coecients between heavy metals in 270

root tissues and in mangrove sediments between roots were also computed. In order to compare the degree of storage of the metals, concentration factors (CF) were calculated as concentration of metal gÿ1 tissue over the concentration of metal gÿ1 sediment (Alberts et al., 1990). In order to compare the degree of sediment contamination, the relative topsoil enrichment (RTE) for each metal was calculated. RTE ˆ total metal in the upper zone (0±10 cm) of soil over the total metal in the lower zone (21±30 cm) of soil (Colbourn and Thornton, 1978).

Results Percentage organic matter in the upper (0±10 cm) and lower (21±30 cm) sections of the sediment cores from the mud¯at did not vary much. Mean % organic matter content was 11.81 (‹ 0.66) in the upper section compared with 11.71 (‹ 0.98) in the deeper section. Total organic matter in mangrove sediments was slightly higher and were 13.02 (‹ 0.32), 11.97 (‹ 0.57) and 13.46 (‹ 1.41) for sediments between roots of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel, respectively. Sur®cial sediments from the mud¯at consisted of 99.83% (‹ 0.11) silt, 0.02% (‹ 0.01) clay and 0.15% (‹ 0.11) sand while deeper sediments di€ered from surface sediment texture by 0.02% only. Heavy metal concentrations in the surface and deeper sections of the sediment cores collected from the Mai Po mud¯at are presented in Table 1. The Relative Topsoil Enrichment (RTE) Index are also shown. Metal concentrations in the surface sediments from the mud¯at were 4±25% higher than those found in the deeper sediments. Relative Topsoil Enrichment Index approximated 1.0 for all the metals. Concentrations of heavy metals in the root tissues of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel, and in sediments between mangrove roots are shown in Table 2. Concentration factors (CF) for each metal for each species are also given. Metal content in the roots of the 3 mangrove species di€ered. Higher concentrations of Zn, Fe and Cu were generally found in A. ilicifolius while K. candel tended to have more elevated concentrations of the remaining 4 metals. Of the heavy metals measured in this study, Fe showed the highest concentration and was 1±4 order of magnitude greater than the other metals. Cd concentrations were less than 1 lg gÿ1 dry weight and Cr concentrations were also low. Concentration factors among the 3 mangrove species varied by a factor of 1.2±2.0. For all 3 species, high concentration factors (> 0.6) were obtained for Fe, Cu and Cd. CF values for Fe were many times greater than 1. Intermediate CF values (0.1±0.3) were obtained for Pb and Ni for all species while CF values for Zn and Cr ranged from intermediate to high, depending on the species.

Volume 39/Numbers 1±12/January±December 1999 TABLE 1 Concentrations of heavy metals (lg gÿ1 dry weight) in the surface (0±10 cm) and deeper (21±30 cm) sections of the mud¯at sediment cores and the Relative Topsoil Enrichment index (RTE) (mean ‹ SD) (SD ˆ standard deviation; % cv ˆ coecient of variation). Zn

Fe

Pb

Ni

Cd

Cr

Cu

0±10 cm core Mean SD Maximum Minimum % cv

222.0 48.1 307.6 129.7 21.7

1762.7 909.1 3328.0 384.8 51.6

135.3 44.9 219.6 68.7 33.2

70.8 12.3 86.9 43.9 17.4

1.2 0.1 1.1 1.4 8.3

33.0 19.7 74.6 20.0 59.5

67.1 10.9 87.4 51.1 16.2

21±30 cm core Mean SD Maximum Minimum % cv

213.3 57.3 349.4 136.8 26.9

1457.8 657.3 2274.5 559.9 45.1

120.3 27.2 158.3 69.9 22.6

66.9 22.1 94.5 25.0 33.0

1.2 0.1 1.1 1.4 8.3

24.6 13.2 51.0 9.8 53.6

60.3 6.5 71.1 48.2 10.8

1.08 ‹ 0.38

1.34 ‹ 1.26

1.24 ‹ 0.50

1.17 ‹ 0.59

1.00 ‹ 0.09

1.86 ‹ 2.23

RTE Index

Mean metal concentrations in both mud¯at and mangrove sediments decreased in the order Fe > Zn > Pb > Ni > Cu > Cr > Cd. Mangrove root tissues also showed the same pattern except that Pb > Cu > Ni. Mud¯at sediment concentrations of Fe, Ni, Cr, Cd and Cu were greater than those found in the mangrove sediments. Except for Fe, concentrations of the other 6 heavy metals were more elevated in the mangrove root sediments than in the corresponding root samples. Table 3 presents the analyses of variance on the metal concentrations in the mangrove root tissues and in the sediments between roots of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel. Metal concentrations in the sediments between the roots of these 3 mangrove species were all not signi®cantly di€erent. Heavy metal concentrations in the roots of the 3 mangrove species were not signi®cantly di€erent for 5 of metals measured. Post-hoc Newman Keuls tests showed signi®cantly higher concentrations of Zn in A. ilicifolius compared to the other 2 species while concentrations of Cu were signi®cantly higher in A. ilicifolius compared to K. candel. Table 4 shows the results of the signi®cance testing on the metal concentrations in mud¯at sediments, mangrove root tissues and in sediments between mangrove roots. Concentration of the 7 heavy metals determined in this study were all very signi®cantly di€erent in the 3 types of sample. Post-hoc Newman±Keuls tests showed that except for Zn and Ni, mangrove sediment concentrations were signi®cantly di€erent from those in the mud¯at sediments while root metal concentrations were all signi®cantly di€erent from those in the sediment samples. Results of the correlation analyses on the degree of association of heavy metals in the root tissues with the corresponding sediment samples between roots are shown in Table 5. Signi®cant correlations were obtained for Cu in A. ilicifolius and K. candel. Negative correla-

1.02 ‹ 0.27

tions were found for Pb and Cd in all three mangrove species but no consistent trend among species may be observed for the other metals.

Discussion Conservation of the Mai Po marshes The Deep Bay/Mai Po area is a wetland of international importance protected under the Ramsar Convention. It is bordered by six Sites of Special Scienti®c Interest (SSSIs): the Mai Po Marshes, Mai Po egretry, Tsim Bei Tsui, Inner Deep Bay and Pak Nai on the Hong Kong side of Deep Bay, and the Fu Tien Nature Reserve on the Shenzhen, Special Economic Zone side. These sites encompass one of the most diverse and extensive mangrove communities along the south China coast and a large expanse of intertidal mud¯at. Over 270 species of waterfowls and migratory birds rely on both mangrove and mud¯at areas for feeding, breeding, nesting and refuelling during winter (Young and Melville, 1993). In recent years, many concerns have been voiced regarding the threat of heavy metal contamination on the Ramsar site due to the growing rate of urbanization and industrialization in the areas surrounding Deep Bay. However, scant information is available to determine the extent of contamination (Young and Melville, 1993). This study presents data on the concentrations of 7 heavy metals (Zn, Fe, Pb, Ni, Cd, Cu Cr) in the mud¯at sediments, in the root tissues of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel and in the sediments between the roots of these 3 mangrove species. The information here may be of use for the conservation and management of the Nature Reserve. Heavy metals in sediments The levels of heavy metals in the bulk sediments from the intertidal mud¯at area at Deep Bay have not been 271

Marine Pollution Bulletin TABLE 2 Concentrations of heavy metals (lg gÿ1 dry weight) in the root tissues and mangrove sediments between roots of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel. Concentration Factors (mean ‹ SD) for each metal for each species are also presented (SD ˆ standard deviation; % cv ˆ coecient of variation). Zn

Fe

Pb

Ni

Cd

Cr

Cu

Mangrove root tissues Acanthus ilicifolius Mean SD Maximum Minimum % cv

207.1 85.6 324.8 134.1 41.3

4950.8 1440.3 7450.0 3600.0 29.1

33.3 16.3 60.0 20.0 48.9

14.3 4.4 20.0 8.0 30.8

0.4 0.2 0.5 0.05 50.0

3.8 1.8 6.2 1.6 47.4

40.7 13.8 65.4 25.2 33.9

Aegicerus corniculatum Mean SD Maximum Minimum % cv

82.5 34.1 136.8 44.0 41.3

3650.0 1343.7 5850.0 2235.0 36.8

30.0 16.7 60.0 20.0 55.7

16.3 10.4 32.0 6.0 63.8

0.3 0.1 0.5 0.07 33.3

3.2 1.5 5.8 1.8 46.9

32.7 9.0 46.2 22.4 27.5

Kandelia candel Mean SD Maximum Minimum % cv

122.9 52.2 208.0 81.6 42.5

4225.8 2544.7 8800.0 1750.0 60.2

40.0 17.9 60.0 20.0 44.8

18.3 10.0 28.0 4.0 54.6

0.5 0.2 0.6 0.1 40.0

4.1 1.9 6.4 1.8 46.3

24.3 3.9 29.4 19.6 16.0

Overall mean

137.5

4275.6

34.4

16.3

0.4

3.5

32.6

Mangrove sediments between roots Acanthus ilicifolius Mean SD Maximum Minimum % cv

321.2 129.8 553.3 209.8 40.4

481.2 182.3 749.8 200.0 37.9

219.8 61.5 300.0 120.0 28.0

65.3 19.8 85.9 31.0 30.3

0.5 0.2 0.6 0.2 32.6

15.3 7.3 27.0 10.0 47.7

49.8 13.7 75.8 38.0 27.5

Aegicerus corniculatum Mean SD Maximum Minimum % cv

281.4 58.8 347.9 202.0 20.9

278.6 213.7 659.7 100.0 76.7

214.9 41.8 259.9 140.0 19.4

66.0 21.3 96.0 30.0 32.3

0.6 0.0 0.6 0.6 6.7

7.8 2.6 11.4 4.0 33.3

46.3 7.6 59.5 37.0 16.4

Kandelia candel Mean SD Maximum Minimum % cv

277.2 78.6 426.6 192.0 28.4

509.0 276.1 825.0 160.0 54.2

161.6 38.7 200.0 90.0 23.9

66.0 23.2 102.0 36.0 35.1

0.6 0.1 0.7 0.5 13.8

17.4 13.8 40.0 4.1 79.3

41.9 8.7 56.0 29.2 12.1

Overall mean

293.3

423.0

198.8

65.7

0.6

13.5

46.0

0.54 ‹ 0.34 0.31 ‹ 0.16 0.48 ‹ 0.26

12.28 ‹ 7.22 20.92 ‹ 15.37 10.16 ‹ 7.08

0.17 ‹ 0.10 0.16 ‹ 0.14 0.29 ‹ 0.21

0.25 ‹ 0.17 0.31 ‹ 0.29 0.31 ‹ 0.23

0.95 ‹ 0.61 0.58 ‹ 0.26 0.92 ‹ 0.46

0.29 ‹ 0.22 0.47 ‹ 0.23 0.51 ‹ 0.56

0.81 ‹ 0.13 0.72 ‹ 0.23 0.59 ‹ 0.07

Concentration factors Species A. ilicifolius A. corniculatum K. candel Overall mean

0.44

14.45

reported upon. Comparing the results of this study with those done in other areas in Hong Kong and in the world shows that heavy metal concentrations in this study were similar in magnitude with those determined at other sites (Table 6). Maximum concentrations of Zn, Pb and Ni were greater at the Mai Po mud¯at than at Tolo Harbour (Chan, 1992) and Victoria Harbour (Wong et al., 1995) 272

0.20

0.29

0.82

0.42

0.71

in Hong Kong. The opposite trend may be seen for Fe, Cr, Cu and Cd. Except for Pb, all of the metals measured in this study were 1±3 fold lower than those measured in sediments from Kwun Tong (Wong et al., 1995) and Cheung Kwan Oh (Fung, 1993). The former is a heavily polluted site within Victoria Harbour, close to an industrialized area and the old airport runway of Hong Kong while the latter is a coastal site, receiving

Volume 39/Numbers 1±12/January±December 1999 TABLE 3 Results of the analyses of variance and post-hoc Newman±Keuls tests testing for signi®cant di€erences in the metal concentrations in the root tissues of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel and in the metal concentrations in the sediments between roots of the 3 mangrove species. Metal

F…2;15† Zn Fe Pb Ni Cd Cr Cu

Root tissues

Mangrove sediments F…2;15†

Acanthus ilicifolius

Aegicerus corniculatum

Kandelia candel

a

b

b

a

ac

c



0.28 2.33 2.30 0.00 1.83 1.11 0.95

8.66 1.01 0.58 0.04 0.32 0.34 5.16

*

Indicates signi®cant di€erence (p < 0.05) while samples sharing a common letter are not signi®cantly di€erent (p > 0.05) in the Newman±Keuls tests.

TABLE 4 Results of the analyses of variance and post-hoc Newman±Keuls tests testing for signi®cant di€erences among metal concentrations in mud¯at sediments, mangrove root tissues and mangrove sediments sampled from between the roots. Metal Zn Fe Pb Ni Cd Cr Cu

F…2;43†

Mud¯at sediments

Mangrove sediments

Root tissues

a a a a a a a

a b b a b b b

b c c b c c c

21.74 84.26 108.47 59.47 19.66 53.50 30.84

***

Indicates signi®cant di€erence at p < 0.001 while samples sharing a common letter are not signi®cantly di€erent (p > 0.05) in the Newman±Keuls tests.

TABLE 5 Correlation coecients showing the degree of association between heavy metals in mangrove root tissues and in mangrove sediments between plant roots. Metal Zn Fe Pb Ni Cd Cr Cu **

Acanthus ilicifolius

Aegicerus corniculatum

0.58 ÿ0.14 ÿ0.11 ÿ0.17 ÿ0.40 ÿ0.46 0.89

ÿ0.23 ÿ0.24 ÿ0.69 ÿ0.39 ÿ0.80 0.02 ÿ0.11

Kandelia candel ÿ0.38 0.49 ÿ0.69 0.08 ÿ0.56 ÿ0.30 0.85**

Indicate that the correlations were signi®cant at p < 0.5.

domestic sewage and industrial pollution from the nearby fast developing new town. Metal concentrations in sediments from the Mai Po gei wais (Ong Che and Cheung, 1998) were generally higher than those in sediments from the mud¯ats. This may be due to the fact that the gei wais are closed o€ from tidal access for several months during the year for shrimp culture. Lacking tidal ¯ushing and good water circulation, anaerobic conditions may prevail which favours the formation of stable and insoluble metal sulphides via the action of sulfate reducing bacteria. In contrast, the mud¯at environment, subject to a periodic immersion and emersion regime, is a more aerobic environment, especially at the sediment-water interface.

Oxidation of sulphide in the upper layers of the sediment may result in mobilization of heavy metals and their export to deeper waters. Comparing the present results with heavy metal concentrations in sediments from other parts of the world shows that the Mai Po mud¯at are moderately contaminated. Sediment metal concentrations at Mai Po were more elevated than the Itaipu lagoon, Rio de Janeiro, Brazil which has permanent access to the sea (Lacerda et al., 1992) and the Eastern Scheldt Estuary, which served as a control site in a study on sediment contamination in dredged material from the port of Rotterdam and an o€shore disposal site (Van den Hurk et al., 1997). Sediment metal concentrations were, 273

Marine Pollution Bulletin TABLE 6 Ranges of heavy metal concentrations (lg gÿ1 dry weight) in surface sediments reported in this and other studies.

1

Tolo Harbour, Hong Kong Victoria Harbour, Hong Kong2 Kwun Tong, Hong Kong2 Cheung Kwan Oh, Hong Kong3 Mai Po (gei wais), Hong Kong4 Mai Po (mud¯at) Hong Kong12 Manila Bay, Philippines5 Marinas, USA6 Darwin Harbour, Australia7 Itaipu, Brazil8 a Eastern Scheldt Estuary, Netherlands9 Tees, River, UK10 Blackwater Estuary, UK11b

Zn

Fe

Pb

Cd

20±182 98±259 610

44000±187000 28900±34100 30200

148±513 130±308 60±329 240±656 103±270 82 ‹ 29 65

2672±16316 385±3328 11400±40900 18400±58800

5±85 47±71 138 616±674 72±195 69±220 6±95 9±359 24±91 25 ‹ 13 20

0.03±0.59 2.6±3.3 3.3 4.3±4.7

37±680 4±231

3±10 0.02±2.51

65±777 21±293

7685±67117

1.1±1.4 0.7±8 0.9±3

Cr 58±171 601 72±84 49±602 20±75 85±275

<0.5 36±577 13±334

Cu

Ni

6±115 45±922 3790 151±161

4±21 24±64 177 30±34

51±87 32±118 44±200 16±32 30 ‹ 4.5 9

44±87 10±19 50±120 10 ‹ 3 8

25±262 1±130

21±49 2±106

(1) Chan (1992); (2) Wong et al. (1995); (3) Fung (1993), (4) Ong Che and Cheung (1998); (5) Prudente et al. (1994); (6) Papadopoulos et al. (1997); (7) Peerzada and Rohoza (1989); (8) Lacerda et al. (1992); (9) Van den Hurk et al. (1997); (10) Jones and Turki (1997); (11) Emmerson et al. (1997); (12) This study. a Mean ‹ standard deviation. b Range of means.

however, much lower than those measured in contaminated dredged material from the Marinas, USA (Papadopoulos et al., 1997) and those from the Tees Estuary, UK which has received domestic sewage and industrial e‚uents since the middle of the 19th century (Jones and Turki, 1997). Metal concentrations in the surface sediments from the mud¯at were 4±25% higher than those found in the deeper sediments, re¯ecting increased anthropogenic input to the sediment metal load. Relative Topsoil Enrichment Index approximated 1.0 for all the metals, re¯ecting a relatively uncontaminated condition in contrast to contaminated soils near mineworkings and smelters which have RTE values ranging up to 20 (Colbourn and Thornton, 1978). Vertical sections of the sediments can give a record of the level of contamination over time, provided that the pollutants are persistent and the sediment stratum has not been seriously disturbed by human activities such as dredging (Fung, 1993). Sedimentation rate within Deep Bay can be as much as 2 cm yrÿ1 (L. Young, pers. comm.). An RTE index of around 1.0 would, therefore, suggest that the heavy metal contamination rate at the mud¯at has been constant over the past 15 years or so. Table 7 compares the heavy metal content in mangrove sediments measured in this study with those in soil samples from mangroves in Hong Kong and in other estuaries. The Futian Nature Reserve, Shenzhen is one of the Sites of Special Scienti®c Interest (SSSI) within the Deep Bay Ramsar Site. Mean concentrations of Zn, Pb and Ni were more elevated in the mangrove sediments from Mai Po compared with those from the Shenzhen mangrove while concentrations of Cu and Cr were approximately similar. Compared with the mangrove at Sai Keng, Northeastern Hong Kong, concentrations of Zn, Cu, Cr and Ni were more elevated at Mai Po while Pb and Cd concentrations were comparable. Di€erences in 274

the sediment metal concentrations in these 3 mangroves may be related to the rate of urbanization and types of industries in their respective catchment areas. Compared with mangroves in other parts of the world, concentrations of some metals, such as Zn, Pb and Cu, were 2±3 times more elevated at Mai Po than those reported upon from the mangrove at Brisbane, Australia which receives industrial and urban discharges (Mackey et al., 1992), and those from the salt marsh close to 2 industrial/port cities on the Georgia coast, USA (Alberts et al., 1990). Metal concentrations were 2±6 fold higher in the mangrove sediments from Mai Po compared with samples from the Bay of Cadiz salt marsh on the southern Atlantic Coast of Spain which is far from pollution sources (Izquierdo et al., 1997) and with samples of unpolluted wetland soil (Scholes et al., 1998). Metal concentrations in the mangrove sediments from Mai Po were, however, much lower than those measured from the Odiel salt marsh which receives sewage from an industrial district and discharges from a mining area (Izquierdo et al., 1997). The di€erence between these last 2 sites could be as much as 1±2 orders of magnitude for some metals. Heavy metal concentrations in the bulk sediments from the mud¯at were generally higher than those measured in sediments between mangrove roots. Similar observations were reported upon by Lacerda et al. (1997) for Cd and Zn concentrations in sediments from the Sepetibo Bay, Rio de Janeiro, Brazil mud¯at and from the Spartina alterni¯ora marshes. Part of sediment metal burden at Mai Po may be of anthropogenic origin. Metals and other wastes discharged from the surrounding industrial areas may be transported by tidal currents and may eventually incorporate into sediments. The area where the mangrove sediments were sampled is situated  1 km upshore from the open mudl¯at area. The mangroves, therefore, are

Volume 39/Numbers 1±12/January±December 1999 TABLE 7 Heavy metal concentrations (lg gÿ1 dry weight) in tissues of salt marsh and mangrove plants determined in this and other studies. Sample 1

Spartina alterni¯ora Spartina alterni¯ora 2 Spartina alterni¯ora 3 Spartina alterni¯ora 3 Spartina maritima 4 Spartina anglica 5 Spartina anglica 5 Aster tripolium 5 Aster tripolium 5 Arthrocnemum fructicosum Halimione portulacoides 4 Typha latifolia 6 Typha latifolia 6 Kandelia candel 7 Kandelia candel 8 Kandelia candel 9 Acanthus ilicifolius 9 Aegicerus corniculatum 8 Aegicerus corniculatum 9

a

4

Whole Plant Shootb Rootsc Stemc Rootsd Rootsc Shootd Rootsc Shootc Rootsd Rootsd Rootse Leavesf Whole Plantd Leaves f Rootsd Rootsd Leavesf Rootsd

Zn

Fe

10±20 8±23 16±173 6±47 58±866 247±559 52±81 21±54 39±65 149±935 275±963

120±1100 900±8000 417±3030 39±372

16±25 70 ‹ 25 82±208 134±325 85 ‹ 29 44±137

9563 70 ‹ 4

Pb

59±920

90±879 235±840

Cd

2.5±34.5 n.d.±0.7 0.4±2.1 0.9±6.2

Cr

0.3

1±3 5±6

0.4±4

1750±8800 3600±7450

20±60 20±60

0.1±0.6 0.1±0.5

2±6 2±6

2235±5850

20±60

0.1±0.5

2±6

Cu

Ni

2±5 2±5 5±12 4±8 47±128 14±110 11±22 21±47 8±17 6±80 60±274 36 13 ‹ 1 2±7 4‹1 20±29 25±65 4 ‹ 0.8 22±46

1±3

<1

<1 1±13 52 55 ‹ 3 4±28 8±20 6±32

(1) Drifmeyer and Redd (1981); (2) Gleason et al. (1979); (3) Alberts et al. (1990); (4) Cacßador et al. (1996); (5) Otte et al. (1993); (6) Taylor and Crowder (1983); (7) Zheng et al. (1996); (8) Tam et al. (1995); (9) This study. Geometric mean ‹ 2 SD. b Range of means of 4 months. c Range of means from several sites. d Range. e Single determination. f Mean ‹ 1 SD. a

less frequently inundated and would receive less anthropogenic input. Mackey and Hodgkinson (1995) determined the total concentrations of 10 trace metals along 12 transects laid down a mangrove woodland near the mouth of the Brisbane River, Australia. They reported that metal concentrations tended to increase from land to sea and attributed this to the role of tidal deposition in determining the spatial distribution of metals in sediments. Metal concentrations in the mud¯at sediments and in sediments between mangrove roots may also di€er because of variations in sediment characteristics in the 2 areas which would a€ect metal availability and consequently, plant uptake. Organic matter and silt-clay content, as determined in this study, were very similar at these 2 sites. Other sediment properties which are related to the presence or absence of vegetation may, however, be more important in determining sediment metal concentrations. According to Ross (1994), the ®ne roots of plants and trees can e€ect small changes in soil conditions in the rhizosphere which can in¯uence metal bioavailability and their transfer from soil to plants. Sarkar and Wyn Jones (1982) showed that small changes in pH in the rhizosphere could make the trace metals more available for uptake. Exudation of H2 CO3 by roots may also help to solubilise metal carbonates and make them more bioavailable (Xian and Shokohifard, 1989). Many marsh and mangrove plants have aerenchymous tissues which supply oxygen to the roots buried in anaerobic soils. The amount of oxygen transported to the root often exceeds the demand of root tissue, re-

sulting in radial oxygen loss into the rhizosphere (Otte, 1991). Oxidation activity in the roots of Kandelia candel was demonstrated by Chiu and Chou (1993). He found that activity was highest in the apical section of the root, declining progressively toward the basal section. Due to this process, the soil at vegetated sites, in many cases, has a much higher redox potential compared to soil at nearby non-vegetated sites. The reduced state of the bulk soil in the mud¯at favours immobilization of heavy metals due to the formation of metal sulphides, but oxidation processes in the rhizosphere may mobilize the metals. Uptake by plant roots may therefore, account, in part, for the lower metal concentrations in the sediments between mangrove roots compared to those in bulk sediments from the mud¯at. Several investigators have conducted sequential extractions of heavy metals from mangrove soils treated with wastewaters. Their results indicate that metals are retained in mangrove soils in the organic fraction as well as in the water-soluble and exchangeable fractions (Chiu and Chou, 1991; Tam and Wong, 1995a, 1996; Izquierdo et al., 1997). These metals may be made available for plant uptake under the action of microbes or when sediment pH or redox potential changes. Symbiosis of salt marsh plants with fungi, like the vesicular arbuscular (VA) mycorrhiza may also be important in the uptake of heavy metals by these plants (Tinker and Gildon, 1983; Otte, 1991). Heavy metals in root tissues Metal concentrations in the root tissues of Acanthus ilicifolius, Aegicerus corniculatum and Kandelia candel 275

Marine Pollution Bulletin

fall within the ranges of concentrations measured for other salt marsh plants (Table 8). Species di€erences in metal concentrations are evident as are the variations in concentrations in di€erent plant parts. Metal content in di€erent plant species can vary greatly because of di€erent uptake systems. Monocotyledonous salt marsh plants, for example, tend to be excluders of heavy metals whereas dicotyledons generally act as accumulators (Rozema et al., 1986). Wide variations in plant metal content, however, can also occur in di€erent populations of the same species as plants respond to the concentration of metals in the soil and the speciation of these metals under particular edaphic conditions. Metals taken up by plant roots together with the uptake of mineral nutrients may be incorporated into the above-ground tissues. The distribution of metals within the plant depends on the ability of these metals to be transported. Some metals, such as Cr, Pb and Hg have low translocation rates and are, therefore, much more concentrated in roots than in stems or leaves (Alberts et al., 1990). Most of the data in Table 8 were obtained from a single sampling and therefore represents a snapshot of the amount of heavy metals in the plant tissues at the sampling time. Aside from species and habitat di€erences, there may be seasonal variations in the tissue metal content as metal concentrations get diluted because of biomass production during the growing season. Translocation and transport processes may also alter metal concentrations in plant organs in the short term (Gleason et al., 1979; Markert, 1993). In this study, concentrations of Zn, Fe, and Cu were the highest among the 7 metals measured in the root tissues. These metals are micronutrients essential for

plant growth so their elevated concentrations in the roots may re¯ect the physiologic requirements of the plants. Concentrations of Fe in the mangrove root tissues were 1±2 orders of magnitude greater than those of the other metals. High concentrations of Fe could be due to the presence of iron plaques on the roots. Plaques are formed when mangrove plant roots leak oxygen and oxidize the rhizosphere sediments. This, in turn, leads to oxidation of the iron and manganese in the soil and the deposition of iron on the roots (Otte, 1991). Plaques of hydrous iron oxides have been reported in a number of wetland species including the cattail Typha spp., the reed Phragmites australis, P. communis, the cord grass Spartina alterni¯ora, the grass Agrostis gigantea, and the sedge Carex rostrata (Taylor et al., 1984; McLaughlin et al., 1985; Crowder and Mac®e, 1986). According to McLaughlin et al. (1985), iron plaques can form up to 8% of total root dry weight and up to 98% of root iron. Oxidation processes in the rhizosphere and iron plaque formation can further change the speciation of heavy metals. Iron and manganese hydroxides are capable of adsorbing large quantities of heavy metals (Br ummer et al., 1988). Zinc, for example, accumulates in the iron plaque to higher concentrations than those found in the bulk soil and Cu may also be adsorbed. According to Otte (1991), adsorbed Zn appears to be still available for plant use. Of the non-essential metals measured in this study, Pb had the highest concentration. Pb is a multimedia pollutant and high concentrations of Pb in the roots may result not just from soil and water-borne Pb but also from atmospheric inputs from industrial processes and combustion of fuels and waste materials which have been absorbed by the foliage. The elevated concentra-

TABLE 8 Heavy metal concentrations (lg gÿ1 dry weight) in mangrove soils measured in this and other studies. Zn Futian nature reserve, Shenzhen Futian nature reserve, Shenzhen Futian nature reserve, Shenzhen Futian nature reserve, Shenzhen Sai Keng, Hong Kong 1 a Sai Keng, Hong Kong 3 a Sai Keng, Hong Kong 4 d Sai Keng, Hong Kong 6 b Mai Po, Hong Kong 7 b Unpolluted wetland soil 8 e Bay of Cadiz, Spain 9 d Odiel, Spain 9 d Brisbane, Australia 10 b Georgia, USA 11 d

1 a 2 b 5 c 3a

143 ‹ 22 146(53±423) 63 ‹ 11 40 ‹ 3 8‹1 31±48 53(17±147) 293(192±553) 23±50 98±117 1000±3450 98(41±144) 18±88

Fe

Pb

Cd

35(0.1±63)

4 ‹ 0.3 3(0.3±8) 0.2 ‹ 0.1 0.7 ‹ 0.3 0.2 ‹ 0.01

51±138 58(8±241) <0.05 423(100±825) 199(90±300) 0.6(0.2±0.7) 4±40 0.1±2 7480±7600 26±61 0.3 40200±55500 116±285 9±19 67(20±82) 0.8(<0.1±1.9) 6040±37700 1.5±2.4

Cr 34(7±57) 8

<0.20 14(4±40) 7±71 67±69 61±67 33(13±54) 9±79

Cu

Ni

44 ‹ 0.5 41(16±308)

11 ‹ 0.6

8 ‹ 0.5 16 ‹ 2 4 ‹ 0.4 12(1±41) 46(29±76) 4±20 25±31 221±757 22(3±30) 2±17

25 2 ‹ 0.6 2 ‹ 0.2 2 ‹ 0.2 13±23 <0.30 66(30±102) 2±23 27±30 43±46 5±24

(1) Tam and Wong (1996); (2) Tam et al. (1995); (3) Tam and Wong (1995a); (4) Tam et al. (1993); (5) Zheng and Lin (1996); (6) Tam and Wong (1995b); (7) This study; (8) Scholes et al. (1998); (9) Izquierdo et al. (1997); (10) Mackey et al. (1992); (11) Alberts et al. (1990). Mean ‹ standard deviation. b Mean (range). c Mean. d Range of means. e Range. a

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Volume 39/Numbers 1±12/January±December 1999

tion of this non-essential metal in the roots suggests a possible function of sequestering toxic metals in this organ. Higher plants, particularly spermatophytes, have been frequently considered for their role as bioindicators of heavy metals (Wittig, 1993; Streit and Stumm, 1993). If the Pb concentration in the roots may be taken to re¯ect the level of the environmental contamination, then the present results show mild contamination compared with the Pb concentration in the roots of the salt marsh species at the Tagus estuary, Portugal, which receives e‚uents from nearby chemical, steelmaking and shipbuilding industries. Concentration factors among the 3 mangrove species varied by a factor of 1.2±2.0. For all the 3 species, concentration factors of Fe and Cu were highest. Fe is a contituent of cytochromes and of nonheme iron proteins involved in photosynthesis, nitrogen ®xation and respiration while Cu is an essential component of ascorbic acid oxidase, tyrosinase, monoamine oxidase, uricase, cytochrome oxidase (Taiz and Zeiger, 1991). A high concentration factor, suggesting active uptake and possibly storage, for these essential metals is, therefore, not surprising. Concentration factor for the nonessential metal, Cd, was also high. It has been suggested that Cd is mostly unavailable for uptake by plants and that uptake is inhibited by the presence of large amounts of other metal ions, especially Zn, present in the soil (Thornton, 1981). Certain higher plant families, however, do accumulate high levels of Cd in their aerial parts (Kuboi et al., 1986). Intermediate values of concentration factors (0.1±0.2) were obtained for Zn, Pb and Ni. This may imply that tissue concentrations were controlled by a steady state exchange, as in the case of Zn, an essential micronutrient, in the root tissues of A. corniculatum and K. candel, or may indicate an active regulation of the internal concentration, as in the case of the non-essential metals. None of the root samples showed low concentration factors (of the order of magnitude 10ÿ2 ), indicating no storage, as has been recorded for Al and Fe in Spartina alterni¯ora and S. cynosuroides and for other metals in some crop plants (Alberts et al., 1990; Ross, 1994). Conclusion Concentration of 7 heavy metals, Zn, Fe, Cu, Cr, Cd, Pb and Ni in mud¯at sediments, mangrove sediments between roots and root tissues of Acanthus ilicifolius, Aegicerus corniculatum, and Kandelia candel from the Mai Po Nature Reserve, Northwest Hong Kong, were measured. Comparison of the results of this study with those from other areas shows a moderate heavy metal contamination in sediments from the mud¯at and mangroves at Mai Po. Such contamination could arise from discharges into Deep Bay from various industries (textile, dyeing, food processing, steel, printed circuit boards and electroplating industries) from the Yuen Long In-

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Volume 39/Numbers 1±12/January±December 1999 Xian, X. and Shokohifard, G. (1989) E€ect of pH on chemical forms and plant availbility of cadmium, zinc and lead in polluted soils. Water, Air and Soil Pollution, 45, 265±273. Young, L. and Melville, D. S. (1993) Conservation of the Deep Bay environment. In The Marine Biology of the South China Sea. Proceedings of the First International Conference on the Marine Biology of Hong Kong and the South China Sea, Hong Kong, 28 October±3 November 1990. (B. Morton, ed.), pp. 211±231. Hong Kong University Press, Hong Kong.

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