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Heavy metals in Metapenaeus ensis, Eriocheir sinensis and sediment from the Mai Po marshes, Hong Kong
The Science of the Total Environment 214 Ž1998. 87]97
Heavy metals in Metapenaeus ensis, Eriocheir sinensis and sediment from the Mai Po marshes, Hong Kong R.G. Ong Che a,U , S.G. Cheung b b
a Department of Applied Science, Hong Kong Technical College, Chai Wan, Hong Kong Department of Biology and Chemistry, City Uni¨ ersity of Hong Kong, Kowloon, Hong Kong
Abstract The Mai Po Marshes Nature Reserve in north-west Hong Kong is a Ramsar site visited by some 60 000 migratory birds each year. Due to increasing industrialization around the Deep Bay area, the environment at Mai Po may be threatened by heavy metal contamination. In this study, concentrations of four heavy metals Žchromium, lead, iron and zinc. were determined in sediment samples and in tissues of the commercial shrimp Metapenaeus ensis and the Chinese mitten crab Eriocheir sinensis. Samples were obtained from four gei wais Ž8, 11, 16r17 and 19. running along a north]south transect within the nature reserve. Measured concentrations Ž m g metal gy1 dry wt.. in sediment, M. ensis and E. sinensis tissues were: for Cr, 49.6]559.1, 1.5]3.5 and 6.0]6.2; for Fe, 3168.1]15 478.7, 91.8]180.3, 845.2]2304.0, for Pb, 100.5]154.8, 8.4]11.7, 15.9]19.2 and for Zn, 226.4]421.1, 75.5]96.8 and 163.7]187.1, respectively. Concentrations of the heavy metals in M. ensis were all below the legislation limit but those in E. sinensis were slightly in excess. Analysis of variance showed no significant differences between sites in the trace metal concentrations in M. ensis tissues. Significant differences between sites were, however, obtained for Fe concentration in E. sinensis and for concentrations of Fe, Cr and Zn in sediments. Discriminant function analysis on the metal concentrations in M. ensis and E. sinensis tissues separated gei wai 16r17 from the other gei wais, mostly on account of the lead concentration in M. ensis and the Zn concentration in E. sinensis. For the sediment samples, gei wais 8 and 11 were well separated from gei wais 16r17 and 19 with both Cr and Fe concentrations contributing significantly to the discrimination of gei wais. Q 1998 Elsevier Science B.V. Keywords: Metapenaeus ensis; Eriocheir sinensis; Marshes; Sediment; Heavy metals
U
Corresponding author. Tel.: q852 27887749; fax: q852 27887406; e-mail: [email protected]
0048-9697r98r$19.00 Q 1998 Elsevier Science B.V. All rights reserved. PII S0048-9697Ž98.00056-4
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R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
1. Introduction Deep Bay is the largest estuarine area in Hong Kong. To its north is the Shenzhen Special Economic Zone ŽSEZ., China while the New Territories, Hong Kong lies to its south. Water from the Shenzhen River from the north-east and the Yuen Long and Tin Shui Wai Creeks from the south-east drain into Deep Bay. The area around Deep Bay encompasses five sites of special scientific interest ŽSSSIs.. Mai Po, on the Hong Kong side of Deep Bay, is one of them. The area around Deep Bay contains a diversity of natural and man-made habitats, including one of the largest and most diverse mangrove communities along the south China coast and a large expanse of intertidal mudflat. A rich flora and fauna occur here, including many species still undescribed. Both the mangrove and mudflat areas serve as important feeding and nesting sites for both resident and migratory birds. Over 60 000 birds belonging to 270 species have been recorded from the area around Deep Bay, including some considered rare or threatened ŽYoung and Melville, 1993.. For these reasons, the Deep BayrMai Po area was declared in 1995 as a wetland of international importance under the Ramsar Convention. The Mai Po Marshes comprises 381 ha of dwarf mangrove, shrimp ponds Žgei wais. and fish ponds. The gei wais have a high natural productivity due to the litter input from vegetation growing inside the ponds and from organic matter brought in from Deep Bay through a single sluice gate at flood tide. In late autumn and winter, shrimp larvae are flushed into the gei wais by opening the sluice gate at high tide. On the ebb tide, the gate is closed and the shrimp larvae are kept inside the gei wais and allowed to mature there. Some 3 months later the sluice gate is opened during the low tide in the bay and the shrimps can be harvested from the net placed across the opened sluice gate. Each gei wai can yield approximately 600 kg of shrimp each year ŽYoung and Melville, 1993.. In addition, many waterbirds like the heron and wader come to feed on the exposed areas of shallow water and mud when the gei wais are drained.
In recent years, the growing urban and industrial developments around Deep Bay are discharging higher levels of domestic and industrial effluents into the bay. The environmental impact of this needs to be assessed but information on the levels of contamination is scant. The Environmental Protection Department, Hong Kong Government measures the sediment levels of heavy metals at some 60 sites around Hong Kong, including one at Inner Deep Bay ŽEPD, 1995, 1996.. Some data also comes from studies on the biomonitoring potential for coastal trace metals of barnacles, amphipods ŽRainbow, 1992; Rainbow and Smith, 1992. and oysters ŽPhillips, 1979; Phillips et al., 1982.. The present study measures the levels of four heavy metals Žchromium, lead, iron and zinc. in the sediments and in the tissues of the commercial shrimp Metapenaeus ensis and the Chinese mitten crab Eriocheir sinensis collected from four gei wais at the Mai Po Nature Reserve. The data here may be of use for the conservation and management of Mai Po. 2. Materials and methods 2.1. Study sites Samples for heavy metal analysis were obtained from four gei wais running along a north]south transect within the Mai Po Nature Reserve. Gei wais 8 and 11 at the northern end of the reserve receive water from Channel No. 3 and is closer to the mouth of the Shenzhen River. Gei wais 16r17 and 19 at the southern end of the reserve is drained by Channels 5 and 6, respectively and are closer to the mouths of the Yuen Long and Tin Shui Wai Creeks ŽFig. 1.. 2.2. Sampling and analyses Approximately 50 g of surface sediments were collected from each of the gei wais. Samples of the commercial shrimp Metapenaeus ensis and the Chinese mitten crab Eriocheir sinensis were obtained during the harvesting season in October 1996. All samples were kept frozen until analysis. Sediment samples were dried at 1058C, ground
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97 Fig. 1. Map of the Mai Po marshes, showing the locations of gei wais 8, 11, 16r17 and 19. Filled circles in the gei wais indicate the sampling sites for sediments. 89
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
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and sieved through a 250-m m mesh. Three replicates of 1 g of dried and sieved sediments from each gei wai were digested in a Kjeldahl Digester with 1 ml of concentrated nitric acid and 10 ml of concentrated sulfuric acid at 2708C. Samples of M. ensis having a carapace length of 28.2]31.6 mm and E. sinensis having a carapace length of 29.6]31.5 mm from each gei wai were selected for analysis. These were dried at 658C and ground. Three replicates of 5 g of dried whole body tissues were digested in 15 ml of concentrated nitric acid at 1508C. Digests or dilutions were analysed for chromium, iron, lead and zinc by flame atomic absorption spectrophotometry on a Perkin Elmer ŽModel 3110. AA spectrophotometer with continuous deuterium background correction. Procedural blanks were prepared and analysed with the samples. Standard solutions were prepared by serial dilution and calibration curves were prepared by the method of standard additions. All metal concentrations are expressed as m g metal gy1 dry weight.
3. Results 3.1. Hea¨ y metal concentrations Heavy metal concentrations in surface sediments and whole body tissues of Metapenaeus ensis and Eriocheir sinensis from four gei wais within the Mai Po Nature Reserve are presented in Table 1. Metals tend to accumulate in sediments so metal concentrations are two to three orders of magnitude greater than that measured in M. ensis and E. sinensis tissues. Of the four metals measured, iron showed the highest concentration, both in sediments and in invertebrate tissues. Although the concentration of chromium in sediments was the second highest, its concentration in invertebrates was the lowest. Comparing among gei wais, the concentration of lead in sediments was relatively uniform, ranging from 100.5 to 154.8 m g gy1 . In contrast, the chromium and iron concentrations in sediments from gei wai 16r17 and gei wai 19 at the southern part of the Nature Reserve, were one order of
Table 1 Heavy metal concentrations Žmean " S.D., m g metal gy1 dry wt.. in surface sediments and whole body tissues of Metapenaeus ensis and Eriocheir sinensis from four gei wais within the Mai Po nature reserve
Sediment Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19 Mean M. ensis Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19 Mean E. sinensis Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19 Mean
Cr
Fe
Pb
Zn
53.8" 3.9 49.6" 0.1 559.1" 43.3 522.8" 29.1
3168.1" 945.7 6762.3" 1989.2 11 497.2" 2709.6 15 478.7" 823.3
154.8" 32.9 107.7" 35.2 100.5" 12.3 148.1" 47.1
226.4" 19.9 244.2" 95.9 248.0" 31.6 421.1" 92.2
296.3" 256.8
9339.1" 4962.9
127.8" 38.4
284.9" 101.4
3.5" 1.4 2.5" 0.5 1.5" 0.1 3.0" 0.3
91.8" 38.2 161.1" 15.1 180.3" 66.7 123.5" 23.2
9.2" 2.2 8.4" 1.8 11.7" 0.5 8.8" 0.2
88.9" 16.7 75.5" 9.7 96.8" 24.3 90.4" 30.7
2.6" 1.0
139.2" 49.8
9.5" 1.8
87.9" 20.3
6.0" 0.9 6.0" 0.5 6.2" 0.7 6.0" 0.5
2304.0" 379.8 1855.4" 655.0 845.2" 148.2 1363.3" 719.9
19.2" 1.0 17.2" 2.7 17.5" 2.4 15.9" 3.0
187.1" 17.2 164.0" 13.3 184.7" 12.2 163.7" 6.3
6.0" 0.6
1592.0" 725.3
17.5" 2.4
174.9" 15.9
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
magnitude greater than those measured from samples from gei wais 8 and 11 at the north. The concentration of zinc in sediments from gei wai 19 was nearly twice that of samples from the other three gei wais. Less obvious are the inter-site differences in metal concentrations in the invertebrate tissues. The concentrations of lead and chromium in both M. ensis and E. sinensis varied by only 0.2]3.3 m g gy1 among gei wais, while a much wider range of metal concentrations at the four gei wais was obtained for iron Ž88.5 and 1458.8 m g gy1 in M. ensis and E. sinensis, respectively. and zinc Ž21.3 and 23.4 m g gy1 , respectively.. For all four metals measured in this study, concentrations were higher in E. sinensis than in M. ensis. 3.2. Analysis of ¨ ariance Table 2 presents the analysis of variance testing for differences between sites in the heavy metal concentrations in surface sediments and whole body tissues of M. ensis and E. sinensis. Inter-site differences were significant for chromium, iron and zinc in sediments and iron in E. sinensis. Neuman]Keuls post-hoc tests on site differTable 2 Analysis of variance testing for differences between sites in the heavy metal concentration in surface sediments and whole body tissues of Metapenaeus ensis and Eriocheir sinensis
Sediment Cr Fe Pb Zn M. ensis Cr Fe Pb Zn E. sinensis Cr Fe Pb Zn
F
P
351.1 25.4 2.0 5.2
0.000 0.000 0.200 0.027
3.5 2.8 3.2 0.5
0.069 0.109 0.083 0.691
0.1 4.3 1.0 3.0
0.950 0.045 0.453 0.098
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Table 3 Newman Keuls post-hoc tests on site differences in selected heavy metals determined from surface sediments and whole body tissues of Metapenaeus ensis and Eriocheir sinensis Žprobability values are given for sites significantly different from each other. Gei wai 8
Gei wai 11
Gei wai 16r17
Sediments: Fe Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19
ns 0.002 0.000
0.012 0.001
0.026
Sediments: Cr Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19
ns 0.000 0.000
0.000 0.000
ns
Sediments: Zn Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19
ns ns 0.035
ns 0.033
0.016
Eriocheir sinensis: Fe Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19
ns 0.040 ns
ns ns
ns
Gei wai 19
ences for selected heavy metals are shown in Table 3. Concentrations of iron, chromium and zinc in sediments from the southern gei wais 16r17 and 19 differed significantly from the northern gei wais 8 and 11. Between the two southern gei wais, concentrations of iron and zinc in sediments were also significantly different. As for the iron concentration in E. sinensis, significant differences were obtained between gei wai 8 and 16r17. 3.3. Discriminant function analysis Table 4 and Fig. 2 show the results of the discriminant function analysis on the heavy metal concentrations in the sediment, M. ensis and E. sinensis sampled from the four gei wais at Mai Po. For the sediment samples, the discriminant
92
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
Table 4 Results of discriminant function analysis on heavy metal concentrations in surface sediment and whole body tissues of Metapenaeus ensis and Eriocheir sinensis sampled from four gei wais at Mai Po A. Sediment samples Wilks’ l: 0.0001 Discriminant function Eigenvalue Cum. proportion Test of significance x2 value Degrees of freedom Variables Cr Fe Pb Zn B. M. ensis samples Wilks’ l: 0.009 Discriminant function Eigenvalue Cum. proportion Test of significance x2 value Degrees of freedom Variables Cr Fe Pb Zn C. E. sinensis samples Wilks’ l: 0.0916 Discriminant function Eigenvalue Cum. proportion Test of significance x2 value Degrees of freedom Variables Cr Fe Pb Zn
F12,13 s 27.916 I 528.863 0.990
P- 0.0000 II 4.246 0.998
60.18UUU 12 Standardized discriminant function coefficients y1.526 y1.644 0.257 y0.840
F12,13 s 5.433 I 52.091 0.982
0.316 y0.915 0.574 y0.896
P- 0.001 II 0.923 0.999
32.63UUU 12 Standardized discriminant function coefficients y3.386 0.280 3.116 0.435
F12,13 s 1.651 I 3.850 0.761
4.82 ns 6 y0.005 0.963 y0.708 y0.289
P- 0.154 II 1.183 0.994
16.71 ns 12 Standardized discriminant function coefficients y0.333 1.273 0.153 y1.014
function analysis was very significant ŽWilks’ l s 0.0001, P- 0.000.. Discriminant functions I and II accounted for 99.8% of the total separation among groups. A plot of the means of the canonical variables clearly separated gei wais 8 and 11 from gei wais 16r17 and 19 along DF I while along DF II, gei wai 8 was well separated from gei wai 11 as was gei wai 16r17 from gei wai 19. Both
16.27UU 6
5.66 ns 6 0.051 0.279 0.548 0.630
chromium and iron had the highest coefficients and contributed most to the discriminatory power of DF I while separation of gei wais along DF II was largely due to iron and zinc. ŽFig. 2A, Table 4A.. For the M. ensis samples, the discriminant function analysis was also very significant ŽWilks’ l s 0.009, P- 0.001.. However, only the first dis-
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
93
Fig. 2. Plots of the discriminant function analysis of heavy metal concentrations in sediment samples and tissues of Metapenaeus ensis and Eriocheir sinensis collected from four gei wais in Mai Po.
94
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
criminant function was significant Ž x 2 s 32.63, Ps 0.001.. DF I accounted for 98.2% of the discrimination among groups. A plot of the means of the canonical variables shows gei wai 16r17 well separated from the other three gei wais along DF I. Discrimination of gei wais along DF I was due to iron, zinc and lead concentrations. Along DF II, segregation of the remaining three gei wais was less clearly delineated ŽFig. 2B, Table 4B.. Discriminant function analysis on the metal concentration in the E. sinensis tissues did not produce significant separation of the gei wais ŽWilks’ l s 0.0916, P- 0.154.. Although the results are not statistically significant, the plot of the means of the canonical variables do reflect some degree of separation of the gei wais. Gei wai 16r17 could still be seen to be different from the other three gei wais along DF I, with iron contributing most to the discrimination along this axis. Segregation of the remaining three gei wais was less distinct ŽFig. 2C, Table 4C.. 4. Discussion 4.1. Conser¨ ation of Mai Po The Mai Po Marshes has been designated as a wetland of international importance under the Ramsar convention. It is an important feeding area for some 60 000 birds migrating along the East AsianrAustralian flyway each year. Growing urbanization and industrialization at both Shenzhen and Yuen Long may result in increasing threats to the environment. Little information is available on the heavy metal contamination levels at Mai Po ŽYoung and Melville, 1993.. The present study gives baseline information on the concentrations of four heavy metals Žchromium, lead, iron and zinc. in sediment, shrimp Ž Metapenaeus ensis. and crab Ž Eriocheir sinensis. tissues for the conservation needs of Mai Po. 4.2. Hea¨ y metals in the sediments The concentrations of heavy metal have been measured in sediments collected from various other localities in Hong Kong, e.g. Tolo Harbour,
a land-locked body of water, flanked by two developing satellite towns, Sha Tin and Tai Po and receiving a heavy load of agricultural and industrial effluent discharges; Victoria Harbour, a highly urbanized and industrialized site, East Lamma Channel, a relatively unpolluted site because of the strong Channel currents which tend to disperse and flush away contaminants discharged from nearby industrialized areas and some 60 other sites throughout the territory which are routinely monitored by the Environmental Protection Department, Hong Kong ŽPhillips and Yim, 1981; Chan, 1992; EPD, 1995, 1996; Wong et al., 1995.. Concentrations of the four metals in the gei wai sediments fall within the ranges reported upon in these other investigations. The contamination profiles of chromium, iron and zinc in the gei wai sediment samples show a north ] south gradient. Concentrations of chromium in the sediments from the northern gei wais 8 and 11 were one order of magnitude lower than that measured in sediments from the southern gei wais 16r17 and 19. A difference of one order of magnitude was also shown between the concentrations of iron in sediments from the northern and southern gei wais. Zinc concentrations in sediments from gei wais 8, 11 and 16r17 were very similar but that from the southernmost gei wai 19 showed a twofold elevation. Only the concentrations of lead in the sediments showed little variation among the gei wais. Of the four metals measured in this study, iron had the highest concentration, but the measured concentrations were lower than the values found for other sites in Hong Kong ŽPhillips and Yim, 1981; Chan, 1992; Wong et al., 1995.. Chromium concentrations in gei wais 8 and 11 sediments were low and are comparable to those reported for sediments from the East Lamma Channel ŽWong et al., 1995.. In contrast, the sediment chromium concentration of gei wais 16r17 and 19 approximated the values recorded for sediments from Kwun Tong ŽWong et al., 1995.. Although the concentrations of zinc in the gei wai sediments were less than that reported upon for Kwun Tong ŽWong et al., 1995., they were one to twofold greater than the measured concentrations of zinc in the Tolo Harbour sediments ŽChan,
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
1992a.. Zinc concentrations for gei wais 8, 11 and 16r17 were almost identical to the levels reported by Phillips and Yim Ž1981. for Victoria Harbour. The concentrations of lead were comparable to the data for the Kwun Tong area ŽWong et al., 1995.. The present study shows significant contamination of chromium, lead and zinc in the gei wai sediments. Several factors may contribute to this. Since sediments act as integrators and amplifiers of metal concentrations, discharges from various industries Žtextile, dyeing, food processing, steel, printed circuit boards and electroplating industries. from the Yuen Long Industrial Estate over the years may cause the elevated levels observed in sediments from the southern gei wais. Industrial and domestic wastes from the Yuen Long area are processed at the Yuen Long Sewage Treatment Plant prior to discharge into Deep Bay, but the treatment does not remove the heavy metals. Furthermore, corrosion of pipelines within the urban water supply network can lead to high levels of heavy metals draining into Deep Bay. The gei wai sediments are composed of more than 90% silt Žunpublished data. brought down by the Pearl River. Since grain size can affect the total surface area for binding of contaminants, the high metal load correlates with silty sediments at the gei wais. However, an important reason for the high metal levels in the gei wai sediments could be the enclosed nature of the gei wais together with irregular access to tidal flushing. This situation is analogous to the elevated metal load often observed in near-shore sediments due to terrestrial and anthropogenic input in contrast to that in the open marine areas. Nevertheless, the present data must be interpreted with caution. Sediment samples in this study were taken from one end of the gei wai and may not be completely representative. A variable sedimentary environment is characteristic of intertidal habitats. Metals are transported on fine particulate and organic materials carried by the tide. Tidal inundation can, therefore, cause a high degree of spatial variation in metal concentrations in sediments ŽMackey and Hodgkinson, 1995..
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At some very polluted sites like San Francisco Bay, the maximum sediment concentrations reported were 2900 m g Pb gy1 DW, 1890 m g Zn gy1 DW and 740 m g Cr gy1 DW ŽLuoma and Phillips, 1988.. Similarly, at Jinzhou Bay, considered the most heavily polluted bay in China, both zinc and lead concentrations were greater than 1000 m g gy1 DW ŽFan, 1989.. The degree of contamination at the gei wais have not reached these levels but in view of the conservation value of the gei wais, measures should be taken to prevent further deterioration. 4.3. Hea¨ y metals in Metapenaeus ensis and Eriocheir sinensis In contrast to the high metal load in sediments, heavy metal concentrations in M. ensis and E. sinensis were low. Tissue concentration of the four metals measured in this study fall within the range of values reported in the literature ŽEisler, 1981; Rainbow, 1990; Chan, 1992; Ismail et al., 1995.. With the exception of iron, the total body burden of zinc, chromium and lead varied over a narrow range in both M. ensis and E. sinensis compared to sediment metal concentrations. This suggests regulation of these metals in these two species. Decapod crustaceans regulate essential metals like zinc, copper, manganese but not nonessential ones like cadmium ŽRainbow, 1985, 1995.. Zinc is one of the more important essential metals, constituent of more than 90 enzymes and proteins and regulating the activity of many other enzymes ŽBryan et al., 1986.. The littoral prawn Palaemon elegans regulates the total body concentration at approximately 80 m g gy1 over a wide range of dissolved metal availabilities ŽWhite and Rainbow, 1982, 1984.. Zinc regulation has also been demonstrated in other decapod crustaceans including P. serratus ŽDevineau and Amiard Triquet, 1985., Pandalus montagui ŽRay et al., 1980., Carcinus maenas ŽRainbow, 1985. and other species of crabs ŽBryan, 1968.. Chromium is an important enzyme cofactor, but its accumulation strategy among decapod crustaceans is less well studied. Paez-Osuna et al. ´
96
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
Ž1995. reported high concentrations of chromium in the muscles of the lobster Panulirus inflatus compared to other tissues. Together with seven other metals, chromium was higher in the estuarine population of Penaeus stylirostris compared to the marine population ŽPaez-Osuna and Ruiz´ . Fernandez, 1995 . ´ No crustacean appears to regulate the body concentration of non-essential metals such as cadmium ŽRainbow, 1985; Rainbow and White, 1989.. The relative constancy of the total body concentration of lead, a non-essential metal, in both M. ensis and E. sinensis is therefore, surprising. This may just reflect the same relative constancy of the concentration of this metal in the sediments, that is, similar bioavailability of lead in the four gei wais. Iron is an oligoelement. It plays a vital role in the enzymatic and respiratory processes of crustaceans. Its concentration in the tissues of the two decapod species was the highest of the four metals measured in this study. Iron accumulated in the tissues due to the high availability of this metal in the sediments. Various groups of crustaceans accumulate iron from the medium ŽEisler, 1981. and iron concentrations in whole specimens of Penaeus sp. can reach 50 mg gy1 DW ŽEisler, 1981.. However, the total body burden of iron in M. ensis and E. sinensis showed a large variation between gei wais, unlike the clear increasing trend of iron sediment concentrations in the gei wais running from north to south. Since iron is adsorbed strongly to sediments, the presence of different amounts of iron-rich sediments in the guts of the specimens may account for this difference. Further comparing between species, the whole body tissue concentrations of the four metals in M. ensis are generally lower than in E. sinensis. Accumulation strategies for individual metals may differ in these two species. It may also result from the dilution of the accumulated metals in the actively growing, newly molted M. ensis. Similar dilution of accumulated metals was observed in Palaemon elegans ŽRainbow and White, 1989; Rainbow, 1990.. The habit and feeding mode may also be contributory factors. M. ensis has a swimming habit and feeds on the algae growing on the mud surface while E. sinensis is a bur-
rower and a deposit-feeder. The latter would therefore tend to accumulate more metals in its tissues. This is shown, for example, in the body burden of iron which is 11 times greater in E. sinensis than in M. ensis. Metapenaeus ensis is one of the major species in the commercial shrimp catch in many south-east Asian countries. It occurs naturally in the Pearl River estuary to the west of Hong Kong and is the shrimp of main economic importance cultured in the gei wais. Eriocheir sinensis is an edible crab also harvested from the gei wais. Heavy metal concentrations in the tissues of these two crustaceans is, therefore, a matter of public health concern. The Hong Kong maximum permitted concentration of chromium in prawns is 1.0 m g gy1 wet weight while that of lead in solid food is 6.0 m g gy1 wet weight. The recommended limit of the Ministry of Agriculture, Fisheries and Food ŽMAFF., UK for zinc is 50 m g gy1 wet weight. Iron concentrations are not legislated. After conversion of the data using a wet weight: dry weight ratio of 3. 86 for M. ensis and 2.85 for E. sinensis Žunpublished data., the measured levels in this study shows that concentrations of chromium, lead and zinc in M. ensis fall within the recommended limits but those in E. sinensis are slightly in excess. Acknowledgements Thanks are due to W.L. Cheung, K.C. Lee, S.F. Sia and S.T. Tong for the technical work done as part of the requirements for their Higher Diploma ŽHong Kong Technical College.. References Bryan GW. Concentrations of zinc and copper in the tissues of decapod crustaceans. J Mar Biol Assoc UK 1968;48:303]321. Bryan GW, Hummerstone LG, Ward E. Zinc regulation in the lobster Homarus gammarus: importance of different pathways of absorption and excretion. J Mar Biol Assoc UK 1986;66:175]199. Chan HM. The tissue contents and distributions of copper and zinc in six species of portunid crabs from Hong Kong. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China III, Proceedings of the Fourth Marine Biological Workshop: The Marine Flora and Fauna
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97 of Hong Kong and Southern China, Hong Kong, 11]29 April 1989. Hong Kong: Hong Kong University Press, 1992:629]640. Chan HM. Heavy metal concentrations in coastal sea water and sediments from Tolo Harbour, Hong Kong. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China III, Proceedings of the Fourth Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 11-29 April 1989. Hong Kong: Hong Kong University Press, 1992:621]628. Devineau J, Amiard Triquet C. Patterns of bioaccumulation of an essential trace element Žzinc. and a pollutant metal Žcadmium. in larvae of the prawn Palaemon serratus. Mar Biol 1985;86:139]143. Eisler R. Trace metal concentrations in marine organisms. New York: Pergamon Press, 1981. EPD. Marine water quality in Hong Kong for 1994. Environmental Protection Department, Hong Kong Government, 1995. EPD. Marine water quality in Hong Kong for 1995. Environmental Protection Department, Hong Kong Government, 1996. Fan ZJ. Tackling the most heavily polluted bay in China. Mar Pollut Bull 1989;20:362. Ismail A, Jusoh NR, Ghani IA. Trace metal concentrations in marine prawns off the Malaysian Coast. Mar Pollut Bull 1995;31:108]110. Luoma SN, Phillips DJH. Distribution, variability and impacts of trace elements in San Francisco Bay. Mar Pollut Bull 1988;19:413]425. Mackey AP, Hodgkinson MC. Concentrations and spatial distribution of trace metals in mangrove sediments from the Brisbane River, Australia. Environ Pollut 1995;90:181]186. Paez-Osuna F, Ruiz-Fernandez C. Comparative bioaccumula´ ´ tion of trace metals in Perlaeus stylirostris in estuarine and coastal environments. Estuarine Coast Shelf Sci 1995;40:35]44. Paez-Osuna F, Perez-Gonzalez R, Izaguirre-Fierro G, ´ Zarzueta-Padilla HM, Flores-Campana LM. Trace metal concentrations and their distribution in the lobster Panulirus inflatus ŽBouvier, 1895. from the Mexican Pacific coast. Environ Pollut 1995;90:163]170. Phillips DJH. The rock oyster Saccostrea glomerata as an indicator of trace metals in Hong Kong. Mar Biol 1979;53:353]360. Phillips DJH, Yim WWS. A comparative evaluation of oysters, mussels and sediments as indicators of trace metals in Hong Kong waters. Mar Ecol Prog Ser 1981;6:285]293. Phillips DJH, Ho CT, Ng LH. Trace elements in the Pacific oyster in Hong Kong. Arch Environ Contam Toxicol 1982;11:533]537. Rainbow PS. Heavy metal levels in marine invertebrates. In:
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Fumess RW, Rainbow PS, editors. Heavy metals in the marine environment. Florida: CRC Press, 1990:67]79. Rainbow PS. Trace metal concentrations in a Hong Kong penaeid prawn, Metapenaeopsis palmensis ŽHaswell.. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China II, Proceedings of the Second Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 1986. Hong Kong: Hong Kong University Press, 1990:1221]1228. Rainbow PS. Accumulation of Zn, Cu, Cd by crabs and barnacles. Estuarine Coast Shelf Sci 1985;21:669]686. Rainbow PS. The Talitrid amphipod Plaforchestia platensis as a potential biomonitor of copper and zinc in Hong Kong: laboratory and field studies. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China III, Proceedings of the Fourth Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 11-29 April 1989. Hong Kong, Hong Kong University Press, 1992:599]609. Rainbow PS. Physiology, physicochemistry and metal uptake } a crustacean perspective. Mar Pollut Bull 1995;31:55]59. Rainbow PS, Smith BD. Biomonitoring of Hong Kong coastal trace metals by barnacles, 1986-1989. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China III, Proceedings of the Fourth Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 11-29 April 1989. Hong Kong: Hong Kong University Press, 1992:585]597. Rainbow PS, White SL. Comparative strategies of heavy metal accumulation by crustaceans: zinc, copper and cadmium in a decapod, an amphipod and a barnacle. Hydrobiologia 1989;174:245]262. Ray S, McLeese DW, Wai wood BA, Pezzack D. The disposition of cadmium and zinc in Pandalus montagui. Arch Environ Contam Toxicol 1980;9:675]681. White SL, Rainbow PS. Regulation and accumulation of copper, zinc and cadmium by the shrimp Palaemon elegans. Mar Ecol Prog Ser 1982;8:95]101. White SL, Rainbow PS. Regulation of zinc concentration by Palaemon elegans ŽCrustacea: Decapoda.: zinc flux and effects of temperature, zinc concentration and moulting. Mar Ecol Prog Ser 1984;16:135]147. Wong YS, Tam NFY, Lau PS, Xue XZ. The toxicity of marine sediments in Victoria Harbour, Hong Kong. Mar Pollut Bull 1995;31:464]470. Young L, Melville DS. Conservation of the deep bay environment. In: Morton B, editor. 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. Hong Kong: Hong Kong University Press, 1993:211]231.
Heavy metals in Metapenaeus ensis, Eriocheir sinensis and sediment from the Mai Po marshes, Hong Kong R.G. Ong Che a,U , S.G. Cheung b b
a Department of Applied Science, Hong Kong Technical College, Chai Wan, Hong Kong Department of Biology and Chemistry, City Uni¨ ersity of Hong Kong, Kowloon, Hong Kong
Abstract The Mai Po Marshes Nature Reserve in north-west Hong Kong is a Ramsar site visited by some 60 000 migratory birds each year. Due to increasing industrialization around the Deep Bay area, the environment at Mai Po may be threatened by heavy metal contamination. In this study, concentrations of four heavy metals Žchromium, lead, iron and zinc. were determined in sediment samples and in tissues of the commercial shrimp Metapenaeus ensis and the Chinese mitten crab Eriocheir sinensis. Samples were obtained from four gei wais Ž8, 11, 16r17 and 19. running along a north]south transect within the nature reserve. Measured concentrations Ž m g metal gy1 dry wt.. in sediment, M. ensis and E. sinensis tissues were: for Cr, 49.6]559.1, 1.5]3.5 and 6.0]6.2; for Fe, 3168.1]15 478.7, 91.8]180.3, 845.2]2304.0, for Pb, 100.5]154.8, 8.4]11.7, 15.9]19.2 and for Zn, 226.4]421.1, 75.5]96.8 and 163.7]187.1, respectively. Concentrations of the heavy metals in M. ensis were all below the legislation limit but those in E. sinensis were slightly in excess. Analysis of variance showed no significant differences between sites in the trace metal concentrations in M. ensis tissues. Significant differences between sites were, however, obtained for Fe concentration in E. sinensis and for concentrations of Fe, Cr and Zn in sediments. Discriminant function analysis on the metal concentrations in M. ensis and E. sinensis tissues separated gei wai 16r17 from the other gei wais, mostly on account of the lead concentration in M. ensis and the Zn concentration in E. sinensis. For the sediment samples, gei wais 8 and 11 were well separated from gei wais 16r17 and 19 with both Cr and Fe concentrations contributing significantly to the discrimination of gei wais. Q 1998 Elsevier Science B.V. Keywords: Metapenaeus ensis; Eriocheir sinensis; Marshes; Sediment; Heavy metals
U
Corresponding author. Tel.: q852 27887749; fax: q852 27887406; e-mail: [email protected]
0048-9697r98r$19.00 Q 1998 Elsevier Science B.V. All rights reserved. PII S0048-9697Ž98.00056-4
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R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
1. Introduction Deep Bay is the largest estuarine area in Hong Kong. To its north is the Shenzhen Special Economic Zone ŽSEZ., China while the New Territories, Hong Kong lies to its south. Water from the Shenzhen River from the north-east and the Yuen Long and Tin Shui Wai Creeks from the south-east drain into Deep Bay. The area around Deep Bay encompasses five sites of special scientific interest ŽSSSIs.. Mai Po, on the Hong Kong side of Deep Bay, is one of them. The area around Deep Bay contains a diversity of natural and man-made habitats, including one of the largest and most diverse mangrove communities along the south China coast and a large expanse of intertidal mudflat. A rich flora and fauna occur here, including many species still undescribed. Both the mangrove and mudflat areas serve as important feeding and nesting sites for both resident and migratory birds. Over 60 000 birds belonging to 270 species have been recorded from the area around Deep Bay, including some considered rare or threatened ŽYoung and Melville, 1993.. For these reasons, the Deep BayrMai Po area was declared in 1995 as a wetland of international importance under the Ramsar Convention. The Mai Po Marshes comprises 381 ha of dwarf mangrove, shrimp ponds Žgei wais. and fish ponds. The gei wais have a high natural productivity due to the litter input from vegetation growing inside the ponds and from organic matter brought in from Deep Bay through a single sluice gate at flood tide. In late autumn and winter, shrimp larvae are flushed into the gei wais by opening the sluice gate at high tide. On the ebb tide, the gate is closed and the shrimp larvae are kept inside the gei wais and allowed to mature there. Some 3 months later the sluice gate is opened during the low tide in the bay and the shrimps can be harvested from the net placed across the opened sluice gate. Each gei wai can yield approximately 600 kg of shrimp each year ŽYoung and Melville, 1993.. In addition, many waterbirds like the heron and wader come to feed on the exposed areas of shallow water and mud when the gei wais are drained.
In recent years, the growing urban and industrial developments around Deep Bay are discharging higher levels of domestic and industrial effluents into the bay. The environmental impact of this needs to be assessed but information on the levels of contamination is scant. The Environmental Protection Department, Hong Kong Government measures the sediment levels of heavy metals at some 60 sites around Hong Kong, including one at Inner Deep Bay ŽEPD, 1995, 1996.. Some data also comes from studies on the biomonitoring potential for coastal trace metals of barnacles, amphipods ŽRainbow, 1992; Rainbow and Smith, 1992. and oysters ŽPhillips, 1979; Phillips et al., 1982.. The present study measures the levels of four heavy metals Žchromium, lead, iron and zinc. in the sediments and in the tissues of the commercial shrimp Metapenaeus ensis and the Chinese mitten crab Eriocheir sinensis collected from four gei wais at the Mai Po Nature Reserve. The data here may be of use for the conservation and management of Mai Po. 2. Materials and methods 2.1. Study sites Samples for heavy metal analysis were obtained from four gei wais running along a north]south transect within the Mai Po Nature Reserve. Gei wais 8 and 11 at the northern end of the reserve receive water from Channel No. 3 and is closer to the mouth of the Shenzhen River. Gei wais 16r17 and 19 at the southern end of the reserve is drained by Channels 5 and 6, respectively and are closer to the mouths of the Yuen Long and Tin Shui Wai Creeks ŽFig. 1.. 2.2. Sampling and analyses Approximately 50 g of surface sediments were collected from each of the gei wais. Samples of the commercial shrimp Metapenaeus ensis and the Chinese mitten crab Eriocheir sinensis were obtained during the harvesting season in October 1996. All samples were kept frozen until analysis. Sediment samples were dried at 1058C, ground
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97 Fig. 1. Map of the Mai Po marshes, showing the locations of gei wais 8, 11, 16r17 and 19. Filled circles in the gei wais indicate the sampling sites for sediments. 89
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
90
and sieved through a 250-m m mesh. Three replicates of 1 g of dried and sieved sediments from each gei wai were digested in a Kjeldahl Digester with 1 ml of concentrated nitric acid and 10 ml of concentrated sulfuric acid at 2708C. Samples of M. ensis having a carapace length of 28.2]31.6 mm and E. sinensis having a carapace length of 29.6]31.5 mm from each gei wai were selected for analysis. These were dried at 658C and ground. Three replicates of 5 g of dried whole body tissues were digested in 15 ml of concentrated nitric acid at 1508C. Digests or dilutions were analysed for chromium, iron, lead and zinc by flame atomic absorption spectrophotometry on a Perkin Elmer ŽModel 3110. AA spectrophotometer with continuous deuterium background correction. Procedural blanks were prepared and analysed with the samples. Standard solutions were prepared by serial dilution and calibration curves were prepared by the method of standard additions. All metal concentrations are expressed as m g metal gy1 dry weight.
3. Results 3.1. Hea¨ y metal concentrations Heavy metal concentrations in surface sediments and whole body tissues of Metapenaeus ensis and Eriocheir sinensis from four gei wais within the Mai Po Nature Reserve are presented in Table 1. Metals tend to accumulate in sediments so metal concentrations are two to three orders of magnitude greater than that measured in M. ensis and E. sinensis tissues. Of the four metals measured, iron showed the highest concentration, both in sediments and in invertebrate tissues. Although the concentration of chromium in sediments was the second highest, its concentration in invertebrates was the lowest. Comparing among gei wais, the concentration of lead in sediments was relatively uniform, ranging from 100.5 to 154.8 m g gy1 . In contrast, the chromium and iron concentrations in sediments from gei wai 16r17 and gei wai 19 at the southern part of the Nature Reserve, were one order of
Table 1 Heavy metal concentrations Žmean " S.D., m g metal gy1 dry wt.. in surface sediments and whole body tissues of Metapenaeus ensis and Eriocheir sinensis from four gei wais within the Mai Po nature reserve
Sediment Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19 Mean M. ensis Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19 Mean E. sinensis Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19 Mean
Cr
Fe
Pb
Zn
53.8" 3.9 49.6" 0.1 559.1" 43.3 522.8" 29.1
3168.1" 945.7 6762.3" 1989.2 11 497.2" 2709.6 15 478.7" 823.3
154.8" 32.9 107.7" 35.2 100.5" 12.3 148.1" 47.1
226.4" 19.9 244.2" 95.9 248.0" 31.6 421.1" 92.2
296.3" 256.8
9339.1" 4962.9
127.8" 38.4
284.9" 101.4
3.5" 1.4 2.5" 0.5 1.5" 0.1 3.0" 0.3
91.8" 38.2 161.1" 15.1 180.3" 66.7 123.5" 23.2
9.2" 2.2 8.4" 1.8 11.7" 0.5 8.8" 0.2
88.9" 16.7 75.5" 9.7 96.8" 24.3 90.4" 30.7
2.6" 1.0
139.2" 49.8
9.5" 1.8
87.9" 20.3
6.0" 0.9 6.0" 0.5 6.2" 0.7 6.0" 0.5
2304.0" 379.8 1855.4" 655.0 845.2" 148.2 1363.3" 719.9
19.2" 1.0 17.2" 2.7 17.5" 2.4 15.9" 3.0
187.1" 17.2 164.0" 13.3 184.7" 12.2 163.7" 6.3
6.0" 0.6
1592.0" 725.3
17.5" 2.4
174.9" 15.9
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
magnitude greater than those measured from samples from gei wais 8 and 11 at the north. The concentration of zinc in sediments from gei wai 19 was nearly twice that of samples from the other three gei wais. Less obvious are the inter-site differences in metal concentrations in the invertebrate tissues. The concentrations of lead and chromium in both M. ensis and E. sinensis varied by only 0.2]3.3 m g gy1 among gei wais, while a much wider range of metal concentrations at the four gei wais was obtained for iron Ž88.5 and 1458.8 m g gy1 in M. ensis and E. sinensis, respectively. and zinc Ž21.3 and 23.4 m g gy1 , respectively.. For all four metals measured in this study, concentrations were higher in E. sinensis than in M. ensis. 3.2. Analysis of ¨ ariance Table 2 presents the analysis of variance testing for differences between sites in the heavy metal concentrations in surface sediments and whole body tissues of M. ensis and E. sinensis. Inter-site differences were significant for chromium, iron and zinc in sediments and iron in E. sinensis. Neuman]Keuls post-hoc tests on site differTable 2 Analysis of variance testing for differences between sites in the heavy metal concentration in surface sediments and whole body tissues of Metapenaeus ensis and Eriocheir sinensis
Sediment Cr Fe Pb Zn M. ensis Cr Fe Pb Zn E. sinensis Cr Fe Pb Zn
F
P
351.1 25.4 2.0 5.2
0.000 0.000 0.200 0.027
3.5 2.8 3.2 0.5
0.069 0.109 0.083 0.691
0.1 4.3 1.0 3.0
0.950 0.045 0.453 0.098
91
Table 3 Newman Keuls post-hoc tests on site differences in selected heavy metals determined from surface sediments and whole body tissues of Metapenaeus ensis and Eriocheir sinensis Žprobability values are given for sites significantly different from each other. Gei wai 8
Gei wai 11
Gei wai 16r17
Sediments: Fe Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19
ns 0.002 0.000
0.012 0.001
0.026
Sediments: Cr Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19
ns 0.000 0.000
0.000 0.000
ns
Sediments: Zn Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19
ns ns 0.035
ns 0.033
0.016
Eriocheir sinensis: Fe Gei wai 8 Gei wai 11 Gei wai 16r17 Gei wai 19
ns 0.040 ns
ns ns
ns
Gei wai 19
ences for selected heavy metals are shown in Table 3. Concentrations of iron, chromium and zinc in sediments from the southern gei wais 16r17 and 19 differed significantly from the northern gei wais 8 and 11. Between the two southern gei wais, concentrations of iron and zinc in sediments were also significantly different. As for the iron concentration in E. sinensis, significant differences were obtained between gei wai 8 and 16r17. 3.3. Discriminant function analysis Table 4 and Fig. 2 show the results of the discriminant function analysis on the heavy metal concentrations in the sediment, M. ensis and E. sinensis sampled from the four gei wais at Mai Po. For the sediment samples, the discriminant
92
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
Table 4 Results of discriminant function analysis on heavy metal concentrations in surface sediment and whole body tissues of Metapenaeus ensis and Eriocheir sinensis sampled from four gei wais at Mai Po A. Sediment samples Wilks’ l: 0.0001 Discriminant function Eigenvalue Cum. proportion Test of significance x2 value Degrees of freedom Variables Cr Fe Pb Zn B. M. ensis samples Wilks’ l: 0.009 Discriminant function Eigenvalue Cum. proportion Test of significance x2 value Degrees of freedom Variables Cr Fe Pb Zn C. E. sinensis samples Wilks’ l: 0.0916 Discriminant function Eigenvalue Cum. proportion Test of significance x2 value Degrees of freedom Variables Cr Fe Pb Zn
F12,13 s 27.916 I 528.863 0.990
P- 0.0000 II 4.246 0.998
60.18UUU 12 Standardized discriminant function coefficients y1.526 y1.644 0.257 y0.840
F12,13 s 5.433 I 52.091 0.982
0.316 y0.915 0.574 y0.896
P- 0.001 II 0.923 0.999
32.63UUU 12 Standardized discriminant function coefficients y3.386 0.280 3.116 0.435
F12,13 s 1.651 I 3.850 0.761
4.82 ns 6 y0.005 0.963 y0.708 y0.289
P- 0.154 II 1.183 0.994
16.71 ns 12 Standardized discriminant function coefficients y0.333 1.273 0.153 y1.014
function analysis was very significant ŽWilks’ l s 0.0001, P- 0.000.. Discriminant functions I and II accounted for 99.8% of the total separation among groups. A plot of the means of the canonical variables clearly separated gei wais 8 and 11 from gei wais 16r17 and 19 along DF I while along DF II, gei wai 8 was well separated from gei wai 11 as was gei wai 16r17 from gei wai 19. Both
16.27UU 6
5.66 ns 6 0.051 0.279 0.548 0.630
chromium and iron had the highest coefficients and contributed most to the discriminatory power of DF I while separation of gei wais along DF II was largely due to iron and zinc. ŽFig. 2A, Table 4A.. For the M. ensis samples, the discriminant function analysis was also very significant ŽWilks’ l s 0.009, P- 0.001.. However, only the first dis-
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
93
Fig. 2. Plots of the discriminant function analysis of heavy metal concentrations in sediment samples and tissues of Metapenaeus ensis and Eriocheir sinensis collected from four gei wais in Mai Po.
94
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
criminant function was significant Ž x 2 s 32.63, Ps 0.001.. DF I accounted for 98.2% of the discrimination among groups. A plot of the means of the canonical variables shows gei wai 16r17 well separated from the other three gei wais along DF I. Discrimination of gei wais along DF I was due to iron, zinc and lead concentrations. Along DF II, segregation of the remaining three gei wais was less clearly delineated ŽFig. 2B, Table 4B.. Discriminant function analysis on the metal concentration in the E. sinensis tissues did not produce significant separation of the gei wais ŽWilks’ l s 0.0916, P- 0.154.. Although the results are not statistically significant, the plot of the means of the canonical variables do reflect some degree of separation of the gei wais. Gei wai 16r17 could still be seen to be different from the other three gei wais along DF I, with iron contributing most to the discrimination along this axis. Segregation of the remaining three gei wais was less distinct ŽFig. 2C, Table 4C.. 4. Discussion 4.1. Conser¨ ation of Mai Po The Mai Po Marshes has been designated as a wetland of international importance under the Ramsar convention. It is an important feeding area for some 60 000 birds migrating along the East AsianrAustralian flyway each year. Growing urbanization and industrialization at both Shenzhen and Yuen Long may result in increasing threats to the environment. Little information is available on the heavy metal contamination levels at Mai Po ŽYoung and Melville, 1993.. The present study gives baseline information on the concentrations of four heavy metals Žchromium, lead, iron and zinc. in sediment, shrimp Ž Metapenaeus ensis. and crab Ž Eriocheir sinensis. tissues for the conservation needs of Mai Po. 4.2. Hea¨ y metals in the sediments The concentrations of heavy metal have been measured in sediments collected from various other localities in Hong Kong, e.g. Tolo Harbour,
a land-locked body of water, flanked by two developing satellite towns, Sha Tin and Tai Po and receiving a heavy load of agricultural and industrial effluent discharges; Victoria Harbour, a highly urbanized and industrialized site, East Lamma Channel, a relatively unpolluted site because of the strong Channel currents which tend to disperse and flush away contaminants discharged from nearby industrialized areas and some 60 other sites throughout the territory which are routinely monitored by the Environmental Protection Department, Hong Kong ŽPhillips and Yim, 1981; Chan, 1992; EPD, 1995, 1996; Wong et al., 1995.. Concentrations of the four metals in the gei wai sediments fall within the ranges reported upon in these other investigations. The contamination profiles of chromium, iron and zinc in the gei wai sediment samples show a north ] south gradient. Concentrations of chromium in the sediments from the northern gei wais 8 and 11 were one order of magnitude lower than that measured in sediments from the southern gei wais 16r17 and 19. A difference of one order of magnitude was also shown between the concentrations of iron in sediments from the northern and southern gei wais. Zinc concentrations in sediments from gei wais 8, 11 and 16r17 were very similar but that from the southernmost gei wai 19 showed a twofold elevation. Only the concentrations of lead in the sediments showed little variation among the gei wais. Of the four metals measured in this study, iron had the highest concentration, but the measured concentrations were lower than the values found for other sites in Hong Kong ŽPhillips and Yim, 1981; Chan, 1992; Wong et al., 1995.. Chromium concentrations in gei wais 8 and 11 sediments were low and are comparable to those reported for sediments from the East Lamma Channel ŽWong et al., 1995.. In contrast, the sediment chromium concentration of gei wais 16r17 and 19 approximated the values recorded for sediments from Kwun Tong ŽWong et al., 1995.. Although the concentrations of zinc in the gei wai sediments were less than that reported upon for Kwun Tong ŽWong et al., 1995., they were one to twofold greater than the measured concentrations of zinc in the Tolo Harbour sediments ŽChan,
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
1992a.. Zinc concentrations for gei wais 8, 11 and 16r17 were almost identical to the levels reported by Phillips and Yim Ž1981. for Victoria Harbour. The concentrations of lead were comparable to the data for the Kwun Tong area ŽWong et al., 1995.. The present study shows significant contamination of chromium, lead and zinc in the gei wai sediments. Several factors may contribute to this. Since sediments act as integrators and amplifiers of metal concentrations, discharges from various industries Žtextile, dyeing, food processing, steel, printed circuit boards and electroplating industries. from the Yuen Long Industrial Estate over the years may cause the elevated levels observed in sediments from the southern gei wais. Industrial and domestic wastes from the Yuen Long area are processed at the Yuen Long Sewage Treatment Plant prior to discharge into Deep Bay, but the treatment does not remove the heavy metals. Furthermore, corrosion of pipelines within the urban water supply network can lead to high levels of heavy metals draining into Deep Bay. The gei wai sediments are composed of more than 90% silt Žunpublished data. brought down by the Pearl River. Since grain size can affect the total surface area for binding of contaminants, the high metal load correlates with silty sediments at the gei wais. However, an important reason for the high metal levels in the gei wai sediments could be the enclosed nature of the gei wais together with irregular access to tidal flushing. This situation is analogous to the elevated metal load often observed in near-shore sediments due to terrestrial and anthropogenic input in contrast to that in the open marine areas. Nevertheless, the present data must be interpreted with caution. Sediment samples in this study were taken from one end of the gei wai and may not be completely representative. A variable sedimentary environment is characteristic of intertidal habitats. Metals are transported on fine particulate and organic materials carried by the tide. Tidal inundation can, therefore, cause a high degree of spatial variation in metal concentrations in sediments ŽMackey and Hodgkinson, 1995..
95
At some very polluted sites like San Francisco Bay, the maximum sediment concentrations reported were 2900 m g Pb gy1 DW, 1890 m g Zn gy1 DW and 740 m g Cr gy1 DW ŽLuoma and Phillips, 1988.. Similarly, at Jinzhou Bay, considered the most heavily polluted bay in China, both zinc and lead concentrations were greater than 1000 m g gy1 DW ŽFan, 1989.. The degree of contamination at the gei wais have not reached these levels but in view of the conservation value of the gei wais, measures should be taken to prevent further deterioration. 4.3. Hea¨ y metals in Metapenaeus ensis and Eriocheir sinensis In contrast to the high metal load in sediments, heavy metal concentrations in M. ensis and E. sinensis were low. Tissue concentration of the four metals measured in this study fall within the range of values reported in the literature ŽEisler, 1981; Rainbow, 1990; Chan, 1992; Ismail et al., 1995.. With the exception of iron, the total body burden of zinc, chromium and lead varied over a narrow range in both M. ensis and E. sinensis compared to sediment metal concentrations. This suggests regulation of these metals in these two species. Decapod crustaceans regulate essential metals like zinc, copper, manganese but not nonessential ones like cadmium ŽRainbow, 1985, 1995.. Zinc is one of the more important essential metals, constituent of more than 90 enzymes and proteins and regulating the activity of many other enzymes ŽBryan et al., 1986.. The littoral prawn Palaemon elegans regulates the total body concentration at approximately 80 m g gy1 over a wide range of dissolved metal availabilities ŽWhite and Rainbow, 1982, 1984.. Zinc regulation has also been demonstrated in other decapod crustaceans including P. serratus ŽDevineau and Amiard Triquet, 1985., Pandalus montagui ŽRay et al., 1980., Carcinus maenas ŽRainbow, 1985. and other species of crabs ŽBryan, 1968.. Chromium is an important enzyme cofactor, but its accumulation strategy among decapod crustaceans is less well studied. Paez-Osuna et al. ´
96
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97
Ž1995. reported high concentrations of chromium in the muscles of the lobster Panulirus inflatus compared to other tissues. Together with seven other metals, chromium was higher in the estuarine population of Penaeus stylirostris compared to the marine population ŽPaez-Osuna and Ruiz´ . Fernandez, 1995 . ´ No crustacean appears to regulate the body concentration of non-essential metals such as cadmium ŽRainbow, 1985; Rainbow and White, 1989.. The relative constancy of the total body concentration of lead, a non-essential metal, in both M. ensis and E. sinensis is therefore, surprising. This may just reflect the same relative constancy of the concentration of this metal in the sediments, that is, similar bioavailability of lead in the four gei wais. Iron is an oligoelement. It plays a vital role in the enzymatic and respiratory processes of crustaceans. Its concentration in the tissues of the two decapod species was the highest of the four metals measured in this study. Iron accumulated in the tissues due to the high availability of this metal in the sediments. Various groups of crustaceans accumulate iron from the medium ŽEisler, 1981. and iron concentrations in whole specimens of Penaeus sp. can reach 50 mg gy1 DW ŽEisler, 1981.. However, the total body burden of iron in M. ensis and E. sinensis showed a large variation between gei wais, unlike the clear increasing trend of iron sediment concentrations in the gei wais running from north to south. Since iron is adsorbed strongly to sediments, the presence of different amounts of iron-rich sediments in the guts of the specimens may account for this difference. Further comparing between species, the whole body tissue concentrations of the four metals in M. ensis are generally lower than in E. sinensis. Accumulation strategies for individual metals may differ in these two species. It may also result from the dilution of the accumulated metals in the actively growing, newly molted M. ensis. Similar dilution of accumulated metals was observed in Palaemon elegans ŽRainbow and White, 1989; Rainbow, 1990.. The habit and feeding mode may also be contributory factors. M. ensis has a swimming habit and feeds on the algae growing on the mud surface while E. sinensis is a bur-
rower and a deposit-feeder. The latter would therefore tend to accumulate more metals in its tissues. This is shown, for example, in the body burden of iron which is 11 times greater in E. sinensis than in M. ensis. Metapenaeus ensis is one of the major species in the commercial shrimp catch in many south-east Asian countries. It occurs naturally in the Pearl River estuary to the west of Hong Kong and is the shrimp of main economic importance cultured in the gei wais. Eriocheir sinensis is an edible crab also harvested from the gei wais. Heavy metal concentrations in the tissues of these two crustaceans is, therefore, a matter of public health concern. The Hong Kong maximum permitted concentration of chromium in prawns is 1.0 m g gy1 wet weight while that of lead in solid food is 6.0 m g gy1 wet weight. The recommended limit of the Ministry of Agriculture, Fisheries and Food ŽMAFF., UK for zinc is 50 m g gy1 wet weight. Iron concentrations are not legislated. After conversion of the data using a wet weight: dry weight ratio of 3. 86 for M. ensis and 2.85 for E. sinensis Žunpublished data., the measured levels in this study shows that concentrations of chromium, lead and zinc in M. ensis fall within the recommended limits but those in E. sinensis are slightly in excess. Acknowledgements Thanks are due to W.L. Cheung, K.C. Lee, S.F. Sia and S.T. Tong for the technical work done as part of the requirements for their Higher Diploma ŽHong Kong Technical College.. References Bryan GW. Concentrations of zinc and copper in the tissues of decapod crustaceans. J Mar Biol Assoc UK 1968;48:303]321. Bryan GW, Hummerstone LG, Ward E. Zinc regulation in the lobster Homarus gammarus: importance of different pathways of absorption and excretion. J Mar Biol Assoc UK 1986;66:175]199. Chan HM. The tissue contents and distributions of copper and zinc in six species of portunid crabs from Hong Kong. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China III, Proceedings of the Fourth Marine Biological Workshop: The Marine Flora and Fauna
R.G. Ong Che, S.G. Cheung r The Science of the Total En¨ ironment 214 (1998) 87]97 of Hong Kong and Southern China, Hong Kong, 11]29 April 1989. Hong Kong: Hong Kong University Press, 1992:629]640. Chan HM. Heavy metal concentrations in coastal sea water and sediments from Tolo Harbour, Hong Kong. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China III, Proceedings of the Fourth Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 11-29 April 1989. Hong Kong: Hong Kong University Press, 1992:621]628. Devineau J, Amiard Triquet C. Patterns of bioaccumulation of an essential trace element Žzinc. and a pollutant metal Žcadmium. in larvae of the prawn Palaemon serratus. Mar Biol 1985;86:139]143. Eisler R. Trace metal concentrations in marine organisms. New York: Pergamon Press, 1981. EPD. Marine water quality in Hong Kong for 1994. Environmental Protection Department, Hong Kong Government, 1995. EPD. Marine water quality in Hong Kong for 1995. Environmental Protection Department, Hong Kong Government, 1996. Fan ZJ. Tackling the most heavily polluted bay in China. Mar Pollut Bull 1989;20:362. Ismail A, Jusoh NR, Ghani IA. Trace metal concentrations in marine prawns off the Malaysian Coast. Mar Pollut Bull 1995;31:108]110. Luoma SN, Phillips DJH. Distribution, variability and impacts of trace elements in San Francisco Bay. Mar Pollut Bull 1988;19:413]425. Mackey AP, Hodgkinson MC. Concentrations and spatial distribution of trace metals in mangrove sediments from the Brisbane River, Australia. Environ Pollut 1995;90:181]186. Paez-Osuna F, Ruiz-Fernandez C. Comparative bioaccumula´ ´ tion of trace metals in Perlaeus stylirostris in estuarine and coastal environments. Estuarine Coast Shelf Sci 1995;40:35]44. Paez-Osuna F, Perez-Gonzalez R, Izaguirre-Fierro G, ´ Zarzueta-Padilla HM, Flores-Campana LM. Trace metal concentrations and their distribution in the lobster Panulirus inflatus ŽBouvier, 1895. from the Mexican Pacific coast. Environ Pollut 1995;90:163]170. Phillips DJH. The rock oyster Saccostrea glomerata as an indicator of trace metals in Hong Kong. Mar Biol 1979;53:353]360. Phillips DJH, Yim WWS. A comparative evaluation of oysters, mussels and sediments as indicators of trace metals in Hong Kong waters. Mar Ecol Prog Ser 1981;6:285]293. Phillips DJH, Ho CT, Ng LH. Trace elements in the Pacific oyster in Hong Kong. Arch Environ Contam Toxicol 1982;11:533]537. Rainbow PS. Heavy metal levels in marine invertebrates. In:
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Fumess RW, Rainbow PS, editors. Heavy metals in the marine environment. Florida: CRC Press, 1990:67]79. Rainbow PS. Trace metal concentrations in a Hong Kong penaeid prawn, Metapenaeopsis palmensis ŽHaswell.. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China II, Proceedings of the Second Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 1986. Hong Kong: Hong Kong University Press, 1990:1221]1228. Rainbow PS. Accumulation of Zn, Cu, Cd by crabs and barnacles. Estuarine Coast Shelf Sci 1985;21:669]686. Rainbow PS. The Talitrid amphipod Plaforchestia platensis as a potential biomonitor of copper and zinc in Hong Kong: laboratory and field studies. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China III, Proceedings of the Fourth Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 11-29 April 1989. Hong Kong, Hong Kong University Press, 1992:599]609. Rainbow PS. Physiology, physicochemistry and metal uptake } a crustacean perspective. Mar Pollut Bull 1995;31:55]59. Rainbow PS, Smith BD. Biomonitoring of Hong Kong coastal trace metals by barnacles, 1986-1989. In: Morton B, editor. The marine flora and fauna of Hong Kong and Southern China III, Proceedings of the Fourth Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 11-29 April 1989. Hong Kong: Hong Kong University Press, 1992:585]597. Rainbow PS, White SL. Comparative strategies of heavy metal accumulation by crustaceans: zinc, copper and cadmium in a decapod, an amphipod and a barnacle. Hydrobiologia 1989;174:245]262. Ray S, McLeese DW, Wai wood BA, Pezzack D. The disposition of cadmium and zinc in Pandalus montagui. Arch Environ Contam Toxicol 1980;9:675]681. White SL, Rainbow PS. Regulation and accumulation of copper, zinc and cadmium by the shrimp Palaemon elegans. Mar Ecol Prog Ser 1982;8:95]101. White SL, Rainbow PS. Regulation of zinc concentration by Palaemon elegans ŽCrustacea: Decapoda.: zinc flux and effects of temperature, zinc concentration and moulting. Mar Ecol Prog Ser 1984;16:135]147. Wong YS, Tam NFY, Lau PS, Xue XZ. The toxicity of marine sediments in Victoria Harbour, Hong Kong. Mar Pollut Bull 1995;31:464]470. Young L, Melville DS. Conservation of the deep bay environment. In: Morton B, editor. 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. Hong Kong: Hong Kong University Press, 1993:211]231.