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Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
Toxicity of contaminated harbour sediment to
grey mullet, Liza macrolepis
hen' & C.-Y. chen2
Dept. of Marine Resources, National Sun Yat-sen University, Taiwan,
R. 0 .C.
2
Dept. of Marine Environmental Engineering, National Kaohsiung
Institute of Marine Technology, Taiwan, R.O. C.
M.-H.
Abstract
Liza macrolepis, a filter and a detritus-mud feeder, were exposed to
contaminated sediment from Kaohsiung Harbour, Taiwan, in order to evaluate
the toxicity and bioaccumulation of metals associated with descending
sediment-contaminated gradients. A 4x2 experimental design containing
contaminated Kaohsiung Harbour sediment in varying amounts (loo%, 50%,
25% and 0%) was employed in duplicate. The experimental sediment contained
30 mg of Hg, 8.0 mg of Cd, 900 mg of Cu, 150 mg of Ni and 6,000 mg of Znlkg
dry wt. of metals, which represented values 1 to 23 times greater than the ER-M
levels (NOAA, 1991). At the end of a 150-day period, the fish were killed and,
along with those which had already died, were measured for their
bioaccumulation levels in the whole body.
The results showed that the mortality in the 100% sediment-exposure
groups was significantly higher than that in the 50% and 25% groups. All of the
experimental fish contained elevated metal levels 2 to 14 times higher than
those of the control groups. In most cases, the bioaccumulation of
sediment-bound metals, namely, Hg, Cd, and Cu, did not correlate with the
contaminated gradients of the sediments. One exception, however, was Zn,
which showed a positive relationship to the sediment gradient. In the case of Ni,
the highest bioaccumulation levels were found in the 50% exposure group.
From these results, it is reasonable to assume that the bioavailability of
sediment-bound metals to the fish was element-dependent. Moreover, it is
suggested that the mortality rate of Liza macrolepis with long-term sedimental
exposure was due to the total toxicity effects of all of the elements combined.
From the point of view of biomonitoring, the bioaccumulated levels of metals in
grey mullet did not only reflect the degree of contamination in the sediment but
also represented the bioavailability of the sediment-bound metals transferred
into the biological phase in the aquatic environment. In light of the findings, the
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
280 Water Pollurion L'!
use of the grey mullet can be considered a most useful vehicle for
biomonitoring.
1
Introduction
Sediment has the dual function of being both the end-product of various
pollutants as well as the source of pollutants in the overlying water and the biota
in an aquatic ecosystem [l-31. Metals bound to the sediment might either leach
into the aqueous phase or come directly in contact with living organisms, which
in turn, would affect the health of the aquatic biota [4].
Therefore, contaminated sediments have been the center of attention of
many researchers focusing on the investigation of toxic effects on aquatic
organisms [5-1 l]. The toxic impact of sediment on aquatic organisms includes
lethality [12-181 and bioaccumulation [19-241.
The grey mullet (Liza macrolepis) are filter and detritus-mud feeders,
dominating the polluted Kaohsiung Harbour [25] in southern Taiwan. Previous
research has shown that they utilize bottom sediments as a source of food and,
as a consequence, bioaccumulate sediment-bound metals from contaminated
harbour sediments [26]. However, to assess the feasibility of using this common
coastal fish species as a bioindicator of metal pollution of sediments in a coastal
area, we conducted a sediment gradient exposure experiment to test the
relationship between the degree of metal contamination in the sediment and the
lethality and bioaccumulation of metals in the grey mullet.
2
Materials and Methods
The experiment was performed using a 4 X 2 design. The grey mullet, Liza
macrolepis, collected from Kaohsiung Harbour were exposed to three gradient
harbour sediment treatments (loo%, 50% and 25%) and one control (O%, i.e.
without any loading of sediment) in duplicate. The experimental sediment was
collected with an Ekman grab from the fifth dock in Kaohsiung Harbour. Later
it was mixed with the reference sediment that was taken from the Chi-ku
Lagoon, in southern Taiwan. Both types of sediment samples were separately
sun-dried, ground, well mixed and screened through a l-mm sieve for further
experimental usage. They were not mixed until they were loaded into the tanks.
In total, eight tanks (150 X 70 X 50 cm) were used in the experiment. Each
sediment-treated tank was loaded with the same total amount of sediment but in
specific proportions (i. e. HarbourILagoon). Representing the 100% experiment
groups were T1 and T5 which were loaded with only Harbour sediment. The
50% groups, namely T2 and T6, had 50% Harbour and 50% Lagoon sediment,
while the 25% groups, i.e. T3 and T7 were loaded with 25% Harbour and 75%
Lagoon sediment. The experimental tanks maintained a sediment-to-water ratio
of 10 kg to 100 litres. The control tanks T4 and T8 did not contain any sediment
whatsoever.
Chi-ku Lagoon sediments were chosen because their metal concentrations
were very low, all falling in the range of below or near the mean concentration
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
of those of the earth's crust. That is, Ag=0.01-0.12; As=6.1-21; Cd=<0.005-0.1;
Co=8.8-16.5; Cu=2.2-24; Fe=16.7-40%; Hg=0.020-0.150; Mn=271-586;
Pb=3-26; Ni=17-39; Se=0.33 -1.1; and Zn=37-198 pg/g dry wt. [27]. In
contrast, metal concentrations in the sediment taken from Kaohsiung Harbour
were highly contaminated: Cd=3-5; Cu=400-500; Pb=120-140 [28]; and
Hg=15-25 [Chen, unpublished data].
The fish were captured with a pond net from Kaohsiung Harbour at
flooding tide in spring and were kept alive in the laboratory for one month of
acclimation, after which they were randomly distributed into the eight tanks. In
total, 25 (TL=6.4*0.5cm, BW=3.9+0.7g) fish were put into each of the 6
experimental tanks and the 2 control tanks. The initial ratio of fish weight to
water volume was sustained at lg to 1.5-2 litres [29]. The temperature and
salinity parameters of the water were maintained at 25+4OC and 1.5+0.3%,
respectively.
During the 150-day experimental period, every one month -that is, on
days 30, 60, 90 and 120- 3 to 5 fish were taken from each tank and anesthetized
to measure their size. Mortality was also recorded daily. Whenever a dead fish
was found, it was removed and its length and weight were measured. It was then
refrigerated at -20°C for further analysis.
The fish were fed with a commercial fish food twice a day. The daily
feeding amount was consistent at approximately 3% of the total weight of all the
fish in each tank. The fish food was mainly composed of protein (35-40%),
carbohydrate (35-40%), lipid (3%), fiber (3%) and ash (17%). It also contained
Hg, Cd, Cu, Ni and Zn concentrations of 0.027,4.38, 18.4, 1.08 and 71.8 m g k g
dry wt., respectively.
At the end of experiment, for the analysis of Cd, Cu, Ni and Zn, sediment
samples (the dried fraction<63pm, Ig) were digested with 15 rnl acid fluid
which was a combination of nitric and hydrochloric acids (Merck, GR grade) in
a 1:2 ratio 1281. The concentrations of Cd, Cu, Ni and Zn in the fish were
determined in a way that pooled and homogenized 5-6 individuals, which either
were killed at the end of the experiment or had died during the experiment. Then,
one gram of the homogenized tissue was acid-digested with nitric acid in a ratio
of W(g):V(ml)=l:lO. Metal concentrations were determined with an atomic
absorption spectrometer (HITACHI 2-8200) following a method established
previously [28, 30-311. However, for the analysis of mercury, 0.5 grams of
sediment powder and 2 grams of fish tissue were digested with a combination of
lml HN03,4ml H2S04 (Merck, GR grade) and 15 rnl KMn04 (15% Merck, GR
grade), based on the method established by Chen and Chou [32]. Mercury
analyses were performed by means of a cold vapour atomic absorption
spectrophotometer (HITACHI 2-8200 with HFS-2). Certified reference
materials, namely DOLT-2 (dogfish liver from the National Research Council of
Canada (NRC)), DORM-2 (dogfish muscle from the NRC), MESS-2 (marine
sediment from the NRC) as well as IAEA-356 (polluted marine sediment from
the International Atomic Energy Agency), were used to verify the accuracy and
precision of the analyses. The results all produced a recovery rate of within i
10%.
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
282
Water Pollution W
Table 1: Mean and standard deviations of total length (TL, cm) and body
weight (BW, g) in the six experimental tanks.
Day 0 Day 60
3
Day 90 Day 120 Day 150
Tank
5.9
100% T1 TL 6.4 _ + O S 6 . 0 k 1.8 6.3 k 0 . 9 6.5 1. 0.3
BW 3 . 9 k 0 . 7 4 . 3 i 3 . 2 5.7k1.5 4 . 3 k 0 . 4
3.1
Table 2: Initial and final metal concentrations (mglkg dry wt.) of experimental
sediment in the six experimental tanks. R%: resident percentage=
percentage of final concentration divided by initial concentration.
I
Tank 1 Period 1
Hg
I Cd I Cu 1 Ni
Zn
100% T1 ( Initial 1 30.1 1.0 1 5.78 0.08 (894 5.41 143 k 1.2 1 6453 k 94
Final 25.2 0.9 3.63 k 0.02 573 k 0.1 104 f 0.71 5380 68
83.9
64.1
62.8
72.7
R%
83.4
T5 Initial 32.2 0.9 8.05 f 0.23 959 5 10 155 2.3 6133 56
Final 29.5 k 1.8 8.01 0.12 938 6.0 149 0.3 4794 +l50
+
+
+
+
+
+
+
+
+
+
+
1 50% T2 I Initial 1 24.1 F 1.3 1 4.68 + 0.06 1837 k 7.61 97.2 k 32 1 6042 + 26 1
Final 21.6 + 2.2 3.84 1 0 . 0 3 723 + 4.7 78.5 + 37 5984 +l65
82.1
89.6
86.4
80.8
R%
99.0
T6 Initial 16.2 + 1.8 3.45 + 0.04 537 + 2.4 102 + 1.5 3645 +- 78
Final 14.1 + 0.8 1.62 + 0.04 326 + 0.3 79.7 i 0.7 2634 + 67
87.0
60.7
47.0
R%
78.1
72.3
25% T3 Initial 12.5 + 2.1 2.45 + 0.10 478 + 9.3 89 k 2.4 3 127 f 45
Final 11.5 k 1.9 2.01 k 0.001 365 i 0.7 73.7 + 0.8 2692 k 24
92.0
82.0
76.4
82.3
R%
76.5
T7 Initial 10.3 + 0.8 2.13 + 0.09 321 + 3.6 64.3 k 3.4 231 1 f 56
Final 8.7 + 0.1 1.64 + 0.06 212 k 4.2 59.5 + 0.2 1740 + 64
l
I
I
I
I
l
I
I
I
R%
84.5
77.0
J
66.0
92.5
75.2
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
3 Results
During the entire experimental period, none of the fish showed any significant
growth. In fact, the size of the sub-sampled fish during the four experimental
sampling periods (i.e.on days 30, 60, 90 and 120) and at the end of experiment
(day 150) varied but did not show any increasing trends in t e r n of total length
or body weight. Given the method, it is not surprising that there was no
difference in fish size between the individual tanks (Table 1). Even so, by the
end of the experiment, in all groups, only the smaller fish had survived.
The final metal concentrations in the experimental sediment did not
exactly correspond to the initial nominal gradients. More specifically, the metal
concentrations of the sediment at the end of the experiment were only 47 to
99.5% of the levels at the onset of the experiments, but the relative decrease in
gradients still clearly remained (Table 2).
Of particular significance were the differences in the accumulative mortality rate
among the three treatment groups. The 100 % treatment groups experienced the
highest accumulative mortality rate throughout the entire experimental periods.
In fact, by the end of the experiment, more than 90% of those fish had died. On
the other hand, no difference was found between the 50% and 25% treatment
groups although these two groups suffered a higher mortality rate than did the
control groups (Figure 1).
The patterns of bioaccumulation of sediment-bound metals in the grey
mullet were obviously element-dependent. The bioaccumulations of metal levels
in the experimental fish were all significantly higher than the background metal
levels of the control groups (one-way ANOVA, p>0.05). To illustrate this, the
bioaccumulated concentrations of Hg, Cd, Cu, Ni and Zn in the grey mullet of
the sediment-exposure groups were, respectively, 2, 3, 4, 3-8 and 7-14 times
more elevated than those of control. Nevertheless, the bioaccumulation of Hg,
Cd and Cu in the grey mullet generally did not positively correlate with the
degree of sediment gradient. Unlike these contaminants, however, in the case of
Zn, there was a distinct correlation between metal levels in the sediment and the
bioaccumulated concentrations in the fish. Of note too is the bioaccumulation of
sediment-bound Ni which varied, with the highest value in the 50% exposure
group (Table 3).
4 Discussion and Conclusions
The Kaohsiung Harbour contaminated sediment was proven to be toxic to the
grey mullet, and the toxic effects seemed to have several detrimental effects,
including higher mortality and greater bioaccumulation. The non-diluted, 100%
harbour sediment significantly increased the mortality rate than did the diluted
50% and 25% sediments. This likely indicates that sediment containing Hg, Cd,
Cu, Ni and Zn concentrations which were, respectively, 6-25, 0.18-0.89, 0 5 2 . 5 ,
1.2-3.1 and 6-24 times higher than the 'effects range-medium' values (ER-M)
[33] had a severe impact on the detritus-mud feeding fish. It is noted that the
ER-M value refers to the contaminant level above which adverse biological
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
284
Water Pollution 1'1
Figure 1: Accumulative mortality in the 6 sediment-treated tanks. Tl&T5,
T2&T6 and T3&T7 indicate the 100, 50 and 25% Kaohsiung Harbour
sediment-treated groups, respectively.
Table 3: Mean and standard deviations of metal concentrations (pglg wet wt.)
of fishes in the 100, 50, 25 and 0% of contaminated sediment
exposure tanks. a, b, c and d indicate the results of Duncan's multiple
range test.
effects are frequently observed (i.e. Hg=1.3, Cd=9, Cu=390, Ni=50, Zn=270.
respectively) [33].
Just as in a previous study [26], the mullet accumulated the
sediment-associated metals, including Hg and Ni, in their bodies. It should be
pointed out that this is the first study to ever observe a bioaccumulation of
sediment-bound Hg in grey mullet. Comparatively, however, the
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
bioaccumulation levels of Cu, Ni and Zn were found to be much more elevated
in this study most likely on account of the higher doses that were applied here.
The bioaccumulation levels in the fish mostly did not show a consistent
relationship to the sediment gradient. Among the five elements examined, only
Zn showed a significant increased metal bioslccumulation trend corresponding to
the degree of contamination of the sediment. For the other elements, namely Hg,
Cd, Cu and Ni, no relationships were found. Nevertheless, the sediment-bound
Ni showed the highest bioaccumulation levels in the 50% sediment exposure
group; however, in the cases of Hg, Cd and Cu, no gradient effect related to the
degree of sediment-contamination was evident.
These results suggest that many factors, including the degree of
contamination in the sediment, the self-regulation ability of fish, the
sediment-binding site of metal and the bioavailability of metal to the fish, all
affected the lethality and bioaccumulation of these metals in the grey mullet.
Cadmium concentrations in the experimental sediment were only one-fourth to
two-thirds of the ER-M values, but the sediment-treated fish in all experimental
groups bioaccumulated 3 times more Cd than did those in the control, which
indicates that sediment-bound Cd was much more readily displaced from the
sediment than were the other elements [35, 361. However, the exposure dosage
of Cd might not have been high enough to form a bioaccumulation gradient in
the three experimental groups of grey mullet.
Copper is an essential element in the various physiological functions of
the fish [37], and it has been reported that these fish regulate it in a homeostatic
way [37]. The experimental doses of Cu may have been within adaptable levels,
which would have resulted in the fish, in the three-treatment groups
bioaccumulating Cu to the same degree.
Another important point is that Liza macrolepis have the ability to select a
particular size of granule in sediment [34, 381. In this study, the sediment grains
in each experimental tank were most likely heterogeneous, which would have
then caused the uptake of sediment-bound metals to vary based on the physical
characteristics of the sediment. This might be one of the factors leading to the
inconsistency in the amount of Ni-bioaccumulation in the fish studied in the
experiment.
Finally, since most sediment-bound Hg was held tight in the
sulphidic-organic (1-10%) and crystalline lattices (80-98%), and it did not easily
leach out [35, 361, it might have been less bioavailable to the digestive tracts of
the fish.
Although the experimental method used here was designed to maintain the
ratio sediment loading to water volume the same proportion, the experimental
contaminated sediments were diluted with Chi-ku sediment. Nevertheless, the
fine clay of the contaminated sediment might still be the major binding-site for
sediment metal and the one which the mullet mostly utilize [38]. The sediment
in the 50% and 25% groups which included sediment from the Chi-ku Lagoon
was not as rich in fine clay as was the sediment from Kaohsiung Harbour.
Therefore, the amount of available sediment-bound metal to the grey mullet in
each experimental tank would not have been equal. The mullet in the
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
experimental groups would have then randomly selected other fractions of
sediment, which could have caused the absence of correlation between the
bioaccumulation levels in the experimental fish and the gradient of the
sediments.
Consequently, it is suggested that the bioaccumulation and uptake of
sediment-bound metal in the grey mullet were both related to the individual
conditions in each tank; that is, the physico-chemical characteristics of the
sediments may have also played a critical role, rather than just the gradient of
the sediment metal concentrations.
From the viewpoint of biomonitoring, the bioaccumulation levels detected
in Liza macrolepis, may well have reflected the status of metal pollution in the
environment. Due to the grey mullet's ability to self-regulate essential elements,
such metal concentrations as Cu and Ni in the fish would not be expected to
correlate exactly with the low environmental contamination levels; on the other
hand, if the contamination levels were high enough such as in the case of Zn in
the experiment, the fish should have reflected the status of pollution in situ.
However, in the case of the non-essential elements, namely, Cd and Hg,
bioaccumulation after long-term exposure to the sediment was understandably
significant in this study. It can safely be concluded therefore that the
bioaccumulations of metals in the grey mullet were indicative of the extent of
environmental contamination.
Acknowledgements
T h e authors would like to express their gratitude to Miss In-nu Hung for her
helpful technical assistance. This research was funded by the National Science
Council, Taiwan, under projects nos. NSC 88-23 1 1-B-110-015 and NSC
88-23 13-B-002-003.
References
[ l ] Warren, L.J., Contamination of sediments by lead, zinc and cadmium: a review.
Environnlental Pollution, 2B, pp. 40 1-436, 198 1.
[2] Leitz, W. & Galling, G., Metals from sediments. Water Research, 23, pp. 247-252,
1989.
[3] Forstner, U., Inorganic sediment chemistry and elemental speciation. Sediments:
Chemistry and Toxicity of In-Pace Pollutants, eds. R. Baudo, J. Giesy & H. Muntau,
Lewis Publishers: Ann Arbor, pp. 6 1- 105, 1990.
[4] D'Itri, F.M., The biomethylation and cycling of selected metals and metalloids in
aquatic sediment. Sedinzents: Chemistry and Toxicity of In-Pace Pollutants, eds. R.
Baudo, J. Giesy & H.Muntau, Lewis Publishers: Ann Arbor, pp. 163-214, 1990.
[S] Waldichuk, M., Biological availability of metals to marine organisms. Marine
Pollution Bulletin, 16, pp. 7-1 1, 1985.
[6] Bryan, G.W. & Langston, W.J., Bioavailability, accumulation and effects of heavy
metal in sediments with special reference to United Kingdom estuaries: a review.
Environmental Pollution, 76, pp. 89-13 1, 1992.
[7] Chapman, P.M., Swartz, R.C., Roddie, B., Phelps, H.L.,
van den Hurk, P. & Butler, R.,
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
An international comparison of sediment toxicity tests in the North Sea. Marine
Ecology-Progress Series, 91, pp. 253-264, 1992.
[8] Rainbow, P.S., Biomonitoring of heavy metal availability in the marine environment.
Marine Pollution Bulletin, 31, pp. 83-192, 1995.
[9] Chapman, P.M., Thomton,I., Persoone, G., Janssen, C., Godtfredsen, K.& N.
Z'Graggen, M,, International harmonization related to persistence and
bioavailability. Human Ecology Risk Assessment, 2, pp. 393-404, 1996.
[l01 Ross, P. & Delorenzo, M.D., Sediment contamination problems in the Caribbean
Islands: Research and regulations. Environmental ~ o x i c i l o g yand Chemistry, 16, pp.
52-58, 1997.
[l l] Chapman, P.M., Wang, F., Janssen, C., Persoone, G. & Allen, H.E., Ecotoxicology of
metals in aquatic sediments: binding and release, bioavailability, risk assessment
and remediation. Canadian Journal of Fisheries and Aquatic Sciences, 55, pp.
2221-2243, 1998.
[l21 Hargis, W.J.Jr., Roberts, M.H.Jr. & Zwemer, D.E., Effects of contaminated
sediments and sediment-exposed effluent water on an estuarine fish: acute toxicity.
Marine Environmental Research, 14, pp. 337-354, 1984.
[l31 Kemble, N.E., Brumbaugh, W.G., Brunson, E.L., Dwyer, E.J., Ingersoll, C.G.,
Monda, D.P. & Woodward, D.F., Toxicity of metal-contaminated sediments from
the upper Clark Fork River, Montana, to aquatic invertebrates and fish in laboratory
exposure. Environmental Toxicology and Chemistry, 13, pp. 1985-1997, 1994.
[l41 Kwan, K.K. & Dutka, B.J., Comparative assessment of two solid-phase toxicity
bioassays: The direct sediment toxicity testing procedure (DSTTP) and the
MicrotoxB soild-phase test (SPT). Bulletin of Environmental. Contamination and
Toxicology, 55, pp. 338-346, 1995.
[l51 Soimasuo, R.. Jokinen, I., Kukkonen, J., Petanen, T., Ristola, T. & Oikari, A.,
Biomarker responses along a pollution gradient: Effects of pulp and paper mill
effluents on caged whitefish. Aquatic Toxicology, 31, pp. 329-345, 1995.
[l61 Wall, S.B., Isely, J.J. & La Point, T.W., Fish bioturbation of cadmium-contaminated
sediments: factors affecting Cd availability to Daphnia magna. Environmental
Toxicology and Chemistry, 15, pp. 294-298, 1996.
[l71 Kong, I.-C., Lee, C.-W., & Kwon,Y.-T., Heavy metal toxicity monitoring in
sediments of Jinhae Bay, Korea. Bulletin of Environmental Contamination and
Toxicology, 61, 505-51 1, 1998.
[l 81 Langston, W.J., Burt, G.R., & Pope, N.D., Bioavailability of metals in sediments of
the Dogger Bank (Central North Sea): A mesocosm study. Estuarine and Coastal
ShelfSciences, 48, pp. 5 19-540, 1999.
[l91 Ozoh, P.T.E., The effect of temperature and salinity on copper body-burden and
copper toxicity of Hediste (Nereis) diversicolor. Environmental Monitoring and
Assessment, 21, pp. 11-17, 1992.
[20] Oost, van der R., van Schooten, F.-J., Ariese, F., Heida, H., Satumalay, K &
Vermerulen, N.P.E. Bioaccumulation, biotransformation and DNA binding of
PAHs in feral eel (Anguilla anguilla) exposed to polluted sediments: a field study.
Environmental Toxicology and Chemistry, 13, pp. 859-870, 1994.
[21] Ramos, L., Gonzalez, M.L. & Hernandez, L.M., Sequential extraction of copper,
lead, cadmium and zinc in sediments from the Ebro River (Spain): Relationship
with levels detected in earthworms. Bulletin Environmental Contamination and
Toxicology, 6 2 , pp. 301-308, 1999.
[22] Dixon, D.G. & Sprague, J.B., Copper bioaccumulation and hepatoprotein synthesis
during acclimation to copper by juvenile rainbow trout. Aquatic Toxicology, 1, pp.
69-81, 1981.
Transactions on Ecology and the Environment vol 49, © 2001 WIT Press, www.witpress.com, ISSN 1743-3541
[23] Ingersoll, C.G., Brumbaugh, W.G., Dwyer, F.J. & Kemble, N.E., Bioaccumulation of
metals by Hyalella azteca exposed to contaminated sediments from the upper Clark
Fork River, Montana. Environmental Toxicology and Chemistry, 13, pp. 2013-2020,
1994.
[24] Barron, M.G., Bioaccumulation and concentration in aquatic organisms. Handbook
ofEcotoxicology, eds. D.J. Hoffman, B.A. Rattner, G.A. Burton, Jr., & J. Cairns, Jr.,
Lewis Publishers: Boca Raton, pp. 652-666, 1995.
[25] Chen, M.-H., Wen, D.-J. & Chen, C.-Y., Reproduction and estuarine utilization of
the grey mullet, Liza macrolepis (Smith, 1846), in the area of Kaohsiung Harbour,
southem Taiwan. Fisheries Science, 65, pp. 1-10, 1999.
[26] Chen, M.-H. & Chen, C-Y., Bioaccumulation of sediment-bound heavy metal in
grey mullet, Liza macrolepis. Marine Pollution Bulletin, 39, 238-243, 1999.
[27] Chen, M.-H, Baseline metal concentrations in the sediment and fishes, and the
determination of bioindicators: the subtropical Chi-ku Lagoon, S. W. Taiwan.
Marine Pollution Bulletin (submitted), 2001.
[28] Chen, M.-H. & Wu, H.-T., Copper, cadmium and lead in sediments from the
Kaohsiung River and its harbour area, Taiwan. Marine Pollution. Bulletin, 30, pp.
879-884, 1995.
[29] Sprague, J.B., Measurement of pollutant toxicity of fish. I. Bioassay methods for
acute toxicity. Water Research, 3, pp.793-821,1969.
[30] Smith, S., Chen, M.H., Bailey, R.G. & Williams, W.P., Concentration and
distributions of copper and cadmium in water, sediments, detritus, plants and
animals in a hardwater lowland river. Hydrobiologica, 341, 71-80, 1996.
[31] Chen, M.-H. & Wu, H.-T., Concentration of copper in sediments and fishes from
Kaohsiung River and its harbour area, Taiwan. Contaminated Soils: 3rd
International Conference on the Biogeochemistry of Trace Element, ed. Prost R.,
INRA Editions: Versailles, 075 PDF (in CD ROM), 1997.
[32].Chen, M.-H. & Chou, C.L. An instrumental correction for the determination of
mercury in biological and sediment samples using cold vapor atomic absorption
spectrophotometry. Journal of Chinese Chemistry Society, 47(5), pp. 1145-1 153,
2000.
[33] National Oceanic and Atmospheric Administration (NOAA), The potential for the
biological effects of sediment-sorbed contaminants tested in the National Status and
Trends Program. NOAA Technical Memorandum NOS OMA 52. 2ndprinting. US
Department of Commerce: Seattle, 175 pp., 199 1.
[34] Brusle, J., Food and feeding in grey mullet. Aquaculture of Grey Mullet, ed. 0 . H.
Oren, Cambridge Univ. Press: Cambridge, pp. 185-2 17, l98 1.
[35] Giordana, R., Musmeci, L., Ciaralli, L., Vemillo, I., Chir~co,M., Piccioni, A. &
Costantini, S., Total contents and sequential extractions of mercury, cadmium and
lead in coastal sediments. Marine Pollution Bulletin, 24(7), pp. 350-357, 1992.
[36] Giani, M,, Gabellini, M., Pellegrini, D., Costantini, S., Beccaloni, E. & Giordano, R.,
Concentration and partitioning of Hg, Cr and Pb in the sediments of dredge and
disposal sites of the northern Adriatic Sea. The Science of the Total Environment,
158, pp. 97-1 12, 1994.
[37] Watanabe, T., Kiron, V. & Satoh, S., Trace minerals in fish nutrition. Aquaculture,
151, pp. 185-207, 1997.
[38] Mariani, A., Panella, S., Monaco, G. & Cataudella, S . , Size analysis of inorganic
particles in the alimentary tracts of Mediterranean mullet species suitable for
aquaculture. Aquaculture, 6 2 , pp. 123-129, 1987.