- Email: [email protected]
Long-term study of mercury concentrations in fish following cessation of a mercury-containing discharge
Marine
0141-I
Environmenrol
136(95)00028-3
Research, Vol. 43, No. l/2, pp. 2740, 1997 Copyright 0 1996 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0141-1136/97/515.00+0.00
LLSEVIER
Long-Term Study of Mercury Concentrations in Fish Following Cessation of a Mercury-Containing Discharge Kevin A. Francesconi,a* Rodney C. J. Lenantoqa & Stewart Jonesb
Nicolavito Caputi”
“Western Australian Marine Research Laboratories, P.O. Box 20, North Beach 6020, Australia hThe Chemistry Centre of Western Australia, 125 Hay Street, East Perth 6004, Australia (Received 6 December 1994; revised version received 20 November 199.5;accepted 30 November 1995)
ABSTRACT Mercury-contaminated industrial efluent was discharged over a 30-year period into Princess Royal Harbour, a marine embayment on the south coast of Western Australia. The discharge of efluent was stopped in 1984 and most fish taken from the harbour at that time contained concentrations of Hg in their muscle tissue which exceeded the maximum permitted concentration (0.5 mg kg-‘) set by Australian health authorities. To allay human health concerns, the contaminatedportion of the harbour was closed to all forms of commercial and recreational fishing in 1984. The course of Hg contamination following cessation of the efluent discharge was monitored by determining Hg concentrations in the muscle tissue of eight teleost fish species, namely cobbler (Cnidoglanis macrocephalus) , rock Jlathead (Platycephalus laevigatus), striped trumpeter (Pelates sexlineatus), King George whiting (Sillaginodes punctata), Australian herring (Arripis georgianus), brown-spotted wrasse (Pseudolabrus parilus), spiny-tailed leatherjacket (Bigener brownii) and six-spined leatherjacket (Meuschenia freycineti), sampled near the efluent outfall on 14 occasions from 1984 to 1993. Mercury concentration showed a signiJicant positive relationship with length of fish for jive of the species and a sign$cant negative relationship with length for two species. Four species showed signljicant differences in Hg concentration depending on season (summer vs winter); summer concentrations were generally higher than those in winter, The Hg concentrations decreased with time and were about 50% of their initial values by 1993. In general, jish Hg levels had decreased to below the maximum permitted concentration by 1991 and the closed portion of the harbour was reopened in 1992. For most species, however, the rate of reduction in Hg concentration was less in the latter part of the study. The data suggest that future reductions in Hg concentrations in fish may be less than those achieved in the$rst 10 years, and that for some species Hg concentrations could remain elevated for many years. Copyright 0 1996 Elsevier Science Ltd *Present address: Institute of Biology, University of Odense, DK-5230 Odense M, Denmark. 27
28
K. A. Francesconi et al.
INTRODUCTION In 1983, high concentrations of Hg were recorded in fish and other biota collected from Princess Royal Harbour on the south coast of Western Australia (Fig. 1). The source of Hg contamination was subsequently identified as effluent from a superphosphate processing plant located on the western shore of the harbour (Jackson et al., 1986). The crude rock phosphate contained about 0.5 mg Hg kg-‘, and during the manufacture of superphosphate fertilizer, some of this Hg was released into the scrubber fluids and discharged into the harbour at a rate of about 14 kg Hg yy’ (Jackson et al., 1986). Contaminated sediments were confined to a relatively small area adjacent to the effluent outfall in the western region (Fig. 1). Mercury contamination of sedentary organisms was also restricted to those from near the outfall site (Francesconi & Lenanton, 1992). Fish sampled from throughout the harbour contained elevated concentrations of Hg but the highest values were found for fish from near the outfall (Francesconi & Lenanton, 1992). Most species of fish in this western region contained Hg in excess of the maximum permitted concentration (MPC) of 0.5 mg kg-’ wet wt set by Australian health authorities (Anon, 1993) whereas most fish from the eastern region contained less than 0.5 mg Hg kg-‘. Because of human health concerns, the discharge of Hg-containing effluent was stopped in 1984, and the contaminated part of the harbour was closed to all forms of fishing. Various restorative and ameliorative measures were considered in order to alleviate the problems caused by Hg contamination (Francesconi & Lenanton, 1992). Generally, these measures were either prohibitively expensive or impracticable for Princess Royal Harbour. Previous studies have shown natural reductions in the concentrations of Hg in fish from contaminated areas following cessation of the source of Hg contamination (Olsson, 1976; Armstrong & Scott, 1979; Langlois et al., 1987; Essink, 1988). This passive approach was adopted for Princess Royal Harbour. We report the results from a lo-year programme, carried out from 1984 to 1993, to monitor the natural declines in the Hg concentrations of eight teleost fish species from this Hg-contaminated marine embayment.
MATERIALS
AND METHODS
Princess Royal Harbour, a marine embayment on the south coast of Western Australia (35” 03’ S, 117” 53’ E; see Fig. l), contains the port facility for the town of Albany, and has several industries on its shores. The harbour has a total area of 29 km2, and consists of a deep basin bordered by shallow sand-flats which are most extensive off the western and southern shores (Anon, 1990). Mean winter and summer water temperatures are 14°C and 20°C respectively (Anon, 1990). The superphosphate plant is located near the western shore and had, over a 30-year period up to 1983, discharged effluent containing low concentrations of Hg via a pipeline with the outfall about 1 km offshore (Fig. 1). Sampling procedures
Earlier work (Francesconi & Lenanton, 1992) on Hg in fish from various regions of the harbour showed that concentrations were highest in fish collected from the western region adjacent to the effluent outfall. In the present study, eight species of fish were routinely sampled from this site, designated the outfall site (Fig. 1). The species chosen (see Table 1)
29
Long-term study of Hg concentrations inJish
PRINCESS
ROYAL
Fig. 1. Princess Royal Harbour showing the effluent outfall X, and fish sampling sites a. The numbers 1-6 represent the six sites sampled for Katelysia scalarina. The area west of the dotted line was closed to all forms of fishing from 1984 to 1992.
Common
Names,
TABLE 1 Scientific Names, Sample Sizes and Lengths and Diets of Fishes Monitoring Study of Princess Royal Harbour, 1984-l 993
used in Hg
Common name
Scientific name Sample size
Total length (mm) Range
Major components of‘diet”
Cobbler
Cnidoglanis macrocephalus Platycephalus laevigatus Pelates sexlineatus Sillaginodes punctata Arripis georgianus Pseudolabrus park Bigener brownii
760
150-625
61
225-515
408
Crustaceans, polychaetes Fish
508
121--285
211
No diet data available
433
154495
272
807
1388327
227
78
133-370
274
298
106371
282
Polychaetes, small crustaceans Fish, crustaceans, polychaetes Molluscs, crustaceans, fish Plants
271
163-374
293
Rock flathead Striped trumpeter King George whiting Australian herring Brown-spotted wrasse Spiny-tailed leatherjacket Six-spined leatherjacket %See Francesconi
Meuschenia freycineti & Lenanton
(1992).
molluscs,
Plants, echinoderms, sponges, large crustaceans
30
K. A. Francesconi
et al.
encompassed a range of diets, and hence Hg concentrations (Francesconi & Lenanton, 1992) and included the most important commercial and recreational species. A winter sample was taken (usually in August) annually from 1984 to 1991 and in 1993, and a summer sample (February) was taken from 1985 to 1987. The eastern region was sampled in March of 1984 and 1986, and in August of 1988 and 1989. The fish were collected with a composite gill net comprising stretched mesh sizes from 1 to 10 cm. We endeavoured to obtain at least 30 individuals of each species on each sampling occasion, but this was not always possible. Sampling was generally carried out over a 3-4 day period. Fish were individually measured and weighed, and stored frozen in polyethylene bags. Within two months of capture, fish were thawed and samples of muscle tissue from just behind the pectoral fin were analysed for Hg. Bivalve molluscs Kuteiysia scalarina (Family Veneridae) were collected in September 1990 from six sites adjacent to and including the outfall site (Fig. 1). These sites corresponded with those sampled for K. scalarina in 1984 (Jackson rt al., 1986). A composite sample comprising whole, drained, wet tissue from 10 individuals (dorsoventral length 3640 mm) from each site was analysed for total Hg. Mercury analyses
Samples were analysed for total Hg using a modification of the technique described in Collett et al. (1981). Samples of 2-3 g were weighed into 200 ml Kjeldahl flasks and digested in a mixture of nitric and sulfuric acids and ammonium metavanadate in a hot air bath. The samples were cooled and diluted to 130 ml. Prior to 1987, the Hg in the diluted samples was determined using a Perkin-Elmer Coleman 50 Mercury Analyser System after reaction of a 50 ml aliquot with a stannous chloride solution. After 1987, Hg was determined using a Varian SpectrAA 20 atomic absorption spectrophotometer with a VGA-76 continuous vapour generation accessory after reaction with hydrochloric acid and sodium borohydride solutions. All Hg concentrations are reported on a wet weight basis. Quality assurance/quality control over the sampling period (19841993) was ensured by conducting repeat analyses on at least 5% of the samples, and primary standards (pre1987) or reference materials (post-1987) were included at the rate of at least two in each batch of 20 samples. The primary standard of 200 ng Hg gave a standard deviation of 5.2% (n = 100). The reference materials used were the Canadian National Research Council’s TORT-l and DORM-l, and an in-house standard material of dried lish muscle tissue. TORT-l (certified value 0.33 f 0.06 mg kg-‘) returned a mean value of 0.34 f 0.03 mg kg-‘, n = 15, DORM-l (certified value 0.798 f 0.074 mg kg-‘) returned a mean value of 0.82 f 0.06 mg kg-‘, n = 16, and the in-house dried fish standard (FISH-l, mean 3.5 mg kg-‘) gave a sample standard deviation of 8.6% (n = 132). During the period of this study the laboratory participated in five interlaboratory surveys on metals in foods obtaining satisfactory results on all occasions. Statistical
analyses
For each of the fish species, an analysis of covariance (ANCOVA) was undertaken on the log-transformed Hg concentrations with the log of fish length as the covariate, and year of sampling and seasons (summer and winter) as factors. The variation in Hg concentrations
Long-rerm
study
of Hg
concentrations
in fish
31
from samples caught on different days during the one sampling period was examined using the ANCOVA with the sampling days nested within the sample period. Geometric mean Hg concentrations, adjusted for variations in fish length between samples and for seasonal differences, were examined for trends over the IO-year period. Mercury concentration differences between the eastern region and the outfall site were also examined. The effect of age (or an index of age such as length) must be considered when comparing Hg data for a particular species from sample to sample. This effect can be compensated for by determining the slope in the log-transformed relationship between fish length and Hg concentration over all sample periods, and comparing the mean Hg concentrations for each sample at the overall group mean length. In the present study, comparison of Hg data between years is based on the geometric mean Hg concentration (calculated from back-transformed log data) at the overall group mean length for each species. This approach assumes a common slope between the log-transformed Hg and length relationships over the sample periods. The annual geometric mean Hg concentrations were then used to examine the annual rate of decline of the Hg concentration using the following relationship: Hg = (I exp( -h YEAR)
(1)
where u and h are parameters obtained from fitting this model using a logarithmic transformation. An estimate of the annual rate of decline of Hg is provided by exp( -6). For some species a more appropriate description of the annual rate of decline of mean Hg concentration would bc: Hg = a exp( --h YEAR) + (’ where the long-term decline in the mean Hg concentration is to a concentration calculated ‘baseline’ level) rather than zero which is implicit in eqn (I).
RESULTS
(2) c (a
AND DISCUSSION
Mercury concentrations in cockles
Mercury concentrations in samples of K. scalarina collected in 1990 from six sites in the western region ranged from 0. I3 to 0.31 mg kg-’ with a mean of 0.23 mg kg- ‘. These values were much lower than those recorded for K. scalarina taken from the same sites in 1984 when the range was 0.4 9.2 mg kg-’ with a mean of 3.8 mg kg -’ (Jackson e[ al., 1986). Derivation of valid fish Hg concentrations for comparison
Depending on the mobility of a particular fish species, there may be variations in Hg concentrations among different schools caught over the 3- 4 day sampling period. This could result in differences in mean Hg concentrations on a daily basis, and the data would be less reliable for use in long-term monitoring. ANCOVA (see Table 2) showed that, for five of the eight species, there were no significant differences in Hg concentrations between days in a single sample period @ > 0.05). Striped trumpeter, Australian herring and sixspined leatherjacket showed significant differences but these were mainly due to daily variations in one sample period only (August 1986 for striped trumpeter, August 1988 for
807
Australian
leatherjacket
271
298
* *
***
NS
***
***
NS
NS
***
NS
*** p < 0.001; NS, not significant.
leatherjacket
wrasse
* p < 0.05; **p<0.01;
Six-spined
Spiny-tailed
Brown-spotted
78
***
433
King George whiting
herring
***
508
Striped trumpeter
***
***
***
***
61
760
Cobbler
Seuson
(ANCOVA)
Year
Rock flathead
N
Species
Results from Analysis of Covariance
(-0.77) *** (2.26) *** (0.37) *** (0.82) *** (7.36) *** (1.17) * (-0.32) NS
***
Log(length) (Slope)
Main eflects
0.230
0.127
0.082
0.794
0.200
0.147
0.192
0.136
RMS
TABLE 2 on Log-transformed
***
0.28
0.57
0.39
NS
NS
NS
**
0.26
0.69
NS
NS
NS
Log(lmgth) x Year
0.15
0.56
0.40
R’
Hg Concentrations
= residual
NS
NS
*
**
NS
NS
NS
NS
x Seu.son
Log(length)
Inteructions
(RMS
NS
NS
NS
NS
NS
NS
NS
**
Year x Season
Day
***
NS
NS
*
NS
**
NS
NS
YYMMDD i Y Y x Season)
mean square)
2
2
2 -.
2 4
s
21
i.L
x
Long-term study of Hg concentrations in fish
33
Australian herring, and September 1990 for six-spined leatherjacket). Consequently, Hg data from catches taken over the 334 days of a sample period were combined with the knowledge that, in general, they accurately represented the Hg status of a species at that time. For five of the eight species, Hg concentrations showed a significant positive relationship with length @ < 0.001). Six-spined leatherjacket showed no relationship between Hg concentration and length @ > 0.1) and two species, cobbler and spinytailed leatherjacket, had a significant negative relationship between Hg concentration and length (p < 0.001 and p < 0.05, respectively). This negative relationship possibly reflects differences in mobility between age classes of cobbler (Francesconi & Lenanton, 1992). Small cobbler are more localised in their movements than are larger cobbler (Lenanton & Caputi, 1989) and, at the time of capture, are likely to have spent a greater proportion of their life in the area of contamination. Of the eight species, only King George whiting and Australian herring showed significant differences in the slope of the Hg/length relationship between years (see Fig. 2 for examples). For both whiting and herring, however, the additional sum of squares associated with the interaction was much less than the mean square assuming a common slope. Thus, as an initial approximation, a common slope was also assumed for these two species for the purpose of correcting the Hg values for differences in size. There were significant differences in the Hg concentrations depending on season for four species - cobbler, striped trumpeter and the two leatherjacket species (Table 3). Mean Hg concentrations for summer samples were generally higher than those for winter samples. However, the strong correlations between Hg concentrations in fish and water temperature reported by Bodaly et al. (1993) in their work on Canadian lakes were not evident in the Princess Royal Harbour study. Comparison of Hg concentrations
in fish: outfall site vs eastern region
Seven of the eight species examined in this study yielded sufficient samples in the eastern region to enable comparison with the outfall site to be made (Table 4). For all seven species, Hg concentrations in fish from the outfall site were significantly higher (by a factor of two to three) than those in fish from the eastern region. Annual comparisons of Hg concentrations
in fish from the outfall site
Mercury concentrations in the eight fish species sampled from the outfall site from 1984 to 1993 are shown in Fig. 3. Mercury concentrations in cobbler decreased markedly from 1984 to 1993 with an estimated average rate of decline of 8% per annum using eqn (1). These decreases, however, were most apparent in the first four years; since 1988 there has been no clear continuing trend to lower concentrations. These data were also fitted to eqn (2) resulting in an estimate of paramater c of 0.5 mg kg-’ which indicates that the long-term decline is not to zero. Equation (2) provided a significantly better fit to the data than eqn (1). Flatheads are non-migratory and at the top of the food chain in the harbour, their diet consisting almost entirely of fish which are high in Hg (Francesconi & Lenanton, 1992). Consequently, rock flathead contained very high concentrations of Hg (about 6 mg kg-‘) at the beginning of this study. The concentrations have significantly decreased with time
34
K. A. Francesconi et al.
2.0
1986
1.0 1
5
1993
O-O. *
4
-1.0.
3
-2.0.
**
-3.0. -4.0 *
*
I -5.O{
5.6
5.5
5.4
5.3
Log
Length
1.0' 0.5. * 0.0. -0.5. -1.0. -1.5.
.,
. 5.4
.
.
.
. 5.6
.
.
.
. 5.6
6.0
6.2
6.4
Log Length Hg-length relationships for two species of fish from Princess Royal Harbour: Fig. 2. Log-transformed (a) Australian herring, showing positive Hg-length relationship and significant difference in slope between years; (b) cobbler, showing a negative Hg-length relationship and no significant difference in slope between years. To enhance clarity, data from two years only are shown.
35
Long-term study of Fig concentrations in fish
TABLE3 Geometric Mean Hg Concentrations Species
-
of Fish -
Summer/Winter
Samples, 1985-l 987, outfall site Season differences
Mercury concentration (mg kg -I) Winter Summer ~ _____~_
Cobbler Rock tlathead Striped trumpeter King George whiting Australian herring Brown-spotted wrasse Spiny-tailed leatherjacket Six-spined leatherjacket ~_.~ -.._
0.66 2.8 0.79 0.47 0.53 2.9 0.08 0.58
***
0.57 3.1 0.65 0.46 0.58 2.4 0.09 0.46
NS *** NS NS NS * * -__
* p < 0.05; *** p < 0.001; NS, not significant.
TABLE4 Geometric Mean Hg Concentrations Species
Cobbler Rock flathead Striped trumpeter King George whiting Australian herring Spiny-tailed leatherjacket Six-spined leatherjacket
of Fish -- Eastern Site vs Outfall Site
Mercury concentration (mg kg- ‘j” Eastern site Outfall site 0.24 1.3 0.29 0.19 0.21 0.03 0.14
Site differences ~_ *** * *** *** *** *+* ***
0.59 2.7 0.72 0.46 0.55 0.09 0.51 _.~_.
“Data represent the mean Hg concentrations for the years when comparisons namely 1984, 1986, 1988 and/or 1989. * p <0.05; *** p
_.~
could be made,
rate of decline 11% per annum, p < 0.05), with a possible levelling-off over recent years. Although striped trumpeter are not commercially fished in Princess Royal Harbour (they,are not generally eaten) they were particularly suitable for Hg monitoring because of their resident status and abundance. The concentrations of Hg showed a slow reduction over time (3% per annum 0.05
K. A. Francesconi
36
et al.
1.0 -
Cobbler
0.6 0.6 -
* *
0.4 -
*
0.2 0.0 r
,
I
6.0
!._:\:_:
* E
1.0:
3
0.0;
,
0.6.
+;
2 a 3
I
*
Striped trumpeter *
*
*0.6 -
*
*
*
5 0.4.
0.6 .
King Georgewhiting
0.6 -
* *
0.4 *
*
*
0.2 -
o.o*
, 1864
1666
I lsa6
1667
1666
ls69
1680
1881
lea2
1983
Fig. 3. Geometric mean Hg concentrations (mg kg-’ wet weight) in fish sampled from the outfall site, Princess Royal Harbour, 1984 to 1993. * Represents actual data; lines have been drawn using eqn (1) or (2) as described in the text.
Brown-spotted wrasse in Princess Royal Harbour have high Hg concentrations (about 4 mg kg-‘) because of their sedentary nature and carnivorous diet (Francesconi & Lenanton, 1992). The rate of decline of the Hg concentration was estimated at 11% per annum using eqn (1) with most of the decrease occurring in the first four years. Brown-spotted wrasse were similar to cobbler in that they showed an improved fit using eqn (2), the parameter estimate for c (the calculated ‘baseline’ level), being 1.6 mg kg-‘. The spiny-tailed leatherjacket is a good indicator species because it spends its entire life cycle in Princess Royal Harbour (B. Hutchins, pers. commun.). This species is a strict herbivore feeding exclusively on algae and seagrasses (Francesconi & Lenanton, 1992).
Long-term study of Hg concentrations infish 1.47 *
12.
Austrdim
herring
1.0. *
* *
0.4 .
*
*
02. 0.0 r
,
0.14, 0.12*
spiny-tailedleatheriadtet
0.10 *
*
mm.
* *
0.06.
*
*
0.04. 0.02. o.oo-
‘ ,gt)rl
1885
IaM
1967
Isa5
lo82
lem
IQol
1892
we3
Y0W Fig. 3.
Contd.
These plants contained only low levels of organic Hg (Francesconi & Lenanton, 1992), and consequently spiny-tailed leatherjacket contained only low concentrations of Hg (about 0.2 mg kg-‘) at the beginning of the monitoring programme. Nevertheless, the Hg concentrations in spiny-tailed leatherjacket decreased a further 50% during the first five years of the study before levelling-off. This trend was also followed by the six-spined leatherjacket, although it initially contained higher Hg concentrations (about 1 mg kg-‘) because of its omnivorous diet (Francesconi & Lenanton, 1992). In general, the fish species monitored in this study showed a uniform trend - Hg concentrations decreased over the first four years before levelling off. The Hg value at which this occurred (the ‘baseline’ level, constant c from eqn (2)) varied considerably between species. For cobbler, King George whiting, Australian herring and the two leatherjacket
38
K. A. Francesconi et al.
species, this value was < 0.5 mg Hg kg-‘, but it was higher for rock flathead (1.7 mg kg-‘) and brown-spotted wrasse (1.6 mg kg-‘). Neither flathead nor wrasse, however, constitute a significant proportion of the total fish catch from Princess Royal Harbour. By 1992, health authorities considered that the Hg levels in fish had reduced to the point where there was negligible human health risk associated with eating fish from the outfall site, and the restriction on fishing in the western region of the harbour was lifted. Hypothesis
for the observed decreases in fish Hg concentrations
Despite the fact that there has been no input of Hg to Princess Royal Harbour for IO years, the Hg levels in fish have levelled off at values much higher than those for fish of the same species from nearby uncontaminated embayments where levels ranged from 0.02 to 0.06 mg kg-’ (Jackson et al., 1986). This effect may be explained by the fate of Hg in water and sediments of contaminated aquatic systems. Jerneliiv and Asell (1975) in their model of the fate of Hg in an aquatic system following cessation of Hg-contaminated effluents predicted that Hg concentrations would decrease quickly in the water column but only slowly in the surface sediments. Results from Princess Royal Harbour are in accord with this view; a survey of the harbour undertaken in 1989 revealed that the water contained very low concentrations of Hg whereas the Hg concentrations in the sediments had not decreased significantly since 1984 (Anon, 1990). Previous work has shown that diet is the major source of Hg for fish in Princess Royal Harbour (Francesconi & Lenanton, 1992). Mercury concentrations in the prey items of fish will depend on the concentrations of Hg in the water and sediments, and the relative contribution of each of these components to body burden. For example, Hg concentrations in suspension-feeding bivalves would be largely influenced by water Hg levels, and those in detrital-feeding organisms would be more influenced by sediments. In Princess Royal Harbour, lower water Hg concentrations were reflected by large decreases in Hg concentrations in the suspension-feeding bivalve K. scalurina ~- in 1990 their Hg levels were only 6% of the 1984 values. Although there are no long-term data on Hg in detritalfeeders from Princess Royal Harbour, the Hg levels are likely to parallel those in the sediments and be little changed from their 1984 values. Consequently, the Hg concentrations of the overall diets of the fish (and hence of the fish themselves) from the harbour may be expected to decrease in two phases. First, a decrease reflecting rapid decline of Hg levels in suspension-feeding bivalves and other organisms which accumulate Hg primarily from the water; and second a more gradual decrease/levelling off reflecting slow decline of Hg levels in detrital-feeding organisms which accumulate Hg primarily from the sediments. The decreases in Hg levels in fish shown in this monitoring study are consistent with such an hypothesis. Moreover, the data indicate that the proposed second phase of Hg reduction has been reached, and further decreases in fish Hg concentrations will be gradual. Comparison of Princess Royal Ha&our with other Hg-contaminated
regions
It is of interest to compare the course of contamination in Princess Royal Harbour with that reported for other Hg-contaminated aquatic systems. Lake Marmen in Sweden received ‘Hg from paper-mill wastes until 1967, and Hg concentrations were determined in pike (ESOX Lucius) sampled from the lake in 1968 and 1972 (Olsson, 1976). The concentrations decreased in this time; from the data presented by Olsson (1976) we
Long-term study of Hg concentrationsin&h
39
estimate the Hg concentration at the overall group mean length to have decreased from 2.2 to 1.8 mg kg-’ wet wt. The Wabigoon-English-Winnipeg River system of Ontario, Canada received about 10,000 kg of Hg from a chlor-alkali plant from 1962 to 1970. The discharge was restricted to about 3% of that level from 1970 to 1975, and then stopped altogether. The concentrations of Hg in three species of fish from Ball Lake, part of the river system, were determined in 1971, 1972 and 1976 (Armstrong & Scott, 1979). All three species showed marked decreases in their Hg concentrations between 1972 and 1976: walleye (Stizostedion vitreum vitreum) from 2.71 to 1.39 mg kg-‘, pike (E. lucks) from 5.72 to 1.80 mg kg-‘, and whitefish (Coregonus clupeuformis) from 0.62 to 0.42 mg kg-’ (Armstrong & Scott, 1979). The sand flathead (Pkztycephalus bussensis) was used as an indicator of Hg contamination in the Derwent Estuary in Tasmania which received Hg-containing wastes from a zinc refinery for several years until 1975 (Ratkowsky et al., 1975; Langlois et al., 1987). P. bassensis was sampled (in 1973/74, and then yearly from 1976/77 to 1982/83) from four sites with different levels of Hg contamination, Interestingly, fish from all four sites showed the same absolute reduction in Hg concentration (~0.3 mg kg-‘) over the IO-year period. In contrast to the trend found in Princess Royal Harbour, the rate of decline remained constant and a plateau of concentrations had not been reached even after 10 years. Discharge of Hg into the Dutch Wadden Sea and Ems Estuary in The Netherlands decreased considerably between 197 1 and 1987. The fish Zoarces viviparus sampled from this area has accordingly shown a steady decrease in its Hg concentrations; in 1987 the Hg concentration was about half that in 1981 (Essink, 1988). Inspection of the slopes for the relationship between Hg concentration and length for the various years suggests that the rate of decrease is declining (Essink, 1988). Liverpool Bay in the United Kingdom has a history of Hg contamination from several sources including sewage sludge and industrial discharges. Mean concentration of Hg in plaice Pleuronectes platessa declined from 0.5 mg kg-’ in the early 1970s to about 0.2 mg kg-’ in 1991, and this reduction was thought to reflect a decline in the input of Hg to Liverpool Bay since 1976 (Leah et al., 1993). There had been, however, no significant decrease in Hg concentrations over the last six years of that study, and the 0.2 mg kg-’ level probably represents an equilibrium position. There is still some input of Hg into Liverpool Bay, and Hg levels in plaice from the Bay remained higher than those in plaice from uncontaminated sites (0.1&O. 15 mg Hg kg-‘). Princess Royal Harbour differs from Liverpool Bay in that there is no continuing input of Hg, but Hg concentrations in the fish remain well above those for fish from uncontaminated sites (Jackson et al., 1986). In contrast to the above, Princess Royal Harbour has not received large quantities of Hg. The total amount of Hg discharged after 30 years of fertilizer manufacture can be estimated at about 400 kg (Jackson et al., 1986). Consequently, the harbour sediments were only moderately contaminated with a maximum value of 1.7 mg Hg kg-i. Mercury levels in the fish, however, were much higher than those for fish from grossly contaminated sites (e.g. Liverpool Bay). It is evident that Hg contamination in fish and its rate of decline depend on factors in addition to the amount discharged to an aquatic system. Influencing factors are likely to include the rate of flushing, type and complexity of food webs, fish mobility and degree of Hg methylation due to sediment type and water chemistry. In Princess Royal Harbour, previous work suggested that food webs and the restricted movement of fish in the harbour contributed to the unusually high Hg levels in fish (Francesconi & Lenanton, 1992). The
40
K. A. Francesconi
et al.
studies in Princess Royal Harbour highlight the need to recognise and understand environmental and ecological factors when predicting possible consequences of discharging a contaminant into an aquatic system. ACKNOWLEDGEMENTS The authors thank Mark Cliff, Jenny Moore, Jenny Shaw and Karen Parker for technical assistance, and our research colleagues at the Western Australian Marine Research Laboratories for constructive comment. REFERENCES Anon, (1990). Albany harbours environmental study (198881989). Environmental Protection Authority, Perth, Western Australia, Bulletin 412, 84 pp. Anon, (1993). Australian Food Standards Code. National Food Authority, Australian Government Publishing Service, Canberra, pp. Al2 l-5. Armstrong, F. A. J. & Scott, D. P. (1979). Decrease in mercury content of fishes in Ball Lake, Ontario, since imposition of controls on mercury discharges. J. Fish. Res. Board Can., 36, 670-672. Bodaly, R. A., Rudd, J. W. M., Fudge, R. J. P. & Kelly, C. A. (1993). Mercury concentrations in fish related to size of remote Canadian shield lakes. Can. J. Fish. Aquat. Sci., 50, 98@-987.
Collett, D. L., Taylor, G. A. & Chegwidden, A. (1981). Alkylmercury levels in marine sediments in Cockburn Sound, WA. Bull. Environm. Contam. Toxicol., 26,7577763. Essink, K. (1988). Decreasing mercury pollution in the Dutch Wadden Sea and Ems Estuary. Mar. Pollut. Bull., 19, 317-3 19. Francesconi, K. A. & Lenanton, R. C. J. (1992). Mercury contamination in a semienclosed marine embayment: organic and inorganic mercury content of biota, and factors influencing mercury levels in fish. Mar. Environ. Res., 33, 189-212. Jackson, M., Hancock, D., Schulz, R., Talbot, V. & Williams, D. (1986). Rock phosphate: the source of mercury pollution in a marine ecosystem at Albany, Western Australia. &far. Environ. Res., 18, 1855202. Jernelbv, A. & Asell, B. (1975). The feasibility of restoring mercury-contaminated waters. In Heavy Metals in the Aquatic Environment, ed. P. A. Krenkel. Pergamon Press, Oxford, pp. 299-309. Langlois, D., Cooper, R. J., Clark, N. H. & Ratkowsky, D. A. (1987). The effect of a mercury containment programme at a zinc smelting plant on the mercury content of sand flathead in the Derwent Estuary. Mar. Polk. Bull., 18, 67-70. Leah, R. T., Collings, S. E., Johnson, M. S. & Evans, S. J. (1993). Mercury in plaice (Pleuronectes pfutessa) from the sludge disposal ground of Liverpool Bay. Mar. Pollut. Bull., 26,436439.
Lenanton, R. C. J. & Caputi, N. (1989). The roles of food supply and shelter in the relationship between fishes, in particular Cnidoglanis macrocephalus (Valenciennes), and detached macrophytes in the surf zone of sandy beaches. J. Exp. Mar. Biol. Ecol., 128, 165-176.
Olsson, M. (1976). Mercury level as a function of size and age in northern pike, one and five years after the mercury ban in Sweden. Ambio, 5,73376. Ratkowsky, D. A., Dix, T. G. & Wilson, K. C. (1975). Mercury in fish in the Derwent Estuary, Tasmania, and its relation to the position of the fish in the food chain. Aust. J. Mar. Freshwater Res., 26, 223-231.
0141-I
Environmenrol
136(95)00028-3
Research, Vol. 43, No. l/2, pp. 2740, 1997 Copyright 0 1996 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0141-1136/97/515.00+0.00
LLSEVIER
Long-Term Study of Mercury Concentrations in Fish Following Cessation of a Mercury-Containing Discharge Kevin A. Francesconi,a* Rodney C. J. Lenantoqa & Stewart Jonesb
Nicolavito Caputi”
“Western Australian Marine Research Laboratories, P.O. Box 20, North Beach 6020, Australia hThe Chemistry Centre of Western Australia, 125 Hay Street, East Perth 6004, Australia (Received 6 December 1994; revised version received 20 November 199.5;accepted 30 November 1995)
ABSTRACT Mercury-contaminated industrial efluent was discharged over a 30-year period into Princess Royal Harbour, a marine embayment on the south coast of Western Australia. The discharge of efluent was stopped in 1984 and most fish taken from the harbour at that time contained concentrations of Hg in their muscle tissue which exceeded the maximum permitted concentration (0.5 mg kg-‘) set by Australian health authorities. To allay human health concerns, the contaminatedportion of the harbour was closed to all forms of commercial and recreational fishing in 1984. The course of Hg contamination following cessation of the efluent discharge was monitored by determining Hg concentrations in the muscle tissue of eight teleost fish species, namely cobbler (Cnidoglanis macrocephalus) , rock Jlathead (Platycephalus laevigatus), striped trumpeter (Pelates sexlineatus), King George whiting (Sillaginodes punctata), Australian herring (Arripis georgianus), brown-spotted wrasse (Pseudolabrus parilus), spiny-tailed leatherjacket (Bigener brownii) and six-spined leatherjacket (Meuschenia freycineti), sampled near the efluent outfall on 14 occasions from 1984 to 1993. Mercury concentration showed a signiJicant positive relationship with length of fish for jive of the species and a sign$cant negative relationship with length for two species. Four species showed signljicant differences in Hg concentration depending on season (summer vs winter); summer concentrations were generally higher than those in winter, The Hg concentrations decreased with time and were about 50% of their initial values by 1993. In general, jish Hg levels had decreased to below the maximum permitted concentration by 1991 and the closed portion of the harbour was reopened in 1992. For most species, however, the rate of reduction in Hg concentration was less in the latter part of the study. The data suggest that future reductions in Hg concentrations in fish may be less than those achieved in the$rst 10 years, and that for some species Hg concentrations could remain elevated for many years. Copyright 0 1996 Elsevier Science Ltd *Present address: Institute of Biology, University of Odense, DK-5230 Odense M, Denmark. 27
28
K. A. Francesconi et al.
INTRODUCTION In 1983, high concentrations of Hg were recorded in fish and other biota collected from Princess Royal Harbour on the south coast of Western Australia (Fig. 1). The source of Hg contamination was subsequently identified as effluent from a superphosphate processing plant located on the western shore of the harbour (Jackson et al., 1986). The crude rock phosphate contained about 0.5 mg Hg kg-‘, and during the manufacture of superphosphate fertilizer, some of this Hg was released into the scrubber fluids and discharged into the harbour at a rate of about 14 kg Hg yy’ (Jackson et al., 1986). Contaminated sediments were confined to a relatively small area adjacent to the effluent outfall in the western region (Fig. 1). Mercury contamination of sedentary organisms was also restricted to those from near the outfall site (Francesconi & Lenanton, 1992). Fish sampled from throughout the harbour contained elevated concentrations of Hg but the highest values were found for fish from near the outfall (Francesconi & Lenanton, 1992). Most species of fish in this western region contained Hg in excess of the maximum permitted concentration (MPC) of 0.5 mg kg-’ wet wt set by Australian health authorities (Anon, 1993) whereas most fish from the eastern region contained less than 0.5 mg Hg kg-‘. Because of human health concerns, the discharge of Hg-containing effluent was stopped in 1984, and the contaminated part of the harbour was closed to all forms of fishing. Various restorative and ameliorative measures were considered in order to alleviate the problems caused by Hg contamination (Francesconi & Lenanton, 1992). Generally, these measures were either prohibitively expensive or impracticable for Princess Royal Harbour. Previous studies have shown natural reductions in the concentrations of Hg in fish from contaminated areas following cessation of the source of Hg contamination (Olsson, 1976; Armstrong & Scott, 1979; Langlois et al., 1987; Essink, 1988). This passive approach was adopted for Princess Royal Harbour. We report the results from a lo-year programme, carried out from 1984 to 1993, to monitor the natural declines in the Hg concentrations of eight teleost fish species from this Hg-contaminated marine embayment.
MATERIALS
AND METHODS
Princess Royal Harbour, a marine embayment on the south coast of Western Australia (35” 03’ S, 117” 53’ E; see Fig. l), contains the port facility for the town of Albany, and has several industries on its shores. The harbour has a total area of 29 km2, and consists of a deep basin bordered by shallow sand-flats which are most extensive off the western and southern shores (Anon, 1990). Mean winter and summer water temperatures are 14°C and 20°C respectively (Anon, 1990). The superphosphate plant is located near the western shore and had, over a 30-year period up to 1983, discharged effluent containing low concentrations of Hg via a pipeline with the outfall about 1 km offshore (Fig. 1). Sampling procedures
Earlier work (Francesconi & Lenanton, 1992) on Hg in fish from various regions of the harbour showed that concentrations were highest in fish collected from the western region adjacent to the effluent outfall. In the present study, eight species of fish were routinely sampled from this site, designated the outfall site (Fig. 1). The species chosen (see Table 1)
29
Long-term study of Hg concentrations inJish
PRINCESS
ROYAL
Fig. 1. Princess Royal Harbour showing the effluent outfall X, and fish sampling sites a. The numbers 1-6 represent the six sites sampled for Katelysia scalarina. The area west of the dotted line was closed to all forms of fishing from 1984 to 1992.
Common
Names,
TABLE 1 Scientific Names, Sample Sizes and Lengths and Diets of Fishes Monitoring Study of Princess Royal Harbour, 1984-l 993
used in Hg
Common name
Scientific name Sample size
Total length (mm) Range
Major components of‘diet”
Cobbler
Cnidoglanis macrocephalus Platycephalus laevigatus Pelates sexlineatus Sillaginodes punctata Arripis georgianus Pseudolabrus park Bigener brownii
760
150-625
61
225-515
408
Crustaceans, polychaetes Fish
508
121--285
211
No diet data available
433
154495
272
807
1388327
227
78
133-370
274
298
106371
282
Polychaetes, small crustaceans Fish, crustaceans, polychaetes Molluscs, crustaceans, fish Plants
271
163-374
293
Rock flathead Striped trumpeter King George whiting Australian herring Brown-spotted wrasse Spiny-tailed leatherjacket Six-spined leatherjacket %See Francesconi
Meuschenia freycineti & Lenanton
(1992).
molluscs,
Plants, echinoderms, sponges, large crustaceans
30
K. A. Francesconi
et al.
encompassed a range of diets, and hence Hg concentrations (Francesconi & Lenanton, 1992) and included the most important commercial and recreational species. A winter sample was taken (usually in August) annually from 1984 to 1991 and in 1993, and a summer sample (February) was taken from 1985 to 1987. The eastern region was sampled in March of 1984 and 1986, and in August of 1988 and 1989. The fish were collected with a composite gill net comprising stretched mesh sizes from 1 to 10 cm. We endeavoured to obtain at least 30 individuals of each species on each sampling occasion, but this was not always possible. Sampling was generally carried out over a 3-4 day period. Fish were individually measured and weighed, and stored frozen in polyethylene bags. Within two months of capture, fish were thawed and samples of muscle tissue from just behind the pectoral fin were analysed for Hg. Bivalve molluscs Kuteiysia scalarina (Family Veneridae) were collected in September 1990 from six sites adjacent to and including the outfall site (Fig. 1). These sites corresponded with those sampled for K. scalarina in 1984 (Jackson rt al., 1986). A composite sample comprising whole, drained, wet tissue from 10 individuals (dorsoventral length 3640 mm) from each site was analysed for total Hg. Mercury analyses
Samples were analysed for total Hg using a modification of the technique described in Collett et al. (1981). Samples of 2-3 g were weighed into 200 ml Kjeldahl flasks and digested in a mixture of nitric and sulfuric acids and ammonium metavanadate in a hot air bath. The samples were cooled and diluted to 130 ml. Prior to 1987, the Hg in the diluted samples was determined using a Perkin-Elmer Coleman 50 Mercury Analyser System after reaction of a 50 ml aliquot with a stannous chloride solution. After 1987, Hg was determined using a Varian SpectrAA 20 atomic absorption spectrophotometer with a VGA-76 continuous vapour generation accessory after reaction with hydrochloric acid and sodium borohydride solutions. All Hg concentrations are reported on a wet weight basis. Quality assurance/quality control over the sampling period (19841993) was ensured by conducting repeat analyses on at least 5% of the samples, and primary standards (pre1987) or reference materials (post-1987) were included at the rate of at least two in each batch of 20 samples. The primary standard of 200 ng Hg gave a standard deviation of 5.2% (n = 100). The reference materials used were the Canadian National Research Council’s TORT-l and DORM-l, and an in-house standard material of dried lish muscle tissue. TORT-l (certified value 0.33 f 0.06 mg kg-‘) returned a mean value of 0.34 f 0.03 mg kg-‘, n = 15, DORM-l (certified value 0.798 f 0.074 mg kg-‘) returned a mean value of 0.82 f 0.06 mg kg-‘, n = 16, and the in-house dried fish standard (FISH-l, mean 3.5 mg kg-‘) gave a sample standard deviation of 8.6% (n = 132). During the period of this study the laboratory participated in five interlaboratory surveys on metals in foods obtaining satisfactory results on all occasions. Statistical
analyses
For each of the fish species, an analysis of covariance (ANCOVA) was undertaken on the log-transformed Hg concentrations with the log of fish length as the covariate, and year of sampling and seasons (summer and winter) as factors. The variation in Hg concentrations
Long-rerm
study
of Hg
concentrations
in fish
31
from samples caught on different days during the one sampling period was examined using the ANCOVA with the sampling days nested within the sample period. Geometric mean Hg concentrations, adjusted for variations in fish length between samples and for seasonal differences, were examined for trends over the IO-year period. Mercury concentration differences between the eastern region and the outfall site were also examined. The effect of age (or an index of age such as length) must be considered when comparing Hg data for a particular species from sample to sample. This effect can be compensated for by determining the slope in the log-transformed relationship between fish length and Hg concentration over all sample periods, and comparing the mean Hg concentrations for each sample at the overall group mean length. In the present study, comparison of Hg data between years is based on the geometric mean Hg concentration (calculated from back-transformed log data) at the overall group mean length for each species. This approach assumes a common slope between the log-transformed Hg and length relationships over the sample periods. The annual geometric mean Hg concentrations were then used to examine the annual rate of decline of the Hg concentration using the following relationship: Hg = (I exp( -h YEAR)
(1)
where u and h are parameters obtained from fitting this model using a logarithmic transformation. An estimate of the annual rate of decline of Hg is provided by exp( -6). For some species a more appropriate description of the annual rate of decline of mean Hg concentration would bc: Hg = a exp( --h YEAR) + (’ where the long-term decline in the mean Hg concentration is to a concentration calculated ‘baseline’ level) rather than zero which is implicit in eqn (I).
RESULTS
(2) c (a
AND DISCUSSION
Mercury concentrations in cockles
Mercury concentrations in samples of K. scalarina collected in 1990 from six sites in the western region ranged from 0. I3 to 0.31 mg kg-’ with a mean of 0.23 mg kg- ‘. These values were much lower than those recorded for K. scalarina taken from the same sites in 1984 when the range was 0.4 9.2 mg kg-’ with a mean of 3.8 mg kg -’ (Jackson e[ al., 1986). Derivation of valid fish Hg concentrations for comparison
Depending on the mobility of a particular fish species, there may be variations in Hg concentrations among different schools caught over the 3- 4 day sampling period. This could result in differences in mean Hg concentrations on a daily basis, and the data would be less reliable for use in long-term monitoring. ANCOVA (see Table 2) showed that, for five of the eight species, there were no significant differences in Hg concentrations between days in a single sample period @ > 0.05). Striped trumpeter, Australian herring and sixspined leatherjacket showed significant differences but these were mainly due to daily variations in one sample period only (August 1986 for striped trumpeter, August 1988 for
807
Australian
leatherjacket
271
298
* *
***
NS
***
***
NS
NS
***
NS
*** p < 0.001; NS, not significant.
leatherjacket
wrasse
* p < 0.05; **p<0.01;
Six-spined
Spiny-tailed
Brown-spotted
78
***
433
King George whiting
herring
***
508
Striped trumpeter
***
***
***
***
61
760
Cobbler
Seuson
(ANCOVA)
Year
Rock flathead
N
Species
Results from Analysis of Covariance
(-0.77) *** (2.26) *** (0.37) *** (0.82) *** (7.36) *** (1.17) * (-0.32) NS
***
Log(length) (Slope)
Main eflects
0.230
0.127
0.082
0.794
0.200
0.147
0.192
0.136
RMS
TABLE 2 on Log-transformed
***
0.28
0.57
0.39
NS
NS
NS
**
0.26
0.69
NS
NS
NS
Log(lmgth) x Year
0.15
0.56
0.40
R’
Hg Concentrations
= residual
NS
NS
*
**
NS
NS
NS
NS
x Seu.son
Log(length)
Inteructions
(RMS
NS
NS
NS
NS
NS
NS
NS
**
Year x Season
Day
***
NS
NS
*
NS
**
NS
NS
YYMMDD i Y Y x Season)
mean square)
2
2
2 -.
2 4
s
21
i.L
x
Long-term study of Hg concentrations in fish
33
Australian herring, and September 1990 for six-spined leatherjacket). Consequently, Hg data from catches taken over the 334 days of a sample period were combined with the knowledge that, in general, they accurately represented the Hg status of a species at that time. For five of the eight species, Hg concentrations showed a significant positive relationship with length @ < 0.001). Six-spined leatherjacket showed no relationship between Hg concentration and length @ > 0.1) and two species, cobbler and spinytailed leatherjacket, had a significant negative relationship between Hg concentration and length (p < 0.001 and p < 0.05, respectively). This negative relationship possibly reflects differences in mobility between age classes of cobbler (Francesconi & Lenanton, 1992). Small cobbler are more localised in their movements than are larger cobbler (Lenanton & Caputi, 1989) and, at the time of capture, are likely to have spent a greater proportion of their life in the area of contamination. Of the eight species, only King George whiting and Australian herring showed significant differences in the slope of the Hg/length relationship between years (see Fig. 2 for examples). For both whiting and herring, however, the additional sum of squares associated with the interaction was much less than the mean square assuming a common slope. Thus, as an initial approximation, a common slope was also assumed for these two species for the purpose of correcting the Hg values for differences in size. There were significant differences in the Hg concentrations depending on season for four species - cobbler, striped trumpeter and the two leatherjacket species (Table 3). Mean Hg concentrations for summer samples were generally higher than those for winter samples. However, the strong correlations between Hg concentrations in fish and water temperature reported by Bodaly et al. (1993) in their work on Canadian lakes were not evident in the Princess Royal Harbour study. Comparison of Hg concentrations
in fish: outfall site vs eastern region
Seven of the eight species examined in this study yielded sufficient samples in the eastern region to enable comparison with the outfall site to be made (Table 4). For all seven species, Hg concentrations in fish from the outfall site were significantly higher (by a factor of two to three) than those in fish from the eastern region. Annual comparisons of Hg concentrations
in fish from the outfall site
Mercury concentrations in the eight fish species sampled from the outfall site from 1984 to 1993 are shown in Fig. 3. Mercury concentrations in cobbler decreased markedly from 1984 to 1993 with an estimated average rate of decline of 8% per annum using eqn (1). These decreases, however, were most apparent in the first four years; since 1988 there has been no clear continuing trend to lower concentrations. These data were also fitted to eqn (2) resulting in an estimate of paramater c of 0.5 mg kg-’ which indicates that the long-term decline is not to zero. Equation (2) provided a significantly better fit to the data than eqn (1). Flatheads are non-migratory and at the top of the food chain in the harbour, their diet consisting almost entirely of fish which are high in Hg (Francesconi & Lenanton, 1992). Consequently, rock flathead contained very high concentrations of Hg (about 6 mg kg-‘) at the beginning of this study. The concentrations have significantly decreased with time
34
K. A. Francesconi et al.
2.0
1986
1.0 1
5
1993
O-O. *
4
-1.0.
3
-2.0.
**
-3.0. -4.0 *
*
I -5.O{
5.6
5.5
5.4
5.3
Log
Length
1.0' 0.5. * 0.0. -0.5. -1.0. -1.5.
.,
. 5.4
.
.
.
. 5.6
.
.
.
. 5.6
6.0
6.2
6.4
Log Length Hg-length relationships for two species of fish from Princess Royal Harbour: Fig. 2. Log-transformed (a) Australian herring, showing positive Hg-length relationship and significant difference in slope between years; (b) cobbler, showing a negative Hg-length relationship and no significant difference in slope between years. To enhance clarity, data from two years only are shown.
35
Long-term study of Fig concentrations in fish
TABLE3 Geometric Mean Hg Concentrations Species
-
of Fish -
Summer/Winter
Samples, 1985-l 987, outfall site Season differences
Mercury concentration (mg kg -I) Winter Summer ~ _____~_
Cobbler Rock tlathead Striped trumpeter King George whiting Australian herring Brown-spotted wrasse Spiny-tailed leatherjacket Six-spined leatherjacket ~_.~ -.._
0.66 2.8 0.79 0.47 0.53 2.9 0.08 0.58
***
0.57 3.1 0.65 0.46 0.58 2.4 0.09 0.46
NS *** NS NS NS * * -__
* p < 0.05; *** p < 0.001; NS, not significant.
TABLE4 Geometric Mean Hg Concentrations Species
Cobbler Rock flathead Striped trumpeter King George whiting Australian herring Spiny-tailed leatherjacket Six-spined leatherjacket
of Fish -- Eastern Site vs Outfall Site
Mercury concentration (mg kg- ‘j” Eastern site Outfall site 0.24 1.3 0.29 0.19 0.21 0.03 0.14
Site differences ~_ *** * *** *** *** *+* ***
0.59 2.7 0.72 0.46 0.55 0.09 0.51 _.~_.
“Data represent the mean Hg concentrations for the years when comparisons namely 1984, 1986, 1988 and/or 1989. * p <0.05; *** p
_.~
could be made,
rate of decline 11% per annum, p < 0.05), with a possible levelling-off over recent years. Although striped trumpeter are not commercially fished in Princess Royal Harbour (they,are not generally eaten) they were particularly suitable for Hg monitoring because of their resident status and abundance. The concentrations of Hg showed a slow reduction over time (3% per annum 0.05
K. A. Francesconi
36
et al.
1.0 -
Cobbler
0.6 0.6 -
* *
0.4 -
*
0.2 0.0 r
,
I
6.0
!._:\:_:
* E
1.0:
3
0.0;
,
0.6.
+;
2 a 3
I
*
Striped trumpeter *
*
*0.6 -
*
*
*
5 0.4.
0.6 .
King Georgewhiting
0.6 -
* *
0.4 *
*
*
0.2 -
o.o*
, 1864
1666
I lsa6
1667
1666
ls69
1680
1881
lea2
1983
Fig. 3. Geometric mean Hg concentrations (mg kg-’ wet weight) in fish sampled from the outfall site, Princess Royal Harbour, 1984 to 1993. * Represents actual data; lines have been drawn using eqn (1) or (2) as described in the text.
Brown-spotted wrasse in Princess Royal Harbour have high Hg concentrations (about 4 mg kg-‘) because of their sedentary nature and carnivorous diet (Francesconi & Lenanton, 1992). The rate of decline of the Hg concentration was estimated at 11% per annum using eqn (1) with most of the decrease occurring in the first four years. Brown-spotted wrasse were similar to cobbler in that they showed an improved fit using eqn (2), the parameter estimate for c (the calculated ‘baseline’ level), being 1.6 mg kg-‘. The spiny-tailed leatherjacket is a good indicator species because it spends its entire life cycle in Princess Royal Harbour (B. Hutchins, pers. commun.). This species is a strict herbivore feeding exclusively on algae and seagrasses (Francesconi & Lenanton, 1992).
Long-term study of Hg concentrations infish 1.47 *
12.
Austrdim
herring
1.0. *
* *
0.4 .
*
*
02. 0.0 r
,
0.14, 0.12*
spiny-tailedleatheriadtet
0.10 *
*
mm.
* *
0.06.
*
*
0.04. 0.02. o.oo-
‘ ,gt)rl
1885
IaM
1967
Isa5
lo82
lem
IQol
1892
we3
Y0W Fig. 3.
Contd.
These plants contained only low levels of organic Hg (Francesconi & Lenanton, 1992), and consequently spiny-tailed leatherjacket contained only low concentrations of Hg (about 0.2 mg kg-‘) at the beginning of the monitoring programme. Nevertheless, the Hg concentrations in spiny-tailed leatherjacket decreased a further 50% during the first five years of the study before levelling-off. This trend was also followed by the six-spined leatherjacket, although it initially contained higher Hg concentrations (about 1 mg kg-‘) because of its omnivorous diet (Francesconi & Lenanton, 1992). In general, the fish species monitored in this study showed a uniform trend - Hg concentrations decreased over the first four years before levelling off. The Hg value at which this occurred (the ‘baseline’ level, constant c from eqn (2)) varied considerably between species. For cobbler, King George whiting, Australian herring and the two leatherjacket
38
K. A. Francesconi et al.
species, this value was < 0.5 mg Hg kg-‘, but it was higher for rock flathead (1.7 mg kg-‘) and brown-spotted wrasse (1.6 mg kg-‘). Neither flathead nor wrasse, however, constitute a significant proportion of the total fish catch from Princess Royal Harbour. By 1992, health authorities considered that the Hg levels in fish had reduced to the point where there was negligible human health risk associated with eating fish from the outfall site, and the restriction on fishing in the western region of the harbour was lifted. Hypothesis
for the observed decreases in fish Hg concentrations
Despite the fact that there has been no input of Hg to Princess Royal Harbour for IO years, the Hg levels in fish have levelled off at values much higher than those for fish of the same species from nearby uncontaminated embayments where levels ranged from 0.02 to 0.06 mg kg-’ (Jackson et al., 1986). This effect may be explained by the fate of Hg in water and sediments of contaminated aquatic systems. Jerneliiv and Asell (1975) in their model of the fate of Hg in an aquatic system following cessation of Hg-contaminated effluents predicted that Hg concentrations would decrease quickly in the water column but only slowly in the surface sediments. Results from Princess Royal Harbour are in accord with this view; a survey of the harbour undertaken in 1989 revealed that the water contained very low concentrations of Hg whereas the Hg concentrations in the sediments had not decreased significantly since 1984 (Anon, 1990). Previous work has shown that diet is the major source of Hg for fish in Princess Royal Harbour (Francesconi & Lenanton, 1992). Mercury concentrations in the prey items of fish will depend on the concentrations of Hg in the water and sediments, and the relative contribution of each of these components to body burden. For example, Hg concentrations in suspension-feeding bivalves would be largely influenced by water Hg levels, and those in detrital-feeding organisms would be more influenced by sediments. In Princess Royal Harbour, lower water Hg concentrations were reflected by large decreases in Hg concentrations in the suspension-feeding bivalve K. scalurina ~- in 1990 their Hg levels were only 6% of the 1984 values. Although there are no long-term data on Hg in detritalfeeders from Princess Royal Harbour, the Hg levels are likely to parallel those in the sediments and be little changed from their 1984 values. Consequently, the Hg concentrations of the overall diets of the fish (and hence of the fish themselves) from the harbour may be expected to decrease in two phases. First, a decrease reflecting rapid decline of Hg levels in suspension-feeding bivalves and other organisms which accumulate Hg primarily from the water; and second a more gradual decrease/levelling off reflecting slow decline of Hg levels in detrital-feeding organisms which accumulate Hg primarily from the sediments. The decreases in Hg levels in fish shown in this monitoring study are consistent with such an hypothesis. Moreover, the data indicate that the proposed second phase of Hg reduction has been reached, and further decreases in fish Hg concentrations will be gradual. Comparison of Princess Royal Ha&our with other Hg-contaminated
regions
It is of interest to compare the course of contamination in Princess Royal Harbour with that reported for other Hg-contaminated aquatic systems. Lake Marmen in Sweden received ‘Hg from paper-mill wastes until 1967, and Hg concentrations were determined in pike (ESOX Lucius) sampled from the lake in 1968 and 1972 (Olsson, 1976). The concentrations decreased in this time; from the data presented by Olsson (1976) we
Long-term study of Hg concentrationsin&h
39
estimate the Hg concentration at the overall group mean length to have decreased from 2.2 to 1.8 mg kg-’ wet wt. The Wabigoon-English-Winnipeg River system of Ontario, Canada received about 10,000 kg of Hg from a chlor-alkali plant from 1962 to 1970. The discharge was restricted to about 3% of that level from 1970 to 1975, and then stopped altogether. The concentrations of Hg in three species of fish from Ball Lake, part of the river system, were determined in 1971, 1972 and 1976 (Armstrong & Scott, 1979). All three species showed marked decreases in their Hg concentrations between 1972 and 1976: walleye (Stizostedion vitreum vitreum) from 2.71 to 1.39 mg kg-‘, pike (E. lucks) from 5.72 to 1.80 mg kg-‘, and whitefish (Coregonus clupeuformis) from 0.62 to 0.42 mg kg-’ (Armstrong & Scott, 1979). The sand flathead (Pkztycephalus bussensis) was used as an indicator of Hg contamination in the Derwent Estuary in Tasmania which received Hg-containing wastes from a zinc refinery for several years until 1975 (Ratkowsky et al., 1975; Langlois et al., 1987). P. bassensis was sampled (in 1973/74, and then yearly from 1976/77 to 1982/83) from four sites with different levels of Hg contamination, Interestingly, fish from all four sites showed the same absolute reduction in Hg concentration (~0.3 mg kg-‘) over the IO-year period. In contrast to the trend found in Princess Royal Harbour, the rate of decline remained constant and a plateau of concentrations had not been reached even after 10 years. Discharge of Hg into the Dutch Wadden Sea and Ems Estuary in The Netherlands decreased considerably between 197 1 and 1987. The fish Zoarces viviparus sampled from this area has accordingly shown a steady decrease in its Hg concentrations; in 1987 the Hg concentration was about half that in 1981 (Essink, 1988). Inspection of the slopes for the relationship between Hg concentration and length for the various years suggests that the rate of decrease is declining (Essink, 1988). Liverpool Bay in the United Kingdom has a history of Hg contamination from several sources including sewage sludge and industrial discharges. Mean concentration of Hg in plaice Pleuronectes platessa declined from 0.5 mg kg-’ in the early 1970s to about 0.2 mg kg-’ in 1991, and this reduction was thought to reflect a decline in the input of Hg to Liverpool Bay since 1976 (Leah et al., 1993). There had been, however, no significant decrease in Hg concentrations over the last six years of that study, and the 0.2 mg kg-’ level probably represents an equilibrium position. There is still some input of Hg into Liverpool Bay, and Hg levels in plaice from the Bay remained higher than those in plaice from uncontaminated sites (0.1&O. 15 mg Hg kg-‘). Princess Royal Harbour differs from Liverpool Bay in that there is no continuing input of Hg, but Hg concentrations in the fish remain well above those for fish from uncontaminated sites (Jackson et al., 1986). In contrast to the above, Princess Royal Harbour has not received large quantities of Hg. The total amount of Hg discharged after 30 years of fertilizer manufacture can be estimated at about 400 kg (Jackson et al., 1986). Consequently, the harbour sediments were only moderately contaminated with a maximum value of 1.7 mg Hg kg-i. Mercury levels in the fish, however, were much higher than those for fish from grossly contaminated sites (e.g. Liverpool Bay). It is evident that Hg contamination in fish and its rate of decline depend on factors in addition to the amount discharged to an aquatic system. Influencing factors are likely to include the rate of flushing, type and complexity of food webs, fish mobility and degree of Hg methylation due to sediment type and water chemistry. In Princess Royal Harbour, previous work suggested that food webs and the restricted movement of fish in the harbour contributed to the unusually high Hg levels in fish (Francesconi & Lenanton, 1992). The
40
K. A. Francesconi
et al.
studies in Princess Royal Harbour highlight the need to recognise and understand environmental and ecological factors when predicting possible consequences of discharging a contaminant into an aquatic system. ACKNOWLEDGEMENTS The authors thank Mark Cliff, Jenny Moore, Jenny Shaw and Karen Parker for technical assistance, and our research colleagues at the Western Australian Marine Research Laboratories for constructive comment. REFERENCES Anon, (1990). Albany harbours environmental study (198881989). Environmental Protection Authority, Perth, Western Australia, Bulletin 412, 84 pp. Anon, (1993). Australian Food Standards Code. National Food Authority, Australian Government Publishing Service, Canberra, pp. Al2 l-5. Armstrong, F. A. J. & Scott, D. P. (1979). Decrease in mercury content of fishes in Ball Lake, Ontario, since imposition of controls on mercury discharges. J. Fish. Res. Board Can., 36, 670-672. Bodaly, R. A., Rudd, J. W. M., Fudge, R. J. P. & Kelly, C. A. (1993). Mercury concentrations in fish related to size of remote Canadian shield lakes. Can. J. Fish. Aquat. Sci., 50, 98@-987.
Collett, D. L., Taylor, G. A. & Chegwidden, A. (1981). Alkylmercury levels in marine sediments in Cockburn Sound, WA. Bull. Environm. Contam. Toxicol., 26,7577763. Essink, K. (1988). Decreasing mercury pollution in the Dutch Wadden Sea and Ems Estuary. Mar. Pollut. Bull., 19, 317-3 19. Francesconi, K. A. & Lenanton, R. C. J. (1992). Mercury contamination in a semienclosed marine embayment: organic and inorganic mercury content of biota, and factors influencing mercury levels in fish. Mar. Environ. Res., 33, 189-212. Jackson, M., Hancock, D., Schulz, R., Talbot, V. & Williams, D. (1986). Rock phosphate: the source of mercury pollution in a marine ecosystem at Albany, Western Australia. &far. Environ. Res., 18, 1855202. Jernelbv, A. & Asell, B. (1975). The feasibility of restoring mercury-contaminated waters. In Heavy Metals in the Aquatic Environment, ed. P. A. Krenkel. Pergamon Press, Oxford, pp. 299-309. Langlois, D., Cooper, R. J., Clark, N. H. & Ratkowsky, D. A. (1987). The effect of a mercury containment programme at a zinc smelting plant on the mercury content of sand flathead in the Derwent Estuary. Mar. Polk. Bull., 18, 67-70. Leah, R. T., Collings, S. E., Johnson, M. S. & Evans, S. J. (1993). Mercury in plaice (Pleuronectes pfutessa) from the sludge disposal ground of Liverpool Bay. Mar. Pollut. Bull., 26,436439.
Lenanton, R. C. J. & Caputi, N. (1989). The roles of food supply and shelter in the relationship between fishes, in particular Cnidoglanis macrocephalus (Valenciennes), and detached macrophytes in the surf zone of sandy beaches. J. Exp. Mar. Biol. Ecol., 128, 165-176.
Olsson, M. (1976). Mercury level as a function of size and age in northern pike, one and five years after the mercury ban in Sweden. Ambio, 5,73376. Ratkowsky, D. A., Dix, T. G. & Wilson, K. C. (1975). Mercury in fish in the Derwent Estuary, Tasmania, and its relation to the position of the fish in the food chain. Aust. J. Mar. Freshwater Res., 26, 223-231.