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A comparative bioassessment of sediment toxicity in lentic and lotic ecosystems of the North American Great Lakes
Aquatic Ecosystem Health and Management 2 (1999) 367–378 www.elsevier.com/locate/aquech
A comparative bioassessment of sediment toxicity in lentic and lotic ecosystems of the North American Great Lakes M. Munawar a,*, R. Dermott a, L.H. McCarthy b, S.F. Munawar c, H.A. van Stam a a
Fisheries and Oceans Canada, Great Lakes Laboratory for Fisheries and Aquatic Science, 867 Lakeshore Road. P.O. Box 5050, Burlington, Ontario, Canada L7R 4A6 b Department of Applied Chemical and biological Sciences. Ryerson Polytechnic University, Toronto, Ontario, M5B 2K3 Canada c Aquatic Ecosystem Health and Management Society. P.O. Box 85388 Brant Plaza Postal Outlet, Burlington, Ontario, Canada L7R 4K5
Abstract The bioavailability of sediment bound contaminants in lentic (Hamilton Harbour, Lake Ontario) and lotic (Detroit River connecting Lakes St. Clair and Erie) environments were assessed by a battery of multi-trophic tests using laboratory grown organisms. Hamilton Harbour is a hyper-eutrophic and highly contaminated environment due to extensive urban and industrial growth, while the Detroit River has been implicated as a major source of contaminants to Lake Erie. An array of sites across Hamilton Harbour and the Detroit River were selected, including the mouth of the Rouge River as well as the Trenton Channel—the contaminated western arm of the Detroit River. Multi-trophic acute assays were conducted using Daphnia magna, Hyalella azteca, Diporeia hoyi, and Lumbriculus variegatus. While the tests were consistent in determining the most toxic hot spots, variability existed in the sensitivities of test organisms to discriminate among less contaminated sites. The most toxic sediment in the Detroit River was at the mouth of the Rouge River, while the site in Windermere Basin in Hamilton harbour was found to be deleterious. The results indicated that the toxicity in a lotic ecosystem such as the Detroit River was caused by both the bottom sediments and the mobile seston component which contributed to the water-borne toxicity. Conversely, lentic and undisturbed ecosystems such as Hamilton Harbour contain much of their toxic component in the bottom sediments and not in the overlying water column. The multi-trophic battery of test approach adopted in our study appears to be effective in detecting and discriminating differential sensitivities of sediment bound contaminants in both lentic and lotic ecosystems. This battery of tests approach needs continued modification, development, and improvement to keep the assays up-to-date, sensitive, cost effective and adaptable in discriminating complex mixtures of sediment bound contaminants found in natural ecosystems. q 1999 Published by Elsevier Science Ltd and AEHMS. All rights reserved. Keywords: Detroit River; Hamilton Harbour; Contaminants; Toxic chemicals; Bioassays
1. Introduction The development of surface water quality guidelines in North America has been extensive, and the regulatory programs of Canada and the United States * Corresponding author. Tel.: 11-905-336-4867; fax: 11-905634-3516. E-mail address: [email protected] (M. Munawar)
have succeeded in mitigating many of the visible effects of pollution, making the water column more habitable for biota (Foran, 1990). However, in marked contrast to the water quality standards which are based on comprehensive toxicological and environmental fate databases, a large amount of research remains to be carried out on the toxicological potential and environmental fate of contaminants in sediments (United States Environmental Protection Agency
1463-4988/99/$20.00 q 1999 Published by Elsevier Science Ltd and AEHMS. All rights reserved. PII: S1463-498 8(99)00057-3
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Table 1 Multi-trophic bioassay protocol Test species
Type of assay
Assay duration
Number of organisms
Number of replicates
Endpoint
Reference
D. magna D. hoyi L. variegatus Hyalella azteca
Acute Acute Acute Acute
48 hours 1 week 2 weeks 1 week
10 5 or 10 10 10
5 5 5 5
Survival Survival Survival Survival
Munawar et al., 1989 Munawar et al., 1989 Dermott and Munawar, 1992 Borgmann and Munawar, 1989
(USEPA) 1992; Hoke et al., 1994). Forbes et al. (1998) report that three factors are primarily responsible for the difficulties in accurately predicting the exposure and bioavailability of organic contaminants in sediment to aquatic biota: (1) the complex geochemistry of sediment makes understanding chemical speciation and kinetics difficult; (2) aquatic organisms interact with the sediment in a myriad of ways, influencing contaminant fate and their own exposure to the pollutants; (3) biological variability is substantial due to numerous biochemical responses that occur once the contaminant has entered the organism, making simple assumptions based on sediment contaminant analysis difficult. Although recently attempts have been made to assess the potential hazard of contaminated sediment using biological systems, there is a tendency to assume toxicity based on bulk chemical characterizations. Also, the majority of studies utilize single organisms in an attempt to represent the entire aquatic food chain. This has led to the establishment of simple cause–effect relationships between chemical concentrations and easily observable biological impact on a single organism, often to the exclusion of less readily measured interactions, and extrapolating throughout the entire aquatic food web. Excellent reviews by Giesy and Hoke (1989), Munawar et al. (1989), USEPA (1992), Calow (1993) and Cairns and Cherry (1993) have been published suggesting the use of a suite of aquatic organisms to assess sediment toxicity. But few studies have incorporated a multi-trophic battery of tests to assess sediment toxicity in the Great Lakes (Munawar et al., 1992, 1993). Moreover, while the database on water pollution in the Great Lakes is enormous, there is still a lack of information linking sediment contamination with impact on aquatic organisms. Forty-two pollution “hot-spots” or areas of concern
exist in the North American Great Lakes areas (IJC, 1989; Hartig and Zarull, 1992). The current study assessed two such areas in detail, one a lentic ecosystem and the other a lotic environment. The lentic environment was Hamilton Harbour, an enclosed bay located at the western end of Lake Ontario. This area has the largest iron and steel industrial complex in Canada. Its sediments contain significant concentrations of heavy metals, PAHs, and PCBs, which are responsible for Hamilton Harbour having 11 out of 14 beneficial use impairments (IJC, 1993). The lotic ecosystem was the Detroit River connecting Lake St. Clair to Lake Erie, and is the international boundary between Michigan and Ontario. It has been implicated as a major source of PCBs to Lake Erie and is the single most important source of mercury. The Detroit River has 8 out of 14 possible beneficial uses impaired, including restrictions on drinking water, fish and wildlife consumption, fish tumours and loss of fish and wildlife habitat (IJC, 1993). Of particular interest was the western portion of the River known as the Trenton Channel. The highest contamination of sediment with heavy metals of the entire Detroit River system has been reported in this waterway (McCarthy, 1994). The largest tributary entering the Detroit River is the Rouge River which flows through the industrial areas on the Michigan side. This area was identified as an Area of Concern because 64 km of the Rouge River do not meet Michigan’s water quality standards. Also, the sediments are highly contaminated with cadmium, copper, lead, mercury, nickel, zinc, and PCBs (IJC, 1993). Thus, the purpose of the current study was to examine the bioavailability of pollutants from contaminated sediment using a multi-trophic battery of aquatic organisms as assessors of toxic potential. The assays incorporated the zooplankter Daphnia
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Fig. 1. Sites sampled, Detroit River and Hamilton Harbour.
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magna, the benthic amphipods Hyalella azteca and Diporeia hoyi, and the aquatic oligochaete Lumbriculus variegatus. The endpoint measured was mortality (Table 1).
2. Materials and methods 2.1. Sampling Sampling was carried out at selected sites in Hamilton Harbour, Detroit River–Rouge River in various seasons and years. Sampling was not carried out in areas where currents were obvious. Also, sediment type of choice was either silt or clay, if the substrate appeared too sandy or gravely, that site was not used. Most sampling was carried out using a Shipek sampler from a small, 16-foot boat, which caused little resuspension of the sediment during retrieval. Water overlaying the sediment was removed by siphon and discarded. The top 10 cm of sediment from each of the three replicate samples was removed and mixed together in clean 5 l polyethylene pails. The sediment was placed into clear, polypropylene bags, and kept in coolers, then refrigerated at 48C in the laboratory until they were used for bioassays. In Hamilton Harbour the samples were collected during April and October 1990 which included four stations of varying contamination (Fig. 1). HH1 and HH6 were furthest from industrial areas but close to inflow areas where pesticides may be present. HH4 in Windermere Basin has a history of pollution problems and HH2 is in close proximity to the western dock of a major steel mill. During August 1989 the Detroit River (mouth of Rouge River) was sampled at DR7 (Fig. 1) and at two sites downstream (DR6, off Great Lakes Steel Corporation and DR1, Trenton Channel at Monanto). In July 1992, additional sites were sampled. Sediment was also collected at RR1 and RR3 upstream on the Rouge River, and three more sites on the Detroit River; DR35 and DR34, which are downstream of the Rouge River mouth and an upstream site, DR23. A reference site from mid Lake Erie was used for the Detroit River samples and in mid Lake Ontario for the Hamilton Harbour sediments.
2.2. Daphnia magna cultures The culturing of D. magna is detailed in Munawar et al. (1989) which is a modified version of the method described by Nebeker et al. (1984). The daphnids were cultivated in large, oxygenated tanks in dechlorinated tap water (from Lake Ontario) under controlled conditions with temperatures of < 218C and a photoperiod of 16 h light: 8 h dark. The animals received three feedings weekly of Tetra-Minq fish food. The day before testing, mature females were removed from the stock culture and placed in breeding tanks. On the day of testing, neonates (animals less than 24 h old) were removed and used as test organisms. 2.3. Acute Daphnia magna bioassays Experimental assays in the current study included the following test protocols outlined in Munawar et al. (1989). 10 daphnid neonates were placed in five randomly arranged 250 ml zooplankton jars containing either 200 ml of integrated sample site water (1–10 m) or reference water. Temperature was maintained at 218C, with a photoperiod regime of 16 h light: 8 h dark. Oxygen was measured before animals were added and once during the bioassay. After 48 h, survivors were enumerated. 2.4. Hyalella azteca cultures The protocol is detailed in Borgmann and Munawar (1989) and Borgmann et al. (1989). Amphipod cultures were maintained in straight-sided glass jars with pieces of surgical bandage-type cotton gauze and dechlorinated tap water and fed Tetra-minq fish food flakes several times weekly. The animals were separated according to age (0–1 week), and kept in separate culturing jars before use in bioassays. 2.5. Acute Hyalella azteca solid phase bioassays The protocol is adapted from Borgmann and Munawar (1989) for use with a smaller amount of sediment. 10 young (less than seven days) animals were exposed to test sediments for seven days at 20–228C, 16 h light: 8 h dark. The H. azteca were obtained from laboratory cultures. Approximately 50 ml of sediment was added to each of five glass beakers containing 200 ml of dechlorinated tap water. Individual air lines were added to each beaker to gently oxygenate without disturbing the sediment. Dechlorinated water was added as needed to keep the
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water level constant. H. azteca were fed Tetra-Minq fish flakes twice. After one week the sediments were sifted through a 275 mm nylon screen and the surviving amphipods were sorted and counted.
Any ‘wild’ tubificid worms or their fragments that were mistakenly counted and weighed before preservation were identified and the final counts were corrected (Dermott and Munawar, 1992).
2.6. Lumbriculus variegatus cultures L. variegatus were purchased from aquaria wholesalers and maintained at 208C in 40 l aquaria on fine 100 mm silicon sand. The water was aerated with a slow water exchange of about one volume per day and the worms were fed commercial trout food pellets once a week. Detailed methodology is given in Dermott and Munawar (1992).
2.8. Acute Diporeia hoyi solid phase bioassay
2.7. Chronic Lumbriculus variegatus solid phase bioassay Unsieved mud (20 ml) was spooned into 100 ml jars resulting in a sediment layer of about 2 cm. Mud was allowed to settle overnight at 20–228C while the surface oxidized under 1 mm of surface water. The jars were gently filled with dechlorinated water to minimize the disturbance of the surface sediment. Ten L. variegatus of similar size were added to each jar using a pipette. The jars were submerged uncovered about 2 cm below the water surface in 10 l aquaria containing 5 l of dechlorinated water. Individual aquaria were used for each test sediment for which five replicates were done. Water in the aquaria was aerated and O2 concentration was measured after 48 h. After exposure for two weeks under a 16 h light: 8 h dark photoperiod, the sediment was gently sieved through a 200 mm mesh screen, and the surviving worms were back-washed onto a white pan and counted. Due to the escape behaviour of L. variegatus when disturbed, the healthy animals could be separated from any Tubificidae or Stylodrilus that may have been present in the tested sediment. The latter worms become tightly coiled when disturbed. At the end of the assay, worms were transferred into labeled vials and preserved by adding 4% formalin. Within 24 h, the worms and fragments were examined under a dissecting microscope for the occurrence of a prostomium (anterior end or ‘head’). Only those worms with a complete or developing prostomium were counted. This is necessary in order to determine if any increase in number was due to reproduction by architomic division (asexual reproduction by budding) and not fragmentation during the screening.
Due to the lower temperature tolerance of D. hoyi this amphipod assay was maintained at 108C and exposure to test sediments was for only one week in the dark. D. hoyi were collected using an Ekman grab from the profundal zone of Lake Ontario and held in 40 l aquaria containing sediment from the collection site for a period of one week to two months before use. Because of the difficulty in obtaining healthy animals during mid summer, only five animals were added to each replicate, giving the minimum statistical requirement of five replicates each with five animals (Hodson et al., 1977). D. hoyi were removed from the holding aquaria using the same method as L. variegatus, however D. hoyi were kept submerged during transfers to ensure that air was not trapped under their coxal plates. After the addition of the animals to the jars, a cover of 0.5 mm mesh gauze was held over the jar with an elastic band. This was necessary to keep the amphipods away from the water surface and to prevent them from leaving the jars. The jars were then submerged in aquaria around an air bubbler to create a current between the jars and the water surface 2 cm above the jars (Jackson et al., 1995). 2.9. Chemical analysis Background chemistry information was obtained from various sources for the two ecosystems known for their pollution. Chemical analysis was performed by the National Laboratory for Environmental Testing, (Environment Canada, 1995) on sediments collected during June 1989 in Hamilton Harbour and August and September 1989 in the Detroit River. PAH data is obtained from McCarthy (1994) for Hamilton Harbour, Detroit and Rouge Rivers collected during 1992. 3. Results and discussion The purpose of the current study was to assess the impact of contaminated sediment from a lentic and a
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Fig. 2. Multi-trophic bioassay results, Hamilton Harbour April 1990, N 10 individuals per replicate for all organisms except for D. hoyi N 5. Bars indicate standard deviation.
lotic environment of the North American Great Lakes with a multi-trophic battery of aquatic organisms. These organisms were known for their sensitivities to a variety of anthropogenic chemicals. While daphnids are not benthic, their propensity for inhabiting the sediment-water interface makes them a useful indicator of sediment toxicity. They feed at the surface of sediments and come into intimate contact with particulate-bound toxicants (Suedel et al. 1993). The benthic amphipods are important components of the sediment community and form a major diet item of bottom-feeding fish (Borgmann et al., 1989). The USEPA (1992) reported that H. azteca were as sensitive as Hexagenia to impacts of various
sediment compounds, and more sensitive than Chironomus. Burton et al. (1992) reported that in 7–14 days whole sediment exposure assays, tests with H. azteca had proven to be some of the most sensitive and discriminatory of 20 different sediment toxicity assays utilizing contaminated sediments from the Great Lakes. The authors highly recommended these organisms as a tool to measure sediment toxicity. The use of L. variegatus in sediment toxicity testing has been widely reported (Chapman et al. 1982; Weiderholm et al., 1987; Keilty et al., 1988). Phipps et al. (1993) suggested that the aquatic oligochaete was an ecologically relevant component of aquatic ecosystems being exposed intimately to
Fig. 3. Multi-trophic bioassay results, Hamilton Harbour October 1990, N 10 individuals per replicate for all organisms except for D. hoyi N 5. Bars indicate standard deviation.
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Fig. 4. Multi-trophic bioassay results, Detroit and Rouge Rivers, August 1989, N 10 individuals per replicate for all organisms except for D. hoyi N 5. Bars indicate standard deviation.
contaminants in the sediment; thus was a suitable bioassay organism. Overall, the four organisms used in the current study were suitable test organisms, in accordance with Giesy and Hoke (1989) and Munawar et al. (1989). The bioassays were rapid, relatively inexpensive, and standardized to facilitate widespread use, while the organisms were easy to culture and use at any time, the response of the control organism was predictable and replicable, and ecologically relevant. In April 1990, the Hamilton Harbour bioassays were conducted using D. magna, H. azteca, D. hoyi and L. variegatus, (Fig. 2). Differential sensitivity was shown by all species. H. azteca were sensitive to many contaminated sites, especially HH4. L. variegatus was
only sensitive to the highly contaminated HH4. D. hoyi and D. magna were not significantly sensitive to any sites. D. magna‘s insensitivity suggests that a mobile seston component is not a significant cause of toxicity in Hamilton Harbour. A differential response of test organisms was shown to different conditions and mixtures of heavy metals and organics. In October 1990, the Hamilton Harbour bioassays were again run using H. azteca, D. hoyi and L. variegatus, and (Fig. 3). Again differential sensitivities were shown by all species. H. azteca and D. hoyi did not show significant differences in sensitivity and were not sensitive to contaminated sites. L. variegatus were only sensitive to highly contaminated HH4, while reproducing in the
Fig. 5. Multi-trophic bioassay results, Detroit (DR) and Rouge Rivers (RR), July 1992, N 10 individuals per replicate for all organisms. Bars indicate standard deviation.
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Table 2 Inorganic sediment chemistry analysis. Detroit River and Hamilton Harbour at selected stations during 1989. (SEL: Severe Effects Level (Bold), LEL: Lowest Effects Level (italics) (Persaud et al., 1993). ND, not determined; na, not available) Detroit River, September 1989 Compound (mg kg 21) DR1
DR6
DR7
LEL
SEL
Al Cd Co Cu Fe Mn Ni Pb Zn As Se Hg Inorganic P Total P %C %N
27300 5.03 13.7 159 134000 1730 135 223 788 8.8 1 0.56 1826 1860 3.1 0.12
50000 5.23 13.3 124 343000 523 51 163 457 10.6 0.8 0.65 935 1080 8.33 0.47
na 0.6 na 16 20000 460 16 31 120 6 na 0.2 na 600 1 na
na 10 na 110 40000 1100 75 250 820 33 na 2 na 2000 10 na
Hamilton Harbour, June 1989 Compound (mg kg 21) HH1
HH2
HH4
LEL
SEL
Al Cd Co Cu Fe Mn Ni Pb Zn As Se Hg Inorganic P Total P
50600 11.3 33.3 185 80000 2980 96.1 529 4790 42.3 8.8 0.9 3790 4120
53800 4 32 193 49400 1020 68.7 256 1240 12.3 8.1 0.62 3720 4220
na 0.6 na 16 20000 460 16 31 120 6 na 0.2 na 600
na 10 na 110 40000 1100 75 250 820 33 na 2 na 2000
33500 11.3 12.4 164 43400 554 58 161 442 12.8 1.1 2.27 880 914 7.54 0.39
53300 4.8 32.4 107 50400 1740 74.4 235 1870 21.4 4.7 0.42 2260 2630
sediments of HH2. The differential response seen was likely due to different conditions and mixtures of heavy metals and organics at each site affecting their bioavailability. In August 1989, the Detroit River bioassays were conducted using D. magna, H. azteca, and D. hoyi (Fig. 4). Differential sensitivities were expressed by all species. While DR6 (Great Lakes Steel Corporation) and DR7 (Mouth of Rouge River) on the Detroit River, located downstream of highly contaminated Rouge River, were toxic to all three species, H. azteca
was more sensitive to contaminated sediment than the other amphipod D. hoyi. Unlike Hamilton Harbour where there was no impact on D. magna, sites on the two rivers were toxic to this water column organism. This suggests that toxicity in a flowing ecosystem such as a river is not only caused by stationary bottom sediments, but also by the mobile seston component. In July 1992, the Detroit River bioassays were conducted again with H. azteca and L. variegatus (Fig. 5). Differential sensitivities were shown by
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Table 3 Organic contaminants in Detroit River and Hamilton Harbour at selected stations during 1989. (SEL, Severe Effects Level (Bold); LEL, Lowest Effects Level (Italics) (Persaud et al. 1993); ND, not determined; na, not available) Detroit River, August 1989 Compound (mg kg 21)
DR1
DR6
DR7
LEL
SEL
HCB G-Chlor A-Chlor p,p 0 -DDE Dieldrin Endrin p,p 0 -TDE o,p-DDT p,p-DD Mirex Total PCB
ND 0.003 0.003 0.023 0.001 ND 0.02 N.D N.D ND 1.732
0.005 0.002 0.003 0.087 0.002 ND 0.089 ND ND ND 3.56
0.005 0.007 0.008 0.049 0.003 ND 0.069 0.001 ND ND 2.726
0.02 na na 0.005 0.002 0.003 na na na 0.007 0.07
24 na na 19 91 130 na na na 130 530
Hamilton Harbour, June 1989 Compound (mg kg 21)
HH2
HH3
HH4
HH6
LEL
SEL
HCB G-Chlor A-Chlor p,p 0 -DDE Dieldrin Endrin p,p 0 -TDE o,p-DDT p,p-DDT Mirex Total PCB
0.0004 0.0072 0.0018 0.006 ND ND 0.0035 ND ND ND 0.5127
0.0002 0.0081 0.0007 0.0027 0.0003 ND 0.0018 ND ND ND 0.3693
0.0002 0.0373 0.001 0.0037 0.0002 ND 0.0016 ND 0.0003 ND 0.752
N.D 0.0006 0.0003 0.001 ND ND 0.0008 ND ND ND 0.0594
0.02 na na 0.005 0.002 0.003 na na na 0.007 0.07
24 na na 19 91 130 na na na 130 530
both species. While the sites on Detroit River downstream of the highly contaminated Rouge River were toxic to H. azteca, L. variegatus was insensitive to contaminated sediment. The trend of impact noted with H. azteca indicates a gradient of increasing toxicity from north of the Rouge River to the highly polluted Trenton Channel in the southern portion of Detroit River. During July 1992, bioassays were also conducted with the Rouge River sediments using H. azteca and L. variegatus (Fig. 5). These species showed differential sensitivity to the test sediments. Rouge River sites RR1 and RR3 are considered to be the most toxic hot spots where the highest concentrations of organic and inorganic contaminants were observed. Interestingly L. variegatus still appeared to be indifferent to such high levels of contaminants. Conversely, H. azteca
were practically eliminated by the end of the experiment. The background chemistry results on the sediments from the various sites in Hamilton Harbour and along the Detroit River (Tables 2–4) were compared to the “Guidelines for the Protection and Management of Aquatic Sediment Quality in Ontario’ developed by the Ontario Ministry of the Environment (OMOE, 1992). Many of the sediment sites sampled in the current study had contaminant levels above the “Severe Effect Level Guideline” as developed by the OMOE (see Table 4). HH1 in Hamilton Harbour, had high levels of Fe, Mn, and Zn. At HH2, Cd, Cu, Fe, Mn, Ni, Pb, Zn, and As were extensive, while high levels of Cu, Fe, Pb, and Zn were observed at HH4 in Hamilton Harbour. Chemical analysis at various sites along the Detroit River were examined, with DR1
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Table 4 PAHs (ng g 21) in Detroit River and Hamilton Harbour during 1992 (data from McCarthy 1994)
Total PAHs Naphthalene Acenaphthylene Acenaphthene Fluorene Phenanthrene Anthracene Fluoranthene Pyrene Benzo(a)anthracene Chrysene Benzo(b)fluorene Benzo(k)fluoranthene Benzo(a)pyrene Dibenzo(a,h)anthracene Indeno(1,2,3-c,d)pyrene Benzo(g,h,i)perylene
Hamilton Harbour Station 2
Detroit River Trenton C. 6
Trenton C. 4.
Rouge R.
458 696 222 522 250 3225 11 305 44 460 11 730 49 140 35 980 16 330 10 210 12 070 10 620 12 770 1784 8304 7996
2358 102 ND ND ND 142 67 286 312 208 231 248 221 236 ND 150 155
32 959 320 14 174 364 3484 652 7571 6684 2023 2008 2319 2002 18 868 285 1672 1519
73624 1614 ND 90 135 5387 1975 10210 10190 6453 6266 5903 6852 7075 515 5647 5312
having only slightly elevated levels of Cd, Fe, and Hg compared to the OMOE sediment guidelines. On the other hand DR6 and DR7, at the mouth of the Rouge River, had higher levels of PCBs than DR1. Overwhelmingly, the most toxic sediment proved to be that originating from DR7 at the mouth of the Rouge River. Chemical analysis indicated various concentrations of PAHs, PCBs, and metals, which may have contributed to the observed toxicity. Several studies have been conducted to assess the toxicity of Hamilton Harbour sediments, in particular Krantzberg and Boyd (1992) noted that sediments from many sites in the Harbour exceeded sediment quality guidelines and implicated metals as contributing the most to the toxicity. The variable sensitivities noted for the organisms reinforces the need to utilize a suite of aquatic biota to assess toxicity potential of contaminated sediment. The abilities differ amongst the species to decontaminate, sequester, or simply not take up chemical compounds present in the sediment. In this suite L. variegatus was obviously able to avoid contaminant insult to a greater degree than H. azteca. Whether the integument of the oligochaete contributes to this advantage or it is less sensitive to the mix of metals and organics present is difficult to discern, but future
studies must also examine body burdens to assess bioaccumulation and routes of exposure. In summary, bioassessment of an array of contaminated sites in a lentic (Hamilton Harbour) and lotic (Detroit River) ecosystem revealed interesting and useful information by using a multi-trophic suite of bioassays. The toxicity in lotic ecosystem such as Detroit River was borne in both the bottom and mobile suspended seston component. Conversely, the lentic and undisturbed habitat like Hamilton Harbour bulk of its toxicity was contained in the bottom sediments. Organisms will be variably sensitive to different chemicals under different conditions is also inherently obvious. Where there is gross chemical contamination and enormous acute toxicity, there is little difference noted between the sensitivities of different species. For example the assays were consistent in determining the most toxic “hot spots”. On the other hand the tests showed considerable variability in their sensitivities to discriminate among less contaminated sites. In any case our study re-emphasizes that the ultimate bioavailability of contaminants from sediments can only be truly assessed with living systems, and not through bulk chemical characterization. Furthermore the use of a suite of multi-trophic
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aquatic organisms to assess the real and potential toxicity of sediment is with out doubt, an essential bioassessment tool. Although the battery of multitrophic tests approach appear to be effective in detecting and discriminating differential toxicity commonly observed in natural environments, it needs continued modification, improvement and up dating to meet growing demands of increasing contamination and the fast-growing ecotechnology. Acknowledgements We sincerely thank Drs Renato Baudo and Sharon Lawrence for the constructive criticism of the manuscript which greatly improved its presentation. The technical editing of I.F. Munawar is also gratefully acknowledged. Thanks are also due to Warren Norwood for his assistance and help in conducting the Hyalella assays. References Borgmann, U., Munawar, M., 1989. A new standardized sediment bioassay protocol using the amphipod Hyalella azteca (Saussure). In: Munawar, M., Dixon, G., Mayfield, C.I., Reynoldson, T., Sadar, M.H. (Eds.). Environmental Bioassays Techniques and Their Application, Hydrobiologia, 188/189. Kluwer, Dordrecht, pp. 425–531. Borgmann, U., Ralph, K.M., Norwood, W.P., 1989. Toxicity test procedures for Hyalella azteca, and chronic toxicity of cadmium and pentachlorophenol to H. azteca, Gammarus faciatus, and Daphnia magna. Arch. Environ. Contam. Toxicol. 18, 756–764. Burton Jr., G.A., Nelson, M.K., Ingersoll, C.G., 1992. Freshwater benthic toxicity tests. In: Burton Jr., G.A. (Ed.). Sediment Toxicity Assessment, Lewis, London, pp. 213–240. Cairns Jr., J., Cherry, D.S., 1993. Freshwater multispecies test systems. In: Calow, P. (Ed.). Handbook of Ecotoxicology, 1. Blackwell, Oxford, pp. 101–116. Calow, P., 1993. General principals and overview. In: Calow, P. (Ed.). Handbook of Ecotoxicology, 1. Blackwell, Oxford, p. 15. Chapman, P.M., Farrell, M.A., Brinkhurst, R.O., 1982. Relative tolerances of selected aquatic oligochaetes to combinations of pollutants and environmental factors. Aquat. Toxicol. 2, 6978. Dermott, R., Munawar, M., 1992. A simple and sensitive assay for evaluation of sediment toxicity using Lumbriculus variegatus (Muller). Hydrobiologia 235/236, 407–414. Environment Canada, 1995. Manual of Analytical Methods: Major Ions and Nutrients, 1. N.W.R.I. Water Quality Branch, Ottawa, Ontario, p. 340. Foran, J.A., 1990. Toxic substances in surface water. Environ. Sci. Technol. 4 (5), 604–608.
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Forbes, T.L., Forbes, V.E., Giessing, A., Hansen, R., Kure, L.K., 1998. Relative role of pore water versus ingested sediment in bioavailability of organic contaminants in marine sediment. Environ. Toxicol. Chem. 17 (12), 2453–2462. Giesy, J.P., Hoke, R.A., 1989. Freshwater sediment toxicity bioassessment: rationale for species selection and test design. J. Great Lakes Res. 15 (4), 539–569. Hodson, P.V., Ross, C.W., Niimi, A.J., Spry, D.J., 1977. Statistical considerations in planning aquatic bioassays. Proc. Third Aquatic Toxicity Workshop. Environmental Protection Service., 15–31 EPS-5-AR-777-1. Hoke, R.A., Ankley, G.T., Cotter, A.M., Goldenstein, T., Kosian, P.A., Phipps, G.L., Vander Meiden, F.M., 1994. Evaluation of equilibrium partitioning theory for predicting acute toxicity of fieldcollected sediments contaminated with DDT, DDE and DDE to the amphipod Hyalella azteca. Environ. Toxicol. Chem. 13, 157–166. IJC, 1989. International Joint Commission. Progress in developing and implementing remedial action plans for areas of concern in the Great Lakes Basin, 1989. Report on Great Lakes Quality, Appendix A. Great Lakes Quality Board Report to the International Joint Commission, p. 196. IJC, 1993. A strategy for virtual elimination of persistent toxic substances, vol. 2. Seven Reports to the Virtual Elimination Task Force, August 1993, p. 112. Jackson, M., Milne, J., Johnston, H., Dermott, R., 1995. Assays of Hamilton Harbour sediments using Diporeia hoyi (Amphipoda) and Chironomus plumosus (Diptera), Canadian Technical Report of Fisheries and Aquatic Sciences. No. 2039, pp. 1–20. Keilty, T.J., White, D.S., Landrum, P.F., 1988. Shortterm lethality and sediment avoidance assays with endrincontaminated sediment and two oligochaetes from Lake Michigan. Arch. Environ. Contain. Toxicol. 17, 95–101. Krantzberg, G., Boyd, D., 1992. The biological significance of contaminants in sediment from Hamilton Harbour, Lake Ontario. Environ. Toxicol. Chem. 11 (11), 1527–1540. McCarthy, L.H., 1994. A study of the toxicity of Great Lakes sediment on aquatic organisms. PhD Thesis, University of Waterloo, Waterloo, Ontario, Canada, 247 pp. Munawar, M., Munawar, I.F., Mayfield, C.I., McCarthy, L.H., 1989. Probing ecosystem health: a multidisciplinary and multitrophic assay strategy. In: Munawar, M., Dixon, G., Mayfield, C.I., Reynoldson, T., Sadar, M.H. (Eds.). Environmental Bioassay Techniques and Their Application, Hydrobiologia, 188/189. Kluwer Academic, Dordrecht, pp. 93–116. Munawar, M., Munawar, I.F., McCarthy, L., Page, W., Gilron, G., 1993. Assessing the impact of sewage effluent on the ecosystem health of the Toronto Waterfront (Ashbridges Bay), Lake Ontario . J. Ecosys. Health 2, 287–315. Munawar, M., Munawar, I.F., Ross, P., Dermott, R., 1992. Exploring aquatic ecosystem health: a multi-trophic and an ecosysstemic approach. J. Aquatic Ecosys. Health 1, 237–252. Nebeker, A.V., Cairns, M.A., Gakstatter, J.H., Malueg, K.W., Schuytema, G.S., Krawczyk, D.F., 1984. Biological methods for determining toxicity of contaminated freshwater sediments to invertebrates. Environ. Toxicol. Chem. 3, 617–630.
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OMOE, 1992. Ontario Ministry of the Environment. Guidelines for the Protection and Management of Aquatic Sediment Quality in Ontario, June 1992, p. 23. Phipps, G.L., Ankley, G.T., Benoit, D.A., Mattson, V.R., 1993. Use of the oligochaete Lumbriculus variegatus for assessing the toxicity and bioaccumulation of sedimentassociated contaminants. Environ. Toxicol. Chem. 12, 269–279. Suedel, B.C., Rodgers, J.r.J.H., Clifford, P.A., 1993. Bioavailability
of fluoranthene in freshwater sediment toxicity tests. Environ. Toxicol. Chem. 12 (1), 155–165. United States Environmental Protection Agency (USEPA), 1992. Proceedings: Tiered Testing Issues for Freshwater and Marine Sediments. Washington, DC, 16–18 September, p. 547. Weiderholm, T., Weiderholm, A.M., Milbrink, G., 1987. Bulk sediment bioassays with five species of freshwater oligochaetes. Water Air Soil Pollut. 36, 131–154.
A comparative bioassessment of sediment toxicity in lentic and lotic ecosystems of the North American Great Lakes M. Munawar a,*, R. Dermott a, L.H. McCarthy b, S.F. Munawar c, H.A. van Stam a a
Fisheries and Oceans Canada, Great Lakes Laboratory for Fisheries and Aquatic Science, 867 Lakeshore Road. P.O. Box 5050, Burlington, Ontario, Canada L7R 4A6 b Department of Applied Chemical and biological Sciences. Ryerson Polytechnic University, Toronto, Ontario, M5B 2K3 Canada c Aquatic Ecosystem Health and Management Society. P.O. Box 85388 Brant Plaza Postal Outlet, Burlington, Ontario, Canada L7R 4K5
Abstract The bioavailability of sediment bound contaminants in lentic (Hamilton Harbour, Lake Ontario) and lotic (Detroit River connecting Lakes St. Clair and Erie) environments were assessed by a battery of multi-trophic tests using laboratory grown organisms. Hamilton Harbour is a hyper-eutrophic and highly contaminated environment due to extensive urban and industrial growth, while the Detroit River has been implicated as a major source of contaminants to Lake Erie. An array of sites across Hamilton Harbour and the Detroit River were selected, including the mouth of the Rouge River as well as the Trenton Channel—the contaminated western arm of the Detroit River. Multi-trophic acute assays were conducted using Daphnia magna, Hyalella azteca, Diporeia hoyi, and Lumbriculus variegatus. While the tests were consistent in determining the most toxic hot spots, variability existed in the sensitivities of test organisms to discriminate among less contaminated sites. The most toxic sediment in the Detroit River was at the mouth of the Rouge River, while the site in Windermere Basin in Hamilton harbour was found to be deleterious. The results indicated that the toxicity in a lotic ecosystem such as the Detroit River was caused by both the bottom sediments and the mobile seston component which contributed to the water-borne toxicity. Conversely, lentic and undisturbed ecosystems such as Hamilton Harbour contain much of their toxic component in the bottom sediments and not in the overlying water column. The multi-trophic battery of test approach adopted in our study appears to be effective in detecting and discriminating differential sensitivities of sediment bound contaminants in both lentic and lotic ecosystems. This battery of tests approach needs continued modification, development, and improvement to keep the assays up-to-date, sensitive, cost effective and adaptable in discriminating complex mixtures of sediment bound contaminants found in natural ecosystems. q 1999 Published by Elsevier Science Ltd and AEHMS. All rights reserved. Keywords: Detroit River; Hamilton Harbour; Contaminants; Toxic chemicals; Bioassays
1. Introduction The development of surface water quality guidelines in North America has been extensive, and the regulatory programs of Canada and the United States * Corresponding author. Tel.: 11-905-336-4867; fax: 11-905634-3516. E-mail address: [email protected] (M. Munawar)
have succeeded in mitigating many of the visible effects of pollution, making the water column more habitable for biota (Foran, 1990). However, in marked contrast to the water quality standards which are based on comprehensive toxicological and environmental fate databases, a large amount of research remains to be carried out on the toxicological potential and environmental fate of contaminants in sediments (United States Environmental Protection Agency
1463-4988/99/$20.00 q 1999 Published by Elsevier Science Ltd and AEHMS. All rights reserved. PII: S1463-498 8(99)00057-3
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Table 1 Multi-trophic bioassay protocol Test species
Type of assay
Assay duration
Number of organisms
Number of replicates
Endpoint
Reference
D. magna D. hoyi L. variegatus Hyalella azteca
Acute Acute Acute Acute
48 hours 1 week 2 weeks 1 week
10 5 or 10 10 10
5 5 5 5
Survival Survival Survival Survival
Munawar et al., 1989 Munawar et al., 1989 Dermott and Munawar, 1992 Borgmann and Munawar, 1989
(USEPA) 1992; Hoke et al., 1994). Forbes et al. (1998) report that three factors are primarily responsible for the difficulties in accurately predicting the exposure and bioavailability of organic contaminants in sediment to aquatic biota: (1) the complex geochemistry of sediment makes understanding chemical speciation and kinetics difficult; (2) aquatic organisms interact with the sediment in a myriad of ways, influencing contaminant fate and their own exposure to the pollutants; (3) biological variability is substantial due to numerous biochemical responses that occur once the contaminant has entered the organism, making simple assumptions based on sediment contaminant analysis difficult. Although recently attempts have been made to assess the potential hazard of contaminated sediment using biological systems, there is a tendency to assume toxicity based on bulk chemical characterizations. Also, the majority of studies utilize single organisms in an attempt to represent the entire aquatic food chain. This has led to the establishment of simple cause–effect relationships between chemical concentrations and easily observable biological impact on a single organism, often to the exclusion of less readily measured interactions, and extrapolating throughout the entire aquatic food web. Excellent reviews by Giesy and Hoke (1989), Munawar et al. (1989), USEPA (1992), Calow (1993) and Cairns and Cherry (1993) have been published suggesting the use of a suite of aquatic organisms to assess sediment toxicity. But few studies have incorporated a multi-trophic battery of tests to assess sediment toxicity in the Great Lakes (Munawar et al., 1992, 1993). Moreover, while the database on water pollution in the Great Lakes is enormous, there is still a lack of information linking sediment contamination with impact on aquatic organisms. Forty-two pollution “hot-spots” or areas of concern
exist in the North American Great Lakes areas (IJC, 1989; Hartig and Zarull, 1992). The current study assessed two such areas in detail, one a lentic ecosystem and the other a lotic environment. The lentic environment was Hamilton Harbour, an enclosed bay located at the western end of Lake Ontario. This area has the largest iron and steel industrial complex in Canada. Its sediments contain significant concentrations of heavy metals, PAHs, and PCBs, which are responsible for Hamilton Harbour having 11 out of 14 beneficial use impairments (IJC, 1993). The lotic ecosystem was the Detroit River connecting Lake St. Clair to Lake Erie, and is the international boundary between Michigan and Ontario. It has been implicated as a major source of PCBs to Lake Erie and is the single most important source of mercury. The Detroit River has 8 out of 14 possible beneficial uses impaired, including restrictions on drinking water, fish and wildlife consumption, fish tumours and loss of fish and wildlife habitat (IJC, 1993). Of particular interest was the western portion of the River known as the Trenton Channel. The highest contamination of sediment with heavy metals of the entire Detroit River system has been reported in this waterway (McCarthy, 1994). The largest tributary entering the Detroit River is the Rouge River which flows through the industrial areas on the Michigan side. This area was identified as an Area of Concern because 64 km of the Rouge River do not meet Michigan’s water quality standards. Also, the sediments are highly contaminated with cadmium, copper, lead, mercury, nickel, zinc, and PCBs (IJC, 1993). Thus, the purpose of the current study was to examine the bioavailability of pollutants from contaminated sediment using a multi-trophic battery of aquatic organisms as assessors of toxic potential. The assays incorporated the zooplankter Daphnia
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Fig. 1. Sites sampled, Detroit River and Hamilton Harbour.
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magna, the benthic amphipods Hyalella azteca and Diporeia hoyi, and the aquatic oligochaete Lumbriculus variegatus. The endpoint measured was mortality (Table 1).
2. Materials and methods 2.1. Sampling Sampling was carried out at selected sites in Hamilton Harbour, Detroit River–Rouge River in various seasons and years. Sampling was not carried out in areas where currents were obvious. Also, sediment type of choice was either silt or clay, if the substrate appeared too sandy or gravely, that site was not used. Most sampling was carried out using a Shipek sampler from a small, 16-foot boat, which caused little resuspension of the sediment during retrieval. Water overlaying the sediment was removed by siphon and discarded. The top 10 cm of sediment from each of the three replicate samples was removed and mixed together in clean 5 l polyethylene pails. The sediment was placed into clear, polypropylene bags, and kept in coolers, then refrigerated at 48C in the laboratory until they were used for bioassays. In Hamilton Harbour the samples were collected during April and October 1990 which included four stations of varying contamination (Fig. 1). HH1 and HH6 were furthest from industrial areas but close to inflow areas where pesticides may be present. HH4 in Windermere Basin has a history of pollution problems and HH2 is in close proximity to the western dock of a major steel mill. During August 1989 the Detroit River (mouth of Rouge River) was sampled at DR7 (Fig. 1) and at two sites downstream (DR6, off Great Lakes Steel Corporation and DR1, Trenton Channel at Monanto). In July 1992, additional sites were sampled. Sediment was also collected at RR1 and RR3 upstream on the Rouge River, and three more sites on the Detroit River; DR35 and DR34, which are downstream of the Rouge River mouth and an upstream site, DR23. A reference site from mid Lake Erie was used for the Detroit River samples and in mid Lake Ontario for the Hamilton Harbour sediments.
2.2. Daphnia magna cultures The culturing of D. magna is detailed in Munawar et al. (1989) which is a modified version of the method described by Nebeker et al. (1984). The daphnids were cultivated in large, oxygenated tanks in dechlorinated tap water (from Lake Ontario) under controlled conditions with temperatures of < 218C and a photoperiod of 16 h light: 8 h dark. The animals received three feedings weekly of Tetra-Minq fish food. The day before testing, mature females were removed from the stock culture and placed in breeding tanks. On the day of testing, neonates (animals less than 24 h old) were removed and used as test organisms. 2.3. Acute Daphnia magna bioassays Experimental assays in the current study included the following test protocols outlined in Munawar et al. (1989). 10 daphnid neonates were placed in five randomly arranged 250 ml zooplankton jars containing either 200 ml of integrated sample site water (1–10 m) or reference water. Temperature was maintained at 218C, with a photoperiod regime of 16 h light: 8 h dark. Oxygen was measured before animals were added and once during the bioassay. After 48 h, survivors were enumerated. 2.4. Hyalella azteca cultures The protocol is detailed in Borgmann and Munawar (1989) and Borgmann et al. (1989). Amphipod cultures were maintained in straight-sided glass jars with pieces of surgical bandage-type cotton gauze and dechlorinated tap water and fed Tetra-minq fish food flakes several times weekly. The animals were separated according to age (0–1 week), and kept in separate culturing jars before use in bioassays. 2.5. Acute Hyalella azteca solid phase bioassays The protocol is adapted from Borgmann and Munawar (1989) for use with a smaller amount of sediment. 10 young (less than seven days) animals were exposed to test sediments for seven days at 20–228C, 16 h light: 8 h dark. The H. azteca were obtained from laboratory cultures. Approximately 50 ml of sediment was added to each of five glass beakers containing 200 ml of dechlorinated tap water. Individual air lines were added to each beaker to gently oxygenate without disturbing the sediment. Dechlorinated water was added as needed to keep the
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water level constant. H. azteca were fed Tetra-Minq fish flakes twice. After one week the sediments were sifted through a 275 mm nylon screen and the surviving amphipods were sorted and counted.
Any ‘wild’ tubificid worms or their fragments that were mistakenly counted and weighed before preservation were identified and the final counts were corrected (Dermott and Munawar, 1992).
2.6. Lumbriculus variegatus cultures L. variegatus were purchased from aquaria wholesalers and maintained at 208C in 40 l aquaria on fine 100 mm silicon sand. The water was aerated with a slow water exchange of about one volume per day and the worms were fed commercial trout food pellets once a week. Detailed methodology is given in Dermott and Munawar (1992).
2.8. Acute Diporeia hoyi solid phase bioassay
2.7. Chronic Lumbriculus variegatus solid phase bioassay Unsieved mud (20 ml) was spooned into 100 ml jars resulting in a sediment layer of about 2 cm. Mud was allowed to settle overnight at 20–228C while the surface oxidized under 1 mm of surface water. The jars were gently filled with dechlorinated water to minimize the disturbance of the surface sediment. Ten L. variegatus of similar size were added to each jar using a pipette. The jars were submerged uncovered about 2 cm below the water surface in 10 l aquaria containing 5 l of dechlorinated water. Individual aquaria were used for each test sediment for which five replicates were done. Water in the aquaria was aerated and O2 concentration was measured after 48 h. After exposure for two weeks under a 16 h light: 8 h dark photoperiod, the sediment was gently sieved through a 200 mm mesh screen, and the surviving worms were back-washed onto a white pan and counted. Due to the escape behaviour of L. variegatus when disturbed, the healthy animals could be separated from any Tubificidae or Stylodrilus that may have been present in the tested sediment. The latter worms become tightly coiled when disturbed. At the end of the assay, worms were transferred into labeled vials and preserved by adding 4% formalin. Within 24 h, the worms and fragments were examined under a dissecting microscope for the occurrence of a prostomium (anterior end or ‘head’). Only those worms with a complete or developing prostomium were counted. This is necessary in order to determine if any increase in number was due to reproduction by architomic division (asexual reproduction by budding) and not fragmentation during the screening.
Due to the lower temperature tolerance of D. hoyi this amphipod assay was maintained at 108C and exposure to test sediments was for only one week in the dark. D. hoyi were collected using an Ekman grab from the profundal zone of Lake Ontario and held in 40 l aquaria containing sediment from the collection site for a period of one week to two months before use. Because of the difficulty in obtaining healthy animals during mid summer, only five animals were added to each replicate, giving the minimum statistical requirement of five replicates each with five animals (Hodson et al., 1977). D. hoyi were removed from the holding aquaria using the same method as L. variegatus, however D. hoyi were kept submerged during transfers to ensure that air was not trapped under their coxal plates. After the addition of the animals to the jars, a cover of 0.5 mm mesh gauze was held over the jar with an elastic band. This was necessary to keep the amphipods away from the water surface and to prevent them from leaving the jars. The jars were then submerged in aquaria around an air bubbler to create a current between the jars and the water surface 2 cm above the jars (Jackson et al., 1995). 2.9. Chemical analysis Background chemistry information was obtained from various sources for the two ecosystems known for their pollution. Chemical analysis was performed by the National Laboratory for Environmental Testing, (Environment Canada, 1995) on sediments collected during June 1989 in Hamilton Harbour and August and September 1989 in the Detroit River. PAH data is obtained from McCarthy (1994) for Hamilton Harbour, Detroit and Rouge Rivers collected during 1992. 3. Results and discussion The purpose of the current study was to assess the impact of contaminated sediment from a lentic and a
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Fig. 2. Multi-trophic bioassay results, Hamilton Harbour April 1990, N 10 individuals per replicate for all organisms except for D. hoyi N 5. Bars indicate standard deviation.
lotic environment of the North American Great Lakes with a multi-trophic battery of aquatic organisms. These organisms were known for their sensitivities to a variety of anthropogenic chemicals. While daphnids are not benthic, their propensity for inhabiting the sediment-water interface makes them a useful indicator of sediment toxicity. They feed at the surface of sediments and come into intimate contact with particulate-bound toxicants (Suedel et al. 1993). The benthic amphipods are important components of the sediment community and form a major diet item of bottom-feeding fish (Borgmann et al., 1989). The USEPA (1992) reported that H. azteca were as sensitive as Hexagenia to impacts of various
sediment compounds, and more sensitive than Chironomus. Burton et al. (1992) reported that in 7–14 days whole sediment exposure assays, tests with H. azteca had proven to be some of the most sensitive and discriminatory of 20 different sediment toxicity assays utilizing contaminated sediments from the Great Lakes. The authors highly recommended these organisms as a tool to measure sediment toxicity. The use of L. variegatus in sediment toxicity testing has been widely reported (Chapman et al. 1982; Weiderholm et al., 1987; Keilty et al., 1988). Phipps et al. (1993) suggested that the aquatic oligochaete was an ecologically relevant component of aquatic ecosystems being exposed intimately to
Fig. 3. Multi-trophic bioassay results, Hamilton Harbour October 1990, N 10 individuals per replicate for all organisms except for D. hoyi N 5. Bars indicate standard deviation.
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Fig. 4. Multi-trophic bioassay results, Detroit and Rouge Rivers, August 1989, N 10 individuals per replicate for all organisms except for D. hoyi N 5. Bars indicate standard deviation.
contaminants in the sediment; thus was a suitable bioassay organism. Overall, the four organisms used in the current study were suitable test organisms, in accordance with Giesy and Hoke (1989) and Munawar et al. (1989). The bioassays were rapid, relatively inexpensive, and standardized to facilitate widespread use, while the organisms were easy to culture and use at any time, the response of the control organism was predictable and replicable, and ecologically relevant. In April 1990, the Hamilton Harbour bioassays were conducted using D. magna, H. azteca, D. hoyi and L. variegatus, (Fig. 2). Differential sensitivity was shown by all species. H. azteca were sensitive to many contaminated sites, especially HH4. L. variegatus was
only sensitive to the highly contaminated HH4. D. hoyi and D. magna were not significantly sensitive to any sites. D. magna‘s insensitivity suggests that a mobile seston component is not a significant cause of toxicity in Hamilton Harbour. A differential response of test organisms was shown to different conditions and mixtures of heavy metals and organics. In October 1990, the Hamilton Harbour bioassays were again run using H. azteca, D. hoyi and L. variegatus, and (Fig. 3). Again differential sensitivities were shown by all species. H. azteca and D. hoyi did not show significant differences in sensitivity and were not sensitive to contaminated sites. L. variegatus were only sensitive to highly contaminated HH4, while reproducing in the
Fig. 5. Multi-trophic bioassay results, Detroit (DR) and Rouge Rivers (RR), July 1992, N 10 individuals per replicate for all organisms. Bars indicate standard deviation.
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Table 2 Inorganic sediment chemistry analysis. Detroit River and Hamilton Harbour at selected stations during 1989. (SEL: Severe Effects Level (Bold), LEL: Lowest Effects Level (italics) (Persaud et al., 1993). ND, not determined; na, not available) Detroit River, September 1989 Compound (mg kg 21) DR1
DR6
DR7
LEL
SEL
Al Cd Co Cu Fe Mn Ni Pb Zn As Se Hg Inorganic P Total P %C %N
27300 5.03 13.7 159 134000 1730 135 223 788 8.8 1 0.56 1826 1860 3.1 0.12
50000 5.23 13.3 124 343000 523 51 163 457 10.6 0.8 0.65 935 1080 8.33 0.47
na 0.6 na 16 20000 460 16 31 120 6 na 0.2 na 600 1 na
na 10 na 110 40000 1100 75 250 820 33 na 2 na 2000 10 na
Hamilton Harbour, June 1989 Compound (mg kg 21) HH1
HH2
HH4
LEL
SEL
Al Cd Co Cu Fe Mn Ni Pb Zn As Se Hg Inorganic P Total P
50600 11.3 33.3 185 80000 2980 96.1 529 4790 42.3 8.8 0.9 3790 4120
53800 4 32 193 49400 1020 68.7 256 1240 12.3 8.1 0.62 3720 4220
na 0.6 na 16 20000 460 16 31 120 6 na 0.2 na 600
na 10 na 110 40000 1100 75 250 820 33 na 2 na 2000
33500 11.3 12.4 164 43400 554 58 161 442 12.8 1.1 2.27 880 914 7.54 0.39
53300 4.8 32.4 107 50400 1740 74.4 235 1870 21.4 4.7 0.42 2260 2630
sediments of HH2. The differential response seen was likely due to different conditions and mixtures of heavy metals and organics at each site affecting their bioavailability. In August 1989, the Detroit River bioassays were conducted using D. magna, H. azteca, and D. hoyi (Fig. 4). Differential sensitivities were expressed by all species. While DR6 (Great Lakes Steel Corporation) and DR7 (Mouth of Rouge River) on the Detroit River, located downstream of highly contaminated Rouge River, were toxic to all three species, H. azteca
was more sensitive to contaminated sediment than the other amphipod D. hoyi. Unlike Hamilton Harbour where there was no impact on D. magna, sites on the two rivers were toxic to this water column organism. This suggests that toxicity in a flowing ecosystem such as a river is not only caused by stationary bottom sediments, but also by the mobile seston component. In July 1992, the Detroit River bioassays were conducted again with H. azteca and L. variegatus (Fig. 5). Differential sensitivities were shown by
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Table 3 Organic contaminants in Detroit River and Hamilton Harbour at selected stations during 1989. (SEL, Severe Effects Level (Bold); LEL, Lowest Effects Level (Italics) (Persaud et al. 1993); ND, not determined; na, not available) Detroit River, August 1989 Compound (mg kg 21)
DR1
DR6
DR7
LEL
SEL
HCB G-Chlor A-Chlor p,p 0 -DDE Dieldrin Endrin p,p 0 -TDE o,p-DDT p,p-DD Mirex Total PCB
ND 0.003 0.003 0.023 0.001 ND 0.02 N.D N.D ND 1.732
0.005 0.002 0.003 0.087 0.002 ND 0.089 ND ND ND 3.56
0.005 0.007 0.008 0.049 0.003 ND 0.069 0.001 ND ND 2.726
0.02 na na 0.005 0.002 0.003 na na na 0.007 0.07
24 na na 19 91 130 na na na 130 530
Hamilton Harbour, June 1989 Compound (mg kg 21)
HH2
HH3
HH4
HH6
LEL
SEL
HCB G-Chlor A-Chlor p,p 0 -DDE Dieldrin Endrin p,p 0 -TDE o,p-DDT p,p-DDT Mirex Total PCB
0.0004 0.0072 0.0018 0.006 ND ND 0.0035 ND ND ND 0.5127
0.0002 0.0081 0.0007 0.0027 0.0003 ND 0.0018 ND ND ND 0.3693
0.0002 0.0373 0.001 0.0037 0.0002 ND 0.0016 ND 0.0003 ND 0.752
N.D 0.0006 0.0003 0.001 ND ND 0.0008 ND ND ND 0.0594
0.02 na na 0.005 0.002 0.003 na na na 0.007 0.07
24 na na 19 91 130 na na na 130 530
both species. While the sites on Detroit River downstream of the highly contaminated Rouge River were toxic to H. azteca, L. variegatus was insensitive to contaminated sediment. The trend of impact noted with H. azteca indicates a gradient of increasing toxicity from north of the Rouge River to the highly polluted Trenton Channel in the southern portion of Detroit River. During July 1992, bioassays were also conducted with the Rouge River sediments using H. azteca and L. variegatus (Fig. 5). These species showed differential sensitivity to the test sediments. Rouge River sites RR1 and RR3 are considered to be the most toxic hot spots where the highest concentrations of organic and inorganic contaminants were observed. Interestingly L. variegatus still appeared to be indifferent to such high levels of contaminants. Conversely, H. azteca
were practically eliminated by the end of the experiment. The background chemistry results on the sediments from the various sites in Hamilton Harbour and along the Detroit River (Tables 2–4) were compared to the “Guidelines for the Protection and Management of Aquatic Sediment Quality in Ontario’ developed by the Ontario Ministry of the Environment (OMOE, 1992). Many of the sediment sites sampled in the current study had contaminant levels above the “Severe Effect Level Guideline” as developed by the OMOE (see Table 4). HH1 in Hamilton Harbour, had high levels of Fe, Mn, and Zn. At HH2, Cd, Cu, Fe, Mn, Ni, Pb, Zn, and As were extensive, while high levels of Cu, Fe, Pb, and Zn were observed at HH4 in Hamilton Harbour. Chemical analysis at various sites along the Detroit River were examined, with DR1
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Table 4 PAHs (ng g 21) in Detroit River and Hamilton Harbour during 1992 (data from McCarthy 1994)
Total PAHs Naphthalene Acenaphthylene Acenaphthene Fluorene Phenanthrene Anthracene Fluoranthene Pyrene Benzo(a)anthracene Chrysene Benzo(b)fluorene Benzo(k)fluoranthene Benzo(a)pyrene Dibenzo(a,h)anthracene Indeno(1,2,3-c,d)pyrene Benzo(g,h,i)perylene
Hamilton Harbour Station 2
Detroit River Trenton C. 6
Trenton C. 4.
Rouge R.
458 696 222 522 250 3225 11 305 44 460 11 730 49 140 35 980 16 330 10 210 12 070 10 620 12 770 1784 8304 7996
2358 102 ND ND ND 142 67 286 312 208 231 248 221 236 ND 150 155
32 959 320 14 174 364 3484 652 7571 6684 2023 2008 2319 2002 18 868 285 1672 1519
73624 1614 ND 90 135 5387 1975 10210 10190 6453 6266 5903 6852 7075 515 5647 5312
having only slightly elevated levels of Cd, Fe, and Hg compared to the OMOE sediment guidelines. On the other hand DR6 and DR7, at the mouth of the Rouge River, had higher levels of PCBs than DR1. Overwhelmingly, the most toxic sediment proved to be that originating from DR7 at the mouth of the Rouge River. Chemical analysis indicated various concentrations of PAHs, PCBs, and metals, which may have contributed to the observed toxicity. Several studies have been conducted to assess the toxicity of Hamilton Harbour sediments, in particular Krantzberg and Boyd (1992) noted that sediments from many sites in the Harbour exceeded sediment quality guidelines and implicated metals as contributing the most to the toxicity. The variable sensitivities noted for the organisms reinforces the need to utilize a suite of aquatic biota to assess toxicity potential of contaminated sediment. The abilities differ amongst the species to decontaminate, sequester, or simply not take up chemical compounds present in the sediment. In this suite L. variegatus was obviously able to avoid contaminant insult to a greater degree than H. azteca. Whether the integument of the oligochaete contributes to this advantage or it is less sensitive to the mix of metals and organics present is difficult to discern, but future
studies must also examine body burdens to assess bioaccumulation and routes of exposure. In summary, bioassessment of an array of contaminated sites in a lentic (Hamilton Harbour) and lotic (Detroit River) ecosystem revealed interesting and useful information by using a multi-trophic suite of bioassays. The toxicity in lotic ecosystem such as Detroit River was borne in both the bottom and mobile suspended seston component. Conversely, the lentic and undisturbed habitat like Hamilton Harbour bulk of its toxicity was contained in the bottom sediments. Organisms will be variably sensitive to different chemicals under different conditions is also inherently obvious. Where there is gross chemical contamination and enormous acute toxicity, there is little difference noted between the sensitivities of different species. For example the assays were consistent in determining the most toxic “hot spots”. On the other hand the tests showed considerable variability in their sensitivities to discriminate among less contaminated sites. In any case our study re-emphasizes that the ultimate bioavailability of contaminants from sediments can only be truly assessed with living systems, and not through bulk chemical characterization. Furthermore the use of a suite of multi-trophic
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aquatic organisms to assess the real and potential toxicity of sediment is with out doubt, an essential bioassessment tool. Although the battery of multitrophic tests approach appear to be effective in detecting and discriminating differential toxicity commonly observed in natural environments, it needs continued modification, improvement and up dating to meet growing demands of increasing contamination and the fast-growing ecotechnology. Acknowledgements We sincerely thank Drs Renato Baudo and Sharon Lawrence for the constructive criticism of the manuscript which greatly improved its presentation. The technical editing of I.F. Munawar is also gratefully acknowledged. Thanks are also due to Warren Norwood for his assistance and help in conducting the Hyalella assays. References Borgmann, U., Munawar, M., 1989. A new standardized sediment bioassay protocol using the amphipod Hyalella azteca (Saussure). In: Munawar, M., Dixon, G., Mayfield, C.I., Reynoldson, T., Sadar, M.H. (Eds.). Environmental Bioassays Techniques and Their Application, Hydrobiologia, 188/189. Kluwer, Dordrecht, pp. 425–531. Borgmann, U., Ralph, K.M., Norwood, W.P., 1989. Toxicity test procedures for Hyalella azteca, and chronic toxicity of cadmium and pentachlorophenol to H. azteca, Gammarus faciatus, and Daphnia magna. Arch. Environ. Contam. Toxicol. 18, 756–764. Burton Jr., G.A., Nelson, M.K., Ingersoll, C.G., 1992. Freshwater benthic toxicity tests. In: Burton Jr., G.A. (Ed.). Sediment Toxicity Assessment, Lewis, London, pp. 213–240. Cairns Jr., J., Cherry, D.S., 1993. Freshwater multispecies test systems. In: Calow, P. (Ed.). Handbook of Ecotoxicology, 1. Blackwell, Oxford, pp. 101–116. Calow, P., 1993. General principals and overview. In: Calow, P. (Ed.). Handbook of Ecotoxicology, 1. Blackwell, Oxford, p. 15. Chapman, P.M., Farrell, M.A., Brinkhurst, R.O., 1982. Relative tolerances of selected aquatic oligochaetes to combinations of pollutants and environmental factors. Aquat. Toxicol. 2, 6978. Dermott, R., Munawar, M., 1992. A simple and sensitive assay for evaluation of sediment toxicity using Lumbriculus variegatus (Muller). Hydrobiologia 235/236, 407–414. Environment Canada, 1995. Manual of Analytical Methods: Major Ions and Nutrients, 1. N.W.R.I. Water Quality Branch, Ottawa, Ontario, p. 340. Foran, J.A., 1990. Toxic substances in surface water. Environ. Sci. Technol. 4 (5), 604–608.
377
Forbes, T.L., Forbes, V.E., Giessing, A., Hansen, R., Kure, L.K., 1998. Relative role of pore water versus ingested sediment in bioavailability of organic contaminants in marine sediment. Environ. Toxicol. Chem. 17 (12), 2453–2462. Giesy, J.P., Hoke, R.A., 1989. Freshwater sediment toxicity bioassessment: rationale for species selection and test design. J. Great Lakes Res. 15 (4), 539–569. Hodson, P.V., Ross, C.W., Niimi, A.J., Spry, D.J., 1977. Statistical considerations in planning aquatic bioassays. Proc. Third Aquatic Toxicity Workshop. Environmental Protection Service., 15–31 EPS-5-AR-777-1. Hoke, R.A., Ankley, G.T., Cotter, A.M., Goldenstein, T., Kosian, P.A., Phipps, G.L., Vander Meiden, F.M., 1994. Evaluation of equilibrium partitioning theory for predicting acute toxicity of fieldcollected sediments contaminated with DDT, DDE and DDE to the amphipod Hyalella azteca. Environ. Toxicol. Chem. 13, 157–166. IJC, 1989. International Joint Commission. Progress in developing and implementing remedial action plans for areas of concern in the Great Lakes Basin, 1989. Report on Great Lakes Quality, Appendix A. Great Lakes Quality Board Report to the International Joint Commission, p. 196. IJC, 1993. A strategy for virtual elimination of persistent toxic substances, vol. 2. Seven Reports to the Virtual Elimination Task Force, August 1993, p. 112. Jackson, M., Milne, J., Johnston, H., Dermott, R., 1995. Assays of Hamilton Harbour sediments using Diporeia hoyi (Amphipoda) and Chironomus plumosus (Diptera), Canadian Technical Report of Fisheries and Aquatic Sciences. No. 2039, pp. 1–20. Keilty, T.J., White, D.S., Landrum, P.F., 1988. Shortterm lethality and sediment avoidance assays with endrincontaminated sediment and two oligochaetes from Lake Michigan. Arch. Environ. Contain. Toxicol. 17, 95–101. Krantzberg, G., Boyd, D., 1992. The biological significance of contaminants in sediment from Hamilton Harbour, Lake Ontario. Environ. Toxicol. Chem. 11 (11), 1527–1540. McCarthy, L.H., 1994. A study of the toxicity of Great Lakes sediment on aquatic organisms. PhD Thesis, University of Waterloo, Waterloo, Ontario, Canada, 247 pp. Munawar, M., Munawar, I.F., Mayfield, C.I., McCarthy, L.H., 1989. Probing ecosystem health: a multidisciplinary and multitrophic assay strategy. In: Munawar, M., Dixon, G., Mayfield, C.I., Reynoldson, T., Sadar, M.H. (Eds.). Environmental Bioassay Techniques and Their Application, Hydrobiologia, 188/189. Kluwer Academic, Dordrecht, pp. 93–116. Munawar, M., Munawar, I.F., McCarthy, L., Page, W., Gilron, G., 1993. Assessing the impact of sewage effluent on the ecosystem health of the Toronto Waterfront (Ashbridges Bay), Lake Ontario . J. Ecosys. Health 2, 287–315. Munawar, M., Munawar, I.F., Ross, P., Dermott, R., 1992. Exploring aquatic ecosystem health: a multi-trophic and an ecosysstemic approach. J. Aquatic Ecosys. Health 1, 237–252. Nebeker, A.V., Cairns, M.A., Gakstatter, J.H., Malueg, K.W., Schuytema, G.S., Krawczyk, D.F., 1984. Biological methods for determining toxicity of contaminated freshwater sediments to invertebrates. Environ. Toxicol. Chem. 3, 617–630.
378
M. Munawar et al. / Aquatic Ecosystem Health and Management 2 (1999) 367–378
OMOE, 1992. Ontario Ministry of the Environment. Guidelines for the Protection and Management of Aquatic Sediment Quality in Ontario, June 1992, p. 23. Phipps, G.L., Ankley, G.T., Benoit, D.A., Mattson, V.R., 1993. Use of the oligochaete Lumbriculus variegatus for assessing the toxicity and bioaccumulation of sedimentassociated contaminants. Environ. Toxicol. Chem. 12, 269–279. Suedel, B.C., Rodgers, J.r.J.H., Clifford, P.A., 1993. Bioavailability
of fluoranthene in freshwater sediment toxicity tests. Environ. Toxicol. Chem. 12 (1), 155–165. United States Environmental Protection Agency (USEPA), 1992. Proceedings: Tiered Testing Issues for Freshwater and Marine Sediments. Washington, DC, 16–18 September, p. 547. Weiderholm, T., Weiderholm, A.M., Milbrink, G., 1987. Bulk sediment bioassays with five species of freshwater oligochaetes. Water Air Soil Pollut. 36, 131–154.