Haler Research Vol 15. pp. 97 to 105 Pergamon Press Lid 1981. Printed in Greal Britain
01N3-135~.'81]0101-0097502.00,0
EPIPELIC ALGAL COMMUNITIES IN A EUTROPHIC NORTHERN LAKE CONTAMINATED WITH MINE WASTES JAMES W. MOORE Alberta Environmental Centre, Bag 4000, Vegreville, Alberta T0B 4L0. Canada
(Receit:ed June 1980) Abstract--The effects of contaminated bottom sediments on the species composition, growth cycles and diversity of epipelic algal communities were determined between April and November 1978 in a shallow, eutrophic lake (Thompson Lake) situated in the Canadian subarctic. The sediments had become contaminated by gold mining wastes, deposited in the lake between 1941 and 1949. Although the concentrations of total mercury, copper, lead and zinc were high near the mine. averagi/Ig 440 gg kg- 1 and 85. 30 and 115 mg kg-t, respectively, they decreased rapidly beyond this distance and were near background levels 2.1-3.0 km from the mine. The algal communities in the zone of heaviest contamination consisted of 63 species, the most common of which were Anomoeoneis t:itrea, Pinnularia brebissonii and Cymbella species. There were more taxa (111-132) at stations situated 1.1-3.0 km from the mine and the main species included several forms of Achnanthes, Fra#ilaria and Navicula. Although epipelic densities in the zone of heaviest contamination were only about 50°,0 of those recorded at the other stations, the seasonal growth patterns of the flora were generally similar throughout the lake. Based on these data. it is concluded that: (ll Mine wastes may have a long-term impact on epipelic algae in northern environments; (21 The effects of heax~ metal pollution on the epipelon in subarctic lakes are similar to those in temperate zone systems: and (3) No species or group of species could be designated as indicators of heavy metal contamination.
INTRODUCTION
STUDY AREA
Although there have been m a n y studies into the lethal and sublethal characteristics of liquid mine effluents, the responses of most species of aquatic plants to contaminated sediments are still poorly known, particularly under actual field conditions (Whitton. 1970: Cairns et al.. 1972; Patrick et al., 1968; M o o r e & Love, 1977). This is perhaps surprising, considering that sediments act as a sink for most mine wastes (Harding & Whitton. 1978; R a m a m o o r t h y et al., 1977) and hence expose plants to high concentrations of heavy metals. Changes in physico-chemical conditions may further result in the release of contaminants from the substrate, thereby exposing macrophytes, fish and planktonic organisms to pollutants (Schindler et al., 1980al. The scarcity of data on the response of plant communities to pollutants is particular exaggerated in arctic and subarctic lakes, where most mines are located far from biological and chemical laboratories. The purpose of this investigation was therefore to assess the impact of contaminated sediments on the density, species composition and diversity of benthic algal communities in a small lake located in the C a n a d i a n subarctic. The lake had become polluted by mine wastes deposited 30-40 years ago and thus provided an opportunity to determine the long term effects of pollutants on the microflora.
Collections were made monthly from April to November 1978 in Thompson Lake, located at Lat. 6T 37'N, Long 113 + 30'W (Fig. 1). The lake, measuring 3.7 km long and up to 1.0kin wide, has average and maximum depths of 3.1 and 10.0 m respectively. It is situated on the Precambrian Shield, in a region of uninhabited boreal forest near the tree.line, and is accessible only by float plane. Bedrock consists of granite, allied plutonic and altered sedimentary rocks. Bottom deposits throughout the lake are composed almost entirely of organically rich sediments with few if any rocks or patches of gravel. During the study, there were no surface streams flowing into or out of the lake. Gold mining operations began on the south-east shore during 1941 and terminated in 1949. Mill tailings, containing mercury, copper, lead. zinc and other metals, were deposited on shore and in the lake immediateb adjacent to the mine (Fig. 1). These tailings are the only known source of waste in the lake.
W+R 15 1~4.1
MATERIALS AND
METHODS
Benthic algae associated with lake sediments (epipelic algael were collected monthly from 35 stations spaced evenly on a grid throughout the lake (Fig. I). The samples, collected from the upper I cm of substrate using a coring tube (5 cm din) lined with plastic, were immediately preserved in a 1°o Lugol's solution. In the laboratory, algal densities were determined by adding 1 I. of tap water to each sample. The material was shaken vigorously for 30 s and three 0.01 ml aliquots were immediately drawn off. The total number of cells in each aliquot
98
JAMES W. MOOR~
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I km
Fig. 1. Map of Thompson Lake showing collection sites and location of tailings deposits. Insert shows location of study area.
photo-micrographs of 15 specimens of all c o m m o n species were taken at 400-1000 x. The areas of these cells were then determined using an automatic area metre. The average depth of the actual cells was then determined at a magnification of I000 ×, thereby permitting an estimate to be made of cell volume. The concentrations of heavy metals in the sediments were determined from samples collected at the 35 stations during June and July. The mater/al, taken from the upper l cm of substrate with a plastic corer, was frozen at - 2 0 ° C within 3 h of collection. The samples were then digested and analyzed as outlined in Table t. In order to compare the effects of heavy metal contamination on the microflora in different parts of the lake, chemical and algal data for stations 1-17. 18-25, and 26-35 were pooled and are presented in Table 2 and Fig. 2, re. spectively. These three groups of stations are located 0-1.0, 1.1-2.0 and 2.1-3.0kin from the tailings deposits in the lake, where the water has average depths of 1.5, 4.0 and 3.8 m respectively. By combining the data three distinct levels of chemical contamination, which show a progressive decrease moving away from the mine, can be delineated; these changes were in turn used to measure the effects of heavy metals on the flora. This method of presentation also facilitates the analysis of data for a large number of species and pollutants. To obtain background data, sediment samples were also collected from Hidden Lake, situated 2.5 km south of Thompson Lake. The sediments were taken from 6 stations at depths of 1--4 m during July 1978. The methods of collection, preservation, digestion and analysis were identical
to those outlined above. Although Hidden Lake is deeper (maximum depth 45 mk longer (6.0 kin) and wider (4.5 km) than Thompson Lake, they both lie on the same bedrock and are surrounded by uninhabited forests. Water temperature and pH were determined at each station on Thompson Lake using a portable meter (Yellow Springs Instrument Co). Water for chemical analysis was collected monthly from stations 8. 10, 17, 24 and 31 from a depth of 0.5 m using a 4-[ Van Dorn bottle. Samples for total mercury determinations were preserved through the addition of nitric acid and potassium dichromate. Other heavy metals were preserved with nitric acid. while total hardness, phosphorus and NOs-N samples were frozen at - 2 0 ° C within 3 h of collection. Determinations were carried out using the methods outlined in Table 1.
RESULTS
Environmental conditions High mercury concentrations, averaging 4 4 0 ~ g kg-~ dry weight, were recorded in the sedim a t s at stations 1-17, whereas at stations 18-25 and 26-35 the corresponding means were 114 and 1 0 0 # g k g -* (Table 2). Although copper, lead, zinc and nickel also occurred in relatively high concentrations near the mine, concentrations of these metals were much lower at 18-35. O n the other hand, arsenic
Epipelic algal communities
99
Table 1. Methods used in the chemical analysis of sediments and water. (DOE, 1974, 1979) Parameter Total mercury
Total arsenic
Total copper, lead, zinc, cadmium, nickel Total hardness Total mercury, copper. lead. zinc, cadmium, nickel Total arsenic Total phosphorus NO3-N
Method Sediment Digestion in nitric and sulphuric acids followed by elemental reduction with stannous chloride and deterruination by cold vapour atomic absorption spectrometry Fusion with potassium pyrosulfate followed by the addition of hydrochloric acid, treatment with stannous chloride, potassium iodide and mossy zinc, and colour development with brueine and silver diethyldithio-carbamate Digestion in hydrofluoric nitric and hydrochloric acids, followed by analysis by plasma emission spectrometry Water Ethylenediaminetetraacetic acid titration to pH 10.1-10.2 with eriochrome black T indicator. Reported as mg 1- ~ CaCO3 Acidified to pH 2.0--2.1 with concentrated nitric acid and aspirated into an atomic absorption spectrometer Reduction to arsine by zinc in acid solution, followed by colour development with lead acetate and silver diethyldithiocarbamate Colorimetry on an automatic analyzer with ammonmm molybdate and stannous chloride after digestion with H2SO4 and Kz(S04): Colorimetry on an automatic analyzer with a cadmium reduction column and colour development by sulfanilimide and N-(1-napthyl)-ethylene-dmmine dihydrochloride
and cadmium were probably distributed more or less evenly throughout the lake. The concentrations of heavy metals in the sediments of Hidden Lake were either similar to or lower than those recorded at stations 26-35 in the Thompson Lake. Mercury in Hidden Lake averaged t0 #g kg- 1, whereas the means for copper, lead, zinc, arsenic, nickel and cadmium were 17, 15, 45, 2, 20 and < 7 m g k g -1 respectively. Thus, the level of contamination in the sediments at stations 26--35 in Thompson Lake was low and approached the levels in Hidden Lake. Total mercury in the water of Thompson Lake at stations 1-17 was <0.2 gg 1-~ on all occasions except two, when values of 2.5 and 0.5/zg 1- i were recorded in June at stations 8 and I0 (Table 2). Arsenic ranged from 0.002 to 0.040 m g l - 1 while the corresponding values for copper, lead, zinc, nickel and cadmium were <0.02, <0.005--0.035, <0.01-0.04, <0.02 and < 0.002 mg 1-1 respectively. In the other parts of the lake, metal concentrations were generally below detectable limits, regardless of station or date (Table 2). Water temperatures were near 0°C during April and May throughout the lake but increased to 5°C by the first of June and 18°C during the middle of July regardless of depth. Thereafter the water cooled, and began to freeze by the first of October. Total phosphorus varied from a maximum of 0.04-0.07 mg 1- ~ in April and May, to 0.01-0.015 mg 1-1 between June
and September. This was followed by another increase to 0.04-0.06 mg 1-1 in October and November. The concentrations o f NO3-N and total hardness also showed corresponding seasonal fluctuations, ranging from 0.01 to 0.03 and 58 to l l 0 m g 1 - 1 respectively, pH of the water ranged from 6.0 to 6.8 regardless of station or collection period.
Benthic algae There were 192 species of benthic algae found in Thompson Lake, of which 181 were diatoms, 8 were chlorophytes and 3 were cyanophytes (Table 3). Sixty three taxa were recorded within 1.0 km of the mine. while at 1.1-2.0 and 2.1-3.0kin, there were 111 and 132 taxa respectively. The most common species near the mine were Anomeoneis vitrea, Cymbella microcephala, Pinnularia brebissonii, Navicula pupula and Cymbella subaequalis, regardless of month (Fig. 2}. These were much rarer in the intermediate sampling area and were replaced by Fragilaria consrruens, Fragilaria pinnata, Achnanthes microcephala and Achnanthes minutissima. While'all four taxa were equally common at stations 26-35, several other forms such as Navicula cuspidata, Navicula viridula and Mastogloeia smithii, also became important. The pattern of seas6nal succession of the epipelon at stations 1-17 was characterized by low densities in
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JAMESW. MOORE Table 3. List of common epipelic algae collected from the sediments at stations 1-17, 18-25. and 26-35. " + " indicates that the species represented 1.0-10.~ by volume of the population in at least one sample. "4- 4-" indicates that it represented > 10~o by volume of the population in at least one sample Species Achnanthes lanceolata (Br6b.) Grun. Achnanthes linearis (W. Sm.) Grun. Achnanthes microcephala (Kiitz.) Grun. Achnanthes minutissima Kiitz. Amphora ovalis (Kiitz.) Kiitz. Amphora ovalis vat. pediculus (Kiitz.) V. H. Anomoenoneis serians var. brachysira (Br6b. ex Kiitz.) Hust. Anomoeoneis vitrea (Grun.) Ross Caloneis bacillum (Grun.) CI. Cymbella cistula (Hemp.) Kirch. Cymbella diluviana (Krasske) Florin Cymbella microcephala Grun. Cymbella minuta f. latens (Krasske) Reim. Cymbella subaequalis Grun. Epithemia sorex Kiitz. Fragilaria construens (Ehr.) Grun. Fragilaria construens var. renter (Ehr.) Grun, Fra#ilaria pinnata Ehr. Fragilaria pinnata vat. intercedens (Grun,) Hust. Gomphonema acuminatum Ehr. Gomphonema gracile Ehr. Mastogloeia smithii Grun. Navicula bacillum Ehr. Navicula cryptocephala Kiitz. Navicula cuspidata Kiitz. Navicula pupula Kiitz. Navicula pupula vat. capitata Hust, Navicula radiosa vat. parva Wall. Navicula viridula (Kiitz.) Kiitz. Navicula vulpma Kiitz. N eidum aJ)fne (Ehr.) Pfitz. N eidum bisulcatum (Lager.) C1. Niteschia amphibia Grun. Nitzschia angustata vat. antiqua (W.Sm.) Grun, Nitzschia dissipata (Kiitz.) Grun. Nitzschia frustulum (Kiitz.) W. Sm. Pinnularia brebissonii (Kiitz.) Raben. Strauroneis phoenicenteron f. gracilis Diptml.
April and May, followed by a gradual increase in numbers until August (Fig. 2). Thereafter, the population waned and did not show a secondary autumnal peak. The standing stock of epipelon at stations 18-25 was almost twice as large as that at 1-17. The population began waxing in May, peaked near the first of July, and then fluctuated inconsistently until November. Although densities were slightly lower at stations 26-35, the population also expanded in May and peaked in July. Thereafter, algal numbers dropped sharply, followed by a secondary peak in October. There was considerable variability in the seasonal cycles of the main species at the various stations. For example,, Anomoeoneis vitrea reached peak abundance during September at stations 1-17, during July at 18-25 and during August at 26-35. Although a similar inconsistent pattern was recorded for most other spe-
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DISCUSSION
Because Thompson Lake is shallow and isothermal, temperature, pH and nutrient levels are generally similar throughout the lake and consequently would not account for observed differences in the density, diversity and species composition of the epipelon among the various stations. Similarly, the absence of surface streams restricts the differential input of di~ solved substances and, since the shore of the lake is uninhabited, there are no isolated discharges of waste material or nutrients. Hence the low density and number of species at stations 1-17 were almost ccr-
Epip¢lic algal communities
103
tainly related to heavy metal contamination in the 0.4 × 10 9//r/l s cm -2, depending o n location (Moore, sediments. Although there are no detailed studies on 1979, 1980). The relatively high densities near the the mechanisms by which pollutants become available mine can be partially related to the high concen. to the epipelon, it is likely that some metals are trans- trations of phosphorus, NO3-N and total hardness in formed into soluble methylated compounds (Thomas water, all of which would promote rapid growth. In & Jaquet, 1976) which are then absorbed by the epi- addition, since the lake is shallow and relatively pelon. In addition, heavy metals which are not subject warm, light and temperature conditions probably to methylation in the sediments probably desorb into favour strong development. Thus, the populations the water due to low pH conditions (Schindler et al., near the mine were likely partially inhibited by the 1980a) resulting in elevated concentrations of dis- contaminated sediments but, at the same time, were solved metals near the substrate surface and in the stimulated by high nutrient concentrations. It should interstitial waters of the sediments. The high levels of also be pointed out that high total hardness levels in mercury, arsenic and zinc, which were occasionally the water may have reduced the toxicities and thus recorded in the water at stations 1-17 are probably the final impact of most of the pollutants (EPA, 1972). the result of such a desorption process. In addition, since heavy metals often interfere with All of the algal spe~es found near the mine are phosphorus metabolism in algae (Planas & Healey, frequently reported from non-polluted water (Duthie 1978}, high nutrient levels also probably reduced the et al,, 1975: Hickman, 1975: Koivo & Ritchie, 1978) extent of the impact. and are particularly common in lakes in the central The epipelon at stations 1-17 showed several resubarctic (Moore, 1979). The species are typical clean- sponses to heavy metal contamination, including a water forms which, previous to this investigation, change in species dominance and a reduction in have not been associated with mine wastes 0Vhitton, densities and diversity. These shifts occurred despite 1970; Palmer, 1959; Cairns et al., 1972). It is therefore low concentrations of pollutants in water, indicating apparent that none of the taxa could be used as indi- that the relatively low temperatures in Thompson cator species for heavy metal contamination despite Lake did not have a major impact on heavy metal the fact that they grew reasonably well on contami- toxicity. In contrast, temperatures of <10°C are nated sediments. This implies that the indicator spe- known to alter the toxicity of heavy metals (Whitton. cies concept may not be used to assess the extent of 1968: Patrick, 1968). While there appear to be no water pollution in Thompson Lake. Furthermore, differences between temperate and subarctic areas in since virtually all of the species are typical of subarc- the effects of heavy metals on algae, it would be intertic lakes, the indicator-community concept involving esting to assess the influence of high arctic mines these forms is also probably of limited value in this (such as Arvik on Little Cornwallis Island at Latitude study. At present, no information is available on the 76 ° North) on the composition and density of abilities of the main species to survive in contami- attached algal communities. The extreme light and nated water. It is possible that there was a physiologi- temperature conditions at this lattitude may contribcal adaptation to pollutants, as often noted in plankute to a reduction in the toxicity of effluents. tonic algae (Stokes et al., 1973; Stokes, 1975; Moore Although there was some variation, the seasonal et al., 1979b). On the other hand, there are no direct growth curves of the epipelon at stations 1-17, 18-25, measurements of the concentrations of dissolved and 26-35 were generally similar and paralled those metals near the substrate surface, and consequently outlined for non-polluted systems in the arctic and the exact magnitude of chemical contamination is not subarctic. For example, Stanely {1976) showed that known. Furthermore, if desorbed metals near the sub- epipelic algae in tundra ponds in Alaska exhibited strate surface were partially complexed by organic one main peak in numbers in July; similarly, the ligands, a process which wotfld reduce toxicity, many attached algal communities in 21 lakes and streams species would probably survive without adaptation near Thompson Lake waxed in May, reached peak (Sunda & Lewis. 1978). Overall therefore, the study of densities in either July or August, and gradually dethe effects of contaminated sediments on plants is creased in the fall (Moore, 1979). The similarity of complex and requires detailed chemical analysis of growth curves at stations 1-17 with other northern interstitial and surface waters. While these latter de- areas was unexpected, considering the reduction in terminations will be difficult to obtain under field densities and diversity of the epipelon, and indicates conditions, particularly in northern areas, they repthat natural environmental factors, such as temperaresent the only definitive means of explaining environ- ture and light, regulated the seasonal cycles of the mental impact data. flora while high heavy metal levels controlled the The total standing crop of the epipelon at stations population size and species composition of the flora. 1-17 was either similar to or higher than the popula- This mechanism is perhaps analogous to algal develtions found in many other northern waters. For opment in unpolluted lakes, where nutrients also have example, the average summer density of littoral algae little impact on the seasonal development of the epiin 21 lakes and streams in the western arctic averaged peion but control maximum densities during the sumabout 0.5 × 109/~m3cm -2, whereas in Great Slave mer. Lake the corresponding values ranged up to Several environmental agencies, such as the Inter-
104
JAMESW. MOORe
national Joint Commission (1976) and the Environ- Duthie H. C., Ostrofsky M. L. & Sreenivasa M. R. (1975) Freshwater algae from western Lahrador--l. Introducmental Protection Agency (1972), have compiled tion and hacillariophyta. Nova Hedwigia 25, 17-31. water quality objectives which are designed to protect Environmental Protection Agency (1972) Water Quality aquatic biota. Although these recommendations repCriteria, 594 pp. Environmental Protection Agency, resent an important aspect of water pollution control, Washington. they do not address potential synergistic or antagon- Hancock F. (1973) Algal ecology of a stream polluted through gold mining on the Witwa.tersrand. Hydrobioloistic effects on biota and consequently may not progin 43, 189-229. tect planktonic algae and other plants (Wong et al., Harding J. P. C. & Whitton .B.A. (1978) Zinc, cadmium 1978; Moore et al., 1979b). Since attached algae are and lead in water, sediments and submerged plants of often important primary producers in lakes, and may the Derwent Reservoir, Northern England. Water Res. 12, 307-316. ultimately support fish populations, it is also reasonable to compile sediment quality objectives which, in Hickman M. (1975) Studies on the epipelic diatom flora of some lakes in the southern Yukon Territory, Canada. addition to providing specific limits, also consider Arch. Hydrobiol. 76, 420--448. synergism and antagonism. These objectives are par- International Joint Commission (1976) Report of the water ticularly important, considering that pollutant levels quality objectives subcommittee. Appendix A to the Water Quality Board Report to the IJC. International in sediments are generally much higher than thos¢ in Joint Commission, Windsor. water; such differences in concentrations may in turn Jones J. R. E. (1958) A further study of the zinc polluted imply that the impact of waste discharges on plants, River Ystwyth. J..4nim. Ecol. 27, 1-14. invertebrates and ultimately fish has been generally Koivo L. K. & Ritchie J. C. (1978) Modern diatom assemblages from lake sediments in the boreal-arctic transition underestimated (Wong et al., 1978; Moore et al., region near the MacKenzie Delta. N.W.T., Canada. Can. 1979a) and that over the long-term, the release of conJ. Bot. 56, I010-1020. taminants from sediments may be more important to McLean R. O. & Jones A. R. (1975) Studies of tolerance to aquatic ecosystems than water contamination (Whitheavy metals in the flora of the rivers Ystwyth and Clarach, Wales. Freshwater Biol. 5, 431-444. ton, 1970; Schindler et al., 1980a). As pointed out by Whitton (1970), no studies are Moore J, E. & Love R. J. (1977) Effect of a pulp and paper mill effluent on the productivity of periphyton and phyavailable on the effects of heavy metals on algae for toplankton. J. Fish. Res. Bd Can. 34, 856-862. periods on the geologic time scale. Jones (1958) and Moore J. W. (1979) Distribution and abundance of McLean & Jones (1975) did, however, demonstrate attached, littoral algae in 21 lakes and streams in the Northwest Territories. Can. J. Bot. ~F/, 568-577. that diatoms and green algae were rare in the River Ystwyth (Wales), which was still polluted by zinc Moore J. W. (1980) Epipelic and epiphytic algal communities in Great Slave Lake. Can. J. Bot. 58, 35--55 years after the cessation of mining. Similarly, 1165-1t73. Hancock (1973) showed that gold mine wastes de- Moore J. W, Bcauhien V. A. & Sutherland D. J. (1979a). Comparative effects of sediment and water contamiposited in the Klip River (South Africa) 20 yr ago nation on benthic invertebrates in four lakes. Bull. envir. resulted in the production of a few tolerant diatoms, comam. Toxic. 23, 840-847. which generally occurred in high numbers. Based on Moore J. W., Sutherland D. J. & B¢auhien V. A. (1979b} these three studies and the Thompson Lake data, it is Algal and invertebrate communities in three subarctic apparent that the long-term impact of metals mines lakes receiving mine wastes. Wet. Res. 13, 1193-1202. on algae may vary from site to site. Heavy contami- Palmer C. N. (1959) Algae in water supplies. Publ. U.S. Public Health S¢rvice No. 657, 1-88. nation (a result of poor waste disposal techniques) can Patrick R. (1968) In Water Quality Criteria, 234 pp. Report result in an extended recovery period, whereas light of the National Technical Advisory Committee to the metal loadings permit the development of moderate secretary of the Interior. section III. Fish. other aquatic epipelic populations. As mentioned in the preceding life, wildlife. paragraph, sediment contamination combined with Patrick R., Cairns J. & seheier A. (1968) The relative sensitivity of diatoms, snails, and fish to twenty common conlong recovery periods may constitute a primary enstituents of industrial wastes. Prog. Fish-Cult. 30, vironmental consideration in lakes and rivers. 137-140, Ptanas D. & Healey R. P. (1978) Effects of arsenate on growth and phosphorus metabolism of phytoplankton. Acknowledoement--Data used in the study were collected J. Phycol. 14, 337-341. while the author was employed by the Environmental ProRamamoorthy S., Springthorpe S. & Kushner D. J. (1977) tection Service, Environment Canada in Yellowknife. Competition for mercury between river sediment and bacteria. Bull. envir, comam. Toxic. 17, 505-511. Schindler D. W., Hesslein R. H. & Wagemann R. (1980a) Effects of acidification on mobilization of heavy metals and radionuclides from the sediments of a freshwater REFERENCES Lake. 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Epipelic algal communities Stokes P. (1975) Uptake and accumulation of copper and nickel by metal-tolerant strains of Scenedesmus. Verb. int. Vet. theor, aonew. Limnol. 19, 2128-2137. Stokes P,, Hutchinson T. C. & Krauter K. (1973) Heavy Metal tolerance in algae isolated from polluted lakes near the Sudbury, Ontario, smelters. War. Pollut. Res. Can. 8, 178-202. Sunda W. G. & Lewis J. M. (1978) Effect of complexation by natural organic ligands on the toxicity of copper to a unicellular alga. Monochrysis lutheri. Limnol. Oceanoor. 23, 870-876.
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Thomas R. L. & Jacquet J. M. (1976) Mercury in the superficial sediments of Lake Erie. J. Fish. Res. Bd Can. 33, 404-412. Whitton B. A. (1968) Effect of light on toxicity of various substances to Anacystis nidulans. Plant Cell Physiol. 9, 23-26. Whitton B. A. (1970)Toxicity of heavy metals to freshwater algae: a review. Phykos 9, 116-125. Wong P. T. S., Chau U. K. & Luxon P. L. (1978) Toxicity of a mixture of metals on freshwater algae. J. Fish. Res. Bd Can. 35, 479--481.