ecotoxicity of copper to aquatic biota: a review

ENVIRONMENTAL RESEARCH 43, 274-282 (1987)

REVIEW

Ecotoxicity of Copper to Aquatic Biota A Review

YAHYA M . N O R

School qf Biological Sciences, Universiti Sains Malaysia, Pulau Pinang, Malaysia

Received August 1985

The toxic effects of copper on numerous aquatic flora and fauna has been studied intensely over the past l0 years. In general, there is a consensus that free cupric ions are more toxic if compared with other chemical forms such as organically complexed copper. Biolog- ical indicators exhibit a tremendously wide range of sensitivity to copper with toxic effects noted at pCu as low as 10 for some algae, while aquatic macrophytes appear to have a much higher tolerance for copper (pCu < 5.0). The sensitivity of various groups of organisms seems discrepant and anomalous with accepted standards for drinking water and industrial discharges, and recommended rates of copper sulfate application to water bodies. The toxicity of copper, however, is mitigated by the presence of naturally occurring organic com- pounds in waters through complexation. The regulatory function of dissolved humic matter will continue to be a vital one for as long as copper is discharged into aquatic environments. ~ 1987 Academic Press, Inc.

INTRODUCTION

The presence of copper in the ecosphere has attracted considerable attention and recently has been the subject of intense research (e.g., Nriagu, 1979; Loner- agan et al . , 1981; Demayo et al . , 1982; Haque and Subramaniam, 1982). In- creased concentrations of copper in the environment may be attributed to both natural and anthropogenic sources. However, man-made activities like mining (Jackson, 1978; Hutchinson, 1979; Taylor et al., 1981), industrial discharges (Paul and Pillai, 1983a; 1983b), sewage sludge disposal (Emmerich et al. , 1982a,b; Mullins et al. , 1982; Taylor et al., 1982), and fertilizer and pesticide applications (NAS, 1969; Mclntosh, 1974; Fryer and Makepeace, 1977; Thornton, 1979) have been the major culprits for elevated levels of copper in various ecosystems. Al- though copper contamination of the environment has been investigated intensely during the past decade, only recently has the complexity of reactions involving copper in both terrestrial and aquatic ecosystems been recognized. The geochem- istry and biogeochemistry of copper are complicated by its ability to form a variety of organic and inorganic complexes.

FREE Cu 2+

A significant number of studies on copper and other heavy metals in soils, sediments, and natural waters have been concerned with surveys and quantifica- tion of total concentration of metals (e.g., Jackson, 1978; Taylor, 1979; Coggins et al. , 1979; Nriagu and Coker, 1980) or have emphasized sequential extraction pro-

0013-9351/87 $3.00 Copyright © 1987 by Academic Press, Inc. All rights of reproduction in any form reserved.

274

ECOTOXICITY OF COPPER 275

cedures of elements from a variety of sources (Thornton, 1979; Harrison et al., 1981; Emmerich et al., 1982a,b; Schalscha et al., 1982). There is now an in- creasing awareness that total copper accumulation as a result of point-source pollution like industrial discharges and pesticide application to water bodies is of little meaning. Instead, knowledge of actual speciation of copper in such ecosystems is crucial. This fact has been affirmed by numerous toxicological studies involving copper and a host of living organisms ranging from algae, insects, and fishes to macrophytes.

Several studies have implicated the role of free Cu 2+ in toxicities without quantifying Cu 2+ in their systems (e.g., Toledo et al., 1979; Brown and Rattigan, 1979; Muramoto, 1982; Tanaka et al., 1982) while others have cited possible roles of hydroxo and carbanato species of copper (Anderson and Morel, 1978; Zamuda and Sunda, 1982). Other researchers, however, have been more explicit, have established relationships between physiological parameters of indicators studied and levels of free Cu 2+ in solution (Andrew et al., 1977; Anderson and Morel, 1978; Sunda and Lewis, 1978; Petersen, 1982; Florence et al., 1983), and have established lower limits of copper toxicities to organisms. In this respect, the work of Petersen (1982) merits further elaboration as it was probably one of the first attempts to model toxicities of copper and zinc to a freshwater alga. The proposed model considered growth rates, chemical speciation, stability constants, and metal interactions, and with further refinements the approach may be a useful one. There are restrictions to models, however, and the most serious limitation is often their lack of general applicability. This aspect should become more obvious when toxicities to different organisms are addressed.

Computer programs appeared to be a popular choice among researchers for modeling levels of free Cu 2+ in test solutions. With the exception of a few (e.g., Sunda and Lewis, 1978; Florence et al., 1983; Perkins, 1983), most researchers have relied on computer programs like MINEQL (Petersen, 1982), REDEQL2 (Anderson and Morel, 1978), and COMICS (Chakoumakos et al., 1979) to com- pute free Cu 2+ in solutions. Depending on a program's level of sophistication and the reliability of stability constants used, however, estimates of free Cu 2+ may vary considerably from one program to another. As an example, Dodge and Theis (1979) obtained pCu of 5.39 at pH 6.5 with the aid of the computer program MINEQLI, whereas predictions using GEOCHEM (Nor, 1984) resulted in a value of only 6.15. While a difference of an order of magnitude may seem insignificant in chemical terms, biologically it could mean survival or death to some organisms like algae (Schenck, 1984). The different computer programs have also been compared and evaluated for their ability to model molalities of various cations and anions (Nordstrom et al., 1979). With copper in river water as the test case, the predictions by different computer programs ranged from pCu of 8.76 to 14.77. Therefore, caution must be exercised when interpreting the available literature data because of the rather large discrepancy between predicted values of copper by one program compared with those of another. Computed values ideally should be validated using actual measurements such as with Cu-ISE or anodic stripping voltammetry (ASV) as an additional check.

276 YAHYA M. NOR

BIOLOGICAL INDICATORS

A great diversity of biological indicators have been used in copper toxicological bioassay studies. Broadly, these indicators may be categorized into four groups according to their respective sensitivities to copper. In descending order of sensitivity, the aquatic biota are thus microorganisms, invertebrates, fishes, bivalves, and macrophytes. Table 1 aptly summarizes some of the pertinent bioassays involving copper and a variety of aquatic indicators. The toxic effects of copper to microbes like algae, for example, were documented by numerous researchers (Sunda and Lewis, 1978; Brown and Rattigan, 1979; Toledo et al . , 1979; Petersen, 1982; Whitton and Shehata, 1982). Algae and planktons are very sensitive to

TABLE I SUMMARY OF TOXICOLOGICAL STUDIES ON COPPER USING VARIOUS INDICATORS

Organism Measurement LCs0/toxic Ref. tested technique levels Remarks

Buckley (1980) Coho Salmon Cu-ISE 6.46-6.57 - - Collvin (1984) Perch ASC/DPP 5.11 - - Borgmann and Ralph Daphnia/ Cu-ISE 4.52-8.15 - -

(1983) Cuppies Perkins (1983) Invertebrates Cu-ISE & 7.50 Index change

diversity/ community indices

Nasu et al. (1983) Lemna None None Uptake Anderson and Morel Phytoplankton REDEQL 2 9.70 Mortality

(1978) Andrew et al. ( 1977 ) Daphnia Computer 7.70 Mortality

calculations Sunda and Lewis Algae Cu-ISE 8.40 Division rate

(1978) Muramoto (1982) Carp None None Mortality Zaroogian and Scallop Calculated 7.50 Bioaccumulation

Johnson (1983) Tanaka el al. (1982) Lemna None None Uptake Dodge and Theis Midge larvae MINEQL 2 5.29 Uptake

(1979) Brown and Rattigan Elodea None 5.63 - -

(1979) Toledo et aL (1980) Algae None 6.10-6.80 Cell Florence et al. Diatom ASV 7.50 Growth

(1983) Piccardi and Clauser Iris None 4.80 - -

(1983) Sutton and Blackburn Hydrilla None 4.20-5.10 Uptake

(1971) Zamuda and Sunda Oyster Calculations 8.50-11.0 Uptake

(1982) Chacoumakos et al. Trout COMICS 6.86-8.50 - -

(1979)


copper, and toxic levels of copper ranging from pCu of 5.5 to 10.0 have been recorded (Anderson and Morel, 1978; Sunda and Lewis, 1978; Whitton and She- hata, 1982; Florence et al., 1983). Aquatic plants like Lemna, Hydrilla, and Elodea spp. appear to have higher tolerance to copper and toxic effects are observed only at pCu < 5.0 (Sutton and Blackburn, 1971; Sutton et al., 1972; Brown and Rattigan, 1979). Bivalves such as oysters and scallops have tremendous capacity to accumulate significant amounts of copper even at low pCu of 7 -9 (Za- muda and Sunda, 1982; Zaroogian and Johnson, 1983). Daphnia and carp, on the other hand, are quite sensitive to copper and suffered high mortality rates at pCu of about 6 and 8, respectively (Andrew et al., 1977; Muramoto, 1982). It is therefore clear that toxicities of copper to organisms vary tremendously depending on their respective sensitivities, hence confounding any attempt at modeling copper toxicities and severely restricting the utility of single-species studies.

Instead of using a single-species indicator, some investigators have utilized in situ ecological techniques and have characterized major macroinvertebrates in stream communities employing diversity/community indices (Perkins, 1983). This approach seems to be a significant innovation as the behavior of the whole aquatic community can be gauged using selected groups of indicators. Single- species bioassays are incapable of providing sufficient information needed to predict the response of the biota in an aquatic ecosystem to different levels of copper. There are now sufficient data in the literature, for instance, to be able to predict fairly accurately levels of copper which are toxic to different organisms (see, e.g., EPA, 1980). There is, however, a paucity of more integrated studies assessing the response of the aquatic community as a whole as is done by a few researchers (Effier et al., 1980; Perkins, 1983). More research along this line seems appropriate and timely.

STANDARDS

Different sets of standards have been adopted by various institutions world- wide, as can be judged from Table 2. The drinking water standard of 1-1.5 rag/ liter has been adopted based on organoleptic effects of copper rather than on toxicological evaluation since the available literature appears to show that copper

TABLE 2 COPPER STANDARDS IN DRINKING WATER AND MINING EFFLUENTS

Copper standard (mg/liter) Source Institution Ref.

1.5 Drinking water 0.05 Mining effluent 0.03 Mining effluent

0.012-0.043 Fresh water 0.004-0.023 Saltwater 0.3-2.0 Copper sulfate

application rate

WHO Coggins et al. (1979) U.S. EPA Bell (1978) Environment Bell (1978)

Canada U.S. EPA EPA (1980) U.S. EPA EPA (1980)

- - NAS (1969) and McIntosh (1974)

278 YAHYA M. NOR

is neither teratogenic nor mutagenic nor carcinogenic (EPA, 1980). The basis for mining effluent standards is not known, but may have been formulated based on the biologic effects of copper on living organisms. Although humans can tolerate relatively high levels of copper, ca. 1.5 rag/liter (after Coggins et al., 1979; WHO drinking water limit), a vast majority of aquatic organisms unfortunately will not tolerate or survive such high levels of copper. Similarly, recommendations for copper sulfate application to fresh water for control of algae at rates ranging from 0.3 to 2.0 rag/liter could be fatal not only to algae but also to most nontarget organisms like bacteria, plankton, fishes, and other aquatic life. Even a mining effluent discharge standard of 0.05 mg/liter (Bell, 1978) may still endanger some sensitive aquatic organisms. Perhaps recognizing the fact that many groups of aquatic organisms are very sensitive to copper, the EPA (1980) has created two ranges of standards for copper (fresh water and saltwater) based primarily on water alkalinity or hardness. There is thus a need to reevaluate current rates of algicide applications as well as copper discharge levels from sources like mining in order to prevent further damage to affected aquatic ecosystems and protect others that may be in jeopardy in view of discrepancies and anomalies between toxicity to various organisms and current standards for copper in water. Table 3 summarizes the toxic range of Cu in various aquatic organisms in relation to cur- rently accepted standards for drinking water and industrial effluent. The discrepancy is exemplified best by copper toxicity to algae which was observed at levels that were about 10,000 to 100,000 times lower than those established for copper concentration in drinking water.

ORGANIC COMPLEXATION

Toxicities of copper to some organisms are at times enhanced in the presence of certain organics. The marine diatom, Nitzchia, showed decreased growth rates in the presence of synthetic ligands even at pCu as low as 9 (Florence et al., 1983). Similarly, Sutton et al. (1972) obtained increased copper uptake in the presence of the pesticide diquat by Hydrilla. The role of organics in enhancing the toxicity and bioavailability of trace metals to aquatic organisms is not known at the mo- ment (Louma, 1983), but could be due to changes in the chemistry of membrane.

It has long been known that toxicities of copper are greatly reduced by the presence of natural and artificial ligands, and that natural waters also possess copper-binding capacities. Binding capacities attributed to humic and fulvic acids

TABLE 3 ANOMALIES IN COPPER STANDARDS AND BIOLOGICAL TOXICITIES

Copper standard (pCu) Source/organism showing toxicity

4.63-6.33 Drinking water and effluents 5.11-8.50 Fishes 7.50 Various invertebrates 6.10-9.70 Phytoplanktons and algae 4.20-5.63 Macrophyte tolerance level

ECOTOXICIT¥ OF COPPER 2"79

in waters (Bresnahan et al., 1978; Giesy et al., 1978; Musani et al., 1980; Hirata, 1981; Visser, 1982) may have several practical implications. First, the total absence of natural complexants in waters could decimate some organisms and bring about profound or even irreversible changes to other aquatic populations. On the other hand, detoxification of copper as a result of natural complexation could trigger uncontrollable algal blooms in waters and may lead to eutrophication and other undesirable features. Thus the effectiveness of copper sulfate as an algicide depends on complexing capacities of waters which in turn influence copper bioavailability to organisms. The biological role of natural organics in waters is a vital one, because they not only provide energy to organisms but also help regu- late the level of bioavailable copper to different aquatic plant and animal communities. This regulatory function of humic substances is even more crucial where discharge levels of copper exceed the tolerable limits of many organisms, which is inadvertently the norm where point-source pollution occurs.

There is little direct evidence in the literature about the ability of aquatic humic substances to inhibit the uptake of copper by organisms. Aquatic humic matter seems to be capable of inhibiting copper absorption in a few selected studies involving algae (e.g., Sunda and Lewis, 1978; Toledo et al., 1979) and fish (Buckley, 1983). Work by Nor and Cheng (1986) indicated that soil-derived humic acid completely inhibited the uptake of copper by Eichornia while fulvic acid did not seem to have any inhibitor property. In the absence of more work on the role of aquatic humic matter in complexing copper, it is difficult to make any broad generalization about its contribution in detoxifying copper. This is thus an area that requires attention.

Any revision of existing standards for copper (and some other heavy metals like zinc, lead, and cadmium) must necessarily consider and account for complexation by humic matter. Thus the copper-binding capacity of natural waters may in the future determine permissible levels of copper that may be discharged. This is based on the premise that aquatic humic matter binds copper in a form that is nonbioavailable and thus nontoxic to organisms. More work certainly needs to be done, especially work involving bioassays of copper availability in the presence of these substances. There is also a need for more standardized terminology and extraction techniques for humic matter, and until this is achieved, comparison of experimental data will be arbitrary and difficult if not meaningless. Future research must therefore address these complex problems be- fore a realistic standard(s) for copper can be formulated. The time is ripe for adopting two sets of standards (primary and secondary) as is done in air pollution control. The primary standard may be based on the effects of copper on primary indicators like fishes, bivalves, or molluscs, while the secondary standard may be formulated based on its effects on secondary indicators such as algae, bacteria, plankton, and other organisms lower down the food chain. This provision should thus cater to the two important and intimately linked categories of aquatic life most crucial for the well-being of man.

SUMMARY In summary, this review has highlighted the anomalies between existing stan-

dards for copper and its toxicity to different aquatic organisms. The role of

2 8 0 YAHYA M. NOR

aquatic humic matter in copper complexation and possible detoxification has also been discussed. A fuller understanding of the ecotoxicity of copper to aquatic biota would not be possible without addressing the following:

(a) Hamic matter. Extraction and chemical characterization techniques require standardization. Its influence on copper bioavailability to biota needs to be as- sessed. The information obtained would be useful in formulating standards based on free Cu 2+ concentrations.

(b) Systems approach. Single-species bioassays must be substituted for mul- tiple-species microcosm or in situ studies to be able to make better predictions of the biologic effects of copper to different aquatic communities.

(c) Revision of standards. Standards have been formulated with little consider- ation for the effects of copper on the biota. The copper-binding capacity of waters is a more realistic parameter to be adopted compared with that of water alkalinity or hardness, for instance.

It is in combining the inputs from physical, chemical, and biological models that a complete understanding of the nature of the interactions of copper with the abiotic and biotic environments can be achieved. Meaningful biologic models can be developed only when the three major problems indicated above and others like metal transport across membrane are resolved.

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ecotoxicity of copper to aquatic biota: a review

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