Environ. Sci. Technol. 2004, 38, 5030-5037
Using the Biotic Ligand Model for Predicting the Acute Sensitivity of Cladoceran Dominated Communities to Copper in Natural Surface Waters BART T. A. BOSSUYT,* KAREL A. C. DE SCHAMPHELAERE, AND COLIN R. JANSSEN Laboratory of Environmental Toxicology and Aquatic Ecology, Ghent University, J. Plateaustraat 22, B-9000 Ghent, Belgium
In this study, the acute copper sensitivity of field-collected cladoceran species was determined using their natural surface waters and a standard reconstituted test water as test medium. A total of 43 species were collected on two occasions from six different sites, representing different water types and chemistries in Europe. The collected species belonged to four different families (Daphniidae, Bosminidae, Macrothricidae, Chydoridae) and 11 different genera (Daphnia, Ctenodaphnia, Ceriodaphnia, Simocephalus, Scapholeberis, Alona, Acroperus, Chydorus, Eurycercus, Disparalona, Pleuroxus). In acute experiments with immobilization as end point, the 48-h median effective concentrations (48-h EC50) for the cladoceran species ranged from 5.30 to 70.6 µg of Cu L-1 in standard test water and from 9.60 to 853 µg of Cu L-1 in natural waters. The mean site sensitivity (the geometric mean of 48-h EC50 values of species within a community) ranged from 10.1 to 27.4 µg of Cu L-1 in standard water and from 16.4 to 281 µg of Cu L-1 in natural water. This indicates that bioavailability is more important than inter-community (species composition) differences in determining the variability of copper toxicity across different aquatic systems. For the four surface waters that had a pH within the range for which the acute Daphnia magna biotic ligand model (BLM) has previously been successfully validated, the BLM predicted 48-h EC50 values for 27 of the 28 tested cladoceran species within factor of 2 of the observed values. For the same sites, all community sensitivities were predicted within a factor of 2.3. The BLM was clearly over-protective for the two acidic surface waters tested. Hence, the BLM can be considered a valuable tool for estimating the potentially harmful effects of copper to natural cladoceran communities, but more research will be needed for acidic surface waters.
Introduction Cladocerans are widely used in aquatic toxicology due to their ecological significance, short life cycle, ease of laboratory culturing, and low space and water volume requirements (1, 2). Among the cladocerans, Daphnia magna Straus is probably the most commonly used test organism in ecotoxicological studies, although its use has been criticized * Corresponding author tel: +32 9 264 79 32; fax: +32 9 264 37 66; e-mail:
[email protected]. 5030
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by several authors because of its limited geographical range and its confinement to small water bodies (3-7). Hence, the continued use of D. magna and other infrequently found zooplankters in testing aimed at setting water quality standards should ideally be accompanied by testing of more ecologically relevant/representative species. Ideally, the toxicity of a chemical to a given species in a specific body of water would be estimated better by toxicity assays using the indigenous species (8, 9) and the specific surface water under consideration. To our knowledge, no detailed copper toxicity studies have been performed with resident cladoceran species originating from different aquatic systems and tested in the surface water of origin. For the further enhancement of the ecological relevance in setting environmental standards, species sensitivity distributions (SSDs) are increasingly recommended to complement or replace the use of arbitrary assessment factors in the risk assessment of chemicals (10, 11). The SSD approach, proposed in both North America (12) and Europe (13), involves fitting a statistical distribution to point effect estimates obtained from toxicity assays with different species. At lower risk assessment tiers, this may involve selecting a threshold level that represents a safe concentration of the substance (i.e., protective for most organisms; usually 95%) in an assemblage of species (14-16). For example, Brix et al. (17) constructed acute SSDs for copper based on literature toxicity data, mostly obtained with species that have been maintained in the laboratory under ideal/controlled circumstances for several years. The latter is a common problem of the SSD approach, as this type of toxicity data may not be fully representative of indigenous natural populations, although this is one of the main assumptions underlying the SSD approach (18). Indeed, we have previously found that field-collected cladoceran species may be slightly more sensitive to copper than laboratory maintained organisms (Bossuyt and Janssen, unpublished data). Another problem with literature-based toxicity data on copper is that they are usually obtained in test media in which the bioavailability is near maximal (i.e., test results obtained in media containing no or very low concentrations of dissolved organic carbon (DOC), a major factor controlling copper bioavailability) (e.g., ref 19). Hence, the often applied hardness correction for metal toxicity data (e.g., ref 17) is probably not sufficient to make an SSD based on literature data representative for that occurring in natural environments. However, the biotic ligand model (BLM) could, by taking into account all water chemistry parameters affecting copper toxicity (e.g., DOC, Ca, Mg, Na, pH, and alkalinity), allow the normalization of laboratory-derived toxicity data to field situations (19, 20). This implies that the BLM should not only be applicable to the organisms for which the model was originally developed/calibrated (i.e., D. magna and D. pulex) but also for a larger number of species. Given the above-mentioned shortcomings and the ecological importance of the cladocerans in aquatic food webs, the goal of the present study was to investigate the sensitivity of individual members of cladoceran-dominated freshwater communities to copper in both standard laboratory test water and in their natural water of origin. Three hypotheses were tested: (i) inter-community differences in copper sensitivity are less important than differences in copper bioavailability in determining the mean site sensitivity, (ii) the BLM can be used to translate toxicity data obtained in artificial laboratory test waters to data obtained in natural surface waters for field-collected cladoceran species, and (iii) the BLM-predicted mean site sensitivity does not differ from the observed mean 10.1021/es049907d CCC: $27.50
2004 American Chemical Society Published on Web 08/27/2004
TABLE 1. Water Characteristics of Sampling Sitesa
site Ankeveen Bokrijk Leuven Markermeer Oberkirchen Teut
sampling (dd-mm-yyyy) 14-06-2002 12-09-2002 22-08-2002 01-10-2002 06-07-2002 23-10-2002 26-05-2001 24-09-2002 19-06-2002 10-09-2002 22-08-2002 01-10-2002
ISO
DOC (mg L-1)
Na (mg L-1)
Ca (mg L-1)
Mg (mg L-1)
K (mg -1 L )
Cl (mg L-1)
Fe (mg L-1)
Al (mg L-1)
Cu (µg L-1)
37.7 27.5 5.7 3.0 7.2 9.8 8.2 10.4 2.3 1.6 4.0 3.7 0.38
8.0 7.6 14.7 13.1 25.8 23.6 76.8 67.6 2.9 2.6 5.4 5.7 17.2
26.6 19.4 7.5 9.7 58.1 71.1 66.5 55.1 14.9 15.2 3.0 2.9 80.1
4.5 4.0 1.3 1.4 6.2 5.1 17.1 14.5 2.9 3.1 1.8 1.5 12.2
2.0 1.1 1.6 bdl 1.3 2.2 9.5 6.4 bdl bdl 1.2 bdl 2.9
13.3 16.9 18.0 26.2 29.8 40.4 127 124 3.4 3.3 7.5 13.1 144.4
0.6 0.3 0.2 0.1 bdl bdl bdl 0.3 0.1 bdl 0.4 bdl nd
0.06 0.03 0.04 0.04 0.20 0.04 0.04 0.34 0.09 0.02 0.23 0.04 nd
3.2 9.2 3.3 2.5 4.4 3.3 5.1 11.0 3.2 3.6 3.3 2.0 bdl
pH
C (µS cm-1)
T (°C)
E350 (L mg-1 cm-1)
6.8 7.4 5.5 5.0 8.2 8.3 8.3 8.0 7.7 7.4 4.3 4.1 7.8
367 412 nd 141 nd 476 nd 780 120 81.4 nd 100 nd
18.5 19.0 18.0 11.8 17.0 12.1 nd nd 13.6 11.8 21.0 14.9 nd
nd nd nd 0.00300 nd 0.00520 0.00574 0.00413 nd nd nd nd nd
a DOC, dissolved organic carbon; C, conductivity; -1 350, UV absorbance at 350 nm; nd, not determined; bdl: below detection limit (K, 5.5) mean site sensitivity to copper can be accurately predicted within a factor of 2.3 when assuming 50% AFA (mean ( standard deviation ) 1.7 ( 0.4, n ) 7). When only those normal sites where UV absorption was measured are considered, the prediction errors were a factor of 2.0 ( 0.2 (n ) 3) with 50% AFA assumed and a factor of 1.2 ( 0.2 (n ) 3) when the optimal % AFA was taken. Furthermore, from a regulatory point of view, the optimal %AFA approach yields more conservative predictions of EC50 than the 50% AFA approach in two of the three cases where the former approach was possible (see Table 5). To conclude, we demonstrated that bioavailability is far more important than inherent mean site sensitivity differences in determining the effect of copper to cladoceran dominated communities in natural surface waters. We have also shown that the acute Cu-BLM, as developed with D. magna, can be used to predict copper toxicity to most fieldcollected cladoceran species occurring in normal waters (pH > 5.5). The BLM was not predictive for organisms living in
acidic waters (pH < 5.5). The BLM can be used for estimating mean site sensitivity to copper of resident communities tested in the spiked natural surface waters. Although this study clearly demonstrates, for the first time, the applicability of the BLM concept for predicting acute copper toxicity in natural waters, future research should investigate if this holds for the recently developed chronic Cu-BLM too (40). The present and the suggested future research will improve the currently applied risk assessment procedures of copper and its substances in freshwater environments.
Acknowledgments We thank Jill van Reybrouck and Leslie Roman for their excellent technical support. We also thank Dr. Christoph Schaefers of IUCT, Kelle Moreau of KUL, Liliane Gora of AMINAL, and Luc Crevecoeur of Groene Huis for their assistance in finding the sites and their permission to collect zooplankton and water samples at the sampling sites. B.T.A. Bossuyt is the recipient of a Ph.D. research grant of the Flemish Institute for the promotion of Scientific and Technological Research in Industry (IWT). This research received additional funding from a Ghent University Research Fund (BOF 01110501).
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Received for review January 19, 2004. Revised manuscript received June 24, 2004. Accepted June 25, 2004. ES049907D
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