Abstract
Multi-species toxicity tests were conducted using a broad range of freshwater nematode species to assess interspecific differences in sensitivity to chemical stress and to compare the toxicity to that on the standard test organism Caenorhabditis elegans. The lethal effects of nine different chemical treatments, including metals and polycyclic aromatic hydrocarbons (PAHs) in single and mixture application, were determined for nematodes exposed for 48 h to spiked aqueous solutions. The investigated freshwater nematodes exhibited distinct differences in their sensitivity. Ranking of the susceptibility of 27 species to chemical stress showed that the effects were largely independent of the tested chemical compounds. Overall, the responses of C. elegans were well within the range of those of freshwater nematode species, being slightly less tolerant to metals, but more tolerant to PAHs than the average freshwater species response. Therefore, this study justified the use of C. elegans as representative model for freshwater nematode species in toxicity testing.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc 3:302–303
Altenburger R, Nendza M, Schüürmann G (2003) Mixture toxicity and its modeling by quantitative structure-activity relationships. Environ Toxicol Chem 22(8):1900–1915. https://doi.org/10.1897/01-386
Amiard J-C, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76(2):160–202. https://doi.org/10.1016/j.aquatox.2005.08.015
Atienzar FA, Conradi M, Evenden AJ, Jha AN, Depledge MH (1999) Qualitative assessment of genotoxicity using random amplified polymorphic DNA: comparison of genomic template stability with key fitness parameters in Daphnia magna exposed to benzo[a]pyrene. Environ Toxicol Chem 18(10):2275–2282. https://doi.org/10.1002/etc.5620181023
Barata C, Baird DJ, Markich SJ (1998) Influence of genetic and environmental factors on the tolerance of Daphnia magna Straus to essential and non-essential metals. Aquat Toxicol 42:115–137. https://doi.org/10.1016/S0166-445X(98)00039-3
Beier S, Traunspurger W (2001) The meiofauna community of two small German streams as indicator of pollution. J Aquat Ecosyst Stress Recover 8(3/4):387–405. https://doi.org/10.1023/A:1012965424527
Beier S, Traunspurger W (2003) Seasonal distribution of free-living nematodes in the Krähenbach, a fine-grained submountain carbonate stream in southwest Germany. Nematology 5(1):113–136. https://doi.org/10.1163/156854102765216740
Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83(1):14–19. https://doi.org/10.1007/BF00324627
Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10(3):239–251. https://doi.org/10.1016/S0929-1393(98)00123-1
Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14(6):224–228. https://doi.org/10.1016/S0169-5347(98)01583-3
Brenner S (1974) Genetics of Caenorhabditis elegans. Genetics 77(1):71–94
Brinke M, Höss S, Fink G, Ternes TA, Heininger P, Traunspurger W (2010) Assessing effects of the pharmaceutical ivermectin on meiobenthic communities using freshwater microcosms. Aquat Toxicol 99(2):126–137. https://doi.org/10.1016/j.aquatox.2010.04.008
Brinke M, Ristau K, Bergtold M, Höss S, Claus E, Heininger P, Traunspurger W (2011) Using meiofauna to assess pollutants in freshwater sediments: a microcosm study with cadmium. Environ Toxicol Chem 30(2):427–438. https://doi.org/10.1002/etc.387
Burton SM, Rundle SD, Jones MB (2001) The relationship between trace metal contamination and stream meiofauna. Environ Pollut 111(1):159–167. https://doi.org/10.1016/S0269-7491(99)00323-1
Canli M (2006) Effects of copper pre-exposure routes on the energy reserves and subsequent copper toxicity in Daphnia Magna. Environ Toxicol 21(5):521–527. https://doi.org/10.1002/tox.20214
Chu KW, Chow KL (2002) Synergistic toxicity of multiple heavy metals is revealed by a biological assay using a nematode and its transgenic derivative. Aquat Toxicol 61(1-2):53–64. https://doi.org/10.1016/S0166-445X(02)00017-6
Clemens S, Schroeder JI, Degenkolb T (2001) Caenorhabditis elegans expresses a functional phytochelatin synthase. Eur J Biochem 268(13):3640–3643. https://doi.org/10.1046/j.1432-1327.2001.02293.x
European Commission (2000) Directive 2000/60/EC of the European Parliament and of the council establishing a framework for the community action in the field of water policy. Luxembourg
Faupel M, Ristau K, Traunspurger W (2011) Biomass estimation across the benthic community in polluted freshwater sediment—a promising endpoint in microcosm studies? Ecotoxicol Environ Saf 74(7):1942–1950. https://doi.org/10.1016/j.ecoenv.2011.06.022
Feldmannová M, Hilscherová K, Maršálek B, Bláha L (2006) Effects of N-heterocyclic polyaromatic hydrocarbons on survival, reproduction, and biochemical parameters in Daphnia magna. Environ Toxicol 21(4):425–431. https://doi.org/10.1002/tox.20198
Félix M-A, Braendle C (2010) The natural history of Caenorhabditis elegans. Curr Biol 20(22):R965–R969. https://doi.org/10.1016/j.cub.2010.09.050
Fischer F, Böhm L, Höss S, Möhlenkamp C, Claus E, Düring RA, Schäfer S (2016) Passive dosing in chronic toxicity tests with the nematode Caenorhabditis elegans. Environ Sci Technol 50(17):9708–9716. https://doi.org/10.1021/acs.est.6b02956
Forbes VE, Calow P (2002) Extrapolation in ecological risk assessment: balancing pragmatism and precaution in chemical controls legislation. Bioscience 52(3):249. https://doi.org/10.1641/0006-3568(2002)052[0249:EIERAB]2.0.CO;2
Haegerbaeumer A, Höss S, Heininger P, Traunspurger W (2015) Experimental studies with nematodes in ecotoxicology: an overview. J Nematol 47:11–27
Haegerbaeumer A, Höss S, Ristau K, Claus E, Möhlenkamp C, Heininger P, Traunspurger W (2016) A comparative approach using ecotoxicological methods from single-species bioassays to model ecosystems. Environ Toxicol Chem 35(12):2987–2997. https://doi.org/10.1002/etc.3482
Heijerick DG, De Schamphelaere KAC, Janssen CR (2002) Predicting acute zinc toxicity for Daphnia magna as a function of key water chemistry characteristics: development and validation of a biotic ligand model. Environ Toxicol Chem 21(6):1309–1315. https://doi.org/10.1002/etc.5620210628
Heininger P, Höss S, Claus E, Pelzer J, Traunspurger W (2007) Nematode communities in contaminated river sediments. Environ Pollut 146(1):64–76. https://doi.org/10.1016/j.envpol.2006.06.023
Higgins RP, Thiel H (1988) Introduction to the Study of Meiofauna. Smithsonian Institution, Washington DC
Höss S, Williams PL (2009) Ecotoxicity testing with nematodes. In: Wilson MJ, Kakouli-Duarte T (eds) Nematodes as environmental indicators. CABI International, Wallingford, pp 208–224. https://doi.org/10.1079/9781845933852.0208
Höss S, Schlottmann K, Traunspurger W (2011) Toxicity of ingested cadmium to the nematode Caenorhabditis elegans. Environ Sci Technol 45(23):102190–10225
International Organization for Standardization (2010) Water quality—determination of the toxic effect of sediment and soil samples on growth, fertility and reproduction of Caenorhabditis elegans (Nematoda). Geneva, Switzerland
Johnson SR, Ferris JM, Ferris VR (1974) Nematode community structure of forest woodlots: III. Ordinations of taxonomic groups and biomass. J Nematol 6(3):118–126
Kammenga JE, Van Gestel CAM, Bakker J (1994) Patterns of sensitivity to cadmium and pentachlorophenol among nematode species from different taxonomic and ecological groups. Arch Environ Contam Toxicol 27(1):88–94. https://doi.org/10.1007/BF00203892
Khangarot BS, Ray PK (1989) Investigation of correlation between physicochemical properties of metals and their toxicity to the water flea Daphnia magna Straus. Ecotoxicol environ Saf 18:109–120. https://doi.org/10.1016/0147-6513(89)90071-7
Könemann H (1981) Quantitative structure-activity relationships in fish toxicity studies. Part 1: relationship for 50 industrial pollutants. Toxicology 19(3):209–221. https://doi.org/10.1016/0300-483X(81)90130-X
Lampi MA, Gurska J, McDonald KIC, Xie F, Huang XD, Dixon DG, Greenberg BM (2006) Photoinduced toxicity of polycyclic aromatic hydrocarbons to Daphnia magna: ultraviolet-mediated effects and the toxicity of polycyclic aromatic hydrocarbon photoproducts. Environ Toxicol Chem 25(4):1079–1087. https://doi.org/10.1897/05-276R.1
Mackay D, Shiu WY (1977) Aqueous solubility of polynuclear aromatic hydrocarbons. J Chem Eng Data 22(4):399–402. https://doi.org/10.1021/je60075a012
Menzel R, Bogaert T, Achazi R (2001) A systematic gene expression screen of Caenorhabditis elegans cytochrome P450 genes reveals CYP35 as strongly xenobiotic inducible. Arch Biochem Biophys 395:158–168. https://doi.org/10.1006/abbi.2001.2568
Michiels IC, Traunspurger W (2004) A three year study of seasonal dynamics of a zoobenthos community in a eutrophic lake. Nematology 6(5):655–669. https://doi.org/10.1163/1568541042843568
OECD (1992) Fish, acute toxicity test. Paris, France. https://doi.org/10.1787/9789264069961-en
OECD (2004) Daphnia sp. acute immobilisation test. Paris, France
Sankaramanachi SK, Qasim SR (1999) Metal toxicity evaluation using bioassay and microtox™. Int J Environ Stud 56(2):187–199. https://doi.org/10.1080/00207239908711199
Seinhorst JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4(1):67–69. https://doi.org/10.1163/187529259X00381
Seinhorst JW (1962) On the killing, fixation and transferring to glycerin of nematodes. Nematologica 8(1):29–32. https://doi.org/10.1163/187529262X00981
Sese BT, Grant A, Reid BJ (2009) Toxicity of polycyclic aromatic hydrocarbons to the nematode Caenorhabditis elegans. J Toxicol Environ Health Part A 72(19):1168–1180. https://doi.org/10.1080/15287390903091814
Spehar RL, Poucher S, Brooke LT, Hansen DJ, Champlin D, Cox D (1999) Comparative toxicity of fluoranthene to freshwater and saltwater species under fluorescent and ultraviolet light. Arch Environ Contam Toxicol 37(4):496–502. https://doi.org/10.1007/s002449900544
Suedel BC, Rodgers JH Jr (1996) Toxicity of fluoranthene to Daphnia magna, Hyalella azteca, Chironomus tentans, and Stylaria lacustris in water-only and whole sediment exposures. Bull Environ Contam Toxicol 57(1):132–138. https://doi.org/10.1007/s001289900166
Sulston J, Hodgkin J (1988) Methods. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Monograph Archive, Long Island, pp 587–606
Swain SC, Keusekotten K, Baumeister R, Stürzenbaum SR (2004) C. elegans metallothioneins: new insights into the phenotypic effects of cadmium toxicosis. J Mol Biol 341(4):951–959. https://doi.org/10.1016/j.jmb.2004.06.050
Tatara CP, Newman MC, McCloskey JT, Williams PL (1997) Predicting relative metal toxicity with ion characteristics: Caenorhabditis elegans LC50. Aquat Toxicol 39(3-4):279–290. https://doi.org/10.1016/S0166-445X(97)00030-1
Tichý M, Cikrt M, Roth Z, Rucki M (1998) QSAR analysis in mixture toxicity assessment. SAR QSAR Environ Res 9(3-4):155–169. https://doi.org/10.1080/10629369808039154
Traunspurger W (1997) Bathymetric, seasonal and vertical distribution of feeding-types of nematodes in an oligotrophic lake. Vie Milieu 47(1):1–7
Traunspurger W, Haitzer M, Höss S, Beier S, Ahlf W, Steinberg C (1997) Ecotoxicological assessment of aquatic sediments with Caenorhabditis elegans (Nematoda)—a method for testing liquid medium and whole-sediment samples. Environ Toxicol Chem 16(2):245–250. https://doi.org/10.1897/1551-5028(1997)016<0245:EAOASW>2.3.CO;2
Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals: Phytochelatin synthase ios required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 276(24):20817–20820. https://doi.org/10.1074/jbc.C100152200
White PA (2002) The genotoxicity of priority polycyclic aromatic hydrocarbons in complex mixtures. Mutat Res Genet Toxicol Environ Mutagen 515(1-2):85–98. https://doi.org/10.1016/S1383-5718(02)00017-7
Williams PL, Dusenbery DB (1990) Aquatic toxicity testing using the nematode C. elegans. Environ Toxicol Chem 9(10):1285–1290. https://doi.org/10.1002/etc.5620091007
Wilson M, Kakouli-Duarte T (2009) Nematodes as environmental indicators. CABI Publishing, Wallingford. https://doi.org/10.1079/9781845933852.0000
Xie F, Koziar SA, Lampi MA, Dixon DG, Norwood WP, Borgmann U, Huang XD, Greenberg BM (2006) Assessment of the toxicity of mixtures of copper, 9,10-phenanthrenequinone, and phenanthrene to Daphnia magna: evidence for a reactive oxygen mechanism. Environ Toxicol Chem 25(2):613–622. https://doi.org/10.1897/05-256R.1
Zullini A (1988) The ecology of the Lambro River. Riv Idrobiol 27:39–58
Zullini A, Peretti E (1986) Lead pollution and moss-inhabiting nematodes of an industrial area. Water Air Soil Pollut 27(3-4):403–410. https://doi.org/10.1007/BF00649421
Acknowledgements
We are grateful to the German Federal Institute of Hydrology (BfG), which funded the study (project: M39620004003) and Kai Ristau and Stefanie Gehner for their support (Bielefeld University, Department of Animal Ecology, Bielefeld, Germany). The gifts of C. elegans and E. coli from the Caenorhabditis Genetic Center (T. Stiernagle), which is funded by the National Center for Research Resources, National Institutes of Health (USA), are gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Electronic supplementary material
ESM 1
(DOCX 22 kb)
Rights and permissions
About this article
Cite this article
Haegerbaeumer, A., Höss, S., Heininger, P. et al. Is Caenorhabditis elegans representative of freshwater nematode species in toxicity testing?. Environ Sci Pollut Res 25, 2879–2888 (2018). https://doi.org/10.1007/s11356-017-0714-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-0714-7