Abstract
The assessment of transgenerational effects should be incorporated in standard chronic toxicity protocols for the sake of a realistic extrapolation of contaminant effects to the population level. We propose a simple add-on to the standard 21-day chronic Daphnia magna assay, allowing the assessment of the reproductive performance of the offspring (F1 generation) born from the first clutch of the parental (F0) generation. The extended generational assay was performed simultaneously with the standard reproduction assay. With this design, we evaluated the lethal, reproductive, and transgenerational effects of four widespread and extensively used substances: a biocide/anti-fouling (copper sulphate), an industrial oxidizing agent (potassium dichromate), a pharmaceutical (paracetamol), and a quaternary ammonium compound (benzalkonium chloride). Benzalkonium chloride was the most toxic in terms of lethality, whereas paracetamol, copper sulphate, and potassium dichromate caused deleterious effects in the reproductive performance of exposed D. magna. Adverse effects in the fitness of the daughter (F1) generation were observed in the case of maternal exposure to paracetamol and copper sulphate, although they were not very pronounced. These findings highlight the usefulness of our approach and reinforce the view—shared by other authors—of the need for a generalised formal assessment of the transgenerational effects of pollutants.
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References
Antunes SC, Castro BB, Gonçalves F (2004) Effect of food level on the acute and chronic responses of daphnids to lindane. Environ Pollut 127:367–375. https://doi.org/10.1016/j.envpol.2003.08.015
Antunes SC, Nunes B, Rodrigues S et al (2016) Effects of chronic exposure to benzalkonium chloride in Oncorhynchus mykiss: cholinergic neurotoxicity, oxidative stress, peroxidative damage and genotoxicity. Environ Toxicol Pharmacol 45:115–122
ASTM (2012) Standard guide for conducting Daphnia magna life-cycle toxicity tests—Standard E1193-97. West Conshohocken, PA
Baker TR, Peterson RE, Heideman W (2014) Using zebrafish as a model system for studying the transgenerational effects of dioxin. Toxicol Sci 138:403–411. https://doi.org/10.1093/toxsci/kfu006
Barata C, Varo I, Navarro JC et al (2005) Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol Part C Toxicol Pharmacol 140:175–186. https://doi.org/10.1016/j.cca.2005.01.013
Barata C, Campos B, Rivetti C et al (2017) Validation of a two-generational reproduction test in Daphnia magna: an interlaboratory exercise. Sci Total Environ 579:1073–1083. https://doi.org/10.1016/j.scitotenv.2016.11.066
Benotti MJ, Trenholm RA, Vanderford BJ et al (2009) Pharmaceuticals and endocrine disrupting compounds in U.S. drinking water. Environ Sci Technol 43:597–603. https://doi.org/10.1021/es801845a
Benzie JAH (2005) Cladocera: the genus Daphnia (including Daphniopsis). Kenobi Productions, Ghent, Belgium & Backhuys Publishers, Leiden, The Netherlands
Berglind D (1984) Acute toxicity of chromate, DDT, PCP, TPBS, and zinc to Daphnia magna cultured in hard and soft water. Bull Environ Contam Toxicol 33(1):63–68. https://doi.org/10.1007/BF01625512
Boersma M (1997) Offspring size and parental fitness in Daphnia magna. Evol Ecol 11:439–450
Bossuyt BTA, De Schamphelaere KAC, Janssen CR (2004) Using the biotic ligand model for predicting the acute sensitivity of cladoceran dominated communities to copper in natural surface waters. Environ Sci Technol. https://doi.org/10.1021/ES049907D
Bossuyt BTA, Muyssen BTA, Janssen CR (2005) Relevance of generic and site-specific species sensitivity distributions in the current risk assessment procedures for copper and zinc. Environ Toxicol Contam 24(2):470–478. https://doi.org/10.1897/03-067R.1
Brandão FP, Rodrigues S, Castro BB et al (2013) Short-term effects of neuroactive pharmaceutical drugs on a fish species: biochemical and behavioural effects. Aquat Toxicol 144–145:218–229. https://doi.org/10.1016/j.aquatox.2013.10.005
Brennan SJ, Brougham CA, Roche JJ, Fogarty AM (2006) Multi-generational effects of four selected environmental oestrogens on Daphnia magna. Chemosphere 64:49–55. https://doi.org/10.1016/j.chemosphere.2005.11.046
Campos B, Jordão R, Rivetti C et al (2016) Two-generational effects of contaminants in Daphnia magna: effects of offspring quality. Environ Toxicol Chem 35:1470–1477. https://doi.org/10.1002/etc.3290
Castro BB, Consciência S, Gonçalves F (2007) Life history responses of Daphnia longispina to mosquitofish (Gambusia holbrooki) and pumpkinseed (Lepomis gibbosus) kairomones. Hydrobiologia 594:165–174. https://doi.org/10.1007/s10750-007-9074-5
Cerejeira MJ, Viana P, Batista S et al (2003) Pesticides in Portuguese surface and ground waters. Water Res 37:1055–1063. https://doi.org/10.1016/S0043-1354(01)00462-6
Chen Y, Huang J, Xing L et al (2014) Effects of multigenerational exposures of D. magna to environmentally relevant concentrations of pentachlorophenol. Environ Sci Pollut Res 21:234–243. https://doi.org/10.1007/s11356-013-1692-z
Coors A, Vanoverbeke J, De Bie T, De Meester L (2009) Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna. Aquat Toxicol 95:71–79. https://doi.org/10.1016/j.aquatox.2009.08.004
Cuco AP, Abrantes N, Gonçalves F et al (2016) Toxicity of two fungicides in Daphnia: is it always temperature-dependent? Ecotoxicology 25:1376–1389. https://doi.org/10.1007/s10646-016-1689-8
Daneshvar A, Aboulfadl K, Viglino L et al (2012) Evaluating pharmaceuticals and caffeine as indicators of fecal contamination in drinking water sources of the Greater Montreal region. Chemosphere 88:131–139. https://doi.org/10.1016/j.chemosphere.2012.03.016
Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 107(Suppl):907–938
de Coors A, Vanoverbeke J, de Bie T, de Meester L (2009) Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna. Aquat Toxicol 95(1):71–79. https://doi.org/10.1016/j.aquatox.2009.08.004
De Voogt P, Janex-Habibi ML, Sacher F et al (2009) Development of a common priority list of pharmaceuticals relevant for the water cycle. Water Sci Technol 59:39–46. https://doi.org/10.2166/wst.2009.764
Fick J, Soderstrom H, Lindberg RH et al (2009) Contamination of surface, ground, and drinking water from pharmaceutical production. Environ Toxicol Chem 28:2522–2527. https://doi.org/10.1897/09-073.1
Forbes VE, Calow P (1999) Is the per capita rate of increase a good measure of population-level effects in ecotoxicology? Environ Toxicol Chem 18:1544–1556. https://doi.org/10.1002/etc.5620180729
García MT, Ribosa I, Guindulain T, Sánchez-Leala J, Vives-Rego J (2001) Fate and effect of monoalkyl quaternary ammonium surfactants in the aquatic environment. Environ Pollut 111(1):169–175. https://doi.org/10.1016/S0269-7491(99)00322-X
Gopi RA, Ayyappan S, Chandrasehar G, Varma KK, Goparaju A (2012) Effect of potassium dichromate on the survival and reproduction of Daphnia magna. Bull Environ Pharmacol 1(7):89–94
Guilhermino L, Sobral O, Chastinet C et al (1999) A Daphnia magna first-brood chronic test: an alternative to the conventional 21-day chronic bioassay? Ecotoxicol Environ Saf 42:67–74. https://doi.org/10.1006/eesa.1998.1730
Guilhermino L, Diamantino T, Silva C, Soares AMVM (2000) Acute toxicity test with Daphnia magna: an alternative to mammals in the prescreening of chemical toxicity? Ecotoxicol Environ Saf 46:357–362. https://doi.org/10.1006/eesa.2000.1916
Hammers-Wirtz M, Ratte HT (2000) Offspring fitness in Daphnia: is the Daphnia reproduction test appropriate for extrapolating effects on the population level? Environ Toxicol Chem 19:1856
Henschel K-P, Wenzel A, Diedrich M, Fliedner A (1997) Environmental hazard assessment of pharmaceuticals. Reg Toxicol Pharmacol 25(3):220–225. https://doi.org/10.1006/rtph.1997.1102
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363. https://doi.org/10.1002/bimj.200810425
IETEG (2005) Chromium (VI) handbook. CRC Press, Boca Raton
ISO (2000) Water quality—determination of long term toxicity of substances to Daphnia magna Straus (Cladocera, Crustacea). ISO 10706:2000. International Organization for Standardization, Geneva, Switzerland
Ivanković T, Hrenović J (2010) Surfactants in the environment. Arhiv za higijenu rada i toksikologiju. https://doi.org/10.2478/10004-1254-61-2010-1943
Jemec A, Tišler T, Drobne D et al (2008) Biochemical biomarkers in chronically metal-stressed daphnids. Comp Biochem Physiol Part C Toxicol Pharmacol 147:61–68. https://doi.org/10.1016/j.cbpc.2007.07.006
Jeong TY, Kim HY, Kim SD (2015) Multi-generational effects of propranolol on Daphnia magna at different environmental concentrations. Environ Pollut 206:188–194. https://doi.org/10.1016/j.envpol.2015.07.003
Johansson HKL, Jacobsen PR, Hass U et al (2016) Perinatal exposure to mixtures of endocrine disrupting chemicals reduces female rat follicle reserves and accelerates reproductive aging. Reprod Toxicol 61:186–194. https://doi.org/10.1016/j.reprotox.2016.03.045
Kaj L, Wallberg P, Brorström-Lundén E (2014) Quaternary ammonium compounds. Analyses in a Nordic cooperation on screening. Nordic Council of Ministers. Rosendahls-Schultz Grafisk. Copenhagen
Kegley SE, Hill BR, Orme S, Choi A (2016) PAN Pesticide Database. In: Pestic. Action Network, North Am. (Oakland, CA, 2016). http://www.pesticideinfo.org/
Kim Y, Choi K, Jung J, Park S, Kim P-G, Park J (2007) Aquatic toxicity of acetaminophen, carbamazepine, cimetidine, diltiazem and six major sulfonamides, and their potential ecological risks in Korea. Environ Int 33(3):370–375. https://doi.org/10.1016/j.envint.2006.11.017
Kreuzinger N, Fuerhacker M, Scharf S et al (2007) Methodological approach towards the environmental significance of uncharacterized substances—quaternary ammonium compounds as an example. Desalination 215:209–222. https://doi.org/10.1016/j.desal.2006.10.036
Kristensen DM, Hass U, Lesne L et al (2011) Intrauterine exposure to mild analgesics is a risk factor for development of male reproductive disorders in human and rat. Hum Reprod 26:235–244. https://doi.org/10.1093/humrep/deq323
Kühn R, Pattard M, Klaus-Dieter P, Winter A (1989) Results of the harmful effects of selected water pollutants (anilines, phenols, aliphatic compounds) to Daphnia magna. Water Res 23(4):495–499. https://doi.org/10.1016/0043-1354(89)90141-3
Lavorgna M, Russo C, D’Abrosca B et al (2016) Toxicity and genotoxicity of the quaternary ammonium compound benzalkonium chloride (BAC) using Daphnia magna and Ceriodaphnia dubia as model systems. Environ Pollut 210:34–39. https://doi.org/10.1016/j.envpol.2015.11.042
Loureiro C, Castro BB, Pereira JL, Gonçalves F (2011) Performance of standard media in toxicological assessments with Daphnia magna: chelators and ionic composition versus metal toxicity. Ecotoxicology 20:139–148. https://doi.org/10.1007/s10646-010-0565-1
Loureiro C, Castro BB, Cuco AP et al (2012) Life-history responses of salinity-tolerant and salinity-sensitive lineages of a stenohaline cladoceran do not confirm clonal differentiation. Hydrobiologia 702:73–82. https://doi.org/10.1007/s10750-012-1308-5
Masteling RP, Castro BB, Antunes SC, Nunes B (2016) Whole-organism and biomarker endpoints in Daphnia magna show uncoupling of oxidative stress and endocrine disruption in phenolic derivatives. Ecotoxicol Environ Saf 134:64–71. https://doi.org/10.1016/j.ecoenv.2016.08.012
Melvin SD, Wilson SP (2013) The utility of behavioral studies for aquatic toxicology testing: a meta-analysis. Chemosphere 93:2217–2223. https://doi.org/10.1016/j.chemosphere.2013.07.036
Meyer JS, Ingersoll CG, McDonald LL, Boyce MS (1986) Estimating uncertainty in population growth rates: jackknife vs. bootstrap techniques. Ecology 67:1156–1166
Monteiro SC, Boxall ABA (2010) Occurrence and fate of human pharmaceuticals in the environment. Springer, New York, pp 53–154
Moore MN, Depledge MH, Readman JW, Leonard DRP (2004) An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res Fundam Mol Mech Mutagen 552:247–268. https://doi.org/10.1016/j.mrfmmm.2004.06.028
Newman TAC, Carleton CR, Leeke B et al (2015) Embryonic oxidative stress results in reproductive impairment for adult zebrafish. Redox Biol 6:648–655. https://doi.org/10.1016/j.redox.2015.10.010
Nunes B (2015) How to answer the question: are drugs real threats to biological systems or overrated innocuous chemicals? In: Andreazza AC, Scola G (eds) Toxicology studies—cells, drugs and environment. In Tech
Nunes B, Antunes SC, Santos J et al (2014) Toxic potential of paracetamol to freshwater organisms: a headache to environmental regulators? Ecotoxicol Environ Saf 107:178–185. https://doi.org/10.1016/j.ecoenv.2014.05.027
OECD (2004) Daphnia sp. acute immobilisation test. Paris, France
OECD (2012) Daphnia magna reproduction test. France, Paris
Oh S, Choi K (2012) Optimal conditions for three brood chronic toxicity test method using a freshwater macroinvertebrate Moina macrocopa. Environ Monit Assess 184:3687–3695. https://doi.org/10.1007/s10661-011-2216-2
Oliveira LLD, Antunes SC, Gonçalves F et al (2015) Evaluation of ecotoxicological effects of drugs on Daphnia magna using different enzymatic biomarkers. Ecotoxicol Environ Saf 119:123–131. https://doi.org/10.1016/j.ecoenv.2015.04.028
Poynton HC, Varshavsky JR, Chang B et al (2006) Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environ Sci Technol. https://doi.org/10.1021/ES0615573
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
Ritz C (2010) Toward a unified approach to dose–response modeling in ecotoxicology. Environ Toxicol Chem 29:220–229. https://doi.org/10.1002/etc.7
Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22. https://doi.org/10.18637/jss.v012.i05
Rocha R, Gonçalves F, Marques C, Nunes B (2014) Environmental effects of anticholinesterasic therapeutic drugs on a crustacean species, Daphnia magna. Environ Sci Pollut Res 21:4418–4429. https://doi.org/10.1007/s11356-013-2339-9
Rodrigues S, Correia AT, Antunes SC, Nunes B (2015) Alterations in gills of Lepomis gibbosus, after acute exposure to several xenobiotics (pesticide, detergent and pharmaceuticals): morphometric and biochemical evaluation. Drug Chem Toxicol 38:126–132. https://doi.org/10.3109/01480545.2014.918999
Rowe CL, Hopkins WA, Congdon J (2001) Integrating individual-based indices of contaminant effects. Sci World 1:703–712. https://doi.org/10.1100/tsw.2001.367
Sánchez M, Ferrando MD, Sancho E, Andreu E (1999) Assessment of the toxicity of a pesticide with a two-generation reproduction test using Daphnia magna. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 124:247–252. https://doi.org/10.1016/S0742-8413(99)00071-7
Sánchez M, Ferrando MD, Sancho E, Andreu E (2000) Physiological perturbations in several generations of Daphnia magna straus exposed to diazinon. Ecotoxicol Environ Saf 46:87–94. https://doi.org/10.1006/eesa.1999.1890
Schwarzenbach RP, Escher B, Fenner K et al (2009) The challenge of micropollutants. Sci Technol 313:1072–1077. https://doi.org/10.1126/science.1127291
Smolders R, Baillieul M, Blust R (2005) Relationship between the energy status of Daphnia magna and its sensitivity to environmental stress. Aquat Toxicol 73:155–170. https://doi.org/10.1016/j.aquatox.2005.03.006
Snijder CA, Kortenkamp A, Steegers EAP et al (2012) Intrauterine exposure to mild analgesics during pregnancy and the occurrence of cryptorchidism and hypospadia in the offspring: the Generation R Study. Hum Reprod 27:1191–1201. https://doi.org/10.1093/humrep/der474
Szöcs E, Schäfer RB (2015) Ecotoxicology is not normal. Environ Sci Pollut Res 22:13990–13999. https://doi.org/10.1007/s11356-015-4579-3
Tsui MTK, Wang W-X (2004) Maternal transfer efficiency and transgenerational toxicity of methylmercury in Daphnia magna. Environ Toxicol Chem 23:1504–1511. https://doi.org/10.1897/03-310
USEPA (2002) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organisms—EPA-821-R-02-013. Washington, DC
Vandegehuchte MB, Lemière F, Janssen CR (2009) Quantitative DNA-methylation in Daphnia magna and effects of multigeneration Zn exposure. Comp Biochem Physiol C Toxicol Pharmacol 150:343–348. https://doi.org/10.1016/j.cbpc.2009.05.014
Vandegehuchte MB, Lemière F, Vanhaecke L et al (2010) Direct and transgenerational impact on Daphnia magna of chemicals with a known effect on DNA methylation. Comp Biochem Physiol C Toxicol Pharmacol 151:278–285. https://doi.org/10.1016/j.cbpc.2009.11.007
Wake H (2005) Oil refineries: a review of their ecological impacts on the aquatic environment. Estuar Coast Shelf Sci 62:131–140. https://doi.org/10.1016/j.ecss.2004.08.013
Watanabe H, Takahashi E, Nakamura Y et al (2007) Development of a Daphnia magna DNA microarray for evaluating the toxicity of environmental chemicals. Environ Toxicol Chem 26:669. https://doi.org/10.1897/06-075R.1
Wickham H (2009) Ggplot2: elegant graphics for data analysis
Wilke CO (2016) Cowplot: streamlined plot theme and plot annotations for “ggplot2.” https://cran.r-project.org/package=cowplot
Willis BE, Bishop WM (2016) Understanding fate and effects of copper pesticides in aquatic systems. J Geosci Environ Prot 4:37–42. https://doi.org/10.4236/gep.2016.45004
Youngson N, Whitelaw E (2008) Transgenerational epigenetic effects. Annu Rev Genomics Hum Genet 9:233–257. https://doi.org/10.1146/annurev.genom.9.081307.164445
Yu Z, Chen X, Zhang J et al (2013) Transgenerational effects of heavy metals on L3 larva of Caenorhabditis elegans with greater behavior and growth inhibitions in the progeny. Ecotoxicol Environ Saf 88:178–184. https://doi.org/10.1016/j.ecoenv.2012.11.012
Acknowledgements
This research was partially supported by the Strategic Funding UID/Multi/04423/2013 through national funds provided by FCT—Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020. Sara Antunes is recipient of individual post-doctoral grant (SFRH/BPD/109951/2015) by the Portuguese Foundation for Science and Technology (FCT). Bruno Nunes was supported by FCT (Researcher Contract IF/01744/2013).
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Castro, B.B., Freches, A.R., Rodrigues, M. et al. Transgenerational Effects of Toxicants: An Extension of the Daphnia 21-day Chronic Assay?. Arch Environ Contam Toxicol 74, 616–626 (2018). https://doi.org/10.1007/s00244-018-0507-0
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DOI: https://doi.org/10.1007/s00244-018-0507-0