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Transgenerational Effects of Toxicants: An Extension of the Daphnia 21-day Chronic Assay?

  • B. B. Castro
  • A. R. Freches
  • M. Rodrigues
  • B. Nunes
  • S. C. Antunes
Article

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.

Notes

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).

References

  1. 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 CrossRefGoogle Scholar
  2. 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 45:115–122CrossRefGoogle Scholar
  3. ASTM (2012) Standard guide for conducting Daphnia magna life-cycle toxicity tests—Standard E1193-97. West Conshohocken, PAGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. Benzie JAH (2005) Cladocera: the genus Daphnia (including Daphniopsis). Kenobi Productions, Ghent, Belgium & Backhuys Publishers, Leiden, The NetherlandsGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. Boersma M (1997) Offspring size and parental fitness in Daphnia magna. Evol Ecol 11:439–450CrossRefGoogle Scholar
  11. 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 Google Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 107(Suppl):907–938CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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):89–94Google Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 19:1856CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. IETEG (2005) Chromium (VI) handbook. CRC Press, Boca RatonGoogle Scholar
  35. 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, SwitzerlandGoogle Scholar
  36. 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 Google Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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. CopenhagenGoogle Scholar
  41. 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/
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. Meyer JS, Ingersoll CG, McDonald LL, Boyce MS (1986) Estimating uncertainty in population growth rates: jackknife vs. bootstrap techniques. Ecology 67:1156–1166CrossRefGoogle Scholar
  52. Monteiro SC, Boxall ABA (2010) Occurrence and fate of human pharmaceuticals in the environment. Springer, New York, pp 53–154Google Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. 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 TechGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. OECD (2004) Daphnia sp. acute immobilisation test. Paris, FranceGoogle Scholar
  58. OECD (2012) Daphnia magna reproduction test. France, ParisCrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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 Google Scholar
  62. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
  63. 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 CrossRefGoogle Scholar
  64. Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22.  https://doi.org/10.18637/jss.v012.i05 CrossRefGoogle Scholar
  65. 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 CrossRefGoogle Scholar
  66. 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 CrossRefGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. 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 CrossRefGoogle Scholar
  69. 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 CrossRefGoogle Scholar
  70. 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 Google Scholar
  71. 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 CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. 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 CrossRefGoogle Scholar
  74. 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 CrossRefGoogle Scholar
  75. USEPA (2002) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organisms—EPA-821-R-02-013. Washington, DCGoogle Scholar
  76. 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 CrossRefGoogle Scholar
  77. 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 CrossRefGoogle Scholar
  78. 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 CrossRefGoogle Scholar
  79. 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 CrossRefGoogle Scholar
  80. Wickham H (2009) Ggplot2: elegant graphics for data analysisGoogle Scholar
  81. Wilke CO (2016) Cowplot: streamlined plot theme and plot annotations for “ggplot2.” https://cran.r-project.org/package=cowplot
  82. 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 Google Scholar
  83. 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 CrossRefGoogle Scholar
  84. 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 CrossRefGoogle Scholar

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Authors and Affiliations

  • B. B. Castro
    • 1
  • A. R. Freches
    • 2
  • M. Rodrigues
    • 2
  • B. Nunes
    • 3
  • S. C. Antunes
    • 2
    • 4
  1. 1.Departamento de Biologia, CBMA (Centro de Biologia Molecular e Ambiental)Universidade do MinhoBragaPortugal
  2. 2.Departamento de BiologiaFaculdade de Ciências da Universidade do PortoPortoPortugal
  3. 3.Departamento de Biologia, CESAM (Centro de Estudos do Ambiente e do Mar)Universidade de AveiroAveiroPortugal
  4. 4.CIIMAR (Centro Interdisciplinar de Investigação Marinha e Ambiental)Universidade do PortoPortoPortugal

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