Abstract
Sediment-living organisms can be subjected to a multi-pollution condition due to an increase in the diversity of contaminants. Sediment mixtures of Mercury (Hg) and some polycyclic aromatics hydrocarbons like Pyrene (Pyr) are common in heavily industrialized coastal zones. In the present study, greater than (>) and less than (<) probable effect concentration levels (PELs) of Hg and Pyr were assessed using spiked sediments in order to determine combined (Hg + Pyr) effects in uptake, metabolization and oxidative balance in the polychaete Perinereis gualpensis at short and medium-term exposure. Hg + Pyr significantly influenced the uptake/kinetics of Hg and Pyr metabolite 1-OH-pyrene in polychaete tissues during the exposure time compared with separate treatments of each analyte (p < 0.05). Both the Hg-only and Pyr-only exposures significantly influenced both enzymatic and non-enzymatic responses respect to control groups (p < 0.05). The Hg-only treatment showed the worst scenario related to the activation and subsequent inhibition of glutathione S- transferase (GST) and peroxidase (GPx) activities, high levels of Thiol-groups (SH-groups), low antioxidant capacity (ACAP) and enhanced lipid peroxidation (TBARS) in the last days of exposure (p < 0.05). In contrast, ragworms exposed to Hg + Pyr showed a significant increase in both enzymatic and non-enzymatic activity during the first days of exposure and the absence of lipid peroxidation during the whole experiment. Our results suggest different oxidative stress scenarios in P. gualpensis when exposed to >PEL Hg concentration with <PEL Pyr in sediments. Results also reveal the importance of the exposure time, endpoints involved as well as of the contaminant monitoring during the whole experiments in assessing the interactive effects of the contaminant mixture.
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References
Ahmad I, Oliveira M, Pacheco M, Santos MA (2005) Anguilla anguilla L. oxidative stress biomarkers responses to copper exposure with or without β-naphthoflavone pre-exposure. Chemosphere 61:267–275. doi:10.1016/j.chemosphere.2005.01.069
Almeida CMR, Mucha AP, Delgado MFC et al. (2008) Can PAHs influence Cu accumulation by salt marsh plants? Mar Environ Res 66:311–318. doi:10.1016/j.marenvres.2008.04.005
Almeida JR, Gravato C, Guilhermino L (2012) Challenges in assessing the toxic effects of polycyclic aromatic hydrocarbons to marine organisms: a case study on the acute toxicity of pyrene to the European seabass (Dicentrarchus labrax L.). Chemosphere 86:926–937. doi:10.1016/j.chemosphere.2011.10.059
Amado LL, Garcia ML, Ramos PB et al. (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123. doi:10.1016/j.scitotenv.2008.11.038
American Public Health Association, American Water Works Association, Water Environment Federation (2012) Standard methods for the examination of water and wastewater. Stand Methods 741. 10.2105/AJPH.51.6.940-a
Amiard-Triquet C, Rainbow PS (2009) Environmental assesment of estuarine ecosystems A case study. CRC press, Boca Raton
Banni M, Bouraoui Z, Clerandeau C et al. (2009) Mixture toxicity assessment of cadmium and benzo[a]pyrene in the sea worm Hediste diversicolor. Chemosphere 77:902–906. doi:10.1016/j.chemosphere.2009.08.041
Bouraoui Z, Banni M, Ghedira J et al. (2009) Evaluation of enzymatic biomarkers and lipoperoxidation level in Hediste diversicolor exposed to copper and benzo[a]pyrene. Ecotoxicol Environ Saf 72:1893–1898. doi:10.1016/j.ecoenv.2009.05.011
Bloom NS, Preus E (2003) Anoxic sediment incubations to assess the methylation potential of mercury contaminated solids. In: Tremblay H, Locat J, Galvez-Cloutier R (eds) Proceedings of the 2nd International Symposium on Contaminated Sediments; 2003 May 26-28, Quebec, Canada; p 331–336.
Broerse M, Oorsprong H, Van Gestel CAM (2012) Cadmium affects toxicokinetics of pyrene in the collembolan Folsomia candida. Ecotoxicol 21:795–802. doi:10.1007/s10646-011-0839-2
Cachot J, Geffard O, Augagneur S et al. (2006) Evidence of genotoxicity related to high PAH content of sediments in the upper part of the Seine estuary (Normandy, France). Aquat Toxicol 79:257–267. doi:10.1016/j.aquatox.2006.06.014
CCME (Canadian Council of Ministers of the Environment) (2002) Canadian sediment quality guidelines for the protection of aquatic life: summary tables. Updated 2002. Canadian Environmental Quality Guidelines (1999). Canadian Council of Ministers of the Environment, Winnipeg
Colacevich A, Sierra MJ, Borghini F et al. (2011) Oxidative stress in earthworms short- and long-term exposed to highly Hg-contaminated soils. J Hazard Mater 194:135–143. doi:10.1016/j.jhazmat.2011.07.091
Davis A, Bloom NS, Que Hee SS et al. (1997) The environmental geochemistry and bioaccessibility of mercury in soils and sediments: a review. Risk Anal 17:557–569. doi:10.1111/j.1539-6924.1997.tb00897.x
Díaz-Jaramillo M, Martins da Rocha A, Gomes V et al. (2011) Multibiomarker approach at different organization levels in the estuarine Perinereis gualpensis (Polychaeta; Nereididae) under chronic and acute pollution conditions. Sci Total Environ 410-411:126–135. doi:10.1016/j.scitotenv.2011.09.007
Díaz-Jaramillo M, Muñoz C, Rudolph I et al. (2013) Seasonal mercury concentrations and δ15N and δ13C values of benthic macroinvertebrates and sediments from a historically polluted estuary in south central Chile. Sci Total Environ 442:198–206. doi:10.1016/j.scitotenv.2012.10.039
Díaz-Jaramillo M, Sandoval N, Barra R et al. (2015) Spatio-temporal population and reproductive responses in Perinereis gualpensis (Polychaeta: Nereididae) from estuaries under different anthropogenic influences. Chem Ecol 1–12. 10.1080/02757540.2015.1022535
Gauthier PT, Norwood WP, Prepas EE, Pyle GG (2014) Metal-PAH mixtures in the aquatic environment: A review of co-toxic mechanisms leading to more-than-additive outcomes. Aquat Toxicol 154:253–269. doi:10.1016/j.aquatox.2014.05.026
Giessing AMB, Mayer LM, Forbes TL (2003) Synchronous fluorescence spectrometry of 1-hydroxypyrene: a rapid screening method for identification of PAH exposure in tissue from marine polychaetes. Mar Environ Res 56:599–615. doi:10.1016/S0141-1136(03)00045-X
Habig WH, Jakoby WB (1981) [51] Assays for differentiation of glutathione S-Transferases. Methods Enzymol 77:398–405. doi:10.1016/S0076-6879(81)77053-8
Hutchins C (2005) Geochemical Response of Cu, Zn & Cd Spiked sediment: A comparison of metal spiking procedures evaluated using whole sediment toxicity test. School of Enviornmental and Applied Sciences. Griffith University, Queensland, p 243, https://www120.secure.griffith.edu.au/rch/items/7697ff4c-be5e-1718-4891-f8ef013049d6/1/
Kopecka-Pilarczyk J, Correia AD (2009) Biochemical response in gilthead seabream (Sparus aurata) to in vivo exposure to pyrene and fluorene. J Exp Mar Bio Ecol 372:49–57. doi:10.1016/j.jembe.2009.02.004
Kovářová J, Svobodová Z (2009) Can thiol compounds be used as biomarkers of aquatic ecosystem contamination by cadmium? Interdiscip Toxicol 2:177–183. doi:10.2478/v10102-009-0013-3
Luís LG, Guilhermino L (2012) Short-term toxic effects of naphthalene and pyrene on the common prawn (Palaemon serratus) assessed by a multi-parameter laboratorial approach: mechanisms of toxicity and impairment of individual fitness. Biomarkers 17:275–285. doi:10.3109/1354750X.2012.666765
Lund B-O, Miller DM, Woods JS (1993) Studies on Hg(II)-induced H2O2 formation and oxidative stress in vivo and in vitro in rat kidney mitochondria. Biochem Pharmacol 45:2017–2024. doi:10.1016/0006-2952(93)90012-L
MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch Environ Contam Toxicol 39:20–31. doi:10.1007/s002440010075
Mai B-X, Fu J-M, Sheng G-Y et al. (2002) Chlorinated and polycyclic aromatic hydrocarbons in riverine and estuarine sediments from Pearl River Delta, China. Environ Pollut 117:457–474. doi:10.1016/S0269-7491(01)00193-2
Maria VL, Bebianno MJ (2011) Antioxidant and lipid peroxidation responses in Mytilus galloprovincialis exposed to mixtures of benzo(a)pyrene and copper. Comp Biochem Physiol Part C Toxicol Pharmacol 154:56–63. doi:10.1016/j.cbpc.2011.02.004
Mason R, Bloom N, Cappellino S et al. (1998) Investigation of porewater sampling methods for mercury and methylmercury. Environ Sci Technol 32:4031–4040. doi:10.1021/es980377t
Newman MC, Unger MA (2003) Fundamentals of Ecotoxicology, 2nd edn. Lewis Publishers, Inc, Boca Raton, FL, p 458
Oakes KD, Van Der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463
Oliveira M, Ribeiro A, Hylland K, Guilhermino L (2013) Single and combined effects of microplastics and pyrene on juveniles (0+group) of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Ecol Indic 34:641–647. doi:10.1016/j.ecolind.2013.06.019
Ouddane B, Mikac N, Cundy AB, et al (2008) A comparative study of mercury distribution and methylation in mudflats from two macrotidal estuaries: The Seine (France) and the Medway (United Kingdom). Appl Geochemistry 23:618–631. doi:10.1016/j.apgeochem.2007.11.001
Pozo K, Perra G, Menchi V et al. (2011) Levels and spatial distribution of polycyclic aromatic hydrocarbons (PAHs) in sediments from Lenga Estuary, central Chile. Mar Pollut Bull 62:1572–1576. doi:10.1016/j.marpolbul.2011.04.037
Richardson BJ, Mak E, De Luca-Abbott SB et al. (2008) Antioxidant responses to polycyclic aromatic hydrocarbons and organochlorine pesticides in green-lipped mussels (Perna viridis): do mussels “integrate” biomarker responses? Mar Pollut Bull 57:503–514. doi:10.1016/j.marpolbul.2008.02.032
Rodrigues NR, Nunes MEM, Silva DGC et al. (2013) Is the lobster cockroach Nauphoeta cinerea a valuable model for evaluating mercury induced oxidative stress? Chemosphere 92:1177–1182. doi:10.1016/j.chemosphere.2013.01.084
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205. doi:10.1016/0003-2697(68)90092-4
Shen G, Lu Y, Hong J (2006) Combined effect of heavy metals and polycyclic aromatic hydrocarbons on urease activity in soil. Ecotoxicol Environ Saf 63:474–480. doi:10.1016/j.ecoenv.2005.01.009
Sies H, Koch OR, Martino E, Boveris A (1979) Increased biliary glutathione disulfide release in chronically ethanol-treated rats. FEBS Lett 103:287–290. doi:10.1016/0014-5793(79)81346-0
Stoichev T, Amouroux D, Wasserman JC et al. (2004) Dynamics of mercury species in surface sediments of a macrotidal estuarine-coastal system (Adour River, Bay of Biscay). Estuar Coast Shelf Sci 59:511–521. doi:10.1016/j.ecss.2003.10.007
UNEP; IOC; IAEA. (1992) Determination of petroleum hydrocarbons in sediments. Ref Methods Mar Pollut Stud [S.1] 20:7
UNEP (2013) Global mercury assessment 2013: Sources, emissions, releases and environmental transport. UNEP Chemicals Branch, Geneva, Switzerland
USEPA. (1991) Method 245.5, mercury in sediments by cold vapor (CV/AAS). Revision 2.3. US Environmental Protection Agency Ofice of Research and Development, Cincinnati
Vega-López A, Ayala-López G, Posadas-Espadas BP et al. (2013) Relations of oxidative stress in freshwater phytoplankton with heavy metals and polycyclic aromatic hydrocarbons. Comp Biochem Physiol A Mol Integr Physiol 165:498–507. doi:10.1016/j.cbpa.2013.01.026
Wang L, Pan L, Liu N et al. (2011) Biomarkers and bioaccumulation of clam Ruditapes philippinarum in response to combined cadmium and benzo[α]pyrene exposure. Food Chem Toxicol 49:3407–3417. doi:10.1016/j.fct.2011.06.015
Wu Y, Wang WX (2012) Thiol compounds induction kinetics in marine phytoplankton during and after mercury exposure. J Hazard Mater 217-218:271–278. doi:10.1016/j.jhazmat.2012.03.024
Yañez J, Guajardo M, Miranda C et al. (2013) New assessment of organic mercury formation in highly polluted sediments in the Lenga estuary, Chile. Mar Pollut Bull 73:16–23. doi:10.1016/j.marpolbul.2013.06.015
Acknowledgements
This article is part of Díaz-Jaramillo’s PhD thesis, supervised by R. Barra and funded by a PhD fellowship “Corporación Red Universitaria Cruz del Sur (Chile)”. FONDAP CRHIAM CONICYT CHILE 15130015 is also acknowledged. We would also like to thank Laboratorio Costero de Recursos Acuáticos-Calfuco, Claudio Bravo, José M. Monserrat, Gilberto Fillman, Sandor Mulsow, Alice Turner, Soraya Céspedes, Ana Araneda, Solange Jara, Francesca Mitton and Mariana Gonzalez for the support during the laboratory assays and field sampling. This study was partially funded by ANPCyT of Argentina (Dr. Pedro Carriquiriborde, PICT-1598).
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Díaz-Jaramillo, M., Miglioranza, K.S.B., Carriquiriborde, P. et al. Sublethal effects in Perinereis gualpensis (Polychaeta: Nereididae) exposed to mercury-pyrene sediment mixture observed in a multipolluted estuary. Ecotoxicology 26, 792–801 (2017). https://doi.org/10.1007/s10646-017-1810-7
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DOI: https://doi.org/10.1007/s10646-017-1810-7