Neurotoxicity, Behavior, and Lethal Effects of Cadmium, Microplastics, and Their Mixtures on Pomatoschistus microps Juveniles from Two Wild Populations Exposed under Laboratory Conditions―Implications to Environmental and Human Risk Assessment
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals
2.2. Ethical Issues
2.3. Collection of Specimens and Samples
2.4. Acclimatization of Fish to Laboratory Conditions
2.5. Exposure Conditions of the Bioassays
2.6. Determination of Biomarkers
2.7. Statistical Analyses
3. Results and Discussion
3.1. Lethal Effects of Cadmium (Cd), Microplastics (MPs) and MPs-Cd Mixtures
3.2. Effects of Cadmium (Cd), Microplastics (MPs) and MPs-Cd Mixtures on Biomarkers
3.2.1. Effects of Cd, MPs and MPs-Cd Mixtures on Biomarkers of M-Est Juveniles
3.2.2. Effects of Cd, MPs, and MPs-Cd Mixtures on Biomarkers of L-Est Juveniles
3.3. Implications to Environmental and Human Risk Assessment
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- WHO. Preventing Disease through Healthy Environments. Exposure to Cadmium: A Major Public Health Concern; World Health Organization: Geneva, Switzerland, 2010. [Google Scholar]
- Ng, E.-L.; Lwanga, E.H.; Eldridge, S.M.; Johnston, P.; Hu, H.-W.; Geissen, V.; Chen, D. An overview of microplastic and nanoplastic pollution in agroecosystems. Sci. Total Environ. 2018, 627, 1377–1388. [Google Scholar] [CrossRef] [PubMed]
- Horton, A.A.; Walton, A.; Spurgeon, D.J.; Lahive, E.; Scendsen, C. Microplastics in freshwater and terrestrial environments: Evaluating the current understanding to identify the knowledge gaps and future research priorities. Sci. Total Environ. 2017, 586, 127–141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barboza, L.G.A.; Vethaak, A.D.; Lavorante, B.R.B.O.; Lundebye, A.-K.; Guilhermino, L. Marine microplastics debris: An emerging issue for food security, food safety and human health. Mar. Pollut. Bull. 2018, 133, 336–348. [Google Scholar] [CrossRef] [PubMed]
- Lehner, R.; Weder, C.; Petri-Fink, A.; Rothen-Rutishauser, B. Emergence of nanoplastic in the environment and possible impact on human health. Environ. Sci. Technol. 2019, 53, 81748–81765. [Google Scholar] [CrossRef] [PubMed]
- Nascimento, S.F.; Kurzweill, H.; Wruss, W.; Fenzl, N. Cadmium in the Amazonian Guajará estuary: Distribution and remobilization. Environ. Pollut. 2006, 140, 29–42. [Google Scholar] [CrossRef] [PubMed]
- Matović, V.; Buha, A.; Bulat, Z.; Đurić-Ćosić, D.; Bulat, Z. Inside into the oxidative stress induced by lead and/or cadmium in blood, liver and kidneys. Food Chem. Toxicol. 2015, 78, 130–140. [Google Scholar] [CrossRef] [PubMed]
- European Commission. Directive 2013/39/EU of the European parliament and of the council of 12 August 2013 amending directives 200/60/EC and 2008/105/EC as regards priority substances in the field of water policy. J. Eur. Union 2013, 226, 1–17. [Google Scholar]
- US EPA. Recommended Aquatic Life Ambient Water Quality Criteria for Cadmium; EPA HQ/OW/2015/0753, FRL 9944-46-OW, Document 2016-07647; US EPA: Washington, DC, USA, 2016.
- International Agency for Research on Cancer (IARC). Cadmium and cadmium compounds. In IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Vol. 58. Beryllium, Cadmium, Mercury, and Exposures in the Glass Manufacturing Industry; IARC: Lyon, France, 1993. [Google Scholar]
- Matović, V.; Buha, A.; Bulat, Z.; Đurić-Ćosić, D. Cadmium toxicity revisited: Focus on oxidative stress induction and interactions with zinc and magnesium. Arth. Hig. Rada Toksikol. 2011, 62, 65–76. [Google Scholar] [CrossRef]
- Caçador, I.; Costa, J.L.; Duarte, B.; Silva, G.; Medeiros, J.P.; Azeda, C.; Castro, N.; Freitas, J.; Pedro, S.; Almeida, P.R.; et al. Macroinvertebrates and fishes as biomonitors of heavy metal concentration in the Seixal Bay (Tagus estuary): Which species perform better? Ecol. Indic. 2012, 19, 184–190. [Google Scholar] [CrossRef]
- Bosch, A.C.; O’Neill, B.; Sigge, G.O.; Kerwath, S.E.; Hoffman, L.C. Heavy metals in marine fish meat and consumer health: A review. J. Sci. Food Agric. 2016, 96, 32–48. [Google Scholar] [CrossRef]
- Zhao, X.-M.; Yao, L.-A.; Ma, Q.-L.; Zhou, G.-J.; Wang, L.; Fang, Q.-L. Distribution and ecological risk assessment of cadmium in water and sediment in Longjiang River, china: Implications on water quality management after pollution accident. Chemosphere 2018, 194, 107–116. [Google Scholar] [CrossRef]
- de Araújo, M.C.; Assis, C.R.D.; Silva, L.C.; Machado, D.C.; Silva, K.C.C.; Lima, A.V.A.; Carvalho, L.B., Jr.; de Souza Bezerra, S.; Oliveira, M.B.M. Brain acetylcholinesterase of jaguar cichlid (Parachromis managuensis): From physicochemical and kinetic properties to its potential as biomarker of pesticides and metal ions. Aquat. Toxicol. 2016, 177, 182–189. [Google Scholar] [CrossRef]
- Liu, X.-J.; Luo, Z.; Li, C.-H.; Xiong, B.-X.; Zhao, Y.-H.; Li, X.-D. Antioxidant responses, hepatic intermediary metabolism, histology and ultrastructure in Synechogobius hasta exposed to waterborne cadmium. Ecotoxicol. Environ. Saf. 2011, 74, 1156–1163. [Google Scholar] [CrossRef]
- Dew, W.A.; Veldhoen, N.; Carew, A.C.; Helbing, C.C.; Pye, G.G. Cadmium-induced olfactory dysfunction in rainbow trout: Effects of binary and quaternary metal mixtures. Aquat. Toxicol. 2016, 172, 86–94. [Google Scholar] [CrossRef]
- Wang, C.-C.; Si, L.-F.; Guo, S.-N.; Zheng, J.-L. Negative effects of acute cadmium on stress defense, immunity, and metal homeostasis in liver of zebrafish: The protective role of environmental zinc pre-exposure. Chemosphere 2019, 222, 91–97. [Google Scholar] [CrossRef]
- Pereira, L.S.; Ribas, J.L.C.; Vicari, T.; Silva, S.B.; Stival, J.; Baldan, A.P.; Valdez Domingos, F.X.; Grassi, M.T.; Cestari, M.M.; Silva de Assis, H.C. Effects of ecologically relevant concentrations of cadmium in a freshwater fish. Ecotoxicol. Environ. Saf. 2016, 130, 29–36. [Google Scholar] [CrossRef]
- Pan, H.; Zhang, X.; Ren, B.; Yang, H.; Ren, Z.; Wang, W. Toxic assessment of cadmium based online swimming behaviour and the continuous AChE activity in the gill of zebrafish. Water Air Soil Pollut. 2017, 228, 355. [Google Scholar] [CrossRef]
- Giari, L.; Manera, M.; Simoni, E.; Dezfuli, B.S. Cellular alterations in diferente organs of European sea bass Dicentrarchus labrax (L.) exposed to cadmium. Chemosphere 2007, 67, 1171–1181. [Google Scholar] [CrossRef]
- Hani, Y.M.I.; Turies, C.; Palluel, O.; Delahaut, L.; Bado-Nilles, A.; Geffard, A.; Dedourge-Geffard, O.; Porcher, J.-M. Effects of a chronic exposure to different water temperatures and/or to an environmental cadmium concentration on the reproduction of the threespine stickleback (Gasterosteus aculeatus). Ecotoxicol. Environ. Saf. 2019, 174, 48–57. [Google Scholar] [CrossRef]
- Krzykwa, J.C.; Saeid, A.; Jeffries, M.K.S. Identifying sublethal endpoints for evaluating neurotoxic compounds utilizing the fish embryo toxicity test. Ecotoxicol. Environ. Saf. 2019, 170, 521–529. [Google Scholar] [CrossRef]
- Raimundo, J.; Vale, C.; Martins, I.; Fontes, J.; Graça, G.; Caetano, M. Elemental composition of two ecologically contrasting seamount fishes, the bluemouth (Helicolenus dactylopterus) and blackspot seabream (Pagellus bogaraveo). Mar. Pollut. 2015, 100, 112–121. [Google Scholar] [CrossRef]
- Andrady, A.L. The plastic in microplastics. Mar. Pollut. Bull. 2017, 119, 12–22. [Google Scholar] [CrossRef]
- Lasee, S.; Maurício, J.; Thompson, W.A.; Karnjanapiboonwong, A.; Kasumba, J.; Subbiah, S.; Morse, A.N.; Anderson, T.A. Microplastics in a freshwater environment receiving treated wastewater effluent. Integr. Environ. Assess. Manag. 2017, 13, 528–532. [Google Scholar] [CrossRef]
- Antunes, J.; Frias, J.; Sobral, P. Microplastics in the Portuguese coast. Mar. Pollut. Bull. 2018, 131, 294–302. [Google Scholar] [CrossRef]
- Barrows, A.P.W.; Cathey, S.E.; Petersen, C.W. Marine environment microfiber contamination: Global patherns and the diversity of microparticle origins. Environ. Pollut. 2018, 237, 275–284. [Google Scholar] [CrossRef]
- Hartmann, N.B.; Rist, S.; Bodin, J.; Jensen, L.H.; Schmidt, S.N.; Mayer, P.; Meibom, A.; Baun, A. Microplastics as vectors for environmental contaminants: Exploring sorption, desorption, and transfer to biota. Integr. Environ. Assess. Manag. 2017, 13, 488–493. [Google Scholar] [CrossRef] [Green Version]
- Hahladakis, J.N.; Velis, C.A.; Weber, R.; Lacovidou, E.; Purnell, P. An overview of chemical additives present in plastics: Migration, release, fate and environmental impact during their use, disposal and recycling. J. Hazard. Mater. 2018, 344, 179–199. [Google Scholar] [CrossRef]
- Wright, S.L.; Kelly, J.F. Plastic and human health: A micro issue? Environ. Sci. Technol. 2017, 51, 6634–6647. [Google Scholar] [CrossRef]
- Neves, D.; Sobral, P.; Ferreira, J.L.; Pereira, T. Ingestion of microplastics by commercial fish of the Portuguese coast. Mar. Pollut. Bull. 2015, 101, 119–126. [Google Scholar] [CrossRef]
- Rochman, C.M.; Tahir, A.; Williams, S.L.; Baxa, D.V.; Lam, R.; Miller, J.T.; Teh, F.-C.; Werorilangi, S.; Teh, S.J. Anthropogenic debris in seafood: Plastic debris and fibers from textiles in fish and bivalves sold for human consumption. Sci. Rep. 2015, 5, 14340. [Google Scholar] [CrossRef]
- Bessa, F.; Barría, P.; Neto, J.M.; Frias, J.P.; Otero, V.; Sobral, P.; Marques, J.C. Occurrence of microplastics in commercial fish from a natural estuarine environment. Mar. Pollut. Bull. 2018, 128, 575–584. [Google Scholar] [CrossRef]
- Abbasi, S.; Soltani, N.; Keshavarzi, B.; Moore, F.; Turner, A.; Hassanaghaei, M. Microplastics in different tissues of fish and prawn from the Musa Estuary, Persian Gulf. Chemosphere 2018, 205, 80–87. [Google Scholar] [CrossRef]
- Akhbarizadeh, R.; Moore, F.; Keshavarzi, B. Investigating a probable relationship between microplastics and potentially toxic elements in fish muscles from northeast of Persian Gulf. Environ. Pollut. 2018, 232, 154–163. [Google Scholar] [CrossRef]
- Smith, M.; Love, D.C.; Rochman, C.M.; Neff, R.A. Microplastics in seafood and the implications for human health. Curr. Environ. Health Rep. 2018, 5, 375–386. [Google Scholar] [CrossRef]
- Oliveira, M.; Ribeiro, A.; Hylland, K.; Guilhermino, L. Single and combined effects of microplastics and pyrene on juveniles (0+ group) of the common goby Pomatoschistus microps (Teleostei: Gobiidae). Ecol. Indic. 2013, 34, 641–647. [Google Scholar] [CrossRef]
- Ding, J.; Zhang, S.; Razanajatovo, R.M.; Zou, H.; Zhu, W. Accumulation, tissue distribution, and biochemical effects of polystyrene microplastics in the freshwater fish red tilapia (Oreochromis niloticus). Environ. Pollut. 2018, 238, 1–9. [Google Scholar] [CrossRef]
- Barboza, L.G.A.; Vieira, L.R.; Branco, V.; Carvalho, C.; Guilhermino, L. Microplastics increase mercury bioconcentration in gills and bioaccumulation in the liver, and cause oxidative stress and damage in Dicentrarchus labrax juveniles. Sci. Rep. 2018, 8, 15655. [Google Scholar] [CrossRef]
- Barboza, L.G.A.; Vieira, L.R.; Branco, V.; Figueiredo, N.; Carvalho, F.; Carvalho, C.; Guilhermino, L. Microplastics cause neurotoxicity, oxidative damage and energy-related changes and interact with the bioaccumulation of mercury in the European seabass Dicentrarchus labrax (Linnaeus, 1758). Aquat. Toxicol. 2018, 195, 49–57. [Google Scholar] [CrossRef]
- Wen, B.; Zhang, N.; Jin, S.R.; Chen, Z.Z.; Gao, J.Z.; Liu, Y.; Liu, H.P.; Xu, Z. Microplastics have a more profound impact than elevated temperatures on the predatory performance, digestion and energy metabolism of an Amazonian cichlid. Aquat. Toxicol. 2018, 195, 67–76. [Google Scholar] [CrossRef]
- Pedà, C.; Caccamo, L.; Fossi, M.C.; Cai, F.; Andaloro, F.; Genovese, L.; Perdichizzi, A.; Romeo, T.; Maricchiolo, G. Intestinal alterations in European sea bass Dicentrarchus labrax (Linnaeus, 1758) exposed to microplastics: Preliminary results. Environ. Pollut. 2016, 212, 251–256. [Google Scholar] [CrossRef]
- Lei, L.; Wu, S.; Lu, S.; Liu, M.; Song, Y.; Fu, Z.; Shi, H.; Raley-susman, K.M.; He, D. Microplastic particles cause intestinal damage and other adverse effect in zebrafish Danio rerio and nematode Caenorhabditis elegans. Sci. Total Environ. 2018, 619–620, 1–8. [Google Scholar] [CrossRef]
- Yin, L.; Chen, B.; Xia, B.; Shi, X.; Qu, K. Polystyrene microplastics alter the behavior, energy reserve and nutritional composition of marine jacopever (Sebastes schlegelii). J. Hazard. Mater. 2018, 360, 97–105. [Google Scholar] [CrossRef]
- Luis, L.G.; Ferreira, P.; Fonte, E.; Oliveira, M.; Guilhermino, L. Does the presence of microplastics influence the acute toxicity of chromium (VI) to early juveniles of the common goby (Pomatoschistus microps)? A study with juveniles from two wild estuarine populations. Aquat. Toxicol. 2015, 164, 163–174. [Google Scholar] [CrossRef]
- Barboza, L.G.A.; Vieira, L.R.; Guilhermino, L. Single and combined effects of microplastics and mercury on juveniles of the European seabass (Dicentrarchus labrax): Changes in behavioural responses and reduction of swimming velocity and resistance time. Environ. Pollut. 2018, 236, 1014–1019. [Google Scholar] [CrossRef]
- Choi, J.S.; Jung, Y.-J.; Hong, N.-H.; Hong, S.H.; Park, J.-W. Toxicological effects of irregularly shaped and spherical microplastics in a marine teleost, the sheepshead minnow (Cyprinodon variegatus). Mar. Pollut. Bull. 2018, 129, 231–240. [Google Scholar] [CrossRef]
- Rochman, C.M.; Kurobe, T.; Flores, I.; Teh, S.J. Early warning signs of endocrine disruption in adult fish from the ingestion of polyethylene with and without sorbed chemical pollutants from the marine environment. Sci. Total Environ. 2014, 493, 656–661. [Google Scholar] [CrossRef]
- Alimba, C.G.; Faggio, C. Microplastics in the marine environment: Current trends in environmental pollution and mechanisms of toxicological profile. Environ. Toxicol. Pharmacol. 2019, 68, 61–74. [Google Scholar] [CrossRef]
- Franzellitti, S.; Canesi, L.; Auguste, M.; Wathsala, R.H.G.R.; Fabbri, E. Microplastic exposure and effects in aquatic organisms: A physiological perspective. Environ. Toxicol. Pharmacol. 2019, 68, 37–51. [Google Scholar] [CrossRef]
- Guilhermino, L.; Vieira, L.R.; Ribeiro, D.; Tavares, A.S.; Cardoso, V.; Alves, A.; Almeida, J.M. Uptake and effects of the antimicrobial florfenicol, microplastics and their mixtures on freshwater exotic invasive bivalve Corbicula fluminea. Sci. Total Environ. 2018, 622–623, 1131–1142. [Google Scholar] [CrossRef]
- Lebreton, L.C.M.; van der Zwet, J.; Damsteeg, J.-W.; Slat, B.; Andrady, A.; Reisser, J. River plastic emissions to the world’s oceans. Nat. Commun. 2017, 8, 15611. [Google Scholar] [CrossRef]
- Rodrigues, S.M.; Almeida, C.M.R.; Silva, D.; Cunha, J.; Antunes, C.; Freitas, V.; Ramos, S. Microplastic contamination in an urban estuary: Abundance and distribution of microplastics and fish larvae in the Douro estuary. Sci. Total Environ. 2019, 659, 1071–1081. [Google Scholar] [CrossRef]
- Holmes, L.A.; Turner, A.; Thompson, R.C. Interactions between trace metals and plastic production pellets under estuarine conditions. Mar. Chem. 2014, 167, 25–32. [Google Scholar] [CrossRef]
- Rochman, C.M.; Hentschel, B.T.; Teh, S.J. Long-term sorption of metals is similar among plastic types: Implications for plastic debris in aquatic environments. PLoS ONE 2014, 9, e85433. [Google Scholar] [CrossRef]
- Lu, K.; Quiao, R.; An, H.; Zhang, Y. Influence of microplastics on the accumulation and chronic toxic effects of cadmium in zebrafish (Danio rerio). Chemosphere 2018, 202, 514–520. [Google Scholar] [CrossRef]
- Wen, B.; Jin, S.R.; Chen, Z.Z.; Gao, J.Z.; Liu, Y.N.; Liu, J.H.; Feng, X.S. Single and combined effects of microplastics and cadmium on the cadmium accumulation, antioxidant defence and innate immunity of the discus fish (Symphysodon aequifasciatus). Environ. Pollut. 2018, 243, 462–471. [Google Scholar] [CrossRef]
- Salgado, J.P.; Cabral, H.N.; Costa, M.J. Feeding ecology of the gobies Pomatoschistus minutus (Pallas, 1770) and Pomatoschistus microps (Krøyer, 1838) in the upper Tagus estuary, Portugal. Sci. Mar. 2004, 68, 425–434. [Google Scholar] [CrossRef]
- Ferreira, P.; Fonte, E.; Soares, M.E.; Carvalho, F.; Guilhermino, L. Effects of multi-stressors on juveniles of the marine fish Pomatoschistus microps: Gold nanoparticles, microplastics and temperature. Aquat. Toxicol. 2016, 170, 89–103. [Google Scholar] [CrossRef]
- Monteiro, M.; Quintaneiro, C.; Nogueira, A.J.A.; Morgado, F.; Soares, A.M.V.M.; Guilhermino, L. Impact of chemical exposure on the fish Pomatoschistus micropsis Krøyer (1838) in estuaries of the Portuguese Northwest coast. Chemosphere 2007, 66, 514–522. [Google Scholar] [CrossRef]
- Vieira, L.R.; Soares, A.M.V.M.; Morgado, F.; Guilhermino, L. Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: Linking biomarkers to behaviour. Chemosphere 2009, 76, 1416–1427. [Google Scholar] [CrossRef]
- Fonte, E.; Ferreira, P.; Guilhermino, L. Temperature rise and microplastics interact with the toxicity of the antibiotic cefalexin to juveniles of the common goby (Pomatoschistus microps): Post-exposure predatory behaviour, acetylcholinesterase activity and lipid peroxidation. Aquat. Toxicol. 2016, 180, 173–185. [Google Scholar] [CrossRef]
- de Sá, L.C.; Luís, L.G.; Guilhermino, L. Effects of microplastics on juveniles of the common goby (Pomatoschistus microps): Confusion with prey, reduction of the predatory performance and efficiency, and possible influence of developmental conditions. Environ. Pollut. 2015, 196, 359–362. [Google Scholar] [CrossRef]
- Guimarães, L.; Medina, M.H.; Guilhermino, L. Health status of Pomatoschistus microps populations in relation to pollution and natural stressors: Implications for ecological risk assessment. Biomarkers 2012, 17, 62–77. [Google Scholar] [CrossRef]
- Baeta, A.; Vieira, L.R.; Lírio, A.V.; Canhoto, C.; Marques, J.C.; Guilhermino, L. Use of stable isotope ratios of fish larvae as indicators to assess diets and patterns of anthropogenic nitrogen pollution in estuarine ecosystems. Ecol. Indic. 2017, 83, 112–121. [Google Scholar] [CrossRef] [Green Version]
- Medina-Gómez, I.; Kjerfve, B.; Mariño, I.; Herrera-Silveira, J. Sources of salinity variation in a coastal lagoon in a Karst landscape. Estuar. Coasts 2014, 37, 1329–1342. [Google Scholar] [CrossRef]
- OECD. Test No. 203: Fish, Acute Toxicity Test. In OECD Guidelines for the Testing of Chemicals, Section 2; OECD Publishing: Paris, France, 1992. [Google Scholar] [CrossRef]
- Miranda Maciel, T.F. Toxic Effects of Cadmium, Alone and in Combination with Microplastics, on Early Juveniles of the Common Goby (Pomatoschistus microps) in Relation to Previous Long-Term Exposure to Environmental Contamination. Master’s Thesis, Institute of Biomedical Sciences of Abel Salazar and Faculty of Sciences of the University of Porto, Porto, Portugal, 2014. [Google Scholar]
- Avio, C.G.; Gorbi, S.; Regoli, F. Plastics and microplastics in the oceans: From emerging pollutants to emerged threat. Mar. Environ. Res. 2017, 128, 2–11. [Google Scholar] [CrossRef]
- Usero, J.; Izquierdo, C.; Morillo, J.; Gracia, I. Heavy metals in fish (Solea vulgaris, Anguilla anguilla and Liza aurata) from salt marshes on the southern Atlantic coast of Spain. Environ. Int. 2003, 29, 949–956. [Google Scholar] [CrossRef]
- Diop, M.; Howsam, M.; Diop, C.; Cazier, F.; Goossens, J.F.; Diouf, A.; Amara, R. Spatial and seasonal variations of trace elements concentrations in liver and muscle of round sardinelle (Sardinella aurita) and Senegalese sole (Solea senegalensis) along the Senegalese coast. Chemosphere 2016, 144, 758–766. [Google Scholar] [CrossRef]
- de Lima, D.; Roque, G.M.; de Almeida, E.A. In vitro and in vivo inhibition of acetycholinesterase and carboxylesterase by metals in zebrafish (Danio rerio). Mar. Environ. Res. 2013, 91, 45–51. [Google Scholar] [CrossRef]
- Monteiro, M.; Quintaneiro, C.; Morgado, F.; Soares, A.M.V.M.; Guilhermino, L. Characterization of the cholinesterases presente in head tissues of the estuarine fish Pomatoschistus micropsis: Application to biomonitoring. Ecotoxicol. Environ. Saf. 2005, 62, 341–347. [Google Scholar] [CrossRef]
- Bradford, M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Guilhermino, L.; Lopes, M.C.; Carvalho, A.P.; Soares, A.M.V.M. Acetylcholinesterase activity in juveniles of Daphnia magna Straus. Bull. Environ. Contam. Toxicol. 1996, 57, 979–985. [Google Scholar] [CrossRef]
- Ellman, G.L.; Courtney, K.D.; Andres, V., Jr.; Feather-Stone, R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 1961, 7, 88–95. [Google Scholar] [CrossRef]
- Habig, W.H.; Pabst, M.J.; Jakoby, W.B. Glutathione-S-transferases, the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974, 249, 7130–7139. [Google Scholar]
- Frasco, M.F.; Guilhermino, L. Effects of dimethoate and betanaphthofavone on selected biomarkers of Poecilia reticulata. Fish Physiol. Biochem. 2002, 26, 149–156. [Google Scholar] [CrossRef]
- Ohkawa, H. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95, 351–358. [Google Scholar] [CrossRef]
- Bird, R.P.; Draper, A.H. Comparative studies on different methods of malondyhaldehyde determination. Methods Enzymol. 1984, 90, 105–110. [Google Scholar]
- Torres, M.A.; Testa, C.P.; Gaspari, C.; Masutti, M.B.; Panitz, C.M.N.; Curi-Pedrosa, R.; de Almeida, E.A.; Di Mascio, P.; Wilhelm, D. Oxidative stress in the mussel Mytella gyyanensis from polluted mangroves on Santa Catarina Island. Braz. Mar. Pollut. Bull. 2002, 44, 923–932. [Google Scholar] [CrossRef]
- Zar, J.H. Biostatistical Analysis; Prentice Hall: Upper Saddle River, NJ, USA, 1999. [Google Scholar]
- Finney, D.J. Probit Analysis, 3rd ed.; Cambridge Press: New York, NY, USA, 1971. [Google Scholar]
- Gelli, F.; Cicero, A.M.; Melotti, P.; Roncarati, A.; Pregnolato, L.; Savorelli, F.; Palazzi, D.; Gasazza, G. A proposal of method to evaluate the quality of marine waters: Optimization of 7 days bioassays using Dicentrarchus labrax (L.) juveniles. Chem. Ecol. 2004, 20 (Suppl. 1), 225–229. [Google Scholar] [CrossRef]
- Thophon, S.; Kruatrachue, M.; Upatham, E.S.; Pokethitiyook, P.; Sahaphong, S.; Jaritkhuan, S. Histopatological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environ. Pollut. 2003, 121, 307–320. [Google Scholar] [CrossRef]
- Sassi, A.; Darias, M.J.; Said, K.; Messaoudi, I.; Gisbert, E. Cadmium exposure affects the expression of genes involved in skeletogenesis and stress response in gilthead sea bream larvae. Fish Physiol. Biochem. 2013, 39, 649–659. [Google Scholar] [CrossRef]
- Zhang, T.; Yang, M.; Pan, H.; Li, S.; Ren, B.; Ren, Z.; Xing, N.; Qi, L.; Ren, Q.; Xu, S.; et al. Does time difference of the acetylcholinesterase (AChE) inhibition in different tissues exist? A case study of zebra fish (Danio rerio) exposed to cadmium chloride and deltamethrin. Chemosphere 2017, 168, 908–916. [Google Scholar] [CrossRef]
- Pino, J.D.; Zeballos, G.; Anadon, M.J.; Díaz, M.J.; Moyano, P.; Díaz, G.G.; García, J.; Lobo, M.; Frejo, M.T. Muscarinic M1 receptor partially modulates higher sensitivity to cadmium-induced cell death in primary basal forebrain cholinergic neurons: A cholinesterase variants dependent mechanism. Toxicology 2016, 361–362, 1–11. [Google Scholar] [CrossRef]
- Alsop, D.; Wood, C.M. Metal and pharmaceutical mixtures: Is ion loss the mechanism underlying acute toxicity and widespread additive toxicity in zebrafish? Aquat. Toxicol. 2013, 140–141, 257–267. [Google Scholar] [CrossRef]
- Moyano, P.; de Frias, M.; Lobo, M.; Anadon, M.J.; Sola, E.; Pelayo, A.; Díaz, M.J.; Frejo, M.T.; Del Pino, J. Cadmium induced ROS alters M1 and M3 receptors, leading to SN56 cholinergic neuronal loss, through AChE variants disruption. Toxicology 2018, 394, 54–62. [Google Scholar] [CrossRef]
- Garcia-Santos, S.; Fontaínhas-Fernandes, A.; Wilson, J.M. Cadmium tolerance in the Nile tilapia (Oreochromis niloticus) following acute exposure: Assessment of some ionoregulatory parameters. Environ. Toxicol. 2006, 21, 33–46. [Google Scholar] [CrossRef]
- Morcillo, P.; Esteban, M.A.; Cuesta, A. Heavy metals produce toxicity, oxidative stress and apoptosis in the marine teleost fish SAF-1 cell line. Chemosphere 2016, 144, 225–233. [Google Scholar] [CrossRef]
- Qi, L.; Ma, J.; Song, J.; Li, S.; Cui, X.; Peng, X.; Wang, W.; Ren, Z.; Han, M.; Zhang, Y. The physiological characteristics of zebra fish (Danio rerio) based on metabolism and behavior: A new method for the online assessment of cadmium stress. Chemosphere 2017, 184, 1150–1156. [Google Scholar] [CrossRef]
- Frasco, M.-F.; Fournier, D.; Carvalho, C.; Guilhermino, L. Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as biomarker of metal toxicity. Biomarkers 2005, 10, 360–375. [Google Scholar] [CrossRef]
- Pretto, A.; Loro, V.L.; Morsch, V.M.; Moraes, B.S.; Menezes, C.; Clasen, B.; Hoehne, L.; Dressler, V. Acetylcholinesterase activity, lipid peroxidation, and bioaccumulation in silver catfish (Rhamdia quelen) exposed to cadmium. Arch. Environ. Contam. Toxicol. 2010, 58, 1008–1014. [Google Scholar] [CrossRef]
- Gupta, R.; Shukla, R.K.; Chandravanshi, L.P.; Srivastava, P.; Dhuryya, Y.K.; Shanker, J.; Singh, M.P.; Pant, A.B.; Khanna, V.K. Protective role of quercetin in cadmium-induced cholinergic dysfunctions in rat brain by modulating mitochondrial integrity and MAP kinase signaling. Mol. Neurobiol. 2017, 54, 4560–4583. [Google Scholar] [CrossRef]
- Vivek, K.G.; Abhishek, K.; Nikhat, J.S.; Bechan, S. Rat brain acetyl cholinesterase as a biomarker of cadmium induced neurotoxicity. Open Access J. Toxicol. 2016, 1, 555553. [Google Scholar]
- Naïja, A.; Kestemont, P.; Chénais, B.; Haouas, Z.; Blust, R.; Helal, A.N.; Marchand, J. Cadmium exposure exerts neurotoxic effects in peacock blennies Salaria pavo. Ecotoxicol. Environ. Saf. 2017, 143, 217–227. [Google Scholar] [CrossRef]
- Rani, S.; Gupta, R.K.; Yadav, J. Heavy metal induced alterations in acetylcholinesterase activity of Indian major carps. J. Entomol. Zool. Stud. 2017, 5, 819–821. [Google Scholar]
- Gill, T.S.; Tewari, H.; Pande, J. In vivo and in vitro effects of cadmium on selected enzymes in different organs of the fish Barbus conchonius ham. (Rosy Barb). Comp. Biochem. Physiol. Part C 1991, 100, 501–505. [Google Scholar] [CrossRef]
- Souid, G.; Souayed, N.; Yaktiti, F.; Maaroufi, K. Effect of acute cadmium exposure on metal accumulation and oxidative stress biomarkers of Sparus aurata. Ecotoxicol. Environ. Saf. 2013, 89, 1–7. [Google Scholar] [CrossRef]
- Jebali, J.; Banni, M.; Guerbej, H. Effects of malathion and cadmium on acetylcholinesterase activity and metallothionein levels in the fish Seriola dumerilli. Fish Physiol. Biochem. 2006, 32, 93–98. [Google Scholar] [CrossRef]
- Cattani, O.; Serra, R.; Isani, G.; Raggi, G.; Cortesi, P.; Carpene, E. Correlation between metallotionein and energy metabolismo in sea bass, Dicentrarchus labrax, exposed to cadmium. Comp. Biochem. Physiol. 1996, 113C, 193–199. [Google Scholar]
- Mattsson, K.; Johnson, E.V.; Malmendal, A.; Linse, S.; Hansson, L.A.; Cedervall, T. Brain damage and behavioural disorders in fish induced by plastic nanoparticles delivered through the food chain. Sci. Rep. 2017, 7, 11452. [Google Scholar] [CrossRef]
- Ribeiro, F.; Garcia, A.R.; Pereira, B.P.; Fonseca, M.; Mestre, N.C.; Fonseca, T.G.; Ilharco, L.M.; Bebianno, M.J. Microplastics effects in Scrobicularia plana. Mar. Pollut. Bull. 2017, 122, 379–391. [Google Scholar] [CrossRef]
- Karami, A.; Golieskardi, A.; Ho, Y.B.; Larat, V.; Salamatinia, B. Microplastics in eviscerated flesh and excised organs of dried fish. Sci. Rep. 2017, 7, 5473. [Google Scholar] [CrossRef]
- Van Cauwenberghe, L.; Janssen, C.R. Microplastics in bivalves cultured for human consumption. Environ. Pollut. 2014, 193, 65–70. [Google Scholar] [CrossRef]
- Santillo, D.; Miller, K.; Johnston, P. Microplastics as contaminants in commercially important seafood species. Integr. Environ. Assess. Manag. 2017, 13, 516–552. [Google Scholar] [CrossRef]
- Li, J.; Green, C.; Reynolds, A.; Shi, H.; Rotchell, J.M. Microplastics in mussels sampled from coastal waters and supermarkets in the United Kingdom. Environ. Pollut. 2018, 241, 35–44. [Google Scholar] [CrossRef]
- Peixoto, D.; Pinheiro, C.; Amorim, J.; Oliva-Teles, L.; Guilhermino, L.; Vieira, M.N. Microplastic pollution in commercial salt for human consumption: A review. Estuar. Coast. Shelf Sci. 2019, 219, 161–168. [Google Scholar] [CrossRef]
- Prata, J.C. Airborne microplastics: Consequences to human health? Environ. Pollut. 2018, 234, 115–126. [Google Scholar] [CrossRef]
- Schwabl, P.; Liebmann, B.; Köppel, S.; Königshofer, P.; Bucsics, T.; Trauner, M.; Reiberger, T. Assessment of microplastics concentrations in human stool—Preliminary results of a prospective study. UEG J. 2018, 6, A127. [Google Scholar]
- Besseling, E.; Wang, B.; Lürling, M.; Koelmans, A.A. Nanoplastics affects growth of S. obliquus and reproduction of Daphnia magna. Environ. Sci. Technol. 2014, 48, 12336–12343. [Google Scholar] [CrossRef]
- Pacheco, A.; Martins, A.; Guilhermino, L. Toxicological interactions induced by chronic exposure to gold nanoparticles and microplastics mixtures in Daphnia magna. Sci. Total Environ. 2018, 628–629, 474–483. [Google Scholar] [CrossRef]
- Martins, A.; Guilhermino, L. Transgerational effects and recovery of microplastics exposure in model populations of the freshwater cladoceran Daphnia magna Straus. Sci. Total Environ. 2018, 631–632, 421–428. [Google Scholar] [CrossRef]
- Foley, C.J.; Feiner, Z.S.; Malinich, T.D.; Höök, T.O. A meta-analysis of the effects of exposure to microplastics on fish and aquatic invertebrates. Sci. Total Environ. 2018, 631–632, 550–559. [Google Scholar] [CrossRef]
- Schirinzi, G.F.; Pérez-Pomeda, I.; Sanchís, J.; Rossini, C.; Farré, M.; Barceló, D. Cytotoxic effects of commonly used nanomaterials and microplastics on cerebral and epitelial human cells. Environ. Res. 2017, 159, 579–587. [Google Scholar] [CrossRef]
- Karami, A.; Romano, N.; Galloway, T.; Hamzah, H. Virgin microplastics cause toxicity and modulate the impacts of phenanthrene on biomarker responses in African catfish (Clarias gariepinus). Environ. Res. 2016, 151, 58–70. [Google Scholar] [CrossRef]
- Sussarellu, R.; Fabioux, C.; Guyomarch, J.; Albentosa, M.; Huvet, A.; Soudant, P. Exposure of marine mussels Mytilus spp. to polystyrene microplastics: Toxicity and influence on fluoranthene bioaccumulation. Environ. Pollut. 2016, 216, 724–737. [Google Scholar]
- Gramby, K.; Rainieri, S.; Rasmussen, R.R.; Kotterman, M.J.J.; Sloth, J.J.; Cederberg, T.L.; Barranco, A.; Marques, A.; Larsen, B.K. The influence of microplastics and halogenated contaminants in feed on toxicokinetics and gene expression in European seabass (Dicentrarchus labrax). Environ. Res. 2018, 164, 430–443. [Google Scholar] [CrossRef]
- Khan, F.R.; Syberg, K.; Shashoua, Y.; Bury, N.R. Influence of polyethylene microplastic beads on the uptake and localization of silver in zebrafish (Danio rerio). Environ. Pollut. 2015, 206, 73–79. [Google Scholar] [CrossRef]
- Kim, D.; Chae, Y.; An, Y.-J. Mixture toxicity of nickel and microplastics with different functional groups on Daphnia magna. Environ. Sci. Technol. 2017, 51, 12852–12858. [Google Scholar] [CrossRef]
Bioassay | Minho Estuary Fish | Lima Estuary Fish | ||||||||
LC10 (mg/L) | LC20 (mg/L) | LC50 (mg/L) | LC10 (mg/L) | LC20 (mg/L) | LC50 (mg/L) | |||||
Cd | 2 (0–5) | 3 (0–7) | 7 (2–17) | 2 (0–5) | 3 (0–7) | 9 (0–54) | ||||
Cd + MP | 2 (0–5) | 3 (0–7) | 7 (2–17) | 2 (0–4) | 2 (0–5) | 5 (0–14) | ||||
Overall: Fish from Both Estuaries | ||||||||||
Cd | Cd + MP | |||||||||
LC10 (mg/L) | LC20 (mg/L) | LC50 (mg/L) | LC10 (mg/L) | LC20 (mg/L) | LC50 (mg/L) | |||||
2 (0–4) | 3 (0–6) | 8 (2–17) | 2 (0–4) | 3 (0–6) | 9 (0–15) | |||||
Biomarkers | ||||||||||
Biomarker | Contaminants | M-Est Fish | L-Est Fish | |||||||
NOEC (mg/L) | LOEC (mg/L) | NOEC (mg/L) | LOEC (mg/L) | |||||||
PEPP | Cd MP Cd + MP | 3 0.14 3 | 6 >0.14 6 | <3 <0.14 <3 | 3 0.14 3 | |||||
AChE | Cd MP Cd + MP | 6 0.14 13 | 13 >0.14 >13 | 13 <0.14 3 | > 13 0.14 6 | |||||
GST | Cd MP Cd + MP | 13 0.14 13 | >13 >0.14 >13 | 13 0.14 13 | >13 >0.14 >13 | |||||
LPO | Cd MP Cd + MP | 13 0.14 13 | >13 >0.14 >13 | 13 0.14 13 | >13 >0.14 >13 |
BIOM | FAC | Level | Minho Estuary Fish | Lima Estuary Fish | ||||
---|---|---|---|---|---|---|---|---|
N | Mean ± SD | ANOVA Results | N | Mean ± SD | ANOVA Results | |||
Pred. | Cd | 0 mg/L | 18 | 80 ± 17 a | F3, 42 = 14.146, p < 0.001 | 16 | 64 ± 30 a | F3, 38 = 10.124, p < 0.001 |
3 mg/L | 14 | 53 ± 26 b | 11 | 37 ± 19 b | ||||
6 mg/L | 10 | 38 ± 25 b | 11 | 31 ± 20 b | ||||
13 mg/L | 8 | 30 ± 22 b | 8 | 23 ± 13 b | ||||
MP | No | 25 | 60 ± 32 | F1, 42 = 1.413, p = 0.241 | 26 | 49 ± 31 | F1, 38 = 4.873, p = 0.033 | |
Yes | 25 | 52 ± 27 | 20 | 34 ± 21 | ||||
Inter. | F3, 42 = 1.011, p = 0.397 | F3, 38 = 6.253, p = 0.001 | ||||||
AChE | Cd | 0 mg/L | 18 | 85 ± 14 a | F3, 42 = 6.956, p = 0.001 | 16 | 67 ± 17 | F3, 38 = 3.281, p = 0.031 |
3 mg/L | 14 | 74 ± 15 a,b | 11 | 65 ± 13 | ||||
6 mg/L | 10 | 75 ± 15 a | 11 | 58 ± 14 | ||||
13 mg/L | 8 | 58 ± 22 b | 8 | 56 ± 11 | ||||
MP | No | 25 | 72 ± 22 | F1, 42 = 8.237, p = 0.006 | 26 | 67 ± 12 | F1, 38 = 7.170, p = 0.011 | |
Yes | 25 | 79 ± 12 | 20 | 56 ± 15 | ||||
Inter. | F3, 42 = 5.301, p = 0.003 | F3, 38 = 8.221, p < 0.001 | ||||||
LPO | Cd | 0 mg/L | 18 | 0.4 ± 0.1 | F3, 42 = 1.536, p = 0.219 | 16 | 0.5 ± 0.3 | F3, 38 = 2.482, p = 0.076 |
3 mg/L | 14 | 0.5 ± 0.1 | 11 | 0.4 ± 0.2 | ||||
6 mg/L | 10 | 0.4 ± 0.1 | 11 | 0.7 ± 0.4 | ||||
13 mg/L | 8 | 0.4 ± 0.1 | 8 | 0.4 ± 0.2 | ||||
MP | No | 25 | 0.4 ± 0.1 | F1, 42 = 0.299, p = 0.587 | 26 | 0.5 ± 0.3 | F1, 38 = 1.582, p = 0.216 | |
Yes | 25 | 0.4 ± 0.1 | 20 | 0.6 ± 0.3 | ||||
Inter. | F3, 42 = 1.280, p = 0.293 | F3, 38 = 1.690, p = 0.185 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Miranda, T.; Vieira, L.R.; Guilhermino, L. Neurotoxicity, Behavior, and Lethal Effects of Cadmium, Microplastics, and Their Mixtures on Pomatoschistus microps Juveniles from Two Wild Populations Exposed under Laboratory Conditions―Implications to Environmental and Human Risk Assessment. Int. J. Environ. Res. Public Health 2019, 16, 2857. https://doi.org/10.3390/ijerph16162857
Miranda T, Vieira LR, Guilhermino L. Neurotoxicity, Behavior, and Lethal Effects of Cadmium, Microplastics, and Their Mixtures on Pomatoschistus microps Juveniles from Two Wild Populations Exposed under Laboratory Conditions―Implications to Environmental and Human Risk Assessment. International Journal of Environmental Research and Public Health. 2019; 16(16):2857. https://doi.org/10.3390/ijerph16162857
Chicago/Turabian StyleMiranda, Tiago, Luis R. Vieira, and Lúcia Guilhermino. 2019. "Neurotoxicity, Behavior, and Lethal Effects of Cadmium, Microplastics, and Their Mixtures on Pomatoschistus microps Juveniles from Two Wild Populations Exposed under Laboratory Conditions―Implications to Environmental and Human Risk Assessment" International Journal of Environmental Research and Public Health 16, no. 16: 2857. https://doi.org/10.3390/ijerph16162857