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Multi-biomarker Assessment in a Native Species Psalidodon eigenmanniorum Under Inorganic Mercury and Recovery Scenarios

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Abstract

The increasing contamination of water bodies with mercury raises concerns about its possible effects on aquatic organisms. The combined use of several biomarkers allows researchers to study the impact of a chemical at different levels of biological organization. In the present work, we determined the response of histological (gills and liver), somatic (condition factor and hepato-somatic index), and behavioral (predator–prey relationship, through the presentation of a computer-animated image) biomarkers in the native species Psalidodon eigenmanniorum exposed to 100 µg L−1 of inorganic Hg (IHg) during 96 h. We also assessed whether there was a change in the biomarkers analyzed after 7 days in Hg-free water compared with those exposed to IHg. In exposed fish, IHg caused damage to the gills and liver tissues. The condition factor showed no difference between IHg-exposed organisms and control organisms, while the hepato-somatic index was lower in IHg-exposed fish. As for the behavioral analyses, it was observed that the presentation of a stimulus induced changes in the behavioral responses of fish exposed to IHg, which showed a heightened state of alertness with respect to control. On the other hand, after 7 days in Hg-free water, the organisms generally showed no changes in biomarkers compared with IHg-exposed fish. Our results contribute new data on IHg toxicity in a native species and provide information on the plasticity of damage to reverse itself. Furthermore, this work provides baseline information for environmental assessments in water bodies where mercury is present.

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References

  • Ahmed O, Seguin D, Gerlai R (2011) An automated predator avoidance task in zebrafish. Behav Brain Res 216:166–171. https://doi.org/10.1016/j.bbr.2010.07.028

    Article  Google Scholar 

  • Alinnor IJ (2005) Assessment of elemental contaminants in water and fish samples from Aba River. Environ Monit Assess 102:15–25. https://doi.org/10.1007/s10661-005-1011-3

    Article  CAS  Google Scholar 

  • AnvariFar H, Amirkolaie AK, Jalali AM et al (2018) Environmental pollution and toxic substances: cellular apoptosis as a key parameter in a sensible model like fish. Aquat Toxicol 204:144–159. https://doi.org/10.1016/j.aquatox.2018.09.010

    Article  CAS  Google Scholar 

  • Atchison GJ, Henry MG, Sandheinrich MB (1987) Effects of metals on fish behavior: a review. Environ Biol Fishes 18:11–25

    Article  Google Scholar 

  • Ballesteros ML, Bianchi GE, Carranza M, Bistoni MA (2007) Endosulfan acute toxicity and histomorphological alterations in Jenynsia multidentata (Anablepidae, Cyprinodontiformes). J Environ Sci Health Part B 42:351–357. https://doi.org/10.1080/03601230701309577

    Article  CAS  Google Scholar 

  • Bernet D, Schmidt H, Meier W et al (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34. https://doi.org/10.1046/j.1365-2761.1999.00134.x

    Article  Google Scholar 

  • Bonifacio AF, Cazenave J, Bacchetta C et al (2016) Alterations in the general condition, biochemical parameters and locomotor activity in Cnesterodon decemmaculatus exposed to commercial formulations of chlorpyrifos, glyphosate and their mixtures. Ecol Indic 67:88–97. https://doi.org/10.1016/j.ecolind.2016.02.011

    Article  CAS  Google Scholar 

  • Bria A, Marda J, Zhou J et al (2017) Hepatic progenitor cell activation in liver repair. Liver Res 1:81–87. https://doi.org/10.1016/j.livres.2017.08.002

    Article  Google Scholar 

  • Brown C, Laland K, Krause J (2006) Fish cognition and behavior. Blackwell, Oxford

    Book  Google Scholar 

  • Cox AG, Goessling W (2015) The lure of zebrafish in liver research: regulation of hepatic growth in development and regeneration. Curr Opin Genet Dev 32:153–161. https://doi.org/10.1016/j.gde.2015.03.002

    Article  CAS  Google Scholar 

  • Di Rienzo J, Casanoves F, Balzarini M et al (2018) InfoStat [Internet]. versión 24

  • Don Xavier ND, Bijoy Nandan S, Jayachandran PR et al (2019) Chronic effects of copper and zinc on the fish, Etroplus suratensis (Bloch, 1790) by continuous flow through (CFT) bioassay. Mar Environ Res 143:141–157. https://doi.org/10.1016/j.marenvres.2018.11.002

    Article  CAS  Google Scholar 

  • Egan RJ, Bergner CL, Hart PC et al (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain 205:38–44

    Article  CAS  Google Scholar 

  • Figueiredo-Fernandes A, Ferreira-Cardoso JV, Garcia-Santos S et al (2007) Histopathological changes in liver and gill epithelium of Nile tilapia, Oreochromis niloticus, exposed to waterborne copper. Pesqui Vet Bras 27:103–109

    Article  Google Scholar 

  • Filenko OF, Xihua DU, Xulong C, Yugi Z (1988) Distribution of mercury in the tissues of carp and its biological effects. Hydrobiol J 24:64–68

    Google Scholar 

  • Flores Quintana C (2009) Células cloro en peces teleósteos. Rev Vet 20:57–60

    Article  Google Scholar 

  • Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22(4):241–253

    Article  Google Scholar 

  • Gammons CH, Slotton DG, Gerbrandt B et al (2006) Mercury concentrations of fish, river water, and sediment in the Río Ramis-Lake Titicaca watershed, Peru. Sci Total Environ 368:637–648. https://doi.org/10.1016/j.scitotenv.2005.09.076

    Article  CAS  Google Scholar 

  • Garnero PL, Monferran MV, González GA et al (2018) Assessment of exposure to metals, As and Se in water and sediment of a freshwater reservoir and their bioaccumulation in fish species of different feeding and habitat preferences. Ecotoxicol Environ Saf 163:492–501. https://doi.org/10.1016/j.ecoenv.2018.07.023

    Article  CAS  Google Scholar 

  • Garnero PL, Monferran MV, Bistoni MA (2020) Uptake, tissue distribution and elimination in a native fish species Astyanax eigenmanniorum exposed to inorganic mercury. Aquat Toxicol 226:105567. https://doi.org/10.1016/j.aquatox.2020.105567

    Article  CAS  Google Scholar 

  • Gerlai R, Fernandes Y, Pereira T (2009) Zebrafish (Danio rerio) responds to the animated image of a predator: Towards the development of an automated aversive task. Behav Brain Res J 201:318–324. https://doi.org/10.1016/j.bbr.2009.03.003

    Article  Google Scholar 

  • Giari L, Manera M, Dezfuli BS (2008) Histo-cytological responses of Dicentrarchus labrax (L.) following mercury exposure. Ecotoxicol Environ Saf 70:400–410. https://doi.org/10.1016/j.ecoenv.2007.08.013

    Article  CAS  Google Scholar 

  • Haro JG, Bistoni MA (2007) “Peces de Córdoba,” 1a ed. Córdoba, Argentina

  • Hinton DE, Lauren DJ (1990) Liver structural alterations accompanying chronic toxicity in fishes: potential biomarkers of exposure. In: Shigart LR (ed) McCarty JF. Biomarkers of environmental contamination, Lewis Publ, pp 15–57

    Google Scholar 

  • Hirt LM, Domitrovic HA (2002) Toxicity and histopathological response in Cichlasoma dimerus (Pisces, Cichlidae) exposes to mercury dichloride in acute and subletal tests. Rev Ictiol 10:37–52

    Google Scholar 

  • Kania HJ, O’Hara J (1974) Behavioral alterations in a simple predator–prey system due to sublethal exposure to mercury. Trans Am Fish Soc 103:134–136. https://doi.org/10.1577/1548-8659(1974)103

    Article  Google Scholar 

  • Leone OL, Valdecantos S, Martínez VH (2018) Histopathological markers of environmental stress in the fish Odonthestes bonariensis (Atheriniformes, Atherinopsidae) in two reservoirs of Argentina. UNED Res J 10:273–282

    Article  Google Scholar 

  • Levin ED, Bencan Z, Cerutti DT (2007) Anxiolytic effects of nicotine in zebrafish. Physiol Behav 90:54–58

    Article  CAS  Google Scholar 

  • Mallatt J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42:630–648

    Article  CAS  Google Scholar 

  • Mela M, Randi MAF, Ventura DF et al (2007) Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus. Ecotoxicol Environ Saf 68:426–435. https://doi.org/10.1016/j.ecoenv.2006.11.013

    Article  CAS  Google Scholar 

  • Monteiro DA, Rantin FT, Kalinin AL (2010) Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã, Brycon amazonicus (Spix and Agassiz, 1829). Ecotoxicology 19:105–123. https://doi.org/10.1007/s10646-009-0395-1

    Article  CAS  Google Scholar 

  • Muñoz L, Weber P, Dressler V et al (2015) Histopathological biomarkers in juvenile silver catfish (Rhamdia quelen) exposed to a sublethal lead concentration. Ecotoxicol Environ Saf 113:241–247

    Article  Google Scholar 

  • Nero V, Farwell A, Lister A et al (2006) Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sands process-affected water. Ecotoxicol Environ Saf 63:365–377. https://doi.org/10.1016/j.ecoenv.2005.04.014

    Article  CAS  Google Scholar 

  • Oliveira Ribeiro CA, Guimaraes JRD, Pfeiffer WC (1996) Accumulation and distribution of inorganic mercury in a tropical fish (Trichomycterus zonatus). Ecotoxicol Environ Saf 34:190–195. https://doi.org/10.1006/eesa.1996.0063

    Article  Google Scholar 

  • Olurin KB, Olojo EAA, Mbaka GO, Akindele AT (2006) Histopathological responses of the gill and liver tissues of Clarias gariepinus fingerlings to the herbicide, glyphosate. African J Biotechnol 5:2480–2487

    CAS  Google Scholar 

  • Polverino G, Liao JC, Porfiri M (2013) Mosquitofish (Gambusia affinis) preference and behavioral response to animated images of conspecifics altered in their color, aspect ratio, and swimming depth. PLoS ONE 8:1–7. https://doi.org/10.1371/journal.pone.0054315

    Article  CAS  Google Scholar 

  • Qin M, Wong A, Seguin D, Gerlai R (2014) Induction of social behavior in zebrafish: live versus computer animated fish as stimuli. Zebrafish 11:185–197. https://doi.org/10.1089/zeb.2013.0969

    Article  Google Scholar 

  • Rautenberg GE, Amé MV, Monferran MV et al (2014) A multi-level approach using Gambusia affinis as a bioindicator of environmental pollution in the middle-lower basin of Suquía River. Ecol Indic 48:706–720. https://doi.org/10.1016/j.ecolind.2014.09.025

    Article  CAS  Google Scholar 

  • Rosso JJ (2006) PECES PAMPEANOS: GUÍA Y ECOLOGÍA, L.O.L.A. L. Buenos Aires

  • Sarmento A, Guilhermino L, Afonso A (2004) Mercury chloride effects on the function and cellular integrity of sea bass (Dicentrarchus labrax) head kidney macrophages. Fish Shellfish Immunol 17:489–498. https://doi.org/10.1016/j.fsi.2004.05.004

    Article  CAS  Google Scholar 

  • Speedie N, Gerlai R (2008) Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav Brain Res 188:168–177

    Article  CAS  Google Scholar 

  • Stentiford GD, Longshaw M, Lyons BP et al (2003) Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Mar Environ Res 55:137–159

    Article  CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149. https://doi.org/10.1016/S1382-6689(02)00126-6

    Article  Google Scholar 

  • Vieira LR, Gravato C, Soares AMVM et al (2009) Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76:1416–1427. https://doi.org/10.1016/j.chemosphere.2009.06.005

    Article  CAS  Google Scholar 

  • Vieira C, Morais S, Ramos S et al (2011) Mercury, cadmium, lead and arsenic levels in three pelagic fish species from the Atlantic Ocean: intra- and inter-specific variability and human health risks for consumption. Food Chem Toxicol 49:923–932. https://doi.org/10.1016/j.fct.2010.12.016

    Article  CAS  Google Scholar 

  • Vogl C, Grillitsch B, Wytek R et al (1999) Qualification of spontaneous undirected locomotor behavior of fish for sublethal toxicity testing. Part I. Variability of measurement parameters under general test conditions. Environ Toxicol Chem 18:2736–2742

    Article  CAS  Google Scholar 

  • Wang X, Wang WX (2019) The three “B” of fish mercury in China: bioaccumulation, biodynamics and biotransformation. Environ Pollut 250:216–232

    Article  CAS  Google Scholar 

  • Wang J, Feng X, Anderson CWN et al (2012) Remediation of mercury contaminated sites—a review. J Hazard Mater 221–222:1–18. https://doi.org/10.1016/j.jhazmat.2012.04.035

    Article  CAS  Google Scholar 

  • Webber HM, Haines TA (2003) Effects of methylmercury on the predator avoidance behavior of a freshwater forage fish, golden shiner (Notemigonus crysoleucas). Environ Toxicol Chem 22:1556–1561

    Article  CAS  Google Scholar 

  • Wendelaar Bonga SE, Lock RAC (2008) The osmoregulatory system. In: Di Giulio RT, Hinton D (eds) The Toxicology of Fishes, p 1071

  • Wood CM (2001) Toxic responses of the gill. In: Schlenk D, Benson WH (eds) Target organ toxicity in marine and freshwater teleosts. CRC Press, Boca Raton, p 363

    Google Scholar 

  • Wu L, Yu Q, Zhang G et al (2019) Single and combined exposures of waterborne Cu and Cd induced oxidative stress responses and tissue injury in female rare minnow (Gobiocypris rarus). Comp Biochem Physiol Part C Toxicol Pharmacol 222:90–99. https://doi.org/10.1016/j.cbpc.2019.04.013

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank the National Scientific and Technical Research Council (CONICET, PIP 112-201101-01084) 461 and the Science and Technology Office (SECYT, 2014–2015. Res no.: 203/14) of the National University of Córdoba (Argentina) for grants and subsidies. We also thank Joaquín Gastaminza for his help during sample measurement with the ICP-MS.

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The authors have not disclosed any funding.

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Authors

Contributions

The authors' contributions are as follows: Paola L. Garnero conducted the laboratory experiments, directed mercury measurements and histological and behavioral data analyses, and wrote the article. María L. Ballesteros collaborated with the behavioral analysis and revision of the manuscript. Magdalena V. Monferran provided expertise in mercury measurements and conceptualization. Natalia G. Rivetti contributed to laboratory tests and data interpretation. María de los Ángeles Bistoni collaborated with the experimental design, conceptualization, and project administration. All authors have read and approved the final version of the manuscript.

Corresponding author

Correspondence to Paola L. Garnero.

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Ethics Approval and Consent to Participate

The use of experimental animals followed the guidelines of the Bioethics and Animal Welfare Committee of the National Scientific and Technical Research Council—Argentina (Res 1047/2005), Argentina. The protocol was approved (Acta 04/2018) by the Institutional Committee for the Care and Use of Laboratory Animals (CICUAL) of the Institute of Animal Diversity and Ecology (IDEA-CONICET).

Competing interests

The authors state that there are no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Garnero, P.L., Ballesteros, M.L., Monferran, M.V. et al. Multi-biomarker Assessment in a Native Species Psalidodon eigenmanniorum Under Inorganic Mercury and Recovery Scenarios. Arch Environ Contam Toxicol 83, 142–154 (2022). https://doi.org/10.1007/s00244-022-00946-3

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