Skip to main content
SpringerLink
Log in

Interactive effects of mercury exposure and hypoxia on ECG patterns in two Neotropical freshwater fish species: Matrinxã, Brycon amazonicus and traíra, Hoplias malabaricus

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Hypoxia and mercury contamination often co-occur in tropical freshwater ecosystems, but the interactive effects of these two stressors on fish populations are poorly known. The effects of mercury (Hg) on recorded changes in the detailed form of the electrocardiogram (ECG) during exposure to progressive hypoxia were investigated in two Neotropical freshwater fish species, matrinxã, Brycon amazonicus and traíra, Hoplias malabaricus. Matrinxã were exposed to a sublethal concentration of 0.1 mg L−1 of HgCl2 in water for 96 h. Traíra were exposed to dietary doses of Hg by being fed over a period of 30 days with juvenile matrinxãs previously exposed to HgCl2, resulting in a dose of 0.45 mg of total Hg per fish, each 96 h. Both species showed a bradycardia in progressive hypoxia. Hg exposure impaired cardiac electrical excitability, leading to first-degree atrioventricular block, plus profound extension of the ventricular action potential (AP) plateau. Moreover, there was the development of cardiac arrhythmias and anomalies such as occasional absence of QRS complexes, extra systoles, negative Q-, R- and S-waves (QRS complex), and T wave inversion, especially in hypoxia below O2 partial pressures (PO2) of 5.3 kPa. Sub-chronic dietary Hg exposure induced intense bradycardia in normoxia in traira, plus lengthening of ventricular AP duration coupled with prolonged QRS intervals. This indicates slower ventricular AP conduction during ventricular depolarization. Overall, the data indicate that both acute waterborne and sub-chronic dietary exposure (trophic level transfer), at sublethal concentrations of mercury, cause damage in electrical stability and rhythm of the heartbeat, leading to myocardial dysfunction, which is further intensified during hypoxia. These changes could lead to impaired cardiac output, with consequences for swimming ability, foraging capacity, and hence growth and/or reproductive performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aldoghachi MA, Azirun MS, Yusoff I, Ashraf MA (2016) Ultrastructural effects on gill tissues induced in red tilapia Oreochromis sp. by a waterborne lead exposure. Saudi J Biol Sci 23:634–641

    CAS  Google Scholar 

  • Alho CJR, Vieira LM (1997) Fish and wildlife resources in the Pantanal wetlands of Brazil and potential disturbances from the release of environmental contaminants. Environ Toxicol Chem 16:71–74

    CAS  Google Scholar 

  • Alinnor IJ (2005) Assessment of elemental contaminants in water and fish samples from Aba River. Environ Monit Assess 102:15–25

    CAS  Google Scholar 

  • Almeida-Val VMF, Gomes ARC, Lopes NP (2006) Metabolic and physiological adjustments to low oxygen and high temperature in fishes of the Amazon. In: Val AL, Almeida-Val VMF, Randall DJ (eds) Fish Physiol. Elsevier, Heidelberg, p 443–500

    Google Scholar 

  • Almeida-Val VMF, Val AL, Walker I (1999) Long- and short-term adaptation of Amazon fishes to varying O2 levels: intraspecific phenotypic plasticity and interspecific variation. In: Val AL, Almeida-Val VMF (eds) Biol Trop Fish. INPA, Manaus, p 185–206

    Google Scholar 

  • Anner BM, Moosmayer M, Imesch E (1992) Mercury blocks the Na-K-ATPase by a ligand-dependent and reversible mechanism. Am J Physiol 262:F830–F836

    CAS  Google Scholar 

  • AOAC (1995) Mercury (methyl) in fish and shellfish: rapid gas chromatographic method. Sec. 9.2.27. Method 988.11. In: Cunniff PA (ed) Official methods of analysis of AOAC international. AOAC International, Maryland, p 24–25

    Google Scholar 

  • Badr A, El-Sayed MF, Vornanen M (2016) Effects of seasonal acclimatization on temperature dependence of cardiac excitability in the roach, Rutilus rutilus. J Exp Biol 219:1495–1504

    CAS  Google Scholar 

  • Beaumont MW, Butler PJ, Taylor EW (2000) Exposure of brown trout, Salmo trutta, to a sub-lethal concentration of copper in soft acidic water: effects upon muscle metabolism and membrane potential. Aquat Toxicol 51:259–272

    CAS  Google Scholar 

  • Breitburg D, Levin LA, Oschlies A et al. (2018) Declining oxygen in the global ocean and coastal waters. Science 359:eaam7240

    Google Scholar 

  • Bollen A, Wenke A, Biester H (2008) Mercury speciation analyses in HgCl2-contaminated soils and groundwater—implications for risks assessment and remediation strategies. Water Res 42:91–100

    CAS  Google Scholar 

  • Di Giulio RT, Clark BW (2015) The Elizabeth River story: a case study in evolutionary toxicology. J Toxicol Environ Health B 18:259–298

    Google Scholar 

  • Dórea JG, Barbosa AC, Silva GS (2006) Fish mercury bioaccumulation as a function of feeding behavior and hydrological cycles of the Rio Negro, Amazon. Comp Biochem Physiol C 142:275–283

    Google Scholar 

  • Driedzic WR, Gesser H (1994) Energy metabolism and contractility in ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature. Physiol Rev 74:221–258

    CAS  Google Scholar 

  • Duranteau J, Chandel NS, Kulisz A, Shao Z, Schumacker PT (1998) Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J Biol Chem 273:11619–11624

    CAS  Google Scholar 

  • Farrell AP (2007) Tribute to P. L. Lutz: a message from the heart—why hypoxic bradycardia in fishes? J Exp Biol 210:1715–1725

    CAS  Google Scholar 

  • Fernandes GW, Goulart FF, Ranieri BD, Coelho MS, Dales K, Boesche N, Bustamante M, Carvalho FA, Carvalho DC, Dirzo R, Fernandes S, Galetti Jr PM, Millan VEG, Mielke C, Ramirez JL, Neves A, Rogass C, Ribeiro SP, Scariot A, Soares-Filho B (2016) Deep into the mud: ecological and socio-economic impacts of the dam breach in Mariana, Brazil. Nat Conserv 14:35–45

    Google Scholar 

  • Figueiredo N, Serralheiro ML, Canário J, Duarte A, Hintelmann H, Carvalho C (2018) Evidence of mercury methylation and demethylation by the estuarine microbial communities obtained in stable Hg isotope studies. Int J Environ Res Public Health 15:2141

    CAS  Google Scholar 

  • Gaztañaga L, Marchlinski FE, Betensky BP (2012) Mechanisms of cardiac arrhythmias. Rev Esp Cardiol 65:174–185

    Google Scholar 

  • Hassinen M, Haverinen J, Vornanen M (2017) Small functional If current in sinoatrial pacemaker cells of the brown trout (Salmo trutta fario) heart despite strong expression of HCN channel transcripts. Am J Physiol 313:R711–R722

    Google Scholar 

  • Hatje V, Pedreira RMA, Rezende CE, Schettini CAF, Souza GC, Marin DC, Hackspacher PC (2017) The environmental impacts of one of the largest tailing dam failures worldwide. Sci Rep 7:10706. https://doi.org/10.1038/s41598-017-11143-x

    Article  CAS  Google Scholar 

  • Hsu-Kim H, Eckley CS, Achá D, Feng X, Gilmour CC, Jonsson S, Mitchell CPJ (2018) Challenges and opportunities for managing aquatic mercury pollution in altered landscapes. Ambio 47:141–169

    Google Scholar 

  • Hechtenberg S, Beyersmann D (1991) Inhibition of sarcoplasmic reticulum Ca(2+)-ATPase activity by cadmium, lead and mercury. Enzyme 45:109–115

    CAS  Google Scholar 

  • Hool LC (2000) Hypoxia increases the sensitivity of the L type Ca(2+) current to beta-adrenergic receptor stimulation via a C2 region-containing protein kinase C isoform. Circ Res 87:1164–1171

    CAS  Google Scholar 

  • Hylander LD, Pinto FN, Guimarães JR, Meili M, Oliveira LJ, de Castro e Silva E (2000) Fish mercury concentration in the Alto Pantanal, Brazil: influence of season and water parameters. Sci Total Environ 261:9–20

    CAS  Google Scholar 

  • Hypolito R, Ferrer LM, Nascimento SC (2004) Comportamento de espécies de mercúrio no sistema sedimento-água do mangue no município de Cubatão, São Paulo. Águas Subterrâneas 19:15–24

    Google Scholar 

  • Kalinin AL, Rantin FT, Glass ML (1993) Dependence on body size of respiratory function in Hoplias malabaricus (Teleostei, Erythrinidae) during graded hypoxia. Fish Physiol Biochem 12:47–51

    CAS  Google Scholar 

  • Langheinrich U, Vacun G, Wagner T (2003) Zebrafish embryos express an orthologue of HERG and are sensitive toward a range of QT-prolonging drugs inducing severe arrhythmia. J Toxicol Appl Pharmacol 193:370–382

    CAS  Google Scholar 

  • Leybaert L, Lampe PD, Dhein S, Kwak BR, Ferdinandy P, Beyer EC, Laird DW, Naus CC, Green CR, Schulz R (2017) Connexins in cardiovascular and neurovascular health and disease: pharmacological implications. Pharmacol Rev 69:396–478

    CAS  Google Scholar 

  • Lin MH, Chou HC, Chen YF, Liu W, Lee CC, Liu LYM, Chuang YJ (2018) Development of a rapid and economic in vivo electrocardiogram platform for cardiovascular drug assay and electrophysiology research in adult zebrafish. Sci Rep 8:15986

    Google Scholar 

  • Liu CC, Li L, Lam YW, Siu CW, Cheng SH (2016) Improvement of surface ECG recording in adult zebrafish reveals that the value of this model exceeds our expectation. Sci Rep 6:25073

    CAS  Google Scholar 

  • Mandic M, Regan MD (2018) Can variation among hypoxic environments explain why different fish species use different hypoxic survival strategies? J Exp Biol 221:jeb161349

    Google Scholar 

  • Matson CW, Timme-Laragy AR, Di Giulio RT (2008) Fluoranthene, but not benzo[a]pyrene, interacts with hypoxia resulting in pericardial effusion and lordosis in developing zebrafish. Chemosphere 74:149–154

    CAS  Google Scholar 

  • Mittal M, Gu XQ, Pak O, Pamenter ME, Haag D, Fuchs DB, Schermuly RT, Ghofrani HA, Brandes RP, Seeger W, Grimminger F, Haddad GG, Weissmann N (2012) Hypoxia induces Kv channel current inhibition by increased NADPH oxidase-derived reactive oxygen species. Free Radic Biol Med 52:1033–1042

    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

    CAS  Google Scholar 

  • Monteiro DA, Taylor EW, Rantin FT, Kalinin AL (2017) Impact of waterborne and trophic mercury exposures on cardiac function of two ecologically distinct Neotropical freshwater fish Brycon amazonicus and Hoplias malabaricus. Comp Biochem Physiol C 201:26–34

    CAS  Google Scholar 

  • Monteiro DA, Thomaz JM, Rantin FT, Kalinin AL (2013) Cardiorespiratory responses to graded hypoxia in the Neotropical fish matrinxã (Brycon amazonicus) and traíra (Hoplias malabaricus) after waterborne or trophic exposure to inorganic mercury. Aquat Toxicol 140:346–355

    Google Scholar 

  • Mu J, Chernick M, Dong W, Di Giulio RT, Hinton DE (2017) Early life co-exposures to a real-world PAH mixture and hypoxia result in later life and next generation consequences in medaka (Oryzias latipes). Aquat Toxicol 190:162–173

    CAS  Google Scholar 

  • Nnamdi AH, Briggs TMD, Togunde OO, Obanya HE (2019) Antagonistic effects of sublethal concentrations of certain mixtures of metal oxide nanoparticles and the bulk (Al2O3, CuO, and SiO2) on gill histology in Clarias gariepinus. J Nanotechnol 2019:11

    Google Scholar 

  • Norin T, Clark TD (2016) Measurement and relevance of maximum metabolic rate in fishes. J Fish Biol 88:122–151

    CAS  Google Scholar 

  • Peregrina-Chávez AG, Ramírez-Galindo MDR, Chávez-Martínez R, Delahanty-Delgado CA, Vazquez-Alaniz F (2018) Full atrioventricular block secondary to acute poisoning mercury: a case report. Int J Environ Res Public Health 15:657

    Google Scholar 

  • Piccoli C, D’Aprile A, Scrima R, Ambrosi L, Zefferino R, Capitanio N (2012) Subcytotoxic mercury chloride inhibits gap junction intercellular communication by a redox- and phosphorylation-mediated mechanism. Free Rad. Biol Med 52:916–927

    CAS  Google Scholar 

  • Pollock MS, Clarke LMJ, Dubé MG (2007) The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ Rev 15:1–14

    CAS  Google Scholar 

  • Posnack NG, Jaimes III R, Asfour H, Swift LM, Wengrowski AM, Sarvazyan N, Kay MW (2014) Bisphenol A exposure and cardiac electrical conduction in excised rat hearts. Environ Health Perspect 122:384–390

    CAS  Google Scholar 

  • Rantin FT, Kalinin AL, Guerra CD, Maricondi-Massari M, Verzola RM (1995) Electrocardiographic characterization of myocardial function in normoxic and hypoxic teleosts. Braz J Med Biol Res 28:1277–1289

    CAS  Google Scholar 

  • Rantin FT, Kalinin AL, Monteiro DA (2020) The cardiovascular system. In: Baldisserotto B, Urbinati EC, Cyrino JEP (eds) Biology and physiology of freshwater neotropical fish, 1st edn. Academic Press, Elsevier Inc., London, pp. 185–216. https://doi.org/10.1016/B978-0-12-815872-2.09995-4

  • Regnell O, Watras CJ (2019) Microbial mercury methylation in aquatic environments: a critical review of published field and laboratory studies. Environ Sci Technol 53:4–19

    CAS  Google Scholar 

  • Ren Z, Liu Y (2018) The monitoring and assessment of Cd2+ stress using zebrafish (Danio rerio). In: Bozkurt Y (ed) Recent advances in zebrafish researches. IntechOpen, London, pp. 135–154. https://doi.org/10.5772/intechopen.74454

  • Rios FS, Oba ET, Fernandes MN, Kalinin AL, Rantin FT (2005) Erythrocyte senescence and haematological changes induced by starvation in the notropical fish traíra, Hoplias malabaricus (Characiformes, Erythrinidae). Comp Biochem Physiol A 140:281–287

    CAS  Google Scholar 

  • Schirrmacher K, Wiemann M, Bingmann D, Büsselberg D (1998) Effects of lead, mercury, and methyl mercury on gap junctions and [Ca2+]i in bone cells. Calcif Tissue Int 63:134–139

    CAS  Google Scholar 

  • Sokolova I, Lannig G (2008) Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: implications of global climate change. Clim Res 37:181–201

    Google Scholar 

  • Stecyk JA, Galli GL, Shiels HA, Farrell AP (2008) Cardiac survival in anoxia-tolerant vertebrates: an electrophysiological perspective. Comp Biochem Physiol C 148:339–354

    Google Scholar 

  • Taylor EW (1992) Nervous control of the heart and cardiorespiratory interactions. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology. Academic Press, New York, NY, p 343–387. volume 12B

    Google Scholar 

  • Taylor EW, Beaumont MW, Butler PJ, Mair J, Mujallid MSI (1996) Lethal and sub-lethal effects of copper upon fish: a role for ammonia toxicity? In: Taylor EW (ed) SEB Seminar Series 57. Toxicology of aquatic pollution: physiological, molecular and cellular approaches. Cambridge University Press, Cambridge, p 85–113

    Google Scholar 

  • Thambithurai D, Crespel A, Norin T, Rácz A, Lindström J, Parsons KJ, Killen SS (2019) Hypoxia alters vulnerability to capture and the potential for trait-based selection in a scaled-down trawl fishery. Conserv Physiol 7:coz082

    Google Scholar 

  • Thomaz JM (2012) Habitat, hábito e morfologia cardíaca: influência destes fatores sobre as respostas cardiorrespiratórias à hipóxia e alterações térmicas em espécies de peixes ecologicamente distintas. Dissertation, Federal University of São Carlos

  • Tikkanen E, Haverinen J, Egginton S, Hassinen M, Vornanen M (2017) Effects of prolonged anoxia on electrical activity of the heart in crucian carp (Carassius carassius). J Exp Biol 220:445–454

    Google Scholar 

  • USEPA - US Environmental Protection Agency (2002) Mercury in Water by Oxidation, Purge and Trap, and Cold Vapor Atomic Fluorescence Spectrometry EPA 821-R- 02–019, Method 163, Revision E. US Environmental Protection Agency, Office of Water, Washington, DC

  • USP - United States Pharmacopoeia (2000) Analytical Methods Flame Atomic Absorption Spectrometry Varian, Publication no. 85. Rockville: United States Pharmacopeial Convention

  • Vornanen M (2017) Electrical excitability of the fish heart and its autonomic regulation. Fish Physiol 36:99–153

    Google Scholar 

  • Wang Q, Kim D, Dionysiou DD, Sorial GA, Timberlake D (2004) Sources and remediation for mercury contamination in aquatic systems—a literature review. Environ Pollut 131:323–336

    Google Scholar 

  • Wildemann TM, Weber LP, Siciliano SD (2015) Combined exposure to lead, inorganic mercury and methylmercury shows deviation from additivity for cardiovascular toxicity in rats. J Appl Toxicol 35:918–926

    CAS  Google Scholar 

  • Wilson RW, Taylor EW (1993) The physiological responses of freshwater rainbow trout (Oncorhynchus mykiss) during acutely lethal copper exposure. J Comp Physiol B 163:38–47

    CAS  Google Scholar 

  • Xing N, Ji L, Song J, Ma J, Li S, Ren Z, Xu F, Zhu J (2017) Cadmium stress assessment based on the electrocardiogram characteristics of zebrafish (Danio rerio): QRS complex could play an important role. Aquati Toxicol 191:236–244

    CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to Águas Claras (Mococa-SP) and Parque do Lago (Dourado-SP) fish farms, which provided the fishes.

Funding

This study was supported by São Paulo State Research Foundation (FAPESP, Proc. #06/50772-6 plus a grant from the Science without Borders program (CNPq 401061/2014-0) to FTR to support the work of EWT at UFSCar.

Author information

Authors and Affiliations

  1. Department of Physiological Sciences, Federal University of São Carlos (UFSCar), São Carlos, São Paulo, Brazil

    Diana A. Monteiro, Francisco T. Rantin & Ana L. Kalinin

  2. School of Biological Sciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK

    Edwin W. Taylor

  3. UMR Marbec, CNRS – IRD – Ifremer – University of Montpellier, Montpellier, France

    David J. McKenzie

Authors
  1. Diana A. Monteiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edwin W. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David J. McKenzie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francisco T. Rantin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ana L. Kalinin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diana A. Monteiro.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical appoval

Ethics in Animal Experimentation: This study was performed with the approval of the Committee of Ethics in Animal Experimentation (CEUA—approval 04/2007) and Committee of Environmental Ethics (CEA—approval 003/2006) of the Federal University of São Carlos.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Monteiro, D.A., Taylor, E.W., McKenzie, D.J. et al. Interactive effects of mercury exposure and hypoxia on ECG patterns in two Neotropical freshwater fish species: Matrinxã, Brycon amazonicus and traíra, Hoplias malabaricus. Ecotoxicology 29, 375–388 (2020). https://doi.org/10.1007/s10646-020-02186-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-020-02186-4

Keywords

Search

Navigation