Skip to main content
SpringerLink
Log in

Ammonia exposure and subsequent recovery trigger oxidative stress responses in juveniles of Brazilian flounder Paralichthys orbignyanus

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The effects of ammonia exposure and recovery on oxidative stress parameters and histology of juvenile Brazilian flounder Paralichthys orbignyanus were evaluated. The fish were exposed to 0.12, 0.28 and 0.57 mg NH3-N L−1, plus a control, for 10 days followed by the same recovery time in ammonia-free water. Gill, liver and muscle samples (n = 9) were collected after 1, 5 and 10 days of exposure and after recovery for oxidative stress analysis (antioxidant capacity against peroxyl radicals (ACAP); glutathione S-transferase (GST) activity; lipoperoxidation levels measured through thiobarbituric acid reactive substances (TBARS) content). For histological assessment, gill, liver and brain samples were collected. Exposure to all NH3-N concentrations induced different time- and dose-dependent changes in oxidative stress parameters. Reduced antioxidant capacity of the liver and muscle and enhanced TBARS levels in the gills and liver were demonstrated. Differently, a high ammonia concentration elicited lower hepatic TBARS levels. Enhanced GST activity in all organs and increased antioxidant capacity of the gills were also observed. No ammonia-induced histopathological effects were demonstrated. After recovery, most parameters (liver ACAP, GST activity in the muscle and liver and TBARS in the gills) returned to baseline levels. However, liver TBARS and gill GST activity remained altered 0.57 mg NH3-N L−1 treatment. The recovery period also led to a decrease in gill antioxidant capacity and an increase in muscle antioxidant capacity. In conclusion, a concentration of 0.12 mg NH3-N L−1 induces oxidative stress and antioxidant responses in juvenile Brazilian flounder. Moreover, a 10-day recovery period is not sufficient to restore fish homeostasis.

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

Similar content being viewed by others

References

  • Ackerman PA, Wicks BJ, Iwama GK, Randall DJ (2006) Low levels of environmental ammonia increase susceptibility to disease in chinook salmon smolts. Physiol Biochem Zool 79:695–707. doi:10.1086/504615

    Article  CAS  PubMed  Google Scholar 

  • Amado LL, Garcia ML, Ramos PB, Freitas RF, Zafalon B, Ferreira JL, Yunes JS, Monserrat JM (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

    Article  CAS  PubMed  Google Scholar 

  • Baldisserotto B, Martos-Sitcha JA, Menezes CC, Toni C, Prati RL, Garcia LO, Salbego J, Mancera JM, Martínez-Rodríguez G (2014) The effects of ammonia and water hardness on the hormonal, osmoregulatory and metabolic responses of the freshwater silver catfish Rhamdia quelen. Aquat Toxicol 152:341–352. doi:10.1016/j.aquatox.2014.04.023

  • Bendschneider K, Robinson RJ (1952) A new spectrophotometric method for the determination of nitrite in sea water. J Mar Res 11:87–96

    CAS  Google Scholar 

  • Bianchini A, Wasielesky W, Filho KC (1996) Toxicity of nitrogenous compounds to juveniles of flatfish Paralichthys orbignyanus. Bull Environ Contam Toxicol 56:453–459. doi:10.1007/s001289900065

    Article  CAS  PubMed  Google Scholar 

  • Blanchette B, Feng X, Singh BR (2007) Marine glutathione S-transferases. Mar Biotechnol 9:513–542. doi:10.1007/s10126-007-9034-0

    Article  CAS  PubMed  Google Scholar 

  • Bolasina SN (2011) Stress response of juvenile flounder (Paralichthys orbignyanus, Valenciennes 1839), to acute and chronic stressors. Aquaculture 313:140–143. doi:10.1016/j.aquaculture.2011.01.011

    Article  Google Scholar 

  • Carvalho-Neta RN, Abreu-Silva AL (2013) Glutathione S-transferase as biomarker in Sciades herzbergii (Siluriformes: Ariidae) for environmental monitoring: the case study of São Marcos Bay, Maranhão, Brazil. Lat Am J Aquat Res 41:217–225. doi:10.3856/vol41-issue2-fulltext-2

    Google Scholar 

  • Cheng CH, Yang FF, Ling RZ, Liao SA, Miao YT, Ye CX, Wang AL (2015) Effects of ammonia exposure on apoptosis, oxidative stress and immune response in pufferfish (Takifugu obscurus). Aquat Toxicol 164:61–71. doi:10.1016/j.aquatox.2015.04.004

    Article  CAS  PubMed  Google Scholar 

  • Ching B, Chew SF, Wong WP, Ip YK (2009) Environmental ammonia exposure induces oxidative stress in gills and brain of Boleophthalmus boddarti (mudskipper). Aquat Toxicol 95:203–212. doi:10.1016/j.aquatox.2009.09.004

    Article  CAS  PubMed  Google Scholar 

  • Colt J (2002) List of spreadsheets prepared as a complement. In: Wedemeyer GA (ed) Fish hatchery management, 2nd edn. American Fish Society Publication http://www.fisheries.org/afs/hatchery.html. Accessed 10 April 2013

  • Da Rocha AM, de Freitas DP, Burns M, Vieira JP, de la Torre FR, Monserrat JM (2009) Seasonal and organ variations in antioxidant capacity, detoxifying competence and oxidative damage in freshwater and estuarine fishes from Southern Brazil. Comp Biochem Phys C Toxicol Pharmacol 150:512–520. doi:10.1016/j.cbpc.2009.07.012

    Article  Google Scholar 

  • Dong X, Zhang X, Qin J, Zong S (2013) Acute ammonia toxicity and gill morphological changes of Japanese flounder Paralichthys olivaceus in normal versus supersaturated oxygen. Aquac Res 44:1752–1759. doi:10.1111/j.1365-2109.2012.03181.x

    Article  CAS  Google Scholar 

  • Eaton AD, Clesceri LS, Rice EW, Greenberg AE (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Washington, D.C.

    Google Scholar 

  • Enamorado AD, Martins AC, Flores JA, Tesser MB, Caldas SS, Primel EG, Monserrat JM (2015) Biochemical responses over time in common carp Cyprinus carpio (Teleostei, Cyprinidae) during fed supplementation with α-lipoic acid. Comp Biochem Phys A Mol Integr Physiol 188:9–16. doi:10.1016/j.cbpa.2015.05.023

    Article  CAS  Google Scholar 

  • FAO–Food and Agriculture Organization of the United Nations (2016) The state of world fisheries and aquaculture—contributing to food security and nutrition for all, Rome http://www.fao.org/3/a-i5555e.pdf. Accessed 13 February 2017

  • Farag AM, May T, Marty GD, Easton M, Harper DD, Little EE, Cleveland L (2006) The effect of chronic chromium exposure on the health of chinook salmon (Oncorhynchus tshawytscha). Aquat Toxicol 76:246–257. doi:10.1016/j.aquatox.2005.09.011

    Article  CAS  PubMed  Google Scholar 

  • Farzad R, Inanlou DN, Cohan RA, Ghorbani M (2015) Effects of the industrial pollution on glutathione S-tranferase in the liver of rainbow trout. Bulg Chem Commun 47:720–724

    Google Scholar 

  • Figueiredo JL, Menezes NA (2000) Manual de peixes marinhos do sudeste do Brasil. São Paulo, Museu de Zoologia/USP

  • Frances J, Nowak BF, Allan GL (2000) Effects of ammonia on juvenile silver perch (Bidyanus bidyanus). Aquaculture 183:95–103. doi:10.1016/S0044-8486(99)00286-0

    Article  CAS  Google Scholar 

  • Fridovich I (2004) Mitochondria: are they the seat of senescence? Aging Cell 3:13–16. doi:10.1046/j.1474-9728.2003.00075.x

    Article  CAS  PubMed  Google Scholar 

  • Garcia LO, Okamoto MH, Riffel AP, Saccol EM, Pavanato MA, Sampaio LA (2015) Oxidative stress parameters in juvenile Brazilian flounder Paralichthys orbignyanus (Valenciennes, 1839) (Pleuronectiformes: Paralichthyidae) exposed to cold and heat shocks. Neotrop Ichthyol 13:607–612. doi:10.1590/1982-0224-20140148

    Article  Google Scholar 

  • Gottschalk S, Zwingmann C (2009) Altered fatty acid metabolism and composition in cultured astrocytes under hyperammonemic conditions. J Neurochem 109:258–264. doi:10.1111/j.1471-4159.2009.05985.x

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JM (2015) Free radicals in biology and medicine. Oxford University Press, USA

    Book  Google Scholar 

  • Hegazi MM, Attia ZI, Ashour OA (2010) Oxidative stress and antioxidant enzymes in liver and white muscle of Nile tilapia juveniles in chronic ammonia exposure. Aquat Toxicol 99:118–125. doi:10.1016/j.aquatox.2010.04.007

    Article  CAS  PubMed  Google Scholar 

  • Hermes-Lima M, Moreira DC, Rivera-Ingraham GA, Giraud-Billoud M, Genaro-Mattos TC, Campos ÉG (2015) Preparation for oxidative stress under hypoxia and metabolic depression: revisiting the proposal two decades later. Free Radical Bio Med 89:1122–1143. doi:10.1016/j.freeradbiomed.2015.07.156

    Article  CAS  Google Scholar 

  • Intergovernmental Oceanographic Commission (1983) Chemical methods for use in marine environmental monitoring. UNESCO, Paris

    Google Scholar 

  • Ip YK, Chew SF (2010) Ammonia production, excretion, toxicity, and defense in fish: a review. Front Physiol 1:134. doi:10.3389/fphys.2010.00134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SH, Kim JH, Park MA, Hwang SD, Kang JC (2015) The toxic effects of ammonia exposure on antioxidant and immune responses in rockfish, Sebastes schlegelii during thermal stress. Environ Toxicol Pharmacol 40:954–959. doi:10.1016/j.etap.2015.10.006

    Article  CAS  PubMed  Google Scholar 

  • Klinger D, Naylor R (2012) Searching for solutions in aquaculture: charting a sustainable course. Annu Rev Environ Resour 37:247–276. doi:10.1146/annurev-environ-021111-161531

    Article  Google Scholar 

  • Kolarevic J, Takle H, Felip O, Ytteborg E, Selset R, Good CM, Baeverfjord G, Asgård T, Terjesen BF (2012) Molecular and physiological responses to long-term sub-lethal ammonia exposure in Atlantic salmon (Salmo salar). Aquat Toxicol 124:48–57. doi:10.1016/j.aquatox.2012.07.003

    Article  PubMed  Google Scholar 

  • Kütter MT, Romano LA, Ventura-Lima J, Tesser MB, Monserrat JM (2014) Antioxidant and toxicological effects elicited by alpha-lipoic acid in aquatic organisms. Comp Biochem Phys C Toxicol Pharmacol 162:70–76. doi:10.1016/j.cbpc.2014.03.008

    Article  Google Scholar 

  • Li M, Gong S, Li Q, Yuan L, Meng F, Wang R (2016) Ammonia toxicity induces glutamine accumulation, oxidative stress and immunosuppression in juvenile yellow catfish Pelteobagrus fulvidraco. Comp Biochem Phys C Toxicol Pharmacol 183-184:1–6. doi:10.1016/j.cbpc.2016.01.005

    Article  CAS  Google Scholar 

  • Li M, Yu N, Qin JG, Li E, Du Z, Chen L (2014) Effects of ammonia stress, dietary linseed oil and Edwardsiella ictaluri challenge on juvenile darkbarbel catfish Pelteobagrus vachelli. Fish Shellfish Immun 38:158–165. doi:10.1016/j.fsi.2014.03.015

    Article  CAS  Google Scholar 

  • Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Revue Méd Vét 154:427–430

    CAS  Google Scholar 

  • Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. doi:10.1016/j.aquatox.2010.10.006

    Article  CAS  PubMed  Google Scholar 

  • Lushchak VI (2014) Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact 224:164–175. doi:10.1016/j.cbi.2014.10.016

    Article  CAS  PubMed  Google Scholar 

  • Medeiros RS, Lopez BA, Sampaio LA, Romano LA, Rodrigues RV (2016) Ammonia and nitrite toxicity to false clownfish Amphiprion ocellaris. Aquacult Int 24:985–993. doi:10.1007/s10499-015-9965-9

    Article  CAS  Google Scholar 

  • Millner R, Walsh SJ, Díaz de Astarloa JM (2005) Atlantic flatfish fisheries. In: Gibson RN (ed) Flatfishes: biology and exploitation, 1st edn. Blackwell Science, Oxford, pp 240–271

    Chapter  Google Scholar 

  • Monserrat JM, Martínez PE, Geracitano LA, Amado LL, Martins CM, Pinho GL, Chaves IS, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Phys C Toxicol Pharmacol 146:221–234. doi:10.1016/j.cbpc.2006.08.012

    Article  Google Scholar 

  • 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. doi:10.1016/S0166-445X(02)00204-7

    Article  CAS  PubMed  Google Scholar 

  • Okamoto MH, Sampaio LA (2012) Sobrevivência e crescimento de juvenis do linguado Paralichthys orbignyanus criados em diferentes temperaturas. Atlântica (Rio Grande) 34:57–61. doi:10.5088/atlântica.v34i1.2710

    Article  Google Scholar 

  • Pan CH, Chien YH, Wang YJ (2011) Antioxidant defence to ammonia stress of characins (Hyphessobrycon eques Steindachner) fed diets supplemented with carotenoids. Aquac Nutr 17:258–266. doi:10.1111/j.1365-2095.2009.00747.x

    Article  CAS  Google Scholar 

  • Paust LO, Foss A, Imsland AK (2011) Effects of chronic and periodic exposure to ammonia on growth, food conversion efficiency and blood physiology in juvenile Atlantic halibut (Hippoglossus hippoglossus L.) Aquaculture 315:400–406. doi:10.1016/j.aquaculture.2011.03.008

    Article  CAS  Google Scholar 

  • Randall DJ, Tsui TK (2002) Ammonia toxicity in fish. Mar Pollut Bull 45:17–23. doi:10.1016/S0025-326X(02)00227-8

    Article  CAS  PubMed  Google Scholar 

  • Rašković B, Jarić I, Koko V, Spasić M, Dulić Z, Marković Z, Poleksić V (2013) Histopathological indicators: a useful fish health monitoring tool in common carp (Cyprinus carpio Linnaeus, 1758) culture. Cent Eur J Biol 8:975–985. doi:10.2478/s11535-013-0220-y

    Google Scholar 

  • Ravindrababu G, Neeraja P (2012) Histological changes in certain tissues of fish on ambient ammonia stress and post ammonia state (recovery). Int J Adv Biol Res 2:430–435

    Google Scholar 

  • Rodrigues RV, Romano LA, Schwarz MH, Delbos B, Sampaio LA (2014) Acute tolerance and histopathological effects of ammonia on juvenile maroon clownfish Premnas biaculeatus (Block 1790). Aquac Res 45:1133–1139. doi:10.1111/are.12054

    Article  CAS  Google Scholar 

  • Roumieh R, Barakat A, Abdelmeguid NE, Ghanawi J, Saoud IP (2013) Acute and chronic effects of aqueous ammonia on marbled spinefoot rabbitfish, Siganus rivulatus (Forsskål 1775). Aquac Res 44:1777–1790. doi:10.1111/j.1365-2109.2012.03188.x

    CAS  Google Scholar 

  • Sampaio LA, Bianchini A (2002) Salinity effects on osmoregulation and growth of the euryhaline flounder Paralichthys orbignyanus. J Exp Mar Biol Ecol 269:187–196. doi:10.1016/S0022-0981(01)00395-1

    Article  CAS  Google Scholar 

  • Sampaio LA, Freitas LS, Okamoto MH, Louzada LR, Rodrigues RV, Robaldo RB (2007) Effects of salinity on Brazilian flounder Paralichthys orbignyanus from fertilization to juvenile settlement. Aquaculture 262:340–346. doi:10.1016/j.aquaculture.2006.09.046

    Article  CAS  Google Scholar 

  • Sampaio LA, Robaldo RB, Bianchini A (2008) Hormone-induced ovulation, natural spawning and larviculture of Brazilian flounder Paralichthys orbignyanus (Valenciennes, 1839). Aquac Res 39:712–717. doi:10.1111/j.1365-2109.2008.01923.x

    Article  Google Scholar 

  • Schram E, Roques JA, Abbink W, Spanings T, de Vries P, Bierman S, van de Vis H, Flik G (2010) The impact of elevated water ammonia concentration on physiology, growth and feed intake of African catfish (Clarias gariepinus). Aquaculture 306:108–115. doi:10.1016/j.aquaculture.2010.06.005

    Article  CAS  Google Scholar 

  • Schreier HJ, Mirzoyan N, Saito K (2010) Microbial diversity of biological filters in recirculating aquaculture systems. Curr Opin Biotech 21:318–325. doi:10.1016/j.copbio.2010.03.011

    Article  CAS  PubMed  Google Scholar 

  • Schwaiger J, Wanke R, Adam S, Pawert M, Honnen W, Triebskorn R (1997) The use of histopathological indicators to evaluate contaminant-related stress in fish. J Aquat Ecosyst Stress Recovery 6:75–86. doi:10.1023/A:1008212000208

    Article  CAS  Google Scholar 

  • Sevcikova M, Modra H, Blahova J, Dobsikova R, Plhalova L, Zitka O, Hynek D, Kizek R, Skoric M, Svobodova Z (2016) Biochemical, haematological and oxidative stress responses of common carp (Cyprinus carpio L.) after sub-chronic exposure to copper. Vet Med 61:35–50. doi:10.17221/8681-VETMED

    Article  Google Scholar 

  • Sinha AK, AbdElgawad H, Giblen T, Zinta G, De Rop M, Asard H, Blust R, De Boeck G (2014) Anti-oxidative defences are modulated differentially in three freshwater teleosts in response to ammonia-induced oxidative stress. PLoS One 9:e95319. doi:10.1371/journal.pone.0095319

    Article  PubMed  PubMed Central  Google Scholar 

  • Stoliar OB, Lushchak VI (2012) Environmental pollution and oxidative stress in fish. In: Lushchak VI (ed) Oxidative stress-environmental induction and dietary antioxidants. InTech. http://www.intechopen.com/books/oxidative-stress-environmental-induction-and-dietary-antioxidants/environmental-pollution-and-oxidative-stress-in-fish. Accessed 2 February 2017

  • Sun H, Wang W, Li J, Yang Z (2014) Growth, oxidative stress responses, and gene transcription of juvenile bighead carp (Hypophthalmichthys nobilis) under chronic-term exposure of ammonia. Environ Toxicol Chem 33:1726–1731. doi:10.1002/etc.2613

    Article  CAS  PubMed  Google Scholar 

  • Velisek J, Stara A, Kolarova J, Svobodova Z (2011) Biochemical, physiological and morfological responses in common carp (Cyprinus carpio L.) after long-term exposure to terbutryn in real environmental concentration. Pestic Biochem Phys 100:305–313. doi:10.1016/j.pestbp.2011.05.004

    Article  CAS  Google Scholar 

  • Wasielesky W, Bianchini A, Miranda FK (1998) Tolerancia a la temperatura de juveniles de lenguado Paralichthys orbignyanus. Frente Marítimo 17:43–48

    Google Scholar 

  • Wasielesky W, Bianchini A, Santos MH, Poersch LH (1997) Tolerance of juvenile flatfish Paralichthys orbignyanus to acid stress. J World Aquacult Soc 28:202–204. doi:10.1111/j.1749-7345.1997.tb00857.x

    Article  Google Scholar 

  • Wilhelm Filho D, Giulivi C, Boveris A (1993) Antioxidant defences in marine fish-I. Teleosts. Comp Biochem Phys C Pharmacol Toxicol Endocrinol 106:409–413. doi:10.1016/0742-8413(93)90154-D

    Article  Google Scholar 

  • Wilkie MP, Wood CM (1996) The adaptations of fish to extremely alkaline environments. Comp Biochem Phys B Biochem Mol Biol 113:665–673. doi:10.1016/0305-0491(95)02092-6

    Article  Google Scholar 

  • Yang W, Sun H, Xiang F, Yang Z, Chen Y (2011) Response of juvenile crucian carp (Carassius auratus) to long-term ammonia exposure: feeding, growth, and antioxidant defenses. J Freshw Ecol 26:563–570. doi:10.1080/02705060.2011.570944

    CAS  Google Scholar 

  • Yang W, Xiang F, Liang L, Yang Z (2010a) Toxicity of ammonia and its effects on oxidative stress mechanisms of juvenile crucian carp (Carassius auratus). J Freshw Ecol 25:297–302. doi:10.1080/02705060.2010.9665080

    Article  CAS  Google Scholar 

  • Yang W, Xiang F, Sun H, Chen Y, Minter E, Yang Z (2010b) Changes in the selected hematological parameters and gill Na+/K+ ATPase activity of juvenile crucian carp Carassius auratus during elevated ammonia exposure and the post-exposure recovery. Biochem Syst Ecol 38:557–562. doi:10.1016/j.bse.2010.06.005

    Article  CAS  Google Scholar 

  • Zhang L, Feng L, Jiang WD, Liu Y, Jiang J, Li SH, Tang L, Kuang SY, Zhou XQ (2016) The impaired flesh quality by iron deficiency and excess is associated with increasing oxidative damage and decreasing antioxidant capacity in the muscle of young grass carp (Ctenopharyngodon idellus). Aquac Nutr 22:191–201. doi:10.1111/anu.12237

    Article  CAS  Google Scholar 

  • Zivna D, Plhalova L, Praskova E, Stepanova S, Siroka Z, Sevcikova M, Blahova J, Bartoskova M, Marsalek P, Skoric M, Svobodova Z (2013) Oxidative stress parameters in fish after subchronic exposure to acetylsalicylic acid. Neuroendocrinol Lett 34:116–122

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by research funds from the Conselho Nacional de Pesquisa e Desenvolvimento Científico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). The authors are grateful to CNPq for productivity research fellowships provided for L. Garcia, L. Sampaio, L. Romano and J. Monserrat, and to CAPES for a PhD scholarship provided for MSc. Lucas C. Maltez.

Author information

Authors and Affiliations

  1. Laboratório de Aquacultura Continental, Instituto de Oceanografia, Universidade Federal do Rio Grande – FURG, Rio Grande, RS, 96201-900, Brazil

    Lucas Campos Maltez, Giovanna Rodrigues Stringhetta & Luciano Garcia

  2. Laboratório de Bioquímica Funcional de Organismos Aquáticos, Universidade Federal do Rio Grande – FURG, Rio Grande, RS, Brazil

    Alain Danilo Enamorado & José María Monserrat

  3. Laboratório de Piscicultura Estuarina e Marinha, Instituto de Oceanografia, Universidade Federal do Rio Grande – FURG, Rio Grande, RS, Brazil

    Marcelo Hideo Okamoto & Luís André Sampaio

  4. Laboratório de Imunologia e Patologia de Organismos Aquáticos, Instituto de Oceanografia, Universidade Federal do Rio Grande – FURG, Rio Grande, RS, Brazil

    Luis Alberto Romano

Authors
  1. Lucas Campos Maltez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giovanna Rodrigues Stringhetta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alain Danilo Enamorado
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcelo Hideo Okamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luis Alberto Romano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. José María Monserrat
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luís André Sampaio
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Luciano Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luciano Garcia.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maltez, L.C., Stringhetta, G.R., Enamorado, A.D. et al. Ammonia exposure and subsequent recovery trigger oxidative stress responses in juveniles of Brazilian flounder Paralichthys orbignyanus . Fish Physiol Biochem 43, 1747–1759 (2017). https://doi.org/10.1007/s10695-017-0406-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-017-0406-8

Keywords

Search

Navigation