Hydrobiologia

, Volume 789, Issue 1, pp 143–155 | Cite as

Are Amazonian fish more sensitive to ammonia? Toxicity of ammonia to eleven native species

  • Luciana R. Souza-Bastos
  • Adalberto Luis Val
  • Chris M. Wood
ADAPTA

Abstract

Little is known about the tolerance of Amazonian fish to ammonia. However, elevated ammonia of anthropogenic origin may now occur. As Amazonian fish evolved in waters which are generally acidic (i.e., low NH3), we hypothesized that they would be more sensitive to ammonia than other freshwater fish. The acute (96-h) toxicity of NH4Cl was tested in native ion-poor soft water (pH 7.0, ~28 °C) using semi-static tests with 11 species. Species sensitivity distributions (SSDs) for LC5096 h and LC1096 h and calculations of the hazardous concentrations to the most sensitive 5% (HC5 values) were tabulated. Values of LC5096 h/LC1096 h (in mM total ammonia) ranged from 2.24/0.78 for Paracheirodon axelrodi (most sensitive) to 19.53/16.07 for Corydoras schwartzi (most tolerant). These results confirm our hypothesis that Amazonian fish are more sensitive to ammonia than other freshwater species. High levels of ammonia may be associated with hypoxia, especially during dry periods. Simultaneous hypoxia (15–20% saturation) exacerbated ammonia toxicity in the most sensitive species (P. axelrodi), but not in Astronotus ocellatus or Corydoras schwartzi, a facultative air-breather where prevention of air access doubled ammonia toxicity. The present data are useful in generating regulatory guidelines in Amazonian waters and indicate that further studies incorporating hypoxia and air access/denial are needed.

Keywords

Air-breathing Amazonian fish Ammonia HC5 Hypoxia LC50 SSD 

Notes

Acknowledgments

The authors wish to acknowledge the financing by INCT-ADAPTA (CNPq No. 573976/2008-2/FAPEAM 3159/08) and Science without Borders (CNPq—CsF No. 400311/2012-7) awarded to A. L. V. and C. M. W. with post-doctoral fellowships awarded to L. R. S-B (CNPq—CsF No. 151446/2014-8). The authors also thank Dr. Aleicia Holland for her contributions to the SSD analyses, Dr. Tyler Linton for advice on U.S. EPA procedures, and Dr Jansen Zuanon for species identification.

Supplementary material

10750_2015_2623_MOESM1_ESM.docx (49 kb)
Supplementary material 1 (DOCX 48 kb)

References

  1. Adad, J. M. T., 1982. Controle químico de qualidade da água. Guanabara Press, Rio de Janeiro.Google Scholar
  2. Almeida-Val, V. M. F., A. L. Val, W. P. Duncan, F. C. A. Souza, M. N. Paula-Silva & S. Land, 2000. Scaling effects on hypoxia tolerance in the Amazon fish Astronotus ocellatus (Perciformes: Cichlidae): contribution of tissue enzyme levels. Comparative Biochemistry and Physiology B 125: 219–226.CrossRefGoogle Scholar
  3. Barbieri, E. & A. C. V. Bondioli, 2015. Acute toxicity of ammonia in Pacu fish (Piaractus mesopotamicus, Holmberg, 1887) at different temperatures levels. Aquaculture Research 46: 565–571.CrossRefGoogle Scholar
  4. Brauner, C. J., C. L. Ballantyne, D. J. Randall & A. L. Val, 1995. Air breathing in the armoured catfish (Hoplosternum littorale) as an adaptation to hypoxic, acidic, and hydrogen sulphide rich waters. Canadian Journal of Zoology 73: 739–744.CrossRefGoogle Scholar
  5. Brauner, C. J., V. Matey, J. M. Wilson, N. J. Bernier & A. L. Val, 2004. Transition in organ function during the evolution of air-breathing; insights from Arapaima gigas, an obligate air-breathing teleost from the Amazon. Journal Experimental Biology 207: 1433–1438.CrossRefGoogle Scholar
  6. Bringel, S. R. B. & D. Pascoaloto, 2012. As águas transfronteiriças do Alto Rio Negro. In: Souza, L. A. G. & E. G. Castellón (eds), Projeto Fronteiras: Desvendando as Fronteiras do conhecimento na Região Amazônica do Alto Rio Negro. Chapter 1: 7–22.Google Scholar
  7. Brito, J. G., L. F. Alves & H. M. V. Espirito Santo, 2014. Seasonal and spatial variations in limnological conditions of a floodplain lake (Lake Catalão) connected to both the Solimões and Negro Rivers, Central Amazonia. Acta Amazonica 44: 121–134.CrossRefGoogle Scholar
  8. Camargo, J. A. & A. Alonso, 2006. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environment International 32: 831–849.CrossRefPubMedGoogle Scholar
  9. Cavero, B. A. S., M. Pereira-Filho, A. M. Bordinhon, F. A. L. Fonseca, D. R. Ituassú, R. Roubach & E. A. Ono, 2004. Tolerância de juvenis de pirarucu ao aumento da concentração de amônia em ambiente confinado. Pesquisa Agropecuária Brasileira 39: 513–516.CrossRefGoogle Scholar
  10. CCME – Canadian Council of Ministers of the Environment, 2010. Ammonia. In Canadian environmental quality guidelines for the protection of aquatic life, 1999 – ammonia. Canadian Council of Ministers of the Environment, Winnipeg, CanadaGoogle Scholar
  11. Chew, S. F., J. M. Wilson, Y. K. Ip & D. J. Randall, 2005. Nitrogen excretion and defense against ammonia toxicity. In: Val, A. L., V. M. F. Almeida-Val & D. J. Randall (eds), Fish Physiology: The Physiology of Tropical Fishes, vol. 21, Chapter 8. Academic Press, San Diego: 307–379.Google Scholar
  12. Chew, S. F. & Y. K. Ip, 2014. Excretory nitrogen metabolism and defence against ammonia toxicity in air-breathing fishes. Journal of Fish Biology 84: 603–638.CrossRefPubMedGoogle Scholar
  13. CONAMA – Conselho Nacional do Meio Ambiente, 2005. Resolução No 357, de 17 de Março de 2005, pp. 58–65. http://www.mma.gov.br/port/conama/res/res05/res35705.pdf. Accessed on 27 Apr, 2015.
  14. Couceiro, S. R., N. Hamada, S. L. Luz, B. R. Forsberg & T. P. Pimentel, 2007. Deforestation and sewage effects on aquatic macroinvertebrates in urban streams in Manaus, Amazonas, Brazil. Hydrobiologia 575: 271–284.CrossRefGoogle Scholar
  15. Cunha, H. B. & D. Pascoaloto, 2009. Hidroquímica dos Rios da Amazônia. Manaus – Governo do Estado do Amazonas – Secretaria do Estado da Cultura, Coleção Cadernos da Amazônia.Google Scholar
  16. Damato, M. & E. Barbieri, 2011. Determinação da toxicidade aguda de cloreto de amônia para uma espécie de peixe (Hyphessobrycon callistus) indicadora regional. O Mundo da Saúde 35: 401–407.Google Scholar
  17. De Boeck, G., C. M. Wood, F. I. Iftikar, V. Matey, G. R. Scott, K. A. Sloman, M. N. P. Silva, V. Almeida-Val & A. L. Val, 2013. Interactions between hypoxia tolerance and food deprivation in Amazonian Oscars, Astronotus ocellatus. Journal of Experimental Biology 216: 4590–4600.CrossRefPubMedGoogle Scholar
  18. Dinesh, B., M. Ramesh & R. K. Poopal, 2013. Effect of ammonia on the electrolyte status of an Indian major carp Catla catla. Aquaculture Research 44: 1677–1684.Google Scholar
  19. Duncan, W. P. & M. N. Fernandes, 2010. Physicochemical characterization of the white, black and clear water rivers of the Amazon Basin and its implications on the distribution of freshwater stingrays (Chondrichthyes, Potamotrygonidae). Pan-American Journal of Aquatic Science 5: 454–464.Google Scholar
  20. Emerson, K., R. C. Russo, R. E. Lund & R. V. Thurston, 1975. Aqueous ammonia equilibrium calculations: effect of pH and temperature. Journal of the Fisheries Research Board of Canada 32: 2379–2383.CrossRefGoogle Scholar
  21. Finney, D. J., 1978. Statistical Methods in Biological Assay, 3rd ed. Charles Griffin & Company, London.Google Scholar
  22. Furch, K., 1984. Water chemistry of the Amazon basin: the distribution of chemical elements among freshwaters. the Amazon. Springer, Netherlands: 167–199.CrossRefGoogle Scholar
  23. Graham, J. B., 1997. Air-Breathing Fishes: Evolution, Diversity and Adaptation. Academic Press, San Diego.Google Scholar
  24. Graham, J. B., 1999. Comparative aspects of air-breathing fish biology: an agenda for some Neotropical species. In Val, A. L. & V. M. F. Almeida-Val (eds), Biology of Tropical Fishes, Chapter 25. Inpa, Manaus: 317–331.Google Scholar
  25. Ip, Y. K. & S. F. Chew, 2010. Ammonia production, excretion, toxicity and defense in fish: A review. Frontiers in Physiology 1: 1–20.CrossRefGoogle Scholar
  26. Ip, Y. K., S. F. Chew & D. J. Randall, 2001. Ammonia toxicity, tolerance and excretion. In Anderson, P. & P. Wright (eds), Fish physiology: nitrogen excretion, v.20, Chapter 4. Academic Press, Elsevier: 109–148.CrossRefGoogle Scholar
  27. Kwok, K. W. H., K. M. Y. Leung, G. S. G. Lui, V. K. H. Chu, P. K. S. Lam, D. Morritt, L. Maltby, T. C. M. Brock, P. J. Van den Brink, M. St, J. Warne & M. Crane, 2007. Comparison of tropical and temperate freshwater animal species’ acute sensitivities to chemicals: implications for deriving safe extrapolation factors. Integrated Environmental Assessment and Management 3: 49–67.CrossRefPubMedGoogle Scholar
  28. Langeani, F., P. A. Buckup, L. R. Malabarba, L. H. R. Py-Daniel, C. A. S. Lucena, R. S. Rosa, J. A. S. Zuanon, Z. M. S. Lucena, M. R. Britto, O. T. Oyakawa & G. Gomes-Filho, 2009. Peixes de Água Doce. In Rocha, R. M. & W. A. Boeger (eds), Estado da Arte e Perspectivas para a Zoologia no Brasil, Ed. UFPR, Curitiba, Chapter 13: 211–230.Google Scholar
  29. Lefevre, S., T. Wang, A. Jensen, N. V. Cong, D. T. T. Huong, N. T. Phuong & M. Bayley, 2014. Air-breathing fishes in aquaculture. What can we learn from physiology? Journal of Fish Biology 84: 705–731.CrossRefPubMedGoogle Scholar
  30. Lévêque, C., T. Oberdorff, D. Paugy, M. J. L. Stiassny & P. A. Tedesco, 2008. Global diversity of fish (Pisces) in freshwater. Hydrobiologia 595: 545–567.CrossRefGoogle Scholar
  31. Martinez, C. B. R., F., Azevedo & E. U. Winkaler, 2006. Toxicidade e efeitos da amônia em peixes neotropicais. In Cyrino J. E. P.& E. C. Urbinati (Eds), Tópicos Especiais em Biologia Aquática e Aqüicultura. Sociedade Brasileira de Aqüicultura e Biologia Aquática. Jaboticabal – SP: 81–95.Google Scholar
  32. Miron, D. S., B. Moraes, A. G. Becker, M. Crestani, R. Spanevello, V. L. Loro & B. Baldisserotto, 2008. Ammonia and pH effects on some metabolic parameters and gill histology of silver catfish, Rhamdia quelen (Heptapteridae). Aquaculture 277: 192–196.CrossRefGoogle Scholar
  33. Muusze, B., J. Marcon, G. V. D. Thillart & V. M. F. Almeida-Val, 1998. Hypoxia tolerance of Amazon fish respirometry and energy metabolism of the cichlid Astronotus ocellatus. Comparative Biochemistry and Physiology A 120: 151–156.CrossRefGoogle Scholar
  34. Nelson, J. A., 2014. Breaking wind to survive: Fishes that breathe air with their gut. Journal of Fish Biology 84: 554–576.CrossRefPubMedGoogle Scholar
  35. Oliveira, S. R., R. T. Y. B. Souza, E. S. S. Nunes, C. S. M. Carvalho, G. C. Menezes, J. L. Marcon, R. Roubach, E. A. Ono & E. G. Affonso, 2008. Tolerance to temperature, pH, ammonia and nitrite in cardinal tetra, Paracheirodon axelrodi, an amazonian ornamental fish. Acta Amazonica 38: 773–780.CrossRefGoogle Scholar
  36. Piedras, S. R. N., J. L. R. Oliveira, P. R. R. Moraes & A. Bager, 2006. Toxicidade aguda da amônia não ionizada e do nitrito em alevinos de Cichlasoma facetum (Jenyns, 1842). Ciência e agrotecnologia 30: 1008–1012.CrossRefGoogle Scholar
  37. Perz, S. G., 2000. The quality of urban environments in the Brazilian Amazon. Social Indicators Research 49: 181–212.CrossRefGoogle Scholar
  38. Randall, D. J. & T. K. N. Tsui, 2002. Ammonia toxicity in fish. Marine Pollution Bulletin 45: 17–23.CrossRefPubMedGoogle Scholar
  39. Randall, D. J. & Y. K. Ip, 2006. Ammonia as a respiratory gas in water and air-breathing fishes. Respiratory Physiology and Neurobiology 154: 216–225.CrossRefPubMedGoogle Scholar
  40. Robertson, L. M., A. L. Val, V. M. F. Almeida-Val & C. M. Wood, 2015. Ionoregulatory aspects of the osmorespiratory compromise during acute environmental hypoxia in 12 tropical and temperate teleosts. Physiological and Biochemical Zoology 88: 357–370.CrossRefPubMedGoogle Scholar
  41. Sprague, J. B., 1969. Measurement of pollutant toxicity to fish. I. Bioassay methods for acute toxicity. Water Research 5: 245–266.CrossRefGoogle Scholar
  42. Tomasso, J. R., C. A. Goudie, B. A. Simco & K. B. Davis, 1980. Effects of environmental pH and calcium on ammonia toxicity in channel catfish. Transactions of the American Fisheries Society 109: 229–234.CrossRefGoogle Scholar
  43. U.S. EPA – United States Environmental Protection Agency, 1999. Update of ambient water quality criteria for ammonia. EPA-822-R-99-014. EPA, Washington.Google Scholar
  44. U.S. EPA – United States Environmental Protection Agency, 2013. Aquatic life ambient water quality criteria for ammonia- freshwater. EPA-822-R-13-001. EPA, Washington.Google Scholar
  45. Val, A. L. & V. M. F. Almeida-Val, 1995. Fishes of the Amazon and their environment. Springer, Berlin.CrossRefGoogle Scholar
  46. Verdouw, H., C. J. A. van Echteld & E. M. J. Dekkers, 1978. Ammonia determination based on indophenols formation with sodium salicylate. Water Research 12: 399–402.CrossRefGoogle Scholar
  47. Wajsbrot, N., A. Gasith, M. D. Krom & D. M. Popper, 1991. Acute toxicity of ammonia to juvenile gilthead seabream Sparus aurata under reduced oxygen levels. Aquaculture 92: 277–288.CrossRefGoogle Scholar
  48. Walsh, P. J., C. M. Veauvy, D. M. McDonald, M. E. Pamenter, L. T. Buck & M. P. Wilkie, 2007. Piscine insights into comparisons of anoxia tolerance, ammonia toxicity, stroke and hepatic encephalopathy. Comparative Biochemistry and Physiology A 147: 332–343.CrossRefGoogle Scholar
  49. Wee, N. L. J., Y. Y. M. Tng, H. T. Cheng, S. M. L. Lee, S. F. Chew & Y. K. Ip, 2007. Ammonia toxicity and tolerance in the brain of the African sharptooth catfish, Clarias gariepinus. Aquatic Toxicology 82: 204–213.CrossRefPubMedGoogle Scholar
  50. Wilkie, M. P., 1997. Mechanism of ammonia excretion across fish gills. Comparative Biochemistry and Physiology A 118: 39–50.CrossRefGoogle Scholar
  51. Wilkie, M. P., 2002. Ammonia excretion and urea handling by fish gills: Present understanding and future research challenges. Journal of Experimental Zoology 293: 284–301.CrossRefPubMedGoogle Scholar
  52. Wood, C. M., M. Kajimura, K. A. Sloman, G. R. Scott, P. J. Walsh, V. M. F. Almeida-Val & A. L. Val, 2007. Rapid regulation of Na+ fluxes and ammonia excretion in response to acute environmental hypoxia in the Amazonian oscar, Astronotus ocellatus. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 292: R2048–R2058.CrossRefPubMedGoogle Scholar
  53. Wood, C. M., F. I. Iftikar, G. R. Scott, G. De Boeck, K. A. Sloman, V. Matey, F. X. Valdez Domingos, R. M. Duarte, V. M. F. Almeida-Val & A. L. Val, 2009. Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): new angles to the osmorespiratory compromise. The Journal of Experimental Biology 212: 1949–1964.CrossRefPubMedGoogle Scholar
  54. Wood, C. M., L. M. Robertson, O. E. Johannsson & A. L. Val, 2014. Mechanisms of Na+ uptake, ammonia excretion, and their potential linkage in native Rio Negro tetras (Paracheirodon axelrodi, Hemigrammus rhodostomus, and Moenkhausia diktyota). The Journal of Comparative Physiology B 184: 877–890.CrossRefGoogle Scholar
  55. Zall, D. M., D. Fisher & M. Q. Garner, 1956. Photometric determination of chloride in water. Analytical Chemistry 28: 1665–1668.CrossRefGoogle Scholar
  56. Zhang, L., D. M. Xiong, B. Li, Z. G. Zhao, W. Fang, K. Yang & Q. X. Fan, 2012. Toxicity of ammonia and nitrite to yellow catfish (Pelteobagrus fulvidraco). Journal of Applied Ichthyology 28: 82–86.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Luciana R. Souza-Bastos
    • 1
  • Adalberto Luis Val
    • 1
  • Chris M. Wood
    • 2
  1. 1.Laboratório de Ecofisiologia e Evolução Molecular, Instituto Nacional de Pesquisas da Amazônia (INPA)ManausBrazil
  2. 2.Department of ZoologyUniversity of British ColumbiaVancouverCanada

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