Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Influence of the natural Rio Negro water on the toxicological effects of a crude oil and its chemical dispersion to the Amazonian fish Colossoma macropomum

Abstract

The increment in crude oil exploitation over the last decades has considerably increased the risk of polycyclic aromatic hydrocarbon (PAH) contamination to Amazonian aquatic environments, especially for the black water environments such as the Rio Negro. The present work was designed to evaluate the acute toxicity of the Urucu crude oil (CO), the chemically dispersed Urucu crude oil (CO + D), and the dispersant alone (D) to the Amazonian fish Colossoma macropomum. Acute toxicity tests were performed, using a more realistic approach, where fish were acclimated to both groundwater (GW), used as internal control, and natural Rio Negro water (RNW) and exposed to CO, CO + D and D. Then, biomarkers such as ethoxyresorufin-O-deethylase (EROD), superoxide dismutase (SOD), lipid peroxidation (LPO), serum sorbitol dehydrogenase (s-SDH) in liver, DNA damage in blood cells, and the presence of the benzo[a]pyrene-type, pyrene-type, and naphthalene-type metabolites in fish bile were assessed. Fish exposed to CO and CO + D, at both water types tested, presented increased biomarker responses and higher PAH-type metabolites in the bile. However, fish exposed to these treatments after the acclimation to RNW increased the levels of LPO, s-SDH (hepatotoxicity), DNA damage in blood cells (genotoxicity), and benzo[a]pyrene-type metabolites when compared to fish in GW. Our data suggests that some physicochemical properties of Rio Negro water (i.e., presence of natural organic matter (NOM)) might cause mild chemical stress responses in fish, which can make it more susceptible to oxidative stress following exposure to crude oil, particularly to those chemically dispersed.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Aas E, Baussant T, Balk L, Liewenborg B (2000) PAH metabolites in bile, cytochrome P4501A and DNA adducts as environmental risk parameters for chronic oil exposure: a laboratory experiment with Atlantic cod. Aquat Toxicol 51:241–258

  2. Achuba, F, Osakwe S (2003) Petroleum-induced free radical toxicity in African catfish (Clarias gariepinus). Fish Physiol Biochem 97–103

  3. Akkanen J, Tuikka A, Kukkonen JVK (2012) On the borderline of dissolved and particulate organic matter: partitioning and bioavailability of polycyclic aromatic hydrocarbons. Ecotoxicol Environ Saf 78:91–98. doi:10.1016/j.ecoenv.2011.11.010

  4. Anderson JW, Neff JM, Cox BA, et al. (1974) Characteristics of dispersions and water-soluble extracts of crude and refined oils and their toxicity to estuarine crustaceans and fish. Mar Biol 27:75–88. doi:10.1007/BF00394763

  5. Bernhardt R (1995) Cytochrome P450: structure, function, and generation of reactive oxygen species. In: Reviews of physiology biochemistry and pharmacology, 127. Springer-Verlag, Berlin/Heidelberg, pp. 137–221

  6. Bradford MM (1976) A rapid and sensitive method for the quantitation microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

  7. Brauner CJ, Ballantyne CL, Vijayan MM, Val AL (1999) Crude oil exposure affects air-breathing frequency, blood phosphate levels and ion regulation in an air-breathing teleost fish, Hoplosternum littorale. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 123:127–134. doi:10.1016/S0742-8413(99)00018-3

  8. Braz-Mota S, Sadauskas-Henrique H, Duarte RM, et al. (2015) Roundup® exposure promotes gills and liver impairments, DNA damage and inhibition of brain cholinergic activity in the Amazon teleost fish Colossoma macropomum. Chemosphere 135:53–60. doi:10.1016/j.chemosphere.2015.03.042

  9. Camus L, Aas E, Børseth JF (1998) Ethoxyresorufin-O-deethylase activity and fixed wavelength fluorescence detection of PAHs metabolites in bile in turbot (Scophthalmus maximus L.) exposed to a dispersed topped crude oil in a continuous flow system. Mar Environ Res 46:29–32. doi:10.1016/S0141-1136(97)00045-7

  10. Cho H-H, Choi J, Goltz MN, Park J-W (2002) Combined effect of natural organic matter and surfactants on the apparent solubility of polycyclic aromatic hydrocarbons. J Environ Qual 31:275–280. doi:10.2134/jeq2002.0275

  11. CONAMA (2000) Resolucao CONAMA no 269, Regulamenta o uso de dispersantes quimicos em derrames de oleo no mar. Conselho Nacional do Meio Ambiente, Brazil

  12. Conte P, Agretto A, Spaccini R, Piccolo A (2005) Soil remediation: humic acids as natural surfactants in the washings of highly contaminated soils. Environ Pollut 135:515–522. doi:10.1016/j.envpol.2004.10.006

  13. Dave D, Ghaly AE (2011) Remediation technologies for marine oil spills : a critical review and comparative analysis. Am J Environ Sci 7:423–440

  14. Dixon DG, Hodson PV, Kaiser KLE (1987) Serum sorbitol dehydrogenase activity as an indicator of chemically induced liver damage in rainbow trout. Environ Toxicol Chem 6:685–696. doi:10.1002/etc.5620060906

  15. Duarte RM, Honda RT, Val AL (2010) Acute effects of chemically dispersed crude oil on gill ion regulation, plasma ion levels and haematological parameters in tambaqui (Colossoma macropomum). Aquat Toxicol 97:134–141. doi:10.1016/j.aquatox.2009.12.020

  16. Duarte RM, Smith DS, Val AL, Wood CM (2016) Dissolved organic carbon from the upper Rio Negro protects zebrafish (Danio rerio) against ionoregulatory disturbances caused by low pH exposure. Sci Rep 6:1–10. doi:10.1038/srep20377

  17. Dû-Lacoste ML, Akcha F, Dévier MH, et al. (2013) Comparative study of different exposure routes on the biotransformation and genotoxicity of PAHs in the flatfish species, Scophthalmus maximus. Environ Sci Pollut Res 20:690–707. doi:10.1007/s11356-012-1388-9

  18. Filizola N, Spínola N, Arruda W, et al. (2010) The Rio Negro and Rio Solimões confluence point – hydrometric observations during the 2006/ 2007 cycle. River, Coast Estuar Morphodynamics RCEM 2009:1003–1006

  19. George-Ares A, Clark JR (2000) Aquatic toxicity of two Corexit® dispersants. Chemosphere 40:897–906. doi:10.1016/S0045-6535(99)00498-1

  20. Haitzer M, Hgss S, Traunspurger W, Steingberg C (2002) Effects of dissolved organic matter (DOM) on the bioconcentration of organic chemicals in aquatic organisms—a review-. Chemosphere 37:1335–1362

  21. Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150. doi:10.1042/BST0351147

  22. He YL, Murby S, Warhurst G, et al. (1998) Species differences in size discrimination in the paracellular pathway reflected by oral bioavailability of poly(ethylene glycol) and D-peptides. J Pharm Sci 87:626–633. doi:10.1021/js970120d

  23. Hemmer MJ, Barron MG, Greene RM (2011) Comparative toxicity of eight oil dispersants, Louisiana sweet crude oil (LSC), and chemically dispersed LSC to two aquatic test species. Environ Toxicol Chem 30:2244–2252. doi:10.1002/etc.619

  24. Jancova P, Anzenbacher P, Anzenbacherova E (2010) Phase II drug metabolizing enzymes. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 154:103–116. doi:10.5507/bp.2010.017

  25. Jiang ZY, Woollard ACS, Wolff SP (1991) Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 26:853–856. doi:10.1007/BF02536169

  26. Johannsson OE, Smith DS, Sadauskas-Henrique H, et al (2016) Photo-oxidation processes, properties of DOC, reactive oxygen species (ROS), and their potential impact on native biota and carbon cycling in the Rio Negro (Amazonia, Brazil). Hydrobiologia in press.

  27. Johnson WP, John WW (1999) PCE solubilization and mobilization by commercial humic acid. J Contam Hydrol 35:343–362

  28. Keen JH, Habig WH, Jakoby WB (1976) Mechanism for the several activities of the glutathione S transferases. J Biol Chem 251:6183–6188

  29. Kobayashi H, Sugiyama C, Morikawa Y, et al. (1995) A comparison between manual microscopic analysis and computerized image analysis in the single cell gel electrophoresis assay. MMS Commun 3:103–115

  30. Kochhann D, Brust SMA, Domingos FXV, Val AL (2013) Linking hematological, biochemical, genotoxic, and behavioral responses to crude oil in the Amazon fish Colossoma macropomum (Cuvier, 1816). Arch Environ Contam Toxicol 65:266–275. doi:10.1007/s00244-013-9894-4

  31. Krahn MM, Rhodes LD, Myers MS, et al. (1986) Associations between metabolites of aromatic compound in bile and the occurrence of hepatic lesions in english sole (Parophrys vetulus) from Puget sound, Washington. Arch Environ Contam Toxicol 15:61–67

  32. Landrum PF, Nihart SR, Eadie BJ, Gardner WS (1984) Reverse-phase separation method for determining pollutant binding to Aldrich humic acid and dissolved organic carbon of natural waters. Environ Sci Technol 18:187–192. doi:10.1021/es00121a010

  33. Lin EL, Cormier SM, Torsella JA (1996) Fish biliary polycyclic aromatic hydrocarbon metabolites estimated by fixed-wavelength fluorescence: comparison with HPLC-fluorescent detection. Ecotoxicol Environ Saf 35:16–23. doi:10.1006/eesa.1996.0077

  34. Lippold H, Gottschalch U, Kupsch H (2008) Joint influence of surfactants and humic matter on PAH solubility. Are mixed micelles formed? Chemosphere 70:1979–1986. doi:10.1016/j.chemosphere.2007.09.040

  35. Matsuo AYO, Duarte RM, Val AL (2005) Unidirectional sodium fluxes and gill CYP1A induction in an Amazonian fish (Hyphessobrycon erythrostigma) exposed to a surfactant and to crude oil. Bull Environ Contam Toxicol 75:851–858. doi:10.1007/s00128-005-0828-3

  36. Matsuo AYO, Woodin BR, Reddy CM, et al. (2006) Humic substances and crude oil induce cytochrome P450 1 A expression in the amazonian fish species Colossoma macropomum (tambaqui). Environ Sci Technol 40:2851–2858. doi:10.1021/es052437i

  37. McCord J, Fridovich I (1969) Superoxide dismutase an Enzymic function for Erythrocuprein (Hemocuprein). J Biol Chem 244:6049–6055

  38. McGeer JC, Szebedinszky C, McDonald DG, Wood CM (2002) The role of dissolved organic carbon in moderating the bioavailability and toxicity of Cu to rainbow trout during chronic waterborne exposure. Comp Biochem Physiol Part C 133:147–160

  39. Menzel R, Stürzenbaum S, Bärenwaldt A, et al. (2005) Humic material induces behavioral and global transcriptional responses in the nematode Caenorhabditis elegans. Environ Sci Technol 39:8324–8332. doi:10.1021/es050884s

  40. Milinkovitch T, Ndiaye A, Sanchez W, et al. (2011) Liver antioxidant and plasma immune responses in juvenile golden grey mullet (Liza aurata) exposed to dispersed crude oil. Aquat Toxicol 101:155–164. doi:10.1016/j.aquatox.2010.09.013

  41. Moeckel C, Monteith DT, Llewellyn NR, et al. (2014) Relationship between the concentrations of dissolved organic matter and polycyclic aromatic hydrocarbons in a typical U.K. upland stream. Environ Sci Technol 48:130–138

  42. Nardi S, Pizzeghello D (2002) Physiological effects of humic substances on higher plants. Soil Biol Biochem 34:1527–1536. doi:10.1016/S0038-0717(02)00174-8

  43. National Research Council (1989) Using oil spills dispersants on the sea. National Academy Press, Washington, DC

  44. Niki E (2009) Lipid peroxidation: physiological levels and dual biological effects. Free Radic Biol Med 47:469–484. doi:10.1016/j.freeradbiomed.2009.05.032

  45. Nogueira L, Rodrigues ACF, Trídico CP, et al. (2011) Oxidative stress in Nile tilapia (Oreochromis niloticus) and armored catfish (Pterygoplichthys anisitsi) exposed to diesel oil. Environ Monit Assess 180:243–255. doi:10.1007/s10661-010-1785-9

  46. Nongnutch K, Nanuam J, Somnuek C (2012) The efficiency of PAH metabolites fluorescence intensity measurement to study PAHs contamination. Environ Nat Resour Res 2:32–37. doi:10.5539/enrr.v2n2p32

  47. Oliveira TCS (2007) Caracterização de marcadores moleculares e uso de diferentes proxis para estudo do registro de combustão em sedimento na Amazônia Central (Coari-Manaus). Pontificia Universidade Catolica/ PUC-Rio

  48. Petrobrás (1997) Características do petróleo de Urucu. CENPES/SEPESQ/DIQUIM/SETAV 10 p. Anexo V

  49. Piccolo A, Mbagwu JSC (1994) Humic substances and surfactants effects on the stability of two tropical soils. Soil Sci Soc Am J 58:950. doi:10.2136/sssaj1994.03615995005800030044x

  50. Pinto AGN, Horbe AMC, Silva MSR, Miranda SAF, Pascoaloto D, Santos HMC (2009) The human action effects on the hydrogeochemistry of negro river at the Manaus shoreline. Acta Amaz 39(3):627–638. doi:10.1590/S0044-59672009000300018

  51. Ramachandran SD, Hodson PV, Khan CW, Lee K (2004) Oil dispersant increases PAH uptake by fish exposed to crude oil. Ecotoxicol Environ Saf 59:300–308. doi:10.1016/j.ecoenv.2003.08.018

  52. Ramachandran SD, Sweezey MJ, Hodson PV, et al. (2006) Influence of salinity and fish species on PAH uptake from dispersed crude oil. Mar Pollut Bull 52:1182–1189. doi:10.1016/j.marpolbul.2006.02.009

  53. Roditi HA, Fisher NS, Sanudo-Wilhelmy SA (2000) Uptake of dissolved organic carbon and trace elements by zebra mussels. Nature 407:78–80

  54. Shukla P, Gopalani M, Ramteke DS, Wate SR (2007) Influence of salinity on PAH uptake from water soluble fraction of crude oil in Tilapia mossambica. Bull Environ Contam Toxicol 79:601–605. doi:10.1007/s00128-007-9272-x

  55. Silva J, Freitas TRO, Marinho JR, et al. (2000) An alkaline single-cell gel electrophoresis (comet) assay for environmental biomonitoring with native rodents. Genet Mol Biol 23:241–245. doi:10.1590/S1415-47572000000100042

  56. Simonato JD, Fernandes MN, Martinez CBR (2011) Gasoline effects on biotransformation and antioxidant defenses of the freshwater fish Prochilodus lineatus. Ecotoxicology 20:1400–1410. doi:10.1007/s10646-011-0697-y

  57. Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191. doi:10.1016/0014-4827(88)90265-0

  58. Steinberg CEW, Paul A, Pflugmacher S, et al. (2003) Pure humic substances have the potential to act as xenobiotic chemicals—a review. Fresenius Environ Bull 12:391–401

  59. Steinberg CEW, Kamara S, Prokhotskaya VY, et al. (2006) Dissolved humic substances—ecological driving forces from the individual to the ecosystem level? Freshw Biol 51:1189–1210. doi:10.1111/j.1365-2427.2006.01571.x

  60. Tiehm A (1994) Degradation of polycyclic aromatic hydrocarbons in the presence of synthetic surfactants. Appl Environ Microbiol 60:258–263

  61. Timofeyev MA, Shatilina ZM, Kolesnichenko AV, et al. (2006) Natural organic matter (NOM) induces oxidative stress in freshwater amphipods Gammarus lacustris Sars and Gammarus tigrinus (sexton). Sci Total Environ 366:673–681. doi:10.1016/j.scitotenv.2006.02.003

  62. Val AL, Almeida-Val VMF (1999) Effects of crude oil on respiratory aspects of some fish species of the Amazon. In: Val AL, Almeida-val VMF (eds) Biology of Tropical Fishes. p 460

  63. 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

  64. Webb D, Gagnon MM (2007) Serum sorbitol dehydrogenase activity as an indicator of chemically induced liver damage in black bream (Acanthopagrus butcheri). Environ Bioindic 2:172–182. doi:10.1080/15555270701591006

  65. Webb and Gagnon (2002) Biomarkers of exposure in fish inhabiting the swan-canning estuary, Western Australia—a preliminary study. J Aquat Ecosyst Stress Recover 9:259–269

  66. Wood CM, Matsuo AYO, Wilson RW, et al. (2003) Protection by natural Blackwater against disturbances in ion fluxes caused by low pH exposure in freshwater stingrays endemic to the Rio Negro. Physiol Biochem Zool 76:12–27. doi:10.1086/367946

  67. Wood CM, Al-Reasi HA, Smith DS (2011) The two faces of DOC. Aquat Toxicol 105:3–8. doi:10.1016/j.aquatox.2011.03.007

  68. Yin Y, Jia H, Sun Y, et al. (2007) Bioaccumulation and ROS generation in liver of Carassius auratus, exposed to phenanthrene. Comp Biochem Physiol - C Toxicol Pharmacol 145:288–293. doi:10.1016/j.cbpc.2007.01.002

  69. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Englewood Cliffs, NJ, 929p

Download references

Acknowledgments

This work was funded by a joint grant, Projeto de inteligência socioambiental da indústria do petróleo na Amazônia (PIATAM), from the FINEP and INCT ADAPTA (CNPq/FAPEAM). HSH was recipient of PhD fellowship from CNPq. SBM is recipient of MSc fellowship from CNPq. VMFAV is recipient of research fellowship from CNPq. Special thanks are given to Maria de Nazaré Paula da Silva for support and to anonymous reviewers for constructive criticism.

Author information

Correspondence to Helen Sadauskas-Henrique.

Additional information

Responsible editor: Cinta Porte

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sadauskas-Henrique, H., Braz-Mota, S., Duarte, R.M. et al. Influence of the natural Rio Negro water on the toxicological effects of a crude oil and its chemical dispersion to the Amazonian fish Colossoma macropomum . Environ Sci Pollut Res 23, 19764–19775 (2016). https://doi.org/10.1007/s11356-016-7190-3

Download citation

Keywords

  • Urucu crude oil
  • Corexit 9500
  • Biomarkers
  • Hepatotoxicity
  • Genotoxicity