Abstract
The health status of Sciaenops ocellatus was studied by qualitative and quantitative histopathological analysis through histological damage prevalence and degree of tissue change (DTC) in response to 96 h and 9 days of exposure to 0.1, 0.8, and 8 g/L of light crude oil in seawater. The histology of the liver, spleen, kidney, and gills of the fish were analyzed and compared between treatments. Our results showed that the exposed fish developed lesions associated with degenerative and necrotic changes. The highest frequency of damage and DTC scores were observed in the liver and kidney from 96 h to 9-days post-exposure. Generalized additive models of location, scale, and shape, showed that the DTC was strongly associated with crude oil compounds such as napthalene, Cd, Ni, Pb, and bile polycyclic aromatic hydrocarbon metabolites. Our findings suggest that exposure to crude oil affects fish health, producing irreversible histological damage.
Similar content being viewed by others
References
Améndola-Pimenta M, Cerqueda-García D, Zamora- Briseño J, Couoh-Puga D, Montero-Muñoz J et al (2020) Toxicity evaluation and microbiota response of the lined sole Achirus lineatus (Chordata: Achiridae) exposed to the light petroleum water accommodated fraction (WAF). J Toxicol Environ Health A. https://doi.org/10.1080/15287394.2020.1758861
Baali A, Yahyaoui A (2020) Polycyclic aromatic hydrocarbons (PAHs) and their influence to some aquatic species. Biochem Toxicol Heavy Method Nanomater. https://doi.org/10.5772/intechopen.86213
Bagenal T, Tesch F (1978) Age and growth. In: Bagenal T (ed) Methods for assessment of fish production in freshwater waters. Blackwell, Oxford, pp 101–136
Boijink CL, Maciel PO, Tavares-Dias M, Iwashita MKP, Morais MS et al (2017) Anesthesia by sprinkling method in the gills of tambaqui Colossoma macropomum does not influence intensity and morphology of monogeneans. Braz J Biol 77(2):367–371. https://doi.org/10.1590/1519-6984.15915
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information—theoretic approach, 2nd edn. Springer, New York
Chen Y (2017) Fish resources of the Gulf of Mexico. In: Ward C (ed) Habitats and biota of the Gulf of Mexico: before the Deepwater Horizon oil spill. Springer, New York. https://doi.org/10.1007/978-1-4939-3456-0_1
Chupani L, Savari A, Zolgharnein H, Rezaie A, Zeinali M (2013) Enzymatic and histopathologic biomarkers in the flatfish Euryglossa orientalis from the northwestern Persian Gulf. Toxicol Ind Health 32(5):866–876. https://doi.org/10.1177/0748233713513490
Costa PM (2018) The handbook of histopathological practices in aquatic environments: guide to histology for environmental toxicology. Academic Press, Cambridge
Harper C, Wolf JC (2009) Morphologic effects of the stress response in fish. ILAR J 50(4):387–396. https://doi.org/10.1093/ilar.50.4.387
Harr KE, Deak K, Murawski SA, Reavill DR, Takeshita RA (2018) Generation of red drum (Sciaenops ocellatus) hematology reference intervals with a focus on identified outliers. Vet Clin Pathol 47:22–28. https://doi.org/10.1111/vcp.12569
Humason GL (1962) Animal tissue techniques. Freeman, San Francisco, p 468
Incardona JP, Collier TK, Scholz NL (2010) Oil spills and fish health: exposing the heart of the matter. J Expo Sci Environ Epidemiol 21(1):3–4. https://doi.org/10.1038/jes.2010.51
Jabeen G, Manzoor F, Javid A, Azmat H, Arshad M, Fatima S (2018) Evaluation of fish health status and histopathology in gills and liver due to metal contaminated sediments exposure. Bull Environ Contam Toxicol 100(4):492–501. https://doi.org/10.1007/s00128-018-2295-7
Javed M, Usmani N (2019) An overview of the adverse effects of heavy metal contamination on fish health. Proc Natl Acad Sci India Sect B 89:389–403. https://doi.org/10.1007/s40011-017-0875-7
Kammann U, Akcha F, Budzinski H, Burgeot T, Gubbins MJ et al (2017) PAH metabolites in fish bile: from the Seine estuary to Iceland. Mar Environ Res 124:41–45. https://doi.org/10.1016/j.marenvres.2016.02.014
Kvenvolden KA, Cooper CK (2003) Natural seepage of crude oil into the marine environment. Geo-Mar Lett 23:140–146
Luna LG (1968) Manual of histologic staining methods of the Armed Forces Institute of Pathology, 3rd edn. McGraw-Hill, New York, p 258
Mager EM, Esbaugh AJ, Stieglitz JD, Hoenig R, Bodinier C, Incardona JP et al (2014) Acute embryonic or juvenile exposure to Deepwater Horizon Crude Oil impairs the swimming performance of mahi-mahi (Coryphaena hippurus). Environ Sci Technol 48:7053–7061
Malarkey DE, Hoenerhoff M, Maronpot RR (2013) Carcinogenesis: mechanisms and manifestations. In: Haschek WM, Rousseaux CG, Wallig MA (eds) Haschek and Rousseaux’s handbook of toxicologic pathology. Academic Press, Waltham, p 107
Murawski SA, Hogarth WT, Peebles EB, Barbeiri L (2014) Prevalence of external skin lesions and polycyclic aromatic hydrocarbon concentrations in Gulf of Mexico fishes, post-Deepwater Horizon. Trans Am Fish Soc 143(4):1084–1097. https://doi.org/10.1080/00028487.2014.911205
Myers MS, Johnson LL, Collier TK (2003) Establishing the causal relationship between polycyclic aromatic hydrocarbon (PAH) exposure and hepatic neoplasms and neoplasia related liver lesions in english sole (Pleuronectes vetulus). Hum Ecol Risk Assess 9:67–94
Paulo D, Fontes F, Flores-Lopes F (2012) Histopathological alterations observed in the liver of Poecilia vivipara (Cyprinodontiformes: Poeciliidae) as a tool for the environmental quality assessment of the Cachoeira River, BA. Braz J Biol 72(1):131–140. https://doi.org/10.1590/s1519-69842012000100015
Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Müller R, Lloyd R (eds) Sublethal and chronic effects of pollutants on freshwater fish. Cambridge University Press, Cambridge, pp 339–352
Prince RC, Nash GW, Hill SJ (2016) The biodegradation of crude oil in the deep ocean. Mar Pollut Bull 111:354–357. https://doi.org/10.1016/j.marpolbul.2016.06.087
Pulster EL, Fogelson SB, Carr B, Murawski SA (2018) A spatiotemporal analysis of hepatic polycyclic aromatic hydrocarbon levels and pathological findings in red snapper (Lutjanus campechanus), post-Deepwater Horizon. In: Gulf of Mexico oil spill & ecosystem science conference, LA, New Orleans, 2018
Pulster EL, Gracia A, Snyder SM, Deak K, Fogleson S, Murawski SA (2020) Chronic sublethal effects observed in wild caught fish following two major oil spills in the Gulf of Mexico: Deepwater Horizon and Ixtoc 1(Chap 24). In: Murawski SA, Ainsworth C, Gilbert S, Hollander D, Paris CB, Schlüter M, Wetzel D (eds) Deep oil spills: facts, fate and effects. Springer International, Cham
Quintanilla-Mena M, Gold-Bouchot G, Zapata-Pérez O, Rubio-Piña J, Quiroz-Moreno A et al (2019) Biological responses of shoal flounder (Syacium gunteri) to toxic environmental pollutants from the southern Gulf of Mexico. Environ Pollut. https://doi.org/10.1016/j.envpol.2019.113669
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rigby RA, Stasinopoulos DM (2005) Generalized additive models for location, scale and shape. J R Stat Soc Ser C 54(3):507–554. https://doi.org/10.1111/j.1467-9876.2005.00510.x
Safahieh A, Monikh A, Savari A, Doraghi A (2011) Heavy metals concentration in mullet fish, Liza abu from petrochemical waste receiving creeks, Musa Estuary (Persian Gulf). J Environ Prot 2(1218):1226
Schmitt CJ, Dethloff GM (2000) Biomonitoring of environmental status and trends (BEST) program: selected methods for monitoring chemical contaminants and their effects in aquatic ecosystems. U.S. Geological survey, Biological resources division, Columbia, (MO): information and technology report USGS/BRD-2000-0005, pp 81
Schwaiger J, Wanke R, Adam S, Pawert M, Hönnen W, Triebskorn R (1997) The use of histopathological indicators to evaluate contaminant-related stress in fish. J Aquat Ecosyst Stress Recovery 6:75–86. https://doi.org/10.1023/A:1008212000208
Simonato JD, Guedes CLB, Martinez CBR (2008) Biochemical, physiological, and histological changes in the neotropical fish Prochilodus lineatus exposed to diesel oil. Ecotoxicol Environ Saf 69(1):112–120. https://doi.org/10.1016/j.ecoenv.2007.01.012
Tjahjaningsih W, Pursetyo KT, Sulmartiwi L (2017) Melanomacrophage centers in kidney, spleen and liver: a toxic response in carp fish (Cyprinus carpio) exposed to mercury chloride. AIP Conf Proc. https://doi.org/10.1063/1.4975950
Vethaak AD, Jol JG, Pieters JP (2009) Long-term trends in the prevalence of cancer and other major diseases among flatfish in the southeastern North Sea as indicators of changing ecosystem health. Environ Sci Technol 43:2151e2158
Wade TL, Sericano JL, Sweet ST, Knap AH, Guinasso NL (2016) Spatial and temporal distribution of water column total polycyclic aromatic hydrocarbons (PAH) and total petroleum hydrocarbons (TPH) from the Deepwater Horizon (Macondo) incident. Mar Pollut Bull 103:286–293. https://doi.org/10.1016/j.marpolbul.2015.12.002
Zar JH (1999) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, p 663
Acknowledgement
The authors thank staff from the aquatic pathology lab at CINVESTAV-Mérida for field and lab help, and from the ecotoxicology, geochemistry and immunology labs for help with the maintenance of fish and contaminant databases. Dr. Ulises N. García Cruz helped in the calculation of crude oil concentrations, logistics, and experimental design. The Mexican government and Yucatan State, Mexico and the Consejo Nacional de Ciencia y Tecnología (CONACyT) provided a PhD student Grant (No. 250380) to D.C. This research was financially supported by the Mexican Ministry of Energy through the Hydrocarbon Foundation and CONACyT (Project 201441). This is a contribution from the Gulf of Mexico Research Consortium (CIGoM). We acknowledge PEMEX for providing the light-crude oil, and the specific request to the Hydrocarbon Foundation to address the environmental effects of oil spills in the Gulf of Mexico.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors report no potential conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Couoh-Puga, E.D., Vidal-Martínez, V.M., Ceja-Moreno, V. et al. Histological Effects of Light Crude Oil on Sciaenops ocellatus Under Experimental Conditions. Bull Environ Contam Toxicol 108, 71–77 (2022). https://doi.org/10.1007/s00128-021-03172-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-021-03172-0