Skip to main content
Log in

Liver lesions in demersal fishes near a large ocean outfall on the San Pedro Shelf, California

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

The prevalence of toxicopathic liver lesions in demersal fish on the San Pedro Shelf, California was determined for a 15-year period (1988–2003). Fish livers were sampled at fixed locations as part of the Orange County Sanitation Districts (OCSD) ocean monitoring program. Histopathological examination of selected fish liver tissues was studied to determine whether the wastewater discharge had affected fish health. The prevalence of toxicopathic lesion classes neoplasms (NEO), preneoplastic foci of cellular alteration (FCA), and hydropic vacuolation (HYDVAC) varied among species and locations. For all species sampled, severe lesions occurred in 6.2% of the fish examined (n = 7,694). HYDVAC (4.1%) was the most common toxicopathic lesion type followed by FCA (1.4%) and NEO (0.7%). HYDVAC occurred only in white croaker (Genyonemus lineatus), accounting for 84.8% of the toxicopathic lesions for this species. Prevalence of HYDVAC, NEO, and FCA in white croaker was 15.2, 2.0, and 0.7%, respectively. The prevalence of HYDVAC and NEO in white croaker increased with age and size but there was no sexual difference. A linear regression model was used for hypothesis testing to account for significant differences in fish size (and age for croakers) at the different sampling locations. This analysis showed that for HYDVAC there was no spatial or location effect for lesion rate or size/age of onset. For NEO, the model predicted that white croaker near the wastewater outfall may acquire these lesions at a smaller size/younger age, and at a higher rate, than at other sites. However, this result may be biased due to the unequal size frequency distributions and the low prevalence of NEO in white croaker at the different sampling sites. Bigmouth sole (Hippoglossina stomata) had a prevalence of FCA and NEO of 1.3 and 0.35%, respectively, but the prevalence and distribution of lesions was too few for statistical testing. There was no sexual difference for lesion prevalence in hornyhead turbot (Pleuronichthys verticalis) and the prevalence of FCA and NEO was 3.4 and 0.37%, respectively. FCA prevalence increased with size in hornyhead turbot and there were no significant spatial differences for lesion rates and fish size at lesion onset. Overall, consistent spatial differences for lesion prevalence were not demonstrated and highlight the analytical difficulties of detecting a possible point source impact when the effect is rare, correlated with the size/age structure of the population, and may be caused by exposure to unknown multiple sources. Thus, the usefulness of liver histopathology as a point-source monitoring tool is best applied to where the spatial scale of impact generally exceeds the home range of the target species.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allen, M. J. (1982). Functional structure of soft-bottom fish communities of the southern California shelf (pp. 577). University of California, San Diego, PhD dissertation.

  • Au, D. W. T. (2004). The application of histo-cytopathological biomarkers in marine pollution monitoring: A review. Marine Pollution Bulletin, 48, 817–834.

    Article  CAS  Google Scholar 

  • Collier, T. K., Singh, S. V., Awasthi, Y. C., & Varanasi, U. (1992). Hepatic xenobiotic metabolizing enzymes in two species of benthic fish showing different prevalences of contaminant-associated liver lesions. Toxicology and Applied Pharmacology, 113, 319–324.

    Article  CAS  Google Scholar 

  • Eganhouse, R. P., & Venkatesan, M. I. (1993). Chemical oceanography and geochemistry. In M. D. Daily, D. J. Reish, & J. W. Anderson (Eds.), Ecology of the Southern California Bight (pp. 71–189). Berkeley: University of California.

    Google Scholar 

  • EPA (U.S. Environmental Protection Agency) (1987). Guidance for conducting fish liver histopathology studies during 301(h) monitoring. Final report TC-3953-03. Washington, D.C.: EPA Office of Marine and Estuarine Protection.

    Google Scholar 

  • Gossett, R. W., Puffer, H. W., Arthur, R. H., Jr., & Young, D. R. (1983). DDT, PCB and benzo(a)pyrene levels in white croaker (Genyonemus lineatus) from southern California. Marine Pollution Bulletin, 14, 60–65.

    Article  CAS  Google Scholar 

  • Harshbarger, J. C., & Clark, J. B. (1990). Epizootiology of neoplasms in bony fish from North America. Science of the Total Environment, 94, 1–32.

    Article  CAS  Google Scholar 

  • Heilprin, D. J., Phillips, C. R., & Basmadjian, E. (2002). Fly larvae in wastewater discharges: A potential source of food and organochlorine contaminants for some southern California fishes. Environmental Biology of Fishes, 65(3), 349–357.

    Article  Google Scholar 

  • Hinton, D. E., & Lauren, D. J. (1990). Liver structural alterations accompanying chronic toxicity in fishes: Potential biomarkers of exposure. In J. F. McCarthy, & L. R. Shagart (Eds.), Biomarkers of environmental contamination, (Chapter 2). Boca Raton: Lewis.

    Google Scholar 

  • Hose, J. E., Cross, J. N., Smith, S. G., & Diehl, D. (1989). Reproductive impairment in a fish inhabiting a contaminated coastal environment off southern California. Environmental Pollution, 57, 139–148.

    Article  CAS  Google Scholar 

  • Inman, D. L., Jenkins, S. A., & Wasyl, J. (1998). Database for streamflow and sediment flux of California rivers. Scripps Institution of Oceanography Reference Series No. 98–9. Scripps Institution of Oceanography, La Jolla, California.

  • Johnson, L. L., Stehr, C. M., Olson, O. P., Myers, M. S., Pierce, S. M., McCain, B. B., et al. (1992). National Status and Trends Program, National Benthic Surveillance Project: Northeast coast, fish histopathology and relationships between lesions and chemical contaminants (1987–89) (pp. 96). US Dept. Comm., NOAA Tech. Memo. NMFS-NWFSC-4.

  • Love, M. S. (1996). Probably more than you want to know about the fishes of the Pacific Coast, 2nd ed (pp. 381). Santa Barbara: Really Big.

    Google Scholar 

  • Love, M. S., McGowen, G. E., Westphal, W., Lavenberg, R. J., & Martin, L. (1984). Aspects of the life history and fishery of the white croaker, Genyonemus lineatus (Sciaenidae) off California. Fishery Bulletin, 82(1), 179–198.

    Google Scholar 

  • Malins, D. C., McCain, B. B., Brown, D. W., Myers, M. S., Krahn, M. M., & Chan, S.-L. (1987). Toxic chemicals, including aromatic and chlorinated hydrocarbons and their derivatives, and liver lesions in white croaker (Genyonemus lineatus) from the vicinity of Los Angeles. Environmental Science and Technology, 21, 765–770.

    Article  CAS  Google Scholar 

  • Martinez-Munoz, M. A., & Ortega-Salas, A. A. (1999). Growth and mortality of the fantail sole, Xystreurys liolepis (Jordan and Gilbert 1881) off the Western Coast of Baja California, Mexico. Bulletin of the Southern California Academy of Sciences, 98, 66–74.

    Google Scholar 

  • McCain, B. B., Chan, S.-L., Krahn, M. M., Brown, D. W., Myers, M. S., Landahl, J. T., et al. (1992). Chemical contamination and associated fish diseases in San Diego Bay. Environmental Science and Technology, 26, 725–733.

    Article  CAS  Google Scholar 

  • McDermott-Ehrlich, D., Sherwood, M. J., Heesen, T. C., Young, D. R., & Mearns, A. J. (1977). Chlorinated hydrocarbons in Dover sole, Microstomus pacificus: Local migrations and fin lesions. Fishery Bulletin, 75, 513–517.

    CAS  Google Scholar 

  • Mearns, A. J., Matta, M., Shigenaka, G., MacDonald, D., Buchman, M., Harris, H., et al. (1991). Contaminant trends in the Southern California Bight: inventory and assessment. Seattle, Washington: NOAA Tech. Memo. NOS ORCA 62. NOAA.

  • Moore, M., Lefkovitz, L., Hall, M., Hillman, R., & Burnett, J. (2005). Reduction in organic contaminant exposure and resultant hepatic hydropic vacuolation in winter flounder (Pseudopleurnectes americanus) following improved effluent quality and relocation of the Boston sewage outfall into Massachusetts Bay, USA: 1987–2003. Marine Pollution Bulletin, 50, 156–166.

    Article  CAS  Google Scholar 

  • Moore, M. J., Shea, D., Hillman, R. E., & Stegeman, J. J. (1996). Trends in hepatic tumours and hydropic vacuolation, fin erosion, organic chemical and stable isotope ratios in winter flounder from Massachusetts, USA. Marine Pollution Bulletin, 32, 458–470.

    Article  CAS  Google Scholar 

  • Moore, M. J., Shea, D., Smolowitz, R. M., & Stegeman, J. J. (1997). Stages of hydropic vacuolation in the liver of winter flounder Pleuronectes americanus from a chemically contaminated site. Diseases of Aquatic Organisms, 31, 19–28.

    Article  Google Scholar 

  • Myers, M. S., & Fournie, J. W. (2002). Histopathological biomarkers as integrators of anthropogenic and environmental stressors. In S. M. Adams (Ed.), Biological indicators of aquatic ecosystem stress (pp. 221–287). Bethesda, MD: American Fisheries Society.

    Google Scholar 

  • Myers, M. S., Johnson, L. L., & Collier, T. K. (2003). Establishing the causal relationship between polycyclic aromatic hydrocarbon (PAH) exposure and hepatic neoplasms and neoplasia-related liver lesions in English sole (Pleuronectes vetulus). Human and Ecological Risk Assessment, 9(1), 67–94.

    Article  CAS  Google Scholar 

  • Myers, M. S., Johnson, L. L., Olson, O. P., Stehr, C. M., Horness, B. H., Collier, T. K., et al. (1999). Toxicopathic hepatic lesions as biomarkers of chemical contaminant exposure and effects in marine bottom fish species from the Northeast and Pacific Coasts, USA. Marine Pollution Bulletin, 37(1–2), 92–113.

    Google Scholar 

  • Myers, M. S., Rhodes, L. S., & McCain, B. B. (1987). Pathologic anatomy and patterns of occurrence of hepatic neoplasms, putative preneoplastic lesions and other idiopathic hepatic conditions in English sole (Parophrys vetulus) from Puget Sound, Washington, USA. Journal of the National Cancer Institute, 78, 333–363.

    CAS  Google Scholar 

  • Myers, M. S., Stehr, C. M., Olson, O. P., Johnson, L. L., McCain, B. B., Chan, S. L., et al. (1993). National status and trends program, national benthic surveillance project: Pacific coast, fish histopathology and relationships between toxicopathic lesions and exposure to chemical contaminants for cycles I to V (1984–1988) (pp. 160). NOAA Tech. Memo. NMFS-NWFSC-6.

  • Myers, M. S., Stehr, C. M., Olson, O. P., Johnson, L. L., McCain, B. B., Chan, S.-L., & Varanasi, U. (1994). Relationships between toxicopathic lesions and exposure to chemical contaminants in English sole (Pleuronectes vetulus), starry flounder (Platichthys stellatus), and white croaker (Genyonemus lineatus) from selected marine sites on the Pacific Coast, USA. Environmental Health Perspectives, 102, 200–215.

    Article  CAS  Google Scholar 

  • NOAA (National Oceanic and Atmospheric Administration) (1998). NOAA’s National Status and Trends Program, Frequency of Tumors in Fish Livers (1984, ’85, ’86, and ’88). http://www-orca.noc.noaa.gov/projects/nsandt/ tumorsinfish.html.

  • OCSD (Orange County Sanitation District) (1999). Annual report, July 1997–June 1998. Fountain Valley, California: Marine Monitoring.

    Google Scholar 

  • OCSD (2001). Annual report, July 1999–June 2000. Fountain Valley, California: Marine Monitoring.

    Google Scholar 

  • Perkins, E. M. (1995). An overview of hepatic neoplasms, putatively preneoplastic lesions, and associated conditions in fish sampled during the County Sanitation Districts of Orange County’s 1986–1992 Ocean Monitoring Program. Bulletin of the Southern California Academy of Sciences, 94, 75–91.

    Google Scholar 

  • Phillips, C. R., Venkatesan, M. I., & Bowen, R. (1997). Interpretations of contaminant sources to San Pedro Shelf sediments using molecular markers and principal components analysis. In R. P. Eganhouse (Ed.), Molecular markers in environmental geochemistry (Chapter 16). Washington, D.C.: American Chemical Society.

    Google Scholar 

  • Phillips, C. R., Venkatesan, M. I., & Lin, T. (2001). The presence and composition of linear alkyl benzenes in muscle tissues of white croaker near a large ocean outfall in southern California. Environmental Toxicology and Chemistry, 20(2), 231–238.

    Article  CAS  Google Scholar 

  • Roy, L. A., Armstrong, J. L., Sakamoto, K., Steinert, S., Perkins, E., Lomax, D. P., et al. (2003). The relationships of biochemical endpoints to histopathology and population metrics in feral flatfish collected near the municipal wastewater outfall of Orange County, California, USA. Environmental Toxicology and Chemistry, 22(6), 1309–1317.

    Article  CAS  Google Scholar 

  • SCCWRP (Southern California Coastal Water Research Project) (1996). Age and growth in the hornyhead turbot (Pleuronichthys verticalis) off Orange County, California. In M. J. Allen, C. Francisco, & D. Hallock (Ed.), Southern California coastal water research project annual report 1994–1995 (pp. 91–96). Westminster, California.

  • Schiff, K. C., Allen, M. J., Zeng, E. Y., & Bay, S. M. (2000). Southern California. Marine Pollution Bulletin, 41, 76–93.

    Article  CAS  Google Scholar 

  • Stehr, C. M., Myers, M. S., Burrows, D. G., Krahn, M. M., Meador, J. P., McCain, B. B. et al. (1997). Chemical contamination and associated liver disease in two species of fish from San Francisco Bay and Bodega Bay. Ecotoxicolgy, 6, 35–65.

    Article  CAS  Google Scholar 

  • Stehr, C. M., Johnson, L. L., & Myers, M. S. (1998). Hydropic vacuolation in the liver of three species of fish from the U.S. west coast: lesion description and risk assessment associated with contaminant exposure. Diseases of Aquatic Organisms, 32, 119–135.

    Article  CAS  Google Scholar 

  • Susani, L. (1986). Liver lesions in feral fish: A discussion of their relationship to environmental pollutants (pp. 20). Rockville, MD: NOAA Tech. Memo. NOS OMA 27, National Oceanic and Atmospheric Administration.

  • Susani, L., Mearns, A., & Long, E. (1986). NOAA quality assurance program workshop on marine fish histopathology (pp. 32). Summary report. Ocean Assessments Division, National Oceanic and Atmospheric Administration, Seattle, Washington.

  • Ware, R. R. (1979). The food habits of the white croaker Genyonemus lineatus and an infaunal analyses near areas of waste discharge in outer Los Angeles harbor (pp. 164) Master’s Thesis. California State University, Long Beach.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edward Basmadjian.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Basmadjian, E., Perkins, E.M., Phillips, C.R. et al. Liver lesions in demersal fishes near a large ocean outfall on the San Pedro Shelf, California. Environ Monit Assess 138, 239–253 (2008). https://doi.org/10.1007/s10661-007-9794-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-007-9794-z

Keywords

Navigation