Life Histories, Salinity Zones, and Sublethal Contributions of Contaminants to Pelagic Fish Declines Illustrated with a Case Study of San Francisco Estuary, California, USA
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Human effects on estuaries are often associated with major decreases in abundance of aquatic species. However, remediation priorities are difficult to identify when declines result from multiple stressors with interacting sublethal effects. The San Francisco Estuary offers a useful case study of the potential role of contaminants in declines of organisms because the waters of its delta chronically violate legal water quality standards; however, direct effects of contaminants on fish species are rarely observed. Lack of direct lethality in the field has prevented consensus that contaminants may be one of the major drivers of coincident but unexplained declines of fishes with differing life histories and habitats (anadromous, brackish, and freshwater). Our review of available evidence indicates that examining the effects of contaminants and other stressors on specific life stages in different seasons and salinity zones of the estuary is critical to identifying how several interacting stressors could contribute to a general syndrome of declines. Moreover, warming water temperatures of the magnitude projected by climate models increase metabolic rates of ectotherms, and can hasten elimination of some contaminants. However, for other pollutants, concurrent increases in respiratory rate or food intake result in higher doses per unit time without changes in the contaminant concentrations in the water. Food limitation and energetic costs of osmoregulating under altered salinities further limit the amount of energy available to fish; this energy must be redirected from growth and reproduction toward pollutant avoidance, enzymatic detoxification, or elimination. Because all of these processes require energy, bioenergetics methods are promising for evaluating effects of sublethal contaminants in the presence of other stressors, and for informing remediation. Predictive models that evaluate the direct and indirect effects of contaminants will be possible when data become available on energetic costs of exposure to contaminants given simultaneous exposure to non-contaminant stressors.
KeywordsSusceptibility to toxins Bioenergetic costs Impaired waterways Multiple stressors Pelagic organism decline Climate change Review
We thank James Orlando, Kelly Smalling, and several anonymous reviewers for helpful comments. This work was supported by cooperative agreement number 113325G004 between the University of California–Santa Barbara and the US Fish and Wildlife Service, and conducted as part of a working group convened in part at the National Center for Ecological Analysis and Synthesis.
- Ankley, G.T., D.C. Bencic, M.S. Breen, T.W. Collette, R.B. Conolly, N.D. Denslow, S.W. Edwards, D.R. Ekman, N. Garcia-Reyero, K.M. Jensen, J.M. Lazorchak, D. Martinovic, D.H. Miller, E.J. Perkins, E.F. Orlando, D.L. Villeneuve, R.L. Wang, and K.H. Watanabe. 2009. Endocrine disrupting chemicals in fish: Developing exposure indicators and predictive models of effects based on mechanism of action. Aquatic Toxicology 92(3): 168–178.CrossRefGoogle Scholar
- Baker, M.E., B. Ruggeri, L.J. Sprague, C. Eckhardt-Ludka, J. Lapira, I. Wick, L. Soverchia, M. Ubaldi, A.M. Polzonetti-Magni, D. Vidal-Dorsch, S. Bay, J.R. Gully, J.A. Reyes, K.M. Kelley, D. Schlenk, E.C. Breen, R. Sasik, and G. Hardiman. 2009. Analysis of endocrine disruption in Southern California coastal fish using an aquatic multispecies microarray. Environmental Health Perspectives 117(2): 223–230.CrossRefGoogle Scholar
- Bennett, W. A. 2005. Critical assessment of the delta smelt population in the San Francisco estuary, California. Available at: http://repositories.cdlib.org/jmie/sfews/vol3/iss2/art1. San Francisco Estuary and Watershed Science 3: 1.
- Brady, J.A., W.W. Wallender, I. Werner, B.M. Fard, F.G. Zalom, M.N. Oliver, B.W. Wilson, M.M. Mata, J.D. Henderson, L.A. Deanovic, and S. Upadhaya. 2006. Pesticide runoff from orchard floors in Davis, California, USA: A comparative analysis of diazinon and esfenvalerate. Agriculture, Ecosystems & Environment 115(1–4): 56–68.CrossRefGoogle Scholar
- Cayan, D., A. L. Luers, M. Hanemann, G. Franco, and B. Croes. 2006. Scenarios of climate change in California: An overview. Sacramento: California Climate Change Center. Available at: http://www.climatechange.ca.gov/biennial_reports/2006report/index.html.
- CDPR. 2009. 1990 to 2007, California Department of Pesticide Regulation, Annual pesticide use reports by county. In http://www.cdpr.ca.gov/docs/pur/purmain.htm. Sacramento, CA Mary Votaw (ed), State of California
- Chapman, P.M., W.J. Adams, M.L. Brooks, C.G. Delos, S.N. Luoma, W.A. Maher, H.M. Ohlendorf, T.S. Presser, and D.P. Shaw (eds.). 2010. Ecological assessment of selenium in the aquatic environment. Pensacola: SETAC Press.Google Scholar
- Connon, R.E., J. Geist, J. Pfeiff, A.V. Loguinov, L.S. D’Abronzo, H. Wintz, C.D. Vulpe, and I. Werner. 2009. Linking mechanistic and behavioral responses to sublethal esfenvalerate exposure in the endangered delta smelt; Hypomesus transpacificus (Fam. Osmeridae). BMC Genomics 10: 18.CrossRefGoogle Scholar
- Connon, R.E., S. Beggel, L.S. D’Abronzo, J.P. Geist, J. Pfeiff, A.V. Loguinov, C.D. Vulpe, and I. Werner. 2011. Linking molecular biomarkers with higher level condition indicators to identify effects of copper exposures on the endangered delta smelt (Hypomesus transpacificus). Environmental Toxicology and Chemistry 30(2): 290–300.CrossRefGoogle Scholar
- Dege, M., and L.R. Brown. 2004. Effect of outflow on spring and summertime distribution and abundance of larval and juvenile fishes in the upper San Francisco Estuary. In Early life history of fishes in the San Francisco Estuary and watershed, ed. L.R.B.F. Feyrer, R.L. Brown, and J.J. Orsi. Bethesda: American Fisheries Society.Google Scholar
- Dileanis, B. P., K. B. Bennett, and J. L. Domagalski. 2002. Occurrence and transport of diazinon in the Sacramento River, California and selected tributaries during three winter storms, January-February 2000. Available at: http://water.usgs.gov/pubs/wri/wri02-4101. U.S. Geological Survey Water Resources Investigations Report 02–4101.
- Dill, W.A., and A.J. Cordone. 1997. History and status of introduced fishes in California, 1871–1996: Conclusions. Fisheries 22(10): 15–18.Google Scholar
- Ducrot, V., A.R.R. Pery, and L. Lagadic. 2010. Modelling effects of diquat under realistic exposure patterns in genetically differentiated populations of the gastropod Lymnaea stagnalis. Philosophical Transactions of the Royal Society B-Biological Sciences 365(1557): 3485–3494.CrossRefGoogle Scholar
- Dupont-Prinet, A., G. Claireaux, and D.J. McKenzie. 2009. Effects of feeding and hypoxia on cardiac performance and gastrointestinal blood flow during critical speed swimming in the sea bass Dicentrarchus labrax. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology 154(2): 233–240.CrossRefGoogle Scholar
- Feyrer, F., K. Newman, M. Nobriga, and T. Sommer. 2010. Modeling the effects of future outflow on the abiotic habitat of an imperiled estuarine fish. Estuaries and Coasts published online, SeptGoogle Scholar
- Geist, J., I. Werner, K.J. Eder, and C.M. Leutenegger. 2007. Comparisons of tissue-specific transcription of stress response genes with whole animal endpoints of adverse effect in striped bass (Morone saxatilis) following treatment with copper and esfenvalerate. Aquatic Toxicology 85(1): 28–39.CrossRefGoogle Scholar
- Gowdy, M. J. and L. F. Grober. 2003. Total Maximum Daily Load for Low Dissolved Oxygen in the San Joaquin River. Sacramento, CA.: Regional Water Quality Control Board Central Valley Region. Available at: http://www.waterboards.ca.gov/centralvalley/water_issues/tmdl/central_valley_projects/san_joaquin_oxygen/low_do_report_6-2003/do_tmdl_rpt.pdf.
- Greenfield, B.K., S.J. Teh, J.R.M. Ross, J. Hunt, G.H. Zhang, J.A. Davis, G. Ichikawa, D. Crane, S.S.O. Hung, D.F. Deng, F.C. Teh, and P.G. Green. 2008. Contaminant concentrations and histopathological effects in Sacramento splittail (Pogonichthys macrolepidotus). Archives of Environmental Contamination and Toxicology 55(2): 270–281.CrossRefGoogle Scholar
- Hall, L.W., M.C. Ziegenfuss, S.A. Fischer, J.A. Sullivan, and D.M. Palmer. 1993. The influence of contaminant and water-quality conditions on larval striped bass in the Potomac River and Upper Chesapeake Bay in 1990—An in situ study. Archives of Environmental Contamination and Toxicology 24(1): 1–10.CrossRefGoogle Scholar
- Ibelings, B. W. and K. E. Havens. 2008. Cyanobacterial toxins: a qualitative meta-analysis of concentrations, dosage and effects in freshwater, estuarine and marine biota. In Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs, edited by H. K. HudnellGoogle Scholar
- Jassby, A. 2008. Phytoplankton in the Upper San Francisco Estuary: Recent biomass trends, their causes and their trophic significance. San Francisco Estuary and Watershed Science 6(1): 1–24.Google Scholar
- Johnson, M. L., I. Werner, S. Teh, and F. Loge. 2010. Evaluation of chemical, toxicological, and histopathologic data to determine their role in the Pelagic Organism Decline Rancho Cordova, CA: Report to the Central Valley Regional Water Quality Control Board. Available at: http://www.waterboards.ca.gov/centralvalley/water_issues/delta_water_quality/comprehensive_monitoring_program/contaminant_synthesis_report.pdf.
- Kratzer, C. R., C. Zamora, and D. L. Knifong. 2002. Diazinon and chlorpyrifos loads in the San Joaquin River Basin, California, January and February 2000. U.S. Geological Survey Water Resources Investigations Report 02–4103. Available at: http://pubs.usgs.gov/wri/wri034091/wrir034091.pdf.
- Kuivila, K.M., and M. Hladik. 2008. Understanding the occurrence and transport of current-use pesticide in the San Francisco Estuary Watershed. San Francisco Estuary and Watershed Science 6(Article 2): 1–19.Google Scholar
- Linton, T.K., I.J. Morgan, P.J. Walsh, and C.M. Wood. 1998a. Chronic exposure of rainbow trout (Oncorhynchus mykiss) to simulated climate warming and sublethal ammonia: A year-long study of their appetite, growth, and metabolism. Canadian Journal of Fisheries and Aquatic Sciences 55(3): 576–586.CrossRefGoogle Scholar
- Linton, T.K., I.J. Morgan, P.J. Walsh, and C.M. Wood. 1998b. Chronic exposure of rainbow trout (Oncorhynchus mykiss) to simulated climate warming and sublethal ammonia: a year-long study of their appetite, growth, and metabolism. Canadian Journal of Fisheries and Aquatic Sciences 55: 576–586.CrossRefGoogle Scholar
- Luo, X.J., B.X. Mai, Q.S. Yang, J.M. Fu, G.Y. Sheng, and Z.S. Wang. 2004. Polycyclic aromatic hydrocarbons (PAHs) and organochlorine pesticides in water columns from the Pearl River and the Macao harbor in the Pearl River Delta in South China. Marine Pollution Bulletin 48(11–12): 1102–1115.CrossRefGoogle Scholar
- Matthiessen, P., and R.J. Law. 2002. Contaminants and their effects on estuarine and coastal organisms in the United Kingdom in the late twentieth century. Environmental Pollution 120(3): 739–757.Google Scholar
- Moyle, P.B. 2002. Inland fishes of California. Revised and expanded. Berkeley: University of California.Google Scholar
- Munkes, B. 2005. Eutrophication, phase shift, the delay and the potential return in the Greifswalder Bodden, Baltic Sea. Aquatic Sciences 67(3): 372–381.Google Scholar
- Nilsen, T.O., L.O.E. Ebbesson, O.G. Kverneland, F. Kroglund, B. Finstad, and S.O. Stefansson. 2010. Effects of acidic water and aluminum exposure on gill Na+, K + −ATPase alpha-subunit isoforms, enzyme activity, physiology and return rates in Atlantic salmon (Salmo salar L.). Aquatic Toxicology 97(3): 250–259.CrossRefGoogle Scholar
- Ostrach, D.J., J.M. Low-Marchelli, K.J. Eder, S.J. Whiteman, and J.G. Zinkl. 2008. Maternal transfer of xenobiotics and effects on larval striped bass in the San Francisco Estuary. Proceedings of the National Academy of Sciences of the United States of America 105(49): 19354–19359.CrossRefGoogle Scholar
- Roy, R.L., and P.G.C. Campbell. 1997. Decreased toxicity of Al to juvenile Atlantic salmon (Salmo salar) in acidic soft water containing natural organic matter: A test of the free-ion model. Environmental Toxicology and Chemistry 16(9): 1962–1969.Google Scholar
- SFEI. 2007. The pulse of the estuary: Monitoring and managing water quality in the San Francisco Estuary. Oakland: San Francisco Estuary Institute.Google Scholar
- Spurlock, F., and M. Lee. 2008. Synthetic pyrethroid use patterns, properties, and environmental effects. In Synthetic pyrethroids: Occurrence and behavior in aquatic environments, ed. J. Gan et al. Washington: American Chemical Society.Google Scholar
- USEPA. 2008. Fourth five-year review report for Iron Mountain Mine superfund site, Redding, California. Available from: http://yosemite.epa.gov/r9/sfund/r9sfdocw.nsf/3dc283e6c5d6056f88257426007417a2/0debbf5424a57c908825774900824131!OpenDocument, edited by K. Salyer. San Francisco, California 94105: U.S. Environmental Protection Agency.
- USGS, C. W. S. C. 2011. Hydrologic data: California Water Science Center http://ca.water.usgs.gov/.
- Werner, I., and K. Moran. 2008. Effects of pyrethroid insecticides on aquatic organisms. In Synthetic pyrethroids: Occurrence and behavior in aquatic environments, ed. J. Gan et al. Washington: American Chemical Society.Google Scholar
- Werner, I., L.A. Deanovic, V. Connor, V. de Vlaming, H.C. Bailey, and D.E. Hinton. 2000. Insecticide-caused toxicity to Ceriodaphnia dubia (Cladocera) in the Sacramento-San Joaquin River Delta, California, USA. Environmental Toxicology and Chemistry 19(1): 215–227.Google Scholar
- Werner, I., L. Deanovic, C. Reece, D. Markiewicz, M. Stillway, J. Khamphanh, R. E. Connon, and S. Beggel. 2009. Pelagic organism decline (POD): Acute and chronic invertebrate and fish toxicity testing in the Sacramento-San Joaquin Delta 2008–2010, progress report, February 27, 2009. Sacramento, CA: Interagency Ecological Program Available at: http://www.waterboards.ca.gov/waterrights/water_issues/programs/bay_delta/deltaflow/docs/exhibits/sac_rcsd/srcsd_exh2b.pdf.
- Werner, I., L.A. Deanovic, D. Markiewicz, M. Khamphanh, C.K. Reece, M. Stillway, and C. Reece. 2010. Monitoring acute and chronic water column toxicity in the Northern Sacramento–San Joaquin Estuary, California, USA, using the euryhaline amphipod, Hyalella azteca: 2006–2007. Environmental Toxicology and Chemistry 29(10): 2190–2199.CrossRefGoogle Scholar