Life Histories, Salinity Zones, and Sublethal Contributions Of
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Estuaries and Coasts (2012) 35:603–621 DOI 10.1007/s12237-011-9459-6 Life Histories, Salinity Zones, and Sublethal Contributions of Contaminants to Pelagic Fish Declines Illustrated with a Case Study of San Francisco Estuary, California, USA Marjorie L. Brooks & Erica Fleishman & Larry R. Brown & Peggy W. Lehman & Inge Werner & Nathaniel Scholz & Carys Mitchelmore & James R. Lovvorn & Michael L. Johnson & Daniel Schlenk & Suzanne van Drunick & James I. Drever & David M. Stoms & Alex E. Parker & Richard Dugdale Received: 13 January 2011 /Revised: 15 June 2011 /Accepted: 25 October 2011 /Published online: 23 November 2011 # Coastal and Estuarine Research Federation 2011 Abstract Human effects on estuaries are often associated chronically violate legal water quality standards; however, with major decreases in abundance of aquatic species. direct effects of contaminants on fish species are rarely However, remediation priorities are difficult to identify observed. Lack of direct lethality in the field has prevented when declines result from multiple stressors with interact- consensus that contaminants may be one of the major ing sublethal effects. The San Francisco Estuary offers a drivers of coincident but unexplained declines of fishes useful case study of the potential role of contaminants in with differing life histories and habitats (anadromous, declines of organisms because the waters of its delta brackish, and freshwater). Our review of available evidence M. L. Brooks (*) : J. R. Lovvorn N. Scholz Department of Zoology, Southern Illinois University, NOAA Fisheries, Northwest Fisheries Science Center, 1125 E. Lincoln Dr., MC 6501, Environmental Conservation Division, Carbondale, IL 62901, USA 2725 Montlake Blvd. E., e-mail: [email protected] Seattle, WA 98112, USA : C. Mitchelmore E. Fleishman D. M. Stoms Chesapeake Biological Laboratory, University of Maryland Center Bren School of Environmental Science and Management, for Environmental Science, University of California, P.O. Box 38, Solomons, MD 20688, USA 3011 Bren Hall, Santa Barbara, CA 93106, USA M. L. Johnson Center for Watershed Sciences, University of California, L. R. Brown One Shields Avenue, U.S. Geological Survey, California Water Science Center, Davis, CA 95616, USA 6000 J Street, Sacramento, CA 95819, USA D. Schlenk Department of Environmental Sciences, University of California, 2258 Geology, P. W. Lehman Riverside, CA 92521, USA California Department of Water Resources, Division of Environmental Services, S. van Drunick 3500 Industrial Boulevard, Cooperative Institute for Research in Environmental Science West Sacramento, CA 95691, USA (CIRES), University of Colorado at Boulder, Box 216 UCB, Boulder, CO 80309, USA I. Werner Aquatic Toxicology Laboratory, Department of Anatomy, J. I. Drever Physiology, and Cell Biology, School of Veterinary Medicine, Department of Geology and Geophysics, Department 3006, University of California, University of Wyoming, 1330 F Haring Hall, 1000 University Avenue, Davis, CA 95616, USA Laramie, WY 82071, USA 604 Estuaries and Coasts (2012) 35:603–621 indicates that examining the effects of contaminants and salinity and turbidity, as well as inputs of municipal other stressors on specific life stages in different seasons wastewater, fertilizers, and pesticides. A common challenge and salinity zones of the estuary is critical to identifying to prioritizing mitigation is that biota are responding to an how several interacting stressors could contribute to a array of stressors that each have sublethal effects. general syndrome of declines. Moreover, warming water Contaminants may be important contributors to death by a temperatures of the magnitude projected by climate models thousand cuts, but the difficulty of quantifying their increase metabolic rates of ectotherms, and can hasten independent effects makes the often high economic cost elimination of some contaminants. However, for other of regulating individual stressors such as pesticides seem pollutants, concurrent increases in respiratory rate or food excessive and unfair when other factors such as wastewater intake result in higher doses per unit time without changes output from municipalities also contribute. The resulting in the contaminant concentrations in the water. Food societal demand for unequivocal proof of appreciable limitation and energetic costs of osmoregulating under mortality hinders progress toward remediation. altered salinities further limit the amount of energy Even when waters are legally impaired according to a available to fish; this energy must be redirected from regulatory standard, it is often hard to attribute declines of a growth and reproduction toward pollutant avoidance, variety of species to contaminants on the basis of standard enzymatic detoxification, or elimination. Because all of toxicological tests that use mortality of a few well-studied these processes require energy, bioenergetics methods are species as the main criterion of effect. The desire to promising for evaluating effects of sublethal contaminants generate legal criteria that address contaminants in isolation in the presence of other stressors, and for informing from confounding factors has led to reliance on standard- remediation. Predictive models that evaluate the direct and ized laboratory tests with limited environmental reality indirect effects of contaminants will be possible when data (Heugens et al. 2001). However, ecological effects of single become available on energetic costs of exposure to contam- or multiple contaminants, like the influences of weather, inants given simultaneous exposure to non-contaminant disease, food shortage, or behavioral disturbance, are more stressors. commonly sublethal contributors to a suite of adverse ecological conditions (Porter et al. 1984). Moreover, Keywords Susceptibility to toxins . Bioenergetic costs . exposure to contaminants along with other stressors is Impaired waterways . Multiple stressors . Pelagic organism often highly episodic, as after major storms or during decline . Climate change . Review blooms of toxic cyanobacteria. Such periodic events can greatly affect populations, but can go undetected by rigidly scheduled environmental monitoring of weekly or monthly Introduction habitat quality. In fish, sublethal effects can occur as subtle or cryptic Urbanization and agricultural development around estuaries impairments such as altered behavior or suppressed are often associated with major changes in the abundance immunity, which are difficult to measure even under and composition of aquatic species (Nichols et al. 1986; controlled laboratory conditions. In rivers and streams or Chaudry and Zwolsman 2008). Such shifts in estuarine tidal systems, detecting such effects requires direct obser- communities coincide with altered hydrology, which affects vation of fish impairment and immediate collection of biological and water samples before the toxicant moves away from the sampling location. A solution to the A. E. Parker : R. Dugdale Romberg Tiburon Center for Environmental Studies, San difficulty of measurement may lie in recognizing that Francisco State University, energy is redirected from growth and reproduction toward 3152 Paradise Drive, avoiding, detoxifying, or eliminating pollutants, and that Tiburon, CA 94920, USA energy demands increase when contaminant exposure is Present Address: coupled with other stressors such as limited food or altered E. Fleishman salinity (Beyers et al. 1999a, b). Thus, measuring energetic John Muir Institute of the Environment, The Barn, University costs by methods such as comparing growth rates or of California, reproductive output to that of control organisms captures One Shields Ave., Davis, CA 95616, USA the impact of single and compounding stressors, and logistically, is more feasible than measuring cryptic effects Present Address: of contaminants. I. Werner In estuaries, salinity and turbidity are key habitat Swiss Centre for Applied Ecotoxicology, Eawag/EPFL, Überlandstrasse 133, parameters, and use of specific habitat zones varies among 8600, Dübendorf, Switzerland species and life stages depending on their osmoregulatory Estuaries and Coasts (2012) 35:603–621 605 capability (Feyrer et al. 2010). In this paper, we present a biological effects of water quality, researchers have conceptual model of the susceptibility to contaminants of collected waters from various locations across the entire four fish species with different habitat-use patterns Delta. After exposing organisms to those water samples (anadromous, brackish, and freshwater) in the San under controlled laboratory conditions, researchers docu- Francisco Estuary. In this scheme, we consider season, mented widespread toxicity to invertebrates, planktonic location, and mode of action of contaminants for each algae, and larval fish during times when the four fish life stage. We then review published evidence of species of interest are in the Delta (Fig. 1). The sublethal but statistically significant effects of contam- percentages of toxic samples range from 0% to 15% inants (including inorganic nitrogen) on fish or their depending on test species, sampling frequency, and food in the San Francisco Estuary and elsewhere. We location, which is highly heterogeneous among projects consider interactions among contaminants as well as (Werner et al. 2000; Johnson et al. 2010;Werneretal. with environmental factors (e.g., salinity, turbidity). We 2010). Despite such evidence of the presence of toxic also explore how warming water