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Environmental Endocrine Disruption In San Francisco Bay Fish Effects Assessment. Kevin Kelley 1-3 , Jesus Reyes 1-3 , Rusty Fairey 4 , Zed Mason 2,3 , Cathy Propper 5 , Julianne Kalman 1,2, 3. 1 EEL --Environmental Endocrinology Laboratory , Marine Biology Program
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Environmental Endocrine Disruption In San Francisco Bay Fish Effects Assessment Kevin Kelley1-3, Jesus Reyes1-3, Rusty Fairey4, Zed Mason2,3, Cathy Propper5, Julianne Kalman1,2,3 1EEL --Environmental Endocrinology Laboratory , Marine Biology Program 2IIRMES --Institute for Integrated Research on Materials, Environment & Society 3CEPA --Center for Education in Proteomics Analysis California State University, Long Beach 4Marine Pollution Laboratory, Moss Landing Marine Laboratories 5Northern Arizona University 6Cabrillo Marine Aquarium, San Pedro, CA
ENDOCRINE SYSTEMS regulate essential physiological functions Reproduction - Somatic Growth - MetabolismDefense/Immune - Thyroid - Developmental Stress Responses - Neuroendocrine - others …Homeostasis, Adaptation, Survival…
Some points about endocrine systems: . . . highly sensitive & responsive . . . respond to presence of environmental factors (stressors) to a degree commensurate with the need to maintain homeostasis . . . endocrine disturbances observed are typically indicative of the type of environmental factor(s) acting
Monitoring programs can take advantage ofendocrine disruptionas asensitive screening tooltoassess effects (impacts) of water/environmental quality & specific contaminant effects Endocrine-disrupting chemicals (EDCs) are present in marine and estuarine environments, particularly along highly populated coastal regions: SF Bay Estuary http://toxics.usgs.gov/photo_gallery/sanfran.html
STUDY OBJECTIVES 1-determine incidence and magnitude of endocrine disruption in wild fishes thyroid, stress responses, growth & repair, reproduction 2- determine whether spatial differences can be establishedbetween different SF Bay locations 3- determine liver contaminant concentrations in individuals Correlatespecificcontaminantconcentrations with types/magnitude ofendocrine disruption
Shiner Surfperch Cymatogaster aggregata Pacific Staghorn Sculpin Leptocottus armatus pelagic benthic
2006 Field Sites [pilot year] San Pablo Bay Berkeley Waterfront Oakland Inner Harbor Redwood City far-field reference:Tomales Bay
Thyroid Hormones T4 T3 • broad physiological actions • essential for brain/neural development • permissive to somatic growth • important regulators of metabolism 3,5,3’-triiodothyronine 3,5,3’,5’-tetraiodothyronine (thyroxine)
Shiner Surfperch Thryoxine (T4) Levels in Shiner Surfperch 100 80 Plasma Thyroxine (T4) Concentration, ng/ml 60 40 20 (19) (19) (9) (14) (11) 0 San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Tomales Bay
Pacific Staghorn Sculpin Thryoxine (T4) Levels in Pacific Staghorn Sculpin 100 80 Plasma Thyroxine (T4) Concentration, ng/ml 60 40 20 (8) (13) (17) (12) (5) 0 San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Tomales Bay
Thryoxine (T4) Levels in SF Bay Fish 100 80 Pacific Staghorn Sculpin Plasma Thyroxine (T4) Concentration, ng/ml 60 40 Shiner Surfperch 20 (19) (8) (13) (19) (17) (12) (9) (5) (14) (11) 0 San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Tomales Bay
Environmental Contaminants are Implicated in Thyroid Endocrine Disruption: …e.g., Phenols, Hg, Cd impair thyroxogenesis in thyroid follicle cells in fish (Bhattacharya et al., ‘89) …e.g., endosulfan, Aroclor 1254 and selected PCBs decrease T4 levels in fish, via effects on iodotyrosine diodinases(Coimbra et al., ‘05; LeRoy et al., ‘06) …e.g., ioxynil, certain PCBs and PBDEs bind transthyretin and TRs with high affinities, altering T4 and T3 levels/ actions in fish (Tomy et al., ‘04; Lema et al., ‘06; Morgado et al., ‘07)
Shiner Surfperch Stress Response a a 1600 b 1200 Plasma Cortisol Concentration (ng/ml) b 800 400 21 21 10 13 0 Oakland Inner Harbor Berkeley Waterfront San Pablo Bay Redwood City
Pacific Staghorn Sculpin Stress Response a a 1200 Plasma Cortisol Concentration (ng/ml) 800 b 400 c 17 13 19 16 0 Oakland Inner Harbor Berkeley Waterfront San Pablo Bay Redwood City
Other wild fish species living in affected marine environments exhibit impairment of their neuroendocrine stress response system ...experimental studies have shown that contaminants, --such as PCBs-- impair stress responses in fish (Quabius et al., 2005; Vijayan et al., 2006)
S U M M A R Y –Year 1 Endocrine Disruption—SF Bay Fish Tomales Bay San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Thyroxine/thyroid Shiner Perch Pacific Staghorn Sculpin Cortisol/stress response Shiner Perch Pacific Staghorn Sculpin IGF-I/growth Shiner Perch ? ? Pacific Staghorn Sculpin ? ?
S U M M A R Y –Year 1 Endocrine Disruption—SF Bay Fish Tomales Bay San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor 17β-Estradiol/Reprod. Pacific Staghorn Sculpin immature 17α-Ethinylestradiol/Pharm. Pacific Staghorn Sculpin Testosterone/Reprod Pacific Staghorn Sculpin
Shiner Perch ? August 2006 Oakland Inner Harbor
S U M M A R Y –Year 1 Endocrine Disruption—SF Bay Fish Tomales Bay San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor 17β-Estradiol/Reprod. ? ? ? ? Shiner Perch ? Pacific Staghorn Sculpin 17α-Ethinylestradiol/Pharm. Shiner Perch Pacific Staghorn Sculpin Testosterone/Reprod ? ? ? ? Shiner Perch ? Pacific Staghorn Sculpin
Contaminant Analyses: • Feasible to measure individuals liver contaminant levels (PCBs, PAHs, pesticides) • Several contaminants measured at high concentrations in shiner perch and Pacific staghorn sculpin • Relatively higher levels of contaminants in livers of Pacific staghorn sculpin • Feasible to correlate individual liver contaminant concentrations with endocrine and physiological indices
Year – 2 Studies under way
Study Sites[August 2007] San Pablo Bay (Loch Lohmand Marina) Richmond(Lauritzen Channel, DDTs) Richmond/Berkeley Waterfront Oakland Inner Harbor San Leandro Bay(PCBs) San Francisco Waterfront Hunter’s Point(POTW) Redwood City Tomales Bay Bodega Bay Two Harbors –Santa Catalina Island(Pacific side)L.A. Harbor –Inner Cabrillo Beach(collab. w/CMA)
Endocrine Parameters in 2007-8 THYROID Thyroxine & Triidothyronine STRESS Cortisol & Cortisone REPRODUCTION 17β-Estradiol, 17α-Ethinylestradiol, Vitellogenin REPRODUCTION Testosterone & 11-ketotestosterone GROWTH IGF-I & IGFBPs
Emphasis:Thyroid Endocrine (HPT) Axis Underlying Mechanisms: • Altered thyroxine levels. -- T4 measurement • Altered T3 levels, T4:T3 ratios? -- T3 measurement, calculate T4:T3 • Altered thyroid gland morphology? -- Thyroid histology • Impaired thyroid responsiveness? -- TSH-challenge • Altered T4 metabolism or TH receptors? -- peripheral iodotyrosine deiodinases(ID1-3),TRα, TRβ • Relationships with specific bioaccumulated chemicals? -- Hepatic contaminants measurement & correlation Environmental Contaminants: Physiological Impacts: • Impaired growth? -- Growth & IGF system indices[IGF-I, IGFBPs, cartilage growth activity]
Emphasis:Stress Endocrine (HPI) Axis Underlying Mechanisms: • Altered cortisol levels. --Cortisol measurement • Altered interrenal gland morphology?-- Interrenal histology • Altered metabolism of cortisol? --cortisone measurement • Impaired interrenal responsiveness?-- ACTH-challenge • Impaired production of cortisol? -- steroidogenic enzyme expression(StAR, 11β-hydroxylase, 11β-HSD-2) Environmental Contaminants: • Relationships with specific bioaccumulated chemicals? -- Hepatic contaminants measurement & correlation • Impaired defense?-- Parasitic infestation assessment • Impaired growth?-- Growth & IGF system indices[IGF-I, IGFBPs, cartilage growth activity] Physiological Impacts:
SUMMARY POINTS • Endocrine responses and/or endocrine disruption serve as sensitive bio-markers of environmental perturbations • Endocrine systems are: • --highly sensitive to environmental stressors • --respond proportionally to the need to maintain homeostasis • --show alterations reflective of the kind of stressor(s) present(different EDCs affect different endocrine axes via distinct underlying mechanisms)
SUMMARY POINTS continued III. Endocrine-disrupted conditions are observed in SF Bay fish(urban, industrial, boat marinas) IV. Endocrine disruption is evident in different fish species V. Endocrine disruption is occurring in different endocrine systems (stress, thyroid, reproduction, growth & repair, defense, metabolism) VI. There may be interactions among endocrine systems(means wider impacts on physiological performance)
DIRECTION • Identification of specific chemicals associated with endocrine disruption • B. Understand mechanisms and test candidate EDCs, to establish cause and effect • C. Build models to estimate ecologically relevant performance alterations from measures of endocrine disruption (growth, reproduction, disease/parasitism) • D. Determine contaminant thresholds of effects • E. Use new technologies (proteomics) to build integrated phenotypic biomarker fingerprints(multifactorial screen)
Long Beach Env’l. Endo. Lab. ? Jesus Reyes, Kathy Sak, Andrew Hamilton, Becki Hagstrom, Maelanie Galima, Dawn Petschauer, Navdeep Brar, Tiffany Price, Tuan Truong, Dana Cianfrani, Shari Smolko, Tami Gonzalez, Claire Wingard, Kenna Koons, Julianne Kalman, Scott Adams, Wendy Hall http://www.csulb.edu/depts/endo
* * *PARTNERS Regional Monitoring Program –San Francisco Estuary Institute * Moss Landing Marine Labs Marine Pollution Laboratory Orange County Sanitation District Env’l Assessment Division California State University, Long Beach –IIRMES & CEPA Southern California Coastal Water Research Project * Northern Arizona Univ. City of Los Angeles Bureau of Sanitation Env’l Monitoring Division University of California, Riverside University of California, San Diego Los Angeles County Sanitation Districts Cabrillo Marine Aquarium *