1. Mercury Risk to Avian Reproduction in San Francisco Bay: Implications for TMDL Implementation Collin Eagles-Smith, Josh Ackerman, Terry Adelsbach, John Takekawa, Keith Miles, Steve Schwarzbach, and Tom Suchanek U. S. Fish and Wildlife Service, Environmental Contaminants Division U. S. Geological Survey, Western Ecological Research Center

2. Mercury in San Francisco Bay-Delta Birds: Trophic Pathways, Bioaccumulation, and Ecotoxicological Risk to Avian Reproduction

3. San Francisco Bay Estuary HEMISPHERIC IMPORTANCE FOR WATERBIRDS

4. Central nervous system effects Altered behavior Impaired vision, hearing, and motor skills Endocrine effects Reduced breeding effort Embryo death Embryo deformities Chick death Wildlife Sensitive to Methyl Mercury Toxicity Forster’s Tern Nest MeHg Reduces Reproductive Success

5. Bird Mercury Questions 1.Mercury differences among species. 2.Spatial and temporal trends in bird and egg mercury. 3.Relate mercury concentrations to reproductive risk. 4.Fish as wildlife indicators? 5.Implications for TMDL implementation.

6. Littoral Foragers – insects & crustaceans American avocet Black-necked stilt Obligate Piscivores - fish Forster’s tern Caspian tern Species Studied

7. Study Sites 3 regions –North Bay (Napa-Sonoma Marsh) –Central Bay (Eden Landing, Newark) –South Bay (Don Edwards SFB NWR) North Bay Central Bay South Bay

8. Radiomarked & tracked Birds Captured Released Mercury Analyzed at USGS Davis Field Station Mercury Lab Methods Whole blood drawn

9. Prey fish collected Telemetry based Methods Continued Nesting monitored

10. Birds Captured SpeciesPre-breedingBreedingTotal Avocet 21835253 Stilt 16639208 Forster’s tern 11943162 Caspian tern 282048 Total Captures = 668

11. Bird Mercury Concentrations 3. Mercury concentrations increased over time P < 0.0001 1. Mercury differed among species 2. Mercury concentrations differed among regions Forster’s tern Blood Hg (ppm ww) 0.1 1 10 Date 4/1 4/10 4/20 4/30 5/10 5/20 5/30

12. North BayCentral BaySouth Bay Forster’s Tern Male Hg > Female Hg (P = 0.003) Breeding > Pre-breeding (P < 0.0001) 0.1 1 10 Blood [Hg] (ppm ww) North Bay > Central Bay < South Bay (P = 0.03) Male Female Pre-breed Breed

13. What Does this Mean for Birds? Risk Factor Analysis Based on Evers et al. 2004 (common loon) & Heinz and Hoffman 2003 (mallard) Documented Effects at Population Level >4Extra High Documented Effects: Molecular, Cellular, Behavioral, Potential Population Effects 3–4High Potential Effects; Reduced Egg Hatchability 1–3Moderate Undocumented; Minimal Effects<1Low Impact Hg Concentration (ppm) Risk Category Blood (ww) Eggs (dw) 6.8–8 3.2–6.8 <3.2 >8

14. North BayCentral BaySouth Bay Forster’s Tern 0.1 1 10 Blood [Hg] (ppm ww) Male Female Pre-breed Breed Low Moderate High Extra high Risk Category

15. North Bay Central BaySouth Bay Stilt 0.1 1 10 Female, breeding Male, pre-breeding Female, pre-breeding Blood [Hg] (ppm ww) Low Moderate High Extra high Risk Category

16. Avocet Stilt Forster’s tern Avocet Stilt Forster’s tern Caspian tern Avocet Stilt Forster’s tern Caspian tern Central Bay North Bay South Bay Percent of Population at Risk Site Specific Low RiskModerate RiskHigh RiskExtra High Risk 0% 2% 4% 29% 0% 1% 22% 10% 27% Risk Factor: High + Extra High

17. Avocet Stilt Caspian tern Forster’s tern Percent of Population at Risk Breeding Birds Only Low RiskModerate RiskHigh RiskExtra High Risk 6% 5% 10% 58% Risk Factor: High + Extra High

18. Avocets Stilts Forster’s Terns Mercury in Eggs Extra High High Risk Category Low Moderate

19. Percent of Population at Risk All Eggs Low RiskModerate RiskHigh RiskExtra High Risk 0% 10% 46% Risk Factor: High + Extra High 020 40 60 80 100 Avocet Stilt Forster’s tern Percent of Population at Risk

20. Management & Regulatory Implications 1.Differences in space and habitat use 2.Differences in diet 3.Differences in prey Hg Differences in mercury exposure

21. Telemetry Map Stilts 2005 South

22. Telemetry Map Avocets 2005 South

23. Telemetry Map Forster’s Terns 2005 South

24. Forster’s Tern Diet by Colony -Estimated from colony returns-

25. Pond A8 N = 42 Forster’s Tern Diet by Colony -Estimated from colony returns- Stickleback Silverside Topsmelt Mudsucker Goby Anchovy Other Pond A1 N = 151 Pond A7 N = 546 Pond A16 N = 168 Newark N = 246 Eden Landing N = 20 Napa Marsh N = 13

26. Prey Fish Hg Concentrations Pond A1Pond A7Pond A8Pond A16North Bay

27. Fish vs. Egg Mercury Relationships

28. Stickleback Mercury(ppm ww) Colony Egg Mercury ( ppm ww ) 0 1 2 3 0 0.1 0.2 R2 = 0.10 P =0.31 Silverside Mercury (ppmww) Colony Egg Mercury ( ppm ww ) 0 1 2 3 0 0.1 0.20.3 Silverside Mercury (ppmww) Colony Egg Mercury ( ppm ww ) 0 1 2 3 0 0.1 0.20.3 MudsuckerMercury (ppmww) Colony Egg Mercury ( ppm ww ) 0 1 2 3 0 0.1 0.2 MudsuckerMercury (ppmww) Colony Egg Mercury ( ppm ww ) 0 1 2 3 0 0.1 0.2 Goby Mercury Colony Egg Mercury ( ppm ww ) 0 1 2 3 0 0.1 0.2 (ppm ww) R2 = 0.19 P =0.33 R 2 = 0.04 P =0.65 R 2 = 0.07 P =0.57

29. Diet-weighted Fish vs. Egg Mercury: Spatially Explicit Diet-weighted Fish Mercury (ppm ww) 0.000.050.100.150.200.250.300.35 Colony Egg Mercury (ppm ww) 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 + + +

30. Diet-weighted Fish vs. Egg Mercury: Spatially Explicit Diet-weighted Fish Mercury (ppm ww) 0.000.050.100.150.200.250.300.35 Colony Egg Mercury (ppm ww) 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 R 2 = 0.68 P = 0.01 1.Need to know bird space use 2.Need to know bird- specific diet 3.Need to know bird prey Hg concentrations

31. Wildlife target exceeds LOAEL Is wildlife target non-protective? Does LOAEL need refinement? OR Are fish inadequate indicators of avian risk? Diet-weighted Fish vs. Egg Mercury: TMDL implications Diet-weighted Fish Mercury (ppm ww) 0.000.050.100.150.200.250.300.35 Colony Egg Mercury (ppm ww) 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 R 2 = 0.68 P = 0.01 TMDL Wildlife Target Avian egg LOAEL

32. Eggs as indicators of wildlife risk Trophic Transfer Maternal Transfer Fail-to-Hatch Hatch Mortality (<10 d) Survive

33. Eggs as indicators of wildlife risk Trophic Transfer Maternal Transfer Fail-to-Hatch Hatch Mortality (<10 d) Survive

34. Birds show high site fidelity Birds are good bioindicators of Hg at small spatial and temporal scales Birds useful for Hg monitoring Conclusions:

35. In breeding birds –Especially Forster’s terns and potentially other fish-eating birds In eggs –Especially Stilts and Forster’s terns Conclusions: Current mercury levels are above toxic thresholds…

36. Individual fish species do not adequately represent wildlife exposure. Spatially explicit data on bird habitat use, diet and prey mercury to predict exposure. Eggs are valuable tools for monitoring mercury in Bay- Delta wildlife. Conclusions:

37. CALFED Ecosystem Restoration Program: – Carol Atkins and Donna Podger Logistical Support: –Don Edwards SF Bay NWR (USFWS): Clyde Morris, Joy Albertson, Mendel Stewart, Joelle Buffa, Eric Mruz –Eden Landing Ecological Reserve: John Krause –Napa/Sonoma Marsh Wildlife Area: Tom Huffman, Larry Wyckoff, Carl Wilcox, Karen Taylor Bird Mercury Project Principles: –USGS: Steve Schwarzbach, Tom Suchanek, John Takekawa, A. Keith Miles, Susan De La Cruz –US FWS: Tom Maurer, Dan Welsh –SFBBO: Cheryl Strong, Janet Hansen –PRBO Conservation Science: Nils Warnock, Mark Herzog Field Support: –Jill Bluso, Scott Demers, Sarah Stoner-Duncan, Angela Rex, John Henderson, Joe Northrup, Brooke Hill, Kristen Dybala, Eli French, Ross Wilming, Lindsay Dembosz, Cathy Johnson, Lani Stinson, Kevin Aceituno Emily Eppinger, Mychal Truwe, River Gates, Mali Nakhai, Lab Support: –Robin Keister, Sarah Spring, Liz Bowen Acknowledgements