Exposure Pathways and Effects of Mercury on Wildlife: Implications for Management

Transcription

1 Exposure Pathways and Effects of Mercury on Wildlife: Implications for Management Josh Ackerman U.S. Geological Survey, Western Ecological Research Center (April 24, 2018) This is information is preliminary and is subject to revision. It is being provided to meet the need for timely best science. The information is provided on the condition that neither the U.S. Geological Survey nor the U.S. Government may be held liable for any damages resulting from the authorized or unauthorized use of the information.

2 Talk Outline 1) Ecological pathways of mercury exposure ecology, location, timing 2) Physiological processes which influence mercury toxicity maternal transfer, mass dilution, excretion into feathers 3) Adverse outcomes of mercury exposure parental behavior, embryo malpositions, egg hatching success, chick survival, body condition, biological processes 4) Tools for monitoring and risk assessment

3 Ecological Pathways Conceptual Model Resource Management Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

4 Ecological Pathways Conceptual Model Why Do the Ecological Pathways of Mercury Bioaccumulation Matter? Because mercury in animals is rarely driven by sources alone, due to the unique cycling of mercury in the environment

5 Methyl Mercury Not Well Correlated With Total Mercury ln MeHg Sediment 245 or 24,500% R 2 =0.25 P= ln THg Sediment Fleck et al Science of the Total Environment 568:

6 Biotic Mercury Not Well Correlated With Mercury Sources THg Fish THg (µg/g ww) MeHg R 2 =0.01 P=0.07 Sediment THg (µg/kg dw) R 2 =0.06 P=0.001 Sediment MeHg (µg/kg dw) Eagles-Smith et al Science of the Total Environment 568:

7 Ecological Pathways Conceptual Model Resource Management Example #1: Species Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

8 Ackerman et al Science of the Total Environment 568: Mercury by Species in Western North America (only showing species with >60 samples; 273 species total) Blood-equivalent THg (µg/g wet wt) Forster's Tern Caspian Tern Clark's Grebe Willet Common Loon Black Skimmer Least Tern Yellow-billed Loon Bald Eagle Laysan Albatross Western Grebe Clapper Rail Red-throated Loon Pacific Loon Snowy Plover Black-necked Stilt Double-crested Cormorant Greater Scaup Northern Shoveler Eared Grebe Glaucous Gull American White Pelican Brown Pelican Snowy Egret Harlequin Duck Pectoral Sandpiper Black-crowned Night-heron Lesser Scaup Common Murre Thick-billed Murre Barrow's Goldeneye Long-billed Dowitcher American Avocet Osprey Western Sandpiper Rusty Blackbird Tree Swallow Red-necked Phalarope Killdeer Great Blue Heron Barn Swallow Piping Plover Semipalmated Sandpiper White-winged Scoter Red Phalarope Common Eider Marsh Wren Dunlin Franklin's Gull Gadwall Tricolored Heron American Coot White-faced Ibis Ash-throated Flycatcher House Wren Mallard Surf Scoter King Eider Ring-billed Gull Spectacled Eider Cliff Swallow California Gull Red-winged Blackbird Wood Duck Green-winged Teal Mountain Plover Yellow-headed Blackbird Snow Goose Canada Goose

9 Bird Mercury Exposure in San Francisco Bay 17 species, N>4, Egg THg (µg/g fresh wet wt) *Ackerman and Eagles-Smith 2008 Schwarzbach and Adelsbach 2003 Tsao et al. 2008

10 Songbird Mercury Exposure in Cache Creek Settling Basin 52 species, N=1,200 Western Kingbird Ruby-crowned Kinglet Black Phoebe American Robin Tree Swallow Marsh Wren Brewer's Blackbird Bewick's Wren House Wren Bullock's Oriole Barn Swallow Western Wood-pewee Red-winged Blackbird Ash-throated Flycatcher Fox Sparrow Song Sparrow Spotted Towhee Common Yellowthroat Pacific-slope Flycatcher Yellow-rumped Warbler Yellow-breasted Chat Nuttall's Woodpecker Hermit Thrush Wilson's Warbler Black-throated Gray Warbler California Towhee Warbling Vireo Lincoln's Sparrow Black-headed Grosbeak Orange-crowned Warbler Dark-eyed Junco Willow Flycatcher Brown-headed Cowbird Downy Woodpecker Blue Grosbeak Blue-gray Gnatcatcher Savannah Sparrow Bushtit Macgillivray's Warbler Hermit Warbler Wild Turkey Lazuli Bunting Yellow Warbler Lark Sparrow Swainson's Thrush Western Tanager Golden-crowned Sparrow White-crowned Sparrow American Goldfinch House Finch Lesser Goldfinch Mourning Dove Cache Creek Settling Basin: Same Hg source Birds captured within riparian habitat <3 miles Hg differs by 425 among species species ecology drives MeHg exposure Blood THg µg/g ww Cache Creek Settling Basin Ackerman, unpublished Preliminary Information Subject to Revision. Not for Citation or Distribution

11 Ecological Pathways Conceptual Model Resource Management Example #2: Foraging Guild Example #3: Diet Example #4: Habitat Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

12 Bird Mercury by Foraging Guild Raw Data Literature-Review Data Piscivore Carnivore Vermivore Insectivore Crustaceovore Molluscovore Omnivore Granivore Herbivore Blood-equivalent THg (µg/g wet wt) Ackerman et al Science of the Total Environment 568:

13 Tern Diet & Prey Fish Mercury Tern Diet N=9,991 fish Fish THg (µg/g dry wt) a a bc cde d d de e Silversides Three-spined stickleback Yellowfin goby Longjaw mudsucker Pacific herring Northern anchovy Staghorn sculpin Other invertebrates & fish Other gobies Rainwater killifish Perches Eagles-Smith & Ackerman 2014 Environmental Pollution 193: Peterson et al PLOS ONE accepted

14 Bird Mercury by Habitat Raw Data Literature-Review Data Ocean Salt marsh Fresh and brackish water Coastal Freshwater Terrestrial-lower canopy Terrestrial-upper canopy Terrestrial-ground Blood-equivalent THg (µg/g wet wt) Ackerman et al Science of the Total Environment 568:

15 Fish THg (µg/g dry wt) Habitat Type Influences Mercury Bioaccumulation Using Caged Fish Caged Mosquitofish Days of Exposure White rice Wild rice Permanent wetlands Increase in 60 Days 12 higher 6 higher 3 higher Ackerman & Eagles-Smith 2010 Environmental Science & Technology 44:

16 Ecological Pathways Conceptual Model Resource Management Example #5: Site-specific processes and food webs Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

17 Large Scale: Bird Mercury Exposure in Western North America (N=29,219) Ackerman et al Science of the Total Environment 568:

18 Small Scale: Mercury Varies Substantially Among Wetlands in SF Bay (11-fold difference for Avocets nesting in 32 wetlands) 0.60 Egg THg (µg/g fresh wet wt) R1 A1 A2W AB1 AB2 A5 A7 A8 A16 A17 New Chicago Marsh Strip Marsh Coyote Creek Lagoon N4/N5 N4A N4AB N6/N7 N6/N9 N8/N9 E10X E14B E2 E4 E6 E6A E8 E8A E8X Mount Eden Creek Marsh - North Mount Eden Creek Marsh - South North Stilt Marsh Pond 4 Wetland Site Ackerman et al USGS Open File Report

19 Mercury in Tree Swallow Eggs along Putah Creek Using Artificial Nest Boxes Egg THg (µg/g fresh wet wt) River Distance from Lake Dam (m) Putah Creek, from Lake Berryessa Ackerman, unpublished Preliminary Information Subject to Revision. Not for Citation or Distribution

20 Mercury in House Wren Eggs along Cache Creek Using Artificial Nest Boxes (wet) (dry) Egg THg (µg/g fresh wet wt) (drought) (re-wetted) 2012 River Distance from Bridge (m) Cache Creek Settling Basin Ackerman, unpublished Preliminary Information Subject to Revision. Not for Citation or Distribution

21 Ecological Pathways Conceptual Model Resource Management Example #6: Timing of Exposure Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

22 Bird Mercury Increases after Arrival in Estuary (Over-Wintering Period) Liver THg (µg/g dry wt) 10 1 Central Bay North Bay Suisun Bay Females Males Sep Nov Jan Mar May Date Eagles-Smith et al Environmental Pollution 157:

23 Bird Mercury Increases after Arrival in Estuary Blood THg (µg/g wet wt) x Pre-breeding Breeding Eagles-Smith et al Environmental Pollution 157:

24 Mercury in Prey Fish is Highest During Bird Reproduction 0.7 Mudsuckers Sticklebacks 0.6 Fish THg (µg/g dry wt) # Nests Initiated Tern nest initiation N=715 nests % at peak prey mercury 68% nests initiated # Chicks Hatched Tern chick hatching N=444 nests 31% chicks hatch 3/1 4/10 5/20 6/30 8/10 Date Eagles-Smith & Ackerman 2009 Environmental Science & Technology 43:

25 Ecological Pathways Conceptual Model Resource Management Example #7: Biosentinel Effectiveness Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

26 Using Biosentinels to Estimate Mercury Risk to Wildlife Problem: Often want to know mercury risk to wildlife, but wildlife is sometimes not sampled Solution: Sampling birds directly is much preferred, but using a cheaper-to-sample biosentinel is sometimes possible. Example for lake wildlife.

27 Mercury Risk to Lake Wildlife Grebe Blood THg (µg/g ww) (0.002) (0.024) (0.24) Prey Fish THg (µg/g dw or (ww)) Ackerman et al Environmental Science & Technology 49:

28 Bird to Prey Fish Models (All Available in the World) Bird Blood THg (µg/g ww) µg/g ww 1.0 for female birds 0.1 But these data all come from lakes, with distinct boundaries and that are widely separated spatially bird and fish mercury are poorly correlated in wetlands (0.002) (0.024) (0.24) (2.42) Prey Fish THg (µg/g dw or (ww)) Ackerman et al. 2015, Clark s Grebe Females in California Ackerman et al. 2015, Western Grebe Females in California Burgess & Meyer 2008, Common Loon Females Scheuhammer et al. 1998, Common Loons, both sexes Evers et al & Report, Common Loon Females, 5-10cm fish Evers et al & Report, Common Loon Females, 10-15cm fish Champoux et al. 2006, Common Loon Females Yu et al. 2011, Common Loon Females Bird Average 0.05 µg/g ww = 0.21 µg/g dw at 76% moisture Prey Fish Water Quality Objective California Regional Water Quality Control Board 2017 Ackerman et al Environmental Science & Technology 49:

29 Bird to Prey Fish Models in Wetlands (tool does not work in most habitats) Ackerman et al USGS Open File Report

30 Management Application: Predictive Tool for Resource Managers Ackerman et al USGS Open File Report

31 Ecological Pathways Conceptual Model Resource Management Example #8: Maternal Transfer Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

32 Maternal Transfer of Mercury: Waterbirds 10 Eggs Blood Geometric Mean Egg THg (µg/g fresh wet wt) P< R 2 =0.95 N=83 Avocets Terns Stilts Data shows geometric mean and range of Hg within each clutch Female Blood THg µg/g ww Ackerman et al Environmental Pollution 210:

33 Maternal Transfer of Mercury: Songbirds 1 Geometric Mean Egg THg (µg/g fresh wet wt) 0.1 P< R 2 =0.95 N=83 Tree Swallow House Wren Data shows geometric mean and range of Hg within each clutch Female Blood THg µg/g ww Ackerman et al Environmental Pollution 230:

34 Different Maternal Transfer Among Species Results in Different Toxicity Risk Geometric Mean Egg THg (µg/g fresh wet wt) Egg Female Blood THg µg/g ww Ackerman et al Environmental Pollution 230: Ackerman et al Environmental Pollution 210:

35 Ecological Pathways Conceptual Model Resource Management Example #8: Change in Body Mass Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

36 Mercury Concentrations as Juvenile Birds Age Blood THg (µg/g wet wt) Low Hg site: N7 High Hg site: A Age (days) Ackerman et al Environmental Science & Technology 45:

37 Mercury as Chicks Age THg (µg/g wet wt) 10 Blood THg Fledge at 28 days of age Mass (g) Proportion of fully grown feathers % 80% 60% 40% 20% 0% Mass Feathers Age (days) Low Hg site: N7 High Hg site: A16 Ackerman et al Environmental Science & Technology 45:

38 Mass Dilution Reduces Mercury Concentrations & Toxicity Risk in Juvenile Birds Change in Blood Mercury (Final THg / Initial THg) Change in Mass (Final mass / Initial mass) Low Hg site: N7 High Hg site: A16 Hg concentrations declined more in chicks which gained more mass Ackerman et al Environmental Science & Technology 45:

39 Toxicity Risk Changes as Juvenile Birds Age Critical Exposure Periods for Toxicity At Hatch Fledged 10 THg (µg/g wet wt) Low Hg site: N7 High Hg site: A Age (days) Ackerman et al Environmental Science & Technology 45:

40 An animal's physiology can profoundly influence contaminant concentrations regardless of their actual environmental contaminant exposure

41 Ecological Pathways Conceptual Model Resource Management Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

42 % Eggs at Risk to Mercury Toxicity in San Francisco Bay % at High Risk Avocet Stilt Caspian tern Forster s tern 3% 31% 13% 79% % of Eggs at Risk Low Risk (<0.5) Moderate Risk ( ) Egg THg (µg/g fresh wet wt) High Risk (>1.0) Ackerman et al USGS Open File Report

43 Behavioral Changes with Mercury in Songbirds (# nest breaks increased by 140% and time incubating declined by 11% over range in mercury) Number of nest breaks per day % of Time Spent Incubating 100% 90% 80% 70% 60% 50% 40% Egg THg µg/g fresh wet wt Cosumnes River Preserve Hartman & Ackerman, unpublished Preliminary Information Subject to Revision. Not for Citation or Distribution

44 Mercury Increases Likelihood of Embryo Malposition in Tern Eggs 2% of Random Eggs are Malpositioned 27% of Failed-to-Hatch Eggs are Malpositioned Probability of embryo malposition 1.0 Malpositioned embryo Malpositioned embryo: beak above right wing Normal embryo 1 10 Egg THg (µg/g fresh wet wt) Herring et al Environmental Toxicology and Chemistry 29:

45 Mercury Highest in Failed-to-Hatch Tern Eggs Egg THg (μg/g fresh wet wt) % gg type Ackerman et al USGS Open File Report

46 Effects of Mercury on Shorebird Chick Mortality at Hatching Chick Down Feather THg (μg/g dry wt) Avocets Stilts Newly Hatched Live chicks Dead chicks Ackerman et al Ecotoxicology 17:

47 Body Condition Declines with Mercury in Songbirds (THg decreased by 23% and 15% over range of body masses and fat scores) BloodTHg µg/g ww Standardized body mass Blood THg µg/g ww Fat score Cache Creek Settling Basin Ackerman, unpublished Preliminary Information Subject to Revision. Not for Citation or Distribution

48 Body Condition Declines with Mercury in Endangered Clapper Rails (mass declined 20-22g [or 5-7% of body mass] over range of mercury) Females Males Bird Mass (g) (partial residual) Blood THg (µg/g wet wt) Bird Mass (g) (partial residual) Head Feather THg (µg/g dry wt) *partial residuals statistically accounted for other variables in the model: sex, body size, date, year, and sex body size Ackerman et al Environmental Pollution 162:

49 Methyl Mercury Detoxification in Bird s Liver Demethylation Thresholds % MeHg in Liver (MeHg/THg 100) 100% 80% 60% 40% 20% 0% 100% 80% 60% 40% 20% Avocets ( ) & Stilts ( ) Threshold: 9.9 μg/g dry wt Slope: -21.2% Forster s Terns ( ) & Caspian Terns ( ) Threshold: 7.5 μg/g dry wt Slope: -12.7% 0% Liver THg (μg/g dry wt) Eagles-Smith et al Environmental Pollution 28:

50 Critical Endpoints for Mercury Toxicity Impaired Reproduction: including parental nesting behaviors, nest abandonment, egg hatching success, nest survival, chick growth and survival Bird Health: including behavior, physiology, demethylation, cellular oxidative stress, body condition, organ masses

51 Ecological Pathways Conceptual Model Resource Management Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

52 Questions?