Exposure Pathways and Effects of Mercury on Wildlife: Tools for Natural Resource Damage Assessment and Restoration

Transcription

1 Exposure Pathways and Effects of Mercury on Wildlife: Tools for Natural Resource Damage Assessment and Restoration Josh Ackerman U.S. Geological Survey, Western Ecological Research Center (February 15, 2018)

2 Talk Outline 1) Ecological pathways of mercury exposure ecology, location, timing 2) Physiological processes which influence mercury toxicity maternal transfer, mass dilution, fasting-associated concentration, 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 NRDAR Injury Assessment recommended tissue types, sample sizes, toxicity risk translators, establishing baseline exposure and toxicity risk, sampling tools (biosentinels, artificial nest boxes, caged fish)

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

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

5 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

6 Bird Mercury Exposure in Great Salt Lake, Utah 29 species, N>1,000 Egg THg (µg/g fresh wet wt) Ackerman et al USGS Open File Report

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

8 Ecological Pathways Conceptual Model Resource Management Example #2: Foraging Guild Example #3: Diet Example #4: Habitat Example #5: Foraging Strategy Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

9 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:

10 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

11 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:

12 Foraging Strategies Influence Mercury Exposure (foraging in mesopelagic zone 200-1,000m deep) Peterson et al Proceedings of the Royal Society B 282:

13 Ecological Pathways Conceptual Model Resource Management Example #6: Site-specific processes and food webs Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

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

15 Small Scale: Mercury Varies Substantially Among Wetlands in a Region (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

16 Eggs Represent Local Mercury Contamination (Space Use Declines Substantially Before Egg Production) Distance From Nest (m) Days Prior To Incubation R 2 = 0.69 Demers et al Waterbirds 31: Area (ha) % Home range 50% Core-use area 0 pre-breeding incubation chick-rearing post-breeding (n = 7) (n = 9) (n = 7) (n = 8) Stage Bluso et al Waterbirds 31:

17 Ecological Pathways Conceptual Model Resource Management Example #7: Timing of Exposure Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

18 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:

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

20 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:

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

22 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:

23 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:

24 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:

25 Ecological Pathways Conceptual Model Resource Management Example #9: Change in Body Mass Ecological Pathways and Processes Physiology Environmental Occurrence Exposure Adverse Outcomes

26 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:

27 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:

28 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:

29 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:

30 Mass Dilution Reduces & Mass Loss Increases Mercury Concentrations & Toxicity Risk in Adult Mammals +17% mass -31% THg +55% mass -29% THg -30% mass +97% THg -27% mass +30% THg Long Foraging Trip (+55% mass) Breeding (fasting: -30% mass) Short Foraging Trip (+17% mass) Molting (fasting: -27% mass) Hg concentrations declined more in seals which gained more mass Peterson et al Proceedings of the Royal Society B

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

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

33 Mercury Risk to Birds in North America Forster's Tern Willet Northern Shoveler American White Pelican Clark's Grebe Least Tern Black Skimmer Clapper Rail Caspian Tern Double-crested Cormorant Common Loon Black-necked Stilt Pacific Loon Red-throated Loon Snowy Plover Green-winged Teal American Coot Western Grebe Bald Eagle Yellow-billed Loon Brown Pelican American Avocet Tree Swallow Greater Scaup Wood Duck Black-crowned Night-heron Eared Grebe Harlequin Duck Great Blue Heron Mallard Laysan Albatross Snowy Egret Pectoral Sandpiper Long-billed Dowitcher Red Phalarope Semipalmated Sandpiper Piping Plover Ash-throated Flycatcher Rusty Blackbird Red-necked Phalarope House Wren Osprey Glaucous Gull Barn Swallow Common Murre Tricolored Heron White-winged Scoter White-faced Ibis Killdeer California Gull Surf Scoter Barrow's Goldeneye Western Sandpiper King Eider Dunlin Common Eider Gadwall Franklin's Gull Thick-billed Murre Lesser Scaup Marsh Wren Cliff Swallow Ring-billed Gull Spectacled Eider Red-winged Blackbird Mountain Plover Yellow-headed Blackbird Canada Goose Snow Goose % of individuals sampled % at High Risk (>3 µg/g ww) 33% 1% Blood THg <0.2 µg/g ww µg/g ww µg/g ww µg/g ww >4.0 µg/g ww Ackerman et al Science of the Total Environment 568:

34 % 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

35 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 % 90% 80% 70% 60% 50% % Egg THg µg/g fresh wet wt

36 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:

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

38 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:

39 Body Condition Declines with Mercury in Songbirds (fat score declined 28% and body mass declined 7% over range of mercury) Fat score Blood THg µg/g wet wt Cache Creek Settling Basin, Yolo County, California Ackerman, unpublished

40 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. 2012; Environmental Pollution 162:

41 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

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

43 Tools for NRDAR Injury Assessment & Restoration Scaling Tool #1: Recommended tissue types for sampling birds Tool #2: Appropriate sample sizes Tool #3: How to sample contaminants from specific locations Tool #4: Using biosentinels Tool #5: Translating toxicity benchmarks Tool #6: Toxicity benchmarks

44 Tool #1: Which Bird Tissue to Sample? Problem: Different tissues represent different time frames Some tissues have some inorganic mercury, so total mercury (which is cheaper to analyze) is not a good representation of risk to animal (methyl mercury is the more toxic form) Solution: Lots of studies! See summary table of suggestions

45 Tool #1: Which Bird Tissue to Sample? sample adult blood, eggs, or chick down feathers avoid fully grown feathers Ackerman et al Science of the Total Environment 568:

46 Tool #2: Sample Size for Monitoring? Problem: What is the required sample size to estimate population s mean contaminant exposure? Egg laying order influences mercury, thus reducing accuracy of estimating actual mean Solution: Model egg mercury variance within clutch and estimate appropriate sample sizes

47 Egg Laying Order Influences Mercury in Parents & Eggs Literature Review % -21% -24% Egg THg concentration (µg/g fresh wet wt) A B B B Avocets Egg laying order Ackerman et al Environmental Toxicology and Chemistry 35:

48 Monitoring Programs Need to Account for Intra-Clutch Variability (Estimated # of Nests that Need to be Sampled using 1 Egg Collected Per Nest) Percentage within actual mean egg THg concentration 50% 40% A) Large populations Suggestion: when population size is large Stilt Avocet Tern Percentage within actual mean egg THg concentration B) Colony Population Size: Forster s terns 30% 30% Sample 15 eggs for small population 20% 20% Sample 60 eggs for large population 10% 10% 50% 40% when colony size is 100 nests Large 0% % Number of nests sampled Number of nests sampled To be within 10% of actual population s mean egg Hg, sample: 58 nests for terns 65 nests for avocets 111 nests for stilts To be within 20% of actual population s mean egg Hg, sample 14 nests To be within 10% of actual population s mean egg Hg, sample 47 nests Ackerman et al Environmental Toxicology and Chemistry 35:

49 Tool #3: How to Measure Site-Specific Contaminant Concentrations when Animals can Move? Problem: We often want to measure contaminant concentrations in wildlife at a fixed location, but we know that animals move and can be exposed to contaminants from multiple areas. Solution: Develop caging methods to keep animals at the site of interest

50 Tool #3: Caged Fish Rapid Mercury Bioaccumulation in Rice Fields Fish THg (µg/g dry wt) 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:

51 Tool #3: Artificial Nest Boxes Mercury in Tree Swallow Eggs along a River Egg THg (µg/g fresh wet wt) River Distance from Lake Dam (m) Putah Creek, from Lake Berryessa Ackerman, unpublished

52 Tool #4: 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.

53 Tool #4: 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:

54 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:

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

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

57 Tool #5: Translating Toxicity Risk Across Bird Tissues Problem: Toxicity benchmarks developed for lots of different bird tissues How to merge these results into a single toxicity reference benchmark? Solution: Translate mercury concentrations across tissue types into same unit Suggest using blood-equivalent units

58 Tool #5: Translating Toxicity Risk Across Bird Tissues [MeHg] (µg/g dry wt) Liver r 2 = 0.88 [MeHg] (µg/g dry wt) Kidney r 2 = 0.88 liver muscle Blood kidney [THg] (µg/g dry wt) Kidney r 2 = 0.87 [THg] (µg/g dry wt) Muscle r 2 = 0.90 feathers Breast feather r 2 = Head feather r 2 = 0.40 [THg] (µg/g dry wt) [THg] (µg/g dry wt) Blood [THg] (µg/g wet wt) Eagles-Smith et al Environmental Toxicology & Chemistry 27:

59 Tool #5: Translating Toxicity Risk Across Bird Tissues eggs Blood Geometric Mean Egg THg (µg/g fresh wet wt) Female Blood THg µg/g ww Ackerman et al Environmental Pollution 230: Ackerman et al Environmental Pollution 210:

60 Tool #5: Translating Toxicity Risk Across Bird Tissues 100 Chick down feather THg (µg/g dry wt) 10 1 Terns Stilts Avocets Fresh whole egg THg (µg/g fresh wet wt) Ackerman et al Environmental Science & Technology 43:

61 Tool #5: Translating Toxicity Risk Across Bird Tissues Ackerman et al Science of the Total Environment 568:

62 Tool #5: Translating Toxicity Risk Across Bird Tissues Use equations carefully, multiple assumptions apply and may not be accurate for your specific species

63 Tool #6: Establishing Baseline Exposure & Toxicity Risk Problem: What are baseline, or normal, levels of mercury contamination in birds? Are there general toxicity benchmarks? Solution: Summarize available data, translate toxicity benchmarks across tissue types, and interpret risk

64 Tool #6: Establishing Baseline Exposure & Toxicity Risk Blood THg <0.2 µg/g ww µg/g ww µg/g ww µg/g ww >4.0 µg/g ww Interpretation Background levels; below known effect levels Lower risk Moderate risk Higher risk Severe risk Important Caveats: Mercury toxicity is known to differ among bird species e.g., songbirds may be more sensitive refer to Heinz et al (Species differences in the sensitivity of avian embryos to methylmercury) Risk is a policy designation informed by science what level of risk are we willing to accept? Ackerman et al Science of the Total Environment 568:

65 Talk Outline 1) Ecological pathways of mercury exposure ecology, location, timing 2) Physiological processes which influence mercury toxicity maternal transfer, mass dilution, fasting-associated concentration, 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 NRDAR Injury Assessment recommended tissue types, sample sizes, toxicity risk translators, establishing baseline exposure and toxicity risk, sampling tools (biosentinels, artificial nest boxes, caged fish)

66 Questions?