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

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Page 1: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Josh AckermanU.S. Geological Survey, Western Ecological Research Center

(February 15, 2018)

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

Page 2: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Talk Outline1) Ecological pathways of mercury exposure

• ecology, location, timing2) Physiological processes which influence mercury

toxicity• maternal transfer, mass dilution, fasting-associated

concentration, excretion into feathers3) 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)

Page 3: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Environmental Occurrence Adverse OutcomesExposure

Resource Management

Ecological Pathways and Processes

Physiology

Page 4: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Ecological Pathways and Processes

Environmental Occurrence Adverse OutcomesExposure

Physiology

Resource Management

Example #1: Species

Page 5: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Bloo

d-eq

uiva

lent

TH

g(µ

g/g

wet

wt)

Fors

ter's

Ter

nC

aspi

an T

ern

Cla

rk's

Gre

beW

illet

Com

mon

Loo

nBl

ack

Skim

mer

Leas

t Ter

nYe

llow

-bille

d Lo

onBa

ld E

agle

Lays

an A

lbat

ross

Wes

tern

Gre

beC

lapp

er R

ail

Red

-thro

ated

Loo

nPa

cific

Loo

nSn

owy

Plov

erBl

ack-

neck

ed S

tilt

Dou

ble-

cres

ted

Cor

mor

ant

Gre

ater

Sca

upN

orth

ern

Shov

eler

Eare

d G

rebe

Gla

ucou

s G

ull

Amer

ican

Whi

te P

elic

anBr

own

Pelic

anSn

owy

Egre

tH

arle

quin

Duc

kPe

ctor

al S

andp

iper

Blac

k-cr

owne

d N

ight

-her

onLe

sser

Sca

upC

omm

on M

urre

Thic

k-bi

lled

Mur

reBa

rrow

's G

olde

neye

Long

-bille

d D

owitc

her

Amer

ican

Avo

cet

Osp

rey

Wes

tern

San

dpip

erR

usty

Bla

ckbi

rdTr

ee S

wal

low

Red

-nec

ked

Phal

arop

eKi

lldee

rG

reat

Blu

e H

eron

Barn

Sw

allo

wPi

ping

Plo

ver

Sem

ipal

mat

ed S

andp

iper

Whi

te-w

inge

d Sc

oter

Red

Pha

laro

peC

omm

on E

ider

Mar

sh W

ren

Dun

linFr

ankl

in's

Gul

lG

adw

all

Tric

olor

ed H

eron

Amer

ican

Coo

tW

hite

-face

d Ib

isAs

h-th

roat

ed F

lyca

tche

rH

ouse

Wre

nM

alla

rdSu

rf Sc

oter

King

Eid

erR

ing-

bille

d G

ull

Spec

tacl

ed E

ider

Clif

f Sw

allo

wC

alifo

rnia

Gul

lR

ed-w

inge

d Bl

ackb

irdW

ood

Duc

kG

reen

-win

ged

Teal

Mou

ntai

n Pl

over

Yello

w-h

eade

d Bl

ackb

irdSn

ow G

oose

Can

ada

Goo

se

0.0

0.2

0.4

0.6

0.8

1.0

1.2

Mercury by Species in Western North America(only showing species with >60 samples; 273 species total)

Ackerman et al. 2016 Science of the Total Environment 568:749-769

Page 6: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Bird Mercury Exposure in Great Salt Lake, Utah29 species, N>1,000

Egg

THg

(µg/

g fre

sh w

et w

t)

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

1.1

1.2

0.0 0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

1.1

1.2

Ackerman et al. 2015 USGS Open File Report 2015-1020

Page 7: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Bird Mercury Exposure in San Francisco Bay, California17 species, N>4,000

*Ackerman and Eagles-Smith 2008†Schwarzbach and Adelsbach 2003§Tsao et al. 2008

0.0

0.5

1.0

1.5Eg

g TH

g(µ

g/g

fresh

wet

wt)

Page 8: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Ecological Pathways and Processes

Environmental Occurrence Adverse OutcomesExposure

Physiology

Resource Management

Example #2: Foraging Guild

Example #3: Diet

Example #4: Habitat

Example #5: Foraging Strategy

Page 9: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Bird Mercury by Foraging Guild

Molluscovore

Crustaceovore

Blood-equivalent THg (µg/g wet wt)0.0 0.1 0.2 0.3 0.4 0.5

Herbivore

Granivore

Omnivore

Insectivore

Vermivore

Carnivore

Piscivore

Raw Data Literature-Review Data

Ackerman et al. 2016 Science of the Total Environment 568:749-769

Page 10: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tern Diet & Prey Fish Mercury

Fish

TH

g(µ

g/g

dry

wt)

0.25

0.50

0.75

1.00a

a

bccde d d de

e §§

Peterson et al. 2018 PLOS ONE acceptedEagles-Smith & Ackerman 2014 Environmental Pollution 193:147-155

SilversidesThree-spined sticklebackYellowfin gobyLongjaw mudsuckerPacific herringNorthern anchovyStaghorn sculpinOther invertebrates & fishOther gobiesRainwater killifishPerches

Tern Diet N=9,991 fish 2005-2015

Page 11: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Blood-equivalent THg (µg/g wet wt)0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7

Terrestrial-ground

Terrestrial-upper canopy

Terrestrial-lower canopy

Freshwater

Coastal

Fresh and brackish water

Salt marsh

Ocean

Bird Mercury by HabitatRaw Data Literature-Review Data

Ackerman et al. 2016 Science of the Total Environment 568:749-769

Page 12: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Foraging Strategies Influence Mercury Exposure(foraging in mesopelagic zone 200-1,000m deep)

Peterson et al. 2015 Proceedings of the Royal Society B 282:20150710

Page 13: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Ecological Pathways and Processes

Environmental Occurrence Adverse OutcomesExposure

Physiology

Resource Management

Example #6: Site-specific processes and food webs

Page 14: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Large Scale:Bird Mercury Exposure in Western North America

(N=29,219)

Ackerman et al. 2016 Science of the Total Environment 568:749-769

Page 15: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Small Scale:Mercury Varies Substantially Among Wetlands in a Region

(11-fold difference for Avocets nesting in 32 wetlands)

R1

A1A2

WAB

1AB

2A5 A7 A8 A1

6A1

7N

ew C

hica

go M

arsh

Strip

Mar

shC

oyot

e C

reek

Lag

oon

N4/

N5

N4A

N4A

BN

6/N

7N

6/N

9N

8/N

9E1

0XE1

4B E2 E4 E6 E6A E8 E8A

E8X

Mou

nt E

den

Cre

ek M

arsh

-N

orth

Mou

nt E

den

Cre

ek M

arsh

-So

uth

Nor

th S

tilt M

arsh

Pond

4

Egg

THg

(µg/

g fre

sh w

et w

t)

0.00

0.10

0.20

0.30

0.40

0.50

0.60

Wetland Site

Ackerman et al. 2014 USGS Open File Report 2014-1251

Page 16: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Eggs Represent Local Mercury Contamination(Space Use Declines Substantially Before Egg Production)

0

5000

10000

15000

20000

pre-breeding incubation chick-rearing post-breeding

Stage

Are

a (h

a)

95% Home range

50% Core-use area

(n = 7) (n = 9) (n = 7) (n = 8)Bluso et al. 2008 Waterbirds 31:357-364

R2 = 0.69

0

1000

2000

3000

4000

5000

6000

40 30 20 10

Days Prior To Incubation

Dist

ance

Fro

m N

est (

m)

Demers et al. 2008 Waterbirds 31:365-371

Page 17: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Ecological Pathways and Processes

Environmental Occurrence Adverse OutcomesExposure

Physiology

Resource Management

Example #7: Timing of Exposure

Page 18: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Bird Mercury Increases after Arrival in Estuary(Over-Wintering Period)

DateSep Nov Jan Mar May

Live

r TH

g(µ

g/g

dry

wt)

1

10

Central BayNorth BaySuisun Bay

FemalesMales

Eagles-Smith et al. 2009 Environmental Pollution 157:1993-2002

Page 19: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Bird Mercury Increases after Arrival in Estuary

Bloo

d TH

g(µ

g/g

wet

wt)

Pre-breeding Breeding

0.0

1.0

2.0

3.0

3x

Eagles-Smith et al. 2009 Environmental Pollution 157: 1993-2002

Page 20: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Mercury in Prey Fish is Highest During Bird Reproduction

Date

Fish

TH

g(µ

g/g

dry

wt)

0.2

0.3

0.4

0.5

0.6

0.7 MudsuckersSticklebacks

Tern nest initiationN=715 nests

Tern chick hatchingN=444 nests

3/1 4/10 5/20 6/30 8/10

50

100

25

75

125

50

100

25

75

125

# N

ests

Initi

ated

#

Chi

cks

Hat

ched

68% nests initiated

31% chicks hatch

% at peak prey mercury

Eagles-Smith & Ackerman 2009 Environmental Science & Technology 43:8658-8664

Page 21: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Ecological Pathways and Processes

Environmental Occurrence Adverse OutcomesExposure

Physiology

Resource Management

Example #8: Maternal Transfer

Page 22: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Maternal Transfer of Mercury: Waterbirds

P<0.0001R2=0.95N=83

AvocetsTernsStilts

Data shows geometric mean and range of Hg within each clutchG

eom

etric

Mea

n Eg

g TH

g(µ

g/g

fresh

wet

wt)

0.01

0.1

1

10

Female Blood THg µg/g ww0.1 1 10

Eggs

Blood

Ackerman et al. 2016 Environmental Pollution 210:145-154

Page 23: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Maternal Transfer of Mercury: Songbirds

P<0.0001R2=0.95N=83

Tree SwallowHouse Wren

Data shows geometric mean and range of Hg within each clutch

Geo

met

ric M

ean

Egg

THg

(µg/

g fre

sh w

et w

t)

Female Blood THg µg/g ww

Ackerman et al. 2017 Environmental Pollution 230:463-468

0.1 1 100.01

0.1

1

Page 24: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Different Maternal Transfer Among Species Results in Different Toxicity Risk

Geo

met

ric M

ean

Egg

THg

(µg/

g fre

sh w

et w

t)

Female Blood THg µg/g ww0.1 1 10

0.1

1

0.55

0.19

0.39

0.25

0.50

Egg

Ackerman et al. 2016 Environmental Pollution 210:145-154Ackerman et al. 2017 Environmental Pollution 230:463-468

Page 25: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Ecological Pathways and Processes

Environmental Occurrence Adverse OutcomesExposure

Physiology

Resource Management

Example #9: Change in Body Mass

Page 26: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

High Hg site: A16

Low Hg site: N7

Mercury Concentrations as Juvenile Birds Age

Blo

od T

Hg

(µg/

g w

et w

t)

Age (days)

0 10 20 30 40

0.1

1

10

Ackerman et al. 2011 Environmental Science & Technology 45:5418-5425

Page 27: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

0 10 20 30 40

0.1

1

10 Blood THg

Mass

Feathers

THg

(µg/

g w

et w

t)Pr

opor

tion

of fu

lly

grow

n fe

athe

rs

Age (days)

Mas

s (g

)

0 10 20 30 400

20406080

100120140160

0 10 20 30 40

0%

20%

40%

60%

80%

100%

Fledge at 28 days of age

Low Hg site: N7

High Hg site: A16

Mercury as Chicks Age

Ackerman et al. 2011 Environmental Science & Technology 45:5418-5425

Page 28: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Mass Dilution Reduces Mercury Concentrations & Toxicity Risk in Juvenile Birds

Cha

nge

in B

lood

Mer

cury

(Fin

al T

Hg

/ Ini

tial T

Hg)

Change in Mass (Final mass / Initial mass)

1 10

0.1

1

High Hg site: A16Low Hg site: N7

Hg concentrations declined more in chicks which gained more mass

Ackerman et al. 2011 Environmental Science & Technology 45:5418-5425

Page 29: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Toxicity Risk Changes as Juvenile Birds Age

THg

(µg/

g w

et w

t)

Age (days)

0 10 20 30 40

0.1

1

10

Low Hg site: N7

High Hg site: A16

At Hatch Fledged

Critical Exposure Periods for Toxicity

Ackerman et al. 2011 Environmental Science & Technology 45:5418-5425

Page 30: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

+17% mass-31% THg

+55% mass-29% THg

-30% mass+97% THg

-27% mass+30% THg

Breeding(fasting:-30% mass)

Molting(fasting:-27% mass)

Short Foraging

Trip(+17% mass)

Long Foraging

Trip(+55% mass)

Mass Dilution Reduces & Mass Loss IncreasesMercury Concentrations & Toxicity Risk in Adult Mammals

Hg concentrations declined more in seals which gained more mass

Peterson et al. 2018 Proceedings of the Royal Society B 20172782

Page 31: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

An animal's physiologycan profoundly influence contaminant

concentrations regardless of their actualenvironmental contaminant exposure

Page 32: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Ecological Pathways and Processes

Environmental Occurrence Adverse OutcomesExposure

Physiology

Resource Management

Page 33: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Mercury Risk to Birds in North America

Ackerman et al. 2016 Science of the Total Environment 568:749-769

33%

1%

<0.2 µg/g ww

0.2-1.0 µg/g ww

1.0-3.0 µg/g ww

3.0-4.0 µg/g ww

>4.0 µg/g ww

% at High Risk(>3 µg/g ww)

0 20 40 60 80 100

Yellow-headed Blackbird

Ash-throated Flycatcher

Semipalmated Sandpiper

Black-crowned Night-heron

Double-crested Cormorant

American White Pelican

Snow GooseCanada Goose

Mountain PloverRed-winged Blackbird

Spectacled EiderRing-billed Gull

Cliff SwallowMarsh Wren

Lesser ScaupThick-billed Murre

Franklin's GullGadwall

Common EiderDunlin

King EiderWestern Sandpiper

Barrow's GoldeneyeSurf Scoter

California GullKilldeer

White-faced IbisWhite-winged Scoter

Tricolored HeronCommon Murre

Barn SwallowGlaucous Gull

OspreyHouse Wren

Red-necked PhalaropeRusty Blackbird

Piping Plover

Red PhalaropeLong-billed Dowitcher

Pectoral SandpiperSnowy Egret

Laysan AlbatrossMallard

Great Blue HeronHarlequin Duck

Eared Grebe

Wood DuckGreater ScaupTree Swallow

American AvocetBrown Pelican

Yellow-billed LoonBald Eagle

Western GrebeAmerican Coot

Green-winged TealSnowy Plover

Red-throated LoonPacific Loon

Black-necked StiltCommon Loon

Caspian TernClapper Rail

Black SkimmerLeast Tern

Clark's Grebe

Northern ShovelerWillet

Forster's Tern

% of individuals sampled

Blood THg

Page 34: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

% Eggs at Risk to Mercury Toxicity in San Francisco Bay

0 20 40 60 80 100

Forster’s tern

Caspian tern

Stilt

Avocet

% of Eggs at Risk

3%

31%

13%

79%

% at High Risk

High Risk (>1.0)Low Risk (<0.5) Moderate Risk (0.5-1.0)

Egg THg (µg/g fresh wet wt)

Ackerman et al. 2014 USGS Open File Report 2014-1251

Page 35: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Behavioral Changes with Mercury in Songbirds(# nest breaks increased by 140% and time incubating declined by 11% over range in mercury)

0.0 0.1 0.2 0.3 0.4 0.5 0.6

Num

ber o

f nes

t bre

aks

per

day

0

10

20

30

40

50

60

70

Egg THg µg/g fresh wet wt0.0 0.1 0.2 0.3 0.4 0.5 0.6

40%

50%

60%

70%

80%

90%

100%%

of T

ime

Spen

t Inc

ubat

ing

Page 36: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

1 10

Prob

abilit

y of

em

bryo

mal

posi

tion

0.0

0.2

0.4

0.6

0.8

1.0

Egg THg (µg/g fresh wet wt) 1 10

0.0

0.2

0.4

0.6

0.8

1.0 Malpositioned embryo

Normal embryo

Herring et al. 2015 Environmental Toxicology and Chemistry 29:1788-1794

Mercury Increases Likelihood of Embryo Malposition in Tern Eggs

2% of Random Eggs are Malpositioned27% of Failed-to-Hatch Eggs are Malpositioned

Malpositioned embryo: beak above right wing

Page 37: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Mercury Highest in Failed-to-Hatch Tern Eggs

Egg type

Egg

THg

(μg/

g fr

esh

wet

wt)

1.0

1.2

1.4

1.6

1.8

2.0

2.2

Ackerman et al. 2014 USGS Open File Report 2014-1251

28%

Page 38: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Effects of Mercury on Shorebird Chick Mortality at Hatching

Avocets Stilts0

5

10

15

20

Chi

ck D

own

Feat

her T

Hg

(μg/

g dr

y w

t)

Live chicksDead chicks

Newly Hatched

Ackerman et al. 2008 Ecotoxicology 17:103-116

Page 39: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Blood THg µg/g wet wt0.001 0.01 0.1 1 10

Fat s

core

0.2

0.4

0.6

0.8

1.0

1.2

Body Condition Declines with Mercury in Songbirds(fat score declined 28% and body mass declined 7% over range of mercury)

Cache Creek Settling Basin, Yolo County, CaliforniaAckerman, unpublished

Page 40: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Body Condition Declines with Mercury in Endangered Clapper Rails(mass declined 20-22g [or 5-7% of body mass] over range of mercury)

-40

-20

0

20

40

60

80

0.1 10.2 20.3 0.5 3

Bird

Mas

s (g

)

(p

artia

l res

idua

l)

Blood THg (µg/g wet wt)

-100

-80

-60

-40

-20

0

20

40

60

1075432 3020 40Head Feather THg (µg/g dry wt)

FemalesMales

*partial residuals statistically accounted for other variables in the model: sex, body size, date, year, and sex×body size

Bird

Mas

s (g

)

(p

artia

l res

idua

l)

Ackerman et al. 2012; Environmental Pollution 162:439-448

Page 41: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

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

Critical Endpoints for Mercury Toxicity

Page 42: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ecological Pathways Conceptual Model

Environmental Occurrence Adverse OutcomesExposure

Resource Management

Ecological Pathways and Processes

Physiology

Page 43: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

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

Tools for NRDAR Injury Assessment & Restoration Scaling

Page 44: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

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

Tool #1:Which Bird Tissue to Sample?

Page 45: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tool #1:Which Bird Tissue to Sample?

• sample adult blood, eggs, or chick down feathers• avoid fully grown feathers

Ackerman et al. 2016 Science of the Total Environment 568:749-769

Page 46: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

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

Tool #2:Sample Size for Monitoring?

Page 47: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ackerman et al. 2016 Environmental Toxicology and Chemistry 35:1458-1469

Egg Laying Order Influences Mercury in Parents & Eggs

Egg

THg

conc

entra

tion

(µg/

g fre

sh w

et w

t)

Egg laying order1 2 3 4

0.20

0.22

0.24

0.26

0.28

0.30

A

BB B

-16% -21% -24%Literature Review

Avocets

Page 48: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Ackerman et al. 2016 Environmental Toxicology and Chemistry 35:1458-1469

Monitoring Programs Need to Account for Intra-Clutch Variability (Estimated # of Nests that Need to be Sampled using 1 Egg Collected Per Nest)

Number of nests sampled

B) Colony Population Size: Forster’s terns

Perc

enta

ge w

ithin

act

ual

m

ean

egg

THg

conc

entra

tion

0 10 20 30 40 50 60 70 80 90 1000%

10%

20%

30%

40%

50%102030405060708090100Large

A) Large populations

Perc

enta

ge w

ithin

act

ual

m

ean

egg

THg

conc

entra

tion

0 100 200 300 400 5000%

10%

20%

30%

40%

50%StiltAvocetTern

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

when population size is large…

when colony size is ≤100 nests….

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

Suggestion:• Sample 15 eggs for small population• Sample 60 eggs for large population

Page 49: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

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

Tool #3:How to Measure Site-Specific Contaminant Concentrations when Animals can Move?

Page 50: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

12 × higher

Caged Mosquitofish

Fish

TH

g(µ

g/g

dry

wt)

0.0

0.5

1.0

1.5

2.0

0 30 60

White riceWild ricePermanent wetlands

Tool #3: Caged FishRapid Mercury Bioaccumulation in Rice Fields

Increase in 60 Days

6 × higher

3 × higher

Ackerman & Eagles-Smith 2010 Environmental Science & Technology 44:1451-1457

Days of Exposure

Page 51: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tool #3: Artificial Nest BoxesMercury in Tree Swallow Eggs along a River

River Distance from Lake Dam (m)0 10000 20000 30000 40000

0.1Eg

g TH

g(µ

g/g

fres

h w

et w

t)

0.02

0.2

Putah Creek, from Lake BerryessaAckerman, unpublished

Page 52: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

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.

Tool #4:Using Biosentinels to Estimate Mercury Risk to Wildlife

Page 53: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tool #4:Mercury Risk to Lake Wildlife

Gre

be B

lood

TH

g(µ

g/g

ww

)

0.1

1.0

10.0

Prey Fish THg (µg/g dw or (ww))

0.01 0.10 1.00(0.002) (0.024) (0.24)

Ackerman et al. 2015 Environmental Science & Technology 49:13596-13604

Page 54: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Bird

Blo

od T

Hg

(µg/

g w

w)

Prey Fish THg (µg/g dw or (ww))(0.002) (0.024) (0.24)

0.01 0.10 1.00 10.000.1

1.0

10.0

(2.42)

Bird to Prey Fish Models(All Available in the World)

Ackerman et al. 2015, Clark’s Grebe Females in CaliforniaAckerman et al. 2015, Western Grebe Females in CaliforniaBurgess & Meyer 2008, Common Loon FemalesScheuhammer et al. 1998, Common Loons, both sexesEvers et al. 2011 & Report, Common Loon Females, 5-10cm fishEvers et al. 2011 & Report, Common Loon Females, 10-15cm fishChampoux et al. 2006, Common Loon FemalesYu et al. 2011, Common Loon FemalesBird 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

0.94 µg/g wwfor female birds

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

Ackerman et al. 2015 Environmental Science & Technology 49:13596-13604

Page 55: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Bird to Prey Fish Models

in Wetlands (tool does not work

in all habitats)

Ackerman et al. 2014 USGS Open File Report 2014-1251

Page 56: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Management Application: Predictive Tool for Resource Managers

https://pubs.usgs.gov/of/2015/1106/

Ackerman et al. 2015 USGS Open File Report 2015-1106

Page 57: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

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”

Tool #5:Translating Toxicity Risk Across Bird Tissues

Page 58: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tool #5:Translating Toxicity Risk

Across Bird Tissues

Eagles-Smith et al. 2008 Environmental Toxicology & Chemistry 27:2136-2153

Blood [THg] (µg/g wet wt)[M

eHg]

(µg/

g dr

y w

t)[T

Hg]

(µg/

g dr

y w

t)[T

Hg]

(µg/

g dr

y w

t)

Kidney

Muscle

Head feather

r2 = 0.88

r2 = 0.90

r2 = 0.40

0.01 0.1 1 10 1000.01

0.1

1

10

100

0.01 0.1 1 10 1000.01

0.1

1

10

100

0.01 0.1 1 10 1000.01

0.1

1

10

100

[MeH

g] (µ

g/g

dry

wt)

[TH

g] (µ

g/g

dry

wt)

[TH

g] (µ

g/g

dry

wt)

Liver

Kidney

Breast feather

r2 = 0.88

r2 = 0.87

r2 = 0.32

0.01 0.1 1 10 1000.01

0.1

1

10

100

0.01 0.1 1 10 1000.01

0.1

1

10

100

0.01 0.1 1 10 1000.01

0.1

1

10

100

kidney

muscle

Blood

feathers

liver

Page 59: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tool #5:Translating Toxicity Risk Across Bird Tissues

Geo

met

ric M

ean

Egg

THg

(µg/

g fre

sh w

et w

t)

Female Blood THg µg/g ww0.1 1 10

0.1

1

Ackerman et al. 2016 Environmental Pollution 210:145-154Ackerman et al. 2017 Environmental Pollution 230:463-468

eggs

Blood

Page 60: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Chi

ck d

own

feat

her T

Hg

(µg/

g dr

y w

t)

Fresh whole egg THg(µg/g fresh wet wt)

0.01 0.1 1 100.1

1

10

100

TernsStiltsAvocets

Ackerman et al. 2009 Environmental Science & Technology 43:2166-2172

Tool #5:Translating Toxicity Risk Across Bird Tissues

Page 61: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tool #5:Translating Toxicity Risk Across Bird Tissues

Ackerman et al. 2016 Science of the Total Environment 568:749-769

Page 62: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tool #5:Translating Toxicity Risk Across Bird Tissues

Use equations carefully, multiple assumptions apply and may not be accurate

for your specific species

Page 63: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

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

Tool #6:Establishing Baseline Exposure & Toxicity Risk

Page 64: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Tool #6:Establishing Baseline Exposure & Toxicity Risk

Ackerman et al. 2016 Science of the Total Environment 568:749-769

Background levels; below known effect levels

Lower risk

Moderate risk

Higher risk

Severe risk

Blood THg<0.2 µg/g ww

0.2-1.0 µg/g ww

1.0-3.0 µg/g ww

3.0-4.0 µg/g ww

>4.0 µg/g ww

Interpretation

Important Caveats:• Mercury toxicity is known to differ among bird species

• e.g., songbirds may be more sensitive• refer to Heinz et al. 2009 (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?

Page 65: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

Talk Outline1) Ecological pathways of mercury exposure

• ecology, location, timing2) Physiological processes which influence mercury

toxicity• maternal transfer, mass dilution, fasting-associated

concentration, excretion into feathers3) 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)

Page 66: Exposure Pathways and Effects of Mercury on Wildlife · 1) Ecological pathways of mercury exposure • ecology, location, timing. 2) Physiological processes which influence mercury

[email protected]

Questions?