Environmental contaminants in Canadian shorebirds

Environmental contaminants in Canadian shorebirds

Birgit M. Braune & David G. Noble

Received: 12 October 2007 /Accepted: 20 December 2007 / Published online: 14 March 2008# Crown Copyright 2008

Abstract Canadian shorebirds are exposed to envi-ronmental contaminants throughout their annual cycle.Contaminant exposure among species varies with diet,foraging behaviour and migration patterns. We sam-pled twelve species of shorebirds from four locationsacross Canada to assess their exposure to PCBs,organochlorine pesticides, as well as four traceelements (Hg, Se, Cd, As). ΣPCB and ΣDDT followedby ΣCHL were most frequently found above tracelevel in the shorebird carcasses. In general, the ploverspecies (American golden, semipalmated, black-bellied) appear to be the most contaminated withorganochlorines, whereas Hudsonian and marbledgodwits appear to be the least contaminated. Amongadult birds, the greater and lesser yellowlegs had thehighest hepatic Hg concentrations (2.4–2.7 μg g−1 dw),whereas American golden plovers as well as Hudso-nian and marbled godwits contained relatively lowlevels of Hg (<1 μg g−1 dw). Renal Se concentrationsvaried from 3.2 to 16.7 μg g−1 dw and exhibited littleinterspecific or seasonal variation. Renal Cd levels in

adult birds were highest in Hudsonian godwits fromQuill Lakes (43 μg g−1 dw) and Cape Churchill(12 μg g−1 dw), and lowest (0.8–1.5 μg g−1 dw) ingreater and lesser yellowlegs from Cape Churchilland Bay of Fundy. Renal As concentrations variedfrom 0.06 μg g−1 dw in golden plovers from CapeChurchill to 4.6 and 5.1 μg g−1 dw in dunlin samplesfrom the Pacific coast. There is no evidence thatcontaminants were adversely affecting the shorebirdssampled from the Canadian locations in this study.

Keywords Arsenic . Cadmium . Canada . DDT.

Mercury . PCBs . Organochlorines . Selenium .

Shorebirds

Introduction

An assessment of shorebird population trends inCanada (Morrison et al. 1994b) indicated that over40% of the species evaluated were experiencingpopulation declines in some part of their range duringthe period prior to the undertaking of this study.Several causes have been suggested for the observedchanges in abundance. These include habitat frag-mentation or loss due to increased disturbance fromhuman activities and weather, as well as deteriorationof habitat, including increased exposure to environ-mental pollutants such as organochlorines and traceelements (Morrison et al. 1994a). Shorebirds areparticularly vulnerable because of their diet of aquatic

Environ Monit Assess (2009) 148:185–204DOI 10.1007/s10661-007-0150-0

B. M. Braune (*)National Wildlife Research Centre, Environment Canada,Carleton University,Raven Road,Ottawa, ON, Canada, K1A 0H3e-mail: [email protected]

D. G. NobleBritish Trust for Ornithology,Thetford, Norfolk IP24 2PU, UK

and marine invertebrates in sediments, estuaries,tailings ponds and agricultural fields where pollutantconcentrations are often elevated. Some informationon contaminants in North American shorebirds hasbeen generated by studies: (1) targeting areas ofknown contamination such as Kesterson Reservoir inCalifornia’s Central Valley (Ohlendorf et al. 1990),the south Texas coast (White et al. 1980), and the ElkRiver in British Columbia (Harding et al. 2005), (2)out of concern for declining shorebird populations(e.g. Blus et al. 1985; Hothem and Powell 2000), (3)out of concern for the health of predatory species suchas peregrine falcons which prey on shorebirds (e.g.DeWeese et al. 1986; Schick et al. 1987; Baril et al.1990; Court et al. 1990; Custer and Myers 1990; Fyfeet al. 1990; Banasch et al. 1992; Johnstone et al.1996), and (4) in areas known to be important staginggrounds (Napolitano et al. 1992; McFarland et al.2002) or overwintering grounds (Hui 1998; Hui et al.2001). However, a survey of contaminants in shore-bird species across several locations has not beenundertaken, particularly not in Canada.

Most shorebirds breed in relatively remote areasbut congregate during migration and in the winter onstaging areas with high concentrations of prey. Inorder to evaluate the exposure of Canadian shorebirdsto environmental contaminants, we undertook tosurvey residue levels in a variety of species collected

from four different regions of Canada: (1) on one ofthe northern breeding grounds, (2) at an inland site inwestern Canada, (3) on a coastal staging area ineastern Canada, and (4) overwintering on the westcoast of Canada.

Methods

Sample collections

Twelve species of shorebirds were sampled byshotgun under Canadian Wildlife Service collectionpermits from one or more Canadian locations repre-senting breeding grounds, stopover/staging areas, andoverwintering areas (Fig. 1). The species collectedwere: American golden plover (Pluvialis dominica),semipalmated plover (Charadrius semipalmatus),black-bellied plover (Pluvialis squatarola), marbledgodwit (Limosa fedoa), Hudsonian godwit (Limosahaemastica), whimbrel (Numenius phaeopus), greateryellowlegs (Tringa melanoleuca), lesser yellowlegs(Tringa flavipes), short-billed dowitcher (Limnodro-mus griseus), long-billed dowitcher (Limnodromusscolopaceus), dunlin (Calidris alpina) and semipal-mated sandpiper (Calidris pusilla). The 12 speciesrepresent a diversity of foraging behaviour andmigratory strategies (Table 1) that influence their

111

CapeChurchill

TofinoBoundaryBay

Bay ofFundy

QuillLakes

Fig. 1 Locations of shore-bird sampling sites inCanada

186 Environ Monit Assess (2009) 148:185–204

Tab

le1

Ecologicalcharacteristicsof

shorebirdspeciessampled

across

Canada

Species

Sam

pling

sites

Maindiet

Foraginghabitat

Foragingbehaviou

rWinterrang

eReferences

American

Golden

Plover

CC

Terrestrial

invertebrates/

berries

Tun

dra/grasslands/

coastalwetland

sStop-Run

-Peck/

Stop

Central

Sou

thAmerica

Richards(199

1);John

son

andCon

nors

(199

6)

Black-bellied

Plover

BF

Insects/worms/aquatic

invertebrates

Tun

dra/mud

flats

Stop-Run

-Peck/

Stop

Atlantic/Pacific

coastsof

US/

Central/Sou

thAmerica

Richards(199

1);Paulson

(199

5)Sem

ipalmated

Plover

CC,BF

Aqu

atic

invertebrates/

insects

Tun

dra/mud

flats

Stop-Run

-Peck/

Stop

Atlantic/Pacific

coastsof

US/

Central/Sou

thAmerica

Richards(199

1);Nol

and

Blank

en(199

9)Sem

ipalmated

Sandp

iper

CC,QL,BF

Aqu

atic/terrestrial

invertebrates

Mud

flats

Pecking

/shallo

wprob

ing

Northern/centralcoasts

ofSou

thAmerica

Richards(199

1);Gratto

-Trevo

r(199

2)Dun

linCC,BF,

PC

Aqu

atic/terrestrial

invertebrates

Mud

flats

Shallo

wprob

ing/

pecking

Coastal

BritishColum

bia-Mexico

(pacifica

race);Eastern

coastalU.S.(hud

soniarace)

Richards(199

1);Warno

ckandGill

(199

6)

Whimbrel

CC

Aqu

atic

invertebrates/

insects/berries

Tun

dra/mud

flats

Shallo

w/deep

prob

ing/pecking

Atlantic/Pacific

coastsof

US/

Central/Sou

thAmerica

Richards(199

1);Skeel

andMallory

(199

6)Sho

rt-billed

Dow

itcher

CC,BF

Aqu

atic/terrestrial

invertebrates

Mud

flats/wetland

s/shallow

water

Deepprob

ing

Atlantic/Pacific

coastsof

US/

Central/Sou

thAmerica

Richards(199

1);Jehl

etal.(200

1)Lon

g-billed

Dow

itcher

QL

Aqu

atic/terrestrial

invertebrates

Mud

flats/wetland

s/shallow

water

Deepprob

ing

Atlantic/Pacific

coastsof

US/

Mexico

Richards(199

1);

TakekawaandWarno

ck(200

0)Hud

sonian

God

wit

CC,QL

Aqu

atic/terrestrial

invertebrates/aquatic

plants

Mud

flats/wetland

s/shallow

water

Deepprob

ing

Sou

therncoastalSou

thAmerica

Richards(199

1);Elphick

andKlim

a(200

2)

Marbled

God

wit

QL

Aqu

atic

invertebrates/

fish/in

sects/aquatic

plants

Mud

flats/wetland

s/shallow

water

Deepprob

ing/

pecking

Atlantic/Pacific

coastsof

US/

Mexico

Richards(199

1);Gratto

-Trevo

r(200

0)

Lesser

Yellowlegs

CC,BF

Aqu

atic/terrestrial

invertebrates/fish

Shallo

wwater/

mud

flats

Dips/pecks/

sweeps

Sou

therncoastalUS/

throug

hout

Central/Sou

thAmerica

Richards(199

1);Tibbitts

andMosko

ff(199

9)

Greater

Yellowlegs

BF

Aqu

atic/terrestrial

invertebrates/frog

s/fish

Shallo

wwater/

mud

flats

Dips/pecks/

sweeps

Sou

therncoastalUS/

throug

hout

Central/Sou

thAmerica

Richards(199

1);Elphick

andTibbitts

(199

8)

CCCapeChu

rchill(breedinggrou

nd),QLQuillLakes

(breeding/stop

-over),BFBay

ofFun

dy(stop-ov

er),PCPacific

Coast(overw

intering

)

Environ Monit Assess (2009) 148:185–204 187

exposure to environmental contaminants. The differ-ences in foraging behaviour among the speciessampled are strongly influenced by bill length andmorphology. Those species having the shortest bills,such as the plovers, forage using the Stop-Run-Peck(prey seen) and Stop-Run-Stop (no prey seen, changevantage point) mode which allows them to glean preyfrom the surface of the substrate (i.e. tundra,mudflats). Sandpipers, such as the semipalmatedsandpiper and dunlin, will peck as well as probe thesubstrate, whereas species with longer bills, such asthe whimbrel, dowitcher and godwit, are capable ofdeeply probing the substrate giving them access toprey not readily available to those species with shorterbills. Species, such as the yellowlegs, have developeda different strategy which allows them to take preyfrom the water column. However, most shorebirds canalso be quite opportunistic and flexible in theirforaging strategies thereby broadening the suite offoods taken (Skagen and Oman 1996).

Sampling sites

See Table 1 for a list of the species sampled at eachlocation.

Cape Churchill Eight species were sampled between12–28 June, 1991, on their eastern arctic breedinggrounds at Cape Churchill (58°47′ N, 94°11′ W), onthe western shore of Hudson Bay in northernManitoba. Most birds were collected foraging on tidalflats, but others were collected from along the edgesof tundra ponds where terrestrial prey such as larvalinsects predominate.

Quill Lakes Four species were sampled at Quill Lakes(52° N, 104° W) in southern Saskatchewan betweenJuly and September, 1991. The Quill Lakes are aseries of shallow, moderately saline lakes in thisheavily cultivated region of western Canada (Alexanderet al. 1996) and they constitute an important stopoversite for migrants as well as a breeding site for marbledgodwit.

Bay of Fundy Seven species of shorebirds weresampled during autumn migration (August to October1990 and 1991) in the Bay of Fundy (45–46° N, 66–67° W) in New Brunswick. This area is an extremelyimportant stopover site for more than a million birds

preparing for their transoceanic flight to SouthAmerican wintering grounds (Hicklin 1987). Themajor food source of birds foraging on tidal flats atthis time is the amphipod Corophium volutator(Hicklin and Smith 1979).

Pacific coast Dunlin overwintering on the Pacificcoast of Canada were collected from two sites insouthern British Columbia; at Tofino (49° N, 125° W),on the west coast of Vancouver Island, and atBoundary Bay (49° N, 122° W), a large intertidal areain the heavily industrial Strait of Georgia, south ofVancouver. The latter is part of the Fraser Riverestuary, which supports the largest overwinteringpopulations of shorebirds (mainly dunlin and black-bellied plovers) on the Pacific coast of Canada (Butlerand Campbell 1987). Dunlin feeding on tidal mudflatsand sandflats were collected during two time periods,first in November–December 1991 and then in March1992.

Tissue preparation

After collection, birds were individually placed inlabelled plastic bags, frozen whole, and shipped to theNational Wildlife Research Centre (NWRC) in Gati-neau, Quebec, where they were dissected underchemically clean conditions. Livers and kidneys wereremoved, homogenized and placed in acid-rinsedpolyethylene vials for trace element analyses, andthe carcasses (defeathered with legs, beak, liver,kidney, gastro-intestinal tract and some breast muscleremoved) were homogenized and placed in solvent-cleaned glass jars for organochlorine residue analyses.Tissues were stored in the NWRC Specimen Bank at−20°C. Pooled (composite) samples for chemicalanalysis (see Turle and Collins 1992) were createdbased on age (hatch year, adult) and/or sex by takingequal aliquots from each bird of a given species/age/sex collected from a specific location.

Chemical residue analyses

Sample pools were analyzed for chlorobenzenes(ΣCBz=1,2,4,5- and 1,2,3,4-tetrachlorobenzene,pentachlorobenzene and hexachlorobenzene), hexa-chlorocyclohexanes (ΣHCH = α-, β- and γ-hexa-chlorocyclohexane), chlordane-related compounds(ΣCHL = oxychlordane, trans-chlordane, cis-chlor-


dane, trans-nonachlor, cis-nonachlor and heptachlorepoxide), octachlorostyrene, DDT and its metabolites(ΣDDT = p,p′-DDE, p,p′-DDD and p,p′-DDT), mirex(ΣMirex = photo-mirex and mirex), dieldrin, andPCBs on a congener-specific basis. The number of PCBcongeners analyzed increased over time and, therefore,total PCBs (ΣPCB) were standardized as the sum of 42PCB congeners reported according to IUPAC numbers(Ballschmiter and Zell 1980): 28, 31, 42, 44, 49, 52,60, 64, 66/95, 70, 74, 87, 97, 99, 101, 105, 110, 118,129, 138, 141, 146, 149, 151, 153, 170/190, 171, 172,174, 180, 182/187, 183, 185, 194, 195, 200, 201, 203,and 206. Sample aliquots were extracted, cleaned upand analyzed using gas chromatography (GC) with anelectron capture detector (ECD) for organochlorinecompounds according to the procedure detailed inNorstrom and Won (1985). PCB congeners were ana-lyzed according to the method described in Norstrom etal. (1988). Quality assurance included the analysis ofreplicate samples, reagent blanks, spiked tissue homo-genates, and an in-house reference material (Wakefordand Turle 1997). Analyses were carried out by the GreatLakes Institute for Environmental Research, Universityof Windsor, Windsor, Ontario, or by NWRC.

Liver samples were analyzed for mercury (Hg) andkidney samples were analyzed for cadmium (Cd),selenium (Se) and arsenic (As). Prior to trace elementdetermination, samples were freeze-dried (Hg, Cd,Se) or oven-dried (As) and digested in mineral acidsas described in Neugebauer et al. (2000) and US EPA(1996). Total Hg was analyzed by cold vapor atomicabsorption spectrophotometry (AAS) (Perkin–Elmer3030B AAS equipped with Varian VGA-76 vaporgenerator and Varian PSC-55 autosampler); Cd wasanalyzed by flame AAS (Perkin–Elmer 3030B AASequipped with deuterium background corrector, highsensitivity nebulizer, and Varian ACT-80 tubes); andSe was analyzed by graphite furnace AAS (Perkin–Elmer 3030B AAS equipped with deuterium back-ground corrector, HGA-300 graphite furnace and AS-40autosampler) according to NWRC Method Nos. MET-CHEM-AA-01 (Cd), MET-CHEM-AA-02 (Se) andMET-CHEM-AA-03 (Hg) (Neugebauer et al. 2000).Arsenic was analyzed using inductively coupledplasma–mass spectrometry (ICP–MS) (Perkin Elmer/Sciex Elan 5000) (US EPA 1994). Analytical accuracyfor each methodology was determined using blanksamples, standard reference materials (SRM 1577a (forAs, Hg, Cd) obtained from the National Bureau of

Standards; DORM-1 (for As, Hg, Cd, Se) and DOLT-2(for Hg, Cd, Se) obtained from the National ResearchCouncil of Canada) and replicate analyses of randomsamples (Wakeford and Turle 1997). Elemental recov-eries of all reference materials were within the certifiedconfidence intervals. Samples were analyzed for totalHg, Cd and Se by NWRC, and for As by FenwickLaboratories, Halifax, Nova Scotia.

Data handling

Given that there were a limited number of samples, thatthe samples were pooled for chemical analyses, and thatorganochlorine concentration data tend to exhibit non-normal distributions, nonparametric statistical methodswere used. Due to the limited number of samplesanalyzed for each trace element, only the organochlorinedata were statistically analyzed. All statistical tests wereperformed using Statistica for Windows Version 7.0(StatSoft Inc., Tulsa, OK) with a significance level ofp<0.05. Only those compounds for which >70% of thesamples had detectable concentrations for a givenspecies were statistically analyzed. Non-detect values(<0.0001 μg g−1 wet weight (ww)) were set to one halfthe detection limit for purposes of statistical analysesbut not for calculation of the sums of the majororganochlorine groups (i.e. ΣPCB, ΣDDT, ΣCBz, etc)which appear in Table 2. Given the wide range in lipidlevels (1.4–41.3%), the organochlorine data were lipid-normalized using the ratio approach (i.e. dividingcontaminant concentration by lipid concentration) priorto statistical analysis. Gender (adults only) and agegroup (hatch-year vs adult) comparisons of organo-chlorine concentrations by species, collection date andlocation were carried out using the Wilcoxon pairedsample test, and inter-species comparisons were carriedout for adults by gender for the samples collected atCape Churchill using Friedman’s test (Zar 1999). Thetabulated data are presented in concentration units ofμg g−1 lipid weight (lw) for the organochlorines andμg g−1 dry weight (dw) for the trace elements.

Results

Organochlorines

The groups of organochlorine compounds most fre-quently found above trace level (≥0.001 μg g−1 ww) in


Tab

le2

Con

centratio

ns(μgg−

1lip

idweigh

t)of

organo

chlorinesin

carcassesa

ofshorebirds

from

variou

sCanadianlocatio

ns,19

90–1

992

Species

Location

Collection

period

Age

Sex

Nb

% Lipid

HCB

ΣCBz

β-

HCH

ΣHCH

oxychl

tran

s-no

nachl

HE

ΣCHL

p,p′

DDE

ΣDDT

Dieldrin

ΣMirex

ΣPCB42

American

Golden

Plover

Chu

rchill

June

Ad

F3

11.1

0.05

40.05

40.01

60.02

20.70

90.53

71.16

2.48

8.70

9.81

6.20

0.05

90.62

3June

Ad

M5

11.9

0.07

70.07

70.01

00.02

22.36

0.81

25.32

8.59

11.6

12.7

7.43

0.14

10.77

9Sem

ipalmated

Plover

Chu

rchill

June

Ad

F5

9.2

0.04

00.04

00.01

30.03

00.12

00.13

00.14

70.40

51.54

1.57

1.16

0.35

21.56

June

Ad

M5

12.4

0.06

00.06

00.01

40.04

40.13

30.12

20.07

90.36

18.18

8.23

2.07

0.65

73.35

Bay

ofFun

dyAug

–Sept

Ad

F4

33.7

0.01

60.01

6nd

nd0.02

10.01

6nd

0.03

70.47

60.47

60.02

30.01

60.36

8Aug

–Sept

Ad

M5

19.4

0.03

40.03

40.01

20.05

40.19

00.08

7nd

0.31

47.08

7.11

nd0.01

51.52

Black-bellied

Plover

Bay

ofFun

dyAug

–Sept

Ad

M/F

314

.40.05

20.05

2nd

nd0.01

00.06

10.13

00.21

90.65

80.65

80.08

30.02

32.13

Aug

–Sept

HY

F2

6.7

0.07

90.07

9tr

0.03

10.04

50.03

70.02

80.13

60.24

90.31

30.06

4nd

1.52

Marbled

God

wit

Quill

Lakes

Sept

HY

F3

34.3

ndnd

ndnd

trnd

nd0.00

70.12

40.12

4nd

0.01

50.06

0Sept

HY

M/

U3

7.9

ndnd

ndnd

0.01

3nd

nd0.10

40.33

50.33

5nd

0.03

70.21

9

Hud

sonian

God

wit

Chu

rchill

June

Ad

F5

9.0

0.01

40.01

4nd

nd0.03

2nd

0.06

20.09

50.90

20.90

2tr

0.04

30.30

9Quill

Lakes

July

Ad

F3

27.5

0.01

00.02

3nd

nd0.00

7tr

0.00

40.02

10.06

40.07

0nd

nd0.08

1July–A

ugAd

F3

41.3

0.00

80.00

8tr

0.00

30.00

70.00

50.011

0.02

70.04

40.04

40.01

90.00

5nd

Whimbrel

Chu

rchill

June

Ad

F5

5.3

0.06

40.06

40.01

90.02

80.113

0.01

90.08

30.21

55.77

6.05

0.07

00.04

02.12

June

Ad

M3

6.2

0.03

90.03

9nd

tr0.08

4nd

0.110

0.25

04.15

4.32

0.08

20.02

91.20

Greater

Yellowlegs

Bay

ofFun

dyOctob

erAd

M/F

311.5

0.011

0.03

1nd

0.01

00.01

50.03

40.02

00.07

50.49

70.50

40.03

30.04

01.09

LesserYellowlegs

Chu

rchill

June

Ad

F5

5.2

ndnd

0.02

30.02

3tr

ndtr

0.02

729

.229

.20.04

20.05

20.70

8June

Ad

M5

9.7

0.02

80.02

80.02

00.02

00.05

80.04

40.08

20.24

02.55

2.56

0.07

20.05

20.59

9Bay

ofFun

dyAug

Ad

U1

1.4

0.08

60.08

6nd

ndtr

trnd

tr12

.17

12.17

ndtr

0.80

7Aug

–Oct

HY

U7

16.1

0.01

70.02

0nd

trnd

0.01

60.01

90.03

50.21

40.21

40.01

90.03

41.04

Sho

rt-billed

Dow

itcher

Chu

rchill

June

Ad

F5

6.0

0.02

30.02

3nd

nd0.03

00.13

50.03

30.28

04.37

4.39

0.16

30.53

50.92

8June

Ad

M5

7.3

0.04

00.04

0tr

tr0.37

81.50

0.23

02.48

3.58

3.68

0.45

10.36

43.37

Bay

ofFun

dyAug

–Sept

Ad

M4

11.1

ndnd

ndnd

nd0.08

9nd

0.08

90.88

60.88

60.05

10.06

03.67

Aug

–Sept

Ad

M4

21.1

ndnd

ndnd

ndnd

ndnd

0.46

10.46

1nd

nd0.55

0Lon

g-billed

Dow

itcher

Dun

lin

Quill

Lakes

July

Ad

F5

21.0

0.02

10.02

10.00

70.00

70.01

80.02

2tr

0.05

50.36

80.38

20.00

60.78

30.43

4July

Ad

M5

11.9

0.02

70.02

7tr

tr0.02

30.03

4tr

0.06

6nd

nd0.01

61.19

10.36

7Chu

rchill

June

Ad

M/F

410

.5nd

ndnd

nd0.06

3nd

nd0.06

31.59

1.59

0.117

1.16

1.26

Bay

ofFun

dySept–Oct

HY

M/

F/U

516

.00.04

40.05

1nd

0.00

80.02

40.00

80.02

20.05

80.16

60.17

20.03

90.02

70.32

3

Pacific

coast

March

cAd

F5

7.4

0.04

10.04

10.05

70.05

70.02

2tr

tr0.09

20.50

50.50

50.04

90.011

0.65

7March

dAd

M/F

48.7

0.06

30.10

20.04

30.04

80.81

70.09

72.46

3.40

12.7

13.0

0.24

50.03

12.00

March

cAd

M5

7.5

0.05

20.05

20.05

30.05

30.02

30.03

3tr

0.117

0.50

30.50

30.01

6nd

0.89

6March

cAd

M1

12.7

0.03

20.03

20.05

50.06

20.00

90.00

90.00

80.02

60.20

20.20

20.05

0nd

0.32

7Nov

dAd

M/F

421

.90.09

90.09

90.02

80.02

80.01

80.03

20.01

60.08

00.32

80.38

60.06

7nd

0.36

7


the shorebird carcasses were ΣPCB and ΣDDT in 98%of all samples followed by ΣCHL in 95% of allsamples (Table 2). ΣHCH was detected above tracelevel the least often (61%) of the major organochlorinegroups reported here. Octachlorostyrene was detectedabove trace level in less than 14% of all samples (nd—0.014 μg g−1 lw) and will not be discussed further.

ΣDDT was comprised almost entirely (96%) of p,p′-DDE with the highest ΣDDT concentration (29 μg g−1

lw) found in the pool of adult female lesser yellowlegsfrom Cape Churchill (Table 2). However, ΣDDTconcentrations in excess of 5 μg g−1 lw were found inspring-collected dunlin from the Pacific coast (BoundaryBay), semipalmated plovers and lesser yellowlegs fromthe Bay of Fundy, and lesser yellowlegs, whimbrels andsemipalmated and American golden plovers from CapeChurchill (Fig. 2). p,p′-DDD and/or p,p′-DDT weredetected in more than 50% of the samples but p,p′-DDD + p,p′-DDT exceeded 1 μg g−1 lw only in goldenplovers from Cape Churchill.

Dieldrin was detected in 86% of all samples withthe highest dieldrin concentrations found in thegolden plovers and semipalmated plovers at CapeChurchill (Table 2). ΣCHL was made up mainly ofoxychlordane (33%), trans-nonachlor (24%) andheptachlor epoxide (25%) over all species. Thehighest ΣCHL levels were found in the goldenplovers from Cape Churchill, spring-collected dunlinfrom the Pacific coast (Boundary Bay), and short-billed dowitchers from the Bay of Fundy (Fig. 2).

Concentrations of ΣHCH were generally low(<0.1 μg g−1 lw). β-HCH accounted for about 65% ofΣHCH over all species but averaged 95% in Pacificcoast dunlin. ΣMirex was comprised primarily of mirex(84%) with the highest concentrations found in long-billed dowitchers from Quill Lakes and dunlin fromCape Churchill (Table 2). Tetra- and penta-chlorinatedbenzenes were detected in less than 14% of the samples,whereas hexachlorobenzene (HCB), which averaged94% of ΣCBz, occurred in 82% of the samples atlevels ≤0.1 μg g−1 lw except in late fall-collected dunlinfrom the Pacific coast (Tofino) (Table 2).

ΣPCB concentrations in the majority of sampleswere less than 1 μg g−1 lw but ranged up to 3–4 μgg−1 lw in short-billed dowitchers from the Bay ofFundy and semipalmated plovers from Cape Church-ill. Major PCB congeners found in the shorebirds, thatis, those congeners averaging more than 5% of ΣPCBoverall, included the following, in order of decreasing

Nov

dHY

M/F

619

.70.06

20.06

20.03

90.04

50.01

90.03

70.02

90.10

90.50

80.62

80.22

6nd

0.78

7Dec

cAd

F3

8.8

0.46

70.46

70.08

30.08

30.02

6nd

0.02

60.06

40.19

10.19

10.06

0nd

0.22

6Dec

cHY

M/F

211.5

0.03

30.03

30.03

40.03

40.01

0nd

tr0.01

70.17

70.17

70.01

9nd

0.20

6Sem

ipalmated

Sandp

iper

Chu

rchill

June

Ad

F5

11.8

0.04

40.04

4tr

0.01

20.02

1nd

0.01

30.06

60.24

20.24

60.01

90.02

20.85

2June

Ad

M5

13.7

0.07

40.07

40.00

80.01

20.04

20.02

30.04

20.12

40.34

70.40

10.03

20.05

71.79

Quill

Lakes

July

Ad

M4

29.0

0.02

60.02

60.00

30.00

30.01

80.02

90.00

30.07

70.08

70.117

0.00

40.04

00.41

0July

HY

F2

37.4

0.02

20.03

10.00

30.00

50.01

40.00

8tr

0.03

10.02

10.02

1tr

tr0.16

3Aug

Ad/

HY

M/F

527

.80.03

20.03

2nd

nd0.00

40.00

5tr

0.02

10.03

10.03

10.00

50.03

30.12

9

Aug

HY

M5

19.7

0.03

30.03

3tr

0.00

60.02

10.01

20.00

50.04

10.03

60.03

60.01

50.03

00.08

1Bay

ofFun

dyAug

–Sept

Ad

F5

22.8

0.02

40.02

4nd

nd0.03

00.02

20.01

50.08

00.07

60.07

80.02

10.02

51.11

Aug

–Sept

Ad

M5

15.3

0.06

70.06

70.00

70.01

60.08

30.04

80.05

00.19

30.08

80.09

90.04

20.09

50.35

7

AdAdu

lt,HYhatchyear,Ffemale,

Mmale,

Uun

know

n,nd

notdetected

(nd=<0.00

01μgg−

1wet

weigh

t),trtracevalue(0.000

1≤tr<

0.00

1μgg−

1wet

weigh

t)aCarcass

isdebeaked,defeathered,

dewinged,

andmissing

liver,kidn

ey,somebreastmuscle,

gastro-intestin

altract,andfemurs

bNum

berof

birdsin

pool

cBirds

collected

atTofino

dBirds

collected

atBou

ndaryBay


contribution: 153, 49, 138, 180, 99, 182/187 and 118.However, PCB 49 averaged <1% of ΣPCB in thesamples from the Bay of Fundy compared with 16–32% at the other sampling locations. In the ploversand the shallow probers (i.e. semipalmated sand-pipers, dunlin, whimbrel), the hexa-, hepta- andpentachlorobiphenyl homologs constituted the largestproportion of ΣPCB, in that order. In the deep probers(i.e. godwits, dowitchers) and the yellowlegs, howev-er, the tetra-, hexa- and heptachlorobiphenyl homo-

logs constituted the largest proportion of ΣPCB. Theprominence of the tetra-homolog in the latter groupwas driven mainly by the godwits from Quill Lakesand the lesser yellowlegs from Cape Churchill.

Interspecific comparisons

Statistical interspecific comparisons of adults by genderwere possible only for Cape Churchill where carcassconcentrations of ΣCBz, ΣHCH, ΣCHL, ΣDDT,

N-DUNL-

M/F

D-DUNL-

F

M-DUNL-

M/F

M-DUNL-

F

M-DUNL-

M

M2-

DUNL-M

AMGP-F

AMGP-M

SEPL-F

SEPL-M

HUGO-F

WHIM

-F

WHIM

-M

LEYE-F

LEYE-M

SBDO-F

SBDO-M

DUNL-M/F

SESA-F

SESA-M0

1

2

3

4

Fall Spring

0

5

10

15

2830

Fall Spring

0

1

2

3

8

9

SpringFall

SEPL-F

SEPL-M

BBPL-M/F

GRYE-M/FLE

YE

SBDO-M1

SBDO-M2

SESA-F

SESA-M

SBDO-M

SBDO-M

SESA-M

DUNL-M

/F

SESA-F

DUNL-F

DUNL-M

/F

DUNL-M

DUNL-F

DUNL-M

DDT

PCB

N-DUNL-

M/F

D-DUNL-

F

M-DUNL-

M/F

M-DUNL-

F

M-DUNL-

M

M2-

DUNL-M

Fall Spring

Fall Spring

SpringFall

P

SBDO-M1

SBDO-M2

SESA-F

SESA-M

SBDO-M

SBDO-M

SESA-M

DUNL-M

/F

SESA-F

DUNL-F

DUNL-M

/F

DUNL-M

DUNL-F

DUNL-M

N-DUNL-

M/F

D-DUNL-

F

M-DUNL-

M/F

M-DUNL-

F

M-DUNL-

M

M2-

DUNL-M

Fall Spring

Fall Spring

SpringFall

SBDO-M1

SBDO-M2

SESA-F

SESA-M

SBDO-M

SBDO-M

SESA-M

DUNL-M

/F

SESA-F

DUNL-F

DUNL-M

/F

DUNL-M

DUNL-F

DUNL-M

Pacific Coast

N-DUNL-

M/F

D-DUNL-

F

M-DUNL-

M/F

M-DUNL-

F

M-DUNL-

M

M2-

DUNL-M

Cape Churchill Quill Lakes

Fall Spring

Fall Spring

ΣCH

L (µ

g g-1

lipi

d w

t)ΣD

DT

(µg

g-1

lipi

d w

t)ΣP

CB

(µg

g-1

lipi

d w

t)

SpringFall

Bay of Fundy

SBDO-M1

SBDO-M2

SESA-F

SESA-M

HUGO-F

HUGO-F

LBDO-F

LBDO-M

SESA-M

SBDO-M

SBDO-M

SESA-M

DUNL-M

/F

SESA-F

DUNL-F

DUNL-M

/F

DUNL-M

DUNL-F

DUNL-M

ΣCHL

ΣDDT

ΣPCB

Fig. 2 Concentrations (μg g−1 lipid weight) of organochlorines incarcasses of adult shorebirds from four Canadian locations. AMGPAmerican golden plover, SEPL semipalmated plover, BBPL black-bellied plover, HUGO Hudsonian godwit,WHIM whimbrel, GRYE

greater yellowlegs, LEYE lesser yellowlegs, SBDO short-billeddowitcher, LBDO long-billed dowitcher, DUNL dunl, SESAsemipalmated sandpiper. Gender composition of sample poolsdesignated as: M male, F female, M/F mix of males and females


ΣMirex, dieldrin and ΣPCB could be compared foradult male American golden plovers, semipalmatedplovers, whimbrels, lesser yellowlegs, short-billeddowitchers and semipalmated sandpipers, and for adultfemales of those same species plus Hudsonian godwits.There were significant differences in organochlorine con-centrations among males (Friedman’s test: n=7, pww<0.001, plw<0.003) and females (Friedman’s test: n=7,pww<0.003, plw<0.007) of the various species sampledat Cape Churchill on both a wet weight and lipid weightbasis. On a lipid weight basis, the rankings, fromhighest to lowest overall organochlorine concentra-tions, were as follows: males—semipalmated plover =American golden plover > short-billed dowitcher >semipalmated sandpiper > whimbrel > lesser yellow-legs; females—semipalmated plover > American gold-en plover > whimbrel > short-billed dowitcher > lesseryellowlegs > semipalmated sandpiper > Hudsoniangodwit. Both males and females of the two ploverspecies were ranked with the highest overall organo-chlorine concentrations. Since the pool of dunlin fromCape Churchill was comprised of two male and twofemale birds, they were compared with both the malesand females and were found to rank identically withthe female yellowlegs, and between the male lesseryellowlegs and whimbrels.

Despite their overall ranking, however, male short-billed dowitchers and semipalmated plovers had thehighestΣPCB concentrations at Cape Churchill (Fig. 2).This pattern is repeated in the Bay of Fundy where oneof the pools of male short-billed dowitchers, followedby the mixed pool of black-bellied plovers and the poolof male semipalmated plovers, had the highest ΣPCBconcentrations (Fig. 2). The pool of female lesseryellowlegs at Cape Churchill had an anomalously highconcentration of ΣDDT (29 μg g−1 lw) followed by theAmerican golden plovers and the male semipalmatedplovers (Fig. 2). Again, the pattern is repeated in theBay of Fundy where the pool of lesser yellowlegs,followed by the male semipalmated plovers, had thehighest ΣDDT concentrations (Fig. 2). Of all of theshorebird carcass pools analyzed in this study, the twopools of American golden plovers, two pools ofsemipalmated plovers, two pools of short-billeddowitchers, two pools of whimbrels and one pool offemale semipalmated sandpipers, all from CapeChurchill, as well as one of the early spring pools ofadult dunlin from the Pacific coast (Boundary Bay)ranked as the 10 most contaminated samples, overall.

The 10 lowest ranked samples for organochlorinecontamination included six pools of hatch-year birds,including the two pools of marbled godwits and threepools of semipalmated sandpipers from Quill Lakes,and a late fall pool of dunlin from the Pacific coast(Tofino), in addition to the two pools of adultHudsonian godwits from Quill Lakes and one pool ofmale short-billed dowitchers and the pool of femalesemipalmated plovers from the Bay of Fundy. Ingeneral, the plovers appear to be the most contaminatedgroup of birds, including the pool of immature black-bellied plovers, which ranked as the most contaminatedof the hatch-year birds, whereas the godwits appear tobe the least contaminated group of birds analyzed.

Age/sex comparisons

Five paired sets of data were available for compar-isons of hatch-year with adult birds of a given speciescollected from the same location and time period:black-bellied plovers and lesser yellowlegs from theBay of Fundy, semipalmated sandpipers from QuillLakes, and two sets of late fall dunlin from the Pacificcoast (Table 2). There were no significant differences(Wilcoxon paired sample test; p>0.05) in either wetweight or lipid weight concentrations of ΣCBz,ΣHCH, ΣCHL, ΣDDT, ΣMirex, dieldrin or ΣPCBbetween adult and hatch-year birds.

There were 10 paired sets of data available forcomparisons of male versus female adult birds of agiven species collected from the same location andtime period: lesser yellowlegs, short-billed dow-itchers, whimbrels, semipalmated sandpipers, semi-palmated and American golden plovers fromChurchill, long-billed dowitchers from Quill Lakes,semipalmated plovers and semipalmated sandpipersfrom the Bay of Fundy, and dunlin from the Pacificcoast (Table 2). There were no significant differences(Wilcoxon paired sample test; p>0.05) in either wetweight or lipid weight concentrations of ΣHCH,ΣDDT, ΣMirex, dieldrin or ΣPCB between adultmales and females, but levels of ΣCBz and ΣCHLwere significantly higher in males on both a wet weight(ΣCBz: p<0.03; ΣCHL: p<0.01) and lipid weight(ΣCBz: p<0.04; ΣCHL: p<0.02) basis. When onlythe adult birds from Cape Churchill were analyzed (i.e.all those presumed to be breeding), dieldrin was alsofound to be significantly higher in males (p<0.03) onboth a wet weight and lipid weight basis.


Changes in organochlorine levels over the winter

Adult dunlin from the coast of British Columbia weresampled twice; during late fall and early spring.Comparisons of pools of the same gender or gender

mix showed increased lipid-weight concentrations ofdieldrin and ΣPCB (4-, 5-fold), ΣDDT and ΣCHL(34-, 42-fold), and ΣMirex (136-fold) at BoundaryBay, and less dramatic increases at Tofino (ΣPCB andΣDDT: 3-fold, ΣMirex: 19-fold) over the winter.

Table 3 Concentrations (μg g−1 dry weight) of total mercury (Hg) in livers, and cadmium (Cd), selenium (Se) and arsenic (As) inkidneys, of shorebirds from various Canadian locations, 1990–1992

Species Location Collection period Age Sex Na Liver Kidney

Hg Cd Se As

American Golden Plover Churchill June Ad F 3 – – 4.50 0.06June Ad M 5 0.64 8.46 3.31 –

Semipalmated Plover Churchill June Ad F 5 – – 3.33 1.32June Ad M 5 2.03 5.97 6.29 –

Bay of Fundy Aug–Sept Ad M 5 1.08 3.28 – –Black-bellied Plover Bay of Fundy Aug–Sept Ad M/F 3 1.44 3.28 8.55 –Marbled Godwit Quill Lakes Sept HY F 3 0.49 – 3.21 0.12

Sept HY M/U 3 – 0.34 6.46 –Hudsonian Godwit Churchill June Ad F 5 0.58 11.9 7.00 –

Quill Lakes July Ad F 3 0.22 – 8.78 0.24July–Aug Ad F 3 0.57 43.1 – –

Whimbrel Churchill June Ad F 5 – – 4.00 0.81June Ad M 3 1.30 6.18 3.84 –

Greater Yellowlegs Bay of Fundy October Ad M/F 3 2.45 1.00 5.05 –Lesser Yellowlegs Churchill June Ad F 5 – – 4.80 0.15

June Ad M 5 2.69 1.50 – –Bay of Fundy Aug Ad U 1 2.40 0.77 3.59 –

Aug–Oct HY U 7 2.56 0.60 2.82 –Short-billed Dowitcher Churchill June Ad M 5 1.60 7.35 – –

Bay of Fundy Aug–Sept Ad M 4 1.62 3.96 5.51 –Aug–Sept Ad M 4 – – 5.86 2.16

Dunlin Churchill June Ad M/F 4 1.08 2.16 7.27 –Bay of Fundy Sept–Oct HY M/F/U 5 2.52 1.07 7.11 –Pacific coast Marchb Ad F 5 – – 16.7 4.61

Marchb Ad M 5 1.13 1.68 – –Marchc Ad M/F 4 0.75 3.52 10.7 –Novc Ad M/F 4 0.93 5.10 – –Novc HY M/F 6 1.03 1.43 – –Decb Ad F 3 0.63 1.10 – –Decb HY M/F 2 – – 13.2 5.08

Semipalmated Sandpiper Churchill June Ad F 5 – – 7.38 0.42June Ad M 5 1.37 2.28 7.02 –

Quill Lakes July Ad M 4 – 3.02 9.00 –Aug HY M 5 1.23 0.70 9.47 –

Bay of Fundy Aug–Sept Ad F 5 2.13 1.87 – –

Ad Adult, HY hatch year, F female, M male, U unknowna Number of birds in poolb Birds collected at Tofinoc Birds collected at Boundary Bay


Metals

Data for Hg in livers, as well as Cd, Se and As inkidneys, are presented on a dry weight (dw) basis inTable 3. The mean moisture content (mean±standarderror) for liver was 67%±0.7% (range: 58–77%), andfor kidney, was 67%±1.9% (range: 16–74%). Mercu-ry was detected in all liver samples analyzed for thiselement and concentrations ranged from 0.22 μg g−1

in female Hudsonian godwits from Quill Lakes to2.7 μg g−1 in male lesser yellowlegs from CapeChurchill (Table 3). Where location-age comparisonswere possible (i.e. lesser yellowlegs from the Bay ofFundy, dunlin from the Pacific coast in November),

there was little difference in hepatic Hg levelsbetween adult and immature (hatch year) birdsalthough the adults had slightly lower Hg levels thanthe immature birds (Table 3). There was also littledifference in Hg concentrations in dunlin sampled onthe Pacific coast upon arrival on the overwinteringgrounds in the late fall versus in the early spring priorto migration (Fig. 3). In fact, all of the dunlinsampled, along with the American golden ploversand Hudsonian and marbled godwits, containedrelatively low levels of Hg compared with the otherspecies analyzed, regardless of sampling location(Table 3; Fig. 3). Among the adult birds, the greaterand lesser yellowlegs had the highest hepatic Hg

AMGPSEPL

HUGOW

HIMLEYE

SBDODUNL

SESA0.0

0.5

1.0

1.5

2.0

2.5

3.00

4

8

12

4244

AMPL-F

AMPL-M

SEPL-F

SEPL-MHUGO

WHIM

-F

WHIM

-MLEYE

DUNL

SESA-F

SESA-M0

3

6

9

12

15

18

HUGOSESA

BBPLGRYE

LEYE

SBDO-1

SBDO-2

DUNL-1

DUNL-2

1HUGO

2HUGOSESA

SEPLBBPL

GRYELEYE

SBDOSESA

N-DUNL

D-DUNL

M-DUNL

M2-DUNL

Fall Spring

Fall Spring

Cd

Se

Hg

HUGOHUGO

DUNLDUNL

DUNLDUNL

SBDODUNL

DUNLSBDO

Cape Churchill

- - -I

Se

in K

idne

y (μ

g g-1

dw

)C

d in

Kid

ney

(μg

g-1 d

w)

Hg

in L

iver

(μg

g-1

dw

)

EL

SBDO-1

SBDO-2

DUNL-1

DUNL-2

Pacific CoastQuillLakes

1HUGO

2HUGOSESA

Bay of Fundy

N-DUNL

D-DUNL

M-DUNL

M2-DUNL

Fall Spring

Fall Spring

Cd

Se

Hg

HUGOHUGO

DUNLDUNL

DUNLDUNL

SBDODUNL

DUNLSBDO

Fig. 3 Concentrations (μg g−1 dry weight) of mercury in liver, and cadmium and selenium in kidneys of adult shorebirds from fourCanadian locations. See Fig. 2 for species codes


concentrations, both on the breeding grounds at CapeChurchill and in the fall on the Bay of Fundy (Fig. 3),although the samples of immature lesser yellowlegsand immature dunlin from the Bay of Fundy also hadrelatively high Hg levels (Table 3). For the otherspecies, there did not appear to be any consistentinterspecific pattern for Hg levels, nor were there anygeographical differences in Hg levels (Fig. 3).

Selenium, Cd and As were detected in all kidneysample pools analyzed for these elements. Renal Seconcentrations varied from 3.2 to 16.7 μg g−1 dw andexhibited little interspecific or seasonal variation,although levels tended to be higher in dunlin sampledfrom the Pacific coast (Table 3; Fig. 3). Where ageand sex comparisons were possible, there were noconsistent differences in Se levels, although thepooled sample of adult male semipalmated sandpipershad renal Se levels which were almost two-foldhigher than the adult females. Renal Cd levels variedfrom 0.34 μg g−1 dw in immature marbled godwits to43 μg g−1 dw in adult Hudsonian godwits collected atQuill Lakes (Table 3). Concentrations in adult birdsvaried among species with the highest Cd concen-trations in Hudsonian godwits from Quill Lakes andCape Churchill, and the lowest levels in greater andlesser yellowlegs from Cape Churchill and Bay ofFundy, although dunlin and semipalmated sandpipersfrom Cape Churchill and semipalmated sandpipersfrom Bay of Fundy were also relatively low as weresome of the dunlin samples from the Pacific coast(Fig. 3). There did not appear to be any greatgeographical variation in Cd levels for any givenspecies. Renal Cd concentrations were higher inadults than in immature birds sampled concurrently(Table 3). Renal As concentrations varied from0.06 μg g−1 dw in golden plovers from CapeChurchill to 4.6 and 5.1 μg g−1 in the two dunlinsamples from the Pacific coast (Table 3). Nointraspecific geographical comparisons were possible.

Discussion

Effects of foraging strategy, migratory habits and ageon contaminant exposure

Differences in contaminant levels among shorebirdspecies may be related to their feeding ecology, i.e.

their diet, foraging behaviour and foraging habitat.Birds which feed on aquatic vegetation are generallyless contaminated than those feeding at higher trophiclevels (Braune and Malone 2006). Therefore, the highproportion of sago pondweed (Potamogeton pectina-tus) tubers ingested by Hudsonian and marbledgodwits collected at Quill Lakes (Alexander et al.1996) may explain the low contaminant concentra-tions in those species. Long-billed dowitchers andsemipalmated sandpipers, which fed primarily oninvertebrates (i.e. larval chironomids) at Quill Lakes(Alexander et al. 1996), contained higher contaminantresidues. The highest concentrations of organochlor-ines were found in lesser yellowlegs, semipalmatedplovers and American golden plovers (Table 2; Fig. 2),all mainly visual predators that obtain prey from thesurface (Johnson and Connors 1996; Nol and Blanken1999; Tibbitts and Moskoff 1999). Plovers, in partic-ular, favour relatively large prey such as polychaetes,bivalves, snails and shrimp, which may have accumu-lated contaminants from lower trophic levels. Even inthe Bay of Fundy, where migrant waders feed primarilyon the abundant burrowing amphipod, Corophiumvolutator (Hicklin 1987), both semipalmated ploversand black-bellied plovers also take large numbers ofpolychaetes (e.g. Nereis sp, Glycera sp.) and othermacro-invertebrates (Napolitano et al. 1992; Paulson1995). Napolitano et al. (1992) reported higher meanDDE levels and maximum individual PCB levels insemipalmated plovers than in sandpipers or dowitchersin the Bay of Fundy (Table 4).

Hepatic Hg concentrations ranged from 0.2–0.6μg g−1

dw in the godwits to 2.4–2.7 μg g−1 dw in theyellowlegs (Table 3), again reflecting the differentfeeding habits of these species, from the godwit’s dietof aquatic vegetation to the inclusion of small fish inthe diet of yellowlegs. In contrast, the yellowlegs hadrelatively low renal concentrations of Cd whereas theHudsonian godwits had the highest Cd concentrations(Table 3; Fig. 3), possibly reflecting the tendency foraquatic plants to assimilate Cd more readily than biota(Peakall and Burger 2003; Mason et al. 2000).

Foraging microhabitat may also play a role inpotential exposure to contaminants. Heavy metalprofiles of sediment cores from Chesapeake Bayshowed that concentrations of lead, as well as copperand zinc were higher at depths of approximately 5 cmthan more recently deposited sediments (Owens andCornwell 1995). White et al. (1983) found that long-


Tab

le4

Com

parisonof

concentrations

(μgg−

1wet

weigh

t)of

organo

chlorinesandtotalHgin

who

lebo

dies

ofshorebirds

from

otherCanadianstud

ies

Species

Location

Collection

period

PCBsa

DDE

HCB

Dieldrin

References

Sem

ipalmated

Plover

Central

Arctic

1980

–85

1.14

0.32

0.01

30.21

Barilet

al.(198

9)RankinInlet

1982

–83

1.06

1.11

0.18

Cou

rtet

al.(199

0)RankinInlet

1991

–94

0.40

(0–2

.06)

0.50

(0.10–

1.07

)0.01

(0–0

.02)

0.02

(0–0.11)

John

ston

eet

al.(199

6)CapeChu

rchill

1991

0.14

,0.42

0.14

,1.01

0.00

4,0.00

70.11,0.26

Thisstud

yAtlantic

1980

–85

0.01

30.06

3Barilet

al.(199

0)Bay

ofFun

dy19

890.30

(0.12–

0.67

)0.02

7(0.012

–0.038

)Napolitano

etal.(199

2)Bay

ofFun

dy19

910.12

,0.30

0.16

,1.4

0.00

5,0.00

70.00

8,nd

Thisstud

ySem

ipalmated

Sandp

iper

Central

Arctic

1980

–85

0.86

0.04

0.02

20.02

Barilet

al.(198

9)RankinInlet

1982

–83

0.21

0.11

0.04

Cou

rtet

al.(199

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billed dowitchers accumulated more DDE thanAmerican avocets (Recurvirostra americana) or west-ern sandpipers (Calidris mauri), and suggested thatspecies which probe deeply into the substrate may beexposed to higher levels of contaminants depositedseveral decades ago when organochlorine pesticideswere more widely used. However, Hui and Beyer(1998) found that digesta of willets (Catoptrophorussemipalmatus), which forage primarily by probingsediments with their long, open bills, contained onlyabout 3% sediment compared with an estimated 29%sediment in the digesta of black-bellied plovers withtheir shorter bills, leading those authors to suggest thatsediment ingestion, which may greatly affect a bird’sexposure to environmental contaminants in sediment,may not necessarily be linked to bill length or probingbehaviours. The results of our study also do not supportthe hypothesis that longer-billed species which probedeeper into the substrate (e.g. dowitchers, godwits) aresubject to greater contaminant exposure. In fact, thehighest overall organochlorine concentrations werefound in the plovers, with their short bills, and the lesseryellowlegs, which do not generally forage by probing.Mercury concentrations, too, were generally higher inthe yellowlegs and shorter-billed sandpipers and plovers(Fig. 3) and, although the Hudsonian godwits had thehighest Cd levels, overall, diet composition seems toprovide a better explanation for the contaminant levelsfound across species. However, the relationshipbetween prey availability and bill length, in additionto differences in sediment ingestion and local contam-inant profiles, is likely to be quite complex.

Contaminants in migratory species are acquiredthroughout the year and hence interspecific differ-ences may also arise from differences in exposure inareas other than those sampled. Elevated levels oforganochlorines, such as DDT, in American goldenplovers may have been acquired on their winteringgrounds. In Argentina, the extensive agricultural areasthat have replaced the grasslands favoured by thisspecies (Johnson and Connors 1996) receive heavypesticide treatments. The closely-related black-belliedplover tends to feed along the coast rather than infields (Paulson 1995). The difference in overwinteringareas is reflected by the ΣDDT:ΣPCB ratio of theAmerican golden plover (16) versus the black-belliedplover (0.3) in this study. No data are available forspring migrants but birds collected in the autumn inthe Bay of Fundy contained relatively low residues of

DDT and DDE (Table 2). The influence of contam-inant exposure during the annual migratory cycle ofNearctic shorebirds will be explored in more detail ina subsequent manuscript.

Age can also be a factor in the accumulation ofcontaminant residues although age-related differencesdepend on the contaminant and the species beingstudied (Burger and Gochfeld 2002). Although intra-specific age comparisons by location did not indicateany obvious differences in this study, Hudsonian andmarbled godwits collected at Quill Lakes were bothfeeding extensively on sago pondweed tubers, but theadult Hudsonian godwits had extremely high, and theimmature marbled godwits extremely low, levels ofCd (Table 3). Although the Hudsonian godwits mayhave accumulated Cd elsewhere, this is most likely anage effect. Cadmium has been shown to accumulatewith age in curlew sandpipers (Calidris ferruginea)and dunlin (Blomqvist et al. 1987).

The suite of species sampled at each samplinglocation represents a variety of feeding strategies andmigratory habits, and includes most of the speciesknown to occur at those sites in abundance. Surveysof contaminants in shorebird migrants in Central andnorthern South American countries found no evidenceto suggest that birds were acquiring increasedcontaminant loads while overwintering in those areas(Banasch et al. 1992) although Fyfe et al. (1990)found some evidence to suggest that exposure ofoverwintering birds to contaminants was still occur-ring in Peru and Ecuador during the early 1980s.Capparella et al. (2003), however, suggest thatwidespread contamination of avifauna with organo-chlorine pesticides has not occurred in South Americaand that contaminated Neotropical migratory birdsthat overwinter in South America are acquiringcontaminants either on their North American breedinggrounds or along their migratory pathway. A study onmigrating ospreys (Pandion haliaetus) by Elliott et al.(2007) also concluded that DDE concentrations andDDE:DDT ratios in osprey eggs were more closelyrelated to breeding ground exposure in the PacificNorthwest rather than specific wintering sites inMexico or Central/South America.

Contaminant uptake at collection sites

The extent to which concentrations in shorebirdsreflect contamination of the collection site is influ-


enced by the period of residency and changes in bodyfat. Birds collected at Cape Churchill in late June hadprobably arrived on the breeding grounds in late May.Semipalmated sandpipers are known to be present forabout three to four weeks before laying their eggs inmid to late June (Gratto and Cooke 1987) and becauseof the close link to peak insect hatch (Holmes andPitelka 1968), breeding in other arctic waders is likelyto have similar timing. Shorebirds at Cape Churchillfeed mainly on terrestrial insect larvae, occasionallysupplemented by marine invertebrates (Baker 1977).DDT was sprayed for mosquito control around FortChurchill between 1947 and 1964, after which avariety of biota were sampled in 1967 from both thesprayed and unsprayed areas to analyzed for DDTresidues (Brown and Brown 1970). Mean ΣDDTconcentrations in the fat of lesser yellowlegs andsemipalmated plovers ranged from 3.3 and 5.0 μg g−1,respectively, in the unsprayed areas to 20 and 52 μg g−1,respectively, in the sprayed area (Brown and Brown1970). Given that the field half-life of DDT is 2–15 years (Augustijn-Beckers et al. 1994), one couldreasonably expect the effects of the spraying to remaindetectable in the environment even after severaldecades. Therefore, the choice of feeding locationaround Cape Churchill may have had an effect on theΣDDT levels found in the birds, and may provide apartial explanation for the wide range of concentrations(0.25–29 μg g−1) found (Table 2). Concentrations ofPCBs, DDE, hexachlorobenzene (HCB) and dieldrinfound in semipalmated plovers, American goldenplovers, semipalmated sandpipers and dunlin fromCape Churchill in this study were not much differentfrom levels measured in those same species fromRankin Inlet, Northwest Territories (now Nunavut) andthe central Arctic in other Canadian studies (Table 4).Although not consistent for all organochlorine groupsor across all species, females of several species hadlower concentrations of many organochlorines (Table 2)which suggests that lipophilic contaminants were beingeliminated into the eggs. Given the period of samplingat Cape Churchill (June 12–28), it cannot be assumedthat all females had laid eggs prior to being collected.

At Quill Lakes, migrants start to pass through inJuly but the juvenile marbled godwits were probablylocal birds. Contaminant concentrations in marbledgodwit and long-billed dowitcher from Quill Lakeswere lower than residues found in these species at otherinland sites in North America (DeWeese et al. 1986;

Hubbard and Schmitt 1988). However, White et al.(1983) reported mean DDE levels of up to 5.7 μg g−1

ww in long-billed dowitchers collected along the southTexas coast in 1979–80.

Stopovers in the Bay of Fundy have durations of 1to 3 weeks, during which time the birds build up highlevels of body fat (Hicklin 1987). Hicklin and Smith(1979) documented the importance of the amphipod,Corophium volutator, to migrant waders in the Bay ofFundy. No DDT (or its metabolites) nor PCBs werefound in lipid extracts of Corophium sampled in thisarea (Napolitano and Ackman 1989). This is reflectedin the low concentrations of organochlorines inspecies such as the semipalmated sandpiper thatspecialize on this food source (Napolitano et al.1992). Concentrations of PCBs, DDE, HCB anddieldrin found in semipalmated plovers, semipalmatedsandpipers and short-billed dowitchers from the Bayof Fundy in this study were generally comparable tolevels measured in those same species collected fromthe Atlantic region and the Bay of Fundy in otherstudies, although some sample pools of plovers anddowitchers from our study had somewhat higherlevels (Table 4). Concentrations of DDE and PCBs inblack-bellied plovers sampled from the Bay of Fundywere similar to levels reported by Schick et al. (1987)for plovers wintering in western Washington state in1981 although HCB levels in the Bay of Fundy birdswere one to two orders of magnitude lower.

Western dunlin begin to arrive at their Pacific coastwintering grounds at Boundary Bay and Tofino in lateSeptember through mid-October and remain thereuntil April–early May (Warnock and Gill 1996).Although there did not appear to be any obviouschanges in Hg or Cd levels between late fall and earlyspring birds, organochlorine concentrations did in-crease in dunlin overwintering at Boundary Bay andTofino. The pattern of higher HCH concentrations andthe higher β-HCH:ΣHCH ratio found in the Pacificcoast birds is in agreement with the pattern of HCHratios calculated by Braune (2007) for seabirds over arange of geographic locations and may be due tohistorically high use of HCH in countries in PacificAsia. Although no data on the diet of dunlin atBoundary Bay or Tofino are available, dunlin else-where on the Pacific coast feed mainly on intertidalinvertebrates, including Corophium sp., Diptera lar-vae and polychaetes (Buchanan et al. 1985). Ingeneral, either decreases or no changes in dunlin


weight (and lipids) have been recorded over thewinter (Pienkowski et al. 1979; Buchanan et al.1985). Lipid content data for dunlin from our study,which ranged from 8.8–22% in November–Decemberto 7.4–13% in March (Table 2), would corroboratethose observations. Given that organochlorines arelipophilic, a potential decrease in body lipid contentover the winter may partially explain some of theincreases recorded for organochlorine concentrationsin this study. Increases in mean levels of DDE andPCBs were also observed in dunlins overwintering inwestern Washington state (Schick et al. 1987; Custerand Myers 1990). Mean residue levels of DDE andPCBs in carcasses of dunlin collected from Wash-ington state during 1975–85 ranged from 0.02 to0.9 μg g−1 ww and 0.06 to 0.50 μg g−1 ww,respectively (Schick et al. 1987) and were similar tolevels found in our study for Pacific coast dunlin(DDE: 0.02–1.1 μg g−1 ww, ΣPCB: 0.02–0.17 μg g−1

ww). Higher mean DDE and PCB carcass concen-trations were found for dunlin in California (DDE:2.4 μg g−1 ww; Custer and Myers 1990) and Texas(DDE: 3.15 μg g−1 ww, PCBs: 1.2 μg g−1 ww; Whiteet al. 1980). Likewise, carcass concentrations of DDEand PCBs in greater and lesser yellowlegs in ourstudy were lower than levels found in those samespecies in Texas (White et al. 1980).

Levels of most trace elements were within orbelow the ranges reported in other shorebirds in NorthAmerica (see White et al. 1980; Baril et al. 1989;Custer and Myers 1990; Hui 1998; Hui et al. 2001;McFarland et al. 2002). However, exposure tocontaminants may be highly site specific and,therefore, individuals of many migrating/winteringwaders may be exposed to significantly differentsuites of contaminants (Hui 1998; McFarland et al.2002; Norris et al. 2007). Although Chou et al. (2003)did not find high levels of Cu, Cd or Zn in the Bay ofFundy’s ecosystem, Hung and Chmura (2006) identi-fied Hg contamination as a priority concern in the Bayof Fundy due to elevated levels observed in fish, birdsand wildlife. Therefore, locally elevated levels of Hg,in addition to the foraging strategies already discussed,may have contributed to the Hg patterns observed inthe birds (Fig. 3). During the 1980’s, elevated levels ofSe in birds from saline evaporation ponds receivingagricultural drainage waters in California’s Central Valley(Kesterson Reservoir) were reported by Ohlendorf et al.(1990), but Se concentrations at Quill Lakes, which are

moderately saline, as well as other sites in our study,were relatively low and comparable to levels measuredin birds from a reference site (Volta Wildlife Area) inthe California study.

Although there did not appear to be any obviouschanges in Hg or Cd levels between late fall and earlyspring dunlin, adult dunlin overwintering in theBoundary Bay area had the highest Cd levels (3.5and 5.1 μg g−1 dw) of the dunlin sampled on thePacific coast in this study. McFarland et al. (2002)suggested that exposure of migratory shorebirds to Cdoccurs at major estuarine areas along the Pacific coastincluding Boundary Bay. Thomas and Bendell-Young(1998) suggested that a possible source of Cd to theBoundary Bay area may have been from use of afungicide, whose active ingredient is cadmium chlo-ride, and which was extensively used on golf coursegreens and agricultural fields in the area. Pacific coastdunlin overwintering at Tofino had the highest Aslevels (4.6 and 5.1 μg g−1 dw) measured in this study.However, the dunlin sampled from Boundary Baywere not analyzed for As, so it is difficult todetermine if the higher As levels are a localgeographical effect or a species effect. Dunlin feedprimarily in coastal marine and intertidal areas(Warnock and Gill 1996), and As is naturally elevatedin the marine environment (Eisler 1988). Similarly, Seis typically higher in marine organisms than thosefrom freshwater ecosystems (Ohlendorf 2003). There-fore, the relatively higher levels of As and Se found inthe dunlin compared with other species in this studymay be a natural result of their foraging habitat.

Toxicological significance

Organochlorines

There has been little experimental work on the toxiceffects of organochlorines or trace elements in shore-birds but adult mortality due to organochlorine poison-ing has been recorded. Two long-billed curlews founddead in Oregon in the early 1980s were diagnosed withorganochlorine poisoning, one due to dieldrin, the otherdue to chlordane (Blus et al. 1985). Diagnostic levelsfor carcasses have not been determined for birds, ratherbrain or egg concentrations are generally used todetermine critical threshold levels. However, Wursteret al. (1965) suggested ΣDDT levels of >30 μg g−1

ww in carcasses of a variety of passerines and


woodpeckers as a minimum lethal threshold. Themaximum ΣDDT levels found in shorebird carcassesin this study were 5% of the lethal threshold suggestedby Wurster et al. (1965). Morrison and Kiff (1979)found little change in eggshell thickness since theadvent of DDT use in 1947 and the 1960–70s in any ofthe 31 shorebird species surveyed, and suggested thatshorebirds are not particularly sensitive to DDE-induced eggshell-thinning. Peakall (1996) suggestedthat brain levels of dieldrin associated with lethality inbirds were 10 μg g−1 ww and that 4–5 μg g−1 wwallowed for a considerable safety margin. Although notdirectly comparable, the maximum levels for dieldrin(0.69 and 0.89 μg g−1 ww in American golden plovercarcasses) were less than 25% of the conservative brainthreshold value, but most of the carcass dieldrin levelsmeasured in this study were <0.03 μg g−1 ww. Themaximum values for heptachlor epoxide (0.63 μg g−1

ww) and oxychlordane (0.28 μg g−1 ww), both ofwhich were again found in American golden plovers,were both less than 10% of the suggestedcorresponding critical brain levels (8 and 5 μg g−1

ww, respectively; Wiemeyer 1996), and maximummirex levels (0.13 and 0.15 μg g−1 ww in long-billeddowitcher carcasses) were three orders of magnitudelower than the 200 μg g−1 ww lethal brain thresholdsuggested by Wiemeyer (1996). It is difficult to assesscritical values for PCBs due to the large number andvariable toxicities of the congeners. However, the max-imum value for ΣPCB in this study was 0.41 μg g−1

ww, which is <1% of the brain levels associated withlethality (75–300 μg g−1 ww) in a variety of birdspecies, and about 5% of egg PCB levels associatedwith reduced reproductive success (8–25 μg g−1 ww)in a variety of bird species (Hoffman et al. 1996).Hence, concentrations of organochlorines in shorebirdcarcasses appear to be below levels associated withlethality. However, sublethal effects are likely atthreshold levels much lower than those associated withacute toxicity. As well, organochlorines may be sud-denly released into the bloodstream by rapid metabo-lism of stored lipids and, therefore, the potential toxicitymay change dramatically in energetically-stressed birds.

Trace elements

Based on a review of the literature, Thompson (1996)suggested that hepatic Hg levels in excess of 20–30 μg g−1 ww are harmful or lethal to nonmarine

birds. This is over an order of magnitude greater thanthe highest Hg concentrations reported in this study.Moreover, shorebirds are largely marine and are,therefore, likely to be more tolerant to mercury(Thompson 1996). Cadmium is considered toxic atkidney levels in excess of 100 μg g−1 ww (Furness1996), also considerably more than those levels foundin any of the shorebirds sampled in this study, even theanomalously high value (13.8 μg g−1 ww) for theHudsonian godwits from Quill Lakes. Arsenic concen-trations are usually low (<1 μg g−1 fresh weight) inmost living organisms (Eisler 1988). The highest renalAs levels (1.3 and 1.6 μg g−1 ww) in this study werefound in two dunlin samples from the Pacific coast(Tofino area). However, since nearly all of the As intissues of marine animals is in the form of nontoxicarsenobetaine (Neff 1997), As poses a low risk to birdsfeeding in the marine environment. Although Se is anessential element, high dietary levels of selenium havebeen associated with reproductive problems in birds(Ohlendorf et al. 1986). Background concentrations ofSe in bird livers are generally <10 μg g−1 dw(Ohlendorf 2003). Assuming that Se concentrations inkidneys are somewhat higher than those in livers ofbirds from Se-normal areas, and similar (i.e. 1:1 ratioof Se in liver and kidney) in Se-contaminated areas(Ohlendorf 2003), dunlin from the Pacific coast ofCanada were the only species to have Se residue levelsin excess of background levels but no species exceededthe threshold level of 10 μg g−1 ww suggested byHeinz (1996) to be associated with sublethal toxiceffects in birds.

Summary

Of the 12 shorebird species sampled from fourCanadian locations, the plovers appear to be the mostcontaminated with organochlorines, whereas the god-wits appear to be the least contaminated. Given that theplovers have short bills and the godwits have longerbills, diet composition seems to provide a betterexplanation for contaminant exposure rather than billlength or probing behaviours. Due to the use of pooledsamples, we have no information regarding the vari-ability in contaminant levels among individuals. How-ever, based on the concentrations measured, there seemsto be no indication that contaminants were adverselyaffecting the shorebird species sampled in this study.


Acknowledgements We would like to thank Martin Gebauer(Enviro-Pacific Consulting, Vancouver), Stuart Alexander(CWS, Saskatoon) and Andy Didyk (University of NewBrunswick, Fredericton) for collecting the samples, MichaelKassera and other staff of NWRC’s national specimen bank forpreparation of the tissues, Ewa Neugebauer for the metalanalyses, and Guy Morrison and Cheri Gratto-Trevor for helpwith aging and sexing some of the birds. Comments from AlainBaril, John Elliott, Cheri Gratto-Trevor and an anonymousreviewer on earlier drafts of this manuscript are gratefullyacknowledged.

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Environmental contaminants in Canadian shorebirds

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