accumulation of environmental contaminants in wood duck valdez veliz sánchez severiche
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Accumulation of Environmental Contaminants in Wood Duck(Aix sponsa) Eggs, with Emphasis on Polychlorinated
Dibenzo-p-Dioxins and Polychlorinated Dibenzofurans
T. P. Augspurger K. R. Echols P. H. Peterman T. W. May
C. E. Orazio D. E. Tillitt R. T. Di Giulio
Received: 18 February 2008 / Accepted: 5 July 2008 / Published online: 26 August 2008
US Government 2008
Abstract We measured polychlorinated dibenzo-p-diox-
ins (PCDDs), polychlorinated dibenzofurans (PCDFs),polychlorinated biphenyls (PCBs), organochlorine pesti-
cides, and mercury in wood duck (Aix sponsa) eggs
collected near a North Carolina (USA) bleached kraft paper
mill. Samples were taken a decade after the mill stopped
using molecular chlorine. Using avian toxic equivalency
factors, 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity
equivalent (TEQ) concentrations were 130 pg/g fresh wet
weight in eggs (n = 48) collected near the mill in 2002
2005 and were significantly higher than those from a ref-
erence site (\1 pg/g) 25 km away. Geometric mean wood
duck egg TEQs (6 pg/g) were one-fifth those measured at
this site prior to the cessation of molecular chlorine
bleaching. Concentrations of mercury in wood duck eggs
from nests of the Roanoke River sites ranged from 0.01 to
0.14 lg/g (geometric mean, 0.04 lg/g) and were signifi-
cantly higher than those from the reference site, where
concentrations did not exceed 0.04 lg/g (geometric mean,
0.02 lg/g). All concentrations were lower than those
associated with adverse effects in birds. The congener
profiles, lack of contamination in reference site eggs, and
decline in contaminant concentrations after process chan-
ges at the mill provide strong evidence that mill dischargesinfluenced contamination of local wood duck eggs. Col-
lectively, the results indicate that the wood duck is an
effective sentinel of the spatial and temporal extent of
PCDD, PCDF, and mercury contamination.
Introduction
The avian egg is frequently used to investigate pollutant
effects on wild birds and monitor pollutant trends in the
environment (Peakall and Boyd 1987; Furness 1993). Eggs
are an important route of chemical elimination for female
birds, particularly for highly lipophilic compounds, and
measurement of contaminants in eggs allows comparison
of maternally deposited doses to those associated with
toxicological effects in field and lab investigations. Colo-
nial waterbirds are frequent subjects of such assessments
because of their high trophic status and the ease with which
large numbers of eggs and corresponding data on produc-
tivity and health of sibling embryos can be collected. The
value of using colonial waterbird reproductive outcomes,
deformity rates, and contaminant accumulation in inte-
grated pollutant assessments has been demonstrated in the
Great Lakes (Fox et al. 1991), the North American Atlantic
and Gulf coasts (Blus 1982; Custer et al. 1983), and Europe
(Bosveld et al. 1995). When the geographic scope of
assessment precludes the use of colonial waterbirds, the
ability to induce other species to nest in artificial structures
can provide some of the same monitoring benefits by
establishing home ranges at the area of interest (to increase
the time spent foraging in that area) and increasing the
number of samples and ease of obtaining them.
T. P. Augspurger (&)
U.S. Fish and Wildlife Service, 551-F Pylon Drive, Raleigh,NC 27606, USA
e-mail: [email protected]
T. P. Augspurger R. T. Di Giulio
Integrated Toxicology Program, Nicholas School of the
Environment and Earth Sciences, Duke University, Box 90328,
Durham, NC 27708, USA
K. R. Echols P. H. Peterman T. W. May
C. E. Orazio D. E. Tillitt
U.S. Geological Survey, Columbia Environmental Research
Center, 4200 New Haven Road, Columbia, MO 65201, USA
123
Arch Environ Contam Toxicol (2008) 55:670682
DOI 10.1007/s00244-008-9199-1
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Passerines such as tree swallows (Tachycineta bicolor),
house wrens (Troglodytes aedon), and European starlings
(Sturnus vulgaris) will occupy nest boxes and are used in
pollutant monitoring (Custer et al. 2002, 2003, 2005;
Arenal et al. 2004; Echols et al. 2004; Neigh et al. 2006;
Maul et al. 2006; Papp et al. 2007). Artificial nest struc-
tures for raptors such as great horned owls (Bubo
virginianus), osprey (Pandion haliaetus), and Americankestrels (Falco sparverius) have also been used for con-
taminant assessments (Lincer and McDuffie 1974; Henny
et al. 1991; Steidl et al. 1991; Strause et al. 2007). Wood
ducks (Aix sponsa) will nest in boxes intended to mimic
natural cavities, and they have been used in wetland pol-
lutant studies (Blus et al. 1993; Beyer et al. 1997;
Kennamer et al. 2005). Wood ducks are useful models for
pollutant assessments because of their wide geographic
distribution in North America, use of artificial nest boxes,
large clutch size, and well-documented breeding biology
and foraging ecology (Hepp and Bellrose 1995). The first
use of wood ducks in polychlorinated dibenzo-p-dioxins(PCDDs) and polychlorinated dibenzofurans (PCDFs) field
studies indicated that the species was sensitive to these
pollutants (White and Hoffman 1995). That led others to
use wood ducks in field assessments of dioxin-like com-
pounds (Beeman and Augspurger 1996; Custer et al. 2002;
Williams 2004). We report contaminant accumulation and
reproductive outcomes in wood duck eggs from an eastern
North Carolina hazardous waste site.
The Roanoke River between Plymouth, North Carolina,
and Albemarle Sound is contaminated by PCDDs and
PCDFs from a pulp and paper mill. Although the mill
virtually eliminated PCDD and PCDF discharge in the
mid-1990s, these contaminants persist in sediments and
biota. Prior measurement of pollutants in wood duck eggs
downstream of this source revealed 2,3,7,8-tetrachlo-
rodibenzo-p-dioxin (TCDD) toxic equivalents (TEQs) up
to 82 pg/g fresh wet weight based on U.S. Environmental
Protection Agency (USEPA 1989) toxic equivalency fac-
tors (TEFs) (Beeman and Augspurger 1996). Because those
samples were taken prior to mill process changes, this
contemporary assessment provides the first application of
wood duck eggs in monitoring PCDD and PCDF trends
over time. Also, the current assessment includes a broader
area than that evaluated in the previous study, including
Welch Creek, a tributary to the Roanoke River which
received mill effluent from 1957 to 1987, and the Eastmost
River, a distributary channel where slower flow favors
pollutant deposition.
In addition to PCDDs and PCDFs, mercury, organo-
chlorine pesticides, and PCBs were included in the current
assessment. Mercury, from a now closed chlor-alkali plant
at the mill, is a site-related bioaccumulative pollutant
which has been implicated in avian reproductive
impairment elsewhere (Thompson 1996). Organochlorine
pesticides and PCBs have not been detected at levels of
concern in fish and sediments from the Roanoke River, but
these chemicals have not been previously measured in the
regions birds. Thus, a subset of wood duck eggs was
analyzed for organochlorine pesticides and PCBs to con-
firm the expected low concentrations.
Methods
Sample Collection
Ten to 17 nest boxes were installed at each of three loca-
tions downstream of the mill: Welch Creek, the Roanoke
River main stem, and the Eastmost River (Fig. 1). During
the breeding seasons from 2002 to 2005, nest boxes were
checked for nest initiation beginning in February and then
every 710 days. One or two fresh eggs per nest box were
collected for contaminant analyses under state and federalpermits. Nests were revisited through the breeding season
to determine clutch size (number of eggs laid, including
those removed for analyses) and percentage hatch
(excluding those removed for analyses). Eggs that failed to
Fig. 1 Location of wood duck nesting boxes on Welch Creek
(squares), Roanoke River (circles), and Eastmost River (triangles)
installed downstream from a pulp and paper mill in Plymouth, North
Carolina, USA, to monitor PCDDs and PCDFs in eggs
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hatch were collected for examination. Eggs were also
collected for analyses from nest boxes at a reference site,
Pocosin Lakes National Wildlife Refuge, about 25 km
southeast of the study area.
Eggs were weighed to the nearest 0.01 g and their length
and breadth were measured with calipers to the nearest
0.1 mm. Shells were gently cleaned with distilled water. A
stainless-steel scalpel, rinsed with acetone, nitric acid, anddistilled water, was used to score each eggshell at its
equator, and egg contents were collected into I-Chem
Research glass jars with Teflon-lined lids.
Analytical Chemistry
The U.S. Geological Surveys Columbia Environmental
Research Center (Columbia, MO, USA) analyzed contents
of 63 eggs for the 2,3,7,8-substituted PCDDs and PCDFs
and mercury. Nine of these samples were also analyzed for
PCB congeners and organochlorine pesticides.
A mixture of15 13C-labeled PCDDs and PCDFs surrogateswas added to all samples, including quality assurance samples
(blanks and chicken egg matrix spikes), before extraction to
monitor recoveries through the cleanup procedures. Also,
surrogates consisting of PCB 029 (2,4,5-trichlorobiphenyl),
PCB 155 (2,20,4,40,6,60-hexachlorobiphenyl), and PCB 204
(2,20,3,4,40,5,6,60-octachlorobiphenyl) were added to the
subset of samples analyzed for PCBs prior to extraction.
Similarly, p,p0-DDD-d8 was added to the subset of samples
analyzed for organochlorine pesticides prior to extraction to
gauge method recovery. Mercury recovery in samples was
assessed by the preparation and analysis of inorganic and
organic mercury spikes and mercury certified reference
tissues.
For organic compound analyses, egg contents were
dehydrated by the addition of anhydrous sodium sulfate
and extracted with dichloromethane. For analysis of
PCDDs, PCDFs, and congener specific PCBs, extracts were
subjected to acid- and base-treated silica gels and adsorbent
chromatography on activated silica gel. Extracts were
further purified by high-performance size-exclusion chro-
matography and fractionated on high-performance porous
graphitic carbon into separate fractions for analyses of 17
PCDDs and PCDFs and 1-4 ortho-chlorinated PCB
congeners.
During analyses, 13C-labeled 1,2,3,4-TCDD and
1,2,3,7,8,9-hexachlorodibenzo-p-dioxin (HxCDD) were
added to the PCDD and PCDF extracts as instrument
internal standards. The PCDFs and PCDDs were quantified
by gas chromatography/high-resolution mass spectrometry
(GC/HRMS) on either of two systems: in 20022003, a
Hewlett Packard (Wilmington, DE, USA) 5890A GC with
a 50 m 9 200 lm 9 0.11 lm Ultra-2 (HP) capillary col-
umn interfaced to a VG 70-AS HRMS (Micromass, UK)
was used; samples from 200405 were analyzed with an
Agilent (Wilmington, DE, USA) 6890 N GC with a
30 m 9 150 lm 9 0.1 lm BPX5 (SGE, Austin, TX,
USA) capillary column interfaced to an Autospec M
HRMS (Micromass) (Peterman 2006). A calibration curve
describing the response of each native congener to that of a
labeled internal standard congener was used directly in the
calculations, and its range of values was determined in thecalibration procedure. Column performance was verified
by analyzing standards of individual components and
observing the chromatographic resolution of the TCDDs,
HxCDDs, and hexachlorodibenzofurans (HxCDFs). Simi-
larly, relative retention times for other congeners were
evaluated with respect to labeled analogues. The efficiency
of the extraction and cleanup for PCDDs and PCDFs was
measured by comparing the quantity of the labeled surro-
gates detected in the final isolated extract (at GC/HRMS
analysis) with the quantity spiked into the sample at the
beginning of extraction. The instrument internal standards
spiked into the final extract were used to calculate theamounts of the surrogates recovered. Performance was also
assessed by monitoring recoveries of a mixture of native
labeled PCDDs and PCDFs spiked into chicken eggs. Peak
confirmation required that areas for selected ion responses
be[3 times background noise, that ion peaks for native
congeners with 13C-labeled analogues occur within -1 to
+3 s of those analogues, and that the ion ratio of the two
principal ion responses be within 15%.
PCBs
Nine of the 63 samples were analyzed for PCBs. Congeners
030 and 207 were used as instrumental internal standards.
Individual PCB congeners were measured using a Hewlett-
Packard 5890 Series II GC with cool on-column capil-
lary injection systems. Analytical columns were 60 m 9
0.25 mm 9 0.25 lm DB-5 (5% phenyl-, 95% methylsili-
cone; Agilent) and DB-17 (50% phenyl-, 50% methylsili-
cone; Agilent). The temperature program began at 60C,
ramped to 150C at 15C/min, then ramped to 260C at
1C/min, and finally ramped to 300C at 10C/min for a
15-min hold. The electron capture detector (ECD) tem-
perature was 330C.
A mix of several Aroclors was used to produce sec-
ondary PCB congener calibration standards which were
previously quantified based on pure primary PCB standards
(AccuStandard, New Haven, CT, USA). The PCB cong-
eners were matched and identified on one or both columns
with known PCB peaks from Aroclor standards. Up to nine
levels of calibration for each congener were used to
quantify approximately 140 congeners in the samples. The
method detection limits (MDLs) for individual PCB
congeners (0.0042.1 ng/g) and total PCBs (21 ng/g) were
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calculated as the mean +3 SD of 10 or more procedural
blanks. Method quantitation limits (MQLs) for congeners
were calculated similarly as the procedural blanks
mean +10 SD.
PCB recoveries were monitored with the three surro-
gates spiked into each sample at extraction and PCB-spiked
(mixed Aroclors 1242, 1248, 1254, and 1260) chicken
eggs. The three surrogates (PCBs 029, 155, and 204) werechosen to represent more volatile early-eluting PCBs
(Cl13), midrange-eluting congeners (C146), and later-
eluting PCBs (C1710), respectively.
Organochlorine Pesticides
Organochlorine pesticides were measured in 9 of the 63
samples (including at least 1 sample from each study area)
with a Hewlett-Packard 5890 Series II GC, cool on-column
capillary injection systems, and ECD. The analytical col-
umns and temperature program were the same as described
above for PCB analyses. Six levels of standards (29 com-ponents) were used for calibration. Detection limits were
calculated as discussed for PCB congeners. Analyte
recoveries were monitored by the recoveries of surrogate
standards spiked into each sample, and either a 29-pesti-
cide-mix chicken egg matrix spike or a PCB matrix spike.
Mercury
Homogenized samples were lyophilized with a Virtis
Genesis 35EL freeze-dryer. Once dried, samples were
further homogenized by mechanical grinding with a glass
rod. Mercury was determined with a Milestone (Shelton,
CT, USA) DMA-80 direct mercury analyzer. A 48- to 58-
mg subsample of each dried egg powder sample was
combusted in a stream of oxygen. Mercury was volatilized
and trapped by amalgamation on a gold substrate and
thermally desorbed and quantitated by atomic absorption
spectrophotometry.
Statistical Analyses
Because eggs dehydrate during incubation and refrigera-
tion (Stickel et al. 1973), regression equations specific to
wood duck eggs (Hoyt 1979) were used to estimate egg
fresh weight from length and breadth measurements. This
allowed calculation of egg-specific adjustment factors for
moisture loss, and we report pollutant concentrations on a
fresh wet weight basis.
Because the PCDDs and PCDFs are structurally similar,
they produce a similar pattern of toxic responses, and their
toxicological mode of action is presumed to be similar,
TEFs have been derived to approximate the toxicity of
individual congeners relative to TCDD. We calculated
TEQs using the TEFs for birds of Van den Berg et al.
(1998).
Contaminant concentrations and TEQs are compared
among sites. Concentrations were analyzed for goodness of
fit to a normal distribution by the Shapiro-Wilk test (JMP
5.1.2; SAS Institute, Inc., Cary, NC). None were normally
distributed, and log-transformations only resulted in a
normal distribution for mercury (lack of normality in thePCDDs and PCDFs was largely due to values reported at
less than MDLs at the reference site, resulting in a left-
skewed distribution; log transformations of contaminant
data for the three Roanoke basin study sites were generally
normally distributed). Accordingly, pollutant concentra-
tions were compared among sites with the nonparametric
KruskalWallis rank sum test followed by Tukeys HSD
test for mean separation (based on rankings of concentra-
tions among all sites). Statistical significance for all
comparisons was based on p\0.05. No statistical analyses
were conducted for compounds detected in less than 50%
of the samples; these included 1,2,3,6,7,8-HxCDF,2,3,4,6,7,8-HxCDF, 1,2,3,7,8,9-HxCDF, 1,2,3,4,6,7,8-hep-
tachlorodibenzofuran (HpCDF), 1,2,3,4,7,8,9-HpCDF, and
octachlorodibenzofuran. For analytes present in at least
50% of samples at concentrations higher than MDLs, a
value of one-half the detection limit was substituted for
nondetects in statistical comparisons. For analytes reported
as estimated values (between the MDL and the MQL), the
estimated concentration was used.
Concentrations of TCDD, TCDF, and TEQs from this
assessment were compared to those in eggs collected from
this same area a decade earlier by the Wilcoxon rank sum
test (mercury was not assessed previously). The TEQ
comparison required that the congener data from the earlier
assessment (Beeman and Augspurger 1996) be used to
recalculate TEQs based on the TEFs used in the contem-
porary assessment (Van den Berg et al. 1998).
Clutch size (number of eggs laid, including those taken
for contaminant analyses) and percent hatch (excluding
eggs taken for analyses) were also compared among sites
with the KruskalWallis test. The sample egg technique
(Blus 1982) was used to determine the degree of correla-
tion (Spearman Rho test) between contaminant
concentrations in a single embryo from a clutch and the
corresponding clutch size and percent hatch of the sibling
eggs from the clutch. There were 40 clutches for which
contaminant and productivity data were available. Statis-
tical analyses were performed on this entire dataset as well
as a dataset culled to exclude clutch sizes of[16 eggs.
This was intended to reduce the potential influence of
dump nests (nest to which two or more females contribute
eggs to a single clutch) (Hepp and Bellrose 1995) on the
summary of productivity data. Although any nest with
more than 1 egg could potentially be a dump nest and there
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is uncertainty in the maximum number of eggs in a normal
clutch, 16 eggs is often an assumed maximum clutch size
from one hen (Bellrose and Holm 1994).
Results
Quality Assurance
Procedural blanks in PCDD and PCDF analyses indicated
no appreciable background contamination of equipment or
reagents. Percentage recoveries (51105%) of 13C-labeled
surrogate PCDDs and PCDFs spiked into all samples were
acceptable (within the quality assurance range of 25
125%). Measured concentrations of PCDDs and PCDFs in
six chicken egg matrix spikes were within 20% of the
spiked values. Four of the 55 samples were analyzed in
triplicate and results indicated very good precision, with
the relative percentage difference (RPD) averaging 40 for
TCDD and 15 for TCDF (the analytes comprising themajority of TEQs in these samples).
Blanks indicated no significant PCB contamination.
Percentage recoveries of individual PCB congeners in
matrix spikes were generally within acceptable ranges for
method accuracy for these compounds (25125%) and
were between 78 and 101% for total PCBs. Recoveries of
PCB surrogates added to all samples and matrix spikes
ranged from 69 to 100%. The RPD for total PCBs in a
sample analyzed in triplicate was 16%. Of the pesticides
detected in these samples, none were present in blanks at
quantities above MDLs. Recoveries of pesticides in matrix
spikes ranged from 56 to 104% and the RPDs for the few
analytes detected in a sample analyzed in triplicate were
between 1.5 and 55.
For mercury, the blank equivalent concentration
(0.0003 lg/g dry weight) was less than the MDL of
0.005 lg/g dry weight. Percentage recoveries of mercury
from precombustion tissue spikes ranged from 91 to 111%.
Recoveries from four reference tissue materials (NIST
RM50, NIST 8415, NRCC DORM-2, CERC Striped Bass)
averaged 108%. Precision, determined as RPD from trip-
licate combustion, amalgamation, and analysis of five
samples was B2.5.
PCDDs, PCDFs, TEQs, and Mercury
There were generally only five PCDD and PCDF analytes
above 1.0 pg/g: TCDD, TCDF, 1,2,3,6,7,8-HxCDD,
1,2,3,4,6,7,8-HpCDD, and OCDD. TCDD was detected in
all samples from the Roanoke River, Welch Creek and the
Eastmost River at concentrations between 0.1 and 4.9 pg/g
but in only 27% of eggs from the reference site where
concentrations did not exceed 0.3 pg/g. TCDF was
detected in all eggs, ranging from 0.5 to 25 pg/g at the
lower Roanoke River study sites (i.e., Welch Creek, the
Roanoke River, and Eastmost River), but B0.9 pg/g in all
reference site eggs. OCDD was the analyte detected at the
highest concentration, ranging from 0.3 to 5.9 pg/g at the
reference site and 1.8 to 90 pg/g at the lower Roanoke
River sites.
Concentrations of most analytes were significantly ele-vated at the three sites associated with the lower Roanoke
River compared to those from the wildlife refuge reference
site (Table 1). While concentrations of TCDD and TCDF
tended to be higher in the eggs from boxes on Welch
Creek, they were not significantly different from those
from areas just downstream in the Roanoke River and
Eastmost River. The TEQs from PCDDs and PCDFs were
significantly elevated at the three sites associated with the
lower Roanoke River compared to those from the reference
site. The highest concentration (30 pg/g) was from a nest
along Welch Creek. TCDD and TCDF comprised the
majority of TEQs in all samples, but their relative contri-bution differed among sites (Table 1). The proportion of
TEQs from TCDD was significantly higher in Welch Creek
than the reference site. The proportion of TEQs from
TCDF was only 30% at the reference site (where TCDF,
1,2,3,7,8-PeCDD, and 2,3,4,7,8-PeCDF at concentrations
near their detection limits contributed about equally to the
overall low TEQs), but significantly higher at 70% in the
sites downstream of the paper mill. Samples in which
TCDD was elevated also tended to have elevated TCDF
(r = 0.953, p\ 0.001, n = 48) (Table 2). For those sam-
ples with higher OCDD, 1,2,3,4,6,7,8-HpCDD was also
elevated. Figure 2 shows trends in TCDD, TCDF, and
TEQs in eggs from 19921993 to 20022005. Each con-
gener and the TEQs have declined significantly and by
about fivefold over the decade.
Concentrations of mercury in wood duck eggs from
nests on Welch Creek, the Roanoke River, and Eastmost
River ranged from 0.01 to 0.14 lg/g. They were signifi-
cantly higher (Table 1) than those from the reference site,
where concentrations did not exceed 0.04 lg/g.
PCBs and Organochlorine Pesticides
All dioxin-like mono-ortho PCBs (PCBs 105, 114, 118,
123, 156, 157, 167, and 189) were detected at very low
concentrations, between 0.01 and 3 ng/g. Total PCBs in
the nine samples (all sites combined) were also low
(\20 to 80 ng/g). Pentachlorobenzene (\0.07 to 0.24 ng/
g), a-BHC (\0.08 to 0.21 ng/g), heptachlor (\0.17 to
0.22 ng/g), heptachlor epoxide (\0.22 to 1.6 ng/g),
dieldrin (0.37 to 1.8 ng/g), endrin (\0.10 to 0.30 ng/g),
oxychlordane (\0.09 to 1.6 ng/g), cis-chlordane (\0.17
to 0.55 ng/g), trans-chlordane (\0.28 to 0.46 ng/g), cis-
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nonachlor (\0.07 to 0.32 ng/g), trans-nonachlor (0.40 to
2.1 ng/g), o,p0-DDD (\0.61 to 0.77 ng/g), o,p0-DDT
(\0.10 to 0.12 ng/g), p,p0-DDE (1.7 to 230 ng/g), p,p0-
DDD (\0.33 to 0.43 ng/g), p,p0-DDT (\0.43 to 3.7 ng/
g), endosulfan I (\0.34 to 0.55 ng/g), and mirex (\0.05
to 1.5 ng/g) were the only pesticides detected. Other
organochlorine pesticides were less than their corre-
sponding MDLs: hexachlorobenzene (\2.5 ng/g),
pentachloroanisole (\0.25 ng/g), b-BHC (\0.20 ng/g),
lindane (\0.50 ng/g), d-BHC (\0.12 ng/g), aldrin
(\0.28 ng/g), dacthal (\0.50 ng/g), o,p0-DDE (\0.17 ng/
g), endosulfan II (\0.16 ng/g), endosulfan sulfate
(\0.95 ng/g), and methoxychlor (\2.0 ng/g). Concentra-
tions of pesticides were generally similar between the
Roanoke study sites and the reference site with the
exception of p,p0-DDE at the Roanoke sites (geometric
mean, 24 ng/g), which was about eight times higher than
at the reference site.
Table 1 Dioxin, furan, avian TCDD toxic equivalent, and mercury concentrations in wood duck eggs from eastern North Carolina, 20022005
Chemical p-valuea Welch
Creek
(n = 16)
Roanoke
River
(n = 18)
Eastmost
River
(n = 14)
PLNWR
(ref. site;
n = 15)
2,3,7,8-TCDD \0.0001 0.8 Ab 0.5 A 0.8 A \0.2 B
0.51.3 0.30.9 0.51.1 11 (ND)c
1,2,3,7,8-PeCDD 0.0056 0.3 A 0.3 A 0.3 A\
0.2 B0.20.5 0.20.4 0.20.5 10 (ND)
1,2,3,4,7,8-HxCDD 0.0020 0.3 A 0.3 A 0.3 A \0.2 B
0.20.4 0.20.4 0.20.5 9 (ND)
1,2,3,6,7,8-HxCDD \0.0001 0.5 A 0.6 A 0.7 A \0.2 B
0.30.8 0.50.8 0.41.0 9 (ND)
1,2,3,7,8,9-HxCDD 0.0440 0.3 A 0.3 AB 0.3 A \0.2 B
0.20.5 0.20.4 0.20.5 9 (ND)
1,2,3,4,6,7,8-HpCDD \0.0001 2.4 A 2.8 A 2.8 A 0.3 B
1.53.8 1.94.0 1.74.7 0.20.5
OCDD \0.0001 10 A 13 A 15 A 1.4 B
5.517 8.521 9.623 0.9 2.2
2,3,7,8-TCDF \0.0001 4.1 A 3.3 A 4.3 A 0.4 B
2.56.7 2.05.5 2.76.8 0.30.4
1,2,3,7,8-PeCDF 0.2812 0.2 0.2 0.2 \0.2
0.10.3 0.10.2 0.10.3 11 (ND)
2,3,4,7,8-PeCDF \0.0004 0.3 A 0.2 AB 0.4 A 0.2 B
0.20.4 0.20.3 0.30.5 0.10.3
1,2,3,4,7,8-HxCDF 0.6704 0.2 0.2 \0.2 \0.2
0.10.2 0.10.2 8 (ND) 11 (ND)
TEQs \0.0001 6 A 5 A 6 A 1 B
49 37 49 11
TCDD/TEQ (%) 0.0223 13 A 11 AB 12 AB 10 B
TCDF/TEQ (%) \0.0001 66 A 68 A 68 A 30 B
Mercury 0.0033 0.04 A 0.04 A 0.04 A 0.02 B
0.020.06 0.020.05 0.030.05 0.010.03
Note: Welch Creek, Roanoke River, and Eastmost River are downstream of a paper mill. Pocosin Lakes National Wildlife Refuge (PLNWR) is a
reference site. Dioxin and furan concentrations (geometric mean and 95% confidence intervals) are picograms per gram fresh wet weight, and
mercury concentration is micrograms per gram fresh wet weight. Other 2,3,7,8-substituted dioxins and furans were not detected in more than half
the samples. TCDD, tetrachlorodibenzo-p-dioxin; PeCDD, pentachlorodibenzo-p-dioxin; HxCDD, hexachlorodibenzo-p-dioxin; HpCDD, hep-
tachlorodibenzo-p-dioxin; OCDD, octachlorodibenzo-p-dioxin; TCDF, tetrachlorodibenzofuran; PeCDF, pentachlorodibenzofuran; HxCDF,
hexachlorodibenzofuran; TEQ, TCDD toxic equivalent concentrations, using avian toxic equivalency factors of Van den Berg et al. (1998)a KruskalWallis test (df = 3, a = 0.05)b Means followed by the same letter capital letter are not significantly differentc
Number of samples in which analyte was not detected
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Table2
CorrelationmatrixofdioxinandfurancongenersandWorldHealth
OrganizationavianTCDDtoxicequivalen
tconcentrationsinwoodduckeggsfromthelowerRoanokeRiver,
NorthCarolina,20022005
Chemical
1,2,3,7,8-
PeCDD
1,2,3,4,7,8-
HxCDD
1,2,3,6,7,8-
HxCDD
1,2,3,7,8,9-
HxCD
D
1,2,3,4,6,7,8-
HpCDD
OCDD
2,3,7,8-
TCDF
1,2,3,7,8-
PeCDF
2,3,4,7,8-
PeCDF
1,2,3,4,7,8-
HxCDF
TEQs
2,3,7,8-TCDD
0.174
-0.013
0.066
0.09
9
0.095
0.026
0.953
0.013
0.036
-0.038
0.970
p
0.238
0.930
0.653
0.50
4
0.521
0.860
\0.001
0.928
0.810
0.797
\0.001
1,2,3,7,8PeCDD
0.657
0.601
0.69
6
0.240
0.110
0.069
0.688
0.581
0.655
0.158
p
\0.001
\0.001
\0.00
1
0.100
0.454
0.642
\0.001
\0.001
\0.001
0.283
1,2,3,4,7,8-HxCDD
0.843
0.79
2
0.707
0.546
-0.104
0.337
0.372
0.385
-0.038
p
\0.001
\0.00
1
\0.001
\0.001
0.483
0.019
0.009
0.007
0.798
1,2,3,6,7,8-HxCDD
0.65
8
0.741
0.502
0.008
0.086
0.211
0.173
0.056
p
\0.00
1
\0.001
\0.001
0.958
0.559
0.150
0.240
0.706
1,2,3,7,8,9-HxCDD
0.668
0.529
-0.044
0.517
0.395
0.525
0.035
p
\0.001
\0.001
0.765
\0.001
0.005
\0.001
0.814
1,2,3,4,6,7,8-HpCDD
0.872
0.014
-0.184
0.002
-0.122
0.041
p
\0.001
0.925
0.210
0.989
0.408
0.780
OCDD
-0.064
-0.196
0.127
-0.188
-0.037
p
0.663
0.183
0.389
0.200
0.801
2,3,7,8-TCDF
-0.058
-0.004
-0.092
0.994
p
0.698
0.981
0.536
\0.001
1,2,3,7,8-PeCDF
0.636
0.897
0.019
p
\0.001
\0.001
0.899
2,3,4,7,8-PeCDF
0.600
0.072
p
\0.001
0.628
1,2,3,4,7,8-HxCDF
-0.021
p
0.886
Note:TCDD,tetrachlorodibenzo-p-dioxin;PeCDD,pentachlorodibenzo-p-diox
in;HxCDD,hexachlorodibenzo-p-dioxin;HpCDD,heptachlorodibenzo-p-dioxin;OCDD,octachlorodibenzo-p-
dioxin;TCDF,tetrachlorodibenzof
uran;PeCDF,pentachlorodibenzofuran;H
xCDF,hexachlorodibenzofuran;TEQ,TCDDtoxicequivalentconcentrations,using
aviantoxicequivalency
factorsofVandenBergetal.(1998).Valuesarecorrelationcoefficientsandp-values;allcomparisonsareforn=48.Other2,3,7,8-substitutedcongenerswerenotd
etectedinmorethanhalf
thesamples
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Productivity
Wood duck productivity data indicate high hatching suc-cess at all sites (Table 3). Clutch sizes were significantly
larger in Roanoke River nests when data for all nests are
evaluated; this difference is less apparent when data from
nests with clutch sizes[16 at all sites are excluded from
the analyses. One malformation was noted upon opening
unhatched eggs from these sites. A single embryo from nest
box 1 (in 2002) on the Roanoke River had exencephaly
(skull defective, causing exposure or extrusion of the
brain).
Spearman rank correlations indicated no significant
association between hatching success and either TCDD,
TCDF, or TEQs. When data for all nests at the three lowerRoanoke River sites (n = 40) were evaluated, weak but
significant negative correlations were determined for the
association between clutch size and each of these param-
eters (Spearman q and p-value: clutch size and TCDD =
-0.396 and 0.012; clutch size and TCDF = -0.435 and
0.005; and clutch size and TEQ = -0.414 and 0.008).
When data from nests with more than 16 eggs (an assumed
maximum clutch size from one hen) are excluded, none of
the correlations among clutch size and contaminants are
significant (although the Spearman q of -0.373 between
clutch size and TCDF in the culled dataset would be sig-
nificant at a = 0.06). The association is driven by two
values which had among the highest TEQs and lowest
clutch sizes (a sample from a clutch of 10 eggs from aWelch Creek nest in 2002 with a corresponding TEQ of
30 pg/g and a sample from a clutch of 8 eggs from a
Roanoke River nest in 2002 with a corresponding TEQ of
28 pg/g).
Discussion
Wood Ducks as Sentinels of PCDD/PCDF Status
and Trends
Three aspects of these results support the wood ducksutility in coplanar halogenated aromatic hydrocarbon
monitoring: (1) the significantly greater PCDD, PCDF, and
TEQ accumulation in eggs from the study areas compared
to those from the reference site, (2) the significantly lower
PCDD and PCDF concentrations in eggs collected during
20022005 compared to 19921993, and (3) the congener
profiles from all sites and all years.
Wood duck eggs from nests along Welch Creek, the
lower Roanoke River, and the Eastmost River were
0
10
20
30
40
50
60
70
80
90
100
TCDD
p=0.0016
TCDF
p=0.0005
TEQ
p=0.0005
pg/gfreshwetweight
1992-93 2002-05
Fig. 2 Trends in 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), 2,3,7,8-
tetrachlorodibenzofuran (TCDF), and TCDD-equivalent (TEQ) concen-
trations in wood duck eggs from nest boxes along the lower Roanoke
River, near Plymouth, North Carolina (geometric mean and upper 95%
confidence interval; n = 10 in 19921993 and n = 48 in 20022005).
Interyear comparisons by Wilcoxon rank sum test
Table 3 Productivity of wood ducks nesting in boxes erected along
the lower Roanoke River basin, 20022003
Dataseta p-valueb Welch
Creek
Roanoke
River
Eastmost
River
All nests (n = 8) (n = 18) (n = 14)
Clutch size (n) 0.031 10 ABc
16 A 10 B
522 1418 616Hatching success (%) 0.068 95 79 85
88100 5886 71100
Nests with B16 eggs (n = 7) (n = 9) (n = 10)
Clutch size (n) 0.273 9 13 8
423 1215 416
Hatching success (%) 0.250 100 75 91
89100 2593 52100
Note: Clutch sizes are geometric mean and 95% confidence intervals,
and percentage hatch data are median and interquartile range. Only
active nests (those with one or more eggs) were included in these
calculationsa
All nests: all 40 clutches for which contaminant and productivity
data were available. Nests with B16 eggs: subset of all nests, culled to
exclude results from nests with a clutch size[16 eggs (an assumed
maximum clutch size from one hen)b
KruskalWallis test (df = 2, a = 0.05)c Means followed by the same capital letter are not significantly
different
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contaminated with PCDDs and PCDFs. On a TEQ basis,
concentrations in these areas significantly exceed those of a
reference site just 25 km distant. Geometric mean TEQs in
the combined lower Roanoke River sites (Welch Creek, the
lower Roanoke River, and the Eastmost River) were six
times those of the reference site. Wood ducks are migratory
(and some are resident in the coastal Carolinas), but our
results indicate that time spent on breeding sites is suffi-cient to reflect local contamination. Female wood ducks
gain fat reserves for reproduction at the nesting site instead
of prior to migrating (Drobney 1982). Although wood
ducks are omnivorous and mainly eat vegetation, they rely
on sediment-emergent insects prior to and during egg
laying (Hepp and Bellrose 1995), increasing their suscep-
tibility to accumulating sediment-associated contaminants.
Sediment ingestion is another important route of exposure
for wood ducks at contaminated sites (Beyer et al. 1997).
Yolk formation in wood ducks takes place over a 7-day
period, followed by an approximately 24-h period of
albumin and eggshell deposition prior to egg laying(Drobney 1980). Accordingly, residues in eggs will largely
reflect those accumulated at nesting areas, as evident in this
study and others (Kennamer et al. 2005).
Wood duck eggs collected from this area in 19921993
allow a comparison to current concentrations and the first
demonstration of this species in monitoring changes in
PCDD and PCDF contamination through time. When
expressed as TEQs with the avian TEFs of Van den Berg
et al. (1998), wood duck eggs collected from lower Roa-
noke River nests in 19921993 (Beeman and Augspurger
1996) ranged from 2 to 500 pg/g. The TEQs in wood duck
eggs analyzed in 20022005 from the same area ranged
from 1 to 30 pg/g, and geometric mean concentrations of
TCDD, TCDF, and TEQs declined about four-, six-, and
fivefold respectively, over the period. About 2 years after
the 19921993 egg collections, the paper mill upstream of
the wood duck nest boxes virtually eliminated PCDD and
PCDF discharge by switching to chlorine dioxide bleaching
from molecular chlorine. Since then, concentrations of
TCDD and TCDF have declined in fish from the lower
Roanoke River. Geometric mean concentrations of TCDD
and TCDF in three whole creek chubsuckers (Erimyzon
oblongus) collected from the Roanoke in 1987 were 152
and 199 pg/g, respectively (USEPA 1992). Monitoring of
TCDD and TCDF in channel catfish (Ictalurus punctatus)
fillets from the Roanoke River downstream of the mill
shows a decline in TEQs (using a TEF of 0.1 for TCDF)
from 19891991 (when TEQs in fillets averaged about
28 pg/g) to 20022004 (when TEQs in fillets averaged
about 4 pg/g) (RMT 2005).
As documented for wood ducks here, a decline of
PCDDs and PCDFs in eggs following cessation of paper
mill bleaching with molecular chlorine has been reported
for birds in the western United States and Canada (Elliott
et al. 2001; Harris et al. 2003). Declines in concentrations
of dioxin-like compounds were evident in osprey and great
blue heron (Ardea herodias) eggs following mill process
changes that reduced PCDD and PCDF discharges (San-
derson et al. 1994; Elliott et al. 1998, 2001). Large
numbers of wood duck boxes can be accessed with less
effort than is required to obtain eggs of these other species.The proportion of wood duck egg TEQs attributed to
TCDF also declined significantly over the decade, from a
geometric mean of 82% (95% confidence interval, 73
92%) in 19921993 to 68% (95% confidence interval, 63
74%) in 20022005. Congener profiles are still dominated
by TCDF and TCDD, two compounds associated with
bleached kraft paper mills in the contamination of avian
eggs elsewhere (Elliott et al. 2001; Harris et al. 2003).
Congener profiles and interrelationships (Table 2) were
informative in assessing PCDD and PCDF sources;
although the dominant source of local PCDDs and PCDFs
in the Roanoke River is well-known, principal componentanalyses of congener profiles (Choi et al. 2001) and dioxin
fingerprinting could be employed to the residues measured
in wood duck eggs to aid in source identification. Wood
duck eggs in this assessment had detectable levels of 11 of
the 17 2,3,7,8-substituted PCDDs and PCDFs in more than
50% of the samples, providing robust data for fingerprint-
ing applications.
The congener profiles, lack of contamination in refer-
ence site eggs, and decline in local concentrations
following a switch from molecular chlorine to chlorine
dioxide bleaching at the mill provide strong evidence that
lower Roanoke River wood duck egg contamination
reflects pulp and paper mill impacts. These observations
also support using wood duck eggs for monitoring PCDD
and PCDF status and trends.
PCDD and PCDF Data in Context
Table 4 provides additional context on eastern North Car-
olina wood duck egg PCDD and PCDF concentrations.
While concentrations in the 19921993 collections were
among the highest recorded for this species, concentrations
are now in the midrange of those reported by others.
There was no definitive evidence of adverse impacts
from current PCDD and PCDF contamination. One
unhatched embryo with exencephaly was observed in 2002.
The same malformation was noted in an embryo from the
19921993 assessment which was also a conjoined twin
(Beeman and Augspurger 1996). Wood duck productivity,
as measured by clutch size and percentage hatch, was high
compared to other sites (Hepp and Bellrose 1995); the
percentage hatch had a wide range in Welch Creek, the
Roanoke River, and Eastmost River (0 to 100), but the
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median and average percentage hatch for these areas is
normal (Hepp and Bellrose 1995). Mercury, TCDD, TCDF,
and TEQs were not significantly correlated with percentage
hatch. There were significant but weak inverse relation-ships between clutch size and TCDD, TCDF, and TEQs
when all data (n = 40) were included. Smaller clutch size
has been shown to be an experimentally reproducible effect
of dioxin-like compounds in multigeneration American
kestrel studies (Fernie et al. 2001), but the relationships
observed here had a low explanatory power (Spearmans
q * -0.4) and were not significant when the analysis was
restricted to clutch sizes B16 eggs (an assumed normal
clutch size from one female). This is evidence that the
correlations may be an artifact of supranormal clutch sizes
(likely from more than one female). However, it is noted
that two nests with the greatest TEQs had among the lowest
clutch sizes (a clutch of 10 eggs with a corresponding TEQ
in a sibling embryo of 30 pg/g and a clutch of 8 eggs with a
corresponding TEQ of 28 pg/g).
The absent or weak relationships between pollutants and
productivity in wood duck eggs from this site in 2002
2005 are not unexpected, given the decline in contaminant
concentrations. The maximum TEQ concentrations mea-
sured in 20022005 are two orders of magnitude lower
than those which did not adversely affect wood duck
embryos following preincubation egg injection of TCDD
(Augspurger et al. 2008). The 6 pg/g geometric mean TEQ
concentration in wood duck eggs from nests downstream of
the mill is less than known adverse effect levels for all butthe most sensitive avian species, the domestic chicken, for
which adverse effects begin near 10 pg/g (USEPA 2003).
Further, only two of the eggs from our 20022005
assessment exceed a 2050 pg/g reproductive effects
threshold for TEQs and wood ducks (White and Hoffman
1995). Because White and Hoffmans (1995) assessment
used a TEF of 0.1 for TCDF (which was generally present
at concentrations similar to those of TCDD), their reported
effects threshold may be an underestimate. Even so, 46 of
48 eggs collected in 20022005 from the Roanoke River
basin had TEQ concentrations lower than this estimate.
Recent molecular characterization of the ligand binding
domain of the aryl hydrocarbon receptor in wood ducks
further indicates that the species would not be responsive to
the concentrations we encountered (Head 2006).
Field no-effect concentrations for other species are also
well above the geometric mean TEQ for wood duck eggs
from the Roanoke River basin in 20022005. Woodford
et al. (1998) found no effect of dioxins and furans on
hatching success of ospreys nesting downstream of Wis-
consin River pulp and paper mills. They estimated a no-
Table 4 Geometric mean and range of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), 2,3,7,8-tetrachlorodibenzofuran (TCDF), and TCDD toxic
equivalents (TEQs) in wood duck eggs from this assessment and others
Site n Year(s) TCDD TCDF TEQs Reference
Roanoke River, NC 48 20022005 0.7 3.8 6 This study
Range 0.14.9 0.525 130
Roanoke River, NCa
10 19921993 2.9 24 30 Beeman and Augspurger (1996)
Range 0.431 1.1460 2500Pocosin Lakes National Wildlife Refuge, NC 15 20022003 \0.2 0.4 1 This study
Range \0.20.3 0.20.9 0.84
Bayou Meto, AR
Area Ia
17 19881989 36 23 59 White and Hoffman (1995)
Range 2480 2240 4720
Area IV 12 19881989 \1 1 2 White and Hoffman (1995)
Range NDb
\13 \14
Wisconsin River, WI 6 19951996 \2 1.1 18 Custer et al. (2002)
Range ND \16 343
Shiawassee National Wildlife Refuge, MI 5 2003 c
140 Williams (2004)
Range 57246
Rose Lake Game Area, MI 5 2003 2 Williams (2004)
Range 1.13.7
Note: All concentrations are picograms per gram wet weight. TEQs were calculated with toxic equivalency factors for birds from Van den Berg
et al. (1998)a TEQs recalculated from datasheets provided by study authorb
Analyte not detectedc No data on individual analytes
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effect level in eggs of 136 pg/g TEQs (using the TEFs of
Safe 1990). In a retrospective analysis, Elliott et al. (2001)
reported negative correlations between great blue heron
chick growth and TEQs at about 360 pg/g. Concentrations
corresponding to observed health effects in chicks upon
hatching were thought not to have impaired hatching suc-
cess (Elliott et al. 1989, 2001). Field studies of tree
swallows at a PCB- and dioxin-contaminated site indicatedthat the concentration at which reproductive failure became
common was 180 pg/g TCDD (Custer et al. 2005).
Other pollutants were present at levels below those
associated with adverse effects to birds. Mercury concen-
trations were significantly higher in eggs from the nests of
the Roanoke River basin sites compared to the reference
site. Mercury is a contaminant of concern in this area due
to historic releases from a now closed chlor-alkali plant at
the mill, and the higher concentrations of mercury in wood
duck eggs downstream of the mill may be indicative of
local contamination. While higher than reference site
concentrations, the maximum mercury concentration of0.14 lg/g fresh wet weight from a nest box on Welch
Creek is well below adverse-effect thresholds. Heinz
(1979) reported abnormal egg-laying and lower produc-
tivity in female mallards fed 0.5 lg/g methylmercury; eggs
of these females contained 0.790.86 lg/g mercury. In
more recent dietary mercury studies with mallards, a wide
range of mercury burdens was associated with normal
hatching and embryo mortality with adversely affected
eggs estimated to contain as little as 0.74 lg/g mercury
(Heinz and Hoffman 2003). In a review of the mallard data
and other avian toxicological data, Thompson (1996)
indicated that mercury concentrations in eggs between 0.5
and 2.0 lg/g were associated with reproductive
impairment.
Only nine samples were analyzed for PCBs which are
low in other media for the lower Roanoke River. Based on
the low total and mono-ortho-PCBs, we infer that non-
ortho-PCBs were also low and not important contributors,
relative to PCDDs and PCDFs, to the TEQs at this mill site.
Organochlorine pesticide concentrations were also low.
Summary
We documented highly significant differences in spatial
and temporal PCDD and PCDF accumulation which
illustrate the utility of the wood duck in measuring PCDD
and PCDF status and trends. While useful for monitoring,
interpretation of contaminant residues in wood duck eggs
should be considered in context of their trophic status.
Omnivorous birds such as the wood duck typically have
PCDD, PCDF, and PCB concentrations intermediate to
those of herbivorous and piscivorous species, in adult tis-
sues (Senthilkumar et al. 2002; Braune and Malone 2006)
and eggs (Custer et al. 2002). Wood duck contaminant
burdens are likely only representative of other omnivorous
species at a contaminated site, with higher concentrations
expected in insectivorous and piscivorous species.
The strengths and weaknesses of using wood ducks in
avian PCDD/PCDF assessments should be considered
when selecting sentinel species at other sites. The growing
body of data on successful use of tree swallows in avianassessments is noteworthy. Tree swallow eggs can accu-
mulate marked concentrations of dioxin-like compounds;
TCDD concentrations exceeding 1000 pg/g (Custer et al.
2005) and TEQs (based on the TEFs of Van den Berg et al.
1998) up to 25,400 pg/g (Secord et al. 1999) are docu-
mented. Concentrations of PCBs and TEQs from PCBs,
PCDDs, and PCDFs were an order of magnitude higher in
eggs of tree swallows than those of wood ducks in a con-
current assessment of those species (Custer et al. 2002).
Site-to-site differences in accumulation and the ability to
measure concentrations in eggs and sibling chicks in this
altricial species allow estimates of contaminant uptakefrom local forage (Custer et al. 2003, 2005; Maul et al.
2006). These data facilitated development of PCB bioac-
cumulation models for tree swallows (Echols et al. 2004).
Also, dioxin-like compounds have been implicated in
adverse effects on tree swallows in the field (McCarty and
Secord 1999a, b; Custer et al. 2003, 2005; Martinovic et al.
2003). Wood ducks remain a useful option. In our study,
the greater PCDD and PCDF contamination of Roanoke
River basin wood duck eggs compared to a nearby refer-
ence site, the decline of PCDDs and PCDFs following
cessation of molecular chlorine bleaching, and the domi-
nance of TCDD and TCDF in congener profiles provides
strong evidence that contamination of lower Roanoke
River wood duck eggs reflects pulp and paper mill impacts.
Acknowledgments Assistance in the lab and field was provided by
Mike Tanner, Sara Ward, Jean Richter, Wendy Stanton, and Michelle
Chappel. Partial funding was provided through USFWSs Environ-
mental Contaminants Program (Study ID No. 200240001).
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