Environmental Toxicology and Chemistry, Vol. 31, No. 5, pp. 1158–1168, 2012
# 2012 SETAC
Printed in the USA
DOI: 10.1002/etc.1780
DIETARY- AND TISSUE-BASED EXPOSURE OF BELTED KINGFISHER TO PCDFs
AND PCDDs IN THE TITTABAWASSEE RIVER FLOODPLAIN, MIDLAND, MI, USA
RITA M. SESTON,*y JOHN P. GIESY,yz§ TIMOTHY B. FREDRICKS,y DUSTIN L. TAZELAAR,k SARAH J. COEFIELD,y
PATRICK W. BRADLEY,k SHAUN A. ROARK,# JOHN L. NEWSTED,k# DENISE P. KAY,# and MATTHEW J. ZWIERNIKk
yDepartment of Zoology, Center for Integrative Toxicology, Michigan State University, East Lansing, Michigan, USA
zDepartment of Veterinary Biomedical Sciences and Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
§Department of Biology and Chemistry and State Key Laboratory in Marine Pollution, City University of Hong Kong, Hong Kong, China
kDepartment of Animal Science, Michigan State University, East Lansing, Michigan, USA
#Cardno ENTRIX, Okemos, Michigan, USA
(Submitted 29 November 2011; Accepted 23 December 2011)
Abstract— Concentrations of polychlorinated dibenzofurans (PCDFs) and other dioxin-like compounds in soils and sediments of the
Tittabawassee River and associated floodplains downstream of Midland, Michigan, USA, are greater than upstream sites. As a result of
these concentrations, which are some of the greatest ever reported, a site-specific exposure assessment of belted kingfisher breeding in
the assessment area was conducted. To reduce the uncertainty associated with predicting exposure from abiotic matrices, concentrations
of residues were quantified in site-specific prey items and in eggs and nestlings of belted kingfisher. Dietary exposure, expressed as the
potential average daily dose, based on site-specific concentrations of PCDFs, polychlorinated dibenzo-p-dioxins (PCDDs), and 2,3,7,8tetrachlorodibenzo-p-dioxin equivalents (TEQWHO-Avian) in prey items was consistently greater along the Tittabawassee River than in
associated reference areas and further downstream sites in the Saginaw River. Concentrations of PCDD/DFs in eggs and nestlings of
belted kingfisher varied among sampling areas, being greater in both eggs and nestlings nesting along the Tittabawassee River compared
to those of belted kingfisher from upstream reference areas. Geometric mean concentrations of PCDD/DFs were 130 and 200 ng/kg wet
weight in eggs and nestlings of belted kingfisher, respectively. These concentrations are the equivalent of 84 and 95 ng TEQWHO-Avian/
kg. Site-specific biomagnification factors for select PCDD/DF congeners ranged from <1.0 to 1.8 in belted kingfisher. Environ. Toxicol.
Chem. 2012;31:1158–1168. # 2012 SETAC
Keywords—Avian diet
Dioxins and furans
Egg
PCB
Bird
Bioaccumulation
Monitoring food
Feeding
aryl hydrocarbon receptor (AhR), and effects include enzyme
induction, immunotoxicity, and adverse effects on reproduction, development, and endocrine functions [4,5]. In particular,
exposure to compounds that bind to the AhR can result in
reduced hatching and fledging success of bird species [6–10].
The sensitivities of several species to AhR-mediated effects
have been determined in laboratory studies or inferred from
observations of populations exposed in the wild and have been
shown to vary among species [11]. For example, the species
considered to be most sensitive, the domestic chicken (Gallus
gallus), is more than 1,000 times more sensitive to embryolethal effects than is the mallard (Anas platyrhyncos) [12].
These differences have been shown to be related to differences
in the affinity of dioxin-like compounds to the ligand-binding
domain of the AhR [12]. The differential sensitivities can be
attributed to differences in amino acid sequences in the ligandbinding domain of the AhR among avian species, which subsequently leads to differential binding of ligands [13]. Based
on these differences, bird species can be classified into groups
with different sensitivities to AhR-mediated effects.
The belted kingfisher (Ceryle alcyon) was selected as a
receptor species because it possesses characteristics desirable
to investigate exposure and the potential effects of PCDD/DFs
via an aquatic exposure pathway. As top aquatic food web
predators with high food consumption rates, belted kingfisher
have a relatively great potential for exposure [14,15]. Additionally, belted kingfisher excavate subterranean burrows in
which they nest; thus, adult and nestling belted kingfisher have
intimate contact with river bank soils. Because belted kingfisher
are territorial of distinct foraging ranges proximal to the nest
INTRODUCTION
Concentrations of polychlorinated dibenzofurans (PCDFs)
and polychlorinated dibenzo-p-dioxins (PCDDs) in the Tittabawassee River and associated floodplains downstream of Midland, Michigan, USA, are greater than at upstream locations and
regional background concentrations. The presence of PCDD/
DFs is the result of historical chemical production and associated waste management practices [1]. Sediments and floodplain soils downstream of Midland, Michigan contain total
concentrations of the seventeen 2,3,7,8-substituted PCDD/DF
congeners (SPCDD/DFs) ranging from 1.0 102 to 5.4 104 ng/kg dry weight, respectively. In contrast, concentrations
of SPCDD/DFs in sediments and soils from upstream reference
areas were 10- to 20-fold less than those downstream [2].
The concentrations of PCDD/DFs within the Tittabawassee
River floodplain led to concerns about their potential effects
on resident wildlife species in the Tittabawassee River and
Saginaw River floodplains.
Both PCDD/DFs and dioxin-like polychlorinated biphenyls
(PCBs) are persistent in the environment and because of their
lipophilic nature tend to biomagnify [3]. These compounds
are known to cause an array of negative effects on mammalian
and avian species. The PCDD/DF and PCB congeners with
the greatest toxic potency act via a common mechanism, the
All Supplemental Data may be found in the online version of this article.
* To whom correspondence may be addressed
(sestonri@msu.edu).
Published online 23 February 2012 in Wiley Online Library
(wileyonlinelibrary.com).
1158
Assessment of belted kingfisher exposure to PCDD/DFs
burrow, the spatial boundaries of the area from which nestling
belted kingfisher are exposed can be better defined than
other species [16]. Their widespread distribution has led to
belted kingfisher being included in other ecological assessments
[17–20]. The dynamics of the Tittabawassee River have lead to
the presence of suitable nesting sites in its riverbanks, thus
the belted kingfisher was included as a study species.
The primary objective of the present study was to characterize and compare dietary and tissue-based assessments of exposure of the belted kingfisher foraging and nesting within the
Tittabawassee River floodplain to 2,3,7,8-substituted PCDD/
DFs congeners. Species-specific characteristics of the belted
kingfisher give it a great potential for exposure and make it well
suited for study using a multiple-lines-of-evidence approach
to ecological risk assessment. The lines of evidence used here
include predicted exposure to contaminants through the diet and
measured concentrations in egg and nestlings of belted kingfisher. Concentrations of SPCDD/DF were measured in dietary
items and belted kingfisher tissues collected from reference
and study areas. These concentrations were also expressed
as 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) equivalents
(TEQWHO-Avian) based on World Health Organization (WHO)
TCDD equivalency factors for birds (TEFWHO-Avian) [21].
Spatial trends in concentrations and relative contributions
of congeners to total concentrations of PCDD/DF and
TEQWHO-Avian in dietary items and belted kingfisher tissues
were also evaluated. An assessment of effects associated with
the exposure to PCDD/DFs outlined here, as well as additional
lines of evidence including reproductive and individual health
measures for these same animals, are discussed in a separate
publication (R.M. Seston et al., Michigan State University, East
Environ. Toxicol. Chem. 31, 2012
1159
Lansing, MI, USA, unpublished manuscript). Integrating data
resulting from multiple assessments reduces the uncertainty
inherent in the risk assessment process [22–24] and provides
better information for use in risk management decisions.
METHODS
Site description
The assessment of exposure was conducted in the vicinity of
the city of Midland, located in the lower peninsula of Michigan
(Fig. 1). The Tittabawassee River is a tributary of the Saginaw
River, which flows into Saginaw Bay and Lake Huron. The
Tittabawassee River runs through the Dow Chemical Company
(Dow), which is the accepted source of the PCDD/DF contamination [1]. The area, henceforth referred to as the study
area, includes approximately 37 km of the Tittabawassee River
(sites T-3 to T-6) extending downstream from Dow to the
convergence of the Tittabawassee River and Saginaw River
and 35 km of the Saginaw River (sites S-7 to S-9) until it flows
into Saginaw Bay. Sampling sites selected in the study area
were chosen to characterize maximal exposure potential designated as ‘‘worst case scenario’’ locations based on a previous
study that measured concentrations of PCDD/DFs in soils and
sediments [2]. Landowner cooperation was also a factor in site
selection. The reference area includes the Tittabawassee River
upstream of Dow, together with the Pine and the Chippewa
rivers, both of which flow into the Tittabawassee River
upstream of Midland. Reference area sampling locations were
on the upstream Tittabawassee River (R-1) and the Pine River
(R-2). Sampling areas were assessed both individually and
in spatial groups based on characteristics of the river and
Fig. 1. Assessment area along the Chippewa, Tittabawassee, and Saginaw River floodplains, Michigan, USA. Sampling locations for dietary components of belted
kingfisher were located in the reference areas (R-1 and R-2), upper Tittabawassee River (T-3 and T-4), lower Tittabawassee River (T-5, T-6, and S-7), and Saginaw
River (S-8 and S-9). Tissues of belted kingfisher were collected in the reference area and along the Tittabawassee River (study area).
1160
Environ. Toxicol. Chem. 31, 2012
associated floodplain. Spatial groupings included reference
areas R-1 and R-2, upper Tittabawassee River T-3 and T-4,
lower Tittabawassee River T-5 to S-7, and Saginaw River S-8
and S-9. Components of the diet, including soil, sediment,
and prey items were collected at each sampling area, whereas
belted kingfisher tissues were collected from nests and were
designated to either a reference area or study area.
Dietary-based exposure assessment
Collection of prey items. Prey items of belted kingfisher
were collected from nine sampling areas (Fig. 1). Forage fish,
crayfish, and amphibians were collected and concentrations of
PCDD/DFs (n ¼ 188) and PCBs (n ¼ 20) were determined. The
sampling scheme maximized information on dietary exposure
including geographically associated contaminant variability
and trends. Detailed sample collection methods have previously
been described [25].
Dietary exposure calculations. Exposure of belted kingfisher to PCDD/DFs via diet was estimated by use of information given in the U.S. Environmental Protection Agency (U.S.
EPA) Wildlife Exposure Factors Handbook [26]. Major factors
influencing dietary exposure included body mass, daily food
intake rate (g wet wt food/g body mass/d, dietary concentrations, and proportion of foraging time spent on-site. A mean
body mass of 147 g and a body-weight normalized food intake
rate of 0.50 kg food (wet wt)/kg body mass/d for belted kingfisher is given in the U.S. EPA Wildlife Exposure Factors
Handbook [26]. The potential average daily dose (ADDpot;
ng/kg body mass/d) was calculated using Equation 4-3 of the
Wildlife Exposure Factors Handbook [26]. Incidental sediment
ingestion was also included in the ADDpot using Equation 4-23
of the Wildlife Exposure Factors Handbook [26].
The relative contribution of each type of prey to the belted
kingfisher diet was determined through collection and identification of prey remains from active nest chambers located in
the assessment area. Collected remains were sorted to prey item
type by distinct elements, such as fish otoliths, pharyngeal
arches, and dentary bones, crayfish chelipeds, and amphibian
femurs or pelvic girdles and quantified as to the minimum
number of individuals from each taxon necessary to account for
the assemblage of remains. Reconstructed dietary composition
was based on the frequency of occurrence of all identifiable prey
items and compiled on the basis of relative (%) composition of
biomass. The relative contribution to the dietary composition
of each prey type was multiplied by its reach-specific concentrations of PCDD/DFs. Exposure was estimated using the
geometric mean and associated 95% confidence interval of
concentrations of residues in prey items from each reach
(reference area, upper Tittabawassee River, lower Tittabawassee River, and Saginaw River). Polychlorinated biphenyls were
not measured in all frogs or crayfish, thus the data set is
incomplete for calculating total TEQWHO-Avian exposure associated with PCDD/DFs and PCBs. However, where both PCDD/
DF and PCB data were available, concentrations of total
TEQsWHO-Avian in fish were greater than those in frogs and
crayfish collected from the same area. Therefore, as a conservative estimate of dietary exposure to total TEQsWHO-Avian,
a diet composed of 100% fish was used in place of the sitespecific diet.
R.M. Seston et al.
result in subsequent renesting, so surveys were performed again
in late June. Belted kingfisher burrows were considered active
when there was evidence of fresh digging around and beneath
the burrow entrance, the presence of parallel longitudinal
depressions left in the burrow by the birds feet, and/or defensive
behavior of belted kingfisher during burrow examination. Confirmation of burrow activity was gained by using an infrared
video camera that was inserted into the burrow opening to
visualize the nest chamber.
Once a burrow was deemed active, the location of the nest
chamber was determined by using a folding wooden ruler to
approximate the length and angle of the burrow tunnel. From
the top of the bank a hole was created approximately 75 cm
beyond the location of the nest chamber, and then the leading
edge of the excavation pit was slowly moved forward until a
small opening was made in the rear of the nest chamber [27].
After the nest chamber was located, a wooden panel with an
access door and video-port was installed to allow access for nest
monitoring and sample collection. The entire excavation was
then covered with a sheet of 2.0-cm exterior-grade plywood and
camouflaged tarpaulin to prevent water and predators from
entering the excavation or nesting chamber. It was optimal
to perform the excavation once the clutch was complete and
incubation had begun to reduce the risk of the adults abandoning
the nest [28].
Nests were monitored from late-April to mid-July. Nests
with complete clutches were checked every other day to determine hatch date, nestling status, and fledge date. All nestlings
were banded with U.S. Fish and Wildlife Service (U.S. FWS)
bands. Various nest activities, including incubation, hatching,
and feeding of nestlings, were recorded using an infrared
camera at the rear of the nest chamber, and during routine
handling, nestling belted kingfisher were monitored for gross
external abnormalities. Additionally, adult belted kingfisher
were trapped and banded with U.S. FWS bands to allow
determination of nest site fidelity and survival.
Both eggs and nestlings of belted kingfisher were collected
from each available nest chamber located within the assessment
area to quantify PCDD/DFs. One egg was selected at random
from each clutch. Mass, length, and three width measurements
were recorded for each egg. Addled or abandoned eggs were
also collected for possible quantification of PCDD/DF congeners. Addled eggs were defined as those that failed to hatch 2 d
posthatch of other eggs in the clutch. Abandoned eggs were
defined as those that were cold on three consecutive visits to the
nest. Individual eggs were wrapped in chemically cleaned foil
and placed inside a glass jar (I-CHEM) for storage and transport
to the laboratory. One nestling from each nest was selected
randomly for collection at age 15 d and euthanized via cervical
dislocation. Individual collected nestlings were stored in similar
jars for storage and transport.
During the 2005 to 2007 breeding seasons, 37 nest chambers
were excavated. Eggs were collected from six and 19 unique
clutches in the reference area and study area, respectively. Five
and 12 nestlings were collected from unique broods in the
reference area and study area, respectively. Of the collected
nestlings, eight (two in the reference area and six in the study
areas) were collected from nests from which an egg was also
analyzed.
Sample processing and analytical techniques
Tissue-based exposure assessment
Active belted kingfisher nest burrows were located via canoe
surveys from mid-April to mid-May. Early nest failures often
Concentrations of seventeen 2,3,7,8-substituted PCDD/DF
congeners were measured in all samples. Concentrations
of PCBs and dichloro-diphenyl-trichloroethane and related
Assessment of belted kingfisher exposure to PCDD/DFs
metabolites were determined in only a subset of samples.
Collected eggs were opened around the girth with a scalpel
blade. Contents were then homogenized in a chemically cleaned
omni-mixer, lyophilized, and stored in chemically cleaned jars
(I-CHEM) until analysis. Concentrations of PCDD/DF in eggs
were reported on a fresh weight basis adjusted to account for
any desiccation during incubation and storage. Adjusted fresh
weight was calculated based on egg volume [29]. The mass of
egg contents was determined by subtracting the eggshell mass at
the time of processing from the adjusted fresh weight. Nestlings
were homogenized in a chemically cleaned omni-mixer, without stomach contents, feathers, legs below the tibiotarsus, or
the beak.
Residues were quantified according to U.S. EPA Method
8290/1668A with minor modifications [30]. Analytical methods
have been detailed elsewhere [31,32]. Briefly, biotic matrices
were homogenized with anhydrous sodium sulfate, spiked with
known amounts of 13C-labeled analytes (as internal standards),
and Soxhlet extracted. A total of 10% of the extract was
removed for lipid content determination. Sample purification
included the following: treatment with concentrated sulfuric
acid, silica gel, sulfuric acid silica gel, acidic alumina, and
carbon column chromatography. Components were analyzed
using high-resolution gas chromatography/high-resolution
mass spectroscopy, a Hewlett-Packard 6890 GC (Agilent Technologies) connected to a MicroMass high-resolution mass
spectrometer (Waters Corp.). Quality control samples generated
during chemical analyses included sample processing blanks
(equipment rinsate and atmospheric), laboratory method blanks,
matrix spike and matrix spike duplicates, unspiked sample
replicates, and blind check samples. Evaluation of the percentage of recovery and relative percentage of difference data
for the matrix spike and matrix spike duplicate samples and
unspiked replicate samples were within 30% at a rate of
greater than 95% acceptability. Soxhlet extractions and instrumental analyses were conducted at AsureQuality Ltd, Lower
Hutt, New Zealand.
Statistical analyses
Total concentrations of the seventeen 2,3,7,8-substituted
PCDD/DF congeners (SPCDD/DFs) are reported as the sum
of all congeners (ng/kg wet wt). Individual congeners for which
concentrations were less than the limit of quantification were
assigned a value of half the sample method detection limit on
a per sample basis. Total concentrations of the 12 dioxin-like
non- and mono-ortho-substituted PCB congeners are reported
as the sum of these congeners (ng/kg wet wt; SPCBs) for
a subset of samples. Concentrations of TEQWHO-Avian (ng/kg
wet wt) were calculated for both PCDD/DFs and dioxinlike PCBs by summing the product of the concentration
of each congener, multiplied by its avian TEFWHO-Avian [21].
Total TEQs throughout the present study refers to the summation of TEQs from SPCDD/DFs (DF-TEQsWHO-Avian)
and SPCBs (PCB-TEQsWHO-Avian). Additionally, dichlorodiphenyl-trichloroethane (20 ,40 and 40 ,40 isomers) and
dichloro-diphenyl-dichloroethylene (40 ,40 ) are reported as the
sum of the o,p and p,p isomers (SDDXs; mg/kg wet wt) for
the same subset of samples as the PCBs.
Statistical analyses were performed using SAS software
(Release 9.1; SAS Institute). Prior to the use of parametric
statistical procedures, normality was evaluated using the
Shapiro–Wilks test and the assumption of homogeneity of
variance was evaluated using Levene’s test. Values that were
not normally distributed were transformed using the natural log
Environ. Toxicol. Chem. 31, 2012
1161
(ln) before statistical analyses. PROC TTEST was used to
make comparisons between the reference area and study area.
PROC GLM was used to make comparisons for three or more
locations. When significant differences among locations were
indicated, the Tukey-Kramer test was used to make comparisons between individual locations. Statistical significance was
inferred at p < 0.05.
RESULTS
PCDD/DFs and PCBs in belted kingfisher prey
Concentrations of the contaminants of concern varied among
sampling reach and prey type, ranging from 1.8 ng SPCDD/
DFs/kg and 0.29 ng DF-TEQWHO-Avian/kg in the reference area
to 3300 ng SPCDD/DFs/kg and 1900 ng DF-TEQWHO-Avian/kg
in the study area (Table 1). Consistent spatial trends in concentrations of SPCDD/DFs and DF-TEQWHO-Avian were
observed for each type of prey. Concentrations were least in
the reference area, greater in the upper Tittabawassee River, and
greatest in the lower Tittabawassee River. Concentrations in
prey items from the Saginaw River were intermediate to those
from the reference area and upper Tittabawassee River. A
majority of SPCDD/DFs in dietary items from the study area
were composed of PCDFs, whereas PCDDs were the predominant contributors in the reference area (Fig. 2). Concentrations
of SPCBs in prey items followed a different spatial trend than
that of SPCDD/DFs, being greatest in the Saginaw River. A
more detailed description of the spatial trends in concentrations
of PCDD/DFs and PCBs in the prey items, along with a
discussion of relative congener concentrations, is available in
Seston et al. [32].
Spatial trends were also seen in the relative contribution
of DF-TEQWHO-Avian and PCB-TEQWHO-Avian to total
TEQWHO-Avian in prey items. In fish from the reference area
and Saginaw River, the majority of total TEQWHO-Avian were
attributed to PCB-TEQsWHO-Avian (63 and 61%, respectively),
in contrast to fish collected from the Tittabawassee River that
had a majority of their total TEQWHO-Avian attributed to DFTEQWHO-Avian (81 and 85% for the upper Tittabawassee River
and lower Tittabawassee River, respectively). Polychlorinated
biphenyls-TEQWHO-Avian were dominated by PCB-126, PCB77, and PCB-81 in all reaches.
Dietary exposure
Prey remains collected from belted kingfisher nest chambers
revealed the site-specific diet to be 90.2% fish, 5.4% crayfish,
and 4.4% frogs. The ADDpot (ng/kg body mass/d) based on the
site-specific diet was consistently greatest along the Tittabawassee River when compared to either the reference area or
Saginaw River, regardless of whether it was based on SPCDD/
DF, DF-TEQWHO-Avian, or total TEQWHO-Avian (Table 2). The
SPCDD/DF ADDpot to belted kingfisher was 44- to 54-fold
greater along the Tittabawassee River and 12-fold greater along
the Saginaw River when compared to the reference areas. When
normalized to DF-TEQWHO-Avian, fold differences in ADDpot
increased, being 150- to 190-fold greater along the Tittabawassee River and 35-fold greater along the Saginaw River when
compared to the reference area. Site-specific prey items contained concentrations of residues that were similar (wet wt),
with those in forage fish composites being slightly greater than
crayfish and frogs. Based on a diet of 100% fish, the ADDpot of
DF-TEQWHO-Avian ranged from 0 to 6.6% greater, resulting in a
slightly more conservative estimate. The ADDpot expressed as
total TEQWHO-Avian based on a 100% fish diet was 76- to 92-fold
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Environ. Toxicol. Chem. 31, 2012
R.M. Seston et al.
Table 1. 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents in prey items of belted kingfisher collected from 2004 through 2006 from the Chippewa,
Tittabawassee, and Saginaw River floodplains, Midland, Michigan, USAa,b
Reachc,d
Frog
SPCDD/DF
SPCB
DF-TEQWHO-Avian
PCB-TEQWHO-Avian
Crayfish
SPCDD/DF
SPCB
DF-TEQWHO-Avian
PCB-TEQWHO-Avian
Forage fish
SPCDD/DF
SPCB
DF-TEQWHO-Avian
PCB-TEQWHO-Avian
Nest chamber soil
SPCDD/DF
DF-TEQWHO-Avian
Reference area
Upper Tittabawassee
Lower Tittabawassee
Saginaw River
5.5 (29) A
4.3–6.9
(1.8–21)
N/Ae
49 (51) B
33–73
(4.4–920)
N/A
6.7 (12) A
4.7–9.4
(3.3–26)
N/A
1.0 (29) A
0.81–1.3
(0.29–3.4)
N/A
20 (51) B
13–31
(1.1–460)
N/A
100 (55) C
78–140
(17–3,300)
1,300 (4)
880–2,000
(940–1,700)
56 (55) C
42–76
(9.1–1,900)
1.5 (4)
0.86–2.5
(1.1–2.0)
5.0 (5) A
1.8–13
(2.3–12)
N/A
140 (7) B
83–240
(86–340)
– (2)
–
(2,200–2,200)
55 (7) B
24–130
(12–190)
– (2)
–
(3.3–4.3)
360 (8) C
200–650
(140–1300)
– (1)
–
(2100)
160 (8) C
110–250
(75–420)
– (1)
–
(5.3)
50 (8) D
34–72
(28–110)
N/A
– (2)
–
(4.1–5.1)
– (2)
–
(880–1,000)
– (2)
–
(0.90–0.91)
– (2)
–
(1.3–1.8)
– (2)
–
(200–220)
– (2)
–
(9,300–15,000)
– (2)
–
(130–170)
– (2)
–
(30–39)
260 (5) A
95–730
(83–610)
18,000 (5) A
4,600–72,000
(7,100–110,000)
180 (5) A
66–480
(74–440)
31 (5) A
10–92
(13–100)
59 (4) B
26–130
(37–210)
25,000 (4) A
10,000–62,000
(15,000–470,00)
33 (4) B
20–56
(25–53)
55 (4) A
12–250
(24–150)
– (2)
–
(17–35)
– (2)
–
(8.8–9.1)
16000 (5)
3700 (7)
N/A
(3000–50000)
1300 (5)
(62–34000)
1400 (7)
N/A
(150–7800)
(15–21000)
0.91 (5) A
0.29–2.8
(0.34–2.9)
N/A
2.9 (12) A
1.9–4.5
(1.5–14)
N/A
27 (8) B
18–41
(13–61)
N/A
a
2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TEQWHO-Avian) were calculated based on the 1998 World Health Organization toxic equivalency factors for
avian species.
b
Values (ng/kg wet wt) have been rounded and represent only two significant figures and are given as the geometric mean and sample size in parentheses (n) over
the 95% confidence interval and range (min-max).
c
Geometric mean and confidence intervals not calculated for sites with fewer than three samples. These sites were not included in reach comparisons.
d
Means identified with the same uppercase letter are not significantly different among reach at the p ¼ 0.05 level using Tukey-Kramer means separation test.
e
N/A ¼ no samples collected from this location.
SPCDD/DF ¼ sum of 2,3,7,8-substituted polychlorinated dibenzo-p-dioxins and dibenzofurans; SPCB ¼ sum of twelve dioxin-like non- and mono-orthosubstituted PCB congeners; DF-TEQWHO-Avian ¼ 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents of SPCDD/DFs; PCB-TEQWHO-Avian ¼ 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents of SPCBs.
greater along the Tittabawassee River and 38-fold greater along
the Saginaw River when compared to the reference area.
PCDD/DFs and PCBs in belted kingfisher tissues
Concentrations of measured residues were consistently
greater in tissues of belted kingfisher collected within the study
area compared to those of the reference area. However, the
differences varied in their statistical significance (Table 3).
Mean concentrations of SPCDD/DFs and DF-TEQWHO-Avian
were significantly greater in belted kingfisher eggs collected
from the study area compared to those from the reference area
(four- and sixfold greater, respectively; p < 0.0001). Although
mean concentrations of PCB-TEQWHO-Avian were twofold
greater in belted kingfisher eggs collected from the study area
than those from the reference area, the difference was not
significant ( p ¼ 0.0767). Mean concentrations of SPCB and
SDDX in belted kingfisher eggs were similar between sampling
areas ( p ¼ 0.7686 and p ¼ 0.7372, respectively).
Assessment of belted kingfisher exposure to PCDD/DFs
Environ. Toxicol. Chem. 31, 2012
1163
Fig. 2. Percentage of mean contribution of individual congeners to total 2,3,7,8-substituted polychlorinated dibenzo-p-dioxins and dibenzofurans in the diet of the
belted kingfisher and their eggs and nestlings collected from reference and study areas. PCDD/DF ¼ polychlorinated dibenzo-p-dioxins/dibenzofurans;
TCDF ¼ 2,3,7,8-tetrachlorodibenzofuran; PeCDF ¼ pentachlorodibenzofurans; HxCDD ¼hexachlorodibenzofurans; HpCDF ¼heptachlorodibenzofurans;
OCDF ¼octachlorodibenzofuran; TCDD ¼ 2,3,7,8-tetrachlorodibenzo-p-dioxin; PeCDD ¼ pentachlorodibenzo-p-dioxins; HxCDD ¼hexachlorodibenzo-pdioxins; HpCDD ¼heptachlorodibenzo-p-dioxins; OCDD ¼octachlorodibenzo-p-dioxin.
Spatial trends in relative contribution of PCDDs, PCDFs,
and individual congeners to SPCDD/DFs and DF- TEQWHOAvian in belted kingfisher eggs were also observed. Belted
kingfisher eggs collected from the study area had a greater
percentage of contribution of furans to both SPCDD/DFs and
DF- TEQWHO-Avian (66 and 73%, respectively) compared to
those collected from the reference area (27 and 29%, respectively). Predominant congeners of SPCDD/DFs in belted kingfisher eggs from the reference area included TCDD (20%) and
1,2,3,7,8-pentachlorodibenzo-p-dioxin (PeCDD; 17%), in contrast to 2,3,4,7,8-pentachlorodibenzofuran (PeCDF; 39%),
which was the predominant congener in eggs collected from
the study area (Fig. 2). When normalized to DF-TEQWHO-Avian,
the predominant congeners remained the same in each area,
with TCDD (36%) and 1,2,3,7,8-PeCDD (34%) in belted
kingfisher eggs collected from the reference area and
2,3,4,7,8-PeCDF (59%) in eggs collected from the study area.
Variability in concentrations of SPCDD/DFs and DFTEQWHO-Avian among eggs collected from the same clutch
was minimal. More than one egg was collected and analyzed
from a total of 11 nests (Table 4). The mean relative percentage
of difference in concentrations of SPCDD/DFs was 11%. When
based on DF-TEQWHO-Avian the mean relative percentage of
difference was 12%.
The spatial trend in concentrations of contaminants in nestlings was similar to that observed in belted kingfisher eggs.
Mean concentrations of SPCDD/DFs and DF-TEQWHO-Avian
were significantly greater in nestlings of belted kingfisher
Table 2. Potential average daily dietary intake of the sum of 2,3,7,8-substituted polychlorinated dibenzo-p-dioxins and dibenzofurans and
2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents for adult belted kingfisher breeding from 2004 through 2006 within the Chippewa, Tittabawassee,
and Saginaw river floodplains, Midland, Michigan, USAa–d
Study area
Referencef
Upper Tittabawassee Riverg,h
Lower Tittabawassee Riveri
Saginaw River
a
SPCDD/DFs
2.6
114
140
31
(2.1–3.5)
(100–130)
(54–370)
(13–110)
DF-TEQWHO-Aviana
0.46
70
88
16
(0.44–0.53)
(60–83)
(34–230)
(9.5–32)
Total TEQWHO-Aviana,e
1.2
91
110
46
(1.1–1.4)
(80–110)
(39–290)
(15–140)
2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TEQWHO-Avian) were calculated based on the 1998 avian World Health Organization toxic equivalency factors
values.
b
Values (ng/kg body wt/d) were rounded and represent only two significant figures.
c
Food ingestion rate was calculated from equations in The Wildlife Exposure Factors Handbook [26].
d
Predictions are based on the geometric mean (95% confidence interval) of site-specific dietary items.
e
Total TEQWHO-Avian based on a diet of 100% fish because of a lack of polychlorinated biphenyl (PCB) data in frogs and crayfish.
f
Two fish composite samples collected from Reference reach. Range represents daily dietary intake based on minimum-maximum of fish concentrations.
g
Upper Tittabawassee River reach includes sites T-3 and T-4.
h
Two fish composite samples collected from upper Tittabawassee River reach. Range represents daily dietary intake based on minimum–maximum of fish
concentrations.
i
Tittabawassee includes sites T-5, T-6, and S-7.
SPCDD/DF ¼ sum of 2,3,7,8-substituted polychlorinated dibenzo-p-dioxins and dibenzofurans; DF-TEQWHO-Avian ¼ 2,3,7,8-tetrachlorodibenzo-p-dioxin
equivalents of SPCDD/DFs.
1164
Environ. Toxicol. Chem. 31, 2012
R.M. Seston et al.
Table 3. Total concentrations of the sum of 2,3,7,8-substituted
polychlorinated dibenzo-p-dioxins and dibenzofurans and
2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents in belted kingfisher eggs
and nestlings collected from 2005 through 2007 from the Chippewa,
Tittabawassee, and Saginaw River floodplains, Midland, Michigan, USAa,b
BKF Eggs
DF-TEQs
PCB-TEQs
Total TEQs
SPCDD/DF
SPCB
SDDX
BKF Nestlings
RA
SA
RA
SA
15 (6) Ac
6.3–35
(6.5–53)
29 (3)
12–74
(19–39)
47 (3) A
10–210
(26–87)
30 (6) A
14–62
(13–73)
120 (3)
20–660
(52–190)
440 (3)
43–4600
(210–1300)
84 (19) B
62–110
(36–260)
64 (11)
41–99
(23–270)
170 (11) B
120–240
(79–520)
130 (19) B
100–170
(63–370)
130 (11)
81–220
(42–650)
540 (11)
310–940
(120–1500)
5.0 (5) ad
2.9–8.6
(2.6–8.5)
6.0 (4) a
3.8–9.6
(4.1–8.5)
9.7 (4) a
8.0–12
(8.6–11)
9.6 (5) a
5.0–18
(4.7–20)
11 (4) a
7.3–15
(8.3–14)
140 (4)
43–430
(82–390)
95 (12) b
73–120
(49–180)
35 (9) b
14–87
(9.4–590)
160 (9) b
100–250
(110–660)
200 (12) b
120–340
(82–1300)
67 (9) b
35–130
(23–430)
210 (9)
160–280
(120–350)
a
2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TEQWHO-Avian) were calculated based on the 1998 World Health Organization toxic equivalency
factors for avian species.
b
Values (ng/kg wet wt) have been rounded and represent only two significant figures and are given as the geometric mean (n) over the 95%
confidence intervals and range in parentheses. The sum of twelve dioxinlike non- and mono-ortho-substituted PCB congeners (SPCB) and
dichloro-diphenyl-trichloroethane (20 ,40 and 40 ,40 isomers) and dichlorodiphenyl-dichloroethylene (40 ,40 ) (SDDX) values are reported in mg/kg
wet weight.
c
Means identified with a unique capitalized letter are significantly different
between locations (across) at the p ¼ 0.05 level, for belted kingfisher
(BKF) eggs.
d
Means identified with a unique lowercase letter are significantly different
between locations (across) at the p ¼ 0.05 level, for BKF nestlings.
SPCDD/DF ¼ sum of 2,3,7,8-substituted polychlorinated dibenzo-pdioxins and dibenzofurans; RA ¼ reference area; SA ¼ study area; DFTEQs ¼ 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents of SPCDD/DFs;
PCB-TEQs ¼ 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents of SPCB.
collected from the study area compared to those from the
reference area (21- and 19-fold greater, respectively;
p < 0.0001). In contrast to eggs, mean concentrations of SPCB
and PCB-TEQWHO-Avian were significantly greater in nestlings
of belted kingfisher collected from the study area compared to
those from the reference area (6- and 6-fold, respectively;
p ¼ 0.0014 and p ¼ 0.0167, respectively). Mean concentrations
of SDDX in nestlings of belted kingfisher were similar between
sampling locations ( p ¼ 0.1492).
Similar spatial trends in relative contributions of PCDDs,
PCDFs, and individual congeners to SPCDD/DFs and DFTEQWHO-Avian were also observed in nestlings of belted kingfisher. Nestlings of belted kingfisher collected from the study
area had a greater percentage of contribution of furans to both
SPCDD/DFs and DF-TEQWHO-Avian (75 and 90%, respectively)
compared to those collected from the reference area (37 and
38%, respectively). Predominant congeners of SPCDD/DFs in
nestlings of belted kingfisher from the reference area included
TCDD (19%) and 1,2,3,7,8-PeCDD (13%), in contrast to
2,3,4,7,8-PeCDF (30%), which was the predominant congener
in nestlings collected from the study area (Fig. 2). When
normalized to DF-TEQWHO-Avian, the predominant congeners
remained the same in each area, with TCDD (36%) and
1,2,3,7,8-PeCDD (25%) in nestlings of belted kingfisher collected from the reference area and 2,3,4,7,8-PeCDF (57%)
in nestlings collected from the study area.
There was also a spatial trend in the relative contribution
of DF-TEQWHO-Avian and PCB-TEQWHO-Avian to total
TEQWHO-Avian in the tissues of belted kingfisher. In the reference area, PCBs accounted for the greatest proportion of total
TEQWHO-Avian in both eggs and nestlings of belted kingfisher
(64 and 62%, respectively). Conversely, PCDD/DFs accounted
for a majority of the total TEQWHO-Avian in both eggs and
nestlings of belted kingfisher collected from the study area
(59 and 72%, respectively). However, PCB-TEQsWHO-Avian
were dominated by PCB-126, PCB-77, and PCB-81 in each
sampling location.
A limited number of correlations of residue concentrations
were observed in soils and eggs (N ¼ 11) and nestlings (N ¼ 5)
collected from the same nest. Concentrations of SPCDD/DFs
( p ¼ 0.04) and DF-TEQWHO-Avian ( p < 0.0001) had a significant positive correlation between co-located soils and nestlings.
However, these relationships were not observed for eggs. Of the
primary congeners of interest, 2,3,4,7,8–PeCDF was the only
congener to also exhibit a significant positive correlation
between co-located soils and either eggs ( p ¼ 0.02) or nestlings
( p < 0.0001).
Correlations between concentrations of certain congeners in
eggs and nestlings were observed (N ¼ 8). Concentrations of
SPCDD/DFs ( p ¼ 0.07) nearly exhibited a significant positive
correlation between eggs and nestlings from the same nest.
Individual congeners 2,3,4,7,8-PeCDF ( p ¼ 0.03) and 2,3,7,8tetrachlorodibenzofuran (TCDF) ( p ¼ 0.03) were observed to
have a significant positive correlation between eggs and nestlings.
DISCUSSION
Belted kingfishers as receptor species
Belted kingfishers possess several characteristics that make
them well suited for some site-specific ecological risk assessments. Belted kingfishers are widely distributed, high-trophiclevel predators that forage locally over a variety of riverine and
lacustrine habitats. Thus, belted kingfishers are likely to be
present in areas of aquatic-based contamination. Because they
have a smaller foraging range relative to other larger piscivorous birds, they are more likely to derive a greater percentage of
their exposure locally. Despite the aforementioned advantages,
the belted kingfisher has been used sparingly as a receptor
species for aquatic-based ecological risk assessments. This is
likely related to the effort required to access nests in contrast to
the communal or cavity-dwelling birds that can be induced to
nest in nest-boxes. These passerine cavity-nesting birds are
often used as receptor species. The belted kingfisher builds
subterranean nests and has not been shown to nest in artificial
structures. As such, locating and accessing nests for monitoring
and sample collection is more difficult and requires significant
training and patience to avoid undue nest disturbance. Furthermore, belted kingfisher can be nest-site limited [28,33] in some
habitats, which might make it difficult to obtain the necessary
sample size in a short-term study. Despite these potential
limitations, belted kingfisher should still be considered an
optimal piscivorous avian species to study because their defined
foraging range allows for greater spatial resolution of their
dietary exposure compared to other species commonly used,
such as the great blue heron (Ardea herodias) or the blackcrowned night heron (Nycticorax nycticorax).
Assessment of belted kingfisher exposure to PCDD/DFs
Environ. Toxicol. Chem. 31, 2012
1165
Table 4. Within-clutch variability of the sum of 2,3,7,8-substituted polychlorinated dibenzo-p-dioxins and dibenzofurans or
2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents in belted kingfisher eggs collected from 2005 through 2007 from within the Chippewa and
Tittabawassee river floodplains, Midland, Michigan, USAa,b
Nest
E1c,d
E2
RA-1
11
(6.0)
44
(12)
59
(43)
29
(13)
130
(71)
200
(140)
89
(60)
76
(48)
130
(68)
120
(65)
200
(150)
14
(6.9)
41
(14)
100
(74)
31
(14)
130
(78)
190
(140)
85
(52)
87
(52)
120
(64)
120
(73)
230
(180)
RA-2
RA-3
RA-4
SA-1
SA-2
SA-3
SA-4
SA-5
SA-6
SA-7
E3
73
(54)
37
(22)
140
(85)
220
(160)
77
(46)
62
(41)
130
(71)
120
(76)
E4
57
(41)
23
(10)
140
(72)
200
(140)
67
(41)
42
(27)
120
(65)
170
(94)
E5
E6
E7
31
(14)
120
(63)
250
(180)
75
(45)
110
(67)
240
(170)
110
(64)
270
(190)
150
(72)
180
(120)
130
(70)
140
(78)
160
(87)
Nest mean SD
73 21
(53 15)
30 5.1
(15 4.2)
120 12
(71 7.6)
220 30
(160 20)
79 8.8
(48 5.8)
67 19
(42 11)
130 11
(68 3.3)
140 24
(85 19)
RPDe
12
(7)
4
(6)
20
(21)
11
(19)
8
(8)
11
(11)
9
(10)
22
(20)
6
(4)
14
(16)
8
(10)
a
2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TEQWHO-Avian) were calculated based on the 1998 World Health Organization toxic equivalency factors for
avian species.
b
The sum of 2,3,7,8-substituted polychlorinated dibenzo-p-dioxins and dibenzofurans (SPCDD/DF) (ng/kg ww) given over TEQsWHO-Avian, which are in
parentheses.
c
Values were rounded and represent only two significant figures.
d
E1 to E7 indicate individual eggs analyzed per clutch; note that lay order is not known.
e
Mean relative percentage of difference (RPD).
RA ¼ reference area; SA ¼ study area.
Dietary exposure
The observed trends in concentrations and relative contribution of individual congeners of dioxin-like compounds in
prey items of the belted kingfisher were consistent with those
observed for dietary items and tissues of other receptor species
studied within the study area [32,34–37]. The tendency of
concentrations to increase with distance downstream of Dow
is likely a result of this historical contamination being present
in a dynamic river system, which is slowly moving away from
the upstream source. When expressed as dietary exposure, the
toxicological proportion of DF–TEQWHO-Avian compared to
SPCDD/DF for ADDpot of belted kingfisher was 18% in the
reference area, while in the study area it ranged from 61 to 63%
and 52% for reaches along the Tittabawassee River and Saginaw River, respectively. The greater percentages observed
along the Tittabawassee River and Saginaw River were because
of prey items from those reaches having greater relative TCDD
potency of SPCDD/DF, from primarily 2,3,7,8-TCDF and
secondarily from 2,3,4,7,8–PeCDF (Fig. 2). Greater concentrations of PCBs in forage fish from the Saginaw River compared to those from the Tittabawassee River are most likely
because of historical PCB contamination in areas downstream
of the Tittabawassee River, including the Saginaw River and
Saginaw Bay [38] as well as some lesser sources upstream of the
reference area. As such, PCBs made up 13 to 20% the total
TEQWHO-Avian ADDpot in the study area, but was 62 and 65% of
the total TEQWHO-Avian ADDpot in the reference area and
Saginaw River, respectively (Table 2).
Tissue exposure
While the order in which eggs are laid is not known due to
the nesting characteristics of the belted kingfisher, the small
amount of variability observed among eggs collected from the
same nest suggests that the order in which eggs are laid is not a
significant factor in the concentration of PCDD/DFs in eggs
of birds. Similar observations of small intraclutch variability in
concentrations of PCDD/DFs were made in passerine species
breeding within the Tittabawassee River floodplain [31].
Concentrations of PCBs and other organohalogenated compounds exhibited relatively small within-clutch variability in
other studies [39,40]. This relatively small variability allows for
the collection and quantification of contaminant residues in one
egg to provide an acceptable representation of all eggs in the
clutch. To further minimize any potential impacts of laying
order, it has been suggested that two eggs from a clutch be
randomly selected and pooled for residue quantification [41].
This approach was not done in the present study in an attempt to
minimize the amount of destructive sampling.
The relative contribution of individual PCDD/DF congeners
was similar between eggs and nestlings of belted kingfisher,
suggesting that the source of exposure was consistent between
egg laying and nestling rearing (Fig. 2). Additionally, the
significant correlations observed for concentrations of the
two site-specific congeners (2,3,4,7,8-PeCDF and TCDF)
between eggs and nestlings of belted kingfisher would suggest
similar exposures. Contaminant profiles in nestlings are generally considered more representative of local contamination
than eggs due to the fact that nestlings are confined to the nest
and rely on food brought to them by adults [42,43]. During
breeding and rearing of nestlings, adult belted kingfisher have a
foraging range that is typically limited to 0.92 to 2.9 km from
the nest [27,28]. Despite the fact the belted kingfisher is a
seasonally migratory species in this area of its range [15], it
would appear that exposure to PCDD/DFs offsite was of
1166
Environ. Toxicol. Chem. 31, 2012
R.M. Seston et al.
Table 5. Biomagnification factors of select polychlorinated dibenzo-p-dioxins and dibenzofurans and polychlorinated biphenyls in the belted kingfisher within
the Tittabawassee River floodplain and for birds with aquatic-based diets, as reported in the literaturea
Predator/Prey
Chemical
TCDD
TCDF
23478-PeCDF
PCB 118
PCB 126
Whole-body
gull/alewife
Osprey
egg/fish
Juvenile albatross/
stomach contents
Tree swallow nestling/
stomach contents
Waterbird
egg/diet
Range in
literature
TR BKF
egg/diet
TR BKF
nestling/diet
32
1.3
6.6
80
NR
24
0.26
NR
NR
1.7–18
9
3
3
4
5
NR
NR
NR
5.4
NR
NR
NR
NR
2.2–15
NR
9–32
<1–3
3–6.6
2.2–80
1.7–18
1.7
0.03
1.2
5.4
4.9
1.2
0.16
1.8
2.9
4.6
a
See Braune and Norstrom [45], Henny et al. [51], Kunisue et al. [52], Maul et al. [53], and Antoniadou et al. [54].
BKF ¼ belted kingfisher; PCB ¼ polychlorinated biphenyl; TR ¼ Tittabawassee River floodplain; TCDD ¼ 2,3,7,8-tetrachlorodibenzo-p-dioxin; TCDF ¼
2,3,7,8-tetrachlorodibenzofuran; 23478-PeCDF ¼ 2,3,4,7,8-pentachlorodibenzofuran; NR ¼ not reported.
minimal concern and the PCDD/DF residues in tissues of belted
kingfisher nesting along the Tittabawassee River floodplain
were of local origination.
The predominant congener present in prey items sampled
from the study area was TCDF, with 2,3,4,7,8-PeCDF also
having a significant presence. In eggs and nestlings of belted
kingfisher, the overall congener profile was similar to that
observed in prey items, although the predominant congener
changed from TCDF to 2,3,4,7,8-PeCDF. This pattern was also
observed in great blue heron, great horned owls, and several
passerine species foraging in the study area [31,32,36,37,44].
Bioaccumulation of TCDF in Forster’s terns and herring gulls
has been reported to be negligible [7,45]. This may be because
of the preferential metabolism of TCDF as reported in various
avian species that have been exposed to mixtures of AhR-active
compounds [46–48]. Although data on toxicokinetics of PCDD/
DF in birds determined during controlled laboratory studies
are limited, studies of mammals have shown the rate of metabolism of TCDF to be elevated with increased concentrations of
dioxin-like compounds and the subsequent induction of cytochrome P450 1A1 and/or 1A2, whereas 2,3,4,7,8-PeCDF is
preferentially sequestered in the liver [49,50]. This difference
in toxicokinetics is a likely explanation for the observed difference in the relative contribution of the two-furan congeners
from diet to tissue observed for belted kingfisher in the present
study.
Because this site has some of the greatest reported concentrations of PCDD/DFs in floodplain soils and the intimate
contact belted kingfisher nestlings might have with these soils
in the nest chamber, this was initially considered to be a relevant
route of exposure. However, correlations of contaminant concentrations between nest chamber soils and nestlings showed
only a limited number of significant relationships, suggesting
that consuming local prey is the primary route of exposure to
PCDD/DFs.
piscivorous avian species (Table 5). Site-specific biomagnification factors were comparable to those from the literature,
though biomagnification factors from the Tittabawassee River
tended to be on the low end of the range of values reported. For
the current study, tissues of belted kingfisher collected from nest
burrows on site were compared to site-specific dietary items
collected at various time points. This greatly reduces the
temporal and spatial variability and uncertainty that might be
present in the other studies reporting biomagnification factors
for PCDD/DFs. The comparability of site-specific biomagnification factors and those from the literature, further suggests that
the dietary- and tissue-based exposure lines of evidence are well
aligned.
CONCLUSIONS
The belted kingfisher proved to be a useful receptor species
in assessing PCDD/DFs along the Tittabawassee River. Given
its relatively small, distinct foraging range, the exposure of
belted kingfisher has a greater spatial resolution than most other
fish-eating birds. Belted kingfisher foraging along the Tittabawassee River were predicted to be more greatly exposed to
PCDD/DFs than those in associated reference areas. This spatial
trend was consistent with what was noted in concentrations of
PCDD/DFs in both eggs and nestlings of belted kingfisher. The
greater exposure of belted kingfisher in the study area compared
to the reference area presents an opportunity to assess the risk to
individuals and populations inhabiting the contaminated floodplain. A multiple-lines-of-evidence risk assessment, based in
part on values presented in the present study, has been conducted (R.M. Seston et al., Michigan State University, East
Lansing, MI, USA, unpublished manuscript).
SUPPLEMENTAL DATA
Tables S1–S10. (202 KB PDF).
Exposure assessment comparison
The consistency of the relative contribution of individual
PCDD/DF congeners among dietary components and the various belted kingfisher tissues collected (Fig. 2) supports the
conclusion that tissue exposure was the result of site-specific
dietary exposure. Thus, concentrations of PCDD/DFs quantified
in the belted kingfisher diet and in tissues of belted kingfisher
foraging and nesting within the Tittabawassee River were used
to determine biomagnification factors of the predominant congeners. Biomagnification factors, which are a ratio of the lipidnormalized concentration in predator to that in the diet, were
calculated for belted kingfisher along the Tittabawassee River
and compared to values reported in the literature for other
Acknowledgement—The authors would like to thank all staff and students of
the Michigan State University–Wildlife Toxicology Laboratory (MSUWTL) field crew; namely, M. Nadeau, D. Hamman, W. Folland, E. Koppel,
and L. Williams. We gratefully acknowledge M. Fales for his design and
fabrication of specialized equipment that was pivotal to the success of this
research. Additionally, we would like to recognize M. Kramer and N. Ikeda
for their support in the laboratory. Key to the success of the project were the
Tittabawassee Township park rangers for access to Tittabawassee Township
Park and Freeland Festival Park, T. Lenon of the Chippewa Nature Center, J.
Dastyck and S. Kahl of the United States Fish and Wildlife Service–
Shiawassee National Wildlife Refuge, Saginaw County Parks and Recreation
Commission for access to Imerman Park, and Mike Bishop of Alma College
for guidance as our Master Bander. We also acknowledge the more than 50
cooperating landowners throughout the study area who made our research
possible by granting us access to their property. Funding was provided
Assessment of belted kingfisher exposure to PCDD/DFs
through an unrestricted grant from the Dow Chemical Company, Midland,
Michigan, to J. Giesy and M. Zwiernik of Michigan State University.
Disclaimer—All aspects of the present study that involved the use of
animals were conducted using the most humane means possible. To achieve
that objective, standard operation procedures approved by Michigan State
University’s Institutional Animal Care and Use Committee (IACUC)
(Protocol for belted kingfisher monitoring and tissue collection 05/07-07100; Field studies in support of Tittabawassee River ERA 03/04-042-00;
Protocol for fish sampling 03/04-043-00) were followed. All required state
and federal permits (Michigan Department of Natural Resources Scientific
Collection Permit SC1254 for belted kingfisher/SC permit for fish
[Zwiernik]/SC permit for amphibians [Zwiernik]; USFWS Migratory Bird
Scientific Collection Permit MB1000062-0; and sub-permitted under U.S.
Department of the Interior Federal Banding Permit 22926) are on file at MSUWTL.
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Table S1. Concentrations of 2378-TCDD equivalents (TEQsa) in eggs and
nestlings of belted kingfisher collected during 2005−2007 from within the
Chippewa and Tittabawassee River floodplains, Midland, MI, USA.
Valuesb (ng/kg ww) are given as the geometric mean (sample size) over the
95% confidence interval.
BKF Eggs
BKF Nestlings
RA
SA
RA
SA
c
PCDD-TEQWHO-Avian
10 (6)
19 (19)
3.1 (5)
8.5 (12)
3.9−28
15−26
1.6−6.0
0.74−3.2
PCDF-TEQWHO-Aviand
4.1 (6)
59 (19)
1.8 (5)
86 (12)
2.4−7.0
40−87
1.2−2.9
65−110
non-ortho PCBTEQWHO-Aviane
26 (3)
58 (11)
5.6 (4)
32 (9)
11−63
37−89
3.5−9.0
12−81
mono-ortho PCBTEQWHO-Avianf
2.5 (3)
5.5 (11)
0.40 (4)
2.6 (9)
6.9−14
3.2−9.3
0.26−0.63 1.3−5.1
Total TEQWHO-Avian
47 (3)
170 (11)
9.7 (4)
170 (9)
10−210
120−240
8.0−12
110−250
a
TEQWHO-Avian were calculated based on the 1998 avian WHO TEF values
Values have been rounded and represent only two significant figures
b
PCDD-TEQWHO-Avian= summation of the TEQs of individual PCDD
congeners
c
PCDF-TEQWHO-Avian= summation of the TEQs of individual PCDF
congeners
e
non-ortho PCB-TEQWHO-Avian= summation of the TEQs of individual nonortho substituted PCB congeners
f
mono-ortho PCB-TEQWHO-Avian= summation of the TEQs of individual
mono-ortho substituted PCB congeners
b
Table S2. Concentrations of seventeen 2,3,7,8-substituted furan and dioxin congeners in
eggs and nestlings of belted kingfisher collected during 2005-2007 within the Chippewa and
Tittabawassee River floodplains, Midland, MI, USA. Valuesa (ng/kg ww) are given as the
arithmetic meanb ± 1 SD over the range.
BKF Eggs
BKF Nestlings
RA
SA
RA
SA
c
Chemical
n=6
n=19
n=5
n=12
2378-TCDF
0.82±0.46
0.22−1.3
7.4±3.8
1.6−14
0.91±0.42
0.52−1.6
26±10
12−49
23478-PeCDF
3.4±2.1
1.3−7.2
67±57
6.7−180
0.87±0.41
0.61−1.6
63±38
12−140
12378-PeCDF
0.30±0.14
0.21−0.66
3ND
0.46±0.17
0.21−0.66
1ND
5.1±2.9
0.88−10
1ND
1.5±1.1
0.47−4.6
0.27±0.026
0.24−0.29
2ND
15±7.9
6.3−34
6ND
1.0±0.48
0.49−1.6
1ND
1.4±0.95
0.62−2.7
1ND
19ND
4.1±3.1
1.1−12
5ND
234678-HxCDF
0.15−0.16
3ND
123789-HxCDF
123678-HxCDF
123478-HxCDF
1234789-HpCDF
16±15
2.1−57
6ND
8.5±9.7
1.8−27
0.52±0.18
0.28−0.77
11ND
2.8±1.3
1.2−5.8
1ND
0.84±0.60
0.36−2.5
5ND
13±9.1
3.8−46
12378-PeCDD
6.6±5.7
1.7−17
10±7.3
2.5−29
123789-HxCDD
0.78±0.29
0.43−1.1
1.1±0.68
0.21−2.8
1234678-HpCDF
6ND
0.31±0.077
0.22−0.39
2ND
12346789-OCDF
2378-TCDD
0.25−2.7
3ND
0.23±0.096
0.17−0.34
2ND
5ND
0.16
4ND
0.16
2.3±2.2
0.69−7.0
0.54−0.99
10ND
5.6±5.6
1.0−18
26±27
3.0−77
3.7±3.7
0.40−9.9
7ND
18±31
1.2−99
4ND
2.0±0.97
0.76−3.2
25±44
0.34−130
2ND
5.6±1.6
2.5−8.2
1.4±0.85
0.69−2.9
3.1±0.94
1.3−4.6
0.86±0.80
0.23−1.9
5ND
7.0±5.3
2.1−21
5ND
1.5±1.3
0.33−3.6
8ND
3.3±3.6
1.4−14
123478-HxCDD
1.6±0.50
0.70−1.9
1ND
1234678-HpCDD 1.6±0.98
0.77−3.5
1.9±1.4
0.60−5.2
3ND
3.7±1.4
2.0−6.2
0.72±0.45
0.34−1.6
5ND
15±29
0.96−97
12346789-OCDD 3.4±2.6
1.4−8.3
9.0±5.2
1.8−20
0.53±0.49
0.23−1.1
2ND
0.60±0.43
0.32−1.2
1ND
0.67±0.088
0.52−0.75
123678-HxCDD
a
2ND
5.5±3.8
1.1−11
85±190
1.1−650
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of arithmetic
means
c
TCDF = tetrachlorodibenzofuran; PeCDF = pentachlorodibenzofuran; HxCDF=
hexachlorodibenzofuran; HpCDF = heptachlorodibenzofuran; OCDF =
octachlorodibenzofuran; TCDD = tetrachlorodibenzo-p-dioxin; PeCDD =
pentachlorodibenzo-p-dioxin; HxCDD = hexachlorodibenzo-p-dioxin; HpCDD =
heptachlorodibenzo-p-dioxin; OCDD = octachlorodibenzo-p-dioxin
b
Table S3. Concentrations of selected co-contaminants in eggs and nestlings of
belted kingfisher collected during 2005-2007 within the Chippewa and
Tittabawassee River floodplains, Midland, MI, USA. Valuesa (µg/kg ww) are
given as the arithmetic meanb ± 1 SD over the range.
BKF Eggs
BKF Nestlings
RA
SA
RA
SA
c
Chemical
n=3
n=11
n=4
n=9
PCB 77
0.099±0.035
0.074−0.14
0.34±0.25
0.11−0.96
0.043±0.016
0.028−0.061
0.49±0.98
0.039−3.1
PCB 81
0.047±0.014
0.036−0.063
0.11±0.073
0.025−0.23
0.010±0.0077
0.0037−0.021
0.44±1.1
0.011−3.5
PCB 126
0.18±0.066
0.10−0.23
0.45±0.54
0.085−2.0
0.026±0.0067
0.020−0.034
0.17±0.18
0.053−0.64
PCB 169
0.025±0.0.006
0.0018−0.030
16±11
4.6−27
1.2±0.66
0.52−1.8
0.041±0.035
0.014−0.13
1ND
43±49
7.6−180
4.0±4.5
0.79−17
0.0030−0.0040
2ND
2.0±0.65
1.3−2.7
0.16±0.045
0.10−0 20
0.011±0.0038
0.0063−0.015
5ND
26±43
5.0−140
2.0±3.1
0.44−10
PCB 118
56±45
19−110
100±91
26−350
6.6±1.4
5.2−8.2
58±66
14−230
PCB 123
1.2±0.0.75
0.53−2.0
2.7±3.2
0.32−11
0.14±0.072
0.067−0.23
1.6±2.6
0.23−8.5
PCB 156
6.7±4.2
2.4−11
14±13
3.6−47
1.0±0.28
0.82−1.4
5.7±5.2
1.7−19
PCB 157
1.7±1.2
0.54−2.9
3.3±3.1
0.76−11
0.21±0.071
0.17−0.32
1.2±1.2
0.36−4.3
PCB 167
4.0±3.2
1.2−7.5
6.8±6.3
2.0−23
0.49±0.058
0.43−0.57
2.7±1.9
0.89−7.4
PCB 189
0.69±0.51
0.24−1.3
1.4±1.2
0.45−4.5
0.098±0.020
0.081−0. 3
0.60±0.49
0.19−1.8
2,4’-DDT c
0.78±0.99
0.035−1.9
0.36±0.18
0.084−0.62
0.012−0.031
0.075±0.045
0.016−0.15
PCB 105
PCB 114
2’,4’-DDE
4, 4’-DDT
a
d
600±580
200−1300
690±500
120−1500
2ND
170±150
82−390
6.4±1.7
5.0−8.3
20±16
4.0−55
0.26±0.32
0.0055−0.69
1ND
220±78
120−350
1.3±1.2
0.028−3.1
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of
arithmetic means
c
DDT = dichloro-diphenyl-trichloroethane
d
DDE = dichloro-diphenyl-dichloroethylene
b
Table S4. Concentrations of seventeen 2,3,7,8-substituted furan and dioxin
congeners in soils collected during 2006 from nest chambers of belted kingfishers
within the Chippewa and Tittabawassee River floodplains, Midland, MI, USA.
Valuesa (ng/kg ww) are given as the arithmetic meanb ± 1 SD over the range.
Reference Area
Study Area
c
Chemical
n=2
n=12
2378-TCDF
7.5−8.1
23478-PeCDF
0.64−0.73
12378-PeCDF
1.1−1.3
234678-HxCDF
0.22
3200±4300
12−15000
1000±1500
1.7−5100
1300±1900
2.4−6800
110±130
0.21−430
1ND
123789-HxCDF
123678-HxCDF
2ND
0.19
22±27
1.2−90
2ND
180±240
0.29−850
1ND
123478-HxCDF
0.22−0.47
1234789-HpCDF
0.10
990±1300
1.1−4500
82±96
0.13−320
1ND
1234678-HpCDF
0.20−0.94
800±1200
2.4−4300
0.35−1.1
1500±2400
3.6−8600
12346789-OCDF
2378-TCDD
0.13
12378-PeCDD
1ND
0.21
123789-HxCDD
1ND
0.25
123678-HxCDD
1ND
0.30
7.4±11
0.26−40
9.6±12
0.22−36
2ND
15±20
0.27−55
2ND
28±43
0.34−130
123478-HxCDD
1ND
0.12
1ND
1234678-HpCDD
0.73−3.0
12346789-OCDD
5.0−19
SUM PCDD/DFs
17−35
a
7.5±9.2
0.13−23
4ND
520±810
4.3−2300
6300±10000
32−29000
16000±16000
62−50000
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of
arithmetic means
c
TCDF = tetrachlorodibenzofuran; PeCDF = pentachlorodibenzofuran; HxCDF=
hexachlorodibenzofuran; HpCDF = heptachlorodibenzofuran; OCDF =
octachlorodibenzofuran; TCDD = tetrachlorodibenzo-p-dioxin; PeCDD =
pentachlorodibenzo-p-dioxin; HxCDD = hexachlorodibenzo-p-dioxin; HpCDD =
heptachlorodibenzo-p-dioxin; OCDD = octachlorodibenzo-p-dioxin
b
Table S5. Concentrations of seventeen 2,3,7,8-substituted furan and dioxin
congeners in sediment collected during 2003-2006 from the Chippewa/Pine,
Tittabawassee, and Saginaw Rivers, Midland, MI, USA. Valuesa (ng/kg ww) are
given as the arithmetic meanb ± 1 SD over the range.
RA
UTR
LTR
SR
Chemicalc
n=16
n=23
n=19
n=8
2378-TCDF
23478-PeCDF
12378-PeCDF
234678-HxCDF
0.80±1.0
0.039−3.4
4ND
0.43±0.42
0.073−1.3
3ND
0.56±0.55
0.083−1.8
7ND
0.51±0.25
0.14−0.82
11ND
123789-HxCDF
123678-HxCDF
123478-HxCDF
1234789-HpCDF
1234678-HpCDF
12346789-OCDF
2378-TCDD
12378-PeCDD
123789-HxCDD
16ND
0.70±0.50
0.14−1.5
9ND
1.3±1.4
0.15−4.5
5ND
0.62±0.25
0.23−40
10ND
4.3±6.6
0.16−22
9.2±13
0.22−40
1ND
0.26±0.16
0.086−0.52
7ND
0.28±0.16
0.099−0.50
8ND
0.60±0.38
0.13−1.1
260±490
10−2100
630±960
1.8−3500
290±450
2.5−1300
87±150
3.1−560
250±460
0.31−1900
130±210
0.57−610
110±170
3.4−570
350±750
0.43−3300
180±290
0.81−860
6.9±8.9
0.36−28
22±40
0.69−160
2ND
5.2±9.4
0.24−37
4ND
58±120
1.6−520
2ND
260±560
0.26−2400
1ND
19±33
1.2−140
2ND
120±110
0.31−480
23±18
6.9−48
4ND
21±24
2.2−48
5ND
53±65
0.34−170
2ND
150±240
0.54−710
2ND
38±21
18−67
4ND
370±450
0.38−1200
230±180
22−620
2ND
1.5±0.91
0.15−3.2
520±510
0.39−1200
1ND
6.9±7.2
0.079−18
1ND
9.7±4.2
4.5−13
4ND
11±4.8
5.4−15
1.9±2.3
0.21−7.3
5ND
16±22
1.7−130
87±120
4.8−390
17±28
1.7−130
210±410
19−1900
730±2100
25−10000
2.0±1.9
0.26−7.5
1ND
110±170
3.4−170
3.2±3.9
0.48−16
1.3±0.68
0.33−2.8
2ND
1.9±1.2
0.44−4.9
123678-HxCDD
123478-HxCDD
1234678-HpCDD
12346789-OCDD
Sum PCDD/DF
a
9ND
0.82±0.69
0.16−1.8
8ND
0.35±0.13
0.13−0.43
11ND
6.8±10
0.34−30
64±97
2.0−280
88±130
2.9−390
200±500
11−2400
2ND
4.4±3.0
0.95−13
2ND
0.85±0.53
0.21−1.9
4ND
64±51
0.35−190
4ND
26±10
15−37
4ND
3.2±1.3
1.2−4.1
4ND
140±160
0.30−350
1900±4800
92−23000
3600±8200
280−40000
630±500
3.0−1800
2600±3400
6.4−14000
1300±1400
1.7−3100
3100±3700
9.7−9700
10±20
0.81−96
1.3±1.4
0.19−5.2
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of
arithmetic means
c
TCDF = tetrachlorodibenzofuran; PeCDF = pentachlorodibenzofuran; HxCDF=
hexachlorodibenzofuran; HpCDF = heptachlorodibenzofuran; OCDF =
octachlorodibenzofuran; TCDD = tetrachlorodibenzo-p-dioxin; PeCDD =
pentachlorodibenzo-p-dioxin; HxCDD = hexachlorodibenzo-p-dioxin; HpCDD =
heptachlorodibenzo-p-dioxin; OCDD = octachlorodibenzo-p-dioxin
b
Table S6. Concentrations of seventeen 2,3,7,8-substituted furan and dioxin
congeners in frogs collected during 2005-2006 from the within the Chippewa,
Tittabawassee, and Saginaw River floodplains, Midland, MI, USA. Valuesa (ng/kg
ww) are given as the arithmetic meanb ± 1 SD over the range.
RA
UTR
LTR
SR
Chemicalc
n=29
n=51
n=55
n=12
2378-TCDF
23478-PeCDF
12378-PeCDF
0.44±0.47
0.076−2.2
2ND
0.20±0.10
0.081−0.49
9ND
0.19±0.079
0.10−0.28
24ND
234678-HxCDF
0.13−0.18
27ND
42±68
0.34−370
86±190
5.1−1400
1.6±0.93
0.70−3.5
11±14
0.21−69
30±64
1.9−450
1.3±2.7
0.33−9.7
8.0±13
0.080−75
26±100
1.3−770
0.33±0.16
0.17−0.60
0.65±0.61
0.15−2.8
24ND
1.7±5.9
0.11−37
16ND
5.8
0.57
51ND
1.0±1.5
0.11−7.4
14ND
3.5±6.7
0.16−33
8ND
1.2±0.93
0.20−2.6
42ND
6.3±10
0.23−42
10ND
10±18
0.22−72
10ND
1.3±1.1
0.27−7.4
54ND
2.5±11
0.087−76
4ND
10±50
0.27−370
12ND
123789-HxCDF
29ND
123678-HxCDF
123478-HxCDF
0.11−0.16
27ND
0.20±0.088
0.092−0.34
20ND
1234789-HpCDF
1234678-HpCDF
12346789-OCDF
2378-TCDD
12378-PeCDD
123789-HxCDD
29ND
0.49±0.29
0.16−0.92
24ND
0.72±0.35
0.38−1.2
21ND
0.43±0.28
0.12−1.1
4ND
0.25±0.13
0.12−0.55
9ND
0.18
0.66±0.44
0.20−2.7
1ND
0.30±0.15
0.13−0.70
1.9±3.8
0.23−14
43ND
5.6±8.3
0.29−50
9.9±15
0.21−67
2ND
0.96±0.77
0.20−4.1
1ND
0.57±0.32
0.18−1.6
3ND
0.29±0.081
0.17−0.41
11ND
0.14−1.1
10ND
0.89±1.2
0.27−3.0
7ND
12ND
0.37±0.29
0.19−1.3
0.30
11ND
0.35±0.13
0.20−0.58
1ND
0.37±0.21
0.18−0.91
1ND
123678-HxCDD
28ND
0.30±0.12
0.16−0.43
24ND
123478-HxCDD
1234678-HpCDD
12346789-OCDD
Sum PCDD/DF
a
29ND
0.68±0.57
0.22−2.8
1ND
3.2±3.4
0.57−13
5.4±4.8
0.96−19
33ND
0.74±0.61
0.14−2.6
5ND
0.30±0.12
0.079−0.59
23ND
4.0±5.8
0.29−28
47ND
0.72±0.48
0.23−2.2
13ND
0.26±0.077
0.19−0.42
43ND
4.0±4.2
0.45−22
12ND
0.37±0.33
0.13−1.1
4ND
0.54
31±56
1.3−250
120±180
3.5−920
31±40
2.6−1220
210±450
17−3300
1.5±0.51
0.67−2.3
7.2±6.1
2.8−25
11ND
0.53±0.39
0.20−1.7
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of
arithmetic means
c
TCDF = tetrachlorodibenzofuran; PeCDF = pentachlorodibenzofuran; HxCDF=
hexachlorodibenzofuran; HpCDF = heptachlorodibenzofuran; OCDF =
octachlorodibenzofuran; TCDD = tetrachlorodibenzo-p-dioxin; PeCDD =
pentachlorodibenzo-p-dioxin; HxCDD = hexachlorodibenzo-p-dioxin; HpCDD =
heptachlorodibenzo-p-dioxin; OCDD = octachlorodibenzo-p-dioxin
b
Table S7. Concentrations of seventeen 2,3,7,8-substituted furan and dioxin
congeners in crayfish collected during 2005-2006 from the within the Chippewa,
Tittabawassee, and Saginaw River floodplains, Midland, MI, USA. Valuesa (ng/kg
ww) are given as the arithmetic meanb ± 1 SD over the range.
RA
UTR
LTR
SR
Chemicalc
n=5
n=7
n=8
n=8
2378-TCDF
0.55±0.44
0.19−1.3
60±53
7.4−160
140±74
59−300
25±13
10−51
23478-PeCDF
0.28±0.23
0.051−0.59
1ND
12±9.1
2.6−26
35±27
12−96
3.7±1.8
0.33−9.7
16±14
2.2−39
1ND
0.43±0.26
0.20−0.77
3ND
44±29
16−110
4.4±2.5
1.9−8.2
12378-PeCDF
0.031−0.45
3ND
234678-HxCDF
0.018−0.18
3ND
0.064−0.12
5ND
0.97±0.46
0.47−1.7
1.7±1.6
0.44−4.9
1ND
0.48±0.38
0.19−0.91
5ND
3.9±3.8
1.2−13
5.2±2.6
1.9−8.7
19±17
5.3−57
8ND
0.50±0.24
0.25−0.72
5ND
1.3±0.64
0.76−2.5
0.71±0.52
0.21−1.4
3ND
7.8±9.3
2.3−28
1.7±1.2
0.64−3.6
3ND
26±25
3.3−64
8ND
2.8±2.3
0.77−7.1
13±16
1.8−48
31±31
3.5−87
2.7±2.0
0.73−6.6
0.89±0.19
0.54−1.1
1.3±0.34
0.84−1.8
0.49±0.15
0.30−0.65
0.86±0.38
0.44−1.6
0.91±0.65
0.35−2.1
2ND
0.49±0.19
0.25−0.71
4ND
0.25±0.12
0.15−0.39
0.19−1.6
123789-HxCDF
5ND
123678-HxCDF
123478-HxCDF
0.019−0.41
3ND
0.56±0.45
0.048−0.89
2ND
1234789-HpCDF
1234678-HpCDF
12346789-OCDF
2378-TCDD
12378-PeCDD
123789-HxCDD
5ND
0.47±0.32
0.11−0.68
2ND
0.36±0.20
0.17−0.57
1ND
0.26±0.18
0.056−0.37
2ND
0.23±0.20
0.030−0.44
2ND
8ND
5ND
6ND
1.4±1.3
0.22−3.7
2ND
5ND
0.42±0.32
0.18−0.83
4ND
0.59±0.34
0.24−1.1
3ND
0.14±0.049
0.11−0.20
4ND
5.0±5.8
1.4−18
0.14−0.90
6ND
15±19
1.9−58
8ND
1.4±0.86
0.52−2.9
2.8±2.1
0.88−5.4
5.4±4.6
1.5−11
44±54
8.1−170
160±100
83−340
140±170
14−520
450±380
140−1300
10±6.8
2.7−22
52±27
27−110
123678-HxCDD
5ND
123478-HxCDD
1234678-HpCDD
12346789-OCDD
Sum PCDD/DF
a
8ND
0.36
7ND
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of
arithmetic means
c
TCDF = tetrachlorodibenzofuran; PeCDF = pentachlorodibenzofuran; HxCDF=
hexachlorodibenzofuran; HpCDF = heptachlorodibenzofuran; OCDF =
octachlorodibenzofuran; TCDD = tetrachlorodibenzo-p-dioxin; PeCDD =
pentachlorodibenzo-p-dioxin; HxCDD = hexachlorodibenzo-p-dioxin; HpCDD =
heptachlorodibenzo-p-dioxin; OCDD = octachlorodibenzo-p-dioxin
b
Table S8. Concentrations of seventeen 2,3,7,8-substituted furan and dioxin
congeners in forage fish composites collected during 2004-2007 from the within the
Chippewa, Tittabawassee, and Saginaw River floodplains, Midland, MI, USA.
Valuesa (ng/kg ww) are given as the arithmetic meanb ± 1 SD over the range.
RA
UTR
LTR
SR
Chemicalc
n=2
n=2
n=5
n=4
2378-TCDF
99−140
170±110
53−300
27±8.4
21−40
19−22
35±30
5.9−78
4.5±2.6
2.1−8.0
14−14
31±30
4.3−78
4.0±3.0
2.0−8.3
0.82−0.91
2.9±2.6
0.35−6.3
1ND
0.18±0.21
0.0080−0.42
1ND
2ND
1.5−1.5
0.38−0.65
3ND
4.5±5.2
0.21−13
4ND
0.55±0.53
0.15−1.3
3.1−5.2
19±24
0.84−58
2.0±2.0
0.54−4.9
5.1−5.5
1.3±1.1
0.26−2.6
1ND
8.2±4.5
2.8−13
0.19±0.15
0.063−0.13
1ND
3.7±2.6
1.3−7.1
0.29−0.35
6.5−11
12±8.1
3.0−25
4.5±3.9
1.3−9.8
0.20−0.23
4.7−6.0
4.6±2.6
1.4−10
1.7±0.96
0.94−3.0
0.095−0.13
1.2−1.6
1.2±0.65
0.33−1.9
0.52±0.26
0.28−0.84
0.47−0.49
23478-PeCDF
0.058−0.077
12378-PeCDF
2ND
234678-HxCDF
2ND
123789-HxCDF
123678-HxCDF
2ND
0.055
1ND
123478-HxCDF
2ND
1234789-HpCDF
0.50−0.54
2ND
1234678-HpCDF
0.072−0.092
12346789-OCDF
2378-TCDD
12378-PeCDD
123789-HxCDD
0.33
0.12−0.49
0.063−0.84
2ND
123678-HxCDD
0.88−1.5
2ND
123478-HxCDD
0.52−1.0
2ND
1234678-HpCDD
0.33−0.34
3.6−4.1
2.1−3.0
20−28
3.8−4.6
200−220
12346789-OCDD
Sum PCDD/DF
a
4ND
1.0±0.49
0.39−1.6
1ND
1.2±0.19
0.99−1.4
2ND
5.0±3.2
1.4−10
2ND
0.55±0.31
0.21−0.85
31±14
8.3−44
330±220
81−610
13±11
4.2−28
64±36
36−120
0.040
3ND
1.9±1.2
0.80−3.5
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of
arithmetic means
c
TCDF = tetrachlorodibenzofuran; PeCDF = pentachlorodibenzofuran; HxCDF=
hexachlorodibenzofuran; HpCDF = heptachlorodibenzofuran; OCDF =
octachlorodibenzofuran; TCDD = tetrachlorodibenzo-p-dioxin; PeCDD =
pentachlorodibenzo-p-dioxin; HxCDD = hexachlorodibenzo-p-dioxin; HpCDD =
heptachlorodibenzo-p-dioxin; OCDD = octachlorodibenzo-p-dioxin
b
Table S9. Concentrations of twelve dioxin-like polychlorinated biphenyl congeners
in forage fish composites collected during 2004-2007 from the within the Chippewa,
Tittabawassee, and Saginaw River floodplains, Midland, MI, USA. Valuesa (µg/kg
ww) are given as the arithmetic meanb ± 1 SD over the range.
RA
UTR
LTR
SR
Chemicalc
n=2
n=2
n=5
n=4
PCB 77
0.012−0.016
0.36−0.47
PCB 81
0.0042−0.0059 0.084−0.11
PCB 126
0.0026−0.0033 0.031−0.042
PCB 169
2ND
2ND
0.17−0.22
1.8−3.3
0.012−0.016
0.14−0.27
0.52−0.62
5.7−9.0
0.020−0.022
0.18−0.29
0.069−0.077
0.56−0.84
0.015−0.017
0.14−0.19
0.040−0.040
0.34−0.41
PCB 105
PCB 114
PCB 118
PCB 123
PCB 156
PCB 157
PCB 167
PCB 189
0.0074−0.0087 0.59−0.88
Sum PCB
0.88−1.0
a
b
9.3−15
0.28±0.16
0.12−0.51
0.17±0.20
0.043−0.52
0.95±0.13
0.017−0.33
0.0089±0.010
0.0026−0.021
2ND
7.5±10
1.6−26
0.61±0.85
0.12−2.1
20±26
4.3−66
0.56±0.73
0.097−1.9
2.1±3.0
0.45−7.5
0.45±0.63
0.098−1.6
0.94±1.3
0.23−3.2
0.22±0.33
0.049−0.80
33±44
7.1−110
1.0±0.95
0.22−2.2
0.18±0.12
0.084−0.33
0.061±0.032
0.033−0.099
4ND
6.0±3.1
3.3−9.8
0.55±0.34
0.26−0.95
18±9.7
9.0−29
0.43±0.26
0.21−0.74
1.3±0.46
0.89−1.9
0.27±0.085
0.19−0.37
0.65±0.21
0.48−0.91
0.13±0.055
0.079−0.19
28±15
15−47
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of
arithmetic means
Table S10. Concentrations of twelve dioxin-like polychlorinated biphenyl congeners
in frogs and crayfish collected during 2004-2007 from the within the Chippewa,
Tittabawassee, and Saginaw River floodplains, Midland, MI, USA. Valuesa (µg/kg
ww) are given as the arithmetic meanb ± 1 SD over the range.
Frog
Crayfish
Crayfish
LTR
UTR
LTR
Chemicalc
n=4
n=2
n=1
PCB 77
PCB 81
PCB 126
PCB 169
PCB 105
PCB 114
PCB 118
PCB 123
PCB 156
PCB 157
PCB 167
PCB 189
Sum PCB
a
b
0.011±0.0055
0.004−0.016
0.0039±0.0013
0.0024−0.0054
0.0057±0.0014
0.0037−0.0072
0.0048±0.0017
0.0030−0.0070
0.14±0.080
0.050−0.24
4ND
0.086
0.050−0.063
0.0035
0.0027−0.0031
0.0057
0.0040−0.0073
0.0040
0.0050−0.0080
0.43
0.27−0.58
2ND
0.81±0.38
0.40−1.1
4ND
1.0−1.4
2ND
0.29±0.089
0.20−0.41
4ND
0.86
1ND
2ND
0.14±0.090
0.033−0.20
4ND
0.16
1ND
2ND
1.4±0.34
0.94−1.7
2.2−2.2
1ND
0.92
1ND
0.44
1ND
0.20
1ND
2.1
Values have been rounded and represent only two significant figures
Concentrations below limit of detection treated as zero in the calculation of
arithmetic means