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Wastewater dilution index partially explains observed
polybrominated diphenyl ether flame retardant concentrations
in osprey eggs from Columbia River Basin, 2008–2009
Charles J. Henny •Robert A. Grove •
James L. Kaiser •Branden L. Johnson •
Chad V. Furl •Robert J. Letcher
Accepted: 1 February 2011 / Published online: 22 February 2011
ÓSpringer Science+Business Media, LLC 2011
Abstract Several polybrominated biphenyl ether (PBDE)
congeners were found in all 175 osprey (Pandion halia-
etus) eggs collected from the Columbia River Basin
between 2002 and 2009. RPBDE concentrations in
2008–2009 were highest in osprey eggs from the two
lowest flow rivers studied; however, each river flowed
through relatively large and populous metropolitan areas
(Boise, Idaho and Spokane, Washington). We used the
volume of Wastewater Treatment Plant (WWTP) dis-
charge, a known source of PBDEs, as a measure of human
activity at a location, and combined with river flow (both
converted to millions of gallons/day) created a novel
approach (an approximate Dilution Index) to relate water-
borne contaminants to levels of these contaminants that
reach avian eggs. This approach provided a useful under-
standing of the spatial osprey egg concentration patterns
observed. Individual osprey egg concentrations along the
Upper Willamette River co-varied with the Dilution Index,
while combined egg data (geometric means) from rivers or
segments of rivers showed a strong, significant relationship
to the Dilution Index with one exception, the Boise River.
There, we believe osprey egg concentrations were lower
than expected because Boise River ospreys foraged perhaps
50–75% of the time off the river at ponds and lakes stocked
with fish that contained relatively low RPBDE concentra-
tions. Our limited temporal data at specific localities
(2004–2009) suggests that RPBDE concentrations in
osprey eggs peaked between 2005 and 2007, and then
decreased, perhaps in response to penta- and octa-PBDE
technical mixtures no longer being used in the USA after
2004. Empirical estimates of biomagnification factors
(BMFs) from fish to osprey eggs were 3.76–7.52 on a wet
weight (ww) basis or 4.37–11.0 lipid weight. Our earlier
osprey study suggested that RPBDE egg concentrations
[1,000 ng/g ww may reduce osprey reproductive success.
Only two of the study areas sampled in 2008–2009 con-
tained individual eggs with RPBDE concentrations
[1,000 ng/g, and non-significant (P[0.30) negative
relationships were found between RPBDEs and reproduc-
tive success. Additional monitoring is required to confirm
not only the apparent decline in PBDE concentrations in
osprey eggs that occurred during this study, but also to
better understand the relationship between PBDEs in eggs
and reproductive success.
Keywords Osprey Polybrominated diphenyl ethers
Oregon Washington Idaho Wastewater treatment
plants Biomagnification factors Productivity
Dilution index
Introduction
Polybrominated diphenyl ethers (PBDEs) are compounds
that have been used since the 1970s as additive flame
retardants in thermoplastics, textiles, polyurethane foams
and electronic circuitry. Individual PBDE congeners
C. J. Henny (&)R. A. Grove J. L. Kaiser B. L. Johnson
U.S. Geological Survey, Forest and Rangeland Ecosystem
Science Center, 3200 SW Jefferson Way, Corvallis,
OR 97331, USA
e-mail: hennyc@usgs.gov
C. V. Furl
Washington State Department of Ecology, Environmental
Assessment Program, Olympia, WA 98504, USA
R. J. Letcher
Environment Canada, National Wildlife Research Centre,
Carleton University, Ottawa, ON K1A 0H3, Canada
123
Ecotoxicology (2011) 20:682–697
DOI 10.1007/s10646-011-0608-2
comprise commercially produced technical mixtures. As
the names imply with respect to PBDE congener consti-
tution, the three most widely used types are deca-BDE,
octa-BDE and penta-BDE mixtures. PBDEs persist in the
environment and bioaccumulate and biomagnify up the
food web to the top predatory fish, mammal and bird
species (de Wit 2002), including birds of prey as recently
reviewed by Chen and Hale (2010).
RPBDE concentrations in mountain whitefish (Proso-
pium williamsoni) from the Columbia River increased
12-fold between 1992 and 2000, with a doubling period of
1.6 years (Rayne et al. 2003). Two osprey (Pandion hal-
iaetus) eggs collected on the Columbia River near Castle-
gar, British Columbia in 1997 increased 15-fold over
RPBDE concentrations reported for two collected in the
area in 1991, prompting concerns over toxicological effects
if residues continued to increase (Elliott et al. 2005).
Analyses of fish collected in the Great Lakes between 1979
and 2005 showed that while long-term trends of RPBDE
concentrations in each lake and fish species increased
exponentially beginning in the early 1980s, a leveling-off
or decrease of concentrations started in the mid-1990s, but
with variability among lakes and species (Batterman et al.
2007). Herring gull (Larus argentatus) eggs collected from
the Great Lakes between 1982 and 2006 showed a similar
pattern, with no increasing trend post-2000 (Gauthier et al.
2008). Though these later studies indicate PBDEs may be
leveling off or declining, Braune et al. (2007) reported
PBDE concentrations in ivory gull (Pagophila eburnea)
eggs from the Canadian arctic, steadily increased between
1976 and 2004, and the increase was primarily driven by
BDE-47.
Between 2002 and 2007, all 120 osprey eggs collected
from Oregon and Washington (including 82 from Colum-
bia River Basin) contained PBDEs (Henny et al. 2009b). In
contrast to DDE and other banned pesticides and poly-
chlorinated biphenyls (PCBs), which decreased in recent
years in fish-eating osprey eggs from the Columbia River
Basin and elsewhere (Henny et al. 2008,2009a,2010),
PBDEs increased in osprey eggs from Puget Sound,
Washington (2003 vs. 2006/2007) and the Lower Columbia
River, Oregon/Washington (2004 vs. 2007) (Henny et al.
2009b). River Mile (RM) is used in this report to define
locations on rivers. RM 0 begins at the ocean or where the
river joins another river. Only in 2006 and 2007 (Upper
Willamette River, RM 61–157 and Lower Columbia River,
RM 29–84) did PBDE concentrations in individual osprey
eggs exceed 1,000 ng/g ww. In those 2 years, there was
evidence that PBDE concentrations may adversely affect
osprey reproductive rates. We hypothesized in our earlier
paper that a small river with low flow associated with a
high human population may lead to higher PBDE con-
centrations in osprey eggs.
Studies of biosolids from Wastewater Treatment Plants
(WWTPs) (Hale et al. 2001; Anderson and MacRae 2006;
Sullivan et al. 2007) reported the presence of extremely
high concentrations of PBDEs. Song et al. (2006) reported
that the bulk (*91%) of the average RPBDE concentration
(RPBDEs; BDE 47, 99, 100, 153 and 154) leaving/entering
the WWTP on the Little River and discharging into the
upper Detroit River in Windsor, Ontario, Canada, ended up
in the primary sludge and waste activated sludge, while the
remaining *9% was discharged with the final effluent.
Thus, liquid releases into rivers from WWTPs were sus-
pected important PBDE sources.
The European Union banned the use of octa- and penta-
BDEs, and the American manufacturer voluntarily stopped
production in 2004 (Manugian 2004). The only PBDE
mixture currently used in the US is the technical deca-BDE
product. The State of Washington’s PBDE Law (RCW
70.76) legislated bans on certain uses of deca-BDE (no use
in mattresses after January 1, 2008, and no use in televi-
sions, computers and upholstered furniture after January 1,
2011). Evidence indicates, including in Great Lakes her-
ring gulls (Gauthier et al. 2008), that deca-BDE can
undergo reductive debromination in the environment to
congeners BDE-206, 207, 208, which can then be further
debrominated (Gerecke et al. 2005; Stapleton et al. 2006;
Kuo et al. 2010). With changes in PBDE use in the United
States occurring post-2004, with evidence that PBDE
concentrations may adversely affect osprey reproductive
rates, and with published long-term studies cited above
terminated in 2007 or earlier, we were especially con-
cerned about possible recent changes (2008, 2009) in
osprey egg concentrations.
This study was designed to: (1) describe regional PBDE
and other brominated flame retardant concentration pat-
terns in osprey eggs (one sample egg collected at random
per nest) and congener profiles at locations within the
Columbia River Basin in Oregon, Washington and Idaho in
2008 and 2009, (2) evaluate a possible relationship
between observed PBDE residue concentrations in osprey
eggs with river flow (cubic feet/second, converted to mil-
lions gallons/day, MGD) and wastewater discharge (MGD)
from major WWTPs, i.e., a dilution effect, (3) investigate
temporal trends in PBDE concentrations and congener
profiles in osprey eggs collected during this study and
earlier investigations at four locations (Upper Willamette
River 2006 vs. 2008, and three segments of the Lower
Columbia River between 2004 and 2009), (4) study PBDE
residue concentrations in fish and osprey eggs from the
Spokane and Boise Rivers to estimate biomagnification
factors from fish to osprey eggs, and (5) investigate
reproductive success (number of young produced) at each
nest to determine if an association exists with PBDE con-
centrations in the sample egg from that nest.
Wastewater dilution index 683
123
Materials and methods
Four of the original study areas (Upper Willamette River
and three segments of Lower Columbia River) were re-
sampled in this study (2008–2009) to determine residue
trends, and additional study areas were added. Washington
Department of Ecology reported that fish from the Spokane
River contained the highest PBDE concentrations in the
state (Johnson et al. 2006); and Willamette River osprey
eggs collected during the earlier study (the highest con-
centrations reported) were only obtained from the upstream
portion of the river with relatively high human populations
and generally lower flows. Thus, in addition to the original
study areas, two smaller tributaries of the Upper Columbia
River Basin (Spokane River in eastern Washington and
Boise River in western Idaho) and a series of small Ref-
erence Lakes south of Spokane, as well as the Lower
Willamette River (Portland Harbor and Multnomah Chan-
nel, Oregon) were added (Fig. 1). Both of the upper basin
tributaries have relatively low river flows (less water
dilution effect) and relatively high human populations,
while the Portland Harbor and Multnomah Channel rep-
resent urban areas with large river flow near the mouth of
the Willamette River.
We located occupied osprey nests by boat, car and air-
craft. Nests were visited at least two to four times, but often
at weekly intervals to determine nesting activity and
reproductive success following definitions of Postupalsky
(1977). One partially incubated egg (usually about 10 days
into incubation) was randomly collected from each nest
(usually 3-eggs laid per clutch) to determine exposure to
contaminants. Egg contents were placed in chemically
clean jars and frozen for subsequent contaminant analysis.
In this study we evaluated reproductive success at indi-
vidual osprey nests by comparing residue concentrations in
a sample egg collected from each nest to the number of
advanced-age young (40–45 days) produced from the
remaining eggs in the nest, i.e., the sample egg technique
(Blus 1984). A helicopter flight scheduling conflict on the
Spokane River in 2009 resulted in an earlier than normal
flight. This resulted in some young being smaller than
usual, with the final production count perhaps biased
slightly high.
We report on major, persistent and bioaccumulative
PBDEs in 93 osprey eggs randomly collected (one per
nest) during this 2008–2009 study in Oregon, Washington
and Idaho, and compare them to 82 eggs previously
reported from the Columbia River Basin between 2002
and 2007 (Henny et al. 2009b). Contaminants other than
PBDEs can potentially influence osprey reproductive
success. Osprey literature was reviewed to evaluate criti-
cal concentration levels for reproductive effects of orga-
nochlorine pesticides, polychlorinated biphenyls, dioxins,
furans and mercury (see Henny et al. 2008). However, of
the eggs collected earlier (2002–2007), only four con-
tained other contaminants, in this case p,p0-DDE, at con-
centrations believed to adversely influence osprey
productivity. The four eggs all came from nests along the
Yakima River (an intensive agriculture area) in 2002, and
were excluded from the earlier analysis (Henny et al.
2009b) and not used in this study. All eggs collected in
2008 were routinely analyzed for several legacy contam-
inants (organochlorine pesticides and 42 polychlorinated
biphenyl congeners), but no concentrations were found at
levels believed to influence osprey productivity, with
concentrations continuing their pattern of decrease over
time (see Henny et al. 2010). No eggs were analyzed for
legacy contaminants in 2009.
As previously mentioned, liquid releases from WWTPs
were suspected important PBDE sources. Furthermore, the
size of human populations associated with various
WWTPs in this study were highly correlated with the
volume of wastewater discharge (Fig. 2). We do not
believe that effluent entering the rivers from WWTPs is
the only PBDE source, but the volume provides an
approximate measure of human and perhaps industrial
activity in a given area. PBDE concentrations in effluent
could be modified by degree of wastewater treatment, but
for purposes of this paper unaltered discharge values were
used. Data provided 12 July 2010 by Daniel Wise,
Hydrologist, U.S. Geological Survey (USGS), Portland,
Oregon, listed the estimated 2002 mean discharge in
Fig. 1 Map of the Columbia Basin study area. (A) Lower Columbia
River (RM 29–84), (B) Lower Columbia River (RM 85–122),
(C) Lower Columbia River (RM 124–143). Open circles represent
urban areas
684 C. J. Henny et al.
123
millions gallons/day (MGD) for 216 WWTPs in the
Pacific Northwest. About one-half of the WWTPs dis-
charge over 1.0 MGD. Although this list was incomplete,
all of the major WWTPs were included and probably most
of the smaller facilities. The USGS stream flow estimates
(converted from cubic feet/second to MGD) for the
receiving rivers at each WWTP site represent USGS
modeled mean annual values for 1974–2004. Although
years for the discharge data from WWTPs (2002), the
average stream flow estimates (1974–2004) and osprey
egg concentrations (2008–2009) were not the same, we
attempt to understand general patterns in this analyses and
believe our simplified approach is useful. Then, the dis-
charge from each WWTP divided by the stream flow
estimate at each site was multiplied by 1,000 to provide a
Dilution Index for each WWTP to compare with observed
osprey RPBDE egg concentrations.
Dilution Index ¼ðWastewater Discharge[MGD]=
River Flow[MGD]Þ1;000
This Dilution Index permits an evaluation of osprey
RPBDE egg concentrations at various river miles along a
specific river, or a general comparison of geometric mean
egg concentrations among rivers. We suspected that
RPBDE concentrations in osprey eggs may be a function of
this approximate index. This initial approximation
approach assumes that wastewater discharge from all
WWTPs contains equal concentrations of RPBDEs, which
may not be true. Concentrations at specific WWTPs could
depend upon degree of wastewater treatment or unique
PBDE use patterns; however, this simple evaluation should
be instructive. Oregon Department of Environmental
Quality is now in the process of evaluating PBDE con-
centrations in discharges at selected WWTPs in Oregon
(J. Coyle, personal comm.).
Analytical chemistry
Eggs collected in 2008 and 2009 were shipped to the
National Wildlife Research Centre (NWRC), Science and
Technology Branch, Environment Canada, Carleton Uni-
versity, Ottawa, Ontario for analysis by the Letcher
Organics Research Lab. As described elsewhere (Gauthier
et al. 2007,2008), sample eggs were analyzed for BDE
congeners: 17, 28, 47, 49, 66, 85, 99, 100, 138, 153, 154,
183, 190, 209 and total-a-HBCD, and polybrominated
biphenyls (BB) 101 and 153 (co-eluted with BDE154). In
2009, an additional twenty BDE congeners and six non-
PBDE, brominated flame retardants (BFRs) were evaluated
(Table 1), but were either not detected or found at very
low, parts-per-billion concentrations and, for comparative
purposes, were not reported or discussed further in this
paper (except see Biomagnification Factors where BDE 71
and 184 were used).
Egg analysis was comprehensively described in Gau-
thier et al. (2008). Briefly, homogenized osprey egg sam-
ples (about 1 g) were spiked with BDE30, BDE71,
BDE156, and/or
13
C
12
-BDE-209 internal standards
(200 pg/ll each and in a 100 ll spike). After clean-up and
isolation of the PBDE/BFR containing fraction, the bro-
minated compounds were determined by GC–MS (in the
electron capture negative ionization (ECNI) mode). An
Agilent Gas Chromatograph (GC) 6890 equipped with a
5973 quadrupole mass spectrometer (MS) detector was
used. Full details are detailed in Gauthier et al. (2008), but
briefly, bromine-containing compounds were identified
based on their
79
Br and
81
Br anion isotopic response
(overwhelmingly the major fragment ion), and on the
basis of their full chromatographically resolved retention
times on a DB-5HTcolumn (15 m 90.25 mm i.d. 9film
thickness of 0.10 lm), and relative to that of authentic
standards, i.e., total-a-HBCD, BB-101, and PBDEs (14
congeners). The a-HBCD is total-a-HBCD as b- and
c-HBCD thermally isomerize to a-HBCD at GC tempera-
tures [160°C.
Quantification of the brominated compounds was per-
formed using an internal standard method based on the
relative ECNI response factor (RRF) of the corresponding
internal standard and target compounds. The quantification
analysis was based on m/z 79 and 81 for the bromine anion
fragment, and the response of the internal standard BDE30,
for the fourteen PBDE congeners, BB-101 and HBCD,
which were of focus in the present study. In the case of
BDE209, the m/z 487 and 489 isotope ions of the abundant
pentabromophenoxy anion fragment were used for identi-
fication and quantification. Ion m/z 495 was used for the
quantification (and m/z 497 for identity confirmation) of
the internal standard of
13
C
12
-BDE-209, and used as the
internal standard for BDE-209.
Population x 1,000
0 50 100 150 200 250 300
Average Effluent Discharge(MGD)
0
10
20
30
40
50
Newberg, OR
Albany, OR
Corvallis, OR
Boise/Eagle, ID
Salem, OR
Eugene, OR
Spokane, WA
Y = 2.256 + 0.153X
r2
= 0.8833, n = 7
P = 0.0017
Fig. 2 Relationship between human population size and Wastewater.
Treatment Plant effluent discharge at Columbia Basin osprey study
areas. MGD million gallons per day
Wastewater dilution index 685
123
Data analysis and quality control
In general, and as surrogates of all PBDEs and non-PBDE
BFRs that were determined, the recoveries of BDE30,
BDE71, BDE156 and/or
13
C
12
-BDE209 internal/recovery
standards that were used were close to or greater than 75%.
Concentrations were inherently recovery-corrected as an
internal standard method of quantification was used to
reduce heterogeneity within and between analyte classes.
Method blank samples were analyzed with each batch of
five samples. The method limit of quantification was gen-
erally about 0.005 ng/g wet weight (ww). To assess the
precision and accuracy of the concentrations of major
PBDEs under study (and by extension to other BFR), an
Table 1 The incidence, geometric mean and highest concentration (ng/g, ww) of additional PBDE congeners and other brominated flame
retardants analyzed in osprey eggs from Lower Columbia River (LCR), Spokane River (SR) and Reference Lakes near Spokane, 2009
Location (N) Incidence, geometric mean, high concentration
LCR RM 29-84 (10) LCR RM 124-143 (5) SR upper segment (8) SR lower segment (7) Reference lakes (8)
BDE-2 1, NC, 0.35 ND ND ND ND
BDE-3 ND ND ND 1, NC, 1.66 ND
BDE-7 ND ND ND 1, NC, 2.29 1, NC, 0.44
BDE-15
a
2, NC, 1.01 ND 1, NC, 0.40 4, 0.06, 2.29 ND
BDE-71 2, NC, 1.01 ND ND 3, NC, 6.22 1, NC, 0.32
BDE-77
b
ND ND 3, NC, 0.99 4, 0.07, 1.88 ND
BDE-119 4, NC, 3.58 2, NC, 1.54 8, 1.17, 8.34 7, 2.95, 14.2 1, NC, 0.35
BDE-140 5, 0.04, 1.10 ND 6, 0.16, 2.38 6, 0.40, 7.04 1, NC, 0.35
BDE-155 10, 1.74, 5.42 5, 0.80, 1.33 7, 0.76, 4.49 7, 3.01, 9.74 1, NC, 0.79
BDE-170 1, NC, 1.01 ND 1, NC, 0.56 ND 1, NC, 0.94
BDE-179 1, NC, 0.36 ND 1, NC, 0.42 1, NC, 0.51 ND
BDE-184 ND ND ND 1, NC, 0.74 ND
BDE-188 2, NC, 2.34 ND 1, NC, 3.85 3, NC, 1.88 ND
BDE-194 ND ND ND ND 2, NC, 3.51
BDE-195 ND ND 1, NC, 0.32 ND 1, NC, 0.51
BDE-196 ND ND ND ND 1, NC, 0.74
BDE-197 ND ND 1, NC, 0.37 1, NC, 0.90 ND
BDE-201 ND ND 1, NC, 0.82 2, NC, 2.05 ND
BDE-202 4, NC, 0.74 ND 1, NC, 1.56 4, 0.07, 3.19 ND
BDE-203 1, NC, 0.92 ND ND ND ND
PBEB ND ND ND 1, NC, 0.5 ND
PBAE 1, NC, 0.6 ND ND 3, NC, 1.2 ND
HBB ND ND ND 3, NC, 4.3 ND
BB-101 7, 0.16, 1.1 ND 1, NC, 0.7 3, NC, 3.1 1, NC, 0.5
PBBA 1, NC, 0.5 ND ND 2, NC, 2.6 ND
HBCD 1, NC, 3.1 ND ND ND ND
BTBPE ND ND ND ND 1, NC, 0.5
OBTMI ND ND 2, NC, 0.5 1, NC, 0.8 2, NC, 0.6
Other BDE congeners analyzed but not detected included 1, 10, 28
c
, 54, 139, 171
d
, 180, 181, 182, 191, 205, 206, 207, 208
a
BDE-15 coeluted with b-TBECH
b
BDE-77 coeluted with BB-101
c
BDE-28 coeluted with PBT
d
BDE-171 coeluted with BDE-190
Additional non-PBDE flame retardants analyzed and not detected included b-TBECH, PBT
d
, TBPAE, a-TBECH, pTBX, TBCT, and DBDPE
ND not detected, NC not calculated, present in\50% of eggs, BB-101 brominated biphenyl-101, HBCD hexabromocyclododecane, TBECH 1,2-
dibomo-4-(1,2-dibromoethyl)-cyclohexane, PBT pentabromotoluene, TBPAE 2,4,6-tribromo allyl ether, pTBX tetrabromo-p-xylene, TBCT
tetrabromochlorotoluene, PBEB pentabromoethylbenzene, PBPAE pentabromophenyl allyl ether, HBB hexabromobenzene, PBBA pentabro-
mobenzyl acrylate, BTBPE 1,2-bis-(2,4,6-tribromophenoxy)ethane, OBTMI octabromo-1,3,3-trimethyl-1-phenyl-indane, DBDPE decabromodi-
phenyl ethane
686 C. J. Henny et al.
123
in-house reference material (IHRM) of double-crested
cormorant (Phalacrocorax auritus) egg pool homogenate
was analyzed (n=5 replicates), where one IHRM sample
was analyzed per batch of osprey egg samples. Also, a
standard reference material (SRM) of NIST 1947 Lake
Michigan Fish Tissue homogenate was analyzed (n=5
replicates), where one SRM sample was analyzed per batch
of osprey egg samples. For both the IHRM and SRM used,
good reproducibility of PBDEs was obtained with a %
RSDs of \10%. For the NIST 1947 SRM, concentrations
of applicable PBDEs were also within 10% of the actual
NIST values.
PBDE residue concentrations in eggs were corrected to
an approximate fresh wet weight using egg volumes
determined by water displacement (Stickel et al. 1973), and
reported as geometric means and log-transformed for sta-
tistical analyses. Because of unequal sample sizes, the
General Linear Models Procedure (SAS Institute, Cary,
NC, 2003) was used for analysis of variance. Tukey’s
Studentized Range Test (a=0.05) was used to separate
means. We used the Jonckheere–Terpstra Test with a one-
sided test, because a priori we wanted to test for a negative
association in productivity versus RPBDE concentrations
in the sample egg from each nest (Hollander and Wolfe
1973). Unless otherwise noted, differences were considered
significant when PB0.05.
Results and discussion
Regional pattern in osprey egg RPBDE concentrations,
2008–2009
Osprey eggs collected in the Pacific Northwest in
2002–2007 indicated that RPBDEs were lowest from the
forested headwater reservoirs of the Willamette River,
while those from the Upper Willamette River (RM 61–157)
contained the highest concentrations (Henny et al. 2009b).
Concentrations in eggs from the Columbia River progres-
sively increased downstream from rural Umatilla, OR (RM
286) to Skamokawa, WA (RM 29) downstream of Port-
land, OR and Vancouver, WA metropolitan areas, which
suggested additive PBDE sources along the river.
We collected osprey eggs in 2008–2009 at several of the
same river reaches sampled in earlier years, but also new
locations (Boise River, Spokane River, Portland Harbor
and Multnomah Channel [lower Willamette River], and
Reference Lakes located south of the city of Spokane in
Northeastern Washington) (Fig. 1). Eggs from the two
smaller rivers (Boise R. and Spokane R.) flowing through
relatively large metropolitan areas contained the highest
RPBDE concentrations (893 and 616 ng/g) in 2008 and
2009, with the Reference Lakes (61.9 ng/g) being the
lowest (Table 2; Fig. 3). RPBDE egg concentrations at the
other sites (Lower Columbia River, Portland Harbor and
Multnomah Channel, and Upper Willamette River) were all
within a relatively narrow range (170–427 ng/g). However,
consistent with our earlier findings in 2002–2007 (Henny
et al. 2009b), the lower segments of the Columbia River in
both 2008—RM 29–84 (427 ng/g) versus RM 85–122
(308 ng/g), and 2009—RM 29–84 (308 ng/g) versus RM
124–143 (170 ng/g), contained higher RPBDE concentra-
tions (Fig. 4). Eggs from 2008 collected at Portland Harbor
(378 ng/g) and Multnomah Channel (262 ng/g) near the
mouth of the Willamette River were similar to those
from the adjacent Lower Columbia River (RM 85–122)
(308 ng/g) and the Upper Willamette River (RM 69–181)
(405 ng/g).
RPBDEs in osprey eggs, wastewater treatment plants
and river flow
In the earlier study (Henny et al. 2009b), differences in
RPBDE concentrations in osprey eggs along three rivers
studied (Columbia, Willamette and Yakima) seemed to
reflect differences in river flow (as a function of a dilution
effect) and the extent of human population and industry
(source inputs) along the rivers. We attempted to further
understand the observed RPBDE concentrations in osprey
eggs collected at fairly regular intervals downstream, as
nest sites permitted, of several WWTPs, e.g., see Fig. 5.
We evaluated the amount of wastewater discharge from
each WWTP (suspected important PBDE source based
upon high concentrations in WWTP biosolids and final
effluent, see Song et al. 2006) and river flow data at the site
of each WWTP with our Dilution Index.
Dilution based upon river flow and WWTP discharges
may be less complicated to evaluate in terms of influence
on osprey RPBDE egg concentrations at the upper portions
of the three smaller rivers studied (Willamette, Boise and
Spokane) in the Columbia River Basin. The main stem of
the lower Columbia River may be influenced by many
WWTPs. The largest series of 23 osprey eggs was collected
along 112 River Miles of the Upper Willamette River in
2008 (Fig. 5). The WWTPs at both Eugene/Springfield and
Salem had similar discharges (37.05 and 37.13 MGD,
respectively); however, the flow of the river was consid-
erably higher at Salem because additional tributaries flo-
wed into the river upstream of Salem. Therefore, with the
added flow, the WWTP discharge was more diluted at
Salem. Both Corvallis and Albany are much smaller cities
with lower WWTP discharges (9.16 and 8.26 MGD,
respectively) into the river. Individual osprey egg con-
centrations along the Willamette River co-varied with the
dilution gradient based upon major WWTP inputs (Fig. 5).
Ten osprey eggs collected in the same general area in 2006
Wastewater dilution index 687
123
Table 2 Geometric means and ranges (in parentheses) of PBDE concentrations (ng/g, ww) in osprey eggs collected from rivers and lakes in the Columbia Basin of the Pacific Northwest,
2008–2009
Location Year N% Lipid PBDE congener
17 28 47 49 66 85
Boise R. (RM 19–45) 2008 11 3.1 3.19 A (1.35–7.05) 12.1 A (6.51–30.4) 383 A (213–807) 2.99 AB (1.55–6.00) 6.48 A (2.73–19.5) NC [1] (ND-0.48)
Lower Columbia R. (RM 29–84) 2008 6 3.0 0.48 B (0.28–0.81) 3.65 B (2.11–7.30) 254 AB (176–411) 0.41 C (ND-1.14) 0.33 B (ND-1.14) ND
Lower Columbia R. (RM 29–84) 2009 10 2.9 1.73 AB (0.44–4.78) 2.96 BC (1.54–7.81) 147 BC (108–292) 0.46 C (ND-1.55) 0.70 AB (ND-9.19) NC [2] (ND-0.55)
Lower Columbia R. (RM 85–122) 2008 5 2.8 0.46 B (0.25–0.66) 3.78 B (1.72–9.66) 184 ABC (95.0–311) 0.59 BC (0.30–0.97) 0.55 B (0.35–0.79) ND
Lower Columbia R. (RM 124–143) 2009 5 2.9 NC [2] (ND-1.24) 1.20 C (0.70–1.95) 91.6 C (70.4–145) 0.32 C (ND-0.54) 0.51 B (ND-2.05) ND
Upper Willamette R. (RM 69–178) 2008 23 2.9 1.39 AB (0.24–7.37) 3.88 B (0.91–13.9) 250 AB (90.0–523) 0.38 C (ND-2.04) 0.33 B (ND-2.57) ND
Multnomah Channel, OR 2008 5 2.4 1.35 AB (0.80–2.24) 4.27 AB (2.58–8.99) 163 BC (114–219) 0.78 ABC (0.45–1.89) 0.48 B (0.32–0.99) ND
Portland Harbor, OR 2008 5 3.2 0.87 AB (0.23–2.32) 2.67 BC (0.82–3.97) 200 AB (123–314) 0.73 BC (0.33–1.03) 0.65 B (0.35–0.95) ND
Spokane R. (RM 47–67) 2009 7 3.7 2.87 A (0.96–27.7) 4.99 AB (2.17–16.9) 295 AB (207–494) 4.46 A (1.86–10.7) 2.82 AB (ND-29.8) ND
Spokane R. (RM 68–96) 2009 8 3.4 1.16 AB (ND-4.44) 1.83 BC (0.49–8.61) 263 AB (90.0–678) 1.83 ABC (ND-3.99) 2.82 AB (0.32–22.4) NC [1] (ND-0.63)
Reference Lakes, Spokane, WA 2009 8 3.3 NC [1] (ND-0.32) NC [1] (ND-0.35) 32.1D (16.1–59.4) NC [3] (ND-2.19) 0.38 B (ND-1.23) NC [1] (ND-0.40)
Location PBDE congener
99 100 138 153 154/BB 153 183 RPBDEs
Boise R. (RM 19–45) 270 A (119–728) 126 A (68.4–298) 0.40 A (ND-1.23) 49.3 AB (19.7–176) 38.5 AB (16.2–102) 0.53 A (0.28–1.48) 893 A (536–2,171)
Lower Columbia R. (RM 29–84) 20.2 DE (14.2–30.8) 93.6 AB (61.9–179) NC [1] (ND-0.27) 26.0 ABC (15.7–39.6) 26.4 BC (16.5–52.8) NC [2] (ND-0.17) 427 ABC (330–723)
Lower Columbia R. (RM 29–84) 23.0 DE (11.2–49.0) 77.5 AB (37.7–211) NC [2] (ND-0.63) 20.6 ABC (1.95–97.4) 24.8 BC (9.82–82.3) ND 308 CD (172–747)
Lower Columbia R. (RM 85–122) 17.1 DE (9.45–30.8) 66.7 AB (28.8–120) NC [1] (ND-0.18) 13.6 BCD (4.23–25.7) 18.5 BC (5.93–31.6) 0.09 B (ND-0.21) 308 CD (148–523)
Lower Columbia R. (RM 124–143) 11.5 E (2.78–31.0) 36.8 B (18.0–67.2) NC [1] (ND-0.52) 10.7 CD (3.32–18.9) 10.9 CD (4.22–18.8) ND 170 D (106–265)
Upper Willamette R. (RM 69–181) 31.6 CDE (5.29–201) 61.4 AB (16.4–163) NC [3] (ND-1.30) 19.4 ABC (3.37–75.5) 23.1 BC (4.75–70.8) NC [9] (ND-0.38) 405 ABC (125–980)
Multnomah Channel, OR 18.2 DE (8.91–25.0) 51.3 AB (33.4–71.0) NC [1] (ND-0.33) 9.45 CD (6.95–11.7) 11.9 BCD (9.03–14.6) ND 262 CD (186–351)
Portland Harbor, OR 44.8 BCD (14.8–78.0) 67.4 AB (21.4–120) NC [2] (ND-1.46) 21.1 ABC (4.11–58.3) 30.2 ABC (7.41–87.4) 0.15 AB (ND-0.45) 378 BCD (172–665)
Spokane R. (RM 47–67) 131 AB (51.0–396) 131 A (72.0–294) 0.43 A (ND-1.64) 67.2 A (22.0–228) 90.4 A (34.8–251) 0.53 A (ND-3.93) 749 AB (401–1,674)
Spokane R. (RM 68–96) 88.3 ABC (17.7–210) 73.8 AB (19.3–331) NC [1] (ND-2.26) 35.6 ABC (8.91–78.5) 36.3 ABC (8.75–68.7) NC [3] (ND-0.82) 518 ABC (147–1,391)
Reference Lakes, Spokane, WA 9.50 E (1.14–31.0) 7.03 C (3.20–16.3) NC [3] (ND-1.03) 3.47 D (0.68–14.5) 4.51 D (1.74–15.1) ND 61.9 E (33.2–120)
Congeners 190 and 209 were not detected in any samples. RPBDE =sum of BDE congeners 17, 28, 47, 66, 85, 99, 100, 138, 153, 154/BB153, and 183. BDE 154 co-eluted with BB153. NC not calculated (\50%
above detection limit), ND not detected, number of samples with detectable residues shown in []. Percent lipid presented as arithmetic mean. Columns sharing the same letter are not significantly different,
Tukey’s Studentized Range (a=0.05)
688 C. J. Henny et al.
123
Location
BR 2008 RM 19-45
SR 2009 RM 47-96
LCR RM 29-84 2008
UWR 2008
PH 2008
LCR RM 85-122 2008
LCR RM 29-84 2009
MC 2008
LCR RM 124-143 2009
REF
Osprey Egg ΣPBDEs (ng/g, ww)
0
200
400
600
800
1000
A
AB
ABC ABC BCD
BCD BCD
CD
D
E
11
15
623 5
510
5
5
8
Fig. 3 RPBDE concentrations
(geo. means) in osprey eggs
collected from the Columbia
River Basin, 2008–2009. Bars
sharing the same letters are not
significantly different from each
other (alpha =0.05). Nvalues
shown inside bars.BR Boise
River, SR Spokane River, LCR
Lower Columbia River, MC
Multnomah Channel, PH
Portland Harbor, REF
Reference Lakes near Spokane,
WA., UWR Upper Willamette
River, RM River Mile
River Mile
20 40 60 80 100 120 140
Osprey egg ΣPBDEs (ng/g, ww)
0
200
400
600
800
1000
1200
1400 2004
2007
2008
2009
Longview
St.Helens
Portland/
Vancouver
Bonneville
Dam
Y = 987.8(e-0.010X)
r2
= 0.2802, n = 77
P < 0.0001
Fig. 4 Relationship between River Mile and RPBDE concentrations in osprey eggs along the Lower Columbia River (data from 2004, 2007,
2008, 2009)
6080100120140160180
0
200
400
600
800
1000
1200
1400
1600
1800
2000
River Mile
0
1
2
3
4
5
6
7
Osprey Egg ΣPBDEs (ng/g, ww)
Dilution Index
Eugene
Corvallis
Albany
Salem
Newberg
Fig. 5 Relationship between
major municipal Wastewater
Treatment Plant (WWTP)
inputs (MGD) as a percentage
of river flow (MGD) 91,000
(Dilution Index, open squares,
dashed line) and RPBDE
concentrations in individual
osprey eggs collected along the
Upper Willamette River,
Oregon in 2006 (open circles,
dotted line) and 2008 (closed
circles,solid line). MGD
million gallons per day
Wastewater dilution index 689
123
contained significantly higher RPBDE concentrations (see
later Results), but showed the same spatial pattern along
the river.
Data from the Upper Willamette River, Boise River
and Spokane River were then evaluated together in an
attempt to better understand relationships among WWTP
discharges, river flow and osprey egg concentrations
(Fig. 6). To evaluate the data obtained from the three
smaller rivers into one analysis, the rivers were divided
into segments. The two smaller rivers studied in 2008 and
2009 had shorter study areas (Boise River with 26 RMs
and Spokane River with 49 RMs) with fewer osprey eggs
collected, 11 and 15, respectively. All Boise River data
were combined together (no data collected above the two
Boise WWTPs, while the Spokane River was subdivided
into two segments (above and below the WWTP at
Spokane). The Reference Lakes south of Spokane, and at
least 17 miles from the Spokane River, likely represent
atmospheric-sourced RPBDE inputs (no WWTPs nearby,
and at least with legacy contaminants, concentrations in
osprey eggs reflect the breeding grounds, not the winter-
ing grounds, see Elliott et al. 2007). The study areas of
the longer Willamette River (see Fig. 5) were subdivided
into three segments (Eugene/Springfield, Corvallis/
Albany, and Salem segments) with splits occurring near
Corvallis and Salem.
Egg residue concentrations from Boise River ospreys
did not follow the pattern observed at the other study
areas (Fig. 6), i.e., egg concentrations were much lower
than expected given the Dilution Index measurements
based upon WWTP discharge and river flow. The rela-
tionship observed among the other study areas, excluding
the Boise River, shows a strong linear relationship
(Fig. 6). The Boise River, when compared to the other
rivers studied, is unique because of the large number of
adjacent ponds and lakes stocked with fish. We believe
that perhaps 50–75% of osprey foraging in the Boise
River study area occurred off river on relatively clean fish
which accounts for the much lower RPBDE egg con-
centrations observed when compared to the expected
relationship based upon the other two rivers. Few off-river
foraging sites were available along the Spokane River and
for the nesting pairs studied along the Willamette River.
The maximum RPBDE concentration recorded in an
osprey egg (2,171 ng/g) during this study was from the
Boise River and approximated the Boise River mean
value (2,241 ng/g) predicted by the equation in Fig. 6.
The egg probably represents a pair that consistently for-
aged in the Boise River. Furthermore, 5 of 11 eggs from
the Boise River contained RPBDEs [1,000 ng/g. Thus,
the high RPBDE concentration predicted for the Boise
River osprey eggs was reached with one pair, while other
pairs fell short (based upon observed egg concentrations)
providing evidence for varying degrees of off-river
foraging.
The high flow Lower Columbia River (RM 85–122)
with a river flow estimated at 120,309–141,640 MGD
between Troutdale and Portland/Vancouver (especially
when compared to the low flow Boise River at 835 MGD
and Spokane River at 4,388 MGD) and a combined WWTP
discharge in that Columbia River segment of 106.02 MGD
resulted in a Dilution Index of 0.75–0.88 (mean 0.815).
Osprey eggs from that segment were collected in 2008 (see
Point 8 in Fig. 6, which was not used in the equation).
Somewhat to our surprise, the observed geometric mean
RPBDE egg concentration in 2008 (308 ng/g) for ospreys
was a good fit with the expected findings based upon the
smaller rivers (277 ng/g). Further upstream (RM 124–143),
where limited WWTP discharge occurs, in 2009 egg con-
centrations were lower (170 ng/g), in fact, only 108 ng/g
above that reported in eggs from our Reference Lakes in
2009, or only 73 ng/g above Willamette Headwater Res-
ervoirs in 2002 (Henny et al. 2009b). Downstream from
RM 85–122 at RM 29–84 in 2008 osprey egg concentra-
tions were higher (427 ng/g), but decreased in 2009 to
308 ng/g. Additional WWTPs exist downstream of RM 85,
which may account for the increase in 2008; however, it
needs to be noted that this portion of the river is influenced
by tide which also may be involved. The same general
downstream pattern of increase in osprey eggs from the
Lower Columbia River was reported in 2004 (Henny et al.
2009b).
Dilution Index
0 5 10 15 20 25 30 35
Osprey Egg ΣPBDEs (ng/g, ww)
0
100
200
300
400
500
600
700
800
900
1000
Y = 226.0 +63.0X
r
2
= 0.7452, n = 6
P = 0.0268
1
2
3
4
5
6
7
8
1 = Reference Lakes, WA
2 = Willamette River (Albany/Corvallis)
3 = Willamette River (Salem)
4 = Upper Spokane River
5 = Willamette River (Eugene)
6 = Lower Spokane River
7 = Boise River
8 = Lower Columbia River (RM 85-122)
Fig. 6 Relationship at smaller rivers between major municipal
Wastewater Treatment Plant (WWTP) inputs (MGD) as a percentage
of river flow 91,000 (Dilution Index) and geometric mean RPBDE
concentrations in osprey eggs collected along the Boise, segments of
the Spokane and Willamette Rivers, and a series of small reference
lakes. Points 1–6used to determine regression line. Point 8 added to
show a high flow river site. MGD million gallons per day
690 C. J. Henny et al.
123
Temporal changes in osprey egg RPBDE
concentrations
With concern about possible PBDE-related reproductive
effects on ospreys, but also recognizing that penta- and
octa-PBDEs were no longer produced in the United States
after 2004, understanding possible changes in osprey
exposure over time was of paramount importance. Seg-
ments of the Lower Columbia River initially sampled in
2004 were again sampled in 2007, 2008 and 2009, together
with the Upper Willamette River in 2006 and 2008
(Fig. 7).
RPBDE concentrations in osprey eggs decreased 55%
along the Upper Willamette River (UWR) from 2006 to
2008 (897 vs. 405 ng/g) (F=16.86, P=0.0003). Like-
wise, eggs collected along the Lower Columbia River
(LCR, RM 29–84) showed a general decrease in RPBDEs
from 2007 (566 ng/g) to 2008 (427 ng/g) to 2009
(308 ng/g), with a concentration in 2004 (403 ng/g) similar
to 2008 (F=2.68, P=0.0587). These findings imply a
RPBDE increase from 2004 to 2007 followed by a decrease
(Fig. 7). The more limited data from LCR, RM 85–122
(285 ng/g in 2004; 308 ng/g in 2008) and from LCR, RM
124–143 (212 ng/g in 2004; 170 ng/g in 2009) (two col-
lection years) show similar concentrations in 2004 and
2008–2009, which are consistent with concentrations
observed at LCR, RM 29–84 during the same time periods.
Available information from this study suggests that
RPBDE concentrations in osprey eggs peaked somewhere
between 2005 and 2007, and then decreased in 2008 and
2009. RPBDE concentrations in largescale suckers (Cato-
stomus macrocheilus) (whole body) from the Spokane
River in 2009 were about 40% lower (wet weight) and
about 24% lower (lipid weight) than reported in 2005 (Furl
and Meredith 2010). This PBDE finding in suckers, a key
osprey prey species, agrees with our recent (2008–2009)
downward trend for PBDEs in osprey eggs at several other
sites including the Lower Columbia River and Upper
Willamette River (Fig. 7).
The congener profiles in the above time series of osprey
eggs were of special interest (Fig. 8). In spite of RPBDE
concentrations in LCR, RM 29–84 first increasing from
2004 to 2007, then decreasing in 2008 and again in 2009,
the contribution of BDE 47 (as a percentage of the total)
steadily decreased during the years (68.6, 62.0, 58.9, and
46.1%, respectively). Corresponding increases during the
years were found in BDE 100 (16.5, 22.0, 22.5 and 26.1%),
BDE 99 (3.81, 3.61, 4.64 and 7.62%), BDE 153 (5.93, 6.10,
6.09 and 8.89%) and BDE 154 (3.85, 4.71, 6.38 and 8.83%).
These congener patterns were also consistent at other sites
including LCR, RM 85–122 (BDE 47 in 2004, 72%; in 2008
59%), LCR, RM 124–143 (BDE 47 in 2004, 66%; in 2009
52%) and UWR (BDE 47 in 2006, 62%; in 2008 60%).
Biomagnification factors for PBDEs (fish to osprey
eggs)
Three of the six largescale sucker collection sites on the
Spokane River in 2009 were upstream of the Spokane
WWTP to the Idaho Stateline, while three collection sites
were downstream to Lower Long Lake (Fig. 9). The
highest PBDE concentrations in largescale suckers were
found in the lower three sub-segments downstream of the
WWTP (Furl and Meredith 2010), which adds additional
support to our earlier decision to separate the Spokane
River into two segments (above and below the WWTP).
Thus, fish residue data and the osprey egg residue data
from the Spokane River were separated into two segments
for calculating biomagnification factors.
Ye a r
2004 2005 2006 2007 2008 2009
Opsrey Egg ΣPBDEs (ng/g, ww)
0
200
400
600
800
1000
LCR, RM 29-84
LCR, RM 85-122
LCR, RM 124-143
UWR
Fig. 7 Temporal pattern of RPBDE residues (geo. means) in osprey
eggs for the Lower Columbia River (LCR) and Upper Willamette
River (UWR), 2004–2009. RM River Mile
Percent of the ΣPBDEs
020406080100
Ye a r
BDE-17
BDE-28
BDE-47
BDE-49
BDE-66
BDE-99
BDE-100
BDE-153
BDE-154
Lower Columbia River, RM 29-84
Lower Columbia River, RM 85-122
Lower Columbia River, RM 124-143
Upper Willamette River
2004
2007
2008
2009
2004
2008
2004
2009
2006
2008
Fig. 8 Temporal patterns associated with mean percent contributions
of individual PBDE congeners to the RPBDEs quantified in osprey
eggs collected from the Lower Columbia River and Upper Willamette
Rivers, 2004–2009. RM River Mile
Wastewater dilution index 691
123
In addition to fish and osprey eggs collected along the
Spokane River in 2009, a similar set of data was collected
from the Boise River in 2008. Eggs from these two
rivers contained the highest RPBDE concentrations in
2008–2009, relative to other sampling sites (Fig. 3). Prey
remains were collected near osprey nest sites along the
Spokane River in 2009 using standard protocol (see
Johnson et al. 2008). Remains of 109 fish were collected
with findings from each nest site weighted equally (N=7).
Suckers (primarily largescale suckers) were the dominant
prey species (72.0% of the biomass), followed by bull-
heads/catfishes 14.1%, northern pikeminnows (Ptychoc-
heilus oregonensis) (10.7%), bass (2.1%), trout (0.4%) and
others (1.9%) (Table 3). Earlier studies of the osprey
diet along the Lower Columbia River and Upper Willam-
ette River also indicated that native largescale suckers were
the dominant fish species preyed upon (Johnson et al.
2008). The Washington Department of Ecology empha-
sized the collection of largescale suckers including 18
composites (3–5 fish) at 6 sites along the Spokane River in
both 2005 and 2009 (Furl and Meredith 2010). Several
other fish species, including 6 composites of northern
pikeminnows, 6 composites of mountain whitefish, 1
composite of smallmouth bass (Micropterus dolomieu) and
1 composite of rainbow trout (Oncorhynchus mykiss), were
also collected in 2009. The mountain whitefish, a non-prey
item of osprey (Table 3), had consistently higher RPBDE
concentrations than largescale suckers, but all other fish
prey species had comparable concentrations to the suckers
(Furl and Meredith 2010). Therefore, to estimate fish to
osprey egg biomagnification factors (BMFs), we used only
the largescale sucker data. On a wet weight basis in 2009,
we estimated the BMF from fish to osprey eggs for
RPBDEs on the Spokane River at 3.76–7.52, but on a lipid
basis 4.37–11.0 (Table 4). Variation in the osprey diet
above and below the WWTP could account for differences
observed, although sampling error was likely a factor.
Data collected along the Boise River in 2008 included
11 osprey eggs and single composites of 7 largescale
suckers, 10 mountain whitefish, and 3 rainbow trout
(Table 5). Although no prey data were collected at osprey
nests on the Boise River in 2008, we assumed largescale
suckers were again the dominant prey species and repre-
sented contaminant loading for the river. The BMF for
RPBDEs from the Boise River was estimated at 2.62
using wet weight values and 7.88 using lipid weight. With
respect to our earlier concern about the many lakes and
ponds adjacent to the Boise River when evaluating
RPBDE egg concentrations in relation to WWTPs and
river flow, the same issue is of concern when calculating
BMF estimates based only upon fish residues from the
river. Many of these lakes were stocked with fish and
provided ospreys an additional source of fish. With the
adjacent lakes not directly associated with the river, we
hypothesize that exposure of those fish to RPBDEs would
be much less than from the river. Quantitative information
on the percentage of fish in the osprey diet obtained from
these lakes, as well as RPBDE concentrations in those
fish, remain unknown. To provide some understanding of
possible effects from foraging off-river on BMF calcula-
tions for the Boise River, we assumed that 50% of the fish
were taken off-river with residue concentrations 25% of
those in largescale suckers from the Boise River which
yielded BMFs of 4.19 (wet weight basis) and 12.9 (lipid
weight basis).
BMFs (wet weight basis) from the Spokane River
(3.76–7.52) and Boise River (2.62, but likely higher, e.g.,
4.19) are within a relatively narrow range and imply that
RPBDEs do not biomagnify from fish to osprey eggs as
much as p,p0-DDD (18-23) and p,p0-DDE (79–87), but
appear more similar to dieldrin (3.2–6.7) and RPCBs
(8.4–11) (Henny et al. 2009a). BMF estimates on a lipid
basis from the Spokane River (4.37–11.0) and Boise River
(7.88, but likely higher, e.g., 12.9) again were less than
p,p0-DDD (25–28) and p,p0-DDE (103–112), and similar to
dieldrin (5.0–7.9) and RPCBs (12–13). Chen et al. (2010)
examined RPBDE biomagnification from fish to osprey
Fig. 9 Spokane River and Reference Lakes. Closed circles are fish
collection sites and open circles are osprey egg collection sites
692 C. J. Henny et al.
123
eggs from the James River, Virginia, using a similar pro-
cedure, and reported a BMF of 23.7 (lipid basis).
Osprey reproductive success and RPBDE
concentrations
During our earlier 2002–2007 study at 120 osprey nests
in Oregon and Washington, we examined the relation
between concentrations of PBDEs as well as other con-
taminants (relative to their known toxicity) in sample eggs
and reproductive success at each nest (Henny et al. 2009b).
Of the other contaminants, only DDE concentrations were
reported at an effect level (Yakima River in 2002) with
those four eggs excluded from the analyses. The initial
study provided no evidence that RPBDE concentrations
below 1,000 ng/g adversely influenced reproductive suc-
cess of ospreys; however, in 2006 (Upper Willamette
River) and 2007 (Lower Columbia River) RPBDE con-
centrations were first reported to exceed 1,000 ng/g in
some eggs and those nests were less successful. We ana-
lyzed those two locations separately. A negative relation-
ship was found between young/active nest and RPBDEs for
the 10 nests from the Upper Willamette (P=0.008) and
the 20 nests on the Lower Columbia (P=0.057) with
Henny et al. (2009b) concluding that observed PBDE
concentrations ‘‘may’’ reduce reproductive success of
ospreys.
In 2008 and 2009, a sample egg was again collected at
an additional 93 nests with data summarized in a manner
similar to the earlier study (Table 6). With residues of
organochlorine pesticides, PCBs, dioxins and furans
decreasing dramatically in the Pacific Northwest in the
early 2000s, and mercury (although increasing) far below
effect concentrations for osprey reproduction (Henny et al.
2008,2009a), legacy contaminants were only evaluated in
the 2008 eggs. None of the egg concentrations were
reported at a reproductive effect level for ospreys
(unpublished data). With RPBDE concentrations appearing
to peak in the study areas between 2005 and 2007 (Fig. 7),
only the Boise River and Spokane River populations
in 2008–2009 contained some eggs with RPBDEs [
1,000 ng/g.
In reviewing the reproductive data in Table 6,it
becomes obvious that 2008 was a ‘‘bad year’’ for osprey
productivity at several locations studied on the west side of
the Cascade Mountains including the Lower Columbia
River (LCR, RM 29–84, RM 85–122; 0.20 and 0.40 young/
active nest attempt, respectively), and Willamette River
(UWR, RM 69–178, Portland Harbor, Multnomah Chan-
nel; 0.48, 0.80 and 1.20 young/active nest, respectively). In
earlier years, when productivity was high, similar produc-
tivity rates were also reported at adjacent segments of the
Lower Columbia River (Henny et al. 2008). In contrast, the
Boise River study area in 2008, located on the east side of
the Cascade Mountains, showed excellent productivity
(1.73 young/active nest). The 2009 studies included two
segments of the Lower Columbia River (RM 29–84 and
RM 124–143) (1.30 and 1.60 young/active nest), the
Table 3 Prey remains collected from osprey nests along the Spokane River, Washington, 2009
River Mile NFish family (% Incidence)
Bass
Micropterus spp.
Bullhead
Ictalurus spp.
N. Pikeminnow
Ptychocheilus spp.
Trout
Salmonid spp.
Sucker
Catostomus spp.
Other species
a
Reference Lake
b
12 33.3 16.7 16.7 33.3
RM 95.9 22 13.6 59.1 18.2 4.5 4.5
RM 93.2 34 17.6 61.8 8.8 5.9 2.9 2.9
RM 80 13 7.7 38.5 7.7 46.2
RM 79.4 14 92.9 7.1
RM 73.6 5 20.0 60.0 20.0
RM 59.6 11 9.1 90.9
RM 56.3 10 10.0 20.0 20.0 50.0
Mean mass (g)
c
102 146 362 190 777 194
% Incidence
d
8.3 38.9 10.7 0.84 37.4 3.9
% biomass 2.1 14.1 9.6 0.40 72.0 1.9
a
Includes peamouth (N=2), sandroller (N=1), pumpkinseed (N=1), black crappie (N=1), tench (N=1), and common carp (N=1)
b
Lake south of Spokane, not included in % Incidence or % biomass calculations for Spokane River
c
Mass determined using opercula lengths (sucker spp., northern pikeminnow, bass), weight for 8–12 inches (203–305 mm) determined by
Oregon Department of Fish and Wildlife (bullhead/catfish, salmonid, peamouth species), previously published information (Henny et al. 2004:
black crappie; Johnson et al. 2008: common carp), and estimated according to Wydoski and Whitney (2003) (tench, pumpkinseed, sandroller)
d
All nests on Spokane River weighted equally on nest by nest basis, N=7
Wastewater dilution index 693
123
Spokane River (RM 47–96) (1.60 young/active nest) and
Reference Lakes (1.50 young/active nest) all showing
excellent productivity. Production rates at LCR RM 29–84
improved from 2008 to 2009 (0.20 and 1.30 young/active
nest) with eggs containing low and decreasing RPBDE
residues (427 and 308 ng/g) with none [750 ng/g. This
implies that PBDEs were not related to the low produc-
tivity reported at several locations in 2008. Similarly,
another segment of the Lower Columbia River (LCR RM
124–143) showed excellent productivity in 2009 (1.60
young/active nest), while an adjacent segment in 2008 (RM
85–122) had poor productivity (0.40 young/active nest)
with no RPBDE residues in either segment or year
[750 ng/g.
Following the above descriptive assessment of produc-
tivity on the west side of the Cascade Mountains, we
evaluated (Jonckeere–Terpstra Test) five datasets in
Table 6with 10 or more nests studied in 2008 and 2009 to
determine if any relation existed between RPBDEs and
young/active nest. The Lower Columbia River in 2008
(RM 29–84 and RM 85–122 combined) and 2009 (RM
29–84 and RM 124–143 combined), the Upper Willamette
River (RM 69–181) and Lower Willamette River (Portland
Harbor and Multnomah Channel combined) in 2008
(N=10, N=15, N=23, N=10) yielded no significant
relationships between RPBDEs and young/active nest
(Z=0.2582, P=0.40; Z=-1.2197, P=0.11; Z=
0.4927, P=0.31; Z=0.3873, P=0.35). No eggs from
these 48 nests contained RPBDE residues [1,000 ng/g
with only two eggs [750 ng/g. Of special interest were the
ospreys nesting along the Boise River in 2008 (N=11)
and Spokane River in 2009 (N=15) where seven eggs
Table 4 RPBDE (ng/g, ww and lw) concentrations in osprey eggs
and whole body largescale suckers from two segments of the Spokane
River, with calculated Biomagnification Factors (BMFs), 2009
Location RPBDEs
Suckers Osprey eggs BMFs
ww lw ww lw ww lw
Upper segment (RM
68–96) (Stateline, ID to
Spokane wastewater
treatment plant)
81.6 1,169 520 20,000
108 1,578 323 8,972
156 3,503 775 18,452
72.6 1,228 1,382 53,154
98.0 2,108 147 5,250
99.0 1,480 430 17,200
30.6 712 741 15,438
33.1 1,195 620 14,762
36.0 1,115
Geometric mean 68.9
B
1,420
B
518
A
15,663
A
7.52 11.0
Lower segment (RM
47–67) (Spokane
wastewater treatment
plant to lower long
lake)
130 4,305 1,637 49,606
145 3,198 939 19,979
348 19,137 826 28,483
143 3,482 639 14,860
254 5,394 849 27,387
314 4,421 485 13,472
125 2,169 397 10,730
163 3,840
320 6,806
Geometric mean 199
A
4,753
A
749
A
20,757
A
3.76 4.37
Value for a sucker does not correspond to the adjacent osprey egg.
Columns sharing the same letter are not significantly different,
Tukey’s Studentized Range (a=0.05). BDE 47, 49, 66, 71, 99, 100,
138, 153, 154, 183, 184, 191 (all non-detects) and 209 (all non-
detects) were analyzed in suckers (Furl and Meredith 2010); there-
fore, for direct comparison, the same congeners were used in osprey
eggs (egg data for BDE 17, 28, 85 and 190 not used)
Table 5 RPBDE (ng/g, ww and lw) concentrations in osprey eggs
and whole body composite fish samples from the Boise River, with
calculated biomagnification factors (BMFs), 2008
River Mile (Osprey eggs) RPBDEs
ww lw
RM 45.5 1,187 43,945
RM 45.3 641 17,311
RM 44.9 1,057 33,032
RM 44.3 1,463 43,025
RM 43.9 711 14,515
RM 41.0 1,005 47,865
RM 34.0 604 16,337
RM 33.0 2,134 88,910
RM 28.8 707 32,143
RM 26.0 713 59,437
RM 19.5 525 12,499
Geometric mean 893 31,070
Fish (Whole body)
Boise River (study area, RM 47.3)
a
Largescale sucker N=7, 1,214–1,714 g 341 3,942
Mountain whitefish N=10, 140–390 g 683 5,701
Rainbow trout N=3, 94–159 g 65.5 4,517
Boise River (Upstream city of Boise, RM 93.3)
b
Largescale sucker N=5, 418–995 g 0.02 0.69
Largescale sucker N=2, 1,065–1,660 g 0.01 0.41
Mountain whitefish N=8, 63–426 g 0.39 2.9
BMF using osprey eggs, RM 19.5–45.5 2.62 7.88
We used the same BDE congeners as in Table 4for the Spokane
River with the exception of BDE 71, 184 and 191 which were not
analyzed in 2008. These congeners were of minor importance in the
Spokane River and reported in low concentrations in only 3, 1 and 0
eggs, respectively
a
Boise wastewater treatment plants located at RM 44 and 50, with
fish collected at RM 47.3
b
Location where no osprey nested
694 C. J. Henny et al.
123
contained RPBDE residues [1,000 ng/g; however, again
no significant relationship was found (Z=-0.241, P=
0.42; Z=-0.4827, P=0.31). Both of these sites had
excellent productivity (1.73 and 1.60 young/active nest),
especially when considering that one egg was collected
from each nest. Osprey reproductive rates for population
maintenance are now estimated at between 0.8 and 1.30
young/active nest depending upon breeding age structure
of the population (Poole 1989; Watts and Paxton 2007).
Conclusions
All 175 osprey eggs collected in the Columbia River Basin
between 2002 and 2009 contained quantifiable PBDE
concentrations. RPBDE concentrations in eggs during
2008–2009 were highest at the two smallest rivers (Boise
and Spokane) with relatively large cities and lowest at a
series of small lakes (a Reference Area) in northeastern
Washington (south of Spokane). Concentrations at other
locations studied were within a relatively narrow range. In
an attempt to better understand RPBDE concentrations
observed in osprey eggs from various rivers, we evaluated
volume of effluent discharge from major WWTPs and river
flow (a Dilution Index). Although WWTPs may not be the
sole source of PBDEs, their volume of discharge provides a
measure of human activity in a locality. Osprey egg con-
centrations along 109 miles of the Willamette River par-
alleled the Dilution Index (WWTP Discharge/River Flow)
91,000 (Fig. 5). By combining information from segments
of the Willamette and Spokane Rivers and the Reference
Lakes, a strong relationship (Y=226.0 ?63.0X,r
2
=
0.7452, P=0.0268) was observed between osprey egg
concentrations and the Dilution Index (Fig. 6). This study
is novel with the information gained valuable and useful
for improving our understanding of the PBDE contaminant
patterns observed in osprey eggs, thereby outweighing any
limitations of the fairly simple approach. Data from the
Boise River could not be used in the above evaluation
because ospreys there often foraged off river in adjacent
lakes and ponds which resulted in lower than expected egg
concentrations. Still, some of the highest PBDE concen-
trations occurred in Boise River eggs, apparently laid by
ospreys that foraged more frequently in the river. It was
fortuitous for ospreys nesting along the Boise River that
adjacent ponds and lakes were available for foraging. If
stocking of these lakes and ponds with fish is continued, it
will likely benefit ospreys in terms of lower exposure to
PBDEs.
Several study areas were sampled during more than
1 year with RPBDE egg concentrations decreasing 55%
(P=0.0003) along the Upper Willamette River from 2006
to 2008, and 46% (P=0.0587) along the Lower Columbia
River (RM 29–84) from 2007 to 2009. Our limited data
suggests that RPBDE concentrations in osprey eggs prob-
ably peaked between 2005 and 2007, and then decreased
(Fig. 7). In addition to concentration changes over time,
congener profiles also changed with the Lower Columbia
River site mentioned above showing a steady decrease in
the contribution of BDE 47 (as a percentage of the total)
from 2004 to 2007 to 2008 to 2009 (68.6, 62.0, 58.9 and
46.1%). The difference was made up by percentage
Table 6 Distribution of RPBDE concentrations (ng/g, ww) in sample eggs from 93 osprey nests and associated young/nesting attempt from
remaining eggs in clutch, 2008–2009
Location
a
Year NRPBDE (ng/g, ww) category Mean
0–250 251–500 501–750 751–1,000 [1,000 Productivity
A 2008 6 4 2 0.20
b
A 2009 10 2 7 1 1.30
B 2008 5 2 2 1 0.40
C 2009 5 4 1 1.60
D 2008 23 5 8 8 2 0.48
E 2008 5 1 2 2 0.80
F 2008 5 1 4 1.20
G 2008 11 6 5 1.73
H 2009 15 1 4 3 5 2 1.60
I 2009 8 8 1.50
RPBDEs includes BDE 17, 28, 47, 49, 66, 85, 99, 100, 138, 153, 154, 183, 190, and 209
a
A=Lower Columbia River (RM 29–84), OR and WA; B =Lower Columbia River (RM 85–122), OR and WA; C =Lower Columbia River
(RM 124–143), OR and WA; D =Upper Willamette River (RM 69–181), OR; E =Willamette River, Portland Harbor, OR; F =Multnomah
Channel, OR; G =Boise River (RM 19–45), ID; H =Spokane River (RM 47–96), WA; I =Reference Lakes, Spokane, WA
b
Productivity based on 5 nests (1 nest not rechecked)
Wastewater dilution index 695
123
increases in BDE 100, BDE 99, BDE 153 and BDE 154,
which was also consistent at other locations. The only
American manufacturer voluntarily stopped production of
penta-BDE and octa-BDE in 2004. Are we observing a
fairly rapid decline in osprey egg residue concentrations as
a result of that production stoppage? Continued monitoring
is necessary in order to confirm these trends in the Pacific
Northwest.
An empirical estimate of the BMF for RPBDE con-
centrations from fish to osprey eggs was estimated at
3.76–7.52 wet weight or 4.37–11.0 lipid weight from the
Spokane River study area. Boise River data were con-
founded by ospreys foraging off river, but a crude adjust-
ment for off-river foraging suggested that BMFs for the
Boise River were in the same general range. These BMFs
are lower than reported in ospreys for p,p0-DDD and
p,p0-DDE, and more similar to dieldrin and RPCBs.
Our earlier study in Oregon and Washington provided
no evidence of reduced osprey reproductive success when
RPBDE egg concentrations were \1,000 ng/g; however, at
two locations (Upper Willamette in 2006 and Lower
Columbia River in 2007) (RM 29–84) some eggs contained
[1,000 ng/g with negative relationships indicated at both
locations between productivity and RPBDE concentrations
in eggs (P=0.008, P=0.057) (Henny et al. 2009b). Eggs
exceeding 1,000 ng/g were only reported from the Boise
and Spokane Rivers in 2008–2009. Osprey production rates
on the Boise and Spokane Rivers were both considered
excellent with no negative relationship found between
productivity and RPBDE concentrations (P=0.42, P=
0.31). Low production rates for ospreys nesting west of the
Cascade Mountains in 2008, based on the results of this
study, were not related to RPBDE concentrations. This lack
of a relationship between PBDEs and reproductive rates
is based on short-term datasets and additional monitoring is
essential to confirm not only the trend of declining
PBDE concentrations in these ospreys, but also the
apparent lack of a relationship with reproductive success of
these birds.
Acknowledgments We thank the electric utility companies (Avista,
Inland Power and Light, Idaho Power, Emerald People’s Utility
District, Eugene Water and Electric Board, Pacific Power and Light
Company, Salem Electric, Portland General Electric Company,
Consumers Power, Inc.) associated with all of the study areas for
providing bucket trucks and personnel to access the nests on power
poles. The US Coast Guard kindly permitted access to osprey nests
built on navigation aids in the Columbia River. D. MacCoy (USGS)
provided fish from the Boise River. We are grateful to the numerous
landowners who permitted access to their property to survey nesting
osprey. P. Haggerty (USGS) and C. Meredith (WSDE) kindly drafted
the study area maps. D. Wise (USGS) provided Wastewater Treat-
ment Plant discharge information. We acknowledge L. Periard and L.
Gauthier in the Letcher Research Group (at NWRC, Ottawa) for
chemical analysis of PBDEs. An earlier draft of the manuscript was
improved by comments from G. Heinz, B. Rattner and R. Lazarus
(all USGS). The study was funded by the US Geological Survey with
the Spokane River study area partially funded by Washington State
Department of Ecology. Any use of trade, product, or firm names is
for descriptive purposes only and does not imply endorsement by the
US Government or State of Washington.
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