Ecological risks (ERs) of pollutants are typically assessed using species sensitivity distributions (SSDs), based on effect concentrations obtained from bioassays with unknown representativeness for field conditions. Alternatively, monitoring data relating breeding success in bird populations to egg concentrations may be used. In this study, we developed a procedure to derive SSDs for birds based on field data of egg concentrations and reproductive success. As an example, we derived field-based SSDs for p, p'-DDE and polychlorinated biphenyls (PCBs) exposure to birds. These SSDs were used to calculate ERs for these two chemicals in the American Great Lakes and the Arctic. First, we obtained field data of p, p'-DDE and PCBs egg concentrations and reproductive success from the literature. Second, these field data were used to fit exposure-response curves along the upper boundary (right margin) of the response's distribution (95th quantile), also called quantile regression analysis. The upper boundary is used to account for heterogeneity in reproductive success induced by other external factors. Third, the species-specific EC10/50s obtained from the field-based exposure-response curves were used to derive SSDs per chemical. Finally, the SSDs were combined with specific exposure data for both compounds in the two areas to calculate the ER. We found that the ERs of combined exposure to these two chemicals were a factor of 5-35 higher in the Great Lakes compared to Arctic regions. Uncertainty in the species-specific exposure-response curves and related SSDs was mainly caused by the limited number of field exposure-response data for bird species. With sufficient monitoring data, our method can be used to quantify field-based ecological risks for other chemicals, species groups, and regions of interest.
Ecological risks (ERs) of pollutants are typically assessed using species sensitivity distributions (SSDs), based on effect concentrations obtained from bioassays with unknown representativeness for field conditions. Alternatively, monitoring data relating breeding success in bird populations to egg concentrations may be used. In this study, we developed a procedure to derive SSDs for birds based on field data of egg concentrations and reproductive success. As an example, we derived field-based SSDs for p, p'-DDE and polychlorinated biphenyls (PCBs) exposure to birds. These SSDs were used to calculate ERs for these two chemicals in the American Great Lakes and the Arctic. First, we obtained field data of p, p'-DDE and PCBs egg concentrations and reproductive success from the literature. Second, these field data were used to fit exposure-response curves along the upper boundary (right margin) of the response's distribution (95th quantile), also called quantile regression analysis. The upper boundary is used to account for heterogeneity in reproductive success induced by other external factors. Third, the species-specific EC10/50s obtained from the field-based exposure-response curves were used to derive SSDs per chemical. Finally, the SSDs were combined with specific exposure data for both compounds in the two areas to calculate the ER. We found that the ERs of combined exposure to these two chemicals were a factor of 5-35 higher in the Great Lakes compared to Arctic regions. Uncertainty in the species-specific exposure-response curves and related SSDs was mainly caused by the limited number of field exposure-response data for bird species. With sufficient monitoring data, our method can be used to quantify field-based ecological risks for other chemicals, species groups, and regions of interest.
In current ecological
risk assessment, chemical risks are often
evaluated using species sensitivity distributions (SSDs).[1−3] The main assumption of an SSD is that the differences in sensitivity
of species toward a chemical can be described by a (cumulative or
probabilistic) distribution function.[4,5] SSDs can be
used to calculate the ecological risk (ER) posed by individual compounds
and compound groups to species in an area.[6] ERs are defined as the probability of measured environmental concentrations
exceeding (no) effect concentrations of species.[6,7] Effect
concentrations, such as half maximal effective concentrations (EC50s) or no-observed-effect concentrations (NOECs), are typically
obtained from lab experiments. In these experiments, individual performance
(e.g., fecundity or mortality) is measured in a controlled setting.[8] The application of these data in the derivation
of SSDs has been subject to much discussion over the years as lab
data fail to acknowledge potential differences with site-specific
conditions.[9] Furthermore, although the
use of a wide range of species when quantifying toxicant-effect relationships
is more representative of actual impacts in bird populations,[10] test species used in these experiments are limited
to those that are easy to breed and do not necessarily reflect natural
compositions of taxonomical groups.[9,11,12] Ecotoxicological data is lacking for many bird species
at higher trophic levels (e.g., piscivores, raptors, and insectivores),
as laboratory experimentation is limited due to practical, financial,
and ethical constraints[13] or focus on acute
lethal toxicity only.[7]Field monitoring
data of breeding success in bird populations and
related chemical concentrations in eggs may be used as an alternative
to laboratory experiments in the derivation of effect concentrations
as input for the SSDs for birds. However, it is important to isolate
the impact of individual chemicals as breeding success is influenced
by a variety of additional environmental or biological factors, such
as climate and population density.[14] Traditional
statistical regression approaches focus on changes in the mean of
the response variable’s distribution only, including the effects
of other extraneous variables and introducing potential bias. Instead
of using traditional regression analysis, quantile regression may
be used to account for hidden bias resulting from extraneous environmental
variables.[6,15,16]By fitting
a sigmoidal exposure-response curve at the upper boundary
of the data’s distribution, the constraints of elevated toxicant
concentrations in eggs imposed on bird reproductive success are expected
to become visible, as it corrects for unmeasured ecological and environmental
factors (hidden bias) potentially limiting the observed response.[16] In this way, constraints imposed solely by chemical
exposure are expected to be revealed.The aim of the present
study was to develop and apply a procedure
to derive ecological risks of bird species, based on field data of
reproductive success and chemical concentrations in eggs of birds.
As an example, we applied the procedure with field data on p,p′-DDE (dichlorodiphenyldichloroethylene,
a DDT metabolite) and the sum of multiple PCB congeners in the North
American Great Lakes and the Arctic. The effects of DDT metabolites
and polychlorinated biphenyls (PCBs) on bird species have received
much attention since the early 1960s.[17,18] These compounds
are known to be persistent and are strongly linked to eggshell thinning,
altered sexual behavior, and hormonal disruption,[19,20] which in turn decrease growth rates in bird populations.
Materials
and Methods
Quantile Regression
Fitting Procedure
Relative reproductive
success (fraction)
was related to a toxicant gradient using the quantile regression approach
as described by Koenker,[21] where the regression
line was fitted to the 95th quantile (τ = 0.95) of the response
variable’s distribution, to account for heterogeneity caused
by other limiting ecological and environmental factors. The quantile
regression model was based on the Hill equation,[22−24] yielding a
sigmoidal curvewhere R is the modeled response
(relative reproductive success) of species i for
chemical j, EC50 is the 50% effective response level or inflection point of
the curve of species i for chemical j, C is the measured contaminant concentration
of chemical j (in mg/kg egg wet weight), and β is the slope coefficient
associated with species i for chemical j, determining the slope of the curve.[22,24] We fitted
a logit transformed regression line on the data set using the quantreg package of Koenker (2013),[21] adapted from Bottai et al. 2010[25] asimplying that the untransformed
relative reproductive
success can be calculated throughwhere LN(C) is the natural
log-transformed chemical concentration in the egg, β0 is defined as the intercept of the regression line, and β is the slope coefficient
equal to β in eq . ε reflects the
error term, in this study set at 0.001, a small quantity ensuring
that the logistic transform is defined for all values of R.[25] The quantile regression algorithm
minimizes the residuals of the regression analysis.[21] The inflection point of the exposure-response curve (or
EC50 in eq , in mg/kg w.w.) was derived asThe EC10 values were derived
by solving eq for C, fixing R at 0.9,[26] using the uniroot function in R statistics 3.3.1. The 95% confidence
intervals associated with the quantile fit were obtained by using
bootstrapped errors, as described by Koenker.[27]
Model Consistency
Regression lines were fitted at three
additional quantiles (τ = 0.25, 0.5, 0.75) to evaluate model
consistency. We expected a negative relationship between exposure
and response for all quantiles, i.e. a negative β. Furthermore, we expected that the larger the
quantile, the larger the EC50- and EC10-values.
If both expectations were not met, data were not considered sufficiently
reliable to derive an exposure-response relationship. The following
selection criteria for the exposure-response curves were applied:1) Exposure-response curves yielding a positive β for τ = 0.95, τ = 0.75, or τ
= 0.50 were not further considered in the analysis.2) Effect
concentrations that have higher EC10- or EC50-values for τ = 0.25 or τ = 0.50 compared to
τ = 0.95 were disregarded.
Species Sensitivity Distributions
SSDs were constructed,
using EC50 and EC10 data obtained from the derived
exposure-response curves. We assumed a log-normal spread in species
sensitivities for SSDs with mean (μ) and standard deviation
(σ) to link the toxicant gradient (x-axis)
to the potentially affected fraction of species (PAF; y-axis).[4,28,29] To assess
the statistical uncertainty in the SSDs, we randomly sampled 10,000
EC10s and EC50s for each species-chemical combination
separately, using the uncertainty in the quantile regressions as a
starting point. Subsequently, for each chemical 10,000 SSDs were fitted
through these sampled effect concentrations over all species under
the assumption of a log-normal distribution.
Ecological Risks
The ecological risk (ER; fraction)
is defined as the probability of a species in a certain area exceeding
its EC10 or EC50 and represents the overlap
between the derived SSD and the exposure concentration distribution
(ECD) of a certain chemical in a specific area (as exemplified in Figure ). ERs are calculated
through integral[6,7]where PDFECD is
defined as the probability density function of the natural log-transformed
exposure concentration distribution of an individual chemical found
in bird’s eggs in a specific area. CDFSSD is the
(cumulative) single substance SSD model based on field-based EC10s and EC50s.
Figure 1
Graphical example of CDFSSD in red, corresponding 95%
confidence intervals (dashed lines), PDFECD in black, and
ER (area under the curve), with corresponding 95% confidence intervals,
in green.
Graphical example of CDFSSD in red, corresponding 95%
confidence intervals (dashed lines), PDFECD in black, and
ER (area under the curve), with corresponding 95% confidence intervals,
in green.ERs based on SSDs derived for
respectively EC10s and
EC50s for single toxicant exposure were calculated based
on Korsman et al. 2016[7] in R statistics
3.3.1 usingin which the function
pnorm returns a probability
distribution function and where μSSD is the natural
log-transformed mean of the SSD and σSSD reflects
the natural log-transformed standard deviation of the SSD. The μECD and σECD are the mean and standard deviation
associated with the natural log-transformed contaminant concentrations
found in bird’s eggs in a certain area.[6]Combined ecological risk (ERc), defined as the
risk
posed by multiple pollutants in an area, was calculated using eq according to the response
addition principle[6,7]where n is the number of substances used in calculation
of the
ERc, and ERi is the ecological risk calculated
for each compound individually. Statistical uncertainty in the ERs
was quantified by random sampling from the SSD realizations, as mentioned
above.
Data Acquisition and Treatment
Exposure-Response Data
A data set was compiled containing p,p′-DDE and ΣPCB concentrations
in eggs (in mg/kg wet weight) and the corresponding reproductive success
of the bird (-population). The relative reproductive success of an
individual bird (or population) was defined as the fraction of fledglings
per occupied or active nest (productivity), over the species theoretical
maximum productivity (the maximum productivity given in the full data
set for that species, see Table S1 and eq S1 in the Supporting Information). Data were obtained from a literature search of the Web of Knowledge
using search strings related to reproductive success and productivity,
combined with species’ names (scientific and common names)
or terms such as birds and avian species on one side, and terms related to organic pollutants (specific compound
names or compound groups) on the other. Additionally, data from scientific
reports (gray literature) were obtained using Google Scholar, using
the same search strings. This search revealed 57 potentially useful
articles and reports,[30−86] including monitoring data for four raptorial bird species or species
groups (bald eagle (Haliaeetus leucocephalus), white-tailed
eagle (Haliaeetus albicilla), Eurasian sparrowhawk
(Accipiter nisus), and falcon species (including Falco peregrinus and Falco sparverius)),
eight piscivorous bird species or species groups (osprey (Pandion haliaetus), herring gull (Larus argentatus), common tern (Sterna hirundo), cormorant species
(including Phalacrocorax auritus, Phalocrocorax
carbo, and Phalacrocorax pelagicus), brown
pelican (Pelecanus occidentalis), snowy egret (Egretta thula), black-crowned night heron (Nycticorax
nycticorax), and black skimmer (Rynchops niger)), and three insectivorous birds (tree swallow (Tachycineta
bicolor), house wren (Troglodytes aedon),
and American robin (Turdus migratorius)). Contaminant
concentration of egg given in terms of lipid or dry weight were converted
to wet weight (mg/kg) using data on lipid or moist percentage, respectively.
The specific composition of PCB congeners included in ΣPCBs
is listed per source in Table S2 of the Supporting Information.
Weights
The data set used in this
study consists of
both data obtained from single nests, as well as averaged bird productivity
and egg residue concentrations, encompassing multiple nests, years,
or locations. Therefore, in order for a larger sample size to yield
a large influence on the analysis, the data points relating toxicant
concentrations in eggs to reproductive success were weighted according
to eq where w defines
the weighting factor corresponding to data point i, Neggs refers to the number of sampled
eggs per toxicant data record, and Nnests refers to the number of active nests per productivity data record.
With eq , we valued
the information required for the productivity (based on the number
of nests sampled) and chemical residues (based on the number of analyzed
eggs) equally. This means that the weights are limited by the smallest
sample size.
Exposure Data Associated with Ecological
Risk
Additional
data describing contaminant concentrations in bird’s eggs used
in calculating ecological risks by p,p′-DDE and PCBs were obtained using the Web of Knowledge in
searches combining the terms egg residues, birds, and multiple specific areas. This search resulted
in contamination data for two distinct areas (the Arctic[87−101] and the American Great Lakes[102−110]). Single toxicant exposure data were natural log-transformed and
used to construct a probability density distribution that was applied
in the calculation of ecological risks. Exposure data were included
without further weighting of number of eggs and nests.
Results
Quantile
Exposure-Response Curves
Quantile exposure-response
curves, set at the 95th percentile, were fitted for 12 (p,p′-DDE) and 14 (ΣPCBs) raptorial,
piscivorous, and insectivorous bird species for the two compounds
as exemplified in Figure for Haliaeetus albicilla. We derived 26
exposure-responses, as for 4 out of 15 species we only found sufficient
data to include one of the two POPs concerned (see Figure S1 (p,p′-DDE)
and Figure S2 (ΣPCBs) in the SI).
Excluding species-substance combinations that were not considered
sufficiently consistent with the other quantiles resulted in 18 exposure-response
curves covering 12 species (see Figures S3 (EC50s) and S4 (EC10s) in the SI).
Figure 2
Quantile exposure-response curves plotting reduction
in reproductive
success at increasing chemical concentrations in eggs for the white-tailed
eagle (Haliaeetus albicilla). Quantile τ was
set at 0.95. The scatter points correspond with single data records,
and their size corresponds with the assigned weight. The 95% C.I.
is indicated through dashed lines. Exposure-response curves for the
other birds species included can be found in the Supporting Information (Figures S1 and S2).
Quantile exposure-response curves plotting reduction
in reproductive
success at increasing chemical concentrations in eggs for the white-tailed
eagle (Haliaeetus albicilla). Quantile τ was
set at 0.95. The scatter points correspond with single data records,
and their size corresponds with the assigned weight. The 95% C.I.
is indicated through dashed lines. Exposure-response curves for the
other birds species included can be found in the Supporting Information (Figures S1 and S2).A significant decrease
of reproductive success in birds along increasing
toxicant gradients was observed for both compounds for exposure-response
curves set at the 95th percentile. EC50s ranged from 4.58
mg/kg egg w.w. (Pandion haliaetus) to 37 mg/kg (Haliaeetus leucocephalus) for p,p′-DDE and from 4.62 mg/kg (Egretta thula) to 124 mg/kg (Larus argentatus) for ΣPCBs.
EC10s ranged from 0.2 mg/kg (Haliaeetus leucocephalus) to 17.7 mg/kg (Accipiter nisus) for p,p′-DDE and from 0.03 mg/kg (Egretta
thula) to 83 mg/kg (Pandion haliaetus) for
ΣPCBs (Table ).
Table 1
Effect Concentrations (mg/kg egg w.w.)
Associated with the Derived Quantile Log-Logistic Regression Curves
(τ = 0.95) and Corresponding 95% Confidence Interval
τ
= 0.95
p,p′-DDE
ΣPCBs
species
N
β (±SE)
EC50
95-CI
EC10
95-CI
N
β (±SE)
EC50
95-CI
EC10
95-CI
Accipiternisusa
54
–5.03 (±0.508)
27.5
19–66.3
17.8
12.1–32.9
54
–5.24 (±0.295)
28.6
10.1–∞
18.8
8.98–∞
Egrettathulab
12
–6.64 (±0.986)
7.65d
3.1–∞
5.5d
2.3–∞
6
–0.434 (±0.0368)
4.62
2.09–69.8
0.0296
0–0.148
Falco sp.a
37
–2.52 (±0.089)
16.9
13.9–∞
7.1
0.023–9.96
37
–1.64 (±0.0638)
27.1
17.7–348
7.1
0.014–12.8
Haliaeetusalbicillaa
68
–0.93 (±0.0257)
14.7
11.1–18.5
1.38
0.276–2.7
88
–1.33 (±0.0381)
46.8
37.3–92.5
8.97
0.0229–17.3
Haliaeetusleucocephalusa
52
–0.428 (±0.0219)
36.9
12–67
0.218
0–0.92
50
–0.693 (±0.0258)
36.2
21.5–56.3
1.52
0.01–8.81
Larusargentatusb
28
–5.21 (±0.771)
16.4
10.9–∞
10.8
8.23–∞
28
–5.53 (±0.285)
124d
92–∞
83.2d
0.746–∞
Nycticoraxnycticoraxb
27
–3.66 (±0.145)
24.8
5.4–∞
13.6
2.01–∞
Pandionhaliaetusb
48
–0.778 (±0.0895)
4.58
0–∞
0.272
0–∞
44
–1.93 (±0.074)
8.5
0.536–9.73
2.72
0–4.36
Pelecanusoccidentalisb
19
–4.64 (±0.137)
15.2
4.6–∞
9.47
1.62–∞
14
–19.2
(±0.754)
7.67d
5.1–∞
6.84d
0–14
Phalacrocorax sp.b
22
–3.66 (±0.239)
8.15d
1.5–∞
4.47d
0.183–∞
33
–1.45 (±0.0125)
14.8d
2.77–∞
3.3d
0–∞
Rynchopsnigerb
11
–9.02 (±0.691)
4.72d
1.43–∞
3.7d
1.76–∞
Sternahirundob
6
–11.2 (±2.3)
9.41
6.66–10.4
7.73
0–16.4
16
–2.77 (±0.062)
55.9
5.1–∞
25.3
1.18–∞
Tachycinetabicolorc
8
–1.25 (±0.0503)
8
0.9–∞
1.38
0–∞
21
–0.934 (±0.0153)
24.4d
3.35–∞
2.32d
0–10.5
Troglodytesaedonc
4
–0.619 (±0.164)
10.8d
0–∞
0.31d
0–∞
Turdusmigratoriusc
6
–3.75 (±1.15)
0.233
0.0032–14.4
0.13
0.14–38.9
Raptorial bird.
Piscivorous bird.
Insectivorous
bird. Additionally,
95% confidence intervals associated with the EC50s/EC10s are given.
Excluded
from SSD derivation according
to set conditions.
Raptorial bird.Piscivorous bird.Insectivorous
bird. Additionally,
95% confidence intervals associated with the EC50s/EC10s are given.Excluded
from SSD derivation according
to set conditions.
Species Sensitivity
Distributions
SSD models were derived
from the field-based effect concentrations for the two contaminants,
based on 18 quantile exposure-response curves set at the 95th percentile.
As the quantile regression estimates in some cases provide zero or
infinite EC50- or EC10-values due to the large
statistical uncertainties involved, not all 10,000 realizations of
the SSD curves yielded numerical results. For p,p′-DDE, only 9–13% of the iterations resulted
in a numerical mean (μ) and standard deviation (σ) of
the SSD, while for ΣPCB this percentage was higher with 32–37%
of the iterations. This most likely results in an underestimation
of the uncertainty bounds of the SSDs, as presented in Figure . Average toxicity (eμ) based on EC50s and EC10s derived for p,p′-DDE is 14.9 mg/kg egg w.w.
(9.1–22.4) and 3.3 mg/kg (2.9–8.2), respectively. Average
toxicity associated with ΣPCB contamination is 12.7 mg/kg egg
w.w. (9.5–24.8) and 2.2 mg/kg (2.1–6.8) based on EC50s and EC10s, respectively.
Figure 3
Species sensitivity distributions
for derived from field-based
EC10s (in red) and EC50s (in blue) for p,p′-DDE (a, c) and ΣPCB (b,
d), respectively. Error bars around each EC10/50 point
indicate its 95% confidence intervals (dashed error bars indicate
infinite confidence intervals). 95% confidence intervals corresponding
to the derived SSDs are indicated as dashed lines. Additionally, the
natural log-transformed μ and σ (s) per SSD was given
(95% confidence interval between brackets).
Species sensitivity distributions
for derived from field-based
EC10s (in red) and EC50s (in blue) for p,p′-DDE (a, c) and ΣPCB (b,
d), respectively. Error bars around each EC10/50 point
indicate its 95% confidence intervals (dashed error bars indicate
infinite confidence intervals). 95% confidence intervals corresponding
to the derived SSDs are indicated as dashed lines. Additionally, the
natural log-transformed μ and σ (s) per SSD was given
(95% confidence interval between brackets).Single toxicant ERs calculated for
the two compounds separately were a factor of 16 (p,p′-DDE) to 4.3 (ΣPCBs) higher in the
North American Great Lakes compared to Arctic regions, based on 10%
response levels. Individual ERs for p,p′-DDE based on 50% response levels were 5 orders of magnitude
(p,p′-DDE) higher in North
American Great Lakes than in Arctic regions, while individual ERs
for ΣPCBs were a factor of 27 higher in North American Great
Lakes than in Arctic regions. Consequently, differences in the overall
combined ER10s calculated for the American Great Lakes
and Arctic sites were shown to be statistically significant, calculating
higher combined ER10s for the American Great Lakes compared
to Arctic sites (5.7 × 10–1 vs 1.1 × 10–1, respectively). The same holds for the combined ER50s (1.7 × 10–1 vs 4.9 × 10–3). PCB-contamination contributed most to combined
ERs in the American Great Lake District and the Arctic based on both
ER10s and ER50s (Figure ).
Figure 4
Ecological risks [fraction] with corresponding
95% confidence intervals
in the Arctic and the Great lakes for PCBs, p,p-DDE, and their combined risk, based on bird EC10s (light) and EC50s (dark).
Ecological risks [fraction] with corresponding
95% confidence intervals
in the Arctic and the Great lakes for PCBs, p,p-DDE, and their combined risk, based on bird EC10s (light) and EC50s (dark).Of all the Great Lakes, the highest combined ER10 and
ER50 were calculated for Lake Ontario (6.3 × 10–1 and 2.2 × 10–1, respectively).
In the Arctic region, the highest combined ER10s and ER50s were calculated for the Barents Sea (1.23 × 10–1 and 5.4 × 10–3, respectively),
Norton Sound (1.31 × 10–1 and 9.6 × 10–3), and Bering Sea (1.2 × 10–1 and 7.42 × 10–3) (see Table S5 in the Supporting Information).
Discussion
Our study explained how field data can be used to systemically
derive chemical-specific and combined ecological risks. We also showed
how the method can be applied in practice for p,p′-DDE and ΣPCBs in the Arctic and the American
Great Lakes. Below, we discuss the three key elements of our study,
i.e. the derivation of exposure-response curves, species sensitivity
distributions, and ecological risks, respectively.
Exposure-Response Curves
In the present study, we derived
exposure-response curves for multiple piscivorous, raptorial, and
insectivorous bird species, relating p,p′-DDE and ΣPCBs in eggs to reproductive success, based
on field data. EC50s obtained in this study were higher
compared to field-based EC50s calculated for the same bird
species from other studies,[45,111−113] likely due to the fact that other field studies use traditional
regression approaches that focus on mean effects.[14] Our exposure-response curves were fitted along the upper
boundary of the response’s distribution, resulting in higher
EC50s. Effect concentrations calculated using traditional
regression analysis (τ = 0.50; Table S3 in the Supporting Information) in the present study were similar
to (for Falco sp.,[111]Pelecanus occidentalis,[113] and Pandion haliaetus(113)) or lower
(for Haliaeetus albicilla/leucocephalus(112)) than those derived in other field studies.It should be noted, however, that our exposure-response curves
resulted in excluding 6 out of 14 species for ΣPCB and 2 out
of 12 species for p,p′-DDE
due to inconsistencies with lower quantile estimates. We also obtained
very large uncertainty intervals for a number of species, depending
on the number and distribution of the field-based exposure response
data. These uncertainties were further propagated to the SSDs and
ERs. We were, however, not able to fully quantify the uncertainty
intervals of the SSDs and ERs, as not all simulations converged to
a numerical outcome. This finding emphasizes the importance of having
sufficient and well-distributed field data to reliably perform quantile
regression analysis.Typically, the utility
of SSD models to predict toxicity effects on the ecosystem level depends
on a number of assumptions.[114] First, it
is typically assumed that a log-normal distribution describes species
sensitivities toward a certain chemical[4] and that including ten or more species is preferable to obtain representative
SSDs.[28] In our case, the toxicity data
were indeed lognormally distributed, while the number of species included
was eight to ten. Another important assumption is that species selection
is unbiased and fully represents the differences in sensitivity toward
a chemical.[4] In the present study, SSDs
were based on raptorial, piscivorous, and insectivorous bird species,
covering multiple taxonomic groups. Differences in sensitivity of
bird species to dioxin-like compounds, such as certain PCB congeners,
are, however, explained by differences in the aryl hydrocarbon receptor
1 ligand-binding domain (AHR1-LB) and not so much by food sources
(see Table S6 in the Supporting Information). In the present study, Larus argentatus and Sterna hirundo were identified as the species with the highest
EC50 for ΣPCBs, followed by Haliaeetus species and Falco sp.. These findings correspond
with the classification of Farmahin et al.,[115] who indicated that these birds are insensitive to dioxin-like compounds.
The species with the highest sensitivity toward ΣPCBs in our
study was the insectivorous bird Turdus migratorius. Farmahin et al.[115] classified this bird
as semisensitive to dioxin-like compounds. Other birds classified
as semisensitive were Tachycineta bicolor, Troglodytes aedon, and Phalacrocorax sp.
Although experimental studies focusing on the reproductive effects
of PCB residues in eggs have been performed on species classified
as highly sensitive (e.g., European starling (Sturnus vulgaris) or the gray catbird (Dumetella carolinensis)),[116,117] field monitoring data on these species was grossly lacking. This
implies that our SSDs most likely underestimate the effects of dioxin-like
PCBs toward birds.Ecological risks
were significantly
higher in the North American Great Lakes compared to the Arctic region.
This is most likely due to the high number of pollutant point sources
located along the Niagara and Detroit Rivers and the massive storage
of organochlorine compounds in lake sediments that are re-emitted
into the water column and subsequently accumulate in the food chain.[118,119] Note, however, that the calculated ecological risks for the American
Great Lakes do not necessarily cover the trophic levels evenly, as
in this area we found egg residue data encompassing a limited set
of species, covering mainly Tachycineta bicolor and Larus argentatus.Contamination with PCBs contributed
highly to our calculated combined ERs in both areas. While the field-based
average toxicity and spread between the species is rather similar
for the two chemicals included in our study, systematically higher
ΣPCBs concentrations were reported in the field compared to p,p′-DDE. Within the Arctic region,
the high relative ecological risk (and thus combined ER) caused by
PCB-contamination is most likely due to point sources from landfill,
drilling rigs, harbors, and urban areas in Alaska (Bering Sea and
Norton Sound) and Northern Norway (Barents Sea).[120] ERs calculated in other Arctic areas were relatively low,
possibly due to geographical remoteness and the lower anthropogenic
stress that is associated with this. The relatively high combined
ERs for the Great Lakes were due to high individual ERs related to
both PCB and p,p′-DDE contamination.
The highest combined ER in the American Great Lake area was calculated
for Lake Ontario, most likely caused by intensive farming in its catchment
basin,[121] followed by Lake Erie and Lake
Huron. These findings are in line with conclusions drawn in previous
studies focusing on chemical residues in sediment, surface water,
and fish, indicating Lake Ontario as most contaminated.[122,123] Obviously, risks may be different for individual bird species in
other areas or specific locations within the Arctic and Great Lakes,
depending on the actual concentrations present and the sensitivity
of the species. For instance, effects on Pelecanus occidentalis in South Carolina and Phalacrocorax auritus in
Green Bay were associated with p,p′-DDE rather than PCBs.[124,125] By contrast,
in Dutch colonies, multiple studies suggest that Phalacrocorax
carbo sinensis survival and reproduction and subsequent population
development could partly be explained by PCB concentrations.[71,126]
Relevancy
SSDs are typically derived using data obtained
from laboratory experiments, including only a limited number of species.[15,116,127] The present study illustrates
how bird species monitoring data can be used to derive field-based
SSDs. Although field-based SSDs are used before in ecotoxicology,[5,127,128] to our knowledge this study
is the first to derive SSDs for piscivorous, raptorial, and insectivorous
bird species that include effect concentrations obtained through quantile
regression analysis that reduces bias associated with extraneous variables.
SSDs derived from field monitoring data are considered more ecologically
relevant. The use of field data is recommended by the U.S. Environmental
Protection Agency Science Advisory Board for the derivation of ecological
risks of chemicals.[129] This study demonstrates
that the field-based approach can be applied to calculate ecological
risks by combining SSDs with measured environmental POP concentrations.
Authors: Cecilie Miljeteig; Hallvard Strøm; Maria V Gavrilo; Andrey Volkov; Bjørn M Jenssen; Geir W Gabrielsen Journal: Environ Sci Technol Date: 2009-07-15 Impact factor: 9.028
Authors: Chris Marvin; Scott Painter; Donald Williams; Violeta Richardson; Ronald Rossmann; Patricia Van Hoof Journal: Environ Pollut Date: 2004-05 Impact factor: 8.071
Authors: Birgit M Braune; Mark L Mallory; H Grant Gilchrist; Robert J Letcher; Ken G Drouillard Journal: Sci Total Environ Date: 2007-04-05 Impact factor: 7.963