ArticlePDF Available

Abstract and Figures

The present study uses bird eggs of 7 wild species as a biomonitoring tool for sunscreens occurrence. Seven UV filters (UV-Fs), including 3 hydroxy-metabolites of oxybenzone (benzophenone 3, BP3) were characterized in unhatched eggs from Doñana Natural Space (Southwestern, Spain). High frequency of detection was observed for all UV-Fs, ranging from 95% to 100%. The oxybenzone metabolite 4-hydroxybenzophenone (4HB) was ubiquitous at concentrations in the range 12.0-3,348ng g⁻¹ dry weight (dw). The parent compound, oxybenzone, was also present in all samples at lower concentrations (16.9-49.3 ng g⁻¹ dw). Due to the three BP3’s metabolites, benzophenone 1 (BP1), 4HB, and 4,4’-dihydroxybenzophenone (4DHB) presence in unhatched eggs, it can be inferred that parent compounds are absorbed into the bird through the upper gut and the OH-derivatives formed are transferred by the mother to the egg before the lying. White stork (Ciconia ciconia) and western marsh harrier (Circus aeruginosus) were the most contaminated species, with mean total UV-Fs concentrations of 834and 985ng g⁻¹ dw, respectively. Results evidenced that biomagnification process across the bird species studied cannot be ruled out.
Content may be subject to copyright.
A Potential New Threat to Wild Life: Presence of UV Filters in Bird
Eggs from a Preserved Area
Daniel Molins-Delgado,
Manuel Má
ñez,
Ana Andreu,
Fernando Hiraldo,
§
Ethel Eljarrat,
DamiàBarceló
,
,
and M. Silvia Díaz-Cruz*
,
Environmental Chemistry Department, Institute of Environmental Assessment and Water Research (IDÆA), Spanish Council of
Scientic Research (CSIC), C/Jordi Girona 18-26, 08034, Barcelona, Spain
Natural Processes Monitoring Team, Doñana Biological Station (EBD-CSIC), C/Amé
rico Vespucio s/n, 41092 Seville, Spain
§
Department of Applied Biology, Doñana Biological Station (EBD-CSIC), Sevilla, Spain
Catalan Institute for Water Research (ICRA), Parc Cientíc i Tecnològic de la Universitat de Girona. C/Emili Grahit, 101 Edici
H2O, 17003 Girona, Spain
*
SSupporting Information
ABSTRACT: The present study uses bird eggs of seven wild species as a
biomonitoring tool for sunscreens occurrence. Seven UV lters (UV-Fs),
including 3 hydroxy-metabolites of oxybenzone (benzophenone 3, BP3)
were characterized in unhatched eggs from Doñana Natural Space
(Spain). High frequency of detection was observed for all UV-Fs, ranging
from 95% to 100%. The oxybenzone metabolite 4-hydroxybenzophenone
(4HB) was ubiquitous at concentrations in the range 12.03348 ng g1
dry weight (dw). The parent compound, oxybenzone, was also present in
all samples at lower concentrations (16.949.3 ng g1dw). Due to the
three BP3s metabolites, benzophenone 1 (BP1), 4HB, and 4,4-
dihydroxybenzophenone (4DHB) presence in unhatched eggs, it can
be inferred that parent compounds are absorbed into the bird through the upper gut and the OH-derivatives formed are
transferred by the mother to the egg before the lying. White stork (Ciconia ciconia) and western marsh harrier (Circus
aeruginosus) were the most contaminated species, with mean total UV-Fs concentrations of 834 and 985 ng g1dw, respectively.
Results evidenced that biomagnication process across the bird species studied cannot be ruled out.
1. INTRODUCTION
In the past decade, ingredients in personal care products
(PCPs) have been described as chemicals of increasing
environmental concern because of their extensive use, toxicity,
persistence, bioaccumulation, and ubiquity.
1
Thousands of tons
per year of PCPs are produced, which ultimately enter the
environment through bathing, industrial and urban sewage
euents discharges and disposal of unwanted products.
2
As a
consequence, PCPs have been frequently detected in water
bodies,
3,4
sediment,
5,6
and aquatic biota,
79
raising environ-
mental concern because of their endocrine disrupting
activity.
10,11
The current knowledge on these compounds reveals that
PCPs cycling in the environment, particularly the correlation
between the aquatic environmental occurrence and bioaccu-
mulation proles, appear to be similar to that of persistent
organic pollutants (POPs). Among PCPs, UV lters (UV-Fs)
have attracted the highest interest of scientists and of the public
in general due to their extensive use, widespread occurrence
and scarcity of data on their environmental impacts. UV-Fs are
important ingredients in hygiene and beauty products, but also
in plastics, paints, textiles and adhesives.
12
As a result of their
lipophilicity (log Kow > 3) these substances tend to accumulate
in living organisms; for instance, 2-ethylhexyl-p-methoxycinna-
mate (EHMC) has been measured above 200 ng g1dry weight
(dw), octocrylene (OC) at 30 ng g1dw, and oxybenzone
(benzophenone 3, BP3) up to 24 ng g1dw in river sh from
Spain.
9
These values are in good agreement with the
concentrations reported in sh from other European
rivers.
8,1315
The highest levels of EHMC (>290 ng g1dw)
were detected in the predator species Andalusian barbel (L.
sclateri), suggesting that EHMC biomagnication may occur.
The potential biomagnication capacity of EHMC was also
pointed out by Fent et al.
8
when detecting EHMC in
crustacean and molluscs from Switzerland in the range 2250
ng g1lipid weight (lw), but above 700 ng g1lw, in aquatic
sh.
The bioaccumulation of UV-Fs in marine biota has also been
investigated. Gago-Ferrero et al.
16
recently provided the rst
data on the occurrence of UV lter residues in marine
mammals. OC was measured up to 782 ng g1lw in liver tissue
Received: June 30, 2017
Revised: September 4, 2017
Accepted: September 4, 2017
Published: September 4, 2017
Article
pubs.acs.org/est
© 2017 American Chemical Society 10983 DOI: 10.1021/acs.est.7b03300
Environ. Sci. Technol. 2017, 51, 1098310990
from Franciscana dolphin (Pontoporia blainvillei) from Brazil. In
another study, the same authors evidenced the maternal
transfer of UV-Fs in Franciscana and Guiana dolphins. UV-Fs
were detected in all mother-fetus pairs from both species.
Unexpectedly, tissues showed up to 20-folds higher burden in
fetuses than in their respective mothers. Hence, transplacental
discharge was suggested as the UV-Fs contamination pathway
to fetuses.
17
In mussels from the French coast EHMC and OC
were found up to 7000 ng g1dw and 200 ng g1dw,
respectively.
18
Benzotriazoles have also been detected in
aquatic species, including tidal at organisms, sh, mussels,
birds, and hammerhead sharks from the Japan coast, at
concentrations in the range 7.9720 ng g1dw.
6
As the removal of unhatched eggs from the nests has no
eect on the population level in the wild bird species, birds
have been adopted as reliable indicators of persistent pollutants
bioaccumulation. Hence, the occurrence of POPs in bird eggs
has been frequently addressed worldwide.
1921
Nevertheless, to
the authorsknowledge no previous study reported bioaccu-
mulation proles of UV-Fs in eggs. In this frame, the aim of the
present study was to investigate the occurrence and to
determine the concentration and maternal transfer of seven
sunscreen agents in unhatched eggs of dierent wild bird
species from Doñana, a preserved natural area located in
southwest Spain. In addition, the stable isotopes δ15N and δ13C
were determined and their ratios calculated in order to
determine whether UV-Fs transfer along the food web occurs.
2. MATERIALS AND METHODS
2.1. Standards and Reagents. The sunscreens 2,4-
dihydroxybenzophenone (BP1, 99%), 2-hydroxy-4-methoxy-
benzophenone (oxybenzone, BP3, 98%), 4-hydroxybenzophe-
none (4HB, 98%), 4,4-dihydroxybenzophenone (4DHB,
99%), 2-ethylhexyl 2-cyano-3,3-diphenyl acrylate (OC, 97%),
and 2-ethylhexyl 4-(dimethylamino)benzoate (ODPABA,
98%), and 2-(2H-benzotriazole-2-yl)-4-methyl-6-(2-propyl)-
phenol (AllylBZT, 99%), used as internal standard for 2-(2-
benzotriazolyl)-p-cresol (UVP) were purchased from Sigma-
Aldrich (Steinheim, Germany). UVP (98%) was obtained from
TCI (Antwerp, Belgium). BP3-d5(98% D), and 3-(4-
methylbenzylidene) camphor-d4(4MBC-d4, 98% D), used as
internal standards, were supplied by CDN isotopes (Quebec,
Canada). Supporting Information (SI) Table S1 lists the name,
abbreviation, CAS number and log Kow of the target
compounds.
Ethyl acetate (AcEt), dichloromethane (DCM), methanol
(MeOH) and water, all HPLC-grade, as well as the adsorbent
Florisil (0.1500.250 mm) were purchased from Merck
(Darmstadt, Germany).
2.2. Sampling Area and Sample Collection. Egg
samples were collected in the Doñana Natural Space, in the
surrounding areas of La Puebla del Ri ́
o and Almonte, as Figure
1shows. This preserved area is located in southwest Spain and
constitutes a sanctuary for thousands of bird species. Its
location between the African and the European continents
together with its proximity to the Mediterranean Sea and the
Atlantic Ocean makes that area a must-step for migrating
birds.
22
In the present study, 39 unhatched bird eggs of 7 wild species
and 4 dierent orders, that is, falconiformes (western marsh
harrier (Circus aeruginosus), common kestrel (Falco tinnuncu-
lus)), ciconiiformes (white stork (Ciconia ciconia)), charadrii-
formes (slender-billed gull (Chroicocephalus genei), black
headed gull (Chrococephalus ridibundus), gull-billed tern
(Gelochelidon nilotica)), and anseriformes (gadwall (Anas
Strepera)) were collected during nest checking and ringing
operations between 2010 and 2012. The eggs were frozen and
shipped to the lab under cool conditions. Once in the lab the
samples were thawed, homogenized, lyophilized and stored at
20 °C until analysis. No embryos were found in any of the
studied eggs. Table 1 compile information related to the
habitat, diet, and general ecology of the studied species.
2.3. Samples Pretreatment and Analysis. The pretreat-
ment procedure and the analysis methodology applied were
adapted from a previously developed method in our laboratory
for the analysis of UV-Fs in sh.
23
A total of 0.1 g of freeze-
dried sample was needed for the simultaneous analysis of the
target UV-Fs. UV-Fs extraction from the samples was carried
out by pressurized liquid extraction (PLE) using an ASE 350
Accelerated Solvent Extractor (Dionex Corporation, Sunnyvale,
CA) followed by a solid phase extraction (SPE) using Isolute
C18 cartridges, from Biotage. The extracts were then prepared
for the analysis. The separation and detection of the analytes
were performed by liquid chromatography-tandem mass
spectrometry in positive ionization mode using a Symbiosis
Pico chromatograph from Spark Holland (Emmen, The
Netherlands) attached to a 4000 Q TRAP MS/MS analyzer
from Applied Biosystems-Sciex (Foster City, CA) (HPLC-
QqLIT-MS/MS). A Hibar Purospher STAR HR R-18 ec. (50
mm ×2.0 mm, 5 μm) from Merck, preceded by a guard
column of the same packaging material was used during the
chromatographic separation. A detailed description of the
pretreatment and analysis methods can be found in section A.1.
of the SI.
The lipid content was determined gravimetrically. Lipids and
water contents are listed in Table S2 in the SI.
2.4. Method Performance. For all target compounds a
linear response was achieved in the range 0.1500 ng g1dw.
The instrumental limits of detection (ILODs) ranged from 0.1
to 5.7 pg, whereas the instrumental limits of quantication
(ILOQs) were in the range 0.518.9 pg. Precision, expressed as
relative standard deviation (RSD), were always below 18%.
Recovery rates were evaluated for ve replicates at two
concentration levels, 25 and 50 ng g1dw obtaining values
Figure 1. Map showing the location of the Doñana Natural Space
(Spain) (in light gray) and the sampling areas of Almonte (A) and La
Puebla del Ri ́
o (B).
Environmental Science & Technology Article
DOI: 10.1021/acs.est.7b03300
Environ. Sci. Technol. 2017, 51, 1098310990
10984
Table 1. Order, Common Name, Scientic Name, Migratory and Feeding Behavior, Number of Samples Analyzed, And
Sampling Point of Each Species
order common
name scientic name migratory behavior feeding behavior number of
samples sampling
location
Western
marsh
harrier
Circus aeruginosus resident and dispersive birds, small mammals, and eggs 1 La Puebla
del Rí
o
Falconiformes
Common
kestrel Falco tinnunculus resident and dispersive birds, small mammals, insects, and reptiles 10 Almonte
Ciconiiformes White stork Ciconia ciconia mainly migratory but with a
resident population small sh and birds, insects, rodents, amphibians,
reptiles, eggs and remains of human food 8 La Puebla
del Rí
o
Charadriiformes Slender-
billed gull Chrococephalus
genei migratory but with a
resident population
sh and invertebrates 1 La Puebla
del Rí
o
Black-
headed gull Chrococephalus
ridibundus dispersive and partially
migratory
sh, insects, earthworms, and urban and industrial
wastes 4 La Puebla
del Rí
o
Gull-billed
tern Gelochelidon
nilotica migratory sh, insects, and crustaceans 4 La Puebla
del Rí
o
Anseriformes Gadwall Anas strepera resident roots, leaves, seeds, and algae 11 La Puebla
del Rí
o
Table 2. Maximum, Minimum, and Mean Concentrations, and Frequency of Detection for the Target UV-Fs in 0.1 g of Egg
Sample of the Studied Species
a
,
b
concentration ngg1dw
order common name species BP1 BP3 4HB 4DHB ODPABA OC UVP
Falconifoormes Western marsh
harrier Circus aeruginosus maximum na na na na na na na
minimum na na na na na na na
mean 40.6 46.7 895 <MLOQ <MLOQ <MLOQ 2.7
frequency
(%) 100 100 100 100 100 100 100
Common kestrel Falco tinnunculus maximum 53.5 35.2 1200 132 <MLOQ <MLOQ 3.0
minimum 27.9 18.3 20.0 <MLOQ <MLOQ <MLOQ 0.4
mean 39.3 24.8 210 132 <MLOQ <MLOQ 1.5
frequency
(%) 100 100 90 100 100 100 100
Ciconiiformes White stork Ciconia ciconia maximum <MLOQ 29.2 3348 29.0 <MLOQ 26.6 <MLOQ
minimum <MLOQ 19.5 104 <MLOQ <MLOQ 15.2 <MLOQ
mean <MLOQ 22.3 761 29.0 <MLOQ 20.9 <MLOQ
frequency
(%) 100 100 100 100 88 100 88
Charadriiformes Slender-billed gull Chorococephalus genei maximum na na na na na na na
minimum na na na na na na na
mean <MLOQ 22.5 266 <MLOQ <MLOQ <MLOQ <MLOQ
frequency
(%) 100 100 100 100 100 100 100
Black-headed gull Chorococephalis
ridibundus maximum 677 44.4 111 <MLOQ <MLOQ 65.2 8.4
minimum <MLOQ 24.7 72.8 <MLOQ <MLOQ 11.4 1.4
mean 433 34.8 88.4 <MLOQ <MLOQ 33.5 4.9
frequency
(%) 100 100 100 100 100 100 75
Gull-billed tern Gelochelidon nilotica maximum 66.1 49.3 472 <MLOQ <MLOQ <MLOQ 2.0
minimum 29.0 18.2 12 <MLOQ <MLOQ <MLOQ 1.2
mean 42.4 28.3 139 <MLOQ <MLOQ <MLOQ 1.6
frequency
(%) 100 100 100 100 100 100 100
Anseriformes Gadwall Anas strepera maximum 87.3 31.5 560 <MLOQ <MLOQ <MLOQ 0.2
minimum 23.3 16.9 13.5 <MLOQ <MLOQ <MLOQ <MLOQ
mean 38.1 22.1 122 <MLOQ <MLOQ <MLOQ 0.2
frequency
(%) 100 100 100 100 100 100 100
a
na, not applicable.
b
<MLOQ, below the MLOQ.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.7b03300
Environ. Sci. Technol. 2017, 51, 1098310990
10985
between 39 and 125%. Method limits of detection (MLOD)
and quantication (MLOQ) were calculated following the
IUPAC guidelines.
24
MLODs were in the range 0.040.5 ng
g1dw, whereas MLOQ ranged from 0.1 to 1.8 ng g1dw. The
complete list of values is presented in SI Table S3.
2.5. δ13C and δ15N Isotope Analysis. The determination
of the stable isotopes δ13C and δ15N is described in a previous
work.
22
Briey, lipids were extracted from the sample using a
mixture of chloroform : MeOH (2:1, v:v). The samples were
completely covered with the mixture for 24 h. before being
removed. This process was repeated 3 times. After drying the
samples at 50 °C, they were combusted at 1020 °C and
determined using MS. The values, expressed using the standard
δnotation () are listed in SI Table S2.
2.6. Statistical Analysis. Prior analysis, the dierences
between samples were assessed performing a t-student test of
equal variances. The statistical signicance was set at 5%. No
signicant dierence was observed and thus the data was not
normalized. All extend of association between two variables
evaluated in the present study were carried out using
Spearmans correlation for nonparametric data test.
3. RESULTS AND DISCUSSION
3.1. UV-FsConcentration Proles in Bird Eggs. The
results revealed that all the eggs contained residues of UV-Fs.
All target analytes were very frequently detected in the samples
(95100% frequency), however 4DHB, ODPABA, OC and
UVP were mostly at levels below the corresponding MLOQs.
In particular, ODPABA was detected but could not be
quantied. Maximum, minimum, and mean concentrations
measured of UV-Fs are shown in Table 2. Oxybenzone, the
parent compound of 4HB, 4DHB and BP1, was present in all
the samples at much lower concentrations, from 16.87 to 49.28
ng g1dw. The hydroxylated (OH) metabolite 4HB was
ubiquitous and the most concentrated one, showing a
maximum level of 3488 ng g1dw in white stork. Another of
its metabolites, BP1, was also accumulated at high concen-
trations in all the species (23.3677 ng g1dw) with the
exception of the white stork, where the compound could not be
quantied. In contrast, the dihydroxylated metabolite, 4DHB,
was scarcely found. OC was detected in all samples, with the
highest levels found in white stork and black-headed gull. UVP
was the less frequently found compound (95%) and the one at
lower concentrations (up to 8.4 ng g1dw). Tables S4, S5, and
S6 in the SI show the complete list of concentrations with
dierent units.
According to the EU Cosmetics Regulation (Regulation
(EC) N°1223/2009), the maximum concentrations of BP3,
ODPABA and OC allowed for PCPs formulations are 10%, 8%
and 10% (as acid), respectively. The lower allowable proportion
of ODPABA, jointly with a relatively short half-life time in
water in the presence of UV sunlight and free chlorine,
25,26
could, therefore, be the reasons behind why this compound was
scarcely determined in the eggs analyzed.
Benzotriazoles (2-hydroxyphenyl benzotriazole derivatives)
are employed as UV light blockers in paints, coatings, adhesives,
polymeric surfaces, food packings, textiles and construction
materials.
27
In the USA, up to 453 tons were produced/
imported in 2005.
28
Similar to the UV-Fs used in PCPs, UVP is
a sun-blocking agent, which prevents light-induced degradation
reactions of host materials. It has exceptionally strong and
broad-range UV light absorption properties being a highly
ecient UV absorber of both UV A and UV B radiation,
recommended for thermoset plastics and coatings that function
as UV radiation screens for photosensitive substrates.
Furthermore, UVP is very photostable and resistant to
oxidizing and reducing agents. This compound is allowed in
the EU as additive in food packing plastics.
29
In polystyrene
UVP is added in 0.20.3% and up to 0.01% in PET.
30
These
gures support the lower use and thus the lower presence of
this compound in the eggs analyzed in this work.
The dierence observed between the UV-Fs and the UVP
concentration levels might be explained by the dierent uses
and maximum percentages in formulations set by the
regulations. For instance, UV-Fs such as BP1 and BP3 are
allowed as additive in both the manufacture of food packing
plastics and in cosmetics industry, whereas a sun-blocking agent
such as UVP is not currently used in cosmetic formulations.
Another feasible reason for such dierence in concentrations
might be the contamination source. According to the study by
Kameda et al.,
31
on the presence of UV blockers in wastewaters,
there was no correlation between domestic wastewaters and the
occurrence of UVP, suggesting an industrial origin. However, it
is well documented that UV-Fs are not eciently removed
under conventional wastewater treatments and the bioaccumu-
lation capacity of these compounds allows them to be retained
by the adipose tissue of aquatic organisms.
9,12,32
Hence, due to
the absence of industrial activity in the area, the wastewater
treatment plants euents discharges, jointly with urban
contributions from the villages surrounding Doñana Natural
Space would be the responsible for the UV-Fs contamination.
This is the rst study on the identication and quantication
of UV-Fs in bird eggs, to the best of our knowledge. Therefore,
there are no available values to compare with. However, when
comparing egg concentrations with other organisms such as sh
and mussels,
8,1315,33
and other predators such as dolphins,
16,17
the determined concentrations lie within a similar range of
concentrations. Nevertheless, regarding bird eggs in previous
studies carried out in Doñana, other contaminants such as
PBDEs and dechloranes,
22
and pyrethroids were investigated.
34
SI Table S7 shows the concentrations of the pollutants found in
the common bird species surveyed in the Park in the three
previous referenced studies. Results indicate that UV-Fs mean
concentrations were notoriously higher (between 10-fold and
100-fold) in all species compared, whereas PBDEs concen-
trations reached mean values of up to 80 ng g1lw, dechloranes
concentrations were almost 2-fold higher (161 ng g1lw), and
similar for pyrethroids (162 ng g1lw). White stork, western
marsh harrier, and black-headed gull were consistent among the
most contaminated species overall. When correlating the mean
concentrations of PBDEs, dechloranes, and pyrethroids with
those of UV-Fs, it is observed that dechloranes and UV-Fs
follow a similar distribution pattern (ρ= 0.964), suggesting
similar accumulation mechanisms. No signicant correlation
was observed between UV-Fs and PBDEs or pyrethroids (ρ=
0.571 and 0.07, respectively). The measured concentrations of
UV-Fs in eggs are in line with those reported for other organic
pollutants such as PBDEs, determined in coastal zones
worldwide (1.8 and 1400 ng g1wet weight (ww)).
3538
However, UV-Fs concentrations were found to be 1 order of
magnitude higher than those observed in bird eggs for PCDD/
Fs and coplanar PCBs, which were in the range 1.21420 ng
g1lw.
19,3941
Despite the scarcity of data available so far, some UV-Fs have
recently been recognized as important organic contaminants of
the aquatic environment by the European Parliament, due to its
Environmental Science & Technology Article
DOI: 10.1021/acs.est.7b03300
Environ. Sci. Technol. 2017, 51, 1098310990
10986
lipophilicity, endocrine disruption properties and potential for
bioaccumulation (European Parliament, 2007).
42
As a tentative
approach and due to the lack of information on PCPs, we
compared our results with the limits set up by the EU for other
organic pollutants of concern. The Directive 2000/60/EC
(Water Framework Directive, WFD)
43
denes maximum
allowable concentrations (MAC) for considered priority
substances and other contaminants in water and biota. In
view of this, the concentrations of BP3, BP1, 4HB and OC
measured in this study exceed the MAC established as
environmental quality standards for hexachlorobenzene,
hexacyclohexane and mercury (10, 50, and 20 ng g1ww,
respectively) in prey tissue of sh, molluscs, crustaceans, and
other biota. It is noteworthy that toxicity between compounds
and species can vary signicantly, so these assessments must be
taken with caution. UVP barely exceeded 2.4 ng g1ww. By
contrast, ODPABA did not reach the MLOQ (0.03 ng g1ww)
and 4DHB and OC seldom exceeded the MLOQ (0.12 and
0.10 ng g1ww, respectively), constituting a lower risk.
3.2. Bioaccumulation Patterns. Because egg concen-
trations reect accumulated contaminants (i.e., parent com-
pounds and metabolites) in food intake by mothers before the
egg laying of the birds, species-related dierences in
contaminants of prey items, foraging ecology, and breeding
cycles is reected in egg contents. The seven analyzed bird
species had comparable levels of BP3. However, the relative
proportion of the hydroxylated metabolites (i.e., 4HB, 4DHB,
and BP1) was variable. 4DHB was not quantiable in any
species, whereas 62% of the samples had superior concentration
of 4HB than BP1. It has to be highlighted that the higher values
reported of 4HB corresponded to white stork, species in which
BP1 was not quantiable.
The pattern of mean concentration values for BP3 and its
metabolites vary across the species. On this basis, three groups
could be distinguished: (i) 4HB > BP1 > BP3 (common
kestrel, western marsh harrier, gadwall, and gull-billed tern), (ii)
4HB > BP3 and BP1 < MLOD (white stork and slender-billed
gull), and (iii) BP1 > 4HB > BP3 (black-headed gull).
Although the actual metabolic mechanism is unknown, main
factors inuencing the BP3 metabolic pattern in birds maybe
exposure, type and anity of ligand binding, and metabolism
process and kinetics, as reported for polychlorinated biphenyls
(PCBs).
44
Given that none of the analyzed eggs had embryos at
any state of development, the potential contribution of
metabolites due to the embryos development was discarded.
Regarding the other compounds, OC was only detected in
species from groups (i) and (ii), and UVP was not observed in
group (ii). It must be pointed out that, in the charadriiformes
group each species presents a dierent concentrations pattern.
with only black-headed gull having a dierent one to the other
species of the same order. Of these three species, black-headed
gull has a dierent pattern to that of other species from the
same order. This could be related to its feeding behavior, as it is
the only one that does not have sh in its diet and nourishes
from urban and industrial wastes.
Regarding their migratory behavior, species in group (i) are
resident species (except gull-billed tern), species in group (ii)
are mainly migratory species, and the species in group (iii) is a
dispersive and partially migratory species (Table 1). This
suggests that the migratory behavior and the diet intake and
further metabolisation of UV-Fs might be correlated. There is
scarce information about the accumulation of ODPABA in
biota, which may be due to its tendency to get adsorbed on
sediment or to readily degrade in the presence of UV sunlight
or free chlorine.
25,45
The mechanisms driving the bioaccumulation of UV-Fs are
not yet well understood. Organic lipophilic pollutants such as
PCBs, with log Kow between 5 and 7.5 are known to be
absorbed through the birdsupper-gut, the same mechanism
used to absorb lipids.
46
This study also pointed out that POPs
distribution among tissues was not dependent on the
compoundslog Kow, but rather on the adipose content of
the tissues. On the contrary, it is known that the excretion of
these pollutants does rely on their log Kow.
46
This is in
agreement with what Gago-Ferrero et al.
9
discussed concerning
lipophilic UV-Fs (log Kow >3)insh and lipid content in the
tissue.
Compounds with higher log Kow are good candidates to
undergo biomagnication through the food web; those more
polar are expected to be metabolized in the gut and excreted.
However, if the metabolism reactions take place within the
organism tissues, contaminants, and metabolites may be
protected from elimination processes, be accumulated, and
then transferred to the ospring.
46,47
The most common
metabolic processes involve the action of enzymes that react
more easily with the alkyl-groups and facilitate the formation of
low log Kow hydroxylated derivatives.
44,46,48
A previous study
analyzing PCBs and their OH-metabolites
49
pointed out that
the generation of metabolites in unhatched eggs was highly
unlikely due to the absence of embryonic development. The
same study concluded that the transfer of the metabolites
occurs through binding processes between the OH-metabolites
and proteins.
49
This is in line with the fact that the highest
exposure to pollutants in birdslife occur during hatching,
whereas in mammals, exposure mainly occurs during the
nursing period.
46,47
Nonetheless, the presence of UV-Fs in bird
eggs could not only aect the avian species involved, but also
has the potential to increase the exposure of these compounds
to egg predators, as other organic pollutants do.
49
Along these
lines, similar processes to those described for POPs may well be
applicable for UV-Fs.
To assess the exposure and biomagnication of contaminants
in organisms through the diet, the determination of stable
isotopes present on a biological sample serves as a powerful
tool. The δ15N indicates the position in the food web, whereas
the carbon food source is identied by δ13C. The stable
isotopes δ15N and δ13C of unhatched eggs were analyzed and
results reect the isotopic signature of mothers.
50
Total concentrations of UV-Fs for each species are shown in
SI Figure S1. The mean values of δ15N and δ13C are shown in
SI Figure S2. As regards δ13C, two species groups were
observed: western marsh harrier, gull-billed tern, white stork,
and common kestrel (mean δ13C between 22.54 and 23.86)
on one hand and black-headed gull, slender-billed gull, and
gadwall (mean δ13C between 17.82 and 19.20) showing two
well-dierentiated habitats. That is in agreement with what is
known about their habitat-based diets, as the species in the rst
group are of land-based diet, whereas the species in the second
group fall upon the aquatic-based diet category.
22
For unknown
reasons, the exceptions to this would be gull-billed tern and
black-headed gull, that shared a habitat-based diet opposite to
the one showed here. δ15N values are responsive to external
sources of nitrogen such as sewage and agricultural activities in
the area, as well as inputs through natural processes, being
manure and sewage waters the biggest contributors of 15N.
51
These values provide information about the position in the
Environmental Science & Technology Article
DOI: 10.1021/acs.est.7b03300
Environ. Sci. Technol. 2017, 51, 1098310990
10987
food web, with higher values of δ15N indicating upper positions.
In order to determine whether between δ15N and UV-Fs
occurrence hinted biomagnication through the food web, the
mean values of δ15N and UV-Fs concentrations were correlated
using a Spearmans test, but the low coecient (ρ= 0.04)
indicated no correlation. However, as argued Barón et al.,
22
the
human activities in the area of Doñana appeared to heavily
impact the overall content of 15N in the mothers, and thus in
their eggs, misleadingly allocating the species at dierent levels
of the food web. To avoid such issue, a larger number of
specimens would be needed.
It has to be highlighted that the highest mean concentrations
of BP3, 4HB, and the total UV-Fs load were observed in
western marsh harrier. The black-headed gull is a dispersive and
partially migratory species. When comparing the migration
behavior of this species with others from the same habitat, and
as suggested in a previous study by Huertas et al.,
52
migration
allows the transfer of contaminants among food webs from
dierent areas. Additionally, the feeding habits of the species
should be considered, as the black-headed gull is the only
reported species in this study that feeds on industrial and urban
wastes.
22
Nevertheless, this assessment must be taken with
caution, as contaminant concentrations can greatly vary
between individuals of the same species, and an in-depth
study would require a larger number of specimens of each
species, as represented in SI Figure S2.
Although most of the species analyzed in this study feed on
invertebrates, sh, or plant material, the white stork and the
western marsh harrier diet contains eggs from other species,
and the western marsh harrier together with the common
kestrel feed on other birds. Given that, the transfer of UV-Fs
through the diet from one species to another, propagating their
presence through the food web, should not be ruled out,
considering that the number of available samples for species is
low. Because of many of the target UV-Fs display endocrine
disrupting activity; these outcomes are indicative of the need
for further risk assessment regarding wildlife to help interpret
the implications for observed trends in UV-Fs bioaccumulation
and evaluation on their potential biomagnication. The data
provided in this rst study corroborate that bird eggs are useful
bioindicators to assess the occurrence of UV-F residues in the
environment.
ASSOCIATED CONTENT
*
SSupporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acs.est.7b03300.
The in-depth description of the methods of analysis and
the additional tables and gures (PDF)
AUTHOR INFORMATION
Corresponding Author
*E-mail: silvia.diaz@idaea.csic.es.
ORCID
Daniel Molins-Delgado: 0000-0002-3105-8155
M. Silvia Díaz-Cruz: 0000-0003-3331-4076
Notes
The authors declare no competing nancial interest.
ACKNOWLEDGMENTS
This work was funded by the Spanish Ministry of Environment
and Rural and Marine Aairs through the project IMPAR (ref.
106/2010). This work has also been partly funded by the
Generalitat de Catalunya (Consolidated Research Group:
Water and Soil Quality Group 2014-SGR-418). We are grateful
to the Doñana Biological Station Natural Processes Monitoring
Team, especially Luis Garci ́
a, JoséLuis del Valle, Rubé
n
Rodri ́
guez, JoséLuis Arroyo, Antonio Marti ́
nez and Alfredo
Chico, as well as to Javier Chicano, for their eorts to collect
bird eggs. Biotage is acknowledged for providing SPE
cartridges. We also want to thank Renaud de Stephanis from
the EBD-CSIC for the nancial support with the stable isotope
analysis, and to Albert Ramoneda for his help in the UV-Fs
analysis.
REFERENCES
(1) Molins-Delgado, D.; Gago-Ferrero, P.; Díaz-Cruz, M. S.; Barceló,
D. Single and joint ecotoxicity data estimation of organic UV filters
and nanomaterials toward selected aquatic organisms. Urban ground-
water risk assessment. Environ. Res. 2016,145, 126134.
(2) Molins-Delgado, D.; Díaz-Cruz, M. S.; Barceló, D. Ecological risk
assessment associated to the removal of endocrine-disrupting parabens
and benzophenone-4 in wastewater treatment. J. Hazard. Mater. 2016,
310, 143151.
(3) Felix, T.; Hall, B.; Brodbelt, J. Determination of benzophenone-3
and metabolites in water and human urine by solid-phase micro-
extraction and quadrupole ion trap GCMS. Anal. Chim. Acta 1988,
371, 195203.
(4) Tanwar, S.; Di Carro, M.; Ianni, C.; Magi, E. Occurrence of PCPs
in natural waters from Europe. Handbook of Environmental Chemistry
2014,36,3772.
(5) Díaz-Cruz, M. S.; Llorca, M.; Barceló, D. Organic UV filters and
their photodegradates, metabolites and disinfection by-products in the
aquatic environment. TrAC, Trends Anal. Chem. 2008,27, 873887.
(6) Nakata, H.; Murata, S.; Filatreau, J. Occurrence and
concentrations of benzotriazole UV stabilizers in marine organisms
and sediments from the Ariake Sea, Japan. Environ. Sci. Technol. 2009,
43, 69206926.
(7) Buser, H.; Balmer, M.; Schmid, P.; Kohler, M. Occurrence of UV
filters 4-methylbenzylidene camphor and octocrylene in fish from
various Swiss rivers with inputs from wastewater treatment plants.
Environ. Sci. Technol. 2006,40, 14271431.
(8) Fent, K.; Zenker, A.; Rapp, M. Widespread occurrence of
estrogenic UV-filters in aquatic ecosystems in Switzerland. Environ.
Pollut. 2010,158, 18171824.
(9) Gago-Ferrero, P.; Díaz-Cruz, M. S.; Barceló, D. UV filters
bioaccumulation in fish from Iberian river basins. Sci. Total Environ.
2015,518, 518525.
(10) Kunz, P.; Fent, K. Multiple hormonal activities of UV filters and
comparison of in vivo and in vitro estrogenic activity of ethyl-4-
aminobenzoate in fish. Aquat. Toxicol. 2006,79, 305324.
(11) Kunz, P.; Galicia, H.; Fent, K. Comparison of in vitro and in
vivo estrogenic activity of UV filters in fish. Toxicol. Sci. 2006,90,
349361.
(12) Molins-Delgado, D.; Díaz-Cruz, M. S.; Barceló, D. Removal of
polar UV stabilizers in biological wastewater treatments and
ecotoxicological implications. Chemosphere 2015,119, S51S57.
(13) Balmer, M.; Buser, H.; Müller, M.; Poiger, T. Occurrence of
some organic UV filters in wastewater, in surface waters, and in fish
from Swiss lakes. Environ. Sci. Technol. 2005,39, 953962.
(14) Meinerling, M.; Daniels, M. A validated method for the
determination of traces of UV filters in fish using LC-MS/MS. Anal.
Bioanal. Chem. 2006,386, 14651473.
(15) Zenker, A.; Schmutz, H.; Fent, K. Simultaneous trace
determination of nine organic UV-absorbing compounds (UV filters)
in environmental samples. J. Chomatogr. A 2008,1202,6474.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.7b03300
Environ. Sci. Technol. 2017, 51, 1098310990
10988
(16) Gago-Ferrero, P.; Alonso, M.; Bertozzi, C.; Marigo, J.; Barbosa,
L.; Cremer, M.; Secchi, E.; Azevedo, A.; Lailson-Brito, J.; Torres, J.;
Malm,O.;Eljarrat,E.;Díaz-Cruz,M.S.;Barcelo
́,D.First
determination of UV filters in marine mammals. Octocrylene levels
in Franciscana dolphins. Environ. Sci. Technol. 2013,47, 56195625.
(17) Alonso, M.; Feo, M.; Corcellas, C.; Gago-Ferrero, P.; Bertozzi,
C.; Marigo, J.; Flach, L.; Meirelles, A.; Carvalho, V.; Avezedo, A.;
Torres, J.; Lailson-Brito, J.; Malm, O.; Díaz-Cruz, M. S.; Eljarrat, E.;
Barceló, D. Toxic heritage: Maternal transfer of pyrethroid insecticides
and sunscreen agents in dolphins from Brazil. Environ. Pollut. 2015,
207, 391402.
(18) Bachelot, M.; Li, Z.; Munaron, D.; Le Gall, P.; Casellas, C.;
Fenet, H.; Gomez, E. Organic UV filter concentrations in marine
mussels from French coastal regions. Sci. Total Environ. 2012,420,
273279.
(19) Wang, Y.; Lam, J.; So, M.; Yeung, L.; Cai, Z.; Hung, C.; Lam, P.
Polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated diben-
zofurans (PCDFs), dioxin-like polychlorinated biphenyls (PCBs) and
polybrominated diphenyl ethers (PBDEs) in waterbird eggs of Hong
Kong, China. Chemosphere 2012,86, 242247.
(20) Bouwman, H.; Kylin, H.; Choong Kwet Yive, N.; Tatayah, V.;
Løken, K.; Utne Skaare, J.; Polder, A. First report of chlorinated and
brominated hydrocarbon pollutants in marine bird eggs from an
oceanic Indian Ocean island. Environ. Res. 2012,118,5364.
(21) Mallory, M.; Braune, B. Tracking contaminants in seabirds of
Arctic Canada: Temporal and spatial insights. Mar. Pollut. Bull. 2012,
64, 14751484.
(22) Barón, E.; Má
ñez, M.; Andreu, A. C.; Sergio, F.; Hiraldo, F.;
Eljarrat, E.; Barceló, D. Bioaccumulation and biomagnification of
emerging and classical flame retardands in birds of 14 species from
Doñana Natural Space and surrounding areas (South-western Spain).
Environ. Int. 2014,68, 118126.
(23) Gago-Ferrero, P.; Díaz-Cruz, M. S.; Barceló, D. Multi-residue
method for trace level determination of UV filters in fish based on
pressurized liquid extraction and liquid chromatographyquadrupole-
linear ion trap-mass spectrometry. J. Chomatogr. A 2013,1286,93
101.
(24) International Union of Pure and Applied Chemistry. Golden
Book, Compendium of Chemical Terminology. 2014.
(25) Sakkas, V.; Giokas, D.; Lambropoulou, D.; Albanis, T. Aqueous
photolysis of the sunscreen agent actyl-dimethyl-p-aminobenzoicc
acid: formation of disinfection byproducts in chlorinated swimming
pool water. J. Chomatogr. A 2003,1016, 211222.
(26) Ahmed, M.; Johir, M.; Zhou, J.; Ngo, H.; Guo, W.; Sornalingam,
K. Photolytic and photocatalytic degradation of organic UV filters in
contaminated water. Current Opinion in Green and Sustainable
Chemistry 2017,6,8592.
(27) Reiter, S.; Buchberger, W.; Klampf, C. Rapid identification and
semi-quantitative determination of polymer additives by desorption
electrospray ionization/time-of-flight mass spectrometry. Anal. Bioa-
nal. Chem. 2011,400, 23172322.
(28) U.S. Environmental Protection Agency. Screening-level hazard
characterization sponsored chemicals Category Phosphoric Acid
Derivatives. 2009.
(29) European Commission. Commission Regulation (EU) No 10/
2011 of 14 January 2011 on plastic materials and articles intended to
come into contact with food. Official Journal of the European Union
2011,50,189.
(30) Smith, S.; Taylor, L. Extraction of various additives from
polystyrene and their subsequent analysis. Chromatographia 2002,56,
165169.
(31) Kameda, Y.; Kimura, K.; Miyazaki, M. Occurrence and profiles
of organic sun-blocking agents in surface waters and sediments in
Japanese rivers and lakes. Environ. Pollut. 2011,159, 15701576.
(32) Montesdeoca-Esponda, S.; Sosa-Ferrera, Z.; Santana-rodriguez,
J. On-line solid-phase extraction coupled to ultra-performance liquid
chromatography with tandem mass spectrometry detection for the
determination of benzotriazole UV stabilizers in coastal marine and
wastewater samples. Anal. Bioanal. Chem. 2012,403, 867876.
(33) Nagtegaal, M.; Ternes, T.; Baumann, W.; Nagel, R. UV-
Filtersubstanzen in Wasser und Fischen. Umweltwiss. Schadst.-Forsch.
1997,9,7986.
(34) Corcellas, C.; Andreu, A.; Má
ñez, M.; Sergio, F.; Hiraldo, F.;
Eljarrat, E.; Barceló, D. Pyrethroid insecticides in wild bird eggs from a
World Heritage Listed Park: A case study in Doñana National Park
(Spain). Environ. Pollut. 2017,228, 321330.
(35) Carpinteiro, I.; Abuín, B.; Rodríguez, I.; Ramil, M.; Cela, R.
Pressurized solvent extraction followed by gas chromatography
tandem mass spectrometry for the determination of benzotriazole
light stabilizers in indoor dust. J. Chomatogr. A 2010,1217, 3729
3735.
(36) Norstrom, R.; Simon, M.; Moisey, J.; Wakeford, B.; Weseloh, D.
Geographical distribution (2000) and temporal trends (1981- 2000) of
brominated diphenyl ethers in Great Lakes herring gull eggs. Environ.
Sci. Technol. 2002,36, 47834789.
(37) Vorkampf, K.; Christensen, J.; Glasius, M.; Riget, F. Persistent
halogenated compounds in black guillemots (Cepphus grylle) from
Greenland - Levels, compound patterns and spatial trends. Mar. Pollut.
Bull. 2004,48, 111121.
(38) Elliot, J.; Wilson, L.; Wakeford, B. Polybrominated Diphenyl
Ether Trends in Eggs of Marine and Freshwater Birds from British
Columbia, Canada, 1979 - 2002. Environ. Sci. Technol. 2005,39, 5584
5591.
(39) Jones, P.; Hannah, D.; Buckland, S.; Day, P.; Leathem, S.;
Porter, L.; Auman, H.; Sanderson, C.; Summer, C.; Ludwig, J.;
Colborn, T.; Geisy, J. Persistent synthetic chlorinated hydrocarbons in
albatross tissue samples from Midway Atoll. Environ. Toxicol. Chem.
1996,15, 17931800.
(40) Kannan, K.; Corsolini, S.; Imagawa, T.; Focardi, S.
Polychlorinated-naphthalenes,-biphenyls,-dibenzo-p-dioxins,-dibenzo-
furans and p, p-DDE in bluefin tuna, swordfish, cormorants and barn
swallows from Italy. Ambio 2002,31, 207211.
(41) Braune, B.; Simon, M. Dioxins, furans, and non- ortho PCBs in
Canadian Arctic seabirds. Environ. Sci. Technol. 2003,37, 30713077.
(42) European Parliament. European Parliament legislative resolution
of 22 May 2007 on the proposal for a directive of the European
Parliament and of the Council on environmental quality standards in
the eld of water policy and amending Directive 2000/60/EC
(COM(2006)0397 C60. 2007.
(43) European Parliament. Water Framework Directive. Directive
2000/60/EC of the European Parliament and of the Council of 23
October 2000 establishing a framework for Community action in the
eld of water policy. 2000.
(44) Letcher, R.; Klasson-Wehler, E.; Bergman, A. Methyl Sulfone
and Hydroxylated Metabolites of Polychlorinated Biphenyls, in:
Anthropogenic Compounds Part K. Handbook of Environmental
Chemistry 2000,3K, 315359.
(45) Nakajima, M.; Kawakami, T.; Niino, T. Aquatic fate of
sunscreen agents octyl-4-methoxycinnamate and octyl-4-dimethylami-
nobenzoate in model swimming pools and the mutagenic assays of
their. J. Health Sci. 2009,55, 363372.
(46) Norstrom, R. Understanding bioaccumulation of POPs in food
webs. Environ. Sci. Pollut. Res. 2002,9, 300303.
(47) Norstrom, R.; Clark, T.; Enright, M.; Leung, B.; Drouillard, K.;
Macdonald, C. ABAM, a model for bioaccumulation of POPs in birds:
Validation for adult herring gulls and their eggs in Lake Ontario.
Environ. Sci. Technol. 2007,41, 43394347.
(48) Nieto, A.; Borrull, F.; Marcé
, R.; Pocurull, E. Determination of
personal care products in sewage sludge by pressurized liquid
extraction and ultra-high performance liquid chromatography-tandem
mass spectrometry. J. Chomatogr. A 2009,1216 (30), 56195625.
(49) Fängström, B.; Athanasiadou, M.; Athanassiadis, I.; Weihle, P.;
Bergmann, A. Hydroxylated PCB metabolites in nonhatched fulmar
eggs from the Faroe Islands. Ambio 2005,34, 184187.
(50) Bearhop, S.; Waldron, S.; Vortier, S.; Furness, R. Factors that
influence assimilation rates and fractionation of nitrogen and carbon
stable isotopes in avian blood and feathers. Physiol. Biochem. Zool.
2002,75, 451458.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.7b03300
Environ. Sci. Technol. 2017, 51, 1098310990
10989
(51) Wunderlin, D. Fate of anthropic pollutants to Suqui ́
a River
basin. Transfer to aquatic biota, including edible sh. NET-SCARCE
International Conferences, Barcelona, 2016.
(52) Huertas, D.; Grimalt, J.; Jover, L.; Sanpera, C.; Ruiz, X.
Organochlorine compounds in Purple Heron eggs (Ardea purpurea)
nesting in sites located around a chlor-alkali plant (Ebro River). Sci.
Total Environ. 2015,540, 211220.
Environmental Science & Technology Article
DOI: 10.1021/acs.est.7b03300
Environ. Sci. Technol. 2017, 51, 1098310990
10990
... Vila et al. (2016) recorded high concentration of BP-3 in Spain (692 mg.L À1 ), during summer in tourist areas. Studies have reported concentrations of UV filters, including BP-3, in aquatic organisms, such as bivalves (Groz et al. 2014;He et al. 2019), crustaceans (He et al. 2017), eels (Fent et al. 2010), freshwater (Zenker et al. 2008) and marine fish (Molins-Delgado et al. 2018), marine mammals (Gago-Ferrero et al. 2013a), seabirds (Molins-Delgado et al. 2017), and aquatic plants (Aznar et al. 2017). Due to their lipophilic properties (Log Kow ¼ 3.79) and relative stability to biotic degradation, UV filters tend to accumulate in biological tissues, such as muscle and adipose tissue (Gago-Ferrero et al. 2013b;Vione et al. 2013). ...
Article
Personal care products, such as UV filters, are frequently present in aquatic ecosystems, but studies on their impact on marine organisms are still scarce. Here we addressed the effects of benzophenone-3 (BP-3) on the antioxidant status of Perna perna mussels exposed to concentrations of 0.1 and 3 μg.L-1 for 72 h and 7 days. Glutathione peroxidase (GPx), glutathione reductase (GR), glutathione S-transferase (GST), glucose-6-phosphate dehydrogenase (G6PDH) activity and lipoperoxidation (MDA) were evaluated in the gills. A significant reduction (p < 0.05) in the activity of G6PDH and GPx was observed after exposure for 7 days to 0.1 µg.L-1. However, no significant differences were observed in GST activity and MDA levels, independently of the exposure time. Principal component analysis (PCA) showed an association of BP-3 highest concentration with GR and MDA at 72 h and only with GR at 7 days of exposure. Similarly, the integrated biomarker response (IBR) demonstrated GR and MDA alterations. In conclusion, environmentally relevant concentrations of BP-3 altered antioxidant and auxiliary enzymes, which could cause long-term damage to P.perna mussels. The need to implement more efficient techniques in wastewater treatment systems is pointed out, especially in summer, when UV filters are used more frequently and abundantly.
... 24 In addition, BP3 was previously found in eggs of various bird species from Donãna National Park in Spain, with mean concentrations ranging from 22.1 to 46.7 ng/g (dry weight). 64 Due to the different units of concentration, it is difficult to compare the results from this previous study with the results of the present study, but assuming that avian eggs have a water content between 70 and 85%, 65 the concentrations of BP3 in Donãna National Park bird eggs were around 3.0 to 7.0 ng/g (ww), which were greater than those of fulmar and murre eggs from PLI, suggesting a potential geographic pattern for this contaminant in birds. The adverse effects of BP3 on birds are largely unknown, as with most chemicals of emerging concern, the potential effects associated with the observed wild levels cannot be determined at this time. ...
Article
Full-text available
Ultraviolet (UV) absorbents and industrial antioxidants are contaminants of emerging concern (CECs), but little is known about their distribution in Arctic wildlife, as well as how these contaminants vary over time, across regions, and between species. We used archived egg samples to examine the temporal patterns of 26 UV absorbents and industrial antioxidants in three seabird species (black-legged kittiwakes Rissa tridactyla, thick-billed murres Uria lomvia, northern fulmars Fulmarus glacialis) sampled in Arctic Canada between 1975 and 2019. Various synthetic phenolic antioxidants, aromatic secondary amines, benzotriazole UV stabilizers, and organic UV filters were detected in the seabird eggs. Overall, kittiwakes had higher levels of several UV absorbents and industrial antioxidants. Most target contaminants reached their peak concentrations at different points during the 44-year study period or did not vary significantly over time. None of these contaminant concentrations have increased in recent years. The antioxidant 2-6-di-tert-butyl-4-methylphenol (BHT) was the most frequently detected contaminant in seabird eggs, and its level significantly declined over the course of the study period in kittiwake eggs but did not change in the eggs of murres and fulmars. Future research should examine the effects of these CECs on the health of avian species, the sources, and exposure pathways of these contaminants.
... Consequently, organic UV filters have been reported to bioaccumulate in various aquatic animals. However, these pollutants are not limited to marine environments only, since they have been detected in Swiss cormorants and bird eggs in Spain (Fent et al. 2010, Molins-Delgado et al. 2017. This fact illustrates the severity of biomagnification, a phenomenon which is very important in the ecosystem pollution analysis. ...
Article
Full-text available
Sunscreen use has increased in recent years, as sunscreen products minimize the damaging effects of solar radiation. Active ingredients called ultraviolet (UV) filters or UV agents, either organic or inorganic, responsible for defending skin tissue against harmful UV rays, are incorporated in sunscreen formulations. UV agents have a serious impact on many members of bio communities, and they are transferred to the environment either directly or indirectly. Many organic UV filters are found to be accumulated in marine environments because of high values of the octanol/water partition coefficient. However, due to the fact that UV agents are not stable in water, unwanted by-products may be formed. Experimental studies or field observations have shown that organic UV filters tend to bioaccumulate in various aquatic animals, such as corals, algae, arthropods, mollusks, echinoderms, marine vertebrates. This review was conducted in order to understand the effects of UV agents on both the environment and marine biota. In vivo and in vitro studies of UV filters show a wide range of adverse effects on the environment and exposed organisms. Coral bleaching receives considerable attention, but the scientific data identify potential toxicities of endocrine, neurologic, neoplastic and developmental pathways. However, more controlled environmental studies and long-term human use data are limited. Several jurisdictions have prohibited specific UV filters, but this does not adequately address the dichotomy of the benefits of photoprotection vs lack of eco-friendly, safe, and approved alternatives.
Article
Anthropogenic activities have caused a steady decline of common kestrel (Falco tinnunculus) since the 1980s. Effects, especially sublethal effects of contaminants, need to be investigated to ensure the conservation of this species. Data about countries, biological material, contaminants classes, and methodological approaches were collected from scientific publications to highlight gaps on common kestrel toxicology and ecotoxicology. We found that most studies have been conducted in Europe and in the field, underlining a lack of in vitro studies. The studies investigated manly contaminant levels, while sublethal effects, evaluation of emerging contaminants and use of non-invasive or low-invasive samples were scarce. This work shows important gaps on toxicological status of the common kestrel, highlighting the importance of developing a non-lethal approach that combines responses at different levels of biological organization, as well as data on chemical contamination and on the environment in which the different populations inhabit.
Article
To carry out risk assessments of benzophenone-type UV filters (BPs), fast and accurate analytical methods are crucial to determine and monitor levels in the environment. This study presents an LC-MS/MS method that requires minimal sample preparation and yet can identify 10 different BPs in environmental samples such as surface or wastewater resulting in a LOQ range from 2 to 1060 ng/L. The method suitability was tested through environmental monitoring, which showed that, BP-4 is the most abundant derivative found in the surface waters of Germany, India, South Africa and Vietnam. BP-4 levels correlate with the WWTP effluent fraction of the respective river for selected samples in Germany. Peak values of 171 ng/L for 4-hydroxybenzophenone (4-OH-BP), as measured in Vietnamese surface water, already exceed the PNEC value of 80 ng/L, elevating 4-OH-BP to the status of a new pollutant that needs more frequent monitoring. Moreover, this study reveals that during biodegradation of benzophenone in river water, the transformation product 4-OH-BP is formed which contain structural alerts for estrogenic activity. By using yeast-based reporter gene assays, this study provides bio-equivalents of 9 BPs, 4-OH-BP, 2,3,4-tri-OH-BP, 4-cresol and benzoate and complements the existing structure-activities relationships of BPs and their degradation products.
Article
Several anthropogenic contaminants have been identified as competing with the thyroid hormone thyroxine (T4) for binding to transport proteins as transthyretin (TTR). This binding can potentially create toxicity mechanisms posing a threat to human health. Many organic UV filters (UVFs) and paraben preservatives (PBs), widely used in personal care products, are chemicals of emerging concern due to their adverse effects as potential thyroid-disrupting compounds. Recently, organic UVFs have been found in paired maternal and fetal samples and PBs have been detected in placenta, which opens the possibility of the involvement of TTR in the transfer of these chemicals across physiological barriers. We aimed to investigate a discrete set of organic UVFs and PBs to identify novel TTR binders. The binding affinities of target UVFs towards TTR were evaluated using in vitro T4 competitive binding assays. The ligand-TTR affinities were determined by isothermal titration calorimetry (ITC) and compared with known TTR ligands. In parallel, computational studies were used to predict the 3-D structures of the binding modes of these chemicals to TTR. Some organic UVFs, compounds 2,2′,4,4′-tetrahydroxybenzophenone (BP2, Kd = 0.43 μM); 2,4-dihydroxybenzophenone (BP1, Kd = 0.60 μM); 4,4′-dihydroxybenzophenone (4DHB, Kd = 0.83 μM), and 4-hydroxybenzophenone (4HB, Kd = 0.93 μM), were found to display a high affinity to TTR, being BP2 the strongest TTR binder (ΔH = −14.93 Kcal/mol). Finally, a correlation was found between the experimental ITC data and the TTR-ligand docking scores obtained by computational studies. The approach integrating in vitro assays and in silico methods constituted a useful tool to find TTR binders among common organic UVFs. Further studies on the involvement of the transporter protein TTR in assisting the transplacental transfer of these chemicals across physiological barriers and the long-term consequences of prenatal exposure to them should be pursued.
Article
Organic ultraviolet absorbents (UVAs) have attracted increasing concern due to their ubiquity, bioaccumulation, and potential toxicity. However, available information on their occurrence and transfer in terrestrial environment is still extremely insufficient. In this study, we investigated twelve UVAs in the soils and five terrestrial plant species from a typical industrial area in South China, and found their total concentrations were 5.87–76.1 (median 13.1) and 17.9–269 (median 82.9) ng/g dry weight, respectively. Homosalate was dominant in soils while benzophenone and octrizole were predominant in plants, likely due to their complex sources and bioaccumulation preferences. The bioaccumulation factors (BAFs) were further evaluated based on the ratios of UVA concentrations in plants and soils. The observed BAFs of UVAs were compound and species-specific, and most of them were much >1.0, indicating the chemicals could be transferred from soils to plants. To the best of our knowledge, this is the first report of organic UVAs in field soil-plant systems, providing information that may improve our understanding of the bioaccumulability of these chemicals in terrestrial environment and the associated risks. More studies are needed to investigate the transfer and bioaccumulation of such chemicals in soils and terrestrial biota.
Article
UV filters are used daily by millions of people. Not all of these filters, however, are 100% biodegradable, and many wastewater treatments plants are ill-equipped to filter them properly. As a result, UV filters are increasingly reaching the environment. Various types have been detected in soil, continental water, oceans, and numerous organisms, including algae, corals, fish, mammals, and even land birds. In addition, some filters, benzophenone-3 and octocrylene in particular, are toxic to these organisms. Toxic effects include coral bleaching and interference with metabolic, enzymatic, and reproductive activities in practically all organisms. Preliminary data suggest that UV filters may be bioaccumulating in humans, as they have been detected in urine and breast milk. It should be noted, however, that research into the environmental impact of UV filters holds challenges and limitations.
Article
Sunscreens containing broad‐spectrum ultraviolet (UV) filters play an essential role in protecting the skin against the damage induced by sun overexposure. However, the widespread use of sunscreens and other personal care products containing these filters has led to these compounds being widely detected in the environment and being identified as emerging pollutants in marine waters. Concerns raised by laboratory studies investigating the potential impact of UV filters on coral communities have already led to bans on the use of some sunscreens in a few tourist hotspots. Although UV filter pollution may be just one of the many environmental factors impacting coral health worldwide, the media attention surrounding these studies and the legislative changes may lead patients to question dermatologists about the environmental safety of some sunscreen products. This review provides an overview of current knowledge on the impact of UV filters on marine ecosystems, concentrating on recent studies examining the effects of commonly used filters on organisms at low trophic levels and of how alternative approaches, such as metabolomics, can be used to further assess UV filter ecotoxicity. Current gaps in our knowledge are also discussed, most notably the need to increase our understanding of the longer‐term fate and behaviour of UV filters in the marine environment, develop more adapted standardized ecotoxicity tests for a wider range of marine species, and evaluate the impact of UV filters on the marine food web. We then discuss future perspectives for the development of new, more environmentally friendly, filters that may enable the use of the most toxic compounds to be reduced without compromising the effectiveness of sunscreen formulations. Finally, we consider how dermatologists play a key role in educating patients on the need for a balanced approach to sun exposure, sun protection, and conservation of the marine environment.
Article
Full-text available
The occurrence of eight organic UV filters (UV-Fs) was assessed in fish from four Iberian river basins. This group of compounds is extensively used in cosmetic products and other industrial goods to avoid the damaging effects of UV radiation, and has been found to be ubiquitous contaminants in the aquatic ecosystem. In particular, fish are considered by the scientific community to be the most feasible organism for contamination monitoring in aquatic ecosystems. Despite that, studies on the bioaccumulation of UV-F are scarce. In this study fish samples from four Iberian river basins under high anthropogenic pressure were analysed by liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). Benzophenone-3 (BP3), ethylhexyl methoxycinnamate (EHMC), 4-methylbenzylidene camphor (4MBC) and octocrylene (OC) were the predominant pollutants in the fish samples, with concentrations in the range of ng/gdryweight (d.w.). The results indicated that most polluted area corresponded to Guadalquivir River basin, where maximum concentrations were found for EHMC (241.7ng/gd.w.). Sediments from this river basin were also analysed. Lower values were observed in relation to fish for OC and EHMC, ranging from below the limits of detection to 23ng/gd.w. Accumulation levels of UV-F in the fish were used to calculate biota-sediment accumulation factors (BSAFs). These values were always below 1, in the range of 0.04-0.3, indicating that the target UV-Fs are excreted by fish only to some extent. The fact that the highest concentrations were determined in predators suggests that biomagnification of UV-F may take place along the freshwater food web. Copyright © 2015. Published by Elsevier B.V.
Article
UV filters as emerging contaminants are of great concern and their wide detection in aquatic environments indicates their chemical stability and persistence. This review summarized the photolytic and photocatalytic degradation of UV filters in contaminated water. The findings indicated that limited research has been conducted on the photolysis and photocatalysis of UV filters. Photolysis of UV filters through UV irradiation in natural water was a slow process, which was accelerated by the presence of photosensitisers e.g. triplet state of chromaphoric dissolved organic matter (³CDOM*) and nutrients but reduced by salinity, dissolved organic matter (DOM) and divalent cations. UV Photocatalysis of 4-methylbenzylidene camphor and 2-phenylbenzimidazole-5-sulfonic acid was very effective with 100% removal within 30 min and 90 min using medicated TiO2/H2O2 and TiO2, respectively. The radiation source, type of catalyst and oxygen content were key factors. Future research should focus on improved understanding of photodegradation pathways and by-products of UV filters.
Article
Recent studies demonstrated that the common pyrethroid insecticides are present in aquatic biota tissues. In this study, 123 samples of unhatched eggs of 16 wild bird species collected from 2010 to 2012 in Doñana National and Natural Park were analysed to determine 13 pyrethroids. This study represents the first time that pyrethroids are detected in tissues of terrestrial biota, 93% of these samples being positive to those pollutants. Levels of total pyrethroids ranged from not detected to 324 ng g⁻¹ lw. The samples were characterized by stable isotope analysis. Species with diets based on anthropogenic food showed higher levels of pyrethroids and lower values of δ¹⁵N. Finally, we characterized the isomers of pyrethroids and discerned some isomeric- and enantiomeric-specific accumulations. In particular, tetramethrin and cyhalothrin showed an enantiomeric-selective accumulation of one enantiomer, highlighting the need to assess toxicological effects of each enantiomer separately to be able to make a correct risk assessment of pyrethroids in birds.
Article
Eggs of Purple Heron (Ardea purpurea) were collected from three sampled sites inside the Ebro River basin in years 2006 and 2007. These sites were located besides (Flix), upstream (Aiguabarreig) and downstream (Delta) a chlor-alkali plant. Organochlorine compounds (OCs) such as dichlorodiphenyltrichloroethanes (DDTs), polychlorobiphenyls (PCBs), polychlorostyrenes (PCSs), hexachlorobenzene (HCB), pentachlorobenzene (PeCB) and hexachlorocyclohexanes (HCHs) were analysed to assess what are the accumulation patterns of these compounds in aquatic migratory birds breeding in the area of influence of the emissions from this industrial installation. Comparison of the egg concentrations between the three sites show higher concentrations of compounds manufactured in the past in the factory (PCBs, p,p'-DDT) or by-products of OC synthesis (HCB, PeCB and PCSs) in Flix than in Aiguabarreig reflecting a clear influence from the emissions of the chlor-alkali plant. The eggs collected in the Ebro Delta showed higher concentrations of total DDTs (mainly p,p'-DDE) than in the reference site (Aiguabarreig) which could reflect past applications of this insecticide in the area for agriculture. In contrast, HCHs were found in higher concentrations in the Delta and Aiguabarreig than in the Flix Reservoir. These compounds have been used as insecticides in agriculture and were not manufactured in the chlor-alkali plant. The present results show that despite Purple Herons are migratory birds, the food web transfer of OCs during the breeding season is sufficient for the accumulation of these compounds in the eggs, leading to statistically significant concentration differences between sites. These differences are consistent with the emissions of these pollutants from industrial or agricultural sources to the aquatic environments. Some of the p,p'-DDE concentrations observed in the area nearby the chlor-alkali plant are above the threshold effects for reproductive impairment.
Chapter
In the framework of the study of emerging pollutants in the aquatic environment, personal care products (PCPs) play a relevant role as they are used in everyday life. They are continuously introduced into the natural water compartment, mainly through treated and untreated sewage but also via different pathways. This chapter describes the “state of the art” of the distribution and impact of PCPs on European natural waters (rivers, lakes, groundwater, drinking water, etc.). An extensive review of the recent literature has been carried out, gathering together the most relevant studies and presenting the results in five sections: fragrances, UV filters, detergents, preservatives, and repellents. In each section, data on the main molecules employed in PCP formulations are reported and compared. The physicochemical properties of many PCP compounds are summarized in the respective tables along with an additional table listing the measured concentrations of all PCPs detected in waters all over Europe.