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Short Communication
Impact of inorganic UV lters contained in sunscreen products on tropical
stony corals (Acropora spp.)
Cinzia Corinaldesi
a,
,1
, Francesca Marcellini
b,1
, Ettore Nepote
c
, Elisabetta Damiani
c
, Roberto Danovaro
c,d
a
Dipartimento di Scienze e Ingegneria della Materia, dell'Ambiente ed Urbanistica, Università Politecnica delle Marche, Via Brecce Bianche, Ancona, Italy
b
Ecoreach Ltd, Corso Stamira 61, 60121 Ancona, Italy
c
Dipartimento di Scienze della Vita e dell'Ambiente, Università Politecnica delle Marche, Via Brecce Bianche, Ancona, Italy
d
Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy
HIGHLIGHTS
Organic UV-lters and preservatives in
sunscreens can harm coral reefs world-
wide.
Among the inorganic UV lters tested in
the Maldives, ZnO caused bleaching of
Acropora spp.
Bleaching induced by ZnO was deter-
mined by its impact on symbiotic algae
and was associated with microbial en-
richment.
Eusolex® T2000 and Optisoldid not
cause evident bleaching, resulting in low
environmental impact to Acropora ssp.
The use of eco-compatible lters in sun-
screens is highly recommended to pro-
tect coral reef health in the future.
GRAPHICAL ABSTRACT
abstractarticle info
Article history:
Received 19 January 2018
Received in revised form 8 May 2018
Accepted 8 May 2018
Available online xxxx
Editor: Daniel Wunderlin
Most coral reefs worldwide are threatened by natural and anthropogenic impacts. Among them, the release in
seawater of sunscreen products commonly used by tourists to protect their skin against the harmful effects of
UV radiations, can affect tropical corals causing extensive and rapid bleaching. The use of inorganic (mineral) l-
ters, such as zinc and titanium dioxide (ZnO and TiO
2
) is increasing due to their broad UV protection spectrum
and their limited penetration into the skin. In the present study, we evaluated through laboratory experiments,
the impact on the corals Acroporaspp. of uncoated ZnO nanoparticles and twomodied forms of TiO
2
(Eusolex®-
T2000 and Optisol), largely utilized in commercial sunscreens together with organiclters. Our results demon-
strate that uncoated ZnO induces a severe and fastcoral bleaching due to the alteration of the symbiosis between
coral and zooxanthellae. ZnO also directly affects symbiotic dinoagellates and stimulates microbial enrichment
in the seawater surrounding the corals. Conversely, Eusolex® T2000 and Optisolcaused minimal alterations in
the symbiotic interactions and did not cause bleaching,resulting more eco-compatible than ZnO. Due to the vul-
nerability of coral reefs to anthropogenic impacts and global change, our ndings underline the need to accu-
rately evaluate the effect of commercial lters on stony corals to minimize or avoid this additional source of
impact to the life and resilience ability of coral reefs.
© 2018 Elsevier B.V. All rights reserved.
Keywords:
Sunscreens
Coral bleaching
Inorganic lters
Titanium dioxide
Zinc oxide
Science of the Total Environment 637638 (2018) 12791285
Corresponding author.
E-mail address: c.corinaldesi@univpm.it (C. Corinaldesi).
1
Equally contributed to this work
https://doi.org/10.1016/j.scitotenv.2018.05.108
0048-9697/© 2018 Elsevier B.V. All rights reserved.
Contents lists available at ScienceDirect
Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
1. Introduction
Coral reefs are among the most diverse and productive ecosystems
on Earth supporting a huge biodiversity (around 830,000 multi-
cellular species, Fisher et al., 2015), and providing ecosystem goods
and services to half a billion people including food provision, nancial
incomes and protection against natural hazards (Ferrario et al., 2014;
Hughes et al., 2012;Teh et al., 2013). Approximately, 70% of coral
reefs are currently threatened by several natural and anthropogenic im-
pacts including overshing, urban-coastal development, pollution and
tourism (Krieger and Chadwick, 2013;Spalding and Brown, 2015,Tsui
et al., 2017). It has been estimated that every year, millions of tourists
travel to tropical destinations (UNWTO, 2015) enhancing the risk of im-
portant consequences on marine life and ecosystems (Danovaro et al.,
2008;Giglio et al., 2015). In the last decades, production and consump-
tion of sunscreens containing active organic (e.g. cinnamates, camphor
derivatives, benzophenones) and/or inorganic (e.g. TiO
2
and ZnO) in-
gredients to protect human skin from UV radiation, have increased in
the cosmetic market on a global scale (Osterwalder et al., 2014;
Sánchez-Quiles and Tovar-Sánchez, 2014).
Despite organic lters dominates the market of sunscreen products,
the combined use of inorganic compounds, such as zinc oxide (ZnO) and
titanium dioxide (TiO
2
), is constantly increasing due to the broad UV
spectrum of protection, and their limited penetration into the skin (Lu
et al., 2015;). However, the potential of these compounds to generate
reactive oxygen species (ROS) and release metal ions into the aquatic
environment has been recently demonstrated, with consequent possi-
ble negative effects on aquatic organisms (Blaise et al., 2008;Haynes
et al., 2017;Hu et al., 2018;Minetto et al., 2017;Wong et al., 2010). At
the same time, investigations on the impact of ZnO and TiO
2
on marine
life, being mostly focused on microalgae, are still too limited to draw
general conclusions (Hazeem et al., 2016;Miller et al., 2010).
Previous studies have also shown that sunscreen products and
their organic ingredients (e.g., organic UV lterssuchasethylhexyl
methoxycinnamate, benzophenone-3, benzophenone-2and preser-
vatives such as butylparaben) can harm tropical reefs worldwide
contributing to coral bleaching (Danovaro et al., 2008;Downs et al.,
2014).
It has also been hypothesised that inorganic lters, such as TiO
2
and
ZnO, depending on their specic physical characteristics (i.e. size, crys-
tal form, morphology of particles), can produce different effects on ma-
rine algae (Peng et al., 2011;Sendra et al., 2017).
It is well known that under UV radiation both ZnOand TiO
2
promote
the formation of reactive oxygen species (ROS) by photocatalytic reac-
tions that lead to important consequences on the health of marine or-
ganisms (Haynes et al., 2017;Ivask et al., 2010;Sánchez-Quiles and
Tovar-Sánchez, 2014). Furthermore, recent studies have conrmed
that ZnO can be toxic to many aquatic organisms (Khosravi-Katuli
et al., 2018;Li et al., 2018;Shin et al., 2018), and dissolved Zn ions
have been implicated as a major mechanism driving the toxicity of
ZnO nanoparticles in aqueous media (Noventa et al., 2017;Wong
et al., 2010).
In the present study, we tested the hypothesis that these lters can
also harm stony corals, possibly through the impact on their symbiotic
microalgae. For this purpose, we evaluated the impact of inorganic UV
lters, largely utilized in commercial sunscreens, on the stony corals of
the genus Acropora of the Maldivian Lhaviyani Atoll (Vavvaru Island).
We conducted eld experiments based on the addition of ZnOnanopar-
ticles and of two forms of TiO
2
(Eusolex®T2000 and Optisol). The
genus Acropora was selected as it is the dominant stony coral in tropical
coral reefs worldwide, and their symbiotic algae (i.e. Symbiodinium sp.)
can be easily recognised, investigated and cultured. The ndings ob-
tained here can expand our knowledge on the impact of inorganic UV
lters on coral reefs in order to understand the best tools and practices
for minimising the impacts of tourism and recreational activities and
preserving these corals and their ecosystems.
2. Materials and methods
2.1. Inorganic UV lters
In the present study, we tested the impact of zinc oxide nanoparti-
cles (SIGMA) characterised by uncoated particles of size ranging from
20 to 200 nm (nanoparticles N50% of the total particles), as observed
by Scanning Electronic Microscopy and two forms of titanium dioxide:
Optisol(Oxonica Ltd. and UK Nanotechnology Company) and
Eusolex®T2000 (Merck KGaA). Eusolex®T2000 is represented by the
crystal form rutilewith particles size of 20 nm and by the surface
coated with alumina and dimethicone. Optisolis another modied
form of titanium dioxide in which a small amount of manganese is in-
corporated into the structural lattice conferring free radical scavenging
power, thus minimising the formation of free radicals (Wakeeld
et al., 2004). These modications (surface coatings and metal doping)
have the scope to reduce the potential reactivity of photo-activated
TiO
2
particles by quenching and/or reducing the reactive species gener-
ated before they can interact with the other ingredients in a formula and
with skin components itself (Tiano et al., 2010).
2.2. Sampling area and experimental design
Coral nubbins (36 cm) belonging to the genus Acropora spp. were
collected from different donor colonies at ca. 5 m water depth in the
front reef area of Vavvaru Island (Lhaviyani Atoll, Maldives). Nubbins
were immediately placed in experimental mesocosms located at ca.
50 m from the sampling site and supplied with a continuous seawater
ow (i.e. with intake in the sampling area), which allowed us to keep
the same conditions present in situ. Corals were acclimatised in aquar-
ium for 48 h at in situ conditions of temperature and salinity (28 °C
and 35, respectively). After acclimatisation, thehealthycorals (i.e. with-
out any sign of bleaching or necrotic tissue, and showing open polyps)
were washed in virus-free seawater (ltered onto 0.02 μmmembranes
Anotop syringe-lters; Whatman, Springeld Mill, UK), and immersed
in polyethylene Whirl-pack bags (Nasco, Fort Atkinson, WI, USA) lled
with 2 L of virus-free seawater taken to the sampling area. Replicate
sets of coral nubbins (n= 3, containing N300 polyps each) were
exposed to aliquots of different UV lters (nal concentration
6.3 mg L
1
of each inorganic UV lter) and compared with untreated
coral nubbins (used as controls). Corals were incubated in aquaria
maintained at in situ conditions (temperature and salinity), with sea-
water in a continuous ow directly from the ocean. This nal concentra-
tion (equivalent to half the maximum concentration of inorganic lters,
permitted in the EU and US, for sunscreen products; i.e. 12%) falls within
the range of values of the same inorganic compounds used in previous
researches (Khosravi-Katuli et al., 2018;Libralato et al., 2013;Mezni
et al., 2018;Sendra et al., 2017;Wang et al., 2016;Yung et al., 2015),
thus allowing us to make proper comparisons.
2.3. Release of zooxanthellae and their health status
Zooxanthellae were analysed from seawater samples collected from
the seawater of the experimental mesocosms in order to quantify
the number ofthe symbiotic organisms released from the coralcolonies.
Ten mL of seawater were collected from treated (added with lters) and
untreated systems immediately after the addition of UV lters (t
0
=
start of the experiment) and after 24 h (t
24
) and 48 h (t
48
) from the be-
ginning of the experiment. Aliquots of seawater samples were ltered
through 2.0-μm polycarbonate lters and mounted on glass slides.
Zooxanthellae were counted under a Zeiss Axioplan epiuorescence mi-
croscope (Carl ZeissInc., Jena, Germany; ×400 and×1000). Based on the
autouorescence and gross cell structure, we discriminated the
zooxanthellae released from coral colonies as pale (P, pale yellow
colour, vacuolated, partially degraded zooxanthellae) and transparent
(T, lacking pigmentations, empty zooxanthellae) from healthy
1280 C. Corinaldesi et al. / Science of the Total Environment 637638 (2018) 12791285
zooxanthellae (H, brown/bright yellow colour, intact zooxanthellae;
Danovaro et al., 2008;Mise and Hidaka, 2003). The abundance of the
damaged zooxanthellae released was obtained from the sum of the
total number of zooxanthellae classied as pale and transparent, that
were detected in the seawater surrounding coral nubbins exposed to
the different inorganic UV lters.
2.4. Bleaching quantication
According to Siebeck et al. (2006), we performed a colorimetric
analysis of digital photographs of corals taken at the beginning of the
experiments and after 48 h of treatment with UV-lters (specied
above). Photographs were taken under identical illumination with a
Canon EOS 400D digital camera (Canon Inc., Tokyo, Japan) with a scale
meter on the background. The photographs were subsequently
analysed with a photo-editing software for colour composition cyan,
magenta, yellow and black (CMYK). Levels of bleaching were measured
as the difference between the coral's colour at the beginning of the ex-
periments (t
0
) and after 48 h of exposure (t
48
). Thirty random measure-
ments of variables CMYK were carried out across the coral area.
Variations in the percentage of the different colour components
(CMYK) were analysed with one-way analysis of variance (ANOVA).
To rank the bleaching effect due to the different sunscreens tested, we
obtained BrayCurtis similarity matrix and multidimensional scaling
analysis of the shifts in CMYK colour composition of treated corals
using Primer 5.0 software (Primer-E Ltd., Plymouth, UK). Bleaching
rates were measured as the variation percentage in CMYK colour com-
position between treated and control corals using Primer 5.0 software
(Primer-E Ltd). In addition, to the mean values obtained we attributed
scores of thebleaching degree by means of a mathematical function, ac-
cording to a scaleorganized in ranks (0 to N60), i.e. from no visible coral
bleaching(010) to total bleachingof 100% of coral nubbinssurface
(N60).
2.5. Prokaryotic and viral abundance
Prokaryotic and viral abundance in seawater samples was deter-
mined according to the protocol described by Noble and Fuhrman
(1998). Sub-samples (10 mL) from treated (added with lters) and un-
treated systems were collected immediately after the addition of sun-
screen (t
0
= start of the experiment) and after 24 h (t
24
) and 48 h
(t
48
) from the beginning of the experiment. After collection, three repli-
cate seawater samples were stored at 20 °C until the analysis. Sub-
samples were ltered onto 0.02 μm poresize lter (Whatmann Anodisc;
diameter, 25 mm; Al
2
O
3
) and stained with 100 μLofSYBRGold(stock
solution diluted 1:5000). The lters were incubated in the dark for
20 min, washed three times with 3 mL of preltered Milli-Q water
and mounted onto glass slides with 20 μL of 50% phosphate buffer
(6.7 mM phosphate, pH 7.8) and 50% glycerol (containing 0.5% ascorbic
acid). Slides were stored at 20 °C. Prokaryotes and viruses' counts
were obtained by epiuorescence microscopy (Zeiss Axioskop 2). For
each slide, at least 20 microscope elds were observed and at least
200 prokaryotes and viruses were counted per lter.
2.6. Statistical analysis
Differences in the investigated variables betweencontrols and treat-
ments were assessed using permutational analyses of variance
(PERMANOVA; Anderson, 2005;McArdle and Anderson, 2001)on
square root transformed data. The design included two xed factors
(time and treatment). When signicant differences were encountered
(pb0.05) post-hoc pairwise tests were also carried out. Statistical anal-
yses were performed using PRIMER 6 (Clarke and Gorley, 2006).
3. Results and discussion
The inorganic UV lters tested here, ZnO and TiO
2
(especially in the
rutile form) nanoparticles are commonly used in sunscreen products for
their UVA (320400 nm) and UVB (290320 nm) coverage and to in-
crease the transparency of cosmetics applied on the skin (Smijs and
Pavel, 2011).
The analyses conducted in this study reveal that ZnO caused the
strongest negative effects in terms of number of zooxanthellae released
from the stony corals investigated (pb0.001, Fig. 1A). In particular, the
release of zooxanthellae after ZnO addition was signicantly higher
than in the control and in the corals treated with both TiO
2
forms
(EusolexT2000 and Optisol) with thestrongest effect after 48 h of expo-
sure (i.e., zooxanthellae release up to two orders of magnitude higher
than in the control and other treatments; Fig. 1A; Table S1). In addition,
ZnO determined the release of the highest fraction of damaged zooxan-
thellae (up to one order of magnitude higher than the other treatments
tested), suggesting that these nanoparticles can strongly affect hard
corals impairing their symbiotic microalgae.
Previous eco-toxicological studies documented the negative effects
of ZnO nanoparticles on marine organisms including algae, crustaceans
and sh (Peng et al., 2011;Wong et al., 2010). Here, we expand the ev-
idence on the negative effect of ZnO nanoparticles, revealing their im-
pact also on tropical corals and their symbiosis with microalgae.
The addition of both Eusolex T2000 and Optisol also caused an in-
crease in the release of zooxanthellae in the seawater surrounding
coral nubbins when compared to the control (Fig. 1A; Table S1). How-
ever, whereas Eusolex T2000 showed effects in the short term (t
0
and
t
24,
pb0.01), Optisol acted only after 2448 h of exposure (pb0.01).
Fig. 1. Impact of the inorganic lters on symbiotic microalgae of Acropora spp. To tal
abundance of zooxanthellae (A) and damaged zooxanthellae (B) relea sed into the
seawater surrounding coral nubbins exposed to 6.3 mgL
1
of zinc oxide and titanium
dioxide (Eusolex T2000 and Optisol) during th e time-course experiment. Results are
reported as mean values ± S.D.
1281C. Corinaldesi et al. / Science of the Total Environment 637638 (2018) 12791285
PERMANOVA analyses conrmed the signicant differences in the re-
sponses of Acropora exposed to the two types of TiO
2
as a result of the
treatment × time interaction (pb0.01).
In the zooxanthellae released from corals, we observed a loss of
photosynthetic pigments already 24 h after exposure to ZnO (Fig. 1B).
The abundance of damaged zooxanthellae, indeed, increased over
time reaching values up to two orders of magnitude higher than in the
controls and in the other treatments (pb0.001). The amount of
damaged zooxanthellae released by corals treated with Eusolex T2000
increased signicantly already after 24 h of exposure compared to the
control (pb0.05) whereas the effect of Optisol was more evident after
48 h of exposure (pb0.001).
Previous studies revealed that inorganic TiO
2
nanoparticles are the
major-oxidizing agents in coastal waters, producing very high rates of
H
2
O
2
in seawater and directly affecting the growth of phytoplankton
(Tovar-Sánchez et al., 2013). Our ndings indicate that Optisol (TiO
2
modied with manganese) has a non-immediate impact on corals and
symbiontmicroalgae, potentially due to its surface or structural modi-
cations (manganese doping), which minimises the reactivity of photo-
activated particles rendering them initially inert in water (Botta et al.,
2011). On the contrary, Eusolex T2000 (TiO
2
lter coated with alumina
and dimethicone) has an immediate effect on corals and symbiont
microalgae. The different response time of corals to the two inorganic
lters (immediate for Eusolex and delayed for Optisol) might be associ-
ated with the diverse characteristics of the TiO
2
lters, which once re-
leased in seawater could have a different behaviour and/or action
mechanism (Tsui et al., 2017). Since Optisol determined a delayed ef-
fecton the symbiotic interaction between corals and zooxanthellae,
we cannot exclude a long-term effect on the corals due to chronic expo-
sure (Tsui et al., 2017).
The loss of zooxanthellae induced by ZnO resulted in a fast coral
bleaching, which was evident after 24 h of exposure (Fig. 2), and at
the end of the experiment bleaching dominated for 67% of the corals'
surface (Fig. 3; Table S2). Conversely, after addition of the two different
types of TiO
2
no visible bleaching was observed in the corals (Fig. 2),
which, indeed, showed only a slight colour loss in 67% of their surface
similarly to the control (3%, Fig. 3;TableS2).
Fig. 3. Bleaching degree in Acropora spp. exposed to the different inorganic UV lters.
Percentage of bleaching in the corals exposed to 6.3 mgL
1 of zinc oxide and titanium
dioxide (Eusolex T2000 and Optisol) and scale of bleaching severity.
Fig. 2. Bleaching of Acropora spp. nubbins caused by the inorganic lters. Photographs of
the corals in the control (unexposed corals to inorganic lters; A and B) and exposed to
zinc oxide (C and D), Eu solex T2000 (E and F) and Optisol (G and H) at the sta rt (t
0
)
and at the end (after 48 h) of the experiment.
1282 C. Corinaldesi et al. / Science of the Total Environment 637638 (2018) 12791285
The lower impact of TiO
2
on the corals when compared to ZnO
was evident also in terms of microbial enrichment in the seawater
surrounding the nubbins of Acropora. Previous studies demonstrated
that tropical corals subjected to environmental stress regulate the
abundance of their associated microbes, essential to coral immunity
and health (Krediet et al., 2013), by increasing the amount of bacteria
and viruses released directly in seawater and/or through mucus
(Garren and Azam, 2012;Nguyen-Kim et al., 2015). In addition, previ-
ous investigations reported that sunscreen products and theirUV lters
increase virus proliferation in seawater like in the same way as other
environmental stressors (Danovaro and Corinaldesi, 2003;Danovaro
et al., 2008;Davy et al., 2006). Here, we observed that in systems treated
with ZnO a strong enrichment of both prokaryotes and viruses (42.05 ±
3.88 × 10
8
cells L
1
and 44.83 ± 0.87 × 10
8
viruses L
1
;pb0.001,
Fig. 4A and B; Table S3) was observed after 48 h of incubation
compared to the control (14.40 ± 0.32 × 10
8
cells L
1
and 16.62 ±
1.07 × 10
8
viruses L
1
). Conversely, the two types of TiO
2
did not
determine any signicant increase in microbial abundance over time
(on overage, 5.44 ± 0.18 × 10
8
cell L
1
and 6.50± 0.23 × 10
8
viruses L
1
in the treatment with Eusolex T2000 and 6.87 ± 0.11 × 10
8
cell L
1
and
9.53 ± 0.22 ×10
8
viruses L
1
in the treatment with Optisol, Fig. 4Aand
B; Table S3). Indeed, TiO
2
particles have been reported to have antimi-
crobial activity due to the generation of free radicals by photoexcitation
or adsorption of the bacterial cells onto TiO
2
particles (Dhanasekar et al.,
2018;Gogniat et al., 2006). However, the specic effect of TiO
2
on pro-
karyotic cells has not yet been dened. Previous studies suggested that
the phototoxicity of nanoTiO
2
on bacteria is not determined by a single
factor but by multiple factors that also include the inorganic material
morphology (Tong et al., 2013).
Concluding, our ndings indicate that uncoated ZnO nanoparticles
induce a complete, and potentially irreversible coral bleaching causing
asignicant rapid and widespread mortality of the symbiotic zooxan-
thellae of the stony corals, and stimulating microbial enrichment in
the seawater surrounding the corals. Supposedly, this result may be
due to the alteration of the cellular membrane lipid composition of
hard corals and their symbiotic organisms (Tang et al., 2017). In addi-
tion, previous investigations reported that dissolved Zn
2+
can cause tox-
icity in algae (Franklin et al., 2007;Lee and An, 2013;Shin et al., 2018)
determining manganese deciency (Miller et al., 2010), mitochondrial
and DNA damage (Sharma et al., 2012), oxidative stress (Xia et al.,
2008;Li et al., 2012) and cell membrane damage (Song et al., 2010).
Other studies highlighted that the cell membrane damage can result
in membrane deformation and morphological changes of cells and
even organelles (Peng et al., 2011;Tang et al., 2017;Trevisan et al.,
2014;Xiong et al., 2011).
Market trends of sunscreen products indicate that ZnO lter utiliza-
tion will overtake nano titanium dioxide (nTiO
2
) in the near future, es-
pecially after the approval of ZnO for cosmetic purposes in the EU since
April 2016 (http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=
CELEX%3A32016R0621). Indeed, ZnO offers high skin protection due
to its greater broad-spectrum UV coverage and reduced opaqueness
thanks to improved formulation technologies (Lademann et al., 2006;
Smijs and Pavel, 2011). The use of ZnO in cosmetic and sunscreen prod-
ucts has been hypothesised to be a safer alternative to conventional
organic-based lters due to several issues related to photoinstability,
skin irritability and endocrine disrupting ability (Biebl et al., 2006;
Hojerová et al., 2011;Krause et al., 2012). However, the results reported
here demonstrate that theuse of ZnO is extremely harmful to the organ-
isms tested, thus suggesting that its use in sunscreen and personal care
products should be further assessed in future investigations because it
might have important consequences on marine environment. Since
the negative impact of ZnO will also be present when it is used in com-
bination with TiO
2
, the concern about these compounds should be also
extended to sunscreen products using a combination of both inorganic
lters. Although the use of coated/modied TiO
2
in sunscreens is not
completely exempt of potential negative effects (Tanvir et al., 2015),
the results of the present study indicate that when used alone (i.e., as
a single ingredient)it can have a limited impact on tropical stony corals.
Accordingly, a similar study conducted on the Montastraea faveolata in
the Caribbean Sea shows that TiO
2
caused signicant zooxanthellae ex-
pulsion in all the colonies, without mortality, suggesting a possible coral
acclimation and recovery from stress (Jovanovićand Guzmán, 2014).
However, further investigation is needed to clarify if its use is fully
eco-compatible with marine life while protecting human skin from UV
damage or if it may be harmful if used under specic conditions or in
combination with other products.
Acknowledgments
This study was conducted within the frame of the projects MERCES
(Marine Ecosystem Restoration in Changing European Seas), funded by
the European Union's Horizon 2020 research and innovation program
(grant agreement no. 689518), and national funds ATENEO 2013
obtained by R. Danovaro and ATENEO 2013-2016 obtained by C.
Corinaldesi provided by MIUR (Italian Ministry of University and
Research).
Conict of interest
The authors declare no competing nancial interests.
Fig. 4. Microbial enrichment in the seawatersurrounding coralsinduced by inorganic lters. Prokaryotic (A)and viral (B) abundancesin seawater surrounding coralsexposed to 6.3 mgL
1
of zinc oxide and titanium dioxide (Eusolex T2000 and Optisol) overtime. Results are reported as mean values ± S.D.
1283C. Corinaldesi et al. / Science of the Total Environment 637638 (2018) 12791285
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2018.05.108.
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... This PNEC is based on an SSD by applying an assessment factor of 1 and, from a general risk assessment point of view, should also capture apparent effects in organisms (including reef building corals), which have not been tested so far. This assumption is supported by available literature data where bleaching effects in stony corals (Acropora sp.) exposed for 48 h to 6.3 mg/L nano ZnO occur (Corinaldesi et al., 2018). Value recalculated based on 33 µl/L and a specific density of 1.108 g/cm 3 . ...
... Furthermore, in the same dossier, the range of NOECs referring to marine algae toxicity tests range from 0.0078 to 0.67 µg/L, based on the dissolved ZnO concentration and, again, does not indicate any higher specific toxicity of the substance to either corals or its associated symbionts. In contrast, Corinaldesi et al. (2018) also observed no significant effect using 6.3 mg/L of the nanoform of TiO 2 in an identical test setup for 48 h, thus agreeing with the corresponding REACH dossier, revealing an EC10 and an EC50 for green algae of >2 and >50 mg/L, respectively (ECHA, 2020e). Based on these examples, it remains unclear whether the coral holobiont (i.e., corals and associated symbionts) is a taxon that is more sensitive than other standard organisms used in OECD guideline conform testing. ...
UV filters used in sunscreens are amongst the anthropogenic substances that may enter the marine environment by both indirect (via wastewater) and direct pathways (leisure activities). Due to the recent global decline in coral population, the impact of those UV filters on the coral health is currently under increased investigation. First results from scientists suggest that some of the filters may be toxic to various coral life stages, but an initial cross comparison with existing data from other freshwater organisms does not indicate that corals are specifically more susceptible to UV filters than other standard species. In fact, the available data for this conclusion is still vague and based on toxicity and bioaccumulation tests with corals, which are both at the research state. To allow for a proper hazard assessment, robust experimental procedures for coral ecotoxicological studies are considered mandatory. In other words, additional efforts should be taken to standardize and validate such new test systems to generate reliable results, which then may be used in regulatory decision making. Furthermore, to allow for a more detailed and site‐specific environmental risk assessment in the marine area, the development of an application‐based exposure scenario is urgently needed. Until these data and tools become available, environmental hazard and risk assessments may be carried out using existing data from freshwater organisms and existing tonnage‐based exposure scenarios as a potential surrogate.
... Recently, two US states (Hawaii and Florida), as well as Mexico and Palau have banned certain organic UV filters (such as oxybenzone and octinoxate) due to the negative impacts on the coral development and bleaching (Downs et al., 2016;He et al., 2019;Schneider and Lim, 2019). However, the environmental risks of UV filters remain controversial due to insufficient research in this field (Corinaldesi et al., 2018;Fel et al., 2019;He et al., 2019), particularly with regard to the potential sublethal effects of environmentally relevant concentrations of organic UV filters (Lozano et al., 2020). Furthermore, many recent studies on sunscreen toxicity focused on the tropical (coral reef) ecosystems (Corinaldesi et al., 2018;Downs et al., 2016;Fel et al., 2019;He et al., 2019), while the impacts of the UV filters on temperate marine organisms remain poorly understood. ...
... However, the environmental risks of UV filters remain controversial due to insufficient research in this field (Corinaldesi et al., 2018;Fel et al., 2019;He et al., 2019), particularly with regard to the potential sublethal effects of environmentally relevant concentrations of organic UV filters (Lozano et al., 2020). Furthermore, many recent studies on sunscreen toxicity focused on the tropical (coral reef) ecosystems (Corinaldesi et al., 2018;Downs et al., 2016;Fel et al., 2019;He et al., 2019), while the impacts of the UV filters on temperate marine organisms remain poorly understood. ...
Article
The global occurrence of organic UV filters in the marine environment is of increasing ecotoxicological concern. Here we assessed the toxicity of UV filters ensulizole and octocrylene in the blue mussels Mytilus edulis exposed to 10 or 100 μg l⁻¹ of octocrylene and ensulizole for two weeks. An integrated battery of biochemical and molecular biomarkers indicating xenobiotics metabolism and cellular toxicity (including oxidative stress, DNA damage, apoptosis, autophagy and inflammation) was used to assess the toxicity of these UV filters in the mussels. Our data show that octocrylene (but not ensulizole) accumulate in the mussel tissues during the waterborne exposures. Both studied UV filters induced sublethal toxic effects in M. edulis at the investigated concentrations. These effects involved induction of oxidative stress, genotoxic effects (indicated by upregulation of DNA damage sensing and repair markers), upregulation of apoptosis and inflammation, and dysregulation of the xenobiotic biotransformation system. Octocrylene induced cellular stress in a concentration-dependent manner, whereas ensulizole appeared to be more toxic at lower (10 μg l⁻¹) concentration than at 100 μg l⁻¹. The different concentration-dependence of sublethal effects and distinct toxicological profiles of ensulizole and octocrylene show that the environmental toxicity is not directly related to lipophilicity and bioaccumulation potential of these UV filters and demonstrate the importance of using bioassays for toxicity assessment of emerging pollutants in coastal marine ecosystems.
... The instream engineered TiO 2 concentrations observed in the current study are higher than the predicted no effect concentration for TiO 2 ENMs to freshwater organisms (e.g., 1-18 μg L −1 ). Further, fluvial transport of TiO 2 engineered particles from the Edisto River as well as other rivers to the ocean could lead to bioaccumulation in estuarine and coastal microflora and induce coral bleaching and coral population declines (Corinaldesi et al., 2018;Jovanović and Guzmán, 2014). Further research is needed on the occurrence and temporal variability of TiO 2 engineered particle concentrations in streambed sediments to better understand the fate, transport, and potential aquatic effects of TiO 2 engineered particles on rural stream ecosystems and estuarine and coastal receptors. ...
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Titanium dioxide (TiO2) is widely used in engineered particles including engineered nanomaterial (ENM) and pigments, yet its occurrence, concentrations, temporal variability, and fate in natural environmental systems are poorly understood. For three years, we monitored TiO2 concentrations in a rural river basin (Edisto River, < 1% urban land cover) in South Carolina, United States. The total concentrations of Ti, Nb, Al, Fe, Ce, and La in the Edisto River trended higher during spring/summer compared to autumn/winter. Upward trending Ti/Nb ratio in the spring/summer compared to near-background autumn/winter ratios of 255.7 ± 8.9 indicated agricultural preparation and growing-season-related increases in TiO2 engineered particles. In contrast, downward trending of the Ti/Al and Ti/Fe ratios in the spring and summer compared to the near-background autumn/winter ratios of 0.05 indicated greater mobilization of Fe and Al, relative to Ti during spring/summer. Surface-water concentrations of TiO2 engineered particles varied between 0 and 128.7 ± 3.9 μg TiO2 L⁻¹. Increases in TiO2 concentrations over the spring/summer were associated with increases in phosphorus, orthophosphate, nitrate, ammonia, anthropogenic gadolinium, water temperature, suspended sediments, organic carbon, and alkalinity, and with decreases in dissolved oxygen. The association between these contaminants together with the timing of the increases in their concentrations is consistent with diffuse wastewater sources, such as reuse application overspray, biosolids fertilization, leaking sewers, or septic tanks, as the driver of instream concentrations; however, other diffuse sources cannot be ruled out. The findings of this study indicate spatially-distributed (non-point source) releases can result in high concentrations of TiO2 engineered particles, which may pose higher risks to rural stream aquatic ecosystems during the agricultural season. The results illustrate the importance of monitoring seasonal variations in engineered particles concentrations in surface waters for a more representative assessment of ecosystem risk.
... corals, crabs, shrimps, prawns, squids, fish, dolphins, and seabirds) (Gago-Ferreiro et al., 2013;;Castro et al. 2018;Tsui et al., 2017), as well as, demonstrated to cause different biological and toxicological responses (e.g. survival, behavior, growth, development, and reproduction, among many others) (Araújo et al., 2018;Corinaldesi et al. 2018). Although, toxic effects in humans after such a prolonged low dose exposure to UV-filters and musks have hardly been investigated. ...
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... Properties such as the ability to absorb UV radiation or inhibit bacteria that make zinc NPs desirable as product ingredients could become harmful if applied in the environment. For example, it has been suggested that ZnO NPs inhibit Azotobacter, P-solubilizing and K-solubilizing bacteria in soils [45] and causes coral bleaching in oceans [46]. The main processes that control zinc NP mobility, availability, bioaccumulation and toxicity in soil are chemical transformation, aggregation/agglomeration, adsorption and dissolution (Figure 1.5), and these must all be investigated, understood and monitored in order to establish robust risk assessments for both acute and chronic zinc NP exposure resulting from environmental release. ...
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... Effects of sunscreens and their components on corals range from changed behavior (McCoshum et al. 2016), impaired swimming and deformed coral larvae (Downs et al. 2014(Downs et al. , 2016, to genotoxic effects (Downs et al. 2016;He et al. 2019), as well as coral bleaching and mortality (Danovaro et al. 2008;Downs et al. 2009Downs et al. , 2016DiNardo and Downs 2018), which can potentially affect the whole coral reef ecosystem (Downs et al. 2016). Uncoated zinc oxide nanoparticles, components of some inorganic sunscreens, have also been found to cause coral bleaching (Corinaldesi et al. 2018). Most of the studies are laboratory-based using high concentrations of the different components of organic sunscreens; therefore, the ecological relevance of the results has been questioned. ...
Chapter
This chapter describes the importance of coral reef ecosystems, particularly those of the Mexican Caribbean and the causes of coral reef degradation. Ironically, the explosion in tourism, while good for the economy, is devastating the natural resources in the region. The focus of the chapter is on the decrease in water quality as an overarching problem affecting Mexican Caribbean coral reefs, which are situated close to the coastline where tourism-associated growth has expanded unsustainably. Wastewater effluents are not adequately treated and eventually reach the sea through the underground aquifer system. The resulting contamination reduces water quality in coastal waters leading to the degradation of the once oligotrophic coral reef ecosystem over time. In recent years, contamination has been exacerbated by Sargassum blooms that accumulate on the coastline and decompose, leading to a further reduction in water quality. The biological effects of the different components of wastewater discharge, particularly, freshwater, nutrients, pathogens and sunscreens are detrimental to corals and can lead to mortality, diseases and bleaching. The synergistic effects of poor water quality, due to unsustainable growth associated with tourism and Sargassum blooms, with stressors related to climate change, will intensify coral reef ecosystem degradation by decreasing resilience to changes in the environment.
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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
Every second, 0.8 litres of sunscreen enters ocean waters, which corresponds to the release of 25.000 tons per year. UV filters may present substantial threats to marine fauna and flora and have an impact similar to that of other contaminants. Coral reefs play a major role in marine biodiversity, and some publications suggest that they are threatened by the release of sunscreen into the environment, which should cause bleaching. The aim of this study was to evaluate the potential impact of sunscreen products on hard corals. Laboratory experiments in which Seriatopora hystrix coral fragments were exposed to 9 sunscreens at concentrations up to 100 mg/L for 96 hours were conducted, and the biological responses of the fragments were assessed. The examined parameters were coral bleaching and polyp retraction. The results obtained revealed that the 9 tested sunscreens had no effects on S. hystrix, with a recorded NOEC (No Observed Effect Concentration) of 100 mg/L for both tested parameters. This concentration is much higher than those of chemicals in the natural environment, Journal of Environmental Science and Public Health 16 which are on the order of µg/L or ng/L. Under the conditions in this experiment, the absence of toxic effects from the tested sunscreens allows us to argue the absence of potential danger on corals.
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Today, the negative effects of ultraviolet radiation on the skin are well known, so we know we should use protection whenever we are exposed to the sun. Sun protection products, therefore, form part of an overall strategy against photo-induced cancers. However, over several years, controversies have led to consumer mistrust of certain sun protection products containing organic filters, said to be allergens, endocrine disrupters or even responsible for coral bleaching. Taking advantage of the dismay this has caused in some consumers, internet sites have promoted plant oils and essential oils as natural solar filters to replace pharmaceutical sun creams. Using an in vitro method, we studied 15 fixed oils, one oily macerate, one butter, eight essential oils, and an essential wax, chosen among the substances most commonly mentioned on the internet. For each substance, we determined the sun protection factor (SPF) and UVA protection factor (PF-UVA), the universal references for protection level in the ultraviolet range. We demonstrated that these fixed oils and essential oils, for which we found SPF and PF-UVA values of only around 1, are totally devoid of any photoprotective properties. So as to avoid potential users suffering serious consequences, therefore, they should not be considered as sunscreens.
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Every second, 0.8 litres of sunscreen enters ocean waters, which corresponds to the release of 25.000 tons per year. UV filters may present substantial threats to marine fauna and flora and have an impact similar to that of other contaminants. Coral reefs play a major role in marine biodiversity, and some publications suggest that they are threatened by the release of sunscreen into the environment, which should cause bleaching. The aim of this study was to evaluate the potential impact of sunscreen products on hard corals. Laboratory experiments in which Seriatopora hystrix coral fragments were exposed to 9 sunscreens at concentrations up to 100 mg/L for 96 hours were conducted, and the biological responses of the fragments were assessed. The examined parameters were coral bleaching and polyp retraction. The results obtained revealed that the 9 tested sunscreens had no effects on S. hystrix , with a recorded NOEC (No Observed Effect Concentration) of 100 mg/L for both tested parameters. This concentration is much higher than those of chemicals in the natural environment, which are on the order of µg/L or ng/L. Under the conditions in this experiment, the absence of toxic effects from the tested sunscreens allows us to argue the absence of potential danger on corals.
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Organic ultraviolet (UV) filters are widely used in personal care products and occur ubiquitously in the aquatic environment. In this study, concentrations of seven commonly used organic UV filters were determined in seawater, sediment and five coral species collected from the eastern Pearl River Estuary of South China Sea. Five compounds, benzophenone-1, -3 and -8 (BP-1, -3 and -8), octocrylene (OC) and octyl dimethyl-p-aminobenzoic acid (ODPABA), were detected in the coral tissues with the highest detection frequencies (>65%) and concentrations (31.8 ? 8.6 and 24.7 ? 10.6 ng/g ww, respectively) found for BP-3 and BP-8. Significantly higher concentrations of BP-3 were observed in coral tissues in the wet season, indicating that higher inputs of sunscreen agents could be attributed to the increased coastal recreational activities. Accumulation of UV filters was only observed in soft coral tissues with bioaccumulation factors (log10-values) ranging from 2.21 to 3.01. The results of a preliminary risk assessment indicated that over 20% of coral samples from the study sites contained BP-3 concentrations exceeding the threshold values for causing larval deformities and mortality in the worst-case scenario. Higher probabilities of negative impacts of BP-3 on coral communities are predicted to occur in wet season.