IMPACTS OF SUNSCREENS ON CORAL REEFS - FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE ...

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IMPACTS OF SUNSCREENS ON CORAL REEFS - FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE ...
AL
ATIVE

        IMPACTS
        OF SUNSCREENS
        ON CORAL REEFS
        FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN
        AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE

                                                                                                   AUTHOR:
                                                                                            ELIZABETH WOOD
                                                                  Impacts of sunscreens on corals - ICRI briefing - Feb 2018   1
IMPACTS OF SUNSCREENS ON CORAL REEFS - FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE ...
SUMMARY                                     This document responds to Goal 3(5) of the International Coral Reef Initiative (ICRI) Plan of Action 2016-2018, which seeks to review
                                            issues relating to the impact of sunscreens on coral reefs.

Sunscreens contain organic (chemical) and/or inorganic        • Damage and deformation of coral larvae (planulae).        • Investigating UV filter toxicity in relation to predicted
(mineral) UV filters that absorb, reflect or scatter UV                                                                     warming and ocean acidification conditions.
                                                              • Damage to coral DNA and to their reproductive
light. They also contain inactive ingredients such as anti-
                                                                success.                                                  • Researching the extent and significance of bio-
microbial preservatives, moisturisers and anti-oxidants.
                                                                                                                            concentration and bio-accumulation of organic UV
                                                              To date, experiments have largely been undertaken ex-         filters as well as the consequences of long-term,
Sunscreen       ingredients      including    chemical
                                                              situ and there are concerns that they may not properly        chronic exposure to sunscreen pollutants.
(benzophenone-3 and -4 (BP-3 or oxybenzone; BP-4),
                                                              reflect conditions on the reef, where pollutants could be
ethylhexyl methoxy cinnamate (EHMC), homosalate                                                                           • Studying the effects of pharmaceutical and personal
                                                              rapidly dispersed and diluted. In general, concentrations
(HMS),    4-methylbenzylidene      camphor    (4-MBC),                                                                      care products (PPCP) mixtures to provide a more
                                                              of UV filters used in experimental work have been higher
diethylamino hydroxybenzoyl hexyl benzoate (DHHB))                                                                          realistic picture of ecological risks posed by the use
                                                              than likely to be encountered in the reef environment.
and mineral (titanium dioxide and zinc oxide) UV filters                                                                    of these products.
                                                              Most experiments have also been of relatively short
have been detected in coastal waters. UV filters reach
                                                              duration (12 or 24 hours). On the reef, while UV filters    • Identifying those ingredients that are safe and those
coastal waters either directly as a consequence of
                                                              may be at lower concentrations, they can accumulate in        that pose a realistic threat to marine ecosystems.
washing off swimmers and/or indirectly from wastewater
                                                              organisms and sediment and thus become persistent,
treatment plant effluents. Many of these components
                                                              with largely unknown consequences.                          Considering the many stresses already faced by reefs
have also been found in marine biota including fish,
                                                                                                                          and current concerns about the toxicity of certain
molluscs and corals as well as in sediments.
                                                              Research to date has also concentrated mainly on            components of sunscreens to corals, a proactive and
                                                              the effects of sunscreens and individual chemicals at       precautionary approach to dealing with this issue may
Where sunscreen components have been detected,
                                                              subcellular, cellular and individual organism level, with   be required. Reducing the amount of harmful sunscreen
concentrations are very variable. They are generally
                                                              very few studies of wider impacts.                          components that reach the reef environment is a high
found at barely detectable levels of a few parts per
                                                                                                                          priority and will require the involvement of governments,
trillion but much higher concentrations of over 1 part per
                                                              Further research is needed to better understand which       reef managers, divers, snorkelers and swimmers, and the
million (ppm) have been reported in a few locations (e.g.
                                                              ingredients are safe and which pose a realistic threat to   tourism and pharmaceutical industries. The following
1.395 ppm BP-3 reported by Downs et al (2015) in the
                                                              marine ecosystems, in particular:                           measures are recommended:
US Virgin Islands).
                                                              • Determining concentrations of different sunscreen         • Encouraging     the     manufacture           of    reef-friendly
A small number of studies have shown that sunscreen             components in the water column, sediment and biota,         sunscreens.
and certain individual components of sunscreen can              comparing locations that are heavily visited and/or
                                                                                                                          • Promoting the use of reef-friendly sunscreens and
have negative effects on corals and other marine                affected by coastal run-off with those that are more
                                                                                                                            other methods of UV protection
organisms under certain circumstances. The chemical             remote.
UV filter oxybenzone has been studied most intensively                                                                    • Regulating the sale and use of sunscreens containing
                                                              • Investigating the effects of sunscreen pollutants at
and the following effects have been described:                                                                              toxins
                                                                reef community and ecosystem level.
• Bleaching of coral fragments and coral cells from                                                                       • Exerting consumer pressure to encourage
                                                              • Exploring links between organismal or cellular/
  various species of hard coral. This effect is more                                                                        development and use of eco-friendly sunscreens
                                                                subcellular-level biomarkers that more easily allow
  pronounced at higher water temperatures.                                                                                • Introducing financial disincentives for manufacture
                                                                the study of pharmaceutical effects on biodiversity/
• Induction of the lytic viral cycle in symbiotic               community composition and ecosystem functioning.            and use of potentially damaging sunscreens
  zooxanthellae with latent infections.

                                                                                                                                          Impacts of sunscreens on corals - ICRI briefing - Feb 2018   2
IMPACTS OF SUNSCREENS ON CORAL REEFS - FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE ...
1/ INTRODUCTION
There is intense concern about the future health and             In recent years, a number of studies have shown that
ecological integrity of coral reefs in the face of global        sunscreens and other cosmetic products contain
climate change. This is considered to be one of the              chemical substances that are adding to the pollution
greatest threats to reefs worldwide and is causing coral         burden faced by coral reefs. Exposure to ultraviolet (UV)
bleaching and ecosystem change at unprecedented                  solar radiation poses a threat to public health, including
levels. Coral reefs are also under considerable stress from      the risk of sunburn, photo-aging and skin cancer (Pathak,
overfishing, destructive fishing, coastal development            1987), and growing concern about these harmful effects
and pollution. There is universal agreement that coral           has led to an increase in use of sunscreens. The world’s
reefs face an unpredictable future and that action needs         coastal population and coastal tourism are expected to
to be taken at all levels if their integrity and values are to   grow during this century and it is anticipated that the
be maintained.                                                   use of sunscreens and cosmetics containing UV-filters
                                                                 will rise further. Given the status of reefs, it is essential
                                                                 that the impact of sunscreens on corals is assessed and
                                                                 addressed.

2/ COMPOSITION OF SUNSCREENS
Early sunscreens worked by providing a physical barrier          against UV radiation. Sunscreens typically comprise up
between the skin and the sun’s rays but by the 1960s,            to 20 or more chemical compounds (Danovaro et al.,
the cosmetic industry had developed more complex                 2008).
sunscreens containing specific UV filters. These filters
come in two forms, organic (chemical) and inorganic              The most widely used mineral filters are zinc oxide and
(mineral), which act by absorbing, reflecting or scattering      titanium dioxide, often in the form of nanoparticles (NPs)
UV light. Organic and inorganic filters are often used in        to avoid the whitening effect on the skin caused by these
combination to offer full protection against both UV-            compounds. The International Cooperation on Cosmetic
A and UV-B radiation. They are also present in a large           Regulation defines a nanomaterial as an insoluble,
number of other pharmaceutical and personal care                 intentionally manufactured ingredient with one or more
products (PPCPs).                                                dimensions ranging from 1 nm to 100 nm in the final
                                                                 formulation (Auffan et al., 2009; Ansell et al., 2010).
Organic filters include benzophenone-3 (BP-3; also               Other minerals used in sunscreens include silicate-
known as oxybenzone), benzophenone-4 (BP-4), para-               based substances such as talc and kaolin. Sunscreens
aminobenzoic acid (PABA) and PABA esters, cinnamates,            also contain inactive ingredients such as anti-microbial
salicylates, camphor derivatives, dibenzoylmethanes              preservatives, moisturisers and anti-oxidants which
and anthranilates (Chisvert et al., 2001; Danovaro               may make up between 30 and 70% of the product.
and Corinaldesi 2003). These are generally used
in combination because no single one, at currently
permitted concentrations, provides sufficient protection
                                                                                  Impacts of sunscreens on corals - ICRI briefing - Feb 2018   3
IMPACTS OF SUNSCREENS ON CORAL REEFS - FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE ...
3/ OCCURRENCE OF SUNSCREEN COMPONENTS
IN THE MARINE ENVIRONMENT
This section reviews studies have been carried out to      The overall quantity of sunscreens that enter the ocean     part per million (mg/L) have been reported (e.g. 1.395
investigate the occurrence and concentration of UV         is not known, although some estimates have been             ppm oxybenzone reported by Downs et al (2015) in the
filters in seawater, marine sediments and biota. These     made. Some 20,000 tons of sunscreen were estimated          US Virgin Islands). It is however, important to note, that
are not confined to areas with coral reefs but provide     by Corinaldesi (2001) to be released annually into          although the concentrations may be low, persistence of
a broad picture of the range of sunscreen components       the northern Mediterranean. Danovaro et al (2008)           low concentrations may have additive effects if these
that reach the marine environment. Risk assessments        estimated that 4,000-6,000 tons of sunscreen wash off       chemicals are sequestered by marine organisms.
have also been conducted to provide an indication of the   people into coral reef areas each year but Downs et al
environmental implications of this pollution.              (2015), citing Shaath and Shaath (2005), UNWTO (2007),
                                                           Danovaro et al. (2008) and Wilkinson (2008), concluded
Organic and inorganic UV-filters reach coastal waters      that 6,000-14,000 tons of sunscreen lotion are released
either directly from people who have applied sunscreens    into coral reef areas each year. Downs et al (2015) note
before entering the water and/or indirectly from           that many of the lotions contain 1-10% of the UV filter
wastewater treatment plant effluents (e.g. Daughton and    oxybenzone and suggest that at least 10% of global
Ternes, 1999; Danovaro et al., 2008; Sánchez-Quiles and    reefs and 40% of coastal reefs are at risk of exposure to
Tovar-Sánchez 2015). Sunscreen ingredients, including      this chemical. However, to date, the level of exposure
oxybenzone, BP-4, ethylhexyl methoxy cinnamate             has only been quantified at a few coral reef sites.
(EHMC), homosalate (HMS), 4-methylbenzylidene
camphor (4-MBC), diethylamino hydroxybenzoyl hexyl         Where sunscreen components have been detected,
benzoate (DHHB), titanium dioxide and zinc oxide, have     concentrations are very variable; most work has been
been detected in coastal waters (Daughton and Ternes       undertaken on oxybenzone and information for this
1999; Giokas et al. 2007, Danovaro et al., 2008; Tovar-    chemical is summarised in Table 1. Sunscreen filters
Sánchez et al., 2013; Sánches Rodrίguez et al., 2015;      are generally found at barely detectable levels of a few
Downs et al., 2015).                                       parts per trillion (ng/L), but concentrations of over 1

                                                                                                                                       Impacts of sunscreens on corals - ICRI briefing - Feb 2018   4
IMPACTS OF SUNSCREENS ON CORAL REEFS - FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE ...
TABLE 1/ CONCENTRATIONS OF OXYBENZONE (BP-3)
REPORTED IN SHALLOW WATERS AT VARIOUS SITES.

Further details for each of the countries/states where research has been undertaken are provided after the table.

                             SITE                                                       SAMPLING LOCATION                                   OXYBENZONE CONCENTRATION

 US VIRGIN ISLANDS: CARIBBEAN SEA

 Trunk Bay 2007 (Downs et al., 2015)                           Shallow water adjacent to reef. 180 people in water prior to sampling    580μg L-1 - 1.395 mg L-1
 Trunk Bay June 2013. (Bargar et al., 2015)                    2 samples at shoreline, 1 sample 30m from offshore island at 1m depth    1,943 – 4,643ng L-1
 Trunk Bay June 2014.
                                                               shoreline at
IMPACTS OF SUNSCREENS ON CORAL REEFS - FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE ...
SITE                                                         SAMPLING LOCATION                                 OXYBENZONE CONCENTRATION

CHINA
Hong Kong (Tsui et al., 2017)                                  4 locations; wet and dry seasons                                        12.9 - 31.9 ng L-1
JAPAN
Okinawa (Tashiro and Kameda, 2013)                             Shallow water 300-600m from beach                                       0.4 - 3.8 ng L-1
HAWAII (DOWNS ET AL., 2015)
                                                                                                                                       Detectable >100 ng L-1; below
Oahu Island; Maunalua Bay May 2011                             4 sites; 35cm depth
                                                                                                                                       quantitative range of 5 μg L-1
                                                                                                                                       1 site: 19.2 μg L-1
                                                               1 site; 35cm depth
Maui Island: Kapalua Bay May 2011                                                                                                      Detectable >100 ng L-1; below
                                                               Often >500 swimmers
                                                                                                                                       quantitative range of 5 μg L-1
PALAU (BELL ET AL., 2017)
                                                                                                                                       4.12 - 10.2 ng L-1 in 3 samples. Not
                                                               8 samples. Tourist location: visited by tens of thousands of people.
Palau: Jellyfish Lake water. Jan 2016                                                                                                  detectable in 4 samples; present but
                                                               Marine lake water
                                                                                                                                       not measurable in 1 sample.
Palau: Jellyfish Lake, from inlet by tourist dock: 8 samples                                                                           4.99 - 5.36 ng L-1 in 2 samples. Not
                                                               8 samples. Marine lake water by tourist dock
Jan 2016.                                                                                                                              detectable in 6 samples
Palau: Outside Jellyfish Lake near outside dock: Jan
                                                               4 samples. Not a swimming area                                          Not detectable in any of 4 samples
2016.
                                                               8 samples. Marine lake water. Intended as control site away from        4.4 to 18.5 ng L-1 at 3 sites; not
Palau: Ngermeuangel Lake water. Jan 2016.
                                                               tourist areas                                                           detected at 9 sites
Palau: lagoon outside entrance to Ngermeuangel Lake:
                                                               4 samples. Not a swimming area                                          Not detectable in any sample
Jan 2016.
Palau: Ocean outside Lighthouse Reef                           4 samples: control site                                                 Not detectable in any sample

                                                                                                                                      Impacts of sunscreens on corals - ICRI briefing - Feb 2018   6
IMPACTS OF SUNSCREENS ON CORAL REEFS - FUNDED WITH THE SUPPORT OF THE GOVERNMENT OF SWEDEN AND THE FONDATION POUR LA RECHERCHE SUR LA BIODIVERSITE ...
3.1. US VIRGIN ISLANDS                                         Carolina sites found the highest concentrations
                                                               measured were > 3700 ng OC L-1 and ~ 2200 ng
                                                                                                                            3.5. HONG KONG
(Caribbean)                                                    oxybenzone L-1 at a local beach front park, where beach      (West Pacific)
                                                               use was the greatest (Bratkovics et al., 2015).
Initial analysis of seawater at Trunk Bay on St John                                                                        Tsui et al. (2017) investigated the occurrence and
Island showed levels of oxybenzophenones in the                                                                             distribution of seven commonly used organic UV filters
water column between 1 ppm and 90 parts per billion
(ppb) (Downs et al., 2011). Further sampling revealed
                                                               3.3. MAJORCA ISLAND                                          in corals, seawater and sediment from the eastern Pearl
                                                                                                                            River Estuary, South China Sea. Three of the sites had
oxybenzone levels of 1.395 ppm (mg L-1) at a site near         (Mediterranean Sea - Spain)                                  coral cover over 65% and were hotspots for snorkeling,
the edge of the Trunk Island coral community (Downs et                                                                      scuba diving and swimming. The remaining site was dived
al., 2015). A sampling site 93 m east of this site contained   Chemical analysis of the surface nearshore waters of         less frequently due to strong currents and low (65%) and concentrations (31.8 ±
and padimate-O were 62–321 ng L−1, 30–264 ng L−1               DHHB) were monitored in samples from six beaches             8.6 and 24.7 ± 10.6 ng g-1 wet weight respectively) were
and
indicated that over 20% of coral samples from the
study sites contained BP-3 concentrations exceeding
                                                             3.7. PALAU
the threshold values for causing larval deformities and      (Pacific Ocean)
mortality in the worst-case scenario. Higher probabilities
of negative impacts of BP-3 on coral communities are         Bell et al (2017) analysed 22 chemicals in water and
predicted to occur in the wet season (Tsui et al., 2017).    23 in sediment and jellyfish samples in Jellyfish Lake
                                                             (a tourist site) and three comparison sites (non-tourist
                                                             sites) in Palau. The chemicals were either found directly
3.6. HAWAI’I                                                 in sunscreen formulations or products (metabolites) that
                                                             the body makes from one of the sunscreen chemicals.
(Pacific Ocean)                                              These were found to be widespread in Jellyfish Lake
                                                             and also present in the sites presumed to be ‘pristine’
Seawater samples were collected in public swimming           with little human use. In general, water samples had low
areas at five sites in Maunalua Bay (Downs et al.,            levels of sunscreen compounds, while jellyfish tissues
2015). Four sites had detectable levels of oxybenzone        and sediment had relatively higher levels of these
([100 pptrillion; ng L-1) but were below the quantitative    compounds and metabolites, a potential indication of
range of measurement (5 ppb (µg L-1). The fifth site         bioaccumulation of these chemicals (Bell et al., 2017).
contained measurable levels of oxybenzone (19.2 ppb          Jellyfish Lake had the highest concentrations of the
(µg L-1). Samples were also collected at two sites along     chemicals, suggesting that these are entering the
the northwest coast of Maui Island. Kapalua Bay is a         environment by washing off tourists and that jellyfish
protected cove and has a public beach that can often         may then be absorbing and metabolizing oxybenzone
receive 500 swimmers per day in the peak tourism season.     (Bell et al., 2017). Compounds were also detected in
The Kapalua sample, taken immediately above remnants         Ngermeuangel Lake, where there are no visitors. Bell et
of a coral reef, had detectable levels of oxybenzone but     al (2017) suggest that the sunscreen compounds here
was below the quantitative range of measurement (5           may have come from effluent/sewer leaking from the
                                                                                                                                      Snorkeling in Jellyfish Lake - Palau. Photo: ©
ppb (µg L-1). Kahekili Beach Park is a public beach that     nearby population centre into the adjacent watersheds.
also serves visitors from a number of nearby hotels and      Bell et al (2017) conclude that the presence of sunscreen
resorts (Downs et al., 2015). Unlike Kapalua, Kahekili is    chemicals in both the jellyfish and the sediments is
an exposed shoreline and not protected within a bay, and     cause for concern. The Golden Jellyfish medusa stage is
retention time of contaminants is thought to be minimal      relatively short lived, with a life span of about 6 months
because of the prevailing currents. The Kahekili sample      and this stage may not live long enough to be directly
had detectable levels of oxybenzone but was below the        affected; however their benthic polyp stage, critical to
quantitative range of measurement (5 ppb). Kahekili is a     their life cycle, could be affected (Bell et al., 2017).
heavily visited beach and had 71 swimmers within 200
m of the sampling site at the time of sampling (11:45 h).

                                                                                                                                                  Extreme tourism in the Caribbean

                                                                                                                          Impacts of sunscreens on corals - ICRI briefing - Feb 2018   8
4/ IMPACT OF SUNSCREENS ON CORALS
AND REEF BIOTA – EVIDENCE TO DATE
Given the growing concern that some sunscreen
ingredients may be having a negative impact on corals
                                                             4.1. Effect of sunscreens                                   The experiments were carried out using aliquots of
                                                                                                                         sunscreens at final quantities of 10, 33, 50, and 100
and other reef biota, investigations are underway and        and selected sunscreen                                      μL/L seawater. In all replicates and at all sampling
this section summarises some of the key work. The
experiments carried out so far have used concentrations
                                                             components on coral                                         sites, addition of commercial sunscreen resulted in the
                                                                                                                         release of large amounts of coral mucous (composed
of sunscreen and sunscreen components that are               fragments                                                   of zooxanthellae and coral tissue) within 18–48 hr,
significantly higher than is generally found in the marine                                                               and complete bleaching of hard corals within 96 hr.
environment (Leonard pers. Comm. 19-12-2017).                The first investigations into the possible harmful          Bleaching was faster in corals subjected to higher
For example, Danovaro et al (2008) used sunscreen            effects of sunscreen on corals (Danovaro et al., 2008)      temperature, suggesting synergistic effects with heat.
concentrations of 10, 33, 50, and 100 μL/L seawater.         consisted of a series of experiments conducted in four      The zooxanthellae released from treated corals had
Assuming that the density of the compounds is close          coral reef areas: Siladen, Celebes Sea (Indonesia);         lost photosynthetic pigments and membrane integrity.
to 1, then µL/L equals mg/L and the experimental             Akumal, Caribbean Sea (Mexico); Phuket, Andaman             In contrast, zooxanthellae membranes from untreated
concentrations were approximately 10, 33, 50 and             Sea (Thailand), and Ras Mohammed, Red Sea (Egypt).          corals were intact (Danovaro et al. 2008).
100mg/L. This is markedly higher than most of the            Nubbins of Acropora were collected and washed
concentrations shown in Table 1, the exceptions being        with virus-free seawater prior to being transferred         Among the individual sunscreen organic compounds that
the swimming ‘hotspots’ where hundreds of people             to polyethylene bags for in-situ incubation with            were tested, butylparaben, ethylhexyl methoxycinnamate,
are in the water as in the US Virgin Islands (Downs et       commercially available sunscreens and also with             oxybenzone and 4-MBC caused rapid and complete
al., 2015). Further research is thus needed before firm      individual sunscreen components. Concentrations used        bleaching even at the lowest concentrations used in the
conclusions can be reached.                                  were 10, 33, 50, and 100 μl L-1 seawater (i.e. between      experiments (10 μL L-1). Conversely, all other compounds
                                                             10 to 100 ppb). Additional experiments were performed       tested (i.e., OC, ethylhexylsalicylate and 4-tert-butyl-
                                                             with two other hard corals, Stylophora pistillata and       4-methoxydibenzoylmethane (avobenzene)) and the
                                                             Millepora complanata.                                       solvent propylene glycol, which is also present in
                                                                                                                         sunscreen formulations, had a minor effect or no effects
                                                             Corals were incubated at the same depth as the donor        when compared with controls (Danovaro et al., 2008).
                                                             colonies at in situ temperatures. Samples of seawater
                                                             were collected at 12-hr intervals and analysed for virus-   After the addition of sunscreens, viral abundance in the
                                                             like particles and zooxanthella released by the corals.     surrounding seawater increased significantly, reaching
                                                             At the end of the experiments, samples of coral tissue      values greater by a factor of 15 than in controls. As
                                                             were preserved and stored for zooxanthellae counts.         with the bleaching, this occurred even at the lowest
                                                             Levels of bleaching were quantified using colorimetric      concentration used in the experiments (10 μL L-1). The
                                                             analysis of digital photographs taken at the beginning      viruses were considered to have been released from the
                                                             of the experiments and after various times of treatment     corals or their symbiotic zooxanthellae, and virus-like
                                                             (Danovaro et al 2008).                                      particles were found around and inside the zooxanthellae.
                                                                                                                         In contrast, addition of organic nutrients without UV

                                                                                                                                        Impacts of sunscreens on corals - ICRI briefing - Feb 2018   9
filters or preservatives (as controls) did not result in a    weekly seawater renewal. PSII photosynthetic efficiency         Orbicella annularis), Montastraea. cavernosa, Porites
significant increase in viral abundance. Viruses were         of the symbiotic micro-algae was monitored using PAM            astreoides and Acropora cervicornis were also used
not found inside or outside the zooxanthellae (Danovaro      (Pulse Amplitude Modulation), to predict the sublethal          to investigate the effects of exposure to oxybenzone.
et al., 2008).                                               endpoint of coral bleaching (Fel et al., 2017). This study      Corals for the cell analysis were obtained from various
                                                             found that the organic UV filters Mexoryl SX, Mexoryl           sources and maintained in glass aquaria with custom
These findings correlate with previous research by           XL, Ethylhexyltriazone and OC did not induce coral              LED lighting (Downs et al., 2015).
Danovaro and Corinaldesi (2003) which investigated the       bleaching nor reduce the photosynthetic efficiency of the
effects of cosmetic sun products on viral abundance          symbiotic micro-algae at nominal concentrations above           The results studies were consistent with the
and bacterial activity in surface seawater samples from      those reported in natural seawaters (Giokas et al., 2007),      morphological observation by Danovaro et al. (2008).
Ancona, northern Adriatic Sea. They tested sunscreen         and avobenzone showed an effect only at the highest             In the light, oxybenzone caused injury directly to
containing both chemical and physical sun-blocking           nominal concentration (5,000 µg L-1). The mineral UV            the zooxanthellae. Under dark conditions, bleaching
agents (Ambre solaire Mexoryl sx 7, Laboratoires             filter zinc oxide had no effect at 10 µg L-1 but altered the    resulted from the symbiophagy of the zooxanthellae, a
Garnier) and a solar oil without UV protection (Bilboa Sun   PSII at 100 µg L-1 and induced coral bleaching at 1,000         process whereby the coral gastrodermal cell ‘digests’
Oil, Cadey) and found that sunscreen supplementation         µg L-1 (nominal concentrations with analytical control).        the zooxanthella (Downs et al. 2009). In addition,
induced the lytic cycle in a large fraction of total                                                                         planulae exhibited an increasing rate of coral bleaching
bacterial abundance (13-24% of bacteria, at low and                                                                          in response to increasing concentrations of both BP-2
high concentrations, respectively), whereas solar oil had
a lower impact (6-9%).
                                                             4.2. Effects of benzophenones                                   and oxybenzone.

                                                             on coral planulae and in vitro                                  The Downs et al (2014; 2015) study showed that both
Danovaro et al (2008) concluded that sunscreens, by
promoting viral infection, potentially play an important
                                                             coral cells                                                     BP-2 and oxybenzone are photo-toxicant, with adverse
                                                                                                                             effects exacerbated in the light versus in darkness.
role in coral bleaching. However, Leonard (personal                                                                          The lethal concentration 50 (LC50: standard measure
                                                             Downs et al. (2014; 2015) examined the effects of
communication 19-12-2017) suggests that there is                                                                             of toxicity: the concentration of the substance that
                                                             benzophenone-2 (BP-2) and oxybenzone on planula
insufficient evidence at this stage to conclude that the                                                                     causes the death of 50% of the test subjects) of planulae
                                                             larvae of Stylophora pistillata at the Inter-University
increase in virus density causes bleaching. He points                                                                        exposed to oxybenzone in the light for an 8- and 24-h
                                                             Institute of Marine Sciences (IUI) in Eilat, Israel. Planulae
out that the coral microbiome is a complex ecosystem                                                                         exposure was 3.1 mg/L and 139 μg L-1, respectively.
                                                             were collected using light traps and exposed to BP-2 and
of bacteria, archea, fungi and viruses whose respective                                                                      The LC50s for oxybenzone in darkness for the same time
                                                             oxybenzone during four different time-period scenarios.
population growths are under subtle controls. When this                                                                      points were 16.8 mg L-1 and 779 μg L-1.
                                                             Six concentrations were used for the experiments,
ecosystem is disorganized by high concentrations of
                                                             ranging from 246 mg L-1 (ppm) to 2.46 μg L-1 (ppb)
an external compound it is to be expected that certain                                                                       Whether in darkness or light, both benzophenones
                                                             for BP-2 and 228 mg L-1 (ppm to 2.28 μg L-1 (ppb) for
organisms (here the virus) will take advantage of the                                                                        induced coral planulae to transform from a motile
                                                             oxybenzone. Histopathology and cellular pathology,
stress situation and multiply when the other partners                                                                        planktonic state to a deformed, sessile condition. Downs
                                                             planula morphology, coral bleaching, DNA damage and
are weakened (Leonard; personal communication 19-                                                                            et al (2015) conclude from these experiments that
                                                             planula mortality were then measured.
12-2017).                                                                                                                    oxybenzone is a skeletal endocrine disruptor, inducing
                                                                                                                             ‘ossification’ of the planula and encasing the entire
                                                             In some experiments, coral cells in culture (calicoblasts)
In experiments designed to more closely mimic conditions                                                                     planula in its own skeleton.
                                                             were also used as a surrogate for coral planulae. Coral
on the reef, coral nubbins of Stylophora pistillata were
                                                             cells from Stylophora pistillata were used in the BP-2
exposed for 5 weeks to low concentrations of UV filters                                                                      It was also shown that both chemicals are genotoxic to
                                                             experiments and this species together with Pocillopora
in 15 litre aquaria, using a closed-circuit system with                                                                      corals, exhibiting a strong positive relationship between
                                                             damicornis, Montastraea annularis (valid name now

                                                                                                                                            Impacts of sunscreens on corals - ICRI briefing - Feb 2018   10
DNA-AP lesions and increasing concentrations. BP-2
exposure in the light induced extensive necrosis in
                                                             Coral larvae released from adult colonies of Porites
                                                             astreoides collected from reefs in the Florida Keys were
                                                                                                                             4.4. Direct and indirect
both the epidermis and gastrodermis, and in the dark,        exposed to each of the 5 sunscreen formulations and             effects exposing reef biota to
it induced autophagy and autophagic cell death (Downs
et al., 2015). Monitoring at Trunk Bay (US Virgin Islands)
                                                             the one ‘reef-friendly’ ingredient (titanium dioxide).
                                                             The three sunscreen/seawater concentrations tested
                                                                                                                             sunscreens
showed minimal recruitment/survival of juvenile coral        were: 100µl L-1 (which corresponds to the maximum
                                                                                                                             McCoshum et al (2016) investigated the effects of
and lack of regeneration from experimentally induced         concentration tested by Danovaro et al. 2008), 1µl L-1
                                                                                                                             sunscreens on lab-reared organisms commonly
lesions in established colonies of Porites astreoides        and 0.01µl L-1. The same procedures were followed for
                                                                                                                             found in shallow coral reef ecosystems, including
over a 5-year period (Downs et al., 2011). Downs et al.      the controls, with sunscreen being replaced by the same
                                                                                                                             included flatworms (Convolutriloba macropyga) with
(2011) found levels of oxybenzophenones in the water         volume of fresh seawater. Treatment order/placement
                                                                                                                             symbiotic algae, soft corals (Xenia elongata), glass
column at this site to be between 90 ppb and 1 ppm and       was randomized and color-coded to enable blind scoring
                                                                                                                             anemones (Aiptasia spp.) and diatoms (Nitzschia
suggested that the severe ecological degradation of          (Sharp et al., 2017).
                                                                                                                             spp.). The organisms were grown together in a 208 litre,
the reefs in this area was caused by sunscreens from
                                                                                                                             established multi-species aquarium. Experiments were
recreational swimmers, given that other forms of land-       In this study, none of the treatments (either ‘reef friendly’
                                                                                                                             conducted using artificial saltwater to which was added
based or marine-based pollution are limited (Downs et        or commercial sunscreens) resulted in significant
                                                                                                                             a commercial sunscreen (‘Equate 50 SPF sunscreen’
al., 2015).                                                  larval mortality compared to the controls. The highest
                                                                                                                             containing homosalate, oxybenzone, OC, octisalate,
                                                             concentration (100µl L-1) of one of the commercial
                                                                                                                             and avobenzone as active ingredients), following the
                                                             brands (Brand 1, containing 7.5% octinoxate, 5.0%
4.3. Effects of organic and                                  octinosalate, 4.0% oxybenzone) significantly inhibited
                                                                                                                             methodology described by Danovaro et al., (2008).

mineral UV sunscreen filters                                 larval settlement but neither of the ‘reef friendly’
                                                             sunscreens significantly decreased larval settlement
                                                                                                                             All test organisms subjected to sunscreen-contaminated
on coral larvae                                              when compared to the controls.
                                                                                                                             water showed reduced population growth compared to
                                                                                                                             control groups, suggesting organisms near populated
                                                                                                                             and common marine tourist destinations, where
Sharp et al., (2017 unpublished; personal communication      Blum (personal communication 18-01-2018) has
                                                                                                                             sunscreen contamination is expected, could be at risk of
09-01-2018) have provided information on the effects         pointed out that testing finished products can be difficult.
                                                                                                                             population and colony decline (McCoshum et al., 2016).
of sunscreens on coral larvae in a technical report. In      Some sunscreen formulas are polymer-based, with the
                                                                                                                             The tested concentrations were 0.26 ml L-1, 0.026 ml
these experiments, the effects of two sunscreens being       result that the active ingredients become suspended
                                                                                                                             L-1 which are equivalent to approximately 260 mg L-1
developed as ‘reef-friendly’ products and one ‘reef          at the surface or on the sides of test containers rather
                                                                                                                             and 26 mg L-1 (ppm) and are very high compared to the
friendly’ sunscreen ingredient (titanium dioxide) were       than dispersing in the water. They eventually disperse,
                                                                                                                             levels of sunscreen generally found in natural waters and
compared with three leading commercially available           releasing the chemical compounds from the polymer
                                                                                                                             in Jellyfish Lake, Palau where Bell et al., (2017) levels of
sunscreen brands. The commercial sunscreens                  beads, but this is unlikely to happen during the initial 24-
                                                                                                                             zero to 1205 ng L-1 (parts per trillion) of UV filters (see
contained the active ingredients oxybenzone,                 48 hour period. Water in oil emulsions or purely oil based
                                                                                                                             Table 1 for oxybenzone).
avobenzone, octinoxate, octisalate, homosalate, and          formulas do not disperse well either and these factors
OC in varying concentrations as UV filters while the         need to be taken into consideration when conducting
                                                                                                                             Nominal sunscreen contamination also affected the
‘reef-friendly’ sunscreens contained non-nano titanium       tests (Blum, personal communication 18-01-2018).
                                                                                                                             behaviour of the study organisms. Although motile
dioxide as the UV filter.
                                                                                                                             flatworms did not appear to avoid sunscreen when given a
                                                                                                                             choice of sunscreen-contaminated and uncontaminated
                                                                                                                             areas, they did select light areas in uncontaminated
                                                                                                                             water and dark areas in sunscreen-contaminated water.

                                                                                                                                             Impacts of sunscreens on corals - ICRI briefing - Feb 2018   11
The lack of avoidance of the sunscreen by flatworms            replaced by other ingredients (Corinaldesi et al., 2017).     ‘oxidative stress’ in cells that can damage health and
suggests these organisms, and potentially other motile        Sunscreen B, containing oxybenzone, homosalate and            ultimately cause death (Sharma et al., 2012).
biota, will not avoid environments polluted by sunscreen.     preservatives, had the strongest impact: it caused
                                                              anomalies (mostly represented by development block or         Titanium dioxide nanoparticles used in sunscreen are
Soft corals showed a reduction in polyp pulses per            cell necrosis) in 100% of embryos after 24h of treatment      coated with silica, magnesium, or aluminium to eliminate
minute in sunscreen contaminated arenas. The observed         at the maximum sunscreen concentration of 50 µL L−1           UV reactivity. It has been shown that, in this form, ROS
reduction of pulses per polyp, and the change in flatworm      (equivalent to about 50mg L-1). The observed impact           production is low when the nanoparticles are exposed
light preference suggest that the sunscreen is causing        was dose dependent with alterations to development            experimentally to ultraviolet light (Lewicka et al., 2013).
some stress, but the mechanisms involved are unknown          seen in half of the embryos treated at the lowest             In contrast, zinc oxide nanoparticles derived from the
(McCoshum et al., 2016). Eyal (personal communication         sunscreen concentrations. Sunscreen A had a lower             same sunscreens do not have coatings and produced
16-01-2018) suggests that reduced pulsations and light        impact, affecting the development of one third of the         substantial amounts of ROS under UVA illumination,
avoidance might be stress responses due to oxygen             embryos of P. lividus at all concentrations (Corinaldesi      and could thus potentially cause high levels of
radicals and/or malfunction of the photosynthetic             et al., 2017). In contrast, the effects of the eco-friendly   oxidative stress in marine organisms (Tagliati personal
apparatus of the symbionts.                                   Sunscreen C were indistinguishable from the control           communication 22-12-2017). People are also less well
                                                              after 24h of treatment.                                       protected from the adverse effects of sun exposure if
                                                                                                                            photoactive nanomaterials are used in sunscreens.
4.5. Effects of sunscreen filters                             An additional set of experiments revealed that the eco-
                                                              friendly sunscreen had a similar efficacy to sunscreens A
                                                                                                                            Lewicka et al (2013) suggest that sunscreens with zinc
                                                                                                                            oxide should have nanoparticle surface coatings to limit
on sea urchin development                                     and B in protecting human fibroblasts from UVA radiation      ROS generation under ultraviolet illumination.
                                                              (Corinaldesi et al., 2017). These findings suggest that       Yung et al., (2014) confirmed that exposure of marine
Corinaldesi et al (2017) compared the effects of different    development of sunscreens that are both effective and         algae and invertebrates to zinc oxide nanoparticles can
sunscreens on embryonic and larval development of             environmentally friendly is potentially feasible.             induce a wide range of toxic effects, both acute lethal and
the sea urchin Paracentrotus lividus, a key species                                                                         chronic sublethal. They also noted that toxicity can occur
of coastal ecosystems of the Mediterranean Sea and                                                                          in certain species when exposed to environmentally
Eastern Atlantic Ocean and one of the most common
model organisms for ecotoxicological studies. Whilst
                                                              4.6. Toxicity effects of                                      realistic concentrations. Wong et al., (2013) showed
                                                                                                                            that in general, zine oxide nanoparticles ZnO were more
this sea urchin is found on coral reefs, the study is         inorganic UV filters                                          toxic to algae (marine diatoms Skeletonema costatum
relevant because it compares the impacts of ‘standard’                                                                      and Thalassiosia pseudonana) than zinc oxide, but
and ‘eco-friendly’ products.                                  Most commercial sunscreens with inorganic filters             relatively less toxic to crustaceans (Tigriopus japonicus
                                                              employ materials with nanoscale dimensions so that            and Elasmopus rapa) and the medaka fish (Oryzias
Two widely used commercial sunscreens in Europe and           the products are both transparent and smooth when             melastigma).
the USA were used, with one whose ingredients had             applied to the skin (Lewicka et al., 2013). These are
been patented as eco-friendly (Danovaro et al., 2014).        generally considered to be safer than chemical UV filters.    Whilst research shows that nanoparticles are potentially
Both the Europe (Sunscreen A) and USA (Sunscreen              However, certain types of titanium dioxide and zinc           hazardous, Hanna et al (2013) point out that many
B) products contained organic and inorganic filters           oxide nanoparticles produce reactive oxygen species           of the studies used short-term laboratory exposure
(titanium dioxiste nanoparticles) already reported to         (ROS) under UV illumination (Lewicka et al., 2013). ROS       tests with relatively short-lived species, and may not
affect marine organisms (Díaz-Cruz and Barceló, 2009;         are a group of free radicals, reactive molecules and          be so relevant in the marine environment. They thus
Manzo et al., 2013; Minetto et al., 2014). The eco-friendly   ions derived from oxygen, that are extremely harmful to       coupled laboratory-based studies of mussels (Mytilus
sunscreen did not have these compounds or they were           organisms at high concentrations and that can induce          galloprovincialis) with modelling in order to simulate

                                                                                                                                            Impacts of sunscreens on corals - ICRI briefing - Feb 2018   12
the effects of nanoparticles on mussel populations               have negative effects on growth and photosynthetic
using results from the studies on individuals. Mussels           activity of coral symbiotic algae (genus Symbiodinium)
exposed to zinc oxide nanoparticles for 12 weeks                 at concentrations estimated to be present in sewage.
had increased respiration rates and concentrations               Nevertheless, it is important to note that a full evaluation
of zinc in their tissues. These impacts were related to          is still lacking (Tagliati et al. unpublished, personal
decreases in growth and survival, and suggested that             communication 19-12-2017).
mussels were expending energy to combat the effects
of excess environmental zinc but were unable to meet
these demands at the highest exposure concentration
of 2 mg L-1. Large mussels seemed to tolerate higher
concentrations of zinc oxide nanoparticles for longer
periods of time, as survival was higher for large than for
small mussels after 6 and 12 weeks of exposure. Hanna
et al (2013) noted that, whilst the results of exposure
to 0.1–2 mg L-1 zinc oxide nanoparticles in seawater
indicated that these are toxic to mussels, these levels
were unlikely to be reached in natural marine waters.
However, these chemicals may accumulate in the tissues
of long-lived organisms following exposure.

Fel et al., (2017) exposed coral nubbins (Stylophora
pistillata) for 5 weeks to the mineral UV filter zinc oxide at
nominal concentrations above those reported in natural
seawaters. They found that this treatment had no effect
at 10 µg L-1 but altered the photosynthetic efficiency at
100 µg L-1 and induced coral bleaching at 1000 µg L-1.

Studies on the impacts of titanium dioxide nanoparticles
on tropical corals are currently in progress by Tagliati
et al. (unpublished, personal communication 19-12-
2017), involving both nanoparticles alone and coated
nanoparticles mixed with cosmetic ingredients to
simulate a commercial-sunscreen composition. Results
so far indicate that titanium dioxide nanoparticles
used as UV filters in sunscreen do not necessarily

                                                                                                                                Impacts of sunscreens on corals - ICRI briefing - Feb 2018   13
5/ KEY RESULTS AND CONCLUSIONS
It is known that significant amounts of sunscreen
wash off into the sea and, in controlled experiments,
                                                                                                                     5.2. Damage and deformation
some sunscreen chemical UV filters are toxic and                                                                     of coral larvae (planulae)
have negative effects on corals and other marine life
even at concentrations as low as 62 parts per trillion.                                                              Some sunscreen chemicals, in certain situations, cause
Oxybenzone has been identified as the main substance                                                                 coral larvae to stop swimming, change shape and
of concern. Organic UV filters have been reported to                                                                  ultimately die. Oxybenzone has been shown to be an
induce acute toxicities, developmental toxicities and                                                                endocrine disruptor, causing the outer epidermal cells
reproductive toxicities to different organisms. Some                                                                 of coral larvae to turn into skeleton at the wrong stage
studies have shown that sunscreen ingredients promote                                                                in their development (Downs et al., 2015). Studies on
viral infections in bacteria and zooxanthellae, causing                                                              other organisms have similarly shown that exposure to
coral bleaching.                                                                                                     sunscreen UV filters such as benzophenones, camphor
                                                                                                                     derivatives and cinnamate derivatives induce various
Although estimates of the quantities of UV filters in
sea water vary, concentrations have been found in          5.1. Bleaching of hard corals                             endocrine disrupting effects (Kim et al, 2014; Wang
                                                                                                                     et al., 2016). However, Wang et al (2016) note that the
sea water that are considered to be ‘environmentally                                                                 effective concentration (26 µg L-1) of oxybenzone, at
relevant’ and pose a threat to reefs. Downs (2016) notes   Laboratory and controlled in-situ studies using           which reproduction of the Japanese medaka fish was
that “emerging research is showing that oxybenzone         fragments and cells from various species of hard coral    significantly decreased, was at least a couple of orders
concentrations on nearshore reefs around the world         have shown bleaching in response to sunscreens. This      of magnitude greater than those detected in the ambient
are commonly between 100 parts per trillion and 100        may be for a number of reasons:                           environment (e.g. 125 ng/ L-1 in a Swiss Lake).
ppb — well within the range of being a significant         • In darkness, bleaching results from the symbiophagy
environmental threat”. Furthermore, Downs et al. (2015)     of the zooxanthellae; a process whereby the host
suggest that the threat of oxybenzone to corals and         cells ‘eats’ the zooxanthellae (Downs et al. 2009).      5.3. Damage to coral DNA
coral reefs from swimmers and point and non-point
sources of waste-water could more extensive than just      • In the light, BP-2 causes damage directly to the        and reproductive success
a few meters surrounding the release area. For example,     zooxanthellae, independent of any host-regulated
                                                            degradation mechanism. Danovaro et al (2008)             Oxybenzone has been shown to be as genotoxic,
in Okinawa, Tashiro and Kameda (2013) demonstrated
                                                            showed that bleaching occurred as a result of organic    meaning that it damages coral DNA, which can reduce
that oxybenzone contamination from beaches can travel
                                                            UV filters inducing the lytic viral cycle in symbiotic   a coral’s lifespan and immunity to disease, as well as
over 0.6 km from the pollution source.
                                                            zooxanthellae with latent infections.                    disrupting normal development and reproduction.
The main impacts of chemical filters (the primary cause    • Oxybenzone induces coral bleaching by lowering
of concern), under certain circumstances, appear to be:     the temperature at which corals bleach when
                                                            exposed to prolonged heat stress. This means that
                                                            the impact of increasing sea surface temperatures
                                                            may be exacerbated by the presence of sunscreen
                                                            contaminants and the resilience of corals to climate
                                                            change undermined.
                                                                                                                                    Impacts of sunscreens on corals - ICRI briefing - Feb 2018   14
6/ KNOWLEDGE GAPS
AND FURTHER RESEARCH REQUIRED
There are concerns that experiments undertaken to date        and Granek, 2016). Studies should focus on locations       framework about nano-ecosafety to saltwater
have been largely ex-situ, and mainly at subcellular,         with high visitor numbers where sunscreens are             organisms, because of fragmentary and incomplete
cellular and organism level, with very few studies of the     suspected as a possible cause of coral bleaching or        information and sometimes profiles of limited
wider impacts of sunscreens and their UV filters. There       reef decline.                                              ecological significance.
is a lack of firm evidence of widespread negative impacts
                                                             • Investigating UV filter toxicity in relation to ocean
at reef community and/or ecosystem level. The evidence                                                                 It is essential that reef scientists work with industry to
                                                              warming and acidification predictions, to assess the
available may not properly reflect conditions on the reef,                                                             ensure that all sunscreen ingredients are subjected to
                                                              effects of global climate change on this issue. While
where pollutants may rapidly disperse and be diluted.                                                                  toxicological testing in a standardised manner. Some
                                                              sunscreen exposure might not cause evident stress
Concentrations of UV filters used in experimental work                                                                 work is already underway to develop simple toxicity
                                                              in healthy corals, the response could be different
have generally been higher than those likely to be                                                                     indicators for sunscreens, using coral nubbins exposed
                                                              if corals are already facing stressful conditions.
encountered in the reef environment, although no study                                                                 for periods of 5 weeks to low concentrations of UV filters
                                                              Studies carried by Danovaro et al. (2008) showed
has assessed the levels of these chemicals in the tissues                                                              (Fel et al., 2017). Given that different sites are exposed to
                                                              that bleaching of corals and coral cells exposed to
of long-lived species.                                                                                                 different pollutants (as found in the US Virgin Islands),
                                                              organic UV filters was faster at higher temperatures.
                                                                                                                       each site must be investigated independently (Downs et
Further research needs include:                              • Researching the extent and significance of bio-         al., 2011). A more rigorous approach of this nature would
                                                              concentration and bio-accumulation of organic UV         enable managers to pinpoint where sunscreen pollution
• Determining concentrations of different sunscreen
                                                              filters, and the consequences of long-term, chronic      is having an impact and to focus attention on remedial
 components in the water column, sediment and biota
                                                              exposure to sunscreen pollutants.                        measures. Biocides, fertilizers and pesticides leaching
 in different locations, comparing sites that are heavily
                                                                                                                       from the coast should be included in such studies.
 visited and/or affected by coastal run-off with those       • Studying the effects of mixtures of pharmaceutical
 that are more remote.                                        and personal care products (PPCP) which would
                                                              provide a more realistic picture of ecological risks,
• Investigating the effects of sunscreen pollutants at
                                                              since organisms are rarely, if ever, exposed to single
 reef community and ecosystem level. Downs et al.
                                                              contaminants.
 (2015) linked some of the pathologies described
 above with reef degradation in the US Virgin Islands,       • Identifying those ingredients that are safe and those
 and it is possible that whole-organism changes could         that pose a realistic threat to marine ecosystems.
 affect nutrient and food web dynamics, biodiversity          The organic UV filters which are widely recognised as
 and community composition, habitat structure, and            being ‘of concern’, but there are other ingredients of
 disease dynamics (Prichard and Granek 2016).                 sunscreens that could have impacts but about which
                                                              little is known. Minetto et al. (2014) in at review of
• Exploring links between organismal or subcellular/
                                                              ecotoxicity of nanoparticle forms of zinc oxide and
 cellular-level   biomarkers     since        studying
                                                              titanium dioxide and other mineral nanoparticles
 pharmaceutical effects on biodiversity/ community
                                                              concluded that it was difficult to determine a clear
 composition in complex systems is difficult (Prichard

                                                                                                                                       Impacts of sunscreens on corals - ICRI briefing - Feb 2018   15
7/ RECOMMENDATIONS
Over-exposure to UV solar radiation is indisputably a          Measures that can be taken include:                           have to abide. For example, a review by Ruszkiewicz et
human health issue and the development of sunscreens                                                                         al., (2017) into neurotoxic effects of active ingredients
with organic and inorganic UV filters has been a significant
factor in reducing risks. However, considering the many
                                                               7.1. Encouraging                                              in sunscreen products advocates revisiting the current
                                                                                                                             safety and regulation of specific sunscreens and
stresses already faced by reefs and the current concerns       the manufacture                                               investing in alternative UV protection technologies.
about the toxicity of certain components of sunscreens
to corals and other marine organisms, a proactive and
                                                               of reef-friendly sunscreens
precautionary approach is required, especially in areas
                                                               IAs with all pharmaceutical products, sunscreen
                                                                                                                             7.2. Promoting the use
with high levels of marine-based tourism. The key
need is to reduce the amount of harmful sunscreen
                                                               manufacturers are governed by detailed regulations that       of reef-friendly sunscreens
components that reach the reef environment. This will
                                                               specify the limits of concentration of allowable UV filters
                                                               before a sunscreen can be placed on the market.
                                                                                                                             and other methods of UV
require the involvement of governments, reef managers,
divers, snorkelers and the tourist and pharmaceutical
                                                                                                                             protection
                                                               The regulations vary in different countries. For example,
industries.
                                                               in Europe, Regulation (EC) No 1223/2009 covers                A growing number of sunscreens are now on the market
                                                               assessment of the potential impact of chemicals on            that are considered to be eco-friendly, safe and non-
Although this document focuses on the effects of
                                                               human health and Regulation (EC) No 1907/2006                 toxic to corals. Initiatives providing information on these
sunscreen components on reef biota and the wider
                                                               covers the Registration, Evaluation, Authorisation and        include:
marine environment, it is important to note that there
                                                               Restriction of Chemicals (REACH). The REACH regulation
are also wider concerns about the effects of these                                                                           • The Environmental Working Group (EWG) in the
                                                               is aimed at ensuring a high level of protection of both
chemicals on human health. Krause et al (2012) point                                                                           USA: a non-profit organisation whose work includes
                                                               human health and the environment and its provisions
out that human exposure to UV-filters in sunscreens is                                                                         advocacy in the area of toxic chemicals (https://
                                                               are underpinned by the precautionary principle (http://
high because they are rapidly absorbed from the skin.                                                                          www.ewg.org/sunscreen).
                                                               eur-lex.europa.eu/eli/reg/2006/1907/2014-04-100).
They note that oxybenzone has been found in 96% of
                                                               The European Union (EU) lists 28 allowable UV filters,        • MarineSafe (www.marinesafe.org): a campaign and
urine samples in the US and that several UV-filters have
                                                               but in the USA, 24 ingredients are covered by the Food          certification scheme that aims to reduce the number
been found in 85% of Swiss breast milk samples.
                                                               and Drug Administration with some of the filters allowed        of toxic chemicals and plastics finding their way
                                                               in the EU being excluded (Pirotta, 2015). In Japan and          into the ocean through replacement, management
                                                               the USA, oxybenzone can be used as an active ingredient         and user engagement. MarineSafe awards an
                                                               at levels of up to only 5-6% but in the EU levels of up to      assurance mark to products formulated without
                                                               10% are permitted (Kim et al.,, 2014).                          marine-toxic ingredients or interactions, and that
                                                                                                                               are independently tested by certified laboratories to
                                                               These regulations have been established to ensure               ensure that the finished product is not harmful.
                                                               human safety and also take environmental concerns
                                                               into account. It is important that research into impacts      Many local authorities, reef managers, tour organisers,
                                                               of sunscreens on reefs and reef biota continues to feed       dive companies and non-profit organisations have
                                                               into the regulatory framework to which manufacturers          campaigns on environmental issues ranging from

                                                                                                                                             Impacts of sunscreens on corals - ICRI briefing - Feb 2018   16
marine litter to protection of endangered species and                         of the most important messages is to ‘Read the Label’,         However, the best information may not be being used:
reef etiquette, and these could be expanded to include                        and check the ingredients to ensure that the product is        sunscreens containing OC, any of the benzophenones,
sunscreens. A good example of this is the U.S. National                       ‘reef safe’ before buying or using it. People are also being   butyl      methoxydibenzoylmethane,      hexyldecanol,
Park Service, responsible for managing reefs in South                         urged to consider alternative protective measures, such        cetyl dimethicone, methylparaben, polyethylene,
Florida, Hawaii, U.S. Virgin Islands and American Samoa,                      as use of sun-protective clothing (McCoshum et al.,            propylparaben, and butylcarbamate, are considered to
who have produced an information sheet entitled Protect                       2016; https://www.ewg.org/sunscreen). By ‘covering-            be non-biodegradable and those containing titanium
Yourself, Protect The Reef! The impacts of sunscreens                         up’ using appropriate clothing and hats, finding shade         oxide and zinc oxide are considered biodegradable and
on our coral reefs (noaa.gov/_docs/Site%20Bulletin_                           and/or avoiding going out in the middle of the day, the        safe3 although mineral substances are by definition,
Sunscreen_final.pdf). This explains the issues and                            need for sunscreens is significantly reduced and there         non-biodegradable. In addition, the nanoparticle form of
potential impacts of sunscreens, asking people to use                         will thus be less pollution. Recent recommendations for        zinc oxide is now known to be toxic and not necessarily
ones that are less likely to damage corals.                                   reducing sunscreen pollution in Jellyfish Lake (Palau)         ‘reef friendly’.
                                                                              include similar practical advice and also that people
Since the first warnings about the dangers of sunscreen                       should be educated in the most responsible use of eco-         Hawaii: Efforts are underway to ban the sale of
toxicity (e.g. Danovaro et al., 2008) the environmental                       friendly sunscreen, which means application at least 20        oxybenzone throughout the state. Legislation stalled
lobby has been highly active in calling for people to buy/                    minutes before entering the lake (Bell et al., 2017).          in the final days of the 2017 session, but the effort
use only non-toxic sunscreens. Dive magazines, dive                                                                                          continues, with state lawmakers already starting their
centres and industry bodies such as PADI are also raising                                                                                    push to pass the bill in 2018 (Yoshioka 2017). If this is
the issue and urging people to use eco-friendly products.                     7.3. Regulating the sale                                       successful it would ban sale of oxybenzone products but
According to Downs (2016) some resorts and dive shops
are even proposing to offer ‘coral safe’ sunscreen for free
                                                                              and use of sunscreens                                          not entirely prevent their use because of international
                                                                                                                                             tourists who might carry sunscreens in with them from
to their guests. In this respect it is important that clear                   containing toxins                                              overseas. This highlights the importance of campaigns
and accurate information is provided and that people                                                                                         to raise awareness amongst visitors.
read the label.                                                               This approach is being taken in Mexico and Hawaii

In Bonaire in the Caribbean, a seminar is planned in                          Mexico: Sunscreens that are known to contain toxic             7.4. Exerting consumer
2018, to raise awareness about the potential threats to
reefs from sunscreens containing oxybenzone (Anon.,
                                                                              chemicals may not be used at the Xcaret and Xel-Há
                                                                              ecological reserves. At the park entrances, visitors must
                                                                                                                                             pressure to encourage
2017) and to encourage all retailers of sunscreen                             hand in their non-biodegradable sunscreens for the             development and use
products on Bonaire to only sell sunscreens that are free
of oxybenzone. Bonaire’s economy depends largely on
                                                                              duration of their visit, and a sample of biodegradable
                                                                              sunscreen is provided; when they leave, their own
                                                                                                                                             of eco-friendly sunscreens
healthy coral reefs and therefore it is not unreasonable                      sunscreen is returned1. At Xel-Há this initiative is
                                                                                                                                             The major sunscreen manufacturers may be reluctant to
to expect local businesses and inhabitants to contribute                      enshrined in the sites Environmental Management
                                                                                                                                             make changes to tried and tested formulations and would
pro-actively to solving this potential problem.                               System which covers a number of activities to reduce
                                                                                                                                             probably not do so unless dictated by official regulations
                                                                              impacts on the environment.          The “chemical-free
                                                                                                                                             or if it becomes more profitable to produce and sell a
Although there are still unanswered questions regarding                       sunscreen exchange program” at Xel-Há leads to about
                                                                                                                                             different product. In this latter respect, consumer
the eco-safety of the many sunscreen products on the                          100,000 chemical-free sunscreens being exchanged
                                                                                                                                             demand and consumer/retailer-led campaigns can be
market, those with higher levels of toxicity are known. One                   annually with visitors2.

1- http://blog.xcaret.com/en/biodegradable-sunscreen-everything-you-need-to-know/
2- http://www.xelha.com/social-responsability-xelha.php 3- http://blog.xcaret.com/en/biodegradable-sunscreen-everything-you-need-to-know
                                                                                                                                                             Impacts of sunscreens on corals - ICRI briefing - Feb 2018   17
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