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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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
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
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
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
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
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
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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