Miller et al. Environ Sci Eur (2021) 33:74 https://doi.org/10.1186/s12302-021-00515-w RESEARCH Open Access Toxic efects of UV flters from sunscreens on coral reefs revisited: regulatory aspects for “reef safe” products Ingo B. Miller1* , Sascha Pawlowski2, Matthias Y. Kellermann1, Mechtild Petersen‑Thiery3, Mareen Moeller1, Samuel Nietzer1 and Peter J. Schupp1,4* Abstract Background: Tropical coral reefs have been recognized for their signifcant ecological and economical value. How‑ ever, increasing anthropogenic disturbances have led to progressively declining coral reef ecosystems on a global scale. More recently, several studies implicated UV flters used in sunscreen products to negatively afect corals and possibly contribute to regional trends in coral decline. Following a public debate, bans were implemented on several organic UV flters and sunscreen products in diferent locations including Hawaii, the U.S. Virgin Islands and Palau. This included banning the widely used oxybenzone and octinoxate, while promoting the use of inorganic flters such as zinc oxide even although their toxicity towards aquatic organisms had been documented previously. The bans of organic UV flters were based on preliminary scientifc studies that showed several weaknesses as there is to this point no standardized testing scheme for scleractinian corals. Despite the lack of sound scientifc proof, the latter contro‑ versial bans have already resulted in the emergence of a new sunscreen market for products claimed to be ‘reef safe’ (or similar). Thus, a market analysis of ‘reef safe’ sunscreen products was conducted to assess relevant environmental safety aspects of approved UV flters, especially for coral reefs. Further, a scientifcally sound decision‑making process in a regulatory context is proposed. Results: Our market analysis revealed that about 80% of surveyed sunscreens contained inorganic UV flters and that there is a variety of unregulated claims being used in the marketing of ‘reef safe’ products with ‘reef friendly’ being the most frequently used term. Predominantly, four organic UV flters are used in ‘reef safe’ sunscreens in the absence of the banned flters oxybenzone and octinoxate. Analysis of safe threshold concentrations for marine water retrieved from existing REACH registration dossiers could currently also safeguard corals. Conclusion: There is a substantial discrepancy of treatments of organic versus inorganic UV flters in politics as well as in the ‘reef safe’ sunscreen market, which to this point is not scientifcally justifed. Thus, a risk‑based approach with equal consideration of organic and inorganic UV flters is recommended for future regulatory measures as well as a clear defnition and regulation of the ‘reef safe’ terminology. Keywords: Coral toxicity, Ecotoxicology, UV flters, Standardization, Reef safe, Sunscreen, Regulation, Coral reef Background Tropical coral reefs are among the most biodiverse and *Correspondence: ingo.miller1@uni‑oldenburg.de; peter.schupp@uni‑ oldenburg.de economically valuable ecosystems on our planet. Tese 1 Environmental Biochemistry Group, Institute for Chemistry and Biology complex systems provide a wide range of vital ecosystem of the Marine Environment (ICBM), Carl von Ossietzky University services to human societies around the globe through of Oldenburg, Schleusenstr. 1, 26382 Wilhelmshaven, Germany Full list of author information is available at the end of the article coastal protection, fsheries, tourism and recreation © The Author(s) 2021. 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Environ Sci Eur (2021) 33:74 Page 2 of 13 opportunities, as well as resource for natural building corals to several widely used UV flters [10, 12, 16, 17, materials (i.e., lime stones) and new medicines [5, 55]. 28, 34, 51, 74, 78, 79, 90]. Following media driven pub- Although tropical coral reefs cover less than 0.1 percent lic attention gained from the fndings of Danovaro et al. of the ocean’s surface [76, 77], they harbor around one- [12] and particularly from those of Downs and colleagues quarter of all known marine species [5]. In particular, [16, 17], Hawaii was the frst state (followed by other tropical hermatypic (reef-building) corals, the actual reef states and nations) to take legislative action to ban (as of engineers, thrive in oligotrophic waters owing to highly January 2021) two organic UV flters commonly used in efcient retention and close nutrient cycling by them and sunscreens: benzophenone-3 (BP3 also known as oxy- other reef organisms [13, 68, 71]. Tis high productivity benzone) and ethylhexyl methoxycinnamate (EHMC or within these otherwise unproductive “marine deserts” octinoxate) [33]. On the other hand, inorganic UV fl- emphasizes the importance of coral reefs as biodiversity ters such as zinc oxide (ZnO), known to be very toxic to hotspots and high value economic resources for human aquatic life [18] (including cnidaria with a no observed populations living in their proximity [40]. efect concentration (NOEC) of 300 µg Zn2+ L−1), are Despite their ecological and economical importance, still allowed to be used in these locations. coral reefs are declining at a historically unprecedented However, sunscreens and the UV flters within are pace due to multiple local and global stressors that are all part of human sun protection measures to shield human caused directly or indirectly by anthropogenic activities skin from harmful UV-A (315–400 nm) and UV-B [4, 5, 42, 47]. Tese man-made disturbances are quickly (280–315 nm) radiation that are well-known causes for progressing, thus pushing coral reefs towards the tip- sunburn, skin aging and skin cancer [6, 30, 61]. As ingre- ping point of functional collapse [41, 45, 48, 70]. As a dients of personal care products, the number of UV flters key driver of climate change, excessive emissions of fos- is highly regulated and limited by various national legisla- sil organic carbon into the atmosphere have been lead- tions. For example, prior to marketing in the EU an UV ing to a steady increase of sea surface temperatures [49]. flter used as cosmetic ingredient requires the positive Already, several major global mass bleaching events have assessment by the independent EU advisory Scientifc occurred in tropical coral reef areas around the world Committee for Consumer Safety (SCCS). Te positive starting in the 1980s [37]. Such mass bleaching events evaluation is typically followed by an approval by the EU have become more frequently, resulting even in recurrent Commission leading to an inclusion of the assessed flter year to year mass bleaching events as observed in 1998, into the respective annex allowing the use in the EU. Cur- 2002 and 2016 [43, 47]. Te latest widespread bleaching rently, 29 UV flters meet the requirements for being used event occurred in 2020 at the world’s largest contigu- in cosmetic products [24] (cf. Additional fle 1: Table S1). ous coral reef, the Great Barrier Reef (AIMS [1]). Tus, In the United States, sunscreen products are classifed as immediate and rapid action to reduce global warming is over-the-counter (OTC) products and are strictly regu- needed to secure the future of tropical coral reefs [42, lated by the US Food and Drug Administration (FDA) 47]. according to pharma requirements. Tus, only 16 UV fl- However, on a local scale, more than 60% of the world’s ters are currently allowed [82, 84, 85]. Because of these reefs are threatened by one or several man-made distur- stringent requirements by US legislation, no approval of bances with overfshing being the most ubiquitous imme- any new UV flter has been granted and consequently diate pressure [5]. Other local perturbations such as listed in the monograph since 1998. Owing to their high destructive fshing, watershed-based pollution, marine- complexity in sunscreen and cosmetic products, sub- based pollution and damage from ships and coastal stituting one UV flter with another is challenging since development, including associated sedimentation, also not all UV flters are compatible with each other and a pose direct and immediate threats to coral reefs [5, combination of several UV flters is required to reach suf- 56]. Given the multitude of stressors and threats, some fcient broad spectrum protection as well as a high sun authors suggest that besides trying to achieve global scale protection factor (SPF; [66, 75]). measures, local actions should be taken into account to Terefore, regulatory measures should be evaluated minimize the impact on coral reefs as this may even con- thoroughly and should be based on actual evidence before tribute to the overall resilience towards mass bleaching legislative action is implemented. In fact, the passed sun- events [2, 3, 32, 42, 44, 46, 47, 72, 87]. screen bans are considered as controversial, since on the Recent research indicates that some ultraviolet (UV) one hand corals are difcult to culture organisms and on flters used in sunscreens and other personal care prod- the other UV flters are difcult test substances [56, 59, ucts (PCPs) may impact coral health on a local scale. 64], leading to a potentially high variability in possible Some researchers have claimed negative health efects, test results if the test procedure does not follow a stand- bleaching and enhanced mortality after exposure of ardized testing protocol.