Corals are home to 25% of the world's underwater fauna and flora; therefore, assessing the effects of chemicals on corals is a major topic in environmental protection. Coral reefs result from a photosynthetic symbiosis between fixed animal colonies, called polyps, and algae (zooxanthellae). These algae play a very important role in the metabolism of polyps by providing them with most of their carbonaceous nutrition; in particular, zooxanthellae provide sugars via photosynthesis12.
Bleaching is a response of corals to external stressors, such as temperature variations, overexposure to light or exposure to chemicals13,14,15. This phenomenon marks the rupture of the symbiosis between the corals and algae, with the partial or total loss of zooxanthellae populations and/or the degradation of the pigments responsible for coral colour within these algae16,17. Without symbiotic algae, corals are more vulnerable and do not have a source of energy. If a disturbance is not too intense and/or is not sustained over time, bleaching can be reversed, and corals can re-establish their symbiosis with zooxanthellae. Conversely, if the suffered effect is too strong, the coral dies18.
Evaluating the effects of chemicals, particularly sunscreen products, on the environment has been a major concern in recent decades. The protection of humans against UV radiation is necessary; however, the use of sunscreen products, which are released into the environment, represents a real threat to ecosystems, especially marine ecosystems and coral reefs. Indeed, due to their lipophilic nature19, sunscreen products tend to accumulate along the food chain and form a film on the water surface20; because of their UV filter, sunscreen products prevent the penetration of solar radiation necessary for underwater life21.
There are two types of UV filters used in sunscreen products: mineral UV filters and organic UV filters. The use of certain organic filters, such as octocrylene, oxybenzone, and 4-methylbenzylidene camphor, is subject to much controversy, as these filters can represent a danger to the environment22,23. It has been demonstrated that these products can cause hormonal effects that affect the fertility and reproduction of fish5,6. They also impact the activities of marine microorganisms and increase the abundance of viruses present in water11. As a result of this growing problem, a few countries have banned some of these organic filters to preserve the environment24.
In this context and considering the demonstrated or suspected harmful effects of some organic filters, the use of mineral filters, i.e., titanium dioxide (TiO2) or zinc oxide (ZnO), is developing in the cosmetics industry. Applying ecolabels to suncare products with mineral filters tends to promote their use, and these filters are reputed to be safer for the marine environment based on their larger particle size and lower solubility in seawater25,26. However, there are studies that did not conclude that these mineral filters, tested individually, are harmless to marine organisms such as green algae, corals or crustaceans27,28,29.
Given the uncertainty about the potential harmful effects of both types of UV filters, it is necessary consider the results of biological tests performed with finished products, in which these filters are integrated into mixtures with other cosmetic ingredients. The different compounds in finished products may interact, especially with the UV filters, potentially causing synergistic activities5. Studying finished products allows a more refined evaluation of the biological effects, allowing the determination of the potential danger from the whole product to the environment, especially to corals.
To study the effects of the 9 Grupo Boticário sunscreens, 3 different analytical series (AS1, AS2 and AS3) were performed. The results of the observations of polyp retraction and fragment bleaching after 48 hours and 96 hours of exposure are shown in Table 1 and Figs. 1–3. Bleaching was observed visually and defined by a bleaching gradient: 2 = no bleaching, 1 = partial bleaching and 0 = complete bleaching.
Table 1
Observations of polyp retraction and fragment bleaching
| | | | Observation after 48 h | Observation after 96 h |
Analytical series and date | Product name | Concentration (mg/L) | Replicate | Polyp retraction (Yes/No) | Bleaching (0–2*) | Polyp retraction (Yes/No) | Bleaching (0–2*) |
AS1: 3rd to 7th February 2020 | Control | 0 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 1 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 2 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 3 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 4 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 5 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
AS2: 31st August to 4th September 2020 | Control | 0 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 7 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 8 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
AS3: 7th to 11th September 2020 | Control | 0 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 9 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
Sunscreen 6 | 100 | 1 | No | 2 | No | 2 |
2 | No | 2 | No | 2 |
3 | No | 2 | No | 2 |
The results obtained were validated by the assessment of the following criteria: retraction of the polyps and bleaching of the fragments were not observed in the 3 replicates of the control for any of the analytical series, and the NOEC (Cu2+)-96 h values were between 33 and 64 µg/L (AS1 = 48 µg/L; AS2 = 33 µg/L; AS3 = 33 µg/L).
No toxic effects on either tested parameter were observed at any of the tested loading rates or for any of the tested sunscreens. Table 1 show results observed at only the highest tested loading rate, as there was no difference in the effects between the 7 tested loading rates. In this study, the coral response to sunscreen exposure was not dose dependent, as the same effects were observed at low and high sunscreen loading rates. For all the tested sunscreens, the NOEC was defined as 100 mg/L, and the LOEC was > 100 mg/L.
The effects of UV filters on living organisms inhabiting marine ecosystems are quite well documented in the scientific literature. Some studies carried out on other species of hard corals (tropical and well-represented species such as S. hystrix) have revealed harmful effects of UV filters, especially ZnO, with short exposure times. ZnO was found to cause strong negative effects in terms of the loss of zooxanthellae by Acropora spp. after as little as 48 hours of exposure to a ZnO concentration of only 6.3 mg/L30. Other work showed that ZnO was responsible for rapid and severe coral bleaching by altering the established symbiosis31, and studies on another hard coral species (Stylophora pistillata) showed a decrease in photosynthetic efficiency at 100 µg/L and bleaching at 1 mg/L29. Concerning the effects of TiO2 on hard corals, it has been determined that this mineral filter may interfere with the symbiotic relationship between corals and zooxanthellae by reducing algal populations within symbioses, without leading to coral death, at a concentration of 10 mg/L over an exposure period of 17 days32. Some organic filters, such as benzophenone 2, benzophenone 3 (oxybenzone), avobenzone, 4-methylbenzylidene camphor and ethylhexylmethoxycinnamate, have impacts on corals. Avobenzone can induce a significant decrease in photosynthetic efficiency at a concentration of 1 mg/L29, and benzophenone 2 and oxybenzone are toxic to corals, causing damage to zooxanthellae and DNA damage to coral cells22,33. Ethylhexylmethoxycinnamate and 4-methylbenzylidene camphor induce rapid bleaching at a concentration of 33 µg/L11. In this last study, finished sunscreen products from three different brands (containing diverse UV filters) were tested and the results revealed significant adverse effects on coral bleaching after only 24 hours of exposure to concentrations much lower than those in our study (between 10 and 100 µg/L).
In conclusion, the two mineral filters currently authorized, TiO2 and ZnO, and the main organic filters that were previously assessed have been shown to have harmful effects on corals, sometimes at very low concentrations. However, previous studies were based on the evaluation of only the filters, not the filters integrated into cosmetic formulations. Moreover, these individually tested filters have physicochemical characteristics (coating, size, etc.) that may differ from those of filters present in cosmetic formulations. The performance of ecotoxicological tests on finished products, such as those carried out in this study, allow the effects of the interactions between filters and the other constituent ingredients of sunscreen products to be assessed and enable the prediction of the potential threat from a product. In our study, we were thus able to observe that the tested finished products, which contained filters in combination with other ingredients, do not have any substantial ecotoxicological effects on corals, in contrast to other finished products tested previously.
The results of this study, which was conducted under "extreme" conditions compared to those in the natural environment (i.e., at product concentrations of 100 mg/L, which is much higher than those measured in coastal waters (on the order of ng/L or µg/L), allow us to argue for the absence of potential danger from the tested products to corals.