Assessment of the Toxicities of Organic Ultraviolet Filters to Tropical and Subtropical Corals
Student thesis: Doctoral Thesis
|Award date||23 Feb 2017|
Organic ultraviolet (UV) filters are active ingredients added to commercial products such as sunscreens, skin whitening products and cosmetics for the purpose of protecting skin from sunburn and cancers caused by UV radiation. These compounds have attracted research attention in recent years because of their high lipophilicity and relative stability. They are released to seawater indirectly in industrial and domestic wastewater, and directly when applied to the skin in sunscreen products used during recreational activities at beaches and in coastal areas. Because of these characteristics and the widespread usage of products containing organic UV filters, these chemicals have been detected in surface seawaters at concentrations ranging from ng/L to µg/L levels. Recently, studies reported that these chemicals caused coral bleaching, which results from the loss of symbiotic zooxanthellae, at low concentrations/quantities.
Coral reefs are known as one of the most productive and biologically rich ecosystems on Earth, and are now threatened by many environmental and artificial stressors, including pollution, coastal development, thermal stress, etc. In recent years, thermal stress has intensified in many coastal areas, and has caused severe and widespread coral bleaching. Although organic UV filters have been widely detected in surface seawater and potential negative effects of organic UV filters and sunscreen products on the health of corals have been reported in a few studies, information is still lacking about their toxicities. In addition, there is limited information on the simultaneous effects of organic UV filter exposure and elevated sea surface temperatures on corals, even though these stressors are expected to co-occur in the environment, especially at popular sea beaches during peak recreational periods (e.g., summer).
This thesis aims to evaluate the toxicities of organic UV filters to corals. First, range-finding toxicity tests of single compounds were carried out. Then, the toxicities of some organic UV filters to corals were compared with a commercial sunscreen product containing those compounds to evaluate the potential impacts of the product to corals and to determine whether toxicity could be attributed to the UV-blocking active ingredients. Lastly, a mesocosm approach was used to investigate the effects of coral co-exposure to organic UV filters at environmentally relevant concentrations and thermal stress.
In the first tests, toxicities of four benzophenone (BP) UV filters (BP-1, BP-3, BP-4, and BP-8) to two coral species (Pocillopora damicornis and Seriatopora caliendrum) were tested. Coral larvae and nubbins were exposed to the selected UV filters at concentrations ranging from 0.1 to 1000 µg/L for 14 days and 7 days, respectively. Settlement, bleaching and survival were measured in the larval exposures, while mortality, polyp retraction, visual bleaching, photosynthetic efficiency, and zooxanthellae density were measured in coral nubbins. Risk assessment of the potential impacts of BP exposure on the health of corals in popular recreational areas in Hong Kong and Taiwan was performed. BP-1 and BP-8 exposure caused significant settlement failure [p < 0.05, Kruskal-Wallis and Mann-Whitney U tests (KM)], bleaching and death of S. caliendrum larvae at lower concentrations [Lowest-observed-effect concentration (LOEC) ≥ 10 µg/L] than the other BPs. None of the tested compounds and concentrations significantly affected P. damicornis larvae. S. caliendrum nubbins were affected by lower levels (LOEC ≥ 10 µg/L) of BP-1 and BP-8 in all the tested parameters than P. damicornis nubbins (LOEC > 1000 µg/L). Overall, BP-1 and BP-8 exerted higher toxicities to corals than BP-3 and BP-4, and P. damicornis was more tolerant than S. caliendrum to BP exposure. Risk assessment showed that BP-1, BP-3 and BP-8 pose medium or high risks to the health of corals in popular recreational areas in Hong Kong and Taiwan based on measured surface water concentrations.
Seven-day exposures to evaluate the toxicities of ethylhexylmethoxy-cinnamate (EHMC), octocrylene (OC) and a commercial sunscreen product containing both compounds [EHMC (7% w/w) and OC (3.6% w/w)] to coral nubbins of S. caliendrum and P. damicornis were conducted. The concentrations of EHMC and OC treatments ranged from 0.1 to 1000 µg/L. The sunscreen product was tested by applying it to the hands of two volunteers (2 mg/cm2) having similar hand surface area, after which the volunteers waved their hands gently in 2 L filtered seawater for 20 minutes. Volunteers were assigned to prepare sunscreen water for each coral species. Then, coral nubbins were exposed to diluted or original sunscreen water treatment (first test: 0%, 5%, 20%, 50% and 100%; second test: 0%, 1%, 5%, 20%, and 50%). Chemical analysis of water samples showed 5% sunscreen water contained 422.34 ± 37.34 µg/L of EHMC and 33.50 ± 7.60 µg/L of OC at Day 0 in the two tests. Three replicates of three nubbins each were prepared, and mortality, bleaching, and polyp retraction were measured. Death (33.3%) and bleaching (83.3%) of S. caliendrum nubbins were found after exposure to 1000 µg/L EHMC (LOEC). Total polyp retraction was the only adverse effect found in P. damicornis exposed to EHMC; this effect was found in both S. caliendrum and P. damicornis exposed to OC. In the sunscreen product exposures, 5% sunscreen water caused mortality in S. caliendrum (66.7% in the first test and 83.3% in the second test) and P. damicornis (33.3% in the first test and 50% in the second test). Complete (100%) mortality of S. caliendrum and P. damicornis nubbins was found in the 20% sunscreen water treatments. These results show that exposure to diluted sunscreen water which contains lower levels of EHMC and OC (e.g. 5%) than single chemical exposures can cause coral bleaching and death, indicating that EHMC and OC may have synergistic effects to corals and/or this product contains some ingredients that are also toxic to corals. Based on these results taken together, EHMC and OC probably are not the only contributors causing the effects of this sunscreen product on S. caliendrum and P. damicornis nubbins, and studies on the toxicities of commercial sunscreen products to corals should not only focus on the toxicities of active ingredients.
In the third set of experiments, a 60-day mesocosm study was performed to test the effects of an organic UV filter mixture under general environmental concentrations and elevated temperature on coral nubbins of S. caliendrum, P. damicornis and Montipora aequituberculata. The mixture contained 200 ng/L BP-1, BP-3, BP-4, BP-8, EHMC, OC, 4-methylbenzylidene camphor, butyl methoxydibenzoyl-methane, ethylhexylsalicylate, homosalate, isoamyl p-methoxy-cinnamate and octyl dimethyl-p-aminobenzoic acid. Treatments including solvent control (I), organic UV filter mixture (II), and organic UV filters mixture + elevated temperature (30 °C) (III) were prepared. Similar parameters as in the EHMC exposures were measured (n = 8), and in addition, enzyme activities of superoxide dismutase (SOD) and catalase (CAT) were determined (Day 1, 4, 7, 14, 30 and 60, n = 4), and gene expression of Symbiodinium ferric manganese SOD (FeMnSOD), copper zinc SOD (CuZnSOD) and catalase peroxidase, and of host FeMnSOD, CuZnSOD, CAT (P-cat) and Cytochrome P450 1A1 (P-cyp1a1) of P. damicornis was also measured (Day 1, 4, 7, 14, 30 and 60, n = 4). Nubbins in treatment I appeared healthy throughout the exposure. Bleaching (37.5%) and death (12.5%) of S. caliendrum in treatment II were observed. In treatment III, 100% bleaching and mortality of S. caliendrum and 100% bleaching and 50% mortality of P. damicornis were found. Bleaching (50%) and total polyp retraction (100%) of M. aequituberculata nubbins in treatment III were also observed. The activities of SOD in S. caliendrum nubbins significantly increased after the 60-day exposure (p < 0.05, KM), and CAT activities in P. damicornis and M. aequituberculata nubbins were also significantly elevated in treatment III (p < 0.01 for both, one-way ANOVA). Expression of P-cat and P-cyp1a1 was significantly upregulated (p < 0.05 for both, KM) in treatment II, while the expression of these genes in treatment III was also significantly increased (p < 0.05 for both, KM) when compared with treatment II. The results suggest that organic UV filters at environmental concentrations caused bleaching and mortality in coral nubbins by inducing a significant oxidative stress and detoxification burden, while thermal stress could intensify these adverse effects.
To conclude, the results of these studies show that single organic UV filters exerted significant or severe toxicity to coral only at levels 10-to-1000 times greater than environmental concentrations based on the parameters tested, while exposure to seawater containing diluted sunscreen product concentrations caused coral nubbin mortality at levels lower than the effect levels of the single organic UV filter (EHMC or OC) exposures. These results suggest that commercial sunscreen products may exert higher toxicities than the organic UV filters they contain, and that toxicities of the other ingredients of commercial sunscreen products to corals should be of concern. Moreover, a two-month exposure of three common coral species to an organic UV filter mixture under environmentally relevant concentrations caused bleaching and mortality of coral nubbins, especially when the nubbins were under thermal stress.
Many coastal beaches and regions, especially in tropical and subtropical zones (e.g. Hong Kong and Taiwan), are popular recreational areas which attract tens of thousands of people. Sunscreen products with unknown toxicities to corals will likely be used and released to coastal waters during these periods when severe thermal stress due to global climate change-induced rising sea surface temperatures is also likely to occur and perhaps persist. The results obtained in the present study indicate that corals exposed to both organic UV filters and/or commercial sunscreen products as well as thermal stress may suffer adverse effects ranging from oxidative stress to bleaching and mortality. Severe bleaching events leading to mortality are irreversible, and consequently lead to reduced areas of living coral, reduced species diversity and impacts on coral reef fisheries. In order to protect the health of reef-building corals, especially those inhabiting popular beach and marine tourism areas, the toxicities of organic UV filters (single chemical or mixture) and commercial sunscreen products, and the simultaneous effects of organic UV filters and other environmental stressors to corals should be tested and evaluated. In the long run, protecting coral health requires that prevalently-occurring organic UV filters with relatively high toxicities that pose relatively high risks to corals be reduced in commercial products (especially in sunscreen products) or even banned, and that commercial sunscreen products which are found to have strong impacts to corals likewise be modified or banned. The results of these studies further indicate that multiple stressors must be taken into account when evaluating threats to reef-building corals and when considering coral management and conservation measures, particularly in light of the ongoing and strongly negative effects of global climate change on corals and coral reefs.