Comparative toxicities of four benzophenone ultraviolet filters to two life stages of two coral species

Highlights

• BP-1 and -8 were up to 10 times more toxic to corals than BP-3.

• Toxicities and bioaccumulation of the tested BPs followed a similar ranking pattern.

• BP-1 and -8 are generated as metabolites of BP-3 in coral tissues.

• Sensitivities to BP exposure differed between coral species and life stages.

• BP-3 and -8 conservatively pose medium-to-high risks to the health of corals.

Abstract

The benzophenone (BP) organic ultraviolet (UV) filters have been measured in seawater at ng/L to μg/L levels, but more data on their effects in non-target marine organisms are needed. Corals can be exposed to BPs due to wastewater discharges and coastal recreational activities. In this study, toxicities and bioaccumulation of BP-1 (2,4-dihydroxybenzophenone), BP-3 (oxybenzone), BP-4 (sulisobenzone) and BP-8 (dioxybenzone) to larvae and adults of two coral species, Pocillopora damicornis and Seriatopora caliendrum, were assessed at concentrations ranging from 0.1–1000 μg/L. BP-1 and BP-8 exposure caused significant settlement failure, bleaching and mortality of S. caliendrum larvae [lowest observed effect concentration (LOEC): ≥10 μg/L] compared to the other BPs, while none of the tested compounds and concentrations affected P. damicornis larvae. Nubbins were more sensitive to BP-3, BP-1 and BP-8 than larvae. Overall, BP-1 and BP-8 were more toxic to the two tested species than BP-3 and BP-4, which matches the relative bioaccumulation potential of the four BPs (BP-8 > BP-1 ≈ BP-3 > BP-4). A conservative risk assessment using the effect concentrations derived from this study showed that BP-3, BP-1 and BP-8 pose high or medium risk to the health of corals in popular recreational areas of Taiwan and Hong Kong. Our study suggests that future ecotoxicological studies of corals should take their sensitivities, life stages and metabolic capacities into consideration.

Introduction

Benzophenone (BP) ultraviolet (UV) filters are one class of organic UV filters that is used in products to prevent burning of the skin by both UVA (320–400 nm) and UVB (280–320 nm) radiation (Santos et al., 2012). Five BP compounds are commonly used in personal care products (PCPs): BP-1, BP-2, BP-3, BP-4 and BP-8 (Table S1) (Fent et al., 2008; Kim and Choi, 2014; Santos et al., 2012). Usage levels of these BPs in PCPs range between 3 and 10% w/w (Table S2). BP-1 and BP-8 have also been measured in mammals as metabolic products of BP-3 (Okereke et al., 1994; Wang and Kannan, 2013). This year, a bill banning sunscreens containing BP-3 and EHMC (octinoxate) was passed by the US state of Hawaii, bringing greater attention to the issue of marine pollution by organic UV filters (Coldwell, 2018).

There are two routes by which BPs may occur in the aquatic environment: directly, as a consequence of recreational water activities (e.g. swimming), and indirectly, via wastewater treatment plants (WWTPs) as a result of the dermal application of PCPs and subsequent showering, washing, and excretion (Diaz-Cruz and Barcelo, 2009). The US Food and Drug Administration recommends a usage amount of sunscreens containing organic UV filters of 0.75 mg/cm² of skin with reapplication at least every 2 h (FDA, 2011), especially in areas with high sun exposure. Sunscreens are often applied shortly before a person enters the water for recreational activities, making direct loss from the surface of the skin more likely (Langford and Thomas, 2008). Among the 53 organic UV filters that are commercially used in PCPs (Santos et al., 2012), BPs have relatively high water solubility (pKa: 9.6 for BP-3 (experimental value), 6.3 for BP-4 (experimental value), 7.53 for BP-1, 6.99 for BP-8; water solubility at 25 °C: 0.21 g/L for BP-3, 0.65 g/L for BP-4) (Table S1). WWTPs are not specifically designed to eliminate these pollutants, and BPs such as BP-3 have been reported to enter the environment after incomplete removal in WWTPs (Balmer et al., 2005; Kupper et al., 2006; Tsui et al., 2014a). The occurrence of BPs at ng/L to mg/L levels has been reported in lake water, river water (Cuderman and Heath, 2007; Ramos et al., 2015), and surface seawater (Ramos et al., 2015; Tsui et al., 2014b).

Because BPs are usually dermally applied by humans, their effects related to human health have been studied and reported (SCCP, 2008). Studies have also been conducted for non-target organisms, and endpoints such as algal growth (Sieratowicz et al., 2011), Daphnia magna immobility (Fent et al., 2010), and induction of the estrogen-modulated protein vitellogenin in fish (Coronado et al., 2008) have been measured.

Although BPs have been widely detected in surface waters, especially in beach seawater, their effects on corals are not well understood. Coral reefs are some of the most productive and biologically rich ecosystems on Earth, and they are under threat from anthropogenic impacts such as ocean acidification, seawater warming due to global climate change, coastal development and chemical pollution (Burke et al., 2011). Previous studies have reported high levels of BPs in surface seawater collected from popular coastal areas and beaches where corals are found (Downs et al., 2016; Tsui et al., 2017), and a recent study reported BP-3, BP-1 and BP-8 levels in wild coral tissues in Hong Kong at maximum concentrations of 38.4, 22.5, and 32.2 ng/g wet weight (ww), respectively (Tsui et al., 2017).

Three studies have reported toxicity assessment of organic UV filters in corals. A study by Danovaro et al. (2008) found that organic UV filters and sunscreens caused coral bleaching at low concentrations via in situ incubation experiments, and that BP-3 caused 86–93% bleaching of Acropora spp. after 24–96 h of exposure. The study concluded that organic UV filter exposure caused the rapid and complete bleaching of hard corals by promoting viral infections in zooxanthellae, even at extremely low concentrations. However, the exposure concentrations of the tested organic UV filters were not measured. Downs et al., 2014, Downs et al., 2016 studied the toxicities of BP-2 and BP-3 to coral larvae of Stylophora pistillata under both light and dark conditions. The results showed that BP exposure led to a concentration-dependent increase in coral bleaching (tested concentrations of BP-2: 2.46–24,600 μg/L; BP-3: 2.28–228,000 μg/L). The 24-h LC₅₀ values were 165 (light) and 508 (dark) μg/L for BP-2, while those for BP-3 were 139 (light) and 779 (dark) μg/L. Bioaccumulation of the tested UV filters was not determined in any of these coral studies.

The aims of this study were therefore to assess and compare the toxicities of four BPs (BP-1, BP-3, BP-4 and BP-8; Table S1) to larval and adult Pocillopora damicornis and Seriatopora caliendrum, two species that are widely distributed in the Western Indo-Pacific, using endpoints relevant to coral growth and health: settlement, bleaching, and mortality in larvae; and mortality, polyp retraction, visual bleaching, and zooxanthellae density in adults. Bioaccumulation of BPs in the tested corals was determined with an investigation on the fate of BP-3 in marine organisms, and values from the toxicity assessment were used to carry out a risk assessment using regional surface seawater BP concentrations measured in Kenting, Taiwan, where the corals used in the present study were collected, as well as Hong Kong.