Toxicological effects of the sunscreen UV filter, benzophenone-2, on planulae and in vitro cells of the coral, Stylophora pistillata

An Erratum to this article was published

Abstract

Benzophenone-2 (BP-2) is an additive to personal-care products and commercial solutions that protects against the damaging effects of ultraviolet light. BP-2 is an “emerging contaminant of concern” that is often released as a pollutant through municipal and boat/ship wastewater discharges and landfill leachates, as well as through residential septic fields and unmanaged cesspits. Although BP-2 may be a contaminant on coral reefs, its environmental toxicity to reefs is unknown. This poses a potential management issue, since BP-2 is a known endocrine disruptor as well as a weak genotoxicant. We examined the effects of BP-2 on the larval form (planula) of the coral, Stylophora pistillata, as well as its toxicity to in vitro coral cells. BP-2 is a photo-toxicant; adverse effects are exacerbated in the light versus in darkness. Whether in darkness or light, BP-2 induced coral planulae to transform from a motile planktonic state to a deformed, sessile condition. Planulae exhibited an increasing rate of coral bleaching in response to increasing concentrations of BP-2. BP-2 is a genotoxicant to corals, exhibiting a strong positive relationship between DNA-AP lesions and increasing BP-2 concentrations. BP-2 exposure in the light induced extensive necrosis in both the epidermis and gastrodermis. In contrast, BP-2 exposure in darkness induced autophagy and autophagic cell death. The LC50 of BP-2 in the light for an 8 and 24 h exposure was 120 and 165 parts per billion (ppb), respectively. The LC50s for BP-2 in darkness for the same time points were 144 and 548 ppb. Deformity EC20 levels (24 h) were 246 parts per trillion in the light and 9.6 ppb in darkness.

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Acknowledgments

We thank Dr. Fuad Al-horani for his assistance, Ms. Maya Vizel for her assistance with the planula exposure challenges, Dr. Gideon Winters for assistance with Molecular Dynamics microplate fluorimeter, and the anonymous reviewers who greatly improved the quality of this manuscript. We also sincerely thank Dr. Sylvia Galloway and James H. Nicholson for their work on formatting the figures for publication.

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The authors can identify no potential conflicts of interest, neither financial or ethically, involved in the writing or publication of this manuscript.

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The intent of this article is purely for dissemination of scientific knowledge, and is neither endorsement nor condemnation of the activities of any government, corporation, their employees or subsidiaries, nor to imply liability on their part. This publication does not constitute an endorsement of any commercial product or intend to be an opinion beyond scientific or other results obtained by the U.S. National Oceanic and Atmospheric Administration (NOAA). No reference shall be made to U.S. NOAA, or this publication furnished by U.S. NOAA, to any advertising or sales promotion which, would indicate or imply that U.S. NOAA recommends or endorses any proprietary product mentioned herein, or which has as its purpose an interest to cause the advertised product to be used or purchased because of this publication.

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a

Proportion of planula alive as a function of benzophenone-2 concentration. Symbol size is proportional to the number of replicates having a given value. Regression line (solid) and 95 % confidence intervals (dashed lines) are shown for each statistically significant fit. a Stylophora pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for 8 h in the dark. c S. pistillata exposed to benzophenone-2 for planulae exposed for 8 h in the light, then 16 h of darkness. d S. pistillata exposed to benzophenone-2 for 24 h in the dark

a

Proportion of non-deformed planulae as a function of benzophenone-2 concentration. Symbol size is proportional to the number of replicates having a given value. Regression line (solid) and 95 % confidence intervals (dashed lines) are shown for each statistically significant fit. a Stylophora pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for 8 h in the dark. c S. pistillata exposed to benzophenone-2 for planulae exposed for 8 h in the light, then 16 h of darkness. d S. pistillata exposed to benzophenone-2 for 24 h in the dark

a

PROBIT analyses of dose–response curves of cells of Stylophora pistillata exposed to benzophenone-2. PROBITs fit using a Gompertz–Weibull exponential distribution were used to calculate LC50s. a S. pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for 8 h in the dark

a

PROBIT analyses of dose–response curves of number of deformed planulae of Stylophora pistillata exposed to benzophenone-2. PROBITs fit using a Gompertz-Weibull exponential distribution were used to calculate EC50s. a S. pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for planulae exposed for 8 h in the light, then 16 h of darkness. c S. pistillata exposed to benzophenone-2 for 8 h in the dark. d S. pistillata exposed to benzophenone-2 for 24 h in the dark

a

PROBIT analyses of dose-lethality curves of planulae of Stylophora pistillata exposed to benzophenone-2. PROBITs fit using a Gompertz–Weibull exponential distribution were used to calculate LC50s. a S. pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for 24 h in the light. c S. pistillata exposed to benzophenone-2 for 8 h in the dark

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Downs, C.A., Kramarsky-Winter, E., Fauth, J.E. et al. Toxicological effects of the sunscreen UV filter, benzophenone-2, on planulae and in vitro cells of the coral, Stylophora pistillata . Ecotoxicology 23, 175–191 (2014). https://doi.org/10.1007/s10646-013-1161-y

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Keywords

  • Coral
  • Benzophenone-2
  • Cell toxicity
  • Coral planula
  • Sunscreen UV filters