Consequences of a contaminant mixture of bisphenol A (BPA) and di-(2-ethylhexyl) phthalate (DEHP), two plastic-derived chemicals, on the diversity of coastal phytoplankton
Introduction
Plastic marine pollution is a major environmental concern in response to the damage to organisms observed, such as the accumulation of debris in invertebrates (Thushari et al., 2017), the ingestion of plastic particles, the entanglement of aquatic organisms (GESAMP, 2015) and the transfer of this components along the trophic webs (Cole et al., 2013; Possatto et al., 2011; Staples et al., 1997). Unfortunately, in the marine environment, plastic debris is persistent and durable. It accumulates in the ecosystem and degrades to smaller micro-plastics (Bergmann et al., 2015; Causey and Padula, 2015). These latter items could, in turn, release plastic-derived chemicals, including endocrine disrupting chemicals (EDCs) such as bisphenol A (BPA) and di-2-ethylhexyl phthalate (DEHP). BPA and DEHP are two man-made chemicals used extensively in commercial and industrial applications, such as in additives and plasticizers. In the environment, plastic items are persistent and take a long time to disappear: from hundreds to thousands of years (Mansui et al., 2015). Furthermore, they are able to release other ester molecules, which impact marine food webs, leading to the bio-accumulation and bio-transport to higher organisms in the trophic levels (Hahladakis et al., 2017; Turki et al., 2014; Ying and Kookana, 2003). BPA and DEHP are hazardous components. They occur in aquatic areas at different levels: hundreds of ng/L to tens of μg/L in rivers and estuaries (Careghini et al., 2014), in coastal seawaters (Huang et al., 2012; Paluselli et al., 2017; Preston and Al-Omran, 1986) and the open ocean (Giam et al., 1978).
Being at the base of the food webs and as primary producers, phytoplankton have a crucial position in maintaining the equilibrium of the aquatic ecosystem (Cloern, 1996; Li et al., 2009). Obviously, they are crucial in the transfer of organic compounds between all matrixes of the marine environment: water, sediments and organisms (Staniszewska et al., 2015). In fact, several previous studies have reported the significant ability of phytoplankton to accumulate organic pollutants, such as polychlorinated biphenyls (PCBs) (Lynn et al., 2007), polycyclic aromatic hydrocarbons (PAHs) (Echeveste et al., 2010) and endocrine disrupting chemicals (for example, bisphenol A (BPA), di-(2-ethylhexyl) phthalate (DEHP) and di-butyl phthalate (DBP) (Chi et al., 2007; Huang et al., 1999; Kang et al., 2007; Liu et al., 2010). Species composition of phytoplankton is highly diverse and expresses different sensitivity responses to environmental changes. Evaluation of the toxicological profile of a pollutant towards phytoplankton, being the lowest trophic level, could define the entry point of contamination to the aquatic ecosystem. This is why phytoplankton are often studied to assess the environmental risk and evaluate the impact of toxic chemicals and other environmental factors. This evidently leads to a prediction of eco-toxicological consequences and, importantly, to the implementation of the necessary measures of prophylaxis to prevent any anomaly occurring in the aquatic system. Also, some sharp increases in phytoplankton biomass are associated with pollution occurrences (Leboulanger et al., 2011; Pandey et al., 2015). This has been interpreted as an adaptive state to minimize the impact of the toxicant (Nizzetto et al., 2012; Söderström et al., 2000). The exposure of phytoplankton to a sediment resuspension results in an enhancement of photosynthetic performance, a stimulation of growth and a change in the community structure in favor of toxic species tolerant to the toxicant (Ben Othman et al., 2017; Lafabrie et al., 2013a, Lafabrie et al., 2013b). Here, the amounts of phytoplankton may lead to disposal problems, such as the outbreak of harmful algal blooms (HABs) in the case of stimulation of toxic algae. Yet other studies have reported a decline in phytoplankton abundance, a decrease of Chlorophyll a and a disruption of photosynthetic performance when exposed to pollutants (Dorigo et al., 2004; Leboulanger et al., 2011; Pandey et al., 2015).
In the context of plastic-derived pollution, Causey and Padula (2015) showed that following the degradation of these items, micro-plastics, considered as hazardous pollutants (Cole et al., 2011), could be mistaken as food by small organisms. Furthermore, emphasizing the interaction between plastic-derived chemicals, such as BPA and DEHP, and primary producers, little is known about the eco-toxicological response of phytoplankton to those components at approximately in situ concentrations (Castañeda and Avlijas, 2014; Lusher et al., 2014). Previous studies have mainly been performed to assess the eco-toxicological response of some phytoplankton species exposed to high concentrations of BPA (up to 3 mg/L) compared to what is observed in situ (Ebenezer and Ki, 2012; Li et al., 2009; Liu et al., 2010) and to evaluate the capacity of these phytoplankton to accumulate and to degrade these components (Chi et al., 2007; Kang et al., 2006; Staniszewska et al., 2015). Considering the lack of information regarding the impact of BPA and DEHP on the base of the aquatic trophic web, this study aimed to investigate the toxicological answer of phytoplankton exposed to these plastic-derived chemicals. We targeted two different marine coastal ecosystems: a lagoon and a bay in the South-Western Mediterranean Sea and during two different seasons: spring and summer. The assessment was based on two strategies: i) mimicking an environment polluted with plastic debris by stimulating the release of BPA and DEHP from plastic items previously incubated in marine water and ii) simulating critical cases of chronic BPA and DEHP contamination in coastal marine ecosystems. For these purposes, monitoring was conducted on the biomass, abundance and the functional diversity (Bellemare et al., 2006; Franklin et al., 2001) of phytoplankton from the marine coast of Bizerte. The whole system (phytoplankton and contaminant) was incubated in microcosms under natural sunlight and temperature to mimic natural conditions.
Section snippets
Study area and plastic release preparation
The study was conducted in South-Western Mediterranean ecosystem: the lagoon and the bay of Bizerte (Tunisia), in April–May 2016 (~20 °C) and August–September 2016 (~28 °C). Bizerte lagoon is an important ecosystem. It is subject to the influence of several anthropogenic pressures, such as agriculture, fishing and farming activities, urbanization, industrialization (a cement factory, metal treatment, a dye-works, metallurgy, a steelworks, a military arsenal, a naval port, a commercial harbor,
In situ phytoplankton structure
A total of 48 phytoplankton species were identified in all samples. The phytoplankton structure was markedly different (only 24% similarity) between spring and summer (Fig. 1) and, to a lesser extent, between offshore and lagoon. Similarity between the two stations was about 48% in spring and 65% in summer, despite the fact that 22 species were common to both ecosystems for both seasons (Fig. 1). Phytoplankton diversity (H′ index) (Fig. 1) and richness (Table 1) for in situ waters was
In situ condition
The diversity of in situ waters was greater in summer than in spring. Despite a strong similarity of phytoplankton richness observed between offshore and lagoon stations (22 species in common out of 28–30 species in total, depending on the season), the phytoplankton structure exhibited important dissimilarities. Phytoplankton diversity and richness in the lagoon and offshore waters were similar to those previously observed in the same area (Lafabrie et al., 2013b; Sakka Hlaili et al., 2007) and
Conclusions
The present study showed that the offshore and lagoon waters in the Bizerte area were more contaminated DEHP relative to similar coastal areas. BPA and DEHP impacted strongly the phytoplankton biomass and structure, with a more pronounced effect offshore relative to lagoon, suggesting a possible phytoplankton resistance in this ecosystem. Nevertheless, the structural changes observed upon contamination were smaller than those induced by the effect of season. Our study has identified few species
Declarations of interest
None.
Acknowledgment
This study was supported by the Laboratoire Mixte Internationale COSYS-Med project and the Tunisian National Agronomic Institute (INAT), U.R.13ES36 Marine Biology (Faculté des Sciences de Tunis-El Manar I) – Carthage University. Charaf M'RABET benefited from a PhD grant by the French Institute of Research for Development (IRD).We wish to thank Pr. Marc Bouvy and Dr. Claire Carré from Montpellier University (UMR 9190 MARBEC) for their contribution in phytoplankton identification. English grammar
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