As for the effects of ocean warming and acidification on pollutant bioaccumulation, the contemporary shortage of experimental investigations focusing on the PAHs bioaccumulation, prevents acceptable comparisons of the results gained in the present study with previous studies. Thus, the present research presented new evidence that future predictions of elevated pCO2 and increased temperature in Persian Gulf waters can modify pollutant accumulation of phenanthrene in the pearl oyster P.radiata.
Our findings revealed that the P. radiata were able to concentrate low molecular weight PhE from seawater. The reduction in phenanthrene concentrations in water after 24 h is probable to display the bioavailability and uptake of the contaminant(Skadsheim et al. 2009; Hannam et al. 2010; Lüchmann et al. 2014). Neff and Anderson (1981) reported that phenanthrene is readily and rapidly taken up by organisms. To retain phenanthrene exposure level and water quality, despite the large uptake of this PAH by P. radiata, it was necessary to exchange the water and add proper PhE concentration in regularity (every 24 h). Some PHE is lost because of adsorption onto the surface of the both the oyster shells and experiment tank walls ( Hannam et al. 2010; Xie et al. 2017; Lima et al. 2018), degradation, volatilization or other unknown mechanism during the exposure time ( Hannam et al. 2010; Lima et al. 2018).
Though elevated temperature and decreased pH have been proposed to affect on bioaccumulation of trace metals (Benedetti et al. 2016; Nardi et al. 2017, 2018a,b; Sampaio et al. 2016, 2018), our study is one of the first to present findings about the effect of ocean climate changes on phenanthrene (as a PAHs model) bioaccumulation in a marine organism. Regarding the increased temperature and decreased pH, the same patterns observed when both stressors acted in combination and isolation (after 28 days of exposure, PhE concentration in whole body of oyster: A + W significantly higher than W and A; W significantly higher than A and contaminant condition; and contaminant condition significantly lower than A), highlighted the significance and urgent of considering the interactions between various abiotic stressors in studies focused on contaminants’ exposure specifically in the circumstance of climate change.
Relevant to the acidification effect, as detected in PhE bioaccumulation due to metabolic changes under hypercapnia condition, the accumulation of pollutant could be increased. It has also been documented in some investigations (e.g. Benedetti et al. 2016; Rosa et al. 2016; Sampaio et al. 2016, 2017; Nardi et al. 2017, 2018a, b).
Some authors state that damages in apical epithelial membrane simplify chemical diffusion into cells (Freitas et al. 2016; Shi et al. 2016; Velez et al. 2016; Sampaio et al. 2016, 2017a; Maulvault et al. 2018). Due to bivalves have a valve closing strategy of protection when exposed to environmental stressors, minor pollutant elimination in hypercapnia condition (increased PCO2) have been previously reported thus, preventing the excretion of compounds and their metabolites into the environment (Freitas et al. 2016; Velez et al. 2016; Maulvault et al. 2018). Such dispute may explain the lower elimination of phenanthrene and its metabolites under increased PCO2. Because of current lack knowledge about PAHs bioaccumulation under hypercapnia condition, it is not possible to compare the present data with previous studies on bivalves PAHs accumulation under climate change conditions however, some authors state that lower pH facilitate the uptake of molecular forms of pollutants ( e.g Higgins and Luthy 2005; Wang et al. 2012; Maulvault et al. 2018).
By increasing animals' metabolism, consequently, enhancing oyster ventilation and feeding rates in response to higher metabolic demands (Dijkstra et al. 2013), raised seawater temperature could probable lead to higher contaminant bioaccumulation in biota (Shen et al. 2010; Sampaio et al. 2016; Maulvault et al. 2017, 2018; Nardi et al. 2018a). Hence, phenanthrene can accumulate in soft tissue due to its lipophilic behavior (Speciale et al. 2018) and low elimination rate under warming seawater condition. Due to increasing filtration rate under high temperature and the low ability of bivalves in PAHs compounds elimination and metabolism capacity, phenanthrene was bioaccmulated in the oyster soft tissues (Bougrier et al. 1995; Haure et al. 1998; Xiao et al. 2014; Hannam et al. 2010; Piazza et al. 2016; Lima et al. 2018; Livingstone 1998; Snyder 2000). Previous studies have been found the bioaccumulation of this compound in some bivalves such as Crassostrea brasiliana (Lima et al. 2018), Chlamys islandica (Hannam et al. 2009), Pecten maximus (Hannam et al. 2010), Mytilus edulis (Law et al. 1999; Moore et al. 2007), Mytilus galloprovincialis (Valavanidis et al. 2008) and Crassostrea virginica (Elder and Dresler 1988). Although Lima et al. (2018) stated that PhE half-life in water was lower in high temperature, the higher concentration PhE in whole soft tissue at W and A-W treatments can be related to renew the contaminant every 24h. Both stressors in combination, enhanced temperature and PCO2, had synergetic spontaneity effect on PhE accumulation in oyster soft tissues. Previous studies on the effect of climate changes on metallic contaminant bioaccumulation revealed no synergic effects of both stressors(Benedetti et al. 2016; Nardi et al. 2018a, b; Sampaio et al. 2017, 2018). Nevertheless, additional investigations, especially focused on effects of the future scenario on PAHs bioaccumulation, need to be carried out to give more information about the synergistic or additive effects of these stressors.
While ocean acidification and warming seawater temperature have been indicated to impact on bioconcentration of trace metals (Baines et al. 2005; Mubiana and Blust 2007; Lacoue-Labarthe et al. 2011, 2009; Götze et al. 2014; Nardi et al. 2018a, 2017; Sampaio et al., 2017, 2018), it has not been documented the effects of this scenario on PAHs bioaccumulation. In the present study, the consequences of experiments revealed higher significant concentration of phenanthrene in the gills digestive gland of p. radiata exposed to this contaminant than mantle and muscle. Our findings showed no difference of phenanthrene uptake in between digestive gland and gills of oysters exposed to the chemical at lower pH and/or higher temperature, as well as between mantle and muscle. These findings revealed that the impact of enhancing temperature and pCO2 on phenanthrene bioconcentration cannot be popularized, depending on biota and the PAHs compounds, hence it is difficult to forecast only from the chemical model.
Our best AIC model indicated that contaminant bioaccumulation influenced by ocean warming and acidification which is coincident with previous studies (Benedetti et al. 2016; Nardi et al. 2017, 2018a, b, Sampaio et al. 2017, 2018). Similarity for phenanthrene bioaccumulation differed amongst oyster tissues with enhancing PhE concentration as follows: digestive gland > gills > mantle > muscle. The findings are supported by previous study carried out by Shahbazi et al. (2010) on PAHs tissue preferential bioaccumulation. The digestive gland is an organ commonly considered for its fundamental role in contaminate accumulation, detoxification and transformation and being responsible for recirculation of contaminants to other tissues, where the contaminant accumulate at higher concentration, compared to mantle and muscle tissues mostly characterized for low contaminant affinity (Yamashita et al. 2005; Jezierska and Witeska 2006; Wang et al. 2012; Sampaio et al. 2017; Maulvault et al. 2017, 2018). Furthermore, because of its high lipophilic property, PAHs concentrates specially in lipid-rich organs, like digestive gland (Guzzi and La Porta. 2008; Maulvault et al. 2016, 2017; Sampaio et al. 2018). Moreover, Being responsible for osmoregulation, acid base balance, nitrogenous waste excretion and respiration, as multifunctional organs, gills are sensitive organs to extensive various chemicals in water (Osman et al. 2017). Besides, due to increased blood supply, gill organs similarly recognized to have higher contaminate affinity in comparison to other organs ( Jezierska and Witeska 2006; Vergilio et al. 2012; Sampaio et al. 2017) such as mantle and muscle organs. Consequently, chronic exposure of oysters to contaminants in their surrounding water and sediments may eventually damage their respiratory ability.
In present study, PhE concentration in all of oyster organs increased during the exposure time. Liu et al. (2014) Liu et al. (2014) reported B[a]P concentration in gill and digestive gland of clam Ruditapes philippinarum increased during the exposure experiment. Other authors also stated that other bivalves exposing B[a]P revealed increasing in contaminant bioaccumulation in their gill and digestive gland tissues. There was no significant differences between two organs (Pan et al. 2008; Wang et al. 2011). Our results are coincident with the former, though the accumulation of PhE in gills and digestive glands were higher than two other tissues (mantle, muscle) during the exposure time; there was no statistically significant differences between digestive gland and gills with mantle and muscle. Bioaccumulation of organic pollutants in aquatic organisms is a balance between principally passive processes of uptake and depuration and elimination of contaminants through biotransformation pathways ( Livingstone 1991). Nonetheless, PAHs metabolism are significantly less than uptake rates in mollusks, resulting in strong bioaccumulation (Livingstone 1998; Liu et al. 2014).
Since oysters are filter-feeder and sessile creatures frequently exposed to PAH compounds in their habitat (Lima et al. 2018), revealing low ability to metabolize and eliminate these compounds (Siebert et al. 2017; Lima et al. 2018), PhE bioaccumulation in oyster different tissues is anticipated. When oysters were exposed under acidic condition, statistically significant increase of phenanthrene uptake was found during the experiment time in each tissue. The effect of reduced pH on PAHs uptake may not be influenced by the chemical compounds, but slightly reveal physiological effects of increasing PCO2 on an organism, which cannot be popularized, depending on PAHs, tissue, exposure time and species-specific individuals (Benedetti et al. 2016; Nardi et al. 2017, 2018b). The impact of enhancing temperature on increased PhE bioaccumulation was observed in all tissues, suggesting a whole organism physiological response, and tissue-specific variations. Increasing PhE concentration in different organs may be due to arrangement prioritization of CO2-excretory physiological processes under hypercapnia condition during exposure time (Perry et al. 1988; Sampaio et al. 2016, 2017). Therefore, taking into consideration that presence of both warming temperature and decreasing pH stressors cause to reduce physiological and subsequently metabolic thresholds (Harvey et al. 2013; Rosa et al. 2013; Sampaio et al. 2016, 2017). It may play a key role to arrest the contaminant in these organs because of decreasing the metabolic processes. Following the depression of total metabolism in the organism, the PhE metabolism and elimination, and excretion will be also reduced, thus it leads to accumulate the contaminant in these organs. In general, these consequences verify the limited effect of ocean acidification in comparison to temperature on the bioaccumulation of phenanthrene, despite the fact that there are statistically significant differences between the two stressors. Storage lipids, lipid composition and membrane phospholipids are the main partitioning places for the contaminant and to preserve ideal membrane functioning and availability to the energy pool, the lipid phases are retained fluid over an extensive temperature range. Fluctuation of temperature leads to change in lipid composition especially partition behavior of PAHs (Hazel 1995; Holmstrup et al. 2007; Muijs and Jonker 2009). Partitioning to these fluid lipids is enthalpy-driven ( Wezel and Opperhuizen 1995; Muijs and Jonker 2009), which subsequently should terminate in positive temperature effect. Additionally, tri- and tetra aromatic compounds are generally accumulated at larger concentrations in bivalves or other marine creatures than the weightier aromatic compounds. Some previous studies revealed such composition pattern in bivalves ( Porte and Albaigés 1994; Baumard et al. 1999; Hong et al. 2016; Ma et al. 2017). PAHs accumulation can be accomplished directly by taking in of low molecular weight PAH compounds via their branches (gills) and indirectly through digestion of fine grain size fraction of sediment and suspended particles, after that, absorption of higher molecular weight PAHs by the gastrointestinal tract and then distribute in other orangs (Oros and Ross. 2005; Ma et al., 2017). Possessing high lipophilic property and being the smallest PAH ,as one of global persistent organic pollutants, PhE be capable of simply penetrating biological membranes and contributes to bioaccumulate readily and rapid in different tissues (Zhang et al. 2014; Jin et al. 2015; Noh et al. 2015; Xiu et al. 2015; Piazza et al. 2016; Speciale et al. 2018) with noticeable tendency for bioaccumulation in digestive gland (Osman et al. 2017).
In the present study, GLM analysis in different organs revealed the time- dependent pattern of PhE uptake. time-dependent pattern of B[a]P uptake was confirmed in scallop’s ovary (Tian et al. 2014). It is plausible to assume that this pattern could be proceeded to saturate the organs completely during the experiment or feasibly the PhE levels were saturated in all tissues of P.radiata before the exposure time has been finished. Similar saturation patterns were also found for other marine biota exposed to various contaminants and temperatures. Oyster Crassostrea brasiliana exposed to phenanthrene at 18, 24 and 32°C (Lima et al. 2018), mussels M. galloprovincialis exposed to cadmium at 20 and 25°C (Nardi et al. 2017), and fish P. flavescens exposed to Ni at three temperature levels of 9, 20 and 28°C (Grasset et al. 2016) presented similar elevated levels of contaminants in high temperatures during the time of experiments.