Assessing indicators of arsenic toxicity using variable fluorescence in a commercially valuable microalgae: Physiological and toxicological aspects.

Indicators signaling Arsenic (As) stress through physiology of microalgae using non-destructive methods like variable fluorescence are rare but requisite. This study reports stress markers indicating arsenic (As) toxicity (in two concentrations 11.25 µg/L and 22.5 µg/L compared to a control) exposed to a microalga (Diacronema lutheri), using fast repetition rate fluorometry (FRRf). Growth and physiological parameters such as cell density, chl a and the maximum quantum yield Fv/Fm showed coherence and impeded after the exponential phase (day 9 - day 12) in As treatments compared to the control (p < 0.05). On contrary photo-physiological constants were elevated showing higher optical (aLHII) and functional [Sigma (σPSII)] absorption cross-section for the As treatments (p < 0.05) further implying the lack of biomass production yet an increase in light absorption. In addition, As exposure increased the energy dissipation by heat (NPQ-NSV) showing a strong relationship with the de-epoxidation ratio (DR) involving photoprotective pigments. Total As bioaccumulation by D. lutheri showed a strong affinity with Fe adsorption throughout the algal growth curve. This study suggests some prompt photo-physiological proxies signaling As contamination and endorsing its usefulness in risk assessments, given the high toxicity and ubiquitous presence of As in the ecosystem.

Trace metals exposure in three different coastal compartments show specific morphological and reproductive traits across generations in a sentinel copepod.

The effect of exposure from several compartments of the environment at the level of individuals was rarely investigated. This study reports the effect of contaminants from varied compartments like sediment resuspension, elutriation from resuspended sediment (extract) and seawater spiked trace metal mixtures (TM) on morphological and reproductive traits of the pelagic bioindicator copepod Eurytemora affinis. At the population level of E. affinis, lowest survival was observed in dissolved exposures (TM and extract) in the first generation (G1), showing some adaptation in the second generation (G2). An opposite trend for resuspended sediment showed higher sensitivity in survival at G2. At the individual level, prosome length and volume proved to be sensitive parameters for resuspended sediments, whereas clutch size and egg diameter were more sensitive to TM and extract. Although the generation of decontamination (G3, no exposure), showed a significant recovery at the population level (survival % along with clutch size) of E. affinis exposed to resuspended sediment, morphological characteristics like prosome length and volume showed no such recovery (lower than control, p < 0.05). To the contrary, dissolved exposure showed no significant recovery from G1 to G3 on neither survival %, clutch size, egg diameter, prosome volume, but an increase of prosome length (p < 0.05). Such tradeoffs in combatting the stress from varied sources of toxicity were observed in all exposures, from G1 to G3. The number of lipid droplets inside the body cavity of E. affinis showed a significant positive correlation with trace metal bioaccumulation (p < 0.01) along with a negative correlation (p < 0.05) with survival and clutch size in each treatment. This confirms the inability of copepods to utilize lipids under stressful conditions. Our study tenders certain morphological and reproductive markers that show specificity to different compartments of exposure, promising an advantage in risk assessment and fish feed studies.

Responses of the copepod Eurytemora affinis to trace metal exposure: A candidate for sentinel to marine sediment resuspension effects.

Our study reports the ability of Eurytemora affinis to indicate certain responses in 96 h when exposed to resuspended sediment from a polluted site (PS, Seine estuary, France), less polluted site (LPS, Canche estuary, France) and dissolved trace metals. Mortality from dissolved trace metal was highest (57.5 %) followed by PS (38.59 %) > LPS (24.04 %). The exposure to PS sediment resulted in significantly lower no. of early larval stage (nauplii < 2), sex-ratio (39.24 % of males) and higher ovigerous female (>10). Eurytemora affinis bioaccumulated high concentrations of copper (27.3 mg/kg), nickel (12.8 mg/kg), lead (21.8 mg/kg) and arsenic (13.7 mg/kg) from PS exposure with significantly lower bioaccumulation of metals from LPS. The bioconcentration factor (BCF) was highest from dissolved toxicity (>2000) followed by PS that showed significantly higher BCF for Nickel and Copper, compared to LPS. The responses of E. affinis to different matrices exemplify its role as a sentinel.

Single toxicity of arsenic and combined trace metal exposure to a microalga of ecological and commercial interest: Diacronema lutheri.

Eco-toxicological assays with species of economic interest such as Diacronema lutheri are essential for industries that produce aquaculture feed, natural food additives and also in drug developing industries. Our study involved the exposure of a single and combined toxicity of arsenic (As V) to D. lutheri for the entire algal growth phase and highlighted that a combined exposure of As V with other essential (Copper, Cu; Nickel, Ni) and non-essential (Cadmium, Cd; Lead, Pb) trace metals reduced significantly the cell number, chlorophyll a content, and also significantly increased the de-epoxidation ratio (DR) as a stress response when compared to the single toxicity of As V. Arsenic, as one of the ubiquitous trace metal and an active industrial effluent is reported to have an increased bio-concentration factor when in mixture with other trace metals in this study. In the combined exposure, the concentration of total As bio-accumulated by D. lutheri was higher than in the single exposure. Hence, polluted areas with the prevalence of multiple contaminants along with the highly toxic trace metals like As can impose a greater risk to the exposed organisms that may get further bio-magnified in the food chain. Our study highlights the consequences and the response of D. lutheri in terms of contamination from single and multiple trace metals in order to obtain a safer biomass production for the growing need of natural derivatives.

Intergenerational effects of resuspended sediment and trace metal mixtures on life cycle traits of a pelagic copepod.

Multiple stressors like metal toxicity, organic compounds and sediment pollution from the Seine estuary are raising concern and novel toxicological approaches are needed to better assess and monitor the risk. In the present study, the copepod Eurytemora affinis from the Seine, was exposed to two different sources of contaminants, which were resuspended polluted sediments and a mixture of trace metals (dissolved phase). The exposure continued for four generations (F0, F1, F2, F3) where F0 is a generation for acclimation to the exposure condition and F3 is a generation for decontamination followed without any exposure, to detect possible maternal carryover effects of pollutants (F0 - F2) and the role of recovery (in F3). Higher accumulation of metals resulted in higher mortalities at both exposure conditions, with particularly F1 being the most sensitive generation showing highest bioaccumulation of metals, highest mortality, and smallest population size. Copper accumulation was highest of all metals in mixture from both the resuspended sediment and the combined trace metal treatment. A significantly lower naupliar production was seen in copepods exposed to resuspended sediment compared to trace metal exposed copepods. However, the decontamination phase (F3) indicated that E. affinis pre-exposed to resuspended sediment had a higher ability to recover the total population size, increase naupliar production, and depurate accumulated Cu. The population exposed to a trace metal mixture showed lower recovery and lower ability to discharge accumulated toxic metals indicating its greater effect on our experimental model when compared to resuspended sediment.

Correction: Occurrence and distribution of anthropogenic persistent organic pollutants in coastal sediments and mud shrimps from the wetland of central Taiwan.

[This corrects the article DOI: 10.1371/journal.pone.0227367.].

Occurrence and distribution of anthropogenic persistent organic pollutants in coastal sediments and mud shrimps from the wetland of central Taiwan.

Sediment profile and mud shrimp (Austinogebia edulis) from the coastal wetland of central Taiwan in 2017 and 2018 were analyzed for concentration, source, and composition of persistent organic pollutants (POPs) including polycyclic aromatic hydrocarbon (PAHs), polybrominated diphenyl ethers (PBDEs), organochlorine pesticides (OCPs; DDT and HCB), and polychlorinated biphenyls (PCBs). Sediment profiling indicated PAH concentrations reaching 254.38 ng/g dw in areas near industrial areas and PAH concentrations of 41.8 and 58.42 ng/g dw in sampling areas further from industrial areas, suggesting that the determining factor for spatial distribution of POPs might be proximity to contaminant sources in industrial zones. Based on molecular indices, PAHs were substantially of both pyrolytic and petrogenic origins. The main sources for PCBs were Aroclor 1016 and 1260 and the congener BDE-209 was the dominant component among PBDE congeners. While we were unable to obtain live mud shrimp samples from the heavily contaminated areas, in samples from less contaminated areas, the risk assessment on mud shrimp still illustrated a borderline threat, with DDT concentrations almost reaching standardized values of Effects Range-Low (ERL). Bioaccumulation factors for DDTs and PCBs (17.33 and 54.59, respectively) were higher than other POPs in this study. Further study is essential to assess and understand the impact of these chemicals on the wetland ecosystem near this heavily industrialized area.

A slender symbiotic goby hiding in burrows of mud shrimp Austinogebia edulis in western Taiwan.

The present study recorded the population of the goby fish (Perciformes: Gobiidae), Eutaeniichthys cf. gilli Jordan & Snyder, 1901, from the tunnel burrowed by the mud shrimp Austinogebia edulis Ngo-Ho and Chan, 1992 in a mudflat in Shengang and Wangong of Changhua County, western Taiwan. This finding is not only a new record of the genus in Taiwan, it is also the first record of this species in a mudflat near an industrial park. In total, 56 individuals of E. cf. gilli were collected from June 2016 to September 2018. Morphological traits of males and females were measured. The resin casting method trapped bodies of E. cf. gilli that were present in the tunnel burrow and proved that the fish inhabits burrows of the mud shrimp A. edulis. In addition, a species of snapping shrimp was also found in the same tunnel. Symbiotic interaction may occur between E. cf. gilli, A. eduli and the snapping shrimp. The China Coastal Current (CCC) runs along the coastlines of Japan, Korea, China, and reaches western Taiwan during the northeast monsoon period. The CCC, therefore, might play an important role in the biogeographic distribution of E. cf. gilli in the western Pacific Ocean. Since E. cf. gilli is listed in the Red List as an endangered species of Japan for many years, Taiwan waters may provide a refuge for this fish species warranting a broader investigation. Since Taiwan is some distance away from the previously recorded locations in Japan, Korea, the Yellow Sea, and the Bohai Sea, a phylogenic analysis is warranted for population and species differentiation in the future.

Effects of cadmium exposure on antioxidant enzymes and histological changes in the mud shrimp Austinogebia edulis (Crustacea: Decapoda).

The trace metal cadmium (Cd) is a toxic pollutant known to induce oxidative stress and other sublethal to lethal effects on aquatic organisms. We exposed the marine mud shrimp Austinogebia edulis to Cd concentrations of 0, 0.5, and 5 mg/kg for up to 4 days (24, 48, 72, 96 h). We studied the activity of antioxidant enzymes in the hepatopancreas, gill, and muscle of A. edulis. Antioxidant enzymes (SOD, CAT, and GPx) decreased with increasing Cd concentration and extended exposure time in these three organs of the mud shrimp A. edulis. Increasing Cd concentration led to an increase in ROS and resulted ultimately in membrane lipid peroxidation at higher Cd concentrations. Significant damage of the hepatopancreas of A. edulis was noticed at higher concentrations of Cd, showing damages like the disappearance of epithelial cell boundaries, detachment of cells from the basal lamina, cellular swelling, necrosis, and reduction of glycogen. In conclusion, Cd caused oxidative damage by reducing the activities of antioxidant enzymes and by damaging the tissue structure in major organs of the mud shrimp A. edulis.

Burrow characteristics of the mud shrimp Austinogebia edulis, an ecological engineer causing sediment modification of a tidal flat.

The mud shrimp Austinogebia edulis, being abundant in the intertidal zone of western Taiwan, constructs deep burrows (>1 m). This study highlights the potential of mud shrimps to modify sediment characteristics of the tidal flat by its burrowing behavior. We studied the structure of the burrow wall, compared the difference in the sediment composition of the burrow and the background sediment, and compared the organic content inside the burrow wall. This study was carried out from September 2015 to November 2016 in three areas of the western coast of Taiwan, namely Shengang, Hanbow, and Wangong. The present study found significant differences between burrow wall and the burrow lumen. The diameter of the burrow wall was double as wide as the inner burrow lumen at the opening and gradually increased to 10 times of the burrow lumen at 30 cm depth. The burrow wall of A. edulis showed low permeability and increased the sheer strength. Statistically, a significant difference was noticed in the comparison between the sediment composition of the burrow wall and the background (p < 0.05, Student's t-test). An accumulation of 3.63 for fine sand (t = -5.22, p < 0.001, fine sand) and 9 for clay (t = -25.01, p < 0.001, clay) was found in the upper burrow wall of A. edulis. This indicated that they somehow chose finer particles to build burrows. This will gradually change the sediment distribution-vertically and horizontally. The burrow wall consisted of a 24 times higher organic matter content than one individual of mud shrimp. The burrow may provide organic material as a potential food source. The mud shrimp thus transforms the sediment characteristics as an ecological engineer, which is expected to have a significant ecological impact on the ecosystem.