Toxicity and Bioremediation of Polybrominated Diphenyl Ethers (PBDEs) in Mangrove Wetland and Effects of Aquaculture Effluent on These Processes

紅樹林濕地對多溴聯苯醚(PBDEs)的毒性反應和生物修復及水產養殖污水對其影響

Student thesis: Doctoral Thesis

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Award date29 Aug 2018

Abstract

Polybrominated diphenyl ethers (PBDEs) extensively used as flame retardants in different products, including textiles, plastics, furniture, electronic equipments and rubbers are ubiquitous environmental contaminants. Mangrove wetlands situated in tropical and sub-tropical coastal areas are subject to PBDE contamination. Mangroves also receive nutrient-rich aquaculture effluent (AE) from nearby aquaculture activities. The effects of PBDEs on germination and the combined effects of PBDEs and AE on the biochemical responses of mangrove plants have not yet been reported. The effects of AE on the removal and transformation of PBDEs are also unknown. The study therefore aims to investigate the effects of 2,2',4,4',5-pentabromodiphenyl ether (BDE-99) and 2,2',3,3',4,4',5,5',6,6'-decabromodiphenyl ether (BDE-209) on mangrove plants, and evaluate the effects of AE on the toxicity and bioremediation of PBDEs in mangrove wetlands.

Germination study showed that BDE-99 in contaminated mangrove sediments suppressed germination rate, leaf formation and growth of Kandelia obovata (Ko). The leaves and roots of BDE-99 treated seedlings (2-months old) had significantly higher superoxide radical (O2-*) release, malondialdehyde (MDA) and total polyphenol (TP) content, and peroxidase (POD) activity than the control seedlings without any PBDE contamination. On the other hand, BDE-209 did not have any significant effect on germination, leaf formation and growth of Ko. The MDA content of the treated seedlings was less than the control, probably due to the enhanced activities of three antioxidative enzymes, namely catalase (CAT), POD and superoxide dismutase (SOD), in roots by BDE-209. PBDEs were found in plant tissues of the treated seedlings, indicating the plant uptake of BDE-99 and -209. This germination study revealed that Ko could tolerate PBDEs due to its antioxidative defense enzymes, but BDE-99 was more toxic than BDE-209. 

BDE-99 not only affected the 2-months old seedling, higher O2-* release and MDA content were also observed in treated Ko leaves at month 3. However, leaf CAT and SOD at month 3, and CAT and POD at month 6 were reduced by BDE-99. In roots, all three antioxidative enzyme activities were significantly reduced by BDE-99 during the 6-months experiment with more production of MDA at month 6. The addition of AE significantly enhanced root CAT, POD and SOD activities, and leaf CAT and SOD at month 3, leading to a lower content of MDA in root, and leaf and root O2-* release in BDE-99 treated Ko. According to the hormesis model, the combined effects of BDE-99 and AE on Ko root CAT activity at month 3 were synergistic, but the effects on leaf and root MDA and O2-* content during the 6-months experiment were antagonistic.

Significant reduction of BDE-99 contamination with the formation of lower brominated congeners, ranging from tetra- to di-BDEs, was found in all BDE-treated sediments, including unplanted (NP), Ko planted (WP), unplanted with AE (NPAE) and Ko planted with AE (WPAE).

At the end of 12-months experiment, more than 60% of the spiked BDE-99 was removed from all treated sediments, and the highest removal was found in WPAE, followed by WP, NPAE and NP treatments. All treated sediments showed a preference in the para position bromine substitution of BDE-99, followed by meta position, and the lowest was ortho bromine substitution. On the contrary, among tri- and di-BDEs congeners, ortho-substituted BDE-28 and -15 were the dominant congeners than that of para-substituted BDE-17 and -7, suggesting that para-substituted congeners could further be debrominated. Di-BDE congeners were only detected in NPAE treated sediment and plant tissues of Ko. The addition of AE enhanced the root uptake, accumulation and bioconcentration of the parent BDE-99 and the debrominated PBDE congeners (de-PBDEs) in Ko. These findings suggested that the addition of AE and planting Ko could be an effective way to remedy BDE-99 in contaminated mangrove sediments.

When the two mangrove species were compared, Ko suffered more from the oxidative stress of BDE-209 than Avicennia marina (Am), as evidenced by the higher production of leaf O2-* and MDA in Ko than Am under BDE-209 treatment. The antioxidative defense mechanisms differed between species and treatments without and with AE. In Am, BDE-209 reduced leaf POD and SOD activities at month 3 but such reduction in root was only observed at month 6. BDE-209 reduced leaf SOD and root POD and SOD activities in Ko at month 3. The addition of AE alleviated the toxic effects of BDE-209 in both species by increasing biomass production and stimulating the antioxidative enzyme activities, but lowering the overproduction of O2-*, especially in Am. The hormesis model showed that the combined effects of BDE-209 and AE on the production of MDA, O2-* and CAT activity in both species were mostly antagonistic, while synergistic effects were found in SOD activity in Ko leaf, and SOD and POD activities in Am root. At the end of the 12-months experiment, a significant removal of BDE-209 was recorded in the planted sediment. Such removal was significantly enhanced by AE addition, probably because of the increases in the concentrations of nitrogen (N) and phosphorous (P) in sediments. The residual percentages of BDE-209 in Ko and Am planted sediments without AE addition were 61.4% and 70.9%, respectively, and the respective values decreased to 46.9% and 48.0% with AE addition. Similar trend was found in the unplanted sediment, with 86.5% BDE-209 retained without AE and reduced to 65.3% with AE supply. High concentrations of de-PBDEs, including di- to nona-BDEs were detected in both planted and unplanted sediments. The AE addition in the planted sediment significantly enhanced the translocation of all de-PBDEs but reduced BDE-209 translocation into the aboveground tissues in both mangrove plants. The addition of AE also stimulated the root uptake of BDE-209 in Ko but de-PBDEs in both Ko and Am. These results demonstrated that AE addition could stimulate the phytoremediation process of BDE-209 in contaminated sediments.

At the end of the 24-months tide tank experiment with mixed mangrove plant species, BDE-209 significantly reduced the leaf, stem and root biomass and pigment contents, including Chl a, Chl b and Car contents, but enhanced the root O2-*, and leaf and root MDA production of Ko. In Aegiceras corniculatum (Ac), only leaf biomass and pigment contents were reduced by BDE-209, but higher leaf O2-* contents than that of control at month 24. On the contrary, growth, pigment contents and the production of O2-* and MDA in Am were not affected by BDE-209. These results indicated that Am was the most tolerant species in BDE-209 contaminated mangrove sediments, followed by Ac and Ko. The tolerance was related to the ability of the antioxidative enzymes to reduce the oxidative stress posed by BDE-209. At the end of 24-months of the experiment, BDE-209 significantly increased leaf POD and SOD activities in both Ko and Am, root POD in Ko and SOD in Am. In Ac, leaf POD and root CAT, POD and SOD activities were stimulated by BDE-209 at month 24. These results indicated that POD and SOD activities in mangrove plants could be induced by BDE-209 to scavenge the reactive oxygen species (ROS).

At the end of the 24-months tide tank experiment, more than 60% and 40% of the spiked BDE-209 were removed from the contaminated sediments with and without plants, respectively. High concentrations of de-PBDEs were observed in both planted and unplanted sediments. More BDE-209 and de-PBDEs were retained in the upper than the bottom layer in both plant ed and unplanted sediments. Among different plant tissues, the concentration of BDE-209 and its total uptake followed the same order in all three plant species, that is roots > propagules (only available for Ko) > stems > leaves. Among three plant species, Ac had the highest total uptake of BDE-209, followed by Am and Ko. On the contrary, Ko had the highest translocation factor of BDE-209 and de-PBDEs, followed by Ac and Am. These results suggested species-specific uptake and translocation of PBDEs.
The present study showed, for the first time, the effect of two PBDE congeners (BDE-99 and -209) on the germination of Ko, a dominant mangrove plant species in Hong Kong, and the combined effects of PBDEs and AE on the growth and antioxidative responses of Ko and Am in pot microcosms. Results showed that AE addition alleviated the toxicity of PBDEs on mangroves and enhanced the bioremediation of PBDEs in contaminated mangrove sediments. The 24-months tide tank experiment, which simulated the natural intertidal mangrove wetland, clearly demonstrated that some mangrove species such as Am was tolerant to BDE-209 contamination and BDE-209 in contaminated mangrove sediments could be removed, especially in the planted sediment. It is possible to use a constructed mangrove wetland system planted with the tolerant species to remedy PBDE contaminated environment, and the remediation efficiency could be enhanced by nutrient-rich wastewater.