Effects of wastewater discharge on root anatomy, radial oxygen loss patterns and formation of iron plaque on the root surface of mangrove plants and their significance in wastewater treatment

Abstract

Mangrove wetlands have been proposed to be low-cost and effective wastewater treatment systems for the removal of pollutants from municipal wastewater. However, mangrove wetlands are often challenged by oxygen stress caused by: i) periodic or permanent flooding; ii) aerobic degradation of nutrients and organic matter and iii) oxidation of heavy metals. Continuous discharge of wastewater rich in nutrients, organic matter and heavy metals, exaggerate the oxygen-stress problem and cause damage to the plants. Mangrove plants have adapted to the anaerobic conditions by developing special features: i) root anatomy, including aerenchyma air spaces and outer layers; ii) radial oxygen loss (ROL) from aerenchyma air spaces and iii) formation of iron (Fe) plaque on their root surfaces. Aerenchyma air spaces provide the internal pathway for oxygen transfer. ROL allows roots to create an aerobic protective rhizosphere for plants when growing in anaerobic environments. The outer layers prevent excessive ROL and protect plant roots against toxic pollutants. The Fe plaque that forms on the root surface has a high capacity to immobilize toxic substances, thus prevents the excessive uptake by plants and contributes to the wastewater treatment. So far, the studies on root anatomy, ROL and Fe plaque formation have mainly focused on important crops, grasses and common wetland plants. Little is known with regards to mangrove plants, a very important group of inter-tidal wetlands in tropical and sub-tropical regions. The effects of wastewater discharge on root anatomy, ROL and Fe plaque formation in mangrove plants have never been reported. The present research aimed: i) to examine the root anatomical features and ROL patterns of seedlings of eight true mangrove species in Hong Kong, namely Avicennia marina (Forsk.) Vierh., Acanthus ilicifolius L., Aegiceras corniculatum (Linn.) Blanco, Bruguiera gymnorrhiza (L.) Poir, Excoecaria agallocha L., Heriteria littoralis Dryand. ex W. Ait., Kandelia obovata Sheue, Liu & Yong and Lumnitzera racemosa Willd.; ii) to investigate the effects of wastewater discharge on root anatomy and ROL patterns in three true mangrove species, B. gymnorrhiza, E. agallocha and A. ilicifolius, with and without tidal flushing and iii) to determine the variation of Fe plaque formation on root surface and heavy metals immobilization in Fe plaque when receiving wastewater containing both nutrients and heavy metals. The spatial patterns of ROL of the eight true mangrove species was comparable, with more oxygen lost from the tip than that from the basal and mature zones, but this extent was species-specific. The roots of A. marina and A. ilicifolius had the largest areas of aerenchyma air spaces but the weakest outer layer. On the other hand, H. littoralis had the least longitudinal oxygen transfer because of its smaller area of aerenchyma air spaces in roots. The tolerance of mangrove species to waterlogged soil followed the order of A. marina (most foreshore species) > A. ilicifolius > K. obovata > A. corniculatum > B. gymnorrhiza > E. agallocha > L. racemosa > H. littoralis (most landward species), which is related to their anatomical features and ROL. The effects of wastewater discharge on root anatomy and ROL varied among three mangrove species. The rates of ROL from roots of B. gymnorrhiza were the highest in the root tip and declined in the basal and mature zones, indicating the 'tight barrier' to ROL, and there was no significant difference among the three treatments, FW (freshwater, control), NW (with concentrations of dissolved organic carbon (DOC), ammonium-N (NH4+-N), nitrate-N (NO3--N), total Kjeldahl N (TKN) and inorganic phosphate (PO43--P), which is the same as that in the primary settled municipal sewage in Hong Kong), and 10NW (10 times the pollutant concentrations of NW). The ROL patterns of E. agallocha in FW and NW treatments exhibited a 'tight barrier', but changed to a 'partial barrier' when receiving 10NW, with similar rates along a lateral root. The effects of wastewater discharge on ROL of A. ilicifolius were the most obvious, with the 'tight barrier' in FW and the 'partial barrier' in NW, but shifted to a 'weak barrier' in 10NW, with much higher rates in the mature zone than in the tip. Wastewater discharge, without tidal flushing, induced more ROL from roots for all three species, the stronger the wastewater, the more ROL. However, this induction was not exhibited under the tidal flushing condition due to the formation of Fe plaque on root surface, which was not found in roots without tidal flushing. The correlation between ROL and Fe plaque was positive in FW but changed to negative in 10NW. When receiving wastewater containing both nutrients and heavy metals, the concentrations of Fe plaque formed on root surface increased with wastewater discharge for all three species; the stronger the wastewater, the more the Fe plaque formed. Among the three species, the concentration of Fe plaque formed on the root surface was the least in B. gymnorrhiza in 5SW (synthetic wastewater with concentrations of DOC, NH4+-N, NO3--N, TKN, PO43--P and heavy metals, including Fe3+, Ni2+, Cu2+, Pb2+, Cr6+, Cd2+, Mn2+ and Zn2+, five times of that in the primary settled municipal sewage in Hong Kong) and 10SW (double the pollutant concentrations in 5SW). More Fe plaque was formed on roots of A. ilicifolius when receiving 5SW, but the plants which received 10SW were all dead at the end of 75-day experiment. The concentrations of heavy metals immobilized in Fe plaque were positively correlated with the concentration of Fe plaque formed, although the correlation coefficient varied from species to species. These results suggested that B. gymnorrhiza was the most tolerant species to pollutants as the root anatomy and ROL were least affected by wastewater discharge, followed by E. agallocha and A. ilicifolius was the most susceptible species, and thus, was not suitable for treating wastewater which contains high concentrations of pollutants. More ROL induced more Fe plaque to form on the root surface. However, excessive ROL from the root led to plant death. On the other hand, Fe plaque formation prevented excessive ROL and acted as a reservoir to immobilize toxic pollutants, thus protecting roots against these pollutants and contributing to the wastewater purification.