Phytoremediation Potential of Macrophytes of Urban Waterbodies in Central India

Background. India's rapidly increasing population and growing urbanization pose a great challenge for wastewater treatment efforts, leading to increased pollution of surrounding waterbodies. Objectives. A field sampling-based study was conducted to analyze water quality, heavy metals and bioconcentration and bioaccumulation in the roots and shoots of naturally growing vegetation in an urban lake, Laxmi Taal. The lake receives domestic sewage from Jhansi city in Central India. Methods. Temperature, pH, electrical conductivity, turbidity, and water-soluble ions were measured with appropriate instruments. Plant accumulation of metals was measured with the bioconcentration factor (BCF), the ratio of metal concentration in the root to wastewater. The translocation factor (TF) was estimated as the ratio of metal concentration in the shoot to the root. Results. Water quality and heavy metal concentrations were found to be within the prescribed limit as per Indian standards IS-2296 “D”. In the present study, BCF was assessed to be >1 and the plants Typha angustifolia and Echhornia crassipus were determined to be accumulator plants. The TF study revealed that translocation of all the metals studied were significant, except for manganese (Mn), where concentration was found to be below detection limit. Conclusions. The present study validated that Typha angustifolia and Echhornia crassipus could be used for bioremediation purposes in cases of urban waterbodies receiving varying amounts of domestic wastewaters which have relatively limited concentrations of toxic metals. Competing Interests. The authors declare no competing financial interests


Introduction
With increasing population and growing urbanization in India, wastewater generation is also increasing at a rapid pace. Lack of appropriate treatment facilities and inadequate policy planning at the local level has aggravated the issue and many rivers, lakes, wetlands, lakes and other waterbodies are polluted. 1,2 Increased pollutants in waterways causes cultural eutrophication. 3 Untreated municipal and partially treated sewage and other external inputs causes changes in surface water quality. 4 Municipal sewage contains partially decomposed materials (inorganic and organics) and trace elements including cadmium (Cd), chromium (Cr), nickel (Ni), lead (Pb), copper (Cu), zinc (Zn), manganese (Mn) and iron (Fe). Waterbodies consisting of turbid heterogeneous liquid with persistent chemicals pose serious challenges due to water-borne diseases and health hazards. [5][6][7] Laxmi Taal in Jhansi, Bundelkhand (Uttar Pradesh) is a historical, previously rain-fed lake of about 32.52 hectares. Today, Laxmi Taal is encroached with an inflow of urban sewage, principally carrying domestic wastewater and runoff from surrounding settlements, temples, gardens and farmland without undergoing any treatment or sedimentation. Monitoring and assessment of water contamination, especially heavy metal accumulation, is a serious concern, as inhabitants depend on the lake for vegetable irrigation, drinking water for livestock and recreation. The consequences of pollution on plants and animals has been extensively studied in lentic and lotic ecosystems.
Phytoremediation can be used as an alternative solution for heavy Research metal remediation processes due to advantages as a cost-effective, efficient, environment-and ecofriendly technology based on the use of metal-accumulating plants. 8,9 Acidic water aids the uptake of heavy metals by plants and the enrichment mechanisms are related to the surface area of the plant exposed to water. 10 Eucalyptus camaldulensis, Zea mays, Potamogeton pectinatus L., and Typha domingensis are some of the best candidate species as hyperaccumulators for phytoremediation of heavy-metal contaminated soils and water. 11-15 To appropriately plan remedial measures using vegetation for heavy metal removal, it is imperative to have adequate knowledge of the role played by detritus (sink/ source). 16 Phytoremediation concerns have gained considerable attention in warm sub-tropical to semi-arid regions. In water scarce areas, surface waterbodies are the main source of water for 'B' grade use. The present study aims to provide an assessment of water quality, level of heavy metals and a comparative phytoremediation potential of Typha angustifolia and Echhornia crassipus. These two species are commonly occurring pre-adopted, successful metal accumulators. 17, 18 An extensive study was carried out on their phytoremediation potential in high metal contamination areas. The present study assesses the metal accumulation potential of the species with lower concentrations of heavy metal contamination. The outcome of the study may be useful in planning for bioremediation and restoration measures for urban waterbodies.

Methods
Laxmi Taal is a shallow, fresh water urban lake in the city of Jhansi, spreading over an area of about 0.162 km 2 . Laxmi Taal is located between latitude 25°27'20"-25°27'50"N and longitude 78°35'20"-78°35'45"E. With temples all along its boundary, it is a central part of the historical, cultural and recreational life of Jhansi city. It is approximately 32.52 hectares across with an average depth of 2.5 m and has a catchment area of 2370 hectares. The sewage carrying domestic wastewater of Jhansi city is dumped into Laxmi Taal through various nallas (channels), namely Kuberau nala, Kasai mandi nala, Laxmi gate nala, Jashiyana nala, Banglaghat nala and Bludgeon nala.
A large influx of people in the last few decades around the fringe of the lake has resulted in rapid deterioration of water quality. Increased inflow of untreated sewage, disposal of municipal solid wastes, excessive use of fertilizers and pesticides are some of the major problems facing the lake environment.

Water sample collection and analysis
The lake water samples were collected in precleaned, acid-treated high-

-Map showing the study area and sampling site in Laxmi Taal
Research density 3L polythene bottles, in triplicate at approximately 30-day intervals from each sampling location in the study area. The sampling area was divided into four zones: inlet lake interface, depicted as blue arrows in Figure 1; lake boundary with macrophytes, depicted as red triangles; middle of lake, depicted by a blue circle; and lake outlet, depicted with a yellow arrow. The four water sampling sites were selected on the basis of input, regeneration capacity, open area and outlet. Water parameters were determined in the present study and the methods adopted are described below. The water samples were brought to the Institute of Environment and

Equation 1
BCF=P/E where, P represents the trace element concentration in plant tissues (mg/ kg dry wt) and E represents the trace element concentration in the water (mg/l). Higher BCF values indicate higher accumulations in plants.
All the sampling values of heavy metals were lower than the prescribed values for surface water quality (IS: 2296). The luxuriant growth of Typha angustifolia indicated favorable conditions. The enrichment coefficient study and translocation factor studies revealed that the bioconcentration factor was >1 in all of the cases. An enrichment coefficient of >1 indicates that the plant is an accumulator and an enrichment coefficient of <1 indicates an excluder plant. Typha angustifolia and Echhornia crassipus are accumulator plants. Heavy metals in decreasing sequence in T. angustifolia were found to be Ni>Pb>Fe>Zn>Cu in the root system, and in the shoot, accumulation of heavy metals was in the order of Fe>Ni>Pb> Zn>Cu. The TF value was found to be >1 in all cases except Mn, where concentration was found to be below detection limit.
Regarding Echhornia crassipus, concentrations in descending order of Fe>Pb>Zn>Ni>Cu were observed in the root system and Ni>Fe> Zn>Pb>Cu in the shoot system. The translocation factor was found to be >1 in all of the cases except Mn, where concentration was found to be below the detection limit.

Discussion
Toxic metal contamination is increasing and has become a worldwide public health concern. 25, 26 Manganese, Cu, Zn, Ni, Pb and Fe compounds cause a variety of adverse human health effects. Copper toxicity leads to retention of Cu in the kidney. Copper begins to deposit in the liver, disrupting the liver's ability to detoxify, further increasing Cu levels, and drastically affects the connective tissue, reproductive system, nervous system, adrenal function, and affects learning in newborn babies. 27, 28 Zinc poisoning leads to gastrointestinal effects, such as abdominal pain, diarrhea and vomiting. 29 In adverse cases, it may lead to sideroblastic anemia, hypochromic microcytic anemia and leukopenia that is primarily due to zinc-induced Cu deficiency. High levels of Zn are known to be cytotoxic and disrupt the homeostasis of other requisite elements. 30-32 Thus, phytoremediation is highly recommended for removal of toxic heavy metals from waterbodies and soil so that they do not enter the food chain and result in disease in humans and animals.

Conclusions
The present study examined naturally growing vegetation in a domestic wastewater receiving lake, Laxmi Taal, in Jhansi, and indicated that parameters of wastewater in the lake were within the prescribed limit of water quality standard IS-2296 grade-D water. The bioconcentration factor study revealed that all of the values were approaching 1 or >1, thus T. angustifolia and E. crassipus are primary bioaccumulator plants.
Among the six heavy metals studied, Mn, Cu, Zn, Ni, Pb and Fe, the heavy metals TF value was found to be >1 in both T. angustifolia and E. crassipus. Heavy metals translocation from root to shoot was effective.
The heavy metal study revealed that accumulation of various metal ions by T. angustifolia and E. crassipus was higher in shoots than other parts of the plant. For all heavy metals, rhizofiltration and phytoextraction mechanisms have been found to be effective.
High levels of heavy metals have detrimental effects on the health of humans and animals. Monitoring of exposures and remedial measures are necessary to mitigate these effects. Phytoremediation has been found to be helpful in limiting the exposure of human beings and animals to the toxicity of water from lake Laxmi Taal, and in decreasing potential soil pollution, thus limiting the flow of these heavy metals further up the food chain. Phytoremediation by T. angustifolia and E. crassipus can be used effectively to help ensure waterbodies are free from toxic heavy